Potentiation of C1 Esterase Inhibitor by StcE, a Metalloprotease Secreted by Escherichia coli O157:H7

Journal of Experimental Medicine

Volumn 199, Issue 8, 2004, Pages 1077-1087

  Lathem, Wyndham W ^a,b   Bergsbaken, Tessa ^a,c   Welch, Rodney A ^a  

^a UNIVERSITY OF WISCONSIN MADISON   (United States)

^b WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Complement; Contact activation; Reactive center loop; Serpins; Serum resistance

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C1S INHIBITOR; METALLOPROTEINASE; SERINE PROTEINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ESCHERICHIA COLI; FLOW CYTOMETRY; HEMOLYSIS; IMMUNOBLOTTING; IMMUNOPRECIPITATION; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEGRADATION; SHEEP;

ANIMALS; COMPLEMENT C1 INACTIVATOR PROTEINS; COMPLEMENT PATHWAY, CLASSICAL; COS CELLS; DRUG SYNERGISM; ERYTHROCYTES; ESCHERICHIA COLI O157; ESCHERICHIA COLI PROTEINS; HEMOLYSIS; HUMANS; IMMUNITY, NATURAL; METALLOENDOPEPTIDASES; MODELS, BIOLOGICAL; SHEEP;

EID: 2442509635     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20030255     Document Type: Article

References (48)

1. Frank, M.M., and L.F. Fries. 1989. Complement. In Fundamental Immunology. W.E. Paul, editor. Raven Press, New York. 679-701.
2. Pensky, J., and H.G. Schwick. 1969. Human serum inhibitor of C′1 esterase: identity with alpha-2-neuraminoglycoprotein. Science. 163:698-699.
3. Weiler, J.M., M.R. Daha, K.F. Austen, and D.T. Fearon. 1976. Control of the amplification convertase of complement by the plasma protein beta1H. Proc. Natl. Acad. Sci. USA. 73: 3268-3272.
4. Gigli, I., T. Fujita, and V. Nussenzweig. 1979. Modulation of the classical pathway C3 convertase by plasma proteins C4 binding protein and C3b inactivator. Proc. Natl. Acad. Sci. USA. 76:6596-6600.
5. van den Berg, R.H., M. Faber-Krol, L.A. van Es, and M.R. Daha. 1995. Regulation of the function of the first component of complement by human C1q receptor. Eur. J. Immunol. 25:2206-2210.
6. Caliezi, C., W.A. Wuillemin, S. Zeerleder, M. Redondo, B. Eisele, and C.E. Hack. 2000. C1-Esterase inhibitor: an anti-inflammatory agent and its potential use in the treatment of diseases other than hereditary angioedema. Pharmacol. Rev. 52:91-112.
7. Potempa, J., E. Korzus, and J. Travis. 1994. The serpin superfamily of proteinase inhibitors: structure, function and regulation. J. Biol. Chem. 269:15957-15960.
8. Huntington, J.A., R.J. Read, and R.W. Carrell. 2000. Structure of a serpin-protease complex shows inhibition by deformation. Nature. 407:923-926.
9. Sim, R.B., A. Reboul, G.J. Arlaud, C.L. Villiers, and M.G. Colomb. 1979. Interaction of I125-labelled complement subcomponents C1r and C1s with protease inhibitors in plasma. FEBS Lett. 97:111-115.
10. Chan, J.Y., C.E. Burrowes, F.M. Habal, and H.Z. Movat. 1977. The inhibition of activated factor XII (Hageman factor) by antithrombin III: the effect of other plasma proteinase inhibitors. Biochem. Biophys. Res. Commun. 74:150-158.
11. Schapira, M., C.F. Scott, and R.W. Colman. 1982. Contribution of plasma protease inhibitors to the inactivation of kallikrein in plasma. J. Clin. Invest. 69:462-468.
12. Van den Graaf, F., J.A. Koedam, and B.N. Bouma. 1983. Inactivation of kallikrein in human plasma. J. Clin. Invest. 71: 149-158.
13. Pixley, R.A., M. Schapira, and R.W. Colman. 1985. The regulation of human factor XIIa by plasma proteinase inhibitors. J. Biol. Chem. 260:1723-1729.
14. Wuillemin, W.A., M. Minnema, J.C. Meijers, D. Roem, A.J.M. Eerenberg, J.H. Nuijens, J.W. ten Cate, and C.E. Hack. 1995. Inactivation of factor XIa in human plasma assessed by measuring factor XIa-protease inhibitor complexes: major role of C1-inhibitor. Blood. 85:1517-1526.
15. Jiang, H., E. Wagner, H. Zhang, and M.M. Frank. 2001. Complement 1 inhbitor is a regulator of the alternative complement pathway. J. Exp. Med. 194:1609-1616.
16. Coutinho, M., K.S. Aulak, and A.E. Davis. 1994. Functional analysis of the serpin domain of C1 inhibitor. J. Immunol. 153:3648-3654.
17. Patston, P.A., M. Qi, J.A. Schifferli, and M. Schapira. 1995. The effect of cleavage by a Crotalus atrox alpha-proteinase fraction on the properties of C1-inhibitor. Toxicon. 33:53-61.
18. Wuillemin, W.A., E. Eldering, F. Citarella, C.P. de Ruig, J.W. ten Cate, and C.E. Hack. 1996. Modulation of contact system proteases by glycosaminoglycans. Selective enhancement of the inhibition of factor XIa. J. Biol. Chem. 271: 12913-12918.
19. Caldwell, E.E., A.M. Andreasen, M.A. Blietz, J.N. Serrahn, V. VanderNoot, Y. Park, G. Yu, R.J. Linhardt, and J.M. Weiler. 1999. Heparin binding and augmentation of C1 inhibitor activity. Arch. Biochem. Biophys. 361:215-222.
20. Schmaier, A.H., S.C. Murray, G.D. Heda, A. Farber, A. Kuo, K. McCrae, and D.B. Cines. 1989. Synthesis and expression of C1 inhibitor by human umbilical vein endothelial cells. J. Biol. Chem. 264:18173-18179.
21. Schmaier, A.H., S. Amenta, T. Xiong, G.D. Heda, and A.M. Gewirtz. 1993. Expression of platelet C1 inhibitor. Blood. 82: 465-474.
22. Frankel, G., A.D. Phillips, I. Rosenshine, G. Dougan, J.B. Kaper, and S. Knutton. 1998. Enteropathogenic and enterohaemorrhagic Escherichia coli: more subversive elements. Mol. Microbiol. 30:911-921.
23. Nataro, J.P., and J.B. Kaper. 1998. Diarrheagenic Escherichia coli. Clin. Microbiol. Rev. 11:142-201.
24. Lathem, W.W., T.E. Grys, S.E. Witowski, A.G. Torres, J.B. Kaper, P.I. Tarr, and R.A. Welch. 2002. StcE, a metalloprotease secreted by Escherichia coli O157:H7, specifically cleaves C1 esterase inhibitor. Mol. Microbiol. 45:277-288.
25. Lathem, W.W., T. Bergsbaken, S.E. Witowski, N.T. Perna, and R.A. Welch. 2003. Acquisition of stcE, a C1 esterase inhibitor-specific metalloprotease, during the evolution of Escherichia coli O157:H7. J. Infect. Dis. 187:1907-1914.
26. Paton, A.W., and J.C. Paton. 2002. Reactivity of convalescent-phase hemolytic-uremic syndrome patient sera with the megaplasmid-encoded TagA protein of shiga toxigenic Escherichia coli O157. J. Clin. Microbiol. 40:1395-1399.
27. Mayer, M.M. 1961. Experimental Immunochemistry. Thomas, Springfield, IL. 905 pp.
28. Harlow, E., and D. Lane. 1988. Antibodies: A Laboratory Manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY. 726 pp.
29. de Agostini, A., M. Schapira, Y.T. Wachtfogel, R.W. Colman, and S. Carrel. 1985. Human plasma kallikrein and C1 inhibitor form a complex possessing an epitope that is not detectable on the parent molecules: demonstration using a monoclonal antibody. Proc. Natl. Acad. Sci. USA. 82:5190-5193.
30. Perna, N.T., G. Plunkett III, V. Burland, B. Mau, J.D. Glasner, D.J. Rose, G.F. Mayhew, P.S. Evans, J. Gregor, H.A. Kirkpatrick, et al. 2001. Genome sequence of enterohaemorrhagic Escherichia coli O157:H7. Nature. 409:529-533.
31. Patston, P.A., and M. Schapira. 1997. Regulation of C1-inhibitor function by binding to type IV collagen and heparin. Biochem. Biophys. Res. Commun. 230:597-601.
32. Hauert, J., P.A. Patston, and M. Schapira. 2000. C1 inhibitor cross-linking by tissue transglutaminase. J. Biol. Chem. 275: 14558-14562.
33. Matsunami, K., S. Miyagawa, M. Yamada, M. Yoshitatsu, and R. Shirakura. 2000. A surface-bound form of human C1 esterase inhibitor improves xenograft rejection. Transplantation. 69:749-755.
34. Bergamaschini, L., G. Gobbo, S. Gatti, L. Caccamo, P. Prato, M. Maggioni, P. Braidotti, R. Di Stefano, and L.R. Fassati. 2001. Endothelial targeting with C1-inhibitor reduces complement activation in vitro and during ex vivo reperfusion of pig liver. Clin. Exp. Immunol. 126:412-420.
35. Minta, J.O. 1981. The role of sialic acid in the functional activity and the hepatic clearance of C1-INH. J. Immunol. 126:245-249.
36. Storm, D., J. Herz, P. Trinder, and M. Loos. 1997. C1 inhibitor-C1s complexes are internalized and degraded by the low density lipoprotein receptor-related protein. J. Biol. Chem. 272:31043-31050.
37. te Loo, D.M., L.A. Monnens, T.J. van Der Velden, M.A. Vermeer, F. Preyers, P.N. Demacker, L.P. van Den Heuvel, and V.W. van Hinsbergh. 2000. Binding and transfer of verocytotoxin by polymorphonuclear leukocytes in hemolytic uremic syndrome. Blood. 95:3396-3402.
38. te Loo, D.M., V.W. van Hinsbergh, L.P. van Den Heuvel, and L.A. Monnens. 2001. Detection of verocytotoxin bound to circulating polymorphonuclear leukocytes of patients with hemolytic uremic syndrome. J. Am. Soc. Nephrol. 12:800-806.
39. Cai, S., and A.E. Davis III. 2003. Complement regulatory protein C1 inhibitor binds to selectins and interferes with endothelial-leukocyte adhesion. J. Immunol. 171:4786-4791.
40. Cooper, N.R. 1991. Complement evasion strategies of microorganisms. Immunol. Today. 12:327-331.
41. Frank, M.M. 1992. The mechanism by which microorganisms avoid complement attack. Curr. Opin. Immunol. 4:14-19.
42. Molla, A., T. Akaike, and H. Maeda. 1989. Inactivation of various proteinases inhibitors and the complement system in human plasma by the 56-kilodalton proteinase from Serratia marcescens. Infect. Immun. 57:1868-1871.
43. Oda, T., Y. Kojima, T. Akaike, S. Ijiri, A. Molla, and H. Maeda. 1990. Inactivation of chemotactic activity of C5a by the serratial 56-kilodalton protease. Infect. Immun. 58:1269-1272.
44. Hong, Y.Q., and B. Ghebrehiwet. 1992. Effect of Pseudomonas aeruginosa elastase and alkaline protease on serum complement and isolated components C1q and C3. Clin. Immunol. Immunopathol. 62:133-138.
45. Hellwage, J., T. Meri, T. Heikkila, A. Alitalo, J. Panelius, P. Lahdenne, I.J. Seppala, and S. Meri. 2001. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276:8427-8435.
46. Berggard, K., E. Johnsson, E. Moffeldt, J. Persson, M. Stalhammar-Carlemalm, and G. Lindahl. 2001. Binding of human C4BP to the hypervariable region of M protein: a molecular mechanism of phagocytosis resistance in Streptococcus pyogenes. Mol. Microbiol. 42:539-551.
47. Them, A., L. Stenberg, B. Dahlback, and G. Lindahl. 1995. Ig-binding surface proteins of Streptococcus pyogenes also bind human C4b-binding protein (C4BP), a regulatory component of the complement system. J. Immunol. 154:375-386.
48. Plunkett, G., III, D.J. Rose, T.J. Durfee, and F.R. Blattner. 1999. Sequence of Shiga toxin 2 phage 933W from Escherichia coli O157:H7: Shiga toxin as a phage late-gene product. J. Bacteriol. 181:1767-1778.