Matrix metalloproteinase-14 mediates a phenotypic shift in the airways to increase mucin production

American Journal of Respiratory and Critical Care Medicine

Volumn 180, Issue 9, 2009, Pages 834-845

  Deshmukh, Hitesh S ^a   McLachlan, Anne ^b   Atkinson, Jeffrey J ^c   Hardie, William D ^d   Korfhagen, Thomas R ^d   Dietsch, Maggie ^a   Liu, Yang ^e   Di, Peter Y P ^e   Wesselkamper, Scott C ^a   Borchers, Michael T ^a   Leikauf, George D ^e  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d CINCINNATI CHILDREN'S HOSPITAL MEDICAL CENTER   (United States)

^e UNIVERSITY OF PITTSBURGH GRADUATE SCHOOL OF PUBLIC HEALTH   (United States)

Author keywords

Acrolein; Chronic obstructive pulmonary disease; Cigarette smoke; Erlotinib; Mucous cell metaplasia

Indexed keywords

ACROLEIN; CYSTEINE; DEXTRO ARGININE; EPIDERMAL GROWTH FACTOR RECEPTOR ANTIBODY; EPIDERMAL GROWTH FACTOR RECEPTOR KINASE INHIBITOR; MATRIX METALLOPROTEINASE 14; MITOGEN ACTIVATED PROTEIN KINASE INHIBITOR; MITOGEN ACTIVATED PROTEIN KINASE P38 INHIBITOR; MUCIN 5AC; NEUTRALIZING ANTIBODY; SMALL INTERFERING RNA; TOBACCO SMOKE; TRANSFORMING GROWTH FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHRONIC OBSTRUCTIVE LUNG DISEASE; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; RESPIRATORY EPITHELIUM;

ACROLEIN; ANIMALS; ENZYME ACTIVATION; EPITHELIAL CELLS; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HUMANS; LUNG; MATRIX METALLOPROTEINASE 14; MICE; MUCINS; PROTEIN KINASE INHIBITORS; PULMONARY DISEASE, CHRONIC OBSTRUCTIVE; QUINAZOLINES; RESPIRATORY MUCOSA;

EID: 70350435126     PISSN: 1073449X     EISSN: 15354970     Source Type: Journal    
DOI: 10.1164/rccm.200903-0328OC     Document Type: Article

References (97)

1. Mannino DM, Homa DM, Akinbami LJ, Ford ES, Redd SC. Chronic obstructive pulmonary disease surveillance:-United States, 1971-2000. MMWR Surveill Summ 2002;51:1-16.
2. Perez-Vilar J. Mucin granule intraluminal organization. Am J Respir Cell Mol Biol 2007;36:183-190.
3. Hogg JC. Pathophysiology of airflow limitation in chronic obstructive pulmonary disease. Lancet 2004;364:709-721. (Pubitemid 39140629)
4. Rabe KF, Hurd S, Anzueto A, Barnes PJ, Buist SA, Calverley P, Fukuchi Y, Jenkins C, Rodriguez-Roisin R, van Weel C, et al. Global strategy for the diagnosis, management, and prevention of chronic obstructive pulmonary disease: GOLD executive summary. Am J Respir Crit Care Med 2007;176:532-555. (Pubitemid 47403272)
5. Shapiro SD, Ingenito EP. The pathogenesis of chronic obstructive pulmonary disease: advances in the past 100 years. Am J Respir Cell Mol Biol 2005;32:367-372. (Pubitemid 40629320)
6. Celli BR, Halbert RJ, Nordyke RJ, Schau B. Airway obstruction in never smokers: results from the Third National Health and Nutrition Examination Survey. Am J Med 2005;118:1364-1372. (Pubitemid 41832329)
7. Andre E, Campi B, Materazzi S, Trevisani M, Amadesi S, Massi D, Creminon C, Vaksman N, Nassini R, Civelli M, et al. Cigarette smoke-induced neurogenic inflammation is mediated by α,β-unsaturated aldehydes and the TRPA1 receptor in rodents. J Clin Invest 2008;118:2574-2582. (Pubitemid 351949784)
8. Morris JB, Symanowicz PT, Olsen JE, Thrall RS, Cloutier MM, Hubbard AK. Immediate sensory nerve-mediated respiratory responses to irritants in healthy and allergic airway-diseased mice. J Appl Physiol 2003;94:1563-1571.
9. Nielsen GD, Wolkoff P, Alarie Y. Sensory irritation: risk assessment approaches. Regul Toxicol Pharmacol 2007;48:6-18. (Pubitemid 46795523)
10. Reddy S, Finkelstein EI, Wong PS, Phung A, Cross CE, van der Vliet A. Identification of glutathione modifications by cigarette smoke. Free Radic Biol Med 2002;33:1490-1498. (Pubitemid 35351592)
11. Borchers MT, Wert SE, Leikauf GD. Acrolein-induced MUC5ac expression in rat airways. Am J Physiol 1998;274:L573-L581. (Pubitemid 28225342)
12. Borchers MT, Wesselkamper S, Wert SE, Shapiro SD, Leikauf GD. Monocyte inflammation augments acrolein-induced Muc5ac expression in mouse lung. Am J Physiol 1999;277:L489-L497. (Pubitemid 29459668)
13. Wright JL, Cosio M, Churg A. Animal models of chronic obstructive pulmonary disease. Am J Physiol Lung Cell Mol Physiol 2008;295:L1-L15.
14. Vestbo J, Hogg JC. Convergence of the epidemiology and pathology of COPD. Thorax 2006;61:86-88.
15. Kim JH, Lee SY, Bak SM, Suh IB, Shin C, Shim JJ, In KH, Kang KH, Yoo SH. Effects of matrix metalloproteinase inhibitor on LPS-induced goblet cell metaplasia. Am J Physiol Lung Cell Mol Physiol 2004;287:L127-L133.
16. Lemaitre V, D'Armiento J. Matrix metalloproteinases in development and disease. Birth Defects Res C Embryo Today 2006;78:1-10.
17. Nadel JA. Innate immune mucin production via epithelial cell surface signaling: relationship to allergic disease. Curr Opin Allergy Clin Immunol 2007;7:57-62.
18. Shao MX, Nakanaga T, Nadel JA. Cigarette smoke induces Muc5ac mucin overproduction via tumor necrosis factor-α-converting enzyme in human airway epithelial (NCI-H292) cells. Am J Physiol Lung Cell Mol Physiol 2004;287:L420-L427. (Pubitemid 38943925)
19. Nagase H, Suzuki K, Morodomi T, Enghild JJ, Salvesen G. Activation mechanisms of the precursors of matrix metalloproteinases 1, 2 and 3. Matrix Suppl 1992;1:237-244.
20. Cowell S, Knauper V, Stewart ML, D'Ortho MP, Stanton H, Hembry RM, Lopez-Otin C, Reynolds JJ, Murphy G. Induction of matrix metalloproteinase activation cascades based on membrane-type 1 matrix metalloproteinase: associated activation of gelatinase A, gelatinase B and collagenase 3. Biochem J 1998;331:453-458. (Pubitemid 28182159)
21. Fridman R, Toth M, Pena D, Mobashery S. Activation of progelatinase B (MMP-9) by gelatinase A (MMP-2). Cancer Res 1995;55:2548-2555.
22. 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. (Pubitemid 46623007)
23. Deshmukh HS, Case LM, Wesselkamper SC, Borchers MT, Martin LD, Shertzer HG, Nadel JA, Leikauf GD. Metalloproteinases mediate mucin 5AC expression by epidermal growth factor receptor activation. Am J Respir Crit Care Med 2005;171:305-314. (Pubitemid 40223396)
24. Deshmukh HS, Shaver C, Case LM, Dietsch M, Wesselkamper SC, Hardie WD, Korfhagen TR, Corradi M, Nadel JA, Borchers MT, et al. Acrolein-activated matrix metalloproteinase 9 contributes to persistent mucin production. Am J Respir Cell Mol Biol 2008;38:446-454. (Pubitemid 351758691)
25. Casalino-Matsuda SM, Monzon ME, Forteza RM. Epidermal growth factor receptor activation by epidermal growth factor mediates oxidant-induced goblet cell metaplasia in human airway epithelium. Am J Respir Cell Mol Biol 2006;34:581-591.
26. Basbaum C, Li D, Gensch E, Gallup M, Lemjabbar H. Mechanisms by which gram-positive bacteria and tobacco smoke stimulate mucin induction through the epidermal growth factor receptor (EGFR). Novartis Found Symp 2002;248:171-176; discussion 176-180, 277-1182
27. Kim HJ, Park YD, Moon UY, Kim JH, Jeon JH, Lee JG, Bae YS, Yoon JH. The role of Nox4 in oxidative stress-induced MUC5AC over-expression in human airway epithelial cells. Am J Respir Cell Mol Biol 2008;39:598-609.
28. Tichelaar JW, Lu W, Whitsett JA. Conditional expression of fibroblast growth factor-7 in the developing and mature lung. J Biol Chem 2000; 275:11858-11864. (Pubitemid 30237754)
29. Hardie WD, Korfhagen TR, Sartor MA, Prestridge A, Medvedovic M, Le Cras TD, Ikegami M, Wesselkamper SC, Davidson C, Dietsch M, et al. Genomic profile of matrix and vasculature remodeling in TGF-α induced pulmonary fibrosis. Am J Respir Cell Mol Biol 2007;37:309-321. (Pubitemid 350067610)
30. Hardie WD, Davidson C, Ikegami M, Leikauf GD, Le Cras TD, Prestridge A, Whitsett JA, Korfhagen TR. EGF receptor tyrosine kinase inhibitors diminish transforming growth factor-α-induced pulmonary fibrosis. Am J Physiol Lung Cell Mol Physiol 2008;294: L1217-L1225.
31. Borchers MT, Carty MP, Leikauf GD. Regulation of human airway mucins by acrolein and inflammatory mediators. Am J Physiol 1999; 276:L549-L555.
32. Feron VJ, Kruysse A, Til HP, Immel HR. Repeated exposure to acrolein vapour: subacute studies in hamsters, rats and rabbits. Toxicology 1978;9:47-57. (Pubitemid 8307317)
33. Atkinson JJ, Senior RM. Matrix metalloproteinase-9 in lung remodeling. Am J Respir Cell Mol Biol 2003;28:12-24.
34. Faroon O, Roney N, Taylor J, Ashizawa A, Lumpkin M, Plewak D. Acrolein environmental levels and potential for human exposure. Toxicol Ind Health 2008;24:543-564. (Pubitemid 352809514)
35. Stevens JF, Maier CS. Acrolein: sources, metabolism, and biomolecular interactions relevant to human health and disease. Mol Nutr Food Res 2008;52:7-25.
36. Leikauf GD. Hazardous air pollutants and asthma. Environ Health Perspect 2002;110:505-526.
37. Nazaroff WW, Singer BC. Inhalation of hazardous air pollutants from environmental tobacco smoke in us residences. J Expo Anal Environ Epidemiol 2004;14:S71-S77. (Pubitemid 38691769)
38. Jermini C, Weber A, Grandjean E. [Quantitative determination of various gas-phase components of the side-stream smoke of cigarettes in the room air as a contribution to the problem of passive-smoking] [author's translation]. Int Arch Occup Environ Health 1976;36:169-181.
39. Weber A, Jermini C, Grandjean E. Irritating effects on man of air pollution due to cigarette smoke. Am J Public Health 1976;66:672-676.
40. Hales CA, Musto SW, Janssens S, JungW, Quinn DA, Witten M. Smoke aldehyde component influences pulmonary edema. J Appl Physiol 1992;72:555-561.
41. Tam BN, Neumann CM. A human health assessment of hazardous air pollutants in Portland, OR. J Environ Manage 2004;73:131-145.
42. Vasilyev N, Williams T, Brennan ML, Unzek S, Zhou X, Heinecke JW, Spitz DR, Topol EJ, Hazen SL, Penn MS. Myeloperoxidase-generated oxidants modulate left ventricular remodeling but not infarct size after myocardial infarction. Circulation 2005;112:2812-2820. (Pubitemid 41643823)
43. Anderson MM, Hazen SL, Hsu FF, Heinecke JW. Human neutrophils employ the myeloperoxidase-hydrogen peroxide-chloride system to convert hydroxy-amino acids into glycolaldehyde, 2-hydroxypropanal, and acrolein: a mechanism for the generation of highly reactive a-hydroxy and α,β-unsaturated aldehydes by phagocytes at sites of inflammation. J Clin Invest 1997;99:424-432.
44. Hazen SL, Hsu FF, d'Avignon A, Heinecke JW. Human neutrophils employ myeloperoxidase to convert a-amino acids to a battery of reactive aldehydes: a pathway for aldehyde generation at sites of inflammation. Biochemistry 1998;37:6864-6873.
45. Shao B, Fu X, McDonald TO, Green PS, Uchida K, O'Brien KD, Oram JF, Heinecke JW. Acrolein impairs ATP binding cassette transporter A1-dependent cholesterol export from cells through site-specific modification of apolipoprotein A-I. J Biol Chem 2005;280:36386-36396. (Pubitemid 41633913)
46. Tabor CW, Tabor H, Bachrach U. Identification of the aminoaldehydes produced by the oxidation of spermine and spermidine with purified plasma amine oxidase. J Biol Chem 1964;239:2194-2203.
47. Houen G, Bock K, Jensen AL. Hplc and nmr investigation of the serum amine oxidase catalyzed oxidation of polyamines. Acta Chem Scand 1994;48:52-60.
48. Lee Y, Sayre LM. Reaffirmation that metabolism of polyamines by bovine plasma amine oxidase occurs strictly at the primary amino termini. J Biol Chem 1998;273:19490-19494. (Pubitemid 28366999)
49. O'Brien PJ, Siraki AG, Shangari N. Aldehyde sources, metabolism, molecular toxicity mechanisms, and possible effects on human health. Crit Rev Toxicol 2005;35:609-662. (Pubitemid 41693601)
50. Sakata K, Kashiwagi K, Sharmin S, Ueda S, Igarashi K. Acrolein produced from polyamines as one of the uraemic toxins. Biochem Soc Trans 2003;31:371-374. (Pubitemid 36520679)
51. Esterbauer H, Schaur RJ, Zollner H. Chemistry and biochemistry of 4-hydroxynonenal, malonaldehyde and related aldehydes. Free Radic Biol Med 1991;11:81-128. (Pubitemid 121003917)
52. Uchida K, Kanematsu M, Morimitsu Y, Osawa T, Noguchi N, Niki E. Acrolein is a product of lipid peroxidation reaction: formation of free acrolein and its conjugate with lysine residues in oxidized low density lipoproteins. J Biol Chem 1998;273:16058-16066. (Pubitemid 28311374)
53. Furuhata A, Nakamura M, Osawa T, Uchida K. Thiolation of proteinbound carcinogenic aldehyde: an electrophilic acrolein-lysine adduct that covalently binds to thiols. J Biol Chem 2002;277:27919-27926. (Pubitemid 34966739)
54. Egle JL Jr. Retention of inhaled formaldehyde, propionaldehyde, and acrolein in the dog. Arch Environ Health 1972;25:119-124.
55. Kasahara DI, Poynter ME, Othman Z, Hemenway D, van der Vliet A. Acrolein inhalation suppresses lipopolysaccharide-induced inflammatory cytokine production but does not affect acute airways neutrophilia. J Immunol 2008;181:736-745.
56. Valacchi G, Pagnin E, Phung A, Nardini M, Schock BC, Cross CE, van der Vliet A. Inhibition of NFkB activation and IL-8 expression in human bronchial epithelial cells by acrolein. Antioxid Redox Signal 2005;7:25-31. (Pubitemid 40187922)
57. Darley EF, Middleton JT, Garber MJ. Plant damage and eye irritation from ozone hydrocarbon reactions. J Agric Food Chem 1960;8:483-485.
58. Steinhagen WH, Barrow CS. Sensory irritation structure-activity study of inhaled aldehydes in B6C3F1 and Swiss-Webster mice. Toxicol Appl Pharmacol 1984;72:495-503.
59. Cohen SM, Garland EM, St John M, Okamura T, Smith RA. Acrolein initiates rat urinary bladder carcinogenesis. Cancer Res 1992;52:3577-3581.
60. Izard C, Libermann C. Acrolein. Mutat Res 1978;47:115-138.
61. Feng Z, Hu W, Hu Y, Tang MS. Acrolein is a major cigarette-related lung cancer agent: preferential binding at p53 mutational hotspots and inhibition of DNA repair. Proc Natl Acad Sci USA 2006;103:15404-15409. (Pubitemid 44625604)
62. Haberzettl P, Vladykovskaya E, Srivastava S, Bhatnagar A. Role of endoplasmic reticulum stress in acrolein-induced endothelial activation. Toxicol Appl Pharmacol 2009;234:14-24.
63. Luo J, Uchida K, Shi R. Accumulation of acrolein-protein adducts after traumatic spinal cord injury. Neurochem Res 2005;30:291-295. (Pubitemid 40880804)
64. Park YS, Taniguchi N. Acrolein induces inflammatory response underlying endothelial dysfunction: a risk factor for atherosclerosis. Ann N Y Acad Sci 2008;1126:185-189. (Pubitemid 351589296)
65. Takino T, Sato H, Yamamoto E, Seiki M. Cloning of a human gene potentially encoding a novel matrix metalloproteinase having a C-terminal transmembrane domain. Gene 1995;155:293-298.
66. Apte SS, Fukai N, Beier DR, Olsen BR. The matrix metalloproteinase- 14 (MMP-14) gene is structurally distinct from other MMP genes and is co-expressed with the TIMP-2 gene during mouse embryogenesis. J Biol Chem 1997;272:25511-25517. (Pubitemid 27438858)
67. Oblander SA, Zhou Z, Galvez BG, Starcher B, Shannon JM, Durbeej M, Arroyo AG, Tryggvason K, Apte SS. Distinctive functions of membrane type 1 matrix-metalloprotease (MT1-MMP or MMP-14) in lung and submandibular gland development are independent of its role in pro-MMP-2 activation. Dev Biol 2005;277:255-269. (Pubitemid 39574267)
68. Strongin AY, Collier I, Bannikov G, Marmer BL, Grant GA, Goldberg GI. Mechanism of cell surface activation of 72-kDa type IV collagenase. Isolation of the activated form of the membrane metalloprotease. J Biol Chem 1995;270:5331-5338.
69. Knauper V, Will H, Lopez-Otin C, Smith B, Atkinson SJ, Stanton H, Hembry RM, Murphy G. Cellular mechanisms for human procollagenase- 3 (MMP-13) activation: evidence that MT1-MMP (MMP-14) and gelatinase A (MMP-2) are able to generate active enzyme. J Biol Chem 1996;271:17124-17131. (Pubitemid 26244262)
70. Leeman MF, Curran S, Murray GI. The structure, regulation, and function of human matrix metalloproteinase-13. Crit Rev Biochem Mol Biol 2002;37:149-166. (Pubitemid 34779350)
71. Hernandez-Barrantes S, Toth M, Bernardo MM, Yurkova M, Gervasi DC, Raz Y, Sang QA, Fridman R. Binding of active (57 kDa) membrane type 1-matrix metalloproteinase (MT1-MMP) to tissue inhibitor of metalloproteinase (TIMP)-2 regulates MT1-MMP processing and pro-MMP-2 activation. J Biol Chem 2000;275:12080-12089. (Pubitemid 30237783)
72. Lehti K, Lohi J, Valtanen H, Keski-Oja J. Proteolytic processing of membrane-type-1 matrix metalloproteinase is associated with gelatinase A activation at the cell surface. Biochem J 1998;334:345-353. (Pubitemid 28448577)
73. Pei D, Weiss SJ. Furin-dependent intracellular activation of the human stromelysin-3 zymogen. Nature 1995;375:244-247.
74. Pei D, Weiss SJ. Transmembrane-deletion mutants of the membranetype matrix metalloproteinase-1 process progelatinase A and express intrinsic matrix-degrading activity. J Biol Chem 1996;271:9135-9140. (Pubitemid 26123348)
75. Fukuda Y, Ishizaki M, Okada Y, Seiki M, Yamanaka N. Matrix metalloproteinases and tissue inhibitor of metalloproteinase-2 in fetal rabbit lung. Am J Physiol Lung Cell Mol Physiol 2000;279:L555-L561.
76. Kunugi S, Fukuda Y, Ishizaki M, Yamanaka N. Role of MMP-2 in alveolar epithelial cell repair after bleomycin administration in rabbits. Lab Invest 2001;81:1309-1318. (Pubitemid 32911979)
77. Esterbauer H, Nohammer G, Schauenstein E, Weber P. [Determination of protein-SH groups with DDD reagent]. Acta Histochem Suppl 1976;16:183-188.
78. Strongin AY, Collier IE, Krasnov PA, Genrich LT, Marmer BL, Goldberg GI. Human 92 kDa type IV collagenase: functional analysis of fibronectin and carboxyl-end domains. Kidney Int 1993;43:158-162.
79. Cao J, Kozarekar P, Pavlaki M, Chiarelli C, Bahou WF, Zucker S. Distinct roles for the catalytic and hemopexin domains of membrane type 1-matrix metalloproteinase in substrate degradation and cell migration. J Biol Chem 2004;279:14129-14139. (Pubitemid 38468949)
80. Zucker S, Mirza H, Conner CE, Lorenz AF, Drews MH, Bahou WF, Jesty J. Vascular endothelial growth factor induces tissue factor and matrix metalloproteinase production in endothelial cells: conversion of prothrombin to thrombin results in progelatinase A activation and cell proliferation. Int J Cancer 1998;75:780-786. (Pubitemid 28145828)
81. Galvez BG, Genis L, Matias-Roman S, Oblander SA, Tryggvason K, Apte SS, Arroyo AG. Membrane type 1-matrix metalloproteinase is regulated by chemokines monocyte-chemoattractant protein-1/CCL2 and interleukin-8/CXCL8 in endothelial cells during angiogenesis. J Biol Chem 2005;280:1292-1298.
82. Galvez BG, Matias-Roman S, Yanez-Mo M, Vicente-Manzanares M, Sanchez-Madrid F, Arroyo AG. Caveolae are a novel pathway for membrane-type 1 matrix metalloproteinase traffic in human endothelial cells. Mol Biol Cell 2004;15:678-687. (Pubitemid 38146484)
83. Kheradmand F, Rishi K, Werb Z. Signaling through the EGF receptor controls lung morphogenesis in part by regulating MT1-MMPmediated activation of gelatinase A/MMP2. J Cell Sci 2002;115:839-848. (Pubitemid 34196343)
84. Udayakumar TS, Nagle RB, Bowden GT. Fibroblast growth factor-1 transcriptionally induces membrane type-1 matrix metalloproteinase expression in prostate carcinoma cell line. Prostate 2004;58:66-75.
85. Munaut C, Noel A, Hougrand O, Foidart JM, Boniver J, Deprez M. Vascular endothelial growth factor expression correlates with matrix metalloproteinases MT1-MMP, MMP-2 and MMP-9 in human glioblastomas. Int J Cancer 2003;106:848-855. (Pubitemid 37071662)
86. Zhang D, Brodt P. Type 1 insulin-like growth factor regulates MT1- MMP synthesis and tumor invasion via PI 3-kinase/Akt signaling. Oncogene 2003;22:974-982. (Pubitemid 36313141)
87. Sato H, Seiki M. Regulatory mechanism of 92 kDa type IV collagenase gene expression which is associated with invasiveness of tumor cells. Oncogene 1993;8:395-405. (Pubitemid 23073756)
88. Tanimura S, Asato K, Fujishiro SH, Kohno M. Specific blockade of the ERK pathway inhibits the invasiveness of tumor cells: down-regulation of matrix metalloproteinase-3/-9/-14 and CD44. Biochem Biophys Res Commun 2003;304:801-806. (Pubitemid 36513560)
89. Boyd PJ, Doyle J, Gee E, Pallan S, Haas TL. MAPK signaling regulates endothelial cell assembly into networks and expression of MT1- MMP and MMP-2. Am J Physiol Cell Physiol 2005;288:C659-C668. (Pubitemid 40229495)
90. Munshi HG, Wu YI, Mukhopadhyay S, Ottaviano AJ, Sassano A, Koblinski JE, Platanias LC, Stack MS. Differential regulation of membrane type 1-matrix metalloproteinase activity by ERK 1/2- and p38 MAPK-modulated tissue inhibitor of metalloproteinases 2 expression controls transforming growth factor-β1-induced pericellular collagenolysis. J Biol Chem 2004;279:39042-39050. (Pubitemid 39296066)
91. Sternlicht MD, Werb Z. How matrix metalloproteinases regulate cell behavior. Annu Rev Cell Dev Biol 2001;17:463-516. (Pubitemid 33096184)
92. Yao PM, Lemjabbar H, D'Ortho MP, Maitre B, Gossett P, Wallaert B, Lafuma C. Balance between MMP-9 and TIMP-1 expressed by human bronchial epithelial cells: relevance to asthma. Ann N Y Acad Sci 1999;878:512-514. (Pubitemid 29353598)
93. Thomas P, Khokha R, Shepherd FA, Feld R, Tsao MS. Differential expression of matrix metalloproteinases and their inhibitors in nonsmall cell lung cancer. J Pathol 2000;190:150-156. (Pubitemid 30082487)
94. Will H, Atkinson SJ, Butler GS, Smith B, Murphy G. The soluble catalytic domain of membrane type 1 matrix metalloproteinase cleaves the propeptide of progelatinase A and initiates autoproteolytic activation: regulation by TIMP-2 and TIMP-3. J Biol Chem 1996; 271:17119-17123. (Pubitemid 26244261)
95. Kinoshita T, Sato H, Takino T, Itoh M, Akizawa T, Seiki M. Processing of a precursor of 72-kilodalton type IV collagenase/gelatinase A by a recombinant membrane-type 1 matrix metalloproteinase. Cancer Res 1996;56:2535-2538. (Pubitemid 26170690)
96. Langton KP, Barker MD, McKie N. Localization of the functional domains of human tissue inhibitor of metalloproteinases-3 and the effects of a Sorsby's fundus dystrophy mutation. J Biol Chem 1998; 273:16778-16781. (Pubitemid 28311703)
97. β1 in vitro and expressed in fibroblastic foci in vivo in idiopathic pulmonary fibrosis. Exp Lung Res 2006;32:201-214.