Role of CD8⁺ T-cell immunity in influenza infection: potential use in future vaccine development

References

• Nichol KL, Treanor JJ. Vaccines for seasonal and pandemic influenza. J. Infect. Dis.194(Suppl. 2), S111–S118 (2006).
   PubMed Web of Science ®Google Scholar
• Meltzer MI, Cox NJ, Fukuda K. The economic impact of pandemic influenza in the United States: priorities for intervention. Emerg. Infect. Dis.5(5), 659–671 (1999).
   PubMed Web of Science ®Google Scholar
• Webby RJ, Webster RG, Richt JA. Influenza viruses in animal wildlife populations. Curr. Top. Microbiol. Immunol.315, 67–83 (2007).
   PubMed Web of Science ®Google Scholar
• Schild GC, Newman RW, Webster RG, Major D, Hinshaw VS. Antigenic analysis of influenza A virus surface antigens: considerations for the nomenclature of influenza virus. Brief review. Arch. Virol.63(3–4), 171–184 (1980).
   PubMed Web of Science ®Google Scholar
• Ito T, Kawaoka Y. Avian influenza. In: Textbook of Influenza. Nicholson KG, Webster RG, Hay AJ (Eds.). Blackwell Science, Oxford, UK, 126–136 (1998).
   Google Scholar
• Smith DJ, Lapedes AS, de Jong JC et al. Mapping the antigenic and genetic evolution of influenza virus. Science305(5682), 371–376 (2004).
   PubMed Web of Science ®Google Scholar
• Rott R, Klenk HD, Nagai Y, Tashiro M. Influenza viruses, cell enzymes, and pathogenicity. Am. J. Respir. Crit. Care Med.152(4 Pt 2), S16–S19 (1995).
   PubMed Web of Science ®Google Scholar
• Lamb RA, Krug RM. Orthomyxoviradae: influenza viruses. In: Fields Virology. Fields BN, Knipe DM, Howley PM (Eds). Lippincott-Raven, PA, USA, 1359–1362 (1996).
   Google Scholar
• Rogers GN, Paulson JC. Receptor determinants of human and animal influenza virus isolates: differences in receptor specificity of the H3 hemagglutinin based on species of origin. Virology127(2), 361–373 (1983).
   PubMed Web of Science ®Google Scholar
• Connor RJ, Kawaoka Y, Webster RG, Paulson JC. Receptor specificity in human, avian, and equine H2 and H3 influenza virus isolates. Virology205(1), 17–23 (1994).
   PubMed Web of Science ®Google Scholar
• Rogers GN, D’Souza BL. Receptor binding properties of human and animal H1 influenza virus isolates. Virology173(1), 317–322 (1989).
   PubMed Web of Science ®Google Scholar
• Palese P, Tobita K, Ueda M, Compans RW. Characterization of temperature sensitive influenza virus mutants defective in neuraminidase. Virology61(2), 397–410 (1974).
   PubMed Web of Science ®Google Scholar
• Taubenberger JK, Reid AH, Janczewski TA, Fanning TG. Integrating historical, clinical and molecular genetic data in order to explain the origin and virulence of the 1918 Spanish influenza virus. Philos. Trans. R Soc. Lond. B Biol. Sci.356(1416), 1829–1839 (2001).
   PubMed Web of Science ®Google Scholar
• Webster RG, Bean WJ, Gorman OT, Chambers TM, Kawaoka Y. Evolution and ecology of influenza A viruses. Microbiol. Rev.56(1), 152–179 (1992).
   PubMedGoogle Scholar
• Kawaoka Y, Krauss S, Webster RG. Avian-to-human transmission of the PB1 gene of influenza A viruses in the 1957 and 1968 pandemics. J. Virol.63(11), 4603–4608 (1989).
   PubMed Web of Science ®Google Scholar
• Itoh Y, Shinya K, Kiso Met al.In vitro and in vivo characterization of new swine-origin H1N1 influenza viruses. Nature460(7258), 1021–1025 (2009).
   PubMed Web of Science ®Google Scholar
• Maines TR, Jayaraman A, Belser JA et al. Transmission and pathogenesis of swine-origin 2009 A(H1N1) influenza viruses in ferrets and mice. Science325(5939), 484–487 (2009).
   PubMed Web of Science ®Google Scholar
• Peiris JS, Poon LL, Guan Y. Emergence of a novel swine-origin influenza A virus (S-OIV) H1N1 virus in humans. J. Clin. Virol.45(3), 169–173 (2009).
   PubMed Web of Science ®Google Scholar
• Hatta M, Kawaoka Y. The continued pandemic threat posed by avian influenza viruses in Hong Kong. Trends Microbiol.10(7), 340–344 (2002).
   PubMed Web of Science ®Google Scholar
• Webby RJ, Webster RG. Are we ready for pandemic influenza? Science302(5650), 1519–1522 (2003).
   PubMed Web of Science ®Google Scholar
• Shinya K, Ebina M, Yamada S, Ono M, Kasai N, Kawaoka Y. Avian flu: influenza virus receptors in the human airway. Nature440(7083), 435–436 (2006).
   PubMed Web of Science ®Google Scholar
• Yamada S, Suzuki Y, Suzuki T et al. Haemagglutinin mutations responsible for the binding of H5N1 influenza A viruses to human-type receptors. Nature444(7117), 378–382 (2006).
   PubMed Web of Science ®Google Scholar
• Tumpey TM, Basler CF, Aguilar PV et al. Characterization of the reconstructed 1918 Spanish influenza pandemic virus. Science310(5745), 77–80 (2005).
   PubMed Web of Science ®Google Scholar
• Chen H, Deng G, Li Z et al. The evolution of H5N1 influenza viruses in ducks in southern China. Proc. Natl Acad. Sci. USA101(28), 10452–10457 (2004).
   PubMed Web of Science ®Google Scholar
• Taubenberger JK, Reid AH, Lourens RM, Wang R, Jin G, Fanning TG. Characterization of the 1918 influenza virus polymerase genes. Nature437(7060), 889–893 (2005).
   PubMed Web of Science ®Google Scholar
• Olsen B, Munster VJ, Wallensten A, Waldenstrom J, Osterhaus AD, Fouchier RA. Global patterns of influenza a virus in wild birds. Science312(5772), 384–388 (2006).
   PubMed Web of Science ®Google Scholar
• El Sahly HM, Keitel WA. Pandemic H5N1 influenza vaccine development: an update. Expert Rev. Vaccines7(2), 241–247 (2008).
   PubMed Web of Science ®Google Scholar
• Leroux-Roels I, Borkowski A, Vanwolleghem T et al. Antigen sparing and cross-reactive immunity with an adjuvanted rH5N1 prototype pandemic influenza vaccine: a randomised controlled trial. Lancet370(9587), 580–589 (2007).
   PubMed Web of Science ®Google Scholar
• Nolan TM, Richmond PC, Skeljo MV et al. Phase I and II randomised trials of the safety and immunogenicity of a prototype adjuvanted inactivated split-virus influenza A (H5N1) vaccine in healthy adults. Vaccine26(33), 4160–4167 (2008).
   PubMed Web of Science ®Google Scholar
• Wu J, Fang HH, Chen JT et al. Immunogenicity, safety, and cross-reactivity of an inactivated, adjuvanted, prototype pandemic influenza (H5N1) vaccine: a Phase II, double-blind, randomized trial. Clin. Infect. Dis.48(8), 1087–1095 (2009).
   PubMed Web of Science ®Google Scholar
• Network WHOGIPS. Evolution of H5N1 avian influenza viruses in Asia. Emerg. Infect. Dis.11(10), 1515–1521 (2005).
   PubMed Web of Science ®Google Scholar
• Yu X, Tsibane T, McGraw PA et al. Neutralizing antibodies derived from the B cells of 1918 influenza pandemic survivors. Nature455(7212), 532–536 (2008).
   PubMed Web of Science ®Google Scholar
• Gerhard W. The role of the antibody response in influenza virus infection. Curr. Top. Microbiol. Immunol.260, 171–190 (2001).
   PubMed Web of Science ®Google Scholar
• Wiley DC, Wilson IA, Skehel JJ. Structural identification of the antibody-binding sites of Hong Kong influenza haemagglutinin and their involvement in antigenic variation. Nature289(5796), 373–378 (1981).
   PubMed Web of Science ®Google Scholar
• Palese P. Making better influenza virus vaccines? Emerg. Infect. Dis.12(1), 61–65 (2006).
   PubMed Web of Science ®Google Scholar
• Carrat F, Flahault A. Influenza vaccine: the challenge of antigenic drift. Vaccine25(39–40), 6852–6862 (2007).
   PubMed Web of Science ®Google Scholar
• Skowronski DM, Masaro C, Kwindt TL et al. Estimating vaccine effectiveness against laboratory-confirmed influenza using a sentinel physician network: results from the 2005–2006 season of dual A and B vaccine mismatch in Canada. Vaccine25(15), 2842–2851 (2007).
   PubMed Web of Science ®Google Scholar
• Webster RG. Immunity to influenza in the elderly. Vaccine18(16), 1686–1689 (2000).
   PubMed Web of Science ®Google Scholar
• CDC. Assessment of the effectiveness of the 2003–04 influenza vaccine among children and adults-Colorado, 2003. Morb. Mortal. Wkly Rep.53, 707–710 (2004).
   PubMedGoogle Scholar
• Jin H, Zhou H, Liu H et al. Two residues in the hemagglutinin of A/Fujian/411/02-like influenza viruses are responsible for antigenic drift from A/Panama/2007/99. Virology336(1), 113–119 (2005).
   PubMed Web of Science ®Google Scholar
• Christensen JP, Doherty PC, Branum KC, Riberdy JM. Profound protection against respiratory challenge with a lethal H7N7 influenza A virus by increasing the magnitude of CD8+ T-cell memory. J. Virol.74(24), 11690–11696 (2000).
   PubMed Web of Science ®Google Scholar
• Furuse Y, Suzuki A, Kamigaki T, Oshitani H. Evolution of the M gene of the influenza A virus in different host species: large-scale sequence analysis. Virol. J.6, 67 (2009).
   PubMed Web of Science ®Google Scholar
• Doherty PC, Kelso A. Toward a broadly protective influenza vaccine. J. Clin. Invest.118(10), 3273–3275 (2008).
   PubMed Web of Science ®Google Scholar
• Thomas PG, Keating R, Hulse-Post DJ, Doherty PC. Cell-mediated protection in influenza infection. Emerg. Infect. Dis.12(1), 48–54 (2006).
   PubMed Web of Science ®Google Scholar
• Belz GT, Smith CM, Kleinert L et al. Distinct migrating and nonmigrating dendritic cell populations are involved in MHC class I-restricted antigen presentation after lung infection with virus. Proc. Natl Acad. Sci. USA101(23), 8670–8675 (2004).
   PubMed Web of Science ®Google Scholar
• Heath WR, Carbone FR. Cross-presentation, dendritic cells, tolerance and immunity. Annu. Rev. Immunol.19, 47–64 (2001).
   PubMed Web of Science ®Google Scholar
• Jenkins MR, Mintern J, La Gruta NL, Kedzierska K, Doherty PC, Turner SJ. Cell cycle-related acquisition of cytotoxic mediators defines the progressive differentiation to effector status for virus-specific CD8+ T cells. J. Immunol.181(6), 3818–3822 (2008).
   PubMed Web of Science ®Google Scholar
• Kaech SM, Ahmed R. Memory CD8+ T cell differentiation: initial antigen encounter triggers a developmental program in naive cells. Nat. Immunol.2(5), 415–422 (2001).
   PubMed Web of Science ®Google Scholar
• Kaech SM, Hemby S, Kersh E, Ahmed R. Molecular and functional profiling of memory CD8 T cell differentiation. Cell111(6), 837–851 (2002).
   PubMed Web of Science ®Google Scholar
• van Stipdonk MJ, Hardenberg G, Bijker MS et al. Dynamic programming of CD8+ T lymphocyte responses. Nat. Immunol.4(4), 361–365 (2003).
   PubMed Web of Science ®Google Scholar
• van Stipdonk MJ, Lemmens EE, Schoenberger SP. Naive CTLs require a single brief period of antigenic stimulation for clonal expansion and differentiation. Nat. Immunol.2(5), 423–429 (2001).
   PubMed Web of Science ®Google Scholar
• Gett AV, Hodgkin PD. Cell division regulates the T cell cytokine repertoire, revealing a mechanism underlying immune class regulation. Proc. Natl Acad. Sci. USA95(16), 9488–9493 (1998).
   PubMed Web of Science ®Google Scholar
• Lawrence CW, Braciale TJ. Activation, differentiation, and migration of naive virus-specific CD8+ T cells during pulmonary influenza virus infection. J. Immunol.173(2), 1209–1218 (2004).
   PubMed Web of Science ®Google Scholar
• Marshall DR, Turner SJ, Belz GT et al. Measuring the diaspora for virus-specific CD8+ T cells. Proc. Natl Acad. Sci. USA98(11), 6313–6318 (2001).
   PubMed Web of Science ®Google Scholar
• Zinkernagel RM, Doherty PC. Restriction of in vitro T cell-mediated cytotoxicity in lymphocytic choriomeningitis within a syngeneic or semiallogeneic system. Nature248(450), 701–702 (1974).
   PubMed Web of Science ®Google Scholar
• Cresswell P, Ackerman AL, Giodini A, Peaper DR, Wearsch PA. Mechanisms of MHC class I-restricted antigen processing and cross-presentation. Immunol. Rev.207, 145–157 (2005).
   PubMed Web of Science ®Google Scholar
• Wherry EJ, Teichgraber V, Becker TC et al. Lineage relationship and protective immunity of memory CD8 T cell subsets. Nat. Immunol.4(3), 225–234 (2003).
   PubMed Web of Science ®Google Scholar
• Bachmann MF, Gallimore A, Linkert S et al. Developmental regulation of Lck targeting to the CD8 coreceptor controls signaling in naive and memory T cells. J. Exp. Med.189(10), 1521–1530 (1999).
   PubMed Web of Science ®Google Scholar
• Flynn KJ, Belz GT, Altman JD, Ahmed R, Woodland DL, Doherty PC. Virus-specific CD8+ T cells in primary and secondary influenza pneumonia. Immunity8(6), 683–691 (1998).
   PubMed Web of Science ®Google Scholar
• Harrington LE, Galvan M, Baum LG, Altman JD, Ahmed R. Differentiating between memory and effector CD8 T cells by altered expression of cell surface O-glycans. J. Exp. Med.191(7), 1241–1246 (2000).
   PubMed Web of Science ®Google Scholar
• Badovinac VP, Messingham KA, Jabbari A, Haring JS, Harty JT. Accelerated CD8+ T-cell memory and prime–boost response after dendritic-cell vaccination. Nat. Med.11(7), 748–756 (2005).
   PubMed Web of Science ®Google Scholar
• Chang JT, Palanivel VR, Kinjyo I et al. Asymmetric T lymphocyte division in the initiation of adaptive immune responses. Science315(5819), 1687–1691 (2007).
   PubMed Web of Science ®Google Scholar
• Kaech SM, Wherry EJ. Heterogeneity and cell-fate decisions in effector and memory CD8+ T cell differentiation during viral infection. Immunity27(3), 393–405 (2007).
   PubMed Web of Science ®Google Scholar
• Kedzierska K, Stambas J, Jenkins MR, Keating R, Turner SJ, Doherty PC. Location rather than CD62L phenotype is critical in the early establishment of influenza-specific CD8+ T cell memory. Proc. Natl Acad. Sci. USA104(23), 9782–9787 (2007).
   PubMed Web of Science ®Google Scholar
• Kedzierska K, Venturi V, Field K, Davenport MP, Turner SJ, Doherty PC. Early establishment of diverse T cell receptor profiles for influenza-specific CD8+CD62Lhi memory T cells. Proc. Natl Acad. Sci. USA103(24), 9184–9189 (2006).
   PubMed Web of Science ®Google Scholar
• Bannard O, Kraman M, Fearon DT. Secondary replicative function of CD8+ T cells that had developed an effector phenotype. Science323(5913), 505–509 (2009).
   PubMed Web of Science ®Google Scholar
• Teixeiro E, Daniels MA, Hamilton SE et al. Different T cell receptor signals determine CD8+ memory versus effector development. Science323(5913), 502–505 (2009).
   PubMed Web of Science ®Google Scholar
• Reiner SL, Sallusto F, Lanzavecchia A. Division of labor with a workforce of one: challenges in specifying effector and memory T cell fate. Science317(5838), 622–625 (2007).
   PubMed Web of Science ®Google Scholar
• Stemberger C, Huster KM, Koffler M et al. A single naive CD8+ T cell precursor can develop into diverse effector and memory subsets. Immunity27(6), 985–997 (2007).
   PubMed Web of Science ®Google Scholar
• Prlic M, Williams MA, Bevan MJ. Requirements for CD8 T-cell priming, memory generation and maintenance. Curr. Opin. Immunol.19(3), 315–319 (2007).
   PubMed Web of Science ®Google Scholar
• Williams MA, Tyznik AJ, Bevan MJ. Interleukin-2 signals during priming are required for secondary expansion of CD8+ memory T cells. Nature441(7095), 890–893 (2006).
   PubMed Web of Science ®Google Scholar
• Bennett SR, Carbone FR, Karamalis F, Flavell RA, Miller JF, Heath WR. Help for cytotoxic-T-cell responses is mediated by CD40 signalling. Nature393(6684), 478–480 (1998).
   PubMed Web of Science ®Google Scholar
• Kilbourne ED. Future influenza vaccines and the use of genetic recombinants. Bull. World Health Organ.41(3), 643–645 (1969).
   PubMed Web of Science ®Google Scholar
• Chen W, Bennink JR, Morton PA, Yewdell JW. Mice deficient in perforin, CD4+ T cells, or CD28-mediated signaling maintain the typical immunodominance hierarchies of CD8+ T-cell responses to influenza virus. J. Virol.76(20), 10332–10337 (2002).
   PubMed Web of Science ®Google Scholar
• Townsend AR, Rothbard J, Gotch FM, Bahadur G, Wraith D, McMichael AJ. The epitopes of influenza nucleoprotein recognized by cytotoxic T lymphocytes can be defined with short synthetic peptides. Cell44(6), 959–968 (1986).
   PubMed Web of Science ®Google Scholar
• Belz GT, Xie W, Altman JD, Doherty PC. A previously unrecognized H-2D(b)-restricted peptide prominent in the primary influenza A virus-specific CD8+ T-cell response is much less apparent following secondary challenge. J. Virol.74(8), 3486–3493 (2000).
   PubMed Web of Science ®Google Scholar
• Belz GT, Xie W, Doherty PC. Diversity of epitope and cytokine profiles for primary and secondary influenza a virus-specific CD8+ T cell responses. J. Immunol.166(7), 4627–4633 (2001).
   PubMed Web of Science ®Google Scholar
• Chen W, Calvo PA, Malide D et al. A novel influenza A virus mitochondrial protein that induces cell death. Nat. Med.7(12), 1306–1312 (2001).
   PubMed Web of Science ®Google Scholar
• Vitiello A, Yuan L, Chesnut RW et al. Immunodominance analysis of CTL responses to influenza PR8 virus reveals two new dominant and subdominant Kb-restricted epitopes. J. Immunol.157(12), 5555–5562 (1996).
   PubMed Web of Science ®Google Scholar
• Eichelberger M, Allan W, Zijlstra M, Jaenisch R, Doherty PC. Clearance of influenza virus respiratory infection in mice lacking class I major histocompatibility complex-restricted CD8+ T cells. J. Exp. Med.174(4), 875–880 (1991).
   PubMed Web of Science ®Google Scholar
• Graham MB, Braciale TJ. Resistance to and recovery from lethal influenza virus infection in B lymphocyte-deficient mice. J. Exp. Med.186(12), 2063–2068 (1997).
   PubMed Web of Science ®Google Scholar
• Cerwenka A, Morgan TM, Dutton RW. Naive, effector, and memory CD8 T cells in protection against pulmonary influenza virus infection: homing properties rather than initial frequencies are crucial. J. Immunol.163(10), 5535–5543 (1999).
   PubMed Web of Science ®Google Scholar
• Cerwenka A, Morgan TM, Harmsen AG, Dutton RW. Migration kinetics and final destination of type 1 and type 2 CD8 effector cells predict protection against pulmonary virus infection. J. Exp. Med.189(2), 423–434 (1999).
   PubMed Web of Science ®Google Scholar
• Webby RJ, Andreansky S, Stambas J et al. Protection and compensation in the influenza virus-specific CD8+ T cell response. Proc. Natl Acad. Sci. USA100(12), 7235–7240 (2003).
   PubMed Web of Science ®Google Scholar
• Peters PJ, Borst J, Oorschot V et al. Cytotoxic T lymphocyte granules are secretory lysosomes, containing both perforin and granzymes. J. Exp. Med.173(5), 1099–1109 (1991).
   PubMed Web of Science ®Google Scholar
• Smyth MJ, Kelly JM, Sutton VR et al. Unlocking the secrets of cytotoxic granule proteins. J. Leukoc. Biol.70(1), 18–29 (2001).
   PubMed Web of Science ®Google Scholar
• Topham DJ, Tripp RA, Doherty PC. CD8+ T cells clear influenza virus by perforin or Fas-dependent processes. J. Immunol.159(11), 5197–5200 (1997).
   PubMed Web of Science ®Google Scholar
• Mullbacher A, Waring P, Tha Hla R et al. Granzymes are the essential downstream effector molecules for the control of primary virus infections by cytolytic leukocytes. Proc. Natl Acad. Sci. USA96(24), 13950–13955 (1999).
   PubMed Web of Science ®Google Scholar
• Jenkins MR, Trapani JA, Doherty PC, Turner SJ. Granzyme K expressing cytotoxic T lymphocytes protects against influenza virus in granzyme AB-/- mice. Viral Immunol.21(3), 341–346 (2008).
   PubMed Web of Science ®Google Scholar
• Jenkins MR, Kedzierska K, Doherty PC, Turner SJ. Heterogeneity of effector phenotype for acute phase and memory influenza A virus-specific CTL. J. Immunol.179(1), 64–70 (2007).
   PubMed Web of Science ®Google Scholar
• Mintern JD, Guillonneau C, Carbone FR, Doherty PC, Turner SJ. Cutting edge: tissue-resident memory CTL down-regulate cytolytic molecule expression following virus clearance. J. Immunol.179(11), 7220–7224 (2007).
   PubMed Web of Science ®Google Scholar
• Jones CM, Cose SC, Coles RM et al. Herpes simplex virus type 1-specific cytotoxic T-lymphocyte arming occurs within lymph nodes draining the site of cutaneous infection. J. Virol.74(5), 2414–2419 (2000).
   PubMed Web of Science ®Google Scholar
• Johnson BJ, Costelloe EO, Fitzpatrick DR et al. Single-cell perforin and granzyme expression reveals the anatomical localization of effector CD8+ T cells in influenza virus-infected mice. Proc. Natl Acad. Sci. USA100(5), 2657–2662 (2003).
   PubMed Web of Science ®Google Scholar
• La Gruta NL, Turner SJ, Doherty PC. Hierarchies in cytokine expression profiles for acute and resolving influenza virus-specific CD8+ T cell responses: correlation of cytokine profile and TCR avidity. J. Immunol.172(9), 5553–5560 (2004).
   PubMed Web of Science ®Google Scholar
• Slifka MK, Rodriguez F, Whitton JL. Rapid on/off cycling of cytokine production by virus-specific CD8+ T cells. Nature401(6748), 76–79 (1999).
   PubMed Web of Science ®Google Scholar
• La Gruta NL, Thomas PG, Webb AI et al. Epitope-specific TCRb repertoire diversity imparts no functional advantage on the CD8+ T cell response to cognate viral peptides. Proc. Natl Acad. Sci. USA105(6), 2034–2039 (2008).
   PubMed Web of Science ®Google Scholar
• Flynn KJ, Riberdy JM, Christensen JP, Altman JD, Doherty PC. In vivo proliferation of naive and memory influenza-specific CD8+ T cells. Proc. Natl Acad. Sci. USA96(15), 8597–8602 (1999).
   PubMed Web of Science ®Google Scholar
• Kohlmeier JE, Woodland DL. Immunity to respiratory viruses. Annu. Rev. Immunol.27, 61–82 (2009).
   PubMed Web of Science ®Google Scholar
• Forrest BD, Pride MW, Dunning AJ et al. Correlation of cellular immune responses with protection against culture-confirmed influenza virus in young children. Clin. Vaccine Immunol.15(7), 1042–1053 (2008).
   PubMed Web of Science ®Google Scholar
• Kreijtz JH, Bodewes R, van Amerongen G et al. Primary influenza A virus infection induces cross-protective immunity against a lethal infection with a heterosubtypic virus strain in mice. Vaccine25(4), 612–620 (2007).
   PubMed Web of Science ®Google Scholar
• Kreijtz JH, de Mutsert G, van Baalen CA, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Cross-recognition of avian H5N1 influenza virus by human cytotoxic T-lymphocyte populations directed to human influenza A virus. J. Virol.82(11), 5161–5166 (2008).
   PubMed Web of Science ®Google Scholar
• Lee LY, Ha do LA, Simmons C et al. Memory T cells established by seasonal human influenza A infection cross-react with avian influenza A (H5N1) in healthy individuals. J. Clin. Invest.118(10), 3478–3490 (2008).
   PubMed Web of Science ®Google Scholar
• McMichael AJ, Gotch FM, Noble GR, Beare PA. Cytotoxic T-cell immunity to influenza. N. Engl. J. Med.309(1), 13–17 (1983).
   PubMed Web of Science ®Google Scholar
• Epstein SL. Prior H1N1 influenza infection and susceptibility of Cleveland Family Study participants during the H2N2 pandemic of 1957: an experiment of nature. J. Infect. Dis.193(1), 49–53 (2006).
   PubMed Web of Science ®Google Scholar
• Berkhoff EG, Geelhoed-Mieras MM, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Assessment of the extent of variation in influenza A virus cytotoxic T-lymphocyte epitopes by using virus-specific CD8+ T-cell clones. J. Gen. Virol.88(Pt 2), 530–535 (2007).
   PubMed Web of Science ®Google Scholar
• Berkhoff EG, Boon AC, Nieuwkoop NJ et al. A mutation in the HLA-B*2705-restricted NP383–391 epitope affects the human influenza A virus-specific cytotoxic T-lymphocyte response in vitro. J. Virol.78(10), 5216–5222 (2004).
   PubMed Web of Science ®Google Scholar
• Berkhoff EG, Geelhoed-Mieras MM, Jonges M et al. An amino acid substitution in the influenza A virus hemagglutinin associated with escape from recognition by human virus-specific CD4+ T-cells. Virus Res.126(1–2), 282–287 (2007).
   PubMed Web of Science ®Google Scholar
• Boon AC, de Mutsert G, Graus YM et al. Sequence variation in a newly identified HLA-B35-restricted epitope in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. J. Virol.76(5), 2567–2572 (2002).
   PubMed Web of Science ®Google Scholar
• Roti M, Yang J, Berger D, Huston L, James EA, Kwok WW. Healthy human subjects have CD4+ T cells directed against H5N1 influenza virus. J. Immunol.180(3), 1758–1768 (2008).
   PubMed Web of Science ®Google Scholar
• Yewdell JW, Haeryfar SM. Understanding presentation of viral antigens to CD8+ T cells in vivo: the key to rational vaccine design. Annu. Rev. Immunol.23, 651–682 (2005).
   PubMed Web of Science ®Google Scholar
• Sidney J, Peters B, Frahm N, Brander C, Sette A. HLA class I supertypes: a revised and updated classification. BMC Immunol.9, 1 (2008).
   PubMed Web of Science ®Google Scholar
• Kumar R, Burns EA. Age-related decline in immunity: implications for vaccine responsiveness. Expert Rev. Vaccines7(4), 467–479 (2008).
   PubMed Web of Science ®Google Scholar
• Yager EJ, Ahmed M, Lanzer K, Randall TD, Woodland DL, Blackman MA. Age-associated decline in T cell repertoire diversity leads to holes in the repertoire and impaired immunity to influenza virus. J. Exp. Med.205(3), 711–723 (2008).
   PubMed Web of Science ®Google Scholar
• Kedzierska K, Day EB, Pi J et al. Quantification of repertoire diversity of influenza-specific epitopes with predominant public or private TCR usage. J. Immunol.177(10), 6705–6712 (2006).
   PubMed Web of Science ®Google Scholar
• Ahmed M, Lanzer KG, Yager EJ, Adams PS, Johnson LL, Blackman MA. Clonal expansions and loss of receptor diversity in the naive CD8 T cell repertoire of aged mice. J. Immunol.182(2), 784–792 (2009).
   PubMed Web of Science ®Google Scholar
• Messaoudi I, Guevara Patino JA, Dyall R, LeMaoult J, Nikolich-Zugich J. Direct link between MHC polymorphism, T cell avidity, and diversity in immune defense. Science298(5599), 1797–1800 (2002).
   PubMed Web of Science ®Google Scholar
• Hammarlund E, Lewis MW, Hansen SG et al. Duration of antiviral immunity after smallpox vaccination. Nat. Med.9(9), 1131–1137 (2003).
   PubMed Web of Science ®Google Scholar
• McMichael AJ, Gotch F, Cullen P, Askonas B, Webster RG. The human cytotoxic T cell response to influenza A vaccination. Clin. Exp. Immunol.43(2), 276–284 (1981).
   PubMed Web of Science ®Google Scholar
• He XS, Holmes TH, Zhang C et al. Cellular immune responses in children and adults receiving inactivated or live attenuated influenza vaccines. J. Virol.80(23), 11756–11766 (2006).
   PubMed Web of Science ®Google Scholar
• Kreijtz JH, Osterhaus AD, Rimmelzwaan GF. Vaccination strategies and vaccine formulations for epidemic and pandemic influenza control. Hum. Vaccin.5(3), 126–135 (2009).
   PubMed Web of Science ®Google Scholar
• Baras B, Stittelaar KJ, Simon JH et al. Cross-protection against lethal H5N1 challenge in ferrets with an adjuvanted pandemic influenza vaccine. PLoS ONE3(1), e1401 (2008).
   PubMed Web of Science ®Google Scholar
• Stephenson I, Nicholson KG, Hoschler K et al. Antigenically distinct MF59-adjuvanted vaccine to boost immunity to H5N1. N. Engl. J. Med.359(15), 1631–1633 (2008).
   PubMed Web of Science ®Google Scholar
• Guillonneau C, Mintern JD, Hubert FX et al. Combined NKT cell activation and influenza virus vaccination boosts memory CTL generation and protective immunity. Proc. Natl Acad. Sci. USA106(9), 3330–3335 (2009).
   PubMed Web of Science ®Google Scholar
• Lawson CM, Subbarao EK, Murphy BR. Nucleotide sequence changes in the polymerase basic protein 2 gene of temperature-sensitive mutants of influenza A virus. Virology191(1), 506–510 (1992).
   PubMed Web of Science ®Google Scholar
• Subbarao EK, Park EJ, Lawson CM, Chen AY, Murphy BR. Sequential addition of temperature-sensitive missense mutations into the PB2 gene of influenza A transfectant viruses can effect an increase in temperature sensitivity and attenuation and permits the rational design of a genetically engineered live influenza A virus vaccine. J. Virol.69(10), 5969–5977 (1995).
   PubMed Web of Science ®Google Scholar
• Lo CY, Wu Z, Misplon JA et al. Comparison of vaccines for induction of heterosubtypic immunity to influenza A virus: cold-adapted vaccine versus DNA prime-adenovirus boost strategies. Vaccine26(17), 2062–2072 (2008).
   PubMed Web of Science ®Google Scholar
• Powell TJ, Strutt T, Reome J et al. Priming with cold-adapted influenza A does not prevent infection but elicits long-lived protection against supralethal challenge with heterosubtypic virus. J. Immunol.178(2), 1030–1038 (2007).
   PubMed Web of Science ®Google Scholar
• Joshi NS, Cui W, Chandele A et al. Inflammation directs memory precursor and short-lived effector CD8+ T cell fates via the graded expression of T-bet transcription factor. Immunity27(2), 281–295 (2007).
   PubMed Web of Science ®Google Scholar
• Zehn D, Lee SY, Bevan MJ. Complete but curtailed T-cell response to very low-affinity antigen. Nature458(7235), 211–214 (2009).
   PubMed Web of Science ®Google Scholar
• Pantaleo G. HIV-1 T-cell vaccines: evaluating the next step. Lancet Infect. Dis.8(2), 82–83 (2008).
   PubMed Web of Science ®Google Scholar
• Ledford H. HIV vaccine may raise risk. Nature450(7168), 325 (2007).
   PubMed Web of Science ®Google Scholar
• McElrath MJ, De Rosa SC, Moodie Z et al. HIV-1 vaccine-induced immunity in the test-of-concept Step Study: a case-cohort analysis. Lancet372(9653), 1894–1905 (2008).
   PubMed Web of Science ®Google Scholar
• Buchbinder SP, Mehrotra DV, Duerr A et al. Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet372(9653), 1881–1893 (2008).
   PubMed Web of Science ®Google Scholar
• Kang SM, Yoo DG, Lipatov AS et al. Induction of long-term protective immune responses by influenza H5N1 virus-like particles. PLoS ONE4(3), e4667 (2009).
   PubMed Web of Science ®Google Scholar
• Deliyannis G, Jackson DC, Dyer W et al. Immunopotentiation of humoral and cellular responses to inactivated influenza vaccines by two different adjuvants with potential for human use. Vaccine16(20), 2058–2068 (1998).
   PubMed Web of Science ®Google Scholar
• Rimmelzwaan GF, Claas EC, van Amerongen G, de Jong JC, Osterhaus AD. ISCOM vaccine induced protection against a lethal challenge with a human H5N1 influenza virus. Vaccine17(11–12), 1355–1358 (1999).
   PubMed Web of Science ®Google Scholar
• Gluck R, Burri KG, Metcalfe I. Adjuvant and antigen delivery properties of virosomes. Curr. Drug Deliv.2(4), 395–400 (2005).
   PubMedGoogle Scholar
• Rimmelzwaan GF, Baars M, van Beek R et al. Induction of protective immunity against influenza virus in a macaque model: comparison of conventional and iscom vaccines. J. Gen. Virol.78(Pt 4), 757–765 (1997).
   PubMed Web of Science ®Google Scholar
• Rimmelzwaan GF, Nieuwkoop N, Brandenburg A et al. A randomized, double blind study in young healthy adults comparing cell mediated and humoral immune responses induced by influenza ISCOM vaccines and conventional vaccines. Vaccine19(9–10), 1180–1187 (2000).
   PubMed Web of Science ®Google Scholar
• Sanders MT, Brown LE, Deliyannis G, Pearse MJ. ISCOM-based vaccines: the second decade. Immunol. Cell Biol.83(2), 119–128 (2005).
   PubMed Web of Science ®Google Scholar
• Voeten JT, Rimmelzwaan GF, Nieuwkoop NJ, Lovgren-Bengtsson K, Osterhaus AD. Introduction of the haemagglutinin transmembrane region in the influenza virus matrix protein facilitates its incorporation into ISCOM and activation of specific CD8+ cytotoxic T lymphocytes. Vaccine19(4–5), 514–522 (2000).
   PubMed Web of Science ®Google Scholar
• Kumagai Y, Takeuchi O, Akira S. TLR9 as a key receptor for the recognition of DNA. Adv. Drug Deliv. Rev.60(7), 795–804 (2008).
   PubMed Web of Science ®Google Scholar
• Porgador A, Irvine KR, Iwasaki A, Barber BH, Restifo NP, Germain RN. Predominant role for directly transfected dendritic cells in antigen presentation to CD8+ T cells after gene gun immunization. J. Exp. Med.188(6), 1075–1082 (1998).
   PubMed Web of Science ®Google Scholar
• Epstein SL, Kong WP, Misplon JA et al. Protection against multiple influenza A subtypes by vaccination with highly conserved nucleoprotein. Vaccine23(46–47), 5404–5410 (2005).
   PubMed Web of Science ®Google Scholar
• Ulmer JB, Donnelly JJ, Parker SE et al. Heterologous protection against influenza by injection of DNA encoding a viral protein. Science259(5102), 1745–1749 (1993).
   PubMed Web of Science ®Google Scholar
• Ulmer JB, Fu TM, Deck RR et al. Protective CD4+ and CD8+ T cells against influenza virus induced by vaccination with nucleoprotein DNA. J. Virol.72(7), 5648–5653 (1998).
   PubMed Web of Science ®Google Scholar
• Raviprakash K, Porter KR. Needle-free injection of DNA vaccines: a brief overview and methodology. Methods Mol. Med.127, 83–89 (2006).
   PubMedGoogle Scholar
• Jones S, Evans K, McElwaine-Johnn H et al. DNA vaccination protects against an influenza challenge in a double-blind randomised placebo-controlled Phase 1b clinical trial. Vaccine27(18), 2506–2512 (2009).
   PubMed Web of Science ®Google Scholar
• Chua BY, Zeng W, Jackson DC. Synthesis of Toll-like receptor-2 targeting lipopeptides as self-adjuvanting vaccines. Methods Mol. Biol.494, 247–261 (2008).
   PubMedGoogle Scholar
• Jackson DC, Lau YF, Le T et al. A totally synthetic vaccine of generic structure that targets Toll-like receptor 2 on dendritic cells and promotes antibody or cytotoxic T cell responses. Proc. Natl Acad. Sci. USA101(43), 15440–15445 (2004).
   PubMed Web of Science ®Google Scholar
• Eriksson EM, Jackson DC. Recent advances with TLR2-targeting lipopeptide-based vaccines. Curr. Protein Pept. Sci.8(4), 412–417 (2007).
   PubMed Web of Science ®Google Scholar
• Alphs HH, Gambhira R, Karanam B et al. Protection against heterologous human papillomavirus challenge by a synthetic lipopeptide vaccine containing a broadly cross-neutralizing epitope of L2. Proc. Natl Acad. Sci. USA105(15), 5850–5855 (2008).
   PubMed Web of Science ®Google Scholar
• Deliyannis G, Kedzierska K, Lau YF et al. Intranasal lipopeptide primes lung-resident memory CD8+ T cells for long-term pulmonary protection against influenza. Eur J. Immunol.36(3), 770–778 (2006).
   PubMed Web of Science ®Google Scholar
• Day EB, Zeng W, Doherty PC, Jackson DC, Kedzierska K, Turner SJ. The context of epitope presentation can influence functional quality of recalled influenza A virus-specific memory CD8+ T cells. J. Immunol.179(4), 2187–2194 (2007).
   PubMed Web of Science ®Google Scholar
• Kawashima Y, Pfafferott K, Frater J et al. Adaptation of HIV-1 to human leukocyte antigen class I. Nature458(7238), 641–645 (2009).
   PubMed Web of Science ®Google Scholar
• Cornberg M, Chen AT, Wilkinson LA et al. Narrowed TCR repertoire and viral escape as a consequence of heterologous immunity. J. Clin. Invest.116(5), 1443–1456 (2006).
   PubMed Web of Science ®Google Scholar
• Price GE, Ou R, Jiang H, Huang L, Moskophidis D. Viral escape by selection of cytotoxic T cell-resistant variants in influenza A virus pneumonia. J. Exp. Med.191(11), 1853–1867 (2000).
   PubMed Web of Science ®Google Scholar
• Boon AC, De Mutsert G, Fouchier RA, Sintnicolaas K, Osterhaus AD, Rimmelzwaan GF. Preferential HLA usage in the influenza virus-specific CTL response. J. Immunol.172(7), 4435–4443 (2004).
   PubMed Web of Science ®Google Scholar
• Boon AC, de Mutsert G, van Baarle D et al. Recognition of homo- and heterosubtypic variants of influenza A viruses by human CD8+ T lymphocytes. J. Immunol.172(4), 2453–2460 (2004).
   PubMed Web of Science ®Google Scholar
• Rimmelzwaan GF, Boon AC, Voeten JT, Berkhoff EG, Fouchier RA, Osterhaus AD. Sequence variation in the influenza A virus nucleoprotein associated with escape from cytotoxic T lymphocytes. Virus Res.103(1–2), 97–100 (2004).
   PubMed Web of Science ®Google Scholar
• Voeten JT, Bestebroer TM, Nieuwkoop NJ, Fouchier RA, Osterhaus AD, Rimmelzwaan GF. Antigenic drift in the influenza A virus (H3N2) nucleoprotein and escape from recognition by cytotoxic T lymphocytes. J. Virol.74(15), 6800–6807 (2000).
   PubMed Web of Science ®Google Scholar
• Berkhoff EG, Geelhoed-Mieras MM, Verschuren EJ et al. The loss of immunodominant epitopes affects interferon-γ production and lytic activity of the human influenza virus-specific cytotoxic T lymphocyte response in vitro. Clin. Exp. Immunol.148(2), 296–306 (2007).
   PubMed Web of Science ®Google Scholar
• Barouch DH, Kunstman J, Kuroda MJ et al. Eventual AIDS vaccine failure in a rhesus monkey by viral escape from cytotoxic T lymphocytes. Nature415(6869), 335–339 (2002).
   PubMed Web of Science ®Google Scholar
• Badovinac VP, Hamilton SE, Harty JT. Viral infection results in massive CD8+ T cell expansion and mortality in vaccinated perforin-deficient mice. Immunity18(4), 463–474 (2003).
   PubMed Web of Science ®Google Scholar
• Cheung CY, Poon LL, Lau AS et al. Induction of proinflammatory cytokines in human macrophages by influenza A (H5N1) viruses: a mechanism for the unusual severity of human disease? Lancet360(9348), 1831–1837 (2002).
   PubMed Web of Science ®Google Scholar
• Zhou J, Law HK, Cheung CY, Ng IH, Peiris JS, Lau YL. Functional tumor necrosis factor-related apoptosis-inducing ligand production by avian influenza virus-infected macrophages. J. Infect. Dis.193(7), 945–953 (2006).
   PubMed Web of Science ®Google Scholar
• Wiley JA, Cerwenka A, Harkema JR, Dutton RW, Harmsen AG. Production of interferon-γ by influenza hemagglutinin-specific CD8 effector T cells influences the development of pulmonary immunopathology. Am. J. Pathol.158(1), 119–130 (2001).
   PubMed Web of Science ®Google Scholar
• La Gruta NL, Kedzierska K, Stambas J, Doherty PC. A question of self-preservation: immunopathology in influenza virus infection. Immunol. Cell Biol.85(2), 85–92 (2007).
   PubMed Web of Science ®Google Scholar
• Selin LK, Brehm MA, Naumov YN et al. Memory of mice and men: CD8+ T-cell cross-reactivity and heterologous immunity. Immunol. Rev.211, 164–181 (2006).
   PubMed Web of Science ®Google Scholar
• Cornberg M, Sheridan BS, Saccoccio FM, Brehm MA, Selin LK. Protection against vaccinia virus challenge by CD8 memory T cells resolved by molecular mimicry. J. Virol.81(2), 934–944 (2007).
   PubMed Web of Science ®Google Scholar