The host immune regulator factor H interacts via two contact sites with the PspC protein of Streptococcus pneumoniae and mediates adhesion to host epithelial cells

Journal of Immunology

Volumn 178, Issue 9, 2007, Pages 5848-5858

  Hammerschimdt, Sven ^a,d   Agarwal, Vaibhav ^a   Kunert, Anja ^b   Haelbich, Steffi ^b   Skerka, Christine ^b   Zipfel, Peter F ^b,c  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b HANS KNÖLL INSTITUTE   (Germany)

^c FRIEDRICH SCHILLER UNIVERSITY JENA   (Germany)

^d UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT FACTOR H; OUTER MEMBRANE PROTEIN; PSPC PROTEIN; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL VIRULENCE; BACTERIUM ADHERENCE; BINDING SITE; COMPLEMENT FIXATION; CONTROLLED STUDY; DELETION MUTANT; ENDOTHELIUM CELL; EPITHELIUM CELL; HOST CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOREGULATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; STREPTOCOCCUS PNEUMONIAE; SURFACE PLASMON RESONANCE; WESTERN BLOTTING;

EID: 34247573934     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.178.9.5848     Document Type: Article

References (56)

1. Austrian, R. 1986. Some aspects of the pneumococcal carrier state. J. Antimicrob. Chemother. 18(Suppl. A): 35-45.
2. Musher, D. M. 1992. Infections caused by Streptococcus pneumoniae: clinical spectrum, pathogenesis, immunity, and treatment. Clin. Infect. Dis. 14: 801-807.
3. Cartwright, K. 2002. Pneumococcal disease in western Europe: burden of disease, antibiotic resistance and management. Eur. J. Pediatr. 161: 188-195.
4. Tuomanen, E. I., R. Austrian, and H. R. Masure. 1995. Pathogenesis of pneumococcal infection. N. Engl. J. Med. 332: 1280-1284.
5. Bergmann, S., and S. Hammerschmidt. 2006. Versatility of pneumococcal surface proteins. Microbiology 152: 295-303.
6. Hammerschmidt, S. 2006. Adherence molecules of pathogenic pneumococci. Curr. Opin. Microbiol. 9: 12-20.
7. Paterson, G. K., and T. J. Mitchell. 2006. Innate immunity and the pneumococcus. Microbiology 152: 285-293.
8. Iannelli, F., M. R. Oggioni, and G. Pozzi. 2002. Allelic variation in the highly polymorphic locus pspC of Streptococcus pneumoniae. Gene 284: 63-71.
9. Brooks-Walter, A., D. E. Briles, and S. K. Hollingshead. 1999. The pspC gene of Streptococcus pneumoniae encodes a polymorphic protein, PspC, which elicits cross-reactive antibodies to PspA and provides immunity to pneumococcal bacteremia. Infect. Immun. 67: 6533-6542.
10. Hammerschmidt, S., S. R. Talay, P. Brandtzaeg, and G. S. Chhatwal. 1997. SpsA, a novel pneumococcal surface protein with specific binding to secretory immunoglobulin A and secretory component. Mol. Microbiol. 25: 1113-1124.
11. Luo, R., B. Mann, W. S. Lewis, A. Rowe, R. Heath, M. L. Stewart, A. E. Hamburger, S. Sivakolundu, E. R. Lacy, P. J. Bjorkman, et al. 2005. Solution structure of choline binding protein A, the major adhesin of Streptococcus pneumoniae. EMBO J. 24: 34-43.
12. Zhang, J. R., K. E. Mostov, M. E. Lamm, M. Nanno, S. Shimida, M. Ohwaki, and E. Tuomanen. 2000. The polymeric immunoglobulin receptor translocates pneumococci across human nasopharyngeal epithelial cells. Cell 102: 827-837.
13. Elm, C., R. Braathen, S. Bergmann, R. Frank, J. P. Vaerman, C. S. Kaetzel, G. S. Chhatwal, F. E. Johansen, and S. Hammerschmidt. 2004. Ectodomains 3 and 4 of human polymeric immunoglobulin receptor (hpIgR) mediate invasion of Streptococcus pneumoniae into the epithelium. J. Biol. Chem. 279: 6296-6304.
14. Lu, L., M. E. Lamm, H. Li, B. Corthesy, and J. R. Zhang. 2003. The human polymeric immunoglobulin receptor binds to Streptococcus pneumoniae via domains 3 and 4. J. Biol. Chem. 278: 48178-48187.
15. Hammerschmidt, S., M. P. Tillig, S. Wolff, J. P. Vaerman, and G. S. Chhatwal. 2000. Species-specific binding of human secretory component to SpsA protein of Streptococcus pneumoniae via a hexapeptide motif. Mol. Microbiol. 36: 726-736.
16. Dave, S., A. Brooks-Walter, M. K. Pangburn, and L. S. McDaniel. 2001. PspC, a pneumococcal surface protein, binds human factor H. Infect. Immun. 69: 3435-3437.
17. Smith, B. L., and M. K. Hostetter. 2000. C3 as substrate for adhesion of Streptococcus pneumoniae. J. Infect. Dis. 182: 497-508.
18. Dave, S., S. Carmicle, S. Hammerschmidt, M. K. Pangburn, and L. S. McDaniel. 2004. Dual roles of PspC, a surface protein of Streptococcus pneumoniae, in binding human secretory IgA and factor H. J. Immunol. 173: 471-477.
19. Janulczyk, R., F. Iannelli, A. G. Sjoholm, G. Pozzi, and L. Bjorck. 2000. Hic, a novel surface protein of Streptococcus pneumoniae that interferes with complement function. J. Biol. Chem. 275: 37257-37263.
20. Zipfel, P. F., C. Skerka, J. Hellwage, S. T. Jokiranta, S. Meri, V. Brade, P. Kraiczy, M. Noris, and G. Remuzzi. 2002. Factor H family proteins: on complement, microbes and human diseases. Biochem. Soc. Trans. 30: 971-978.
21. 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.
22. Alitalo, A., T. Meri, L. Ramo, T. S. Jokiranta, T. Heikkila, I. J. Seppala, J. Oksi, M. Viljanen, and S. Meri. 2001. Complement evasion by Borrelia burgdorferi: serum-resistant strains promote C3b inactivation. Infect. Immun. 69: 3685-3691.
23. Areschoug, T., M. Stalhammar-Carlemalm, I. Karlsson, and G. Lindahl. 2002. Streptococcal β protein has separate binding sites for human factor H and IgA-Fc. J. Biol. Chem. 277: 12642-12648.
24. Horstmann, R. D., H. J. Sievertsen, J. Knobloch, and V. A. Fischetti. 1988. Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc. Natl. Acad. Sci. USA 85: 1657-1661.
25. Kraiczy, P., C. Skerka, M. Kirschfink, V. Brade, and P. F. Zipfel. 2001. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and factor H. Eur. J. Immunol. 31: 1674-1684.
26. Meri, T., A. Hartmann, D. Lenk, R. Eck, R. Wurzner, J. Hellwage, S. Meri, and P. F. Zipfel. 2002. The yeast Candida albicans binds complement regulators factor H and FHL-1. Infect. Immun. 70: 5185-5192.
27. Ram, S., A. K. Sharma, S. D. Simpson, S. Gulati, D. P. McQuillen, M. K. Pangburn, and P. A. Rice. 1998. A novel sialic acid binding site on factor H mediates serum resistance of sialylated Neisseria gonorrhoeae. J. Exp. Med. 187: 743-752.
28. Ram, S., F. G. Mackinnon, S. Gulati, D. P. McQuillen, U. Vogel, M. Frosch, C. Elkins, H. K. Guttormsen, L. M. Wetzler, M. Oppermann, et al. 1999. The contrasting mechanisms of serum resistance of Neisseria gonorrhoeae and group B Neisseria meningitidis. Mol. Immunol. 36: 915-928.
29. Iannelli, F., D. Chiavolini, S. Ricci, M. R. Oggioni, and G. Pozzi. 2004. Pneumococcal surface protein C contributes to sepsis caused by Streptococcus pneumoniae in mice. Infect. Immun. 72: 3077-3080.
30. Jarva, H., R. Janulczyk, J. Hellwage, P. F. Zipfel, L. Bjorck, and S. Meri. 2002. Streptococcus pneumoniae evades complement attack and opsonophagocytosis by expressing the pspC locus-encoded Hic protein that binds to short consensus repeats 8-11 of factor H. J. Immunol. 168: 1886-1894.
31. Peppoloni, S., B. Colombari, R. Neglia, D. Quaglino, F. Iannelli, M. R. Oggioni, G. Pozzi, and E. Blasi. 2006. The lack of pneumococcal surface protein C (PspC) increases the susceptibility of Streptococcus pneumoniae to the killing by microglia. Med. Microbiol. Immunol. 195: 21-28.
32. Meri, S., and M. K. Pangburn. 1990. Discrimination between activators and non-activators of the alternative pathway of complement: regulation via a sialic acid/polyanion binding site on factor H. Proc. Natl. Acad. Sci. USA 87: 3982-3986.
33. Jokiranta, T. S., V. P. Jaakola, M. J. Lehtinen, M. Parepalo, S. Meri, and A. Goldman. 2006. Structure of complement factor H carboxyl-terminus reveals molecular basis of atypical haemolytic uremic syndrome. EMBO J. 25: 1784-1794.
34. Manuelian, T., J. Hellwage, S. Meri, J. Caprioli, M. Noris, S. Heinen, M. Jozsi, H. P. Neumann, G. Remuzzi, and P. F. Zipfel. 2003. Mutations in factor H reduce binding affinity to C3b and heparin and surface attachment to endothelial cells in hemolytic uremic syndrome. J. Clin. Invest. 111: 1181-1190.
35. Hellwage, J., S. Kuhn, and P. F. Zipfel. 1997. The human complement regulatory factor-H-like protein 1, which represents a truncated form of factor H, displays cell-attachment activity. Biochem. J. 326: 321-327.
36. DiScipio, R. G., P. J. Daffern, I. U. Schraufstatter, and P. Sriramarao. 1998. Human polymorphonuclear leukocytes adhere to complement factor H through an interaction that involves αMβ2 (CD11b/CD18). J. Immunol. 160: 4057-4066.
37. Jozsi, M., S. Heinen, A. Hartmann, C. W. Ostrowicz, S. Halbich, H. Richter, A. Kunert, C. Licht, R. E. Saunders, S. J. Perkins, et al. 2006. Factor H and atypical hemolytic uremic syndrome: mutations in the C-terminus cause structural changes and defective recognition functions. J. Am. Soc. Nephrol. 17: 170-177.
38. Duthy, T. G., R. J. Ormsby, E. Giannakis, A. D. Ogunniyi, U. H. Stroeher, J. C. Paton, and D. L. Gordon. 2002. The human complement regulator factor H binds pneumococcal surface protein PspC via short consensus repeats 13 to 15. Infect. Immun. 70: 5604-5611.
39. Hermans, P. W., P. V. Adrian, C. Albert, S. Estevao, T. Hoogenboezem, I. H. Luijendijk, T. Kamphausen, and S. Hammerschmidt. 2006. The streptococcal lipoprotein rotamase A (SlrA) is a functional peptidyl-prolyl isomerase involved in pneumococcal colonization. J. Biol. Chem. 281: 968-976.
40. Kuhn, S., and P. F. Zipfel. 1995. The baculovirus expression vector pBSV-8His directs secretion of histidine-tagged proteins. Gene 162: 225-229.
41. Kuhn, S., C. Skerka, and P. F. Zipfel. 1995. Mapping of the complement regulatory domains in the human factor H-like protein 1 and in factor H1. J. Immunol. 155: 5663-5670.
42. Oppermann, M., T. Manuelian, M. Jozsi, E. Brandt, T. S. Jokiranta, S. Heinen, S. Meri, C. Skerka, O. Gotze, and P. F. Zipfel. 2006. The C-terminus of complement regulator factor H mediates target recognition: evidence for a compact conformation of the native protein. Clin. Exp. Immunol. 144: 342-352.
43. Pracht, D., C. Elm, J. Gerber, S. Bergmann, M. Rohde, M. Seiler, K. S. Kim, H. F. Jenkinson, R. Nau, and S. Hammerschmidt. 2005. PavA of Streptococcus pneumoniae modulates adherence, invasion, and meningeal inflammation. Infect. Immun. 73: 2680-2689.
44. Ormsby, R. J., T. S. Jokiranta, T. G. Duthy, K. M. Griggs, T. A. Sadlon, E. Giannakis, and D. L. Gordon. 2006. Localization of the third heparin-binding site in the human complement regulator factor H1. Mol. Immunol. 43: 1624-1632.
45. Hammerschmidt, S., S. Wolff, A. Hocke, S. Rosseau, E. Muller, and M. Rohde. 2005. Illustration of pneumococcal polysaccharide capsule during adherence and invasion of epithelial cells. Infect. Immun. 73: 4653-4667.
46. Jarva, H., J. Hellwage, T. S. Jokiranta, M. J. Lehtinen, P. F. Zipfel, and S. Meri. 2004. The group B streptococcal β and pneumococcal Hic proteins are structurally related immune evasion molecules that bind the complement inhibitor factor H in an analogous fashion. J. Immunol. 172: 3111-3118.
47. Lu, L., Y. Ma, and J. R. Zhang. 2006. Streptococcus pneumoniae recruits complement factor H through the amino terminus of CbpA. J. Biol. Chem. 281: 15464-15474.
48. Kraiczy, P., and R. Wurzner. 2006. Complement escape of human pathogenic bacteria by acquisition of complement regulators. Mol. Immunol. 43: 31-44.
49. Yuste, J., M. Botto, J. C. Paton, D. W. Holden, and J. S. Brown. 2005. Additive inhibition of complement deposition by pneumolysin and PspA facilitates Streptococcus pneumoniae septicemia. J. Immunol. 175: 1813-1819.
50. Ren, B., M. A. McCrory, C. Pass, D. C. Bullard, C. M. Ballantyne, Y. Xu, D. E. Briles, and A. J. Szalai. 2004. The virulence function of Streptococcus pneumoniae surface protein A involves inhibition of complement activation and impairment of complement receptor-mediated protection 1. J. Immunol. 173: 7506-7512.
51. Ren, B., A. J. Szalai, O. Thomas, S. K. Hollingshead, and D. E. Briles. 2003. Both family 1 and family 2 PspA proteins can inhibit complement deposition and confer virulence to a capsular serotype 3 strain of Streptococcus pneumoniae. Infect. Immun. 71: 75-85.
52. Tu, A. H., R. L. Fulgham, M. A. McCrory, D. E. Briles, and A. J. Szalai. 1999. Pneumococcal surface protein A inhibits complement activation by Streptococcus pneumoniae. Infect. Immun. 67: 4720-4724.
53. Quin, L. R., C. Onwubiko, S. Carmicle, and L. S. McDaniel. 2006. Interaction of clinical isolates of Streptococcus pneumoniae with human complement factor H. FEMS Microbiol. Lett. 264: 98-103.
54. Pandiripally, V., L. Wei, C. Skerka, P. F. Zipfel, and D. Cue. 2003. Recruitment of complement factor H-like protein 1 promotes intracellular invasion by group A streptococci. Infect. Immun. 71: 7119-7128.
55. Tiraby, J. G., and M. S. Fox. 1974. Marker discrimination and mutagen-induced alterations in pneumococcal transformation. Genetics 77: 449-458.
56. Pearce, B. J., F. Iannelli, and G. Pozzi. 2002. Construction of new unencapsulated (rough) strains of Streptococcus pneumoniae. Res. Microbiol. 153: 243-247.