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

Volumn 7, Issue 2, 2012, Pages

  Sheehy, Susanne H ^a   Duncan, Christopher J A ^a   Elias, Sean C ^b   Biswas, Sumi ^b   Collins, Katharine A ^b   O'Hara, Geraldine A ^a   Halstead, Fenella D ^b   Ewer, Katie J ^b   Mahungu, Tabitha ^c   Spencer, Alexandra J ^b   Miura, Kazutoyo ^d   Poulton, Ian D ^a   Dicks, Matthew D J ^b   Edwards, Nick J ^b   Berrie, Eleanor ^b   Moyle, Sarah ^b   Colloca, Stefano ^e   Cortese, Riccardo ^e,f   Gantlett, Katherine ^a   Long, Carole A ^d   Lawrie, Alison M ^a   Gilbert, Sarah C ^b   Doherty, Tom ^c   Nicosia, Alfredo ^e,f   Hill, Adrian V S ^b   Draper, Simon J ^b   more..

^a CHURCHILL HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY COLLEGE HOSPITAL   (United Kingdom)

^d NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^e Okairòs AG ^*  (Italy)

^f CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; ADJUVANT; APICAL MEMBRANE ANTIGEN 1; IMMUNOGLOBULIN G; MODIFIED VACCINIA VIRUS ANKARA VECTOR; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG; VIRUS VECTOR; GAMMA INTERFERON; MALARIA VACCINE; NEUTRALIZING ANTIBODY; PARASITE ANTIGEN; PROTOZOON ANTIBODY;

ADULT; ALLELE; ANTIBODY RESPONSE; ARTICLE; CD4+ T LYMPHOCYTE; CD8+ T LYMPHOCYTE; CELLULAR IMMUNITY; CLINICAL EVALUATION; DRUG ACTIVITY; DRUG SAFETY; FEMALE; HUMAN; HUMAN EXPERIMENT; HUMORAL IMMUNITY; IMMUNOGENICITY; IN VITRO STUDY; MALARIA FALCIPARUM; MALE; NORMAL HUMAN; PERIPHERAL BLOOD MONONUCLEAR CELL; PHASE 1 CLINICAL TRIAL; PHENOTYPE; PLASMODIUM FALCIPARUM; VACCINE PRODUCTION; ADOLESCENT; ANIMAL; CLINICAL TRIAL; ENZYME LINKED IMMUNOSPOT ASSAY; GENE VECTOR; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNIZATION; IMMUNOLOGY; LIFE CYCLE STAGE; MIDDLE AGED; SIMIAN VIRUS; T LYMPHOCYTE; VACCINIA VIRUS;

ADENOVIRUSES, SIMIAN; ADOLESCENT; ADULT; ANIMALS; ANTIBODIES, NEUTRALIZING; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ENZYME-LINKED IMMUNOSPOT ASSAY; FEMALE; GENETIC VECTORS; HUMANS; IMMUNIZATION; INTERFERON-GAMMA; LIFE CYCLE STAGES; MALARIA VACCINES; MALARIA, FALCIPARUM; MALE; MIDDLE AGED; PLASMODIUM FALCIPARUM; T-LYMPHOCYTES; VACCINIA VIRUS; YOUNG ADULT;

EID: 84857399087     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0031208     Document Type: Article

References (55)

1. Das P, Horton R, (2010) Malaria elimination: worthy, challenging, and just possible. Lancet 376: 1515-1517.
2. Langhorne J, Ndungu FM, Sponaas AM, Marsh K, (2008) Immunity to malaria: more questions than answers. Nat Immunol 9: 725-732.
3. Goodman AL, Draper SJ, (2010) Blood-stage malaria vaccines- recent progress and future challenges. Ann Trop Med Parasitol 104: 189-211.
4. Sirima SB, Cousens S, Druilhe P, (2011) Protection against malaria by MSP3 candidate vaccine. N Engl J Med 365: 1062-1064.
5. Cech PG, Aebi T, Abdallah MS, Mpina M, Machunda EB, et al. (2011) Virosome-formulated Plasmodium falciparum AMA-1 & CSP derived peptides as malaria vaccine: randomized phase 1b trial in semi-immune adults & children. PLoS One 6: e22273.
6. Thera MA, Doumbo OK, Coulibaly D, Laurens MB, Ouattara A, et al. (2011) A field trial to assess a blood-stage malaria vaccine. N Engl J Med 365: 1004-1013.
7. 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.
8. Ellis RD, Sagara I, Doumbo O, Wu Y, (2010) Blood stage vaccines for Plasmodium falciparum: Current status and the way forward. Hum Vaccin 6.
9. Good MF, Engwerda C, (2011) Defying malaria: Arming T cells to halt malaria. Nat Med 17: 49-51.
10. Good MF, Xu H, Wykes M, Engwerda CR, (2005) Development and regulation of cell-mediated immune responses to the blood stages of malaria: implications for vaccine research. Annu Rev Immunol 23: 69-99.
11. Su Z, Stevenson MM, (2000) Central role of endogenous gamma interferon in protective immunity against blood-stage Plasmodium chabaudi AS infection. Infect Immun 68: 4399-4406.
12. Yoneto T, Waki S, Takai T, Tagawa Y, Iwakura Y, et al. (2001) A critical role of Fc receptor-mediated antibody-dependent phagocytosis in the host resistance to blood-stage Plasmodium berghei XAT infection. J Immunol 166: 6236-6241.
13. Joos C, Marrama L, Polson HE, Corre S, Diatta AM, et al. (2010) Clinical protection from falciparum malaria correlates with neutrophil respiratory bursts induced by merozoites opsonized with human serum antibodies. PLoS One 5: e9871.
14. Bouharoun-Tayoun H, Attanath P, Sabchareon A, Chongsuphajaisiddhi T, Druilhe P, (1990) Antibodies that protect humans against Plasmodium falciparum blood stages do not on their own inhibit parasite growth and invasion in vitro, but act in cooperation with monocytes. J Exp Med 172: 1633-1641.
15. Draper SJ, Goodman AL, Biswas S, Forbes EK, Moore AC, et al. (2009) Recombinant viral vaccines expressing merozoite surface protein-1 induce antibody- and T cell-mediated multistage protection against malaria. Cell Host Microbe 5: 95-105.
16. Kawabata Y, Udono H, Honma K, Ueda M, Mukae H, et al. (2002) Merozoite surface protein 1-specific immune response is protective against exoerythrocytic forms of Plasmodium yoelii. Infect Immun 70: 6075-6082.
17. Belnoue E, Voza T, Costa FT, Gruner AC, Mauduit M, et al. (2008) Vaccination with live Plasmodium yoelii blood stage parasites under chloroquine cover induces cross-stage immunity against malaria liver stage. J Immunol 181: 8552-8558.
18. Hill AVS, Reyes-Sandoval A, O'Hara G, Ewer K, Lawrie AM, et al. (2010) Prime-boost vectored malaria vaccines: progress and prospects. Hum Vaccin 6: 78-83.
19. Biswas S, Dicks MD, Long CA, Remarque EJ, Siani L, et al. (2011) Transgene Optimization, Immunogenicity and In Vitro Efficacy of Viral Vectored Vaccines Expressing Two Alleles of Plasmodium falciparum AMA1. PLoS One 6: e20977.
20. Draper SJ, Biswas S, Spencer AJ, Remarque EJ, Capone S, et al. (2010) Enhancing blood-stage malaria subunit vaccine immunogenicity in rhesus macaques by combining adenovirus, poxvirus, and protein-in-adjuvant vaccines. J Immunol 185: 7583-7595.
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. Takala SL, Coulibaly D, Thera MA, Batchelor AH, Cummings MP, et al. (2009) Extreme polymorphism in a vaccine antigen and risk of clinical malaria: implications for vaccine development. Sci Transl Med 1: 2ra5.
23. 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.
24. 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.
25. Bruder JT, Stefaniak ME, Patterson NB, Chen P, Konovalova S, et al. (2010) Adenovectors induce functional antibodies capable of potent inhibition of blood stage malaria parasite growth. Vaccine 28: 3201-3210.
26. Sedegah M, Kim Y, Peters B, McGrath S, Ganeshan H, et al. (2010) Identification and localization of minimal MHC-restricted CD8+ T cell epitopes within the Plasmodium falciparum AMA1 protein. Malar J 9: 241.
27. 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.
28. Draper SJ, Heeney JL, (2010) Viruses as vaccine vectors for infectious diseases and cancer. Nat Rev Microbiol 8: 62-73.
29. Barouch DH, (2010) Novel adenovirus vector-based vaccines for HIV-1. Curr Opin HIV AIDS 5: 386-390.
30. Sheehy SH, Duncan CJ, Elias SC, Collins KA, Ewer KJ, et al. (2011) Phase Ia Clinical Evaluation of the Plasmodium falciparum Blood-stage Antigen MSP1 in ChAd63 and MVA Vaccine Vectors. Mol Ther.
31. Dutta S, Lee SY, Batchelor AH, Lanar DE, (2007) Structural basis of antigenic escape of a malaria vaccine candidate. Proc Natl Acad Sci U S A 104: 12488-12493.
32. Porter DW, Thompson FM, Berthoud TK, Hutchings CL, Andrews L, et al. (2011) A human Phase I/IIa malaria challenge trial of a polyprotein malaria vaccine. Vaccine.
33. Kennedy MC, Wang J, Zhang Y, Miles AP, Chitsaz F, et al. (2002) In vitro studies with recombinant Plasmodium falciparum apical membrane antigen 1 (AMA1): production and activity of an AMA1 vaccine and generation of a multiallelic response. Infect Immun 70: 6948-6960.
34. Roederer M, Nozzi JL, Nason MC, (2011) SPICE: exploration and analysis of post-cytometric complex multivariate datasets. Cytometry A 79: 167-174.
35. Miura K, Orcutt AC, Muratova OV, Miller LH, Saul A, et al. (2008) Development and characterization of a standardized ELISA including a reference serum on each plate to detect antibodies induced by experimental malaria vaccines. Vaccine 26: 193-200.
36. Miura K, Zhou H, Diouf A, Moretz SE, Fay MP, et al. (2009) Anti-apical-membrane-antigen-1 antibody is more effective than anti-42-kilodalton-merozoite-surface-protein-1 antibody in inhibiting plasmodium falciparum growth, as determined by the in vitro growth inhibition assay. Clin Vaccine Immunol 16: 963-968.
37. Capone S, Meola A, Ercole BB, Vitelli A, Pezzanera M, et al. (2006) A novel adenovirus type 6 (Ad6)-based hepatitis C virus vector that overcomes preexisting anti-ad5 immunity and induces potent and broad cellular immune responses in rhesus macaques. J Virol 80: 1688-1699.
38. Dudareva M, Andrews L, Gilbert SC, Bejon P, Marsh K, et al. (2009) Prevalence of serum neutralizing antibodies against chimpanzee adenovirus 63 and human adenovirus 5 in Kenyan Children, in the context of vaccine vector efficacy. Vaccine 27: 3501-3504.
39. Walther M, Thompson FM, Dunachie S, Keating S, Todryk S, et al. (2006) Safety, immunogenicity, and efficacy of prime-boost immunization with recombinant poxvirus FP9 and modified vaccinia virus Ankara encoding the full-length Plasmodium falciparum circumsporozoite protein. Infect Immun 74: 2706-2716.
40. Keefer MC, Frey SE, Elizaga M, Metch B, De Rosa SC, et al. (2011) A phase I trial of preventive HIV vaccination with heterologous poxviral-vectors containing matching HIV-1 inserts in healthy HIV-uninfected subjects. Vaccine 29: 1948-1958.
41. Douglas AD, de Cassan SC, Dicks MD, Gilbert SC, Hill AV, et al. (2010) Tailoring subunit vaccine immunogenicity: Maximizing antibody and T cell responses by using combinations of adenovirus, poxvirus and protein-adjuvant vaccines against Plasmodium falciparum MSP1. Vaccine 28: 7167-7178.
42. Goodman AL, Epp C, Moss D, Holder AA, Wilson JM, et al. (2010) New candidate vaccines against blood-stage Plasmodium falciparum malaria: prime-boost immunization regimens incorporating human and simian adenoviral vectors and poxviral vectors expressing an optimized antigen based on merozoite surface protein 1. Infect Immun 78: 4601-4612.
43. 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.
44. Lyke KE, Daou M, Diarra I, Kone A, Kouriba B, et al. (2009) Cell-mediated immunity elicited by the blood stage malaria vaccine apical membrane antigen 1 in Malian adults: results of a Phase I randomized trial. Vaccine 27: 2171-2176.
45. Duncan CJ, Sheehy SH, Ewer KJ, Douglas AD, Collins KA, et al. (2011) Impact on Malaria Parasite Multiplication Rates in Infected Volunteers of the Protein-in-Adjuvant Vaccine AMA1-C1/Alhydrogel+CPG 7909. PLoS One 6: e22271.
46. 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.
47. Pierce MA, Ellis RD, Martin LB, Malkin E, Tierney E, et al. (2010) Phase 1 safety and immunogenicity trial of the Plasmodium falciparum blood-stage malaria vaccine AMA1-C1/ISA 720 in Australian adults. Vaccine 28: 2236-2242.
48. Mullen GE, Ellis RD, Miura K, Malkin E, Nolan C, et al. (2008) Phase 1 trial of AMA1-C1/Alhydrogel plus CPG 7909: an asexual blood-stage vaccine for Plasmodium falciparum malaria. PLoS ONE 3: e2940.
49. Ellis RD, Mullen GE, Pierce M, Martin LB, Miura K, et al. (2009) A Phase 1 study of the blood-stage malaria vaccine candidate AMA1-C1/Alhydrogel with CPG 7909, using two different formulations and dosing intervals. Vaccine 27: 4104-4109.
50. Bett AJ, Dubey SA, Mehrotra DV, Guan L, Long R, et al. (2010) Comparison of T cell immune responses induced by vectored HIV vaccines in non-human primates and humans. Vaccine 28: 7881-7889.
51. 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.
52. Draper SJ, Moore AC, Goodman AL, Long CA, Holder AA, et al. (2008) Effective induction of high-titer antibodies by viral vector vaccines. Nat Med 14: 819-821.
53. 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.
54. Kusi KA, Faber BW, Thomas AW, Remarque EJ, (2009) Humoral immune response to mixed PfAMA1 alleles; multivalent PfAMA1 vaccines induce broad specificity. PLoS One 4: e8110.
55. de Cassan SC, Forbes EK, Douglas AD, Milicic A, Singh B, et al. (2011) The requirement for potent adjuvants to enhance the immunogenicity and protective efficacy of protein vaccines can be overcome by prior immunization with a recombinant adenovirus. J Immunol 187: 2602-2616.