DNA Prime/Adenovirus Boost Malaria Vaccine Encoding P. falciparum CSP and AMA1 Induces Sterile Protection Associated with Cell-Mediated Immunity

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  Chuang, Ilin ^a   Sedegah, Martha ^a   Cicatelli, Susan ^b   Spring, Michele ^b   Polhemus, Mark ^b   Tamminga, Cindy ^a   Patterson, Noelle ^a   Guerrero, Melanie ^b   Bennett, Jason W ^b   McGrath, Shannon ^a   Ganeshan, Harini ^a   Belmonte, Maria ^a   Farooq, Fouzia ^a   Abot, Esteban ^a   Banania, Jo Glenna ^a   Huang, Jun ^a   Newcomer, Rhonda ^b   Rein, Lisa ^b   Litilit, Dianne ^a   Richie, Nancy O ^b   Wood, Chloe ^b   Murphy, Jittawadee ^b   Sauerwein, Robert ^c   Hermsen, Cornelus C ^c   McCoy, Andrea J ^a   Kamau, Edwin ^b   Cummings, James ^b   Komisar, Jack ^b   Sutamihardja, Awalludin ^a   Shi, Meng ^b   Epstein, Judith E ^a   Maiolatesi, Santina ^a   Tosh, Donna ^b   Limbach, Keith ^a   Angov, Evelina ^b   Bergmann Leitner, Elke ^b   Bruder, Joseph T ^d   Doolan, Denise L ^a   King, C Richter ^d   Carucci, Daniel ^a   Dutta, Sheetij ^b   Soisson, Lorraine ^e   Diggs, Carter ^e   Hollingdale, Michael R ^a   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 RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^d GENVEC INC   (United States)

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

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; APICAL MEMBRANE ANTIGEN 1; CHLOROQUINE; CIRCUMSPOROZOITE PROTEIN; DNA VACCINE; GAMMA INTERFERON; MALARIA VACCINE; NEUTRALIZING ANTIBODY; PLASMID DNA;

ABDOMINAL PAIN; ADULT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; AMA1 GENE; ANTIBODY RESPONSE; ANTIBODY TITER; ARTHRALGIA; ARTICLE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CHILL; CLINICAL ARTICLE; CONTROLLED CLINICAL TRIAL; CONTROLLED STUDY; CSP GENE; CYTOKINE RELEASE; DIARRHEA; DRUG DELIVERY SYSTEM; DRUG FEVER; DRUG INDUCED HEADACHE; DRUG SAFETY; DRUG TOLERABILITY; ENZYME LINKED IMMUNOSORBENT ASSAY; ENZYME LINKED IMMUNOSPOT ASSAY; FATIGUE; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; HEMOGLOBIN BLOOD LEVEL; HUMAN; IMMUNOGENICITY; INJECTION SITE ERYTHEMA; INJECTION SITE INDURATION; INJECTION SITE PAIN; INJECTION SITE REACTION; INJECTION SITE SWELLING; INSECT BITE; LEUKOCYTOSIS; LEUKOPENIA; MALARIA FALCIPARUM; MALE; MYALGIA; NAUSEA; NONHUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; RIGOR; SIDE EFFECT; SPOROZOITE; THROMBOCYTOPENIA; VACCINATION; VOMITING;

ADENOVIRUSES, HUMAN; ADOLESCENT; ADULT; ANTIGENS, PROTOZOAN; CD8-POSITIVE T-LYMPHOCYTES; FEMALE; HUMANS; IMMUNITY, CELLULAR; INTERFERON-GAMMA; MALARIA VACCINES; MALARIA, FALCIPARUM; MALE; MEMBRANE PROTEINS; MIDDLE AGED; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; VACCINES, DNA; YOUNG ADULT;

EID: 84874015160     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0055571     Document Type: Article

References (53)

1. WHO (2011) World Malaria Report.
2. PMI (2011) Fifth Annual Report to Congress.
3. Clyde DF, (1975) Immunization of man against falciparum and vivax malaria by use of attenuated sporozoites. Am J Trop Med Hyg 24: 397-401.
4. Roestenberg M, McCall M, Hopman J, Wiersma J, Luty AJ, et al. (2009) Protection against a malaria challenge by sporozoite inoculation. N Engl J Med 361: 468-477.
5. Roestenberg M, Teirlinck AC, McCall MB, Teelen K, Makamdop KN, et al. (2011) Long-term protection against malaria after experimental sporozoite inoculation: an open-label follow-up study. Lancet 377: 1770-1776.
6. Weiss WR, Jiang CG, (2012) Protective CD8+ T lymphocytes in primates immunized with malaria sporozoites. PLoS One 7: e31247.
7. 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.
8. Doolan DL, Martinez-Alier N, (2006) Immune response to pre-erythrocytic stages of malaria parasites. Curr Mol Med 6: 169-185.
9. Butler NS, Schmidt NW, Vaughan AM, Aly AS, Kappe SH, et al. (2011) Superior antimalarial immunity after vaccination with late liver stage-arresting genetically attenuated parasites. Cell Host Microbe 9: 451-462.
10. Epstein JE, Tewari K, Lyke KE, Sim BK, Billingsley PF, et al. (2011) Live attenuated malaria vaccine designed to protect through hepatic CD8(+) T cell immunity. Science 334: 475-480.
11. 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.
12. Agnandji ST, Lell B, Soulanoudjingar SS, Fernandes JF, Abossolo BP, et al. (2011) First results of phase 3 trial of RTS,S/AS01 malaria vaccine in African children. N Engl J Med 365: 1863-1875.
13. Moorthy VS, Ballou WR, (2009) Immunological mechanisms underlying protection mediated by RTS,S: a review of the available data. Malar J 8: 312.
14. Halstead SB, Thomas SJ, (2011) New Japanese encephalitis vaccines: alternatives to production in mouse brain. Expert Rev Vaccines 10: 355-364.
15. Sedegah M, Tamminga C, McGrath S, House B, Ganeshan H, et al. (2011) Adenovirus 5-vectored P. falciparum Vaccine Expressing CSP and AMA1. Part A: Safety and Immunogenicity in Seronegative Adults. PLoS One 6: e24586.
16. Tamminga C, Sedegah M, Regis D, Chuang I, Epstein JE, et al. (2011) Adenovirus-5-vectored P. falciparum Vaccine Expressing CSP and AMA1. Part B: Safety, Immunogenicity and Protective Efficacy of the CSP component. PLoS One 6: e25868.
17. Webster DP, Dunachie S, Vuola JM, Berthoud T, Keating S, et al. (2005) Enhanced T cell-mediated protection against malaria in human challenges by using the recombinant poxviruses FP9 and modified vaccinia virus Ankara. Proc Natl Acad Sci U S A 102: 4836-4841.
18. Wang R, Epstein J, Baraceros FM, Gorak EJ, Charoenvit Y, et al. (2001) Induction of CD4(+) T cell-dependent CD8(+) type 1 responses in humans by a malaria DNA vaccine. Proc Natl Acad Sci U S A 98: 10817-10822.
19. Wang R, Doolan DL, Charoenvit Y, Hedstrom RC, Gardner MJ, et al. (1998) Simultaneous induction of multiple antigen-specific cytotoxic T lymphocytes in nonhuman primates by immunization with a mixture of four Plasmodium falciparum DNA plasmids. Infect Immun 66: 4193-4202.
20. Reyes-Sandoval A, Berthoud T, Alder N, Siani L, Gilbert SC, et al. (2010) 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 78: 145-153.
21. 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.
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. Stowers AW, Kennedy MC, Keegan BP, Saul A, Long CA, et al. (2002) Vaccination of monkeys with recombinant Plasmodium falciparum apical membrane antigen 1 confers protection against blood-stage malaria. Infect Immun 70: 6961-6967.
24. 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.
25. Coppi A, Natarajan R, Pradel G, Bennett BL, James ER, et al. (2011) The malaria circumsporozoite protein has two functional domains, each with distinct roles as sporozoites journey from mosquito to mammalian host. J Exp Med 208: 341-356.
26. Bongfen SE, Torgler R, Romero JF, Renia L, Corradin G, (2007) Plasmodium berghei-infected primary hepatocytes process and present the circumsporozoite protein to specific CD8+ T cells in vitro. J Immunol 178: 7054-7063.
27. 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.
28. Hermsen CC, de Vlas SJ, van Gemert GJ, Telgt DS, Verhage DF, et al. (2004) Testing vaccines in human experimental malaria: statistical analysis of parasitemia measured by a quantitative real-time polymerase chain reaction. Am J Trop Med Hyg 71: 196-201.
29. 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.
30. 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.
31. Le TP, Coonan KM, Hedstrom RC, Charoenvit Y, Sedegah M, et al. (2000) Safety, tolerability and humoral immune responses after intramuscular administration of a malaria DNA vaccine to healthy adult volunteers. Vaccine 18: 1893-1901.
32. Epstein JE, Gorak EJ, Charoenvit Y, Wang R, Freydberg N, et al. (2002) 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. Hum Gene Ther 13: 1551-1560.
33. Wang R, Doolan DL, Le TP, Hedstrom RC, Coonan KM, et al. (1998) Induction of antigen-specific cytotoxic T lymphocytes in humans by a malaria DNA vaccine. Science 282: 476-480.
34. 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.
35. McGill R, (1978) Variations of Box Plots. Am Stat 32: 12-16.
36. 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.
37. Sheehy SH, Duncan CJ, Elias SC, Biswas S, Collins KA, et al. (2012) Phase Ia Clinical Evaluation of the Safety and Immunogenicity of the Plasmodium falciparum Blood-Stage Antigen AMA1 in ChAd63 and MVA Vaccine Vectors. PLoS One 7: e31208.
38. Tamminga C, Sedegah M, Regis D, Chuang I, Epstein JE, et al. (2011) Adenovirus-5-vectored P. falciparum vaccine expressing CSP and AMA1. Part B: safety, immunogenicity and protective efficacy of the CSP component. PLoS One 6: e25868.
39. Brun A, Barcena J, Blanco E, Borrego B, Dory D, et al. (2011) Current strategies for subunit and genetic viral veterinary vaccine development. Virus Res 157: 1-12.
40. Liu MA, (2010) Gene-based vaccines: Recent developments. Curr Opin Mol Ther 12: 86-93.
41. Redding L, Weiner DB, (2009) DNA vaccines in veterinary use. Expert Rev Vaccines 8: 1251-1276.
42. Peiperl L, Morgan C, Moodie Z, Li H, Russell N, et al. (2010) Safety and immunogenicity of a replication-defective adenovirus type 5 HIV vaccine in Ad5-seronegative persons: a randomized clinical trial (HVTN 054). PLoS One 5: e13579.
43. Radosevic K, Rodriguez A, Lemckert AA, van der Meer M, Gillissen G,et al. The Th1 immune response to Plasmodium falciparum circumsporozoite protein is boosted by adenovirus vectors 35 and 26 with a homologous insert. Clin Vaccine Immunol 17: 1687-1694.
44. Plotkin SA, (2008) Vaccines: correlates of vaccine-induced immunity. Clin Infect Dis 47: 401-409.
45. 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.
46. Frimpong-Boateng K, van Rooijen N, Geiben-Lynn R, (2010) Regulatory T cells suppress natural killer cells during plasmid DNA vaccination in mice, blunting the CD8+ T cell immune response by the cytokine TGFbeta. PLoS One 5: e12281.
47. Nwanegbo E, Vardas E, Gao W, Whittle H, Sun H, et al. (2004) Prevalence of neutralizing antibodies to adenoviral serotypes 5 and 35 in the adult populations of The Gambia, South Africa, and the United States. Clin Diagn Lab Immunol 11: 351-357.
48. Thorner AR, Vogels R, Kaspers J, Weverling GJ, Holterman L, et al. (2006) Age dependence of adenovirus-specific neutralizing antibody titers in individuals from sub-Saharan Africa. J Clin Microbiol 44: 3781-3783.
49. Buchbinder SP, Mehrotra DV, Duerr A, Fitzgerald DW, Mogg R, et al. (2008) Efficacy assessment of a cell-mediated immunity HIV-1 vaccine (the Step Study): a double-blind, randomised, placebo-controlled, test-of-concept trial. Lancet 372: 1881-1893.
50. Gilbert SC, Moorthy VS, Andrews L, Pathan AA, McConkey SJ, et al. (2006) Synergistic DNA-MVA prime-boost vaccination regimes for malaria and tuberculosis. Vaccine 24: 4554-4561.
51. 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.
52. Jaoko W, Karita E, Kayitenkore K, Omosa-Manyonyi G, Allen S, et al. (2010) Safety and immunogenicity study of Multiclade HIV-1 adenoviral vector vaccine alone or as boost following a multiclade HIV-1 DNA vaccine in Africa. PLoS One 5: e12873.
53. Koup RA, Roederer M, Lamoreaux L, Fischer J, Novik L, et al. (2010) Priming immunization with DNA augments immunogenicity of recombinant adenoviral vectors for both HIV-1 specific antibody and T-cell responses. PLoS One 5: e9015.