Modeling and measuring extracellular matrix alterations in fibrosis: challenges and perspectives for antifibrotic drug discovery

References

• Kolb M, Gauldie J, Bellaye PS. Editorial: extracellular matrix: the common thread of disease progression in fibrosis? Arthritis Rheumatol 2016;68(5):1053–1056.
   PubMed Web of Science ®Google Scholar
• Ghatak S, Maytin EV, Mack JA, Hascall VC, Atanelishvili I, Moreno Rodriguez R, et al. . Roles of proteoglycans and glycosaminoglycans in wound healing and fibrosis. Int J Cell Biol 2015;2015:834893.
   PubMedGoogle Scholar
• Hutchenreuther J, Leask A, Thompson K. Studying the CCN proteins in fibrosis. Methods Mol Biol 2017;1489:423–429.
   PubMedGoogle Scholar
• O’Dwyer DN, Moore BB. The role of periostin in lung fibrosis and airway remodeling. Cell Mol Life Sci 2017;74(23):4305–4314.
   PubMed Web of Science ®Google Scholar
• Wong SL, Sukkar MB. The SPARC protein: an overview of its role in lung cancer and pulmonary fibrosis and its potential role in chronic airways disease. Br J Pharmacol 2017;174(1):3–14.
   PubMed Web of Science ®Google Scholar
• Daley WP, Peters SB, Larsen M. Extracellular matrix dynamics in development and regenerative medicine. J Cell Sci 2008;121(Pt 3):255–264.
   PubMed Web of Science ®Google Scholar
• Karsdal MA, Manon-Jensen T, Genovese F, Kristensen JH, Nielsen MJ, Sand JM, et al. . Novel insights into the function and dynamics of extracellular matrix in liver fibrosis. Am J Physiol Gastrointest Liver Physiol 2015;308(10):G807–30.
   PubMed Web of Science ®Google Scholar
• Herrera J, Henke CA, Bitterman PB. Extracellular matrix as a driver of progressive fibrosis. J Clin Invest 2018;128(1):45–53.
   PubMed Web of Science ®Google Scholar
• Hinz B. The extracellular matrix and transforming growth factor-beta1: tale of a strained relationship. Matrix Biol 2015;47:54–65.
   PubMed Web of Science ®Google Scholar
• Santos A, Lagares D. Matrix stiffness: the conductor of organ fibrosis. Curr Rheumatol Rep 2018;20(1):2.
   PubMed Web of Science ®Google Scholar
• Wipff PJ, Hinz B. Integrins and the activation of latent transforming growth factor beta1 - an intimate relationship. Eur J Cell Biol 2008;87(8–9):601–615.
   PubMed Web of Science ®Google Scholar
• Cichon MA, Radisky DC. Extracellular matrix as a contextual determinant of transforming growth factor-beta signaling in epithelial-mesenchymal transition and in cancer. Cell Adh Migr 2014;8(6):588–594.
   PubMed Web of Science ®Google Scholar
• Yang C, Zeisberg M, Mosterman B, Sudhakar A, Yerramalla U, Holthaus K, et al. . Liver fibrosis: insights into migration of hepatic stellate cells in response to extracellular matrix and growth factors. Gastroenterology 2003;124(1):147–159.
   PubMed Web of Science ®Google Scholar
• Blaauboer ME, Boeijen FR, Emson CL, Turner SM, Zandieh-Doulabi B, Hanemaaijer R, et al. . Extracellular matrix proteins: a positive feedback loop in lung fibrosis? Matrix Biol 2014;34:170–178.
   PubMed Web of Science ®Google Scholar
• Gaggar A, Weathington N. Bioactive extracellular matrix fragments in lung health and disease. J Clin Invest 2016;126(9):3176–3184.
   PubMed Web of Science ®Google Scholar
• Ricard-Blum S, Salza R. Matricryptins and matrikines: biologically active fragments of the extracellular matrix. Exp Dermatol 2014;23(7):457–463.
   PubMed Web of Science ®Google Scholar
• Yamaguchi Y, Feghali-Bostwick CA. Role of endostatin in fibroproliferative disorders.-as a candidate for anti-fibrosis therapy. Nihon Rinsho Meneki Gakkai Kaishi 2013;36(6):452–458.
   PubMedGoogle Scholar
• Park J, Scherer PE. Adipocyte-derived endotrophin promotes malignant tumor progression. J Clin Invest 2012;122(11):4243–4256.
   PubMed Web of Science ®Google Scholar
• Sun K, Park J, Gupta OT, Holland WL, Auerbach P, Zhang N, et al. . Endotrophin triggers adipose tissue fibrosis and metabolic dysfunction. Nat Commun 2014;5:3485.
   PubMed Web of Science ®Google Scholar
• Jones B, Bucks C, Wilkinson P, Pratta M, Farrell F, Sivakumar P. Development of cell-based immunoassays to measure type I collagen in cultured fibroblasts. Int J Biochem Cell Biol 2010;42(11):1808–1815.
   PubMed Web of Science ®Google Scholar
• Fire A, Xu S, Montgomery MK, Kostas SA, Driver SE, Mello CC. Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 1998;391(6669):806–811.
   PubMed Web of Science ®Google Scholar
• Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T. Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 2001;411(6836):494–498.
   PubMed Web of Science ®Google Scholar
• Sachse C, Echeverri CJ. Oncology studies using siRNA libraries: the dawn of RNAi-based genomics. Oncogene 2004;23(51):8384–8391.
   PubMed Web of Science ®Google Scholar
• Massague J. TGFbeta signalling in context. Nat Rev Mol Cell Biol 2012;13(10):616–630.
   PubMed Web of Science ®Google Scholar
• Krieg T, Abraham D, Lafyatis R. Fibrosis in connective tissue disease: the role of the myofibroblast and fibroblast-epithelial cell interactions. Arthritis Res Ther 2007;9(Suppl 2):S4.
   PubMed Web of Science ®Google Scholar
• Sakai N, Tager AM. Fibrosis of two: epithelial cell-fibroblast interactions in pulmonary fibrosis. Biochim Biophys Acta 2013;1832(7):911–921.
   PubMed Web of Science ®Google Scholar
• Barron L, Wynn TA. Fibrosis is regulated by Th2 and Th17 responses and by dynamic interactions between fibroblasts and macrophages. Am J Physiol Gastrointest Liver Physiol 2011;300(5):G723–8.
   PubMed Web of Science ®Google Scholar
• Prasse A, Pechkovsky DV, Toews GB, Jungraithmayr W, Kollert F, Goldmann T, et al. . A vicious circle of alveolar macrophages and fibroblasts perpetuates pulmonary fibrosis via CCL18. Am J Respir Crit Care Med 2006;173(7):781–792.
   PubMed Web of Science ®Google Scholar
• Pradere JP, Kluwe J, De Minicis S, Jiao JJ, Gwak GY, Dapito DH, et al. . Hepatic macrophages but not dendritic cells contribute to liver fibrosis by promoting the survival of activated hepatic stellate cells in mice. Hepatology 2013;58(4):1461–1473.
   PubMed Web of Science ®Google Scholar
• Prasad S, Hogaboam CM, Jarai G. Deficient repair response of IPF fibroblasts in a co-culture model of epithelial injury and repair. Fibrogenesis Tissue Repair 2014;7:7.
   PubMedGoogle Scholar
• Van de Bovenkamp M, Groothuis GM, Meijer DK, Olinga P. Liver fibrosis in vitro: cell culture models and precision-cut liver slices. Toxicol in Vitro 2007;21(4):545–557.
   PubMed Web of Science ®Google Scholar
• Wygrecka M, Dahal BK, Kosanovic D, Petersen F, Taborski B, Von Gerlach S, et al. . Mast cells and fibroblasts work in concert to aggravate pulmonary fibrosis: role of transmembrane SCF and the PAR-2/PKC-alpha/Raf-1/p44/42 signaling pathway. Am J Pathol 2013;182(6):2094–2108.
   PubMed Web of Science ®Google Scholar
• Zhu L, Fu X, Chen X, Han X, Dong PM. 2 macrophages induce EMT through the TGF-beta/Smad2 signaling pathway. Cell Biol Int 2017;41(9):960–968.
   PubMed Web of Science ®Google Scholar
• Krause P, Saghatolislam F, Koenig S, Unthan-Fechner K, Probst I. Maintaining hepatocyte differentiation in vitro through co-culture with hepatic stellate cells. In Vitro Cell Dev Biol Anim 2009;45(5–6):205–212.
   PubMed Web of Science ®Google Scholar
• Kasuya J, Sudo R, Mitaka T, Ikeda M, Tanishita K. Hepatic stellate cell-mediated three-dimensional hepatocyte and endothelial cell triculture model. Tissue Eng Part A 2011;17(3–4):361–370.
   PubMed Web of Science ®Google Scholar
• Lee SA, No Da Y, Kang E, Ju J, Kim DS, Lee SH. Spheroid-based three-dimensional liver-on-a-chip to investigate hepatocyte-hepatic stellate cell interactions and flow effects. Lab Chip 2013;13(18):3529–3537.
   PubMed Web of Science ®Google Scholar
• Nguyen DG, Funk J, Robbins JB, Crogan-Grundy C, Presnell SC, Singer T, et al. . Bioprinted 3D primary liver tissues allow assessment of organ-level response to clinical drug induced toxicity in vitro. PLoS One 2016;11(7):e0158674.
   PubMed Web of Science ®Google Scholar
• Ramaiahgari SC, den Braver MW, Herpers B, Terpstra V, Commandeur JN, van de Water B, et al. . A 3D in vitro model of differentiated HepG2 cell spheroids with improved liver-like properties for repeated dose high-throughput toxicity studies. Arch Toxicol 2014;88(5):1083–1095.
   PubMed Web of Science ®Google Scholar
• van Grunsven LA. 3D in vitro models of liver fibrosis. Adv Drug Deliv Rev 2017;121:133–146.
   PubMed Web of Science ®Google Scholar
• Beckwitt CH, Clark AM, Wheeler S, Taylor DL, Stolz DB, Griffith L, et al. Liver ‘organ on a chip’. Exp Cell Res 2018;363(1):15–25.
   PubMed Web of Science ®Google Scholar
• Doryab A, Amoabediny G, Salehi-Najafabadi A. Advances in pulmonary therapy and drug development: lung tissue engineering to lung-on-a-chip. Biotechnol Adv 2016;34(5):588–596.
   PubMed Web of Science ®Google Scholar
• Gori M, Simonelli MC, Giannitelli SM, Businaro L, Trombetta M, Rainer A. Investigating Nonalcoholic Fatty liver disease in a liver-on-a-chip microfluidic device. PLoS One 2016;11(7):e0159729.
   PubMed Web of Science ®Google Scholar
• Knowlton S, Tasoglu S. A bioprinted liver-on-a-chip for drug screening applications. Trends Biotechnol 2016;34(9):681–682.
   PubMed Web of Science ®Google Scholar
• Konar D, Devarasetty M, Yildiz DV, Atala A, Murphy SV. Lung-on-a-chip technologies for disease modeling and drug development. Biomed Eng Comput Biol 2016;7(Suppl 1):17–27.
   PubMedGoogle Scholar
• Service RF. Bioengineering. Lung-On-A-Chip Breathes New Life into Drug Discovery Science 2012;338(6108):731.
   Google Scholar
• Chen CZ, Peng YX, Wang ZB, Fish PV, Kaar JL, Koepsel RR, et al. . The Scar-in-a-Jar: studying potential antifibrotic compounds from the epigenetic to extracellular level in a single well. Br J Pharmacol 2009;158(5):1196–1209.
   PubMed Web of Science ®Google Scholar
• Henjakovic M, Sewald K, Switalla S, Kaiser D, Muller M, Veres TZ, et al. . Ex vivo testing of immune responses in precision-cut lung slices. Toxicol Appl Pharmacol 2008;231(1):68–76.
   PubMed Web of Science ®Google Scholar
• Morin JP, Baste JM, Gay A, Crochemore C, Corbiere C, Monteil C. Precision cut lung slices as an efficient tool for in vitro lung physio-pharmacotoxicology studies. Xenobiotica 2013;43(1):63–72.
   PubMed Web of Science ®Google Scholar
• Olinga P, Schuppan D. Precision-cut liver slices: a tool to model the liver ex vivo. J Hepatol 2013;58(6):1252–1253.
   PubMed Web of Science ®Google Scholar
• Westra IM, Oosterhuis D, Groothuis GM, Olinga P. Precision-cut liver slices as a model for the early onset of liver fibrosis to test antifibrotic drugs. Toxicol Appl Pharmacol 2014;274(2):328–338.
   PubMed Web of Science ®Google Scholar
• Henjakovic M, Martin C, Hoymann HG, Sewald K, Ressmeyer AR, Dassow C, et al. . Ex vivo lung function measurements in precision-cut lung slices (PCLS) from chemical allergen-sensitized mice represent a suitable alternative to in vivo studies. Toxicol Sci 2008;106(2):444–453.
   PubMed Web of Science ®Google Scholar
• Roach KM, Sutcliffe A, Matthews L, Elliott G, Newby C, Amrani Y, et al. . A model of human lung fibrogenesis for the assessment of anti-fibrotic strategies in idiopathic pulmonary fibrosis. Sci Rep 2018;8(1):342.
   PubMed Web of Science ®Google Scholar
• Karsdal MA, Henriksen K, Leeming DJ, Woodworth T, Vassiliadis E, Bay-Jensen AC. Novel combinations of Post-Translational Modification (PTM) neo-epitopes provide tissue-specific biochemical markers–are they the cause or the consequence of the disease? Clin Biochem 2010;43(10–11):793–804.
   PubMed Web of Science ®Google Scholar
• Karsdal MA, Henriksen K, Nielsen MJ, Byrjalsen I, Leeming DJ, Gardner S, et al. . Fibrogenesis assessed by serological type III collagen formation identifies patients with progressive liver fibrosis and responders to a potential antifibrotic therapy. Am J Physiol Gastrointest Liver Physiol 2016;311(6):G1009–G17.
   PubMed Web of Science ®Google Scholar
• Jenkins RG, Simpson JK, Saini G, Bentley JH, Russell AM, Braybrooke R, et al. . Longitudinal change in collagen degradation biomarkers in idiopathic pulmonary fibrosis: an analysis from the prospective, multicentre PROFILE study. Lancet Respir Med 2015;3(6):462–472.
   PubMed Web of Science ®Google Scholar
• Leeming D, He Y, Veidal S, Nguyen Q, Larsen D, Koizumi M, et al. . A novel marker for assessment of liver matrix remodeling: an enzyme-linked immunosorbent assay (ELISA) detecting a MMP generated type I collagen neo-epitope (C1M). Biomarkers 2011;16(7):616–628.
   PubMed Web of Science ®Google Scholar
• Nielsen MJ, Kazankov K, Leeming DJ, Karsdal MA, Krag A, Barrera F, et al. . Markers of collagen remodeling detect clinically significant fibrosis in chronic hepatitis C patients. PLoS One 2015;10(9):e0137302.
   PubMed Web of Science ®Google Scholar
• Nielsen MJ, Veidal SS, Karsdal MA, Orsnes-Leeming DJ, Vainer B, Gardner SD, et al. . Plasma Pro-C3 (N-terminal type III collagen propeptide) predicts fibrosis progression in patients with chronic hepatitis C. Liver Int 2015;35(2):429–437.
   PubMed Web of Science ®Google Scholar
• Sakaida I, Matsumura Y, Kubota M, Kayano K, Takenaka K, Okita K. The prolyl 4-hydroxylase inhibitor HOE 077 prevents activation of Ito cells, reducing procollagen gene expression in rat liver fibrosis induced by choline-deficient L-amino acid-defined diet. Hepatology 1996;23(4):755–763.
   PubMed Web of Science ®Google Scholar
• Sakaida I, Uchida K, Hironaka K, Okita K. Prolyl 4-hydroxylase inhibitor (HOE 077) prevents TIMP-1 gene expression in rat liver fibrosis. J Gastroenterol 1999;34(3):376–377.
   PubMed Web of Science ®Google Scholar
• van der Slot AJ, Zuurmond AM, Bardoel AF, Wijmenga C, Pruijs HE, Sillence DO, et al. . Identification of PLOD2 as telopeptide lysyl hydroxylase, an important enzyme in fibrosis. J Biol Chem 2003;278(42):40967–40972.
   PubMed Web of Science ®Google Scholar
• Staab-Weijnitz CA, Fernandez IE, Knuppel L, Maul J, Heinzelmann K, Juan-Guardela BM, et al. . FK506-binding protein 10, a potential novel drug target for idiopathic pulmonary fibrosis. Am J Respir Crit Care Med 2015;192(4):455–467.
   PubMed Web of Science ®Google Scholar
• Otsuka M, Shiratori M, Chiba H, Kuronuma K, Sato Y, Niitsu Y, et al. . Treatment of pulmonary fibrosis with siRNA against a collagen-specific chaperone HSP47 in vitamin A-coupled liposomes. Exp Lung Res 2017;43(6–7):271–282.
   PubMed Web of Science ®Google Scholar
• Chung HJ, Steplewski A, Chung KY, Uitto J, Fertala A. Collagen fibril formation. New Target Limit Fibrosis J Biol Chem 2008;283(38):25879–25886.
   PubMed Web of Science ®Google Scholar
• Magdaleno F, Trebicka J. Selective LOXL2 inhibition: potent antifibrotic effects in ongoing fibrosis and fibrosis regression. Gut 2017;66(9):1540–1541.
   PubMed Web of Science ®Google Scholar
• Ikenaga N, Peng ZW, Vaid KA, Liu SB, Yoshida S, Sverdlov DY, et al. . Selective targeting of lysyl oxidase-like 2 (LOXL2) suppresses hepatic fibrosis progression and accelerates its reversal. Gut 2017;66(9):1697–1708.
   PubMed Web of Science ®Google Scholar
• Strandjord TP, Madtes DK, Weiss DJ, Sage EH. Collagen accumulation is decreased in SPARC-null mice with bleomycin-induced pulmonary fibrosis. Am J Physiol 1999;277(3 Pt 1):L628–35.
   PubMedGoogle Scholar
• Wang JC, Lai S, Guo X, Zhang X, De Crombrugghe B, Sonnylal S, et al. . Attenuation of fibrosis in vitro and in vivo with SPARC siRNA. Arthritis Res Ther 2010;12(2):R60.
   PubMed Web of Science ®Google Scholar
• Bhattacharyya S, Wang W, Morales-Nebreda L, Feng G, Wu M, Zhou X, et al. . Tenascin-C drives persistence of organ fibrosis. Nat Commun 2016;7:11703.
   PubMed Web of Science ®Google Scholar
• Craig VJ, Zhang L, Hagood JS, Owen CA. Matrix metalloproteinases as therapeutic targets for idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 2015;53(5):585–600.
   PubMed Web of Science ®Google Scholar
• Roderfeld M. Matrix metalloproteinase functions in hepatic injury and fibrosis. Matrix Biol 2018;68(69):452–62.
   PubMed Web of Science ®Google Scholar