Induction of CD8 T cell heterologous protection by a single dose of single-cycle infectious influenza virus

Journal of Virology

Volumn 88, Issue 20, 2014, Pages 12006-12016

  Guo, Hailong ^a   Baker, Steven F ^b   Martínez Sobrido, Luis ^b   Topham, David J ^b  

^a ROCHESTER GENERAL HOSPITAL   (United States)

^b UNIVERSITY OF ROCHESTER MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOKINE; HEMAGGLUTININ; INFLUENZA VACCINE; NP366 PEPTIDE; PA224 PEPTIDE; PEPTIDE; SINGLE CYCLE INFECTIOUS INFLUENZA VIRUS VACCINE; TETRAMER; UNCLASSIFIED DRUG; INFLUENZA VIRUS HEMAGGLUTININ;

ANIMAL EXPERIMENT; ANTIGEN SPECIFICITY; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; EFFECTOR CELL; FEMALE; IN VITRO STUDY; IN VIVO STUDY; INFLUENZA; INFLUENZA VIRUS; LUNG LAVAGE; MDCK CELL LINE; MEDIASTINUM LYMPH NODE; MOUSE; NONHUMAN; PATHOGENICITY; SINGLE DRUG DOSE; SPLEEN; VIRION; VIRUS REPLICATION; VIRUS STRAIN; ANIMAL; C57BL MOUSE; DOG; DOSE RESPONSE; ENZYME LINKED IMMUNOSORBENT ASSAY; FLOW CYTOMETRY; HEK293 CELL LINE; HUMAN; IMMUNOLOGY; INFLUENZA VIRUS A H1N1; INFLUENZA VIRUS A H3N2; LYMPHOCYTE DEPLETION;

ANIMALS; CD8-POSITIVE T-LYMPHOCYTES; DOGS; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; FLOW CYTOMETRY; HEK293 CELLS; HEMAGGLUTININ GLYCOPROTEINS, INFLUENZA VIRUS; HUMANS; INFLUENZA A VIRUS, H1N1 SUBTYPE; INFLUENZA A VIRUS, H3N2 SUBTYPE; LYMPHOCYTE DEPLETION; MICE; MICE, INBRED C57BL;

EID: 84907437846     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01847-14     Document Type: Article

References (50)

1. Osterholm MT, Kelley NS, Sommer A, Belongia EA. 2012. Efficacy and effectiveness of influenza vaccines: a systematic review and meta-analysis. Lancet Infect. Dis. 12:36-44. http://dx.doi.org/10.1016/S1473-3099(11) 70295-X.
2. Grohskopf LA, Shay DK, Shimabukuro TT, Sokolow LZ, Keitel WA, Bresee JS. 2013. Prevention and control of seasonal influenza with vaccines: recommendations of the Advisory Committee on Immunization Practices-United States, 2013-2014. MMWR Recomm. Rep. 62:1-43.
3. Molinari NA, Ortega-Sanchez IR, Messonnier ML, Thompson WW, Wortley PM, Weintraub E, Bridges CB. 2007. The annual impact of seasonal influenza in the US: measuring disease burden and costs. Vaccine 25:5086-5096.
4. + T cell effector mechanisms in resistance to infection. Annu. Rev. Immunol. 18:275-308. http: //dx.doi.org/10.1146/annurev.immunol.18.1.275.
5. + T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol. 159:5197-5200.
6. + T-cell memory in a model of localized transient infection. Immunol. Rev. 211:133-145. http://dx.doi.org/10.1111/j.0105-2896.2006.00386.x.
7. Guo H, Santiago F, Lambert K, Takimoto T, Topham DJ. 2011. T cell-mediated protection against lethal 2009 pandemic H1N1 influenza virus infection in a mouse model. J. Virol. 85:448-455. http://dx.doi.org /10.1128/JVI.01812-10.
8. O'Neill E, Krauss SL, Riberdy JMR, Webster G, Woodland DL. 2000. Heterologous protection against lethal A/HongKong/156/97 (H5N1) influenza virus infection in C57BL/6 mice. J. Gen. Virol. 81:2689-2696.
9. Kreijtz JH, de Mutsert G, van Baalen CA, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. 2008. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J. Virol. 82:5161-5166. http://dx.doi.org/10.1128/JVI.02694-07.
10. Dudek T, Knipe DM. 2006. Replication-defective viruses as vaccines and vaccine vectors. Virology 344:230-239. http://dx.doi.org/10.1016/j.virol.2005.09.020.
11. Franchini M, Abril C, Schwerdel C, Ruedl C, Ackermann M, Suter M. 2001. Protective T-cell-based immunity induced in neonatal mice by a single replicative cycle of herpes simplex virus. J. Virol. 75:83-89. http: //dx.doi.org/10.1128/JVI.75.1.83-89.2001.
12. Jia B, Ng SK, DeGottardi MQ, Piatak M, Yuste E, Carville A, Mansfield KG, Li W, Richardson BA, Lifson JD, Evans DT. 2009. Immunization with single-cycle SIV significantly reduces viral loads after an intravenous challenge with SIV(mac)239. PLoS Pathog. 5:e1000272. http://dx.doi.org /10.1371/journal.ppat.1000272.
13. Widman DG, Ishikawa T, Fayzulin R, Bourne N, Mason PW. 2008. Construction and characterization of a second-generation pseudoinfectious West Nile virus vaccine propagated using a new cultivation system. Vaccine 26:2762-2771. http://dx.doi.org/10.1016/j.vaccine.2008.03.009.
14. Gomme EA, Faul EJ, Flomenberg P, McGettigan JP, Schnell MJ. 2010. Characterization of a single-cycle rabies virus-based vaccine vector. J. Virol. 84:2820-2831. http://dx.doi.org/10.1128/JVI.01870-09.
15. Rodrigo WW, de la Torre JC, Martinez-Sobrido L. 2011. Use of singlecycle infectious lymphocytic choriomeningitis virus to study hemorrhagic fever arenaviruses. J. Virol. 85:1684-1695. http://dx.doi.org/10.1128/JVI.02229-10.
16. + T cell immunity. Nat. Med. 16:339-345. http://dx.doi.org /10.1038/nm.2104.
17. + T cell memory inflation after infection with a single-cycle cytomegalovirus. PLoS Pathog. 7:e1002295. http://dx.doi.org/10.1371/journal.ppat.1002295.
18. Martinez-Sobrido L, Cadagan R, Steel J, Basler CF, Palese P, Moran TM, Garcia-Sastre A. 2010. Hemagglutinin-pseudotyped green fluorescent protein-expressing influenza viruses for the detection of influenza virus neutralizing antibodies. J. Virol. 84:2157-2163. http://dx.doi.org/10.1128/JVI.01433-09.
19. Baker SF, Guo H, Albrecht RA, Garcia-Sastre A, Topham DJ, Martinez-Sobrido L. 2013. Protection against lethal influenza with a viral mimic. J. Virol. 87:8591-8605. http://dx.doi.org/10.1128/JVI.01081-13.
20. Schickli JH, Flandorfer A, Nakaya T, Martinez-Sobrido L, Garcia-Sastre A, Palese P. 2001. Plasmid-only rescue of influenza A virus vaccine candidates. Philos. Trans. R. Soc. Lond. B Biol. Sci. 356:1965-1973. http://dx.doi.org/10.1098/rstb.2001.0979.
21. Martinez-Sobrido L, Garcia-Sastre A. 2010. Generation of recombinant influenza virus from plasmid DNA. J. Vis. Exp. 3:2057. http://dx.doi.org /10.3791/2057.
22. Kilbourne ED. 1969. Future influenza vaccines and the use of genetic recombinants. Bull. World Health Organ. 41:643-645.
23. Marsh GA, Hatami R, Palese P. 2007. Specific residues of the influenza A virus hemagglutinin viral RNA are important for efficient packaging into budding virions. J. Virol. 81:9727-9736.
24. Richter M, Ray SJ, Chapman TJ, Austin SJ, Rebhahn J, Mosmann TR, Gardner H, Kotelianski V, deFougerolles AR, Topham DJ. 2007. Col-lagen distribution and expression of collagen-binding α1β1 (VLA-1) and α2β1 (VLA-2) integrins on CD4 and CD8 T cells during influenza infection. J. Immunol. 178:4506-4516. http://dx.doi.org/10.4049/jimmunol.178.7.4506.
25. + T cell crossreactivity and specificities revealed after 2009 H1N1 influenza A virus infection in mice. PLoS One 7:e46166. http://dx.doi.org/10.1371/journal.pone.0046166.
26. Bouvier NM, Lowen AC. 2010. Animal models for influenza virus pathogenesis and transmission. Viruses 2:1530-1563. http://dx.doi.org/10.3390 /v20801530.
27. Roberts AI, Brolin RE, Ebert EC. 1999. Integrin α1β1 (VLA-1) mediates adhesion of activated intraepithelial lymphocytes to collagen. Immunology 97:679-685. http://dx.doi.org/10.1046/j.1365-2567.1999.00812.x.
28. Ray SJ, Franki SN, Pierce RH, Dimitrova S, Koteliansky V, Sprague AG, Doherty PC, de Fougerolles AR, Topham DJ. 2004. The collagen binding α1β1 integrin VLA-1 regulates CD8 T cell-mediated immune protection against heterologous influenza infection. Immunity 20:167-179. http://dx.doi.org/10.1016/S1074-7613(04)00021-4.
29. Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. 1992. Evolution and ecology of influenza A viruses. Microbiol. Rev. 56:152-179.
30. Bouvier NM, Palese P. 2008. The biology of influenza viruses. Vaccine 26(Suppl 4):D49-D53.
31. Egorov A, Brandt S, Sereinig S, Romanova J, Ferko B, Katinger D, Grassauer A, Alexandrova G, Katinger H, Muster T. 1998. Transfectant influenza A viruses with long deletions in the NS1 protein grow efficiently in Vero cells. J. Virol. 72:6437-6441.
32. Garcia-Sastre A, Egorov A, Matassov D, Brandt S, Levy DE, Durbin JE, Palese P, Muster T. 1998. Influenza A virus lacking the NS1 gene replicates in interferon-deficient systems. Virology 252:324-330. http://dx.doi.org/10.1006/viro.1998.9508.
33. Ferko B, Stasakova J, Romanova J, Kittel C, Sereinig S, Katinger H, Egorov A. 2004. Immunogenicity and protection efficacy of replicationdeficient influenza A viruses with altered NS1 genes. J. Virol. 78:13037-13045. http://dx.doi.org/10.1128/JVI.78.23.13037-13045.2004.
34. Talon J, Salvatore M, O'Neill RE, Nakaya Y, Zheng H, Muster T, Garcia-Sastre A, Palese P. 2000. Influenza A and B viruses expressing altered NS1 proteins: a vaccine approach. Proc. Natl. Acad. Sci. U. S. A. 97:4309-4314. http://dx.doi.org/10.1073/pnas.070525997.
35. Anhlan D, Hrincius ER, Scholtissek C, Ludwig S. 2012. Introduction of silent mutations into the NP gene of influenza A viruses as a possible strategy for the creation of a live attenuated vaccine. Vaccine 30:4480-4489. http://dx.doi.org/10.1016/j.vaccine.2012.04.070.
36. Watanabe S, Watanabe T, Kawaoka Y. 2009. Influenza A virus lacking M2 protein as a live attenuated vaccine. J. Virol. 83:5947-5950. http://dx.doi.org/10.1128/JVI.00450-09.
37. Greenbaum JA, Kotturi MF, Kim Y, Oseroff C, Vaughan K, Salimi N, Vita R, Ponomarenko J, Scheuermann RH, Sette A, Peters B. 2009. Pre-existing immunity against swine-origin H1N1 influenza viruses in the general human population. Proc. Natl. Acad. Sci. U. S. A. 106:20365-20370. http://dx.doi.org/10.1073/pnas.0911580106.
38. Stambas J, Guillonneau C, Kedzierska K, Mintern JD, Doherty PC, La Gruta NL. 2008. Killer T cells in influenza. Pharmacol. Ther. 120:186-196. http://dx.doi.org/10.1016/j.pharmthera.2008.08.007.
39. Brown LE, Kelso A. 2009. Prospects for an influenza vaccine that induces cross-protective cytotoxic T lymphocytes. Immunol. Cell Biol. 87:300-308. http://dx.doi.org/10.1038/icb.2009.16.
40. Uchida T. 2011. Development of a cytotoxic T-lymphocyte-based, broadly protective influenza vaccine. Microbiol. Immunol. 55:19-27. http://dx.doi.org/10.1111/j.1348-0421.2010.00273.x.
41. Yap KL, Ada GL, McKenzie IF. 1978. Transfer of specific cytotoxic T lymphocytes protects mice inoculated with influenza virus. Nature 273: 238-239. http://dx.doi.org/10.1038/273238a0.
42. Zweerink HJ, Courtneidge SA, Skehel JJ, Crumpton MJ, BA Askonas. 1977. Cytotoxic T cells kill influenza virus infected cells but do not distinguish between serologically distinct type A viruses. Nature 267:354-356. http://dx.doi.org/10.1038/267354a0.
43. Liang S, Mozdzanowska K, Palladino G, Gerhard W. 1994. Heterosubtypic immunity to influenza typeAvirus in mice: effector mechanisms and their longevity. J. Immunol. 152:1653-1661.
44. + T cells expressing gamma interferon. J. Virol. 76:4886-4890. http://dx.doi.org/10.1128/JVI.76.10.4886-4890.2002.
45. Weinfurter JT, Brunner K, Capuano SV, III, Li C, Broman KW, Kawaoka Y, Friedrich TC. 2011. Cross-reactiveTcells are involved in rapid clearance of 2009 pandemic H1N1 influenza virus in nonhuman primates. PLoS Pathog. 7:e1002381. http://dx.doi.org/10.1371/journal.ppat.1002381.
46. + T-cell immunity to the H7N9 influenza A virus varies across ethnicities. Proc. Natl. Acad. Sci. U. S. A. 111:1049-1054. http://dx.doi.org/10.1073/pnas.1322229111.
47. Kees U, Krammer PH. 1984. Most influenza A virus-specific memory cytotoxic T lymphocytes react with antigenic epitopes associated with internal virus determinants. J. Exp. Med. 159:365-377. http://dx.doi.org/10.1084/jem.159.2.365.
48. Yewdell JW, Bennink JR, Smith GL, Moss B. 1985. Influenza A virus nucleoprotein is a major target antigen for cross-reactive anti-influenza A virus cytotoxic T lymphocytes. Proc. Natl. Acad. Sci. U. S. A. 82:1785-1789. http://dx.doi.org/10.1073/pnas.82.6.1785.
49. Townsend AR, Rothbard J, Gotch FM, Bahadur G, Wraith D, McMichael AJ. 1986. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell 44:959-968. http://dx.doi.org/10.1016/0092-8674(86)90019-X.
50. + T-cell response is much less apparent following secondary challenge. J. Virol. 74:3486-3493. http://dx.doi.org/10.1128/JVI.74.8.3486-3493.2000.