Matrix biology of idiopathic pulmonary fibrosis: A workshop report of the national heart, lung, and blood institute

American Journal of Pathology

Volumn 184, Issue 6, 2014, Pages 1643-1651

  Thannickal, Victor J ^a   Henke, Craig A ^b   Horowitz, Jeffrey C ^c   Noble, Paul W ^d   Roman, Jesse ^e   Sime, Patricia J ^f   Zhou, Yong ^a   Wells, Rebecca G ^g   White, Eric S ^c   Tschumperlin, Daniel J ^h  

^a University of Alabama at Birmingham   (United States)

^b UNIVERSITY OF MINNESOTA   (United States)

^c UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^d DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e University of Louisville School of Medicine   (United States)

^f UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

^g UNIVERSITY OF PENNSYLVANIA   (United States)

^h MAYO GRADUATE SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL SURFACE RECEPTOR; COLLAGEN; GLYCOPROTEIN; HYALURONIC ACID; INTEGRIN; POLYSACCHARIDE; PROTEOGLYCAN;

AGING; CYTOLOGY; DISEASE COURSE; EXTRACELLULAR MATRIX; FIBROSING ALVEOLITIS; HUMAN; LUNG ALVEOLUS CELL; LUNG DEVELOPMENT; NATIONAL HEALTH ORGANIZATION; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW; TISSUE REPAIR; ANIMAL; EDUCATION; GENETICS; METABOLISM; PATHOLOGY; PHYSIOLOGY; UNITED STATES;

AGING; ANIMALS; EDUCATION; EXTRACELLULAR MATRIX; HUMANS; IDIOPATHIC PULMONARY FIBROSIS; NATIONAL HEART, LUNG, AND BLOOD INSTITUTE (U.S.); UNITED STATES;

EID: 84901020197     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2014.02.003     Document Type: Review

References (84)

1. R.O. Hynes, and A. Naba Overview of the matrisome: an inventory of extracellular matrix constituents and functions Cold Spring Harb Perspect Biol 4 2012 a004903
2. C. Frantz, K.M. Stewart, and V.M. Weaver The extracellular matrix at a glance J Cell Sci 123 2010 4195 4200
3. S.E. McGowan Extracellular matrix and the regulation of lung development and repair FASEB J 6 1992 2895 2904
4. J.M. Shannon Induction of alveolar type II cell differentiation in fetal tracheal epithelium by grafted distal lung mesenchyme Dev Biol 166 1994 600 614
5. J.M. Shannon, and B.A. Hyatt Epithelial-mesenchymal interactions in the developing lung Annu Rev Physiol 66 2004 625 645
6. M. Selman, A. Pardo, and N. Kaminski Idiopathic pulmonary fibrosis: aberrant recapitulation of developmental programs? PLoS Med 5 2008 e62
7. W.D. Hardie, S.W. Glasser, and J.S. Hagood Emerging concepts in the pathogenesis of lung fibrosis Am J Pathol 175 2009 3 16
8. G. Raghu, D. Weycker, J. Edelsberg, W.Z. Bradford, and G. Oster Incidence and prevalence of idiopathic pulmonary fibrosis Am J Respir Crit Care Med 174 2006 810 816
9. S.P. Robins Biochemistry and functional significance of collagen cross-linking Biochem Soc Trans 35 2007 849 852
10. V.L. Kinnula, C.L. Fattman, R.J. Tan, and T.D. Oury Oxidative stress in pulmonary fibrosis: a possible role for redox modulatory therapy Am J Respir Crit Care Med 172 2005 417 422
11. J.M. Larios, R. Budhiraja, B.L. Fanburg, and V.J. Thannickal Oxidative protein cross-linking reactions involving L-tyrosine in transforming growth factor-beta1-stimulated fibroblasts J Biol Chem 276 2001 17437 17441
12. S.S. Iyer, A.M. Ramirez, J.D. Ritzenthaler, E. Torres-Gonzalez, S. Roser-Page, A.L. Mora, K.L. Brigham, D.P. Jones, J. Roman, and M. Rojas Oxidation of extracellular cysteine/cystine redox state in bleomycin-induced lung fibrosis Am J Physiol Lung Cell Mol Physiol 296 2009 L37 L45
13. G. Raghu, L.J. Striker, L.D. Hudson, and G.E. Striker Extracellular matrix in normal and fibrotic human lungs Am Rev Respir Dis 131 1985 281 289
14. A.J. Booth, R. Hadley, A.M. Cornett, A.A. Dreffs, S.A. Matthes, J.L. Tsui, K. Weiss, J.C. Horowitz, V.F. Fiore, T.H. Barker, B.B. Moore, F.J. Martinez, L.E. Niklason, and E.S. White Acellular normal and fibrotic human lung matrices as a culture system for in vitro investigation Am J Respir Crit Care Med 186 2012 866 876
15. C. Kuhn III, J. Boldt, T.E. King Jr., E. Crouch, T. Vartio, and J.A. McDonald An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis Am Rev Respir Dis 140 1989 1693 1703
16. H. Koyama, E.W. Raines, K.E. Bornfeldt, J.M. Roberts, and R. Ross Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of Cdk2 inhibitors Cell 87 1996 1069 1078
17. J. Ivaska, L. Nissinen, N. Immonen, J.E. Eriksson, V.M. Kahari, and J. Heino Integrin alpha 2 beta 1 promotes activation of protein phosphatase 2A and dephosphorylation of Akt and glycogen synthase kinase 3 beta Mol Cell Biol 22 2002 1352 1359
18. H. Xia, J. Seeman, J. Hong, P. Hergert, V. Bodem, J. Jessurun, K. Smith, R. Nho, J. Kahm, P. Gaillard, and C. Henke Low alpha(2)beta(1) integrin function enhances the proliferation of fibroblasts from patients with idiopathic pulmonary fibrosis by activation of the beta-catenin pathway Am J Pathol 181 2012 222 233
19. H. Xia, W. Khalil, J. Kahm, J. Jessurun, J. Kleidon, and C.A. Henke Pathologic caveolin-1 regulation of PTEN in idiopathic pulmonary fibrosis Am J Pathol 176 2010 2626 2637
20. H. Xia, D. Diebold, R. Nho, D. Perlman, J. Kleidon, J. Kahm, S. Avdulov, M. Peterson, J. Nerva, P. Bitterman, and C. Henke Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis J Exp Med 205 2008 1659 1672
21. G. Serini, M.L. Bochaton-Piallat, P. Ropraz, A. Geinoz, L. Borsi, L. Zardi, and G. Gabbiani The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factor-beta1 J Cell Biol 142 1998 873 881
22. A.L. Olsen, B.K. Sackey, C. Marcinkiewicz, D. Boettiger, and R.G. Wells Fibronectin extra domain-A promotes hepatic stellate cell motility but not differentiation into myofibroblasts Gastroenterology 142 2012 928 937.e3
23. A.F. Muro, F.A. Moretti, B.B. Moore, M. Yan, R.G. Atrasz, C.A. Wilke, K.R. Flaherty, F.J. Martinez, J.L. Tsui, D. Sheppard, F.E. Baralle, G.B. Toews, and E.S. White An essential role for fibronectin extra type III domain A in pulmonary fibrosis Am J Respir Crit Care Med 177 2008 638 645
24. P.K. Naik, P.D. Bozyk, J.K. Bentley, A.P. Popova, C.M. Birch, C.A. Wilke, C.D. Fry, E.S. White, T.H. Sisson, N. Tayob, B. Carnemolla, P. Orecchia, K.R. Flaherty, M.B. Hershenson, S. Murray, F.J. Martinez, B.B. Moore COMET Investigators Periostin promotes fibrosis and predicts progression in patients with idiopathic pulmonary fibrosis Am J Physiol Lung Cell Mol Physiol 303 2012 L1046 L1056
25. P. Teder, R.W. Vandivier, D. Jiang, J. Liang, L. Cohn, E. Pure, P.M. Henson, and P.W. Noble Resolution of lung inflammation by CD44 Science 296 2002 155 158
26. Y. Li, D. Jiang, J. Liang, E.B. Meltzer, A. Gray, R. Miura, L. Wogensen, Y. Yamaguchi, and P.W. Noble Severe lung fibrosis requires an invasive fibroblast phenotype regulated by hyaluronan and CD44 J Exp Med 208 2011 1459 1471
27. F.S. Cavalcante, S. Ito, K. Brewer, H. Sakai, A.M. Alencar, M.P. Almeida, J.S. Andrade Jr., A. Majumdar, E.P. Ingenito, and B. Suki Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue J Appl Physiol 98 2005 672 679
28. A. Fust, F. LeBellego, R.V. Iozzo, P.J. Roughley, and M.S. Ludwig Alterations in lung mechanics in decorin-deficient mice Am J Physiol Lung Cell Mol Physiol 288 2005 L159 L166
29. F. Liu, J.D. Mih, B.S. Shea, A.T. Kho, A.S. Sharif, A.M. Tager, and D.J. Tschumperlin Feedback amplification of fibrosis through matrix stiffening and COX-2 suppression J Cell Biol 190 2010 693 706
30. E.U. Azeloglu, J. Bhattacharya, and K.D. Costa Atomic force microscope elastography reveals phenotypic differences in alveolar cell stiffness J Appl Physiol 105 2008 652 661
31. C. Schulze, F. Wetzel, T. Kueper, A. Malsen, G. Muhr, S. Jaspers, T. Blatt, K.P. Wittern, H. Wenck, and J.A. Kas Stiffening of human skin fibroblasts with age Biophys J 99 2010 2434 2442
32. M. Dolhnikoff, T. Mauad, and M.S. Ludwig Extracellular matrix and oscillatory mechanics of rat lung parenchyma in bleomycin-induced fibrosis Am J Respir Crit Care Med 160 1999 1750 1757
33. R.J. Petrie, N. Gavara, R.S. Chadwick, and K.M. Yamada Nonpolarized signaling reveals two distinct modes of 3D cell migration J Cell Biol 197 2012 439 455
34. W.M. Kuebler, K. Parthasarathi, J. Lindert, and J. Bhattacharya Real-time lung microscopy J Appl Physiol 102 2007 1255 1264
35. T. Sera, H. Fujioka, H. Yokota, A. Makinouchi, R. Himeno, R.C. Schroter, and K. Tanishita Localized compliance of small airways in excised rat lungs using microfocal X-ray computed tomography J Appl Physiol 96 2004 1665 1673
36. K.P. McGee, R.D. Hubmayr, and R.L. Ehman MR elastography of the lung with hyperpolarized 3He Magn Reson Med 59 2008 14 18
37. J. Foucher, L. Castera, P.H. Bernard, X. Adhoute, D. Laharie, J. Bertet, P. Couzigou, and V. de Ledinghen Prevalence and factors associated with failure of liver stiffness measurement using FibroScan in a prospective study of 2114 examinations Eur J Gastroenterol Hepatol 18 2006 411 412
38. O. Rouviere, M. Yin, M.A. Dresner, P.J. Rossman, L.J. Burgart, J.L. Fidler, and R.L. Ehman MR elastography of the liver: preliminary results Radiology 240 2006 440 448
39. Z. Li, J.A. Dranoff, E.P. Chan, M. Uemura, J. Sevigny, and R.G. Wells Transforming growth factor-beta and substrate stiffness regulate portal fibroblast activation in culture Hepatology 46 2007 1246 1256
40. J.L. Balestrini, S. Chaudhry, V. Sarrazy, A. Koehler, and B. Hinz The mechanical memory of lung myofibroblasts Integr Biol (Camb) 4 2012 410 421
41. X. Huang, N. Yang, V.F. Fiore, T.H. Barker, Y. Sun, S.W. Morris, Q. Ding, V.J. Thannickal, and Y. Zhou Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction Am J Respir Cell Mol Biol 47 2012 340 348
42. P.J. Wipff, D.B. Rifkin, J.J. Meister, and B. Hinz Myofibroblast contraction activates latent TGF-beta1 from the extracellular matrix J Cell Biol 179 2007 1311 1323
43. C.P. Ng, B. Hinz, and M.A. Swartz Interstitial fluid flow induces myofibroblast differentiation and collagen alignment in vitro J Cell Sci 118 2005 4731 4739
44. F. Boudreault, and D.J. Tschumperlin Stretch-induced mitogen-activated protein kinase activation in lung fibroblasts is independent of receptor tyrosine kinases Am J Respir Cell Mol Biol 43 2010 64 73
45. W.H. Goldmann Mechanotransduction and focal adhesions Cell Biol Int 36 2012 649 652
46. V.J. Thannickal, D.Y. Lee, E.S. White, Z. Cui, J.M. Larios, R. Chacon, J.C. Horowitz, R.M. Day, and P.E. Thomas Myofibroblast differentiation by transforming growth factor-beta1 is dependent on cell adhesion and integrin signaling via focal adhesion kinase J Biol Chem 278 2003 12384 12389
47. J.C. Horowitz, D.S. Rogers, V. Sharma, R. Vittal, E.S. White, Z. Cui, and V.J. Thannickal Combinatorial activation of FAK and AKT by transforming growth factor-beta1 confers an anoikis-resistant phenotype to myofibroblasts Cell Signal 19 2007 761 771
48. H. Xia, R.S. Nho, J. Kahm, J. Kleidon, and C.A. Henke Focal adhesion kinase is upstream of phosphatidylinositol 3-kinase/Akt in regulating fibroblast survival in response to contraction of type I collagen matrices via a beta 1 integrin viability signaling pathway J Biol Chem 279 2004 33024 33034
49. V.W. Wong, K.C. Rustad, S. Akaishi, M. Sorkin, J.P. Glotzbach, M. Januszyk, E.R. Nelson, K. Levi, J. Paterno, I.N. Vial, A.A. Kuang, M.T. Longaker, and G.C. Gurtner Focal adhesion kinase links mechanical force to skin fibrosis via inflammatory signaling Nat Med 18 2012 148 152
50. E.N. Olson, and A. Nordheim Linking actin dynamics and gene transcription to drive cellular motile functions Nat Rev Mol Cell Biol 11 2010 353 365
51. Y. Zhou, X. Huang, L. Hecker, D. Kurundkar, A. Kurundkar, H. Liu, T.H. Jin, L. Desai, K. Bernard, and V.J. Thannickal Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis J Clin Invest 123 2013 1096 1108
52. M.S. Samuel, J.I. Lopez, E.J. McGhee, D.R. Croft, D. Strachan, P. Timpson, J. Munro, E. Schroder, J. Zhou, V.G. Brunton, N. Barker, H. Clevers, O.J. Sansom, K.I. Anderson, V.M. Weaver, and M.F. Olson Actomyosin-mediated cellular tension drives increased tissue stiffness and beta-catenin activation to induce epidermal hyperplasia and tumor growth Cancer Cell 19 2011 776 791
53. E. Charbonney, P. Speight, A. Masszi, H. Nakano, and A. Kapus Beta-catenin and Smad3 regulate the activity and stability of myocardin-related transcription factor during epithelial-myofibroblast transition Mol Biol Cell 22 2011 4472 4485
54. S. Dupont, L. Morsut, M. Aragona, E. Enzo, S. Giulitti, M. Cordenonsi, F. Zanconato, J. Le Digabel, M. Forcato, S. Bicciato, N. Elvassore, and S. Piccolo Role of YAP/TAZ in mechanotransduction Nature 474 2011 179 183
55. S. Sukharev, and F. Sachs Molecular force transduction by ion channels: diversity and unifying principles J Cell Sci 125 2012 3075 3083
56. G.J. Laurent Rates of collagen synthesis in lung, skin and muscle obtained in vivo by a simplified method using [3H]proline Biochem J 206 1982 535 544
57. G.J. Laurent, and R.J. McAnulty Protein metabolism during bleomycin-induced pulmonary fibrosis in rabbits: in vivo evidence for collagen accumulation because of increased synthesis and decreased degradation of the newly synthesized collagen Am Rev Respir Dis 128 1983 82 88
58. J.S. Duffield, M. Lupher, V.J. Thannickal, and T.A. Wynn Host responses in tissue repair and fibrosis Annu Rev Pathol 8 2013 241 276
59. N.C. Henderson, and J.P. Iredale Liver fibrosis: cellular mechanisms of progression and resolution Clin Sci 112 2007 265 280
60. C.G. Lee, S.J. Cho, M.J. Kang, S.P. Chapoval, P.J. Lee, P.W. Noble, T. Yehualaeshet, B. Lu, R.A. Flavell, J. Milbrandt, R.J. Homer, and J.A. Elias Early growth response gene 1-mediated apoptosis is essential for transforming growth factor beta1-induced pulmonary fibrosis J Exp Med 200 2004 377 389
61. W.E. Lawson, V.V. Polosukhin, G.T. Stathopoulos, O. Zoia, W. Han, K.B. Lane, B. Li, E.F. Donnelly, G.E. Holburn, K.G. Lewis, R.D. Collins, W.M. Hull, S.W. Glasser, J.A. Whitsett, and T.S. Blackwell Increased and prolonged pulmonary fibrosis in surfactant protein C-deficient mice following intratracheal bleomycin Am J Pathol 167 2005 1267 1277
62. L.G. McHugh, J.A. Milberg, M.E. Whitcomb, R.B. Schoene, R.J. Maunder, and L.D. Hudson Recovery of function in survivors of the acute respiratory distress syndrome Am J Respir Crit Care Med 150 1994 90 94
63. J.P. Iredale, R.C. Benyon, J. Pickering, M. McCullen, M. Northrop, S. Pawley, C. Hovell, and M.J. Arthur Mechanisms of spontaneous resolution of rat liver fibrosis: hepatic stellate cell apoptosis and reduced hepatic expression of metalloproteinase inhibitors J Clin Invest 102 1998 538 549
64. T.S. Blackwell, A.M. Tager, Z. Borok, B.B. Moore, D.A. Schwartz, and K.J. Anstrom et al. Future directions in idiopathic pulmonary fibrosis research: an NHLBI workshop report Am J Respir Crit Care Med 189 2014 214 222
65. A. Desmouliere, M. Redard, I. Darby, and G. Gabbiani Apoptosis mediates the decrease in cellularity during the transition between granulation tissue and scar Am J Pathol 146 1995 56 66
66. T. Kisseleva, M. Cong, Y. Paik, D. Scholten, C. Jiang, C. Benner, K. Iwaisako, T. Moore-Morris, B. Scott, H. Tsukamoto, S.M. Evans, W. Dillmann, C.K. Glass, and D.A. Brenner Myofibroblasts revert to an inactive phenotype during regression of liver fibrosis Proc Natl Acad Sci U S A 109 2012 9448 9453
67. L. Hecker, R. Jagirdar, T. Jin, and V.J. Thannickal Reversible differentiation of myofibroblasts by MyoD Exp Cell Res 317 2011 1914 1921
68. V. Krizhanovsky, M. Yon, R.A. Dickins, S. Hearn, J. Simon, C. Miething, H. Yee, L. Zender, and S.W. Lowe Senescence of activated stellate cells limits liver fibrosis Cell 134 2008 657 667
69. V.J. Thannickal, and J.C. Horowitz Evolving concepts of apoptosis in idiopathic pulmonary fibrosis Proc Am Thorac Soc 3 2006 350 356
70. K. Kis, X. Liu, and J.S. Hagood Myofibroblast differentiation and survival in fibrotic disease Expert Rev Mol Med 13 2011 e27
71. A. Pardo, M. Selman, and N. Kaminski Approaching the degradome in idiopathic pulmonary fibrosis Int J Biochem Cell Biol 40 2008 1141 1155
72. J.E. Gadek, J.A. Kelman, G. Fells, S.E. Weinberger, A.L. Horwitz, H.Y. Reynolds, J.D. Fulmer, and R.G. Crystal Collagenase in the lower respiratory tract of patients with idiopathic pulmonary fibrosis N Engl J Med 301 1979 737 742
73. R.C. Dancer, A.M. Wood, and D.R. Thickett Metalloproteinases in idiopathic pulmonary fibrosis Eur Respir J 38 2011 1461 1467
74. T.H. Sisson, and R.H. Simon The plasminogen activation system in lung disease Curr Drug Targets 8 2007 1016 1029
75. J.C. Horowitz, D.S. Rogers, R.H. Simon, T.H. Sisson, and V.J. Thannickal Plasminogen activation induced pericellular fibronectin proteolysis promotes fibroblast apoptosis Am J Respir Cell Mol Biol 38 2008 78 87
76. J.S. Duffield, S.J. Forbes, C.M. Constandinou, S. Clay, M. Partolina, S. Vuthoori, S. Wu, R. Lang, and J.P. Iredale Selective depletion of macrophages reveals distinct, opposing roles during liver injury and repair J Clin Invest 115 2005 56 65
77. R. Issa, X. Zhou, N. Trim, H. Millward-Sadler, S. Krane, C. Benyon, and J. Iredale Mutation in collagen-1 that confers resistance to the action of collagenase results in failure of recovery from CCl4-induced liver fibrosis, persistence of activated hepatic stellate cells, and diminished hepatocyte regeneration FASEB J 17 2003 47 49
78. R. Issa, X. Zhou, C.M. Constandinou, J. Fallowfield, H. Millward-Sadler, M.D. Gaca, E. Sands, I. Suliman, N. Trim, A. Knorr, M.J. Arthur, R.C. Benyon, and J.P. Iredale Spontaneous recovery from micronodular cirrhosis: evidence for incomplete resolution associated with matrix cross-linking Gastroenterology 126 2004 1795 1808
79. P.J. Sime, and K.M. O'Reilly Fibrosis of the lung and other tissues: new concepts in pathogenesis and treatment Clin Immunol 99 2001 308 319
80. G.S. Horan, S. Wood, V. Ona, D.J. Li, M.E. Lukashev, P.H. Weinreb, K.J. Simon, K. Hahm, N.E. Allaire, N.J. Rinaldi, J. Goyal, C.A. Feghali-Bostwick, E.L. Matteson, C. O'Hara, R. Lafyatis, G.S. Davis, X. Huang, D. Sheppard, and S.M. Violette Partial inhibition of integrin alpha(v)beta6 prevents pulmonary fibrosis without exacerbating inflammation Am J Respir Crit Care Med 177 2008 56 65
81. K.C. Olsen, R.E. Sapinoro, R.M. Kottmann, A.A. Kulkarni, S.E. Iismaa, G.V. Johnson, T.H. Thatcher, R.P. Phipps, and P.J. Sime Transglutaminase 2 and its role in pulmonary fibrosis Am J Respir Crit Care Med 184 2011 699 707
82. S. Li, X. Yang, W. Li, J. Li, X. Su, L. Chen, and G. Yan N-acetylcysteine downregulation of lysyl oxidase activity alleviating bleomycin-induced pulmonary fibrosis in rats Respiration 84 2012 509 517
83. P.C. Georges, J.J. Hui, Z. Gombos, M.E. McCormick, A.Y. Wang, M. Uemura, R. Mick, P.A. Janmey, E.E. Furth, and R.G. Wells Increased stiffness of the rat liver precedes matrix deposition: implications for fibrosis Am J Physiol Gastrointest Liver Physiol 293 2007 G1147 G1154
84. R.G. Wells The role of matrix stiffness in hepatic stellate cell activation and liver fibrosis J Clin Gastroenterol 39 2005 S158 S161