Compartmentalised expression of meprin in small intestinal mucosa: enhanced expression in lamina propria in coeliac disease
-
Daniel Lottaz
, Caroline Buri , Giovanni Monteleone , Sandra Rösmann , Thomas T. MacDonald , Ian R. Sanderson and Erwin E. Sterchi
Abstract
Epithelial cells in the human small intestine express meprin, an astacin-like metalloprotease, which accumulates normally at the brush border membrane and in the gut lumen. Therefore, meprin is targeted towards luminal components. In coeliac disease patients, peptides from ingested cereals trigger mucosal inflammation in the small intestine, disrupting epithelial cell differentiation and function. Using in situ hybridisation on duodenal tissue sections, we observed a marked shift of meprin mRNA expression from epithelial cells, the predominant expression site in normal mucosa, to lamina propria leukocytes in coeliac disease. Meprin thereby gains access to the substrate repertoire present beneath the epithelium.
References
Becker, C., Kruse, M.N., Slotty, K.A., Köhler, D., Harris, J.R., Rösmann, S., Sterchi, E.E., and Stöcker, W. (2003). Differences in the activation mechanism between the α and β subunits of human meprin. Biol. Chem.384, 825–831.10.1515/BC.2003.092Search in Google Scholar
Bertenshaw, G.P., Turk, B.E., Hubbard, S.J., Matters, G.L., Bylander, J.E., Crisman, J.M., Cantley, L.C., and Bond, J.S. (2001). Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. J. Biol. Chem.276, 13248–13255.10.1074/jbc.M011414200Search in Google Scholar
Bertenshaw, G.P., Norcum, M.T., and Bond, J.S. (2003). Structure of homo- and hetero-oligomeric meprin metalloproteases. Dimers, tetramers, and high molecular mass multimers. J. Biol. Chem.278, 2522–2532.10.1074/jbc.M208808200Search in Google Scholar
Crisman, J.M., Zhang, B., Norman, L.P., and Bond, J.S. (2004). Deletion of the mouse meprin beta metalloprotease gene diminishes the ability of leukocytes to disseminate through extracellular matrix. J. Immunol.172, 4510–4519.10.4049/jimmunol.172.7.4510Search in Google Scholar
Daum, S., Bauer, U., Foss, H.D., Schuppan, D., Stein, H., Riecken, E.O., and Ullrich, R. (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. Gut44, 17–25.10.1136/gut.44.1.17Search in Google Scholar
Dumermuth, E., Sterchi, E.E., Jiang, W.P., Wolz, R.L., Bond, J.S., Flannery, A.V., and Beynon, R.J. (1991). The astacin family of metalloendopeptidases. J. Biol. Chem.266, 21381–21385.10.1016/S0021-9258(18)54648-2Search in Google Scholar
Dunnill, M.S. and Whitehead, R. (1972). A method for the quantitation of small intestinal biopsy specimens. J. Clin. Pathol.25, 243–246.10.1136/jcp.25.3.243Search in Google Scholar
Eldering, J.A., Grünberg, J., Hahn, D., Croes, H.J., Fransen, J.A., and Sterchi, E.E. (1997). Polarised expression of human intestinal N-benzoyl-l-tyrosyl-p-aminobenzoic acid hydrolase (human meprin) α and β subunits in Madin-Darby canine kidney cells. Eur. J. Biochem.247, 920–932.10.1111/j.1432-1033.1997.00920.xSearch in Google Scholar
Fais, S., Maiuri, L., Pallone, F., De Vincenzi, M., De Ritis, G., Troncone, R., and Auricchio, S. (1992). Gliadin induced changes in the expression of MHC-class II antigens by human small intestinal epithelium. Organ culture studies with coeliac disease mucosa. Gut33, 472–475.Search in Google Scholar
Grünberg, J., Dumermuth, E., Eldering, J.A., and Sterchi, E.E. (1993). Expression of the α subunit of PABA peptide hydrolase (EC 3.4.24.18) in MDCK cells. Synthesis and secretion of an enzymatically inactive homodimer. FEBS Lett.335, 376–379.Search in Google Scholar
Halstensen, T.S. and Brandtzaeg, P. (1993). Activated T lymphocytes in the celiac lesion: non-proliferative activation (CD25) of CD4+α/β cells in the lamina propria but proliferation (Ki- 67) of α/β and γ/δ cells in the epithelium. Eur. J. Immunol.23, 505–510.10.1002/eji.1830230231Search in Google Scholar
Henning, S.J., Oesterreicher, T.J., Osterholm, D.E., Lottaz, D., Hahn, D., and Sterchi, E.E. (1999). Meprin mRNA in rat intestine during normal and glucocorticoid-induced maturation: divergent patterns of expression of α and β subunits. FEBS Lett.462, 368–372.10.1016/S0014-5793(99)01558-6Search in Google Scholar
Herzog, C., Kaushal, G.P., and Haun, R.S. (2005). Generation of biologically active interleukin-1β by meprin B. Cytokine31, 394–403.10.1016/j.cyto.2005.06.012Search in Google Scholar
Jabri, B., de Serre, N.P., Cellier, C., Evans, K., Gache, C., Carvalho, C., Mougenot, J.F., Allez, M., Jian, R., Desreumaux, P., et al. (2000). Selective expansion of intraepithelial lymphocytes expressing the HLA-E-specific natural killer receptor CD94 in celiac disease. Gastroenterology118, 867–879.10.1016/S0016-5085(00)70173-9Search in Google Scholar
Kaushal, G.P., Walker, P.D., and Shah, S.V. (1994). An old enzyme with a new function: purification and characterization of a distinct matrix-degrading metalloproteinase in rat kidney cortex and its identification as meprin. J. Cell Biol.126, 1319–1327.10.1083/jcb.126.5.1319Search in Google Scholar
Koning, F. (2005). Celiac disease: caught between a rock and a hard place. Gastroenterology129, 1294–1301.10.1053/j.gastro.2005.07.030Search in Google Scholar
Köhler, D., Kruse, M., Stöcker, W., and Sterchi, E.E. (2000). Heterologously overexpressed, affinity-purified human meprin α is functionally active and cleaves components of the basement membrane in vitro. FEBS Lett.465, 2–7.10.1016/S0014-5793(99)01712-3Search in Google Scholar
Lahat, N., Shapiro, S., Karban, A., Gerstein, R., Kinarty, A., and Lerner, A. (1999). Cytokine profile in coeliac disease. Scand. J. Immunol.49, 441–446.10.1046/j.1365-3083.1999.00523.xSearch in Google Scholar
Lionetti, P., Breese, E., Braegger, C.P., Murch, S.H., Taylor, J., and MacDonald, T.T. (1993). T-Cell activation can induce either mucosal destruction or adaptation in cultured human fetal small intestine. Gastroenterology105, 373–381.10.1016/0016-5085(93)90710-TSearch in Google Scholar
Lottaz, D., Hahn, D., Müller, S., Müller, C., and Sterchi, E.E. (1999a). Secretion of human meprin from intestinal epithelial cells depends on differential expression of the α and β subunits. Eur. J. Biochem.259, 496–504.10.1046/j.1432-1327.1999.00071.xSearch in Google Scholar
Lottaz, D., Maurer, C.A., Hahn, D., Büchler, M.W., and Sterchi, E.E. (1999b). Nonpolarized secretion of human meprin α in colorectal cancer generates an increased proteolytic potential in the stroma. Cancer Res59, 1127–1133.Search in Google Scholar
MacDonald, T.T. and Spencer, J. (1988). Evidence that activated mucosal T cells play a role in the pathogenesis of enteropathy in human small intestine. J. Exp. Med.167, 1341–1349.10.1084/jem.167.4.1341Search in Google Scholar
MacDonald, T.T., Bajaj-Elliott, M., and Pender, S.L. (1999). T cells orchestrate intestinal mucosal shape and integrity. Immunol. Today20, 505–510.10.1016/S0167-5699(99)01536-4Search in Google Scholar
Marsh, M.N. (1992). Gluten, major histocompatibility complex, and the small intestine. A molecular and immunobiologic approach to the spectrum of gluten sensitivity (‘celiac sprue’). Gastroenterology102, 330–354.10.1016/0016-5085(92)91819-PSearch in Google Scholar
Monteleone, G., MacDonald, T.T., Wathen, N.C., Pallone, F., and Pender, S.L. (1999). Enhancing lamina propria Th1 cell responses with interleukin 12 produces severe tissue injury. Gastroenterology117, 1069–1077.10.1016/S0016-5085(99)70391-4Search in Google Scholar
Monteleone, G., Pender, S.L., Alstead, E., Hauer, A.C., Lionetti, P., McKenzie, C., and MacDonald, T.T. (2001a). Role of interferon α in promoting T helper cell type 1 responses in the small intestine in coeliac disease. Gut48, 425–429.10.1136/gut.48.3.425Search in Google Scholar
Monteleone, G., Pender, S.L., Wathen, N.C., and MacDonald, T.T. (2001b). Interferon-α drives T cell-mediated immunopathology in the intestine. Eur. J. Immunol.31, 2247–2255.10.1002/1521-4141(200108)31:8<2247::AID-IMMU2247>3.0.CO;2-4Search in Google Scholar
Norman, L.P., Jiang, W., Han, X., Saunders, T.L., and Bond, J.S. (2003). Targeted disruption of the meprin β gene in mice leads to underrepresentation of knockout mice and changes in renal gene expression profiles. Mol. Cell. Biol.23, 1221–1230.10.1128/MCB.23.4.1221-1230.2003Search in Google Scholar
Pender, S.L., Tickle, S.P., Docherty, A.J., Howie, D., Wathen, N.C., and MacDonald, T.T. (1997). A major role for matrix metalloproteinases in T cell injury in the gut. J. Immunol.158, 1582–1590.10.4049/jimmunol.158.4.1582Search in Google Scholar
Pischitzis, A., Hahn, D., Leuenberger, B., and Sterchi, E.E. (1999). N-Benzoyl-l-tyrosyl-p-aminobenzoic acid hydrolase β (human meprin β). A 13-amino-acid sequence is required for proteolytic processing and subsequent secretion. Eur. J. Biochem.261, 421–429.Search in Google Scholar
Salmela, M.T., Pender, S.L., Reunala, T., MacDonald, T., and Saarialho-Kere, U. (2001). Parallel expression of macrophage metalloelastase (MMP-12) in duodenal and skin lesions of patients with dermatitis herpetiformis. Gut48, 496–502.10.1136/gut.48.4.496Search in Google Scholar
Shan, L., Molberg, O., Parrot, I., Hausch, F., Filiz, F., Gray, G.M., Sollid, L.M., and Khosla, C. (2002). Structural basis for gluten intolerance in celiac sprue. Science297, 2275–2279.10.1126/science.1074129Search in Google Scholar
Shan, L., Qiao, S.W., Arentz-Hansen, H., Molberg, O., Gray, G.M., Sollid, L.M., and Khosla, C. (2005). Identification and analysis of multivalent proteolytically resistant peptides from gluten: implications for celiac sprue. J. Proteome Res.4, 1732–1741.10.1021/pr050173tSearch in Google Scholar
Sollid, L.M. (2002). Coeliac disease: dissecting a complex inflammatory disorder. Nat. Rev. Immunol.2, 647–655.10.1038/nri885Search in Google Scholar
Spencer, J., MacDonald, T.T., Finn, T., and Isaacson, P.G. (1986). The development of gut associated lymphoid tissue in the terminal ileum of fetal human intestine. Clin. Exp. Immunol.64, 536–543.Search in Google Scholar
Sterchi, E.E., Naim, H.Y., and Lentze, M.J. (1988a). Biosynthesis of N-benzoyl-l-tyrosyl-p-aminobenzoic acid hydrolase: disulfide-linked dimers are formed at the site of synthesis in the rough endoplasmic reticulum. Arch. Biochem. Biophys.265, 119–127.10.1016/0003-9861(88)90377-3Search in Google Scholar
Sterchi, E.E., Naim, H.Y., Lentze, M.J., Hauri, H.P., and Fransen, J.A. (1988b). N-Benzoyl-l-tyrosyl-p-aminobenzoic acid hydrolase: a metalloendopeptidase of the human intestinal microvillus membrane which degrades biologically active peptides. Arch. Biochem. Biophys.265, 105–118.10.1016/0003-9861(88)90376-1Search in Google Scholar
Walker, P.D., Kaushal, G.P., and Shah, S.V. (1998). Meprin A, the major matrix degrading enzyme in renal tubules, produces a novel nidogen fragment in vitro and in vivo. Kidney Int.53, 1673–1680.10.1046/j.1523-1755.1998.00949.xSearch in Google Scholar PubMed
Zweibaum, A., Hauri, H.P., Sterchi, E., Chantret, I., Haffen, K., Bamat, J., and Sordat, B. (1984). Immunohistological evidence, obtained with monoclonal antibodies, of small intestinal brush border hydrolases in human colon cancers and foetal colons. Int. J. Cancer34, 591–598.10.1002/ijc.2910340502Search in Google Scholar PubMed
©2007 by Walter de Gruyter Berlin New York
Articles in the same Issue
- Supplementary material to the paper “Evolutionary selection pressure and family relationships among connexin genes”
- Evolutionary selection pressure and family relationships among connexin genes
- Characterization of the large subunit of EcoHK31I methyltransferase by structural modeling and mutagenesis
- Purification, characterization, and molecular gene cloning of an antifungal protein from Ginkgo biloba seeds
- Maximal Ca2+i stimulation of cardiac Na+/Ca2+ exchange requires simultaneous alkalinization and binding of PtdIns-4,5-P2 to the exchanger
- A highly conserved protein secreted by the prostate cancer cell line PC-3 is expressed in benign and malignant prostate tissue
- Properties and partial purification of sialate-O-acetyltransferase from bovine submandibular glands
- Raft association and lipid droplet targeting of flotillins are independent of caveolin
- On the presence of C2-ceramide in mammalian tissues: possible relationship to etherphospholipids and phosphorylation by ceramide kinase
- Specific inhibition of interleukin-13 activity by a recombinant human single-chain immunoglobulin domain directed against the IL-13 receptor α1 chain
- Effects of disease-modifying anti-rheumatic drugs (DMARDs) on the activities of rheumatoid arthritis-associated cathepsins K and S
- Compartmentalised expression of meprin in small intestinal mucosa: enhanced expression in lamina propria in coeliac disease
- Human dipeptidyl peptidase III acts as a post-proline-cleaving enzyme on endomorphins
- Transgenic mouse brains for the evaluation and quality control of BSE tests
Articles in the same Issue
- Supplementary material to the paper “Evolutionary selection pressure and family relationships among connexin genes”
- Evolutionary selection pressure and family relationships among connexin genes
- Characterization of the large subunit of EcoHK31I methyltransferase by structural modeling and mutagenesis
- Purification, characterization, and molecular gene cloning of an antifungal protein from Ginkgo biloba seeds
- Maximal Ca2+i stimulation of cardiac Na+/Ca2+ exchange requires simultaneous alkalinization and binding of PtdIns-4,5-P2 to the exchanger
- A highly conserved protein secreted by the prostate cancer cell line PC-3 is expressed in benign and malignant prostate tissue
- Properties and partial purification of sialate-O-acetyltransferase from bovine submandibular glands
- Raft association and lipid droplet targeting of flotillins are independent of caveolin
- On the presence of C2-ceramide in mammalian tissues: possible relationship to etherphospholipids and phosphorylation by ceramide kinase
- Specific inhibition of interleukin-13 activity by a recombinant human single-chain immunoglobulin domain directed against the IL-13 receptor α1 chain
- Effects of disease-modifying anti-rheumatic drugs (DMARDs) on the activities of rheumatoid arthritis-associated cathepsins K and S
- Compartmentalised expression of meprin in small intestinal mucosa: enhanced expression in lamina propria in coeliac disease
- Human dipeptidyl peptidase III acts as a post-proline-cleaving enzyme on endomorphins
- Transgenic mouse brains for the evaluation and quality control of BSE tests