MMP9 is protective against lethal inflammatory mass lesions in the mouse colon

DMM Disease Models and Mechanisms

Volumn 4, Issue 2, 2011, Pages 212-227

  Hald, Andreas ^a,b   Rønø, Birgitte ^a,b   Melander, Maria C ^b   Ding, Ming ^c   Holck, Susanne ^d   Lund, Leif R ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

^b FINSEN LABORATORY   (Denmark)

^c ODENSE UNIVERSITY HOSPITAL   (Denmark)

^d UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME PRECURSOR; GELATINASE B; PLASMIN; PLASMINOGEN; SERINE PROTEINASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLOOD ANALYSIS; BONE STRUCTURE; CHRONIC INFLAMMATION; COLITIS; COLON INJURY; CONTROLLED STUDY; CYTOTOXIC T LYMPHOCYTE; DISEASE ASSOCIATION; FEMALE; FIBRIN DEPOSITION; GRANULOCYTE; HELPER CELL; HISTOLOGY; HISTOPATHOLOGY; LYMPH FOLLICLE; LYMPHOID HYPERPLASIA; MALE; MESENTERY LYMPH NODE; MOUSE; NATURAL KILLER CELL; NEUTROPHIL; NEUTROPHILIA; NONHUMAN; ORGAN SIZE; PRIORITY JOURNAL; PROTEIN FUNCTION; RECTUM PROLAPSE; REGULATORY T LYMPHOCYTE; SPLEEN; SPLENOMEGALY; SURVIVAL TIME; T LYMPHOCYTE; THYMUS; WOUND HEALING IMPAIRMENT;

ALLELES; ANIMALS; B-LYMPHOCYTES; COLON; EPITHELIAL CELLS; FIBRIN; GRANULOCYTES; INFLAMMATION; LEUKOCYTE COUNT; LYMPHOCYTE ACTIVATION; LYMPHOID TISSUE; MATRIX METALLOPROTEINASE 9; MICE; PLASMINOGEN; PROTECTIVE AGENTS; SPLEEN; T-LYMPHOCYTES; THYMUS GLAND; WOUND HEALING;

ANIMALIA; MUS;

EID: 79952323816     PISSN: 17548403     EISSN: 17548411     Source Type: Journal    
DOI: 10.1242/dmm.005801     Document Type: Article

References (62)

1. Abrahams, N. A., Vesoulis, Z. and Petras, R. E. (2001). Angiogenic polypoid proliferation adjacent to ileal carcinoid tumors: a nonspecific finding related to mucosal prolapse. Mod. Pathol. 14, 821-827.
2. Alexander, C. M., Hansell, E. J., Behrendtsen, O., Flannery, M. L., Kishnani, N. S., Hawkes, S. P. and Werb, Z. (1996). Expression and function of matrix metalloproteinases and their inhibitors at the maternal-embryonic boundary during mouse embryo implantation. Development 122, 1723-1736. (Pubitemid 26192738)
3. Allibone, R. O., Hoffman, J., Gosney, J. R. and Helliwell, T. R. (1993). Granulation tissue polyposis associated with carcinoid tumours of the small intestine. Histopathology 22, 475-480.
4. Allport, J. R., Lim, Y. C., Shipley, J. M., Senior, R. M., Shapiro, S. D., Matsuyoshi, N., Vestweber, D. and Luscinskas, F. W. (2002). Neutrophils from MMP-9- or neutrophil elastase-deficient mice show no defect in transendothelial migration under flow in vitro. J. Leukoc. Biol. 71, 821-828.
5. Annes, J. P., Munger, J. S. and Rifkin, D. B. (2003). Making sense of latent TGFbeta activation. J. Cell Sci. 116, 217-224.
6. Bugge, T. H., Flick, M. J., Daugherty, C. C. and Degen, J. L. (1995). Plasminogen deficiency causes severe thrombosis but is compatible with development and reproduction. Genes Dev. 9, 794-807.
7. Bugge, T. H., Kombrinck, K. W., Flick, M. J., Daugherty, C. C., Danton, M. J. and Degen, J. L. (1996). Loss of fibrinogen rescues mice from the pleiotropic effects of plasminogen deficiency. Cell 87, 709-719.
8. Campbell, A. P., Cobb, C. A., Chapman, R. W., Kettlewell, M., Hoang, P., Haot, B. J. and Jewell, D. P. (1993). Cap polyposis-an unusual cause of diarrhoea. Gut 34, 562-564. (Pubitemid 23093504)
9. Castaneda, F. E., Walia, B., Vijay-Kumar, M., Patel, N. R., Roser, S., Kolachala, V. L., Rojas, M., Wang, L., Oprea, G., Garg, P. et al. (2005). Targeted deletion of metalloproteinase 9 attenuates experimental colitis in mice: central role of epithelial-derived MMP. Gastroenterology 129, 1991-2008.
10. Cheng, M. M. (2009). Is the drugstore safe? Counterfeit diabetes products on the shelves. J. Diabetes Sci. Technol. 3, 1516-1520.
11. Chichlowski, M., Westwood, G. S., Abraham, S. N., Hale, L. P. (2010). Role of mast cells in inflammatory bowel diseasae and inflammation-associated colorectal neoplasia in IL-10-deficient mice. PLoS ONE 17, e12220.
12. Cohen, J. J. (1992). Glucocorticoid-induced apoptosis in the thymus. Semin. Immunol. 4, 363-369.
13. Coussens, L. M., Raymond, W. W., Bergers, G., Laig-Webster, M., Behrendtsen, O., Werb, Z., Caughey, G. H. and Hanahan, D. (1999). Inflammatory mast cells upregulate angiogenesis during squamous epithelial carcinogenesis. Genes Dev. 13, 1382-1397. (Pubitemid 29270244)
14. Dallas, S. L., Rosser, J. L., Mundy, G. R. and Bonewald, L. F. (2002). Proteolysis of latent transforming growth factor-beta (TGF-beta)-binding protein-1 by osteoclasts. A cellular mechanism for release of TGF-beta from bone matrix. J. Biol. Chem. 277, 21352-21360.
15. Danø, K., Rømer, J., Nielsen, B. S., Bjørn, S., Pyke, C., Rygaard, J. and Lund, L. R. (1999). Cancer invasion and tissue remodeling - cooperation of preotease systems and cell types. APMIS. 107, 120-127.
16. Degen, S. J., Bell, S. M., Schaefer, L. A. and Elliott, R. W. (1990). Characterization of the cDNA coding for mouse plasminogen and localization of the gene to mouse chromosome 17. Genomics 8, 49-61.
17. DiLillo, D. J., Hamaguchi, Y., Ueda, Y., Yang, K., Uchida, J., Haas, K. M., Kelsoe, G. and Tedder, T. F. (2008). Maintenance of long-lived plasma cells and serological memory despite mature and memory B cell depletion during CD20 immunotherapy in mice. J. Immunol. 180, 361-371.
18. Ding, M., Odgaard, A., Danielsen, C. C. and Hvid, I. (2002). Mutual associations among microstructural, physical and mechanical properties of human cancellous bone. J. Bone Joint Surg. Br. 84, 900-907. (Pubitemid 34918901)
19. Dunker, N. and Krieglstein, K. (2000). Targeted mutations of transforming growth factor-beta genes reveal important roles in mouse development and adult homeostasis. Eur. J. Biochem. 267, 6982-6988. (Pubitemid 32009439)
20. Engsig, M. T., Chen, Q. J., Vu, T. H., Pedersen, A. C., Therkidsen, B., Lund, L. R., Henriksen, K., Lenhard, T., Foged, N. T., Werb, Z. et al. (2000). Matrix metalloproteinase 9 and vascular endothelial growth factor are essential for osteoclast recruitment into developing long bones. J. Cell Biol. 151, 879-889.
21. Fenoglio, L., Cena, P., Bracco, C., Pomero, F., Migliore, E., Benedetti, V., Morino, M. and Perin, P. C. (2008). Proximalisation of colorectal carcinoma: a 10-year study in Italy. Dig. Dis. Sci. 53, 736-740.
22. Fingleton, B. (2008). MMPs as therapeutic targets-still a viable option? Semin. Cell Dev. Biol. 19, 61-68.
23. Froicu, M. and Cantorna, M. T. (2007). Vitamin D and the vitamin D receptor are critical for control of the innate immune response to colonic injury. BMC Immunol. 8, 5.
24. Frøssing, S., Rønø, B., Hald, A., Rømer, J. and Lund, L. R. (2010). Skin wound healing in MMP2-deficient and MMP2 / Plasminogen double-deficient mice. Exp. Dermatol. 19, e234-e240.
25. Garg, P., Vijay-Kumar, M., Wang, L., Gewirtz, A. T., Merlin, D. and Sitaraman, S. V. (2009). Matrix metalloproteinase-9-mediated tissue injury overrides the protective effect of matrix metalloproteinase-2 during colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 296, G175-G184.
26. Gong, Y., Hart, E., Shchurin, A. and Hoover-Plow, J. (2008). Inflammatory macrophage migration requires MMP-9 activation by plasminogen in mice. J. Clin. Invest. 118, 3012-3024.
27. Green, K. A., Almholt, K., Ploug, M., Rønø, B., Castellino, F. J., Johnsen, M., Bugge, T. H., Rømer, J. and Lund, L. R. (2008). Profibrinolytic effects of metalloproteinases during skin wound healing in the absence of plasminogen. J. Invest. Dermatol. 128, 2092-2101.
28. Greenlee, K. J., Corry, D. B., Engler, D. A., Matsunami, R. K., Tessier, P., Cook, R. G., Werb, Z. and Kheradmand, F. (2006). Proteomic identification of in vivo substrates for matrix metalloproteinases 2 and 9 reveals a mechanism for resolution of inflammation. J. Immunol. 177, 7312-7321. (Pubitemid 44715101)
29. Hattori, N., Mochizuki, S., Kishi, K., Nakajima, T., Takaishi, H., D'Armiento, J. and Okada, Y. (2009). MMP-13 plays a role in keratinocyte migration, angiogenesis, and contraction in mouse skin wound healing. Am. J. Pathol. 175, 533-546.
30. Heissig, B., Lund, L. R., Akiyama, H., Ohki, M., Morita, Y., Rømer, J., Nakauchi, H., Okumura, K., Ogawa, H., Werb, Z. et al. (2007). The plasminogen fibrinolytic pathway is required for hematopoietic regeneration. Cell Stem Cell 1, 658-670. (Pubitemid 350215332)
31. Johnsen, M., Lund, L. R., Rømer, J., Almholt, K. and Danø, K. (1998). Cancer invasion and tissue remodeling: common themes in proteolytic matrix degradation. Curr. Opin. Cell Biol. 10, 667-671. (Pubitemid 28477027)
32. Kawasaki, Y., Xu, Z. Z., Wang, X., Park, J. Y., Zhuang, Z. Y., Tan, P. H., Gao, Y. J., Roy, K., Corfas, G., Lo, E. H. et al. (2008). Distinct roles of matrix metalloproteases in the early- and late-phase development of neuropathic pain. Nat. Med. 14, 331-336. (Pubitemid 351347915)
33. Kelly, J. K. (1991). Polypoid prolapsing mucosal folds in diverticular disease. Am. J. Surg. Pathol. 15, 871-878.
34. Leco, K. J., Harvey, M. B., Hogan, A., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., Edwards, D. R. and Schultz, G. A. (1997). Matrix metalloproteinase-9 maps to the distal end of chromosome 2 in the mouse. Dev. Genet. 21, 55-60.
35. Lelongt, B., Bengatta, S., Delauche, M., Lund, L. R., Werb, Z. and Ronco, P. M. (2001). Matrix metalloproteinase 9 protects mice from anti-glomerular basement membrane nephritis through its fibrinolytic activity. J. Exp. Med. 193, 793-802.
36. Liu, Z., Li, N., Diaz, L. A., Shipley, M., Senior, R. M. and Werb, Z. (2005). Synergy between a plasminogen cascade and MMP-9 in autoimmune disease. J. Clin. Invest. 115, 879-887. (Pubitemid 40489392)
37. Lopez-Otin, C. and Matrisian, L. M. (2007). Emerging roles of proteases in tumour suppression. Nat. Rev. Cancer 7, 800-808.
38. Lund, L. R., Rømer, J., Bugge, T. H., Nielsen, B. S., Frandsen, T. L., Degen, J. L., Stephens, R. W. and Danø, K. (1999). Functional overlap between two classes of matrix-degrading proteases in wound healing. EMBO J. 18, 4645-4656. (Pubitemid 29415519)
39. Lund, L. R., Green, K. A., Stoop, A. A., Ploug, M., Almholt, K., Lilla, J., Nielsen, B. S., Christensen, I. J., Craik, C. S., Werb, Z. et al. (2006). Plasminogen activation independent of uPA and tPA maintains wound healing in gene-deficient mice. EMBO J. 25, 2686-2697. (Pubitemid 43980377)
40. Mohan, R., Chintala, S. K., Jung, J. C., Villar, W. V., McCabe, F., Russo, L. A., Lee, Y., McCarthy, B. E., Wollenberg, K. R., Jester, J. V. et al. (2002). Matrix metalloproteinase gelatinase B (MMP-9) coordinates and effects epithelial regeneration. J. Biol. Chem. 277, 2065-2072. (Pubitemid 34968789)
41. Odaka, C., Tanioka, M. and Itoh, T. (2005). Matrix metalloproteinase-9 in macrophages induces thymic neovascularization following thymocyte apoptosis. J. Immunol. 174, 846-853. (Pubitemid 40094279)
42. Page-McCaw, A., Ewald, A. J. and Werb, Z. (2007). Matrix metalloproteinases and the regulation of tissue remodelling. Nat. Rev. Mol. Cell Biol. 8, 221-233.
43. Pyo, R., Lee, J. K., Shipley, J. M., Curci, J. A., Mao, D., Ziporin, S. J., Ennis, T. L., Shapiro, S. D., Senior, R. M. and Thompson, R. W. (2000). Targeted gene disruption of matrix metalloproteinase-9 (gelatinase B) suppresses development of experimental abdominal aortic aneurysms. J. Clin. Invest. 105, 1641-1649.
44. Rasch, M. G., Lund, I. K., Illemann, M., Høyer-Hansen, G. and Gårdsvoll, H. (2010). Purification and characterization of recombinant full-length and protease domain of murine MMP-9 expressed in Drosophila S2 cells. Protein Expr. Purif. 72, 87-94.
45. Rivier, C., Chizzonite, R. and Vale, W. (1989). In the mouse, the activation of the hypothalamic-pituitary-adrenal axis by a lipopolysaccharide (endotoxin) is mediated through interleukin-1. Endocrinology 125, 2800-2805. (Pubitemid 20010650)
46. Rømer, J., Bugge, T. H., Pyke, C., Lund, L. R., Flick, M. J., Degen, J. L. and Danø, K. (1996). Plasminogen and wound healing. Nat. Med. 2, 725.
47. Santana, A., Medina, C., Paz-Cabrera, M. C., Diaz-Gonzalez, F., Farre, E., Salas, A., Radomski, M. W. and Quintero, E. (2006). Attenuation of dextran sodium sulphate induced colitis in matrix metalloproteinase-9 deficient mice. World J. Gastroenterol. 12, 6464-6472. (Pubitemid 44742583)
48. Sappino, A. P., Huarte, J., Belin, D. and Vassalli, J. D. (1989). Plasminogen activators in tissue remodeling and invasion: mRNA localization in mouse ovaries and implanting embryos. J. Cell Biol. 109, 2471-2479.
49. Sato, Y. and Rifkin, D. B. (1989). Inhibition of endothelial cell movement by pericytes and smooth muscle cells: activation of a latent transforming growth factor-beta 1-like molecule by plasmin during co-culture. J. Cell Biol. 109, 309-315.
50. Savino, W., Mendes-Da-Cruz, D. A., Smaniotto, S., Silva-Monteiro, E. and Villa-Verde, D. M. (2004). Molecular mechanisms governing thymocyte migration: combined role of chemokines and extracellular matrix. J. Leukoc. Biol. 75, 951-961.
51. Schafer, M. and Werner, S. (2008). Cancer as an overhealing wound: an old hypothesis revisited. Nat. Rev. Mol. Cell Biol. 9, 628-638.
52. Singh, B., Mortensen, N. J. and Warren, B. F. (2007). Histopathological mimicry in mucosal prolapse. Histopathology 50, 97-102.
53. Sinnamon, M, J., Carter, K. J., Sims, L. P., Lafleur, B., Fingleton, B. and Matrisian, L. M. (2008). A protective role of mast cells in intestinal tumorigenesis. Carcinogenesis 29, 880-886.
54. Solberg, H., Rinkenberger, J., Danø, K., Werb, Z. and Lund, L. R. (2003). A functional overlap of plasminogen and MMPs regulates vascularization during placental development. Development 130, 4439-4450.
55. Sternlicht, M. D. and Werb, Z. (2001). How matrix metalloproteinases regulate cell behavior. Annu. Rev. Cell Dev. Biol. 17, 463-516. (Pubitemid 33096184)
56. Teesalu, T., Blasi, F. and Talarico, D. (1996). Embryo implantation in mouse: fetomaternal coordination in the pattern of expression of uPA, uPAR, PAI-1 and alpha 2MR/LRP genes. Mech. Dev. 56, 103-116.
57. Teesalu, T., Masson, R., Basset, P., Blasi, F. and Talarico, D. (1999). Expression of matrix metalloproteinases during murine chorioallantoic placenta maturation. Dev. Dyn. 214, 248-258. (Pubitemid 29117585)
58. Vu, T. H., Shipley, J. M., Bergers, G., Berger, J. E., Helms, J. A., Hanahan, D., Shapiro, S. D., Senior, R. M. and Werb, Z. (1998). MMP-9/gelatinase B is a key regulator of growth plate angiogenesis and apoptosis of hypertrophic chondrocytes. Cell 93, 411-422. (Pubitemid 28232085)
59. Warren, B. F., Dankwa, E. K. and Davies, J. D. (1990). 'Diamond-shaped' crypts and mucosal elastin: helpful diagnostic features in biopsies of rectal prolapse. Histopathology 17, 129-134. (Pubitemid 20258636)
60. Yoon, H. K., Cho, H. Y. and Kleeberger, S. R. (2007). Protective role of matrix metalloproteinase-9 in ozone-induced airway inflammation. Environ. Health Perspect. 115, 1557-1563.
61. Yu, Q. and Stamenkovic, I. (2000). Cell surface-localized matrix metalloproteinase-9 proteolytically activates TGF-beta and promotes tumor invasion and angiogenesis. Genes Dev. 14, 163-176. (Pubitemid 30070982)
62. Zuckerman, S. H., Shellhaas, J. and Butler, L. D. (1989). Differential regulation of lipopolysaccharide-induced interleukin 1 and tumor necrosis factor synthesis: effects of endogenous and exogenous glucocorticoids and the role of the pituitary-adrenal axis. Eur. J. Immunol. 19, 301-305.