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Research Paper

DNA vaccine prime followed by boost with live attenuated virus significantly improves antigen-specific T cell responses against human cytomegalovirus

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Pages 2120-2132 | Received 30 May 2013, Accepted 14 Jul 2013, Published online: 25 Jul 2013

References

  • Crough T, Khanna R. Immunobiology of human cytomegalovirus: from bench to bedside. Clin Microbiol Rev 2009; 22:76 - 98; http://dx.doi.org/10.1128/CMR.00034-08; PMID: 19136435
  • Whitley RJ. Congenital cytomegalovirus infection: epidemiology and treatment. Adv Exp Med Biol 2004; 549:155 - 60; http://dx.doi.org/10.1007/978-1-4419-8993-2_21; PMID: 15250528
  • Stratton K, Kurch J, Lawrence R. Vaccine for the 21st Century: a tool for decision making. Washington, D.C.: National Academy Press, 2000.
  • Plotkin SA, Starr SE, Friedman HM, Brayman K, Harris S, Jackson S, et al. Effect of Towne live virus vaccine on cytomegalovirus disease after renal transplant. A controlled trial. Ann Intern Med 1991; 114:525 - 31; http://dx.doi.org/10.7326/0003-4819-114-7-525; PMID: 1848053
  • Heineman TC, Schleiss M, Bernstein DI, Spaete RR, Yan L, Duke G, et al. A phase 1 study of 4 live, recombinant human cytomegalovirus Towne/Toledo chimeric vaccines. J Infect Dis 2006; 193:1350 - 60; http://dx.doi.org/10.1086/503365; PMID: 16619181
  • Pass RF, Zhang C, Evans A, Simpson T, Andrews W, Huang M-L, et al. Vaccine prevention of maternal cytomegalovirus infection. N Engl J Med 2009; 360:1191 - 9; http://dx.doi.org/10.1056/NEJMoa0804749; PMID: 19297572
  • Abel K, Martinez J, Yue Y, Lacey SF, Wang Z, Strelow L, et al. Vaccine-induced control of viral shedding following rhesus cytomegalovirus challenge in rhesus macaques. J Virol 2011; 85:2878 - 90; http://dx.doi.org/10.1128/JVI.00883-10; PMID: 21191005
  • Wussow F, Yue Y, Martinez J, Deere JD, Longmate J, Herrmann A, et al. A vaccine based on the rhesus cytomegalovirus UL128 complex induces broadly neutralizing antibodies in rhesus macaques. J Virol 2013; 87:1322 - 32; http://dx.doi.org/10.1128/JVI.01669-12; PMID: 23152525
  • Gibson L, Piccinini G, Lilleri D, Revello MG, Wang Z, Markel S, et al. Human cytomegalovirus proteins pp65 and immediate early protein 1 are common targets for CD8+ T cell responses in children with congenital or postnatal human cytomegalovirus infection. J Immunol 2004; 172:2256 - 64; PMID: 14764694
  • Sylwester AW, Mitchell BL, Edgar JB, Taormina C, Pelte C, Ruchti F, et al. Broadly targeted human cytomegalovirus-specific CD4+ and CD8+ T cells dominate the memory compartments of exposed subjects. J Exp Med 2005; 202:673 - 85; http://dx.doi.org/10.1084/jem.20050882; PMID: 16147978
  • Berencsi K, Gyulai Z, Gönczöl E, Pincus S, Cox WI, Michelson S, et al. A canarypox vector-expressing cytomegalovirus (CMV) phosphoprotein 65 induces long-lasting cytotoxic T cell responses in human CMV-seronegative subjects. J Infect Dis 2001; 183:1171 - 9; http://dx.doi.org/10.1086/319680; PMID: 11262198
  • Bernstein DI, Reap EA, Katen K, Watson A, Smith K, Norberg P, et al. Randomized, double-blind, Phase 1 trial of an alphavirus replicon vaccine for cytomegalovirus in CMV seronegative adult volunteers. Vaccine 2009; 28:484 - 93; http://dx.doi.org/10.1016/j.vaccine.2009.09.135; PMID: 19857446
  • Seder RA, Darrah PA, Roederer M. T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 2008; 8:247 - 58; http://dx.doi.org/10.1038/nri2274; PMID: 18323851
  • Donnelly JJ, Ulmer JB, Shiver JW, Liu MA. DNA vaccines. Annu Rev Immunol 1997; 15:617 - 48; http://dx.doi.org/10.1146/annurev.immunol.15.1.617; PMID: 9143702
  • Ramshaw IA, Ramsay AJ. The prime-boost strategy: exciting prospects for improved vaccination. Immunol Today 2000; 21:163 - 5; http://dx.doi.org/10.1016/S0167-5699(00)01612-1; PMID: 10740236
  • Schneider J, Gilbert SC, Hannan CM, Dégano P, Prieur E, Sheu EG, et al. Induction of CD8+ T cells using heterologous prime-boost immunisation strategies. Immunol Rev 1999; 170:29 - 38; http://dx.doi.org/10.1111/j.1600-065X.1999.tb01326.x; PMID: 10566139
  • Lu S. Heterologous prime-boost vaccination. Curr Opin Immunol 2009; 21:346 - 51; http://dx.doi.org/10.1016/j.coi.2009.05.016; PMID: 19500964
  • 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 2002; 14:31 - 7; http://dx.doi.org/10.1093/intimm/14.1.31; PMID: 11751749
  • McShane H. Prime-boost immunization strategies for infectious diseases. Curr Opin Mol Ther 2002; 4:23 - 7; PMID: 11883691
  • Hu SL, Abrams K, Barber GN, Moran P, Zarling JM, Langlois AJ, et al. Protection of macaques against SIV infection by subunit vaccines of SIV envelope glycoprotein gp160. Science 1992; 255:456 - 9; http://dx.doi.org/10.1126/science.1531159; PMID: 1531159
  • Harari A, Bart PA, Stöhr W, Tapia G, Garcia M, Medjitna-Rais E, 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 2008; 205:63 - 77; http://dx.doi.org/10.1084/jem.20071331; PMID: 18195071
  • Dunachie SJ, Walther M, Epstein JE, Keating S, Berthoud T, Andrews L, et al. A DNA prime-modified vaccinia virus ankara boost vaccine encoding thrombospondin-related adhesion protein but not circumsporozoite protein partially protects healthy malaria-naive adults against Plasmodium falciparum sporozoite challenge. Infect Immun 2006; 74:5933 - 42; http://dx.doi.org/10.1128/IAI.00590-06; PMID: 16988273
  • Magalhaes I, Sizemore DR, Ahmed RK, Mueller S, Wehlin L, Scanga C, et al. rBCG induces strong antigen-specific T cell responses in rhesus macaques in a prime-boost setting with an adenovirus 35 tuberculosis vaccine vector. PLoS One 2008; 3:e3790; http://dx.doi.org/10.1371/journal.pone.0003790; PMID: 19023426
  • Biswas S, Reddy GS, Srinivasan VA, Rangarajan PN. Preexposure efficacy of a novel combination DNA and inactivated rabies virus vaccine. Hum Gene Ther 2001; 12:1917 - 22; http://dx.doi.org/10.1089/104303401753153965; PMID: 11589833
  • Xiao-wen H, Shu-han S, Zhen-lin H, Jun L, Lei J, Feng-juan Z, et al. Augmented humoral and cellular immune responses of a hepatitis B DNA vaccine encoding HBsAg by protein boosting. Vaccine 2005; 23:1649 - 56; http://dx.doi.org/10.1016/j.vaccine.2004.10.013; PMID: 15705468
  • Spaete RR, Saxena A, Scott PI, Song GJ, Probert WS, Britt WJ, et al. Sequence requirements for proteolytic processing of glycoprotein B of human cytomegalovirus strain Towne. J Virol 1990; 64:2922 - 31; PMID: 2159553
  • Wang S, Chou TH, Sakhatskyy PV, Huang S, Lawrence JM, Cao H, et al. Identification of two neutralizing regions on the severe acute respiratory syndrome coronavirus spike glycoprotein produced from the mammalian expression system. J Virol 2005; 79:1906 - 10; http://dx.doi.org/10.1128/JVI.79.3.1906-1910.2005; PMID: 15650214
  • Lu S, Wyatt R, Richmond JF, Mustafa F, Wang S, Weng J, et al. Immunogenicity of DNA vaccines expressing human immunodeficiency virus type 1 envelope glycoprotein with and without deletions in the V1/2 and V3 regions. AIDS Res Hum Retroviruses 1998; 14:151 - 5; http://dx.doi.org/10.1089/aid.1998.14.151; PMID: 9462925
  • Shen S, Wang S, Britt WJ, Lu S. DNA vaccines expressing glycoprotein complex II antigens gM and gN elicited neutralizing antibodies against multiple human cytomegalovirus (HCMV) isolates. Vaccine 2007; 25:3319 - 27; http://dx.doi.org/10.1016/j.vaccine.2007.01.011; PMID: 17287056
  • Gyulai Z, Endresz V, Burian K, Pincus S, Toldy J, Cox WI, et al. Cytotoxic T lymphocyte (CTL) responses to human cytomegalovirus pp65, IE1-Exon4, gB, pp150, and pp28 in healthy individuals: reevaluation of prevalence of IE1-specific CTLs. J Infect Dis 2000; 181:1537 - 46; http://dx.doi.org/10.1086/315445; PMID: 10823751
  • Bunde T, Kirchner A, Hoffmeister B, Habedank D, Hetzer R, Cherepnev G, et al. Protection from cytomegalovirus after transplantation is correlated with immediate early 1-specific CD8 T cells. J Exp Med 2005; 201:1031 - 6; http://dx.doi.org/10.1084/jem.20042384; PMID: 15795239
  • Britt WJ, Vugler LG, Butfiloski EJ, Stephens EB. Cell surface expression of human cytomegalovirus (HCMV) gp55-116 (gB): use of HCMV-recombinant vaccinia virus-infected cells in analysis of the human neutralizing antibody response. J Virol 1990; 64:1079 - 85; PMID: 2154594
  • Shimamura M, Mach M, Britt WJ. Human cytomegalovirus infection elicits a glycoprotein M (gM)/gN-specific virus-neutralizing antibody response. J Virol 2006; 80:4591 - 600; http://dx.doi.org/10.1128/JVI.80.9.4591-4600.2006; PMID: 16611919
  • Plotkin SA, Smiley ML, Friedman HM, Starr SE, Fleisher GR, Wlodaver C, et al. Towne-vaccine-induced prevention of cytomegalovirus disease after renal transplants. Lancet 1984; 1:528 - 30; http://dx.doi.org/10.1016/S0140-6736(84)90930-9; PMID: 6142252
  • Adler SP, Starr SE, Plotkin SA, Hempfling SH, Buis J, Manning ML, et al. Immunity induced by primary human cytomegalovirus infection protects against secondary infection among women of childbearing age. J Infect Dis 1995; 171:26 - 32; http://dx.doi.org/10.1093/infdis/171.1.26; PMID: 7798679
  • Jacobson MA, Sinclair E, Bredt B, Agrillo L, Black D, Epling CL, et al. Antigen-specific T cell responses induced by Towne cytomegalovirus (CMV) vaccine in CMV-seronegative vaccine recipients. J Clin Virol 2006; 35:332 - 7; http://dx.doi.org/10.1016/j.jcv.2005.09.019; PMID: 16387547
  • Hahn G, Revello MG, Patrone M, Percivalle E, Campanini G, Sarasini A, et al. Human cytomegalovirus UL131-128 genes are indispensable for virus growth in endothelial cells and virus transfer to leukocytes. J Virol 2004; 78:10023 - 33; http://dx.doi.org/10.1128/JVI.78.18.10023-10033.2004; PMID: 15331735
  • Lilja AE, Shenk T. Efficient replication of rhesus cytomegalovirus variants in multiple rhesus and human cell types. Proc Natl Acad Sci U S A 2008; 105:19950 - 5; http://dx.doi.org/10.1073/pnas.0811063106; PMID: 19064925
  • Cui X, Meza BP, Adler SP, McVoy MA. Cytomegalovirus vaccines fail to induce epithelial entry neutralizing antibodies comparable to natural infection. Vaccine 2008; 26:5760 - 6; http://dx.doi.org/10.1016/j.vaccine.2008.07.092; PMID: 18718497
  • Liu MA. DNA vaccines: an historical perspective and view to the future. Immunol Rev 2011; 239:62 - 84; http://dx.doi.org/10.1111/j.1600-065X.2010.00980.x; PMID: 21198665
  • Schleiss MR. VCL-CB01, an injectable bivalent plasmid DNA vaccine for potential protection against CMV disease and infection. Curr Opin Mol Ther 2009; 11:572 - 8; PMID: 19806506
  • Lu S, Wang S, Grimes-Serrano JM. Current progress of DNA vaccine studies in humans. Expert Rev Vaccines 2008; 7:175 - 91; http://dx.doi.org/10.1586/14760584.7.2.175; PMID: 18324888
  • Wang S, Kennedy JS, West K, Montefiori DC, Coley S, Lawrence J, et al. Cross-subtype antibody and cellular immune responses induced by a polyvalent DNA prime-protein boost HIV-1 vaccine in healthy human volunteers. Vaccine 2008; 26:3947 - 57; http://dx.doi.org/10.1016/j.vaccine.2007.12.060; PMID: 18724414
  • Ledgerwood JE, Wei CJ, Hu Z, Gordon IJ, Enama ME, Hendel CS, et al, VRC 306 Study Team. DNA priming and influenza vaccine immunogenicity: two phase 1 open label randomised clinical trials. Lancet Infect Dis 2011; 11:916 - 24; http://dx.doi.org/10.1016/S1473-3099(11)70240-7; PMID: 21975270
  • Wang S, Parker C, Taaffe J, Solórzano A, García-Sastre A, Lu S. Heterologous HA DNA vaccine prime--inactivated influenza vaccine boost is more effective than using DNA or inactivated vaccine alone in eliciting antibody responses against H1 or H3 serotype influenza viruses. Vaccine 2008; 26:3626 - 33; http://dx.doi.org/10.1016/j.vaccine.2008.04.073; PMID: 18538900
  • Suguitan ALJ Jr., Cheng X, Wang W, Wang S, Jin H, Lu S. Influenza H5 hemagglutinin DNA primes the antibody response elicited by the live attenuated influenza A/Vietnam/1203/2004 vaccine in ferrets. PLoS One 2011; 6:e21942; http://dx.doi.org/10.1371/journal.pone.0021942; PMID: 21760928
  • Morello CS, Ye M, Spector DH. Development of a vaccine against murine cytomegalovirus (MCMV), consisting of plasmid DNA and formalin-inactivated MCMV, that provides long-term, complete protection against viral replication. J Virol 2002; 76:4822 - 35; http://dx.doi.org/10.1128/JVI.76.10.4822-4835.2002; PMID: 11967299
  • Morello CS, Ye M, Hung S, Kelley LA, Spector DH. Systemic priming-boosting immunization with a trivalent plasmid DNA and inactivated murine cytomegalovirus (MCMV) vaccine provides long-term protection against viral replication following systemic or mucosal MCMV challenge. J Virol 2005; 79:159 - 75; http://dx.doi.org/10.1128/JVI.79.1.159-175.2005; PMID: 15596812
  • Jacobson MA, Adler SP, Sinclair E, Black D, Smith A, Chu A, et al. A CMV DNA vaccine primes for memory immune responses to live-attenuated CMV (Towne strain). Vaccine 2009; 27:1540 - 8; http://dx.doi.org/10.1016/j.vaccine.2009.01.006; PMID: 19168107
  • Kern F, Surel IP, Faulhaber N, Frömmel C, Schneider-Mergener J, Schönemann C, et al. Target structures of the CD8(+)-T-cell response to human cytomegalovirus: the 72-kilodalton major immediate-early protein revisited. J Virol 1999; 73:8179 - 84; PMID: 10482568
  • Wang Z, La Rosa C, Maas R, Ly H, Brewer J, Mekhoubad S, et al. Recombinant MVA expressing a soluble form of Glycoprotein B causes durable immunity and neutralizing antibodies against multiple strains of CMV. J Virol 2004; 78:3965 - 76; http://dx.doi.org/10.1128/JVI.78.8.3965-3976.2004; PMID: 15047812
  • Wang Z, La Rosa C, Mekhoubad S, Lacey SF, Villacres MC, Markel S, et al. Attenuated poxviruses generate clinically relevant frequencies of CMV-specific T cells. Blood 2004; 104:847 - 56; http://dx.doi.org/10.1182/blood-2003-10-3469; PMID: 15090456
  • La Rosa C, Wang Z, Lacey SF, Markel SF, Sharma MC, Martinez J, et al. Characterization of host immunity to cytomegalovirus pp150 (UL32). Hum Immunol 2005; 66:116 - 26; http://dx.doi.org/10.1016/j.humimm.2004.10.008; PMID: 15694996
  • Wang Z, La Rosa C, Li Z, Ly H, Krishnan A, Martinez J, et al. Vaccine properties of a novel marker gene-free recombinant modified vaccinia Ankara expressing immunodominant CMV antigens pp65 and IE1. Vaccine 2007; 25:1132 - 41; http://dx.doi.org/10.1016/j.vaccine.2006.09.067; PMID: 17049414
  • Lu S, Manning S, Arthos J. Antigen engineering in DNA immunization. Totowa, NJ: Humana Press, 1999:355-74.
  • Wang S, Pal R, Mascola JR, Chou TH, Mboudjeka I, Shen S, et al. Polyvalent HIV-1 Env vaccine formulations delivered by the DNA priming plus protein boosting approach are effective in generating neutralizing antibodies against primary human immunodeficiency virus type 1 isolates from subtypes A, B, C, D and E. Virology 2006; 350:34 - 47; http://dx.doi.org/10.1016/j.virol.2006.02.032; PMID: 16616287
  • Wang S, Joshi S, Lu S. Delivery of DNA to skin by particle bombardment. Methods Mol Biol 2004; 245:185 - 96; PMID: 14707379
  • Gonczol E, Furlini G, Ianacone J, Plotkin SA. A rapid microneutralization assay for cytomegalovirus. J Virol Methods 1986; 14:37 - 41; http://dx.doi.org/10.1016/0166-0934(86)90005-4; PMID: 3021795
  • Andreoni M, Faircloth M, Vugler L, Britt WJ. A rapid microneutralization assay for the measurement of neutralizing antibody reactive with human cytomegalovirus. J Virol Methods 1989; 23:157 - 67; http://dx.doi.org/10.1016/0166-0934(89)90129-8; PMID: 2542350

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