A conserved multi-gene family induces cross-reactive antibodies effective in defense against Plasmodium falciparum

PLoS ONE

Volumn 4, Issue 4, 2009, Pages

  Singh, Subhash ^a,c   Soe, Soe ^a   Weisman, Simon ^a   Barnwell, John W ^b   Pérignon, Jean Louis ^a   Druilhe, Pierre ^a  

^a INSTITUT PASTEUR   (France)

^b CENTERS FOR DISEASE CONTROL AND PREVENTION   (United States)

^c Gennova Biopharmaceuticals Limited   (India)

Author keywords

[No Author keywords available]

Indexed keywords

EPITOPE; MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 3; MEROZOITE SURFACE PROTEIN 6; UNCLASSIFIED DRUG; MEROZOITE SURFACE PROTEIN 3, PLASMODIUM; MEROZOITE SURFACE PROTEIN 6, PLASMODIUM; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

AMINO ACID SEQUENCE; ARTICLE; BACTERIUM ISOLATION; BINDING AFFINITY; CARBOXY TERMINAL SEQUENCE; CHROMOSOME 10; CONTROLLED STUDY; CROSS REACTING ANTIBODY; GENE EXPRESSION; GENE LOCATION; GENE SEQUENCE; GENETIC CONSERVATION; GENETIC IDENTIFICATION; GENETIC ORGANIZATION; GENETIC SIMILARITY; HUMAN; IMMUNOASSAY; IMMUNOGENICITY; MALARIA; NONHUMAN; OPEN READING FRAME; PLASMODIUM FALCIPARUM; PROTEIN TARGETING; ANIMAL; ANTIBODY DEPENDENT CELLULAR CYTOTOXICITY; ANTIBODY PRODUCTION; CROSS REACTION; GENETICS; IMMUNOLOGY; MULTIGENE FAMILY; NUCLEOTIDE SEQUENCE;

PLASMODIUM FALCIPARUM; PRIMATES;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIBODY FORMATION; ANTIBODY-DEPENDENT CELL CYTOTOXICITY; ANTIGENS, PROTOZOAN; CONSERVED SEQUENCE; CROSS REACTIONS; HUMANS; MEMBRANE PROTEINS; MULTIGENE FAMILY; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS;

EID: 65549143622     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0005410     Document Type: Article

References (44)

1. McGregor IA, Wilson RJM (1988) Specific immunity acquired in man. In: Wernsdorfer WH, McGregor I, eds. Malaria: Principles and practice of malariology. Edinburgh: Churchill Livingstone. pp 559-620.
2. Sergent ED, Parrot L (1935) L'immunité, la prémunition et la résistance innée. Archives de l'institut Pasteur d'Algérie TXIII. pp 279-319.
3. Cohen S, Mc Gregor A, carrington S (1961) Gamma globulin and acquired immunity to human malaria. Nature 192: 733-737.
4. Edozien JC, Gilles HM, Udeozo IOK (1962) Adult and cord blood gammaglobulin and immunity to malaria in Nigerians. Lancet 2: 951-955.
5. McGregor IA, Carrington SP, Cohen S (1963) Treatment of East African P. falciparum with West African human gammaglobulin. Trans Roy Soc Trop Med Hyg 57: 170-175.
6. Sabchareon A, Burnouf T, Ouattara D, Attanath P, Bouharoun-Tayoun H, et al. (1991) Parasitologic and clinical human response to immunoglobulin administration in falciparum malaria. Am J Trop Med Hyg 45: 297-308.
7. Khusmith S, Druilhe P (1983) Cooperation between antibodies and monocytes that inhibit in vitro proliferation of Plasmodium falciparum. Infec Immun 41: 219-223.
8. Bouharoun-Tayoun H, Attanah 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.
9. Oeuvray C, Bouharoun-Tayoun H, Gras-Masse H, Bottius E, Kaidoh T, et al. (1994) Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Blood 84: 1594-1602.
10. Roussilhon C, Oeuvray C, Muller-Graf C, Tall A, Rogier C, et al. (2007) Longterm clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. PLoS Med 4: e320.
11. Soe S, Theisen M, Roussilhon C, Aye KS, Druilhe P (2004) Association between protection against clinical malaria and antibodies to merozoite surface antigens in an area of hyperendemicity in Myanmar: complementarity between responses to merozoite surface protein 3 and the 220-kilodalton glutamate-rich protein. Infect Immun 72: 247-252.
12. Singh S, Soe S, Mejia JP, Roussilhon C, Theisen M, et al. (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.
13. Polley SD, Tetteh KK, Lloyd JM, Akpogheneta OJ, Greenwood BM, et al. (2007) Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis 195: 279-287.
14. Osier FH, Polley SD, Mwangi T, Lowe B, Conway DJ, et al. (2007) Naturally acquired antibodies to polymorphic and conserved epitopes of Plasmodium falciparum merozoite surface protein 3. Parasite Immunol 29: 387-394.
15. Jafarshad A, Dziegiel MH, Lundquist R, Nielsen LK, Singh S, et al. (2007) A novel antibody-dependent cellular cytotoxicity mechanism involved in defense against malaria requires costimulation of monocytes FcgammaRII and FcgammaRIII. J Immunol 178: 3099-3106.
16. Hisaeda H, Saul A, Reece JJ, Kennedy MC, Long CA, et al. (2002) Merozoite surface protein 3 and protection against malaria in Aotus nancymai monkeys. J Infect Dis 185: 657-664.
17. Druilhe P, Spertini F, Soe Soe D, Corradin GP, Mejia P, et al. (2005) A malaria vaccine that elicits antibodies able to kill P. falciparum. PLoS Med 2: e344.
18. Sirima SB, et al. (2008) A double blind randomized controlled dose escalation Phase Ib field trial in 12-24 months old children in Burkina Faso to evaluate the safety and immunogenicity of the Plasmodium falciparum merozoite surface protein-3 LSP adjuvanted in aluminium hydroxyde versus Engerix B. Am J Trop Med Hyg 79: 252.
19. Lusingu J, et al. (2008) A phase Ib study of the safety of MSP3-LSP candidate malaria vaccine in Tanzanian children aged 12-24 months. Am J TropMed Hyg 79: 7.
20. Singh S, Soe S, Roussilhon C, Corradin G, Druilhe P (2005) Plasmodium falciparum merozoite surface protein 6 displays multiple targets for naturally occurring antibodies that mediate monocyte-dependent parasite killing. Infect Immun 73: 1235-1238.
21. Galinski MR, Ingravallo P, Corredor-Medina C, Al-Khedery B, Povoa M, et al. (2001) Plasmodium vivax merozoite surface proteins-3beta and-3gamma share structural similarities with P. vivax merozoite surface protein-3alpha and define a new gene family. Mol Biochem Parasitol 115: 41-53.
22. David PH, Hudson DE, Hadley TJ, Klotz FW, M LH (1985) Immunization of monkeys with a 140 kilodalton merozoite surface protein of Plasmodium knowlesi malaria: appearance of alternate forms of this protein. J Immunol 134: 4146-4152.
23. Lupas A, Van Dyke M, Stock J (1991) Predicting coiled coils from protein sequences. Science 252: 1162-1164.
24. Wolf E, Kim PS, Berger B (1997) MultiCoil: a program for predicting two- and three-stranded coiled coils. Protein Sci 6: 1179-1189.
25. Bornberg-Bauer E, Rivals E, M V (1998) Computational approaches to identify leucine zippers. Nucleic Acids Res 26: 2740-2746.
26. Bouharoun-Tayoun H, Druilhe P (1992) Plasmodium falciparum malaria: evidence for an isotype imbalance which may be responsible for delayed acquisition of protective immunity. Infect Immun 60: 1473-1481.
27. Druilhe P, Bouharoun-Tayoun H (2002) Human antibody subclass ELISA. Methods Mol Med 72: 457-459.
28. Bouharoun-Tayoun H, Attanath P, Sabchareon A, Chongsuphajaisiddhi T, P. D (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.
29. McColl DJ, Silva A, Foley M, Kun JF, Favaloro JM, et al. (1994) Molecular variation in a novel polymorphic antigen associated with Plasmodium falciparum merozoites. Mol Biochem Parasitol 68: 53-67.
30. Trucco C, Fernandez-Reyes D, Howell S, Stafford WH, Scott-Finnigan TJ, et al. (2001) The merozoite surface protein 6 gene codes for a 36 kDa protein associated with the Plasmodium falciparum merozoite surface protein-1 complex. Mol Biochem Parasitol 112: 91-101.
31. Pearce JA, Mills K, Triglia T, Cowman AF, Anders RF (2005) Characterisation of two novel proteins from the asexual stage of Plasmodium falciparum, H101 and H103. Mol Biochem Parasitol 139: 141-151.
32. Cowman AF, BS C (2002) The Plasmodium falciparum genome-a blueprint for erythrocyte invasion. Science 298: 126-128.
33. Reed MB, Caruana SR, Batchelor AH, Thompson JK, Crabb BS, et al. (2000) Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proc Natl Acad Sci U S A 97: 7509-7514.
34. Kaneko O, Fidock DA, Schwartz OM, M LH (2000) Disruption of the C-terminal region of EBA-175 in the Dd2/Nm clone of Plasmodium falciparum does not affect erythrocyte invasion. Mol Biochem Parasitol 110: 135-146.
35. Duraisingh MT, Triglia T, Ralph SA, Rayner JC, Barnwell JW, et al. (2003) Phenotypic variation of Plasmodium falciparum merozoite proteins directs receptor targeting for invasion of human erythrocytes. EMBO J 22: 1047-1057.
36. Chattopadhyay R, Sharma A, Srivastava VK, Pati SS, Sharma SK, et al. (2003) Plasmodium falciparum infection elicits both variant-specific and cross-reactive antibodies against variant surface antigens. Infect Immun 71: 597-604.
37. Black CG, Wang L, Hibbs AR, Werner E, RL C (1999) Identification of the Plasmodium chabaudi homologue of merozoite surface proteins 4 and 5 of Plasmodium falciparum. Infect Immun 67: 217-226.
38. Black CG, Wang L, Wu T, RL C (2003) Apical location of a novel EGF-like domain-containing protein of Plasmodium falciparum. Mol Biochem Parasitol 127: 59-68.
39. Mills KE, Pearce JA, Crabb BS, Cowman AF (2002) Truncation of merozoite surface protein 3 disrupts its trafficking and that of acidic-basic repeat protein to the surface of Plasmodium falciparum merozoites. Mol Microbiol 43: 1401-1411.
40. Pain A, Böhme U, Berry AE, Mungall K, Finn RD, et al. (2008) The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature 455: 799-803.
41. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, et al. (2008) Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 455: 757-63.
42. Rayner JC, Corredor V, Feldman D, Ingravallo P, Iderabdullah F, et al. (2002) Extensive polymorphism in the Plasmodium vivax merozoite surface coat protein MSP-3alpha is limited to specific domains. Parasitology 125: 393-405.
43. Rayner JC, Huber CS, Feldman D, Ingravallo P, Galinski MR, et al. (2004) Plasmodium vivax merozoite surface protein PvMSP-3 beta is radically polymorphic through mutation and large insertions and deletions. Infect Genet Evol 4: 309-19.
44. Audran R, Cachat M, Lurati F, Soe S, Leroy O, et al. (2005) Phase I malaria vaccine trial with a long synthetic peptide derived from the merozoite surface protein 3 antigen. Infect Immun 73: 8017-26.