Lack of MMP10 exacerbates experimental colitis and promotes development of inflammation-associated colonic dysplasia

Laboratory Investigation

Volumn 92, Issue 12, 2012, Pages 1749-1759

  Koller, Felicitas L ^a   Dozier, E Ashley ^a   Nam, Ki Taek ^a   Swee, Mei ^b   Birkland, Timothy P ^b   Parks, William C ^b   Fingleton, Barbara ^a  

^a VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF WASHINGTON   (United States)

Author keywords

bone marrow derived cells; cancer; colitis; protease; resolution

Indexed keywords

DEXTRAN SULFATE; STROMELYSIN 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; COLITIS; COLON DISEASE; COLONIC DYSPLASIA; CONTROLLED STUDY; DISEASE COURSE; DISEASE EXACERBATION; DISEASE SEVERITY; FEMALE; HUMAN; HUMAN CELL; INFLAMMATION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; TISSUE INJURY;

ANIMALS; BONE MARROW; BONE MARROW TRANSPLANTATION; CELL LINE; COLITIS, ULCERATIVE; COLON; CYTOKINES; DEXTRAN SULFATE; DISEASE MODELS, ANIMAL; FEMALE; HISTOCYTOCHEMISTRY; HUMANS; INFLAMMATORY BOWEL DISEASES; LEUKOCYTES; MALE; MATRIX METALLOPROTEINASE 10; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 84870429871     PISSN: 00236837     EISSN: 15300307     Source Type: Journal    
DOI: 10.1038/labinvest.2012.141     Document Type: Article

References (47)

1. Osterman MT, Lichtenstein GR. Chapter 112-ulcerative colitis. In: Feldman M, Friedman LS, Brandt LJ (eds) Sleisenger's and Fordtran's Gastrointestinal and Liver Disease. 9th edn. (, Philadelphia, PA, 2010) pp1982.
2. Itzkowitz SH, Yio X. Inflammation and cancer IV. Colorectal cancer in inflammatory bowel disease: the role of inflammation. Am J Physiol Gastrointest Liver Physiol 2004;287:G7-17.
3. Sandborn WJ, Loftus EV. Balancing the risks and benefits of infliximab in the treatment of inflammatory bowel disease. Gut 2004;53:780-782.
4. Ng SC, Kamm MA. Therapeutic strategies for the management of ulcerative colitis. Inflamm Bowel Dis 2009;15:935-950.
5. Baugh MD, Perry MJ, Hollander AP, et al. Matrix metalloproteinase levels are elevated in inflammatory bowel disease. Gastroenterology 1999;117:814-822.
6. von Lampe B, Barthel B, Coupland SE, et al. Differential expression of matrix metalloproteinases and their tissue inhibitors in colon mucosa of patients with inflammatory bowel disease. Gut 2000;47:63-73.
7. Matsuno K, Adachi Y, Yamamoto H, et al. The expression of matrix metalloproteinase matrilysin indicates the degree of inflammation in ulcerative colitis. J Gastroenterol 2003;38:348-354.
8. Vaalamo M, Karjalainen-Lindsberg ML, Puolakkainen P, et al. Distinct expression profiles of stromelysin-2 (MMP-10), collagenase-3 (MMP-13), macrophage metalloelastase (MMP-12), and tissue inhibitor of metalloproteinases-3 (TIMP-3) in intestinal ulcerations. Am J Pathol 1998;152:1005-1014.
9. Saarialho-Kere UK, Vaalamo M, Puolakkainen P, et al. Enhanced expression of matrilysin, collagenase, and stromelysin-1 in gastrointestinal ulcers. Am J Pathol 1996;148:519-526.
10. Di Sebastiano P, di Mola FF, Artese L, et al. Beneficial effects of Batimastat (BB-94), a matrix metalloproteinase inhibitor, in rat experimental colitis. Digestion 2001;63:234-239.
11. Sykes AP, Bhogal R, Brampton C, et al. The effect of an inhibitor of matrix metalloproteinases on colonic inflammation in a trinitroben-zenesulphonic acid rat model of inflammatory bowel disease. Aliment Pharmacol Ther 1999;13:1535-1542.
12. Coussens LM, Fingleton B, Matrisian LM. Matrix metalloproteinase inhibitors and cancer: trials and tribulations. Science 2002;295: 2387-2392.
13. Egeblad M, Werb Z. New functions for the matrix metalloproteinases in cancer progression. Nat Rev Cancer 2002;2:161-174.
14. Parks WC, Wilson CL, Lopez-Boado YS. Matrix metalloproteinases as modulators of inflammation and innate immunity. Nat Rev Immunol 2004;4:617-629.
15. Mähler M, Bristol IJ, Leiter EH, et al. Differential susceptibility of inbred mouse strains to dextran sulfate sodium-induced colitis. Am J Physiol 1998;274:G544-G551.
16. Gack S, Vallon R, Schmidt J, et al. Expression of interstitial collagenase during skeletal development of the mouse is restricted to osteoblast-like cells and hypertrophic chondrocytes. Cell Growth Differ 1995;6: 759-767.
17. Swee M, Wilson CL, Wang Y, et al. Matrix metalloproteinase-7 (matrilysin) controls neutrophil egress by generating chemokine gradients. J Leukoc Biol 2008;83:1404-1412.
18. Salmela MT, Pender SL, Karjalainen-Lindsberg ML, et al. Collagenase-1 (MMP-1), matrilysin-1 (MMP-7), and stromelysin-2 (MMP-10) are expressed by migrating enterocytes during intestinal wound healing. Scand J Gastroenterol 2004;39:1095-1104.
19. Kuhn R, Lohler J, Rennick D, et al. Interleukin-10-deficient mice develop chronic enterocolitis. Cell 1993;75:263-274.
20. Kassim SY, Gharib SA, Mecham BH, et al. Individual matrix metalloproteinases control distinct transcriptional responses in airway epithelial cells infected with Pseudomonas aeruginosa. Infect Immun 2007;75:5640-5650.
21. Garg P, Rojas M, Ravi A, et al. Selective ablation of matrix metallopro-teinase-2 exacerbates experimental colitis: contrasting role of gelatinases in the pathogenesis of colitis. J Immunol 2006;177:4103-4112.
22. Wang Y, Wang YP, Zheng G, et al. Ex vivo programmed macrophages ameliorate experimental chronic inflammatory renal disease. Kidney Int 2007;72:290-299.
23. Zaynagetdinov R, Sherrill TP, Polosukhin VV, et al. A critical role for macrophages in promotion of urethane-induced lung carcinogenesis. J Immunol 2011;187:5703-5711.
24. Clapper ML, Cooper HS, Chang WC. Dextran sulfate sodium-induced colitis-associated neoplasia: a promising model for the development of chemopreventive interventions. Acta Pharmacol Sin 2007;28:1450-1459.
25. Kim HS, Berstad A. Experimental colitis in animal models. Scand J Gastroenterol 1992;27:529-537.
26. te Velde AA, Verstege MI, Hommes DW. Critical appraisal of the current practice in murine TNBS-induced colitis. Inflamm Bowel Dis 2006;12:995-999.
27. Perse M, Cerar A. Dextran sodium sulphate colitis mouse model: traps and tricks. J Biomed Biotech 2012;2012:718617.
28. Laroui H, Ingersoll SA, Liu HC, et al. Dextran sodium sulfate (DSS) induces colitis in mice by forming nano-lipocomplexes with medium-chain-length fatty acids in the colon. PLoS One 2012;7:e32084.
29. van den Berg TK, Kraal G. A function for the macrophage F4/80 molecule in tolerance induction. Trends Immunol 2005;26:506-509.
30. Medina C, Santana A, Llopis M, et al. Induction of colonic transmural inflammation by Bacteroides fragilis: implication of matrix metalloproteinases. Inflamm Bowel Dis 2005;11:99-105.
31. Medina C, Santana A, Paz MC, et al. Matrix metalloproteinase-9 modulates intestinal injury in rats with transmural colitis. J Leukoc Biol 2006;79:954-962.
32. Medina C, Santana A, Paz-Cabrera MC, et al. Increased activity and expression of gelatinases in ischemic colitis. Dig Dis Sci 2006;51:2393-2399.
33. Naito Y, Yoshikawa T. Role of matrix metalloproteinases in inflammatory bowel disease. Mol Aspects Med 2005;26:379-390.
34. Kobayashi K, Arimura Y, Goto A, et al. Therapeutic implications of the specific inhibition of causative matrix metalloproteinases in experimental colitis induced by dextran sulphate sodium. J Pathol 2006;209: 376-383.
35. Gill SE, Kassim SY, Birkland TP, et al. Mouse models of MMP and TIMP function. Methods Mol Biol 2010;622:31-52.
36. Overall CM, Kleifeld O. Tumour microenvironment-opinion: validating matrix metalloproteinases as drug targets and anti-targets for cancer therapy. Nat Rev Cancer 2006;6:227-239.
37. Martin MD, Matrisian LM. The other side of MMPs: protective roles in tumor progression. Cancer Metastasis Rev 2007;26:717-724.
38. Sinnamon MJ, Carter KJ, Sims LP, et al. A protective role of mast cells in intestinal tumorigenesis. Carcinogenesis 2008;29:880-886.
39. Sabates-Bellver J, Van der Flier LG, de Palo M, et al. Transcriptome profile of human colorectal adenomas. Mol Cancer Res 2007;5:1263-1275.
40. Li O, Park PW, Wilson CL, et al. Matrilysin shedding of syndecan-1 regulates chemokine mobilization and transepithelial efflux of neutrophils in acute lung injury. Cell 2002;111:635-646.
41. Corry DB, Rishi K, Kanellis J, et al. Decreased allergic lung inflammatory cell egression and increased susceptibility to asphyxiation in MMP2-deficiency. Nat Immunol 2002;3:347-353.
42. Qualls JE, Kaplan AM, van Rooijen N, et al. Suppression of experimental colitis by intestinal mononuclear phagocytes. J Leukoc Biol 2006;80:802-815.
43. Medina-Contreras O, Geem D, Laur O, et al. CX3CR1 regulates intestinal macrophage homeostasis, bacterial translocation, and colitogenic Th17 responses in mice. J Clin Invest 2011;121:4787-4795.
44. Pull SL, Doherty JM, Mills JC, et al. Activated macrophages are an adaptive element of the colonic epithelial progenitor niche necessary for regenerative responses to injury. Proc Natl Acad Sci USA 2005; 102:99-104.
45. Seno H, Miyoshi H, Brown SL, et al. Efficient colonic mucosal wound repair requires Trem2 signaling. Proc Natl Acad Sci USA 2009;106:256-261.
46. Rizzo A, Monteleone I, Fina D, et al. Inhibition of colitis by IL-25 associates with induction of alternatively activated macrophages. Inflamm Bowel Dis 2012;18:449-459.
47. Weisser SB, Brugger HK, Voglmaier NS, et al. SHIP-deficient, alternatively activated macrophages protect mice during DSS-induced colitis. J Leukoc Biol 2011;90:483-492.