Protective cellular responses elicited by vaccination with influenza nucleoprotein delivered by a live recombinant attenuated Salmonella vaccine

Vaccine

Volumn 29, Issue 23, 2011, Pages 3990-4002

  Ashraf, Shamaila ^a   Kong, Wei ^a   Wang, Shifeng ^a   Yang, Jiseon ^a,b   Curtiss, Roy ^a,b  

^a ARIZONA STATE UNIVERSITY   (United States)

^b ARIZONA STATE UNIVERSITY   (United States)

Author keywords

Influenza; Nucleoprotein; RASV; Salmonella; SifA

Indexed keywords

ANTIGEN; GAMMA INTERFERON; LIVE VACCINE; NUCLEOPROTEIN; SALMONELLOSIS VACCINE;

ANIMAL EXPERIMENT; ARTICLE; BACTERIAL STRAIN; CD8+ T LYMPHOCYTE; CHROMOSOME DELETION; CONTROLLED STUDY; CYTOSOL; FEMALE; HOST CELL; IMMUNE RESPONSE; INFLUENZA; INFLUENZA VACCINATION; LD 50; LYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; T LYMPHOCYTE; TH1 CELL;

ANIMALS; CYTOSOL; FEMALE; HISTOCOMPATIBILITY ANTIGENS CLASS I; IMMUNIZATION, SECONDARY; INFLUENZA VACCINES; INTERFERON-GAMMA; MICE; MICE, INBRED BALB C; ORTHOMYXOVIRIDAE; ORTHOMYXOVIRIDAE INFECTIONS; RNA-BINDING PROTEINS; SALMONELLA TYPHIMURIUM; T-LYMPHOCYTES; VACCINATION; VACCINES, ATTENUATED; VACCINES, SYNTHETIC; VIRAL CORE PROTEINS;

EID: 79955671015     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2011.03.066     Document Type: Article

References (65)

1. Li Y.C., Norton E.C., Dow W.H. Influenza and pneumococcal vaccination demand responses to changes in infectious disease mortality. Health Serv Res 2004, 39(4 Pt 1):905-926.
2. Epstein S.L., Tumpey T.M., Misplon J.A., Lo C.Y., Cooper L.A., Subbarao K., et al. DNA vaccine expressing conserved influenza virus proteins protective against H5N1 challenge infection in mice. Emerg Infect Dis 2002, 8(8):796-801.
3. Bui H.H., Peters B., Assarsson E., Mbawuike I., Sette A. Antibody and T cell epitopes of influenza A virus, knowledge and opportunities. Proc Natl Acad Sci 2007, 104(1):246-251.
4. + T cells against influenza virus induced by vaccination with nucleoprotein DNA. J Virol 1998, 72(7):5648-5653.
5. Tite J.P.H.-J.C., Hughes-Jenkins C., O'Callaghan D., Dougan G., Russell S.M., Gao X.M., et al. Anti-viral immunity induced by recombinant nucleoprotein of influenza A virus. II. Protection from influenza infection and mechanism of protection. Immunology 1990, 71(2):202-207.
6. Wraith D.C., Vessey A.E., Askonas B.A. Purified influenza virus nucleoprotein protects mice from lethal infection. J Gen Virol 1987, 68(2):433-440.
7. Wesley R.D., Tang M., Lager K.M. Protection of weaned pigs by vaccination with human adenovirus 5 recombinant viruses expressing the hemagglutinin and the nucleoprotein of H3N2 swine influenza virus. Vaccine 2004, 22(25-26):3427-3434.
8. Altstein A.D., Gitelman A.K., Smirnov Y.A., Piskareva L.M., Zakharova L.G., Pashvykina G.V., et al. Immunization with influenza A NP-expressing vaccinia virus recombinant protects mice against experimental infection with human and avian influenza viruses. Arch Virol 2006, 151(5):921-931.
9. Ulmer J.B., Donnelly J.J., Parker S.E., Rhodes G.H., Felgner P.L., Dwarki V.J., et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science 1993, 259(5102):1745-1749.
10. Epstein S.L., Kong W.P., Misplon J.A., Lo C.Y., Tumpey T.M., Xu L., et al. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine 2005, 23(46-47):5404-5410.
11. + T cells can promote survival and recovery after challenge. Int Immunol 2000, 12(1):91-101.
12. Cardenas L., Clements J.D. Oral immunization using live attenuated Salmonella spp. as carriers of foreign antigens. Clin Microbiol Rev 1992, 5(3):328-342.
13. Galan J.E., Curtiss R. Cloning and molecular characterization of genes whose products allow Salmonella typhimurium to penetrate tissue culture cells. Proc Natl Acad Sci 1989, 86(16):6383-6387.
14. Bollen W.S., Gunn B.M., Mo H., Lay M.K., Curtiss R. Presence of wild-type and attenuated Salmonella enterica strains in brain tissues following inoculation of mice by different routes. Infect Immun 2008, 76(7):3268-3272.
15. Srivastava I.K., Liu M.A. Gene vaccines. Ann Intern Med 2003, 138(7):550-559.
16. Hess J., Schaible U., Raupach B., Kaufmann S.H.E. Exploiting the immune system: toward new vaccines against intracellular bacteria. Adv Immunol 2000, 75:1-88.
17. Sizemore D.R., Branstrom A.A., Sadoff J.C. Attenuated Shigella as a DNA delivery vehicle for DNA-mediated immunization. Science 1995, 270(5234):299-303.
18. Tite J.P., Gao X.M., Hughes-Jenkins C.M., Lipscombe M., O'Callaghan D., Dougan G., et al. Anti-viral immunity induced by recombinant nucleoprotein of influenza A virus. III. Delivery of recombinant nucleoprotein to the immune system using attenuated Salmonella typhimurium as a live carrier. Immunology 1990, 70(4):540-546.
19. McSorley S.J.A.S., Costalonga M., Reinhardt R.L., Jenkins M.K. Tracking Salmonella-specific CD4 T cells in vivo reveals a local mucosal response to a disseminated infection. Immunity 2002, 16(3):365-377.
20. Sadoff J.C., Ballou W.R., Baron L.S., Majarian W.R., Brey R.N., Hockmeyer W.T., et al. Oral Salmonella typhimurium vaccine expressing circumsporozoite protein protects against malaria. Science 1988, 240(4850):336-338.
21. + cytotoxic T cells. J Exp Med 1990, 172(4):1083-1090.
22. Hess J., Gentschevt I., Miko D., Welzel M., Ladel C., Goebel W., et al. Superior efficacy of secreted over somatic antigen display in recombinant Salmonella vaccine induced protection against listeriosis. Proc Natl Acad Sci 1996, 93:1458-1463.
23. Gentschev I., Dietricha G., Spreng S., Kolb-Mäurer A., Brinkmann V., Grode L., et al. Recombinant attenuated bacteria for the delivery of subunit vaccines. Vaccine 2001, 19:2621-2628.
24. Galán J.E., Collmer A. Type III secretion machines: bacterial devices for protein delivery into host cells. Science 1999, 284(5418):1322-1328.
25. Galán J.E. Salmonella interactions with host cells: type III secretion at work. Annu Rev Cell Dev Biol 2001, 17(1):53-86.
26. Konjufca V., Wanda S.Y., Jenkins M.C., Curtiss R. A recombinant attenuated Salmonella enterica serovar Typhimurium vaccine encoding Eimeria acervulina antigen offers protection against E. acervulina challenge. Infect Immun 2006, 74(12):6785-6796.
27. Rüssmann H.S.H., Poblete F., Fu Y., Galán J.E., Donis R.O. Delivery of epitopes by the Salmonella type III secretion system for vaccine development. Science 1998, 281(5376):565-568.
28. Evans D.T., Chen L.M., Gillis J., Lin K.C., Harty B., Mazzara G.P., et al. Mucosal priming of simian immunodeficiency virus-specific cytotoxic T-lymphocyte responses in rhesus macaques by the Salmonella type III secretion antigen delivery system. J Virol 2003, 77(4):2400-2409.
29. Chen L.M., Briones G., Donis R.O., Galan J.E. Optimization of the delivery of heterologous proteins by the Salmonella enterica serovar Typhimurium type III secretion system for vaccine development. Infect Immun 2006, 74(10):5826-5833.
30. Branger C.G., Torres-Escobar A., Sun W., Perry R., Fetherston J., Roland K.L., et al. Oral vaccination with LcrV from Yersinia pestis KIM delivered by live attenuated Salmonella enterica serovar Typhimurium elicits a protective immune response against challenge with Yersinia pseudotuberculosis and Yersinia enterocolitica. Vaccine 2009, 27(39):5363-5370.
31. Li Y., Wang S., Scarpellini G., Gunn B., Xin W., Wanda S.Y., et al. Evaluation of new generation Salmonella enterica serovar Typhimurium vaccines with regulated delayed attenuation to induce immune responses against PspA. Proc Natl Acad Sci 2009, 106(2):593-598.
32. Xin W., Li Y., Mo H., Roland K.L., Curtiss R. PspA family fusion proteins delivered by attenuated Salmonella enterica serovar Typhimurium extend and enhance protection against Streptococcus pneumoniae. Infect Immun 2009, 77(10):4518-4528.
33. Nakayama K., Kelly S.M., Curtiss R. Construction of an Asd+ expression-cloning vector: stable maintenance and high level expression of cloned genes in a Salmonella vaccine strain. Nat Biotechnol 1988, 6:693-697.
34. Kong W., Wanda S.Y., Zhang X., Bollen W., Tinge S.A., Roland K.L., et al. Regulated programmed lysis of recombinant Salmonella in host tissues to release protective antigens and confer biological containment. Proc Natl Acad Sci 2008, 105(27):9361-9366.
35. Brumell J.H., Tang P., Zaharik M.L., Finlay B.B. Disruption of the Salmonella-containing vacuole leads to increased replication of Salmonella enterica serovar Typhimurium in the cytosol of epithelial cells. Infect Immun 2002, 70(6):3264-3270.
36. Beuzón C.R., Méresse S., Unsworth K.E., Ruíz-Albert J., Garvis S., Waterman S.R., et al. Salmonella maintains the integrity of its intracellular vacuole through the action of SifA. EMBO J 2000, 19(13):3235-3249.
37. Karasova D., Sebkova A., Vrbas V., Havlickova H., Sisak F., Rychlik I. Comparative analysis of Salmonella enterica serovar Enteritidis mutants with a vaccine potential. Vaccine 2009, 27:5265-5270.
38. Micheal A., Stratford R., Khan S., Dalgleish A., Pandha H. Novel strains of Salmonella typhimurium as potential vectors for gene delivery. FEMS Mircrobiol Lett 2004, 238:345-351.
39. Curtiss R., Porter S.B., Munson M., Tinge S.A., Hassan J.O., Gentry-Weeks C., et al. Nonrecombinant and recombinant avirulent Salmonella live vaccines for poultry. Colonization control of human bacterial enteropathogens in poultry 1991, 169-198. Academic Press, New York, NY. L.C. Blanken-Ship, J.S. Bailey, N.A. Cox, N.J. Stern, R.J. Meinersmann (Eds.).
40. Kang H.Y., Dozois C.M., Tinge S.A., Lee T.H., Curtiss R. Transduction-mediated transfer of unmarked deletion and point mutations through use of counterselectable suicide vectors. J Bacteriol 2002, 184(1):307-312.
41. Bertani G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J Bacteriol 1951, 62(3):293-300.
42. Hitchcock P.J., Brown T.M. Morphological heterogeneity among Salmonella lipopolysaccharide chemotypes in silver-stained polyacrylamide gels. J Bacteriol 1983, 154(1):269-277.
43. Sambrook J., Fritsch E.F., Maniatis T. Molecular cloning: a laboratory manual 1989, Cold Spring Harbor Laboratory Press, New York. 2nd ed.
44. Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 1970, 227(5259):680-685.
45. McCown M.F., Pekosz A. The influenza A virus M2 cytoplasmic tail is required for infectious virus production and efficient genome packaging. J Virol 2005, 79(6):3595-3605.
46. McCown M.F., Pekosz A. Distinct domains of the influenza a virus M2 protein cytoplasmic tail mediate binding to the M1 protein and facilitate infectious virus production. J Virol 2006, 80(16):8178-8189.
47. Sedgwick J.D., Holt P.G. A solid-phase immunoenzymatic technique for the enumeration of specific antibody-secreting cells. J Immunol Methods 1983, 57(1-3):301-309.
48. Seder R.A., Hill A.V.S. Vaccines against intracellular infections requiring cellular immunity. Nature 2000, 406(6797):793-798.
49. Reed L.J, Muench H. A simple method for estimating fifty percent endpoints. Am J Hyg 1938, 27:493-496.
50. Harlow E., Lane D. Antibodies: a laboratory manual 1988, CSHL Press.
51. Sun K., Ye J., Perez D.R., Metzger D.W. Seasonal FluMist vaccination induces cross-reactive T cell immunity against H1N1 (2009) influenza and secondary bacterial infections. J Immunol 2011, 186(2):987-993.
52. Doherty P.C., Kelso A. Towards a broadly protective influenza vaccine. J Clin Invest 2008, 118(10):3273-3275.
53. Deliyannis G., Jackson D.C., Ede N.J., Zeng W., Hourdakis I., Sakabetis E., et al. Induction of long-term memory CD8+ T cells for recall of viral clearing responses against influenza virus. J Virol 2002, 76(9):4212-4221.
54. Petrovska L., Aspinall R.J., Barber L., Clare S., Simmons C.P., Stratford R., et al. Salmonella enterica serovar Typhimurium interaction with dendritic cells: impact of the sifA gene. Cell Microbiol 2004, 6(11):1071-1084.
55. Kaech S.M., Wherry E.J., Ahmed R. Effector and memory T-cell differentiation: implications for vaccine development. Nat Rev Immunol 2002, 2(4):251-262.
56. Markine-Goriaynoff D., van der Logt J., Truyens C., Nguyen T.D., Heessen F.W.A., Bigaignon G., et al. IFN-γ independent IgG2a production in mice infected with viruses and parasites. Int Immunol 2000, 12(2):223-230.
57. Spellberg B., Edwards J.E. Type 1/Type 2 immunity in infectious diseases. Clin Infect Dis 2001, 32:76-102.
58. Andrew M.E., Coupar B.E., Boyle D.B., Ada G.L. The roles of influenza virus haemagglutinin and nucleoprotein in protection: analysis using vaccinia virus recombinants. Scand J Immunol 1987, 25(1):21-28.
59. De Boer G.F., Back W., Osterhaus A. An ELISA for detection of antibodies against influenza A nucleoprotein in humans and various animal species. Arch Virol 1990, 115(1):47-61.
60. Carragher D.M., Kaminski D.A., Moquin A., Hartson L., Randall T.D. A novel role for non-neutralizing antibodies against nucleoprotein in facilitating resistance to influenza virus. J Immunol 2008, 181(6):4168-4176.
61. Graham M.B., Dalton D.K., Giltinan D., Braciale V.L., Stewart T.A., Braciale T.J. Response to influenza infection in mice with a targeted disruption in the interferon gamma gene. J Exp Med 1993, 178(5):1725-1732.
62. Nguyen H.H.V.F., Vu H.L., Novak M.J., McGhee J.R., Mestecky J. Gamma interferon is not required for mucosal cytotoxic T-lymphocyte responses or heterosubtypic immunity to influenza A virus infection in mice. J Virol 2000, 74(12):5595-5601.
63. Wherry E., Teichgräber V., Becker T.C., Masopust D., Kaech S.M., Antia R., et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat Immunol 2003, 4:225-234.
64. Ameiss K., Ashraf S., Kong W., Pekosz A., Wu W.H., Milich D., et al. Delivery of woodchuck hepatitis virus-like particle presented influenza M2e by recombinant attenuated Salmonella displaying a delayed lysis phenotype. Vaccine 2010, 28:6704-6713.
65. Roland K., Curtiss R., Sizemore D. Construction and evaluation of a delta cya delta crp Salmonella typhimurium strain expressing avian pathogenic Escherichia coli O78 LPS as a vaccine to prevent airsacculitis in chickens. Avian Dis 1999, 43(3):429-441.