Pulmonary fibroblasts mobilize the membrane-tethered matrix metalloprotease, MT1-MMP, to destructively remodel and invade interstitial type I collagen barriers

American Journal of Physiology - Lung Cellular and Molecular Physiology

Volumn 301, Issue 5, 2011, Pages

  Rowe, R Grant ^a   Keena, Daniel ^a   Sabeh, Farideh ^a   Willis, Amanda L ^a   Weiss, Stephen J ^a  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

Author keywords

Collagenase; Extracellular matrix; Proteolysis

Indexed keywords

COLLAGEN TYPE 1; GAMMA INTERFERON; INTERLEUKIN 1BETA; INTERSTITIAL COLLAGENASE; MATRIX METALLOPROTEINASE; MATRIX METALLOPROTEINASE 14; MATRIX METALLOPROTEINASE 15; MEMBRANE TYPE 1 MATRIX METALLOPROTEASE; PLATELET DERIVED GROWTH FACTOR BB; SMALL INTERFERING RNA; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; COLLAGEN DEGRADATION; CONTROLLED STUDY; CROSS LINKING; EXTRACELLULAR MATRIX; FIBROBLAST; HUMAN; HUMAN CELL; HYDROGEL; IN VIVO STUDY; LUNG FIBROBLAST; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION;

AIRWAY REMODELING; ANIMALS; ASTHMA; CELL MOVEMENT; CHRONIC DISEASE; COLLAGEN TYPE I; EXTRACELLULAR MATRIX; FIBROBLASTS; GENE SILENCING; HUMANS; HYDROGELS; LUNG; MATRIX METALLOPROTEINASE 1; MATRIX METALLOPROTEINASE 14; MICE; MICE, KNOCKOUT; MICROSCOPY, CONFOCAL; PRIMARY CELL CULTURE; PROTEIN BINDING; PULMONARY FIBROSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING;

EID: 80055121889     PISSN: 10400605     EISSN: 15221504     Source Type: Journal    
DOI: 10.1152/ajplung.00187.2011     Document Type: Article

References (65)

1. Aimes RT, Quigley JP. Matrix metalloproteinase-2 is an interstitial collagenase. Inhibitor-free enzyme catalyzes the cleavage of collagen fibrils and soluble native type I collagen generating the specific 3/4- and 1/4-length fragments. J Biol Chem 270: 5872-5876, 1995.
2. Asano K, Shikama Y, Shoji N, Hirano K, Suzaki H, Nakajima H. Tiotropium bromide inhibits TGF-beta-induced MMP production from lung fibroblasts by interfering with Smad and MAPK pathways in vitro. Int J Chron Obstruct Pulmon Dis 5: 277-286, 2010.
3. Belvisi MG, Bottomley KM. The role of matrix metalloproteinases (MMPs) in the pathophysiology of chronic obstructive pulmonary disease (COPD): a therapeutic role for inhibitors of MMPs? Inflamm Res 52: 95-100, 2003.
4. Brinckerhoff CE, Matrisian LM. Matrix metalloproteinases: a tail of a frog that became a prince. Nat Rev Mol Cell Biol 3: 207-214, 2002.
5. Brown PD. Matrix metalloproteinase inhibitors in the treatment of cancer. Med Oncol 14: 1-10, 1997.
6. Chang HY, Chi JT, Dudoit S, Bondre C, van de Rijn M, Botstein D, Brown PO. Diversity, topographic differentiation, and positional memory in human fibroblasts. Proc Natl Acad Sci USA 99: 12877-12882, 2002.
7. Chapman HA. Epithelial-mesenchymal interactions in pulmonary fibrosis. Annu Rev Physiol 73: 413-435, 2011.
8. Chapman HA, Riese RJ, Shi GP. Emerging roles for cysteine proteases in human biology. Annu Rev Physiol 59: 63-88, 1997.
9. Chun TH, Hotary KB, Sabeh F, Saltiel AR, Allen ED, Weiss SJ. A pericellular collagenase directs the 3-dimensional development of white adipose tissue. Cell 125: 577-591, 2006.
10. Chun TH, Sabeh F, Ota I, Murphy H, McDonagh KT, Holmbeck K, Birkedal-Hansen H, Allen ED, Weiss SJ. MT1-MMP-dependent neovessel formation within the confines of the three-dimensional extracellular matrix. J Cell Biol 167: 757-767, 2004.
11. Corbel M, Belleguic C, Boichot E, Lagente V. Involvement of gelatinases (MMP-2 and MMP-9) in the development of airway inflammation and pulmonary fibrosis. Cell Biol Toxicol 18: 51-61, 2002.
12. Corbel M, Caulet-Maugendre S, Germain N, Molet S, Lagente V, Boichot E. Inhibition of bleomycin-induced pulmonary fibrosis in mice by the matrix metalloproteinase inhibitor batimastat. J Pathol 193: 538-545, 2001.
13. Creemers LB, Jansen DC, van Veen-Reurings A, van den Bos T, Everts V. Microassay for the assessment of low levels of hydroxyproline. Biotechniques 22: 656-658, 1997.
14. Crosby LM, Waters CM. Epithelial repair mechanisms in the lung. Am J Physiol Lung Cell Mol Physiol 298: L715-L731, 2010.
15. D'Alessio S, Ferrari G, Cinnante K, Scheerer W, Galloway AC, Roses DF, Rozanov DV, Remacle AG, Oh ES, Shiryaev SA, Strongin AY, Pintucci G, Mignatti P. Tissue inhibitor of metalloproteinases-2 binding to membrane-type 1 matrix metalloproteinase induces MAPK activation and cell growth by a non-proteolytic mechanism. J Biol Chem 283: 87-99, 2008.
16. Davidson JM. Biochemistry and turnover of lung interstitium. Eur Respir J 3: 1048-1063, 1990.
17. Devy L, Huang L, Naa L, Yanamandra N, Pieters H, Frans N, Chang E, Tao Q, Vanhove M, Lejeune A, van Gool R, Sexton DJ, Kuang G, Rank D, Hogan S, Pazmany C, Ma YL, Schoonbroodt S, Nixon AE, Ladner RC, Hoet R, Henderikx P, Tenhoor C, Rabbani SA, Valentino ML, Wood CR, Dransfield DT. Selective inhibition of matrix metalloproteinase-14 blocks tumor growth, invasion, and angiogenesis. Cancer Res 69: 1517-1526, 2009.
18. Dunsmore SE, Rannels DE. Extracellular matrix biology in the lung. Am J Physiol Lung Cell Mol Physiol 270: L3-L27, 1996.
19. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2: 161-174, 2002.
20. Elkington PT, Friedland JS. Matrix metalloproteinases in destructive pulmonary pathology. Thorax 61: 259-266, 2006.
21. Fredriksson K, Liu XD, Lundahl J, Klominek J, Rennard SI, Skold CM. Red blood cells increase secretion of matrix metalloproteinases from human lung fibroblasts in vitro. Am J Physiol Lung Cell Mol Physiol 290: L326-L333, 2006.
22. Friedl P, Wolf K. Plasticity of cell migration: a multiscale tuning model. J Cell Biol 188: 11-19, 2010.
23. Garcia-Alvarez J, Ramirez R, Sampieri CL, Nuttall RK, Edwards DR, Selman M, Pardo A. Membrane type-matrix metalloproteinases in idiopathic pulmonary fibrosis. Sarcoidosis Vasc Diffuse Lung Dis 23: 13-21, 2006.
24. Hinz B, Phan SH, Thannickal VJ, Galli A, Bochaton-Piallat ML, Gabbiani G. The myofibroblast: one function, multiple origins. Am J Pathol 170: 1807-1816, 2007.
25. Holmbeck K, Bianco P, Caterina J, Yamada S, Kromer M, Kuznetsov SA, Mankani M, Robey PG, Poole AR, Pidoux I, Ward JM, Birkedal-Hansen H. MT1-MMP-deficient mice develop dwarfism, osteopenia, arthritis, and connective tissue disease due to inadequate collagen turnover. Cell 99: 81-92, 1999.
26. Hotary K, Allen E, Punturieri A, Yana I, Weiss SJ. Regulation of cell invasion and morphogenesis in a three-dimensional type I collagen matrix by membrane-type matrix metalloproteinases 1, 2, and 3. J Cell Biol 149: 1309-1323, 2000.
27. Hotary K, Li XY, Allen E, Stevens SL, Weiss SJ. A cancer cell metalloprotease triad regulates the basement membrane transmigration program. Genes Dev 20: 2673-2686, 2006.
28. Hotary KB, Allen ED, Brooks PC, Datta NS, Long MW, Weiss SJ. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 114: 33-45, 2003.
29. Hotary KB, Yana I, Sabeh F, Li XY, Holmbeck K, Birkedal-Hansen H, Allen ED, Hiraoka N, Weiss SJ. Matrix metalloproteinases (MMPs) regulate fibrin-invasive activity via MT1-MMP-dependent and -independent processes. J Exp Med 195: 295-308, 2002.
30. Ignat'eva NY, Danilov NA, Averkiev SV, Obrezkova MV, Lunin VV, Sobol EN. Determination of hydroxyproline in tissues and the evaluation of the collagen content of the tissues. Anal Chem 62: 51-57, 2007.
31. Inada M, Wang Y, Byrne MH, Rahman MU, Miyaura C, Lopez-Otin C, Krane SM. Critical roles for collagenase-3 (Mmp13) in development of growth plate cartilage and in endochondral ossification. Proc Natl Acad Sci USA 101: 17192-17197, 2004.
32. Itoh T, Tanioka M, Yoshida H, Yoshioka T, Nishimoto H, Itohara S. Reduced angiogenesis and tumor progression in gelatinase A-deficient mice. Cancer Res 58: 1048-1051, 1998.
33. Kang T, Yi J, Yang W, Wang X, Jiang A, Pei D. Functional characterization of MT3-MMP in transfected MDCK cells: progelatinase A activation and tubulogenesis in 3-D collagen lattice. FASEB J 14: 2559-2568, 2000.
34. Krane SM, Inada M. Matrix metalloproteinases and bone. Bone 43: 7-18, 2008.
35. Kunugi S, Fukuda Y, Ishizaki M, Yamanaka N. Role of MMP-2 in alveolar epithelial cell repair after bleomycin administration in rabbits. Lab Invest 81: 1309-1318, 2001.
36. Langlois S, Nyalendo C, Di Tomasso G, Labrecque L, Roghi C, Murphy G, Gingras D, Beliveau R. Membrane-type 1 matrix metalloproteinase stimulates cell migration through epidermal growth factor receptor transactivation. Mol Cancer Res 5: 569-583, 2007.
37. Li Q, Park PW, Wilson CL, Parks WC. Matrilysin shedding of syndecan- 1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 111: 635-646, 2002.
38. Li XY, Ota I, Yana I, Sabeh F, Weiss SJ. Molecular dissection of the structural machinery underlying the tissue-invasive activity of membrane type-1 matrix metalloproteinase. Mol Biol Cell 19: 3221-3233, 2008.
39. Maher TM, Wells AU, Laurent GJ. Idiopathic pulmonary fibrosis: multiple causes and multiple mechanisms? Eur Respir J 30: 835-839, 2007.
40. Maisi P, Prikk K, Sepper R, Pirila E, Salo T, Hietanen J, Sorsa T. Soluble membrane-type 1 matrix metalloproteinase (MT1-MMP) and gelatinase A (MMP-2) in induced sputum and bronchoalveolar lavage fluid of human bronchial asthma and bronchiectasis. APMIS 110: 771-782, 2002.
41. Martin P. Wound healing-aiming for perfect skin regeneration. Science 276: 75-81, 1997.
42. Masur SK, Dewal HS, Dinh TT, Erenburg I, Petridou S. Myofibroblasts differentiate from fibroblasts when plated at low density. Proc Natl Acad Sci USA 93: 4219-4223, 1996.
43. Mikko M, Fredriksson K, Wahlstrom J, Eriksson P, Grunewald J, Skold CM. Human T cells stimulate fibroblast-mediated degradation of extracellular matrix in vitro. Clin Exp Immunol 151: 317-325, 2008.
44. Netzel-Arnett S, Mitola DJ, Yamada SS, Chrysovergis K, Holmbeck K, Birkedal-Hansen H, Bugge TH. Collagen dissolution by keratinocytes requires cell surface plasminogen activation and matrix metalloproteinase activity. J Biol Chem 277: 45154-45161, 2002.
45. Nyalendo C, Michaud M, Beaulieu E, Roghi C, Murphy G, Gingras D, Beliveau R. Src-dependent phosphorylation of membrane type I matrix metalloproteinase on cytoplasmic tyrosine 573: role in endothelial and tumor cell migration. J Biol Chem 282: 15690-15699, 2007.
46. Ohnishi K, Takagi M, Kurokawa Y, Satomi S, Konttinen YT. Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema. Lab Invest 78: 1077-1087, 1998.
47. Page-McCaw A, Ewald AJ, Werb Z. Matrix metalloproteinases and the regulation of tissue remodelling. Nat Rev Mol Cell Biol 8: 221-233, 2007.
48. Pardo A, Selman M. Matrix metalloproteases in aberrant fibrotic tissue remodeling. Proc Am Thorac Soc 3: 383-388, 2006.
49. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 4: 617-629, 2004.
50. Racke K, Haag S, Bahulayan A, Warnken M. Pulmonary fibroblasts, an emerging target for anti-obstructive drugs. Naunyn Schmiedebergs Arch Pharmacol 378: 193-201, 2008.
51. Rowe RG, Weiss SJ. Breaching the basement membrane: who, when and how? Trends Cell Biol 18: 560-574, 2008.
52. Rowe RG, Weiss SJ. Navigating ECM barriers at the invasive front: the cancer cell-stroma interface. Annu Rev Cell Dev Biol 25: 567-595, 2009.
53. Sabeh F, Li XY, Saunders TL, Rowe RG, Weiss SJ. Secreted versus membrane-anchored collagenases: relative roles in fibroblast-dependent collagenolysis and invasion. J Biol Chem 284: 23001-23011, 2009.
54. Sabeh F, Ota I, Holmbeck K, Birkedal-Hansen H, Soloway P, Balbin M, Lopez-Otin C, Shapiro S, Inada M, Krane S, Allen E, Chung D, Weiss SJ. Tumor cell traffic through the extracellular matrix is controlled by the membrane-anchored collagenase MT1-MMP. J Cell Biol 167: 769-781, 2004.
55. Sabeh F, Shimizu-Hirota R, Weiss SJ. Protease-dependent versus -independent cancer cell invasion programs: three-dimensional amoeboid movement revisited. J Cell Biol 185: 11-19, 2009.
56. Sasaki M, Kashima M, Ito T, Watanabe A, Izumiyama N, Sano M, Kagaya M, Shioya T, Miura M. Differential regulation of metalloproteinase production, proliferation and chemotaxis of human lung fibroblasts by PDGF, interleukin-1beta and TNF-alpha. Mediators Inflamm 9: 155-160, 2000.
57. Sato H, Takino T. Coordinate action of membrane-type matrix metalloproteinase- 1 (MT1-MMP) and MMP-2 enhances pericellular proteolysis and invasion. Cancer Sci 101: 843-847, 2010.
58. Scotton CJ, Chambers RC. Molecular targets in pulmonary fibrosis: the myofibroblast in focus. Chest 132: 1311-1321, 2007.
59. Sounni NE, Dehne K, van Kempen L, Egeblad M, Affara NI, Cuevas I, Wiesen J, Junankar S, Korets L, Lee J, Shen J, Morrison CJ, Overall CM, Krane SM, Werb Z, Boudreau N, Coussens LM. Stromal regulation of vessel stability by MMP14 and TGFbeta. Dis Model Mech 3: 317-332, 2010.
60. Tang ML, Wilson JW, Stewart AG, Royce SG. Airway remodelling in asthma: current understanding and implications for future therapies. Pharmacol Ther 112: 474-488, 2006.
61. Togo S, Holz O, Liu X, Sugiura H, Kamio K, Wang X, Kawasaki S, Ahn Y, Fredriksson K, Skold CM, Mueller KC, Branscheid D, Welker L, Watz H, Magnussen H, Rennard SI. Lung fibroblast repair functions in patients with chronic obstructive pulmonary disease are altered by multiple mechanisms. Am J Respir Crit Care Med 178: 248-260, 2008.
62. van den Brule S, Misson P, Buhling F, Lison D, Huaux F. Overexpression of cathepsin K during silica-induced lung fibrosis and control by TGF-beta. Respir Res 6: 84-97, 2005.
63. Weiss SJ. Tissue destruction by neutrophils. N Engl J Med 320: 365-376, 1989.
64. Zhou X, Rowe RG, Hiraoka N, George JP, Wirtz D, Mosher DF, Virtanen I, Chernousov MA, Weiss SJ. Fibronectin fibrillogenesis regulates three-dimensional neovessel formation. Genes Dev 22: 1231-1243, 2008.
65. Zhu Y, Liu X, Skold CM, Wang H, Kohyama T, Wen FQ, Ertl RF, Rennard SI. Collaborative interactions between neutrophil elastase and metalloproteinases in extracellular matrix degradation in three-dimensional collagen gels. Respir Res 2: 300-305, 2001.