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

Malaria Journal

Volumn 6, Issue , 2007, Pages

  Jiang, George ^a,b   Charoenvit, Yupin ^a   Moreno, Alberto ^c,d   Baraceros, Maria F ^a,b   Banania, Glenna ^a,b   Richie, Nancy ^a,b   Abot, Steve ^a,b   Ganeshan, Harini ^a,b   Fallarme, Victoria ^a,b   Patterson, Noelle B ^a,b   Geall, Andrew ^e   Weiss, Walter R ^a   Strobert, Elizabeth ^d   Caro Aquilar, Ivette ^d   Lanar, David E ^f   Saul, Allan ^g   Martin, Laura B ^g   Gowda, Kalpana ^a   Morrissette, Craig R ^f   Kaslow, David C ^e   Carucci, Daniel J ^a   Galinski, Mary R ^c,d   Doolan, Denise L ^a,h,i   more..

^a NAVAL MEDICAL RESEARCH CENTER   (United States)

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

^c EMORY UNIVERSITY   (United States)

^d EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e VICAL INC   (United States)

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

^g NATIONAL INSTITUTES OF HEALTH   (United States)

^h JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

ⁱ ROYAL BRISBANE AND WOMEN'S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

CD4 ANTIGEN; CYTOKINE; DNA VACCINE; GAMMA INTERFERON; INTERLEUKIN 2; PARASITE ANTIGEN; PHOSPHATE BUFFERED SALINE; PLASMID DNA; POLOXAMER; POLOXAMER CRL 1005; RECOMBINANT PROTEIN; SYNTHETIC PEPTIDE; UNCLASSIFIED DRUG; VIRUS VACCINE; MALARIA VACCINE; PROTOZOON ANTIBODY;

ALVAC PF7; ANTIBODY RESPONSE; ARTICLE; CANARYPOX VIRUS; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; COMPARATIVE STUDY; ENZYME LINKED IMMUNOSPOT ASSAY; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOASSAY; IMMUNOGENICITY; NONHUMAN; PLASMODIUM FALCIPARUM; POXVIRUS; RHESUS MONKEY; STAINING; STATISTICAL ANALYSIS; T LYMPHOCYTE; ANIMAL; BIOSYNTHESIS; GENETICS; IMMUNOLOGY; MACACA; MALARIA FALCIPARUM; METHODOLOGY; PLASMID;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; IMMUNIZATION; IMMUNIZATION, SECONDARY; MACACA MULATTA; MALARIA VACCINES; MALARIA, FALCIPARUM; PLASMIDS; PLASMODIUM FALCIPARUM; POXVIRIDAE; VACCINES, DNA;

EID: 37349068504     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-6-135     Document Type: Article

References (82)

1. World Malaria Report 2005. WHO, 2005 http://rbm.who.int/wmr2005/index. html
2. The economic burden of malaria. JL Gallup JD Sachs, Am J Trop Med Hyg 2001 64 1-2 Suppl 85 96 11425181
3. A review of human vaccine research and development: malaria. MP Girard ZH Reed M Friede MP Kieny, Vaccine 2007 25 9 1567 1580 10.1016/j.vaccine.2006.09. 074 17045367
4. Specificity of protection of man immunized against sporozoite-induced falciparum malaria. DF Clyde VC McCarthy RM Miller RB Hornick, Am J Med Sci 1973 266 6 398 403 10.1097/00000441-197312000-00001 4590095
5. Protection of humans against malaria by immunization with radiation-attenuated Plasmodium falciparum sporozoites. SL Hoffman LM Goh TC Luke I Schneider TP Le DL Doolan J Sacci P de la Vega M Dowler C Paul DM Gordon JA Stoute LW Church M Sedegah DG Heppner WR Ballou TL Richie, J Infect Dis 2002 185 8 1155 1164 10.1086/339409 11930326
6. Protective immunity produced by the injection of x-irradiated sporozoites of plasmodium berghei. RS Nussenzweig J Vanderberg H Most C Orton, Nature 1967 216 111 160 162 10.1038/216160a0 6057225
7. Preliminary studies on vaccination of rhesus monkeys with irradiated sporozoites of Plasmodium knowlesi and characterization of surface antigens of these parasites. RW Gwadz AH Cochrane V Nussenzweig RS Nussenzweig, Bull World Health Organ 1979 57 Suppl 1 165 173 120766
8. Age-dependent characteristics of protection v. susceptibility to Plasmodium falciparum. JK Baird, Ann Trop Med Parasitol 1998 92 4 367 390 10.1080/00034989859366 9683890
9. Immune effector mechanisms in malaria. MF Good DL Doolan, Curr Opin Immunol 1999 11 4 412 419 10.1016/S0952-7915(99)80069-7 10448141
10. The immunology of malaria infection. M Plebanski AV Hill, Curr Opin Immunol 2000 12 4 437 441 10.1016/S0952-7915(00)00117-5 10899022
11. Immune response to pre-erythrocytic stages of malaria parasites. DL Doolan N Martinez-Alier, Curr Mol Med 2006 6 2 169 185 10.2174/ 156652406776055249 16515509
12. Gamma-globulin and acquired immunity to human malaria. S Cohen GI Mc S Carrington, Nature 1961 192 733 737 10.1038/192733a0 13880318
13. Malaria blood-stage infection and its control by the immune system. P Perlmann M Troye-Blomberg, Folia Biol (Praha) 2000 46 6 210 218 11140853
14. Immune responses to asexual blood-stages of malaria parasites. SS Yazdani P Mukherjee VS Chauhan CE Chitnis, Curr Mol Med 2006 6 2 187 203 10.2174/156652406776055212 16515510
15. DNA-based vaccines against malaria: status and promise of the Multi-Stage Malaria DNA Vaccine Operation. DL Doolan SL Hoffman, Int J Parasitol 2001 31 8 753 762 10.1016/S0020-7519(01)00184-9 11403765
16. Boosting of DNA vaccine-elicited gamma interferon responses in humans by exposure to malaria parasites. R Wang TL Richie MF Baraceros N Rahardjo T Gay JG Banania Y Charoenvit JE Epstein T Luke DA Freilich J Norman SL Hoffman, Infect Immun 2005 73 5 2863 2872 15845492 10.1128/IAI.73.5.2863-2872.2005
17. Safety and immunogenicity of rts,s+trap malaria vaccine, formulated in the as02a adjuvant system, in infant rhesus monkeys. DS Walsh S Pichyangkul M Gettayacamin P Tongtawe CA Siegrist P Hansukjariya KE Kester CA Holland G Voss J Cohen AV Stewart RS Miller WR Ballou DG Heppner Jr., Am J Trop Med Hyg 2004 70 5 499 509 15155981
18. Reduced immunogenicity of DNA vaccine plasmids in mixtures. M Sedegah Y Charoenvit L Minh M Belmonte VF Majam S Abot H Ganeshan S Kumar DJ Bacon A Stowers DL Narum DJ Carucci WO Rogers, Gene Ther 2004 11 5 448 456 10.1038/sj.gt.3302139 14973538
19. Reduced production of RNA transcripts from individual DNA plasmids given in a multivalent DNA vaccine formula. DJ Bacon M Sedegah, Hum Vaccin 2007 3 2 48 53 17312401
20. Cloning and expression in E. coli of the malarial sporozoite surface antigen gene from Plasmodium knowlesi. J Ellis LS Ozaki RW Gwadz AH Cochrane V Nussenzweig RS Nussenzweig GN Godson, Nature 1983 302 5908 536 538 10.1038/302536a0 6339949
21. DNA sequence of the gene encoding a Plasmodium falciparum malaria candidate vaccine antigen. JR Campbell, Nucleic Acids Res 1989 17 14 5854 2668895 10.1093/nar/17.14.5854
22. A highly conserved amino-acid sequence in thrombospondin, properdin and in proteins from sporozoites and blood stages of a human malaria parasite. KJ Robson JR Hall MW Jennings TJ Harris K Marsh CI Newbold VE Tate DJ Weatherall, Nature 1988 335 6185 79 82 10.1038/335079a0 3045563
23. Characterization of Plasmodium falciparum sporozoite surface protein 2. WO Rogers A Malik S Mellouk K Nakamura MD Rogers A Szarfman DM Gordon AK Nussler M Aikawa SL Hoffman, Proc Natl Acad Sci U S A 1992 89 19 9176 9180 1409621 10.1073/pnas.89.19.9176
24. A liver-stage-specific antigen of Plasmodium falciparum characterized by gene cloning. C Guerin-Marchand P Druilhe B Galey A Londono J Patarapotikul RL Beaudoin C Dubeaux A Tartar O Mercereau-Puijalon G Langsley, Nature 1987 329 6135 164 167 10.1038/329164a0 3306406
25. Structure of Plasmodium falciparum liver stage antigen-1. J Zhu MR Hollingdale, Mol Biochem Parasitol 1991 48 2 223 226 10.1016/0166-6851(91)90117- O 1840628
26. Stage-specific protein synthesis by asexual blood stage parasites of Plasmodium knowlesi. JA Deans AW Thomas S Cohen, Mol Biochem Parasitol 1983 8 1 31 44 10.1016/0166-6851(83)90032-4 6877279
27. Diversity of the vaccine candidate AMA-1 of Plasmodium falciparum. VM Marshall L Zhang RF Anders RL Coppel, Mol Biochem Parasitol 1996 77 1 109 113 10.1016/0166-6851(96)02583-2 8784778
28. Immunization against blood-stage rodent malaria using purified parasite antigens. AA Holder RR Freeman, Nature 1981 294 5839 361 364 10.1038/294361a0 7312033
29. A direct and rapid sequencing strategy for the Plasmodium falciparum antigen gene gp190/MSA1. W Pan R Tolle H Bujard, Mol Biochem Parasitol 1995 73 1-2 241 244 10.1016/0166-6851(95)00094-H 8577332
30. Protection against dengue type 2 virus induced in mice immunized with a DNA plasmid encoding the non-structural 1 (NS1) gene fused to the tissue plasminogen activator signal sequence. SM Costa MV Paes DF Barreto AT Pinhao OM Barth JL Queiroz GR Armoa MS Freire AM Alves, Vaccine 2006 24 2 195 205 10.1016/j.vaccine.2005.07.059 16122850
31. A potential disruptive technology in vaccine development: gene-based vaccines and their application to infectious diseases. DC Kaslow, Trans R Soc Trop Med Hyg 2004 98 10 593 601 10.1016/j.trstmh.2004.03.007 15289096
32. Gene-based vaccines: recent technical and clinical advances. JB Ulmer B Wahren MA Liu, Trends Mol Med 2006 12 5 216 222 10.1016/j.molmed.2006.03.007 16621717
33. Protection against malaria by immunization with plasmid DNA encoding circumsporozoite protein. M Sedegah R Hedstrom P Hobart SL Hoffman, Proc Natl Acad Sci U S A 1994 91 21 9866 9870 7937907 10.1073/pnas.91.21.9866
34. Boosting with recombinant vaccinia increases immunogenicity and protective efficacy of malaria DNA vaccine. M Sedegah TR Jones M Kaur R Hedstrom P Hobart JA Tine SL Hoffman, Proc Natl Acad Sci U S A 1998 95 13 7648 7653 9636204 10.1073/pnas.95.13.7648
35. Improving protective immunity induced by DNA-based immunization: priming with antigen and GM-CSF-encoding plasmid DNA and boosting with antigen-expressing recombinant poxvirus. M Sedegah W Weiss JB Sacci Jr. Y Charoenvit R Hedstrom K Gowda VF Majam J Tine S Kumar P Hobart SL Hoffman, J Immunol 2000 164 11 5905 5912 10820272
36. Circumventing genetic restriction of protection against malaria with multigene DNA immunization: CD8+ cell-, interferon gamma-, and nitric oxide-dependent immunity. DL Doolan M Sedegah RC Hedstrom P Hobart Y Charoenvit SL Hoffman, J Exp Med 1996 183 4 1739 1746 10.1084/jem.183.4.1739 8666931
37. Simultaneous induction of multiple antigen-specific cytotoxic T lymphocytes in nonhuman primates by immunization with a mixture of four Plasmodium falciparum DNA plasmids. R Wang DL Doolan Y Charoenvit RC Hedstrom MJ Gardner P Hobart J Tine M Sedegah V Fallarme JB Sacci Jr. M Kaur DM Klinman SL Hoffman WR Weiss, Infect Immun 1998 66 9 4193 4202 9712767
38. Multistage multiantigen heterologous prime boost vaccine for Plasmodium knowlesi malaria provides partial protection in rhesus macaques. WO Rogers JK Baird A Kumar JA Tine W Weiss JC Aguiar K Gowda R Gwadz S Kumar M Gold SL Hoffman, Infect Immun 2001 69 9 5565 5572 11500430 10.1128/IAI.69.9.5565-5572. 2001
39. Protection of rhesus macaques against lethal Plasmodium knowlesi malaria by a heterologous DNA priming and poxvirus boosting immunization regimen. WO Rogers WR Weiss A Kumar JC Aguiar JA Tine R Gwadz JG Harre K Gowda D Rathore S Kumar SL Hoffman, Infect Immun 2002 70 8 4329 4335 12117942 10.1128/IAI.70.8. 4329-4335.2002
40. Induction of CD4(+) T cell-dependent CD8(+) type 1 responses in humans by a malaria DNA vaccine. R Wang J Epstein FM Baraceros EJ Gorak Y Charoenvit DJ Carucci RC Hedstrom N Rahardjo T Gay P Hobart R Stout TR Jones TL Richie SE Parker DL Doolan J Norman SL Hoffman, Proc Natl Acad Sci U S A 2001 98 19 10817 10822 11526203 10.1073/pnas.181123498
41. Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. R Wang DL Doolan TP Le RC Hedstrom KM Coonan Y Charoenvit TR Jones P Hobart M Margalith J Ng WR Weiss M Sedegah C de Taisne JA Norman SL Hoffman, Science 1998 282 5388 476 480 10.1126/science.282.5388.476 9774275
42. Safety, tolerability and humoral immune responses after intramuscular administration of a malaria DNA vaccine to healthy adult volunteers. TP Le KM Coonan RC Hedstrom Y Charoenvit M Sedegah JE Epstein S Kumar R Wang DL Doolan JD Maguire SE Parker P Hobart J Norman SL Hoffman, Vaccine 2000 18 18 1893 1901 10.1016/S0264-410X(99)00407-7 10699338
43. Safety, tolerability, and lack of antibody responses after administration of a PfCSP DNA malaria vaccine via needle or needle-free jet injection, and comparison of intramuscular and combination intramuscular/intradermal routes. JE Epstein EJ Gorak Y Charoenvit R Wang N Freydberg O Osinowo TL Richie EL Stoltz F Trespalacios J Nerges J Ng V Fallarme-Majam E Abot L Goh S Parker S Kumar RC Hedstrom J Norman R Stout SL Hoffman, Hum Gene Ther 2002 13 13 1551 1560 10.1089/10430340260201644 12228010
44. Induction in humans of CD8+ and CD4+ T cell and antibody responses by sequential immunization with malaria DNA and recombinant protein. R Wang J Epstein Y Charoenvit FM Baraceros N Rahardjo T Gay JG Banania R Chattopadhyay P de la Vega TL Richie N Tornieporth DL Doolan KE Kester DG Heppner J Norman DJ Carucci JD Cohen SL Hoffman, J Immunol 2004 172 9 5561 5569 15100299
45. Technological advances to increase immunogenicity of DNA vaccines. P Lemieux, Expert Rev Vaccines 2002 1 1 85 93 10.1586/14760584.1.1.85 12908515
46. Jump-starting the immune system: prime-boosting comes of age. DL Woodland, Trends Immunol 2004 25 2 98 104 10.1016/j.it.2003.11.009 15102369
47. Progress in DNA-based heterologous prime-boost immunization strategies for malaria. AC Moore AV Hill, Immunol Rev 2004 199 126 143 10.1111/j.0105-2896. 2004.00138.x 15233731
48. DNA vaccines: progress and challenges. JJ Donnelly B Wahren MA Liu, J Immunol 2005 175 2 633 639 16002657
49. A DNA-based vaccine for the prevention of human cytomegalovirus- associated disease. LC Selinsky C Wloch M, Geall A, Hermanson G, Kaslow D,, Human Vaccines 2005 1 1 16 23 17038834
50. Use of nonionic block copolymers in vaccines and therapeutics. MJ Newman JK Actor M Balusubramanian C Jagannath, Crit Rev Ther Drug Carrier Syst 1998 15 2 89 142 9592626
51. Characterization and biological evaluation of a microparticle adjuvant formulation for plasmid DNA vaccines. RK Evans DM Zhu DR Casimiro DK Nawrocki H Mach RD Troutman A Tang S Wu S Chin C Ahn LA Isopi DM Williams Z Xu JW Shiver DB Volkin, J Pharm Sci 2004 93 7 1924 1939 10.1002/jps.20112 15176079
52. Development of an adjuvant-active nonionic block copolymer for use in oil-free subunit vaccines formulations. CW Todd LA Pozzi JR Guarnaccia M Balasubramanian WG Henk LE Younger MJ Newman, Vaccine 1997 15 5 564 570 10.1016/S0264-410X(97)00209-0 9160526
53. Comparative immunogenicity in rhesus monkeys of DNA plasmid, recombinant vaccinia virus, and replication-defective adenovirus vectors expressing a human immunodeficiency virus type 1 gag gene. DR Casimiro L Chen TM Fu RK Evans MJ Caulfield ME Davies A Tang M Chen L Huang V Harris DC Freed KA Wilson S Dubey DM Zhu D Nawrocki H Mach R Troutman L Isopi D Williams W Hurni Z Xu JG Smith S Wang X Liu L Guan R Long W Trigona GJ Heidecker HC Perry N Persaud TJ Toner Q Su X Liang R Youil M Chastain AJ Bett DB Volkin EA Emini JW Shiver, J Virol 2003 77 11 6305 6313 12743287 10.1128/JVI.77.11.6305-6313.2003
54. A nonionic block co-polymer adjuvant (CRL1005) enhances the immunogenicity and protective efficacy of inactivated influenza vaccine in young and aged mice. JM Katz X Lu CW Todd MJ Newman, Vaccine 2000 18 21 2177 2187 10.1016/S0264-410X(00)00022-0 10717336
55. Heterologous prime-boost vaccination strategies for HIV-1: augmenting cellular immune responses. MJ Newman, Curr Opin Investig Drugs 2002 3 3 374 378 12054082
56. Immunization with recombinant modified vaccinia Ankara (rMVA) constructs encoding the HA or NP gene protects ponies from equine influenza virus challenge. CC Breathnach HJ Clark RC Clark CW Olsen HG Townsend DP Lunn, Vaccine 2006 24 8 1180 1190 10.1016/j.vaccine.2005.08.091 16194586
57. Advances in tuberculosis vaccine strategies. YA Skeiky JC Sadoff, Nat Rev Microbiol 2006 4 6 469 476 10.1038/nrmicro1419 16710326
58. An OspA-based DNA vaccine protects mice against infection with Borrelia burgdorferi. CJ Luke K Carner X Liang AG Barbour, J Infect Dis 1997 175 1 91 97 8985201
59. Codon optimization of gene fragments encoding Plasmodium falciparum merzoite proteins enhances DNA vaccine protein expression and immunogenicity in mice. DL Narum S Kumar WO Rogers SR Fuhrmann H Liang M Oakley A Taye BK Sim SL Hoffman, Infect Immun 2001 69 12 7250 7253 11705894 10.1128/IAI.69.12.7250-7253. 2001
60. Two-step chromatographic purification of recombinant Plasmodium falciparum circumsporozoite protein from Escherichia coli. N Kolodny S Kitov MA Vassell VL Miller LA Ware K Fegeding P De La Vega JB Sacci Jr. DE Lanar, J Chromatogr B Biomed Sci Appl 2001 762 1 77 86 10.1016/S0378-4347(01)00340-1 11589461
61. Purification, characterization, and immunogenicity of the refolded ectodomain of the Plasmodium falciparum apical membrane antigen 1 expressed in Escherichia coli. S Dutta PV Lalitha LA Ware A Barbosa JK Moch MA Vassell BB Fileta S Kitov N Kolodny DG Heppner JD Haynes DE Lanar, Infect Immun 2002 70 6 3101 3110 12011004 10.1128/IAI.70.6.3101-3110.2002
62. ELISPOT assay for detection of peptide specific interferon-gamma secreting cells in rhesus macaques. A Kumar W Weiss JA Tine SL Hoffman WO Rogers, J Immunol Methods 2001 247 1-2 49 60 10.1016/S0022-1759(00)00310-0 11150536
63. Characterization of Plasmodium yoelii monoclonal antibodies directed against stage-specific sporozoite antigens. Y Charoenvit MF Leef LF Yuan M Sedegah RL Beaudoin, Infect Immun 1987 55 3 604 608 2434426
64. Monoclonal, but not polyclonal, antibodies protect against Plasmodium yoelii sporozoites. Y Charoenvit S Mellouk C Cole R Bechara MF Leef M Sedegah LF Yuan FA Robey RL Beaudoin SL Hoffman, J Immunol 1991 146 3 1020 1025 1988490
65. Genetic control of the immune response in mice to a Plasmodium falciparum sporozoite vaccine. Widespread nonresponsiveness to single malaria T epitope in highly repetitive vaccine. MF Good JA Berzofsky WL Maloy Y Hayashi N Fujii WT Hockmeyer LH Miller, J Exp Med 1986 164 2 655 660 10.1084/jem.164.2.655 2425037
66. A functional dichotomy in CD4+ T lymphocytes. K Bottomly, Immunol Today 1988 9 9 268 274 10.1016/0167-5699(88)91308-4 2908229
67. Transcription status of vaccine candidate genes of Plasmodium falciparum during the hepatic phase of its life cycle. M Bodescot O Silvie A Siau P Refour P Pino JF Franetich L Hannoun R Sauerwein D Mazier, Parasitol Res 2004 92 6 449 452 10.1007/s00436-003-1061-9 14963770
68. Phase 1 clinical trial of apical membrane antigen 1: an asexual blood-stage vaccine for Plasmodium falciparum malaria. EM Malkin DJ Diemert JH McArthur JR Perreault AP Miles BK Giersing GE Mullen A Orcutt O Muratova M Awkal H Zhou J Wang A Stowers CA Long S Mahanty LH Miller A Saul AP Durbin, Infect Immun 2005 73 6 3677 3685 15908397 10.1128/IAI.73.6.3677-3685.2005
69. A human phase 1 vaccine clinical trial of the Plasmodium falciparum malaria vaccine candidate apical membrane antigen 1 in Montanide ISA720 adjuvant. A Saul G Lawrence A Allworth S Elliott K Anderson C Rzepczyk LB Martin D Taylor DP Eisen DO Irving D Pye PE Crewther AN Hodder VJ Murphy RF Anders, Vaccine 2005 23 23 3076 3083 10.1016/j.vaccine.2004.09.040 15811655
70. Control of a mucosal challenge and prevention of AIDS by a multiprotein DNA/MVA vaccine. RR Amara F Villinger JD Altman SL Lydy SP O'Neil SI Staprans DC Montefiori Y Xu JG Herndon LS Wyatt MA Candido NL Kozyr PL Earl JM Smith HL Ma BD Grimm ML Hulsey J Miller HM McClure JM McNicholl B Moss HL Robinson, Science 2001 292 5514 69 74 10.1126/science.1058915 11393868
71. Replication-incompetent adenoviral vaccine vector elicits effective anti-immunodeficiency-virus immunity. JW Shiver TM Fu L Chen DR Casimiro ME Davies RK Evans ZQ Zhang AJ Simon WL Trigona SA Dubey L Huang VA Harris RS Long X Liang L Handt WA Schleif L Zhu DC Freed NV Persaud L Guan KS Punt A Tang M Chen KA Wilson KB Collins GJ Heidecker VR Fernandez HC Perry JG Joyce KM Grimm JC Cook PM Keller DS Kresock H Mach RD Troutman LA Isopi DM Williams Z Xu KE Bohannon DB Volkin DC Montefiori A Miura GR Krivulka MA Lifton MJ Kuroda JE Schmitz NL Letvin MJ Caulfield AJ Bett R Youil DC Kaslow EA Emini, Nature 2002 415 6869 331 335 10.1038/415331a 11797011
72. Immunogenicity in Mamu-A*01 rhesus macaques of a CCR5-tropic human immunodeficiency virus type 1 envelope from the primary isolate (Bx08) after synthetic DNA prime and recombinant adenovirus 5 boost. L Vinner EG Wee S Patel S Corbet GP Gao C Nielsen JM Wilson HC Ertl T Hanke A Fomsgaard, J Gen Virol 2003 84 Pt 1 203 213 10.1099/vir.0.18589-0 12533717
73. Development of a preventive vaccine for Ebola virus infection in primates. NJ Sullivan A Sanchez PE Rollin ZY Yang GJ Nabel, Nature 2000 408 6812 605 609 10.1038/35046108 11117750
74. Accelerated vaccination for Ebola virus haemorrhagic fever in non-human primates. NJ Sullivan TW Geisbert JB Geisbert L Xu ZY Yang M Roederer RA Koup PB Jahrling GJ Nabel, Nature 2003 424 6949 681 684 10.1038/nature01876 12904795
75. Approaches to enhance the efficacy of DNA vaccines. S Manoj LA Babiuk S van Drunen Littel-van den Hurk, Crit Rev Clin Lab Sci 2004 41 1 1 39 10.1080/10408360490269251 15077722
76. CD8+ T cells (cytotoxic/suppressors) are required for protection in mice immunized with malaria sporozoites. WR Weiss M Sedegah RL Beaudoin LH Miller MF Good, Proc Natl Acad Sci U S A 1988 85 2 573 576 2963334 10.1073/pnas.85.2.573
77. Induction of nitric oxide synthase protects against malaria in mice exposed to irradiated Plasmodium berghei infected mosquitoes: involvement of interferon gamma and CD8+ T cells. MC Seguin FW Klotz I Schneider JP Weir M Goodbary M Slayter JJ Raney JU Aniagolu SJ Green, J Exp Med 1994 180 1 353 358 10.1084/jem.180.1.353 7516412
78. The complexity of protective immunity against liver-stage malaria. DL Doolan SL Hoffman, J Immunol 2000 165 3 1453 1462 10903750
79. Malaria vaccines-targeting infected hepatocytes. SL Hoffman DL Doolan, Nat Med 2000 6 11 1218 1219 10.1038/81315 11062530
80. IL-12 and NK cells are required for antigen-specific adaptive immunity against malaria initiated by CD8+ T cells in the Plasmodium yoelii model. DL Doolan SL Hoffman, J Immunol 1999 163 2 884 892 10395683
81. Are trials in New World monkeys on the critical path for blood-stage malaria vaccine development? AW Stowers LH Miller, Trends Parasitol 2001 17 9 415 419 10.1016/S1471-4922(01)02011-6 11530352
82. New World monkey efficacy trials for malaria vaccine development: critical path or detour? DG Heppner JF Cummings C Ockenhouse KE Kester JA Lyon DM Gordon, Trends Parasitol 2001 17 9 419 425 10.1016/S1471-4922(01)02012-8 11530353