Differential idiotype utilization for the in vivo type 14 capsular polysaccharide-specific Ig responses to intact Streptococcus pneumoniae versus a pneumococcal conjugate vaccine

Journal of Immunology

Volumn 189, Issue 2, 2012, Pages 575-586

  Colino, Jesus ^a   Duke, Leah ^a   Arjunaraja, Swadhinya ^a,b   Chen, Quanyi ^a   Liu, Leyu ^c   Lucas, Alexander H ^c   Snapper, Clifford M ^a  

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

^b BIRLA INSTITUTE OF TECHNOLOGY AND SCIENCE   (India)

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

Author keywords

[No Author keywords available]

Indexed keywords

IMMUNOGLOBULIN G; IMMUNOGLOBULIN M; MONOCLONAL ANTIBODY; PNEUMOCOCCAL CAPSULAR POLYSACCHARIDE SEROTYPE 14; PNEUMOCOCCUS POLYSACCHARIDE; PNEUMOCOCCUS VACCINE; UNCLASSIFIED DRUG;

ALLOTYPE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; B LYMPHOCYTE; BACTERIAL STRAIN; BIOTINYLATION; CD4+ T LYMPHOCYTE; CELL MATURATION; CONTROLLED STUDY; FEMALE; GENETIC REGULATION; HUMORAL IMMUNITY; IMMUNE RESPONSE; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN ISOLATION; PROTEIN PURIFICATION; PROTEIN STRUCTURE; STREPTOCOCCUS AGALACTIAE; STREPTOCOCCUS PNEUMONIAE;

ANIMALS; ANTIBODIES, MONOCLONAL; ANTIGENS, BACTERIAL; BACTERIAL CAPSULES; BINDING SITES, ANTIBODY; FEMALE; IMMUNOGLOBULIN IDIOTYPES; MICE; MICE, INBRED BALB C; MICE, INBRED C57BL; MICE, SCID; PNEUMOCOCCAL VACCINES; STREPTOCOCCUS PNEUMONIAE; VACCINES, CONJUGATE;

EID: 84863633033     PISSN: 00221767     EISSN: 15506606     Source Type: Journal    
DOI: 10.4049/jimmunol.1200599     Document Type: Article

References (80)

1. Mond, J. J., A. Lees, and C. M. Snapper. 1995. T cell-independent antigens type 2. Annu. Rev. Immunol. 13: 655-692.
2. 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.
3. 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)
4. 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.
5. Beuvery, E. C., F. van Rossum, and J. Nagel. 1982. Comparison of the induction of immunoglobulin M and G antibodies in mice with purified pneumococcal type 3 and meningococcal group C polysaccharides and their protein conjugates. Infect. Immun. 37: 15-22. (Pubitemid 12095175)
6. Schneerson, R., O. Barrera, A. Sutton, and J. B. Robbins. 1980. Preparation, characterization, and immunogenicity of Haemophilus influenzae type b polysaccharide- protein conjugates. J. Exp. Med. 152: 361-376. (Pubitemid 10037059)
7. 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.
8. 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.
9. 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)
10. Seale, A., and A. Finn. 2011. What is the best way to use conjugate vaccines? Curr. Opin. Infect. Dis. 24: 219-224.
11. Jedrzejas, M. J. 2001. Pneumococcal virulence factors: structure and function. Microbiol. Mol. Biol. Rev. 65: 187-207. (Pubitemid 32538177)
12. Kraal, G., H. Ter Hart, C. Meelhuizen, G. Venneker, and E. Claassen. 1989. Marginal zone macrophages and their role in the immune response against T-independent type 2 antigens: modulation of the cells with specific antibody. Eur. J. Immunol. 19: 675-680. (Pubitemid 19152935)
13. 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.
14. Kovacsovics-Bankowski, M., K. Clark, B. Benacerraf, and K. L. Rock. 1993. Efficient major histocompatibility complex class I presentation of exogenous antigen upon phagocytosis by macrophages. Proc. Natl. Acad. Sci. USA 90: 4942-4946. (Pubitemid 23182951)
15. Ziegler, H. K., C. A. Orlin, and C. W. Cluff. 1987. Differential requirements for the processing and presentation of soluble and particulate bacterial antigens by macrophages. Eur. J. Immunol. 17: 1287-1296. (Pubitemid 17148168)
16. Vidard, L., M. Kovacsovics-Bankowski, S. K. Kraeft, L. B. Chen, B. Benacerraf, and K. L. Rock. 1996. Analysis of MHC class II presentation of particulate antigens of B lymphocytes. J. Immunol. 156: 2809-2818. (Pubitemid 126660628)
17. Snapper, C. M. 2012. Mechanisms underlying in vivo polysaccharide- specific immunoglobulin responses to intact extracellular bacteria. Ann. N. Y. Acad. Sci. 1253: 92-101.
18. Lucas, A. H., D. M. Granoff, R. E. Mandrell, C. C. Connolly, A. S. Shan, and D. C. Powers. 1997. Oligoclonality of serum immunoglobulin G antibody responses to Streptococcus pneumoniae capsular polysaccharide serotypes 6B, 14, and 23F. Infect. Immun. 65: 5103-5109. (Pubitemid 27513556)
19. Zhou, J., K. R. Lottenbach, S. J. Barenkamp, and D. C. Reason. 2004. Somatic hypermutation and diverse immunoglobulin gene usage in the human antibody response to the capsular polysaccharide of Streptococcus pneumoniae Type 6B. Infect. Immun. 72: 3505-3514. (Pubitemid 38697777)
20. Pawlak, L. L., E. B. Mushinski, A. Nisonoff, and M. Potter. 1973. Evidence for the linkage of the IGC H locus to a gene controlling the idiotypic specificity of anti-p-azophenylarsonate antibodies in strain A mice. J. Exp. Med. 137: 22-31.
21. Stall, A. M., J. Quintáns, and M. R. Loken. 1986. T15 idiotype expression in the murine response to phosphorylcholine is actively regulated by genes linked to the Igh-C locus. J. Immunol. 136: 2689-2696. (Pubitemid 16136858)
22. Pène, J., H. Zaghouani, and M. Stanislawski. 1983. Regulation of the response to alpha 1-3 dextran in IghCb mice. Ann. N. Y. Acad. Sci. 418: 296-304. (Pubitemid 14190518)
23. Sanchez, P., D. Juy, and P. A. Cazenave. 1983. Allotypic restriction of the expression of MOPC460 idiotope after immunization with either anti-2,4-dinitrophenyl (DNP) or anti-idiotypic antibodies. Eur. J. Immunol. 13: 999-1003. (Pubitemid 14223579)
24. Lucas, A. H., K. D. Moulton, V. R. Tang, and D. C. Reason. 2001. Combinatorial library cloning of human antibodies to Streptococcus pneumoniae capsular polysaccharides: variable region primary structures and evidence for somatic mutation of Fab fragments specific for capsular serotypes 6B, 14, and 23F. Infect. Immun. 69: 853-864. (Pubitemid 32109549)
25. Zhou, J., K. R. Lottenbach, S. J. Barenkamp, A. H. Lucas, and D. C. Reason. 2002. Recurrent variable region gene usage and somatic mutation in the human antibody response to the capsular polysaccharide of Streptococcus pneumoniae type 23F. Infect. Immun. 70: 4083-4091. (Pubitemid 34790916)
26. Baxendale, H. E., Z. Davis, H. N. White, M. B. Spellerberg, F. K. Stevenson, and D. Goldblatt. 2000. Immunogenetic analysis of the immune response to pneumococcal polysaccharide. Eur. J. Immunol. 30: 1214-1223. (Pubitemid 30216239)
27. Snapper, C. M. 2006. Differential regulation of protein- and polysaccharide-specific Ig isotype production in vivo in response to intact Streptococcus pneumoniae. Curr. Protein Pept. Sci. 7: 295-305.
28. 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.
29. Arjunaraja, S., L. C. Paoletti, and C. M. Snapper. 2012. Structurally identical capsular polysaccharide expressed by intact Group B Streptococcus versus Streptococcus pneumoniae elicits distinct murine polysaccharide-specific IgG responses in vivo. J. Immunol. In press.
30. National Research Council. 1996. Guide for the Care and Use of Laboratory Animals. National Academy Press, Washington, DC.
31. 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.
32. Briles, D. E., J. D. King, M. A. Gray, L. S. McDaniel, E. Swiatlo, and K. A. Benton. 1996. PspA, a protection-eliciting pneumococcal protein: immunogenicity of isolated native PspA in mice. Vaccine 14: 858-867. (Pubitemid 26280926)
33. Lucas, A. H., R. J. Langley, D. M. Granoff, M. H. Nahm, M. Y. Kitamura, and M. G. Scott. 1991. An idiotypic marker associated with a germ-line encoded kappa light chain variable region that predominates the vaccine-induced human antibody response to the Haemophilus influenzae b polysaccharide. J. Clin. Invest. 88: 1811-1818.
34. O'Shannessy, D. J., and R. H. Quarles. 1985. Specific conjugation reactions of the oligosaccharide moieties of immunoglobulins. J. Appl. Biochem. 7: 347-355. (Pubitemid 16130699)
35. Pullen, G. R., M. G. Fitzgerald, and C. S. Hosking. 1986. Antibody avidity determination by ELISA using thiocyanate elution. J. Immunol. Methods 86: 83-87. (Pubitemid 16187291)
36. van Dam, G. J., A. F. Verheul, G. J. Zigterman, M. J. de Reuver, and H. Snippe. 1989. Estimation of the avidity of antibodies in polyclonal antisera against Streptococcus pneumoniae type 3 by inhibition ELISA. Mol. Immunol. 26: 269-274. (Pubitemid 19082779)
37. Colino, J., and C. M. Snapper. 2007. Dendritic cell-derived exosomes express a Streptococcus pneumoniae capsular polysaccharide type 14 cross-reactive antigen that induces protective immunoglobulin responses against pneumococcal infection in mice. Infect. Immun. 75: 220-230. (Pubitemid 46047896)
38. Lindberg, B., J. Lönngren, and D. A. Powell. 1977. Structural studies on the specific type-14 pneumococcal polysaccharide. Carbohydr. Res. 58: 177-186.
39. Kenny, J. J., E. G. Derby, J. A. Yoder, S. A. Hill, R. T. Fischer, P. W. Tucker, J. L. Claflin, and D. L. Longo. 2000. Positive and negative selection of antigen-specific B cells in transgenic mice expressing variant forms of the V(H)1 (T15) heavy chain. Int. Immunol. 12: 873-885. (Pubitemid 30410460)
40. Wessels, M. R., and D. L. Kasper. 1989. Antibody recognition of the type 14 pneumococcal capsule. Evidence for a conformational epitope in a neutral polysaccharide. J. Exp. Med. 169: 2121-2131. (Pubitemid 19162971)
41. Safari, D., H. A. Dekker, J. A. Joosten, D. Michalik, A. C. de Souza, R. Adamo, M. Lahmann, A. Sundgren, S. Oscarson, J. P. Kamerling, and H. Snippe. 2008. Identification of the smallest structure capable of evoking opsonophagocytic antibodies against Streptococcus pneumoniae type 14. Infect. Immun. 76: 4615-4623.
42. Harris, S. L., and P. Fernsten. 2009. Thermodynamics and density of binding of a panel of antibodies to high-molecular-weight capsular polysaccharides. Clin. Vaccine Immunol. 16: 37-42.
43. Celada, F., D. Schmidt, and R. Strom. 1969. Determination of avidity of antialbumin antibodies in the mouse. Influence of the number of cells transferred on the quality of the secondary adoptive response. Immunology 17: 189-198.
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. Colino, J., Y. Shen, and C. M. Snapper. 2002. Dendritic cells pulsed with intact Streptococcus pneumoniae elicit both protein- and polysaccharide- specific immunoglobulin isotype responses in vivo through distinct mechanisms. J. Exp. Med. 195: 1-13. (Pubitemid 34074491)
46. Taketo, M., A. C. Schroeder, L. E. Mobraaten, K. B. Gunning, G. Hanten, R. R. Fox, T. H. Roderick, C. L. Stewart, F. Lilly, C. T. Hansen, et al. 1991. FVB/ N: an inbred mouse strain preferable for transgenic analyses. Proc. Natl. Acad. Sci. USA 88: 2065-2069. (Pubitemid 21916354)
47. 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)
48. Jedrzejas, M. J. 2004. Extracellular virulence factors of Streptococcus pneumoniae. Front. Biosci. 9: 891-914. (Pubitemid 39043760)
49. Wessels, M. R., V. Pozsgay, D. L. Kasper, and H. J. Jennings. 1987. Structure and immunochemistry of an oligosaccharide repeating unit of the capsular polysaccharide of type III group B Streptococcus. A revised structure for the type III group B streptococcal polysaccharide antigen. J. Biol. Chem. 262: 8262-8267.
50. 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.
51. Kraal, G., and R. Mebius. 2006. New insights into the cell biology of the marginal zone of the spleen. Int. Rev. Cytol. 250: 175-215. (Pubitemid 44067206)
52. Berek, C., A. Berger, and M. Apel. 1991. Maturation of the immune response in germinal centers. Cell 67: 1121-1129. (Pubitemid 121001525)
53. Jacob, J., G. Kelsoe, K. Rajewsky, and U. Weiss. 1991. Intraclonal generation of antibody mutants in germinal centres. Nature 354: 389-392. (Pubitemid 21896846)
54. McHeyzer-Williams, L. J., N. Pelletier, L. Mark, N. Fazilleau, and M. G. McHeyzer-Williams. 2009. Follicular helper T cells as cognate regulators of B cell immunity. Curr. Opin. Immunol. 21: 266-273.
55. Herlands, R. A., S. R. Christensen, R. A. Sweet, U. Hershberg, and M. J. Shlomchik. 2008. T cell-independent and toll-like receptor-dependent antigen-driven activation of autoreactive B cells. Immunity 29: 249-260.
56. William, J., C. Euler, S. Christensen, and M. J. Shlomchik. 2002. Evolution of autoantibody responses via somatic hypermutation outside of germinal centers. Science 297: 2066-2070.
57. MacLennan, I. C., K. M. Toellner, A. F. Cunningham, K. Serre, D. M. Sze, E. Zúñiga, M. C. Cook, and C. G. Vinuesa. 2003. Extrafollicular antibody responses. Immunol. Rev. 194: 8-18. (Pubitemid 36886424)
58. Chang, P. P., P. Barral, J. Fitch, A. Pratama, C. S. Ma, A. Kallies, J. J. Hogan, V. Cerundolo, S. G. Tangye, R. Bittman, et al. 2012. Identification of Bcl-6-dependent follicular helper NKT cells that provide cognate help for B cell responses. Nat. Immunol. 13: 35-43.
59. Inamine, A., Y. Takahashi, N. Baba, K. Miyake, T. Tokuhisa, T. Takemori, and R. Abe. 2005. Two waves of memory B-cell generation in the primary immune response. Int. Immunol. 17: 581-589. (Pubitemid 41417855)
60. Martin, F., and J. F. Kearney. 2002. Marginal-zone B cells. Nat. Rev. Immunol. 2: 323-335. (Pubitemid 37328755)
61. Carey, J. B., C. S. Moffatt-Blue, L. C. Watson, A. L. Gavin, and A. J. Feeney. 2008. Repertoire-based selection into the marginal zone compartment during B cell development. J. Exp. Med. 205: 2043-2052.
62. Schelonka, R. L., J. Tanner, Y. Zhuang, G. L. Gartland, M. Zemlin, and H. W. Schroeder, Jr. 2007. Categorical selection of the antibody repertoire in splenic B cells. Eur. J. Immunol. 37: 1010-1021. (Pubitemid 46925338)
63. Pillai, S., and A. Cariappa. 2009. The follicular versus marginal zone B lymphocyte cell fate decision. Nat. Rev. Immunol. 9: 767-777.
64. Pillai, S., A. Cariappa, and S. T. Moran. 2005. Marginal zone B cells. Annu. Rev. Immunol. 23: 161-196. (Pubitemid 40563168)
65. Wen, L., J. Brill-Dashoff, S. A. Shinton, M. Asano, R. R. Hardy, and K. Hayakawa. 2005. Evidence of marginal-zone B cell-positive selection in spleen. Immunity 23: 297-308. (Pubitemid 41317797)
66. Snapper, C. M., H. Yamada, D. Smoot, R. Sneed, A. Lees, and J. J. Mond. 1993. Comparative in vitro analysis of proliferation, Ig secretion, and Ig class switching by murine marginal zone and follicular B cells. J. Immunol. 150: 2737-2745. (Pubitemid 23127523)
67. Oliver, A. M., F. Martin, G. L. Gartland, R. H. Carter, and J. F. Kearney. 1997. Marginal zone B cells exhibit unique activation, proliferative and immunoglobulin secretory responses. Eur. J. Immunol. 27: 2366-2374. (Pubitemid 27404323)
68. 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)
69. Genestier, L., M. Taillardet, P. Mondiere, H. Gheit, C. Bella, and T. Defrance. 2007. TLR agonists selectively promote terminal plasma cell differentiation of B cell subsets specialized in thymus-independent responses. J. Immunol. 178: 7779-7786. (Pubitemid 46898049)
70. 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)
71. Haas, K. M., J. C. Poe, D. A. Steeber, and T. F. Tedder. 2005. B-1a and B-1b cells exhibit distinct developmental requirements and have unique functional roles in innate and adaptive immunity to S. pneumoniae. Immunity 23: 7-18. (Pubitemid 41019653)
72. Alugupalli, K. R., J. M. Leong, R. T. Woodland, M. Muramatsu, T. Honjo, and R. M. Gerstein. 2004. B1b lymphocytes confer T cell-independent long-lasting immunity. Immunity 21: 379-390. (Pubitemid 39208339)
73. Bowen, M. B., and C. J. Bellone. 1987. Allotype-linked production of an idiotype-specific factor that promotes idiotype expression in nonresponder strains. J. Immunol. 139: 1780-1785. (Pubitemid 17141602)
74. Masmoudi, H., T. Mota-Santos, F. Huetz, A. Coutinho, and P.-A. Cazenave. 1990. All T15 Id-positive antibodies (but not the majority of VHT15+ antibodies) are produced by peritoneal CD5+ B lymphocytes. Int. Immunol. 2: 515-520. (Pubitemid 20218428)
75. Mahmoud, T. I., and J. F. Kearney. 2010. Terminal deoxynucleotidyl transferase is required for an optimal response to the polysaccharide a-1,3 dextran. J. Immunol. 184: 851-858.
76. Konradsen, H. B., V. A. Oxelius, M. Hahn-Zoric, and L. A. Hanson. 1994. The importance of G1m and 2 allotypes for the IgG2 antibody levels and avidity against pneumococcal polysaccharide type 1 within mono- and dizygotic twinpairs. Scand. J. Immunol. 40: 251-256. (Pubitemid 24251745)
77. 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.
78. Shriner, A. K., S. L. Smithson, D. M. Prinz, B. Rabquer, S. Khuder, R. Goomber, and M. A. Westerink. 2006. Comparison of the human immune response to conjugate and polysaccharide pneumococcal vaccination using a reconstituted SCID mouse model. Vaccine 24: 7197-7203. (Pubitemid 46110798)
79. Granoff, D. M., P. G. Shackelford, S. J. Holmes, and A. H. Lucas; The Collaborative Vaccine Study Group. 1993. Variable region expression in the antibody responses of infants vaccinated with Haemophilus influenzae type b polysaccharide-protein conjugates. Description of a new lambda light chain-associated idiotype and the relation between idiotype expression, avidity, and vaccine formulation. J. Clin. Invest. 91: 788-796. (Pubitemid 23095251)
80. Lucas, A. H., and D. M. Granoff. 1995. Functional differences in idiotypically defined IgG1 anti-polysaccharide antibodies elicited by vaccination with Haemophilus influenzae type B polysaccharide-protein conjugates. J. Immunol. 154: 4195-4202.