Folia Biologica
Journal of Cellular and Molecular Biology, Charles University 

Crossref logo

Fol. Biol. 2014, 60, 113-122

https://doi.org/10.14712/fb2014060030113

Differential Expression and Processing of Matrix Metalloproteinase 19 Marks Progression of Gastrointestinal Diseases

M. Červinková1, P. Horák2, I. Kanchev1, R. Matěj3, J. Fanta2, R. Sequens4, P. Kašpárek1,5, L. Sarnová1, J. Turečková1, Radislav Sedláček1

1Laboratory of Transgenic Models of Diseases, Institute of Molecular Genetics of the ASCR, v. v. i., Prague, Czech Republic
2Department of Surgery, First Faculty of Medicine, Charles University in Prague and Na Bulovce Hospital, Prague, Czech Republic
3Department of Pathology and Molecular Medicine, Thomayer Hospital, Prague, Czech Republic
4Gastroenterology Surgical Centre, Hospital of Merciful Sisters of St. Borromeo, Prague, Czech Republic
5Department of Genetics and Microbiology, Faculty of Sciences, Charles University in Prague, Czech Republic

Received November 2013
Accepted January 2014

References

1. Beck, I. M., Ruckert, R., Brandt, K., Mueller, M. S., Sadowski, T., Brauer, R., Schirmacher, P., Mentlein, R., Sedlacek, R. (2008) MMP19 is essential for T cell development and T cell-mediated cutaneous immune responses. PLoS One 3, e2343. <https://doi.org/10.1371/journal.pone.0002343>
2. Bister, V. O., Salmela, M. T., Karjalainen-Lindsberg, M. L., Uria, J., Lohi, J., Puolakkainen, P., Lopez-Otin, C., Saarialho-Kere, U. (2004) Differential expression of three matrix metalloproteinases, MMP-19, MMP-26, and MMP-28, in normal and inflamed intestine and colon cancer. Dig. Dis. Sci. 49, 653-661. <https://doi.org/10.1023/B:DDAS.0000026314.12474.17>
3. Brauer, R., Beck, I. M., Roderfeld, M., Roeb, E., Sedlacek, R. (2011) Matrix metalloproteinase-19 inhibits growth of endothelial cells by generating angiostatin-like fragments from plasminogen. BMC Biochem. 12, 38. <https://doi.org/10.1186/1471-2091-12-38>
4. Buryova, H., Chalupsky, K., Zbodakova, O., Kanchev, I., Jirouskova, M., Gregor, M., Sedlacek, R. (2013) Liver protective effect of ursodeoxycholic acid includes regulation of ADAM17 activity. BMC Gastroenterol. 13, 155. <https://doi.org/10.1186/1471-230X-13-155>
5. Chalupský K, Kanchev I, Žbodáková O, Buryová H, Jiroušková M, Kořínek V, Gregor M, Sedláček R (2013) ADAM10/17-dependent release of soluble c-Met correlates with hepatocellular damage. Folia Biol. (Praha) 59, 76-86. <https://doi.org/10.14712/fb2013059020076>
6. Chan, K. C., Ko, J. M., Lung, H. L., Sedlacek, R., Zhang, Z. F., Luo, D. Z., Feng, Z. B., Chen, S., Chen, H., Chan, K. W., Tsao, S. W., Chua, D. T., Zabarovsky, E. R., Stanbridge, E. J., Lung, M. L. (2011) Catalytic activity of matrix metalloproteinase-19 is essential for tumor suppressor and antiangiogenic activities in nasopharyngeal carcinoma. Int. J. Cancer 129, 1826-1837. <https://doi.org/10.1002/ijc.25855>
7. Cox, J. H., Dean, R. A., Roberts, C. R., Overall, C. M. (2008) Matrix metalloproteinase processing of CXCL11/I-TAC results in loss of chemoattractant activity and altered glycosaminoglycan binding. J. Biol. Chem. 283, 19389-19399. <https://doi.org/10.1074/jbc.M800266200>
8. Curry, T. E., Jr., Osteen, K. G. (2003) The matrix metalloproteinase system: changes, regulation, and impact throughout the ovarian and uterine reproductive cycle. Endocr. Rev. 24, 428-465. <https://doi.org/10.1210/er.2002-0005>
9. Dean, R. A., Cox, J. H., Bellac, C. L., Doucet, A., Starr, A. E., Overall, C. M. (2008) Macrophage-specific metalloelastase (MMP-12) truncates and inactivates ELR+ CXC chemokines and generates CCL2, -7, -8, and -13 antagonists: potential role of the macrophage in terminating polymorphonuclear leukocyte influx. Blood 112, 3455-3464. <https://doi.org/10.1182/blood-2007-12-129080>
10. Djonov, V., Hogger, K., Sedlacek, R., Laissue, J., Draeger, A. (2001) MMP-19: cellular localization of a novel metalloproteinase within normal breast tissue and mammary gland tumours. J. Pathol. 195, 147-155. <https://doi.org/10.1002/path.927>
11. Hadler-Olsen, E., Winberg, J. O., Uhlin-Hansen, L. (2013) Matrix metalloproteinases in cancer: their value as diagnostic and prognostic markers and therapeutic targets. Tumour Biol. 34, 2041-2051. <https://doi.org/10.1007/s13277-013-0842-8>
12. Jirouskova, M., Zbodakova, O., Gregor, M., Chalupsky, K., Sarnova, L., Hajduch, M., Ehrmann, J., Jirkovska, M., Sedlacek, R. (2012) Hepatoprotective effect of MMP-19 deficiency in a mouse model of chronic liver fibrosis. PLoS One 7, e46271. <https://doi.org/10.1371/journal.pone.0046271>
13. Jost, M., Folgueras, A. R., Frerart, F., Pendas, A. M., Blacher, S., Houard, X., Berndt, S., Munaut, C., Cataldo, D., Alvarez, J., Melen-Lamalle, L., Foidart, J. M., Lopez-Otin, C., Noel, A. (2006) Earlier onset of tumoral angiogenesis in matrix metalloproteinase-19-deficient mice. Cancer Res. 66, 5234-5241. <https://doi.org/10.1158/0008-5472.CAN-05-4315>
14. Khokha, R., Murthy, A., Weiss, A. (2013) Metalloproteinases and their natural inhibitors in inflammation and immunity. Nat. Rev. Immunol. 13, 649-65. <https://doi.org/10.1038/nri3499>
15. Kolb, C., Mauch, S., Peter, H. H., Krawinkel, U., Sedlacek, R. (1997) The matrix metalloproteinase RASI-1 is expressed in synovial blood vessels of a rheumatoid arthritis patient. Immunol. Lett. 57, 83-88. <https://doi.org/10.1016/S0165-2478(97)00057-6>
16. Kolb, C., Mauch, S., Krawinkel, U., Sedlacek, R. (1999) Matrix metalloproteinase-19 in capillary endothelial cells: expression in acutely, but not in chronically, inflamed synovium. Exp. Cell Res. 250, 122-130. <https://doi.org/10.1006/excr.1999.4493>
17. Lettau, I., Hattermann, K., Held-Feindt, J., Brauer, R., Sedlacek, R., Mentlein, R. (2010) Matrix metalloproteinase-19 is highly expressed in astroglial tumors and promotes invasion of glioma cells. J. Neuropathol. Exp. Neurol. 69, 215-223. <https://doi.org/10.1097/NEN.0b013e3181ce9f67>
18. Mauch, S., Kolb, C., Kolb, B., Sadowski, T., Sedlacek, R. (2002) Matrix metalloproteinase-19 is expressed in myeloid cells in an adhesion-dependent manner and associates with the cell surface. J. Immunol. 168, 1244-1251. <https://doi.org/10.4049/jimmunol.168.3.1244>
19. Medina, C., Radomski, M. W. (2006) Role of matrix metalloproteinases in intestinal inflammation. J. Pharmacol. Exp. Ther. 318, 933-938. <https://doi.org/10.1124/jpet.106.103465>
20. Meijer, M. J., Mieremet-Ooms, M. A., van der Zon, A. M., van Duijn, W., van Hogezand, R. A., Sier, C. F., Hommes, D. W., Lamers, C. B., Verspaget, H. W. (2007) Increased mucosal matrix metalloproteinase-1, -2, -3 and -9 activity in patients with inflammatory bowel disease and the relation with Crohn’s disease phenotype. Dig. Liver Dis. 39, 733-739. <https://doi.org/10.1016/j.dld.2007.05.010>
21. Monteleone, G., Caruso, R., Fina, D., Peluso, I., Gioia, V., Stolfi, C., Fantini, M. C., Caprioli, F., Tersigni, R., Alessandroni, L., MacDonald, T. T., Pallone, F. (2006) Control of matrix metalloproteinase production in human intestinal fibroblasts by interleukin 21. Gut 55, 1774-1780. <https://doi.org/10.1136/gut.2006.093187>
22. Mueller, M. S., Harnasch, M., Kolb, C., Kusch, J., Sadowski, T., Sedlacek, R (2000) The murine ortholog of matrix metalloproteinase 19: its cloning, gene organization, and expression. Gene 256, 101-111. <https://doi.org/10.1016/S0378-1119(00)00369-3>
23. Muller, M., Beck, I. M., Gadesmann, J., Karschuk, N., Paschen, A., Proksch, E., Djonov, V., Reiss, K., Sedlacek, R. (2010) MMP19 is upregulated during melanoma progression and increases invasion of melanoma cells. Mod. Pathol. 23, 511-521. <https://doi.org/10.1038/modpathol.2009.183>
24. Nagase, H., Visse, R., Murphy, G. (2006) Structure and function of matrix metalloproteinases and TIMPs. Cardiovasc. Res. 69, 562-573. <https://doi.org/10.1016/j.cardiores.2005.12.002>
25. Naito, Y., Takagi, T., Kuroda, M., Katada, K., Ichikawa, H., Kokura, S., Yoshida, N., Okanoue, T., Yoshikawa, T. (2004) An orally active matrix metalloproteinase inhibitor, ONO4817, reduces dextran sulfate sodium-induced colitis in mice. Inflamm. Res. 53, 462-468. <https://doi.org/10.1007/s00011-004-1281-1>
26. Naito, Y., Yoshikawa, T. (2005) Role of matrix metalloproteinases in inflammatory bowel disease. Mol. Aspects Med. 26, 379-390. <https://doi.org/10.1016/j.mam.2005.07.009>
27. Page-McCaw, A., Ewald, A. J., Werb, Z. (2007) Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233. <https://doi.org/10.1038/nrm2125>
28. Parks, W. C., Wilson, C. L., Lopez-Boado, Y. S. (2004) Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat. Rev. Immunol. 4, 617-629. <https://doi.org/10.1038/nri1418>
29. Pedersen, G., Saermark, T., Kirkegaard, T., Brynskov, J. (2009) Spontaneous and cytokine induced expression and activity of matrix metalloproteinases in human colonic epithelium. Clin. Exp. Immunol. 155, 257-265. <https://doi.org/10.1111/j.1365-2249.2008.03836.x>
30. Pendás, A. M., Knäuper, V., Puente, X. S., Llano, E., Mattei, M. G., Apte, S., Murphy, G., Lopez-Otin, C. (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. <https://doi.org/10.1074/jbc.272.7.4281>
31. Pender, S. L., MacDonald, T. T. (2004) Matrix metalloproteinases and the gut – new roles for old enzymes. Curr. Opin. Pharmacol. 4, 546-450. <https://doi.org/10.1016/j.coph.2004.06.005>
32. Ponder, A., Long, M. D. (2013) A clinical review of recent findings in the epidemiology of inflammatory bowel disease. Clin. Epidemiol. 5, 237-247.
33. Ravi, A., Garg, P., Sitaraman, S. V. (2007) Matrix metalloproteinases in inflammatory bowel disease: boon or a bane? Inflamm. Bowel Dis. 13, 97-107. <https://doi.org/10.1002/ibd.20011>
34. Roy, R., Yang, J., Moses, M. A. (2009) Matrix metalloproteinases as novel biomarkers and potential therapeutic targets in human cancer. J. Clin. Oncol. 27, 5287-5297. <https://doi.org/10.1200/JCO.2009.23.5556>
35. Rumessen, J. J., Vanderwinden, J. M., Horn, T. (2011) Crohn’s disease: ultrastructure of interstitial cells in colonic myenteric plexus. Cell Tissue Res. 344, 471-479. <https://doi.org/10.1007/s00441-011-1175-9>
36. Sadowski, T., Dietrich, S., Koschinsky, F., Sedlacek, R. (2003) Matrix metalloproteinase 19 regulates insulin-like growth factor-mediated proliferation, migration, and adhesion in human keratinocytes through proteolysis of insulin-like growth factor binding protein-3. Mol. Biol. Cell 14, 4569-4580. <https://doi.org/10.1091/mbc.e03-01-0009>
37. Sadowski, T., Dietrich, S., Koschinsky, F., Ludwig, A., Proksch, E., Titz, B., Sedlacek, R. (2005) Matrix metalloproteinase 19 processes the laminin 5 γ2 chain and induces epithelial cell migration. Cell. Mol. Life Sci. 62, 870-880. <https://doi.org/10.1007/s00018-005-4478-8>
38. Sanders, K. M., Hwang, S. J., Ward, S. M. (2010) Neuroeffector apparatus in gastrointestinal smooth muscle organs. J. Physiol. 588, 4621-4639. <https://doi.org/10.1113/jphysiol.2010.196030>
39. Sedlacek, R., Mauch, S., Kolb, B., Schatzlein, C., Eibel, H., Peter, H. H., Schmitt, J., Krawinkel, U. (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. <https://doi.org/10.1016/S0171-2985(98)80049-1>
40. Stracke, J. O., Fosang, A. J., Last, K., Mercuri, F. A., Pendas, A. M., Llano, E., Perris, R., Di Cesare, P. E., Murphy, G., Knauper, V. (2000a) Matrix metalloproteinases 19 and 20 cleave aggrecan and cartilage oligomeric matrix protein (COMP). FEBS Lett. 478, 52-56. <https://doi.org/10.1016/S0014-5793(00)01819-6>
41. Stracke, J. O., Hutton, M., Stewart, M., Pendas, A. M., Smith, B., Lopez-Otin, C., Murphy, G., Knauper, V. (2000b) 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. <https://doi.org/10.1074/jbc.275.20.14809>
42. Titz, B., Dietrich, S., Sadowski, T., Beck, C., Petersen, A., Sedlacek, R. (2004) Activity of MMP-19 inhibits capillary-like formation due to processing of nidogen-1. Cell. Mol. Life Sci. 61, 1826-1833. <https://doi.org/10.1007/s00018-004-4105-0>
43. Van Wart, H. E., Birkedal-Hansen, H. (1990) The cysteine switch: a principle of regulation of metalloproteinase activity with potential applicability to the entire matrix metalloproteinase gene family. Proc. Natl. Acad. Sci. USA 87, 5578-5582. <https://doi.org/10.1073/pnas.87.14.5578>
44. Vu, T. H., Werb, Z. (2000) Matrix metalloproteinases: effectors of development and normal physiology. Genes Dev. 14, 2123-2133. <https://doi.org/10.1101/gad.815400>
45. Wang, X. Y., Zarate, N., Soderholm, J. D., Bourgeois, J. M., Liu, L. W., Huizinga, J. D. (2007) Ultrastructural injury to interstitial cells of Cajal and communication with mast cells in Crohn’s disease. Neurogastroenterol. Motil. 19, 349-364. <https://doi.org/10.1111/j.1365-2982.2006.00894.x>
46. Wang, Y. D., Wang, W. (2008) Protective effect of ilomastat on trinitrobenzenesulfonic acid-induced ulcerative colitis in rats. World J. Gastroenterol. 14, 5683-5688. <https://doi.org/10.3748/wjg.14.5683>
47. Yu, G., Kovkarova-Naumovski, E., Jara, P., Parwani, A., Kass, D., Ruiz, V., Lopez-Otin, C., Rosas, I. O., Gibson, K. F., Cabrera, S., Ramirez, R., Yousem, S. A., Richards, T. J., Chensny, L. J., Selman, M., Kaminski, N., Pardo, A. (2012) MMP19 is a key regulator of lung fibrosis in mice and humans. Am. J. Respir. Crit. Med. 186, 752-762. <https://doi.org/10.1164/rccm.201202-0302OC>
front cover

ISSN 0015-5500 (Print) ISSN 2533-7602 (Online)

Open access journal

Submissions

Archive