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Review

Innate immune recognition of poxviral vaccine vectors

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Pages 1435-1449 | Published online: 09 Jan 2014

References

  • Pastoret PP, Vanderplasschen A. Poxviruses as vaccine vectors. Comp. Immunol. Microbiol. Infect. Dis.26(5–6), 343–355 (2003).
  • Carroll MW, Moss B. Poxviruses as expression vectors. Curr. Opin. Biotechnol.8(5), 573–577 (1997).
  • Parrino J, Graham BS. Smallpox vaccines: past, present, and future. J. Allergy Clin. Immunol.118(6), 1320–1326 (2006).
  • Jacobs BL, Langland JO, Kibler KV et al. Vaccinia virus vaccines: past, present and future. Antivir. Ther.84(1), 1–13 (2009).
  • McKinney BA, Reif DM, Rock MT et al. Cytokine expression patterns associated with systemic adverse events following smallpox immunization. J. Infect. Dis.194(4), 444–453 (2006).
  • Gomez CE, Najera JL, Krupa M, Esteban M. The poxvirus vectors MVA and NYVAC as gene delivery systems for vaccination against infectious diseases and cancer. Curr. Gene Ther.8(2), 97–120 (2008).
  • Blanchard TJ, Alcami A, Andrea P, Smith GL. Modified vaccinia virus ankara undergoes limited replication in human cells and lacks several immunomodulatory proteins: implications for use as a human vaccine. J. Gen. Virol.79(5), 1159–1167 (1998).
  • Antoine G, Scheiflinger F, Dorner F, Falkner FG. The complete genomic sequence of the modified vaccinia ankara strain: comparison with other orthopoxviruses. Virology244(2), 365–396 (1998).
  • Mayr A. Smallpox vaccination and bioterrorism with pox viruses. Comp. Immunol. Microbiol. Infect. Dis.26(5–6), 423–430 (2003).
  • Dorrell L, Williams P, Suttill A et al. Safety and tolerability of recombinant modified vaccinia virus Ankara expressing an HIV-1 gag/multiepitope immunogen (MVA.HIVA) in HIV-1-infected persons receiving combination antiretroviral therapy. Vaccine25(17), 3277–3283 (2007).
  • Kennedy JS, Greenberg RN. IMVAMUNE®: modified vaccinia Ankara strain as an attenuated smallpox vaccine. Expert Rev. Vaccines8(1), 13–24 (2009).
  • Elkord E, Dangoor A, Burt DJ et al. Immune evasion mechanisms in colorectal cancer liver metastasis patients vaccinated with TroVax (MVA-5T4). Cancer Immunol. Immunother.58(10), 1657–1667 (2009).
  • Tartaglia J, Perkus ME, Taylor J et al. NYVAC: a highly attenuated strain of vaccinia virus. Virology188(1), 217–232 (1992).
  • Bart P-A, Goodall R, Barber T et al. EV01: a Phase I trial in healthy HIV negative volunteers to evaluate a clade C HIV vaccine, NYVAC-C undertaken by the EuroVacc Consortium. Vaccine26(25), 3153–3161 (2008).
  • Harari A, Bart P-A, Stöhr W et al. An HIV-1 clade C DNA prime, NYVAC boost vaccine regimen induces reliable, polyfunctional, and long-lasting T cell responses. J. Exp. Med.205(1), 63–77 (2008).
  • Ockenhouse CF, Sun PF, Lanar DE et al. Phase I/IIa safety, immunogenicity, and efficacy trial of NYVAC-Pf7, a pox-vectored, multiantigen, multistage vaccine candidate for Plasmodium falciparum malaria. J. Infect. Dis.177(6), 1664–1673 (1998).
  • Tulman ER, Afonso CL, Lu Z, Zsak L, Kutish GF, Rock DL. The genome of canarypox virus. J. Virol.78(1), 353–366 (2004).
  • Soboll G, Hussey SB, Minke JM et al. Onset and duration of immunity to equine influenza virus resulting from canarypox-vectored (ALVAC®) vaccination. Vet. Immunol. Immunopathol.135(1–2), 100–107 (2010).
  • Seino KK, Long MT, Gibbs EPJ et al. Comparative efficacies of three commercially available vaccines against West Nile Virus (WNV) in a short-duration challenge trial involving an equine WNV encephalitis model. Clin. Vaccine Immunol.14(11), 1465–1471 (2007).
  • Larson LJ, Schultz RD. Three-year duration of immunity in dogs vaccinated with a canarypox-vectored recombinant canine distemper virus vaccine. Vet. Ther.8(2), 101–106 (2007).
  • Taylor J, Tartaglia J, Riviere M et al. Applications of canarypox (ALVAC) vectors in human and veterinary vaccination. Dev. Biol. Stand.82, 131–135 (1994).
  • Gilbert PB, Chiu YL, Allen M et al. Long-term safety analysis of preventive HIV-1 vaccines evaluated in AIDS vaccine evaluation group NIAID-sponsored Phase I and II clinical trials. Vaccine21(21–22), 2933–2947 (2003).
  • Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S et al. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N. Engl. J. Med.361(23), 2209–2220 (2009).
  • Gonczol E, Plotkin S. Development of a cytomegalovirus vaccine: lessons from recent clinical trials. Expert Opin. Biol. Ther.1(3), 401–412 (2001).
  • Tartaglia J, Bonnet M-C, Berinstein N, Barber B, Klein M, Moingeon P. Therapeutic vaccines against melanoma and colorectal cancer. Vaccine19(17–19), 2571–2575 (2001).
  • Boyle DB, Coupar BE. Construction of recombinant fowlpox viruses as vectors for poultry vaccines. Virus Res.10, 343–356 (1988).
  • Taylor J, Weinberg R, Kawaoka Y, Webster RG, Paoletti E. Protective immunity against avian influenza induced by a fowlpox virus recombinant. Vaccine6(6), 504–508 (1988).
  • Taylor J, Edbauer C, Rey-Senelonge A et al. Newcastle disease virus fusion protein expressed in a fowlpox virus recombinant confers protection in chickens. J. Virol.64(4), 1441–1450 (1990).
  • Baxby D, Paoletti E. Potential use of non-replicating vectors as recombinant vaccines. Vaccine10(1), 8–9 (1992).
  • Taylor J, Weinberg R, Languet B, Desmettre P, Paoletti E. Recombinant fowlpox virus inducing protective immunity in non-avian species. Vaccine6, 497–503 (1988).
  • Beard CW, Schnitzlein WM, Tripathy DN. Protection of chickens against highly pathogenic avian influenza virus (H5N2) by recombinant fowlpox viruses. Avian Dis.35(2), 356–359 (1991).
  • Emery S, Kelleher AD, Workman C et al. Influence of IFNγ 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).
  • Emery S, Workman C, Puls RL et al. Randomized, placebo-controlled, Phase I/IIa evaluation of the safety and immunogenicity of fowlpox virus expressing HIV gag-pol and interferon-γ in HIV-1 infected subjects. Hum. Vaccin.1(6), 232–238 (2005).
  • Zhu J, Martinez J, Huang X, Yang Y. Innate immunity against vaccinia virus is mediated by TLR2 and requires TLR-independent production of IFN-β. Blood109(2), 619–625 (2007).
  • Barbalat R, Lau L, Locksley RM, Barton GM. Toll-like receptor 2 on inflammatory monocytes induces type I interferon in response to viral but not bacterial ligands. Nat. Immunol.10(11), 1200–1207 (2009).
  • Sutherland DB, Ranasinghe C, Regner M et al. Evaluating vaccinia virus cytokine co-expression in TLR GKO mice. Immunol. Cell Biol.89, 706–715 (2010).
  • Quigley M, Martinez J, Huang X, Yang Y. A critical role for direct TLR2–MyD88 signaling in CD8 T-cell clonal expansion and memory formation following vaccinia viral infection. Blood113(10), 2256–2264 (2009).
  • Zhao Y, De Trez C, Flynn R, Ware CF, Croft M, Salek-Ardakani S. The adaptor molecule MyD88 directly promotes CD8 T cell responses to vaccinia virus. J. Immunol.182(10), 6278–6286 (2009).
  • Martinez J, Huang X, Yang Y. Direct TLR2 signaling is critical for NK cell activation and function in response to vaccinia viral infection. PLoS Pathog.6(3), e1000811 (2010).
  • Takeuchi O, Hoshino K, Kawai T et al. Differential roles of TLR2 and TLR4 in recognition of Gram-negative and Gram-positive bacterial cell wall components. Immunity11, 443–451 (1999).
  • Huang B, Sikorski R, Kirn DH, Thorne SH. Synergistic anti-tumor effects between oncolytic vaccinia virus and paclitaxel are mediated by the IFN response and HMGB1. Gene Ther.18(2), 164–172 (2010).
  • Bianchi ME. HMGB1 loves company. J. Leukoc. Biol.86, 573–576 (2009).
  • Hutchens M, Luker KE, Sottile P et al. TLR3 increases disease morbidity and mortality from vaccinia infection. J. Immunol.180(1), 483–491 (2008).
  • Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med.10(12), 1366–1373 (2004).
  • Gowen BB, Hoopes JD, Wong MH et al. TLR3 deletion limits mortality and disease severity due to Phlebovirus infection. J. Immunol.177(9), 6301–6307 (2006).
  • Le Goffic R, Balloy V, Lagranderie M et al. Detrimental contribution of the Toll-like receptor (TLR)3 to influenza A virus-induced acute pneumonia. PLoS Pathog.2(6), e53 (2006).
  • Martinez J, Huang X, Yang Y. Toll-like receptor 8-mediated activation of murine plasmacytoid dendritic cells by vaccinia viral DNA. Proc. Natl Acad. Sci. USA107(14), 6442–6447 (2010).
  • Lysakova-Devine T, Keogh B, Harrington B et al. Viral inhibitory peptide of TLR4, a peptide derived from vaccinia protein A46, specifically inhibits TLR4 by directly targeting MyD88 adaptor-like and TRIF-related adaptor molecule. J. Immunol.185(7), 4261–4271 (2010).
  • Hornung V, Ablasser A, Charrel-Dennis M et al. AIM2 recognizes cytosolic dsDNA and forms a caspase-1-activating inflammasome with ASC. Nature458(7237), 514–518 (2009).
  • Chisholm SE, Reyburn HT. Recognition of vaccinia virus-infected cells by human natural killer cells depends on natural cytotoxicity receptors. J. Virol.80(5), 2225–2233 (2006).
  • Brooks CR, Elliott T, Parham P, Khakoo SI. The inhibitory receptor NKG2A determines lysis of vaccinia virus-infected autologous targets by NK cells. J. Immunol.176(2), 1141–1147 (2006).
  • Meisinger-Henschel C, Schmidt M, Lukassen S et al. Genomic sequence of chorioallantois vaccinia virus Ankara, the ancestor of modified vaccinia virus Ankara. J. Gen. Virol.88(Pt 12), 3249–3259 (2007).
  • Delaloye J, Roger T, Steiner-Tardivel Q-G et al. Innate immune sensing of modified vaccinia virus Ankara (MVA) is mediated by TLR2–TLR6, MDA-5 and the NALP3 inflammasome. PLoS Pathog.5(6), e1000480 (2009).
  • Waibler Z, Anzaghe M, Ludwig H et al. Modified vaccinia virus ankara induces Toll-like receptor-independent type I interferon responses. J. Virol.81(22), 12102–12110 (2007).
  • Myskiw C, Arsenio J, Booy EP et al. RNA species generated in vaccinia virus infected cells activate cell type-specific MDA5 or RIG-I dependent interferon gene transcription and PKR dependent apoptosis. Virology413(2), 183–193 (2011).
  • Samuelsson C, Hausmann J, Lauterbach H et al. Survival of lethal poxvirus infection in mice depends on TLR9, and therapeutic vaccination provides protection. J. Clin. Invest.118(5), 1776–1784 (2008).
  • Lousberg EL, Diener KR, Fraser CK et al. Antigen-specific T-cell responses to a recombinant fowlpox virus are dependent on MyD88 and interleukin-18 and independent of Toll-like receptor 7 (TLR7)- and TLR9-mediated innate immune recognition. J. Virol.85(7), 3385–3396 (2011).
  • Harenberg A, Guillaume F, Ryan EJ, Burdin N, Spada F. Gene profiling analysis of ALVAC infected human monocyte derived dendritic cells. Vaccine26(39), 5004–5013 (2008).
  • Stack J, Haga IR, Schroder M et al. Vaccinia virus protein A46R targets multiple Toll-like-interleukin-1 receptor adaptors and contributes to virulence. J. Exp. Med.201(6), 1007–1018 (2005).
  • Bowie A, Kiss-Toth E, Symons JA, Smith GL, Dower SK, O’Neill LAJ. A46R and A52R from vaccinia virus are antagonists of host IL-1 and toll-like receptor signaling. Proc. Natl Acad. Sci. USA97(18), 10162–10167 (2000).
  • Harte MT, Haga IR, Maloney G et al. The poxvirus protein A52R targets Toll-like receptor signaling complexes to suppress host defense. J. Exp. Med.197(3), 343–351 (2003).
  • Gedey R, Jin XL, Hinthong O, Shisler JL. Poxviral regulation of the host NF-κB response: the vaccinia virus M2L protein inhibits induction of NF-κB activation via an ERK2 pathway in virus-infected human embryonic kidney cells. J. Virol.80(17), 8676–8685 (2006).
  • Deng L, Dai P, Ding W, Granstein RD, Shuman S. Vaccinia virus infection attenuates innate immune responses and antigen presentation by epidermal dendritic cells. J. Virol.80(20), 9977–9987 (2006).
  • Jacobs N, Bartlett NW, Clark RH, Smith GL. Vaccinia virus lacking the Bcl-2-like protein N1 induces a stronger natural killer cell response to infection. J. Gen. Virol.89(11), 2877–2881 (2008).
  • Lynch HE, Ray CA, Oie KL et al. Modified vaccinia virus ankara can activate NFκB transcription factors through a double-stranded RNA-activated protein kinase (PKR)-dependent pathway during the early phase of virus replication. Virology391(2), 177–186 (2009).
  • DiPerna G, Stack J, Bowie AG et al. Poxvirus protein N1L targets the IκB kinase complex, inhibits signaling to NF-κB by the tumor necrosis factor superfamily of receptors, and inhibits NF-κB and IRF3 signaling by Toll-like receptors. J. Biol. Chem.279(35), 36570–36578 (2004).
  • Tovey MG, Lallemand C, Thyphronitis G. Adjuvant activity of type I interferons. Biol. Chem.389(5), 541–545 (2008).
  • Alsharifi M, Lobigs M, Regner M, Lee E, Koskinen A, Mullbacher A. Type I interferons trigger systemic, partial lymphocyte activation in response to viral infection. J. Immunol.175(7), 4635–4640 (2005).
  • Samuel CE. Antiviral actions of interferons. Clin. Microbiol. Rev.14(4), 778–809 (2001).
  • Alsharifi M, Mullbacher A, Regner M. Interferon type I responses in primary and secondary infections. Immunol. Cell Biol.86, 239–245 (2008).
  • Hance KW, Rogers CJ, Zaharoff DA, Canter D, Schlom J, Greiner JW. The antitumor and immunoadjuvant effects of IFN-α in combination with recombinant poxvirus vaccines. Clin. Cancer Res.15(7), 2387–2396 (2009).
  • Fitzgerald-Bocarsly P, Feng D. The role of type I interferon production by dendritic cells in host defense. Biochimie89, 843–855 (2007).
  • Lousberg EL, Fraser CK, Tovey MG, Diener KR, Hayball JD. Type I interferons mediate the innate cytokine response to recombinant fowlpox virus but not the induction of plasmacytoid dendritic cell-dependent adaptive immunity. J. Virol.84(13), 6549–6563 (2010).
  • Quakkelaar ED, Redeker A, Haddad EK et al. Improved innate and adaptive immunostimulation by genetically modified HIV-1 protein expressing NYVAC vectors. PLoS ONE6(2), e16819 (2011).
  • Symons JA, Alcami A, Smith GL. Vaccinia virus encodes a soluble type I interferon receptor of novel structure and broad species specificity. Cell81(4), 551–560 (1995).
  • Waibler Z, Anzaghe M, Frenz T et al. Vaccinia virus-mediated inhibition of type I interferon responses is a multi-factorial process involving the soluble type I interfreon receptor B18 and intracellular components. J. Virol.83(4), 1563–1571 (2009).
  • Day SL, Ramshaw IA, Ramsay AJ, Ranasinghe C. Differential effects of the type I interferons α4, β, and ε on antiviral activity and vaccine efficacy. J. Immunol.180(11), 7158–7166 (2008).
  • Beattie E, Denzler KL, Tartaglia J, Perkus ME, Paoletti E, Jacobs BL. Reversal of the interferon-sensitive phenotype of a vaccinia virus lacking E3L by expression of the reovirus S4 gene. J. Virol.69(1), 499–505 (1995).
  • Beattie E, Paoletti E, Tartaglia J. Distinct patterns of IFN sensitivity observed in cells infected with vaccinia K3L- and E3L- mutant viruses. Virology210(2), 254–263 (1995).
  • Arsenio J, Deschambault Y, Cao J. Antagonizing activity of vaccinia virus E3L against human interferons in Huh7 cells. Virology377(1), 124–132 (2008).
  • Xiang Y, Condit RC, Vijaysri S, Jacobs B, Williams BRG, Silverman RH. Blockade of interferon induction and action by the E3L double-stranded RNA binding proteins of vaccinia virus. J. Virol.76(10), 5251–5259 (2002).
  • Beattie E, Tartaglia J, Paoletti E. Vaccinia virus-encoded elF-2α homolog abrogates the antiviral effect of interferon. Virology183(1), 419–422 (1991).
  • Mann BA, Huang JH, Li P et al. Vaccinia virus blocks Stat1-dependent and Stat1-independent gene expression induced by type I and type II interferons. J. Interferon Cytokine Res.28(6), 367–380 (2008).
  • Banadyga L, Veugelers K, Campbell S, Barry M. The fowlpox virus Bcl-2 homologue, FPV039, interacts with activated Bax and a discrete subset of BH3-only proteins to inhibit apoptosis. J. Virol.83(14), 7085–7098 (2009).
  • Banadyga L, Gerig J, Stewart T, Barry M. Fowlpox virus encodes a Bcl-2 homologue that protects cells from apoptotic death through interaction with the proapoptotic protein Bak. J. Virol.81(20), 11032–11045 (2007).
  • Huang J, Huang Q, Zhou X et al. The poxvirus p28 virulence factor is an E3 ubiquitin ligase. J. Biol. Chem.279(52), 54110–54116 (2004).
  • Brick DJ, Burke RD, Schiff L, Upton C. Shope fibroma virus RING finger protein N1R binds DNA and inhibits apoptosis. Virology249(1), 42–51 (1998).
  • Jesenberger V, Jentsch S. Deadly encounter: ubiquitin meets apoptosis. Nat. Rev. Mol. Cell Biol.3(2), 112–121 (2002).
  • Cooray S, Bahar MW, Abrescia NGA et al. Functional and structural studies of the vaccinia virus virulence factor N1 reveal a Bcl-2-like anti-apoptotic protein. J. Gen. Virol.88(6), 1656–1666 (2007).
  • Wasilenko ST, Banadyga L, Bond D, Barry M. The vaccinia virus F1L protein interacts with the proapoptotic protein Bak and inhibits Bak activation. J. Virol.79(22), 14031–14043 (2005).
  • Campbell S, Hazes B, Kvansakul M, Colman P, Barry M. Vaccinia virus F1L interacts with Bak using highly divergent Bcl-2 homology domains and replaces the function of Mcl-1. J. Biol. Chem.285(7), 4695–4708 (2010).
  • Fischer SF, Ludwig H, Holzapfel J et al. Modified vaccinia virus Ankara protein F1L is a novel BH3-domain-binding protein and acts together with the early viral protein E3L to block virus-associated apoptosis. Cell Death Differentiation13(1), 109–118 (2005).
  • Heinkelein M, Pilz S, Jassoy C. Inhibition of CD95 (Fas/Apo1)-mediated apoptosis by vaccinia virus WR. Clin. Exp. Immunol.103(1), 8–14 (1996).
  • Billiau A, Matthys P. Interferon-γ: a historical perspective. Cytokine Growth Factor Rev.20(2), 97–113 (2009).
  • Puehler F, Schwarz H, Waidner B et al. An interferon-γ-binding protein of novel structure encoded by the fowlpox virus. J. Biol. Chem.278(9), 6905–6911 (2003).
  • Verardi PH, Jones LA, Aziz FH, Ahmad S, Yilma TD. Vaccinia virus vectors with an inactivated γ interferon receptor homolog gene (B8R) are attenuated in vivo without a concomitant reduction in immunogenicity. J. Virol.75(1), 11–18 (2001).
  • Mossman K, Upton C, Buller RML, McFadden G. Species specificity of ectromelia virus and vaccinia virus interferon-γ binding proteins. Virology208(2), 762–769 (1995).
  • Lalani AS, McFadden G. Secreted poxvirus chemokine binding proteins. J. Leukoc. Biol.62(5), 570–576 (1997).
  • Afonso CL, Tulman ER, Lu Z et al. The genome of swinepox virus. J. Virol.76(2), 783–790 (2002).
  • Sakala IG, Chaudhri G, Buller RM et al. Poxvirus-encoded gamma interferon binding protein dampens the host immune response to infection. J. Virol.81(7), 3346–3353 (2007).
  • Shi X-M, Zhao Y, Gao H-B et al. Evaluation of recombinant fowlpox virus expressing infectious bronchitis virus S1 gene and chicken interferon-γ gene for immune protection against heterologous strains. Vaccine29(8), 1576–1582 (2011).
  • Franchi L, Munoz-Planillo R, Reimer T, Eigenbrod T, Nunez G. Inflammasomes as microbial sensors. Eur. J. Immunol.40(3), 611–615 (2010).
  • Alcami A, Smith GL. A soluble receptor for interleukin-1β encoded by vaccinia virus: a novel mechanism of virus modulation of the host response to infection. Cell71(1), 153–167 (1992).
  • Alcami A, Smith GL. A mechanism for the inhibition of fever by a virus. Proc. Natl Acad. Sci. USA93, 11029–11034 (1996).
  • Staib C, Kisling S, Erfle V, Sutter G. Inactivation of the viral interleukin 1β receptor improves CD8+ T-cell memory responses elicited upon immunization with modified vaccinia virus Ankara. J. Gen. Virol.86(7), 1997–2006 (2005).
  • Afonso C, Tulman E, Lu Z, Zsak L, Kutish G, Rock D. The genome of fowlpox virus. J. Virol.74(8), 3815–3831 (2000).
  • Reading PC, Smith GL. Vaccinia virus interleukin-18-binding protein promotes virulence by reducing gamma interferon production and natural killer and T-cell activity. J. Virol.77(18), 9960–9968 (2003).
  • Smith VP, Bryant NA, Alcami A. Ectromelia, vaccinia and cowpox viruses encode secreted interleukin-18-binding proteins. J. Gen. Virol.81(5), 1223–1230 (2000).
  • Johnston JB, Barrett JW, Nazarian SH et al. A poxvirus-encoded pyrin domain protein interacts with ASC-1 to inhibit host inflammatory and apoptotic responses to infection. Immunity23(6), 587–598 (2005).
  • Rahman MM, Mohamed MR, Kim M, Smallwood S, McFadden G. Co-regulation of NF-κB and inflammasome-mediated inflammatory responses by Myxoma virus pyrin domain-containing protein M013. PLoS Pathog.5(10), e1000635 (2009).
  • Sanchez-Puig J, Sanchez L, Roy G, Blasco R. Susceptibility of different leukocyte cell types to Vaccinia virus infection. Virol. J.1(1), 10 (2004).
  • Yu Q, Hu N, Ostrowski M. Poxvirus tropism for primary human leukocytes and hematopoietic cells. In: Viral Applications of Green Fluorescent Protein. Humana Press, NY, USA, 309–328 (2009).
  • Jenne L, Hauser C, Arrighi JF, Saurat JH, Hugin AW. Poxvirus as a vector to transduce human dendritic cells for immunotherapy: abortive infection but reduced APC function. Gene Ther.7, 1575–1583 (2000).
  • Engelmayer J, Larsson M, Subklewe M et al. Vaccinia virus inhibits the maturation of human dendritic cells: a novel mechanism of immune evasion. J. Immunol.163, 6762–6768 (1999).
  • Walzer T, Galibert L, De Smedt T. Poxvirus semaphorin A39R inhibits phagocytosis by dendritic cells and neutrophils. Eur. J. Immunol.35(2), 391–398 (2005).
  • Humrich JY, Thumann P, Greiner S et al. Vaccinia virus impairs directional migration and chemokine receptor switch of human dendritic cells. Eur. J. Immunol.37(4), 954–965 (2007).
  • Chahroudi A, Garber DA, Reeves P, Liu L, Kalman D, Feinberg MB. Differences and similarities in viral life cycle progression and host cell physiology after infection of human dendritic cells with modified vaccinia virus Ankara and Vaccinia virus. J. Virol.80(17), 8469–8481 (2006).
  • Liu L, Chavan R, Feinberg M. Dendritic cells are preferentially targeted among hematolymphocytes by modified vaccinia virus ankara and play a key role in the induction of virus-specific T cell responses in vivo. BMC Immunol.9(1), 15 (2008).
  • Yao Y, Li P, Singh P et al. Vaccinia virus infection induces dendritic cell maturation but inhibits antigen presentation by MHC class II. Cell Immunol.246(2), 92–102 (2007).
  • Drillien R, Spehner D, Hanau D. Modified vaccinia virus Ankara induces moderate activation of human dendritic cells. J. Gen. Virol.85(8), 2167–2175 (2004).
  • Agrawal S, Gupta S, Agrawal A. Vaccinia virus proteins activate human dendritic cells to induce T cell responses in vitro. Vaccine27(1), 88–92 (2009).
  • Berthoud TK, Fletcher H, Porter D, Thompson F, Hill AVS, Todryk SM. Comparing human T cell and NK cell responses in viral-based malaria vaccine trials. Vaccine28(1), 21–27 (2009).
  • Diener KR, Lousberg EL, Beukema EL et al. Recombinant fowlpox virus elicits transient cytotoxic T cell responses due to suboptimal innate recognition and recruitment of T cell help. Vaccine26(29–30), 3566–3573 (2008).
  • Ryan EJ, Harenberg A, Burdin N. The canarypox-virus vaccine vector ALVAC triggers the release of IFN-γ by natural killer (NK) cells enhancing Th1 polarization. Vaccine25(17), 3380–3390 (2007).
  • Trakatelli M, Toungouz M, Lambermont M, Heenen M, Velu T, Bruyns C. Immune characterization of clinical grade-dendritic cells generated from cancer patients and genetically modified by an ALVAC vector carrying MAGE minigenes. Cancer Gene Ther.12(6), 552–559 (2005).
  • Ilett EJ, Prestwich RJD, Melcher AA. The evolving role of dendritic cells in cancer therapy. Expert Opin. Biol. Ther.10(3), 369–379 (2010).
  • Gandhi RT, O’Neill D, Bosch RJ et al. A randomized therapeutic vaccine trial of canarypox–HIV-pulsed dendritic cells vs. canarypox-HIV alone in HIV-1-infected patients on antiretroviral therapy. Vaccine27(43), 6088–6094 (2009).
  • Engelmayer J, Larsson M, Lee A et al. Mature dendritic cells infected with canarypox virus elicit strong anti-human immunodeficiency virus CD8+ and CD4+ T-cell responses from chronically infected individuals. J. Virol.75(5), 2142–2153 (2001).
  • Emu B, Sinclair E, Favre D et al. Phenotypic,functional, and kinetic parameters associated with apparent T-cell control of human immunodeficiency virus replication in individuals with and without antiretroviral treatment. J. Virol.79(22), 14169–14178 (2005).
  • Friedrich TC, Valentine LE, Yant LJ et al. Subdominant CD8+ T-cell responses are involved in durable control of AIDS virus replication. J. Virol.81(7), 3465–3476 (2007).
  • Morse MA, Clay TM, Hobeika AC et al. Phase I study of immunisation with dendritic cells modified with fowlpox encoding carcinoembryonic antigen and costimulatory molecules. Clin. Cancer Res.11(8), 3017–3024 (2005).
  • Liu A, Guardino A, Chinsangaram L, Goldstein MJ, Panicali D, Levy R. Therapeutic vaccination against murine lymphoma by intratumoral injection of recombinant fowlpox virus encoding CD40 ligand. Cancer Res.67(14), 7037–7044 (2007).
  • 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).
  • Gómez CE, Nájera JL, Sánchez R, Jiménez V, Esteban M. Multimeric soluble CD40 ligand (sCD40L) efficiently enhances HIV specific cellular immune responses during DNA prime and boost with attenuated poxvirus vectors MVA and NYVAC expressing HIV antigens. Vaccine27(24), 3165–3174 (2009).
  • Belyakov IM, Isakov D, Zhu Q, Dzutsev A, Klinman D, Berzofsky JA. Enhancement of CD8+ T cell immunity in the lung by CpG oligodeoxynucleotides increases protective efficacy of a modified vaccinia ankara vaccine against lethal poxvirus infection even in a CD4-deficient host. J. Immunol.177(9), 6336–6343 (2006).
  • Kwissa M, Amara RR, Robinson HL et al. Adjuvanting a DNA vaccine with a TLR9 ligand plus Flt3 ligand results in enhanced cellular immunity against the Simian immunodeficiency virus. J. Exp. Med.204(11), 2733–2746 (2007).
  • Rees DGC, Gates AJ, Green M et al. CpG-DNA protects against a lethal orthopoxvirus infection in a murine model. Antiviral Res.65(2), 87–95 (2005).
  • Kass E, Parker J, Schlom J, Greiner JW. Compartive studies of the effects of recombinant GM-CSF and GM-CSF administered via a poxvirus to enhance the concentration of antigen-presenting cells in the regional lymph nodes. Cytokine12(7), 960–971 (2000).
  • Chavan R, Marfatia KA, An IC, Garber DA, Feinberg MB. Expression of CCL20 and granulocyte–macrophage colony-stimulating factor, but not Flt3-L, from modified vaccinia virus ankara enhances antiviral cellular and humoral immune responses. J. Virol.80(15), 7676–7687 (2006).
  • Kass E, Panicali DL, Mazzara G, Schlom J, Greiner JW. Granulocyte/macrophage-colony stimulating factor produced by recombinant avian poxviruses enriches the regional lymph nodes with antigen-presenting cells and acts as an immunoadjuvant. Cancer Res.61(1), 206–214 (2001).
  • Reali E, Canter D, Zeytin H, Schlom J, Greiner JW. Comparative studies of avipox-GM-CSF versus recombinant GM-CSF protein as immune adjuvants with different vaccine platforms. Vaccine23(22), 2909–2921 (2005).
  • Marshall JL, Gulley JL, Arlen PM et al. Phase I study of sequential vaccinations with fowlpox-CEA(6D)-TRICOM alone and sequentially with vaccinia-CEA(6D)-TRICOM, with and without granulocyte–macrophage colony-stimulating factor, in patients with carcinoembryonic antigen-expressing carcinomas. J. Clin. Oncol.23(4), 720–731 (2005).
  • Hofbauer GF, Baur T, Bonnet MC et al. Clinical Phase I intratumoral administration of two recombinant ALVAC canarypox viruses expressing human granulocyte–macrophage colony-stimulating factor or interleukin-2: the transgene determines the composition of the inflammatory infiltrate. Melanoma Res.18(2), 104–111 (2008).
  • Abaitua F, Rodríguez JR, Garzón A, Rodríguez D, Esteban M. Improving recombinant MVA immune responses: potentiation of the immune responses to HIV-1 with MVA and DNA vectors expressing Env and the cytokines IL-12 and IFN-γ. Virus Res.116(1–2), 11–20 (2006).
  • Ahmed CM, Martin JP, Johnson HM. IFN mimetic as a therapeutic for lethal vaccinia virus infection: possible effects on innate and adaptive immune responses. J. Immunol.178(7), 4576–4583 (2007).
  • Mingxiao M, Ningyi J, Zhenguo W et al. Construction and immunogenicity of recombinant fowlpox vaccines coexpressing HA of AIV H5N1 and chicken IL18. Vaccine24(20), 4304–4311 (2006).
  • Guoshun S, Ningyi J, Mingxiao M et al. Immune responses of pigs inoculated with a recombinant fowlpox virus coexpressing GP5/GP3 of porcine reproductive and respiratory syndrome virus and swine IL-18. Vaccine25(21), 4193–4202 (2007).
  • Gherardi MM, Ramirez JC, Esteban M. IL-12 and IL-18 act in synergy to clear vaccinia virus infection: involvement of innate and adaptive components of the immune system. J. Gen. Virol.84(8), 1961–1972 (2003).
  • Perera P-Y, Derrick SC, Kolibab K et al. A multi-valent vaccinia virus-based tuberculosis vaccine molecularly adjuvanted with interleukin-15 induces robust immune responses in mice. Vaccine27(15), 2121–2127 (2009).
  • Poon LLM, Leung YHC, Nicholls JM et al. Vaccinia virus-based multivalent H5N1 avian influenza vaccines adjuvanted with IL-15 confer sterile cross-clade protection in mice. J. Immunol.182(5), 3063–3071 (2009).
  • Foong YY, Jans DA, Rolph MS, Gahan ME, Mahalingam S. Interleukin-15 mediates potent antiviral responses via an interferon-dependent mechanism. Virology393(2), 228–237 (2009).
  • Boudet F, Chevalier M, Jourdier TM, Tartaglia J, Moste C. Modulation of the antibody response to the HIV envelope subunit by co-administration of infectious or heat-inactivated canarypoxvirus (ALVAC) preparations. Vaccine19(30), 4267–4275 (2001).
  • Franchini M, Hefti H, Vollstedt S et al. Dendritic cells from mice neonatally vaccinated with modified vaccinia virus ankara transfer resistance against herpes simplex virus type I to naive one-week-old mice. J. Immunol.172(10), 6304–6312 (2004).

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