Comparative assessment of transmission-blocking vaccine candidates against plasmodium falciparum

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Kapulu, M C ^a   Da, D F ^b   Miura, K ^c   Li, Y ^a   Blagborough, A M ^d   Churcher, T S ^d   Nikolaeva, D ^a   Williams, A R ^a   Goodman, A L ^a   Sangare, I ^b   Turner, A V ^a   Cottingham, M G ^a   Nicosia, A ^e,f,g   Straschil, U ^d   Tsuboi, T ^h   Gilbert, S C ^a   Long, Carole A ^c   Sinden, R E ^a,d   Draper, S J ^a   Hill, A V S ^a   Cohuet, A ^b   Biswas, S ^a   more..

^a UNIVERSITY OF OXFORD   (United Kingdom)

^b University de Montpellier   (France)

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

^d IMPERIAL COLLEGE LONDON   (United Kingdom)

^e Department of Infectious Disease Epidemiology Imperial College London ^*  (Italy)

^f CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^g UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^h EHIME UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

HYBRID PROTEIN; IMMUNOGLOBULIN G; MALARIA VACCINE; PARASITE ANTIGEN; PROTOZOON ANTIBODY;

ANIMAL; ANOPHELES GAMBIAE; DISEASE MODEL; GENE VECTOR; GENETICS; HUMAN; IMMUNIZATION; IMMUNOLOGY; MALARIA, FALCIPARUM; MOSQUITO; MOUSE; PLASMODIUM FALCIPARUM; TRANSMISSION;

ANIMALS; ANOPHELES GAMBIAE; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CULICIDAE; DISEASE MODELS, ANIMAL; GENETIC VECTORS; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN G; MALARIA VACCINES; MALARIA, FALCIPARUM; MICE; PLASMODIUM FALCIPARUM; RECOMBINANT FUSION PROTEINS;

EID: 84931292044     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep11193     Document Type: Article

References (62)

1. Birkett, A. J., Moorthy, V. S., Loucq, C., Chitnis, C. E. , Kaslow, D. C. Malaria vaccine R&D in the Decade of Vaccines: breakthroughs, challenges and opportunities. Vaccine 31 Suppl 2, B233-243 (2013).
2. Agnandji, S. T. et al. A phase 3 trial of RTS, S/AS01 malaria vaccine in African infants. N Engl J Med 367, 2284-2295 (2012).
3. Carter, R. Transmission blocking malaria vaccines. Vaccine 19, 2309-2314 (2001).
4. Lavazec, C. , Bourgouin, C. Mosquito-based transmission blocking vaccines for interrupting Plasmodium development. Microbes and infection/Institut Pasteur 10, 845-849 (2008).
5. Carter, R., Mendis, K., Miller, L., Molineaux, L. , Saul, A. Malaria transmission-blocking vaccines-how can their development be supported? Nat Med 6, 241-244 (2000).
6. Malkin, E. M. et al. Phase 1 vaccine trial of Pvs25H: a transmission blocking vaccine for Plasmodium vivax malaria. Vaccine 23, 3131-3138 (2005).
7. Wu, Y. et al. Phase 1 trial of malaria transmission blocking vaccine candidates Pfs25 and Pvs25 formulated with montanide ISA 51. PLoS One 3, e2636 (2008).
8. Kaslow, D. et al. A vaccine candidate from the sexual stage of human malaria that contains EGF-like domains. Nature 333, 74-76 (1988).
9. Barr, P. et al. Recombinant Pfs25 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in experimental animals. J Exp Med 174, 1203-1208 (1991).
10. Miura, K. et al. Transmission-blocking activity induced by malaria vaccine candidates Pfs25/Pvs25 is a direct and predictable function of antibody titer. Malar J 6, 107 (2007).
11. Eksi, S. et al. Malaria transmission-blocking antigen, Pfs230, mediates human red blood cell binding to exflagellating male parasites and oocyst production. Mol Microbiol 61, 991-998 (2006).
12. van Dijk, M. R. et al. A central role for P48/45 in malaria parasite male gamete fertility. Cell 104, 153-164 (2001).
13. Bousema, T. et al. The dynamics of naturally acquired immune responses to Plasmodium falciparum sexual stage antigens Pfs230 & Pfs48/45 in a low endemic area in Tanzania. PLoS One 5, e14114 (2010).
14. Bousema, J. et al. A longitudinal study of immune responses to Plasmodium falciparum sexual stage antigens in Tanzanian adults. Parasite Immunol 29, 309-317 (2007).
15. Healer, J., McGuinness, D., Carter, R. , Riley, E. Transmission-blocking immunity to Plasmodium falciparum in malariaimmune individuals is associated with antibodies to the gamete surface protein Pfs230. Parasitology 119 ( Pt 5), 425-433 (1999).
16. Roeffen, W. et al. Association between anti-Pfs48/45 reactivity and P. falciparum transmission-blocking activity in sera from Cameroon. Parasite Immunol 18, 103-109 (1996).
17. Lavazec, C. et al. Carboxypeptidases B of Anopheles gambiae as Targets for a Plasmodium falciparum Transmission-Blocking Vaccine. Infect. Immun. 75, 1635-1642 (2007).
18. Raz, A., Dinparast Djadid, N. , Zakeri, S. Molecular characterization of the carboxypeptidase B1 of Anopheles stephensi and its evaluation as a target for transmission-blocking vaccines. Infection and immunity 81, 2206-2216 (2013).
19. Dinglasan, R. R. et al. Disruption of Plasmodium falciparum development by antibodies against a conserved mosquito midgut antigen. Proc Natl Acad Sci USA 104, 13461-13466 (2007).
20. Nikolaeva, D., Draper, S. J. , Biswas, S. Toward the development of effective transmission-blocking vaccines for malaria. Expert review of vaccines, 1-28, doi:10.1586/14760584.2015.993383 (2015).
21. van Dijk, M. R. et al. Three members of the 6-cys protein family of Plasmodium play a role in gamete fertility. PLoS Pathog 6, e1000853 (2010).
22. Williamson, K. C., Fujioka, H., Aikawa, M. , Kaslow, D. C. Stage-specific processing of Pfs230, a Plasmodium falciparum transmission-blocking vaccine candidate. Mol Biochem Parasitol 78, 161-169 (1996).
23. Williamson, K. C., Keister, D. B., Muratova, O. , Kaslow, D. C. Recombinant Pfs230, a Plasmodium falciparum gametocyte protein, induces antisera that reduce the infectivity of Plasmodium falciparum to mosquitoes. Mol Biochem Parasitol 75, 33-42 (1995).
24. Chowdhury, D. R., Angov, E., Kariuki, T. , Kumar, N. A potent malaria transmission blocking vaccine based on codon harmonized full length Pfs48/45 expressed in Escherichia coli. PLoS One 4, e6352 (2009).
25. Wu, Y. et al. Sustained high-titer antibody responses induced by conjugating a malarial vaccine candidate to outer-membrane protein complex. Proc Natl Acad Sci USA 103, 18243-18248 (2006).
26. Goodman, A. L. et al. A viral vectored prime-boost immunization regime targeting the malaria Pfs25 antigen induces transmission-blocking activity. PLoS One 6, e29428 (2011).
27. Draper, S. J. et al. Enhancing blood-stage malaria subunit vaccine immunogenicity in rhesus macaques by combining adenovirus, poxvirus, and protein-in-adjuvant vaccines. J Immunol 185, 7583-7595 (2010).
28. Draper, S. J. et al. Effective induction of high-titer antibodies by viral vector vaccines. Nat Med 14, 819-821 (2008).
29. Sheehy, S. H. et al. Phase Ia clinical evaluation of the Plasmodium falciparum blood-stage antigen MSP1 in ChAd63 and MVA vaccine vectors. Mol Ther 19, 2269-2276 (2011).
30. Sheehy, S. H. et al. ChAd63-MVA-vectored blood-stage malaria vaccines targeting MSP1 and AMA1: assessment of efficacy against mosquito bite challenge in humans. Mol Ther 20, 2355-2368 (2012).
31. Dudareva, M. et al. 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 (2009).
32. Sridhar, S. et al. Single-Dose Protection against Plasmodium berghei by a Simian Adenovirus Vector Using a Human Cytomegalovirus Promoter Containing Intron A. J. Virol. 82, 3822-3833 (2008).
33. Biswas, S. et al. Transgene Optimization, Immunogenicity and In Vitro Efficacy of Viral Vectored Vaccines Expressing Two Alleles of Plasmodium falciparum AMA1. PLoS One 6, e20977 (2011).
34. Milek, R. L., Stunnenberg, H. G. , Konings, R. N. Assembly and expression of a synthetic gene encoding the antigen Pfs48/45 of the human malaria parasite Plasmodium falciparum in yeast. Vaccine 18, 1402-1411 (2000).
35. Mathias, D. K. et al. Expression, immunogenicity, histopathology, and potency of a mosquito-based malaria transmissionblocking recombinant vaccine. Infect. Immun. 80, 1606-1614 (2012).
36. Healer, J. et al. Complement-mediated lysis of Plasmodium falciparum gametes by malaria-immune human sera is associated with antibodies to the gamete surface antigen Pfs230. Infect. Immun. 65, 3017-3023 (1997).
37. Read, D. et al. Transmission-blocking antibodies against multiple, non-variant target epitopes of the Plasmodium falciparum gamete surface antigen Pfs230 are all complement-fixing. Parasite Immunol 16, 511-519 (1994).
38. Niederwieser, I., Felger, I. , Beck, H. P. Limited polymorphism in Plasmodium falciparum sexual-stage antigens. Am J Trop Med Hyg 64, 9-11 (2001).
39. Escalante, A. A., Lal, A. A. , Ayala, F. J. Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics 149, 189-202 (1998).
40. Sheehy, S. H. et al. 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 (2012).
41. Douglas, A. D. et al. The blood-stage malaria antigen PfRH5 is susceptible to vaccine-inducible cross-strain neutralizing antibody. Nat Commun 2, 601 (2011).
42. Outchkourov, N. S. et al. Correctly folded Pfs48/45 protein of Plasmodium falciparum elicits malaria transmission-blocking immunity in mice. Proc Natl Acad Sci USA 105, 4301-4305 (2008).
43. Kocken, C. H. et al. Cloning and expression of the gene coding for the transmission blocking target antigen Pfs48/45 of Plasmodium falciparum. Mol Biochem Parasitol 61, 59-68 (1993).
44. Galli, G. et al. Adjuvanted H5N1 vaccine induces early CD4+ T cell response that predicts long-term persistence of protective antibody levels. Proc Natl Acad Sci USA 106, 3877-3882 (2009).
45. Douglas, A. D. et al. 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 (2010).
46. Elias, S. C. et al. Analysis of human B-cell responses following ChAd63-MVA MSP1 and AMA1 immunization and controlled malaria infection. Immunology 141, 628-644 (2014).
47. Haddad, D., Maciel, J. , Kumar, N. Infection with Plasmodium berghei boosts antibody responses primed by a DNA vaccine encoding gametocyte antigen Pbs48/45. Infect. Immun. 74, 2043-2051 (2006).
48. Milek, R. L. et al. Plasmodium falciparum: heterologous synthesis of the transmission-blocking vaccine candidate Pfs48/45 in recombinant vaccinia virus-infected cells. Exp Parasitol 90, 165-174 (1998).
49. Bushkin, G. G. et al. Suggestive evidence for Darwinian Selection against asparagine-linked glycans of Plasmodium falciparum and Toxoplasma gondii. Eukaryot Cell 9, 228-241 (2010).
50. Theisen, M. et al. A multi-stage malaria vaccine candidate targeting both transmission and asexual parasite life-cycle stages. Vaccine 32, 2623-2630 (2014).
51. Churcher, T. S. et al. Measuring the blockade of malaria transmission-an analysis of the Standard Membrane Feeding Assay. Int J Parasitol 42, 1037-1044 (2012).
52. Armistead, J. S. et al. Antibodies to a single, conserved epitope in Anopheles APN1 inhibit universal transmission of Plasmodium falciparum and Plasmodium vivax malaria. Infection and immunity 82, 818-829 (2014).
53. Duffy, P. E. , Kaslow, D. C. A novel malaria protein, Pfs28, and Pfs25 are genetically linked and synergistic as falciparum malaria transmission-blocking vaccines. Infect. Immun. 65, 1109-1113 (1997).
54. Gozar, M. M., Price, V. L. , Kaslow, D. C. Saccharomyces cerevisiae-secreted fusion proteins Pfs25 and Pfs28 elicit potent Plasmodium falciparum transmission-blocking antibodies in mice. Infect. Immun. 66, 59-64 (1998).
55. Cheru, L. et al. The IC(50) of anti-Pfs25 antibody in membrane-feeding assay varies among species. Vaccine 28, 4423-4429 (2010).
56. Berthoud, T. K. et al. Potent CD8+ T-cell immunogenicity in humans of a novel heterosubtypic influenza A vaccine, MVANP+ M1. Clin Infect Dis 52, 1-7 (2011).
57. Tameris, M. D. et al. Safety and efficacy of MVA85A, a new tuberculosis vaccine, in infants previously vaccinated with BCG: a randomised, placebo-controlled phase 2b trial. Lancet 381, 1021-1028 (2013).
58. Bustamante, P. J. et al. Differential ability of specific regions of Plasmodium falciparum sexual-stage antigen, Pfs230, to induce malaria transmission-blocking immunity. Parasite Immunol 22, 373-380 (2000).
59. Tachibana, M. et al. N-terminal prodomain of Pfs230 synthesized using a cell-free system is sufficient to induce complementdependent malaria transmission-blocking activity. Clinical and vaccine immunology : CVI 18, 1343-1350 (2011).
60. Miura, K. et al. 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 (2008).
61. Tsuboi, T. et al. Wheat germ cell-free system-based production of malaria proteins for discovery of novel vaccine candidates. Infection and immunity 76, 1702-1708 (2008).
62. Blagborough, A. M. , Sinden, R. E. Plasmodium berghei HAP2 induces strong malaria transmission-blocking immunity in vivo and in vitro. Vaccine 27, 5187-5194 (2009).