Enhancing poxvirus vectors vaccine immunogenicity

Human Vaccines and Immunotherapeutics

Volumn 10, Issue 8, 2014, Pages 2235-2244

  García Arriaza, Juan ^a   Esteban, Mariano ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

Author keywords

Immunogenicity; Poxvirus; Recombinants; Vaccines; Vector improvements

Indexed keywords

HUMAN IMMUNODEFICIENCY VIRUS VACCINE; IMMUNOLOGICAL ADJUVANT; POXVIRUS VECTOR; SMALLPOX VACCINE; VACCINE; VIRUS ANTIGEN; DRUG CARRIER; LIVE VACCINE; RECOMBINANT VACCINE; VIRUS VACCINE;

ANTIGEN EXPRESSION; CELLULAR IMMUNITY; CLINICAL PROTOCOL; DRUG DESIGN; DRUG EFFICACY; DRUG RESEARCH; DRUG SAFETY; GENE DELETION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOGENICITY; IMMUNOMODULATION; IMMUNOSTIMULATION; NONHUMAN; NOTE; PROMOTER REGION; SMALLPOX; VACCINE PRODUCTION; VETERINARY MEDICINE; VIRUS GENE; VIRUS GENOME; VIRUS RECOMBINANT; VIRUS REPLICATION; DNA REPLICATION; GENE EXPRESSION; GENE VECTOR; GENETICS; IMMUNOLOGY; POXVIRIDAE; PROCEDURES; VACCINATION;

DNA REPLICATION; DRUG CARRIERS; GENE EXPRESSION; GENETIC VECTORS; HUMANS; POXVIRIDAE; VACCINATION; VACCINES, ATTENUATED; VACCINES, SYNTHETIC; VIRAL VACCINES;

EID: 84908374121     PISSN: 21645515     EISSN: 2164554X     Source Type: Journal    
DOI: 10.4161/hv.28974     Document Type: Note

References (144)

1. Fauci AS. The global challenge of infectious diseases: the evolving role of the National Institutes of Health in basic and clinical research. Nat Immunol 2005; 6:743-7; PMID:16034426; http://dx.doi.org/10.1038/ni0805-743
2. Mackett M, Smith GL, Moss B. Vaccinia virus: a selectable eukaryotic cloning and expression vector. Proc Natl Acad Sci U S A 1982; 79:7415-9; PMID:6296831; http://dx.doi.org/10.1073/pnas.79.23.7415
3. Panicali D, Paoletti E. Construction of poxviruses as cloning vectors: insertion of the thymidine kinase gene from herpes simplex virus into the DNA of infectious vaccinia virus. Proc Natl Acad Sci U S A 1982; 79:4927-31; PMID:6289324; http://dx.doi.org/10.1073/pnas.79.16.4927
4. Boukhebza H, Bellon N, Limacher JM, Inchauspé G. Therapeutic vaccination to treat chronic infectious diseases: current clinical developments using MVA-based vaccines. Hum Vaccin Immunother 2012; 8:1746-57; PMID:22894957; http://dx.doi.org/10.4161/hv.21689
5. Cottingham MG, Carroll MW. Recombinant MVA vaccines: dispelling the myths. Vaccine 2013; 31:4247-51; PMID:23523407; http://dx.doi.org/10.1016/j.vaccine.2013.03.021
6. Draper SJ, Cottingham MG, Gilbert SC. Utilizing poxviral vectored vaccines for antibody inductionprogress and prospects. Vaccine 2013; 31:4223-30; PMID:23746455; http://dx.doi.org/10.1016/j.vaccine.2013.05.091
7. Gilbert SC. Clinical development of Modified Vaccinia virus Ankara vaccines. Vaccine 2013; 31:4241-6; PMID:23523410; http://dx.doi.org/10.1016/j.vaccine.2013.03.020
8. Gómez CE, Nájera JL, Krupa M, Perdiguero B, Esteban M. MVA and NYVAC as vaccines against emergent infectious diseases and cancer. Curr Gene Ther 2011; 11:189-217; PMID:21453284; http://dx.doi.org/10.2174/156652311795684731
9. Gómez CE, Perdiguero B, Garcia-Arriaza J, Esteban M. Poxvirus vectors as HIV/AIDS vaccines in humans. Hum Vaccin Immunother 2012; 8:1192-207; PMID:22906946; http://dx.doi.org/10.4161/hv.20778
10. Gómez CE, Perdiguero B, García-Arriaza J, Esteban M. Clinical applications of attenuated MVA poxvirus strain. Expert Rev Vaccines 2013; 12:1395-416; PMID:24168097; http://dx.doi.org/10.1586/14760584.2013.845531
11. Hill AV, Reyes-Sandoval A, O'Hara G, Ewer K, Lawrie A, Goodman A, Nicosia A, Folgori A, Colloca S, Cortese R, et al. Prime-boost vectored malaria vaccines: progress and prospects. Hum Vaccin 2010; 6:78-83; PMID:20061802; http://dx.doi.org/10.4161/hv.6.1.10116
12. Izzi V, Buler M, Masuelli L, Giganti MG, Modesti A, Bei R. Poxvirus-based vaccines for cancer immunotherapy: new insights from combined cytokines/co-stimulatory molecules delivery and "uncommon" strains. Anticancer Agents Med Chem 2014; 14:183-9; PMID:24237219; http://dx.doi.org/10.2174/18715206113136660376
13. Kim JW, Gulley JL. Poxviral vectors for cancer immunotherapy. Expert Opin Biol Ther 2012; 12:463-78; PMID:22413824; http://dx.doi.org/10.1517/14712598.2012.668516
14. Kreijtz JH, Gilbert SC, Sutter G. Poxvirus vectors. Vaccine 2013; 31:4217-9; PMID:23834812; http://dx.doi.org/10.1016/j.vaccine.2013.06.073
15. Pantaleo G, Esteban M, Jacobs B, Tartaglia J. Poxvirus vector-based HIV vaccines. Curr Opin HIV AIDS 2010; 5:391-6; PMID:20978379; http://dx.doi.org/10.1097/COH.0b013e32833d1e87
16. Volz A, Sutter G. Protective efficacy of Modified Vaccinia virus Ankara in preclinical studies. Vaccine 2013; 31:4235-40; PMID:23523402; http://dx.doi.org/10.1016/j.vaccine.2013.03.016
17. Walsh SR, Dolin R. Vaccinia viruses: vaccines against smallpox and vectors against infectious diseases and tumors. Expert Rev Vaccines 2011; 10:1221-40; PMID:21854314; http://dx.doi.org/10.1586/erv.11.79
18. Li S, Rodrigues M, Rodriguez D, Rodriguez JR, Esteban M, Palese P, Nussenzweig RS, Zavala F. Priming with recombinant influenza virus followed by administration of recombinant vaccinia virus induces CD8+ T-cell-mediated protective immunity against malaria. Proc Natl Acad Sci U S A 1993; 90:5214-8; PMID:7685119; http://dx.doi.org/10.1073/pnas.90.11.5214
19. Miyahira Y, García-Sastre A, Rodriguez D, Rodriguez JR, Murata K, Tsuji M, Palese P, Esteban M, Zavala F, Nussenzweig RS. Recombinant viruses expressing a human malaria antigen can elicit potentially protective immune CD8+ responses in mice. Proc Natl Acad Sci U S A 1998; 95:3954-9; PMID:9520474; http://dx.doi.org/10.1073/pnas.95.7.3954
20. Zavala F, Rodrigues M, Rodriguez D, Rodriguez JR, Nussenzweig RS, Esteban M. A striking property of recombinant poxviruses: efficient inducers of in vivo expansion of primed CD8(+) T cells. Virology 2001; 280:155-9; PMID:11162829; http://dx.doi.org/10.1006/viro.2000.0792
21. González-Aseguinolaza G, Nakaya Y, Molano A, Dy E, Esteban M, Rodríguez D, Rodríguez JR, Palese P, García-Sastre A, Nussenzweig RS. Induction of protective immunity against malaria by priming-boosting immunization with recombinant cold-adapted influenza and modified vaccinia Ankara viruses expressing a CD8+-T-cell epitope derived from the circumsporozoite protein of Plasmodium yoelii. J Virol 2003; 77:11859-66; PMID:14557672; http://dx.doi.org/10.1128/JVI.77.21.11859-11866.2003
22. Barouch DH, Liu J, Li H, Maxfield LF, Abbink P, Lynch DM, Iampietro MJ, SanMiguel A, Seaman MS, Ferrari G, et al. Vaccine protection against acquisition of neutralization-resistant SIV challenges in rhesus monkeys. Nature 2012; 482:89-93; PMID:22217938; http://dx.doi.org/10.1038/nature10766
23. Boyd AC, Ruiz-Hernandez R, Peroval MY, Carson C, Balkissoon D, Staines K, Turner AV, Hill AV, Gilbert SC, Butter C. Towards a universal vaccine for avian influenza: protective efficacy of modified Vaccinia virus Ankara and Adenovirus vaccines expressing conserved influenza antigens in chickens challenged with low pathogenic avian influenza virus. Vaccine 2013; 31:670-5; PMID:23200938; http://dx.doi.org/10.1016/j.vaccine.2012.11.047
24. Ratto-Kim S, Currier JR, Cox JH, Excler JL, Valencia-Micolta A, Thelian D, Lo V, Sayeed E, Polonis VR, Earl PL, et al. Heterologous prime-boost regimens using rAd35 and rMVA vectors elicit stronger cellular immune responses to HIV proteins than homologous regimens. PLoS One 2012; 7:e45840; PMID:23049876; http://dx.doi.org/10.1371/journal.pone.0045840
25. Reyes-Sandoval A, Berthoud T, Alder N, Siani L, Gilbert SC, Nicosia A, Colloca S, Cortese R, Hill AV. Prime-boost immunization with adenoviral and modified vaccinia virus Ankara vectors enhances the durability and polyfunctionality of protective malaria CD8+ T-cell responses. Infect Immun 2010; 78:145-53; PMID:19858306; http://dx.doi.org/10.1128/IAI.00740-09
26. Reyes-Sandoval A, Rollier CS, Milicic A, Bauza K, Cottingham MG, Tang CK, Dicks MD, Wang D, Longley RJ, Wyllie DH, et al. Mixed vector immunization with recombinant adenovirus and MVA can improve vaccine efficacy while decreasing antivector immunity. Mol Ther 2012; 20:1633-47; PMID:22354374; http://dx.doi.org/10.1038/mt.2012.25
27. Gómez CE, Nájera JL, Jiménez EP, Jiménez V, Wagner R, Graf M, Frachette MJ, Liljeström P, Pantaleo G, Esteban M. 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. Vaccine 2007; 25:2863-85; PMID:17113200; http://dx.doi.org/10.1016/j.vaccine.2006.09.090
28. Mooij P, Balla-Jhagjhoorsingh SS, Koopman G, Beenhakker N, van Haaften P, Baak I, Nieuwenhuis IG, Kondova I, Wagner R, Wolf H, et al. Differential CD4+ versus CD8+ T-cell responses elicited by different poxvirus-based human immunodeficiency virus type 1 vaccine candidates provide comparable efficacies in primates. J Virol 2008; 82:2975-88; PMID:18184713; http://dx.doi.org/10.1128/JVI.02216-07
29. Vaccari M, Keele BF, Bosinger SE, Doster MN, Ma ZM, Pollara J, Hryniewicz A, Ferrari G, Guan Y, Forthal DN, et al. Protection afforded by an HIV vaccine candidate in macaques depends on the dose of SIVmac251 at challenge exposure. J Virol 2013; 87:3538-48; PMID:23325681; http://dx.doi.org/10.1128/JVI.02863-12
30. Santra S, Sun Y, Parvani JG, Philippon V, Wyand MS, Manson K, Gomez-Yafal A, Mazzara G, Panicali D, Markham PD, et al. Heterologous prime/boost immunization of rhesus monkeys by using diverse poxvirus vectors. J Virol 2007; 81:8563-70; PMID:17553898; http://dx.doi.org/10.1128/JVI.00744-07
31. 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-gamma. Virus Res 2006; 116:11-20; PMID:16214252; http://dx.doi.org/10.1016/j.virusres.2005.08.008
32. Gherardi MM, Ramírez 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 2000; 74:6278-86; PMID:10864637; http://dx.doi.org/10.1128/JVI.74.14.6278-6286.2000
33. Gherardi MM, Ramirez JC, Rodríguez D, Rodríguez JR, Sano G, Zavala F, Esteban M. IL-12 delivery from recombinant vaccinia virus attenuates the vector and enhances the cellular immune response against HIV-1 Env in a dose-dependent manner. J Immunol 1999; 162:6724-33; PMID:10352291
34. Gonzalo RM, Rodríguez JR, Rodríguez D, González-Aseguinolaza G, Larraga V, Esteban M. Protective immune response against cutaneous leishmaniasis by prime/booster immunization regimens with vaccinia virus recombinants expressing Leishmania infantum p36/LACK and IL-12 in combination with purified p36. Microbes Infect 2001; 3:701-11; PMID:11489418; http://dx.doi.org/10.1016/S1286-4579(01)01426-5
35. Nemeckova S, Sroller V, Hainz P, Krystofova J, Smahel M, Kutinova L. Experimental therapy of HPV16 induced tumors with IL12 expressed by recombinant vaccinia virus in mice. Int J Mol Med 2003; 12:789-96; PMID:14533011
36. Rodríguez AM, Pascutti MF, Maeto C, Falivene J, Holgado MP, Turk G, Gherardi MM. IL-12 and GM-CSF in DNA/MVA immunizations against HIV-1 CRF12-BF Nef induced T-cell responses with an enhanced magnitude, breadth and quality. PLoS One 2012; 7:e37801; PMID:22655069; http://dx.doi.org/10.1371/journal.pone.0037801
37. Tapia E, Pérez-Jiménez E, López-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 2003; 5:73-84; PMID:12650765; http://dx.doi.org/10.1016/S1286-4579(02)00077-1
38. Gómez CE, Abaitua F, Rodríguez D, Esteban M. Efficient CD8+ T cell response to the HIV-env V3 loop epitope from multiple virus isolates by a DNA prime/vaccinia virus boost (rWR and rMVA strains) immunization regime and enhancement by the cytokine IFN-gamma. Virus Res 2004; 105:11-22; PMID:15325077; http://dx.doi.org/10.1016/j.virusres.2004.04.008
39. Bertley FM, Kozlowski PA, Wang SW, Chappelle J, Patel J, Sonuyi O, Mazzara G, Montefiori D, Carville A, Mansfield KG, et al. Control of simian/human immunodeficiency virus viremia and disease progression after IL-2-augmented DNA-modified vaccinia virus Ankara nasal vaccination in nonhuman primates. J Immunol 2004; 172:3745-57; PMID:15004179; http://dx.doi.org/10.4049/jimmunol.172.6.3745
40. Dreicer R, Stadler WM, Ahmann FR, Whiteside T, Bizouarne N, Acres B, Limacher JM, Squiban P, Pantuck A. MVA-MUC1-IL2 vaccine immunotherapy (TG4010) improves PSA doubling time in patients with prostate cancer with biochemical failure. Invest New Drugs 2009; 27:379-86; PMID:18931824; http://dx.doi.org/10.1007/s10637-008-9187-3
41. Kaufman HL, Taback B, Sherman W, Kim DW, Shingler WH, Moroziewicz D, DeRaffele G, Mitcham J, Carroll MW, Harrop R, et al. Phase II trial of Modified Vaccinia Ankara (MVA) virus expressing 5T4 and high dose Interleukin-2 (IL-2) in patients with metastatic renal cell carcinoma. J Transl Med 2009; 7:2; PMID:19128501; http://dx.doi.org/10.1186/1479-5876-7-2
42. Kolibab K, Yang A, Derrick SC, Waldmann TA, Perera LP, Morris SL. Highly persistent and effective prime/boost regimens against tuberculosis that use a multivalent modified vaccine virus Ankara-based tuberculosis vaccine with interleukin-15 as a molecular adjuvant. Clin Vaccine Immunol 2010; 17:793-801; PMID:20357059; http://dx.doi.org/10.1128/CVI.00006-10
43. Li S, Qi X, Gao Y, Hao Y, Cui L, Ruan L, He W. IL-15 increases the frequency of effector memory CD8+ T cells in rhesus monkeys immunized with HIV vaccine. Cell Mol Immunol 2010; 7:491-4; PMID:20871629; http://dx.doi.org/10.1038/cmi.2010.44
44. Oh S, Berzofsky JA, Burke DS, Waldmann TA, Perera LP. Coadministration of HIV vaccine vectors with vaccinia viruses expressing IL-15 but not IL-2 induces long-lasting cellular immunity. Proc Natl Acad Sci U S A 2003; 100:3392-7; PMID:12626740; http://dx.doi.org/10.1073/pnas.0630592100
45. Perera LP, Waldmann TA, Mosca JD, Baldwin N, Berzofsky JA, Oh SK. Development of smallpox vaccine candidates with integrated interleukin-15 that demonstrate superior immunogenicity, efficacy, and safety in mice. J Virol 2007; 81:8774-83; PMID:17553867; http://dx.doi.org/10.1128/JVI.00538-07
46. Perera PY, Derrick SC, Kolibab K, Momoi F, Yamamoto M, Morris SL, Waldmann TA, Perera LP. A multi-valent vaccinia virus-based tuberculosis vaccine molecularly adjuvanted with interleukin-15 induces robust immune responses in mice. Vaccine 2009; 27:2121-7; PMID:19356615; http://dx.doi.org/10.1016/j.vaccine.2009.01.132
47. Poon LL, Leung YH, Nicholls JM, Perera PY, Lichy JH, Yamamoto M, Waldmann TA, Peiris JS, Perera LP. Vaccinia virus-based multivalent H5N1 avian influenza vaccines adjuvanted with IL-15 confer sterile cross-clade protection in mice. J Immunol 2009; 182:3063-71; PMID:19234203; http://dx.doi.org/10.4049/jimmunol.0803467
48. Goulding J, Tahiliani V, Salek-Ardakani S. OX40:OX40L axis: emerging targets for improving poxvirus-based CD8(+) T-cell vaccines against respiratory viruses. Immunol Rev 2011; 244:149-68; PMID:22017437; http://dx.doi.org/10.1111/j.1600-065X.2011.01062.x
49. Grosenbach DW, Schlom J, Gritz L, Gómez Yafal A, Hodge JW. A recombinant vector expressing transgenes for four T-cell costimulatory molecules (OX40L, B7-1, ICAM-1, LFA-3) induces sustained CD4+ and CD8+ T-cell activation, protection from apoptosis, and enhanced cytokine production. Cell Immunol 2003; 222:45-57; PMID:12798307; http://dx.doi.org/10.1016/S0008-8749(03)00080-7
50. Liu J, Ngai N, Stone GW, Yue FY, Ostrowski MA. The adjuvancy of OX40 ligand (CD252) on an HIV-1 canarypox vaccine. Vaccine 2009; 27:5077-84; PMID:19573639; http://dx.doi.org/10.1016/j.vaccine.2009.06.046
51. Gulley JL, Arlen PM, Tsang KY, Yokokawa J, Palena C, Poole DJ, Remondo C, Cereda V, Jones JL, Pazdur MP, et al. Pilot study of vaccination with recombinant CEA-MUC-1-TRICOM poxviral-based vaccines in patients with metastatic carcinoma. Clin Cancer Res 2008; 14:3060-9; PMID:18483372; http://dx.doi.org/10.1158/1078-0432.CCR-08-0126
52. Hodge JW, Higgins J, Schlom J. Harnessing the unique local immunostimulatory properties of modified vaccinia Ankara (MVA) virus to generate superior tumor-specific immune responses and antitumor activity in a diversified prime and boost vaccine regimen. Vaccine 2009; 27:4475-82; PMID:19450631; http://dx.doi.org/10.1016/j.vaccine.2009.05.017
53. Kudo-Saito C, Schlom J, Hodge JW. Intratumoral vaccination and diversified subcutaneous/ intratumoral vaccination with recombinant poxviruses encoding a tumor antigen and multiple costimulatory molecules. Clin Cancer Res 2004; 10:1090-9; PMID:14871989; http://dx.doi.org/10.1158/1078-0432.CCR-03-0145
54. Morse MA, Clay TM, Hobeika AC, Osada T, Khan S, Chui S, Niedzwiecki D, Panicali D, Schlom J, Lyerly HK. Phase I study of immunization with dendritic cells modified with fowlpox encoding carcinoembryonic antigen and costimulatory molecules. Clin Cancer Res 2005; 11:3017-24; PMID:15837756; http://dx.doi.org/10.1158/1078-0432.CCR-04-2172
55. Palena C, Zhu M, Schlom J, Tsang KY. Human B cells that hyperexpress a triad of costimulatory molecules via avipox-vector infection: an alternative source of efficient antigen-presenting cells. Blood 2004; 104:192-9; PMID:15010371; http://dx.doi.org/10.1182/blood-2003-09-3211
56. Shankar P, Schlom J, Hodge JW. Enhanced activation of rhesus T cells by vectors encoding a triad of costimulatory molecules (B7-1, ICAM-1, LFA-3). Vaccine 2001; 20:744-55; PMID:11738738; http://dx.doi.org/10.1016/S0264-410X(01)00409-1
57. Zhu M, Terasawa H, Gulley J, Panicali D, Arlen P, Schlom J, Tsang KY. Enhanced activation of human T cells via avipox vector-mediated hyperexpression of a triad of costimulatory molecules in human dendritic cells. Cancer Res 2001; 61:3725-34; PMID:11325845
58. Vasir B, Zarwan C, Ahmad R, Crawford KD, Rajabi H, Matsuoka K, Rosenblatt J, Wu Z, Mills H, Kufe D, et al. Induction of antitumor immunity ex vivo using dendritic cells transduced with fowl pox vector expressing MUC1, CEA, and a triad of costimulatory molecules (rF-PANVAC). J Immunother 2012; 35:555-69; PMID:22892452; http://dx.doi.org/10.1097/CJI.0b013e31826a73de
59. 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. Vaccine 2009; 27:3165-74; PMID:19446187; http://dx.doi.org/10.1016/j.vaccine.2009.03.049
60. Lauterbach H, Pätzold J, Kassub R, Bathke B, Brinkmann K, Chaplin P, Suter M, Hochrein H. Genetic Adjuvantation of Recombinant MVA with CD40L Potentiates CD8 T Cell Mediated Immunity. Front Immunol 2013; 4:251; PMID:23986761; http://dx.doi.org/10.3389/fimmu.2013.00251
61. Liu J, Yu Q, Stone GW, Yue FY, Ngai N, Jones RB, Kornbluth RS, Ostrowski MA. 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. Vaccine 2008; 26:4062-72; PMID:18562053; http://dx.doi.org/10.1016/j.vaccine.2008.05.018
62. Parviainen S, Ahonen M, Diaconu I, Hirvinen M, Karttunen A˚, Vähä-Koskela M, Hemminki A, Cerullo V. CD40 ligand and tdTomato-armed vaccinia virus for induction of antitumor immune response and tumor imaging. Gene Ther 2014; 21:195-204; PMID:24305418; http://dx.doi.org/10.1038/gt.2013.73
63. 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 2006; 80:7676-87; PMID:16840346; http://dx.doi.org/10.1128/JVI.02748-05
64. Lai L, Kwa S, Kozlowski PA, Montefiori DC, Ferrari G, Johnson WE, Hirsch V, Villinger F, Chennareddi L, Earl PL, et al. Prevention of infection by a granulocyte-macrophage colony-stimulating factor co-expressing DNA/modified vaccinia Ankara simian immunodeficiency virus vaccine. J Infect Dis 2011; 204:164-73; PMID:21628671; http://dx.doi.org/10.1093/infdis/jir199
65. Lee JH, Roh MS, Lee YK, Kim MK, Han JY, Park BH, Trown P, Kirn DH, Hwang TH. Oncolytic and immunostimulatory efficacy of a targeted oncolytic poxvirus expressing human GM-CSF following intravenous administration in a rabbit tumor model. Cancer Gene Ther 2010; 17:73-9; PMID:19629143; http://dx.doi.org/10.1038/cgt.2009.50
66. Morse MA, Niedzwiecki D, Marshall JL, Garrett C, Chang DZ, Aklilu M, Crocenzi TS, Cole DJ, Dessureault S, Hobeika AC, et al. A randomized phase II study of immunization with dendritic cells modified with poxvectors encoding CEA and MUC1 compared with the same poxvectors plus GM-CSF for resected metastatic colorectal cancer. Ann Surg 2013; 258:879-86; PMID:23657083; http://dx.doi.org/10.1097/SLA.0b013e318292919e
67. Nemeckova S, Smahel M, Hainz P, Mackova J, Zurkova K, Gabriel P, Indrova M, Kutinova L. Combination of intratumoral injections of vaccinia virus MVA expressing GM-CSF and immunization with DNA vaccine prolongs the survival of mice bearing HPV16 induced tumors with downregulated expression of MHC class I molecules. Neoplasma 2007; 54:326-33; PMID:17822323
68. Alcami A. Viral mimicry of cytokines, chemokines and their receptors. Nat Rev Immunol 2003; 3:36-50; PMID:12511874; http://dx.doi.org/10.1038/nri980
69. Perdiguero B, Esteban M. The interferon system and vaccinia virus evasion mechanisms. J Interferon Cytokine Res 2009; 29:581-98; PMID:19708815; http://dx.doi.org/10.1089/jir.2009.0073
70. Smith GL, Benfield CT, Maluquer de Motes C, Mazzon M, Ember SW, Ferguson BJ, Sumner RP. Vaccinia virus immune evasion: mechanisms, virulence and immunogenicity. J Gen Virol 2013; 94:2367-92; PMID:23999164; http://dx.doi.org/10.1099/vir.0.055921-0
71. Cottingham MG, Andersen RF, Spencer AJ, Saurya S, Furze J, Hill AV, Gilbert SC. Recombination-mediated genetic engineering of a bacterial artificial chromosome clone of modified vaccinia virus Ankara (MVA). PLoS One. 2008 Feb 20;3(2):e1638
72. Falivene J, Del Médico Zajac MP, Pascutti MF, Rodríguez AM, Maeto C, Perdiguero B, Gómez CE, Esteban M, Calamante G, Gherardi MM. Improving the MVA vaccine potential by deleting the viral gene coding for the IL-18 binding protein. PLoS One 2012; 7:e32220; PMID:22384183; http://dx.doi.org/10.1371/journal.pone.0032220
73. García-Arriaza J, Arnáez P, Gómez CE, Sorzano CO, Esteban M. Improving Adaptive and Memory Immune Responses of an HIV/AIDS Vaccine Candidate MVA-B by Deletion of Vaccinia Virus Genes (C6L and K7R) Blocking Interferon Signaling Pathways. PLoS One 2013; 8:e66894; PMID:23826170; http://dx.doi.org/10.1371/journal.pone.0066894
74. García-Arriaza J, Gómez CE, Sorzano CO, Esteban M. Deletion of the vaccinia virus N2L gene encoding an inhibitor of IRF3 improves the immunogenicity of modified vaccinia virus Ankara expressing HIV-1 antigens. J Virol 2014; 88:3392-410; PMID:24390336; http://dx.doi.org/10.1128/JVI.02723-13
75. García-Arriaza J, Nájera JL, Gómez CE, Sorzano CO, Esteban M. Immunogenic profiling in mice of a HIV/AIDS vaccine candidate (MVA-B) expressing four HIV-1 antigens and potentiation by specific gene deletions. PLoS One 2010; 5:e12395; PMID:20811493; http://dx.doi.org/10.1371/journal.pone.0012395
76. García-Arriaza J, Nájera JL, Gómez CE, Tewabe N, Sorzano CO, Calandra T, Roger T, Esteban M. A candidate HIV/AIDS vaccine (MVA-B) lacking vaccinia virus gene C6L enhances memory HIV-1-specific T-cell responses. PLoS One 2011; 6:e24244; PMID:21909386; http://dx.doi.org/10.1371/journal.pone.0024244
77. Gómez CE, Perdiguero B, Nájera JL, Sorzano CO, Jiménez V, González-Sanz R, Esteban M. Removal of vaccinia virus genes that block interferon type I and II pathways improves adaptive and memory responses of the HIV/AIDS vaccine candidate NYVAC-C in mice. J Virol 2012; 86:5026-38; PMID:22419805; http://dx.doi.org/10.1128/JVI.06684-11
78. Perdiguero B, Gómez CE, Di Pilato M, Sorzano CO, Delaloye J, Roger T, Calandra T, Pantaleo G, Esteban M. Deletion of the vaccinia virus gene A46R, encoding for an inhibitor of TLR signalling, is an effective approach to enhance the immunogenicity in mice of the HIV/AIDS vaccine candidate NYVAC-C. PLoS One 2013; 8:e74831; PMID:24069354; http://dx.doi.org/10.1371/journal.pone.0074831
79. Perdiguero B, Gómez CE, Nájera JL, Sorzano CO, Delaloye J, González-Sanz R, Jiménez V, Roger T, Calandra T, Pantaleo G, et al. Deletion of the viral anti-apoptotic gene F1L in the HIV/AIDS vaccine candidate MVA-C enhances immune responses against HIV-1 antigens. PLoS One 2012; 7:e48524; PMID:23119046; http://dx.doi.org/10.1371/journal.pone.0048524
80. Garber DA, O'Mara LA, Gangadhara S, McQuoid M, Zhang X, Zheng R, Gill K, Verma M, Yu T, Johnson B, et al. Deletion of specific immune-modulatory genes from modified vaccinia virus Ankara-based HIV vaccines engenders improved immunogenicity in rhesus macaques. J Virol 2012; 86:12605-15; PMID:22973033; http://dx.doi.org/10.1128/JVI.00246-12
81. Garber DA, O'Mara LA, Zhao J, Gangadhara S, An I, Feinberg MB. Expanding the repertoire of Modified Vaccinia Ankara-based vaccine vectors via genetic complementation strategies. PLoS One 2009; 4:e5445; PMID:19421328; http://dx.doi.org/10.1371/journal.pone.0005445
82. Addo MM, Draenert R, Rathod A, Verrill CL, Davis BT, Gandhi RT, Robbins GK, Basgoz NO, Stone DR, Cohen DE, et al. Fully differentiated HIV-1 specific CD8+ T effector cells are more frequently detectable in controlled than in progressive HIV-1 infection. PLoS One 2007; 2:e321; PMID:17389912; http://dx.doi.org/10.1371/journal.pone.0000321
83. Hess C, Altfeld M, Thomas SY, Addo MM, Rosenberg ES, Allen TM, Draenert R, Eldrige RL, van Lunzen J, Stellbrink HJ, et al. HIV-1 specific CD8+ T cells with an effector phenotype and control of viral replication. Lancet 2004; 363:863-6; PMID:15031033; http://dx.doi.org/10.1016/S0140-6736(04)15735-8
84. Northfield JW, Loo CP, Barbour JD, Spotts G, Hecht FM, Klenerman P, Nixon DF, Michaëlsson J. Human immunodeficiency virus type 1 (HIV-1)-specific CD8+ T(EMRA) cells in early infection are linked to control of HIV-1 viremia and predict the subsequent viral load set point. J Virol 2007; 81:5759-65; PMID:17376902; http://dx.doi.org/10.1128/JVI.00045-07
85. Hansen SG, Ford JC, Lewis MS, Ventura AB, Hughes CM, Coyne-Johnson L, Whizin N, Oswald K, Shoemaker R, Swanson T, et al. Profound early control of highly pathogenic SIV by an effector memory T-cell vaccine. Nature 2011; 473:523-7; PMID:21562493; http://dx.doi.org/10.1038/nature10003
86. Hansen SG, Vieville C, Whizin N, Coyne-Johnson L, Siess DC, Drummond DD, Legasse AW, Axthelm MK, Oswald K, Trubey CM, et al. Effector memory T cell responses are associated with protection of rhesus monkeys from mucosal simian immunodeficiency virus challenge. Nat Med 2009; 15:293-9; PMID:19219024; http://dx.doi.org/10.1038/nm.1935
87. García-Arriaza J, Cepeda V, Hallengärd D, Sorzano CO, Kümmerer BM, Liljeström P, Esteban M. A novel poxvirus-based vaccine, MVA-CHIKV, is highly immunogenic and protects mice against chikungunya infection. J Virol 2014; 88:3527-47; PMID:24403588; http://dx.doi.org/10.1128/JVI.03418-13
88. Wyatt LS, Earl PL, Vogt J, Eller LA, Chandran D, Liu J, Robinson HL, Moss B. Correlation of immunogenicities and in vitro expression levels of recombinant modified vaccinia virus Ankara HIV vaccines. Vaccine 2008; 26:486-93; PMID:18155813; http://dx.doi.org/10.1016/j.vaccine.2007.11.036
89. Baur K, Brinkmann K, Schweneker M, Pätzold J, Meisinger-Henschel C, Hermann J, Steigerwald R, Chaplin P, Suter M, Hausmann J. Immediate-early expression of a recombinant antigen by modified vaccinia virus ankara breaks the immunodominance of strong vector-specific B8R antigen in acute and memory CD8 T-cell responses. J Virol 2010; 84:8743-52; PMID:20538860; http://dx.doi.org/10.1128/JVI.00604-10
90. Moutaftsi M, Bui HH, Peters B, Sidney J, Salek-Ardakani S, Oseroff C, Pasquetto V, Crotty S, Croft M, Lefkowitz EJ, et al. Vaccinia virus-specific CD4+ T cell responses target a set of antigens largely distinct from those targeted by CD8+ T cell responses. J Immunol 2007; 178:6814-20; PMID:17513729; http://dx.doi.org/10.4049/jimmunol.178.11.6814
91. Moutaftsi M, Tscharke DC, Vaughan K, Koelle DM, Stern L, Calvo-Calle M, Ennis F, Terajima M, Sutter G, Crotty S, et al. Uncovering the interplay between CD8, CD4 and antibody responses to complex pathogens. Future Microbiol 2010; 5:221-39; PMID:20143946; http://dx.doi.org/10.2217/fmb.09.110
92. Yang Z, Reynolds SE, Martens CA, Bruno DP, Porcella SF, Moss B. Expression profiling of the intermediate and late stages of poxvirus replication. J Virol 2011; 85:9899-908; PMID:21795349; http://dx.doi.org/10.1128/JVI.05446-11
93. Moutaftsi M, Salek-Ardakani S, Croft M, Peters B, Sidney J, Grey H, Sette A. Correlates of protection efficacy induced by vaccinia virus-specific CD8+ T-cell epitopes in the murine intranasal challenge model. Eur J Immunol 2009; 39:717-22; PMID:19224639; http://dx.doi.org/10.1002/eji.200838815
94. Geiben-Lynn R, Greenland JR, Frimpong-Boateng K, Letvin NL. Kinetics of recombinant adenovirus type 5, vaccinia virus, modified vaccinia ankara virus, and DNA antigen expression in vivo and the induction of memory T-lymphocyte responses. Clin Vaccine Immunol 2008; 15:691-6; PMID:18272665; http://dx.doi.org/10.1128/CVI.00418-07
95. Pasquetto V, Bui HH, Giannino R, Banh C, Mirza F, Sidney J, Oseroff C, Tscharke DC, Irvine K, Bennink JR, et al. HLA-A∗0201, HLA-A∗1101, and HLA-B∗0702 transgenic mice recognize numerous poxvirus determinants from a wide variety of viral gene products. J Immunol 2005; 175:5504-15; PMID:16210659; http://dx.doi.org/10.4049/jimmunol.175.8.5504
96. Wilson EH, Hunter CA. Immunodominance and recognition of intracellular pathogens. J Infect Dis 2008; 198:1579-81; PMID:18922096; http://dx.doi.org/10.1086/593020
97. Sette A, Grey H, Oseroff C, Peters B, Moutaftsi M, Crotty S, Assarsson E, Greenbaum J, Kim Y, Kolla R, et al. Definition of epitopes and antigens recognized by vaccinia specific immune responses: their conservation in variola virus sequences, and use as a model system to study complex pathogens. Vaccine 2009; 27(Suppl 6):G21-6; PMID:20006135; http://dx.doi.org/10.1016/j.vaccine.2009.10.011
98. Kastenmuller W, Gasteiger G, Gronau JH, Baier R, Ljapoci R, Busch DH, Drexler I. Cross-competition of CD8+ T cells shapes the immunodominance hierarchy during boost vaccination. J Exp Med 2007; 204:2187-98; PMID:17709425; http://dx.doi.org/10.1084/jem.20070489
99. Assarsson E, Greenbaum JA, Sundström M, Schaffer L, Hammond JA, Pasquetto V, Oseroff C, Hendrickson RC, Lefkowitz EJ, Tscharke DC, et al. Kinetic analysis of a complete poxvirus transcriptome reveals an immediate-early class of genes. Proc Natl Acad Sci U S A 2008; 105:2140-5; PMID:18245380; http://dx.doi.org/10.1073/pnas.0711573105
100. Yang Z, Bruno DP, Martens CA, Porcella SF, Moss B. Simultaneous high-resolution analysis of vaccinia virus and host cell transcriptomes by deep RNA sequencing. Proc Natl Acad Sci U S A 2010; 107:11513-8; PMID:20534518; http://dx.doi.org/10.1073/pnas.1006594107
101. Sutter G, Moss B. Nonreplicating vaccinia vector efficiently expresses recombinant genes. Proc Natl Acad Sci U S A 1992; 89:10847-51; PMID:1438287; http://dx.doi.org/10.1073/pnas.89.22.10847
102. Orubu T, Alharbi NK, Lambe T, Gilbert SC, Cottingham MG. Expression and cellular immunogenicity of a transgenic antigen driven by endogenous poxviral early promoters at their authentic loci in MVA. PLoS One 2012; 7:e40167; PMID:22761956; http://dx.doi.org/10.1371/journal.pone.0040167
103. Chakrabarti S, Sisler JR, Moss B. Compact, synthetic, vaccinia virus early/late promoter for protein expression. Biotechniques 1997; 23:1094-7; PMID:9421642
104. Cochran MA, Puckett C, Moss B. In vitro mutagenesis of the promoter region for a vaccinia virus gene: evidence for tandem early and late regulatory signals. J Virol 1985; 54:30-7; PMID:3973982
105. Wyatt LS, Shors ST, Murphy BR, Moss B. Development of a replication-deficient recombinant vaccinia virus vaccine effective against parainfluenza virus 3 infection in an animal model. Vaccine 1996; 14:1451-8; PMID:8994321; http://dx.doi.org/10.1016/S0264-410X(96)00072-2
106. Liu X, Kremer M, Broyles SS. A natural vaccinia virus promoter with exceptional capacity to direct protein synthesis. J Virol Methods 2004; 122:141-5; PMID:15542137; http://dx.doi.org/10.1016/j.jviromet.2004.08.009
107. Di Pilato M, Mejías-Pérez E, Gómez CE, Perdiguero B, Sorzano CO, Esteban M. New vaccinia virus promoter as a potential candidate for future vaccines. J Gen Virol 2013; 94:2771-6; PMID:24077296; http://dx.doi.org/10.1099/vir.0.057299-0
108. Isshiki M, Zhang X, Sato H, Ohashi T, Inoue M, Shida H. Effects of different promoters on the virulence and immunogenicity of a HIV-1 Env-expressing recombinant vaccinia vaccine. Vaccine 2014; 32:839-45; PMID:24370703; http://dx.doi.org/10.1016/j.vaccine.2013.12.022
109. Wennier ST, Brinkmann K, Steinhäußer C, Mayländer N, Mnich C, Wielert U, Dirmeier U, Hausmann J, Chaplin P, Steigerwald R. A novel naturally occurring tandem promoter in modified vaccinia virus ankara drives very early gene expression and potent immune responses. PLoS One 2013; 8:e73511; PMID:23951355; http://dx.doi.org/10.1371/journal.pone.0073511
110. Dai K, Liu Y, Liu M, Xu J, Huang W, Huang X, Liu L, Wan Y, Hao Y, Shao Y. Pathogenicity and immunogenicity of recombinant Tiantan Vaccinia Virus with deleted C12L and A53R genes. Vaccine 2008; 26:5062-71; PMID:18573290; http://dx.doi.org/10.1016/j.vaccine.2008.06.011
111. Huang X, Lu B, Yu W, Fang Q, Liu L, Zhuang K, Shen T, Wang H, Tian P, Zhang L, et al. A novel replication-competent vaccinia vector MVTT is superior to MVA for inducing high levels of neutralizing antibody via mucosal vaccination. PLoS One 2009; 4:e4180; PMID:19159014; http://dx.doi.org/10.1371/journal.pone.0004180
112. Nájera JL, Gómez CE, García-Arriaza J, Sorzano CO, Esteban M. Insertion of vaccinia virus C7L host range gene into NYVAC-B genome potentiates immune responses against HIV-1 antigens. PLoS One 2010; 5:e11406; PMID:20613977; http://dx.doi.org/10.1371/journal.pone.0011406
113. Vijaysri S, Jentarra G, Heck MC, Mercer AA, McInnes CJ, Jacobs BL. Vaccinia viruses with mutations in the E3L gene as potential replication-competent, attenuated vaccines: intra-nasal vaccination. Vaccine 2008; 26:664-76; PMID:18096276; http://dx.doi.org/10.1016/j.vaccine.2007.11.045
114. Kibler KV, Gomez CE, Perdiguero B, Wong S, Huynh T, Holechek S, Arndt W, Jimenez V, Gonzalez-Sanz R, Denzler K, et al. Improved NYVAC-based vaccine vectors. PLoS One 2011; 6:e25674; PMID:22096477; http://dx.doi.org/10.1371/journal.pone.0025674
115. Quakkelaar ED, Redeker A, Haddad EK, Harari A, McCaughey SM, Duhen T, Filali-Mouhim A, Goulet JP, Loof NM, Ossendorp F, et al. Improved innate and adaptive immunostimulation by genetically modified HIV-1 protein expressing NYVAC vectors. PLoS One 2011; 6:e16819; PMID:21347234; http://dx.doi.org/10.1371/journal.pone.0016819
116. Sánchez-Sampedro L, Gómez CE, Mejías-Pérez E, Pérez-Jiménez E, Oliveros JC, Esteban M. Attenuated and replication-competent vaccinia virus strains M65 and M101 with distinct biology and immunogenicity as potential vaccine candidates against pathogens. J Virol 2013; 87:6955-74; PMID:23596295; http://dx.doi.org/10.1128/JVI.03013-12
117. Kennedy JS, Gurwith M, Dekker CL, Frey SE, Edwards KM, Kenner J, Lock M, Empig C, Morikawa S, Saijo M, et al. Safety and immunogenicity of LC16m8, an attenuated smallpox vaccine in vaccinia-naive adults. J Infect Dis 2011; 204:1395-402; PMID:21921208; http://dx.doi.org/10.1093/infdis/jir527
118. Kenner J, Cameron F, Empig C, Jobes DV, Gurwith M. LC16m8: an attenuated smallpox vaccine. Vaccine 2006; 24:7009-22; PMID:17052815; http://dx.doi.org/10.1016/j.vaccine.2006.03.087
119. Saito T, Fujii T, Kanatani Y, Saijo M, Morikawa S, Yokote H, Takeuchi T, Kuwabara N. Clinical and immunological response to attenuated tissue-cultured smallpox vaccine LC16m8. JAMA 2009; 301:1025-33; PMID:19278946; http://dx.doi.org/10.1001/jama.2009.289
120. Xiao H, Liu L, Zhu Q, Tan Z, Yu W, Tang X, Zhan D, Du Y, Wang H, Liu D, et al. A replicating modified vaccinia tiantan strain expressing an avian-derived influenza H5N1 hemagglutinin induce broadly neutralizing antibodies and cross-clade protective immunity in mice. PLoS One 2013; 8:e83274; PMID:24358269; http://dx.doi.org/10.1371/journal.pone.0083274
121. Zhu R, Huang W, Wang W, Liu Q, Nie J, Meng S, Yu Y, Wang Y. Comparison on virulence and immunogenicity of two recombinant vaccinia vaccines, Tian Tan and Guang9 strains, expressing the HIV-1 envelope gene. PLoS One 2012; 7:e48343; PMID:23139778; http://dx.doi.org/10.1371/journal.pone.0048343
122. Chan WM, Rahman MM, McFadden G. Oncolytic myxoma virus: the path to clinic. Vaccine 2013; 31:4252-8; PMID:23726825; http://dx.doi.org/10.1016/j.vaccine.2013.05.056
123. Yang S, Carroll MW, Torres-Duarte AP, Moss B, Davidson EA. Addition of the MSA1 signal and anchor sequences to the malaria merozoite surface antigen 1 C-terminal region enhances immunogenicity when expressed by recombinant vaccinia virus. Vaccine 1997; 15:1303-13; PMID:9302735; http://dx.doi.org/10.1016/S0264-410X(97)00039-X
124. Santra S, Liao HX, Zhang R, Muldoon M, Watson S, Fischer W, Theiler J, Szinger J, Balachandran H, Buzby A, et al. Mosaic vaccines elicit CD8+ T lymphocyte responses that confer enhanced immune coverage of diverse HIV strains in monkeys. Nat Med 2010; 16:324-8; PMID:20173754; http://dx.doi.org/10.1038/nm.2108
125. Barouch DH, Stephenson KE, Borducchi EN, Smith K, Stanley K, McNally AG, Liu J, Abbink P, Maxfield LF, Seaman MS, et al. Protective efficacy of a global HIV-1 mosaic vaccine against heterologous SHIV challenges in rhesus monkeys. Cell 2013; 155:531-9; PMID:24243013; http://dx.doi.org/10.1016/j.cell.2013.09.061
126. Hanke T. Conserved immunogens in prime-boost strategies for the next-generation HIV-1 vaccines. Expert Opin Biol Ther 2014; 14:601-16; PMID:24490585; http://dx.doi.org/10.1517/14712598.2014.885946
127. Gómez CE, Nájera JL, Jiménez V, Bieler K, Wild J, Kostic L, Heidari S, Chen M, Frachette MJ, Pantaleo G, et al. Generation and immunogenicity of novel HIV/AIDS vaccine candidates targeting HIV-1 Env/Gag-Pol-Nef antigens of clade C. Vaccine 2007; 25:1969-92; PMID:17224219; http://dx.doi.org/10.1016/j.vaccine.2006.11.051
128. Bart PA, Goodall R, Barber T, Harari A, Guimaraes-Walker A, Khonkarly M, Sheppard NC, Bangala Y, Frachette MJ, Wagner R, et al.; EuroVacc Consortium. EV01: a phase I trial in healthy HIV negative volunteers to evaluate a clade C HIV vaccine, NYVAC-C undertaken by the EuroVacc Consortium. Vaccine 2008; 26:3153-61; PMID:18502002; http://dx.doi.org/10.1016/j.vaccine.2008.03.083
129. García F, Bernaldo de Quirós JC, Gómez CE, Perdiguero B, Nájera JL, Jiménez V, García-Arriaza J, Guardo AC, Pérez I, Díaz-Brito V, et al. Safety and immunogenicity of a modified pox vector-based HIV/AIDS vaccine candidate expressing Env, Gag, Pol and Nef proteins of HIV-1 subtype B (MVA-B) in healthy HIV-1-uninfected volunteers: A phase I clinical trial (RISVAC02). Vaccine 2011; 29:8309-16; PMID:21907749; http://dx.doi.org/10.1016/j.vaccine.2011.08.098
130. Gómez CE, Nájera JL, Perdiguero B, García-Arriaza J, Sorzano CO, Jiménez V, González-Sanz R, Jiménez JL, Muñoz-Fernández MA, López Bernaldo de Quirós JC, et al. The HIV/AIDS vaccine candidate MVA-B administered as a single immunogen in humans triggers robust, polyfunctional, and selective effector memory T cell responses to HIV-1 antigens. J Virol 2011; 85:11468-78; PMID:21865377; http://dx.doi.org/10.1128/JVI.05165-11
131. Harari A, Bart PA, Stöhr W, Tapia G, Garcia M, Medjitna-Rais E, Burnet S, Cellerai C, Erlwein O, Barber T, 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; PMID:18195071; http://dx.doi.org/10.1084/jem.20071331
132. McCormack S, Stöhr W, Barber T, Bart PA, Harari A, Moog C, Ciuffreda D, Cellerai C, Cowen M, Gamboni R, 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. Vaccine 2008; 26:3162-74; PMID:18502003; http://dx.doi.org/10.1016/j.vaccine.2008.02.072
133. Rerks-Ngarm S, Pitisuttithum P, Nitayaphan S, Kaewkungwal J, Chiu J, Paris R, Premsri N, Namwat C, de Souza M, Adams E, et al.; MOPHTAVEG Investigators. Vaccination with ALVAC and AIDSVAX to prevent HIV-1 infection in Thailand. N Engl J Med 2009; 361:2209-20; PMID:19843557; http://dx.doi.org/10.1056/NEJMoa0908492
134. Chung AW, Ghebremichael M, Robinson H, Brown E, Choi I, Lane S, Dugast AS, Schoen MK, Rolland M, Suscovich TJ, et al. Polyfunctional Fc-Effector Profiles Mediated by IgG Subclass Selection Distinguish RV144 and VAX003 Vaccines. Sci Transl Med. 2014 Mar 19;6(228):228ra38
135. Gottardo R, Bailer RT, Korber BT, Gnanakaran S, Phillips J, Shen X, Tomaras GD, Turk E, Imholte G, Eckler L, et al. Plasma IgG to linear epitopes in the V2 and V3 regions of HIV-1 gp120 correlate with a reduced risk of infection in the RV144 vaccine efficacy trial. PLoS One 2013; 8:e75665; PMID:24086607; http://dx.doi.org/10.1371/journal.pone.0075665
136. Haynes BF, Gilbert PB, McElrath MJ, Zolla-Pazner S, Tomaras GD, Alam SM, Evans DT, Montefiori DC, Karnasuta C, Sutthent R, et al. Immunecorrelates analysis of an HIV-1 vaccine efficacy trial. N Engl J Med 2012; 366:1275-86; PMID:22475592; http://dx.doi.org/10.1056/NEJMoa1113425
137. Yates NL, Liao HX, Fong Y, Decamp A, Vandergrift NA, Williams WT, Alam SM, Ferrari G, Yang ZY, Seaton KE, et al. Vaccine-Induced Env V1-V2 IgG3 Correlates with Lower HIV-1 Infection Risk and Declines Soon After Vaccination. Sci Transl Med. 2014;6(228):228ra39
138. Zolla-Pazner S, deCamp A, Gilbert PB, Williams C, Yates NL, Williams WT, Howington R, Fong Y, Morris DE, Soderberg KA, et al. Vaccine-induced IgG antibodies to V1V2 regions of multiple HIV-1 subtypes correlate with decreased risk of HIV-1 infection. PLoS One 2014; 9:e87572; PMID:24504509; http://dx.doi.org/10.1371/journal.pone.0087572
139. McKay PF, Cope AV, Mann JF, Joseph S, Esteban M, Tatoud R, Carter D, Reed SG, Weber J, Shattock RJ. Glucopyranosyl lipid A adjuvant significantly enhances HIV specific T and B cell responses elicited by a DNA-MVA-protein vaccine regimen. PLoS One 2014; 9:e84707; PMID:24465426; http://dx.doi.org/10.1371/journal.pone.0084707
140. Fouda GG, Amos JD, Wilks AB, Pollara J, Ray CA, Chand A, Kunz EL, Liebl BE, Whitaker K, Carville A, et al. Mucosal immunization of lactating female rhesus monkeys with a transmitted/founder HIV-1 envelope induces strong Env-specific IgA antibody responses in breast milk. J Virol 2013; 87:6986-99; PMID:23596289; http://dx.doi.org/10.1128/JVI.00528-13
141. Pattacini L, Mize GJ, Graham JB, Fluharty TR, Graham TM, Lingnau K, Wizel B, Perdiguero B, Esteban M, Pantaleo G, et al. A novel HIV vaccine adjuvanted by IC31 induces robust and persistent humoral and cellular immunity. PLoS One 2012; 7:e42163; PMID:22848738; http://dx.doi.org/10.1371/journal.pone.0042163
142. Flynn BJ, Kastenmüller K, Wille-Reece U, Tomaras GD, Alam M, Lindsay RW, Salazar AM, Perdiguero B, Gomez CE, Wagner R, et al. Immunization with HIV Gag targeted to dendritic cells followed by recombinant New York vaccinia virus induces robust T-cell immunity in nonhuman primates. Proc Natl Acad Sci U S A 2011; 108:7131-6; PMID:21467219; http://dx.doi.org/10.1073/pnas.1103869108
143. Collado M, Rodríguez D, Rodríguez JR, Vázquez I, Gonzalo RM, Esteban M. Chimeras between the human immunodeficiency virus (HIV-1) Env and vaccinia virus immunogenic proteins p14 and p39 generate in mice broadly reactive antibodies and specific activation of CD8+ T cell responses to Env. Vaccine 2000; 18:3123-33; PMID:10856792; http://dx.doi.org/10.1016/S0264-410X(00)00112-2
144. Vijayan A, Gómez CE, Espinosa DA, Goodman AG, Sanchez-Sampedro L, Sorzano CO, Zavala F, Esteban M. Adjuvant-like effect of vaccinia virus 14K protein: a case study with malaria vaccine based on the circumsporozoite protein. J Immunol 2012; 188:6407-17; PMID:22615208; http://dx.doi.org/10.4049/jimmunol.1102492