Matrix remodeling in pulmonary fibrosis and emphysema

American Journal of Respiratory Cell and Molecular Biology

Volumn 54, Issue 6, 2016, Pages 751-760

  Kulkarni, Tejaswini ^a,b   O'Reilly, Philip ^a,b   Antony, Veena B ^a,b   Gaggar, Amit ^a,b,c   Thannickal, Victor J ^a,b,c  

^a University of Alabama at Birmingham   (United States)

^b Program in Protease and Matrix Biology   (United States)

^c BIRMINGHAM VA MEDICAL CENTER   (United States)

Author keywords

Emphysema; Extracellular matrix; Myofibroblasts; Pulmonary fibrosis; Transforming growth factor

Indexed keywords

BLEOMYCIN; COLLAGEN; DECORIN; ELASTIN; FIBRONECTIN; GLYCOPROTEIN; GLYCOSAMINOGLYCAN; HYALURONIC ACID; PROTEOGLYCAN; SCLEROPROTEIN; TENASCIN; TRANSFORMING GROWTH FACTOR BETA1;

AIRWAY REMODELING; BLEOMYCIN-INDUCED PULMONARY FIBROSIS; CELL COMPOSITION; CELL DIFFERENTIATION; CELL FATE; CELL INTERACTION; CELL POPULATION; CELL REGENERATION; CELL SURVIVAL; CYTOLOGY; EXTRACELLULAR MATRIX; HISTOPATHOLOGY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LUNG EMPHYSEMA; LUNG FIBROBLAST; LUNG FIBROSIS; LUNG INJURY; MESENCHYME CELL; MOLECULAR DYNAMICS; MYOFIBROBLAST; NONHUMAN; PROTEIN EXPRESSION; REVIEW; RISK FACTOR; TISSUE INJURY; ANIMAL; COMPLICATION; FIBROBLAST; METABOLISM; PATHOLOGY; WOUND HEALING;

ANIMALS; EXTRACELLULAR MATRIX; FIBROBLASTS; HUMANS; LUNG INJURY; PULMONARY EMPHYSEMA; PULMONARY FIBROSIS; WOUND HEALING;

EID: 84988878332     PISSN: 10441549     EISSN: 15354989     Source Type: Journal    
DOI: 10.1165/rcmb.2015-0166PS     Document Type: Review

References (116)

1. Thannickal VJ, Henke CA, Horowitz JC, Noble PW, Roman J, Sime PJ, Zhou Y, Wells RG, White ES, Tschumperlin DJ. Matrix biology of idiopathic pulmonary fibrosis: a workshop report of the National Heart, Lung, and Blood Institute. Am J Pathol 2014;184:1643-1651.
2. Gross TJ, Hunninghake GW. Idiopathic pulmonary fibrosis. N Engl J Med 2001;345:517-525.
3. Kuhn III C, Boldt J, King TE Jr, Crouch E, Vartio T, McDonald JA. An immunohistochemical study of architectural remodeling and connective tissue synthesis in pulmonary fibrosis. Am Rev Respir Dis 1989;140:1693-1703.
4. Raghu G, Collard HR, Egan JJ, Martinez FJ, Behr J, Brown KK, Colby TV, Cordier JF, Flaherty KR, Lasky JA, et al.; ATS/ERS/JRS/ALAT Committee on Idiopathic Pulmonary Fibrosis. An official ATS/ERS/ JRS/ALAT statement: idiopathic pulmonary fibrosis: evidence-based guidelines for diagnosis and management. Am J Respir Crit Care Med 2011;183:788-824.
5. McDonough JE, Yuan R, Suzuki M, Seyednejad N, Elliott WM, Sanchez PG, Wright AC, Gefter WB, Litzky L, Coxson HO, et al. Small-airway obstruction and emphysema in chronic obstructive pulmonary disease. N Engl J Med 2011;365:1567-1575.
6. Taraseviciene-Stewart L, Voelkel NF. Molecular pathogenesis of emphysema. J Clin Invest 2008;118:394-402.
7. Awadalla NJ, Hegazy A, Elmetwally RA, Wahby I. Occupational and environmental risk factors for idiopathic pulmonary fibrosis in Egypt: a multicenter case-control study. Int J Occup Environ Med 2012;3: 107-116.
8. Taskar V, Coultas D. Exposures and idiopathic lung disease. Semin Respir Crit Care Med 2008;29:670-679.
9. Salvi SS, Barnes PJ. Chronic obstructive pulmonary disease in nonsmokers. Lancet 2009;374:733-743.
10. Chilosi M, Poletti V, Rossi A. The pathogenesis of COPD and IPF: distinct horns of the same devil? Respir Res 2012;13:3.
11. Thannickal VJ, Toews GB, White ES, Lynch III JP, Martinez FJ. Mechanisms of pulmonary fibrosis. Annu Rev Med 2004;55:395-417.
12. Antoniades HN, Bravo MA, Avila RE, Galanopoulos T, Neville-Golden J, Maxwell M, Selman M. Platelet-derived growth factor in idiopathic pulmonary fibrosis. J Clin Invest 1990;86:1055-1064.
13. Khalil N, O'Connor RN, Unruh HW, Warren PW, Flanders KC, Kemp A, Bereznay OH, Greenberg AH. Increased production and immunohistochemical localization of transforming growth factor-b in idiopathic pulmonary fibrosis. Am J Respir Cell Mol Biol 1991;5: 155-162.
14. Pan LH, Yamauchi K, Uzuki M, Nakanishi T, Takigawa M, Inoue H, Sawai T. Type II alveolar epithelial cells and interstitial fibroblasts express connective tissue growth factor in IPF. Eur Respir J 2001;17: 1220-1227.
15. Piguet PF, Ribaux C, Karpuz V, Grau GE, Kapanci Y. Expression and localization of tumor necrosis factor-a and its mRNA in idiopathic pulmonary fibrosis. Am J Pathol 1993;143:651-655.
16. Kolb M, Margetts PJ, Anthony DC, Pitossi F, Gauldie J. Transient expression of IL-1b induces acute lung injury and chronic repair leading to pulmonary fibrosis. J Clin Invest 2001;107: 1529-1536.
17. Giannandrea M, Parks WC. Diverse functions of matrix metalloproteinases during fibrosis. Dis Model Mech 2014;7: 193-203.
18. Noble PW, Barkauskas CE, Jiang D. Pulmonary fibrosis: patterns and perpetrators. J Clin Invest 2012;122:2756-2762.
19. Thannickal VJ, Zhou Y, Gaggar A, Duncan SR. Fibrosis: ultimate and proximate causes. J Clin Invest 2014;124:4673-4677.
20. Molet S, Belleguic C, Lena H, Germain N, Bertrand CP, Shapiro SD, Planquois JM, Delaval P, Lagente V. Increase in macrophage elastase (MMP-12) in lungs from patients with chronic obstructive pulmonary disease. Inflamm Res 2005;54:31-36.
21. Russell RE, Culpitt SV, DeMatos C, Donnelly L, Smith M, Wiggins J, Barnes PJ. Release and activity of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 by alveolar macrophages from patients with chronic obstructive pulmonary disease. Am J Respir Cell Mol Biol 2002;26:602-609.
22. Shapiro SD, Goldstein NM, Houghton AM, Kobayashi DK, Kelley D, Belaaouaj A. Neutrophil elastase contributes to cigarette smokeinduced emphysema in mice. Am J Pathol 2003;163:2329-2335.
23. Gaggar A, Jackson PL, Noerager BD, O'Reilly PJ, McQuaid DB, Rowe SM, Clancy JP, Blalock JE. A novel proteolytic cascade generates an extracellular matrix-derived chemoattractant in chronic neutrophilic inflammation. J Immunol 2008;180:5662-5669.
24. Houghton AM, Quintero PA, Perkins DL, Kobayashi DK, Kelley DG, Marconcini LA, Mecham RP, Senior RM, Shapiro SD. Elastin fragments drive disease progression in a murine model of emphysema. J Clin Invest 2006;116:753-759.
25. Liu Z, Zhou X, Shapiro SD, Shipley JM, Twining SS, Diaz LA, Senior RM, Werb Z. The serpin a1-proteinase inhibitor is a critical substrate for gelatinase B/MMP-9 in vivo. Cell 2000;102:647-655.
26. Togo S, Holz O, Liu X, Sugiura H, Kamio K, Wang X, Kawasaki S, Ahn Y, Fredriksson K, Skold CM, et al. Lung fibroblast repair functions in patients with chronic obstructive pulmonary disease are altered by multiple mechanisms. Am J Respir Crit Care Med 2008;178:248-260.
27. Hinz B, Phan SH, Thannickal VJ, Prunotto M, Desmoulière A, Varga J, De Wever O, Mareel M, Gabbiani G. Recent developments in myofibroblast biology: paradigms for connective tissue remodeling. Am J Pathol 2012;180:1340-1355.
28. Tomasek JJ, Gabbiani G, Hinz B, Chaponnier C, Brown RA. Myofibroblasts and mechano-regulation of connective tissue remodelling. Nat Rev Mol Cell Biol 2002;3:349-363.
29. Boström H, Willetts K, Pekny M, Levéen P, Lindahl P, Hedstrand H, Pekna M, Hellström M, Gebre-Medhin S, Schalling M, et al. PDGF-A signaling is a critical event in lung alveolar myofibroblast development and alveogenesis. Cell 1996;85:863-873.
30. Hashimoto N, Jin H, Liu T, Chensue SW, Phan SH. Bone marrowderived progenitor cells in pulmonary fibrosis. J Clin Invest 2004;113: 243-252.
31. Quan TE, Cowper S, Wu SP, Bockenstedt LK, Bucala R. Circulating fibrocytes: collagen-secreting cells of the peripheral blood. Int J Biochem Cell Biol 2004;36:598-606.
32. Willis BC, Liebler JM, Luby-Phelps K, Nicholson AG, Crandall ED, du Bois RM, Borok Z. Induction of epithelial-mesenchymal transition in alveolar epithelial cells by transforming growth factor-b1: potential role in idiopathic pulmonary fibrosis. Am J Pathol 2005;166: 1321-1332.
33. Rock JR, Barkauskas CE, Cronce MJ, Xue Y, Harris JR, Liang J, Noble PW, Hogan BL. Multiple stromal populations contribute to pulmonary fibrosis without evidence for epithelial to mesenchymal transition. Proc Natl Acad Sci USA 2011;108: E1475-E1483.
34. Desmoulière A, Geinoz A, Gabbiani F, Gabbiani G. Transforming growth factor-b 1 induces a-smooth muscle actin expression in granulation tissue myofibroblasts and in quiescent and growing cultured fibroblasts. J Cell Biol 1993;122:103-111.
35. Sime PJ, Xing Z, Graham FL, Csaky KG, Gauldie J. Adenovectormediated gene transfer of active transforming growth factor-b1 induces prolonged severe fibrosis in rat lung. J Clin Invest 1997;100: 768-776.
36. Huang X, Yang N, Fiore VF, Barker TH, Sun Y, Morris SW, Ding Q, Thannickal VJ, Zhou Y. Matrix stiffness-induced myofibroblast differentiation is mediated by intrinsic mechanotransduction. Am J Respir Cell Mol Biol 2012;47:340-348.
37. Parker MW, Rossi D, Peterson M, Smith K, Sikström K, White ES, Connett JE, Henke CA, Larsson O, Bitterman PB. Fibrotic extracellular matrix activates a profibrotic positive feedback loop. J Clin Invest 2014;124:1622-1635.
38. Zhou Y, Hagood JS, Lu B, Merryman WD, Murphy-Ullrich JE. Thy-1-integrin avb5 interactions inhibit lung fibroblast contraction-induced latent transforming growth factor-b1 activation and myofibroblast differentiation. J Biol Chem 2010;285:22382-22393.
39. Blaauboer ME, Boeijen FR, Emson CL, Turner SM, Zandieh-Doulabi B, Hanemaaijer R, Smit TH, Stoop R, Everts V. Extracellular matrix proteins: a positive feedback loop in lung fibrosis? Matrix Biol 2014;34:170-178.
40. Carthy JM, Meredith AJ, Boroomand S, Abraham T, Luo Z, Knight D, McManus BM. Versican V1 overexpression induces a myofibroblast-like phenotype in cultured fibroblasts. PLoS One 2015;10:e0133056.
41. Muro AF, Moretti FA, Moore BB, Yan M, Atrasz RG, Wilke CA, Flaherty KR, Martinez FJ, Tsui JL, Sheppard D, et al. An essential role for fibronectin extra type III domain A in pulmonary fibrosis. Am J Respir Crit Care Med 2008;177:638-645.
42. Serini G, Bochaton-Piallat ML, Ropraz P, Geinoz A, Borsi L, Zardi L, Gabbiani G. The fibronectin domain ED-A is crucial for myofibroblastic phenotype induction by transforming growth factorb1. J Cell Biol 1998;142:873-881.
43. Hecker L, Logsdon NJ, Kurundkar D, Kurundkar A, Bernard K, Hock T, Meldrum E, Sanders YY, Thannickal VJ. Reversal of persistent fibrosis in aging by targeting Nox4-Nrf2 redox imbalance. Sci Transl Med 2014;6:231ra47.
44. Thannickal VJ, Horowitz JC. Evolving concepts of apoptosis in idiopathic pulmonary fibrosis. Proc Am Thorac Soc 2006;3:350-356.
45. Lovgren AK, Kovacs JJ, Xie T, Potts EN, Li Y, Foster WM, Liang J, Meltzer EB, Jiang D, Lefkowitz RJ, et al. b-arrestin deficiency protects against pulmonary fibrosis in mice and prevents fibroblast invasion of extracellular matrix. Sci Transl Med 2011;3:74ra23.
46. Castella LF, Buscemi L, Godbout C, Meister JJ, Hinz B. A new lockstep mechanism of matrix remodelling based on subcellular contractile events. J Cell Sci 2010;123:1751-1760.
47. Huang S, Wettlaufer SH, Hogaboam C, Aronoff DM, Peters-Golden M. Prostaglandin E(2) inhibits collagen expression and proliferation in patient-derived normal lung fibroblasts via E prostanoid 2 receptor and cAMP signaling. Am J Physiol Lung Cell Mol Physiol 2007;292: L405-L413.
48. Kohyama T, Ertl RF, Valenti V, Spurzem J, Kawamoto M, Nakamura Y, Veys T, Allegra L, Romberger D, Rennard SI. Prostaglandin E(2) inhibits fibroblast chemotaxis. Am J Physiol Lung Cell Mol Physiol 2001;281:L1257-L1263.
49. Li YJ, Wang XQ, Sato T, Kanaji N, Nakanishi M, Kim M, Michalski J, Nelson AJ, Sun JH, Farid M, et al. Prostaglandin E2 inhibits human lung fibroblast chemotaxis through disparate actions on different E-prostanoid receptors. Am J Respir Cell Mol Biol 2011;44:99-107.
50. DiCamillo SJ, Carreras I, Panchenko MV, Stone PJ, Nugent MA, Foster JA, Panchenko MP. Elastase-released epidermal growth factor recruits epidermal growth factor receptor and extracellular signalregulated kinases to down-regulate tropoelastin mRNA in lung fibroblasts. J Biol Chem 2002;277:18938-18946.
51. DiCamillo SJ, Yang S, Panchenko MV, Toselli PA, Naggar EF, Rich CB, Stone PJ, Nugent MA, Panchenko MP. Neutrophil elastase-initiated EGFR/MEK/ERK signaling counteracts stabilizing effect of autocrine TGF-b on tropoelastin mRNA in lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2006;291:L232-L243.
52. Yang S, Nugent MA, Panchenko MP. EGF antagonizes TGF-b-induced tropoelastin expression in lung fibroblasts via stabilization of Smad corepressor TGIF. Am J Physiol Lung Cell Mol Physiol 2008;295: L143-L151.
53. Ning W, Dong Y, Sun J, Li C, Matthay MA, Feghali-Bostwick CA, Choi AM. Cigarette smoke stimulates matrix metalloproteinase-2 activity via EGR-1 in human lung fibroblasts. Am J Respir Cell Mol Biol 2007;36:480-490.
54. Kim H, Liu X, Kohyama T, Kobayashi T, Conner H, Abe S, Fang Q, Wen FQ, Rennard SI. Cigarette smoke stimulates MMP-1 production by human lung fibroblasts through the ERK1/2 pathway. COPD 2004;1: 13-23.
55. Carnevali S, Petruzzelli S, Longoni B, Vanacore R, Barale R, Cipollini M, Scatena F, Paggiaro P, Celi A, Giuntini C. Cigarette smoke extract induces oxidative stress and apoptosis in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2003;284:L955-L963.
56. Hynes RO, Naba A. Overview of the matrisome-an inventory of extracellular matrix constituents and functions. Cold Spring Harb Perspect Biol 2012;4:a004903.
57. Dunsmore SE, Rannels DE. Extracellular matrix biology in the lung. Am J Physiol 1996;270:L3-L27.
58. Bonnans C, Chou J, Werb Z. Remodelling the extracellular matrix in development and disease. Nat Rev Mol Cell Biol 2014;15:786-801.
59. Chien JW, Richards TJ, Gibson KF, Zhang Y, Lindell KO, Shao L, Lyman SK, Adamkewicz JI, Smith V, Kaminski N, et al. Serum lysyl oxidase-like 2 levels and idiopathic pulmonary fibrosis disease progression. Eur Respir J 2014;43:1430-1438.
60. Xia H, Seeman J, Hong J, Hergert P, Bodem V, Jessurun J, Smith K, Nho R, Kahm J, Gaillard P, et al. Low a(2)b(1) integrin function enhances the proliferation of fibroblasts from patients with idiopathic pulmonary fibrosis by activation of the b-catenin pathway. Am J Pathol 2012;181:222-233.
61. Xia H, Diebold D, Nho R, Perlman D, Kleidon J, Kahm J, Avdulov S, Peterson M, Nerva J, Bitterman P, et al. Pathological integrin signaling enhances proliferation of primary lung fibroblasts from patients with idiopathic pulmonary fibrosis. J Exp Med 2008;205: 1659-1672.
62. Kononov S, Brewer K, Sakai H, Cavalcante FS, Sabayanagam CR, Ingenito EP, Suki B. Roles of mechanical forces and collagen failure in the development of elastase-induced emphysema. Am J Respir Crit Care Med 2001;164:1920-1926.
63. Braber S, Koelink PJ, Henricks PA, Jackson PL, Nijkamp FP, Garssen J, Kraneveld AD, Blalock JE, Folkerts G. Cigarette smoke-induced lung emphysema in mice is associated with prolyl endopeptidase, an enzyme involved in collagen breakdown. Am J Physiol Lung Cell Mol Physiol 2011;300:L255-L265.
64. O'Reilly PJ, Hardison MT, Jackson PL, Xu X, Snelgrove RJ, Gaggar A, Galin FS, Blalock JE. Neutrophils contain prolyl endopeptidase and generate the chemotactic peptide, PGP, from collagen. J Neuroimmunol 2009;217:51-54.
65. Weathington NM, van Houwelingen AH, Noerager BD, Jackson PL, Kraneveld AD, Galin FS, Folkerts G, Nijkamp FP, Blalock JE. A novel peptide CXCR ligand derived from extracellular matrix degradation during airway inflammation. Nat Med 2006;12:317-323.
66. Shifren A, Mecham RP. The stumbling block in lung repair of emphysema: elastic fiber assembly. Proc Am Thorac Soc 2006;3: 428-433.
67. Owen CA. Proteinases and oxidants as targets in the treatment of chronic obstructive pulmonary disease. Proc Am Thorac Soc 2005; 2: 373-385.
68. Hautamaki RD, Kobayashi DK, Senior RM, Shapiro SD. Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice. Science 1997;277:2002-2004.
69. Pankov R, Yamada KM. Fibronectin at a glance. J Cell Sci 2002;115: 3861-3863.
70. Muro AF, Chauhan AK, Gajovic S, Iaconcig A, Porro F, Stanta G, Baralle FE. Regulated splicing of the fibronectin EDA exon is essential for proper skin wound healing and normal lifespan. J Cell Biol 2003;162: 149-160.
71. Martinez NM, Lynch KW. Control of alternative splicing in immune responses: many regulators, many predictions, much still to learn. Immunol Rev 2013;253:216-236.
72. Estany S, Vicens-Zygmunt V, Llatjós R, Montes A, Penín R, Escobar I, Xaubet A, Santos S, Manresa F, Dorca J, et al. Lung fibrotic tenascin-C upregulation is associated with other extracellular matrix proteins and induced by TGFb1. BMC Pulm Med 2014;14:120.
73. Borsi L, Castellani P, Risso AM, Leprini A, Zardi L. Transforming growth factor-b regulates the splicing pattern of fibronectin messenger RNA precursor. FEBS Lett 1990;261:175-178.
74. Balza E, Borsi L, Allemanni G, Zardi L. Transforming growth factor b regulates the levels of different fibronectin isoforms in normal human cultured fibroblasts. FEBS Lett 1988;228:42-44.
75. Olsen AL, Sackey BK, Marcinkiewicz C, Boettiger D, Wells RG. Fibronectin extra domain-A promotes hepatic stellate cell motility but not differentiation into myofibroblasts. Gastroenterology 2012; 142:928-937.
76. Trebaul A, Chan EK, Midwood KS. Regulation of fibroblast migration by tenascin-C. Biochem Soc Trans 2007;35:695-697.
77. Kohan M, Muro AF, White ES, Berkman N. EDA-containing cellular fibronectin induces fibroblast differentiation through binding to a4b7 integrin receptor and MAPK/Erk 1/2-dependent signaling. FASEB J 2010;24:4503-4512.
78. Carey WA, Taylor GD, Dean WB, Bristow JD. Tenascin-C deficiency attenuates TGF-?-mediated fibrosis following murine lung injury. Am J Physiol Lung Cell Mol Physiol 2010;299:L785-L793.
79. Annoni R, Lanças T, Yukimatsu Tanigawa R, de Medeiros Matsushita M, de Morais Fernezlian S, Bruno A, Fernando Ferraz da Silva L, Roughley PJ, Battaglia S, Dolhnikoff M, et al. Extracellular matrix composition in COPD. Eur Respir J 2012;40:1362-1373.
80. Karvonen HM, Lehtonen ST, Harju T, Sormunen RT, Lappi-Blanco E, Mäkinen JM, Laitakari K, Johnson S, Kaarteenaho RL. Myofibroblast expression in airways and alveoli is affected by smoking and COPD. Respir Res 2013;14:84.
81. Cavalcante FS, Ito S, Brewer K, Sakai H, Alencar AM, Almeida MP, Andrade JS Jr, Majumdar A, Ingenito EP, Suki B. Mechanical interactions between collagen and proteoglycans: implications for the stability of lung tissue. J Appl Physiol (1985) 2005;98:672-679.
82. Schaefer L, Schaefer RM. Proteoglycans: from structural compounds to signaling molecules. Cell Tissue Res 2010;339:237-246.
83. Bensadoun ES, Burke AK, Hogg JC, Roberts CR. Proteoglycan deposition in pulmonary fibrosis. Am J Respir Crit Care Med 1996;154:1819-1828.
84. Bracke KR, Dentener MA, Papakonstantinou E, Vernooy JH, Demoor T, Pauwels NS, Cleutjens J, van Suylen RJ, Joos GF, Brusselle GG, et al. Enhanced deposition of low-molecular-weight hyaluronan in lungs of cigarette smoke-exposed mice. Am J Respir Cell Mol Biol 2010;42:753-761.
85. Takahashi A, Majumdar A, Parameswaran H, Bartolák-Suki E, Suki B. Proteoglycans maintain lung stability in an elastase-treated mouse model of emphysema. Am J Respir Cell Mol Biol 2014;51:26-33.
86. Venkatesan N, Ebihara T, Roughley PJ, Ludwig MS. Alterations in large and small proteoglycans in bleomycin-induced pulmonary fibrosis in rats. Am J Respir Crit Care Med 2000;161:2066-2073.
87. Venkatesan N, Ouzzine M, Kolb M, Netter P, Ludwig MS. Increased deposition of chondroitin/dermatan sulfate glycosaminoglycan and upregulation of b1,3-glucuronosyltransferase I in pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2011;300:L191-L203.
88. Venkatesan N, Tsuchiya K, Kolb M, Farkas L, Bourhim M, Ouzzine M, Ludwig MS. Glycosyltransferases and glycosaminoglycans in bleomycin and transforming growth factor-b1-induced pulmonary fibrosis. Am J Respir Cell Mol Biol 2014;50:583-594.
89. Hallgren O, Nihlberg K, Dahlbäck M, Bjermer L, Eriksson LT, Erjefält JS, Löfdahl CG, Westergren-Thorsson G. Altered fibroblast proteoglycan production in COPD. Respir Res 2010;11:55.
90. Merrilees MJ, Ching PS, Beaumont B, Hinek A, Wight TN, Black PN. Changes in elastin, elastin binding protein and versican in alveoli in chronic obstructive pulmonary disease. Respir Res 2008;9:41.
91. Shimizukawa M, Ebina M, Narumi K, Kikuchi T, Munakata H, Nukiwa T. Intratracheal gene transfer of decorin reduces subpleural fibroproliferation induced by bleomycin. Am J Physiol Lung Cell Mol Physiol 2003;284:L526-L532.
92. Kolb M, Margetts PJ, Sime PJ, Gauldie J. Proteoglycans decorin and biglycan differentially modulate TGF-b-mediated fibrotic responses in the lung. Am J Physiol Lung Cell Mol Physiol 2001;280: L1327-L1334.
93. Yamaguchi Y, Mann DM, Ruoslahti E. Negative regulation of transforming growth factor-b by the proteoglycan decorin. Nature 1990;346:281-284.
94. van Straaten JF, Coers W, Noordhoek JA, Huitema S, Flipsen JT, Kauffman HF, Timens W, Postma DS. Proteoglycan changes in the extracellular matrix of lung tissue from patients with pulmonary emphysema. Mod Pathol 1999;12:697-705.
95. Noordhoek JA, Postma DS, Chong LL, Menkema L, Kauffman HF, Timens W, van Straaten JF, van der Geld YM. Different modulation of decorin production by lung fibroblasts from patients with mild and severe emphysema. COPD 2005;2:17-25.
96. Brandsma CA, Timens W, Jonker MR, Rutgers B, Noordhoek JA, Postma DS. Differential effects of fluticasone on extracellular matrix production by airway and parenchymal fibroblasts in severe COPD. Am J Physiol Lung Cell Mol Physiol 2013;305: L582-L589.
97. Turino GM, Cantor JO. Hyaluronan in respiratory injury and repair. Am J Respir Crit Care Med 2003;167:1169-1175.
98. Jiang D, Liang J, Noble PW. Hyaluronan in tissue injury and repair. Annu Rev Cell Dev Biol 2007;23:435-461.
99. Jiang D, Liang J, Fan J, Yu S, Chen S, Luo Y, Prestwich GD, Mascarenhas MM, Garg HG, Quinn DA, et al. Regulation of lung injury and repair by Toll-like receptors and hyaluronan. Nat Med 2005;11:1173-1179.
100. McDevitt CA, Beck GJ, Ciunga MJ, O'Brien J. Cigarette smoke degrades hyaluronic acid. Lung 1989;167:237-245.
101. Horton MR, Shapiro S, Bao C, Lowenstein CJ, Noble PW. Induction and regulation of macrophage metalloelastase by hyaluronan fragments in mouse macrophages. J Immunol 1999;162:4171-4176.
102. McKee CM, Penno MB, Cowman M, Burdick MD, Strieter RM, Bao C, Noble PW. Hyaluronan (HA) fragments induce chemokine gene expression in alveolar macrophages. The role of HA size and CD44. J Clin Invest 1996;98:2403-2413.
103. Zhou Y, Huang X, Hecker L, Kurundkar D, Kurundkar A, Liu H, Jin TH, Desai L, Bernard K, Thannickal VJ. Inhibition of mechanosensitive signaling in myofibroblasts ameliorates experimental pulmonary fibrosis. J Clin Invest 2013;123:1096-1108.
104. Annes JP, Munger JS, Rifkin DB. Making sense of latent TGFb activation. J Cell Sci 2003;116:217-224.
105. Munger JS, Huang X, Kawakatsu H, Griffiths MJ, Dalton SL, Wu J, Pittet JF, Kaminski N, Garat C, Matthay MA, et al. The integrin avb6 binds and activates latent TGF-b1: a mechanism for regulating pulmonary inflammation and fibrosis. Cell 1999;96: 319-328.
106. Wipff PJ, Rifkin DB, Meister JJ, Hinz B. Myofibroblast contraction activates latent TGF-b1 from the extracellular matrix. J Cell Biol 2007;179:1311-1323.
107. MassaguéJ. TGFb signalling in context. Nat Rev Mol Cell Biol 2012;13:616-630.
108. Shi Y, MassaguéJ. Mechanisms of TGF-b signaling from cell membrane to the nucleus. Cell 2003;113:685-700.
109. Horowitz JC, Rogers DS, Sharma V, Vittal R, White ES, Cui Z, Thannickal VJ. Combinatorial activation of FAK and AKT by transforming growth factor-b1 confers an anoikis-resistant phenotype to myofibroblasts. Cell Signal 2007;19:761-771.
110. Wu L, Chau J, Young RP, Pokorny V, Mills GD, Hopkins R, McLean L, Black PN. Transforming growth factor-b1 genotype and susceptibility to chronic obstructive pulmonary disease. Thorax 2004;59:126-129.
111. Zhang L, Chang WW, Ding H, Su H, Wang HY. Transforming growth factor-b1 polymorphisms and chronic obstructive pulmonary disease: a meta-analysis. Int J Tuberc Lung Dis 2011;15: 1301-1307.
112. Kessenbrock K, Plaks V, Werb Z. Matrix metalloproteinases: regulators of the tumor microenvironment. Cell 2010;141:52-67.
113. Kuang PP, Zhang XH, Rich CB, Foster JA, Subramanian M, Goldstein RH. Activation of elastin transcription by transforming growth factor-b in human lung fibroblasts. Am J Physiol Lung Cell Mol Physiol 2007;292:L944-L952.
114. Morris DG, Huang X, Kaminski N, Wang Y, Shapiro SD, Dolganov G, Glick A, Sheppard D. Loss of integrin avb6-mediated TGF-b activation causes Mmp12-dependent emphysema. Nature 2003;422:169-173.
115. Zhao J, Shi W, Wang YL, Chen H, Bringas P Jr, Datto MB, Frederick JP, Wang XF, Warburton D. Smad3 deficiency attenuates bleomycin-induced pulmonary fibrosis in mice. Am J Physiol Lung Cell Mol Physiol 2002;282:L585-L593.
116. Bonniaud P, Kolb M, Galt T, Robertson J, Robbins C, Stampfli M, Lavery C, Margetts PJ, Roberts AB, Gauldie J. Smad3 null mice develop airspace enlargement and are resistant to TGF-b-mediated pulmonary fibrosis. J Immunol 2004;173:2099-2108.