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


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

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 Lab. (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
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
American Society for Microbiology
Country of Publication:
United States
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. 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., and Maurelli, Anthony T. Tue . "Modeling Host-Pathogen Interactions in the Context of the Microenvironment: Three-Dimensional Cell Culture Comes of Age". United States. doi:10.1128/IAI.00282-18.
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 = {2018},
month = {9}

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