Three dimensional fibrotic extracellular matrix directs microenvironment fiber remodeling by fibroblasts

Idiopathic pulmonary fibrosis (IPF), for which effective treatments are limited, results in excessive and disorganized deposition of an aberrant extracellular matrix (ECM). An altered ECM microenvironment is postulated to contribute to disease perpetuation in a feed-forward manner through inducing profibrotic behavior by lung fibroblasts, the main producers and regulators of ECM. Here, we examined this hypothesis in a 3D in vitro model system by growing primary human lung fibroblasts in ECM-derived hydrogels from non-fibrotic (control) or IPF lung tissue. Culture of fibroblasts in fibrotic hydrogels did not trigger a change in the overall amount of collagen or glycosaminoglycans but did cause a drastic change in fiber organization compared to culture in control hydrogels. Mechanical properties of fibrotic hydrogels were modified by fibroblasts while control hydrogels were not. These results illustrate how the 3D microenvironment plays a crucial role in directing cells to exhibit pro-fibrotic responses by providing biochemical and/or biomechanical cues.

[1]  J. Otero,et al.  Innovative three-dimensional models for understanding mechanisms underlying lung diseases: powerful tools for translational research , 2023, European Respiratory Review.

[2]  J. Vonk,et al.  Age-associated Differences in the Human Lung Extracellular Matrix , 2023, bioRxiv.

[3]  J. Burgess,et al.  Current possibilities and future opportunities provided by three-dimensional lung ECM-derived hydrogels , 2023, Frontiers in Pharmacology.

[4]  D. Mooney,et al.  Hydrogel viscoelasticity modulates migration and fusion of mesenchymal stem cell spheroids , 2022, Bioengineering & translational medicine.

[5]  P. Šerbedžija,et al.  Chemical modification of human decellularized extracellular matrix for incorporation into phototunable hybrid-hydrogel models of tissue fibrosis , 2022, bioRxiv.

[6]  C. Sihlbom,et al.  Increased expression and accumulation of GDF15 in IPF extracellular matrix contribute to fibrosis , 2022, JCI insight.

[7]  Bradford J. Smith,et al.  Engineering Hybrid-Hydrogels Comprised of Healthy or Diseased Decellularized Extracellular Matrix to Study Pulmonary Fibrosis , 2022, Cellular and Molecular Bioengineering.

[8]  H. Tønnesen,et al.  Tuning of 2D cultured human fibroblast behavior using lumichrome photocrosslinked collagen hydrogels , 2022, Materials Today Communications.

[9]  Prashant K. Sharma,et al.  An in vitro model of fibrosis using crosslinked native extracellular matrix-derived hydrogels to modulate biomechanics without changing composition , 2022, bioRxiv.

[10]  J. Burgess,et al.  The Multi-Faceted Extracellular Matrix: Unlocking Its Secrets for Understanding the Perpetuation of Lung Fibrosis , 2021, Current Tissue Microenvironment Reports.

[11]  P. Sharma,et al.  Architecture and Composition Dictate Viscoelastic Properties of Organ-Derived Extracellular Matrix Hydrogels , 2021, Polymers.

[12]  M. D. de Jager,et al.  Adipose Stromal Cell-Secretome Counteracts Profibrotic Signals From IPF Lung Matrices , 2021, Frontiers in Pharmacology.

[13]  M. Schuliga,et al.  Regulation of Cellular Senescence Is Independent from Profibrotic Fibroblast-Deposited ECM , 2021, Cells.

[14]  Shalin B. Mehta,et al.  Contractility, focal adhesion orientation, and stress fiber orientation drive cancer cell polarity and migration along wavy ECM substrates , 2021, Proceedings of the National Academy of Sciences.

[15]  C. M. Magin,et al.  Engineering Tissue-Informed Biomaterials to Advance Pulmonary Regenerative Medicine , 2021, Frontiers in Medicine.

[16]  T. Wynn,et al.  Fibrosis: from mechanisms to medicines , 2020, Nature.

[17]  Christopher D. Davidson,et al.  Microengineered 3D pulmonary interstitial mimetics highlight a critical role for matrix degradation in myofibroblast differentiation , 2020, Science Advances.

[18]  Deniz A. Bölükbas,et al.  Clickable decellularized extracellular matrix as a new tool for building hybrid-hydrogels to model chronic fibrotic diseases in vitro. , 2020, Journal of materials chemistry. B.

[19]  M. Harmsen,et al.  Human lung extracellular matrix hydrogels resemble the stiffness and viscoelasticity of native lung tissue , 2020, American journal of physiology. Lung cellular and molecular physiology.

[20]  Danielle Park,et al.  A FIJI macro for quantifying pattern in extracellular matrix , 2019, Life Science Alliance.

[21]  P. Campagnola,et al.  Analysis of fibroblast migration dynamics in idiopathic pulmonary fibrosis using image-based scaffolds of the lung extracellular matrix. , 2019, American journal of physiology. Lung cellular and molecular physiology.

[22]  K. Stenmark,et al.  Tissue-informed engineering strategies for modeling human pulmonary diseases. , 2019, American journal of physiology. Lung cellular and molecular physiology.

[23]  L. Wollin,et al.  Fibroblast–matrix interplay: Nintedanib and pirfenidone modulate the effect of IPF fibroblast‐conditioned matrix on normal fibroblast phenotype , 2018, Respirology.

[24]  Mark G. Jones,et al.  Nanoscale dysregulation of collagen structure-function disrupts mechano-homeostasis and mediates pulmonary fibrosis , 2018, eLife.

[25]  E. White,et al.  Lysyl oxidases regulate fibrillar collagen remodelling in idiopathic pulmonary fibrosis , 2017, Disease Models & Mechanisms.

[26]  R. Hubbard,et al.  Extracellular Matrix Cross‐Linking Enhances Fibroblast Growth and Protects against Matrix Proteolysis in Lung Fibrosis , 2017, American journal of respiratory cell and molecular biology.

[27]  Adib Keikhosravi,et al.  Fluorescence of Picrosirius Red Multiplexed With Immunohistochemistry for the Quantitative Assessment of Collagen in Tissue Sections , 2017, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[28]  H. Schiller,et al.  The instructive extracellular matrix of the lung: basic composition and alterations in chronic lung disease , 2017, European Respiratory Journal.

[29]  R. Chambers,et al.  An Official American Thoracic Society Workshop Report: Use of Animal Models for the Preclinical Assessment of Potential Therapies for Pulmonary Fibrosis , 2017, American journal of respiratory cell and molecular biology.

[30]  S. Badylak,et al.  Extracellular matrix hydrogels from decellularized tissues: Structure and function. , 2017, Acta biomaterialia.

[31]  J. Karlsson,et al.  The extracellular matrix – the under‐recognized element in lung disease? , 2016, The Journal of pathology.

[32]  M. Sakagami,et al.  Development and characterization of a naturally derived lung extracellular matrix hydrogel. , 2016, Journal of biomedical materials research. Part A.

[33]  B. Alman,et al.  Prestress in the extracellular matrix sensitizes latent TGF-β1 for activation , 2014, The Journal of cell biology.

[34]  Vikas Singh,et al.  Second harmonic generation microscopy analysis of extracellular matrix changes in human idiopathic pulmonary fibrosis. , 2014, Journal of biomedical optics.

[35]  J. Connett,et al.  Fibrotic extracellular matrix activates a profibrotic positive feedback loop. , 2014, The Journal of clinical investigation.

[36]  T. Jensen,et al.  Can stem cells be used to generate new lungs? Ex vivo lung bioengineering with decellularized whole lung scaffolds , 2013, Respirology.

[37]  Kevin Weiss,et al.  Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation. , 2012, American journal of respiratory and critical care medicine.

[38]  Johannes E. Schindelin,et al.  Fiji: an open-source platform for biological-image analysis , 2012, Nature Methods.

[39]  H. Busscher,et al.  A comparative study on the viscoelastic properties of human and animal lenses. , 2011, Experimental eye research.

[40]  G. Raghu,et al.  Idiopathic pulmonary fibrosis: a disease with similarities and links to cancer biology , 2010, European Respiratory Journal.

[41]  R. Wells Faculty Opinions recommendation of Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix. , 2008 .

[42]  F Verrecchia,et al.  [Cellular and molecular mechanisms of fibrosis]. , 2006, Annales de pathologie.

[43]  D. Scharnweber,et al.  Fibrillogenesis of collagen types I, II, and III with small leucine-rich proteoglycans decorin and biglycan. , 2006, Biomacromolecules.

[44]  D. Postma,et al.  Different Modulation of Decorin Production by Lung Fibroblasts from Patients with Mild and Severe Emphysema , 2005, COPD.

[45]  Justin M. Dunn,et al.  Contractility , 2019, Contemporary Cardiology.

[46]  S. Rosselot Idiopathic pulmonary fibrosis. , 2014, Nursing standard (Royal College of Nursing (Great Britain) : 1987).