221
Views
39
CrossRef citations to date
0
Altmetric
Special Focus Issues: DNA Vaccines - Review

Genetic heterologous prime–boost vaccination strategies for improved systemic and mucosal immunity

&
Pages 1171-1181 | Published online: 09 Jan 2014

References

  • Fynan EF, Webster RG, Fuller DH, Haynes JR, Santoro JC, Robinson HL. DNA vaccines: protective immunizations by parenteral, mucosal, and gene-gun inoculations. Proc. Natl Acad. Sci. USA90(24), 11478–11482 (1993).
  • Pardoll DM, Beckerleg AM. Exposing the immunology of naked DNA vaccines. Immunity3(2), 165–169 (1995).
  • Leong KH, Ramsay AJ, Boyle DB, Ramshaw IA. Selective induction of immune responses by cytokines coexpressed in recombinant fowlpox virus. J. Virol.68(12), 8125–8130 (1994).
  • Ramsay AJ, Husband AJ, Ramshaw IA et al. The role of interleukin-6 in mucosal IgA antibody responses in vivo. Science264(5158), 561–563 (1994).
  • Somogyi P, Frazier J, Skinner MA. Fowlpox virus host range restriction: gene expression, DNA replication, and morphogenesis in nonpermissive mammalian cells. Virology197(1), 439–444 (1993).
  • Leong KH, Ramsay AJ, Morin MJ, Robinson HL, Boyle DB, Ramshaw IA. Molecular approaches to the control of infectious diseases. Vaccine95, 327–331 (1995).
  • Kent SJ, Zhao A, Best SJ, Chandler JD, Boyle DB, Ramshaw IA. Enhanced T-cell immunogenicity and protective efficacy of a human immunodeficiency virus type 1 vaccine regimen consisting of consecutive priming with DNA and boosting with recombinant fowlpox virus. J. Virol.72(12), 10180–10188 (1998).
  • Allen TM, Vogel TU, Fuller DH et al. Induction of AIDS virus-specific CTL activity in fresh, unstimulated peripheral blood lymphocytes from rhesus macaques vaccinated with a DNA prime/modified vaccinia virus Ankara boost regimen. J. Immunol.164(9), 4968–4978 (2000).
  • Barnett SW, Rajasekar S, Legg H et al. Vaccination with HIV-1 gp120 DNA induces immune responses that are boosted by a recombinant gp120 protein subunit. Vaccine15(8), 869–873 (1997).
  • Caver TE, Lockey TD, Srinivas RV, Webster RG, Hurwitz JL. A novel vaccine regimen utilizing DNA, vaccinia virus and protein immunizations for HIV-1 envelope presentation. Vaccine17(11–12), 1567–1572 (1999).
  • Epstein JE, Charoenvit Y, Kester KE et al. Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS,S/AS02A. Vaccine22(13–14), 1592–1603 (2004).
  • Amara RR, Villinger F, Altman JD et al. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. Science292(5514), 69–74 (2001).
  • Horton H, Vogel TU, Carter DK et al. Immunization of rhesus macaques with a DNA prime/modified vaccinia virus Ankara boost regimen induces broad simian immunodeficiency virus (SIV)-specific T-cell responses and reduces initial viral replication but does not prevent disease progression following challenge with pathogenic SIVmac239. J. Virol.76(14), 7187–7202 (2002).
  • Casimiro DR, Wang F, Schleif WA et al. Attenuation of simian immunodeficiency virus SIVmac239 infection by prophylactic immunization with DNA and recombinant adenoviral vaccine vectors expressing Gag. J. Virol.79(24), 15547–15555 (2005).
  • De Rose R, Batten CJ, Smith MZ et al. Comparative efficacy of subtype AE simian-human immunodeficiency virus priming and boosting vaccines in pigtail macaques. J. Virol.81(1), 292–300 (2007).
  • Guimaraes-Walker A, Mackie N, McCormack S et al. Lessons from IAVI-006, a Phase I clinical trial to evaluate the safety and immunogenicity of the pTHr.HIVA DNA and MVA.HIVA vaccines in a prime-boost strategy to induce HIV-1 specific T-cell responses in healthy volunteers. Vaccine26(51), 6671–6677 (2008).
  • McCormack S, Stohr W, Barber T et al. EV02: a Phase I trial to compare the safety and immunogenicity of HIV DNA-C prime-NYVAC-C boost to NYVAC-C alone. Vaccine26(25), 3162–3174 (2008).
  • Kelleher AD, Puls RL, Bebbington M et al. A randomised, placebo-controlled Phase I trial of DNA prime, recombinant fowlpox virus boost prophylactic vaccine for HIV-1. AIDS20(2), 294–297 (2006).
  • Sekaly RP. The failed HIV Merck vaccine study: a step back or a launching point for future vaccine development? J. Exp. Med.205(1), 7–12 (2008).
  • Dale CJ, De Rose R, Wilson KM et al. Evaluation in macaques of HIV-1 DNA vaccines containing primate CpG motifs and fowlpoxvirus vaccines co-expressing IFNγ or IL-12. Vaccine23(2), 188–197 (2004).
  • Kutzler MA, Weiner DB. DNA vaccines: ready for prime time? Nat. Rev. Genet.9(10), 776–788 (2008).
  • Mathiesen I. Electropermeabilization of skeletal muscle enhances gene transfer in vivo. Gene Ther.6(4), 508–514 (1999).
  • Tollefsen S, Vordermeier M, Olsen I et al. DNA injection in combination with electroporation: a novel method for vaccination of farmed ruminants. Scand. J. Immunol.57(3), 229–238 (2003).
  • Wallace M, Evans B, Woods S et al. Tolerability of two sequential electroporation treatments using MedPulser DNA delivery system (DDS) in healthy adults. Mol. Ther.17(5), 922–928 (2009).
  • Shortman K, Lahoud MH, Caminschi I. Improving vaccines by targeting antigens to dendritic cells. Exp. Mol. Med.41(2), 61–66 (2009).
  • Mitchell EA, Bergmeier LA, Doyle C et al. Homing of mononuclear cells from iliac lymph nodes to the genital and rectal mucosa in non-human primates. Eur. J. Immunol.28(10), 3066–3074 (1998).
  • Ogra PL, Faden H, Welliver RC. Vaccination strategies for mucosal immune responses. Clin. Microbiol. Rev.14(2), 430–445 (2001).
  • Kozlowski PA, Neutra MR. The role of mucosal immunity in prevention of HIV transmission. Curr. Mol. Med.3(3), 217–228 (2003).
  • Stevceva L, Strober W. Mucosal HIV vaccines: where are we now? Curr. HIV Res.2(1), 1–10 (2004).
  • Belyakov IM, Ahlers JD, Berzofsky JA. Mucosal AIDS vaccines: current status and future directions. Expert Rev. Vaccines3(4 Suppl.), S65–S73 (2004).
  • Veazey RS, DeMaria M, Chalifoux LV et al. Gastrointestinal tract as a major site of CD4+ T cell depletion and viral replication in SIV infection. Science280(5362), 427–431 (1998).
  • Veazey RS, Gauduin MC, Mansfield KG et al. Emergence and kinetics of simian immunodeficiency virus-specific CD8+ T cells in the intestines of macaques during primary infection. J. Virol.75(21), 10515–10519 (2001).
  • Kaul R, Plummer FA, Kimani J et al. HIV-1-specific mucosal CD8+ lymphocyte responses in the cervix of HIV-1-resistant prostitutes in Nairobi. J. Immunol. (164), 1602–1611 (2000).
  • Santosuosso M, Zhang X, McCormick S, Wang J, Hitt M, Xing Z. Mechanisms of mucosal and parenteral tuberculosis vaccinations: adenoviral-based mucosal immunization preferentially elicits sustained accumulation of immune protective CD4 and CD8 T cells within the airway lumen. J. Immunol.174(12), 7986–7994 (2005).
  • Kallenius G, Pawlowski A, Brandtzaeg P, Svenson S. Should a new tuberculosis vaccine be administered intranasally? Tuberculosis (Edinb.)87(4), 257–266 (2007).
  • Giri PK, Khuller GK. Is intranasal vaccination a feasible solution for tuberculosis? Expert Rev. Vaccines7(9), 1341–1356 (2008).
  • Belyakov IM, Derby MA, Ahlers JD et al. Mucosal immunization with HIV-1 peptide vaccine induces mucosal and systemic cytotoxic T lymphocytes and protective immunity in mice against intrarectal recombinant HIV-vaccinia challenge. Proc. Natl Acad. Sci. USA95(4), 1709–1714 (1998).
  • Eo SK, Gierynska M, Kamar AA, Rouse BT. Prime–boost immunization with DNA vaccine: mucosal route of administration changes the rules. J. Immunol.166(9), 5473–5479 (2001).
  • Jeyanathan M, Mu J, Kugathasan K et al. Airway delivery of soluble mycobacterial antigens restores protective mucosal immunity by single intramuscular plasmid DNA tuberculosis vaccination: role of proinflammatory signals in the lung. J. Immunol.181(8), 5618–5626 (2008).
  • Skinner MA, Ramsay AJ, Buchan GS et al. A DNA prime-live vaccine boost strategy in mice can augment IFN-γ responses to mycobacterial antigens but does not increase the protective efficacy of two attenuated strains of Mycobacterium bovis against bovine tuberculosis. Immunology108(4), 548–555 (2003).
  • Hanke T, Samuel RV, Blanchard TJ et al. Effective induction of simian immunodeficiency virus-specific cytotoxic T lymphocytes in macaques by using a multiepitope gene and DNA prime-modified vaccinia virus Ankara boost vaccination regimen. J. Virol.73(9), 7524–7532 (1999).
  • Hawkins RA, Rank RG, Kelly KA. Expression of mucosal homing receptor α4β7 is associated with enhanced migration to the Chlamydia-infected murine genital mucosa in vivo. Infect. Immun.68(10), 5587–5594 (2000).
  • Evans DT, Chen LM, Gillis J 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.77(4), 2400–2409 (2003).
  • Krieg C, Maier R, Meyerhans A. Gut-homing (α(4)β(7)+) Th1 memory responses after inactivated poliovirus immunization in poliovirus orally pre-immunized donors. J. Gen. Virol.85(Pt 6), 1571–1579 (2004).
  • Stenstad H, Ericsson A, Johansson-Lindbom B et al. Gut associated lymphoid tissue primed CD4+ T cells display CCR9 dependent and independent homing to the small intestine. Blood107(9), 3447–3454 (2006).
  • Breinig T, Sester M, Sester U, Meyerhans A. Antigen-specific T cell responses: determination of their frequencies, homing properties, and effector functions in human whole blood. Methods38(2), 77–83 (2006).
  • Baig J, Levy DB, McKay PF et al. Elicitation of simian immunodeficiency virus-specific cytotoxic T lymphocytes in mucosal compartments of rhesus monkeys by systemic vaccination. J. Virol.76(22), 11484–11490 (2002).
  • Musey L, Ding Y, Elizaga M, Ha R, Celum C, McElrath MJ. HIV-1 vaccination administered intramuscularly can induce both systemic and mucosal T cell immunity in HIV-1-uninfected individuals. J. Immunol.171(2), 1094–1101 (2003).
  • Stambas J, Brown SA, Gutierrez A et al. Long lived multi-isotype anti-HIV antibody responses following a prime-double boost immunization strategy. Vaccine23(19), 2454–2464 (2005).
  • Klavinskis LS, Bergmeier LA, Gao L et al. Mucosal or targeted lymph node immunization of macaques with a particulate SIVp27 protein elicits virus-specific CTL in the genito–rectal mucosa and draining lymph nodes. J. Immunol.157(6), 2521–2527 (1996).
  • Wang B, Dang K, Agadjanyan MG et al. Mucosal immunization with a DNA vaccine induces immune responses against HIV-1 at a mucosal site. Vaccine15(8), 821–825 (1997).
  • Imaoka K, Miller CJ, Kubota M et al. Nasal immunisation of nonhuman primates with simian immunodeficiency virus p55gag and cholera toxin adjuvant induces Th1/Th2 help for virus-specific immune responses in reproductive tissues. J. Immunol.161, 5952–5958 (1998).
  • Crotty S, Lohman BL, Lu FX, Tang S, Miller CJ, Andino R. Mucosal immunization of cynomolgus macaques with two serotypes of live poliovirus vectors expressing simian immunodeficiency virus antigens: stimulation of humoral, mucosal, and cellular immunity. J. Virol.73(11), 9485–9495 (1999).
  • Xiang ZQ, Pasquini S, Ertl HCJ. Induction of genital immunity by DNA priming and intranasal booster immunisation with a replication-defective adenoviral recombinant. J. Immunol.162, 6716–6723 (1999).
  • Wang R, Epstein J, Charoenvit Y et al. Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. J. Immunol.172(9), 5561–5569 (2004).
  • Gherardi MM, Najera JL, Perez-Jimenez E, Guerra S, Garcia-Sastre A, Esteban M. Prime–boost immunisation schedules based on influenza virus and vaccinia virus vectors potentiate cellular immune responses against human immunodeficiency virus Env proteins systemically and in genitorectal draining lymph nodes. J. Virol.77(12), 7048–7057 (2003).
  • Shiver JW, Fu T-M, Chen L et al. Replication-incompetent adenivoral vaccine vector elicits effective anti-immunodeficiency-virus immunity. Nature415, 331–335 (2002).
  • Peters C, Pen X, Douven D, Pan Z, Paterson Y. The induction of HIV gag specific CD8+ T cells in spleen and gut-associated lymphoid tissue by parenteral or mucosal immunisation with recombinant Lestiria monocytogenes HIV gag. J. Immunol.170, 5176–5187 (2003).
  • Zhang H, Fayad R, Wang X, Quinn D, Qiao L. Human immunodeficiency virus type 1 gag-specific mucosal immunity after oral immunization with papillomavirus pseudoviruses encoding gag. J. Virol.78(19), 10249–10257 (2004).
  • Wright PF, Mestecky J, McElrath MJ et al. Comparison of systemic and mucosal delivery of 2 canarypox virus vaccines expressing either HIV-1 genes or the gene for rabies virus G protein. J. Infect. Dis.189(7), 1221–1231 (2004).
  • Kent SJ, Dale CJ, Ranasinghe C et al. Mucosally-administered human-simian immunodeficiency virus DNA and fowlpoxvirus-based recombinant vaccines reduce acute phase viral replication in macaques following vaginal challenge with CCR5-tropic SHIV(SF162P3). Vaccine23, 5009–5021 (2005).
  • Ranasinghe C, Medveczky JC, Woltring D et al. Evaluation of fowlpox-vaccinia virus prime-boost vaccine strategies for high-level mucosal and systemic immunity against HIV-1. Vaccine24, 5881–5895 (2006).
  • Gomez CE, Najera JL, Jimenez EP et al. Head-to-head comparison on the immunogenicity of two HIV/AIDS vaccine candidates based on the attenuated poxvirus strains MVA and NYVAC co-expressing in a single locus the HIV-1BX08 gp120 and HIV-1(IIIB) Gag-Pol-Nef proteins of clade B. Vaccine25(15), 2863–2885 (2007).
  • Corbett M, Bogers WM, Heeney JL et al. Aerosol immunization with NYVAC and MVA vectored vaccines is safe, simple, and immunogenic. Proc. Natl Acad. Sci. USA105(6), 2046–2051 (2008).
  • Huang X, Liu L, Ren L, Qiu C, Wan Y, Xu J. Mucosal priming with replicative Tiantan vaccinia and systemic boosting with DNA vaccine raised strong mucosal and systemic HIV-specific immune responses. Vaccine25(52), 8874–8884 (2007).
  • Kubota M, Miller CJ, Imaoka K et al. Oral immunisation with simian immunodeficiency virus p55gag and cholera toxin elicits both mucosal IgA and systemic IgG immune responses in nonhuman primates. J. Immunol.158, 5321–5329 (1997).
  • Hagiwara Y, Kawamura YI, Kataoka K et al. A second generation of double mutant cholera toxin adjuvants: enhanced immunity without intracellular trafficking. J. Immunol.177(5), 3045–3054 (2006).
  • Cox E, Verdonck F, Vanrompay D, Goddeeris B. Adjuvants modulating mucosal immune responses or directing systemic responses towards the mucosa. Vet. Res.37(3), 511–539 (2006).
  • Klavinskis LS, Barnfield C, Gao L, Parker S. Intranasal immunization with plasmid DNA-lipid complexes elicits mucosal immunity in the female genital and rectal tracts. J. Immunol.162(1), 254–262 (1999).
  • Rosada RS, de la Torre LG, Frantz FG et al. Protection against tuberculosis by a single intranasal administration of DNA-hsp65 vaccine complexed with cationic liposomes. BMC Immunol.9, 38 (2008).
  • Ramsay AJ, Leong KH, Ramshaw IA. DNA vaccination against virus infection and enhancement of antiviral immunity following consecutive immunization with DNA and viral vectors. Immunol. Cell. Biol.75(4), 382–388 (1997).
  • Toka FN, Rouse BT. Mucosal application of plasmid-encoded IL-15 sustains a highly protective anti-Herpes simplex virus immunity. J. Leukoc. Biol.78(1), 178–186 (2005).
  • Lillard JW Jr, Boyaka PN, Hedrick JA, Zlotnik A, McGhee JR. Lymphotactin acts as an innate mucosal adjuvant. J. Immunol.162(4), 1959–1965 (1999).
  • Lillard JW Jr, Boyaka PN, Taub DD, McGhee JR. RANTES potentiates antigen-specific mucosal immune responses. J. Immunol.166(1), 162–169 (2001).
  • Gherardi MM, Esteban M. Recombinant poxviruses and mucosal vaccine vectors. J. Gen. Virol.86, 2925–2936 (2005).
  • Belyakov IM, Ahlers JD, Nabel GJ, Moss B, Berzofsky JA. Generation of functionally active HIV-1 specific CD8+ CTL in intestinal mucosa following mucosal, systemic or mixed prime–boost immunization. Virology381(1), 106–115 (2008).
  • Ramirez JC, Finke D, Esteban M, Kraehenbuhl JP, Acha-Orbea H. Tissue distribution of the Ankara strain of vaccinia virus (MVA) after mucosal or systemic administration. Arch. Virol.148(5), 827–839 (2003).
  • Ko SY, Cheng C, Kong WP et al. Enhanced induction of intestinal cellular immunity by oral priming with enteric adenovirus 41 vectors. J. Virol.83(2), 748–756 (2009).
  • Yang K, Whalen BJ, Tirabassi RS et al. A DNA vaccine prime followed by a liposome-encapsulated protein boost confers enhanced mucosal immune responses and protection. J. Immunol.180(9), 6159–6167 (2008).
  • Kim JJ, Yang JS, Dentchev T, Dang K, Weiner DB. Chemokine gene adjuvants can modulate immune responses induced by DNA vaccines. J. Interferon Cytokine Res.20(5), 487–498 (2000).
  • Ramsay AJ, Kent SJ, Strugnell RA, Suhrbier A, Thomson SA, Ramshaw IA. Genetic vaccination strategies for enhanced cellular, humoral and mucosal immunity. Immunol. Rev.171, 27–44 (1999).
  • Perez-Jimenez E, Kochan G, Gherardi MM, Esteban M. MVA-LACK as a safe and efficient vector for vaccination against leishmaniasis. Microbes Infect.8(3), 810–822 (2006).
  • Day SL, Ramshaw IA, Ramsay AJ, Ranasinghe C. Differential effects of the type I interferons α4, β, and e on antiviral activity and vaccine efficacy. J. Immunol.180(11), 7158–7166 (2008).
  • Gherardi MM, Ramirez JC, Esteban M. Interleukin-12 (IL-12) enhancement of the cellular immune response against human immunodeficiency virus type 1 Env antigen in a DNA prime/vaccinia virus boost vaccine regimen is time and dose dependent: suppressive effects of IL-12 boost are mediated by nitric oxide. J. Virol.74(14), 6278–6286 (2000).
  • Boyer JD, Robinson TM, Kutzler MA et al. SIV DNA vaccine co-administered with IL-12 expression plasmid enhances CD8 SIV cellular immune responses in cynomolgus macaques. J. Med. Primatol.34(5–6), 262–270 (2005).
  • Kutzler MA, Robinson TM, Chattergoon MA et al. Coimmunization with an optimized IL-15 plasmid results in enhanced function and longevity of CD8 T cells that are partially independent of CD4 T cell help. J. Immunol.175(1), 112–123 (2005).
  • Tapia E, Perez-Jimenez E, Lopez-Fuertes L, Gonzalo R, Gherardi MM, Esteban M. The combination of DNA vectors expressing IL-12 + IL-18 elicits high protective immune response against cutaneous leishmaniasis after priming with DNA-p36/LACK and the cytokines, followed by a booster with a vaccinia virus recombinant expressing p36/LACK. Microbes Infect.5(2), 73–84 (2003).
  • Barouch DH, McKay PF, Sumida SM et al. Plasmid chemokines and colony-stimulating factors enhance the immunogenicity of DNA priming-viral vector boosting human immunodeficiency virus type 1 vaccines. J. Virol.77(16), 8729–8735 (2003).
  • Song S, Liu C, Wang J et al. Vaccination with combination of Fit3L and RANTES in a DNA prime–protein boost regimen elicits strong cell-mediated immunity and antitumor effect. Vaccine27(7), 1111–1118 (2009).
  • Liu J, Yu Q, Stone GW et al. CD40L expressed from the canarypox vector, ALVAC, can boost immunogenicity of HIV-1 canarypox vaccine in mice and enhance the in vitro expansion of viral specific CD8+ T cell memory responses from HIV-1-infected and HIV-1-uninfected individuals. Vaccine26(32), 4062–4072 (2008).
  • Harrison JM, Bertram EM, Boyle DB, Coupar BE, Ranasinghe C, Ramshaw IA. 4–1BBL coexpression enhances HIV-specific CD8 T cell memory in a poxvirus prime–boost vaccine. Vaccine24(47–48), 6867–6874 (2006).
  • Boyer JD, Cohen AD, Ugen KE et al. Therapeutic immunisation of HIV-infected chimpanzees using HIV-1 plasmid antigens and interleukin-12 expressing plasmids. AIDS14(11), 1515–1522 (2000).
  • Demberg T, Boyer JD, Malkevich N et al. Sequential priming with simian immunodeficiency virus (SIV) DNA vaccines, with or without encoded cytokines, and a replicating adenovirus-SIV recombinant followed by protein boosting does not control a pathogenic SIVmac251 mucosal challenge. J. Virol.82(21), 10911–10921 (2008).
  • O’Neill E, Martinez I, Villinger F et al. Protection by SIV VLP DNA prime/protein boost following mucosal SIV challenge is markedly enhanced by IL-12/GM-CSF co-administration. J. Med. Primatol.31(4–5), 217–227 (2002).
  • Ranasinghe C, Turner SJ, McArthur C et al. Mucosal HIV-1 pox virus prime–boost immunization induces high-avidity CD8+ T cells with regime-dependent cytokine/granzyme B profiles. J. Immunol.178(4), 2370–2379 (2007).
  • Emery S, Kelleher AD, Workman C et al. Influence of IFN-γ co-expression on the safety and antiviral efficacy of recombinant fowlpox virus HIV therapeutic vaccines following interruption of antiretroviral therapy. Hum. Vaccin.3(6), 260–267 (2007).
  • Rowland-Jones SL, Pinheiro S, Kaul R et al. How important is the ‘quality’ of the cytotoxic T lymphocyte (CTL) response in protection against HIV infection? Immunol. Lett.79, 15–20 (2001).
  • Belyakov IM, Kuznetsov VA, Kelsall B et al. Impact of vaccine-induced mucosal high-avidity CD8+ CTLs in delay of AIDS viral dissemination from mucosa. Blood107(8), 3258–3264 (2006).
  • Belyakov IM, Isakov D, Zhu Q, Dzutsev A, Berzofsky JA. A novel functional CTL avidity/activity compartmentalization to the site of mucosal immunization contributes to protection of macaques against simian/human immunodeficiency viral depletion of mucosal CD4+ T cells. J. Immunol.178(11), 7211–7221 (2007).
  • Alexander-Miller MA, Leggatt GR, Sarin A, Berzofsky JA. Role of antigen, CD8, and cytotoxic T lymphocyte (CTL) avidity in high dose antigen induction of apoptosis of effector CTL. J. Exp. Med.184(2), 485–492 (1996).
  • 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).
  • Yee C, Savage PA, Lee PP, Davis MM, Greenberg PD. Isolation of high avidity melanoma-reactive CTL from heterogeneous populations using peptide–MHC tetramers. J. Immunol.162(4), 2227–2234 (1999).
  • Derby M, Alexander-Miller M, Tse R, Berzofsky J. High-avidity CTL exploit two complementary mechanisms to provide better protection against viral infection than low-avidity CTL. J. Immunol.166(3), 1690–1697 (2001).
  • Alexander-Miller MA. High-avidity CD8+ T cells: optimal soldiers in the war against viruses and tumors. Immunol. Res.31(1), 13–24 (2005).
  • Alexander-Miller MA. Differential expansion and survival of high and low avidity cytotoxic T cell populations during the immune response to a viral infection. Cell Immunol.201(1), 58–62 (2000).
  • Yoshizawa I, Soda Y, Mizuochi T. Enhancement of mucosal immune responses against HIV-1 gag by DNA immunization. Vaccine19, 2995–3003 (2001).
  • Bullock TN, Mullins DW, Engelhard VH. Antigen density presented by dendritic cells in vivo differentially affects the number and avidity of primary, memory, and recall CD8+ T cells. J. Immunol.170(4), 1822–1829 (2003).
  • Gray PM, Parks GD, Alexander-Miller MA. Modulation of CD8+ T cell avidity by increasing the turnover of viral antigen during infection. Cell. Immunol.231(1–2), 14–19 (2004).
  • Estcourt MJ, Ramsay AJ, Brooks A, Thomson SA, Medveckzy CJ, Ramshaw IA. Prime-boost immunization generates a high frequency, high-avidity CD8+ cytotoxic T lymphocyte population. Int. Immunol.14(1), 31–37 (2002).
  • Masopust D, Vezys V, Wherry EJ, Barber DL, Ahmed R. Cutting edge: gut microenvironment promotes differentiation of a unique memory CD8 T cell population. J. Immunol.176(4), 2079–2083 (2006).
  • Kiyono H, Fukuyama S. NALT- versus Peyer’s-patch mediated mucosal immunity. Nat. Immunol.4, 699–710 (2004).
  • Ranasinghe C, Ramshaw IA. Immunisation route dependent expression of IL-4/IL-13 can modulate HIV-specific CD8+ CTL avidity. Eur. J. Immunol.39(7), 1819–1830 (2009).
  • Kienzle N, Baz A, Kelso A. Profiling the CD8low phenotype, an alternative career choice for CD8 T cells during primary differentiation. Immunol. Cell Biol.82(1), 75–83 (2004).
  • Maggi E, Giudizi MG, Biagiotti R et al. Th2-like CD8+ T cells showing B cell helper function and reduced cytolytic activity in human immunodeficiency virus type 1 infection. J. Exp. Med.180(2), 489–495 (1994).
  • Imrie A, Meeks J, Gurary A et al. Differential functional avidity of dengue virus-specific T-cell clones for variant peptides representing heterologous and previously encountered serotypes. J. Virol.81(18), 10081–10091 (2007).
  • Ahlers JD, Belyakov IM, Terabe M et al. A push-pull approach to maximize vaccine efficacy: abrogating suppression with an IL-13 inhibitor while augmenting help with granulocyte/macrophage colony-stimulating factor and CD40L. Proc. Natl Acad. Sci. USA99(20), 13020–13025 (2002).

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.