Mannan-binding protein blocks the activation of metalloproteases meprin α and β

Journal of Immunology

Volumn 175, Issue 5, 2005, Pages 3177-3185

  Hirano, Makoto ^a   Ma, Bruce Yong ^a   Kawasaki, Nana ^b   Okimura, Kazumichi ^a   Baba, Makoto ^a   Nakagawa, Tomoaki ^a   Miwa, Keiko ^a   Kawasaki, Nobuko ^a   Oka, Shogo ^a   Kawasaki, Toshisuke ^a,c  

^a KYOTO UNIVERSITY   (Japan)

^b NATIONAL INSTITUTE OF HEALTH SCIENCES   (Japan)

^c RITSUMEIKAN UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

FUCOSE; MANNAN BINDING LECTIN; MANNOSE; MEPRIN; MEPRIN ALPHA; MEPRIN BETA; METALLOPROTEINASE; N ACETYLGLUCOSAMINE; SCLEROPROTEIN; UNCLASSIFIED DRUG;

ACUTE KIDNEY FAILURE; AFFINITY CHROMATOGRAPHY; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; DEGLYCOSYLATION; ENTERITIS; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME GLYCOSYLATION; HOST RESISTANCE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INNATE IMMUNITY; KIDNEY PROXIMAL TUBULE; LEUKOCYTE; MASS SPECTROMETRY; METASTASIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DEGRADATION; PROTEIN EXPRESSION; SMALL INTESTINE MUCOSA; TUMOR GROWTH;

EID: 23844493371     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.5.3177     Document Type: Article

References (56)

1. Kawasaki, N., T. Kawasaki, and I. Yamashina. 1983. Isolation and characterization of a mannan-binding protein from human serum. J Biochem. 94: 937-947.
2. Ohta, M., M. Okada, I. Yamashina, and T. Kawasaki. 1990. The mechanism of carbohydrate-mediated complement activation by the serum mannan-binding protein. J. Biol. Chem. 265: 1980-1984.
3. Ikeda, K., T. Sannoh, N. Kawasaki, T. Kawasaki, and I. Yamashina. 1987. Serum lectin with known structure activates complement through the classical pathway. J. Biol. Chem. 262: 7451-7454.
4. Matsushita, M., and T. Fujita. 1992. Activation of the classical complement pathway by mannose-binding protein in association with a novel Cls-like protease. J. Exp. Med. 176: 1497-1502.
5. Thiel, S., T. Vorup-Jensen, C. M. Stover, W. Schwaeble, S. B. Laursen, K. Poulsen, A. C. Willis, P. Eggleton, S. Hansen, U. Holmskov, et al. 1997. A second serine protease associated with mannan-binding lectin that activates complement. Nature 386: 506-510.
6. Dahl, M. R., S. Thiel, M. Matsushita, T. Fujita, A. C. Willis, T. Christensen, T. Vorup-Jensen, and J. C. Jensenius. 2001. MASP-3 and its association with distinct complexes of the mannan-binding lectin complement activation pathway. Immunity 15: 127-135.
7. Janeway, C. A., Jr., P. Travers, M. Walport, and M. Shlomchik. 2001. Immunobiology, the Immune System in Health and Disease, 5th Ed. Garland Publishing, New York, p. 35-91.
8. Jack, D. L., and M. W. Turner. 2003. Anti-microbial activities of mannose-binding lectin. Biochem. Soc. Trans. 31: 753-757.
9. Kawasaki, N., T. Kawasaki, and I. Yamashina. 1989. A serum lectin (mannan-binding protein) has complement-dependent bactericidal activity. J. Biochem. 106: 483-489.
10. Kuhlman, M., K. A. Joiner, and R. A. B. Ezekowitz. 1989. The human mannose-binding protein functions as an opsonin. J. Exp. Med. 169: 1733-1745.
11. Ogden, C. A., A. deCathelineau, P. R. Hoffmann, D. Bratton, B. Ghebrehiwet, V. A. Fadok, and P. M. Henson. 2001. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp. Med. 194: 781-795.
12. Nauta, A. J., G. Castellano, W. Xu, A. M. Woltman, M. C. Borrias, M. R. Daha, C. V. Kooten, and A. Roos. 2004. Opsonization with C1q and mannose-binding lectin targets apoptotic cells to dendritic cells. J. Immunol. 173: 3044-3050.
13. Hartley, C. A., D. C. Jackson, and E. M. Anders. 1992. Two distinct serum mannose-binding lectins function as β inhibitors of influenza virus: identification of bovine serum β inhibitor as conglutinin. J. Virol. 66: 4358-4363.
14. Ezekowitz, R. A. B., M. Kuhlman, J. Groopman, and R. Byrn. 1989. A human serum mannose-binding protein inhibits in vitro infection by human immunodeficiency virus. J. Exp. Med. 169: 185-196.
15. Hegele, R. A., M. R. Ban, C. M. Anderson, and J. D. Spence. 2000. Infection susceptibility alleles of mannose-binding lectin are associated with increased carotid plaque area. J. Invest. Med. 48: 198-202.
16. Nagy, A., G. T. Kozma, M. Keszei, A. Treszl, A. Falus, and C. Szalai. 2003. The development of asthma in children infected with Chlamydia pneumoniae is dependent on the modifying effect of mannose-binding lectin. J. Allergy Clin. Immunol. 4: 729-734.
17. Eisen, D. P., and R. M. Minchinton. 2003. Impact of mannose-binding lectin on susceptibility to infectious diseases. Clin. Infect. Dis. 37: 1496-1505.
18. Drickamer, K., M. S. Dordal, and L. Reynolds. 1986. Mannose-binding proteins isolated from rat liver contain carbohydrate-recognition domains linked to collagenous tails. J. Biol. Chem. 261: 6878-6887.
19. Valdimarsson, H., M. Stefansson, T. Vikingsdottir, G. J. Arason, C. Koch, S. Tiehl, and J. C. Jensenius. 1998. Reconstitution of opsonizing activity by infusion of mannan-binding lectin (MBL) to MBL-deficient humans. Scand. J. Immunol. 48: 116-123.
20. Garred, P., H. O. Madsen, B. Hofmann, and A. Svejgaard. 1995. Increased frequency of homozygosity of abnormal mannan-binding protein alleles in patients with suspected immunodeficiency. Lancet 346: 941-943.
21. Garred, P., J. J. Strom, L. Quist, E. Taaning, and H. O. Madsen. 2003. Association of mannose-binding lectin polymorphisms with sepsis and fatal outcome, in patients with systemic inflammatory response syndrome. J. Infect. Dis. 188: 1394-1403.
22. Garred, P., F. Larsen, H. O. Madsen, and C. Koch. 2003. Mannose-binding lectin deficiency: revisited. Mol. Immunol. 40: 73-84.
23. Ohta, M., and T. Kawasaki. 1994. Complement-dependent cytotoxic activity of serum mannan-binding protein towards mammalian cells with surface-exposed high-mannose type glycans. Glycoconj. J. 11: 304-308.
24. Ma, Y., H. Shida, and T. Kawasaki. 1997. Functional expression of human mannan-binding proteins (MBPs) in human hepatoma cell lines infected by recombinant vaccinia virus: post-translational modification, molecular assembly, and differentiation of serum and liver MBP. J. Biochem. 122: 810-818.
25. Ma, Y., K. Uemura, S. Oka, Y. Kozutsumi, N. Kawasaki, and T. Kawasaki. 1999. Antitumor activity of mannan-binding protein in vivo as revealed by a virus expression system: mannan-binding protein-dependent cell-mediated cytotoxicity. Proc. Natl. Acad. Sci. USA 96: 371-375.
26. Nepomuceno, R. R., A. H. Henschen-Edman, W. H. Burgess, and A. J. Tenner. 1997. cDNA cloning and primary structure analysis of C1qR(P), the human C1q/MBL/SPA receptor that mediates enhanced phagocytosis in vitro. Immunity 6: 119-129.
27. Ghiran, I., S. F. Barbashov, L. B. Klickstein, S. W. Tas, J. C. Jensenius, and A. Nicholson-Weller. 2000. Complement receptor 1/CD35 is a receptor for mannan-binding lectin. J. Exp. Med. 192: 1797-1808.
28. Marchand, P., J. Tang, and J. S. Bond. 1994. Membrane association and oligomeric organization of the α and β subunits of mouse meprin A. J. Biol. Chem. 269: 15388-15393.
29. Gorbea, C. M., P. Marchand, W. Jiang, N. G. Copeland, D. J. Gilbert, N. A. Jenkins, and J. S. Bond. 1993. Cloning, expression, and chromosomal localization of the mouse meprin β subunit. J. Biol. Chem. 268: 21035-21043.
30. Kadowaki, T., T. Tsukuba, G. P. Bertenshaw, and J. S. Bond. 2000. N-linked oligosaccharides on the meprin A metalloproteinase are important for secretion and enzymatic activity, but not for apical targeting. J. Biol. Chem. 275: 25577-25584.
31. Tsukuba, T., and J. S. Bond. 1998. Role of the COOH-terminal domains of meprin A in folding, secretion, and activity of the metalloendopeptidase. J. Biol. Chem. 273: 35260-35267.
32. Bond, J. S., and R. J. Beynon. 1995. The astacin family of metalloendopeptidases. Protein Sci. 4: 1247-1261.
33. Matters, G. L., and J. S. Bond. 1999. Expression and regulation of the meprin β gene in human cancer cells. Mol. Carcinog. 25: 169-178.
34. Kumar, J. M., and J. S. Bond. 2001. Developmental expression of meprin metalloprotease subunits in ICR and C3H/He mouse kidney and intestine in the embryo, postnatally and after weaning. Biochim. Biophys. Acta 1518: 106-114.
35. Kounnas, M. Z., R. L. Wolz, C. M. Gorbea, and J. S. Bond. 1991. Meprin-A and -B: cell surface endopeptidases of the mouse kidney. J. Biol. Chem. 266: 17350-17357.
36. Butler, P. E., and J. S. Bond. 1988. A latent proteinase in mouse kidney membranes: characterization and relationship to meprin. J. Biol. Chem. 263: 13419-13426.
37. Bertenshaw, G. P., B. E. Turk, S. J. Hubbard, G. L. Matters, J. E. Bylander, J. M. Crisman, L. C. Cantley, and J. S. Bond. 2001. Marked differences between metalloproteases meprin A and B in substrate and peptide bond specificity. J. Biol. Chem. 276: 13248-13255.
38. Leuenberger, B., D. Hahn, A. Pischitzis, M. K. Hansen, and E. E. Sterchi. 2003. Human meprin β: O-linked glycans in the intervening region of the type I membrane protein protect the C-terminal region from proteolytic cleavage and diminish its secretion. Biochem. J. 369: 659-665.
39. Lottaz, D., D. Hahn, S. Muller, C. Muller, and E. E. Sterchi. 1999. Secretion of human meprin from intestinal epithelial cells depends on differential expression of the α and β subunits. Eur. J. Biochem. 259: 496-504.
40. Matters, G. L., and J. S. Bond. 1999. Expression and regulation of the meprin β gene in human cancer cells. Mol. Carcinog. 25: 169-178.
41. Marchand, P., J. Tang, G. D. Johnson, and J. S. Bond. 1995. COOH-terminal proteolytic processing of secreted and membrane forms of the α subunit of the metalloprotease meprin A: requirement of the I domain for processing in the endoplasmic reticulum. J. Biol. Chem. 270: 5449-5456.
42. Ellgarrd, L., M. Molinari, and A. Helenius. 1999. Setting the standards: quality control in the secretory pathway. Science 286: 1882-1888.
43. Crisman, J. M., B. Zhang, L. P. Norman, and J. S. Bond. 2004. Deletion of the mouse meprin β metalloprotease gene diminishes the ability of leukocytes to disseminate through extracellular matrix. J. Immunol. 172: 4510-4519.
44. Hansen, S., S. Thiel, A. Willis, U. Holmskov, and J. C. Jensenius. 2000. Purification and characterization of two mannan-binding lectins from mouse serum. J. Immunol. 164: 2610-2618.
45. Lottaz, D., C. A. Maurer, D. Hahn, M. W. Buchler, and E. E. Sterchi. 1999. Nonpolarized secretion of human meprin α in colorectal cancer generates an increased proteolytic potential in the stroma. Cancer Res. 59: 1127-1133.
46. Trachtman, H., E. Valderrama, J. M. Dietrich, and J. S. Bond. 1995. The role of meprin A in the pathogenesis of acute renal failure. Biochem. Biophys. Res. Commun. 208: 498-505.
47. Carmago, S., S. V. Shah, and P. D. Walker. 2002. Meprin, a brush-border enzyme, plays an important role in hypoxic/ischemic acute renal tubular injury in rats. Kidney Int. 61: 959-966.
48. Kaushal, G. P., P. D. Walker, and S. V. Shah. 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.
49. Walker, P. D., G. P. Kaushal, and S. V. Shah. 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.
50. Lazarus, J. M., and B. M. Brenner. 1993. Acute Renal Failure. J. M. Lazarus and B. M. Brenner, eds. Churchill-Livingstone, New York.
51. Wolz, R. L., R. B. Harris, and J. S. Bond. 1991. Mapping the active site of meprin A with peptide substrates and inhibitors. Biochemistry 30: 8488-8493.
52. Opdenakker, G., P. E. Van den Steen, B. Dubois, I. Nelissen, E. Van Coillie, S. Masure, P. Proost, and J. Van Damme. 2001. Gelatinase B functions as regulator and effector in leukocyte biology. J. Leukocyte Biol. 69: 851-859.
53. Faveeuw, C., G. Preece, and A. Ager. 2001. Transendothelial migration of lymphocytes across high endothelial venules into lymph nodes is affected by metalloproteinases. Blood 98: 688-695.
54. Leppert, D., E. Waubant, R. Galardy, N. W. Bunnett, and S. L. Hauser. 1995. T cell gelatinases mediate basement membrane transmigration in vitro. J. Immunol. 154: 4379-4389.
55. Terada, M., K. H. Khoo, R. Inoue, C. I. Chen, K. Yamada, H. Sakaguchi, N. Kadowaki, B. Y. Ma, S. Oka, T. Kawasaki, and N. Kawasaki. 2005. Characterization of oligosaccharide ligands expressed on SW1116 cells recognized by mannan-binding protein: a highly fucosylated polylactosamine type N-glycan. J. Biol. Chem. 280: 10897-10913.
56. Johnson, G. D., and R. J. Bond. 1998. Handbook of Proteolytic Enzymes. A. J. Barrett, F. Woessner, and N. Rawlings, eds. Academic Press, San p. 1222-1229.