Extracellular matrix in lung development, homeostasis and disease

Zhou, Yong; Horowitz, Jeffrey C.; Naba, Alexandra; Ambalavanan, Namasivayam; Atabai, Kamran; Balestrini, Jenna; Bitterman, Peter B.; Corley, Richard A.; Ding, Bi -Sen; Engler, Adam J.; Hansen, Kirk C.; Hagood, James S.; Kheradmand, Farrah; Lin, Qing S.; Neptune, Enid; Niklason, Laura; Ortiz, Luis A.; Parks, William C.; Tschumperlin, Daniel J.; White, Eric S.; Chapman, Harold A.; Thannickal, Victor J.

doi:10.1016/j.matbio.2018.03.005

Title: Extracellular matrix in lung development, homeostasis and disease

Abstract

Here, the lung's unique extracellular matrix (ECM), while providing structural support for cells, is critical in the regulation of developmental organogenesis, homeostasis and injury-repair responses. The ECM, via biochemical or biomechanical cues, regulates diverse cell functions, fate and phenotype. The composition and function of lung ECM become markedly deranged in pathological tissue remodeling. ECM-based therapeutics and bioengineering approaches represent promising novel strategies for regeneration/repair of the lung and treatment of chronic lung diseases. In this review, we assess the current state of lung ECM biology, including fundamental advances in ECM composition, dynamics, topography, and biomechanics; the role of the ECM in normal and aberrant lung development, adult lung diseases and autoimmunity; and ECM in the regulation of the stem cell niche. We identify opportunities to advance the field of lung ECM biology and provide a set recommendations for research priorities to advance knowledge that would inform novel approaches to the pathogenesis, diagnosis, and treatment of chronic lung diseases.

Authors:

Zhou, Yong ^[1]; Horowitz, Jeffrey C. ^[2];

^[3];

^[4]; Atabai, Kamran ^[5];

^[6];

^[7]; Corley, Richard A. ^[8]; Ding, Bi -Sen ^[9];

^[10]; Hansen, Kirk C. ^[11]; Hagood, James S. ^[12]; Kheradmand, Farrah ^[13]; Lin, Qing S. ^[14]; Neptune, Enid ^[15];

^[6];

^[16]; Parks, William C. ^[17]; Tschumperlin, Daniel J. ^[18];

^[2] more »

Univ. of Alabama, Birmingham, AL (United States). Division of Pulmonary, Allergy and Critical Care Medicine
Univ. of Michigan, Ann Arbor, MI (United States). Division of Pulmonary and Critical Care Medicine
Univ. of Illinois, Chicago, IL (United States). Dept. of Physiology & Biophysics
Univ. of Alabama, Birmingham, AL (United States). Dept. of Pediatrics
Univ. of California, San Francisco, CA (United States). Lung Biology Center
Yale Univ., New Haven, CT (United States). Dept. of Anesthesiology
Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Medicine
Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Systems Toxicology & Exposure Science
Cornell Univ., Ithaca, NY (United States). Weill Cornell Medical College
Univ. of California, San Diego, CA (United States). Sanford Consortium for Regenerative Medicine
Univ. of Colorado, Denver, CO (United States). Biochemistry & Molecular Genetics
Univ. of California, San Diego, CA (United States). Pediatric Respiratory Medicine
Baylor College of Medicine, Houston, TX (United States). Division of Pulmonary and Critical Care
National Heart, Lung, and Blood Inst., Bethesda, MD (United States). Division of Lung Diseases
Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine. Division of Pulmonary and Critical Care Medicine
Univ. of Pittsburgh, PA (United States). Division of Environmental and Occupational Health
Cedars-Sinai Medical Center, Los Angeles, CA (United States). Dept. of Medicine
Mayo Clinic College of Medicine, Rochester, MN (United States). Dept. of Physiology & Biomedical Engineering
Univ. of California, San Francisco, CA (United States). Division of Pulmonary and Critical Care Medicine

Publication Date:: 2018-03-08

Research Org.:: Pacific Northwest National Lab. (PNNL), Richland, WA (United States)

Sponsoring Org.:: USDOE

OSTI Identifier:: 1437148

Grant/Contract Number:: AC05-76RL01830

Resource Type:: Accepted Manuscript

Journal Name:: Matrix Biology

Additional Journal Information:: Journal Volume: 73; Journal ID: ISSN 0945-053X

Country of Publication:: United States

Language:: English

Subject:: 59 BASIC BIOLOGICAL SCIENCES

Citation Formats


                    Zhou, Yong, Horowitz, Jeffrey C., Naba, Alexandra, Ambalavanan, Namasivayam, Atabai, Kamran, Balestrini, Jenna, Bitterman, Peter B., Corley, Richard A., Ding, Bi -Sen, Engler, Adam J., Hansen, Kirk C., Hagood, James S., Kheradmand, Farrah, Lin, Qing S., Neptune, Enid, Niklason, Laura, Ortiz, Luis A., Parks, William C., Tschumperlin, Daniel J., White, Eric S., Chapman, Harold A., and Thannickal, Victor J. Extracellular matrix in lung development, homeostasis and disease.  United States: N. p., 2018. 
Web.  doi:10.1016/j.matbio.2018.03.005.

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                    Zhou, Yong, Horowitz, Jeffrey C., Naba, Alexandra, Ambalavanan, Namasivayam, Atabai, Kamran, Balestrini, Jenna, Bitterman, Peter B., Corley, Richard A., Ding, Bi -Sen, Engler, Adam J., Hansen, Kirk C., Hagood, James S., Kheradmand, Farrah, Lin, Qing S., Neptune, Enid, Niklason, Laura, Ortiz, Luis A., Parks, William C., Tschumperlin, Daniel J., White, Eric S., Chapman, Harold A., & Thannickal, Victor J. Extracellular matrix in lung development, homeostasis and disease.  United States.  https://doi.org/10.1016/j.matbio.2018.03.005

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                    Zhou, Yong, Horowitz, Jeffrey C., Naba, Alexandra, Ambalavanan, Namasivayam, Atabai, Kamran, Balestrini, Jenna, Bitterman, Peter B., Corley, Richard A., Ding, Bi -Sen, Engler, Adam J., Hansen, Kirk C., Hagood, James S., Kheradmand, Farrah, Lin, Qing S., Neptune, Enid, Niklason, Laura, Ortiz, Luis A., Parks, William C., Tschumperlin, Daniel J., White, Eric S., Chapman, Harold A., and Thannickal, Victor J. Thu .  
"Extracellular matrix in lung development, homeostasis and disease".  United States.  https://doi.org/10.1016/j.matbio.2018.03.005.  https://www.osti.gov/servlets/purl/1437148.

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@article{osti_1437148,

  title        = {Extracellular matrix in lung development, homeostasis and disease},

  author       = {Zhou, Yong and Horowitz, Jeffrey C. and Naba, Alexandra and Ambalavanan, Namasivayam and Atabai, Kamran and Balestrini, Jenna and Bitterman, Peter B. and Corley, Richard A. and Ding, Bi -Sen and Engler, Adam J. and Hansen, Kirk C. and Hagood, James S. and Kheradmand, Farrah and Lin, Qing S. and Neptune, Enid and Niklason, Laura and Ortiz, Luis A. and Parks, William C. and Tschumperlin, Daniel J. and White, Eric S. and Chapman, Harold A. and Thannickal, Victor J.},

  abstractNote = {Here, the lung's unique extracellular matrix (ECM), while providing structural support for cells, is critical in the regulation of developmental organogenesis, homeostasis and injury-repair responses. The ECM, via biochemical or biomechanical cues, regulates diverse cell functions, fate and phenotype. The composition and function of lung ECM become markedly deranged in pathological tissue remodeling. ECM-based therapeutics and bioengineering approaches represent promising novel strategies for regeneration/repair of the lung and treatment of chronic lung diseases. In this review, we assess the current state of lung ECM biology, including fundamental advances in ECM composition, dynamics, topography, and biomechanics; the role of the ECM in normal and aberrant lung development, adult lung diseases and autoimmunity; and ECM in the regulation of the stem cell niche. We identify opportunities to advance the field of lung ECM biology and provide a set recommendations for research priorities to advance knowledge that would inform novel approaches to the pathogenesis, diagnosis, and treatment of chronic lung diseases.},

  doi          = {10.1016/j.matbio.2018.03.005},

  journal      = {Matrix Biology},

  number       = ,

  volume       = 73,

  place        = {United States},

  year         = {2018},

  month        = {3}

}

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https://doi.org/10.1016/j.matbio.2018.03.005

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Cited by: 12 works

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Figures / Tables:

Figure 1: Role of the ECM in lung homeostasis and disease. N and the maintenance of lung homeostasis in adulthood. Abe composition, biomechanics, dynamics and topography, are ch including IPF, COPD and BPD. IPF = idiopathic pulmonary f BPD = bronchopulmonary dysplasia.

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Tenascin-C in the extracellular matrix promotes the selection of highly proliferative and tubulogenesis-defective endothelial cells

Journal Article Alves, Tercia Rodrigues ; Universidade Federal do Rio de Janeiro ; Carvalho da Fonseca, Anna Carolina ; ... - Experimental Cell Research

The extracellular matrix (ECM) contains important cues for tissue homeostasis and morphogenesis. The matricellular protein tenascin-C (TN-C) is overexpressed in remodeling tissues and cancer. In the present work, we studied the effect of different ECM-which exhibited a significant diversity in their TN-C content-in endothelial survival, proliferation and tubulogenic differentiation: autologous (endothelial) ECM devoid of TN-C, but bearing large amounts of FN; fibroblast ECM, bearing both high TN-C and FN contents; and finally, glioma-derived matrices, usually poor in FN, but very rich in TN-C. HUVECs initially adhered to the immobilized matrix produced by U373 MG glioma cells, but significantly detached andmore »« less
https://doi.org/10.1016/J.YEXCR.2011.06.006
Endomembrane Cation Transporters and Membrane Trafficking

Technical Report Sze, Heven

Multicellular, as well as unicellular, organisms have evolved mechanisms to regulate ion and pH homeostasis in response to developmental cues and to a changing environment. The working hypothesis is that the balance of fluxes mediated by diverse transporters at the plasma membrane and in subcellular organelles determines ionic cellular distribution, which is critical for maintenance of membrane potential, pH control, osmolality, transport of nutrients, and protein activity. An emerging theme in plant cell biology is that cells respond and adapt to diverse cues through changes of the dynamic endomembrane system. Yet we know very little about the transporters that mightmore »« less
https://doi.org/10.2172/1351059

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Title: Extracellular matrix in lung development, homeostasis and disease

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Developmental alveolarization of the mouse lung journal, August 2008

Extracellular matrix and the regulation of lung development and repair 1 journal, August 1992

Idiopathic Pulmonary Fibrosis: Aberrant Recapitulation of Developmental Programs? journal, March 2008

Developmental Reprogramming in Mesenchymal Stromal Cells of Human Subjects with Idiopathic Pulmonary Fibrosis journal, November 2016

Distribution of laminin 5, integrin receptors, and branching morphogenesis during human fetal lung development journal, September 2002

Hyaluronic acid of wound fluid in adult and fetal rabbits journal, January 1997

Epithelial laminin α5 is necessary for distal epithelial cell maturation, VEGF production, and alveolization in the developing murine lung journal, June 2005

Developmental Regulation of the Laminin α5 Chain Suggests a Role in Epithelial and Endothelial Cell Maturation journal, September 1997

The Laminin α Chains: Expression, Developmental Transitions, and Chromosomal Locations of α1-5, Identification of Heterotrimeric Laminins 8–11, and Cloning of a Novel α3 Isoform journal, May 1997

Immunohistochemical study of collagen types in human foetal lung and fibrotic lung disease. journal, September 1981

Structural basis for the changing physical properties of human pulmonary vessels with age. journal, June 1978

Control of Elastin Synthesis. journal, July 1982

Differential expression of matrix metalloproteinases and their inhibitors in human and mouse lung development journal, January 2005

Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase journal, December 2004

Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea journal, August 1998

Proteoglycan and collagen expression during human air conducting system development journal, June 2012

Heparan sulfate–FGF10 interactions during lung morphogenesis journal, June 2003

Expression Profiling of the Developing Mouse Lung: Insights into the Establishment of the Extracellular Matrix journal, May 2002

PDGF-A Signaling Is a Critical Event in Lung Alveolar Myofibroblast Development and Alveogenesis journal, June 1996

Sulfatases are determinants of alveolar formation journal, May 2012

Membrane-type 1 matrix metalloproteinase is required for normal alveolar development journal, January 2005

Role of Matrix Metalloproteinase-2 in Newborn Mouse Lungs under Hypoxic Conditions journal, January 2008

Low amniotic pressure in oligohydramnios—Is this the cause of pulmonary hypoplasia? . journal, November 1989

Experimental pulmonary hypoplasia and oligohydramnios: Relative contributions of lung fluid and fetal breathing movements journal, December 1984

The Strength of Mechanical Forces Determines the Differentiation of Alveolar Epithelial Cells journal, February 2018

Mechanical Forces Program the Orientation of Cell Division during Airway Tube Morphogenesis journal, February 2018

Stretch-induced alternative splicing of serum response factor promotes bronchial myogenesis and is defective in lung hypoplasia journal, December 2000

Extracellular Matrix Structure and Tissue Stiffness Control Postnatal Lung Development through the Lipoprotein Receptor–Related Protein 5/Tie2 Signaling System journal, December 2013

Pathology of Bronchopulmonary Dysplasia journal, August 2006

Bronchopulmonary dysplasia: new insights journal, September 2004

Collagen Scaffolding During Development and Its Deformation With Chronic Lung Disease journal, April 2003

Lung Elastic Tissue Maturation and Perturbations During the Evolution of Chronic Lung Disease journal, December 2000

Lysyl Oxidase Activity Is Dysregulated during Impaired Alveolarization of Mouse and Human Lungs journal, December 2009

Mechanical ventilation uncouples synthesis and assembly of elastin and increases apoptosis in lungs of newborn mice.: Prelude to defective alveolar septation during lung development? journal, January 2008

Diffuse Lung Disease in Young Children: Application of a Novel Classification Scheme journal, December 2007

Prominent Intrapulmonary Bronchopulmonary Anastomoses and Abnormal Lung Development in Infants and Children with Down Syndrome journal, January 2017

Overview of the Matrisome--An Inventory of Extracellular Matrix Constituents and Functions journal, September 2011

Towards definition of an ECM parts list: An advance on GO categories journal, September 2012

Defining the extracellular matrix using proteomics journal, February 2013

The Matrisome: In Silico Definition and In Vivo Characterization by Proteomics of Normal and Tumor Extracellular Matrices journal, April 2012

The extracellular matrix: Tools and insights for the “omics” era journal, January 2016

Characterization of the Extracellular Matrix of Normal and Diseased Tissues Using Proteomics journal, July 2017

Quantitative extracellular matrix proteomics to study mammary and liver tissue microenvironments journal, December 2016

Targeted proteomics effectively quantifies differences between native lung and detergent-decellularized lung extracellular matrices journal, December 2016

Time‐ and compartment‐resolved proteome profiling of the extracellular niche in lung injury and repair journal, July 2015

ISDoT: in situ decellularization of tissues for high-resolution imaging and proteomic analysis of native extracellular matrix journal, June 2017

Proteomic Analysis of Altered Extracellular Matrix Turnover in Bleomycin-induced Pulmonary Fibrosis journal, July 2014

Quantitative proteomics identify Tenascin-C as a promoter of lung cancer progression and contributor to a signature prognostic of patient survival journal, June 2017

Deep Proteome Profiling Reveals Common Prevalence of MZB1-Positive Plasma B Cells in Human Lung and Skin Fibrosis journal, November 2017

The instructive extracellular matrix of the lung: basic composition and alterations in chronic lung disease journal, July 2017

Extracellular Matrix Remodeling: The Common Denominator in Connective Tissue Diseases Possibilities for Evaluation and Current Understanding of the Matrix as More Than a Passive Architecture, but a Key Player in Tissue Failure journal, March 2013

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

Proteolytic Post-translational Modification of Proteins: Proteomic Tools and Methodology journal, December 2013

Glycomics Approach to Structure-Function Relationships of Glycosaminoglycans journal, August 2006

A method for automated detection of gene expression required for the establishment of a digital transcriptome-wide gene expression atlas journal, March 2005

A Suite of Activity-Based Probes for Human Cytochrome P450 Enzymes journal, July 2009

Molecular imaging and depth profiling by mass spectrometry—SIMS, MALDI or DESI? journal, January 2011

Tissue Imaging Using Nanospray Desorption Electrospray Ionization Mass Spectrometry journal, December 2011

Automated Platform for High-Resolution Tissue Imaging Using Nanospray Desorption Electrospray Ionization Mass Spectrometry journal, September 2012

SNAP-tag Based Proteomics Approach for the Study of the Retrograde Route: Proteomics of Retrograde Route journal, April 2012

Decellularization of intact tissue enables MALDI imaging mass spectrometry analysis of the extracellular matrix: MALDI IMS of the extracellular matrix journal, October 2015

Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure journal, March 2012

Increased formation of pyridinoline cross-links due to higher telopeptide lysyl hydroxylase levels is a general fibrotic phenomenon journal, July 2004

From The Cover: Dysregulation of TGF- 1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice journal, October 2005

Oxidative Protein Cross-linking Reactions Involvingl-Tyrosine in Transforming Growth Factor-β1-stimulated Fibroblasts journal, May 2001

Systemic Soluble Receptor for Advanced Glycation Endproducts Is a Biomarker of Emphysema and Associated with AGER Genetic Variants in Patients with Chronic Obstructive Pulmonary Disease journal, October 2013

Stem cell fate dictated solely by altered nanotube dimension journal, January 2009

Contact Guidance Mediated Three-Dimensional Cell Migration is Regulated by Rho/ROCK-Dependent Matrix Reorganization journal, December 2008

Random versus directionally persistent cell migration journal, July 2009

Integrin α 4 β 1 Regulates Migration across Basement Membranes by Lung Fibroblasts: A Role for Phosphatase and Tensin Homologue Deleted on Chromosome 10 journal, August 2003

Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44 journal, June 2011

Idiopathic Pulmonary Fibrosis: Clinical Relevance of Pathologic Classification journal, April 1998

Engineering Substrate Topography at the Micro- and Nanoscale to Control Cell Function journal, July 2009

Microfabrication of poly (glycerol–sebacate) for contact guidance applications journal, April 2006

Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography journal, April 2003

Nanofibrous structured biomimetic strategies for skin tissue regeneration: Nanofibrous structures for wound healing journal, November 2012

Developmental alveolarization of the mouse lung
journal, August 2008

Extracellular matrix and the regulation of lung development and repair ¹
journal, August 1992

Idiopathic Pulmonary Fibrosis: Aberrant Recapitulation of Developmental Programs?
journal, March 2008

Developmental Reprogramming in Mesenchymal Stromal Cells of Human Subjects with Idiopathic Pulmonary Fibrosis
journal, November 2016

Distribution of laminin 5, integrin receptors, and branching morphogenesis during human fetal lung development
journal, September 2002

Hyaluronic acid of wound fluid in adult and fetal rabbits
journal, January 1997

Epithelial laminin α5 is necessary for distal epithelial cell maturation, VEGF production, and alveolization in the developing murine lung
journal, June 2005

Developmental Regulation of the Laminin α5 Chain Suggests a Role in Epithelial and Endothelial Cell Maturation
journal, September 1997

The Laminin α Chains: Expression, Developmental Transitions, and Chromosomal Locations of α1-5, Identification of Heterotrimeric Laminins 8–11, and Cloning of a Novel α3 Isoform
journal, May 1997

Immunohistochemical study of collagen types in human foetal lung and fibrotic lung disease.
journal, September 1981

Structural basis for the changing physical properties of human pulmonary vessels with age.
journal, June 1978

Control of Elastin Synthesis.
journal, July 1982

Differential expression of matrix metalloproteinases and their inhibitors in human and mouse lung development
journal, January 2005

Inhibition of cardiac myofibroblast formation and collagen synthesis by activation and overexpression of adenylyl cyclase
journal, December 2004

Mesenchyme specifies epithelial differentiation in reciprocal recombinants of embryonic lung and trachea
journal, August 1998

Proteoglycan and collagen expression during human air conducting system development
journal, June 2012

Heparan sulfate–FGF10 interactions during lung morphogenesis
journal, June 2003

Expression Profiling of the Developing Mouse Lung: Insights into the Establishment of the Extracellular Matrix
journal, May 2002

PDGF-A Signaling Is a Critical Event in Lung Alveolar Myofibroblast Development and Alveogenesis
journal, June 1996

Sulfatases are determinants of alveolar formation
journal, May 2012

Membrane-type 1 matrix metalloproteinase is required for normal alveolar development
journal, January 2005

Role of Matrix Metalloproteinase-2 in Newborn Mouse Lungs under Hypoxic Conditions
journal, January 2008

Low amniotic pressure in oligohydramnios—Is this the cause of pulmonary hypoplasia? .
journal, November 1989

Experimental pulmonary hypoplasia and oligohydramnios: Relative contributions of lung fluid and fetal breathing movements
journal, December 1984

The Strength of Mechanical Forces Determines the Differentiation of Alveolar Epithelial Cells
journal, February 2018

Mechanical Forces Program the Orientation of Cell Division during Airway Tube Morphogenesis
journal, February 2018

Stretch-induced alternative splicing of serum response factor promotes bronchial myogenesis and is defective in lung hypoplasia
journal, December 2000

Extracellular Matrix Structure and Tissue Stiffness Control Postnatal Lung Development through the Lipoprotein Receptor–Related Protein 5/Tie2 Signaling System
journal, December 2013

Pathology of Bronchopulmonary Dysplasia
journal, August 2006

Bronchopulmonary dysplasia: new insights
journal, September 2004

Collagen Scaffolding During Development and Its Deformation With Chronic Lung Disease
journal, April 2003

Lung Elastic Tissue Maturation and Perturbations During the Evolution of Chronic Lung Disease
journal, December 2000

Lysyl Oxidase Activity Is Dysregulated during Impaired Alveolarization of Mouse and Human Lungs
journal, December 2009

Mechanical ventilation uncouples synthesis and assembly of elastin and increases apoptosis in lungs of newborn mice.: Prelude to defective alveolar septation during lung development?
journal, January 2008

Diffuse Lung Disease in Young Children: Application of a Novel Classification Scheme
journal, December 2007

Prominent Intrapulmonary Bronchopulmonary Anastomoses and Abnormal Lung Development in Infants and Children with Down Syndrome
journal, January 2017

Overview of the Matrisome--An Inventory of Extracellular Matrix Constituents and Functions
journal, September 2011

Towards definition of an ECM parts list: An advance on GO categories
journal, September 2012

Defining the extracellular matrix using proteomics
journal, February 2013

The Matrisome: In Silico Definition and In Vivo Characterization by Proteomics of Normal and Tumor Extracellular Matrices
journal, April 2012

The extracellular matrix: Tools and insights for the “omics” era
journal, January 2016

Characterization of the Extracellular Matrix of Normal and Diseased Tissues Using Proteomics
journal, July 2017

Quantitative extracellular matrix proteomics to study mammary and liver tissue microenvironments
journal, December 2016

Targeted proteomics effectively quantifies differences between native lung and detergent-decellularized lung extracellular matrices
journal, December 2016

Time‐ and compartment‐resolved proteome profiling of the extracellular niche in lung injury and repair
journal, July 2015

ISDoT: in situ decellularization of tissues for high-resolution imaging and proteomic analysis of native extracellular matrix
journal, June 2017

Proteomic Analysis of Altered Extracellular Matrix Turnover in Bleomycin-induced Pulmonary Fibrosis
journal, July 2014

Quantitative proteomics identify Tenascin-C as a promoter of lung cancer progression and contributor to a signature prognostic of patient survival
journal, June 2017

Deep Proteome Profiling Reveals Common Prevalence of MZB1-Positive Plasma B Cells in Human Lung and Skin Fibrosis
journal, November 2017

The instructive extracellular matrix of the lung: basic composition and alterations in chronic lung disease
journal, July 2017

Extracellular Matrix Remodeling: The Common Denominator in Connective Tissue Diseases Possibilities for Evaluation and Current Understanding of the Matrix as More Than a Passive Architecture, but a Key Player in Tissue Failure
journal, March 2013

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

Proteolytic Post-translational Modification of Proteins: Proteomic Tools and Methodology
journal, December 2013

Glycomics Approach to Structure-Function Relationships of Glycosaminoglycans
journal, August 2006

A method for automated detection of gene expression required for the establishment of a digital transcriptome-wide gene expression atlas
journal, March 2005

A Suite of Activity-Based Probes for Human Cytochrome P450 Enzymes
journal, July 2009

Molecular imaging and depth profiling by mass spectrometry—SIMS, MALDI or DESI?
journal, January 2011

Tissue Imaging Using Nanospray Desorption Electrospray Ionization Mass Spectrometry
journal, December 2011

Automated Platform for High-Resolution Tissue Imaging Using Nanospray Desorption Electrospray Ionization Mass Spectrometry
journal, September 2012

SNAP-tag Based Proteomics Approach for the Study of the Retrograde Route: Proteomics of Retrograde Route
journal, April 2012

Decellularization of intact tissue enables MALDI imaging mass spectrometry analysis of the extracellular matrix: MALDI IMS of the extracellular matrix
journal, October 2015

Second harmonic generation microscopy for quantitative analysis of collagen fibrillar structure
journal, March 2012

Increased formation of pyridinoline cross-links due to higher telopeptide lysyl hydroxylase levels is a general fibrotic phenomenon
journal, July 2004

From The Cover: Dysregulation of TGF- 1 receptor activation leads to abnormal lung development and emphysema-like phenotype in core fucose-deficient mice
journal, October 2005

Oxidative Protein Cross-linking Reactions Involvingl-Tyrosine in Transforming Growth Factor-β1-stimulated Fibroblasts
journal, May 2001

Systemic Soluble Receptor for Advanced Glycation Endproducts Is a Biomarker of Emphysema and Associated with AGER Genetic Variants in Patients with Chronic Obstructive Pulmonary Disease
journal, October 2013

Stem cell fate dictated solely by altered nanotube dimension
journal, January 2009

Contact Guidance Mediated Three-Dimensional Cell Migration is Regulated by Rho/ROCK-Dependent Matrix Reorganization
journal, December 2008

Random versus directionally persistent cell migration
journal, July 2009

Integrin α ₄ β ₁ Regulates Migration across Basement Membranes by Lung Fibroblasts: A Role for Phosphatase and Tensin Homologue Deleted on Chromosome 10
journal, August 2003

Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44
journal, June 2011

Idiopathic Pulmonary Fibrosis: Clinical Relevance of Pathologic Classification
journal, April 1998

Engineering Substrate Topography at the Micro- and Nanoscale to Control Cell Function
journal, July 2009

Microfabrication of poly (glycerol–sebacate) for contact guidance applications
journal, April 2006

Nucleus alignment and cell signaling in fibroblasts: response to a micro-grooved topography
journal, April 2003

Nanofibrous structured biomimetic strategies for skin tissue regeneration: Nanofibrous structures for wound healing
journal, November 2012

Engineering microscale topographies to control the cell–substrate interface
journal, July 2012

An algorithm-based topographical biomaterials library to instruct cell fate
journal, September 2011

Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression
journal, August 2010

Acellular Normal and Fibrotic Human Lung Matrices as a Culture System for In Vitro Investigation
journal, November 2012