Streptococcus pneumoniae resistance to complement-mediated immunity is dependent on the capsular serotype

Infection and Immunity

Volumn 78, Issue 2, 2010, Pages 716-725

  Hyams, Catherine ^a   Yuste, Jose ^a,d   Bax, Katie ^b   Camberlein, Emilie ^a   Weiser, Jeffrey N ^c   Brown, Jeremy S ^a  

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

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

^d CSIC   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENT; COMPLEMENT COMPONENT C3B; COMPLEMENT FACTOR I; IMMUNOGLOBULIN G;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; BACTERIUM MUTANT; CELLULAR IMMUNITY; CONTROLLED STUDY; FLOW CYTOMETRY; HUMAN; MOUSE; NEUTROPHIL; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; SEROTYPE; STREPTOCOCCUS PNEUMONIAE; THICKNESS;

ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL CAPSULES; BACTERIAL PROTEINS; CELL SEPARATION; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; FLOW CYTOMETRY; HUMANS; MICE; SEROTYPING; STREPTOCOCCUS PNEUMONIAE; VIRULENCE;

EID: 76749155083     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01056-09     Document Type: Article

References (46)

1. Aanensen, D. M., A. Mavroidi, S. D. Bentley, P. R. Reeves, and B. G. Spratt. 2007. Predicted functions and linkage specificities of the products of the Streptococcus pneumoniae capsular biosynthetic loci. J. Bacteriol. 189:7856-7876.
2. Abeyta, M., G. G. Hardy, and J. Yother. 2003. Genetic alteration of capsule type but not PspA type affects accessibility of surface-bound complement and surface antigens of Streptococcus pneumoniae. Infect. Immun. 71:218-225.
3. Arredouani, M., Z. Yang, Y. Ning, G. Qin, R. Soininen, K. Tryggvason, and L. Kobzik. 2004. The scavenger receptor MARCO is required for lung defense against pneumococcal pneumonia and inhaled particles. J. Exp. Med. 200:267-272.
4. Austrian, R. 1981. Some observations on the pneumococcus and on the current status of pneumococcal disease and its prevention. Rev. Infect. Dis. 3(Suppl.):S1-S17.
5. Austrian, R., H. P. Bernheimer, E. E. Smith, and G. T. Mills. 1959. Simultaneous production of two capsular polysaccharides by pneumococcus. II. The genetic and biochemical bases of binary capsulation. J. Exp. Med. 110:585-602.
6. Avery, O., and R. Dubos. 1931. The protective action of a specific enzyme against type III pneumococcus infection in mice. J. Exp. Med. 54:73-89.
7. Bentley, S. D., D. M. Aanensen, A. Mavroidi, D. Saunders, E. Rabbinowitsch, M. Collins, K. Donohoe, D. Harris, L. Murphy, M. A. Quail, G. Samuel, I. C. Skovsted, M. S. Kaltoft, B. Barrell, P. R. Reeves, J. Parkhill, and B. G. Spratt. 2006. Genetic analysis of the capsular biosynthetic locus from all 90 pneumococcal serotypes. PLoS Genet. 2:e31.
8. Bootsma, H. J., M. Egmont-Petersen, and P. W. Hermans. 2007. Analysis of the in vitro transcriptional response of human pharyngeal epithelial cells to adherent Streptococcus pneumoniae: evidence for a distinct response to encapsulated strains. Infect. Immun. 75:5489-5499.
9. Briles, D. E., M. J. Crain, B. M. Gray, C. Forman, and J. Yother. 1992. Strong association between capsular type and virulence for mice among human isolates of Streptococcus pneumoniae. Infect. Immun. 60:111-116.
10. Brown, J. S., S. M. Gilliland, B. G. Spratt, and D. W. Holden. 2004. A locus contained within a variable region of pneumococcal pathogenicity island 1 contributes to virulence in mice. Infect. Immun. 72:1587-1593.
11. 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. U. S. A. 99:16969-16974.
12. Brueggemann, A. B., T. E. Peto, D. W. Crook, J. C. Butler, K. G. Kristinsson, and B. G. Spratt. 2004. Temporal and geographic stability of the serogroupspecific invasive disease potential of Streptococcus pneumoniae in children. J. Infect. Dis. 190:1203-1211.
13. Hakenbeck, R., N. Balmelle, B. Weber, C. Gardes, W. Keck, and A. de Saizieu. 2001. Mosaic genes and mosaic chromosomes: intra- and interspecies genomic variation of Streptococcus pneumoniae. Infect. Immun. 69:2477-2486.
14. 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.
15. Hanage, W. P., T. H. Kaijalainen, R. K. Syrjanen, K. Auranen, M. Leinonen, P. H. Makela, and B. G. Spratt. 2005. Invasiveness of serotypes and clones of Streptococcus pneumoniae among children in Finland. Infect. Immun. 73:431-435.
16. Hiller, N. L., B. Janto, J. S. Hogg, R. Boissy, S. Yu, E. Powell, R. Keefe, N. E. Ehrlich, K. Shen, J. Hayes, K. Barbadora, W. Klimke, D. Dernovoy, T. Tatusova, J. Parkhill, S. D. Bentley, J. C. Post, G. D. Ehrlich, and F. Z. Hu. 2007. Comparative genomic analyses of seventeen Streptococcus pneumoniae strains: insights into the pneumococcal supragenome. J. Bacteriol. 189:8186-8195.
17. Hollingshead, S. K., R. Becker, and D. E. Briles. 2000. Diversity of PspA: mosaic genes and evidence for past recombination in Streptococcus pneumoniae. Infect. Immun. 68:5889-5900.
18. Hostetter, M. K. 1986. Serotypic variations among virulent pneumococci in deposition and degradation of covalently bound C3b: implications for phagocytosis and antibody production. J. Infect. Dis. 153:682-693.
19. Hyams, C., E. Camberlein, J. M. Cohen, K. Bax, and J. S. Brown. 2010. The Streptococcus pneumoniae capsule inhibits complement activity and neutrophil phagocytosis by multiple mechanisms. Infect. Immun. 78:704-715.
20. Jonsson, G., L. Truedsson, G. Sturfelt, V. A. Oxelius, J. H. Braconier, and A. G. Sjoholm. 2005. Hereditary C2 deficiency in Sweden: frequent occurrence of invasive infection, atherosclerosis, and rheumatic disease. Medicine (Baltimore) 84:23-34.
21. Kang, Y. S., Y. Do, H. K. Lee, S. H. Park, C. Cheong, R. M. Lynch, J. M. Loeffler, R. M. Steinman, and C. G. Park. 2006. A dominant complement fixation pathway for pneumococcal polysaccharides initiated by SIGN-R1 interacting with C1q. Cell 125:47-58.
22. Kelly, T., J. P. Dillard, and J. Yother. 1994. Effect of genetic switching of capsular type on virulence of Streptococcus pneumoniae. Infect. Immun. 62:1813-1819.
23. Kim, J. O., S. Romero-Steiner, U. B. Sorensen, J. Blom, M. Carvalho, S. Barnard, G. Carlone, and J. N. Weiser. 1999. Relationship between cell surface carbohydrates and intrastrain variation on opsonophagocytosis of Streptococcus pneumoniae. Infect. Immun. 67:2327-2333.
24. Kim, J. O., and J. N. Weiser. 1998. Association of intrastrain phase variation in quantity of capsular polysaccharide and teichoic acid with the virulence of Streptococcus pneumoniae. J. Infect. Dis. 177:368-377.
25. MacLeod, C. M., and M. R. Krauss. 1950. Relation of virulence of pneumococcal strains for mice to the quantity of capsular polysaccharide formed in vitro. J. Exp. Med. 92:1-9.
26. Magee, A. D., and J. Yother. 2001. Requirement for capsule in colonization by Streptococcus pneumoniae. Infect. Immun. 69:3755-3761.
27. Mavroidi, A., D. Godoy, D. M. Aanensen, D. A. Robinson, S. K. Hollingshead, and B. G. Spratt. 2004. Evolutionary genetics of the capsular locus of serogroup 6 pneumococci. J. Bacteriol. 186:8181-8192.
28. Melin, M., H. Jarva, L. Siira, S. Meri, H. Kayhty, and M. Vakevainen. 2009. Streptococcus pneumoniae capsular serotype 19F is more resistant to C3 deposition and less sensitive to opsonophagocytosis than serotype 6B. Infect. Immun. 77:676-684.
29. Nelson, A. L., A. M. Roche, J. M. Gould, K. Chim, A. J. Ratner, and J. N. Weiser. 2007. Capsule enhances pneumococcal colonization by limiting mucus-mediated clearance. Infect. Immun. 75:83-90.
30. Paton, J. C., J. K. Morona, and R. Morona. 1997. Characterization of the capsular polysaccharide biosynthesis locus of Streptococcus pneumoniae type 19F. Microb. Drug Resist. 3:89-99.
31. Quin, L. R., Q. C. Moore III, and L. S. McDaniel. 2007. Pneumolysin, PspA, and PspC contribute to pneumococcal evasion of early innate immune responses during bacteremia in mice. Infect. Immun. 75:2067-2070.
32. Sabharwal, V., S. Ram, M. Figueira, I. H. Park, and S. I. Pelton. 2009. Role of complement in host defense against pneumococcal otitis media. Infect. Immun. 77:1121-1127.
33. Sandgren, A., B. Albiger, C. J. Orihuela, E. Tuomanen, S. Normark, and B. Henriques-Normark. 2005. Virulence in mice of pneumococcal clonal types with known invasive disease potential in humans. J. Infect. Dis. 192:791-800.
34. Segal, A. W., and O. T. Jones. 1980. Absence of cytochrome b reduction in stimulated neutrophils from both female and male patients with chronic granulomatous disease. FEBS Lett. 110:111-114.
35. Trzcinski, K., C. M. Thompson, and M. Lipsitch. 2003. Construction of otherwise isogenic serotype 6B, 7F, 14, and 19F capsular variants of Streptococcus pneumoniae strain TIGR4. Appl. Environ. Microbiol. 69: 7364-7370.
36. von Pawel-Rammingen, U., B. P. Johansson, and L. Bjorck. 2002. IdeS, a novel streptococcal cysteine proteinase with unique specificity for immunoglobulin G. EMBO J. 21:1607-1615.
37. Wartha, F., K. Beiter, B. Albiger, J. Fernebro, A. Zychlinsky, S. Normark, and B. Henriques-Normark. 2007. Capsule and D-alanylated lipoteichoic acids protect Streptococcus pneumoniae against neutrophil extracellular traps. Cell. Microbiol. 9:1162-1171.
38. Watson, D., and D. Musher. 1990. Interruption of capsule production in Streptococcus pneumoniae serotype 3 by insertion of transposon Tn916. Infect. Immun. 58:3135-3138.
39. Weinberger, D. M., K. Trzcinski, Y. J. Lu, D. Bogaert, A. Brandes, J. Galagan, P. W. Anderson, R. Malley, and M. Lipsitch. 2009. Pneumococcal capsular polysaccharide structure predicts serotype prevalence. PLoS Pathog. 5:e1000476.
40. Weiser, J. N., R. Austrian, P. K. Sreenivasan, and H. R. Masure. 1994. Phase variation in pneumococcal opacity: relationship between colonial morphology and nasopharyngeal colonization. Infect. Immun. 62:2582-2589.
41. Wenig, K., L. Chatwell, U. von Pawel-Rammingen, L. Bjorck, R. Huber, and P. Sondermann. 2004. Structure of the streptococcal endopeptidase IdeS, a cysteine proteinase with strict specificity for IgG. Proc. Natl. Acad. Sci. U. S. A. 101:17371-17376.
42. Winkelstein, J. A. 1981. The role of complement in the host's defense against Streptococcus pneumoniae. Rev. Infect. Dis. 3:289-298.
43. Yother, J., L. S. McDaniel, and D. E. Briles. 1986. Transformation of encapsulated Streptococcus pneumoniae. J. Bacteriol. 168:1463-1465.
44. Yuste, J., M. Botto, S. E. Bottoms, and J. S. Brown. 2007. Serum amyloid P aids complement-mediated immunity to Streptococcus pneumoniae. PLoS Pathog. 3:1208-1219.
45. 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.
46. Yuste, J., A. Sen, L. Truedsson, G. Jonsson, L. S. Tay, C. Hyams, H. E. Baxendale, F. Goldblatt, M. Botto, and J. S. Brown. 2008. Impaired opsonization with C3b and phagocytosis of Streptococcus pneumoniae in sera from subjects with defects in the classical complement pathway. Infect. Immun. 76:3761-3770.