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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:
 [1];  [2]; ORCiD logo [3]; ORCiD logo [4];  [5]; ORCiD logo [6]; ORCiD logo [7];  [8];  [9]; ORCiD logo [10];  [11];  [12];  [13];  [14];  [15]; ORCiD logo [6]; ORCiD logo [16];  [17];  [18]; ORCiD logo [2] more »;  [19];  [1] « less
  1. Univ. of Alabama, Birmingham, AL (United States). Division of Pulmonary, Allergy and Critical Care Medicine
  2. Univ. of Michigan, Ann Arbor, MI (United States). Division of Pulmonary and Critical Care Medicine
  3. Univ. of Illinois, Chicago, IL (United States). Dept. of Physiology & Biophysics
  4. Univ. of Alabama, Birmingham, AL (United States). Dept. of Pediatrics
  5. Univ. of California, San Francisco, CA (United States). Lung Biology Center
  6. Yale Univ., New Haven, CT (United States). Dept. of Anesthesiology
  7. Univ. of Minnesota, Minneapolis, MN (United States). Dept. of Medicine
  8. Pacific Northwest National Lab. (PNNL), Richland, WA (United States). Systems Toxicology & Exposure Science
  9. Cornell Univ., Ithaca, NY (United States). Weill Cornell Medical College
  10. Univ. of California, San Diego, CA (United States). Sanford Consortium for Regenerative Medicine
  11. Univ. of Colorado, Denver, CO (United States). Biochemistry & Molecular Genetics
  12. Univ. of California, San Diego, CA (United States). Pediatric Respiratory Medicine
  13. Baylor College of Medicine, Houston, TX (United States). Division of Pulmonary and Critical Care
  14. National Heart, Lung, and Blood Inst., Bethesda, MD (United States). Division of Lung Diseases
  15. Johns Hopkins Univ., Baltimore, MD (United States). School of Medicine. Division of Pulmonary and Critical Care Medicine
  16. Univ. of Pittsburgh, PA (United States). Division of Environmental and Occupational Health
  17. Cedars-Sinai Medical Center, Los Angeles, CA (United States). Dept. of Medicine
  18. Mayo Clinic College of Medicine, Rochester, MN (United States). Dept. of Physiology & Biomedical Engineering
  19. Univ. of California, San Francisco, CA (United States). Division of Pulmonary and Critical Care Medicine
Publication Date:
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.
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
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.
@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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Figures / Tables:

Figure 1 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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Exploring the Origins of Turbulence in Multiphase Flow Using Compressed Sensing MRI
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Noninvasive Imaging of Experimental Lung Fibrosis
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Stereological assessment of mouse lung parenchyma via nondestructive, multiscale micro-CT imaging validated by light microscopic histology
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Determinants of regional ventilation and blood flow in the lung
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High-resolution spatial measurements of ventilation-perfusion heterogeneity in rats
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Dynamic lineage analysis of embryonic morphogenesis using transgenic quail and 4D multispectral imaging
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Programmable in situ amplification for multiplexed imaging of mRNA expression
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Measurement of protein turnover rates by heavy water labeling of nonessential amino acids
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Longitudinal change in collagen degradation biomarkers in idiopathic pulmonary fibrosis: an analysis from the prospective, multicentre PROFILE study
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An overview of tissue and whole organ decellularization processes
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Decellularization of Human and Porcine Lung Tissues for Pulmonary Tissue Engineering
journal, September 2013


Comparative decellularization and recellularization of normal versus emphysematous human lungs
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Perfusion decellularization of human and porcine lungs: Bringing the matrix to clinical scale
journal, March 2014

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Production and Assessment of Decellularized Pig and Human Lung Scaffolds
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The effect of age and emphysematous and fibrotic injury on the re-cellularization of de-cellularized lungs
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The grateful dead: damage-associated molecular pattern molecules and reduction/oxidation regulate immunity
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Damage associated molecular pattern molecules
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Porcine small intestine submucosa (SIS) is not an acellular collagenous matrix and contains porcine DNA: Possible implications in human implantation
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Consequences of ineffective decellularization of biologic scaffolds on the host response
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Quantification of DNA in Biologic Scaffold Materials
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Influence of pH on Extracellular Matrix Preservation During Lung Decellularization
journal, December 2014

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Strategies for Whole Lung Tissue Engineering
journal, May 2014

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Can stem cells be used to generate new lungs? Ex vivo lung bioengineering with decellularized whole lung scaffolds: Ex vivo lung bioengineering
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A Nonhuman Primate Model of Lung Regeneration: Detergent-Mediated Decellularization and Initial In Vitro Recellularization with Mesenchymal Stem Cells
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Tissue-Engineered Lungs for in Vivo Implantation
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Development of a Decellularized Lung Bioreactor System for Bioengineering the Lung: The Matrix Reloaded
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Works referencing / citing this record:

Tissue-informed engineering strategies for modeling human pulmonary diseases
journal, February 2019

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ECM in Differentiation: A Review of Matrix Structure, Composition and Mechanical Properties
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Limitations of recellularized biological scaffolds for human transplantation
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  • Bilodeau, Claudia; Goltsis, Olivia; Rogers, Ian M.
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Matrisome analysis of intrahepatic cholangiocarcinoma unveils a peculiar cancer-associated extracellular matrix structure
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TM4SF5-mediated CD44v8-10 splicing variant promotes survival of type II alveolar epithelial cells during idiopathic pulmonary fibrosis
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Recent advances in our understanding of the mechanisms of lung alveolarization and bronchopulmonary dysplasia
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  • Lignelli, Ettore; Palumbo, Francesco; Myti, Despoina
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Amino acid transporters as tetraspanin TM4SF5 binding partners
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Integrating multiomics longitudinal data to reconstruct networks underlying lung development
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  • Ding, Jun; Ahangari, Farida; Espinoza, Celia R.
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Exploring the extracellular matrix in health and disease using proteomics
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β1 Integrin regulates adult lung alveolar epithelial cell inflammation
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Targeting arginine metabolism pathway to treat arginine-dependent cancers
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Figures/Tables have been extracted from DOE-funded journal article accepted manuscripts.