The Rickettsial OmpB β-peptide of Rickettsia conorii is sufficient to facilitate factor h-mediated serum resistance

Infection and Immunity

Volumn 80, Issue 8, 2012, Pages 2735-2743

  Riley, Sean P ^a,b   Patterson, Jennifer L ^a,c   Martinez, Juan J ^a,b  

^a UNIVERSITY OF CHICAGO   (United States)

^b Howard T Ricketts Laboratory   (United States)

^c Illinois State Police   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CELL ANTIGEN; COMPLEMENT FACTOR H; COMPLEMENT MEMBRANE ATTACK COMPLEX; RICKETTSIAL OMPB BETA PEPTIDE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL VIRULENCE; BACTERICIDAL ACTIVITY; CELL SURFACE; DISEASE PREDISPOSITION; FACILITATION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; RICKETTSIA CONORII;

AMINO ACID SEQUENCE; BACTERIAL OUTER MEMBRANE PROTEINS; CELL MEMBRANE; COMPLEMENT FACTOR H; GENE EXPRESSION REGULATION, BACTERIAL; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN SUBUNITS; RICKETTSIA CONORII;

EID: 84864807329     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00349-12     Document Type: Article

References (86)

1. Ahearn JM, Fearon DT. 1989. Structure and function of the complement receptors, CR1 (CD35) and CR2 (CD21). Adv. Immunol. 46:183-219.
2. Alexander JJ, Hack BK, Cunningham PN, Quigg RJ. 2001. A protein with characteristics of factorHis present on rodent platelets and functions as the immune adherence receptor. J. Biol. Chem. 276:32129 -32135.
3. Alitalo A, et al. 2001. Complement evasion by Borrelia burgdorferi: serum-resistant strains promote C3b inactivation. Infect. Immun. 69:3685- 3691.
4. Ammerman NC, Beier-Sexton M, Azad AF. 2008. Laboratory maintenance of Rickettsia rickettsii. Curr. Protoc. Microbiol. Chapter 3:Unit 3A5.
5. Aslam M, Perkins SJ. 2001. Folded-back solution structure of monomeric factor H of human complement by synchrotron X-ray and neutron scattering, analytical ultracentrifugation, and constrained molecular modeling. J. Mol. Biol. 309:1117-1138.
6. Bartra SS, et al. 2008. Resistance of Yersinia pestis to complementdependent killing is mediated by the Ail outer membrane protein. Infect. Immun. 76:612- 622.
7. Biedzka-Sarek M, Jarva H, Hyytiainen H, Meri S, Skurnik M. 2008. Characterization of complement factor H binding to Yersinia enterocolitica serotype O:3. Infect. Immun. 76:4100-4109.
8. Biedzka-Sarek M, et al. 2008. Functional mapping of YadA- and Ailmediated binding of human factor H to Yersinia enterocolitica serotype O:3. Infect. Immun. 76:5016 -5027.
9. Blackmore TK, Fischetti VA, Sadlon TA, Ward HM, Gordon DL. 1998. M protein of the group A streptococcus binds to the seventh short consensus repeat of human complement factor H. Infect. Immun. 66:1427- 1431.
10. Blanc G, et al. 2005. Molecular evolution of rickettsia surface antigens: evidence of positive selection. Mol. Biol. Evol. 22:2073-2083.
11. Blom AM, Hallstrom T, Riesbeck K. 2009. Complement evasion strategies of pathogens: acquisition of inhibitors and beyond. Mol. Immunol. 46:2808 -2817.
12. Carl M, Dobson ME, Ching WM, Dasch GA. 1990. Characterization of the gene encoding the protective paracrystalline-surface-layer protein of Rickettsia prowazekii: presence of a truncated identical homolog in Rickettsia typhi. Proc. Natl. Acad. Sci. U. S. A. 87:8237- 8241.
13. Chan YG, Cardwell MM, Hermanas TM, Uchiyama T, Martinez JJ. 2009. Rickettsial outer-membrane protein B (rOmpB) mediates bacterial invasion through Ku70 in an actin, c-Cbl, clathrin, and caveolin 2-dependent manner. Cell Microbiol. 11:629-644.
14. Chan YG, Riley SP, Chen E, Martinez JJ. 2011. Molecular basis of immunity to rickettsial infection conferred through outer membrane protein B. Infect. Immun. 79:2303-2313.
15. China B, Sory MP, N=Guyen BT, De Bruyere M, Cornelis GR. 1993. Role of the YadA protein in prevention of opsonization of Yersinia enterocolitica by C3b molecules. Infect. Immun. 61:3129 -3136.
16. Cirillo DM, et al. 1996. Identification of a domain in Rck, a product of the Salmonella typhimurium virulence plasmid, required for both serum resistance and cell invasion. Infect. Immun. 64:2019 -2023.
17. de Sousa R, Nobrega SD, Bacellar F, Torgal J. 2003. Mediterranean spotted fever in Portugal: risk factors for fatal outcome in 105 hospitalized patients. Ann. N. Y. Acad. Sci. 990:285-294.
18. Diaz A, Ferreira A, Sim RB. 1997. Complement evasion by Echinococcus granulosus: sequestration of host factor H in the hydatid cyst wall. J. Immunol. 158:3779 -3786.
19. DiScipio RG. 1992. Ultrastructures and interactions of complement factors H and I. J. Immunol. 149:2592-2599.
20. Duthy TG, et al. 2002. The human complement regulator factor H binds pneumococcal surface protein PspC via short consensus repeats 13 to 15. Infect. Immun. 70:5604 -5611.
21. Ember JA, Hugli TE. 1997. Complement factors and their receptors. Immunopharmacology 38:3-15.
22. Fairman JW, Noinaj N, Buchanan SK. The structural biology of betabarrel membrane proteins: a summary of recent reports. Curr. Opin. Struct. Biol. 21:523-531.
23. Fallman M, Andersson R, Andersson T. 1993. Signaling properties of CR3 (CD11b/CD18) and CR1 (CD35) in relation to phagocytosis of complement-opsonized particles. J. Immunol. 151:330 -338.
24. Ferreira VP, Pangburn MK, Cortes C. Complement control protein factor H: the good, the bad, and the inadequate. Mol. Immunol. 47:2187- 2197.
25. Gilmore RD, Jr, Cieplak W, Jr, Policastro PF, Hackstadt T. 1991. The 120-kilodalton outer membrane protein (rOmpB) of Rickettsia rickettsii is encoded by an unusually long open reading frame: evidence for protein processing from a large precursor. Mol. Microbiol. 5:2361-2370.
26. Gilmore RD, Jr, Joste N, McDonald GA. 1989. Cloning, expression and sequence analysis of the gene encoding the 120-kDa surface-exposed protein of Rickettsia rickettsii. Mol. Microbiol. 3:1579 -1586.
27. Hackstadt T, Messer R, Cieplak W, Peacock MG. 1992. Evidence for proteolytic cleavage of the 120-kilodalton outer membrane protein of rickettsiae: identification of an avirulent mutant deficient in processing. Infect. Immun. 60:159 -165.
28. Hallstrom T, et al. 2008. Haemophilus influenzae interacts with the human complement inhibitor factor H. J. Immunol. 181:537-545.
29. Hammerschmidt S, et al. 2007. 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. J. Immunol. 178: 5848-5858.
30. Harrison RA, Lachmann PJ. 1980. The physiological breakdown of the third component of human complement. Mol. Immunol. 17:9 -20.
31. Hellwage J, et al. 2001. The complement regulator factor H binds to the surface protein OspE of Borrelia burgdorferi. J. Biol. Chem. 276:8427- 8435.
32. Ho DK, Jarva H, Meri S. 2010. Human complement factor H binds to outer membrane protein Rck of Salmonella. J. Immunol. 185:1763-1769.
33. Horstmann RD, Muller-Eberhard HJ. 1985. Isolation of rabbit C3, factor B, and factor H and comparison of their properties with those of the human analog. J. Immunol. 134:1094 -1100.
34. Horstmann RD, Sievertsen HJ, Knobloch J, Fischetti VA. 1988. Antiphagocytic activity of streptococcal M protein: selective binding of complement control protein factor H. Proc. Natl. Acad. Sci. U. S. A. 85:1657- 1661.
35. Hu VW, Esser AF, Podack ER, Wisnieski BJ. 1981. The membrane attack mechanism of complement: photolabeling reveals insertion of terminal proteins into target membrane. J. Immunol. 127:380 -386.
36. Jacob-Dubuisson F, Fernandez R, Coutte L. 2004. Protein secretion through autotransporter and two-partner pathways. Biochim. Biophys. Acta 1694:235-257.
37. Johnsson E, et al. 1998. Role of the hypervariable region in streptococcal Mproteins: binding of a human complement inhibitor. J. Immunol. 161: 4894-4901.
38. Kelley LA, Sternberg MJ. 2009. Protein structure prediction on the Web: a case study using the Phyre server. Nat. Protoc. 4:363-371.
39. Kotarsky H, et al. 1998. Identification of a domain in human factorHand factor H-like protein-1 required for the interaction with streptococcal M proteins. J. Immunol. 160:3349 -3354.
40. Kraiczy P, Skerka C, Kirschfink M, Brade V, Zipfel PF. 2001. Immune evasion of Borrelia burgdorferi by acquisition of human complement regulators FHL-1/reconectin and factor H. Eur. J. Immunol. 31:1674 -1684.
41. Kristensen T, Tack BF. 1986. Murine protein H is comprised of 20 repeating units, 61 amino acids in length. Proc. Natl. Acad. Sci. U. S. A. 83:3963-3967.
42. Laarman A, Milder F, van Strijp J, Rooijakkers S. Complement inhibition by gram-positive pathogens: molecular mechanisms and therapeutic implications. J. Mol. Med. (Berlin) 88:115-120.
43. Lambris JD, Ricklin D, Geisbrecht BV. 2008. Complement evasion by human pathogens. Nat. Rev. Microbiol. 6:132-142.
44. Leffler J, et al. 2010. Annexin II, DNA, and histones serve as factor H ligands on the surface of apoptotic cells. J. Biol. Chem. 285:3766 -3776.
45. Madico G, et al. 2007. Factor H binding and function in sialylated pathogenic neisseriae is influenced by gonococcal, but not meningococcal, porin. J. Immunol. 178:4489-4497.
46. Martin DE, Chiu FJ, Gigli I, Muller-Eberhard HJ. 1987. Killing of human melanoma cells by the membrane attack complex of human complement as a function of its molecular composition. J. Clin. Invest. 80: 226-233.
47. Maruvada R, Blom AM, Prasadarao NV. 2008. Effects of complement regulators bound to Escherichia coli K1 and group B streptococcus on the interaction with host cells. Immunology 124:265-276.
48. Mayer MM. 1981. Membrane damage by complement. Johns Hopkins Med. J. 148:243-258.
49. McDowell JV, Huang B, Fenno JC, Marconi RT. 2009. Analysis of a unique interaction between the complement regulatory protein factor H and the periodontal pathogen Treponema denticola. Infect. Immun. 77: 1417-1425.
50. Meri S, Jarva H. 1998. Complement regulation. Vox Sang 74(Suppl 2): 291-302.
51. Miller VL, Beer KB, Heusipp G, Young BM, Wachtel MR. 2001. Identification of regions of Ail required for the invasion and serum resistance phenotypes. Mol. Microbiol. 41:1053-1062.
52. Muller-Eberhard HJ. 1986. The membrane attack complex of complement. Annu. Rev. Immunol. 4:503-528.
53. Neeleman C, et al. 1999. Resistance to both complement activation and phagocytosis in type 3 pneumococci is mediated by the binding of complement regulatory protein factor H. Infect. Immun. 67:4517- 4524.
54. Nilsson UR, Mueller-Eberhard HJ. 1965. Isolation of beta If-globulin from human serum and its characterization as the fifth component of complement. J. Exp. Med. 122:277-298.
55. Pangburn MK, Schreiber RD, Muller-Eberhard HJ. 1977. Human complement C3b inactivator: isolation, characterization, and demonstration of an absolute requirement for the serum protein β1H for cleavage of C3b and C4b in solution. J. Exp. Med. 146:257-270.
56. Perkins SJ, Haris PI, Sim RB, Chapman D. 1988. A study of the structure of human complement component factorHby Fourier transform infrared spectroscopy and secondary structure averaging methods. Biochemistry 27:4004-4012.
57. Perkins SJ, et al. 2010. Multiple interactions of complement factorHwith its ligands in solution: a progress report. Adv. Exp. Med. Biol. 703:25- 47.
58. Perkins SJ, Nealis AS, Sim RB. 1991. Oligomeric domain structure of human complement factor H by X-ray and neutron solution scattering. Biochemistry 30:2847-2857.
59. Podack ER, Tschopp J. 1982. Polymerization of the ninth component of complement (C9): formation of poly(C9) with a tubular ultrastructure resembling the membrane attack complex of complement. Proc. Natl. Acad. Sci. U. S. A. 79:574 -578.
60. Quin LR, et al. 2007. Factor H binding to PspC of Streptococcus pneumoniae increases adherence to human cell lines in vitro and enhances invasion of mouse lungs in vivo. Infect. Immun. 75:4082- 4087.
61. Ram S, et al. 1999. The contrasting mechanisms of serum resistance of Neisseria gonorrhoeae and group B Neisseria meningitidis. Mol. Immunol. 36:915-928.
62. Ram S, et al. 1998. Binding of complement factor H to loop 5 of porin protein 1A: a molecular mechanism of serum resistance of nonsialylated Neisseria gonorrhoeae. J. Exp. Med. 188:671- 680.
63. Raoult D, Roux V. 1997. Rickettsioses as paradigms of new or emerging infectious diseases. Clin. Microbiol. Rev. 10:694 -719.
64. Renesto P, et al. 2006. Identification of two putative rickettsial adhesins by proteomic analysis. Res. Microbiol. 157:605- 612.
65. Rodriguez de Cordoba S, Esparza-Gordillo J, Goicoechea de Jorge E, Lopez-Trascasa M, Sanchez-Corral P. 2004. The human complement factor H: functional roles, genetic variations and disease associations. Mol. Immunol. 41:355-367.
66. Schneider MC, et al. 2006. Functional significance of factor H binding to Neisseria meningitidis. J. Immunol. 176:7566 -7575.
67. Shaughnessy J, et al. 2011. Molecular characterization of the interaction between sialylated Neisseria gonorrhoeae and factor H. J. Biol. Chem. 286: 22235-22242.
68. Silverman DJ, and Wisseman CL, Jr. 1978. Comparative ultrastructural study on the cell envelopes of Rickettsia prowazekii, Rickettsia rickettsii, and Rickettsia tsutsugamushi. Infect. Immun. 21:1020 -1023.
69. Stevenson B, El-Hage N, Hines MA, Miller JC, Babb K. 2002. Differential binding of host complement inhibitor factor H by Borrelia burgdorferi Erp surface proteins: a possible mechanism underlying the expansive host range of Lyme disease spirochetes. Infect. Immun. 70:491- 497.
70. Stoiber H, Clivio A, Dierich MP. 1997. Role of complement in HIV infection. Annu. Rev. Immunol. 15:649-674.
71. Stoiber H, Pinter C, Siccardi AG, Clivio A, Dierich MP. 1996. Efficient destruction of human immunodeficiency virus in human serum by inhibiting the protective action of complement factor H and decay accelerating factor (DAF, CD55). J. Exp. Med. 183:307-310.
72. Stoiber H, Schneider R, Janatova J, Dierich MP. 1995. Human complement proteins C3b, C4b, factorHand properdin react with specific sites in gp120 and gp41, the envelope proteins of HIV-1. Immunobiology. 193: 98-113.
73. Tegla CA, et al. 2011. Membrane attack by complement: the assembly and biology of terminal complement complexes. Immunol. Res. 51:45- 60.
74. Thanassi DG, et al. 1998. The PapC usher forms an oligomeric channel: implications for pilus biogenesis across the outer membrane. Proc. Natl. Acad. Sci. U. S. A. 95:3146 -3151.
75. Uchiyama T, Kawano H, Kusuhara Y. 2006. The major outer membrane protein rOmpB of spotted fever group rickettsiae functions in the rickettsial adherence to and invasion of Vero cells. Microbes Infect. 8:801- 809.
76. Van den Berg B. 2010. Crystal structure of a full-length autotransporter. J. Mol. Biol. 396:627- 633.
77. Walker DH, Gear JH. 1985. Correlation of the distribution of Rickettsia conorii, microscopic lesions, and clinical features in South African tick bite fever. Am. J. Trop. Med. Hyg. 34:361-371.
78. Walport MJ. 2001. Complement: first of two parts. N. Engl. J. Med. 344: 1058-1066.
79. Walport MJ. 2001. Complement: second of two parts. N. Engl. J. Med. 344:1140 -1144.
80. Weiler JM, Daha MR, Austen KF, Fearon DT. 1976. Control of the amplification convertase of complement by the plasma protein beta1H. Proc. Natl. Acad. Sci. U. S. A. 73:3268 -3272.
81. Weinert LA, Tinsley MC, Temperley M, Jiggins FM. 2007. Are we underestimating the diversity and incidence of insect bacterial symbionts? A case study in ladybird beetles. Biol. Lett. 3:678-681.
82. Whaley K, Schur PH, Ruddy S. 1976. C3b inactivator in the rheumatic diseases: measurement by radial immunodiffusion and by inhibition of formation of properdin pathway C3 convertase. J. Clin. Invest. 57:1554- 1563.
83. Wimley WC. 2003. The versatile beta-barrel membrane protein. Curr. Opin. Struct. Biol. 13:404-411.
84. Xia Y, et al. 1999. The beta-glucan-binding lectin site of mouse CR3 (CD11b/CD18) and its function in generating a primed state of the receptor that mediates cytotoxic activation in response to iC3b-opsonized target cells. J. Immunol. 162:2281-2290.
85. Zipfel PF, Skerka C. 2009. Complement regulators and inhibitory proteins. Nat. Rev. Immunol. 9:729 -740.
86. Zipfel PF, et al. 2002. Factor H family proteins: on complement, microbes, and human diseases. Biochem. Soc. Trans. 30:971-978.