Plasmodium falciparum merozoite surface protein 1 (MSP-1)-MSP-3 chimeric protein: Immunogenicity determined with human-compatible adjuvants and induction of protective immune response

Infection and Immunity

Volumn 78, Issue 2, 2010, Pages 872-883

  Mazumdar, Suman ^a   Mukherjee, Paushali ^a   Yazdani, Syed Shams ^a   Jain, S K ^b   Mohmmed, Asif ^a   Chauhan, Virander Singh ^a  

^a INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^b HAMDARD UNIVERSITY   (India)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIPARASITIC AGENT; GAMMA INTERFERON; IMMUNOGLOBULIN G; MALARIA VACCINE; MEROZOITE SURFACE PROTEIN 1; MEROZOITE SURFACE PROTEIN 3; MSP FU 24 PROTEIN; PROTOZOAL PROTEIN; RECOMBINANT PROTEIN; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ANIMAL EXPERIMENT; ANTIMICROBIAL ACTIVITY; ARTICLE; BLOOD SAMPLING; CELLULAR IMMUNITY; CONTROLLED STUDY; CYTOKINE PRODUCTION; ESCHERICHIA COLI; GROWTH INHIBITION; HUMAN; IMMUNE RESPONSE; IMMUNOGENICITY; IMMUNOGLOBULIN BLOOD LEVEL; IN VITRO STUDY; MALARIA FALCIPARUM; MOUSE; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN CONFORMATION; RABBIT;

ADJUVANTS, IMMUNOLOGIC; ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; ENZYME-LINKED IMMUNOSORBENT ASSAY; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; MALARIA VACCINES; MALARIA, FALCIPARUM; MEROZOITE SURFACE PROTEIN 1; MICE; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RABBITS; RECOMBINANT PROTEINS;

EID: 76749111160     PISSN: 00199567     EISSN: 10985522     Source Type: Journal    
DOI: 10.1128/IAI.00427-09     Document Type: Article

References (48)

1. Blackman, M. J., T. J. Scott-Finnigan, S. Shai, and A. A. Holder. 1994. Antibodies inhibit the protease-mediated processing of a malaria merozoite surface protein. J. Exp. Med. 180:389-393.
2. Blackman, M. J., H. G. Heidrich, S. Donachie, J. S. McBride, and A. A. Holder. 1990. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasioninhibiting antibodies. J. Exp. Med. 172:379-382.
3. Bouharoun-Tayoun, H., C. Oeuvray, F. Lunel, and P. Druilhe. 1995. Mechanisms underlying the monocyte-mediated antibody-dependent killing of Plasmodium falciparum asexual blood stages. J. Exp. Med. 182:409-418.
4. Bouharoun-Tayoun, H., P. Attanath, A. Sabchareon, T. Chongsuphajaisiddhi, and P. Druilhe. 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.
5. Burghaus, P. A., and A. A. Holder. 1994. Expression of the 19-kilodalton carboxy-terminal fragment of the Plasmodium falciparum merozoite surface protein-1 in Escherichia coli as a correctly folded protein. Mol. Biochem. Parasitol. 64:165-169.
6. Carvalho, L. J., S. G. Oliveira, M. Theisen, F. A. Alves, M. C. Andrade, G. M. Zanini, M. C. Brígido, C. Oeuvray, M. M. Póvoa, J. A. Muniz, P. Druilhe, and C. T. Daniel-Ribeiro. 2004. Immunization of Saimiri sciureus monkeys with Plasmodium falciparum merozoite surface protein-3 and glutamate-rich protein suggests that protection is related to antibody levels. Scand. J. Immunol. 59:363-372.
7. Chappel, J. A., and A. A. Holder. 1993. Monoclonal antibodies that inhibit Plasmodium falciparum invasion in vitro recognise the first growth factor-like domain of merozoite surface protein-1. Mol. Biochem. Parasitol. 60:303-311.
8. Chitarra, V., I. Holm, G. A. Bentley, S. Petres, and S. Longacre. 1999. The crystal structure of C-terminal merozoite surface protein 1 at 1.8A resolution, a highly protective malaria vaccine candidate. Mol. Cell 3:457-464.
9. Corran, P. H., R. A. O'Donnell, J. Todd, C. Uthaipibull, A. A. Holder, B. S. Crabb, and E. M. Riley. 2004. The fine specificity, but not the invasion inhibitory activity, of 19-kilodalton merozoite surface protein 1-specific antibodies is associated with resistance to malarial parasitemia in a crosssectional survey in The Gambia. Infect. Immun. 72:6185-6189.
10. Daly, T. M., and C. A. Long. 1995. 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. 155:236-243.
11. Druilhe, P., F. Spertini, D. Soesoe, G. Corradin, P. Mejia, S. Singh, R. Audran, A. Bouzidi, C. Oeuvray, and C. Roussilhon. 2005. A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. PLoS Med. 2:e344.
12. Egan, A. F., M. J. Blackman, and D. C. Kaslow. 2000. Vaccine efficacy of recombinant Plasmodium falciparum merozoite surface protein 1 in malarianaive, -exposed, and/or -rechallenged Aotus vociferans monkeys. Infect. Immun. 68:1418-1427.
13. Guevara-Patino, J. A., A. A. Holder, J. S. McBride, and M. J. Blackman. 1997. Antibodies that inhibit malaria merozoite surface protein-1 processing and erythrocyte invasion are blocked by naturally acquired human antibodies. J. Exp. Med. 186:1689-1699.
14. Hermsen, C. C., D. F. Verhage, D. S. Telgt, K. Teelen, J. T. Bousema, M. Roestenberg, A. Bolad, K. Berzins, G. Corradin, O. Leroy, M. Theisen, and R. W. Sauerwein. 2007. Glutamate-rich protein (GLURP) induces antibodies that inhibit in vitro growth of Plasmodium falciparum in a phase 1 malaria vaccine trial. Vaccine 25:2930-2940.
15. Hirunpetcharat, C., J. H. Tian, D. C. Kaslow, N. van Rooijen, S. Kumar, J. A. Berzofsky, L. H. Miller, and M. F. Good. 1997. Complete protective immunity induced in mice by immunization with the 19-kilodalton carboxyl-terminal fragment of the merozoite surface protein-1 (MSP-1[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. 159:3400-3411.
16. Hisaeda, H., A. Saul, J. J. Reece, M. C. Kennedy, C. A. Long, L. H. Miller, and A. W. Stowers. 2002. Merozoite surface protein 3 and protection against malaria in Aotus nancymai monkeys. J. Infect. Dis. 185:657-664.
17. Hodder, A. N., P. E. Crewther, M. L. Matthew, G. E. Reid, R. L. Moritz, R. J. Simpson, and R. F. Anders. 1996. The disulfide bond structure of Plasmodium apical membrane antigen-1. J. Biol. Chem. 271:29446-29452.
18. Holder, A. A., and E. M. Riley. 1996. Human immune response to MSP-1. Parasitol. Today 12:173-174.
19. Hunter, R. L., and A. A. Lal. 1994. Copolymer adjuvants in malaria vaccine development. Am. J. Trop. Med. Hyg. 50(Suppl. 4):52-58.
20. 19) can play a protective role against bloodstage Plasmodium falciparum infection in individuals in a malaria endemic area of Africa. J. Immunol. 173:666-672.
21. Kumar, S., W. Collins, A. Egan, A. Yadava, O. Garraud, M. J. Blackman, J. A. Guevara-Patino, C. Diggs, and D. C. Kaslow. 2000. 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. 68:2215-2223.
22. Lambros, C., and J. P. Vanderberg. 1979. Synchronization of Plasmodium falciparum erythrocytic stage in culture. J. Parasitol. 65:418-420.
23. Mahanty, S., A. Saul, and L. H. Miller. 2003. Progress in the development of recombinant and synthetic blood-stage malaria vaccines. J. Exp. Biol. 206: 3781-3788.
24. McColl, D. J., and R. F. Anders. 1997. Conservation of structural motifs and antigenic diversity in the Plasmodium falciparum merozoite surface protein-3 (MSP-3). Mol. Biochem. Parasitol. 90:21-31.
25. McColl, D. J., A. Silva, M. Foley, J. F. Kun, J. M. Favaloro, J. K. Thompson, V. M. Marshall, R. L. Coppel, D. J. Kemp, and R. F. Anders. 1994. Molecular variation in a novel polymorphic antigen associated with Plasmodium falciparum merozoites. Mol. Biochem. Parasitol. 68:53-67.
26. Morgan, W. D., B. Birdsall, T. A. Frenkiel, M. G. Gradwell, P. A. Burghaus, S. E. Syed, C. Uthaipibull, A. A. Holder, and J. Feeney. 1999. Solution structure of an EGF module pair from the Plasmodium falciparum merozoite surface protein 1. J. Mol. Biol. 289:113-122.
27. O'Donnell, R. A., T. F. de Koning-Ward, R. A. Burt, M. Bockarie, J. C. Reeder, A. F. Cowman, and B. S. Crabb. 2001. Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J. Exp. Med. 193:1403-1412.
28. Oeuvray, C., H. Bouharoun-Tayoun, H. Gras-Masse, E. Bottius, T. Kaidoh, M. Aikawa, M. C. Filgueira, A. Tartar, and P. Druilhe. 1994. Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Blood 84:1594-1602.
29. Oeuvray, C., M. Theisen, C. Rogier, J. F. Trape, S. Jepsen, and P. Druilhe. 2000. Cytophilic immunoglobulin responses to Plasmodium falciparum glutamate-rich protein are correlated with protection against clinical malaria in Dielmo, Senegal. Infect. Immun. 68:2617-2620.
30. Okech, B. A., P. H. Corran, J. Todd, A. Joynson-Hicks, C. Uthaipibull, T. G. Egwang, A. A. Holder, and E. M. Riley. 2004. Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1(19), predicts protection from malaria infection and high-density parasitemia. Infect. Immun. 72:1557-1567.
31. Pan, W., D. Huang, Q. Zhang, L. Qu, D. Zhang, X. Zhang, X. Xue, and F. Qian. 2004. Fusion of two malaria vaccine candidate antigens enhances product yield, immunogenicity, and antibody-mediated inhibition of parasite growth in vitro. J. Immunol. 172:6167-6174.
32. Parren, P. W., P. A. Warmerdam, L. C. Boeije, J. Arts, N. A. Westerdaal, A. Vlug, P. J. Capel, L. A. Aarden, and J. G. van de Winkel. 1992. On the interaction of IgG subclasses with the low affinity Fc gamma RIIa (CD32) on human monocytes, neutrophils, and platelets. Analysis of a functional polymorphism to human IgG2. J. Clin. Invest. 90:1537-1546.
33. Pleass, R. J., and J. M. Woof. 2001. Fc receptors and immunity to parasites. Trends Parasitol. 17:545-551.
34. Richie, T. L., and A. Saul. 2002. Progress and challenges for malaria vaccines. Nature 415:694-701.
35. Rotman, H. L., T. M. Daly, and C. A. Long. 1999. Plasmodium: immunization with carboxyl-terminal regions of MSP-1 protects against homologous but not heterologous blood-stage parasite challenge. Exp. Parasitol. 91:78-85.
36. Sachdeva, S., A. Mohmmed, P. V. Dasaradhi, B. S. Crabb, A. Katyal, P. Malhotra, and V. S. Chauhan. 2006. Immunogenicity and protective efficacy of Escherichia coli expressed Plasmodium falciparum merozoite surface protein-1(42) using human compatible adjuvants. Vaccine 24:2007-2016.
37. Saul, A., G. Lawrence, A. Smillie, C. M. Rzepczyk, C. Reed, D. Taylor, K. Anderson, A. Stowers, R. Kemp, A. Allworth, R. F. Anders, G. V. Brown, D. Pye, P. Schoofs, D. O. Irving, S. L. Dyer, G. C. Woodrow, W. R. Briggs, R. Reber, and D. Stürchler. 1999. Human phase I vaccine trials of 3 recombinant asexual stage malaria antigens with Montanide ISA720 adjuvant. Vaccine 17:3145-3159.
38. Shi, Q., M. M. Lynch, M. Romero, and J. M. Burns, Jr. 2007. Enhanced protection against malaria by a chimeric merozoite surface protein vaccine. Infect. Immun. 75:1349-1358.
39. Singh, S., K. Miura, H. Zhou, O. Muratova, B. Keegan, A. Miles, L. B. Martin, A. J. Saul, L. H. Miller, and C. A. Long. 2006. 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. 74:4573-4580.
40. Singh, S., S. Soe, J. P. Mejia, C. Roussilhon, M. Theisen, G. Corradin, and P. Druilhe. 2004. Identification of a conserved region of Plasmodium falciparum MSP3 targeted by biologically active antibodies to improve vaccine design. J. Infect. Dis. 190:1010-1018.
41. Snow, R. W., C. A. Guerra, A. M. Noor, H. Y. Myint, and S. I. Hay. 2005. The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature 434:214-217.
42. Theisen, M., S. Soe, C. Oeuvray, A. W. Thomas, J. Vuust, S. Danielsen, S. Jepsen, and P. Druilhe. 1998. The glutamate-rich protein (GLURP) of Plasmodium falciparum is a target for antibody-dependent monocyte-mediated inhibition of parasite growth in vitro. Infect. Immun. 66:11-17.
43. Theisen, M., S. Soe, K. Brunstedt, F. Follmann, L. Bredmose, H. Israelsen, S. M. Madsen, and P. Druilhe. 2004. A Plasmodium falciparum GLURP-MSP3 chimeric protein; expression in Lactococcus lactis, immunogenicity and induction of biologically active antibodies. Vaccine 22:1188-1198.
44. Trager, W., and J. B. Jensen. 1976. Human malaria parasite in continuous culture. Science 193:673-675.
45. Uthaipibull, C., B. Aufiero, S. E. Syed, B. Hansen, J. A. Guevara-Patiño, E. Angov, I. T. Ling, K. Fegeding, W. D. Morgan, C. Ockenhouse, B. Birdsall, J. Feeney, J. A. Lyon, and A. A. Holder. 2001. Inhibitory and blocking monoclonal antibody epitopes on merozoite surface protein 1 of the malaria parasite Plasmodium falciparum. J. Mol. Biol. 307:1381-1394.
46. Wickramarachchi, T., Y. S. Devi, A. Mohmmed, and V. S. Chauhan. 2008. Identification and characterization of a novel Plasmodium falciparum merozoite apical protein involved in erythrocyte binding and invasion. PLoS One 3:e1732.
47. Zhang, D., and W. Pan. 2005. Evaluation of three Pichia pastoris-expressed Plasmodium falciparum merozoite proteins as a combination vaccine against infection with blood-stage parasites. Infect. Immun. 73:6530-6536.
48. Zhang, Q., X. Xue, L. Qu, and W. Pan. 2007. Construction and evaluation of a multistage combination vaccine against malaria. Vaccine 25:2112-2119.