A recombinant adenovirus prime-virus-like particle boost regimen elicits effective and specific immunities against norovirus in mice

Vaccine

Volumn 27, Issue 38, 2009, Pages 5233-5238

  Guo, Li ^a,b   Zhou, Hongli ^b   Wang, Min ^a   Song, Jingdong ^a   Han, Bingjuan ^a   Shu, Yi ^a   Ren, Lili ^b   Si, Hongli ^a   Qu, Jianguo ^a   Zhao, Zhendong ^b   Wang, Jianwei ^a,b   Hung, Tao ^a  

^a CHINESE CENTER FOR DISEASE CONTROL AND PREVENTION   (China)

^b INSTITUTE OF PATHOGEN BIOLOGY   (China)

Author keywords

Immune response; Norovirus; rAd prime VLP boost

Indexed keywords

ADENOVIRUS VECTOR; CAPSID PROTEIN; CPG OLIGODEOXYNUCLEOTIDE; GAMMA INTERFERON; IMMUNOGLOBULIN A ANTIBODY; IMMUNOGLOBULIN G ANTIBODY; INTERLEUKIN 2; INTERLEUKIN 4; INTERLEUKIN 5; POLYINOSINIC POLYCYTIDYLIC ACID; TUMOR NECROSIS FACTOR ALPHA; VIRUS VACCINE;

ADJUVANT THERAPY; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIBODY TITER; ARTICLE; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE RELEASE; DRUG EFFICACY; EMBRYO; FEMALE; HUMAN; HUMAN CELL; HUMORAL IMMUNITY; IMMUNIZATION; MOUSE; MUCOSAL IMMUNITY; NONHUMAN; NOROVIRUS; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; VACCINATION; VIRUS INFECTION; VIRUS LIKE AGENT;

ADENOVIRIDAE; ANIMALS; ANTIBODIES, VIRAL; CALICIVIRIDAE INFECTIONS; CAPSID PROTEINS; FEMALE; IMMUNITY, CELLULAR; IMMUNITY, MUCOSAL; IMMUNIZATION, SECONDARY; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; NOROVIRUS; VIRAL VACCINES;

EID: 67651100868     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2009.06.065     Document Type: Article

References (49)

1. Green K.Y. Caliciviridae: the noroviruses. In: Knipe D.M., Howley P.M., Griffin D.E., Lamb R.A., Martin M.A., Roizman B., and Strauset S.E. (Eds). Fields virology. 5th ed. (2007), Lippincott Williams & Wilkins, Philadelphia 949-979
2. Arness M.K., Feighner B.H., Canham M.L., Taylor D.N., Monroe S.S., Cieslak T.J., et al. Norwalk-like viral gastroenteritis outbreak in U.S. Army trainees. Emerg Infect Dis 6 2 (2000) 204-207
3. Zheng D.P., Ando T., Fankhauser R.L., Beard R.S., Glass R.I., and Monroe S.S. Norovirus classification and proposed strain nomenclature. Virology 346 2 (2006) 312-323
4. Siebenga J.J., Vennema H., Duizer E., and Koopmans M.P. Gastroenteritis caused by norovirus GGII.4, The Netherlands, 1994-2005. Emerg Infect Dis 13 1 (2007) 144-146
5. Papaventsis D.C., Dove W., Cunliffe N.A., Nakagomi O., Combe P., Grosjean P., et al. Norovirus infection in children with acute gastroenteritis, Madagascar, 2004-2005. Emerg Infect Dis 13 6 (2007) 908-911
6. Chen S.Y., Tsai C.N., Lai M.W., Chen C.Y., Lin K.L., Lin T.Y., et al. Norovirus infection as a cause of diarrhea-associated benign infantile seizures. Clin Infect Dis 48 7 (2009) 849-855
7. Guo L., Song J., Xu X., Ren L., Li J., Zhou H., et al. Genetic analysis of norovirus in children affected with acute gastroenteritis in Beijing, 2004-2007. J Clin Virol 44 1 (2009) 94-98
8. Sdiri-Loulizi K., Ambert-Balay K., Gharbi-Khelifi H., Sakly N., Hassine M., Chouchane S., et al. Molecular epidemiology of norovirus gastroenteritis investigated using samples collected from children in Tunisia during a four-year period: detection of the norovirus variant GGII.4 Hunter as early as January 2003. J Clin Microbiol 47 2 (2009) 421-429
9. Buesa J., Montava R., Abu-Mallouh R., Fos M., Ribes J.M., Bartolomé R., et al. Sequential evolution of genotype GII.4 norovirus variants causing gastroenteritis outbreaks from 2001 to 2006 in Eastern Spain. J Med Virol 80 7 (2008) 1288-1295
10. Siebenga J.J., Vennema H., Renckens B., de Bruin E., van der Veer B., Siezen R.J., et al. Epochal evolution of GGII.4 norovirus capsid proteins from 1995 to 2006. J Virol 81 18 (2007) 9932-9941
11. Xi J.N., Graham D.Y., Wang K.N., and Estes M.K. Norwalk virus genome cloning and characterization. Science 250 4987 (1990) 1580-1583
12. Jiang X., Wang M., Wang K., and Estes M.K. Sequence and genomic organization of Norwalk virus. Virology 95 1 (1993) 51-61
13. Zintz C., Bok K., Parada E., Barnes-Eley M., Berke T., Staat M.A., et al. Prevalence and genetic characterization of caliciviruses among children hospitalized for acute gastroenteritis in the United States. Infect Genet Evol 5 3 (2005) 281-290
14. Jiang X., Wang M., Graham D.Y., and Estes M.K. Expression, self-assembly, and antigenicity of the Norwalk virus capsid protein. J Virol 66 11 (1992) 6527-6532
15. Baric R.S., Yount B., Lindesmith L., Harrington P.R., Greene S.R., Tseng F.C., et al. Expression and self-assembly of norwalk virus capsid protein from Venezuelan equine encephalitis virus replicons. J Virol 76 6 (2002) 3023-3030
16. Harrington P.R., Yount B., Johnston R.E., Davis N., Moe C., and Baric R.S. Systemic, mucosal, and heterotypic immune induction in mice inoculated with Venezuelan equine encephalitis replicons expressing Norwalk virus-like particles. J Virol 76 2 (2002) 730-742
17. Xia M., Farkas T., and Jiang X. Norovirus capsid protein expressed in yeast forms virus-like particles and stimulates systemic and mucosal immunity in mice following an oral administration of raw yeast extracts. J Med Virol 79 1 (2007) 74-83
18. Nicollier-Jamot B., Ogier A., Piroth L., Pothier P., and Kohli E. Recombinant virus-like particles of a norovirus (genogroup II strain) administered intranasally and orally with mucosal adjuvants LT and LT(R192G) in BALB/c mice induce specific humoral and cellular Th1/Th2-like immune responses. Vaccine 22 9-10 (2004) 1079-1086
19. Lindesmith L., Moe C., Lependu J., Frelinger J.A., Treanor J., and Baric R.S. Cellular and humoral immunity following Snow Mountain virus challenge. J Virol 79 5 (2005) 2900-2909
20. Guo L., Wang J.W., Zhou H.L., Si H.L., Wang M., Song J.D., et al. Intranasal administration of a recombinant adenovirus expressing the norovirus capsid protein stimulates specific humoral, mucosal, and cellular immune responses in mice. Vaccine 26 4 (2008) 460-468
21. Lemckert A.A., Sumida S.M., Holterman L., Vogels R., Truitt D.M., Lynch D.M., et al. Immunogenicity of heterologous prime-boost regimens involving recombinant adenovirus serotype 11 (Ad11) and Ad35 vaccine vectors in the presence of anti-ad5 immunity. J Virol 79 5 (2005) 9694-9701
22. Sumida S.M., Truitt D.M., Lemckert A.A., Vogels R., Custers J.H., Addo M.M., et al. Neutralizing antibodies to adenovirus serotype 5 vaccine vectors are directed primarily against the adenovirus hexon protein. J Immunol 174 11 (2005) 7179-7185
23. Thorner A.R., Vogels R., Kaspers J., Weverling G.J., Holterman L., Lemckert A.A., et al. Age dependence of adenovirus-specific neutralizing antibody titers in individuals from sub-Saharan Africa. J Clin Microbiol 44 10 (2006) 3781-3783
24. Mascola J.R., Sambor A., Beaudry K., Santra S., Welcher B., Louder M.K., et al. Neutralizing antibodies elicited by immunization of monkeys with DNA plasmids and recombinant adenoviral vectors expressing human immunodeficiency virus type 1 proteins. J Virol 79 2 (2005) 771-779
25. Li Z., Zhang M., Zhou C., Zhao X., Iijima N., and Frankel F.R. Novel vaccination protocol with two live mucosal vectors elicits strong cell-mediated immunity in the vagina and protects against vaginal virus challenge. J Immunol 180 4 (2008) 2504-2513
26. Lo C.Y., Wu Z., Misplon J.A., Price G.E., Pappas C., Kong W.P., et al. Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine 26 17 (2008) 2062-2072
27. Guo L., Zhou H.L., Qu J.G., Wang J.W., Xu X.W., and Hung T. Codon optimization and expression of norovirus capsid proteins in insect cells. Virolog Sin 21 2 (2006) 121-125
28. Kanegae Y., Makimura M., and Saito I. A simple and efficient method for purification of infectious recombinant adenovirus. Jpn J Med Sci Biol 47 3 (1994) 157-166
29. Sambrook J., Fritsch E.F., and Maniatis T. Molecular cloning. 2nd ed. vol. 3 (1989), Cold Spring Harbor Laboratory Press, Plainview, NY 1847-1875
30. Gao W., Soloff A.C., Lu X., Montecalvo A., Nguyen D.C., Matsuoka Y., et al. Protection of mice and poultry from lethal H5N1 avian influenza virus through adenovirus-based immunization. J Virol 80 4 (2006) 1959-1964
31. Estes M.K., Ball J.M., Guerrero R.A., Opekun A.R., Gilger M.A., Pacheco S.S., et al. Norwalk virus vaccines: challenges and progress. J Infect Dis 181 Suppl. 2 (2000) S367-S373
32. Wu L., Kong W.P., and Nabel G.J. Enhanced breadth of CD4 T-cell immunity by DNA prime and adenovirus boost immunization to human immunodeficiency virus Env and Gag immunogens. J Virol 79 13 (2005) 8024-8031
33. Nociari M., Ocheretina O., Murphy M., and Falck-Pedersen E. Adenovirus induction of IRF3 occurs through a binary trigger targeting JNK and TBK-1 kinase cascades and type I IFN autocrine signaling. J Virol 83 9 (2009) 4081-4091
34. Nociari M., Ocheretina O., Schoggins J.W., and Falck-Pedersen E. Sensing infection by adenovirus: toll-like receptor-independent viral DNA recognition signals activation of the interferon regulatory factor 3 master regulator. J Virol 81 8 (2007) 4145-4157
35. Hu X., Herrero C., Li W.P., Antoniv T.T., Falck-Pedersen E., Koch A.E., et al. Sensitization of IFN-gamma Jak-STAT signaling during macrophage activation. Nat Immunol 3 9 (2002) 859-866
36. Wick W.D., Gilbert P.B., and Yang O.O. Predicting the impact of blocking human immunodeficiency virus type 1 Nef in vivo. J Virol 83 5 (2009) 2349-2356
37. Ramduth D., Day C.L., Thobakgale C.F., Mkhwanazi N.P., de Pierres C., Reddy S., et al. Immunodominant HIV-1 Cd4+ T cell epitopes in chronic untreated clade C HIV-1 infection. PLoS One 4 4 (2009) e5013
38. Palmowski M.J., Parker M., Choudhuri K., Chiu C., Callan M.F., van der Merwe P.A., et al. A single-chain H-2Db molecule presenting an influenza virus nucleoprotein epitope shows enhanced ability at stimulating CD8+ T cell responses in vivo. J Immunol 182 8 (2009) 4565-4571
39. Larke N., Murphy A., Wirblich C., Teoh D., Estcourt M.J., McMichael A.J., et al. Induction of human immunodeficiency virus type 1-specific T cells by a bluetongue virus tubule-vectored vaccine prime-recombinant modified virus Ankara boost regimen. J Virol 79 23 (2005) 14822-14833
40. Kang S.M., Guo L., Yao Q., Skountzou I., and Compans R.W. Intranasal immunization with inactivated influenza virus enhances immune responses to coadministered simian-human immunodeficiency virus-like particle antigens. J Virol 78 18 (2004) 9624-9632
41. Arrode G., Hegde R., Mani A., Jin Y., Chebloune Y., and Narayan O. Phenotypic and functional analysis of immune CD8+ T cell responses induced by a single injection of a HIV DNA vaccine in mice. J Immunol 178 4 (2007) 2318-2327
42. Da Silva D.M., Fausch S.C., Verbeek J.S., and Kast W.M. Uptake of human papillomavirus virus-like particles by dendritic cells is mediated by Fcgamma receptors and contributes to acquisition of T cell immunity. J Immunol 178 12 (2007) 7587-7597
43. Murata K., Lechmann M., Qiao M., Gunji T., Alter H.J., and Liang T.J. Immunization with hepatitis C virus-like particles protects mice from recombinant hepatitis C virus-vaccinia infection. Proc Natl Acad Sci USA 100 11 (2003) 6753-6758
44. Woo G.J., Chun E.Y., Kim K.H., and Kim W. Analysis of immune responses against nucleocapsid protein of the Hantaan virus elicited by virus infection or DNA vaccination. J Microbiol 43 6 (2005) 537-545
45. Souza M., Costantini V., Azevedo M.S., and Saif L.J. A human norovirus-like particle vaccine adjuvanted with ISCOM or mLT induces cytokine and antibody responses and protection to the homologous GII.4 human norovirus in a gnotobiotic pig disease model. Vaccine 25 50 (2007) 8448-8459
46. Souza M., Azevedo M.S., Jung K., Cheetham S., and Saif L.J. Pathogenesis and immune responses in gnotobiotic calves after infection with the genogroup II. 4-HS66 strain of human norovirus. J Virol 82 4 (2008) 1777-1786
47. Santosuosso M., Zhang X., McCormick S., Wang J., Hitt M., and Xing Z. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization referentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J Immunol 174 12 (2005) 7986-7994
48. Yu J.R., Kim S., Lee J.B., and Chang J. Single intranasal immunization with recombinant adenovirus-based vaccine induces protective immunity against respiratory syncytial virus infection. J Virol 82 5 (2008) 2350-2357
49. Lemiale F., Kong W.P., Akyürek L.M., Ling X., Huang Y., Chakrabarti B.K., et al. Enhanced mucosal immunoglobulin A response of intranasal adenoviral vector human immunodeficiency virus vaccine and localization in the central nervous system. J Virol 77 18 (2003) 10078-10087