Identification of the targets of cross-reactive antibodies induced by Streptococcus pneumoniae colonization

Infection and Immunity

Volumn 78, Issue 5, 2010, Pages 2231-2239

  Roche, Aoife M ^a   Weiser, Jeffrey N ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL ANTIGEN; CROSS REACTING ANTIBODY; CROSS REACTING ANTIGEN; IMMUNOGLOBULIN G; MEMBRANE ANTIGEN; MEMBRANE PROTEIN; PNEUMOCOCCAL SURFACE ADHESIN A; PNEUMOCOCCAL SURFACE PROTEIN A; PNEUMOCOCCUS VACCINE; PROTEINASE MATURATION PROTEIN A; UNCLASSIFIED DRUG;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BACTERIAL COLONIZATION; BINDING COMPETITION; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HUMAN; IMMUNOGENICITY; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; PROTEIN TARGETING; STREPTOCOCCUS PNEUMONIAE; WESTERN BLOTTING; WILD TYPE;

ADHESINS, BACTERIAL; ANIMALS; ANTIBODIES, BACTERIAL; BACTERIAL PROTEINS; BLOTTING, WESTERN; CARRIER STATE; COLONY COUNT, MICROBIAL; CROSS REACTIONS; FEMALE; FLOW CYTOMETRY; HUMANS; IMMUNOGLOBULIN G; LIPOPROTEINS; MICE; MICE, INBRED C57BL; PNEUMOCOCCAL INFECTIONS; PROTEIN BINDING; STREPTOCOCCUS PNEUMONIAE; SURVIVAL ANALYSIS;

EID: 77951214467     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.01058-09     Document Type: Article

References (50)

1. Achen, M. G., B. E. Davidson, and A. J. Hillier. 1986. Construction of plasmid vectors for the detection of streptococcal promoters. Gene 45:45-49.
2. Adamou, J. E., J. H. Heinrichs, A. L. Erwin, W. Walsh, T. Gayle, M. Dormitzer, R. Dagan, Y. A. Brewah, P. Barren, R. Lathigra, S. Langermann, S. Koenig, and S. Johnson. 2001. Identification and characterization of a novel family of pneumococcal proteins that are protective against sepsis. Infect. Immun. 69:949-958.
3. Alexander, J. E., R. A. Lock, C. C. Peeters, J. T. Poolman, P. W. Andrew, T. J. Mitchell, D. Hansman, and J. C. Paton. 1994. Immunization of mice with pneumolysin toxoid confers a significant degree of protection against at least nine serotypes of Streptococcus pneumoniae. Infect. Immun. 62:5683-5688.
4. Avery, O. T., C. M. MacLeod, and M. McCarty. 1944. Studies on the chemical nature of the substance inducing transformation of pneumococcal types. J. Exp. Med. 79:137-157.
5. Bogaert, D., R. D. Groot, and P. Hermans. 2004. Streptococcus pneumoniae colonisation: the key to pneumococcal disease. Lancet Infect. Dis. 4:144-154.
6. Briles, D. E., E. Ades, J. C. Paton, J. S. Sampson, G. M. Carlone, R. C. Huebner, A. Virolainen, E. Swiatlo, and S. K. Hollingshead. 2000. Intranasal immunization of mice with a mixture of the pneumococcal proteins PsaA and PspA is highly protective against nasopharyngeal carriage of Streptococcus pneumoniae. Infect. Immun. 68:796-800.
7. Briles, D., S. Hollingshead, J. Paton, E. Ades, L. Novak, F. van Ginkel, and W. J. Benjamin. 2003. Immunizations with pneumococcal surface protein A and pneumolysin are protective against pneumonia in a murine model of pulmonary infection with Streptococcus pneumoniae. J. Infect. Dis. 188:339-348. (Pubitemid 36966099)
8. Briles, D. E., S. K. Hollingshead, J. King, A. Swift, P. A. Braun, M. K. Park, L. M. Ferguson, M. H. Nahm, and G. S. Nabors. 2000. Immunization of humans with recombinant pneumococcal surface protein A (rPspA) elicits antibodies that passively protect mice from fatal infection with Streptococcus pneumoniae bearing heterologous PspA. J. Infect. Dis. 182:1694-1701.
9. Brooks-Walters, A., D. Briles, and S. Hollingshead. 1999. The pspC gene of Streptococcus pneumoniae encodes a polymorphic protein, PspC, which elicits cross-reactive antibodies to PspA and provides immunity to pneumococcal bacteremia. Infect. Immun. 67:6533-6542.
10. Dagan, R., N. Givon-Lavi, D. Fraser, M. Lipsitch, G. R. Siber, and R. Kohberger. 2005. Serum serotype-specific pneumococcal anticapsular immunoglobulin G concentrations after immunization with a 9-valent conjugate pneumococcal vaccine correlate with nasopharyngeal acquisition of pneumococcus. J. Infect. Dis. 192:367-376.
11. Daniels, C. C., T. C. Briles, S. Mirza, A. P. Hakansson, and D. E. Briles. 2006. Capsule does not block antibody binding to PspA, a surface virulence protein of Streptococcus pneumoniae. Microb. Pathog. 40:228-233.
12. Darrieux, M., E. N. Miyaji, D. M. Ferreira, L. M. Lopes, A. P. Lopes, B. Ren, D. E. Briles, S. K. Hollingshead, and L. C. Leite. 2007. Fusion proteins containing family 1 and family 2 PspA fragments elicit protection against Streptococcus pneumoniae that correlates with antibody-mediated enhancement of complement deposition. Infect. Immun. 75:5930-5938.
13. Dintilhac, A., G. Alloing, C. Granadel, and J. P. Claverys. 1997. Competence and virulence of Streptococcus pneumoniae: Adc and PsaA mutants exhibit a requirement for Zn and Mn resulting from inactivation of putative ABC metal permeases. Mol. Microbiol. 25:727-739.
14. Eskola, J., T. Kilpi, A. Palmu, J. Jokinen, J. Haapakoski, E. Herva, A. Takala, H. Kayhty, P. Karma, R. Kohberger, G. Siber, P. Makela, and F. O. M. S. Group. 2001. Efficacy of a pneumococcal conjugate vaccine against acute otitis media. N. Engl. J. Med. 344:403-409.
15. Fireman, B., S. B. Black, H. R. Shinefield, J. Lee, E. Lewis, and P. Ray. 2003. Impact of the pneumococcal conjugate vaccine on otitis media. Pediatr. Infect. Dis. J. 22:10-16.
16. Giefing, C., A. L. Meinke, M. Hanner, T. Henics, M. D. Bui, D. Gelbmann, U. Lundberg, B. M. Senn, M. Schunn, A. Habel, B. Henriques-Normark, A. Ortqvist, M. Kalin, A. von Gabain, and E. Nagy. 2008. Discovery of a novel class of highly conserved vaccine antigens using genomic scale antigenic fingerprinting of pneumococcus with human antibodies. J. Exp. Med. 205:117-131.
17. Goldblatt, D., M. Hussain, N. Andrews, L. Ashton, C. Virta, A. Melegaro, R. Pebody, R. George, A. Soininen, J. Edmunds, N. Gay, H. Kayhty, and E. Miller. 2005. Antibody responses to nasopharyngeal carriage of Streptococcus pneumoniae in adults: a longitudinal household study. J. Infect. Dis. 192:387-393.
18. Gor, D. O., X. Ding, D. E. Briles, M. R. Jacobs, and N. S. Greenspan. 2005. Relationship between surface accessibility for PpmA, PsaA, and PspA and antibody-mediated immunity to systemic infection by Streptococcus pneumoniae. Infect. Immun. 73:1304-1312.
19. Granat, S. M., J. Ollgren, E. Herva, Z. Mia, K. Auranen, and P. H. Makela. 2009. Epidemiological evidence for serotype-independent acquired immunity to pneumococcal carriage. J. Infect. Dis. 200:99-106.
20. Harriman, G. R., M. Bogue, P. Rogers, M. Finegold, S. Pacheco, A. Bradley, Y.-X. Zhang, and I. N. Mbawuike. 1999. Targeted deletion of the IgA constant region in mice leads to IgA deficiency with alterations in expression of other immunoglobulin isotypes. J. Immunol. 162:2521-2529.
21. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and L. R. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59. (Pubitemid 19125653)
22. Johnson, S., J. Dykes, D. Jue, J. Sampson, G. Carlone, and A. E. W. 2002. Inhibition of pneumococcal carriage in mice by subcutaneous immunization with peptides from the common surface protein pneumococcal surface adhesin A. J. Infect. Dis. 185:489-496.
23. Kim, J., and J. 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. (Pubitemid 28063761)
24. Kitamura, D., J. Roes, R. Kuhn, and K. Rajewsky. 1991. A B cell-deficient mouse by targeted disruption of the membrane exon of the immunoglobulin mu chain gene. Nature 350:423-426. (Pubitemid 21912244)
25. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
26. Malley, R., M. Lipsitch, A. Stack, R. Saladino, G. Fleisher, S. Pelton, C. Thompson, D. Briles, and P. Anderson. 2001. Intranasal immunization with killed unencapsulated whole cells prevents colonization and invasive disease by capsulated pneumococci. Infect. Immun. 69:4870-4873.
27. Malley, R., A. Srivastava, M. Lipsitch, C. Thompson, C. Watkins, A. Tzianabos, and P. Anderson. 2006. Antibody-independent, interleukin-17 A-mediated, cross-serotype immunity to pneumococci in mice immunized intranasally with the cell wall polysaccharide. Infect. Immun. 74:2187-2195.
28. Malley, R., K. Trzcinski, A. Srivastava, C. Thompson, P. Anderson, and M. Lipsitch. 2005. CD4+ T cells mediate antibody-independent acquired immunity to pneumococcal colonization. Proc. Natl. Acad. Sci. U. S. A. 102:4848-4853.
29. McCool, T., T. Cate, G. Moy, and J. Weiser. 2002. The immune response to pneumococcal proteins during experimental human carriage. J. Exp. Med. 195:359-365.
30. McCool, T., and J. Weiser. 2004. Limited role of antibody in clearance of Streptococcus pneumoniae in a murine model of colonization. Infect. Immun. 72:5807-5813.
31. McDaniel, L. S., D. O. McDaniel, S. K. Hollingshead, and D. E. Briles. 1998. Comparison of the PspA sequence from Streptococcus pneumoniae EF5668 to the previously identified PspA sequence from strain Rx1 and ability of PspA from EF5668 to elicit protection against pneumococci of different capsular types. Infect. Immun. 66:4748-4754.
32. McDaniel, L. S., J. S. Sheffield, P. Delucchi, and D. E. Briles. 1991. PspA, a surface protein of Streptococcus pneumoniae, is capable of eliciting protection against pneumococci of more than one capsular type. Infect. Immun. 59:222-228.
33. Millar, E. V., J. P. Watt, M. A. Bronsdon, J. Dallas, R. Reid, M. Santosham, and K. L. O'Brien. 2008. Indirect effect of 7-valent pneumococcal conjugate vaccine on pneumococcal colonization among unvaccinated household members. Clin. Infect. Dis. 47:989-996.
34. 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.
35. Nurkka, A., H. Ahman, M. Korkeila, V. Jantti, H. Kayhty, and J. Eskola. 2001. Serum and salivary anti-capsular antibodies in infants and children immunized with the heptavalent pneumococcal conjugate vaccine. Pediatr. Infect. Dis. J. 20:25-33.
36. Oma, K., J. Zhao, H. Ezoe, Y. Akeda, S. Koyama, K. J. Ishii, K. Kataoka, and K. Oishi. 2009. Intranasal immunization with a mixture of PspA and a Toll-like receptor agonist induces specific antibodies and enhances bacterial clearance in the airways of mice. Vaccine 27:3181-3188.
37. Overweg, K., A. Kerr, M. Sluijter, M. Jackson, T. Mitchell, A. De Jong, R. De Groot, and P. Hermans. 2000. The putative proteinase maturation protein A of Streptococcus pneumoniae is a conserved surface protein with potential to elicit protective immune responses. Infect. Immun. 68:4180-4188.
38. Pimenta, F. C., E. N. Miyaji, A. P. Areas, M. L. Oliveira, A. L. de Andrade, P. L. Ho, S. K. Hollingshead, and L. C. Leite. 2006. Intranasal immunization with the cholera toxin B subunit-pneumococcal surface antigen A fusion protein induces protection against colonization with Streptococcus pneumoniae and has negligible impact on the nasopharyngeal and oral microbiota of mice. Infect. Immun. 74:4939-4944.
39. Roche, A. M., S. J. King, and J. N. Weiser. 2007. Live attenuated Streptococcus pneumoniae strains induce serotype-independent mucosal and systemic protection in mice. Infect. Immun. 75:2469-2475.
40. Seo, J. Y., S. Y. Seong, B. Y. Ahn, I. C. Kwon, H. Chung, and S. Y. Jeong. 2002. Cross-protective immunity of mice induced by oral immunization with pneumococcal surface adhesin A encapsulated in microspheres. Infect. Immun. 70:1143-1149.
41. Siber, G., Klugman, K. and P. H. Makela (ed.). 2008. Pneumococcal vaccines: the impact of conjugate vaccine. ASM Press, Washington, DC.
42. Swiatlo, E., J. King, G. S. Nabors, B. Mathews, and D. E. Briles. 2003. Pneumococcal surface protein A is expressed in vivo, and antibodies to PspA are effective for therapy in a murine model of pneumococcal sepsis. Infect. Immun. 71:7149-7153.
43. Tanaka, N., S. Fukuyama, T. Fukuiwa, M. Kawabata, Y. Sagara, H. O. Ito, Y. Miwa, T. Nagatake, H. Kiyono, and Y. Kurono. 2007. Intranasal immunization with phosphorylcholine induces antigen specific mucosal and systemic immune responses in mice. Vaccine 25:2680-2687. (Pubitemid 46400925)
44. Tettelin, H. N. K., I. T. Paulsen, J. A. Eisen, T. D. Read, S. Peterson, J. Heidelberg, R. T. DeBoy, D. H. Haft, R. J. Dodson, A. S. Durkin, M. Gwinn, J. F. Kolonay, W. C. Nelson, J. D. Peterson, L. A. Umayam, O. White, S. L. Salzberg, M. R. Lewis, D. Radune, E. Holtzapple, H. Khouri, A. M. Wolf, T. R. Utterback, C. L. Hansen, L. A. McDonald, T. V. Feldblyum, S. Angiuoli, T. Dickinson, E. K. Hickey, I. E. Holt, B. J. Loftus, F. Yang, H. O. Smith, J. C. Venter, B. A. Dougherty, D. A. Morrison, S. K. Hollingshead, and C. M. Fraser. 2001. Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498-506.
45. Tsai, C. J., M. R. Griffin, J. P. Nuorti, and C. G. Grijalva. 2008. Changing epidemiology of pneumococcal meningitis after the introduction of pneumococcal conjugate vaccine in the United States. Clin. Infect. Dis. 46:1664-1672.
46. Vainio, A., R. Fagerlund, K. Melen, M. J. Lehtinen, I. Julkunen, and A. Virolainen. 2006. Serum antibodies to putative proteinase maturation protein A in children with acute otitis media. Vaccine 24:1792-1799. (Pubitemid 43238260)
47. Whitney, C., M. Farley, J. Hadler, L. Harrison, N. Bennett, R. Lynfield, A. Reingold, P. Cieslak, T. Pilishvili, D. Jackson, R. Facklam, J. Jorgensen, A. Schuchat, and Active Bacterial Core Surveillance of the Emerging Infections Network. 2003. Decline in invasive pneumococcal disease after the introduction of protein-polysaccharide conjugate vaccine. N. Engl. J. Med. 348:1737-1746.
48. Wizemann, T., J. Heinrichs, J. Adamou, A. Erwin, C. Kunsch, G. Choi, S. Barash, C. Rosen, H. Masure, E. Tuomanen, A. Gayle, Y. Brewah, W. Walsh, P. Barren, R. Lathigra, M. Hanson, S. Langermann, S. Johnson, and S. Koenig. 2001. Use of a whole genome approach to identify vaccine molecules affording protection against Streptococcus pneumoniae infection. Infect. Immun. 69:1593-1598.
49. Yother, J., L. S. McDaniel, and D. E. Briles. 1986. Transformation of encapsulated Streptococcus pneumoniae. J. Bacteriol. 168:1463-1465.
50. Yother, J., and J. M. White. 1994. Novel surface attachment mechanism of the Streptococcus pneumoniae protein PspA. J. Bacteriol. 176:2976-2985.