Skip to main content
Top
Published in: Digestive Diseases and Sciences 10/2006

01-10-2006 | Original Paper

Increased Protein Expression of Matrix Metalloproteinases -1, -3, and -9 and TIMP-1 in Patients with Gluten-Sensitive Enteropathy

Authors: Bashir M. Mohamed, Conleth Feighery, Jacinta Kelly, Christian Coates, Una O’Shea, Louise Barnes, Mohamed Abuzakouk

Published in: Digestive Diseases and Sciences | Issue 10/2006

Login to get access

Abstract

Gluten-sensitive enteropathy is characterized by small intestinal damage. The pathogenic mechanisms involved are not precisely understood. There is recent interest in the possibility that matrix metalloproteinases might play a pathogenic role. Using immunohistochemistry technique, we examined the protein expression of matrix metalloproteinases-1, -3, and -9 and the tissue inhibitor metalloproteinase-1 in duodenal biopsies from 30 patients with celiac disease and dermatitis herpetiformis. We demonstrated that the percentage of cells expressing these enzymes and their inhibitor in all patients was significantly greater than in the normal controls (P < 0.0001). This was evident even in patients with a minimal lesion but was most marked in patients with severe damage, mirroring the degree of inflammation in the small intestinal tissue. The increased expression of these enzymes and their inhibitor in the duodenal mucosa of patients with gluten-sensitive enteropathy suggests a role for these enzymes in the tissue remodeling which is a feature of these disorders.
Literature
2.
go back to reference Savilahti E, Reunala T, Maki M (1992) Increase of lymphocytes bearing the gamma/delta T cell receptor in the jejunum of patients with dermatitis herpetiformis. Gut 33:206–211PubMed Savilahti E, Reunala T, Maki M (1992) Increase of lymphocytes bearing the gamma/delta T cell receptor in the jejunum of patients with dermatitis herpetiformis. Gut 33:206–211PubMed
4.
go back to reference Kilmartin C, Lynch S, Abuzakouk M, et al. (2003) Avenin fails to induce a Th1 response in coeliac tissue following in vitro culture. Gut 52:47–52PubMedCrossRef Kilmartin C, Lynch S, Abuzakouk M, et al. (2003) Avenin fails to induce a Th1 response in coeliac tissue following in vitro culture. Gut 52:47–52PubMedCrossRef
5.
go back to reference Forsberg G, Hernell O, Melgar S, Israelsson A, Hammarstrom S, Hammarstrom ML (2002) Paradoxical coexpression of proinflammatory and down-regulatory cytokines in intestinal T cells in childhood celiac disease. Gastroenterology 123:667–678PubMedCrossRef Forsberg G, Hernell O, Melgar S, Israelsson A, Hammarstrom S, Hammarstrom ML (2002) Paradoxical coexpression of proinflammatory and down-regulatory cytokines in intestinal T cells in childhood celiac disease. Gastroenterology 123:667–678PubMedCrossRef
6.
go back to reference Daum S, Bauer U, Foss HD, et al. (1999) Increased expression of mRNA for matrix metalloproteinases-1 and -3 and tissue inhibitor of metalloproteinases-1 in intestinal biopsy specimens from patients with coeliac disease. Gut 44:17–25PubMedCrossRef Daum S, Bauer U, Foss HD, et al. (1999) Increased expression of mRNA for matrix metalloproteinases-1 and -3 and tissue inhibitor of metalloproteinases-1 in intestinal biopsy specimens from patients with coeliac disease. Gut 44:17–25PubMedCrossRef
7.
go back to reference Salmela MT, Pender SL, Reunala T, MacDonald TT, Saarialho-Kere U (2001) Parallel expression of macrophage metalloelastase (MMP-12) in duodenal and skin lesions of patients with dermatitis herpetiformis. Gut 48:496–502PubMedCrossRef Salmela MT, Pender SL, Reunala T, MacDonald TT, Saarialho-Kere U (2001) Parallel expression of macrophage metalloelastase (MMP-12) in duodenal and skin lesions of patients with dermatitis herpetiformis. Gut 48:496–502PubMedCrossRef
8.
go back to reference Ciccocioppo R, Sabatino AD, Bauer M, et al. (2005) Matrix metalloproteinase pattern in celiac duodenal mucosa. Lab Invest 85:397–407PubMedCrossRef Ciccocioppo R, Sabatino AD, Bauer M, et al. (2005) Matrix metalloproteinase pattern in celiac duodenal mucosa. Lab Invest 85:397–407PubMedCrossRef
9.
go back to reference Khasigov PZ, Podobed OV, Ktzoeva SA, et al. (2001) Matrix metalloproteinases of normal human tissues. Biochemistry (Mosc) 66:130–140CrossRef Khasigov PZ, Podobed OV, Ktzoeva SA, et al. (2001) Matrix metalloproteinases of normal human tissues. Biochemistry (Mosc) 66:130–140CrossRef
10.
11.
go back to reference Goetzl EJ, Banda MJ, Leppert D (1996) Matrix metalloproteinases in immunity. J Immunol 156:1–4PubMed Goetzl EJ, Banda MJ, Leppert D (1996) Matrix metalloproteinases in immunity. J Immunol 156:1–4PubMed
12.
go back to reference Salmela MT, Pender SL, Karjalainen-Lindsberg ML, Puolakkainen P, Macdonald TT, Saarialho-Kere U (2004) 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 39:1095–1104PubMedCrossRef Salmela MT, Pender SL, Karjalainen-Lindsberg ML, Puolakkainen P, Macdonald TT, Saarialho-Kere U (2004) 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 39:1095–1104PubMedCrossRef
13.
go back to reference Kirkegaard T, Hansen A, Bruun E, Brynskov J (2004) Expression and localisation of matrix metalloproteinases and their natural inhibitors in fistulae of patients with Crohn’s disease. Gut 53:701–709PubMedCrossRef Kirkegaard T, Hansen A, Bruun E, Brynskov J (2004) Expression and localisation of matrix metalloproteinases and their natural inhibitors in fistulae of patients with Crohn’s disease. Gut 53:701–709PubMedCrossRef
14.
go back to reference de Coignac AB, Elson G, Delneste Y, et al. (2000) Cloning of MMP-26, a novel matrilysin-like proteinase. Eur J Biochem 267:3323–3329PubMedCrossRef de Coignac AB, Elson G, Delneste Y, et al. (2000) Cloning of MMP-26, a novel matrilysin-like proteinase. Eur J Biochem 267:3323–3329PubMedCrossRef
15.
go back to reference Grant GM, Giambernardi TA, Grant AM, et al. (1999) Overview of expression of matrix metalloproteinases (MMP-17, MMP-18, and MMP-20) in cultured human cells. Matrix Biol 18:145–148PubMedCrossRef Grant GM, Giambernardi TA, Grant AM, et al. (1999) Overview of expression of matrix metalloproteinases (MMP-17, MMP-18, and MMP-20) in cultured human cells. Matrix Biol 18:145–148PubMedCrossRef
16.
go back to reference Welgus HG, Fliszar CJ, Seltzer JL, et al. (1990) Differential susceptibility of type X collagen to cleavage by two mammalian interstitial collagenases and 72-kDa type IV collagenase. J Biol Chem 265:13521–13527PubMed Welgus HG, Fliszar CJ, Seltzer JL, et al. (1990) Differential susceptibility of type X collagen to cleavage by two mammalian interstitial collagenases and 72-kDa type IV collagenase. J Biol Chem 265:13521–13527PubMed
17.
go back to reference Welgus HG, Jeffrey JJ, Eisen AZ (1981) The collagen substrate specificity of human skin fibroblast collagenase. J Biol Chem 256:9511–9515PubMed Welgus HG, Jeffrey JJ, Eisen AZ (1981) The collagen substrate specificity of human skin fibroblast collagenase. J Biol Chem 256:9511–9515PubMed
18.
go back to reference Salmela MT, MacDonald TT, Black D, et al. (2002) Upregulation of matrix metalloproteinases in a model of T cell mediated tissue injury in the gut: analysis by gene array and in situ hybridisation. Gut 51:540–547PubMedCrossRef Salmela MT, MacDonald TT, Black D, et al. (2002) Upregulation of matrix metalloproteinases in a model of T cell mediated tissue injury in the gut: analysis by gene array and in situ hybridisation. Gut 51:540–547PubMedCrossRef
19.
go back to reference von Lampe B, Barthel B, Coupland SE, et al. (2000) Differential expression of matrix metalloproteinases and their tissue inhibitors in colon mucosa of patients with inflammatory bowel disease. Gut 47:63–73PubMedCrossRef von Lampe B, Barthel B, Coupland SE, et al. (2000) Differential expression of matrix metalloproteinases and their tissue inhibitors in colon mucosa of patients with inflammatory bowel disease. Gut 47:63–73PubMedCrossRef
20.
go back to reference Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477:267–283PubMed Brew K, Dinakarpandian D, Nagase H (2000) Tissue inhibitors of metalloproteinases: evolution, structure and function. Biochim Biophys Acta 1477:267–283PubMed
21.
go back to reference Gomez DE, Alonso DF, Yoshiji H, et al. (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 74:111–122PubMed Gomez DE, Alonso DF, Yoshiji H, et al. (1997) Tissue inhibitors of metalloproteinases: structure, regulation and biological functions. Eur J Cell Biol 74:111–122PubMed
22.
go back to reference Pender SL, Tickle SP, Docherty AJ, Howie D, Wathen NC, MacDonald TT (1997) A major role for matrix metalloproteinases in T cell injury in the gut. J Immunol 158:1582–1590PubMed Pender SL, Tickle SP, Docherty AJ, Howie D, Wathen NC, MacDonald TT (1997) A major role for matrix metalloproteinases in T cell injury in the gut. J Immunol 158:1582–1590PubMed
23.
go back to reference Bailey CJ, Hembry RM, Alexander A, et al. (1994) Distribution of the matrix metalloproteinases stromelysin, gelatinases A and B, and collagenase in Crohn’s disease and normal intestine. J Clin Pathol 47:113–116PubMed Bailey CJ, Hembry RM, Alexander A, et al. (1994) Distribution of the matrix metalloproteinases stromelysin, gelatinases A and B, and collagenase in Crohn’s disease and normal intestine. J Clin Pathol 47:113–116PubMed
24.
go back to reference Kontakou M, Przemioslo RT, Sturgess RP, et al. (1995) Cytokine mRNA expression in the mucosa of treated coeliac patients after wheat peptide challenge. Gut 37:52–57PubMed Kontakou M, Przemioslo RT, Sturgess RP, et al. (1995) Cytokine mRNA expression in the mucosa of treated coeliac patients after wheat peptide challenge. Gut 37:52–57PubMed
25.
go back to reference Pender SL, MacDonald TT (1998) Regulation of matrix metalloproteinase production in human fetal intestinal mesenchymal cells by cytokines and the bacterial superantigen Staphylococcus aureus enterotoxin B. Ann NY Acad Sci 859:188–191PubMedCrossRef Pender SL, MacDonald TT (1998) Regulation of matrix metalloproteinase production in human fetal intestinal mesenchymal cells by cytokines and the bacterial superantigen Staphylococcus aureus enterotoxin B. Ann NY Acad Sci 859:188–191PubMedCrossRef
26.
go back to reference Heuschkel RB, MacDonald TT, Monteleone G, et al. (2000) Imbalance of stromelysin-1 and TIMP-1 in the mucosal lesions of children with inflammatory bowel disease. Gut 47:57–62PubMedCrossRef Heuschkel RB, MacDonald TT, Monteleone G, et al. (2000) Imbalance of stromelysin-1 and TIMP-1 in the mucosal lesions of children with inflammatory bowel disease. Gut 47:57–62PubMedCrossRef
27.
go back to reference Yoshihara Y, Nakamura H, Obata K, et al. (2000) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis. Ann Rheum Dis 59:455–461PubMedCrossRef Yoshihara Y, Nakamura H, Obata K, et al. (2000) Matrix metalloproteinases and tissue inhibitors of metalloproteinases in synovial fluids from patients with rheumatoid arthritis or osteoarthritis. Ann Rheum Dis 59:455–461PubMedCrossRef
28.
go back to reference Klimiuk PA, Sierakowski S, Latosiewicz R, Cylwik B, Skowronski J, Chwiecko J (2000) Serum matrix metalloproteinases and tissue inhibitors of metalloproteinases in different histological variants of rheumatoid synovitis. Rheumatology (Oxford) 41:78–87CrossRef Klimiuk PA, Sierakowski S, Latosiewicz R, Cylwik B, Skowronski J, Chwiecko J (2000) Serum matrix metalloproteinases and tissue inhibitors of metalloproteinases in different histological variants of rheumatoid synovitis. Rheumatology (Oxford) 41:78–87CrossRef
29.
go back to reference Zhang S, Li L, Lin JY, Lin H (2003) Imbalance between expression of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in invasiveness and metastasis of human gastric carcinoma. World J Gastroenterol 9:899–904PubMed Zhang S, Li L, Lin JY, Lin H (2003) Imbalance between expression of matrix metalloproteinase-9 and tissue inhibitor of metalloproteinase-1 in invasiveness and metastasis of human gastric carcinoma. World J Gastroenterol 9:899–904PubMed
30.
go back to reference Murray GI, Duncan ME, Arbuckle E, et al. (1998) Matrix metalloproteinases and their inhibitors in gastric cancer. Gut 43:791–797PubMedCrossRef Murray GI, Duncan ME, Arbuckle E, et al. (1998) Matrix metalloproteinases and their inhibitors in gastric cancer. Gut 43:791–797PubMedCrossRef
31.
go back to reference Stallmach A, Chan CC, Ecker KW, et al. (2000) Comparable expression of matrix metalloproteinases 1 and 2 in pouchitis and ulcerative colitis. Gut 47:415–422PubMedCrossRef Stallmach A, Chan CC, Ecker KW, et al. (2000) Comparable expression of matrix metalloproteinases 1 and 2 in pouchitis and ulcerative colitis. Gut 47:415–422PubMedCrossRef
32.
go back to reference Louis E, Ribbens C, Godon A, et al. (2000) Increased production of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinase-1 by inflamed mucosa in inflammatory bowel disease. Clin Exp Immunol 120:241–246PubMedCrossRef Louis E, Ribbens C, Godon A, et al. (2000) Increased production of matrix metalloproteinase-3 and tissue inhibitor of metalloproteinase-1 by inflamed mucosa in inflammatory bowel disease. Clin Exp Immunol 120:241–246PubMedCrossRef
33.
go back to reference Wiercinska-Drapalo A, Jaroszewicz J, Flisiak R, Prokopowicz D (2003) Plasma matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 as biomarkers of ulcerative colitis activity. World J Gastroenterol 9:2843–2845PubMed Wiercinska-Drapalo A, Jaroszewicz J, Flisiak R, Prokopowicz D (2003) Plasma matrix metalloproteinase-1 and tissue inhibitor of metalloproteinase-1 as biomarkers of ulcerative colitis activity. World J Gastroenterol 9:2843–2845PubMed
34.
go back to reference Bamba S, Andoh A, Yasui H, Araki Y, Bamba T, Fujiyama Y (2003) Matrix metalloproteinase-3 secretion from human colonic subepithelial myofibroblasts: role of interleukin-17. J Gastroenterol 38:548–554PubMed Bamba S, Andoh A, Yasui H, Araki Y, Bamba T, Fujiyama Y (2003) Matrix metalloproteinase-3 secretion from human colonic subepithelial myofibroblasts: role of interleukin-17. J Gastroenterol 38:548–554PubMed
Metadata
Title
Increased Protein Expression of Matrix Metalloproteinases -1, -3, and -9 and TIMP-1 in Patients with Gluten-Sensitive Enteropathy
Authors
Bashir M. Mohamed
Conleth Feighery
Jacinta Kelly
Christian Coates
Una O’Shea
Louise Barnes
Mohamed Abuzakouk
Publication date
01-10-2006
Published in
Digestive Diseases and Sciences / Issue 10/2006
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-005-9038-4

Other articles of this Issue 10/2006

Digestive Diseases and Sciences 10/2006 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.