DOE PAGES title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age

Abstract

Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen interactions and infectious disease mechanisms, these reductionist models lack many essential features present in the native host microenvironment that are known to regulate infection, including three-dimensional (3-D) architecture, multicellular complexity, commensal microbiota, gas exchange and nutrient gradients, and physiologically relevant biomechanical forces (e.g., fluid shear, stretch, compression). Here, a major challenge in tissue engineering for infectious disease research is recreating this dynamic 3-D microenvironment (biological, chemical, and physical/mechanical) to more accurately model the initiation and progression of host-pathogen interactions in the laboratory. Here we review selected 3-D models of human intestinal mucosa, which represent a major portal of entry for infectious pathogens and an important niche for commensal microbiota. We highlight seminal studies that have used these models to interrogate host-pathogen interactions and infectious disease mechanisms, and we present this literature in the appropriate historical context. Models discussed include 3-D organotypic cultures engineered in the rotating wall vessel (RWV) bioreactor, extracellular matrix (ECM)-embedded/organoid models, and organ-on-a-chip (OAC) models. Collectively, these technologiesmore » provide a more physiologically relevant and predictive framework for investigating infectious disease mechanisms and antimicrobial therapies at the intersection of the host, microbe, and their local microenvironments.« less

Authors:
ORCiD logo [1]; ORCiD logo [2];  [1];  [1];  [1];  [1];  [1];  [1];  [3]; ORCiD logo [4];  [5]; ORCiD logo [1];  [6]
  1. Arizona State Univ., Tempe, AZ (United States)
  2. Ghent Univ., Ghent (Belgium)
  3. NASA Johnson Space Center, Houston, TX (United States)
  4. Univ. of Pittsburgh, Pittsburgh, PA (United States)
  5. Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States)
  6. Univ. of Florida, Gainesville, FL (United States)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1580337
Grant/Contract Number:  
AC02-05CH11231; NNX13AM01G; NNX15AL06G; R01-AI081759
Resource Type:
Accepted Manuscript
Journal Name:
Infection and Immunity
Additional Journal Information:
Journal Volume: 86; Journal Issue: 11; Journal ID: ISSN 0019-9567
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; 3-D; 3D; RWV; rotating wall vessel; gut-on-a-chip; host-microbe interaction; host-pathogen interactions; mechanotransduction; organ-on-a-chip; organoid

Citation Formats

Barrila, Jennifer, Crabbé, Aurélie, Yang, Jiseon, Franco, Karla, Nydam, Seth D., Forsyth, Rebecca J., Davis, Richard R., Gangaraju, Sandhya, Ott, C. Mark, Coyne, Carolyn B., Bissell, Mina J., Nickerson, Cheryl A., and Maurelli, Anthony T. Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age. United States: N. p., 2018. Web. doi:10.1128/IAI.00282-18.
Barrila, Jennifer, Crabbé, Aurélie, Yang, Jiseon, Franco, Karla, Nydam, Seth D., Forsyth, Rebecca J., Davis, Richard R., Gangaraju, Sandhya, Ott, C. Mark, Coyne, Carolyn B., Bissell, Mina J., Nickerson, Cheryl A., & Maurelli, Anthony T. Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age. United States. https://doi.org/10.1128/IAI.00282-18
Barrila, Jennifer, Crabbé, Aurélie, Yang, Jiseon, Franco, Karla, Nydam, Seth D., Forsyth, Rebecca J., Davis, Richard R., Gangaraju, Sandhya, Ott, C. Mark, Coyne, Carolyn B., Bissell, Mina J., Nickerson, Cheryl A., and Maurelli, Anthony T. Tue . "Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age". United States. https://doi.org/10.1128/IAI.00282-18. https://www.osti.gov/servlets/purl/1580337.
@article{osti_1580337,
title = {Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age},
author = {Barrila, Jennifer and Crabbé, Aurélie and Yang, Jiseon and Franco, Karla and Nydam, Seth D. and Forsyth, Rebecca J. and Davis, Richard R. and Gangaraju, Sandhya and Ott, C. Mark and Coyne, Carolyn B. and Bissell, Mina J. and Nickerson, Cheryl A. and Maurelli, Anthony T.},
abstractNote = {Tissues and organs provide the structural and biochemical landscapes upon which microbial pathogens and commensals function to regulate health and disease. While flat two-dimensional (2-D) monolayers composed of a single cell type have provided important insight into understanding host-pathogen interactions and infectious disease mechanisms, these reductionist models lack many essential features present in the native host microenvironment that are known to regulate infection, including three-dimensional (3-D) architecture, multicellular complexity, commensal microbiota, gas exchange and nutrient gradients, and physiologically relevant biomechanical forces (e.g., fluid shear, stretch, compression). Here, a major challenge in tissue engineering for infectious disease research is recreating this dynamic 3-D microenvironment (biological, chemical, and physical/mechanical) to more accurately model the initiation and progression of host-pathogen interactions in the laboratory. Here we review selected 3-D models of human intestinal mucosa, which represent a major portal of entry for infectious pathogens and an important niche for commensal microbiota. We highlight seminal studies that have used these models to interrogate host-pathogen interactions and infectious disease mechanisms, and we present this literature in the appropriate historical context. Models discussed include 3-D organotypic cultures engineered in the rotating wall vessel (RWV) bioreactor, extracellular matrix (ECM)-embedded/organoid models, and organ-on-a-chip (OAC) models. Collectively, these technologies provide a more physiologically relevant and predictive framework for investigating infectious disease mechanisms and antimicrobial therapies at the intersection of the host, microbe, and their local microenvironments.},
doi = {10.1128/IAI.00282-18},
journal = {Infection and Immunity},
number = 11,
volume = 86,
place = {United States},
year = {Tue Sep 04 00:00:00 EDT 2018},
month = {Tue Sep 04 00:00:00 EDT 2018}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record

Citation Metrics:
Cited by: 84 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

The Cytosolic Bacterial Peptidoglycan Sensor Nod2 Affords Stem Cell Protection and Links Microbes to Gut Epithelial Regeneration
journal, June 2014


Closing the phenotypic gap between transformed neuronal cell lines in culture and untransformed neurons
journal, September 2008


Bacteria in the Vaginal Microbiome Alter the Innate Immune Response and Barrier Properties of the Human Vaginal Epithelia in a Species-Specific Manner
journal, January 2014

  • Doerflinger, Sylvie Y.; Throop, Andrea L.; Herbst-Kralovetz, Melissa M.
  • The Journal of Infectious Diseases, Vol. 209, Issue 12
  • DOI: 10.1093/infdis/jiu004

In vitro generation of human pluripotent stem cell derived lung organoids
journal, March 2015


In Search of the Pivot Point of Mechanotransduction: Mechanosensing of Stem Cells
journal, January 2014


Enhanced cardiac differentiation of mouse embryonic stem cells by use of the slow-turning, lateral vessel (STLV) bioreactor
journal, April 2011

  • Rungarunlert, Sasitorn; Klincumhom, Nuttha; Bock, Istvan
  • Biotechnology Letters, Vol. 33, Issue 8
  • DOI: 10.1007/s10529-011-0614-8

Intestinal epithelial cell polarity defects in disease: lessons from microvillus inclusion disease
journal, February 2018

  • Schneeberger, Kerstin; Roth, Sabrina; Nieuwenhuis, Edward E. S.
  • Disease Models & Mechanisms, Vol. 11, Issue 2
  • DOI: 10.1242/dmm.031088

Morphologic differentiation of colon carcinoma cell lines HT-29 and HT-29KM in rotating-wall vessels
journal, January 1992

  • Goodwin, Thomas J.; Milburn Jessup, J.; Wolf, David A.
  • In Vitro Cellular & Developmental Biology - Animal, Vol. 28, Issue 1
  • DOI: 10.1007/BF02631079

Novel anisotropic engineered cardiac tissues: Studies of electrical propagation
journal, October 2007

  • Bursac, Nenad; Loo, Yihua; Leong, Kam
  • Biochemical and Biophysical Research Communications, Vol. 361, Issue 4
  • DOI: 10.1016/j.bbrc.2007.07.138

Investigation of simulated microgravity effects on Streptococcus mutans physiology and global gene expression
journal, January 2017


Junction Adhesion Molecule Is a Receptor for Reovirus
journal, February 2001


Invasion of Human Tissue Ex Vivo by Borrelia burgdorferi
journal, May 2005

  • Duray, Paul H.; Yin, Shu‐Rong; Ito, Yoshinori
  • The Journal of Infectious Diseases, Vol. 191, Issue 10
  • DOI: 10.1086/429632

Development and Characterization of a Three-Dimensional Organotypic Human Vaginal Epithelial Cell Model1
journal, March 2010


Reconstituting Organ-Level Lung Functions on a Chip
journal, June 2010


Endothelialized Networks with a Vascular Geometry in Microfabricated Poly(dimethyl siloxane)
journal, December 2004


A Human Breathing Lung-on-a-Chip
journal, March 2015


CD44 Plays a Functional Role in Helicobacter pylori-induced Epithelial Cell Proliferation
journal, February 2015


Acoustically detectable cellular-level lung injury induced by fluid mechanical stresses in microfluidic airway systems
journal, November 2007

  • Huh, D.; Fujioka, H.; Tung, Y. -C.
  • Proceedings of the National Academy of Sciences, Vol. 104, Issue 48
  • DOI: 10.1073/pnas.0610868104

Salmonella - the ultimate insider. Salmonella virulence factors that modulate intracellular survival
journal, November 2009


The Impact of the Gut Microbiota on Human Health: An Integrative View
journal, March 2012


Microgravity as a Novel Environmental Signal Affecting Salmonella enterica Serovar Typhimurium Virulence
journal, June 2000


Microfluidic organ-on-chip technology for blood-brain barrier research
journal, January 2016


Laminin regulates PI3K basal localization and activation to sustain STAT5 activation
journal, November 2010

  • Xu, Ren; Spencer, Virginia A.; Groesser, Dinah Levy
  • Cell Cycle, Vol. 9, Issue 21
  • DOI: 10.4161/cc.9.21.13578

Low-shear modeled microgravity: a global environmental regulatory signal affecting bacterial gene expression, physiology, and pathogenesis
journal, July 2003


Characterization of a microfluidic in vitro model of the blood-brain barrier (μBBB)
journal, January 2012


Matrix Mechanics and Fluid Shear Stress Control Stem Cells Fate in Three Dimensional Microenvironment
journal, May 2013


Enterohemorrhagic Escherichia coli Reduces Mucus and Intermicrovillar Bridges in Human Stem Cell-Derived Colonoids
journal, January 2016

  • In, Julie; Foulke-Abel, Jennifer; Zachos, Nicholas C.
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 2, Issue 1
  • DOI: 10.1016/j.jcmgh.2015.10.001

Salmonella Transforms Follicle-Associated Epithelial Cells into M Cells to Promote Intestinal Invasion
journal, November 2012


Epithelial cell polarity affects susceptibility to Pseudomonas aeruginosa invasion and cytotoxicity.
journal, January 1997


Characterization of microfluidic human epidermal keratinocyte culture
journal, March 2008

  • O’Neill, Adrian T.; Monteiro-Riviere, Nancy A.; Walker, Glenn M.
  • Cytotechnology, Vol. 56, Issue 3
  • DOI: 10.1007/s10616-008-9149-9

In Vitro and In Vivo Model Systems for Studying Enteropathogenic Escherichia coli Infections
journal, March 2013

  • Law, R. J.; Gur-Arie, L.; Rosenshine, I.
  • Cold Spring Harbor Perspectives in Medicine, Vol. 3, Issue 3
  • DOI: 10.1101/cshperspect.a009977

Spatial variation of the colonic microbiota in patients with ulcerative colitis and control volunteers
journal, January 2015


Influenza Virus Infects Epithelial Stem/Progenitor Cells of the Distal Lung: Impact on Fgfr2b-Driven Epithelial Repair
journal, June 2016


The nocturnal jejunal migrating motor complex: defining normal ranges by study of 51 healthy adult volunteers and meta-analysis
journal, October 2006


Redefining the In Vivo Origin of Metanephric Nephron Progenitors Enables Generation of Complex Kidney Structures from Pluripotent Stem Cells
journal, January 2014


Induction of Attachment-Independent Biofilm Formation and Repression of hfq Expression by Low-Fluid-Shear Culture of Staphylococcus aureus
journal, July 2011

  • Castro, Sarah L.; Nelman-Gonzalez, Mayra; Nickerson, Cheryl A.
  • Applied and Environmental Microbiology, Vol. 77, Issue 18
  • DOI: 10.1128/AEM.00175-11

Epithelium damage and protection during reopening of occluded airways in a physiologic microfluidic pulmonary airway model
journal, April 2011

  • Tavana, Hossein; Zamankhan, Parsa; Christensen, Paul J.
  • Biomedical Microdevices, Vol. 13, Issue 4
  • DOI: 10.1007/s10544-011-9543-5

Contributions of microbiome and mechanical deformation to intestinal bacterial overgrowth and inflammation in a human gut-on-a-chip
journal, December 2015

  • Kim, Hyun Jung; Li, Hu; Collins, James J.
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 1
  • DOI: 10.1073/pnas.1522193112

The Motogenic Effects of Cyclic Mechanical Strain on Intestinal Epithelial Monolayer Wound Closure Are Matrix Dependent
journal, October 2006


Generation of Multipotent Foregut Stem Cells from Human Pluripotent Stem Cells
journal, October 2013


Organoids as an in vitro model of human development and disease
journal, February 2016

  • Fatehullah, Aliya; Tan, Si Hui; Barker, Nick
  • Nature Cell Biology, Vol. 18, Issue 3
  • DOI: 10.1038/ncb3312

3-D Intestinal Scaffolds for Evaluating the Therapeutic Potential of Probiotics
journal, February 2014

  • Costello, Cait M.; Sorna, Rachel M.; Goh, Yih-Lin
  • Molecular Pharmaceutics, Vol. 11, Issue 7
  • DOI: 10.1021/mp5001422

Glia co-culture with neurons in microfluidic platforms promotes the formation and stabilization of synaptic contacts
journal, January 2013

  • Shi, Mingjian; Majumdar, Devi; Gao, Yandong
  • Lab on a Chip, Vol. 13, Issue 15
  • DOI: 10.1039/c3lc50249j

Human Enteroids/Colonoids and Intestinal Organoids Functionally Recapitulate Normal Intestinal Physiology and Pathophysiology
journal, December 2015

  • Zachos, Nicholas C.; Kovbasnjuk, Olga; Foulke-Abel, Jennifer
  • Journal of Biological Chemistry, Vol. 291, Issue 8
  • DOI: 10.1074/jbc.R114.635995

The Antibacterial Lectin RegIII  Promotes the Spatial Segregation of Microbiota and Host in the Intestine
journal, October 2011


Human Clostridium difficile infection: altered mucus production and composition
journal, March 2015

  • Engevik, Melinda A.; Yacyshyn, Mary Beth; Engevik, Kristen A.
  • American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 308, Issue 6
  • DOI: 10.1152/ajpgi.00091.2014

Gut-on-a-Chip microenvironment induces human intestinal cells to undergo villus differentiation
journal, January 2013

  • Kim, Hyun Jung; Ingber, Donald E.
  • Integrative Biology, Vol. 5, Issue 9
  • DOI: 10.1039/c3ib40126j

Stem cell-derived organoids and their application for medical research and patient treatment
journal, April 2017


Mycophenolic acid potently inhibits rotavirus infection with a high barrier to resistance development
journal, September 2016


Microbial Responses to Microgravity and Other Low-Shear Environments
journal, June 2004


A hydrodynamic mechanosensory hypothesis for brush border microvilli
journal, October 2000


Modeling infectious diseases and host-microbe interactions in gastrointestinal organoids
journal, December 2016


BBB ON CHIP: microfluidic platform to mechanically and biochemically modulate blood-brain barrier function
journal, September 2012


Three-dimensional Huh7 cell culture system for the study of Hepatitis C virus infection
journal, January 2009

  • Sainz, Bruno; TenCate, Veronica; Uprichard, Susan L.
  • Virology Journal, Vol. 6, Issue 1
  • DOI: 10.1186/1743-422X-6-103

Three-dimensional growth patterns of various human tumor cell lines in simulated microgravity of a NASA bioreactor
journal, June 1997

  • Ingram, M.; Techy, G. B.; Saroufeem, R.
  • In Vitro Cellular & Developmental Biology - Animal, Vol. 33, Issue 6
  • DOI: 10.1007/s11626-997-0064-8

A three-dimensional tissue culture model for the study of attach and efface lesion formation by enteropathogenic and enterohaemorrhagic Escherichia coli
journal, December 2005


Organoid Models of Human Gastrointestinal Development and Disease
journal, May 2016


The Mechanical World of Bacteria
journal, May 2015


Expression of Human Decay-Accelerating Factor on Intestinal Epithelium of Transgenic Mice Does Not Facilitate Infection by the Enteral Route
journal, February 2015

  • Pan, Jieyan; Zhang, Lili; Odenwald, Matthew A.
  • Journal of Virology, Vol. 89, Issue 8
  • DOI: 10.1128/JVI.03468-14

Of Extracellular Matrix, Scaffolds, and Signaling: Tissue Architecture Regulates Development, Homeostasis, and Cancer
journal, November 2006


Role of Hfq in an animal–microbe symbiosis under simulated microgravity conditions
journal, October 2013

  • Grant, Kyle C.; Khodadad, Christina L. M.; Foster, Jamie S.
  • International Journal of Astrobiology, Vol. 13, Issue 1
  • DOI: 10.1017/S1473550413000359

Wnt/β-catenin promotes gastric fundus specification in mice and humans
journal, January 2017

  • McCracken, Kyle W.; Aihara, Eitaro; Martin, Baptiste
  • Nature, Vol. 541, Issue 7636
  • DOI: 10.1038/nature21021

The Actin Cytoskeleton as a Barrier to Virus Infection of Polarized Epithelial Cells
journal, December 2011

  • Delorme-Axford, Elizabeth; Coyne, Carolyn B.
  • Viruses, Vol. 3, Issue 12
  • DOI: 10.3390/v3122462

IMMUNOLOGY: Keeping the Gut Microflora at Bay
journal, March 2004


Subversion of Mucosal Barrier Polarity by Pseudomonas Aeruginosa
journal, January 2011


Role of mechanical stress in regulating airway surface hydration and mucus clearance rates
journal, November 2008


Human intestinal organoids express histo-blood group antigens, bind norovirus VLPs, and support limited norovirus replication
journal, October 2017


Microfluidic Cardiac Cell Culture Model (μCCCM)
journal, September 2010

  • Giridharan, Guruprasad A.; Nguyen, Mai-Dung; Estrada, Rosendo
  • Analytical Chemistry, Vol. 82, Issue 18
  • DOI: 10.1021/ac1012893

A murine tumor producing a matrix of basement membrane
journal, January 1977


Intestinal organoids and personalized medicine in cystic fibrosis: a successful patient-oriented research collaboration
journal, January 2016

  • Noordhoek, Jacquelien; Gulmans, Vincent; van der Ent, Kors
  • Current Opinion in Pulmonary Medicine, Vol. 22, Issue 6
  • DOI: 10.1097/MCP.0000000000000315

Soft Lithography in Biology and Biochemistry
journal, August 2001

  • Whitesides, George M.; Ostuni, Emanuele; Takayama, Shuichi
  • Annual Review of Biomedical Engineering, Vol. 3, Issue 1
  • DOI: 10.1146/annurev.bioeng.3.1.335

Salmonella -infected crypt-derived intestinal organoid culture system for host-bacterial interactions
journal, September 2014

  • Zhang, Yong-Guo; Wu, Shaoping; Xia, Yinglin
  • Physiological Reports, Vol. 2, Issue 9
  • DOI: 10.14814/phy2.12147

Paradigms for Mechanical Signal Transduction in the Intestinal Epithelium
journal, January 2003


Three-dimensional organotypic models of human colonic epithelium to study the early stages of enteric salmonellosis
journal, June 2006


Development of a Multicellular Three-dimensional Organotypic Model of the Human Intestinal Mucosa Grown Under Microgravity
journal, January 2016

  • Salerno-Goncalves, Rosangela; Fasano, Alessio; Sztein, Marcelo B.
  • Journal of Visualized Experiments, Issue 113
  • DOI: 10.3791/54148

A small intestinal organoid model of non-invasive enteric pathogen–epithelial cell interactions
journal, August 2014

  • Wilson, S. S.; Tocchi, A.; Holly, M. K.
  • Mucosal Immunology, Vol. 8, Issue 2
  • DOI: 10.1038/mi.2014.72

Emulating human microcapillaries in a multi-organ-chip platform
journal, December 2015


Crosstalk between H9N2 avian influenza virus and crypt-derived intestinal organoids
journal, November 2017


Recellularization of Decellularized Lung Scaffolds Is Enhanced by Dynamic Suspension Culture
journal, May 2015


Cellular mechanotransduction: putting all the pieces together again
journal, May 2006


Zonation related function and ubiquitination regulation in human hepatocellular carcinoma cells in dynamic vs. static culture conditions
journal, January 2012


Modelling human development and disease in pluripotent stem-cell-derived gastric organoids
journal, October 2014

  • McCracken, Kyle W.; Catá, Emily M.; Crawford, Calyn M.
  • Nature, Vol. 516, Issue 7531
  • DOI: 10.1038/nature13863

Cell Polarization and Epigenetic Status Shape the Heterogeneous Response to Type III Interferons in Intestinal Epithelial Cells
journal, June 2017

  • Bhushal, Sudeep; Wolfsmüller, Markus; Selvakumar, Tharini A.
  • Frontiers in Immunology, Vol. 8
  • DOI: 10.3389/fimmu.2017.00671

Enteroviruses infect human enteroids and induce antiviral signaling in a cell lineage-specific manner
journal, January 2017

  • Drummond, Coyne G.; Bolock, Alexa M.; Ma, Congrong
  • Proceedings of the National Academy of Sciences, Vol. 114, Issue 7
  • DOI: 10.1073/pnas.1617363114

Sustained in vitro intestinal epithelial culture within a Wnt-dependent stem cell niche
journal, April 2009

  • Ootani, Akifumi; Li, Xingnan; Sangiorgi, Eugenio
  • Nature Medicine, Vol. 15, Issue 6
  • DOI: 10.1038/nm.1951

Remodelling the extracellular matrix in development and disease
journal, November 2014

  • Bonnans, Caroline; Chou, Jonathan; Werb, Zena
  • Nature Reviews Molecular Cell Biology, Vol. 15, Issue 12
  • DOI: 10.1038/nrm3904

Gastrointestinal Organoids: Understanding the Molecular Basis of the Host–Microbe Interface
journal, March 2017

  • Hill, David R.; Spence, Jason R.
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 3, Issue 2
  • DOI: 10.1016/j.jcmgh.2016.11.007

Extracellular Matrix Degradation and Remodeling in Development and Disease
journal, September 2011


Virus-Induced Abl and Fyn Kinase Signals Permit Coxsackievirus Entry through Epithelial Tight Junctions
journal, January 2006


Novel Quantitative Biosystem for Modeling Physiological Fluid Shear Stress on Cells
journal, December 2006

  • Nauman, E. A.; Ott, C. M.; Sander, E.
  • Applied and Environmental Microbiology, Vol. 73, Issue 3
  • DOI: 10.1128/AEM.02428-06

The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction
journal, December 2001

  • Cohen, C. J.; Shieh, J. T. C.; Pickles, R. J.
  • Proceedings of the National Academy of Sciences, Vol. 98, Issue 26
  • DOI: 10.1073/pnas.261452898

M Cell Differentiation: Distinct Lineage or Phenotypic Transition? Salmonella Provides Answers
journal, November 2012


A Human Disease Model of Drug Toxicity–Induced Pulmonary Edema in a Lung-on-a-Chip Microdevice
journal, November 2012

  • Huh, Dongeun; Leslie, Daniel C.; Matthews, Benjamin D.
  • Science Translational Medicine, Vol. 4, Issue 159
  • DOI: 10.1126/scitranslmed.3004249

Bacterial mechanotransduction
journal, April 2017


Capturing complex 3D tissue physiology in vitro
journal, March 2006

  • Griffith, Linda G.; Swartz, Melody A.
  • Nature Reviews Molecular Cell Biology, Vol. 7, Issue 3
  • DOI: 10.1038/nrm1858

Liver-Specific Functional Studies in a Microfluidic Array of Primary Mammalian Hepatocytes
journal, July 2006

  • Kane, Bartholomew J.; Zinner, Michael J.; Yarmush, Martin L.
  • Analytical Chemistry, Vol. 78, Issue 13
  • DOI: 10.1021/ac051856v

A novel human gastric primary cell culture system for modelling Helicobacter pylori infection in vitro
journal, December 2014


The effects of mechanical forces on intestinal physiology and pathology
journal, August 2009


Cerebral organoids model human brain development and microcephaly
journal, August 2013

  • Lancaster, Madeline A.; Renner, Magdalena; Martin, Carol-Anne
  • Nature, Vol. 501, Issue 7467
  • DOI: 10.1038/nature12517

Salmonella Manipulation of Host Signaling Pathways Provokes Cellular Transformation Associated with Gallbladder Carcinoma
journal, June 2015


Organoids: A historical perspective of thinking in three dimensions
journal, December 2016

  • Simian, Marina; Bissell, Mina J.
  • The Journal of Cell Biology, Vol. 216, Issue 1
  • DOI: 10.1083/jcb.201610056

Long-term Expansion of Epithelial Organoids From Human Colon, Adenoma, Adenocarcinoma, and Barrett's Epithelium
journal, November 2011


The Notch and Wnt pathways regulate stemness and differentiation in human fallopian tube organoids
journal, December 2015

  • Kessler, Mirjana; Hoffmann, Karen; Brinkmann, Volker
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms9989

Microgravity Culture Reduces Apoptosis and Increases the Differentiation of a Human Colorectal Carcinoma cell line
journal, January 2000


Evaluation of a microfluidic based cell culture platform with primary human hepatocytes for the prediction of hepatic clearance in human
journal, September 2009


Bacterial Adhesion to Target Cells Enhanced by Shear Force
journal, June 2002


Goodbye flat biology – time for the 3rd and the 4th dimensions
journal, January 2017


Microengineered physiological biomimicry: Organs-on-Chips
journal, January 2012

  • Huh, Dongeun; Torisawa, Yu-suke; Hamilton, Geraldine A.
  • Lab on a Chip, Vol. 12, Issue 12
  • DOI: 10.1039/c2lc40089h

Bacterial Stress Responses during Host Infection
journal, August 2016


Low-Shear Modeled Microgravity Alters the Salmonella enterica Serovar Typhimurium Stress Response in an RpoS-Independent Manner
journal, November 2002


Gastrointestinal organoids: How they gut it out
journal, December 2016


Fluid shear triggers microvilli formation via mechanosensitive activation of TRPV6
journal, November 2015

  • Miura, Shigenori; Sato, Koji; Kato-Negishi, Midori
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms9871

Mechanobiology and diseases of mechanotransduction
journal, January 2003


Reciprocal interactions of the intestinal microbiota and immune system
journal, September 2012

  • Maynard, Craig L.; Elson, Charles O.; Hatton, Robin D.
  • Nature, Vol. 489, Issue 7415
  • DOI: 10.1038/nature11551

Diversity, stability and resilience of the human gut microbiota
journal, September 2012

  • Lozupone, Catherine A.; Stombaugh, Jesse I.; Gordon, Jeffrey I.
  • Nature, Vol. 489, Issue 7415
  • DOI: 10.1038/nature11550

Of plasticity and specificity: dialectics of the microenvironment and macroenvironment and the organ phenotype: Of plasticity and specificity
journal, November 2013

  • Bhat, Ramray; Bissell, Mina J.
  • Wiley Interdisciplinary Reviews: Developmental Biology, Vol. 3, Issue 2
  • DOI: 10.1002/wdev.130

Analysis of Interactions of Salmonella Type Three Secretion Mutants with 3-D Intestinal Epithelial Cells
journal, December 2010


Replication of human noroviruses in stem cell-derived human enteroids
journal, August 2016


Small airway-on-a-chip enables analysis of human lung inflammation and drug responses in vitro
journal, December 2015

  • Benam, Kambez H.; Villenave, Remi; Lucchesi, Carolina
  • Nature Methods, Vol. 13, Issue 2
  • DOI: 10.1038/nmeth.3697

A Three-Dimensional Cell Culture System To Model RNA Virus Infections at the Blood-Brain Barrier
journal, June 2017


Microbial pathogenesis and cytoskeletal function
journal, April 2003


The tumor microenvironment is a dominant force in multidrug resistance
journal, February 2012


Liver-Tumor Hybrid Organoids for Modeling Tumor Growth and Drug Response In Vitro
journal, March 2015

  • Skardal, Aleksander; Devarasetty, Mahesh; Rodman, Christopher
  • Annals of Biomedical Engineering, Vol. 43, Issue 10
  • DOI: 10.1007/s10439-015-1298-3

Use of the rotating wall vessel technology to study the effect of shear stress on growth behaviour of Pseudomonas aeruginosa PA01
journal, August 2008


The intestinal epithelium tuft cells: specification and function
journal, April 2012

  • Gerbe, François; Legraverend, Catherine; Jay, Philippe
  • Cellular and Molecular Life Sciences, Vol. 69, Issue 17
  • DOI: 10.1007/s00018-012-0984-7

Engineered In Vitro Disease Models
journal, January 2015


Advantages and challenges of microfluidic cell culture in polydimethylsiloxane devices
journal, January 2015

  • Halldorsson, Skarphedinn; Lucumi, Edinson; Gómez-Sjöberg, Rafael
  • Biosensors and Bioelectronics, Vol. 63
  • DOI: 10.1016/j.bios.2014.07.029

Regional specialization within the intestinal immune system
journal, September 2014

  • Mowat, Allan M.; Agace, William W.
  • Nature Reviews Immunology, Vol. 14, Issue 10
  • DOI: 10.1038/nri3738

Air–liquid interface cultures enhance the oxygen supply and trigger the structural and functional differentiation of intestinal porcine epithelial cells (IPEC)
journal, June 2011

  • Nossol, Constanze; Diesing, A. -K.; Walk, N.
  • Histochemistry and Cell Biology, Vol. 136, Issue 1
  • DOI: 10.1007/s00418-011-0826-y

From 3D cell culture to organs-on-chips
journal, December 2011

  • Huh, Dongeun; Hamilton, Geraldine A.; Ingber, Donald E.
  • Trends in Cell Biology, Vol. 21, Issue 12
  • DOI: 10.1016/j.tcb.2011.09.005

Modeling tissue-specific signaling and organ function in three dimensions
journal, June 2003

  • Schmeichel, K. L.
  • Journal of Cell Science, Vol. 116, Issue 12
  • DOI: 10.1242/jcs.00503

Artificial three-dimensional niches deconstruct pancreas development in vitro
journal, October 2013

  • Greggio, C.; De Franceschi, F.; Figueiredo-Larsen, M.
  • Development, Vol. 140, Issue 21
  • DOI: 10.1242/dev.096628

Tensegrity-based mechanosensing from macro to micro
journal, June 2008


The gastrointestinal microbiome – Functional interference between stomach and intestine
journal, December 2014

  • Lopetuso, Loris R.; Scaldaferri, Franco; Franceschi, Francesco
  • Best Practice & Research Clinical Gastroenterology, Vol. 28, Issue 6
  • DOI: 10.1016/j.bpg.2014.10.004

Pseudomonas aeruginosa strains possess specific adhesins for laminin.
journal, January 1996


Mechanical Control of Tissue Morphogenesis
journal, August 2008


Generating human intestinal tissue from pluripotent stem cells in vitro
journal, November 2011

  • McCracken, Kyle W.; Howell, Jonathan C.; Wells, James M.
  • Nature Protocols, Vol. 6, Issue 12
  • DOI: 10.1038/nprot.2011.410

Making cardiomyocytes: How mechanical stimulation can influence differentiation of pluripotent stem cells
journal, September 2013

  • Geuss, Laura R.; Suggs, Laura J.
  • Biotechnology Progress, Vol. 29, Issue 5
  • DOI: 10.1002/btpr.1794

Engineering of a Multicellular Organotypic Model of the Human Intestinal Mucosa
journal, August 2011


In Vitro Expansion of Human Gastric Epithelial Stem Cells and Their Responses to Bacterial Infection
journal, January 2015


Directed differentiation of human pluripotent stem cells into intestinal tissue in vitro
journal, December 2010

  • Spence, Jason R.; Mayhew, Christopher N.; Rankin, Scott A.
  • Nature, Vol. 470, Issue 7332
  • DOI: 10.1038/nature09691

Intestinal organoids model human responses to infection by commensal and Shiga toxin producing Escherichia coli
journal, June 2017


Chondrogenesis in aggregates of embryonic limb cells grown in a Rotating Wall Vessel
journal, January 1996


Intestinal epithelial cells: regulators of barrier function and immune homeostasis
journal, February 2014

  • Peterson, Lance W.; Artis, David
  • Nature Reviews Immunology, Vol. 14, Issue 3
  • DOI: 10.1038/nri3608

Tissue architecture: the ultimate regulator of epithelial function?
journal, June 1998

  • Hagios, Carmen; Lochter, André; Bissell, Mina J.
  • Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 353, Issue 1370
  • DOI: 10.1098/rstb.1998.0250

Effects of microgravity on the embryonic pancreas
journal, November 1999

  • Rose, Michael I.; Brown, Dale C.; Pellis, Neil R.
  • In Vitro Cellular & Developmental Biology - Animal, Vol. 35, Issue 10
  • DOI: 10.1007/s11626-999-0092-7

A lung-on-a-chip array with an integrated bio-inspired respiration mechanism
journal, January 2015

  • Stucki, Andreas O.; Stucki, Janick D.; Hall, Sean R. R.
  • Lab on a Chip, Vol. 15, Issue 5
  • DOI: 10.1039/C4LC01252F

Preservation of glucose responsiveness in human islets maintained in a rotational cell culture system
journal, June 2005

  • Murray, Hilary E.; Paget, Michelle B.; Downing, Richard
  • Molecular and Cellular Endocrinology, Vol. 238, Issue 1-2
  • DOI: 10.1016/j.mce.2005.03.014

Microfluidic organs-on-chips
journal, August 2014

  • Bhatia, Sangeeta N.; Ingber, Donald E.
  • Nature Biotechnology, Vol. 32, Issue 8
  • DOI: 10.1038/nbt.2989

Detection of Epithelial‐Cell Injury, and Quantification of Infection, in the HCT‐8 Organoid Model of Cryptosporidiosis
journal, July 2008

  • Alcantara Warren, Cirle; Destura, Raul V.; Sevilleja, Jesus Emmanuel A. D.
  • The Journal of Infectious Diseases, Vol. 198, Issue 1
  • DOI: 10.1086/588819

Organs-on-a-chip for drug discovery
journal, October 2013

  • Selimović, Šeila; Dokmeci, Mehmet R.; Khademhosseini, Ali
  • Current Opinion in Pharmacology, Vol. 13, Issue 5
  • DOI: 10.1016/j.coph.2013.06.005

Identification of stem cells in small intestine and colon by marker gene Lgr5
journal, October 2007

  • Barker, Nick; van Es, Johan H.; Kuipers, Jeroen
  • Nature, Vol. 449, Issue 7165
  • DOI: 10.1038/nature06196

Innate immune recognition of the microbiota promotes host-microbial symbiosis
journal, June 2013

  • Chu, Hiutung; Mazmanian, Sarkis K.
  • Nature Immunology, Vol. 14, Issue 7
  • DOI: 10.1038/ni.2635

Role and Regulation of  s in General Resistance Conferred by Low-Shear Simulated Microgravity in Escherichia coli
journal, December 2004


Human-on-a-chip design strategies and principles for physiologically based pharmacokinetics/pharmacodynamics modeling
journal, January 2015

  • Abaci, Hasan Erbil; Shuler, Michael L.
  • Integrative Biology, Vol. 7, Issue 4
  • DOI: 10.1039/C4IB00292J

Cytoskeletal tension induces the polarized architecture of the nucleus
journal, April 2015


A Three-Dimensional Cell Culture Model To Study Enterovirus Infection of Polarized Intestinal Epithelial Cells
journal, November 2015


Induction of three-dimensional assembly of human liver cells by simulated microgravity
journal, October 1999

  • Khaoustov, Vladimir I.; Darlington, Gretchen J.; Soriano, Humberto E.
  • In Vitro Cellular & Developmental Biology - Animal, Vol. 35, Issue 9
  • DOI: 10.1007/s11626-999-0060-2

Connecting the nucleus to the cytoskeleton by SUN–KASH bridges across the nuclear envelope
journal, February 2013


Conservation of the Low-shear Modeled Microgravity Response in Enterobacteriaceae and Analysis of the trp Genes in this Response
journal, June 2014


Demonstration of mechanical connections between integrins, cytoskeletal filaments, and nucleoplasm that stabilize nuclear structure
journal, February 1997

  • Maniotis, A. J.; Chen, C. S.; Ingber, D. E.
  • Proceedings of the National Academy of Sciences, Vol. 94, Issue 3
  • DOI: 10.1073/pnas.94.3.849

Ex vivo 2D and 3D HSV-2 infection model using human normal vaginal epithelial cells
journal, January 2017


Innate Immunity in the Respiratory Epithelium
journal, August 2011

  • Parker, Dane; Prince, Alice
  • American Journal of Respiratory Cell and Molecular Biology, Vol. 45, Issue 2
  • DOI: 10.1165/rcmb.2011-0011RT

Human intestinal tract serves as an alternative infection route for Middle East respiratory syndrome coronavirus
journal, November 2017


Control of pathogens and pathobionts by the gut microbiota
journal, June 2013

  • Kamada, Nobuhiko; Chen, Grace Y.; Inohara, Naohiro
  • Nature Immunology, Vol. 14, Issue 7
  • DOI: 10.1038/ni.2608

The Biology of Intestinal Immunoglobulin A Responses
journal, June 2008


A Microscale In Vitro Physiological Model of the Liver: Predictive Screens for Drug Metabolism and Enzyme Induction
journal, December 2005


How does the extracellular matrix direct gene expression?
journal, November 1982


Characterization of Escherichia coli MG1655 grown in a low-shear modeled microgravity environment
journal, January 2007


The immune geography of IgA induction and function
journal, December 2007

  • Macpherson, A. J.; McCoy, K. D.; Johansen, F-E
  • Mucosal Immunology, Vol. 1, Issue 1
  • DOI: 10.1038/mi.2007.6

On chip porous polymer membranes for integration of gastrointestinal tract epithelium with microfluidic ‘body-on-a-chip’ devices
journal, July 2012

  • Esch, Mandy Brigitte; Sung, Jong Hwan; Yang, Jennifer
  • Biomedical Microdevices, Vol. 14, Issue 5
  • DOI: 10.1007/s10544-012-9669-0

Interaction of Salmonella enterica Serovar Typhimurium with Intestinal Organoids Derived from Human Induced Pluripotent Stem Cells
journal, May 2015

  • Forbester, Jessica L.; Goulding, David; Vallier, Ludovic
  • Infection and Immunity, Vol. 83, Issue 7
  • DOI: 10.1128/IAI.00161-15

Simultaneous Generation of Gradients with Gradually Changed Slope in a Microfluidic Device for Quantifying Axon Response
journal, August 2013

  • Xiao, Rong-Rong; Zeng, Wen-Juan; Li, Yu-Tao
  • Analytical Chemistry, Vol. 85, Issue 16
  • DOI: 10.1021/ac4022055

Human Fetal-Derived Enterospheres Provide Insights on Intestinal Development and a Novel Model to Study Necrotizing Enterocolitis (NEC)
journal, January 2018

  • Senger, Stefania; Ingano, Laura; Freire, Rachel
  • Cellular and Molecular Gastroenterology and Hepatology, Vol. 5, Issue 4
  • DOI: 10.1016/j.jcmgh.2018.01.014

Patterning osteogenesis by inducible gene expression in microfluidic culture systems
journal, January 2011

  • Zhang, Yue; Gazit, Zulma; Pelled, Gadi
  • Integr. Biol., Vol. 3, Issue 1
  • DOI: 10.1039/C0IB00053A

The two mucus layers of colon are organized by the MUC2 mucin, whereas the outer layer is a legislator of host-microbial interactions
journal, June 2010

  • Johansson, M. E. V.; Larsson, J. M. H.; Hansson, G. C.
  • Proceedings of the National Academy of Sciences, Vol. 108, Issue Supplement_1
  • DOI: 10.1073/pnas.1006451107

Helicobacter pylori Activates and Expands Lgr5+ Stem Cells Through Direct Colonization of the Gastric Glands
journal, June 2015


Microfabrication of human organs-on-chips
journal, October 2013

  • Huh, Dongeun; Kim, Hyun Jung; Fraser, Jacob P.
  • Nature Protocols, Vol. 8, Issue 11
  • DOI: 10.1038/nprot.2013.137

Human gut-on-a-chip inhabited by microbial flora that experiences intestinal peristalsis-like motions and flow
journal, January 2012

  • Kim, Hyun Jung; Huh, Dongeun; Hamilton, Geraldine
  • Lab on a Chip, Vol. 12, Issue 12
  • DOI: 10.1039/c2lc40074j

Interplay between metabolic identities in the intestinal crypt supports stem cell function
journal, March 2017

  • Rodríguez-Colman, Maria J.; Schewe, Matthias; Meerlo, Maaike
  • Nature, Vol. 543, Issue 7645
  • DOI: 10.1038/nature21673

Human mini-guts: new insights into intestinal physiology and host–pathogen interactions
journal, September 2016

  • In, Julie G.; Foulke-Abel, Jennifer; Estes, Mary K.
  • Nature Reviews Gastroenterology & Hepatology, Vol. 13, Issue 11
  • DOI: 10.1038/nrgastro.2016.142

Enhancement of Matrix Production and Cell Proliferation in Human Annulus Cells Under Bioreactor Culture
journal, June 2011


Deep nuclear invaginations are linked to cytoskeletal filaments – integrated bioimaging of epithelial cells in 3D culture
journal, August 2016

  • Jorgens, Danielle M.; Inman, Jamie L.; Wojcik, Michal
  • Journal of Cell Science, Vol. 130, Issue 1
  • DOI: 10.1242/jcs.190967

Three-dimensional co-cultures of human endothelial cells and embryonic stem cell-derived pericytes inside a microfluidic device
journal, January 2013

  • van der Meer, Andries D.; Orlova, Valeria V.; ten Dijke, Peter
  • Lab on a Chip, Vol. 13, Issue 18
  • DOI: 10.1039/c3lc50435b

Rotating-Wall Vessel Coculture of Small Intestine as a Prelude to Tissue Modeling: Aspects of Simulated Microgravity
journal, February 1993

  • Goodwin, T. J.; Schroeder, W. F.; Wolf, D. A.
  • Experimental Biology and Medicine, Vol. 202, Issue 2
  • DOI: 10.3181/00379727-202-43525

Helicobacter pylori -induced gastric pathology: insights from in vivo and ex vivo models
journal, February 2017

  • Burkitt, Michael D.; Duckworth, Carrie A.; Williams, Jonathan M.
  • Disease Models & Mechanisms, Vol. 10, Issue 2
  • DOI: 10.1242/dmm.027649

Integration and application of vitrified collagen in multilayered microfluidic devices for corneal microtissue culture
journal, January 2009

  • Puleo, Christopher M.; McIntosh Ambrose, Winnette; Takezawa, Toshiaki
  • Lab on a Chip, Vol. 9, Issue 22
  • DOI: 10.1039/b908332d

Personalized Proteome Profiles of Healthy and Tumor Human Colon Organoids Reveal Both Individual Diversity and Basic Features of Colorectal Cancer
journal, January 2017


Peyer's Patches: The Immune Sensors of the Intestine
journal, January 2010

  • Jung, Camille; Hugot, Jean-Pierre; Barreau, Frédérick
  • International Journal of Inflammation, Vol. 2010
  • DOI: 10.4061/2010/823710

RIG-I/MAVS and STING signaling promote gut integrity during irradiation- and immune-mediated tissue injury
journal, April 2017

  • Fischer, Julius C.; Bscheider, Michael; Eisenkolb, Gabriel
  • Science Translational Medicine, Vol. 9, Issue 386
  • DOI: 10.1126/scitranslmed.aag2513

Lipopolysaccharide from Crypt-Specific Core Microbiota Modulates the Colonic Epithelial Proliferation-to-Differentiation Balance
journal, October 2017


Influence of Acellular Natural Lung Matrix on Murine Embryonic Stem Cell Differentiation and Tissue Formation
journal, August 2010


The origins and the future of microfluidics
journal, July 2006


Metabolic monitoring of the electrically stimulated single heart cell within a microfluidic platform
journal, January 2006

  • Cheng, Wei; Klauke, Norbert; Sedgwick, Helen
  • Lab on a Chip, Vol. 6, Issue 11
  • DOI: 10.1039/b608202e

Mycoplasma genitalium Infection Activates Cellular Host Defense and Inflammation Pathways in a 3-Dimensional Human Endocervical Epithelial Cell Model
journal, March 2013

  • McGowin, Chris L.; Radtke, Andrea L.; Abraham, Kyle
  • The Journal of Infectious Diseases, Vol. 207, Issue 12
  • DOI: 10.1093/infdis/jit101

Synthetic hydrogels for human intestinal organoid generation and colonic wound repair
journal, October 2017

  • Cruz-Acuña, Ricardo; Quirós, Miguel; Farkas, Attila E.
  • Nature Cell Biology, Vol. 19, Issue 11
  • DOI: 10.1038/ncb3632

A three-dimensional model of human lung development and disease from pluripotent stem cells
journal, April 2017

  • Chen, Ya-Wen; Huang, Sarah Xuelian; de Carvalho, Ana Luisa Rodrigues Toste
  • Nature Cell Biology, Vol. 19, Issue 5
  • DOI: 10.1038/ncb3510

The Bacterial Fimbrial Tip Acts as a Mechanical Force Sensor
journal, May 2011


The regulation of IgA class switching
journal, June 2008

  • Cerutti, Andrea
  • Nature Reviews Immunology, Vol. 8, Issue 6
  • DOI: 10.1038/nri2322

Bacteria and host interactions in the gut epithelial barrier
journal, December 2011

  • Ashida, Hiroshi; Ogawa, Michinaga; Kim, Minsoo
  • Nature Chemical Biology, Vol. 8, Issue 1
  • DOI: 10.1038/nchembio.741

In vitro expansion of single Lgr5+ liver stem cells induced by Wnt-driven regeneration
journal, January 2013

  • Huch, Meritxell; Dorrell, Craig; Boj, Sylvia F.
  • Nature, Vol. 494, Issue 7436
  • DOI: 10.1038/nature11826

In Vitro Cell Culture Infectivity Assay for Human Noroviruses
journal, March 2007

  • Straub, Timothy M.; Höner zu Bentrup, Kerstin; Coghlan, Patricia Orosz
  • Emerging Infectious Diseases, Vol. 13, Issue 3
  • DOI: 10.3201/eid1303.060549

Generation of tissue-engineered small intestine using embryonic stem cell-derived human intestinal organoids
journal, October 2015

  • Finkbeiner, S. R.; Freeman, J. J.; Wieck, M. M.
  • Biology Open, Vol. 4, Issue 11
  • DOI: 10.1242/bio.013235

The gut microbiota and host health: a new clinical frontier
journal, September 2015


Immune Responses to the Microbiota at the Intestinal Mucosal Surface
journal, September 2009


Frizzled proteins are colonic epithelial receptors for C. difficile toxin B
journal, September 2016


Use of a Rotating Bioreactor toward Tissue Engineering the Temporomandibular Joint Disc
journal, July 2005


A nomenclature for intestinal in vitro cultures
journal, June 2012

  • Stelzner, Matthias; Helmrath, Michael; Dunn, James C. Y.
  • American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 302, Issue 12
  • DOI: 10.1152/ajpgi.00493.2011

Cardiovascular Physiology During Fetal Development and Implications for Tissue Engineering
journal, February 2001


The relevance and potential roles of microphysiological systems in biology and medicine
journal, September 2014


Receptors in the Pseudomonas Aeruginosa Adherence to Injured and Repairing Airway Epithelium
journal, October 1996

  • de Bentzmann, Sophie; Plotkowski, Cristina; Puchelle, Edith
  • American Journal of Respiratory and Critical Care Medicine, Vol. 154, Issue 4_pt_2
  • DOI: 10.1164/ajrccm/154.4_Pt_2.S155

A microfluidic hepatic coculture platform for cell-based drug metabolism studies
journal, April 2010


The Human Microbiome Project
journal, October 2007

  • Turnbaugh, Peter J.; Ley, Ruth E.; Hamady, Micah
  • Nature, Vol. 449, Issue 7164
  • DOI: 10.1038/nature06244

Organoid culture systems to study host–pathogen interactions
journal, October 2017


Dynamin- and Lipid Raft-Dependent Entry of Decay-Accelerating Factor (DAF)-Binding and Non-DAF-Binding Coxsackieviruses into Nonpolarized Cells
journal, August 2009

  • Patel, K. P.; Coyne, C. B.; Bergelson, J. M.
  • Journal of Virology, Vol. 83, Issue 21
  • DOI: 10.1128/JVI.01016-09

The Impact of Simulated and Real Microgravity on Bone Cells and Mesenchymal Stem Cells
journal, January 2014

  • Ulbrich, Claudia; Wehland, Markus; Pietsch, Jessica
  • BioMed Research International, Vol. 2014
  • DOI: 10.1155/2014/928507

Co-culture of epithelial cells and bacteria for investigating host–pathogen interactions
journal, January 2010

  • Kim, Jeongyun; Hegde, Manjunath; Jayaraman, Arul
  • Lab Chip, Vol. 10, Issue 1
  • DOI: 10.1039/B911367C

Critical analysis of 3-D organoid in vitro cell culture models for high-throughput drug candidate toxicity assessments
journal, April 2014


The extracellular matrix at a glance
journal, December 2010

  • Frantz, C.; Stewart, K. M.; Weaver, V. M.
  • Journal of Cell Science, Vol. 123, Issue 24
  • DOI: 10.1242/jcs.023820

Loss of Paneth Cell Autophagy Causes Acute Susceptibility to Toxoplasma gondii-Mediated Inflammation
journal, February 2018

  • Burger, Elise; Araujo, Alessandra; López-Yglesias, Américo
  • Cell Host & Microbe, Vol. 23, Issue 2
  • DOI: 10.1016/j.chom.2018.01.001

Mechanosensing via cell-matrix adhesions in 3D microenvironments
journal, April 2016


Generation of multiciliated cells in functional airway epithelia from human induced pluripotent stem cells
journal, March 2014

  • Firth, A. L.; Dargitz, C. T.; Qualls, S. J.
  • Proceedings of the National Academy of Sciences, Vol. 111, Issue 17
  • DOI: 10.1073/pnas.1403470111

Fecal Microbiota Transplantation for Clostridium difficile Infection: Systematic Review and Meta-Analysis
journal, January 2013

  • Kassam, Zain; Lee, Christine H.; Yuan, Yuhong
  • American Journal of Gastroenterology, Vol. 108, Issue 4
  • DOI: 10.1038/ajg.2013.59

The Human Intestinal Microbiome in Health and Disease
journal, December 2016

  • Lynch, Susan V.; Pedersen, Oluf
  • New England Journal of Medicine, Vol. 375, Issue 24
  • DOI: 10.1056/NEJMra1600266

3D Printing of Organs-On-Chips
journal, January 2017


Persistence and Toxin Production by Clostridium difficile within Human Intestinal Organoids Result in Disruption of Epithelial Paracellular Barrier Function
journal, October 2014

  • Leslie, Jhansi L.; Huang, Sha; Opp, Judith S.
  • Infection and Immunity, Vol. 83, Issue 1
  • DOI: 10.1128/IAI.02561-14

Translating tissue culture results into animal models: the case of Salmonella typhimurium
journal, December 2003


Organs-on-chips with integrated electrodes for trans-epithelial electrical resistance (TEER) measurements of human epithelial barrier function
journal, January 2017

  • Henry, Olivier Y. F.; Villenave, Remi; Cronce, Michael J.
  • Lab on a Chip, Vol. 17, Issue 13
  • DOI: 10.1039/C7LC00155J

A Gutsy Task: Generating Intestinal Tissue from Human Pluripotent Stem Cells
journal, March 2013


Modeling Tissue Morphogenesis and Cancer in 3D
journal, August 2007


Effect of simulated microgravity and shear stress on microcin B17 production by Escherichia coli and on its excretion into the medium.
journal, January 1997


Organs-on-chips at the frontiers of drug discovery
journal, March 2015

  • Esch, Eric W.; Bahinski, Anthony; Huh, Dongeun
  • Nature Reviews Drug Discovery, Vol. 14, Issue 4
  • DOI: 10.1038/nrd4539

Mimicking the niche of lung epithelial stem cells and characterization of several effectors of their in vitro behavior
journal, July 2015


Modeling rotavirus infection and antiviral therapy using primary intestinal organoids
journal, November 2015


Increased Filamentous Growth of Candida albicans in Simulated Microgravity
journal, January 2008

  • Altenburg, Sara D.; Nielsen-Preiss, Sheila M.; Hyman, Linda E.
  • Genomics, Proteomics & Bioinformatics, Vol. 6, Issue 1
  • DOI: 10.1016/S1672-0229(08)60019-4

Metabolic Characterization of Primary Rat Hepatocytes Cultivated in Parallel Microfluidic Biochips
journal, September 2013

  • Legendre, Audrey; Baudoin, Régis; Alberto, Giulia
  • Journal of Pharmaceutical Sciences, Vol. 102, Issue 9
  • DOI: 10.1002/jps.23466

A microfluidic culture model of the human reproductive tract and 28-day menstrual cycle
journal, March 2017

  • Xiao, Shuo; Coppeta, Jonathan R.; Rogers, Hunter B.
  • Nature Communications, Vol. 8, Issue 1
  • DOI: 10.1038/ncomms14584

A microfluidic 3D hepatocyte chip for drug toxicity testing
journal, January 2009

  • Toh, Yi-Chin; Lim, Teck Chuan; Tai, Dean
  • Lab on a Chip, Vol. 9, Issue 14
  • DOI: 10.1039/b900912d

Host attachment and fluid shear are integrated into a mechanical signal regulating virulence in Escherichia coli O157:H7
journal, April 2015

  • Alsharif, Ghadah; Ahmad, Sadia; Islam, Md Shahidul
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 17
  • DOI: 10.1073/pnas.1422986112

Identification of Multipotent Luminal Progenitor Cells in Human Prostate Organoid Cultures
journal, September 2014


Engineered human pluripotent-stem-cell-derived intestinal tissues with a functional enteric nervous system
journal, November 2016

  • Workman, Michael J.; Mahe, Maxime M.; Trisno, Stephen
  • Nature Medicine, Vol. 23, Issue 1
  • DOI: 10.1038/nm.4233

3D cell technologies head to the R&D assembly line
journal, December 2016


Enterotypes of the human gut microbiome
journal, April 2011

  • Arumugam, Manimozhiyan; Raes, Jeroen; Pelletier, Eric
  • Nature, Vol. 473, Issue 7346
  • DOI: 10.1038/nature09944

Biology's new dimension
journal, August 2003


Lung Organoids and Their Use To Study Cell-Cell Interaction
journal, April 2017


Brain-Region-Specific Organoids Using Mini-bioreactors for Modeling ZIKV Exposure
journal, May 2016


Peyer's Patch M Cells Derived from Lgr5+ Stem Cells Require SpiB and Are Induced by RankL in Cultured "Miniguts"
journal, July 2012

  • de Lau, W.; Kujala, P.; Schneeberger, K.
  • Molecular and Cellular Biology, Vol. 32, Issue 18
  • DOI: 10.1128/MCB.00434-12

Epidemic multiple drug resistant Salmonella Typhimurium causing invasive disease in sub-Saharan Africa have a distinct genotype
journal, November 2009

  • Kingsley, R. A.; Msefula, C. L.; Thomson, N. R.
  • Genome Research, Vol. 19, Issue 12
  • DOI: 10.1101/gr.091017.109

Modeling Development and Disease with Organoids
journal, June 2016


Cellular Fluid Mechanics and Mechanotransduction
journal, December 2005

  • Tarbell, John M.; Weinbaum, Sheldon; Kamm, Roger D.
  • Annals of Biomedical Engineering, Vol. 33, Issue 12
  • DOI: 10.1007/s10439-005-8775-z

Organogenesis in a dish: Modeling development and disease using organoid technologies
journal, July 2014


Dynamic reciprocity revisited
journal, April 2015


Three-dimensional modeling of T-24 human bladder carcinoma cell line: A new simulated microgravity culture vessel
journal, March 1993

  • Prewett, Tacey L.; Goodwin, Thomas J.; Spaulding, Glenn F.
  • Journal of Tissue Culture Methods, Vol. 15, Issue 1
  • DOI: 10.1007/BF02387287

Microengineering of Cellular Interactions
journal, August 2000


Diversity of the Human Intestinal Microbial Flora
journal, June 2005


Simulated microgravity conditions enhance differentiation of cultured PC12 cells towards the neuroendocrine phenotype
journal, April 1998

  • Lelkes, Peter I.; Galvan, Daniel L.; Thomas Hayman, G.
  • In Vitro Cellular & Developmental Biology - Animal, Vol. 34, Issue 4
  • DOI: 10.1007/s11626-998-0008-y

Mammalian cell cultures as models for Mycobacterium tuberculosis –human immunodeficiency virus (HIV) interaction studies: A review
journal, September 2016

  • Chingwaru, Walter; Glashoff, Richard H.; Vidmar, Jerneja
  • Asian Pacific Journal of Tropical Medicine, Vol. 9, Issue 9
  • DOI: 10.1016/j.apjtm.2016.07.002

Interaction with Decay-Accelerating Factor Facilitates Coxsackievirus B Infection of Polarized Epithelial Cells
journal, September 2002


A functional CFTR assay using primary cystic fibrosis intestinal organoids
journal, June 2013

  • Dekkers, Johanna F.; Wiegerinck, Caroline L.; de Jonge, Hugo R.
  • Nature Medicine, Vol. 19, Issue 7
  • DOI: 10.1038/nm.3201

Bioreactor Systems for Bone Tissue Engineering
journal, August 2011

  • Rauh, Juliane; Milan, Falk; Günther, Klaus-Peter
  • Tissue Engineering Part B: Reviews, Vol. 17, Issue 4
  • DOI: 10.1089/ten.teb.2010.0612

Mechanobiology and Developmental Control
journal, October 2013


Human pathogens utilize host extracellular matrix proteins laminin and collagen for adhesion and invasion of the host
journal, November 2012


Isolation and in vitro expansion of human colonic stem cells
journal, September 2011

  • Jung, Peter; Sato, Toshiro; Merlos-Suárez, Anna
  • Nature Medicine, Vol. 17, Issue 10
  • DOI: 10.1038/nm.2470

Human Gut-On-A-Chip Supports Polarized Infection of Coxsackie B1 Virus In Vitro
journal, February 2017


Maintenance and induction of morphological differentiation in dissociated mammary epithelium on floating collagen membranes
journal, May 1977

  • Emerman, Joanne T.; Pitelka, Dorothy R.
  • In Vitro, Vol. 13, Issue 5
  • DOI: 10.1007/BF02616178

Ischemia/reperfusion injury of primary porcine cardiomyocytes in a low-shear microfluidic culture and analysis device
journal, January 2011

  • Khanal, Grishma; Chung, Kiyong; Solis-Wever, Ximena
  • The Analyst, Vol. 136, Issue 17
  • DOI: 10.1039/c0an00845a

Effect of Shear Stress on Pseudomonas aeruginosa Isolated from the Cystic Fibrosis Lung
journal, August 2016


The effects of low-shear stress on Adherent-invasive Escherichia coli: AIEC and low-shear stress
journal, February 2008


Tissue engineering of functional cardiac muscle: molecular, structural, and electrophysiological studies
journal, January 2001


Secondary metabolism in simulated microgravity
journal, January 2001

  • Demain, Arnold L.; Fang, Aiqi
  • The Chemical Record, Vol. 1, Issue 4
  • DOI: 10.1002/tcr.1018

Mesenchymal stem cells support growth and organization of host-liver colorectal-tumor organoids and possibly resistance to chemotherapy
journal, June 2017


Flagellar Hooks and Hook Protein FlgE Participate in Host Microbe Interactions at Immunological Level
journal, May 2017


Prospective Derivation of a Living Organoid Biobank of Colorectal Cancer Patients
journal, May 2015


The Collagen Binding α1β1 Integrin VLA-1 Regulates CD8 T Cell-Mediated Immune Protection against Heterologous Influenza Infection
journal, February 2004


Vortex-mediated Mechanical Stress Induces Integrin-dependent Cell Adhesion Mediated by Inositol 1,4,5-Trisphosphate-sensitive Ca 2+ Release in THP-1 Cells
journal, January 2003

  • Ashida, Noboru; Takechi, Hajime; Kita, Toru
  • Journal of Biological Chemistry, Vol. 278, Issue 11
  • DOI: 10.1074/jbc.M212316200

Human Enteroids as a Model of Upper Small Intestinal Ion Transport Physiology and Pathophysiology
journal, March 2016


Shear stress-mediated NO production in inner medullary collecting duct cells
journal, August 2000


Stem Cell-Derived Human Intestinal Organoids as an Infection Model for Rotaviruses
journal, July 2012


Matrigel: Basement membrane matrix with biological activity
journal, October 2005


Primary culture of parenchymal liver cells on collagen membranes
journal, August 1975


Secretory IgA is Concentrated in the Outer Layer of Colonic Mucus along with Gut Bacteria
journal, April 2014


Disease Modeling in Stem Cell-Derived 3D Organoid Systems
journal, May 2017


3D tissue-like assemblies: A novel approach to investigate virus–cell interactions
journal, November 2015


Impenetrable barriers or entry portals? The role of cell–cell adhesion during infection
journal, October 2011

  • Bonazzi, Matteo; Cossart, Pascale
  • The Journal of Cell Biology, Vol. 195, Issue 3
  • DOI: 10.1083/jcb.201106011

The effect of astrocytes on the induction of barrier properties in aortic endothelial cells
journal, May 2011

  • Shayan, Gilda; Shuler, Michael L.; Lee, Kelvin H.
  • Biotechnology Progress, Vol. 27, Issue 4
  • DOI: 10.1002/btpr.620

Self-organizing optic-cup morphogenesis in three-dimensional culture
journal, April 2011

  • Eiraku, Mototsugu; Takata, Nozomu; Ishibashi, Hiroki
  • Nature, Vol. 472, Issue 7341
  • DOI: 10.1038/nature09941

Asialo GM1 is a receptor for Pseudomonas aeruginosa adherence to regenerating respiratory epithelial cells.
journal, January 1996


The use of a three-dimensional cell culture model to investigate host–pathogen interactions of Francisella tularensis in human lung epithelial cells
journal, September 2014


Context, tissue plasticity, and cancer
journal, January 2005


Microscale technologies for tissue engineering and biology
journal, February 2006

  • Khademhosseini, A.; Langer, R.; Borenstein, J.
  • Proceedings of the National Academy of Sciences, Vol. 103, Issue 8
  • DOI: 10.1073/pnas.0507681102

Dependence of the differentiated state on the cellular environment: modulation of collagen synthesis in tendon cells.
journal, October 1977

  • Schwarz, R. I.; Bissell, M. J.
  • Proceedings of the National Academy of Sciences, Vol. 74, Issue 10
  • DOI: 10.1073/pnas.74.10.4453

Composition and functional role of the mucus layers in the intestine
journal, September 2011

  • Johansson, Malin E. V.; Ambort, Daniel; Pelaseyed, Thaher
  • Cellular and Molecular Life Sciences, Vol. 68, Issue 22
  • DOI: 10.1007/s00018-011-0822-3

Physiological fluid shear alters the virulence potential of invasive multidrug-resistant non-typhoidal Salmonella Typhimurium D23580
journal, June 2016


Human Three-Dimensional Endometrial Epithelial Cell Model To Study Host Interactions with Vaginal Bacteria and Neisseria gonorrhoeae
journal, January 2017

  • Łaniewski, Paweł; Gomez, Adriana; Hire, Geoffrey
  • Infection and Immunity, Vol. 85, Issue 3
  • DOI: 10.1128/IAI.01049-16

Unlimited in vitro expansion of adult bi-potent pancreas progenitors through the Lgr5/R-spondin axis
journal, September 2013

  • Huch, Meritxell; Bonfanti, Paola; Boj, Sylvia F.
  • The EMBO Journal, Vol. 32, Issue 20
  • DOI: 10.1038/emboj.2013.204

Dancing with the Host
journal, July 2002


A human gut microbial gene catalogue established by metagenomic sequencing
journal, March 2010

  • Qin, Junjie; Li, Ruiqiang; Raes, Jeroen
  • Nature, Vol. 464, Issue 7285
  • DOI: 10.1038/nature08821

Establishment of Gastrointestinal Epithelial Organoids
journal, December 2013


Innate immunity in the lung: how epithelial cells fight against respiratory pathogens
journal, February 2004


Molecular Basis of the Interaction of Salmonella with the Intestinal Mucosa
journal, July 1999

  • Darwin, K. Heran; Miller, Virginia L.
  • Clinical Microbiology Reviews, Vol. 12, Issue 3
  • DOI: 10.1128/CMR.12.3.405

Exposure of Mycobacterium marinum to low-shear modeled microgravity: effect on growth, the transcriptome and survival under stress
journal, December 2016

  • Abshire, Camille F.; Prasai, Kanchanjunga; Soto, Israel
  • npj Microgravity, Vol. 2, Issue 1
  • DOI: 10.1038/npjmgrav.2016.38

Escherichia coli growth under modeled reduced gravity
journal, December 2004

  • Baker, Paul W.; Meyer, Michelle L.; Leff, Laura G.
  • Microgravity - Science and Technology, Vol. 15, Issue 4
  • DOI: 10.1007/BF02870967

Molecular mechanisms underlying the enhanced functions of three-dimensional hepatocyte aggregates
journal, February 2014


Mucin dynamics and enteric pathogens
journal, March 2011

  • McGuckin, Michael A.; Lindén, Sara K.; Sutton, Philip
  • Nature Reviews Microbiology, Vol. 9, Issue 4
  • DOI: 10.1038/nrmicro2538

Response of Pseudomonas aeruginosa PAO1 to low shear modelled microgravity involves AlgU regulation
journal, April 2010


Tissue architecture: the ultimate regulator of breast epithelial function
journal, December 2003

  • Bissell, Mina J.; Rizki, Aylin; Mian, I. Saira
  • Current Opinion in Cell Biology, Vol. 15, Issue 6
  • DOI: 10.1016/j.ceb.2003.10.016

Human enteroids as an ex-vivo model of host–pathogen interactions in the gastrointestinal tract
journal, April 2014

  • Foulke-Abel, Jennifer; In, Julie; Kovbasnjuk, Olga
  • Experimental Biology and Medicine, Vol. 239, Issue 9
  • DOI: 10.1177/1535370214529398

Mechanical stimulation activates Gαq signaling pathways and 5-hydroxytryptamine release from human carcinoid BON cells
journal, October 2001

  • Kim, Minsoo; Javed, Najma H.; Yu, Jun-Ge
  • Journal of Clinical Investigation, Vol. 108, Issue 7
  • DOI: 10.1172/JCI12467

Single luminal epithelial progenitors can generate prostate organoids in culture
journal, September 2014

  • Chua, Chee Wai; Shibata, Maho; Lei, Ming
  • Nature Cell Biology, Vol. 16, Issue 10
  • DOI: 10.1038/ncb3047

Interactions of bacterial adhesins with extracellular matrix and plasma proteins: pathogenic implications and therapeutic possibilities
journal, December 1996


Effect of shear stress on growth, adhesion and biofilm formation of Pseudomonas aeruginosa with antibiotic-induced morphological changes
journal, September 2007


A primary human macrophage-enteroid co-culture model to investigate mucosal gut physiology and host-pathogen interactions
journal, March 2017

  • Noel, Gaelle; Baetz, Nicholas W.; Staab, Janet F.
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep45270

The outer mucus layer hosts a distinct intestinal microbial niche
journal, September 2015

  • Li, Hai; Limenitakis, Julien P.; Fuhrer, Tobias
  • Nature Communications, Vol. 6, Issue 1
  • DOI: 10.1038/ncomms9292

Organotypic 3D cell culture models: using the rotating wall vessel to study host–pathogen interactions
journal, October 2010

  • Barrila, Jennifer; Radtke, Andrea L.; Crabbé, Aurélie
  • Nature Reviews Microbiology, Vol. 8, Issue 11
  • DOI: 10.1038/nrmicro2423

Bone tissue engineering in a rotating bioreactor using a microcarrier matrix system
journal, January 2001


Microarray analysis identifies Salmonella genes belonging to the low-shear modeled microgravity regulon
journal, October 2002

  • Wilson, J. W.; Ramamurthy, R.; Porwollik, S.
  • Proceedings of the National Academy of Sciences, Vol. 99, Issue 21
  • DOI: 10.1073/pnas.212387899

Accelerated and Improved Differentiation of Retinal Organoids from Pluripotent Stem Cells in Rotating-Wall Vessel Bioreactors
journal, January 2018


Escherichia coli Biofilms Formed under Low-Shear Modeled Microgravity in a Ground-Based System
journal, October 2006

  • Lynch, S. V.; Mukundakrishnan, K.; Benoit, M. R.
  • Applied and Environmental Microbiology, Vol. 72, Issue 12
  • DOI: 10.1128/AEM.01294-06

Ensembles of engineered cardiac tissues for physiological and pharmacological study: Heart on a chip
journal, January 2011

  • Grosberg, Anna; Alford, Patrick W.; McCain, Megan L.
  • Lab on a Chip, Vol. 11, Issue 24
  • DOI: 10.1039/c1lc20557a

Free and complexed-secretory immunoglobulin A triggers distinct intestinal epithelial cell responses: Immune Complexes and Gut Homeostasis
journal, July 2016

  • Salerno-Goncalves, R.; Safavie, F.; Fasano, A.
  • Clinical & Experimental Immunology, Vol. 185, Issue 3
  • DOI: 10.1111/cei.12801

Impact of scaffold micro and macro architecture on Schwann cell proliferation under dynamic conditions in a rotating wall vessel bioreactor
journal, January 2011

  • Valmikinathan, Chandra M.; Hoffman, John; Yu, Xiaojun
  • Materials Science and Engineering: C, Vol. 31, Issue 1
  • DOI: 10.1016/j.msec.2010.04.001

Microfluidic heart on a chip for higher throughput pharmacological studies
journal, January 2013

  • Agarwal, Ashutosh; Goss, Josue Adrian; Cho, Alexander
  • Lab on a Chip, Vol. 13, Issue 18
  • DOI: 10.1039/c3lc50350j

Adhesion of Plasmodium falciparum-infected erythrocytes to hyaluronic acid in placental malaria
journal, January 2000

  • Beeson, James G.; Rogerson, Stephen J.; Cooke, Brian M.
  • Nature Medicine, Vol. 6, Issue 1
  • DOI: 10.1038/71582

Three-dimensional organotypic co-culture model of intestinal epithelial cells and macrophages to study Salmonella enterica colonization patterns
journal, February 2017


The generation of 3-D tissue models based on hyaluronan hydrogel-coated microcarriers within a rotating wall vessel bioreactor
journal, November 2010


Normal Physiology of Small Intestinal Motility
journal, December 1993


Long term Organ Culture of Human Prostate Tissue in a Nasa-Designed Rotating wall Bioreactor
journal, January 1999


Tensegrity II. How structural networks influence cellular information processing networks
journal, April 2003


Development of a primary human Small Intestine-on-a-Chip using biopsy-derived organoids
journal, February 2018

  • Kasendra, Magdalena; Tovaglieri, Alessio; Sontheimer-Phelps, Alexandra
  • Scientific Reports, Vol. 8, Issue 1
  • DOI: 10.1038/s41598-018-21201-7

An artificial liver sinusoid with a microfluidic endothelial-like barrier for primary hepatocyte culture
journal, January 2007

  • Lee, Philip J.; Hung, Paul J.; Lee, Luke P.
  • Biotechnology and Bioengineering, Vol. 97, Issue 5
  • DOI: 10.1002/bit.21360

Three-dimensional growth of extravillous cytotrophoblasts promotes differentiation and invasion
journal, November 2005


Type IV pili mechanochemically regulate virulence factors in Pseudomonas aeruginosa
journal, June 2015

  • Persat, Alexandre; Inclan, Yuki F.; Engel, Joanne N.
  • Proceedings of the National Academy of Sciences, Vol. 112, Issue 24
  • DOI: 10.1073/pnas.1502025112

Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche
journal, March 2009

  • Sato, Toshiro; Vries, Robert G.; Snippert, Hugo J.
  • Nature, Vol. 459, Issue 7244
  • DOI: 10.1038/nature07935

Human Clostridium difficile infection: inhibition of NHE3 and microbiota profile
journal, March 2015

  • Engevik, Melinda A.; Engevik, Kristen A.; Yacyshyn, Mary Beth
  • American Journal of Physiology-Gastrointestinal and Liver Physiology, Vol. 308, Issue 6
  • DOI: 10.1152/ajpgi.00090.2014

Three-Dimensional Tissue Assemblies: Novel Models for the Study of Salmonella enterica Serovar Typhimurium Pathogenesis
journal, November 2001


Tensegrity I. Cell structure and hierarchical systems biology
journal, April 2003


Establishment of a three-dimensional human prostate organoid coculture under microgravity-simulated conditions: Evaluation of androgen-induced growth and psa expression
journal, May 1997

  • Zhau, Haiyen E.; Goodwin, Thomas J.; Chang, Shi-Ming
  • In Vitro Cellular & Developmental Biology - Animal, Vol. 33, Issue 5
  • DOI: 10.1007/s11626-997-0008-3

A549 Lung Epithelial Cells Grown as Three-Dimensional Aggregates: Alternative Tissue Culture Model for Pseudomonas aeruginosa Pathogenesis
journal, January 2005


Mucosal immunity and vaccines
journal, April 2005

  • Holmgren, Jan; Czerkinsky, Cecil
  • Nature Medicine, Vol. 11, Issue S4
  • DOI: 10.1038/nm1213

Pathways and functions of gut microbiota metabolism impacting host physiology
journal, December 2015


Epithelial cell specific Raptor is required for initiation of type 2 mucosal immunity in small intestine
journal, July 2017


Subversion of the actin cytoskeleton during viral infection
journal, April 2011

  • Taylor, Matthew P.; Koyuncu, Orkide O.; Enquist, Lynn W.
  • Nature Reviews Microbiology, Vol. 9, Issue 6
  • DOI: 10.1038/nrmicro2574

The Extracellular Matrix Regulates Granuloma Necrosis in Tuberculosis
journal, February 2015

  • Al Shammari, Basim; Shiomi, Takayuki; Tezera, Liku
  • Journal of Infectious Diseases, Vol. 212, Issue 3
  • DOI: 10.1093/infdis/jiv076

A driving force for change: interstitial flow as a morphoregulator
journal, January 2007


Human iPS cell–derived alveolar epithelium repopulates lung extracellular matrix
journal, October 2013

  • Ghaedi, Mahboobe; Calle, Elizabeth A.; Mendez, Julio J.
  • Journal of Clinical Investigation, Vol. 123, Issue 11
  • DOI: 10.1172/JCI68793

Development of a Renal Microchip for In Vitro Distal Tubule Models
journal, August 2007

  • Baudoin, R.; Griscom, L.; Monge, M.
  • Biotechnology Progress, Vol. 0, Issue 0
  • DOI: 10.1021/bp0603513

Influence of a reconstituted basement membrane and its components on casein gene expression and secretion in mouse mammary epithelial cells.
journal, January 1987

  • Li, M. L.; Aggeler, J.; Farson, D. A.
  • Proceedings of the National Academy of Sciences, Vol. 84, Issue 1
  • DOI: 10.1073/pnas.84.1.136

Probing Functional Properties of Nociceptive Axons Using a Microfluidic Culture System
journal, November 2013


Signalling at tight junctions during epithelial differentiation and microbial pathogenesis
journal, August 2014

  • Zihni, C.; Balda, M. S.; Matter, K.
  • Journal of Cell Science, Vol. 127, Issue 16
  • DOI: 10.1242/jcs.145029

TEER Measurement Techniques for In Vitro Barrier Model Systems
journal, April 2015

  • Srinivasan, Balaji; Kolli, Aditya Reddy; Esch, Mandy Brigitte
  • Journal of Laboratory Automation, Vol. 20, Issue 2
  • DOI: 10.1177/2211068214561025

The present and future role of microfluidics in biomedical research
journal, March 2014

  • Sackmann, Eric K.; Fulton, Anna L.; Beebe, David J.
  • Nature, Vol. 507, Issue 7491
  • DOI: 10.1038/nature13118

A multi-layer microfluidic device for efficient culture and analysis of renal tubular cells
journal, January 2010

  • Jang, Kyung-Jin; Suh, Kahp-Yang
  • Lab Chip, Vol. 10, Issue 1
  • DOI: 10.1039/B907515A

Gut biogeography of the bacterial microbiota
journal, October 2015

  • Donaldson, Gregory P.; Lee, S. Melanie; Mazmanian, Sarkis K.
  • Nature Reviews Microbiology, Vol. 14, Issue 1
  • DOI: 10.1038/nrmicro3552

Self-Organized Formation of Polarized Cortical Tissues from ESCs and Its Active Manipulation by Extrinsic Signals
journal, November 2008


Human kidney proximal tubule-on-a-chip for drug transport and nephrotoxicity assessment
journal, May 2013

  • Jang, Kyung-Jin; Mehr, Ali Poyan; Hamilton, Geraldine A.
  • Integrative Biology, Vol. 5, Issue 9
  • DOI: 10.1039/c3ib40049b

Directed Stem Cell Differentiation by Fluid Mechanical Forces
journal, September 2011

  • Adamo, Luigi; García-Cardeña, Guillermo
  • Antioxidants & Redox Signaling, Vol. 15, Issue 5
  • DOI: 10.1089/ars.2011.3907

Vascularized and functional human liver from an iPSC-derived organ bud transplant
journal, July 2013

  • Takebe, Takanori; Sekine, Keisuke; Enomura, Masahiro
  • Nature, Vol. 499, Issue 7459
  • DOI: 10.1038/nature12271

Vascular Mechanobiology
journal, January 2009


Salmonella enterica Serovar Senftenberg Human Clinical Isolates Lacking SPI-1
journal, February 2008

  • Hu, Q.; Coburn, B.; Deng, W.
  • Journal of Clinical Microbiology, Vol. 46, Issue 4
  • DOI: 10.1128/JCM.01255-07

A three-dimensional culture system recapitulates placental syncytiotrophoblast development and microbial resistance
journal, March 2016

  • McConkey, Cameron A.; Delorme-Axford, Elizabeth; Nickerson, Cheryl A.
  • Science Advances, Vol. 2, Issue 3
  • DOI: 10.1126/sciadv.1501462

Characterization of a gastrointestinal tract microscale cell culture analog used to predict drug toxicity
journal, September 2009

  • Mahler, Gretchen J.; Esch, Mandy B.; Glahn, Raymond P.
  • Biotechnology and Bioengineering, Vol. 104, Issue 1
  • DOI: 10.1002/bit.22366

Three-dimensional organotypic culture: experimental models of mammalian biology and disease
journal, September 2014

  • Shamir, Eliah R.; Ewald, Andrew J.
  • Nature Reviews Molecular Cell Biology, Vol. 15, Issue 10
  • DOI: 10.1038/nrm3873

The Viral Mimetic Polyinosinic:Polycytidylic Acid Alters the Growth Characteristics of Small Intestinal and Colonic Crypt Cultures
journal, September 2015


A single-cell survey of the small intestinal epithelium
journal, November 2017

  • Haber, Adam L.; Biton, Moshe; Rogel, Noga
  • Nature, Vol. 551, Issue 7680
  • DOI: 10.1038/nature24489

Accelerated and Improved Differentiation of Retinal Organoids from Pluripotent Stem Cells in Rotating-Wall Vessel Bioreactors
journal, January 2021


The Viral Mimetic Polyinosinic:Polycytidylic Acid Alters the Growth Characteristics of Small Intestinal and Colonic Crypt Cultures
text, January 2015

  • J., von Furstenberg, Richard; T., Abreu, Maria; J., Henning, Susan
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/jc4x-f373

Role of mechanical stress in regulating airway surface hydration and mucus clearance rates
text, January 2008

  • Brian, Button,; Richard, Boucher,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/vy7s-yd16

Characterization of microfluidic human epidermal keratinocyte culture
text, January 2008

  • T., O’Neill, Adrian; A., Monteiro-Riviere, Nancy; M., Walker, Glenn
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/yj6a-4a87

The outer mucus layer hosts a distinct intestinal microbial niche
text, January 2015

  • Li, Hai; Limenitakis, Julien Periclis Jean; Fuhrer, Tobias
  • Nature Publishing Group
  • DOI: 10.7892/boris.77343

The coxsackievirus and adenovirus receptor is a transmembrane component of the tight junction
text, January 2001

  • J., Cohen, Christopher; Tsong, Hsieh, Jer; Takatsugu, Okegawa,
  • The University of North Carolina at Chapel Hill University Libraries
  • DOI: 10.17615/v5ss-a196

Patterning Osteogenesis by Inducible Gene Expression in Microfluidic Culture Systems
text, January 2011

  • Vunjak-Novakovic, Gordana; Zhang, Yue; Gazit, Zulma
  • Columbia University
  • DOI: 10.7916/d85x26x7

Impenetrable barriers or entry portals? The role of cell–cell adhesion during infection
journal, November 2011

  • Bonazzi, Matteo; Cossart, Pascale
  • The Journal of Experimental Medicine, Vol. 208, Issue 12
  • DOI: 10.1084/jem20812oia33

Lung Organoids and Their Use To Study Cell-Cell Interaction
text, January 2017

  • Nikolić, Mz; Rawlins, Emma
  • Apollo - University of Cambridge Repository
  • DOI: 10.17863/cam.9489

The outer mucus layer hosts a distinct intestinal microbial niche
text, January 2015


Works referencing / citing this record:

Infection-induced signals generated at the plasma membrane epigenetically regulate Wnt signaling in vitro and in vivo
journal, December 2019

  • Ahmed, Ishfaq; Roy, Badal Chandra; Rao Jakkula, Laxmi Uma Maheswar
  • Journal of Biological Chemistry, Vol. 295, Issue 4
  • DOI: 10.1074/jbc.ra119.010285

Host metabolites stimulate the bacterial proton motive force to enhance the activity of aminoglycoside antibiotics
journal, April 2019


3D Primary Hepatocyte Culture Systems for Analyses of Liver Diseases, Drug Metabolism, and Toxicity: Emerging Culture Paradigms and Applications
journal, May 2019

  • Lauschke, Volker M.; Shafagh, Reza Z.; Hendriks, Delilah F. G.
  • Biotechnology Journal, Vol. 14, Issue 7
  • DOI: 10.1002/biot.201800347

Extracellular matrix dynamics in cell migration, invasion and tissue morphogenesis
journal, June 2019

  • Yamada, Kenneth M.; Collins, Joshua W.; Cruz Walma, David A.
  • International Journal of Experimental Pathology, Vol. 100, Issue 3
  • DOI: 10.1111/iep.12329

An Advanced Human Intestinal Coculture Model Reveals Compartmentalized Host and Pathogen Strategies during Salmonella Infection
journal, February 2020

  • Schulte, Leon N.; Schweinlin, Matthias; Westermann, Alexander J.
  • mBio, Vol. 11, Issue 1
  • DOI: 10.1128/mbio.03348-19

Three Dimensional Vero Cell-Platform for Rapid and Sensitive Screening of Shiga-Toxin Producing Escherichia coli
journal, May 2019


From Entry to Early Dissemination—Toxoplasma gondii's Initial Encounter With Its Host
journal, March 2019

  • Delgado Betancourt, Estefania; Hamid, Benjamin; Fabian, Benedikt T.
  • Frontiers in Cellular and Infection Microbiology, Vol. 9
  • DOI: 10.3389/fcimb.2019.00046

Organoids in immunological research
journal, December 2019

  • Bar-Ephraim, Yotam E.; Kretzschmar, Kai; Clevers, Hans
  • Nature Reviews Immunology, Vol. 20, Issue 5
  • DOI: 10.1038/s41577-019-0248-y