Diet-induced obesity and reduced skin cancer susceptibility in matrix metalloproteinase-19 deficient mice

[en] Matrix metalloproteinase 19 (MMP-19) is a member of the MMP family of endopeptidases that, in contrast to most MMPs, is widely expressed in human tissues under normal quiescent conditions. MMP-19 has been found to be associated with ovulation and angiogenic processes and is deregulated in diverse pathological conditions such as rheumatoid arthritis and cancer. To gain further insights into the in vivo functions of this protease, we have generated mutant mice deficient in Mmp19. These mice are viable and fertile and do not display any obvious abnormalities. However, Mmp19-null mice develop a diet-induced obesity due to adipocyte hypertrophy and exhibit decreased susceptibility to skin tumors induced by chemical carcinogens. Based on these results, we suggest that this enzyme plays an in vivo role in some of the tissue remodeling events associated with adipogenesis, as well as in pathological processes such as tumor progression

Disciplines :

Biochemistry, biophysics & molecular biology

Author, co-author :

Pendas, A. M.

Folgueras, A. R.

LLano, E.

Caterina, J.

Frerard, F.

Rodriguez, F.

Astudillo, A.

Noël, Agnès ; Université de Liège - ULiège > Département des sciences biomédicales et précliniques > Biologie cellulaire et moléculaire appliquée à l'homme

Birkedal-Hansen, H.

Lopez-Otin, C.

Language :

English

Title :

Diet-induced obesity and reduced skin cancer susceptibility in matrix metalloproteinase-19 deficient mice

Publication date :

2004

Journal title :

Molecular and Cellular Biology

ISSN :

0270-7306

eISSN :

1098-5549

Publisher :

American Society for Microbiology (ASM), Washington, United States - District of Columbia

Volume :

Issue :

Pages :

5304-13

Peer reviewed :

Peer Reviewed verified by ORBi

Available on ORBi :

since 21 December 2009

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Bibliography

Alexander, C. M., S. Selvarajan, J. Mudgett, and Z. Werb. 2001. Stromelysin-1 regulates adipogenesis during mammary gland involution. J. Cell Biol. 152:693-703.
Balbin, M., A. Fueyo, A. M. Tester, A. M. Pendas, A. S. Pitiot, A. Astudillo, C. M. Overall, S. D. Shapiro, and C. Lopez-Otin. 2003. Loss of collagenase-2 confers increased skin tumor susceptibility to male mice. Nat. Genet. 35:252-257.
Blacher, S., L. Devy, M. F. Burbridge, G. Roland, G. Tucker, A. Noel, and J. M. Foidart. 2001. Improved quantification of angiogenesis in the rat aortic ring assay. Angiogenesis 4:133-142.
Bouloumie, A., C. Sengenes, G. Portolan, J. Galitzky, and M. Lafontan. 2001. Adipocyte produces matrix metalloproteinases 2 and 9: involvement in adipose differentiation. Diabetes 50:2080-2086.
Brinckerhoff, C. E., and L. M. Matrisian. 2002. Matrix metalloproteinases: a tail of a frog that became a prince. Nat. Rev. Mol. Cell. Biol. 3:207-214.
Chavey, C., B. Mari, M. N. Monthouel, S. Bonnafous, P. Anglard, E. Van Obberghen, and S. Tartare-Deckert. 2003. Matrix metalloproteinases are differentially expressed in adipose tissue during obesity and modulate adipocyte differentiation. J. Biol. Chem. 278:11888-11896.
Cossins, J., T. J. Dudgeon, G. Catlin, A. J. Gearing, and J. M. Clements. 1996. Identification of MMP-18, a putative novel human matrix metalloproteinase. Biochem. Biophys. Res. Commun. 228:494-498.
Coussens, L. M., B. Fingleton, and L. M. Matrisian. 2002. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 295:2387-2392.
Croissandeau, G., M. Chretien, and M. Mbikay. 2002. Involvement of matrix metalloproteinases in the adipose conversion of 3T3-L1 preadipocytes. Biochem. J. 364:739-746.
Devy, L., S. Blacher, C. Grignet-Debrus, K. Bajou, V. Masson, R. D. Gerard, A. Gils, G. Carmeliet, P. Carmeliet, P. J. Declerck, A. Noel, and J. M. Foidart. 2002. The pro- or antiangiogenic effect of plasminogen activator inhibitor 1 is dose dependent. FASEB J. 16:147-154.
Egeblad, M., and Z. Werb. 2002. New functions for the matrix metalloproteinases in cancer progression. Nat. Rev. Cancer. 2:161-174.
Freije, J. M., M. Balbin, A. M. Pendas, L. M. Sanchez, X. S. Puente, and C. Lopez-Otin. 2003. Matrix metalloproteinases and tumor progression. Adv. Exp. Med. Biol. 532:91-107.
Halpert, I., U. I. Sires, J. D. Roby, S. Potter-Perigo, T. N. Wight, S. D. Shapiro, H. G. Welgus, S. A. Wickline, and W. C. Parks. 1996. Matrilysin is expressed by lipid-laden macrophages at sites of potential rupture in atherosclerotic lesions and localizes to areas of versican deposition, a proteoglycan substrate for the enzyme. Proc. Natl. Acad. Sci. USA 93:9748-9753.
Hieta, N., U. Impola, C. Lopez-Otin, U. Saarialho-Kere, and V. M. Kahari. 2003. Matrix metalloproteinase-19 expression in dermal wounds and by fibroblasts in culture. J. Investig. Dermatol. 121:997-1004.
Jackson, R. S., J. W. Creemers, S. Ohagi, M. L. Raffin-Sanson, L. Sanders, C. T. Montague, J. C. Hutton, and S. O'Rahilly. 1997. Obesity and impaired prohormone processing associated with mutations in the human prohormone convertase 1 gene. Nat. Genet. 16:303-306.
Kawaguchi, N., X. Xu, R. Tajima, P. Kronqvist, C. Sundberg, F. Loechel, R. Albrechtsen, and U. M. Wewer. 2002. ADAM 12 protease induces adipogenesis in transgenic mice. Am. J. Pathol. 160:1895-1903.
Kim, C. S., T. Kawada, H. Yoo, B. S. Kwon, and R. Yu. 2003. Macrophage inflammatory protein-related protein-2, a novel CC chemokine, can regulate preadipocyte migration and adipocyte differentiation. FEBS Lett. 548:125-130.
Kolb, C., S. Mauch, U. Krawinkel, and R. Sedlacek. 1999. Matrix metalloproteinase-19 in capillary endothelial cells: expression in acutely, but not in chronically, inflamed synovium. Exp. Cell Res. 250:122-130.
Konttinen, Y. T., M. Ainola, H. Valleala, J. Ma, H. Ida, J. Mandelin, R. W. Kinne, S. Santavirta, T. Sorsa, C. Lopez-Otin, and M. Takagi. 1999. Analysis of 16 different matrix metalloproteinases (MMP-1 to MMP-20) in the synovial membrane: different profiles in trauma and rheumatoid arthritis. Ann. Rheum Dis. 58:691-697.
Kurisaki, T., A. Masuda, K. Sudo, J. Sakagami, S. Higashiyama, Y. Matsuda, A. Nagabukuro, A. Tsuji, Y. Nabeshima, M. Asano, Y. Iwakura, and A. Sehara-Fujisawa. 2003. Phenotypic analysis of Meltrin alpha (ADAM12)-deficient mice: involvement of Meltrin alpha in adipogenesis and myogenesis. Mol. Cell. Biol. 23:55-61.
Lijnen, H. R., E. Maquoi, L. B. Hansen, B. Van Hoef, L. Frederix, and D. Collen. 2002. Matrix metalloproteinase inhibition impairs adipose tissue development in mice. Arterioscler. Thromb. Vasc. Biol. 22:374-379.
Lijnen, H. R., H. B. Van, L. Frederix, M. C. Rio, and D. Collen. 2002. Adipocyte hypertrophy in stromelysin-3 deficient mice with nutritionally induced obesity. Thromb. Haemost. 87:530-535.
MacDougald, O. A., and S. Mandrup. 2002. Adipogenesis: forces that tip the scales. Trends Endocrinol. Metab. 13:5-11.
Maquoi, E., D. Demeulemeester, G. Voros, D. Collen, and H. R. Lijnen. 2003. Enhanced nutritionally induced adipose tissue development in mice with stromelysin-1 gene inactivation. Thromb. Haemost. 89:696-704.
Maquoi, E., C. Munaut, A. Colige, D. Collen, and H. R. Lijnen. 2002. Modulation of adipose tissue expression of murine matrix metalloproteinases and their tissue inhibitors with obesity. Diabetes 51:1093-1101.
Masson, V. V., L. Devy, C. Grignet-Debrus, S. Bernt, K. Bajou, S. Blacher, G. Roland, Y. Chang, T. Fong, P. Carmeliet, J. M. Foidart, and A. Noel. 2002. Mouse aortic ring assay: a new approach of the molecular genetics of angiogenesis. Biol. Proced. Online 4:24-31.
Mueller, M. S., S. Mauch, and R. Sedlacek. 2000. Structure of the human MMP-19 gene. Gene 252:27-37.
Nagase, H., and J. F. Woessner, Jr. 1999. Matrix metalloproteinases. J. Biol. Chem. 274:21491-21494.
Naggert, J. K., L. D. Fricker, O. Varlamov, P. M. Nishina, Y. Rouille, D. F. Steiner, R. J. Carroll, B. J. Paigen, and E. H. Leiter. 1995. Hyperproinsulinaemia in obese fat/fat mice associated with a carboxypeptidase E mutation which reduces enzyme activity. Nat. Genet. 10:135-142.
Overall, C. M., and C. Lopez-Otin. 2002. Strategies for MMP inhibition in cancer: innovations for the post-trial era. Nat. Rev. Cancer. 2:657-672.
Pendas, A. M., M. Balbin, E. Llano, M. G. Jimenez, and C. Lopez-Otin. 1997. Structural analysis and promoter characterization of the human collagenase-3 gene (MMP13). Genomics 40:222-233.
Pendas, A. M., V. Knauper, X. S. Puente, E. Llano, M. G. Mattei, S. Apte, G. Murphy, and C. Lopez-Otin. 1997. Identification and characterization of a novel human matrix metalloproteinase with unique structural characteristics, chromosomal location, and tissue distribution. J. Biol. Chem. 272:4281-4286.
Rangwala, S. M., and M. A. Lazar. 2000. Transcriptional control of adipogenesis. Annu. Rev. Nutr. 20:535-559.
Sadowski, T., S. Dietrich, F. Koschinsky, and R. Sedlacek. 2003. Matrix metalloproteinase 19 regulates insulin-like growth factor-mediated proliferatin, migration, and adhesion in human keratinocytes through proteolysis of insulin-like growth factor binding protein-3. Mol. Biol. Cell 14:45694580.
Sadowski, T., S. Dietrich, M. Muller, B. Havlickova, M. Schunck, E. Proksch, M. S. Muller, and R. Sedlacek. 2003. Matrix metalloproteinase-19 expression in normal and diseased skin: dysregulation by epidermal proliferation. J. Investig. Dermatol. 121:989-996.
Sedlacek, R., S. Mauch, B. Kolb, C. Schatzlein, H. Eibel, H. H. Peter, J. Schmitt, and U. Krawinkel. 1998. Matrix metalloproteinase MMP-19 (RASI-1) is expressed on the surface of activated peripheral blood mononuclear cells and is detected as an autoantigen in rheumatoid arthritis. Immunobiology 198:408-423.
Selvarajan, S., L. R. Lund, T. Takeuchi, C. S. Craik, and Z. Werb. 2001. A plasma kallikrein-dependent plasminogen cascade required for adipocyte differentiation. Nat. Cell Biol. 3:267-275.
Stracke, J. O., A. J. Fosang, K. Last, F. A. Mercuri, A. M. Pendas, E. Llano, R. Perris, P. E. Di Cesare, G. Murphy, and V. Knauper. 2000. Matrix metalloproteinases 19 and 20 cleave aggrecan and cartilage oligomeric matrix protein (COMP). FEBS Lett. 478:52-56.
Stracke, J. O., M. Hutton, M. Stewart, A. M. Pendas, B. Smith, C. Lopez-Otin, G. Murphy, and V. Knauper. 2000. Biochemical characterization of the catalytic domain of human matrix metalloproteinase 19: evidence for a role as a potent basement membrane degrading enzyme. J. Biol. Chem. 275:14809-14816.
Vu, T. H., and Z. Werb. 2000. Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14:2123-2133.
Yang, M., and M. Kurkinen. 1998. Cloning and characterization of a novel matrix metalloproteinase (MMP), CMMP, from chicken embryo fibroblasts. CMMP, Xenopus XMMP, and human MMP19 have a conserved unique cysteine in the catalytic domain. J. Biol. Chem. 273:17893-17900.