Staphylococcal Ecb protein and host complement regulator factor H enhance functions of each other in bacterial immune evasion

Journal of Immunology

Volumn 191, Issue 4, 2013, Pages 1775-1784

  Amdahl, Hanne ^a   Jongerius, Ilse ^b,d   Meri, Taru ^a,c   Pasanen, Tanja ^a,c   Hyvärinen, Satu ^a   Haapasalo, Karita ^a   Van Strijp, Jos A ^b   Rooijakkers, Suzan H ^b   Sakari Jokiranta, T ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^c UNIVERSITY OF HELSINKI   (Finland)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING PROTEIN; COMPLEMENT COMPONENT C3B; COMPLEMENT COMPONENT C3D; COMPLEMENT FACTOR H; EXTRACELLULAR COMPLEMENT BINDING PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CARBOXY TERMINAL SEQUENCE; CELL SURFACE; COMPLEMENT ACTIVATION; COMPLEX FORMATION; CONTROLLED STUDY; DOWN REGULATION; HAEMOPHILUS INFLUENZAE; HOST; HUMAN; IMMUNE EVASION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; STAPHYLOCOCCUS AUREUS;

BACTERIAL PROTEINS; BINDING SITES; COMPLEMENT C3B; COMPLEMENT FACTOR H; COMPLEMENT INACTIVATOR PROTEINS; COMPLEMENT PATHWAY, ALTERNATIVE; HAEMOPHILUS INFLUENZAE; HUMANS; IMMUNE EVASION; IMMUNITY, INNATE; MODELS, MOLECULAR; MULTIPROTEIN COMPLEXES; PEPTIDE FRAGMENTS; POINT MUTATION; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; PROTEIN STRUCTURE, TERTIARY; SERUM; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; VIRULENCE FACTORS;

EID: 84881439690     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1300638     Document Type: Article

References (54)

1. Lowy, F. D. 1998. Staphylococcus aureus infections. N. Engl. J. Med. 339: 520-532.
2. Otto, M. 2010. Novel targeted immunotherapy approaches for staphylococcal infection. Expert Opin. Biol. Ther. 10: 1049-1059.
3. Proctor, R. A. 2012. Challenges for a universal Staphylococcus aureus vaccine. Clin. Infect. Dis. 54: 1179-1186.
4. Rooijakkers, S. H., K. P. van Kessel, and J. A. van Strijp. 2005. Staphylococcal innate immune evasion. Trends Microbiol. 13: 596-601.
5. Walport, M. J. 2001. Complement. First of two parts. N. Engl. J. Med. 344: 1058-1066.
6. Pangburn, M. K., and H. J. Müller-Eberhard. 1986. The C3 convertase of the alternative pathway of human complement. Enzymic properties of the bimolecular proteinase. Biochem. J. 235: 723-730.
7. Forneris, F., D. Ricklin, J. Wu, A. Tzekou, R. S. Wallace, J. D. Lambris, and P. Gros. 2010. Structures of C3b in complex with factors B and D give insight into complement convertase formation. Science 330: 1816-1820.
8. Esparza-Gordillo, J., J. M. Soria, A. Buil, L. Almasy, J. Blangero, J. Fontcuberta, and S. Rodríguez de Córdoba. 2004. Genetic and environmental factors influencing the human factor H plasma levels. Immunogenetics 56: 77-82.
9. Kühn, 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.
10. Gordon, D. L., R. M. Kaufman, T. K. Blackmore, J. Kwong, and D. M. Lublin. 1995. Identification of complement regulatory domains in human factor H. J. Immunol. 155: 348-356.
11. Whaley, K., and S. Ruddy. 1976. Modulation of the alternative complement pathways by beta 1 H globulin. J. Exp. Med. 144: 1147-1163.
12. Wu, J., Y. Q. Wu, D. Ricklin, B. J. Janssen, J. D. Lambris, and P. Gros. 2009. Structure of complement fragment C3b-factor H and implications for host protection by complement regulators. Nat. Immunol. 10: 728-733.
13. 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.
14. Meri, S., and M. K. Pangburn. 1990. Discrimination between activators and nonactivators 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.
15. Pangburn, M. K. 2002. Cutting edge: localization of the host recognition functions of complement factor H at the carboxyl-terminal: implications for hemolytic uremic syndrome. J. Immunol. 169: 4702-4706.
16. Jokiranta, T. S., Z. Z. Cheng, H. Seeberger, M. Jò zsi, S. Heinen, M. Noris, G. Remuzzi, R. Ormsby, D. L. Gordon, S. Meri, et al. 2005. Binding of complement factor H to endothelial cells is mediated by the carboxy-terminal glycosaminoglycan binding site. Am. J. Pathol. 167: 1173-1181.
17. Kavanagh, D., and T. Goodship. 2010. Genetics and complement in atypical HUS. Pediatr. Nephrol. 25: 2431-2442.
18. Kajander, T., M. J. Lehtinen, S. Hyvärinen, A. Bhattacharjee, E. Leung, D. E. Isenman, S. Meri, A. Goldman, and T. S. Jokiranta. 2011. Dual interaction of factor H with C3d and glycosaminoglycans in host-nonhost discrimination by complement. Proc. Natl. Acad. Sci. USA 108: 2897-2902.
19. Morgan, H. P., C. Q. Schmidt, M. Guariento, B. S. Blaum, D. Gillespie, A. P. Herbert, D. Kavanagh, H. D. Mertens, D. I. Svergun, C. M. Johansson, et al. 2011. Structural basis for engagement by complement factor H of C3b on a self surface. Nat. Struct. Mol. Biol. 18: 463-470.
20. Hallström, T., T. Nordström, T. T. Tan, T. Manolov, J. D. Lambris, D. E. Isenman, P. F. Zipfel, A. M. Blom, and K. Riesbeck. 2011. Immune evasion of Moraxella catarrhalis involves ubiquitous surface protein A-dependent C3d binding. J. Immunol. 186: 3120-3129.
21. Lambris, J. D., D. Ricklin, and B. V. Geisbrecht. 2008. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6: 132-142.
22. Meri, T., H. Amdahl, M. J. Lehtinen, S. Hyvärinen, J. V. McDowell, A. Bhattacharjee, S. Meri, R. Marconi, A. Goldman, and T. S. Jokiranta. 2013. Microbes bind complement inhibitor factor H via a common site. PLoS Pathog. 9: e1003308.
23. Rooijakkers, S. H., M. Ruyken, A. Roos, M. R. Daha, J. S. Presanis, R. B. Sim, W. J. van Wamel, K. P. van Kessel, and J. A. van Strijp. 2005. Immune evasion by a staphylococcal complement inhibitor that acts on C3 convertases. Nat. Immunol. 6: 920-927.
24. Rooijakkers, S. H., J. Wu, M. Ruyken, R. van Domselaar, K. L. Planken, A. Tzekou, D. Ricklin, J. D. Lambris, B. J. Janssen, J. A. van Strijp, and P. Gros. 2009. Structural and functional implications of the alternative complement pathway C3 convertase stabilized by a staphylococcal inhibitor. Nat. Immunol. 10: 721-727.
25. Ricklin, D., A. Tzekou, B. L. Garcia, M. Hammel, W. J. McWhorter, G. Sfyroera, Y. Q. Wu, V. M. Holers, A. P. Herbert, P. N. Barlow, et al. 2009. A molecular insight into complement evasion by the staphylococcal complement inhibitor protein family. J. Immunol. 183: 2565-2574.
26. Haupt, K., M. Reuter, J. van den Elsen, J. Burman, S. Hälbich, J. Richter, C. Skerka, and P. F. Zipfel. 2008. The Staphylococcus aureus protein Sbi acts as a complement inhibitor and forms a tripartite complex with host complement Factor H and C3b. PLoS Pathog. 4: e1000250.
27. Burman, J. D., E. Leung, K. L. Atkins, M. N. O'Seaghdha, L. Lango, P. Bernadó, S. Bagby, D. I. Svergun, T. J. Foster, D. E. Isenman, and J. M. van den Elsen. 2008. Interaction of human complement with Sbi, a staphylococcal immunoglobulin-binding protein: indications of a novel mechanism of complement evasion by Staphylococcus aureus. J. Biol. Chem. 283: 17579-17593.
28. Bodén, M. K., and J. I. Flock. 1994. Cloning and characterization of a gene for a 19 kDa fibrinogen-binding protein from Staphylococcus aureus. Mol. Microbiol. 12: 599-606.
29. Shannon, O., A. Uekötter, and J. I. Flock. 2005. Extracellular fibrinogen binding protein, Efb, from Staphylococcus aureus as an antiplatelet agent in vivo. Thromb. Haemost. 93: 927-931.
30. Lee, L. Y., X. Liang, M. Höök, and E. L. Brown. 2004. Identification and characterization of the C3 binding domain of the Staphylococcus aureus extracellular fibrinogen-binding protein (Efb). J. Biol. Chem. 279: 50710-50716.
31. Hammel, M., G. Sfyroera, S. Pyrpassopoulos, D. Ricklin, K. X. Ramyar, M. Pop, Z. Jin, J. D. Lambris, and B. V. Geisbrecht. 2007. Characterization of Ehp, a secreted complement inhibitory protein from Staphylococcus aureus. J. Biol. Chem. 282: 30051-30061.
32. Jongerius, I., J. Köhl, M. K. Pandey, M. Ruyken, K. P. van Kessel, J. A. van Strijp, and S. H. Rooijakkers. 2007. Staphylococcal complement evasion by various convertase-blocking molecules. J. Exp. Med. 204: 2461-2471.
33. Jongerius, I., M. von Köckritz-Blickwede, M. J. Horsburgh, M. Ruyken, V. Nizet, and S. H. Rooijakkers. 2012. Staphylococcus aureus virulence is enhanced by secreted factors that block innate immune defenses. J. Innate Immun. 4: 301-311.
34. Palma, M., O. Shannon, H. C. Quezada, A. Berg, and J. I. Flock. 2001. Extracellular fibrinogen-binding protein, Efb, from Staphylococcus aureus blocks platelet aggregation due to its binding to the alpha-chain. J. Biol. Chem. 276: 31691-31697.
35. Jongerius, I., B. L. Garcia, B. V. Geisbrecht, J. A. van Strijp, and S. H. Rooijakkers. 2010. Convertase inhibitory properties of staphylococcal extracellular complement-binding protein. J. Biol. Chem. 285: 14973-14979.
36. Chen, H., D. Ricklin, M. Hammel, B. L. Garcia, W. J. McWhorter, G. Sfyroera, Y. Q. Wu, A. Tzekou, S. Li, B. V. Geisbrecht, et al. 2010. Allosteric inhibition of complement function by a staphylococcal immune evasion protein. Proc. Natl. Acad. Sci. USA 107: 17621-17626.
37. Ricklin, D., S. K. Ricklin-Lichtsteiner, M. M. Markiewski, B. V. Geisbrecht, and J. D. Lambris. 2008. Cutting edge: members of the Staphylococcus aureus extracellular fibrinogen-binding protein family inhibit the interaction of C3d with complement receptor 2. J. Immunol. 181: 7463-7467.
38. Hammel, M., G. Sfyroera, D. Ricklin, P. Magotti, J. D. Lambris, and B. V. Geisbrecht. 2007. A structural basis for complement inhibition by Staphylococcus aureus. Nat. Immunol. 8: 430-437.
39. Haapasalo, K., H. Jarva, T. Siljander, W. Tewodros, J. Vuopio-Varkila, and T. S. Jokiranta. 2008. Complement factor H allotype 402H is associated with increased C3b opsonization and phagocytosis of Streptococcus pyogenes. Mol. Microbiol. 70: 583-594.
40. Jokiranta, T. S., V. P. Jaakola, M. J. Lehtinen, M. Pärepalo, 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.
41. Lehtinen, M. J., A. L. Rops, D. E. Isenman, J. van der Vlag, and T. S. Jokiranta. 2009. Mutations of factor H impair regulation of surface-bound C3b by three mechanisms in atypical hemolytic uremic syndrome. J. Biol. Chem. 284: 15650-15658.
42. Blanc, C., L. T. Roumenina, Y. Ashraf, S. Hyvärinen, S. K. Sethi, B. Ranchin, P. Niaudet, C. Loirat, A. Gulati, A. Bagga, et al. 2012. Overall neutralization of complement factor H by autoantibodies in the acute phase of the autoimmune form of atypical hemolytic uremic syndrome. J. Immunol. 189: 3528-3537.
43. Koistinen, V., S. Wessberg, and J. Leikola. 1989. Common binding region of complement factors B, H and CR1 on C3b revealed by monoclonal anti-C3d. Complement Inflamm. 6: 270-280.
44. Jokiranta, T. S., P. F. Zipfel, J. Hakulinen, S. Kühn, M. K. Pangburn, J. D. Tamerius, and S. Meri. 1996. Analysis of the recognition mechanism of the alternative pathway of complement by monoclonal anti-factor H antibodies: evidence for multiple interactions between H and surface bound C3b. FEBS Lett. 393: 297-302.
45. Krych-Goldberg, M., R. E. Hauhart, V. B. Subramanian, B. M. Yurcisin, II, D. L. Crimmins, D. E. Hourcade, and J. P. Atkinson. 1999. Decay accelerating activity of complement receptor type 1 (CD35). Two active sites are required for dissociating C5 convertases. J. Biol. Chem. 274: 31160-31168.
46. Jokiranta, T. S., J. Hellwage, V. Koistinen, P. F. Zipfel, and S. Meri. 2000. Each of the three binding sites on complement factor H interacts with a distinct site on C3b. J. Biol. Chem. 275: 27657-27662.
47. Koch, T. K., M. Reuter, D. Barthel, S. Böhm, J. van den Elsen, P. Kraiczy, P. F. Zipfel, and C. Skerka. 2012. Staphylococcus aureus proteins Sbi and Efb recruit human plasmin to degrade complement C3 and C3b. PLoS ONE 7: e47638.
48. Sharp, J. A., and K. M. Cunnion. 2011. Disruption of the alternative pathway convertase occurs at the staphylococcal surface via the acquisition of factor H by Staphylococcus aureus. Mol. Immunol. 48: 683-690.
49. Hellwage, J., T. Meri, T. Heikkilä, A. Alitalo, J. Panelius, P. Lahdenne, I. J. Seppälä, and S. Meri. 2001. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276: 8427-8435.
50. Madico, G., J. A. Welsch, L. A. Lewis, A. McNaughton, D. H. Perlman, C. E. Costello, J. Ngampasutadol, U. Vogel, D. M. Granoff, and S. Ram. 2006. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 177: 501-510.
51. 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.
52. 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.
53. Luo, S., S. Poltermann, A. Künert, S. Rupp, and P. F. Zipfel. 2009. Immune evasion of the human pathogenic yeast Candida albicans: Pra1 is a Factor H, FHL-1 and plasminogen binding surface protein. Mol. Immunol. 47: 541-550.
54. Smith, E. J., L. Visai, S. W. Kerrigan, P. Speziale, and T. J. Foster. 2011. The Sbi protein is a multifunctional immune evasion factor of Staphylococcus aureus. Infect. Immun. 79: 3801-3809.