Factor h-dependent alternative pathway inhibition mediated by porin B contributes to virulence of Neisseria meningitidis

mBio

Volumn 4, Issue 5, 2013, Pages

  Lewis, Lisa A ^a   Vu, David M ^b   Vasudhev, Shreekant ^a   Shaughnessy, Jutamas ^a   Granoff, Dan M ^b   Ram, Sanjay ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b CHILDREN S HOSPITAL OAKLAND RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL POLYSACCHARIDE; BACTERIAL PROTEIN; CAPSULAR POLYSACCHARIDE; COMPLEMENT COMPONENT C3A; COMPLEMENT FACTOR H; FACTOR H BINDING PROTEIN; FACTOR H BINDING PROTEIN VACCINE; FACTOR H LIKE PROTEIN 1; IMMUNOGLOBULIN FC FRAGMENT; MENINGOCOCCUS VACCINE; NEISSERIAL SURFACE PROTEIN A; PORIN B PROTEIN; PORIN B2 PROTEIN; PORIN B3 PROTEIN; SIALIC ACID; UNCLASSIFIED DRUG;

ALLELE; ARTICLE; BACTERIAL CAPSULE; BACTERIAL STRAIN; BACTERIAL VIRULENCE; BINDING AFFINITY; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT DEPOSITION; CONTROLLED STUDY; HUMAN; IMMUNOREGULATION; MOUSE; NEISSERIA MENINGITIDIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; RABBIT; STRAIN DIFFERENCE;

ANIMALS; ANTIGENS, BACTERIAL; BACTERIAL PROTEINS; COMPLEMENT C3-C5 CONVERTASES, ALTERNATIVE PATHWAY; COMPLEMENT FACTOR H; DOWN-REGULATION; FEMALE; HUMANS; MALE; MENINGITIS, MENINGOCOCCAL; MICE; MICE, INBRED BALB C; NEISSERIA MENINGITIDIS; PORINS; RABBITS; VIRULENCE;

EID: 84887153617     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.00339-13     Document Type: Article

References (37)

1. Ram S, Lewis LA, Rice PA. 2010. Infections of people with complement deficiencies and patients who have undergone splenectomy. Clin. Microbiol. Rev. 23:740-780.
2. Austen KF, Fearon DT. 1979. A molecular basis of activation of the alternative pathway of human complement. Adv. Exp. Med. Biol. 120B: 3-17.
3. Giuntini S, Reason DC, Granoff DM. 2012. The combined roles of human IgG subclass, alternative complement pathway activation, and epitope density on bactericidal activity of antibodies to meningococcal factor H binding protein. Infect. Immun. 80:187-194.
4. Ferreira VP, Pangburn MK, Cortés C. 2010. Complement control protein factor H: the good, the bad, and the inadequate. Mol. Immunol. 47:2187-2197.
5. Madico G, Welsch JA, Lewis LA, McNaughton A, Perlman DH, Costello CE, Ngampasutadol J, Vogel U, Granoff DM, Ram S. 2006. The meningococcal vaccine candidate GNA1870 binds the complement regulatory protein factor H and enhances serum resistance. J. Immunol. 177: 501-510.
6. Lewis LA, Ngampasutadol J, Wallace R, Reid JE, Vogel U, Ram S. 2010. The meningococcal vaccine candidate neisserial surface protein A (NspA) binds to factor H and enhances meningococcal resistance to complement. PLoS Pathog. 6:e1001027.
7. Lewis LA, Carter M, Ram S. 2012. The relative roles of factor H binding protein, neisserial surface protein A, and lipooligosaccharide sialylation in regulation of the alternative pathway of complement on meningococci. J. Immunol. 188:5063-5072.
8. Jarvis GA, Vedros NA. 1987. Sialic acid of group B Neisseria meningitides regulates alternative complement pathway activation. Infect. Immun. 55: 174-180.
9. Ram S, Lewis LA, Agarwal S. 2011. Meningococcal group W-135 and Y capsular polysaccharides paradoxically enhance activation of the alternative pathway of complement. J. Biol. Chem. 286:8297-8307.
10. Granoff DM, Welsch JA, Ram S. 2009. Binding of complement factor H (fH) to Neisseria meningitidis is specific for human fH and inhibits complement activation by rat and rabbit sera. Infect. Immun. 77:764-769.
11. Vu DM, Shaughnessy J, Lewis LA, Ram S, Rice PA, Granoff DM. 2012. Enhanced bacteremia in human factor H transgenic rats infected by Neisseria meningitidis. Infect. Immun. 80:643-650.
12. Lucidarme J, Tan L, Exley RM, Findlow J, Borrow R, Tang CM. 2011. Characterization of Neisseria meningitidis isolates that do not express the virulence factor and vaccine antigen factor H binding protein. Clin. Vaccine Immunol. 18:1002-1014.
13. Lewis LA, Ram S, Prasad A, Gulati S, Getzlaff S, Blom AM, Vogel U, Rice PA. 2008. Defining targets for complement components C4b and C3b on the pathogenic neisseriae. Infect. Immun. 76:339-350.
14. Ram S, Cox AD, Wright JC, Vogel U, Getzlaff S, Boden R, Li J, Plested JS, Meri S, Gulati S, Stein DC, Richards JC, Moxon ER, Rice PA. 2003. Neisserial lipooligosaccharide is a target for complement component C4b: inner core phosphoethanolamine residues define C4b linkage specificity. J. Biol. Chem. 278:50853-50862.
15. Nawar H, Smith K, Amer L, Vann W, Bash M. 2012. Analysis of the effect of antigenic diversity of the Neisseria meningitidis outer membrane porin B protein (PorB) on strain fitness, p 202. In Frosch M, Rudel T, Vogel U (ed), XVIIIth International Pathogenic Neisseria Conference. Wuerzburg, Germany. Conventus Congressmanagement and Marketing GmbH, Jena, Germany.
16. Blom AM, Hallström T, Riesbeck K. 2009. Complement evasion strategies of pathogens-acquisition of inhibitors and beyond. Mol. Immunol. 46:2808-2817.
17. Shaughnessy J, Lewis LA, Jarva H, Ram S. 2009. Functional comparison of the binding of factor H short consensus repeat 6 (SCR 6) to factor H binding protein from Neisseria meningitidis and the binding of factor H SCR 18 to 20 to Neisseria gonorrhoeae porin. Infect. Immun. 77: 2094-2103.
18. Zipfel PF, Skerka C. 1999. FHL-1/reconnection: a human complement and immune regulator with cell-adhesive function. Immunol. Today 20: 135-140.
19. Granoff DM, Bartoloni A, Ricci S, Gallo E, Rosa D, Ravenscroft N, Guarnieri V, Seid RC, Shan A, Usinger WR, Tan S, McHugh YE, Moe GR. 1998. Bactericidal monoclonal antibodies that define unique meningococcal B polysaccharide epitopes that do not cross-react with human polysialic acid. J. Immunol. 160:5028-5036.
20. Tanabe M, Nimigean CM, Iverson TM. 2010. Structural basis for solute transport, nucleotide regulation, and immunological recognition of Neisseria meningitidis PorB. Proc. Natl. Acad. Sci. U. S. A. 107:6811-6816.
21. Ram S, Cullinane M, Blom AM, Gulati S, McQuillen DP, Monks BG, O'Connell C, Boden R, Elkins C, Pangburn MK, Dahlbäck B, Rice PA. 2001. Binding of C4b-binding protein to porin: a molecular mechanism of serum resistance of Neisseria gonorrhoeae. J. Exp. Med. 193:281-296.
22. Ram S, McQuillen DP, Gulati S, Elkins C, Pangburn MK, Rice PA. 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.
23. Massari P, Visintin A, Gunawardana J, Halmen KA, King CA, Golenbock DT, Wetzler LM. 2006. Meningococcal porin PorB binds to TLR2 and requires TLR1 for signaling. J. Immunol. 176:2373-2380.
24. Giuntini S, Vu DM, Granoff DM. 2013. fH-dependent complement evasion by disease-causing meningococcal strains with absent fHbp genes or frameshift mutations. Vaccine 31:4192-4199.
25. Nissen MD, Marshall HS, Richmond PC, Jiang Q, Harris SL, Jones TR, Jansen KU, Perez JL. 2013. A randomized, controlled, phase 1/2 trial of a Neisseria meningitidis serogroup B bivalent rLP2086 vaccine in healthy children and adolescents. Pediatr. Infect. Dis. J. 32:364-371.
26. Santolaya ME, O'Ryan ML, Valenzuela MT, Prado V, Vergara R, Muñoz A, Toneatto D, Graña G, Wang H, Clemens R, Dull PM, V72P10 Meningococcal B Adolescent Vaccine Study Group. 2012. Immunogenicity and tolerability of a multicomponent meningococcal serogroup B (4CMenB) vaccine in healthy adolescents in Chile: a phase 2b/3 randomised, observer-blind, placebo-controlled study. Lancet 379: 617-624.
27. Jelfs J, Munro R, Wedege E, Caugant DA. 2000. Sequence variation in the porA gene of a clone of Neisseria meningitidis during epidemic spread. Clin. Diagn. Lab. Immunol. 7:390-395.
28. Van der Ende A, Hopman CT, Dankert J. 1999. Deletion of porA by recombination between clusters of repetitive extragenic palindromic sequences in Neisseria meningitidis. Infect. Immun. 67:2928-2934.
29. Elias J, Vogel U. 2007. IS1301 fingerprint analysis of Neisseria meningitidis strains belonging to the ET-15 clone. J. Clin. Microbiol. 45:159-167.
30. Seib KL, Brunelli B, Brogioni B, Palumbo E, Bambini S, Muzzi A, DiMarcello F, Marchi S, van der Ende A, Aricó B, Savino S, Scarselli M, Comanducci M, Rappuoli R, Giuliani MM, Pizza M. 2011. Characterization of diverse subvariants of the meningococcal factor H (fH) binding protein for their ability to bind fH, to mediate serum resistance, and to induce bactericidal antibodies. Infect. Immun. 79:970-981.
31. Dunphy KY, Beernink PT, Brogioni B, Granoff DM. 2011. Effect of factor H-binding protein sequence variation on factor H binding and survival of Neisseria meningitidis in human blood. Infect. Immun. 79: 353-359.
32. Makou E, Mertens HD, Maciejewski M, Soares DC, Matis I, Schmidt CQ, Herbert AP, Svergun DI, Barlow PN. 2012. Solution structure of CCP modules 10-12 illuminates functional architecture of the complement regulator, factor H. J. Mol. Biol. 424:295-312.
33. Okemefuna AI, Nan R, Gor J, Perkins SJ. 2009. Electrostatic interactions contribute to the folded-back conformation of wild type human factor H. J. Mol. Biol. 391:98-118.
34. Madico G, Ngampasutadol J, Gulati S, Vogel U, Rice PA, Ram S. 2007. Factor H binding and function in sialylated pathogenic neisseriae is influenced by gonococcal, but not meningococcal, porin. J. Immunol. 178: 4489-4497.
35. Hammer CH, Wirtz GH, Renfer L, Gresham HD, Tack BF. 1981. Large scale isolation of functionally active components of the human complement system. J. Biol. Chem. 256:3995-4006.
36. Ngampasutadol J, Ram S, Gulati S, Agarwal S, Li C, Visintin A, Monks B, Madico G, Rice PA. 2008. Human factor H interacts selectively with Neisseria gonorrhoeae and results in species-specific complement evasion. J. Immunol. 180:3426-3435.
37. Visintin A, Halmen KA, Latz E, Monks BG, Golenbock DT. 2005. Pharmacological inhibition of endotoxin responses is achieved by targeting the TLR4 coreceptor, MD-2. J. Immunol. 175:6465-6472.