Concomitant administration of Mycobacterium bovis BCG with the meningococcal C conjugate vaccine to neonatal mice enhances antibody response and protective efficacy

Clinical and Vaccine Immunology

Volumn 18, Issue 11, 2011, Pages 1936-1942

  Brynjolfsson, Siggeir F ^a,b   Bjarnarson, Stefania P ^a,b   Mori, Elena ^c   Del Giudice, Giuseppe ^c   Jonsdottir, Ingileif ^a,b,d  

^a Landspitali ^*  (Iceland)

^b UNIVERSITY OF ICELAND   (Iceland)

^c NOVARTIS VACCINES AND DIAGNOSTICS   (Italy)

^d DECODE GENETICS   (Iceland)

Author keywords

[No Author keywords available]

Indexed keywords

BCG VACCINE; IMMUNOGLOBULIN G; IMMUNOGLOBULIN G1; IMMUNOGLOBULIN G2A; IMMUNOGLOBULIN G2B; MENINGOCOCCAL C CRM197 CONJUGATE VACCINE; MENINGOCOCCUS VACCINE; UNCLASSIFIED DRUG;

ADJUVANT THERAPY; ANIMAL EXPERIMENT; ANTIBODY AFFINITY; ANTIBODY PRODUCTION; ANTIBODY RESPONSE; ANTIBODY SPECIFICITY; ANTIBODY TITER; ARTICLE; BACTERICIDAL ACTIVITY; BCG VACCINATION; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; IMMUNE RESPONSE; INFECTION PREVENTION; MENINGOCOCCOSIS; MONOTHERAPY; MOUSE; NEWBORN; NONHUMAN; PRIORITY JOURNAL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES, BACTERIAL; BCG VACCINE; BLOOD BACTERICIDAL ACTIVITY; IMMUNIZATION, SECONDARY; IMMUNOGLOBULIN G; INJECTIONS, SUBCUTANEOUS; MENINGOCOCCAL VACCINES; MICE; VACCINATION;

EID: 80455129070     PISSN: 15566811     EISSN: 1556679X     Source Type: Journal    
DOI: 10.1128/CVI.05247-11     Document Type: Article

References (66)

1. Andersen, P., and T. M. Doherty. 2005. The success and failure of BCG - implications for a novel tuberculosis vaccine. Nat. Rev. Microbiol. 3:656-662. (Pubitemid 41052152)
2. Avery, D. T., V. L. Bryant, C. S. Ma, R. de Waal Malefyt, and S. G. Tangye. 2008. IL-21-induced isotype switching to IgG and IgA by human naive B cells is differentially regulated by IL-4. J. Immunol. 181:1767-1779.
3. Baudner, B. C., et al. 2002. Enhancement of protective efficacy following intranasal immunization with vaccine plus a nontoxic LTK63 mutant delivered with nanoparticles. Infect. Immun. 70:4785-4790.
4. Bjarnarson, S. P., et al. 2005. The advantage of mucosal immunization for polysaccharide-specific memory responses in early life. Eur. J. Immunol. 35:1037-1045. (Pubitemid 40542210)
5. Borrow, R., P. Balmer, and E. Miller. 2005. Meningococcal surrogates of protection-serum bactericidal antibody activity. Vaccine 23:2222-2227. (Pubitemid 40341456)
6. Brewer, T. F. 2000. Preventing tuberculosis with bacillus Calmette-Guerin vaccine: a meta-analysis of the literature. Clin. Infect. Dis. 31(Suppl. 3):S64-S67. (Pubitemid 32269590)
7. Brynjolfsson, S. F., S. P. Bjarnarson, E. Mori, G. Del Giudice, and I. Jonsdottir. 2008. Neonatal immune response and serum bactericidal activity induced by a meningococcal conjugate vaccine is enhanced by LT-K63 and CpG2006. Vaccine 26:4557-4562.
8. Chackerian, A. A., and S. M. Behar. 2003. Susceptibility to Mycobacterium tuberculosis: lessons from inbred strains of mice. Tuberculosis (Edinb.) 83:279-285. (Pubitemid 37175893)
9. Clutterbuck, E. A., et al. 2008. Serotype-specific and age-dependent generation of pneumococcal polysaccharide-specific memory B-cell and antibody responses to immunization with a pneumococcal conjugate vaccine. Clin. Vaccine Immunol. 15:182-193. (Pubitemid 352025528)
10. Del Giudice, G. 2003. Vaccination strategies. An overview. Vaccine 21(Suppl. 2):S83-S88.
11. Dellicour, S., and B. Greenwood. 2007. Systematic review: impact of meningococcal vaccination on pharyngeal carriage of meningococci. Trop. Med. Int. Health 12:1409-1421. (Pubitemid 350212705)
12. Freudenstein, H., E. Weinmann, and I. Hill. 1988. Potency testing of BCG vaccines on white mice: influence of variables on survival time, lung findings and vaccine assessment. Vaccine 6:315-327.
13. Gheesling, L. L., et al. 1994. Multicenter comparison of Neisseria meningitidis serogroup C anti-capsular polysaccharide antibody levels measured by a standardized enzyme-linked immunosorbent assay. J. Clin. Microbiol. 32:1475-1482. (Pubitemid 24179378)
14. Giri, P. K., I. Verma, and G. K. Khuller. 2006. Protective efficacy of intranasal vaccination with Mycobacterium bovis BCG against airway Mycobacterium tuberculosis challenge in mice. J. Infect. 53:350-356. (Pubitemid 44524702)
15. Gold, R., M. L. Lepow, I. Goldschneider, T. L. Draper, and E. C. Gotschlich. 1975. Clinical evaluation of group A and group C meningococcal polysaccharide vaccines in infants. J. Clin. Invest. 56:1536-1547.
16. Goldblatt, D., L. van Etten, F. J. van Milligen, R. C. Aalberse, and M. W. Turner. 1993. The role of pH in modified ELISA procedures used for the estimation of functional antibody affinity. J. Immunol. Methods 166:281-285. (Pubitemid 24034893)
17. Goldschneider, I., E. C. Gotschlich, and M. S. Artenstein. 1969. Human immunity to the meningococcus. I. The role of humoral antibodies. J. Exp. Med. 129:1307-1326.
18. Goriely, S., et al. 2001. Deficient IL-12(p35) gene expression by dendritic cells derived from neonatal monocytes. J. Immunol. 166:2141-2146. (Pubitemid 32114705)
19. Granoff, D. M., J. A. Welsch, and S. Ram. 2009. Binding of complement factor H (fH) to Neisseria meningitidis is specific for human fH and inhibits complement activation by rat and rabbit sera. Infect. Immun. 77:764-769.
20. Hannesdottir, S. G., T. A. Olafsdottir, G. D. Giudice, and I. Jonsdottir. 2008. Adjuvants LT-K63 and CpG enhance the activation of dendritic cells in neonatal mice. Scand. J. Immunol. 68:469-475.
21. Harrison, L. H., et al. 2011. The Global Meningococcal Initiative: recommendations for reducing the global burden of meningococcal disease. Vaccine 29:3363-3371.
22. Holsapple, M. P., L. J. West, and K. S. Landreth. 2003. Species comparison of anatomical and functional immune system development. Birth Defects Res. B Dev. Reprod. Toxicol. 68:321-334. (Pubitemid 37238421)
23. Jain, V., S. P. Vyas, and D. V. Kohli. 2009. Well-defined and potent liposomal hepatitis B vaccines adjuvanted with lipophilic MDP derivatives. Nanomedicine 5:334-344.
24. Jakobsen, H., et al. 2002. Intranasal immunization with pneumococcal conjugate vaccines with LT-K63, a nontoxic mutant of heat-labile enterotoxin, as adjuvant rapidly induces protective immunity against lethal pneumococcal infections in neonatal mice. Infect. Immun. 70:1443-1452. (Pubitemid 34163422)
25. Jakobsen, H., et al. 2006. Early life T cell responses to pneumococcal conjugates increase with age and determine the polysaccharide-specific antibody response and protective efficacy. Eur. J. Immunol. 36:287-295. (Pubitemid 43257451)
26. Jeon, B. Y., et al. 2008. Mycobacterium bovis BCG immunization induces protective immunity against nine different Mycobacterium tuberculosis strains in mice. Infect. Immun. 76:5173-5180.
27. Jiao, X., et al. 2002. Dendritic cells are host cells for mycobacteria in vivo that trigger innate and acquired immunity. J. Immunol. 168:1294-1301. (Pubitemid 34094498)
28. Kaufmann, S. H., G. Hussey, and P. H. Lambert. 2010. New vaccines for tuberculosis. Lancet 375:2110-2119.
29. Knuf, M., et al. 2008. Neonatal vaccination with an acellular pertussis vaccine accelerates the acquisition of pertussis antibodies in infants. J. Pediatr. 152:655-660.
30. Kvalsvig, A. J., and D. J. Unsworth. 2003. The immunopathogenesis of meningococcal disease. J. Clin. Pathol. 56:417-422. (Pubitemid 36724207)
31. Lambert, P. H., M. Liu, and C. A. Siegrist. 2005. Can. successful vaccines teach us how to induce efficient protective immune responses? Nat. Med. 11:S54-S62. (Pubitemid 40562304)
32. Leach, A., et al. 1997. Induction of immunologic memory in Gambian children by vaccination in infancy with a group A plus group C meningococcal polysaccharide-protein conjugate vaccine. J. Infect. Dis. 175:200-204. (Pubitemid 27020849)
33. MacLennan, J., et al. 2001. Immunologic memory 5 years after meningococcal A/C conjugate vaccination in infancy. J. Infect. Dis. 183:97-104. (Pubitemid 32043046)
34. MacLennan, J., et al. 1999. Immune response to revaccination with meningococcal A and C polysaccharides in Gambian children following repeated immunisation during early childhood. Vaccine 17:3086-3093. (Pubitemid 29366989)
35. Marchant, A., et al. 1999. Newborns develop a Th1-type immune response to Mycobacterium bovis bacillus Calmette-Guerin vaccination. J. Immunol. 163:2249-2255. (Pubitemid 29382234)
36. Maslanka, S. E., et al. 1997. Standardization and a multilaboratory comparison of Neisseria meningitidis serogroup A and C serum bactericidal assays. The Multilaboratory Study Group. Clin. Diagn. Lab Immunol. 4:156-167. (Pubitemid 27130227)
37. 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.
38. Olafsdottir, T. A., K. Lingnau, E. Nagy, and I. Jonsdottir. 2009. IC31, a two-component novel adjuvant mixed with a conjugate vaccine enhances protective immunity against pneumococcal disease in neonatal mice. Scand. J. Immunol. 69:194-202.
39. Ota, M. O., et al. 2002. Influence of Mycobacterium bovis bacillus Calmette-Guerin on antibody and cytokine responses to human neonatal vaccination. J. Immunol. 168:919-925. (Pubitemid 34049596)
40. Pihlgren, M., et al. 2003. 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. 170:2824-2832. (Pubitemid 36302152)
41. Poland, G. A. 2010. Prevention of meningococcal disease: current use of polysaccharide and conjugate vaccines. Clin. Infect. Dis. 50(Suppl. 2):S45-S53.
42. Pollard, A. J. 2004. Global epidemiology of meningococcal disease and vaccine efficacy. Pediatr. Infect. Dis. J. 23:S274-S279. (Pubitemid 44544509)
43. Rahman, M. J., and C. Fernandez. 2009. Neonatal vaccination with Mycobacterium bovis BCG: potential effects as a priming agent shown in a heterologous prime-boost immunization protocol. Vaccine 27:4038-4046.
44. Rennels, M., J. King, Jr., R. Ryall, T. Papa, and J. Froeschle. 2004. Dosage escalation, safety and immunogenicity study of four dosages of a tetravalent meningococcal polysaccharide diphtheria toxoid conjugate vaccine in infants. Pediatr. Infect. Dis. J. 23:429-435. (Pubitemid 38621482)
45. Richmond, P., et al. 2001. Ability of 3 different meningococcal C conjugate vaccines to induce immunologic memory after a single dose in UK toddlers. J. Infect. Dis. 183:160-163. (Pubitemid 32043057)
46. Robbins, J. B., R. Schneerson, P. Anderson, and D. H. Smith. 1996. Prevention of systemic infections, especially meningitis, caused by Haemophilus influenzae type b. JAMA 276:1181-1185.
47. Roduit, C., et al. 2002. Immunogenicity and protective efficacy of neonatal vaccination against Bordetella pertussis in a murine model: evidence for early control of pertussis. Infect. Immun. 70:3521-3528. (Pubitemid 34665988)
48. Sabirov, A., and D. W. Metzger. 2008. Intranasal vaccination of infant mice induces protective immunity in the absence of nasal-associated lymphoid tissue. Vaccine 26:1566-1576.
49. Schmitt, N., et al. 2009. Human dendritic cells induce the differentiation of interleukin-21-producing T follicular helper-like cells through interleukin-12. Immunity 31:158-169.
50. Sharip, A., et al. 2006. Population-based analysis of meningococcal disease mortality in the United States: 1990-2002. Pediatr. Infect. Dis. J. 25:191-194. (Pubitemid 43379054)
51. Siegrist, C. A. 2001. Neonatal and early life vaccinology. Vaccine 19:3331-3346.
52. Snape, M. D., et al. 2008. Immunogenicity of a tetravalent meningococcal glycoconjugate vaccine in infants: a randomized controlled trial. JAMA 299:173-184.
53. Tan, L. K., G. M. Carlone, and R. Borrow. 2010. Advances in the development of vaccines against Neisseria meningitidis. N. Engl. J. Med. 362:1511-1520.
54. Taunay, A., P. A. Galvao, J. S. de Morais, E. C. Gotschlich, and R. A. Feldman. 1974. Disease prevention by meningococcal serogroup C polysaccharide vaccine in preschool children: results after eleven months in Sao Paulo, Brazil. Pediatr. Res. 8:429A.
55. Trotter, C. L., and M. E. Ramsay. 2007. Vaccination against meningococcal disease in Europe: review and recommendations for the use of conjugate vaccines. FEMS Microbiol. Rev. 31:101-107. (Pubitemid 46058826)
56. Tsuji, S., et al. 2000. Maturation of human dendritic cells by cell wall skeleton of Mycobacterium bovis bacillus Calmette-Guerin: involvement of Toll-like receptors. Infect. Immun. 68:6883-6890. (Pubitemid 32463398)
57. Uehori, J., et al. 2005. Dendritic cell maturation induced by muramyl dipeptide (MDP) derivatives: monoacylated MDP confers TLR2/TLR4 activation. J. Immunol. 174:7096-7103. (Pubitemid 40705675)
58. Unkeless, J. C., E. Scigliano, and V. H. Freedman. 1988. Structure and function of human and murine receptors for IgG. Annu. Rev. Immunol. 6:251-281. (Pubitemid 19141584)
59. van den Biggelaar, A. H., et al. 2009. Neonatal pneumococcal conjugate vaccine immunization primes T cells for preferential Th2 cytokine expression: a randomized controlled trial in Papua New Guinea. Vaccine 27:1340-1347.
60. Veenhoven, R. H., et al. 2004. Nasopharyngeal pneumococcal carriage after combined pneumococcal conjugate and polysaccharide vaccination in children with a history of recurrent acute otitis media. Clin. Infect. Dis. 39:911-919. (Pubitemid 39313443)
61. Vekemans, J., et al. 2001. Neonatal bacillus Calmette-Guerin vaccination induces adult-like IFN-gamma production by CD4+ T lymphocytes. Eur. J. Immunol. 31:1531-1535. (Pubitemid 32454701)
62. Vogelzang, A., et al. 2008. A fundamental role for interleukin-21 in the generation of T follicular helper cells. Immunity 29:127-137.
63. World Health Organization. 2001. Epidemics of meningococcal disease African meningitis belt. Wkly. Epidemiol. Rec. 76:281-288.
64. World Health Organization. 2010. Meningitis in Chad, Niger and Nigeria: 2009 epidemic season. Wkly. Epidemiol. Rec. 85:57-68.
65. Zandvoort, A., et al. 2001. CD27 expression in the human splenic marginal zone: the infant marginal zone is populated by naive B cells. Tissue Antigens 58:234-242. (Pubitemid 34015426)
66. Zollinger, W. D., and R. E. Mandrell. 1983. Importance of complement source in bactericidal activity of human antibody and murine monoclonal antibody to meningococcal group B polysaccharide. Infect. Immun. 40:257-264. (Pubitemid 13163064)