Structurally identical capsular polysaccharide expressed by intact group B Streptococcus versus Streptococcus pneumoniae elicits distinct murine polysaccharide-specific IgG responses in vivo

Journal of Immunology

Volumn 188, Issue 11, 2012, Pages 5238-5246

  Arjunaraja, Swadhinya ^a,b   Paoletti, Lawrence C ^c   Snapper, Clifford M ^a  

^a UNIFORMED SERVICES UNIVERSITY OF THE HEALTH SCIENCES   (United States)

^b BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

^c BRIGHAM AND WOMEN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

B7 ANTIGEN; BACTERIAL POLYSACCHARIDE; CD28 ANTIGEN; CD40 LIGAND; CD86 ANTIGEN; ICOS PROTEIN; IMMUNOGLOBULIN G ANTIBODY; IMMUNOGLOBULIN M ANTIBODY; PNEUMOCOCCAL POLYSACCHARIDE TYPE 14; STREPTOCOCCUS VACCINE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANTIBODY RESPONSE; ANTIBODY TITER; ARTICLE; BACTERIAL STRAIN; CD4+ T LYMPHOCYTE; CONTROLLED STUDY; CROSS REACTION; FEMALE; IMMUNOLOGICAL MEMORY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; BACTERIAL CAPSULES; FEMALE; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; MICE; MICE, INBRED BALB C; POLYSACCHARIDES, BACTERIAL; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY; STREPTOCOCCAL VACCINES; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PNEUMONIAE; VACCINES, CONJUGATE;

EID: 84862059440     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200132     Document Type: Article

References (64)

1. Ferrieri, P. 1990. Neonatal susceptibility and immunity to major bacterial pathogens. Rev. Infect. Dis. 12(Suppl 4): S394-S400. (Pubitemid 20168623)
2. Tikhomirov, E., M. Santamaria, and K. Esteves. 1997. Meningococcal disease: public health burden and control. World Health Stat. Q. 50: 170-177. (Pubitemid 28133356)
3. Scott, J. A. 2007. The preventable burden of pneumococcal disease in the developing world. Vaccine 25: 2398-2405. (Pubitemid 46366119)
4. AlonsoDeVelasco, E., A. F. Verheul, J. Verhoef, and H. Snippe. 1995. Streptococcus pneumoniae: virulence factors, pathogenesis, and vaccines. Microbiol. Rev. 59: 591-603.
5. Harding, C. V., R. W. Roof, P. M. Allen, and E. R. Unanue. 1991. Effects of pH and polysaccharides on peptide binding to class II major histocompatibility complex molecules. Proc. Natl. Acad. Sci. USA 88: 2740-2744. (Pubitemid 21916494)
6. Ishioka, G. Y., A. G. Lamont, D. Thomson, N. Bulbow, F. C. Gaeta, A. Sette, and H. M. Grey. 1992. MHC interaction and T cell recognition of carbohydrates and glycopeptides. J. Immunol. 148: 2446-2451.
7. Mond, J. J., A. Lees, and C. M. Snapper. 1995. T cell-independent antigens type 2. Annu. Rev. Immunol. 13: 655-692.
8. Brunswick, M., F. D. Finkelman, P. F. Highet, J. K. Inman, H. M. Dintzis, and J. J. Mond. 1988. Picogram quantities of anti-Ig antibodies coupled to dextran induce B cell proliferation. J. Immunol. 140: 3364-3372.
9. Snapper, C. M., and J. J. Mond. 1996. A model for induction of T cellindependent humoral immunity in response to polysaccharide antigens. J. Immunol. 157: 2229-2233. (Pubitemid 126450429)
10. Snapper, C. M. 2006. Differential regulation of protein- and polysaccharidespecific Ig isotype production in vivo in response to intact Streptococcus pneumoniae. Curr. Protein Pept. Sci. 7: 295-305.
11. Briles, D. E., M. Nahm, T. N. Marion, R. M. Perlmutter, and J. M. Davie. 1982. Streptococcal group A carbohydrate has properties of both a thymusindependent (TI-2) and a thymus-dependent antigen. J. Immunol. 128: 2032-2035. (Pubitemid 12086481)
12. Khan, A. Q., A. Lees, and C. M. Snapper. 2004. Differential regulation of IgG anti-capsular polysaccharide and antiprotein responses to intact Streptococcus pneumoniae in the presence of cognate CD4+ T cell help. J. Immunol. 172: 532-539. (Pubitemid 38020510)
13. Chen, Q., J. L. Cannons, J. C. Paton, H. Akiba, P. L. Schwartzberg, and C. M. Snapper. 2008. A novel ICOS-independent, but CD28- and SAPdependent, pathway of T cell-dependent, polysaccharide-specific humoral immunity in response to intact Streptococcus pneumoniae versus pneumococcal conjugate vaccine. J. Immunol. 181: 8258-8266.
14. Wu, Z.-Q., Q. Vos, Y. Shen, A. Lees, S. R. Wilson, D. E. Briles, W. C. Gause, J. J. Mond, and C. M. Snapper. 1999. In vivo polysaccharide-specific IgG isotype responses to intact Streptococcus pneumoniae are T cell dependent and require CD40- and B7-ligand interactions. J. Immunol. 163: 659-667. (Pubitemid 29328070)
15. Chattopadhyay, G., A. Q. Khan, G. Sen, J. Colino, W. DuBois, A. Rubtsov, R. M. Torres, M. Potter, and C. M. Snapper. 2007. Transgenic expression of BclxL or Bcl-2 by murine B cells enhances the in vivo antipolysaccharide, but not antiprotein, response to intact Streptococcus pneumoniae. J. Immunol. 179: 7523-7534.
16. Khan, A. Q., G. Sen, S. Guo, O. N. Witte, and C. M. Snapper. 2006. Induction of in vivo antipolysaccharide immunoglobulin responses to intact Streptococcus pneumoniae is more heavily dependent on Btk-mediated B-cell receptor signaling than antiprotein responses. Infect. Immun. 74: 1419-1424. (Pubitemid 43185587)
17. Arjunaraja, S., P. Massari, L. M. Wetzler, A. Lees, J. Colino, and C. M. Snapper. 2012. The nature of an in vivo anti-capsular polysaccharide response is markedly influenced by the composition and/or architecture of the bacterial subcapsular domain. J. Immunol. 188: 569-577.
18. Snapper, C. M. 2012. Mechanisms underlying in vivo polysaccharide- specific immunoglobulin responses to intact extracellular bacteria. Ann. N. Y. Acad. Sci. In press.
19. Sørensen, U. B., J. Henrichsen, H. C. Chen, and S. C. Szu. 1990. Covalent linkage between the capsular polysaccharide and the cell wall peptidoglycan of Streptococcus pneumoniae revealed by immunochemical methods. Microb. Pathog. 8: 325-334. (Pubitemid 20303859)
20. Jedrzejas, M. J. 2004. Extracellular virulence factors of Streptococcus pneumoniae. Front. Biosci. 9: 891-914. (Pubitemid 39043760)
21. Ellis, T. N., and M. J. Kuehn. 2010. Virulence and immunomodulatory roles of bacterial outer membrane vesicles. Microbiol. Mol. Biol. Rev. 74: 81-94.
22. Massari, P., P. Henneke, Y. Ho, E. Latz, D. T. Golenbock, and L. M. Wetzler. 2002. Cutting edge: Immune stimulation by neisserial porins is toll-like receptor 2 and MyD88 dependent. J. Immunol. 168: 1533-1537. (Pubitemid 34135744)
23. Lanoue, A., M. R. Clatworthy, P. Smith, S. Green, M. J. Townsend, H. E. Jolin, K. G. Smith, P. G. Fallon, and A. N. McKenzie. 2004. SIGN-R1 contributes to protection against lethal pneumococcal infection in mice. J. Exp. Med. 200: 1383-1393. (Pubitemid 39657286)
24. Kanswal, S., N. Katsenelson, W. Allman, K. Uslu, M. S. Blake, and M. Akkoyunlu. 2011. Suppressive effect of bacterial polysaccharides on BAFF system is responsible for their poor immunogenicity. J. Immunol. 186: 2430-2443.
25. Dintzis, H. M., R. Z. Dintzis, and B. Vogelstein. 1976. Molecular determinants of immunogenicity: the immunon model of immune response. Proc. Natl. Acad. Sci. USA 73: 3671-3675.
26. Kalka-Moll, W. M., A. O. Tzianabos, P. W. Bryant, M. Niemeyer, H. L. Ploegh, and D. L. Kasper. 2002. Zwitterionic polysaccharides stimulate T cells by MHC class II-dependent interactions. J. Immunol. 169: 6149-6153. (Pubitemid 36903459)
27. Courtney, A. H., E. B. Puffer, J. K. Pontrello, Z. Q. Yang, and L. L. Kiessling. 2009. Sialylated multivalent antigens engage CD22 in trans and inhibit B cell activation. Proc. Natl. Acad. Sci. USA 106: 2500-2505.
28. Kasper, D. L., C. J. Baker, R. S. Baltimore, J. H. Crabb, G. Schiffman, and H. J. Jennings. 1979. Immunodeterminant specificity of human immunity to type III group B streptococcus. J. Exp. Med. 149: 327-339. (Pubitemid 9122854)
29. Guttormsen, H. K., C. J. Baker, M. H. Nahm, L. C. Paoletti, S. M. Zughaier, M. S. Edwards, and D. L. Kasper. 2002. Type III group B streptococcal polysaccharide induces antibodies that cross-react with Streptococcus pneumoniae type 14. Infect. Immun. 70: 1724-1738.
30. Wessels, M. R., R. F. Haft, L. M. Heggen, and C. E. Rubens. 1992. Identification of a genetic locus essential for capsule sialylation in type III group B streptococci. Infect. Immun. 60: 392-400.
31. Colino, J., G. Chattopadhyay, G. Sen, Q. Chen, A. Lees, D. H. Canaday, A. Rubtsov, R. Torres, and C. M. Snapper. 2009. Parameters underlying distinct T cell-dependent polysaccharide-specific IgG responses to an intact gram-positive bacterium versus a soluble conjugate vaccine. J. Immunol. 183: 1551-1559.
32. Wessels, M. R., L. C. Paoletti, D. L. Kasper, J. L. DiFabio, F. Michon, K. Holme, and H. J. Jennings. 1990. Immunogenicity in animals of a polysaccharide-protein conjugate vaccine against type III group B Streptococcus. J. Clin. Invest. 86: 1428-1433. (Pubitemid 20372587)
33. Yang, H. H., S. J. Mascuch, L. C. Madoff, and L. C. Paoletti. 2008. Recombinant group B Streptococcus alpha-like protein 3 is an effective immunogen and carrier protein. Clin. Vaccine Immunol. 15: 1035-1041.
34. Sen, G., M. Flora, G. Chattopadhyay, D. M. Klinman, A. Lees, J. J. Mond, and C. M. Snapper. 2004. The critical DNA flanking sequences of a CpG oligodeoxynucleotide, but not the 6 base CpG motif, can be replaced with RNA without quantitative or qualitative changes in Toll-like receptor 9-mediated activity. Cell. Immunol. 232: 64-74. (Pubitemid 40732721)
35. Lindahl, G., M. Stålhammar-Carlemalm, and T. Areschoug. 2005. Surface proteins of Streptococcus agalactiae and related proteins in other bacterial pathogens. Clin. Microbiol. Rev. 18: 102-127.
36. Obukhanych, T. V., and M. C. Nussenzweig. 2006. T-independent type II immune responses generate memory B cells. J. Exp. Med. 203: 305-310. (Pubitemid 43290839)
37. Elgueta, R., M. J. Benson, V. C. de Vries, A. Wasiuk, Y. Guo, and R. J. Noelle. 2009. Molecular mechanism and function of CD40/CD40L engagement in the immune system. Immunol. Rev. 229: 152-172.
38. Banchereau, J., F. Bazan, D. Blanchard, F. Brière, J. P. Galizzi, C. van Kooten, Y. J. Liu, F. Rousset, and S. Saeland. 1994. The CD40 antigen and its ligand. Annu. Rev. Immunol. 12: 881-922. (Pubitemid 24140434)
39. Greenwald, R. J., G. J. Freeman, and A. H. Sharpe. 2005. The B7 family revisited. Annu. Rev. Immunol. 23: 515-548. (Pubitemid 40563179)
40. Harding, F. A., J. G. McArthur, J. A. Gross, D. H. Raulet, and J. P. Allison. 1992. CD28-mediated signalling co-stimulates murine T cells and prevents induction of anergy in T-cell clones. Nature 356: 607-609.
41. Liang, L., andW. C. Sha. 2002. The right place at the right time: novel B7 family members regulate effector T cell responses. Curr. Opin. Immunol. 14: 384-390. (Pubitemid 34327983)
42. Dong, C., A. E. Juedes, U. A. Temann, S. Shresta, J. P. Allison, N. H. Ruddle, and R. A. Flavell. 2001. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature 409: 97-101. (Pubitemid 32098632)
43. Hutloff, A., A. M. Dittrich, K. C. Beier, B. Eljaschewitsch, R. Kraft, I. Anagnostopoulos, and R. A. Kroczek. 1999. ICOS is an inducible T-cell costimulator structurally and functionally related to CD28. Nature 397: 263-266.
44. Khan, A. Q., Q. Chen, Z. Q. Wu, J. C. Paton, and C. M. Snapper. 2005. Both innate immunity and type 1 humoral immunity to Streptococcus pneumoniae are mediated by MyD88 but differ in their relative levels of dependence on toll-like receptor 2. Infect. Immun. 73: 298-307. (Pubitemid 40041121)
45. von Bülow, G. U., J. M. van Deursen, and R. J. Bram. 2001. Regulation of the Tindependent humoral response by TACI. Immunity 14: 573-582.
46. Balázs, M., F. Martin, T. Zhou, and J. F. Kearney. 2002. Blood dendritic cells interact with splenic marginal zone B cells to initiate T-independent immune responses. Immunity 17: 341-352. (Pubitemid 35279554)
47. Sen, G., A. Q. Khan, Q. Chen, and C. M. Snapper. 2005. In vivo humoral immune responses to isolated pneumococcal polysaccharides are dependent on the presence of associated TLR ligands. J. Immunol. 175: 3084-3091. (Pubitemid 41170528)
48. Welsh, R. M., and L. K. Selin. 2002. No one is naive: the significance of heterologous T-cell immunity. Nat. Rev. Immunol. 2: 417-426. (Pubitemid 37328749)
49. Avci, F. Y., X. Li, M. Tsuji, and D. L. Kasper. 2011. A mechanism for glycoconjugate vaccine activation of the adaptive immune system and its implications for vaccine design. Nat. Med. 17: 1602-1609.
50. Muthukkumar, S., and K. E. Stein. 2004. Immunization with meningococcal polysaccharide-tetanus toxoid conjugate induces polysaccharide-reactive T cells in mice. Vaccine 22: 1290-1299. (Pubitemid 38296674)
51. Guttormsen, H. K., L. M. Wetzler, R. W. Finberg, and D. L. Kasper. 1998. Immunologic memory induced by a glycoconjugate vaccine in a murine adoptive lymphocyte transfer model. Infect. Immun. 66: 2026-2032.
52. Guttormsen, H. K., A. H. Sharpe, A. K. Chandraker, A. K. Brigtsen, M. H. Sayegh, and D. L. Kasper. 1999. Cognate stimulatory B-cell-T-cell interactions are critical for T-cell help recruited by glycoconjugate vaccines. Infect. Immun. 67: 6375-6384.
53. Sette, A., M. Moutaftsi, J. Moyron-Quiroz, M. M. McCausland, D. H. Davies, R. J. Johnston, B. Peters, M. Rafii-El-Idrissi Benhnia, J. Hoffmann, H. P. Su, et al. 2008. Selective CD4+ T cell help for antibody responses to a large viral pathogen: deterministic linkage of specificities. Immunity 28: 847-858. (Pubitemid 351778408)
54. Souwer, Y., A. Griekspoor, T. Jorritsma, J. de Wit, H. Janssen, J. Neefjes, and S. M. van Ham. 2009. B cell receptor-mediated internalization of salmonella: a novel pathway for autonomous B cell activation and antibody production. J. Immunol. 182: 7473-7481.
55. Carrasco, Y. R., and F. D. Batista. 2007. B cells acquire particulate antigen in a macrophage-rich area at the boundary between the follicle and the subcapsular sinus of the lymph node. Immunity 27: 160-171. (Pubitemid 47089026)
56. Wykes, M., A. Pombo, C. Jenkins, and G. G. MacPherson. 1998. Dendritic cells interact directly with naive B lymphocytes to transfer antigen and initiate class switching in a primary T-dependent response. J. Immunol. 161: 1313-1319. (Pubitemid 28380559)
57. Chattopadhyay, G., Q. Chen, J. Colino, A. Lees, and C. M. Snapper. 2009. Intact bacteria inhibit the induction of humoral immune responses to bacterial-derived and heterologous soluble T cell-dependent antigens. J. Immunol. 182: 2011-2019.
58. Lee, K. S., G. Sen, and C. M. Snapper. 2005. Endogenous CD4+ CD25+ regulatory T cells play no apparent role in the acute humoral response to intact Streptococcus pneumoniae. Infect. Immun. 73: 4427-4431. (Pubitemid 40923194)
59. Harnett, M. M., A. J. Melendez, and W. Harnett. 2010. The therapeutic potential of the filarial nematode-derived immunodulator, ES-62 in inflammatory disease. Clin. Exp. Immunol. 159: 256-267.
60. Casey, R., J. Newcombe, J. McFadden, and K. B. Bodman-Smith. 2008. The acute-phase reactant C-reactive protein binds to phosphorylcholine-expressing Neisseria meningitidis and increases uptake by human phagocytes. Infect. Immun. 76: 1298-1304. (Pubitemid 351428094)
61. Lysenko, E. S., J. Gould, R. Bals, J. M. Wilson, and J. N. Weiser. 2000. Bacterial phosphorylcholine decreases susceptibility to the antimicrobial peptide LL-37/ hCAP18 expressed in the upper respiratory tract. Infect. Immun. 68: 1664-1671. (Pubitemid 30108570)
62. Weiser, J. N., J. B. Goldberg, N. Pan, L. Wilson, and M. Virji. 1998. The phosphorylcholine epitope undergoes phase variation on a 43-kilodalton protein in Pseudomonas aeruginosa and on pili of Neisseria meningitidis and Neisseria gonorrhoeae. Infect. Immun. 66: 4263-4267. (Pubitemid 28402700)
63. Henneke, P., and R. Berner. 2006. Interaction of neonatal phagocytes with group B streptococcus: recognition and response. Infect. Immun. 74: 3085-3095. (Pubitemid 43794497)
64. Henneke, P., O. Takeuchi, R. Malley, E. Lien, R. R. Ingalls, M. W. Freeman, T. Mayadas, V. Nizet, S. Akira, D. L. Kasper, and D. T. Golenbock. 2002. Cellular activation, phagocytosis, and bactericidal activity against group B streptococcus involve parallel myeloid differentiation factor 88-dependent and independent signaling pathways. J. Immunol. 169: 3970-3977.