Early life T Cell responses to pneumucoccal conjugates increase with age and determine the polysaccharide-specific antibody response and protective efficacy

European Journal of Immunology

Volumn 36, Issue 2, 2006, Pages 287-295

  Jakobsen, Håvard ^a,b   Hannesdottir, Solveig ^a,e   Bjarnarson, Stefania P ^a,b   Schulz, Dominique ^c   Trannoy, Emanuelle ^c   Siegrist, Claire Anne ^d   Jonsdottir, Ingileif ^a,b  

^a LANDSPITALI UNIVERSITY HOSPITAL   (Iceland)

^b UNIVERSITY OF ICELAND   (Iceland)

^c SANOFI PASTEUR   (France)

^d UNIVERSITY OF GENEVA   (Switzerland)

^e NORD UNIVERSITY   (Norway)

Author keywords

Antibodies; Conjugate vaccine; Neonatal vaccination; Pneumococcus; T cell responses

Indexed keywords

GAMMA INTERFERON; IMMUNOGLOBULIN G; INTERLEUKIN 5; POLYSACCHARIDE VACCINE; STREPTOCOCCUS VACCINE;

AGE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; CELL PROLIFERATION; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; ENZYME LINKED IMMUNOSORBENT ASSAY; IMMUNIZATION; IMMUNOGENICITY; IN VITRO STUDY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL; PROTECTION; SPLEEN CELL; STREPTOCOCCUS INFECTION; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

ADJUVANTS, IMMUNOLOGIC; AGING; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, BACTERIAL; ANTIBODY FORMATION; IMMUNOLOGIC MEMORY; LYMPHOCYTE ACTIVATION; MICE; PNEUMOCOCCAL VACCINES; POLYSACCHARIDES, BACTERIAL; TETANUS TOXOID; TH1 CELLS; TH2 CELLS; VACCINES, CONJUGATE;

EID: 32944466431     PISSN: 00142980     EISSN: None     Source Type: Journal    
DOI: 10.1002/eji.200535102     Document Type: Article

References (55)

1. Gray, B. M. and Dillon, H. C., Clinical and epidemiologic studies of pneumococcal infection in children. Pediatr. Infect. Dis. J. 1986. 5: 201-207.
2. Dagan, R. and Musher, D., Is the pneumococcus the one and only in acute otitis media? Pediatr. Infect. Dis. J. 2000. 19: 399-400.
3. Jokinen, C., Heiskanen, L., Juvonen, H., Kallinen, S., Kleemola, M., Koskela, M., Leinonen, M. et al., Microbial etiology of community-acquired pneumonia in the adult population of 4 municipalities in eastern Finland. Clin. Infect. Dis. 2001. 32: 1141-1154.
4. Shann, F., Etiology of severe pneumonia in children in developing countries. Pediatr. Infect. Dis. 1986. 5: 247-252.
5. Adegbola, R. A. and Obaro, S. K., Diagnosis of childhood pneumonia in the tropics. Ann. Trop. Med. Parasitol. 2000. 94: 197-207.
6. Gold, R., Epidemiology of bacterial meningitis. Infect. Dis. Clin. North Am. 1999. 13: 515-525.
7. Mond, J. J., Lees, A. and Snapper, C. M., T cell-independent antigens type 2. Ann. Rev. Immunol. 1995. 13: 655-692.
8. Ishioka, G. Y., Lamont, A. G., Thomson, D., Bulbow, N., Gaeta, F. C. A., Sette, A. and Grey, H. M., MHC interaction and T cell recognition of carbohydrates and glycopeptides. J. Immunol. 1992. 148: 2446-2451.
9. Harding, C. V., Roof, R. W., Allen, P. M. and Unanue, E. R., Effect of pH and polysaccharides on peptide binding to class II major histocompatibility complex molecules. Proc. Natl. Acad. Sci. USA 1991. 88: 2740-2744.
10. McCool, T. L., Harding, C. V., Greenspan, N. S. and Schreiber, J. R., B- and T cell immune responses to pneumococcal conjugate vaccines: Divergence between carrier-and polysaccharide-specific immunogenicity. Infect. Immun. 1999. 67: 4862-4869.
11. + T cell cytokine response that correlates with the isotype of antipolysaccharide antibody. J. Infect. Dis. 2001. 184: 931-935.
12. Wuorimaa, T., Käyhty, H., Eskola, J., Bloigu, A., Leroy, O. and Surcel, H. M., Activation of cell-mediated immunity following immunization with pneumococcal conjugate or polysaccharide vaccine. Scand. J. Immunol. 2001. 53: 422-428.
13. Mawas, F., Feavers, I. M. and Corbel, M. J., Serotype of Streptococcus pneumoniae capsular polysaccharide can modify the Th1/Th2 cytokine profile and IgG subclass response to pneumococal-CRM(197) conjugate vaccines in a murine model. Vaccine 2000. 19: 1159-1166.
14. Guttormsen, H. K., Sharpe, A., Chandraker, A. K., Brigtsen, A. R., Sayegh, M. M. and Kasper, D. L., Cognate stimulatory B-cell-T cell interactions are critical for T cell help required by glycoconjugate vaccines. Infect. Immun. 1999. 67: 6375-6384.
15. Wuorimaa, T. and Kayhty, H., Current state of pneumococcal vaccines. Scand. J. Immunol. 2002. 56: 111-129.
16. Black, S., Shinefield, H., Fireman, B., Lewis, E., Ray, P., Hansen, J., Elvin, L. et al., Efficacy, safety and immunogenicity of heptavalent pneumococcal conjugate vaccine in children. Northern California Kaiser Permanente Vaccine Study Center Group. Pediatr. Infect. Dis. J. 2000. 19: 187-195.
17. Shinefield, H., Black, S., Ray, P., Fireman, B., Schwallbe, J. and Lewis, E., Efficacy, immunogenicity and safety of heptavalent pneumococcal conjugate vaccine in low birth weight and preterm infants. Pediatr. Infect. Dis. J. 2002. 21: 182-186.
18. Eskola, J., Kilpi, T., Palmu, A., Jokinen, J., Haapakoski, J., Herva, E., Takala, A. et al., Efficacy of a pneumococcal conjugate vaccine against acute otitis media. N. Engl. J. Med. 2001. 344: 403-409.
19. Jonsdottir, I., Ingolfsdottir, G., Saeland, E., Davidsdottir, K., Yaich, M., Leroy, O. and Sigurdardottir, S. T., A single dose of pneumococcal conjugate vaccine elicits functional antibodies and induces memory in toddlers, abstr. G-43. In Abstracts, in Programs and Abstracts of the 40th Interscience Conference on Antimicrobial Agents and Chemotherapy. American Society for Microbiology, Washington D.C. 2000
20. Åhman, H., Käyhty, H., Lehtonen, H., Leroy, O., Froeschle, J. and Eskola, J., Streptococcus pneumoniae capsular polysaccharide-diphtheria toxoid conjugate vaccine is immunogenic in early infancy and able to induce immunologic memory. Pediatr. Infect. Dis. J. 1998. 17: 211-216.
21. Obaro, S. K., Huo, Z., Banya, W. A., Henderson, D. C., Monteil, M. A., Leach, A. and Greenwood, B. M., A glycoprotein pneumococcal conjugate vaccine primes for antibody responses to a pneumococcal polysaccharide vaccine in Gambian children. Pediatr. Infect. Dis. J. 1997. 16: 1135-1140.
22. Adkins, B., Leclerc, C. and Marshall-Clarke, S., Neonatal adaptive immunity comes of age. Nat. Rev. Immunol. 2004. 4: 553-564.
23. Siegrist, C. A., Neonatal and early life vaccinology. Vaccine 2001. 19: 3331-3346.
24. Zola, H., The development of antibody responses in the infant. Immunol. Cell. Biol. 1997 75: 587-590.
25. Ridings, J., Nicholson, I. C., Goldsworthy, W., Haslam, R., Roberton, D. M. and Zola, H., Somatic hypermutation of immunoglobulin genes in human neonates. Clin. Exp. Immunol. 1997. 108: 366-374.
26. Fadel, S. and Sarzotti, M., Cellular responses in neonates. Intern. Rev. Immunol. 2000. 19: 173-193.
27. Adkins, B., T cell function in newborn mice and humans. Immunol. Today 1999. 20: 330-335.
28. + lymph node cells are highly deficient in the development of antigen-specific Th1 function in adoptive adult hosts. J. Immunol. 2002. 169: 4998-5004.
29. Siegrist, C. A., Plotnicky-Gilquin, H., Cordova, M., Berney, M., Bonnefoy, J. Y., Nguyen, T. N., Lambert, P. H. and Power, U. F., Protective efficacy against respiratory syncytial virus following murine neonatal immunization with BBG2Na vaccine: Influence of adjuvants and maternal antibodies. J. Infect. Dis. 1999. 179: 1326-1333.
30. Barrios, C., Brawand, P., Berney, M., Brandt, C., Lambert, P. H. and Siegrist, C. A., Neonatal and early life immune responses to various forms of vaccine antigens qualitatively differ from adult responses: predominance of a Th2-based pattern which persists after adult boosting. Eur. J. Immunol. 1996. 26: 1489-1496.
31. Ribeiro-do-Couto, L. M., Boeije, L. C., Kroon, J. S., Hooibrink, B., Breur-Vriesendorp, B. S., Aarden, L. A. and Boog, C. J., High IL-13 production by human neonatal T cells: neonate immune system regulator? Eur. J. Immunol. 2001. 31: 3394-3402.
32. Adkins, B. and Hamilton, K., Freshly isolated, murine neonatal T cells produce IL-4 in response to anti-CD3 stimulation. J. Immunol. 1992. 149: 3448-3455.
33. Barrios, C., Brandt, C., Burney, M., Lambert, P. H. and Siegrist, C. A., Partial correction of the TH2/TH1 imbalance in neonatal murine responses to vaccine antigens through selective adjuvant effects. Eur. J. Immunol. 1996. 26: 2666-2670.
34. Jakobsen, H., Bjarnarson, S. P., Del Giudice, G., Moreau, M., Siegrist, C. A. and Jonsdottir, I., Intranasal immunization with pneumococcal conjugate vaccines with LT-K63, a non toxic mutant of heat-labile enterotoxin, as adjuvant rapidly induces protective immunity against lethal pneumococcal infections in neonatal mice. Infect. Immun. 2002. 70: 1443-1452.
35. Saeland, E., Vidarsson, G. and Jonsdottir, I., Pneumococcal pneumonia and bacteremia model in mice for the analysis of protective antibodies. Microb. Pathog. 2000. 29: 81-91.
36. Jakobsen, H., Adarna, B. C., Schulz, D., Rappuoli, R. and Jonsdottir, I., Characterization of the antibody response to pneumococcal glycoconjugates and the effect of heat-labile enterotoxin on IgG subclasses after intranasal immunization. J. Infect. Dis. 2001. 183: 1494-1500.
37. Adkins, B. and Du, R. Q., Newborn mice develop balanced Th1/Th2 primary effector responses in vivo but are biased to Th2 secondary responses. J. Immunol. 1998. 160: 4217-4224.
38. Adkins, B., Bu, Y. and Guevara, P., The generation of Th memory in neonates versus adults: prolonged primary Th2 effector function and impaired development of Th1 memory effector function in murine neonates. J. Immunol. 2001. 166: 918-925.
39. Rubinstein, L. J. and Stein, K. E., Murine immune response to the Neisseria meningitidis group C capsular polysaccharide. I. Ontogeny. J. Immunol. 1988. 141: 4352-4356.
40. Siber, G. R., Pneumococcal disease: Prospects for a new generation of vaccines. Science 1994. 265: 1385-1387.
41. Vernacchio, L., Bernstein, H., Pelton, S., Allen, C., MacDonald, K., Dunn, J., Duncan, D. D. et al., Effect of monophosphoryl lipid A (MPL) on T-helper cells when administered as an adjuvant with pneumocococcal-CRM197 conjugate vaccine in healthy toddlers. Vaccine 2002. 20: 3658-3667.
42. Bjarnarson, S. P., Jakobsen, H., Del Giudice, G., Trannoy, E., Siegrist, C. A. and Jonsdottir, I., The advantage of mucosal immunization for polysaccharide-specific memory responses in early life. Eur. J. Immunol. 2005. 35: 1037-1045.
43. Pihlgren, M., Tougne, C., Bozzotti, P., Fulurija, A., Duchosal, M. A., Lambert, P. H. and Siegrist, C. A., Unresponsiveness to lymphoid-mediated signals at the neonatal follicular dendritic cell precursor level contributes to delayed germinal center induction and limitations of neonatal antibody responses to T-dependent antigens. J. Immunol. 2003. 170: 2824-2832.
44. Kamboj, K. K., Kirchner, H. L., Kimmel, R., Greenspan, N. S. and Schreiber, J. R., Significant variation in serotype-specific immunogenicity of the seven-valent Streptococcus pneumoniae capsular polysaccharide-CRM197 conjugate vaccine occurs despite vigorous Tcell help induced by the carrier protein. J. Infect. Dis. 2003. 187: 1629-1638.
45. Leonard, E. G., Canaday, D. H., Harding, C. V. and Schreiber, J. R., Antigen processing of the heptavalent pneumococcal conjugate vaccine carrier protein CRM(197) differs depending on the serotype of the attached polysaccharide. Infect. Immun. 2003. 71: 4186-4189.
46. Stingele, F., Corthesy, B., Kusy, N., Porcelli, S. A., Kasper, D. L. and Tzianabos, A. O., Zwitterionic polysaccharides stimulate T cells with no preferential V beta usage and promote anergy, resulting in protection against experimental abscess formation. J. Immunol. 2004. 172: 1483-1490.
47. Petty, R. E. and Hunt, D. W., Neonatal dendritic cells. Vaccine 1998. 16: 1378-1382.
48. Steinman, R. M., The dendritic cell system and its role in immunogenicity. Ann. Rev. Immunol. 1991. 9: 271-296.
49. Guermonprez, P., Valladeau, J., Zitvogel, L., Thery, C. and Amigorena, S., Antigen presentation and T cell stimulation by dendritic cells. Ann. Rev. Immunol 2002. 20: 667.
50. Hunt, D. W., Huppertz, H. I., Jiang, H. J. and Petty, R. E., Studies of human cord blood dendritic cells: evidence for functional immaturity. Blood 1994. 84: 4333-4343.
51. Muthukkumar, S., Goldstein, J. and Stein, K. E., The ability of B cells and dentritic cells to present antigen increases during ontogeny. J. Immunol. 2000. 165: 4803-4813.
52. Goriely, S., Vincart, B., Stordeur, P., Vekemans, J., Willems, F., Goldman, M. and De Wit, D., Deficient IL-12(p35) gene expression by dendritic cells derived from neonatal monocytes. J. Immunol. 2001. 166: 2141-2146.
53. Trinchieri, G., Interleukin-12: a proinflammatory cytokine with immunoregulatory functions that bridge innate resistance and antigen-specific adaptive immunity. Ann. Rev. Immunol. 1995. 13: 251-276.
54. Lambert, P. H., Liu, M. and Siegrist, C. A., Can successful vaccines teach us how to induce efficient protective immune responses? Nat. Med. 2005. 11: S54-62.
55. Szu, S. C., Taylor, D. N., Trofa, A. C., Clements, J. D., Shiloach, J., Sadoff, J. C., Bryla, D. A. and Robbins, J. B., Laboratory and preliminary clinical characterization of Vi capsular polysaccharide-protein conjugate vaccines. Infect. Immun. 1994. 62: 4440-4444.