Additive inhibition of complement deposition by pneumolysin and PspA facilitates Streptococcus pneumoniae septicemia

Journal of Immunology

Volumn 175, Issue 3, 2005, Pages 1813-1819

  Yuste, Jose ^a   Botto, Marina ^b   Paton, James C ^c   Holden, David W ^b   Brown, Jeremy S ^a  

^a ROYAL FREE AND UNIVERSITY COLLEGE MEDICAL SCHOOL   (United Kingdom)

^b IMPERIAL COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF ADELAIDE   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PNEUMOLYSIN; PROTEIN PSPA; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIUM MUTANT; COMPLEMENT ALTERNATIVE PATHWAY; COMPLEMENT CLASSICAL PATHWAY; COMPLEMENT DEPOSITION; COMPLEMENT INHIBITION; COMPLEMENT SYSTEM; CONTROLLED STUDY; IMMUNE RESPONSE; IMMUNOCOMPETENCE; LUNG INFECTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; SEPTICEMIA; STREPTOCOCCUS PNEUMONIAE;

EID: 22544455943     PISSN: 00221767     EISSN: None     Source Type: Journal    
DOI: 10.4049/jimmunol.175.3.1813     Document Type: Article

References (40)

1. Walport, M. J. 2001. Complement. First of two parts. N. Engl. J. Med. 344: 1058-1066.
2. Alper, C. A., N. Abramson, R. B. Johnston, Jr., J. H. Jandl, and F. S. Rosen. 1970. Increased susceptibility to infection associated with abnormalities of complement-mediated functions and of the third component of complement (C3). N. Engl. J. Med. 282: 350-354.
3. Gross, G. N., S. R. Rehm, and A. K. Pierce. 1978. The effect of complement depletion on Lung clearance of bacteria. J. Clin. Invest. 62: 373-378.
4. Winkelstein, J. A. 1981. The role of complement in the host's defense against Streptococcus pneumoniae. Rev. Infect. Dis. 3: 289-298.
5. Sampson, H. A., A. M. Walchner, and P. J. Baker. 1982. Recurrent pyogenic infections in individuals with absence of the second component of complement. J. Clin. Immunol. 2: 39-45.
6. Mold, C., B. Rodic-Polic, and T. W. Du Clos. 2002. Protection from Streptococcus pneumoniae infection by C-reactive protein and natural antibody requires complement but not Fcγ receptors. J. Immunol. 168: 6375-6381.
7. Brown, J. S., T. Hussell, S. M. Gilliland, D. W. Holden, J. C. Paton, M. R. Ehrenstein, M. J. Walport, and M. Botto. 2002. The classical pathway is the dominant complement pathway required for innate immunity to Streptococcus pneumoniae infection in mice. Proc. Natl. Acad. Sci. USA 99: 16969-16974.
8. 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. J. Immunol. 173: 7506-7512.
9. Jarva, H., T. S. Jokiranta, R. Wurzner, and S. Meri. 2003. Complement resistance mechanisms of streptococci. Mol. Immunol. 40: 95-107.
10. 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.
11. 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.
12. Ren, B., A. J. Szalai, S. K. Hollingshead, and D. E. Briles. 2004. Effects of PspA and antibodies to PspA on activation and deposition of complement on the pneumococcal surface. Infect. Immun. 72: 114-122.
13. Berry, A. M., J. Yother, D. E. Briles, D. Hansman, and J. C. Paton. 1989. Reduced virulence of a defined pneumolysin-negative mutant of Streptococcus pneumoniae. Infect. Immun. 57: 2037-2042.
14. Berry, A. M., J. E. Alexander, T. J. Mitchell, P. W. Andrew, D. Hansman, and J. C. Paton. 1995. Effect of defined point mutations in the pneumolysin gene on the virulence of Streptococcus pneumoniae. Infect. Immun. 63: 1969-1974.
15. Paton, J. C. 1996. The contribution of pneumolysin to the pathogenicity of Streptococcus pneumoniae. Trends Microbiol. 4: 103-106.
16. Berry, A. M., A. D. Ogunniyi, D. C. Miller, and J. C. Paton. 1999. Comparative virulence of Streptococcus pneumoniae strains with insertion-duplication, point, and deletion mutations in the pneumolysin gene. Infect. Immun. 67: 981-985.
17. Paton, J. C., B. Rowan-Kelly, and A. Ferrante. 1984. Activation of human complement by the pneumococcal toxin pneumolysin. Infect. Immun. 43: 1085-1087.
18. Mitchell, T. J., P. W. Andrew, F. K. Saunders, A. N. Smith, and G. J. Boulnois. 1991. Complement activation and antibody binding by pneumolysin via a region of the toxin homologous to a human acute-phase protein. Mol. Microbiol. 5: 1883-1888.
19. Rossjohn, J., R. J. Gilbert, D. Crane, P. J. Morgan, T. J. Mitchell, A. J. Rowe, P. W. Andrew, J. C. Paton, R. K. Tweten, and M. W. Parker. 1998. The molecular mechanism of pneumolysin, a virulence factor from Streptococcus pneumoniae. J. Mol. Biol. 284: 449-461.
20. Paton, J. C., and A. Ferrante. 1983. Inhibition of human polymorphonuclear leukocyte respiratory burst, bactericidal activity, and migration by pneumolysin. Infect. Immun. 41: 1212-1216.
21. Feldman, C., N. C. Munro, P. K. Jeffery, T. J. Mitchell, P. W. Andrew, G. J. Boulnois, D. Guerreiro, J. A. Rohde, H. C. Todd, P. J. Cole, et al. 1991. Pneumolysin induces the salient histologic features of pneumococcal infection in the rat lung in vivo. Am. J. Respir. Cell Mol. Biol. 5: 416-423.
22. Malley, R., P. Henneke, S. C. Morse, M. J. Cieslewicz, M. Lipsitch, C. M. Thompson, E. Kurt-Jones, J. C. Paton, M. R. Wessels, and D. T. Golenbock. 2003. Recognition of pneumolysin by Toll-like receptor 4 confers resistance to pneumococcal infection. Proc. Natl. Acad. Sci. USA 100: 1966-1971.
23. Rubins, J. B., D. Charboneau, J. C. Paton, T. J. Mitchell, P. W. Andrew, and E. N. Janoff. 1995. Dual function of pneumolysin in the early pathogenesis of murine pneumococcal pneumonia. J. Clin. Invest. 95: 142-150.
24. Rubins, J. B., D. Charboneau, C. Fasching, A. M. Berry, J. C. Paton, J. E. Alexander, P. W. Andrew, T. J. Mitchell, and E. N. Janoff. 1996. Distinct roles for pneumolysin's cytotoxic and complement activities in the pathogenesis of pneumococcal pneumonia. Am. J. Respir. Crit. Care Med. 153: 1339-1346.
25. Benton, K. A., J. C. Paton, and D. E. Briles. 1997. The hemolytic and complement-activating properties of pneumolysin do not contribute individually to virulence in a pneumococcal bacteremia model. Microb. Pathog. 23: 201-209.
26. Alexander, J. E., A. M. Berry, J. C. Paton, J. B. Rubins, P. W. Andrew, and T. J. Mitchell. 1998. Amino acid changes affecting the activity of pneumolysin alter the behaviour of pneumococci in pneumonia. Microb. Pathog. 24: 167-174.
27. Berry, A. M., and J. C. Paton. 2000. Additive attenuation of virulence of Streptococcus pneumoniae by mutation of the genes encoding pneumolysin and other putative pneumococcal virulence proteins. Infect. Immun. 68: 133-140.
28. Brown, J. S., S. M. Gilliland, and D. W. Holden. 2001. A Streptococcus pneumoniae pathogenicity island encoding an ABC transporter involved in iron uptake and virulence. Mol. Microbiol. 40: 572-585.
29. Ogunniyi, A. D., R. L. Folland, D. E. Briles, S. K. Hollingshead, and J. C. Paton. 2000. Immunization of mice with combinations of pneumococcal virulence proteins elicits enhanced protection against challenge with Streptococcus pneumoniae. Infect. Immun. 68: 3028-3033.
30. Wessels, M. R., P. Butko, M. Ma, H. B. Warren, A. L. Lage, and M. C. Carroll. 1995. Studies of group B streptococcal infection in mice deficient in complement component C3 or C4 demonstrate an essential role for complement in both innate and acquired immunity. Proc. Natl. Acad. Sci. USA 92: 11490-11494.
31. Matsumoto, M., W. Fukuda, A. Circolo, J. Goellner, J. Strauss-Schoenberger, X. Wang, S. Fujita, T. Hidvegi, D. D. Chaplin, and H. R. Colten. 1997. Abrogation of the alternative complement pathway by targeted deletion of murine factor B. Proc. Natl. Acad. Sci. USA 94: 8720-8725.
32. Botto, M., C. Dell'Agnola, A. E. Bygrave, E. M. Thompson, H. T. Cook, F. Petry, M. Loos, P. P. Pandolfi, and M. J. Walport. 1998. Homozygous C1q deficiency causes glomerulonephritis associated with multiple apoptotic bodies. Nat. Genet. 19: 56-59.
33. Beuzon, C. R., and D. W. Holden. 2001. Use of mixed infections with Salmonella strains to study virulence genes and their interactions in vivo. Microbes Infect. 3: 1345-1352.
34. Hammerschmidt, S., G. Bethe, P. H. Remane, and G. S. Chhatwal. 1999. Identification of pneumococcal surface protein A as a lactoferrin-binding protein of Streptococcus pneumoniae. Infect. Immun. 67: 1683-1687.
35. Hakansson, A., H. Roche, S. Mirza, L. S. McDaniel, A. Brooks-Walter, and D. E. Briles. 2001. Characterization of binding of human lactoferrin to pneumococcal surface protein A. Infect. Immun. 69: 3372-3381.
36. Ogunniyi, A. D., P. Giammarinaro, and J. C. Paton. 2002. The genes encoding virulence-associated proteins and the capsule of Streptococcus pneumoniae are upregulated and differentially expressed in vivo. Microbiology 148: 2045-2053.
37. Berry, A. M., R. A. Lock, D. Hansman, and J. C. Paton. 1989. Contribution of autolysin to virulence of Streptococcus pneumoniae. Infect. Immun. 57: 2324-2330.
38. Balachandran, P., S. K. Hollingshead, J. C. Paton, and D. E. Briles. 2001. The autolytic enzyme LytA of Streptococcus pneumoniae is not responsible for releasing pneumolysin. J. Bacteriol. 183: 3108-3116.
39. Spreer, A., H. Kerstan, T. Bottcher, J. Gerber, A. Siemer, G. Zysk, T. J. Mitchell, H. Eiffert, and R. Nau. 2003. Reduced release of pneumolysin by Streptococcus pneumoniae in vitro and in vivo after treatment with nonbacteriolytic antibiotics in comparison to ceftriaxone. Antimicrob. Agents Chemother. 47: 2649-2654.
40. 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.