matrix metalloproteinase; tissue inhibitor of MMP; asthma; cytokine; growth factors
Abstract :
[en] In healthy lung, Matrix Metalloproteinases (MMPs) and their physiological inhibitors, tissue inhibitors of matrix metalloproteinases (TIMPs), are produced in the respiratory tract by a panel of different structural cells. These activities are mandatory for many physiological processes including development, wound healing and cell trafficking. Deregulation of proteolytic-antiproteolytic network and inappropriate secretion of various MMPs by stimulated structural or inflammatory cells is thought to take part to pathophysiology of numerous lung diseases including asthma, chronic obstructive pulmonary disease (COPD), lung fibrosis and lung cancer. Cytokines and growth factors are involved in these inflammatory processes and some of those mediators interact directly with MMPs and TIMPs leading either to a regulation of their expression or changes in their biological activities by proteolytic cleavage. In turn, cytokines and growth factors modulate secretion of MMPs establishing a complex network of reciprocal interactions. Every MMP seem to play a rather specific role and some variations of their expression are observed in different lung diseases. The precise role of these enzymes and their inhibitors is now studied in depth as they could represent relevant therapeutic targets for many diseases. Indeed, MMP inhibition can lead either to a decrease of the intensity of a pathological process or, in the contrary for some of them, to an increase of disease severity. In this review, we focus on the role played by MMPs and TIMPs in asthma and we provide an overview of their potential roles in COPD, lung fibrosis and lung cancer, with a special emphasis on loops including MMPs and cytokines and growth factors relevant in these diseases.
Disciplines :
Pharmacy, pharmacology & toxicology
Author, co-author :
Guéders, Maud ; Université de Liège - ULiège > Département des sciences cliniques > Labo de biologie des tumeurs et du développement
Foidart, Jean-Michel ; Université de Liège - ULiège > Département des sciences cliniques > Gynécologie - Obstétrique
Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme
Cataldo, Didier ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biochimie et physiologie générales, humaines et path.
Language :
English
Title :
Matrix metalloproteinases (MMPs) and tissue inhibitors of MMPs in the respiratory tract: Potential implications in asthma and other lung diseases
A.H. Baker, D.R. Edwards, and G. Murphy Metalloproteinase inhibitors: biological actions and therapeutic opportunities J. Cell Sci. 115 2002 3719 3727
M. Balbin, A. Fueyo, A.M. Tester, A.M. Pendas, A.S. Pitiot, A. Astudillo, C.M. Overall, S.D. Shapiro, and C. Lopez-Otin Loss of collagenase-2 confers increased skin tumor susceptibility to male mice Nat. Genet. 35 2003 252 257
D. Baram, G.G. Vaday, P. Salamon, I. Drucker, R. Hershkoviz, and Y.A. Mekori Human mast cells release metalloproteinase-9 on contact with activated T cells: juxtacrine regulation by TNF-alpha J. Immunol. 167 2001 4008 4016
P.J. Barnes Mechanisms in COPD - differences from asthma Chest 117 2000 10 14
C. Becerril, A. Pardo, M. Montano, C. Ramos, R. Ramirez, and M. Selman Acidic fibroblast growth factor induces an antifibrogenic phenotype in human lung fibroblasts Am. J. Respir. Cell Mol. Biol. 20 1999 1020 1027
C. Belleguic, M. Corbel, N. Germain, H. Lena, E. Boichot, P.H. Delaval, and V. Lagente Increased release of matrix metalloproteinase-9 in the plasma of acute severe asthmatic patients Clin. Exp. Allergy 32 2002 217 223
C. Bergeron, N. Page, P. Joubert, B. Barbeau, Q. Hamid, and J. Chakir Regulation of procollagen I (alpha 1) by interleukin-4 in human bronchial fibroblasts: a possible role in airway remodelling in asthma Clin. Exp. Allergy 33 2003 1389 1397
T. Betsuyaku, M. Nishimura, K. Takeyabu, M. Tanino, P. Venge, S.Y. Xu, and Y. Kawakami Neutrophil granule proteins in BAL fluid from subjects with subclinical emphysema Am. J. Respir. Crit. Care Med. 159 1999 A193
F. Blasi Proteolysis, cell adhesion, chemotaxis, and invasiveness are regulated by the u-PA-u-PAR-PAI-1 system Thromb. Haemost. 82 1999 298 304
M. Bosse, J. Chakir, M. Rouabhia, L.P. Boulet, M. Audette, and M. Laviolette Serum matrix metalloproteinase-9: tissue inhibitor of metalloproteinase-1 ratio correlates with steroid responsiveness in moderate to severe asthma Am. J. Respir. Crit. Care Med. 159 1999 596 602
M.E. Boulay, P. Prince, F. Deschesnes, J. Chakir, and L.P. Boulet Metalloproteinase-9 in induced sputum correlates with the severity of the late allergen-induced asthmatic response Respiration 71 2004 216 224
J. Bousquet, P. Chanez, J.Y. Lacoste, R. White, P. Vic, P. Godard, and F.B. Michel Asthma - a disease remodeling the airways Allergy 47 1992 3 11
Ken Bracke, D. Cataldo, T. Maes, M. Gueders, A. Noel, J.M. Foidart, G. Brusselle, and R. Pauwels Matrix metalloproteinase-12 expression in pulmonary dendritic cells of cigarette smoke exposed mice Int. Arch. All. Immunol. 138 2 2005 169 179
K. Brew, D. Dinakarpandian, and H. Nagase Tissue inhibitors of metalloproteinases: evolution, structure and function Biochim. Biophys. Acta Prot. Struct. Mol. Enzymol. 1477 2000 267 283
D. Cataldo, C. Munaut, A. Noel, F. Frankenne, P. Bartsch, J.M. Foidart, and R. Louis MMP-2-and MMP-9-linked gelatinolytic activity in the sputum from patients with asthma and chronic obstructive pulmonary disease Int. Arch. Allergy Immunol. 123 2000 259 267
D. Cataldo, C. Munaut, A. Noel, F. Frankenne, P. Bartsch, J.M. Foidart, and R. Louis Matrix metalloproteinases and TIMP-1 production by peripheral blood granulocytes from COPD patients and asthmatics Allergy 56 2001 145 151
D. Cataldo, M. Gueders, A. Noel, J.M. Foidart, P. Bartsch, and R. Louis Matrix metalloproteinases (MMPs) and tissue inhibitors of matrix metalloproteinases (TIMPs) mRNA transcripts in the bronchial secretions of asthmatics and COPD Lab. Invest. 84 2002 418 424
D.D. Cataldo, K.G. Tournoy, K. Vermaelen, C. Munaut, J.M. Foidart, R. Louis, A. Noel, and R.A. Pauwels Matrix metalloproteinase-9 deficiency impairs cellular infiltration and bronchial hyperresponsiveness during allergen-induced airway inflammation Am. J. Pathol. 161 2002 491 498
D.D. Cataldo, M.M. Gueders, N. Rocks, N.E. Sounni, B. Evrard, P. Bartsch, R. Louis, A. Noel, and J.M. Foidart Pathogenic role of matrix metalloproteases and their inhibitors in asthma and chronic obstructive pulmonary disease and therapeutic relevance of matrix metalloproteases inhibitors Cell. Mol. Biol. 49 2003 875 884
S.H. Cho, C.H. Ryu, and C.K. Oh Plasminogen activator inhibitor-1 in the pathogenesis of asthma Exp. Biol. Med. 229 2004 138 146
K.F. Chung, and P.J. Barnes Cytokines in asthma Thorax 54 1999 825 857
M. Corbel, C. Belleguic, E. Boichot, and V. Lagente Involvement of gelatinases (MMP-2 and MMP-9) in the development of airway inflammation and pulmonary fibrosis Cell Biol. Toxicol. 18 2002 51 61
D.B. Corry, K. Rishi, J. Kanellis, A. Kiss, L.Z. Song, J. Xu, L.L. Feng, Z. Werb, and F. Kheradmand Decreased allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency Nat. Immunol. 3 2002 347 353
G.P. Cosgrove, M.I. Schwarz, M.W. Geraci, K.K. Brown, and G.S. Worthen Overexpression of matrix metalloproteinase-7 in pulmonary fibrosis Chest 121 2002 25S 26S
E. Crouch Pathobiology of pulmonary fibrosis Am. J. Physiol. 259 1990 L159 L184
M. Egeblad, and Z. Werb New functions for the matrix metalloproteinases in cancer progression Nat. Rev. Cancer 2 2002 161 174
S.R. Elshaw, N. Henderson, A.J. Knox, S.A. Watson, D.J. Buttle, and S.R. Johnson Matrix metalloproteinase expression and activity in human airway smooth muscle cells Br. J. Pharmacol. 142 2004 1318 1324
ENFUMOSA group The ENFUMOSA cross-sectional European multicentre study of the clinical phenotype of chronic severe asthma, European Network for Understanding Mechanisms of Severe Asthma Eur. Respir. J. 22 2003 470 477
G.A. Finlay, L.R. ODriscoll, K.J. Russell, E.M. Darcy, J.B. Masterson, M.X. Fitzgerald, and C.M. OConnor Matrix metalloproteinase expression and production by alveolar macrophages in emphysema Am. J. Respir. Crit. Care Med. 156 1997 240 247
G.A. Finlay, K.J. Russell, K.J. McMahon, E.M. Darcy, J.B. Masterson, M.Z. FitzGerald, and C.M. OConnor Elevated levels of matrix metalloproteinases in bronchoalveolar lavage fluid of emphysematous patients Thorax 52 1997 502 506
P. Flood-Page, A. Menzies-Gow, S. Phipps, S. Ying, A. Wangoo, M.S. Ludwig, N. Barnes, D. Robinson, and A.B. Kay Anti-IL-5 treatment reduces deposition of ECM proteins in the bronchial subepithelial basement membrane of mild atopic asthmatics J. Clin. Invest. 112 2003 1029 1036
A.R. Folgueras, A.M. Pendas, L.M. Sanchez, and C. Lopez-Otin Matrix metalloproteinases in cancer: from new functions to improved inhibition strategies Int. J. Dev. Biol. 48 2004 411 424
T. Fujisawa, Y. Kato, A. Terada, K. Iguchi, and H. Kamiya Matrix metalloproteinase-9 in peripheral blood eosinophils Int. Arch. Allergy Immunol. 120 1999 65 69
Y. Fukuda, M. Ishizaki, S. Kudoh, M. Kitaichi, and N. Yamanaka Localization of matrix metalloproteinases-1, -2, and -9 and tissue inhibitor of metalloproteinase-2 in interstitial lung diseases Lab. Invest. 78 1998 687 698
C. Gilles, M. Polette, C. Coraux, J.M. Tournier, G. Meneguzzi, C. Munaut, L. Volders, P. Rousselle, P. Birembaut, and J.M. Foidart Contribution of MT1-MMP and of human laminin-5 gamma 2 chain degradation to mammary epithelial cell migration J. Cell Sci. 114 2001 2967 2976
Global Initiative for Asthma (GINA). Global strategy for asthma management and prevention. NIH Publication 02-3659 issued January 1995 (Updated 2004).
J. Gross, and C.M. Lapière Collagenolytic activity in amphibian tissues: a tissue culture assay Proc. Natl. Acad. Sci. U. S. A. 48 1962 1014 1022
G. Grunig, J. Padilla, E. Daley, K. Robinson, and D.D. Donaldson IL-13 controls the immune response to inhaled antigens FASEB J. 19 2005 A939
M.M. Gueders, M. Balbin, N. Rocks, J.M. Foidart, P. Gosset, R. Louis, S.D. Shapiro, C. Lopez-Otin, A. Noel, and D.D. Cataldo Matrix metalloproteinase-8 deficiency promotes granulocytic allergen-induced airway inflammation J. Immunol. 175 2005 2589 2597
Z. Han, Junxu, and N. Zhong Expression of matrix metalloproteinases MMP-9 within the airways in asthma Resp. Med. 97 2003 563 567
M.M. Handsley, and D.R. Edwards Metalloproteinases and their inhibitors in tumor angiogenesis Int. J. Cancer 115 2005 849 860
R.D. Hautamaki, D.K. Kobayashi, R.M. Senior, and S.D. Shapiro Requirement for macrophage elastase for cigarette smoke-induced emphysema in mice Science 277 1997 2002 2004
S.J. Hirst, and C.H.C. Twort The proliferative response of airway smooth-muscle Clin. Exp. Allergy 22 1992 907 915
R. Hoekstra, F.A.L.M. Eskens, and J. Verweij Matrix metalloproteinase inhibitors: current developments and future perspectives Oncologist 6 2001 415 427
M. Hoshino, M. Takahashi, Y. Takai, and J. Sim Inhaled corticosteroids decrease subepithelial collagen deposition by modulation of the balance between matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 expression in asthma J. Allergy Clin. Immunol. 104 1999 356 363
S. Ishikawa, K. Takenaka, K. Yanagihara, R. Miyahara, Y. Kawano, Y. Otake, S. Hasegawa, H. Wada, and F. Tanaka Matrix metalloproteinase-2 status in stromal fibroblasts, not in tumor cells, is a significant prognostic factor in non-small-cell lung cancer Clin. Cancer Res. 10 2004 6579 6585
T. Itoh, M. Tanioka, H. Matsuda, H. Nishimoto, T. Yoshioka, R. Suzuki, and M. Uehira Experimental metastasis is suppressed in MMP-9-deficient mice Clin. Exp. Metastasis 17 1999 177 181
P.K. Jeffery Remodeling in asthma and chronic obstructive lung disease Am. J. Respir. Crit. Care Med. 164 2001 S28 S38
Y.F. Jiang, M.S. Wang, M.Y. Celiker, Y.E. Liu, Q.X.A. Sang, I.D. Goldberg, and Y.E. Shi Stimulation of mammary tumorigenesis by systemic tissue inhibitor of matrix metalloproteinase 4 gene delivery Cancer Res. 61 2001 2365 2370
S. Johnson, and A. Knox Autocrine production of matrix metalloproteinase-2 is required for human airway smooth muscle proliferation Am. J. Physiol. Lung Cell. Mol. Physiol. 277 1999 L1109 L1117
C. Jumper, E. Cobos, and C. Lox Determination of the serum matrix metalloproteinase-9 (MMP-9) and tissue inhibitor of matrix metalloproteinase-1 (TIMP-1) in patients with either advanced small-cell lung cancer or non-small-cell lung cancer prior to treatment Respir. Med. 98 2004 173 177
A.L.A. Katzenstein, and J.L. Myers Idiopathic pulmonary fibrosis - clinical relevance of pathologic classification Am. J. Respir. Crit. Care Med. 157 1998 1301 1315
E.A.B. Kelly, W.W. Busse, and N.N. Jarjour Increased matrix metalloproteinase-9 in the airway after allergen challenge Am. J. Respir. Crit. Care Med. 162 2000 1157 1161
M. Kodate, T. Kasai, H. Hashimoto, K. Yasumoto, Y. Iwata, and H. Manabe Expression of matrix metalloproteinase (gelatinase) in T1 adenocarcinoma of the lung Pathol. Int. 47 1997 461 469
K. Kumagai, I. Ohno, S. Okada, Y. Ohkawara, K. Suzuki, K. Masu, T. Shinya, H. Nagase, K. Iwata, and K. Shirato Inhibition of matrix metalloproteinases prevents allergen-induced airway inflammation in a murine model of asthma Am. J. Respir. Crit. Care Med. 159 1999 A325
K. Kumagai, I. Ohno, K. Imai, J. Nawata, K. Hayashi, S. Okada, H. Senoo, T. Hattori, and K. Shirato The involvement of matrix metalloproteinases in basement membrane injury in a murine model of acute allergic airway inflammation Clin. Exp. Allergy 32 2002 1527 1534
D.A. Kuperman, X.Z. Huang, L.L. Koth, G.H. Chang, G.M. Dolganov, Z. Zhu, J.A. Elias, D. Sheppard, and D.J. Erle Direct effects of interleukin-13 on epithelial cells cause airway hyperreactivity and mucus overproduction in asthma Nat. Med. 8 2002 885 889
P. Lange, J. Parner, J. Vestbo, P. Schnohr, and G. Jensen A 15-year follow-up study of ventilatory function in adults with asthma N. Engl. J. Med. 339 1998 1194 1200
S. Lanone, T. Zheng, Z. Zhu, W. Liu, C.G. Lee, B. Ma, Q.S. Chen, R.J. Homer, J.M. Wang, L.A. Rabach, M.E. Rabach, J.M. Shipley, S.D. Shapiro, R.M. Senior, and J.A. Elias Overlapping and enzyme-specific contributions of matrix metalloproteinases-9 and-12 in IL-13-induced inflammation and remodeling J. Clin. Invest. 110 2002 463 474
U. Lappalainen, J.A. Whitsett, S.E. Wert, J.W. Tichelaar, and K. Bry Interleukin-1 beta causes pulmonary inflammation, emphysema, and airway remodeling in the adult murine lung Am. J. Respir. Mol. Biol. 32 2005 311 318
M.C. Lavigne, P. Thakker, J. Gunn, A. Wong, J.S. Miyashiro, A.M. Wasserman, S.Q. Wei, J.W. Pelker, M. Kobayashi, and M.J. Eppihimer Human bronchial epithelial cells express and secrete MMP-12 Biochem. Biophys. Res. Commun. 324 2004 534 546
Y.C. Lee, H.B. Lee, Y.K. Rhee, and C.H. Song The involvement of matrix metalloproteinase-9 in airway inflammation of patients with acute asthma Clin. Exp. Allergy 31 2001 1623 1630
K.S. Lee, S.M. Jin, S.S. Kim, and Y.C. Lee Doxycycline reduces airway inflammation and hyperresponsiveness in a murine model of toluene diisocyanate-induced asthma J. Allergy Clin. Immunol. 113 2004 902 909
H. Lemjabbar, P. Gosset, E. Lechapt-Zalcman, M.L. Franco-Montoya, B. Wallaert, A. Harf, and C. Lafuma Overexpression of alveolar macrophage gelatinase B (MMP-9) in patients with idiopathic pulmonary fibrosis - effects of steroid and immunosuppressive treatment Am. J. Respir. Cell Mol. Biol. 20 1999 903 913
J.M. Lewalle, C. Munaut, B. Pichot, D. Cataldo, E. Baramova, and J.M. Foidart Plasma membrane-dependent activation of gelatinase A in human vascular endothelial-cells J. Cell. Physiol. 165 1995 475 483
C. Lopez-Otin, and C.M. Overall Protease degradomics: a new challenge for proteomics Nat. Rev. Mol. Cell Biol. 3 2002 509 519
B. Manoury, S. Nenan, O. Leclerc, I. Guenon, E. Boichot, J.M. Planquois, C.P. Bertrand, and V. Lagente The absence of reactive oxygen species production protects mice against bleomycin-induced pulmonary fibrosis Respir. Res. 6 2005 11
R. Martin, S. Shapiro, S. Tong, and H. Van Wart Macrophage metalloelastase inhibitors Prog. Respir. Res. (Karger, Basel) 31 2001 177 180
W. Mattos, S. Lim, R. Russell, A. Jatakanon, F. Chung, and P.J. Barnes Matrix metalloproteinase-9 expression in asthma - effect of asthma severity, allergen challenge, and inhaled corticosteroids Chest 122 2002 1543 1552
G. Mautino, N. Oliver, P. Chanez, J. Bousquet, and F. Capony Increased release of matrix metalloproteinase-9 in bronchoalveolar lavage fluid and by alveolar macrophages of asthmatics Am. J. Respir. Cell Mol. Biol. 17 1997 583 591
G. Mautino, C. Henriquet, C. Gougat, A. Le Cam, J.M. Dayer, J. Bousquet, and F. Capony Increased expression of tissue inhibitor of metalloproteinase-1 and loss of correlation with matrix metalloproteinase-9 by macrophages in asthma Lab. Invest. 79 1999 39 47
S.J. McMillan, J. Kearley, J.D. Campbell, X.W. Zhu, K.Y. Larbi, J.M. Shipley, R.M. Senior, S. Nourshargh, and C.M. Lloyd Matrix metalloproteinase-9 deficiency results in enhanced allergen-induced airway inflammation J. Immunol. 172 2004 2586 2594
M. Michael, B. Babic, R. Khokha, M. Tsao, J. Ho, M. Pintilie, K. Leco, D. Chamberlain, and F.A. Shepherd Expression and prognostic significance of metalloproteinases and their tissue inhibitors in patients with small-cell lung cancer J. Clin. Oncol. 17 1999 1802 1808
Y. Morimoto, H. Kim, T. Oyabu, M. Hirohashi, H. Nagatomo, A. Ogami, H. Yamato, T. Higashi, I. Tanaka, and T. Kasai Effect of long-term inhalation of toner on extracellular matrix in the lungs of rats in vivo Inhal. Toxicol. 17 2005 153 159
J.D. Mott, and Z. Werb Regulation of matrix biology by matrix metalloproteinases Curr. Opin. Cell Biol. 16 2004 558 564
G. Murphy, and V. Knauper Relating matrix metalloproteinase structure to function: why the "'hemopexin" domain? Matrix Biol. 15 1997 511 518
G. Murphy, and F. Willenbrock Tissue inhibitors of matrix metalloendopeptidases Proteolytic Enzymes: Aspartic and Metallo Peptidases vol. 248 1995 496 510
H. Nagase Activation mechanisms of matrix metalloproteinases Biol. Chem. 378 1997 151 160
S. Nenan, E. Boichot, V. Lagente, and C.P. Bertrand Macrophage elastase (MMP-12): a pro-inflammatory mediator? Mem. Inst. Oswaldo Cruz 100 2005 167 172
A. Noel, C. Maillard, N. Rocks, M. Jost, V. Chabottaux, N.E. Sounni, E. Maquoi, D. Cataldo, and J.M. Foidart Membrane associated proteases and their inhibitors in tumour angiogenesis J. Clin. Pathol. 57 2004 577 584
C.K. Oh, B. Ariue, R.F. Alban, B. Shaw, and S.H. Cho PAI-1 promotes extracellular matrix deposition in the airways of a murine asthma model Biochem. Biophys. Res. Commun. 294 2002 1155 1160
H. Ohbayashi Matrix metalloproteinases in lung diseases Curr. Protein Pept. Sci. 3 2002 409 421
K. Ohnishi, M. Takagi, Y. Kurokawa, S. Satomi, and Y.T. Konttinen Matrix metalloproteinase-mediated extracellular matrix protein degradation in human pulmonary emphysema Lab. Invest. 78 1998 1077 1087
I. Ohno, H. Ohtani, Y. Nitta, J. Suzuki, H. Hoshi, M. Honma, S. Isoyama, Y. Tanno, G. Tamura, K. Yamauchi, H. Nagura, and K. Shirato Eosinophils as a source of matrix metalloproteinase-9 in asthmatic airway inflammation Am. J. Respir. Cell Mol. Biol. 16 1997 212 219
O. Prause, S. Bozinovski, G.P. Anderson, and A. Linden Increased matrix metalloproteinase-9 concentration and activity after stimulation with interleukin-17 in mouse airways Thorax 59 2004 313 317
K. Prikk, P. Maisi, E. Pirila, M.A. Reintam, T. Salo, T. Sorsa, and R. Sepper Airway obstruction correlates with collagenase-2 (MMP-8) expression and activation in bronchial asthma Lab. Invest. 82 2002 1535 1545
S.C. Pritchard, M.C. Nicolson, C. Lloret, J.A. Mckay, V.G. Ross, K.M. Kerr, G.I. Murray, and H.L. Mcleod Expression of matrix metalloproteinases 1, 2, 9 and their tissue inhibitors in stage II non-small cell lung cancer: implications for MMP inhibition therapy Oncol. Rep. 8 2001 421 424
M. Profita, R. Gagliardo, R. Di Giorgi, A. Bruno, L. Riccobono, A. Bonanno, J. Bousquet, and A.M. Vignola In vitro effects of flunisolide on MMP-9, TIMP-1, fibronectin, TGF-beta1 release and apoptosis in sputum cells freshly isolated from mild to moderate asthmatics Allergy 59 2004 927 932
R. Rajah, R.V. Nachajon, M.H. Collins, H. Hakonarson, M.M. Grunstein, and P. Cohen Elevated levels of the IGF-binding protein protease MMP-1 in asthmatic airway smooth muscle Am. J. Respir. Crit. Care Med. 20 1999 199 208
F. Reichenberger, O. Eickelberg, C. Wyser, A.P. Perruchoud, M. Roth, and M. Tamm Distinct endobronchial expression of matrix-metalloproteinases (MMP) and their endogenous inhibitors in lung cancer Swiss Med. Wkly. 131 2001 273 279
J.C. Renauld New insights into the role of cytokines in asthma J. Clin. Pathol. 54 2001 577 589
V. Ruiz, R.M. Ordonez, J. Berumen, R. Ramirez, B. Uhal, C. Becerril, A. Pardo, and M. Selman Unbalanced collagenases/TIMP-1 expression and epithelial apoptosis in experimental lung fibrosis Am. J. Physiol. Lung Cell. Mol. Physiol. 285 2003 L1026 L1036
H. Sagara, T. Okada, K. Okumura, H. Ogawa, C. Ra, T. Fukuda, and A. Nakao Activation of TGF-beta/Smad2 signaling is associated with airway remodeling in asthma J. Allergy Clin. Immunol. 110 2002 249 254
J.F. Santibanez, J. Guerrero, M. Quintanilla, A. Fabra, and J. Martinez Transforming growth factor-beta1 modulates matrix metalloproteinase-9 production through the Ras/MAPK signaling pathway in transformed keratinocytes Biochem. Biophys. Res. Commun. 296 2002 267 273
J.F. Scabilloni, L.Y. Wang, J.M. Antonini, J.R. Roberts, V. Castranova, and R.R. Mercer Matrix metalloproteinase induction in fibrosis and fibrotic nodule formation due to silica inhalation Am. J. Physiol. Lung Cell. Mol. Physiol. 288 2005 L709 L717
U. Schonbeck, F. Mach, and P. Libby Generation of biologically active IL-1 beta by matrix metalloproteinases: a novel caspase-1-independent pathway of IL-1 beta processing J. Immunol. 161 1998 3340 3346
M. Seiki, N. Koshikawa, and I. Yana Role of pericellular proteolysis by membrane-type 1 matrix metalloproteinase in cancer invasion and angiogenesis Cancer Metastasis Rev. 22 2003 129 143
M. Selman, V. Ruiz, S. Cabrera, L. Segura, R. Ramirez, R. Barrios, and A. Pardo TIMP-1,-2,-3, and-4 in idiopathic pulmonary fibrosis. A prevailing nondegradative lung microenvironment? Am. J. Physiol. Lung Cell. Mol. Physiol. 279 2000 L562 L574
Y. Shou, T. Hirano, Y. Gong, Y. Kato, K. Yoshida, T. Ohira, N. Ikeda, C. Konaka, Y. Ebihara, F. Zhao, and H. Kato Influence of angiogenetic factors and matrix metalloproteinases upon tumour progression in non-small-cell lung cancer Br. J. Cancer 85 2001 1706 1712
N.E. Sounni, and A. Noel Membrane type-matrix metalloproteinases and tumor progression Biochimie 87 2005 329 342
M.D. Sternlicht, and Z. Werb How matrix metalloproteinases regulate cell behavior Annu. Rev. Cell Dev. Biol. 17 2001 463 516
A.Y. Strongin, I. Collier, G. Bannikov, B.L. Marmer, G.A. Grant, and G.I. Goldberg Mechanism of cell-surface activation of 72-Kda Type-Iv collagenase - isolation of the activated form of the membrane metalloprotease J. Biol. Chem. 270 1995 5331 5338
R.E. Swiderski, J.E. Dencoff, C.S. Floerchinger, S.D. Shapiro, and G.W. Hunninghake Differential expression of extracellular matrix remodeling genes in a murine model of bleomycin-induced pulmonary fibrosis Am. J. Pathol. 152 1998 821 828
P. Thomas, R. Khokha, F.A. Shepherd, R. Feld, and M.S. Tsao Differential expression of matrix metalloproteinases and their inhibitors in non-small cell lung cancer J. Pathol. 190 2000 150 156
M. Tokuraku, H. Sato, S. Murakami, Y. Okada, Y. Watanabe, and M. Seiki Activation of the precursor of gelatinase A/72 Kda Type-Iv collagenase/Mmp-2 in lung carcinomas correlates with the express ion of membrane-type matrix metallo proteinase (Mt-Mmp) and with lymph-node metastasis Int. J. Cancer 64 1995 355 359
K.Y. Vermaelen, D. Cataldo, K. Tournoy, T. Maes, A. Dhulst, R. Louis, J.M. Foidart, A. Noel, and R. Pauwels Matrix metalloproteinase-9-mediated dendritic cell recruitment into the airways is a critical step in a mouse model of asthma J. Immunol. 171 2003 1016 1022
A.M. Vignola, P. Chanez, G. Chiappara, A. Merendino, E. Pace, A. Rizzo, A.M. laRocca, V. Bellia, G. Bonsignore, and J. Bousquet Transforming growth factor-beta expression in mucosal biopsies in asthma and chronic bronchitis Am. J. Respir. Crit. Care Med. 156 1997 591 599
A.M. Vignola, P. Chanez, L. Siena, G. Chiappara, G. Bonsignore, and J. Bousquet Airways remodelling in asthma Pulm. Pharmacol. Ther. 11 1998 359 367
A.M. Vignola, L. Riccobono, A. Mirabella, M. Profita, P. Chanez, V. Bellia, G. Mautino, P. D'Accardi, J. Bousquet, and G. Bonsignore Sputum metalloproteinase-9 tissue inhibitor of metalloproteinase-1 ratio correlates with airflow obstruction in asthma and chronic bronchitis Am. J. Respir. Crit. Care Med. 158 1998 1945 1950
H. Vliagoftis, M.D. Hollenberg, A.D. Befus, and R. Moqbel Airway epithelial cells release eosinophil survival promoting factors following stimulation of proteinase-activated receptor-2 (PAR-2) J. Allergy Clin. Immunol. 105 2000 S171
R.L. Warner, N.W. Lukacs, S.D. Shapiro, N. Bhagarvathula, K.C. Nerusu, J. Varani, and K.J. Johnson Role of metalloelastase in a model of allergic lung responses induced by cockroach allergen Am. J. Pathol. 165 2004 1921 1930
S. Wojtowicz-Praga, J. Torri, M. Johnson, V. Steen, J. Marshall, E. Ness, R. Dickson, M. Sale, H.S. Rasmussen, T.A. Chiodo, and M.J. Hawkins Phase I trial of marimastat, a novel matrix metalloproteinase inhibitor, administered orally to patients with advanced lung cancer J. Clin. Oncol. 16 1998 2150 2156
J. Xu, R.C. Benyon, S.H. Leir, S. Zhang, S.T. Holgate, and P.M. Lackie Matrix metalloproteinase-2 from bronchial epithelial cells induces the proliferation of subepithelial fibroblasts Clin. Exp. Allergy 32 2002 881 888
T. Yaguchi, Y. Fukuda, M. Ishizaki, and N. Yamanaka Immunohistochemical and gelatin zymography studies for matrix metalloproteinases in bleomycin-induced pulmonary fibrosis Pathol. Int. 48 1998 954 963
G.Y. Yang, L. Li, A. Volk, E. Emmell, T. Petley, J. Giles-Komar, P. Rafferty, M. Lakshminarayanan, D.E. Griswold, P.J. Bugelski, and A.M. Das Therapeutic dosing with anti-interleukin-13 monoclonal antibody inhibits asthma progression in mice J. Pharmacol. Exp. Ther. 313 2005 8 15
S. Ylisirnio, M. Hoyhtya, and T. Turpeenniemi-Hujanen Serum matrix metalloproteinases-2, -9 and tissue inhibitors of metalloproteinases-1, -2 in lung cancer - TIMP-1 as a prognostic marker Anticancer Res. 20 2000 1311 1316
H. Yoshisue, and K. Hasegawa Effect of MMP/ADAM inhibitors in goblet cell hyperplasia in cultured human bronchial epithelial cells Biosci. Biotechnol. Biochem. 68 2004 2024 2031
D.L. Zhang, M. Bar-Eli, S. Meloche, and P. Brodt Dual regulation of MMP-2 expression by the type 1 insulin-like growth factor receptor - the phosphatidylinositol 3-kinase/Akt and Raf/ERK pathways transmit opposing signals J. Biol. Chem. 279 2004 19683 19690
T. Zheng, Z. Zhu, Z.D. Wang, R.J. Homer, B. Ma, R.J. Riese, H.A. Chapman, S.D. Shapiro, and J.A. Elias Inducible targeting of IL-13 to the adult lung causes matrix metalloproteinase- and cathepsin-dependent emphysema J. Clin. Invest. 106 2000 1081 1093
X.X. Zhou, J.B. Trudeau, K.J. Schoonover, J.I. Lundin, S.M. Barnes, M.J. Cundall, and S.E. Wenzel Interleukin-13 augments transforming growth factor-beta 1-induced tissue inhibitor of metalloproteinase-1 expression in primary human airway fibroblasts Am. J. Physiol. Cell Physiol. 288 2005 C435 C442
S. Zucker, D.Q. Pei, J. Cao, and C. Lopez-Otin Membrane type-matrix metalloproteinases (MT-MMP) Cell Surf. Proteases 54 2003 1 74
F.R. Zuo, N. Kaminski, E. Eugui, J. Allard, Z. Yakhini, A. Ben Dor, L. Lollini, D. Morris, Y. Kim, B. DeLustro, D. Sheppard, A. Pardo, M. Selman, and R.A. Heller Gene expression analysis reveals matrilysin as a key regulator of pulmonary fibrosis in mice and humans Proc. Natl. Acad. Sci. U. S. A. 99 2002 6292 6297