Protective immune responses elicited by immunization with a chimeric blood-stage malaria vaccine persist but are not boosted by Plasmodium yoelii challenge infection

Vaccine

Volumn 28, Issue 42, 2010, Pages 6876-6884

  Alaro, James R ^a   Lynch, Michele M ^a   Burns, James M ^a  

^a DREXEL UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

Blood stage vaccines; Malaria; Merozoite surface proteins; Plasmodium yoelii

Indexed keywords

ANTIGEN; EPITOPE; MALARIA VACCINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIBODY RESPONSE; ARTICLE; B LYMPHOCYTE; CELLULAR IMMUNITY; CONTROLLED STUDY; DRUG EFFICACY; DRUG FORMULATION; IMMUNE RESPONSE; IMMUNIZATION; MALARIA; MALE; MOUSE; NONHUMAN; PLASMODIUM YOELII; PLASMODIUM YOELII INFECTION; PRIORITY JOURNAL; T LYMPHOCYTE;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIBODY FORMATION; ANTIGENS, PROTOZOAN; B-LYMPHOCYTES; CELL PROLIFERATION; EPITOPES, B-LYMPHOCYTE; MALARIA; MALARIA VACCINES; MALE; MEROZOITE SURFACE PROTEIN 1; MICE; MICE, INBRED BALB C; PLASMODIUM YOELII; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; T-LYMPHOCYTES;

EID: 77956882268     PISSN: 0264410X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.vaccine.2010.08.018     Document Type: Article

References (58)

1. Chan M. World Malaria Report 2009 Geneva 2009, World Health Organization.
2. Holder A.A. Preventing merozoite invasion of erythrocytes. Malaria vaccine development: a multi-immune response approach 1996, 77-104. ASM Press, Washington, DC. S.L. Hoffman (Ed.).
3. Berzins K. Merozoite antigens involved in invasion. Chem Immunol 2002, 80:125-143.
4. Mahanty S., Saul A., Miller L.H. Progress in the development of recombinant and synthetic blood-stage malaria vaccines. J Exp Biol 2003, 206(Pt 21):3781-3788.
5. Galinsky M.R., Dluzewski A.R., Barnwell J.W. A mechanistic approach to merozoite invasion of red blood cells: merozoite biogenesis, rupture and invasion of erythrocytes. Molecular approaches to malaria 2005, 113-168. ASM Press, Washington, DC. I.W. Sherman (Ed.).
6. 19 across distantly related Plasmodium species. Nat Med 2000, 6(1):91-95.
7. Holder A.A., Freeman R.R. The three major antigens on the surface of Plasmodium falciparum merozoites are derived from a single high molecular weight precursor. J Exp Med 1984, 160(2):624-629.
8. Lyon J.A., Geller R.H., Haynes J.D., Chulay J.D., Weber J.L. Epitope map and processing scheme for the 195,000-dalton surface glycoprotein of Plasmodium falciparum merozoites deduced from cloned overlapping segments of the gene. Proc Natl Acad Sci USA 1986, 83(9):2989-2993.
9. McBride J.S., Heidrich H.G. Fragments of the polymorphic Mr 185,000 glycoprotein from the surface of isolated Plasmodium falciparum merozoites form an antigenic complex. Mol Biochem Parasitol 1987, 23(1):71-84.
10. Pachebat J.A., Ling I.T., Grainger M., Trucco C., Howell S., Fernandez-Reyes D., et al. The 22kDa component of the protein complex on the surface of Plasmodium falciparum merozoites is derived from a larger precursor, merozoite surface protein 7. Mol Biochem Parasitol 2001, 117(1):83-89.
11. Trucco C., Fernandez-Reyes D., Howell S., Stafford W.H., Scott-Finnigan T.J., Grainger M., et al. The merozoite surface protein 6 gene codes for a 36kDa protein associated with the Plasmodium falciparum merozoite surface protein-1 complex. Mol Biochem Parasitol 2001, 112(1):91-101.
12. Blackman M.J., Heidrich H.G., Donachie S., McBride J.S., Holder A.A. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 1990, 172(1):379-382.
13. Blackman M.J., Ling I.T., Nicholls S.C., Holder A.A. Proteolytic processing of the Plasmodium falciparum merozoite surface protein-1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Mol Biochem Parasitol 1991, 49(1):29-33.
14. Miller L.H., Roberts T., Shahabuddin M., McCutchan T.F. Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). Mol Biochem Parasitol 1993, 59(1):1-14.
15. Chitarra V., Holm I., Bentley G.A., Petres S., Longacre S. The crystal structure of C-terminal merozoite surface protein 1 at 1.8A resolution, a highly protective malaria vaccine candidate. Mol Cell 1999, 3(4):457-464.
16. Burns J.M., Parke L.A., Daly T.M., Cavacini L.A., Weidanz W.P., Long C.A. A protective monoclonal antibody recognizes a variant-specific epitope in the precursor of the major merozoite surface antigen of the rodent malarial parasite Plasmodium yoelii. J Immunol 1989, 142(8):2835-2840.
17. Chappel J.A., Holder A.A. Monoclonal antibodies that inhibit Plasmodium falciparum invasion in vitro recognise the first growth factor-like domain of merozoite surface protein-1. Mol Biochem Parasitol 1993, 60(2):303-311.
18. Ling I.T., Ogun S.A., Holder A.A. Immunization against malaria with a recombinant protein. Parasite Immunol 1994, 16(2):63-67.
19. Daly T.M., Long C.A. Humoral response to a carboxyl-terminal region of the merozoite surface protein-1 plays a predominant role in controlling blood-stage infection in rodent malaria. J Immunol 1995, 155(1):236-243.
20. Kumar S., Yadava A., Keister D.B., Tian J.H., Ohl M., Perdue-Greenfield K.A., et al. Immunogenicity and in vivo efficacy of recombinant Plasmodium falciparum merozoite surface protein-1 in Aotus monkeys. Mol Med 1995, 1(3):325-332.
21. Egan A.F., Morris J., Barnish G., Allen S., Greenwood B.M., Kaslow D.C., et al. Clinical immunity to Plasmodium falciparum malaria is associated with serum antibodies to the 19-kDa C-terminal fragment of the merozoite surface antigen, PfMSP-1. J Infect Dis 1996, 173(3):765-769.
22. 19) of Plasmodium yoelii expressed in Saccharomyces cerevisiae: correlation of protection with antigen-specific antibody titer, but not with effector CD4+ T cells. J Immunol 1997, 159(7):3400-3411.
23. 19 are a major component of the invasion-inhibitory response in individuals immune to malaria. J Exp Med 2001, 193(12):1403-1412.
24. Shi Y.P., Sayed U., Qari S.H., Roberts J.M., Udhayakumar V., Oloo A.J., et al. Natural immune response to the C-terminal 19-kilodalton domain of Plasmodium falciparum merozoite surface protein 1. Infect Immun 1996, 64(7):2716-2723.
25. Egan A., Waterfall M., Pinder M., Holder A., Riley E. Characterization of human T- and B-cell epitopes in the C terminus of Plasmodium falciparum merozoite surface protein 1: evidence for poor T-cell recognition of polypeptides with numerous disulfide bonds. Infect Immun 1997, 65(8):3024-3031.
26. Hensmann M., Li C., Moss C., Lindo V., Greer F., Watts C., et al. Disulfide bonds in merozoite surface protein 1 of the malaria parasite impede efficient antigen processing and affect the in vivo antibody response. Eur J Immunol 2004, 34(3):639-648.
27. Udhayakumar V., Anyona D., Kariuki S., Shi Y.P., Bloland P.B., Branch O.H., et al. Identification of T and B cell epitopes recognized by humans in the C-terminal 42-kDa domain of the Plasmodium falciparum merozoite surface protein (MSP)-1. J Immunol 1995, 154(11):6022-6030.
28. Huaman M.C., Martin L.B., Malkin E., Narum D.L., Miller L.H., Mahanty S., et al. Ex vivo cytokine and memory T cell responses to the 42-kDa fragment of Plasmodium falciparum merozoite surface protein-1 in vaccinated volunteers. J Immunol 2008, 180(3):1451-1461.
29. Ahlborg N., Ling I.T., Howard W., Holder A.A., Riley E.M. Protective immune responses to the 42-kilodalton (kDa) region of Plasmodium yoelii merozoite surface protein 1 are induced by the C-terminal 19-kDa region but not by the adjacent 33-kDa region. Infect Immun 2002, 70(2):820-825.
30. Yuen D., Leung W.H., Cheung R., Hashimoto C., Ng S.F., Ho W., et al. Antigenicity and immunogenicity of the N-terminal 33-kDa processing fragment of the Plasmodium falciparum merozoite surface protein 1, MSP1: implications for vaccine development. Vaccine 2007, 25(3):490-499.
31. Ockenhouse C.F., Angov E., Kester K.E., Diggs C., Soisson L., Cummings J.F., et al. Phase I safety and immunogenicity trial of FMP1/AS02A, a Plasmodium falciparum MSP-1 asexual blood stage vaccine. Vaccine 2006, 24(15):3009-3017.
32. Thera M.A., Doumbo O.K., Coulibaly D., Diallo D.A., Sagara I., Dicko A., et al. Safety and allele-specific immunogenicity of a malaria vaccine in Malian adults: results of a phase I randomized trial. PLoS Clin Trials 2006, 1(7):e34.
33. Withers M.R., McKinney D., Ogutu B.R., Waitumbi J.N., Milman J.B., Apollo O.J., et al. Safety and reactogenicity of an MSP-1 malaria vaccine candidate: a randomized phase Ib dose-escalation trial in Kenyan children. PLoS Clin Trials 2006, 1(7):e32.
34. 42) vaccines for Plasmodium falciparum malaria. PLoS Clin Trials 2007, 2(4):e12.
35. Stoute J.A., Gombe J., Withers M.R., Siangla J., McKinney D., Onyango M., et al. Phase 1 randomized double-blind safety and immunogenicity trial of Plasmodium falciparum malaria merozoite surface protein FMP1 vaccine, adjuvanted with AS02A, in adults in western Kenya. Vaccine 2007, 25(1):176-184.
36. Ogutu B.R., Apollo O.J., McKinney D., Okoth W., Siangla J., Dubovsky F., et al. Blood stage malaria vaccine eliciting high antigen-specific antibody concentrations confers no protection to young children in Western Kenya. PLoS ONE 2009, 4(3):e4708.
37. Burns J.M., Belk C.C., Dunn P.D. A protective glycosylphosphatidylinositol-anchored membrane protein of Plasmodium yoelii trophozoites and merozoites contains two epidermal growth factor-like domains. Infect Immun 2000, 68(11):6189-6195.
38. Black C.G., Wu T., Wang L., Hibbs A.R., Coppel R.L. Merozoite surface protein 8 of Plasmodium falciparum contains two epidermal growth factor-like domains. Mol Biochem Parasitol 2001, 114(2):217-226.
39. Drew D.R., O'Donnell R.A., Smith B.J., Crabb B.S. A common cross-species function for the double epidermal growth factor-like modules of the highly divergent Plasmodium surface proteins MSP-1 and MSP-8. J Biol Chem 2004, 279(19):20147-20153.
40. Shi Q., Cernetich A., Daly T.M., Galvan G., Vaidya A.B., Bergman L.W., et al. Alteration in host cell tropism limits the efficacy of immunization with a surface protein of malaria merozoites. Infect Immun 2005, 73(10):6363-6371.
41. Shi Q., Lynch M.M., Romero M., Burns J.M. Enhanced protection against malaria by a chimeric merozoite surface protein vaccine. Infect Immun 2007, 75(3):1349-1358.
42. Daly T.M., Long C.A. Influence of adjuvants on protection induced by a recombinant fusion protein against malarial infection. Infect Immun 1996, 64(7):2602-2608.
43. Darko C.A., Angov E., Collins W.E., Bergmann-Leitner E.S., Girouard A.S., Hitt S.L., et al. The clinical-grade 42-kilodalton fragment of merozoite surface protein 1 of Plasmodium falciparum strain FVO expressed in Escherichia coli protects Aotus nancymai against challenge with homologous erythrocytic-stage parasites. Infect Immun 2005, 73(1):287-297.
44. 42 is strain-specific, antigen and adjuvant dependent, and correlates with antibody responses. PLoS ONE 2008, 3(7):e2830.
45. Singh S., Miura K., Zhou H., Muratova O., Keegan B., Miles A., et al. Immunity to recombinant Plasmodium falciparum merozoite surface protein 1 (MSP1): protection in Aotus nancymai monkeys strongly correlates with anti-MSP1 antibody titer and in vitro parasite-inhibitory activity. Infect Immun 2006, 74(8):4573-4580.
46. Bojang K.A., Milligan P.J., Pinder M., Vigneron L., Alloueche A., Kester K.E., et al. Efficacy of RTS,S/AS02 malaria vaccine against Plasmodium falciparum infection in semi-immune adult men in The Gambia: a randomised trial. Lancet 2001, 358(9297):1927-1934.
47. Alonso P.L., Sacarlal J., Aponte J.J., Leach A., Macete E., Milman J., et al. Efficacy of the RTS,S/AS02A vaccine against Plasmodium falciparum infection and disease in young African children: randomised controlled trial. Lancet 2004, 364(9443):1411-1420.
48. Polhemus M.E., Magill A.J., Cummings J.F., Kester K.E., Ockenhouse C.F., Lanar D.E., et al. Phase I dose escalation safety and immunogenicity trial of Plasmodium falciparum apical membrane protein (AMA-1) FMP2.1, adjuvanted with AS02A, in malaria-naive adults at the Walter Reed Army Institute of Research. Vaccine 2007, 25(21):4203-4212.
49. Thera M.A., Doumbo O.K., Coulibaly D., Laurens M.B., Kone A.K., Guindo A.B., et al. Safety and immunogenicity of an AMA1 malaria vaccine in Malian children: results of a phase 1 randomized controlled trial. PLoS ONE 2010, 5(2):e9041.
50. Jeamwattanalert P., Mahakunkijcharoen Y., Kittigul L., Mahannop P., Pichyangkul S., Hirunpetcharat C. Long-lasting protective immune response to the 19-kilodalton carboxy-terminal fragment of Plasmodium yoelii merozoite surface protein 1 in mice. Clin Vaccine Immunol 2007, 14(4):342-347.
51. Chang S.P., Case S.E., Gosnell W.L., Hashimoto A., Kramer K.J., Tam L.Q., et al. A recombinant baculovirus 42-kilodalton C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 protects Aotus monkeys against malaria. Infect Immun 1996, 64(1):253-261.
52. Kumar S., Collins W., Egan A., Yadava A., Garraud O., Blackman M.J., et al. Immunogenicity and efficacy in Aotus monkeys of four recombinant Plasmodium falciparum vaccines in multiple adjuvant formulations based on the 19-kilodalton C terminus of merozoite surface protein 1. Infect Immun 2000, 68(4):2215-2223.
53. Wipasa J., Xu H., Liu X., Hirunpetcharat C., Stowers A., Good M.F. Effect of Plasmodium yoelii exposure on vaccination with the 19-kilodalton carboxyl terminus of merozoite surface protein 1 and vice versa and implications for the application of a human malaria vaccine. Infect Immun 2009, 77(2):817-824.
54. Yoshida S., Araki H., Yokomine T. Baculovirus-based nasal drop vaccine confers complete protection against malaria by natural boosting of vaccine-induced antibodies in mice. Infect Immun 2010, 78(2):595-602.
55. Wipasa J., Xu H., Stowers A., Good M.F. Apoptotic deletion of Th cells specific for the 19-kDa carboxyl-terminal fragment of merozoite surface protein 1 during malaria infection. J Immunol 2001, 167(7):3903-3909.
56. Xu H., Wipasa J., Yan H., Zeng M., Makobongo M.O., Finkelman F.D., et al. The mechanism and significance of deletion of parasite-specific CD4(+) T cells in malaria infection. J Exp Med 2002, 195(7):881-892.
57. Wykes M.N., Zhou Y.H., Liu X.Q., Good M.F. Plasmodium yoelii can ablate vaccine-induced long-term protection in mice. J Immunol 2005, 175(4):2510-2516.
58. Hirunpetcharat C., Vukovic P., Liu X.Q., Kaslow D.C., Miller L.H., Good M.F. Absolute requirement for an active immune response involving B cells and Th cells in immunity to Plasmodium yoelii passively acquired with antibodies to the 19-kDa carboxyl-terminal fragment of merozoite surface protein-1. J Immunol 1999, 162(12):7309-7314.