JE-ADVAX vaccine protection against Japanese encephalitis virus mediated by memory B cells in the absence of CD8+ T cells and pre-exposure neutralizing antibody

Journal of Virology

Volumn 87, Issue 8, 2013, Pages 4395-4402

  Larena, Maximilian ^a   Prow, Natalie A ^b   Hall, Roy A ^b   Petrovsky, Nikolai ^c,d   Lobigs, Mario ^a  

^a Biology and Environment   (Australia)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c VAXINE PTY LTD   (Australia)

^d FLINDERS UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

BIOLOGICAL PRODUCT; CHIMERIVAX JE; JAPANESE ENCEPHALITIS VACCINE; JE ADVAX; NEUTRALIZING ANTIBODY; UNCLASSIFIED DRUG; VIRUS VACCINE;

ADOPTIVE TRANSFER; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY BLOOD LEVEL; ANTIBODY PRODUCTION; ARTICLE; CD8+ T LYMPHOCYTE; CELL COMPARTMENTALIZATION; CELLULAR IMMUNITY; EFFECTOR CELL; FEMALE; HUMORAL IMMUNITY; IMMUNOCOMPETENT CELL; JAPANESE ENCEPHALITIS; JAPANESE ENCEPHALITIS VIRUS; LYMPHOCYTE SUBPOPULATION; MEMORY CELL; MOUSE; NONHUMAN; PRIORITY JOURNAL; SINGLE DRUG DOSE; SPLEEN CELL;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, VIRAL; B-LYMPHOCYTES; CD8-POSITIVE T-LYMPHOCYTES; DISEASE MODELS, ANIMAL; ENCEPHALITIS, JAPANESE; INULIN; JAPANESE ENCEPHALITIS VACCINES; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT;

FLAVIVIRUS; JAPANESE ENCEPHALITIS VIRUS; MUS; WEST NILE VIRUS;

EID: 84875765134     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.03144-12     Document Type: Article

References (47)

1. Gould EA, Solomon T. 2008. Pathogenic flaviviruses. Lancet 371:500-509.
2. Halstead SB, Jacobson J. 2003. Japanese encephalitis. Adv. Virus Res. 61:103-138.
3. Campbell GL, Hills SL, Fischer M, Jacobson JA, Hoke CH, Hombach JM, Marfin AA, Solomon T, Tsai TF, Tsu VD, Ginsburg AS. 2011. Estimated global incidence of Japanese encephalitis: a systematic review. Bull. World Health Organ. 89:766-774, 774A-774E.
4. Erlanger TE, Weiss S, Keiser J, Utzinger J, Wiedenmayer K. 2009. Past, present, and future of Japanese encephalitis. Emerg. Infect. Dis. 15:1-7.
5. Mackenzie JS, Gubler DJ, Petersen LR. 2004. Emerging flaviviruses: the spread and resurgence of Japanese encephalitis, West Nile and dengue viruses. Nat. Med. 10:S98 -S109.
6. Monath TP. 2002. Japanese encephalitis vaccines: current vaccines and future prospects. Curr. Top. Microbiol. Immunol. 267:105-138.
7. Halstead SB, Thomas SJ. 2011. New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev. Vaccines 10: 355-364.
8. Tauber E, Kollaritsch H, Korinek M, Rendi-Wagner P, Jilma B, Firbas C, Schranz S, Jong E, Klingler A, Dewasthaly S, Klade CS. 2007. Safety and immunogenicity of a Vero-cell-derived, inactivated Japanese encephalitis vaccine: a non-inferiority, phase III, randomised controlled trial. Lancet 370:1847-1853.
9. Toriniwa H, Komiya T. 2008. Long-term stability of Vero cell-derived inactivated Japanese encephalitis vaccine prepared using serum-free medium. Vaccine 26:3680-3689.
10. Cooper PD, Petrovsky N. 2011. Delta inulin: a novel, immunologically active, stable packing structure comprising beta-D-[2 1] poly(fructofuranosyl) alpha-D-glucose polymers. Glycobiology 21:595-606.
11. Lobigs M, Pavy M, Hall RA, Lobigs P, Cooper P, Komiya T, Toriniwa H, Petrovsky N. 2010. An inactivated Vero cell-grown Japanese encephalitis vaccine formulated with Advax, a novel inulin-based adjuvant, induces protective neutralizing antibody against homologous and heterologous flaviviruses. J. Gen. Virol. 91:1407-1417.
12. Lobigs M, Larena M, Alsharifi M, Lee E, Pavy M. 2009. Live chimeric and inactivated Japanese encephalitis virus vaccines differ in their crossprotective values against Murray Valley encephalitis virus. J. Virol. 83: 2436-2445.
13. Bosco-Lauth A, Mason G, Bowen R. 2011. Pathogenesis of Japaneseencephalitis virus infection in a golden hamster model and evaluation of flavivirus cross-protective immunity. Am. J. Trop. Med. Hyg. 84:727-732.
14. Lobigs M, Diamond MS. 2012. Feasibility of cross-protective vaccination against flaviviruses of the Japanese encephalitis serocomplex. Expert Rev. Vaccines 11:177-187.
15. Plotkin SA. 2010. Correlates of protection induced by vaccination. Clin. Vaccine Immunol. 17:1055-1065.
16. Licon Luna RM, Lee E, Müllbacher A, Blanden RV, Langman R, Lobigs M. 2002. Lack of both Fas ligand and perforin protects from flavivirusmediated encephalitis in mice. J. Virol. 76:3202-3211.
17. Kitamura D, Rajewsky K. 1992. Targeted disruption of mu chain membrane exon causes loss of heavy-chain allelic exclusion. Nature 356:154-156.
18. + T-cells. Science 248:1227-1230.
19. Monath TP, Guirakhoo F, Nichols R, Yoksan S, Schrader R, Murphy C, Blum P, Woodward S, McCarthy K, Mathis D, Johnson C, Bedford P. 2003. Chimeric live, attenuated vaccine against Japanese encephalitis (ChimeriVax-JE): phase 2 clinical trials for safety and immunogenicity, effect of vaccine dose and schedule, and memory response to challenge with inactivated Japanese encephalitis antigen. J. Infect. Dis. 188:1213-1230.
20. Lee E, Hall RA, Lobigs M. 2004. Common E protein determinants for attenuation of glycosaminoglycan-binding variants of Japanese encephalitis and West Nile viruses. J. Virol. 78:8271-8280.
21. + T cells to recovery from infection in a murine model of Japanese encephalitis. J. Virol. 85:5446-5455.
22. Colombage G, Hall R, Pavy M, Lobigs M. 1998. DNA-based and alphavirus- vectored immunisation with prM and E proteins elicits long-lived and protective immunity against the flavivirus, Murray Valley encephalitis virus. Virology 250:151-163.
23. Honda-Okubo Y, Saade F, Petrovsky N. 2012. Advax, a polysaccharide adjuvant derived from delta inulin, provides improved influenza vaccine protection through broad-based enhancement of adaptive immune responses. Vaccine 30:5373-5381.
24. Hombach J, Solomon T, Kurane I, Jacobson J, Wood D. 2005. Report on a WHO consultation on immunological endpoints for evaluation of new Japanese encephalitis vaccines, WHO, Geneva, 2-3 September, 2004. Vaccine 23:5205-5211.
25. Markoff L. 2000. Points to consider in the development of a surrogate for efficacy of novel Japanese encephalitis virus vaccines. Vaccine 18(Suppl. 2):26-32.
26. Van Gessel Y, Klade CS, Putnak R, Formica A, Krasaesub S, Spruth M, Cena B, Tungtaeng A, Gettayacamin M, Dewasthaly S. 2011. Correlation of protection against Japanese encephalitis virus and JE vaccine (IXIARO(R)) induced neutralizing antibody titers. Vaccine 29:5925-5931.
27. Junghans RP, Anderson CL. 1996. The protection receptor for IgG catabolism is the beta2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl. Acad. Sci. U. S. A. 93:5512-5516.
28. + T-cell-deficient mice survive inoculation with high doses of vaccinia virus and exhibit altered IgG responses. Proc. Natl. Acad. Sci. U. S. A. 89:6070-6074.
29. Suzuki T, Ishii-Watabe A, Tada M, Kobayashi T, Kanayasu-Toyoda T, Kawanishi T, Yamaguchi T. 2010. Importance of neonatal FcR in regulating the serum half-life of therapeutic proteins containing the Fc domain of human IgG1: a comparative study of the affinity of monoclonal antibodies and Fc-fusion proteins to human neonatal FcR. J. Immunol. 184: 1968-1976.
30. West AP, Jr, Bjorkman PJ. 2000. Crystal structure and immunoglobulin G binding properties of the human major histocompatibility complexrelated Fc receptor. Biochemistry 39:9698-9708.
31. Ghetie V, Ward ES. 2000. Multiple roles for the major histocompatibility complex class I-related receptor FcRn. Annu. Rev. Immunol. 18:739-766.
32. Junghans RP. 1997. Finally! The Brambell receptor (FcRB). Mediator of transmission of immunity and protection from catabolism for IgG. Immunol. Res. 16:29-57.
33. Kimura T, Sasaki M, Okumura M, Kim E, Sawa H. 2010. Flavivirus encephalitis: pathological aspects of mouse and other animal models. Vet. Pathol. 47:806-818.
34. Oya A. 1988. Japanese encephalitis vaccine. Acta Paediatr. Jpn. 30: 175-184.
35. Goncalvez AP, Chien CH, Tubthong K, Gorshkova I, Roll C, Donau O, Schuck P, Yoksan S, Wang SD, Purcell RH, Lai CJ. 2008. Humanized monoclonal antibodies derived from chimpanzee Fabs protect against Japanese encephalitis virus in vitro and in vivo. J. Virol. 82:7009-7021.
36. Kimura-Kuroda J, Yasui K. 1988. Protection of mice against Japanese encephalitis virus by passive administration of monoclonal antibodies. J. Immunol. 141:3606-3610.
37. Konishi E, Ajiro N, Nukuzuma C, Mason PW, Kurane I. 2003. Comparison of protective efficacies of plasmid DNAs encoding Japanese encephalitis virus proteins that induce neutralizing antibody or cytotoxic T lymphocytes in mice. Vaccine 21:3675-3683.
38. + cytotoxic T-cell responses. J. Virol. 75:11457-11463.
39. Konishi E, Suzuki T. 2002. Ratios of subclinical to clinical Japanese encephalitis (JE) virus infections in vaccinated populations: evaluation of an inactivated JE vaccine by comparing the ratios with those in unvaccinated populations. Vaccine 21:98-107.
40. Konishi E, Yamaoka M, Khin Sane W, Kurane I, Takada K, Mason PW. 1999. The anamnestic neutralizing antibody response is critical for protection of mice from challenge following vaccination with a plasmid encoding the Japanese encephalitis virus premembrane and envelope genes. J. Virol. 73:5527-5534.
41. Swain SL, McKinstry KK, Strutt TM. 2012. Expanding roles for CD4(+) T cells in immunity to viruses. Nat. Rev. Immunol. 12:136-148.
42. Kasturi SP, Skountzou I, Albrecht RA, Koutsonanos D, Hua T, Nakaya HI, Ravindran R, Stewart S, Alam M, Kwissa M, Villinger F, Murthy N, Steel J, Jacob J, Hogan RJ, Garcia-Sastre A, Compans R, Pulendran B. 2011. Programming the magnitude and persistence of antibody responses with innate immunity. Nature 470:543-547.
43. McHeyzer-Williams M, Okitsu S, Wang N, McHeyzer-Williams L. 2012. Molecular programming of B cell memory. Nat. Rev. Immunol. 12:24-34.
44. Zinkernagel RM, Hengartner H. 2006. Protective 'immunity' by preexistent neutralizing antibody titers and preactivated T cells but not by so-called 'immunological memory'. Immunol. Rev. 211:310-319.
45. Diamond MS, Sitati EM, Friend LD, Higgs S, Shrestha B, Engle M. 2003. A critical role for induced IgM in the protection against West Nile virus infection. J. Exp. Med. 198:1853-1862.
46. Liang JJ, Liao CL, Liao JT, Lee YL, Lin YL. 2009. A Japanese encephalitis virus vaccine candidate strain is attenuated by decreasing its interferon antagonistic ability. Vaccine 27:2746-2754.
47. Klingel K, Schnorr JJ, Sauter M, Szalay G, Kandolf R. 2003. beta2- microglobulin-associated regulation of interferon-gamma and virusspecific immunoglobulin G confer resistance against the development of chronic coxsackievirus myocarditis. Am. J. Pathol. 162:1709-1720.