Adenovirus-5-vectored P. falciparum vaccine expressing CSP and AMA1. Part B: Safety, immunogenicity and protective efficacy of the CSP component

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Tamminga, Cindy ^a   Sedegah, Martha ^a   Regis, David ^a   Chuang, Ilin ^a   Epstein, Judith E ^a   Spring, Michele ^b,d   Mendoza Silveiras, Jose ^a,d   McGrath, Shannon ^b,c   Maiolatesi, Santina ^a,d   Reyes, Sharina ^a,d   Steinbeiss, Victoria ^a,d   Fedders, Charlotte ^a,d   Smith, Kathryn ^a,d   House, Brent ^a   Ganeshan, Harini ^a,d   Lejano, Jennylynn ^a,d   Abot, Esteban ^a,d   Banania, Glenna J ^a,d   Sayo, Renato ^a,d   Farooq, Fouzia ^a,d   Belmonte, Maria ^a,d   Murphy, Jittawadee ^b   Komisar, Jack ^b   Williams, Jackie ^b,c   Shi, Meng ^a,b   Brambilla, Donald ^e   Manohar, Nalini ^a,d   Richie, Nancy O ^b,c   Wood, Chloe ^b,c   Limbach, Keith ^a,d   Patterson, Noelle B ^a,d   Bruder, Joseph T ^f   Doolan, Denise L ^a,j   King, C Richter ^f   Diggs, Carter ^g   Soisson, Lorraine ^g   Carucci, Daniel ^a,k   Levine, Gail ^h   Dutta, Sheetij ^b,c   Hollingdale, Michael R ⁱ   Ockenhouse, Christian F ^b   Richie, Thomas L ^a   more..

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

^b WALTER REED ARMY INSTITUTE OF RESEARCH   (United States)

^c Clinical Research Management   (United States)

^d HENRY M JACKSON FOUNDATION FOR THE ADVANCEMENT OF MILITARY MEDICINE   (United States)

^e RTI INTERNATIONAL   (United States)

^f GENVEC INC   (United States)

^g UNITED STATES AGENCY FOR INTERNATIONAL DEVELOPMENT   (United States)

^h NATIONAL INSTITUTES OF HEALTH   (United States)

ⁱ NMRC   (United States)

^j QIMR BERGHOFER MEDICAL RESEARCH INSTITUTE   (Australia)

^k UNITED NATIONS   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; APICAL MEMBRANE ANTIGEN 1; CIRCUMSPOROZOITE PROTEIN; MALARIA VACCINE; APICAL MEMBRANE ANTIGEN I, PLASMODIUM; CIRCUMSPOROZOITE PROTEIN, PROTOZOAN; MEMBRANE PROTEIN; PARASITE ANTIGEN; PROTOZOAL PROTEIN;

ADENOVIRUS 5; ADULT; ANTIBODY RESPONSE; ARTICLE; CELLULAR IMMUNITY; CHILL; CONJUNCTIVITIS; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; DIARRHEA; DIZZINESS; DRUG EFFICACY; DRUG SAFETY; DRUG TOLERABILITY; ENZYME LINKED IMMUNOSPOT ASSAY; EYE IRRITATION; EYE PAIN; FATIGUE; FEMALE; FEVER; HEADACHE; HUMAN; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOFLUORESCENCE TEST; IMMUNOGENICITY; MALAISE; MALARIA FALCIPARUM; MALE; NAUSEA; NONHUMAN; NOSE CONGESTION; PAIN; PHARYNGITIS; PLASMODIUM FALCIPARUM; SERODIAGNOSIS; URTICARIA; VOMITING; ADENOVIRUS; ADOLESCENT; CLINICAL TRIAL; CYTOLOGY; DOSE RESPONSE; GENE EXPRESSION; GENE VECTOR; GENETICS; IMMUNOLOGY; MIDDLE AGED; SPOROZOITE;

ADENOVIRIDAE; HUMAN ADENOVIRUS TYPE 5; PLASMODIUM FALCIPARUM;

ADENOVIRIDAE; ADOLESCENT; ADULT; ANTIGENS, PROTOZOAN; DOSE-RESPONSE RELATIONSHIP, IMMUNOLOGIC; FEMALE; GENE EXPRESSION; GENETIC VECTORS; HUMANS; MALARIA VACCINES; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; SPOROZOITES; YOUNG ADULT;

EID: 80053894662     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025868     Document Type: Article

References (84)

1. WHO, (2009) World Malaria Report. http://wwwwhoint/malaria/world_malaria_report_2009/en/indexhtml.
2. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, et al. (2008) Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 359: 2619-2620.
3. Sigler CI, Leland P, Hollingdale MR, (1984) In vitro infectivity of irradiated Plasmodium berghei sporozoites to cultured hepatoma cells. Am J Trop Med Hyg 33: 544-547.
4. Nussenzweig RS, Vanderberg J, Most H, Orton C, (1967) Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. Nature 216: 160-162.
5. Hoffman SL, Goh LM, Luke TC, Schneider I, Le TP, et al. (2002) Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. J Infect Dis 185: 1155-1164.
6. Schmidt NW, Podyminogin RL, Butler NS, Badovinac VP, Tucker BJ, et al. (2008) Memory CD8 T cell responses exceeding a large but definable threshold provide long-term immunity to malaria. Proc Natl Acad Sci U S A 105: 14017-14022.
7. Oliveira GA, Kumar KA, Calvo-Calle JM, Othoro C, Altszuler D, et al. (2008) Class II-restricted protective immunity induced by malaria sporozoites. Infect Immun 76: 1200-1206.
8. Tarun AS, Dumpit RF, Camargo N, Labaied M, Liu P, et al. (2007) Protracted sterile protection with Plasmodium yoelii pre-erythrocytic genetically attenuated parasite malaria vaccines is independent of significant liver-stage persistence and is mediated by CD8+ T cells. J Infect Dis 196: 608-616.
9. Doolan DL, Hoffman SL, (2000) The complexity of protective immunity against liver-stage malaria. J Immunol 165: 1453-1462.
10. Doolan DL, Martinez-Alier N, (2006) Immune response to pre-erythrocytic stages of malaria parasites. Curr Mol Med 6: 169-185.
11. Fowkes FJ, Richards JS, Simpson JA, Beeson JG, The relationship between anti-merozoite antibodies and incidence of Plasmodium falciparum malaria: A systematic review and meta-analysis. PLoS Med 7: e1000218.
12. Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, et al. (1991) Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg 45: 297-308.
13. Beeson JG, Osier FH, Engwerda CR, (2008) Recent insights into humoral and cellular immune responses against malaria. Trends Parasitol 24: 578-584.
14. Marsh K, Kinyanjui S, (2006) Immune effector mechanisms in malaria. Parasite Immunol 28: 51-60.
15. Stoute JA, Slaoui M, Heppner DG, Momin P, Kester KE, et al. (1997) A preliminary evaluation of a recombinant circumsporozoite protein vaccine against Plasmodium falciparum malaria. RTS,S Malaria Vaccine Evaluation Group. N Engl J Med 336: 86-91.
16. Aponte JJ, Aide P, Renom M, Mandomando I, Bassat Q, et al. (2007) Safety of the RTS,S/AS02D candidate malaria vaccine in infants living in a highly endemic area of Mozambique: a double blind randomised controlled phase I/IIb trial. Lancet 370: 1543-1551.
17. Overstreet MG, Cockburn IA, Chen YC, Zavala F, (2008) Protective CD8 T cells against Plasmodium liver stages: immunobiology of an 'unnatural' immune response. Immunol Rev 225: 272-283.
18. Frevert U, Moreno A, Calvo-Calle JM, Klotz C, Nardin E, (2009) Imaging effector functions of human cytotoxic CD4+ T cells specific for Plasmodium falciparum circumsporozoite protein. Int J Parasitol 39: 119-132.
19. Kumar KA, Sano G, Boscardin S, Nussenzweig RS, Nussenzweig MC, et al. (2006) The circumsporozoite protein is an immunodominant protective antigen in irradiated sporozoites. Nature 444: 937-940.
20. Narum DL, Thomas AW, (1994) Differential localization of full-length and processed forms of PF83/AMA-1 an apical membrane antigen of Plasmodium falciparum merozoites. Mol Biochem Parasitol 67: 59-68.
21. Remarque EJ, Faber BW, Kocken CH, Thomas AW, (2008) Apical membrane antigen 1: a malaria vaccine candidate in review. Trends Parasitol 24: 74-84.
22. Silvie O, Franetich JF, Charrin S, Mueller MS, Siau A, et al. (2004) A role for apical membrane antigen 1 during invasion of hepatocytes by Plasmodium falciparum sporozoites. J Biol Chem 279: 9490-9496.
23. Thomas AW, Trape JF, Rogier C, Goncalves A, Rosario VE, et al. (1994) High prevalence of natural antibodies against Plasmodium falciparum 83-kilodalton apical membrane antigen (PF83/AMA-1) as detected by capture-enzyme-linked immunosorbent assay using full-length baculovirus recombinant PF83/AMA-1. Am J Trop Med Hyg 51: 730-740.
24. Thomas AW, Narum D, Waters AP, Trape JF, Rogier C, et al. (1994) Aspects of immunity for the AMA-1 family of molecules in humans and non-human primates malarias. Mem Inst Oswaldo Cruz 89 (Suppl 2): 67-70.
25. Udhayakumar V, Kariuki S, Kolczack M, Girma M, Roberts JM, et al. (2001) Longitudinal study of natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in a holoendemic region of malaria in western Kenya: Asembo Bay Cohort Project VIII. Am J Trop Med Hyg 65: 100-107.
26. Polley SD, Mwangi T, Kocken CH, Thomas AW, Dutta S, et al. (2004) Human antibodies to recombinant protein constructs of Plasmodium falciparum Apical Membrane Antigen 1 (AMA1) and their associations with protection from malaria. Vaccine 23: 718-728.
27. Lal AA, Hughes MA, Oliveira DA, Nelson C, Bloland PB, et al. (1996) Identification of T-cell determinants in natural immune responses to the Plasmodium falciparum apical membrane antigen (AMA-1) in an adult population exposed to malaria. Infect Immun 64: 1054-1059.
28. Stowers AW, Cioce V, Shimp RL, Lawson M, Hui G, et al. (2001) Efficacy of two alternate vaccines based on Plasmodium falciparum merozoite surface protein 1 in an Aotus challenge trial. Infect Immun 69: 1536-1546.
29. Malkin EM, Diemert DJ, McArthur JH, Perreault JR, Miles AP, et al. (2005) Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum malaria. Infect Immun 73: 3677-3685.
30. Saul A, Lawrence G, Allworth A, Elliott S, Anderson K, et al. (2005) A human phase 1 vaccine clinical trial of the Plasmodium falciparum malaria vaccine candidate apical membrane antigen 1 in Montanide ISA720 adjuvant. Vaccine 23: 3076-3083.
31. Dicko A, Diemert DJ, Sagara I, Sogoba M, Niambele MB, et al. (2007) Impact of a Plasmodium falciparum AMA1 Vaccine on Antibody Responses in Adult Malians. PLoS ONE 2: e1045.
32. Dicko A, Sagara I, Ellis RD, Miura K, Guindo O, et al. (2008) Phase 1 study of a combination AMA1 blood stage malaria vaccine in Malian children. PLoS ONE 3: e1563.
33. Huaman MC, Mullen GE, Long CA, Mahanty S, (2009) Plasmodium falciparum apical membrane antigen 1 vaccine elicits multifunctional CD4 cytokine-producing and memory T cells. Vaccine 27: 5239-5246.
34. Spring MD, Cummings JF, Ockenhouse CF, Dutta S, Reidler R, et al. (2009) Phase 1/2a study of the malaria vaccine candidate apical membrane antigen-1 (AMA-1) administered in adjuvant system AS01B or AS02A. PLoS One 4: e5254.
35. Brice GT, Dobano C, Sedegah M, Stefaniak M, Graber NL, et al. (2007) Extended immunization intervals enhance the immunogenicity and protective efficacy of plasmid DNA vaccines. Microbes Infect 9: 1439-1446.
36. Sedegah M, Hoffman SL, (2006) Immunological responses of neonates and infants to DNA vaccines. Methods Mol Med 127: 239-251.
37. Wang R, Epstein J, Charoenvit Y, Baraceros FM, Rahardjo N, et al. (2004) Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. J Immunol 172: 5561-5569.
38. Epstein JE, Charoenvit Y, Kester KE, Wang R, Newcomer R, et al. (2004) Safety, tolerability, and antibody responses in humans after sequential immunization with a PfCSP DNA vaccine followed by the recombinant protein vaccine RTS,S/AS02A. Vaccine 22: 1592-1603.
39. Sedegah M, Brice GT, Rogers WO, Doolan DL, Charoenvit Y, et al. (2002) Persistence of protective immunity to malaria induced by DNA priming and poxvirus boosting: characterization of effector and memory CD8(+)-T-cell populations. Infect Immun 70: 3493-3499.
40. Jiang G, Charoenvit Y, Moreno A, Baraceros MF, Banania G, et al. (2007) Induction of multi-antigen multi-stage immune responses against Plasmodium falciparum in rhesus monkeys, in the absence of antigen interference, with heterologous DNA prime/poxvirus boost immunization. Malar J 6: 135.
41. Rogers WO, Weiss WR, Kumar A, Aguiar JC, Tine JA, et al. (2002) Protection of rhesus macaques against lethal Plasmodium knowlesi malaria by a heterologous DNA priming and poxvirus boosting immunization regimen. Infect Immun 70: 4329-4335.
42. Weiss WR, Kumar A, Jiang G, Williams J, Bostick A, et al. (2007) Protection of rhesus monkeys by a DNA prime/poxvirus boost malaria vaccine depends on optimal DNA priming and inclusion of blood stage antigens. PLoS ONE 2: e1063.
43. Rodriguez A, Goudsmit J, Companjen A, Mintardjo R, Gillissen G, et al. (2008) Impact of recombinant adenovirus serotype 35 priming versus boosting of a Plasmodium falciparum protein: characterization of T- and B-cell responses to liver-stage antigen 1. Infect Immun 76: 1709-1718.
44. Jiang G, Shi M, Conteh S, Richie N, Banania G, et al. (2009) Sterile protection against Plasmodium knowlesi in rhesus monkeys from a malaria vaccine: comparison of heterologous prime boost strategies. PLoS One 4: e6559.
45. Stewart MJ, Nawrot RJ, Schulman S, Vanderberg JP, (1986) Plasmodium berghei sporozoite invasion is blocked in vitro by sporozoite-immobilizing antibodies. Infect Immun 51: 859-864.
46. Stewart VA, McGrath SM, Dubois PM, Pau MG, Mettens P, et al. (2007) Priming with an adenovirus 35-circumsporozoite protein (CS) vaccine followed by RTS,S/AS01B boosting significantly improves immunogenicity to Plasmodium falciparum CS compared to that with either malaria vaccine alone. Infect Immun 75: 2283-2290.
47. Bojang KA, Milligan PJ, Pinder M, Vigneron L, Alloueche A, et al. (2001) Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 358: 1927-1934.
48. Bojang KA, Olodude F, Pinder M, Ofori-Anyinam O, Vigneron L, et al. (2005) Safety and immunogenicty of RTS,S/AS02A candidate malaria vaccine in Gambian children. Vaccine 23: 4148-4157.
49. Kester KE, McKinney DA, Tornieporth N, Ockenhouse CF, Heppner DG Jr, et al. (2007) A phase I/IIa safety, immunogenicity, and efficacy bridging randomized study of a two-dose regimen of liquid and lyophilized formulations of the candidate malaria vaccine RTS,S/AS02A in malaria-naive adults. Vaccine 25: 5359-5366.
50. Sun P, Schwenk R, White K, Stoute JA, Cohen J, et al. (2003) Protective immunity induced with malaria vaccine, RTS,S, is linked to Plasmodium falciparum circumsporozoite protein-specific CD4+ and CD8+ T cells producing IFN-gamma. J Immunol 171: 6961-6967.
51. Mettens P, Dubois PM, Demoitie MA, Bayat B, Donner MN, et al. (2008) Improved T cell responses to Plasmodium falciparum circumsporozoite protein in mice and monkeys induced by a novel formulation of RTS,S vaccine antigen. Vaccine 26: 1072-1082.
52. Reyes-Sandoval A, Sridhar S, Berthoud T, Moore AC, Harty JT, et al. (2008) Single-dose immunogenicity and protective efficacy of simian adenoviral vectors against Plasmodium berghei. Eur J Immunol 38: 732-741.
53. Rodrigues EG, Zavala F, Eichinger D, Wilson JM, Tsuji M, (1997) Single immunizing dose of recombinant adenovirus efficiently induces CD8+ T cell-mediated protective immunity against malaria. J Immunol 158: 1268-1274.
54. Shiratsuchi T, Rai U, Krause A, Worgall S, Tsuji M, (2011) Replacing adenoviral vector HVR1 with a malaria B cell epitope improves immunogenicity and circumvents preexisting immunity to adenovirus in mice. J Clin Invest 120: 3688-3701.
55. Gaziano TA, Young CR, Fitzmaurice G, Atwood S, Gaziano JM, (2008) Laboratory-based versus non-laboratory-based method for assessment of cardiovascular disease risk: the NHANES I Follow-up Study cohort. Lancet 371: 923-931.
56. Doolan DL, Hoffman SL, Southwood S, Wentworth PA, Sidney J, et al. (1997) Degenerate cytotoxic T cell epitopes from P. falciparum restricted by multiple HLA-A and HLA-B supertype alleles. Immunity 7: 97-112.
57. Blum-Tirouvanziam U, Servis C, Habluetzel A, Valmori D, Men Y, et al. (1995) Localization of HLA-A2.1-restricted T cell epitopes in the circumsporozoite protein of Plasmodium falciparum. J Immunol 154: 3922-3931.
58. Good MF, Pombo D, Quakyi IA, Riley EM, Houghten RA, et al. (1988) Human T-cell recognition of the circumsporozoite protein of Plasmodium falciparum: immunodominant T-cell domains map to the polymorphic regions of the molecule. Proc Natl Acad Sci U S A 85: 1199-1203.
59. Ockenhouse CF, Angov E, Kester KE, Diggs C, Soisson L, et al. (2006) Phase I safety and immunogenicity trial of FMP1/AS02A, a Plasmodium falciparum MSP-1 asexual blood stage vaccine. Vaccine 24: 3009-3017.
60. Charoenvit Y, Mellouk S, Cole C, Bechara R, Leef MF, et al. (1991) Monoclonal, but not polyclonal, antibodies protect against Plasmodium yoelii sporozoites. J Immunol 146: 1020-1025.
61. Chulay JD, Schneider I, Cosgriff TM, Hoffman SL, Ballou WR, et al. (1986) Malaria transmitted to humans by mosquitoes infected from cultured Plasmodium falciparum. Am J Trop Med Hyg 35: 66-68.
62. Harro CD, Robertson MN, Lally MA, O'Neill LD, Edupuganti S, et al. (2009) Safety and immunogenicity of adenovirus-vectored near-consensus HIV type 1 clade B gag vaccines in healthy adults. AIDS Res Hum Retroviruses 25: 103-114.
63. Sprangers MC, Lakhai W, Koudstaal W, Verhoeven M, Koel BF, et al. (2003) Quantifying adenovirus-neutralizing antibodies by luciferase transgene detection: addressing preexisting immunity to vaccine and gene therapy vectors. J Clin Microbiol 41: 5046-5052.
64. Priddy FH, Brown D, Kublin J, Monahan K, Wright DP, et al. (2008) Safety and immunogenicity of a replication-incompetent adenovirus type 5 HIV-1 clade B gag/pol/nef vaccine in healthy adults. Clin Infect Dis 46: 1769-1781.
65. Zhu J, Huang X, Yang Y, (2007) Innate immune response to adenoviral vectors is mediated by both Toll-like receptor-dependent and-independent pathways. J Virol 81: 3170-3180.
66. Krieg AM, Efler SM, Wittpoth M, Al Adhami MJ, Davis HL, (2004) Induction of systemic TH1-like innate immunity in normal volunteers following subcutaneous but not intravenous administration of CPG 7909, a synthetic B-class CpG oligodeoxynucleotide TLR9 agonist. J Immunother 27: 460-471.
67. Leonard JP, Link BK, Emmanouilides C, Gregory SA, Weisdorf D, et al. (2007) Phase I trial of toll-like receptor 9 agonist PF-3512676 with and following rituximab in patients with recurrent indolent and aggressive non Hodgkin's lymphoma. Clin Cancer Res 13: 6168-6174.
68. Ellis RD, Martin LB, Shaffer D, Long CA, Miura K, et al. Phase 1 trial of the Plasmodium falciparum blood stage vaccine MSP1(42)-C1/Alhydrogel with and without CPG 7909 in malaria naive adults. PLoS ONE 5: e8787.
69. Kester KE, Cummings JF, Ofori-Anyinam O, Ockenhouse CF, Krzych U, et al. (2009) Randomized, double-blind, phase 2a trial of falciparum malaria vaccines RTS,S/AS01B and RTS,S/AS02A in malaria-naive adults: safety, efficacy, and immunologic associates of protection. J Infect Dis 200: 337-346.
70. Moorthy VS, Ballou WR, (2009) Immunological mechanisms underlying protection mediated by RTS,S: a review of the available data. Malar J 8: 312.
71. Kester KE, Cummings JF, Ockenhouse CF, Nielsen R, Hall BT, et al. (2008) Phase 2a trial of 0, 1, and 3 month and 0, 7, and 28 day immunization schedules of malaria vaccine RTS,S/AS02 in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 26: 2191-2202.
72. Cox KS, Clair JH, Prokop MT, Sykes KJ, Dubey SA, et al. (2008) DNA gag/adenovirus type 5 (Ad5) gag and Ad5 gag/Ad5 gag vaccines induce distinct T-cell response profiles. J Virol 82: 8161-8171.
73. Asmuth DM, Brown EL, DiNubile MJ, Sun X, del Rio C, et al. (2009) Comparative cell-mediated immunogenicity of DNA/DNA, DNA/adenovirus type 5 (Ad5), or Ad5/Ad5 HIV-1 clade B gag vaccine prime-boost regimens. J Infect Dis 201: 132-141.
74. Harvey BG, Hackett NR, El-Sawy T, Rosengart TK, Hirschowitz EA, et al. (1999) Variability of human systemic humoral immune responses to adenovirus gene transfer vectors administered to different organs. J Virol 73: 6729-6742.
75. Seder RA, Darrah PA, Roederer M, (2008) T-cell quality in memory and protection: implications for vaccine design. Nat Rev Immunol 8: 247-258.
76. Cheng C, Gall JG, Nason M, King CR, Koup RA,et al. Differential specificity and immunogenicity of adenovirus type 5 neutralizing antibodies elicited by natural infection or immunization. J Virol 84: 630-638.
77. McCoy K, Tatsis N, Korioth-Schmitz B, Lasaro MO, Hensley SE, et al. (2007) Effect of preexisting immunity to adenovirus human serotype 5 antigens on the immune responses of nonhuman primates to vaccine regimens based on human- or chimpanzee-derived adenovirus vectors. J Virol 81: 6594-6604.
78. Sedegah M, Charoenvit Y, Aguiar J, Sacci J, Hedstrom R, et al. (2004) Effect on antibody and T-cell responses of mixing five GMP-produced DNA plasmids and administration with plasmid expressing GM-CSF. Genes Immun 5: 553-561.
79. Pichyangkul S, Tongtawe P, Kum-Arb U, Yongvanitchit K, Gettayacamin M, et al. (2009) Evaluation of the safety and immunogenicity of Plasmodium falciparum apical membrane antigen 1, merozoite surface protein 1 or RTS,S vaccines with adjuvant system AS02A administered alone or concurrently in rhesus monkeys. Vaccine 28: 452-462.
80. Sedegah M, Charoenvit Y, Minh L, Belmonte M, Majam VF, et al. (2004) Reduced immunogenicity of DNA vaccine plasmids in mixtures. Gene Ther 11: 448-456.
81. Cerullo V, Seiler MP, Mane V, Brunetti-Pierri N, Clarke C, et al. (2007) Toll-like receptor 9 triggers an innate immune response to helper-dependent adenoviral vectors. Mol Ther 15: 378-385.
82. Dunachie SJ, Walther M, Epstein JE, Keating S, Berthoud T, et al. (2006) 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 74: 5933-5942.
83. Kalia V, Sarkar S, Ahmed R CD8 T-cell memory differentiation during acute and chronic viral infections. Adv Exp Med Biol 684: 79-95.
84. Wherry EJ, Ahmed R, (2004) Memory CD8 T-cell differentiation during viral infection. J Virol 78: 5535-5545.