Plasmodium vivax Merozoite Surface Protein-3 (PvMSP3): Expression of an 11 Member Multigene Family in Blood-Stage Parasites

PLoS ONE

Volumn 8, Issue 5, 2013, Pages

  Jiang, Jianlin ^a   Barnwell, John W ^b   Meyer, Esmeralda V S ^a   Galinski, Mary R ^c  

^a EMORY UNIVERSITY   (United States)

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

^c EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 3; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CHROMOSOME 10; CONTROLLED STUDY; DEVELOPMENTAL STAGE; FEMALE; GENE LOCUS; GENE NUMBER; GENETIC TRANSCRIPTION; HYDROPHILICITY; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; MALE; MEROZOITE; NONHUMAN; OPEN READING FRAME; PLASMODIUM VIVAX MALARIA; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTIST LIFE CYCLE STAGE; RNA TRANSLATION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; CONSENSUS SEQUENCE; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; HOST-PARASITE INTERACTIONS; MEROZOITES; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; PLASMODIUM VIVAX; PROTOZOAN PROTEINS; SAIMIRI; SEQUENCE HOMOLOGY, AMINO ACID;

EID: 84878150145     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0063888     Document Type: Article

References (66)

1. Guerra CA, Howes RE, Patil AP, Gething PW, Van Boeckel TP, et al. (2010) The international limits and population at risk of Plasmodium vivax transmission in 2009. PLoS neglected tropical diseases 4: e774.
2. Lacerda MV, Fragoso SC, Alecrim MG, Alexandre MA, Magalhaes BM, et al. (2012) Postmortem Characterization of Patients With Clinical Diagnosis of Plasmodium vivax Malaria: To What Extent Does This Parasite Kill? Clinical infectious diseases: an official publication of the Infectious Diseases Society of America 55: e67-74.
3. Galinski MR, Barnwell JW, (2008) Plasmodium vivax: who cares? Malar J 7Suppl 1: S9.
4. Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, et al. (2009) Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. The Lancet infectious diseases 9: 555-566.
5. White NJ, (2011) Determinants of relapse periodicity in Plasmodium vivax malaria. Malaria journal 10: 297.
6. Bannister LH, Mitchell GH, (2009) The malaria merozoite, forty years on. Parasitology 136: 1435-1444.
7. Galinski MR, Barnwell JW, (1996) Plasmodium vivax: Merozoites, invasion of reticulocytes and considerations for malaria vaccine development. Parasitology today 12: 20-29.
8. Galinski M, Dluzewski A, Barnwell J (2005) Merozoite Invasion of Red Blood Cells. In: IW S, editor. Molecular Approaches to Malaria. Washington, DC: ASM Press. 113-168.
9. Gaur D, Chitnis CE, (2011) Molecular interactions and signaling mechanisms during erythrocyte invasion by malaria parasites. Current opinion in microbiology 14: 422-428.
10. Li J, Han ET, (2012) Dissection of the Plasmodium vivax reticulocyte binding-like proteins (PvRBPs). Biochemical and biophysical research communications 426: 1-6.
11. Gunalan K, Gao X, Yap SS, Huang X, Preiser PR (2012) The role of the reticulocyte-binding-like protein homologues of Plasmodium in erythrocyte sensing and invasion. Cellular microbiology.
12. Tham WH, Healer J, Cowman AF, (2012) Erythrocyte and reticulocyte binding-like proteins of Plasmodium falciparum. Trends in parasitology 28: 23-30.
13. 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.
14. Galinski MR, Corredor-Medina C, Povoa M, Crosby J, Ingravallo P, et al. (1999) Plasmodium vivax merozoite surface protein-3 contains coiled-coil motifs in an alanine-rich central domain. Mol Biochem Parasitol 101: 131-147.
15. Lupas A, (1996) Coiled coils: new structures and new functions. Trends Biochem Sci 21: 375-382.
16. 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.
17. McColl DJ, Anders RF, (1997) Conservation of structural motifs and antigenic diversity in the Plasmodium falciparum merozoite surface protein-3 (MSP-3). Mol Biochem Parasitol 90: 21-31.
18. Mulhern TD, Howlett GJ, Reid GE, Simpson RJ, McColl DJ, et al. (1995) Solution structure of a polypeptide containing four heptad repeat units from a merozoite surface antigen of Plasmodium falciparum. Biochemistry 34: 3479-3491.
19. Burgess BR, Schuck P, Garboczi DN, (2005) Dissection of merozoite surface protein 3, a representative of a family of Plasmodium falciparum surface proteins, reveals an oligomeric and highly elongated molecule. J Biol Chem 280: 37236-37245.
20. Jimenez MC, Ramos CH, Barbosa JA, Galinski MR, Barnwell JW, et al. (2008) Biophysical characterization of the recombinant merozoite surface protein-3 of Plasmodium vivax. Biochim Biophys Acta 1780: 983-988.
21. 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: 309-319.
22. 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.
23. Prajapati SK, Joshi H, Valecha N, (2010) Plasmodium vivax merozoite surface protein-3 alpha: a high-resolution marker for genetic diversity studies. Journal of vector borne diseases 47: 85-90.
24. Bang G, Prieur E, Roussilhon C, Druilhe P, (2011) Pre-clinical assessment of novel multivalent MSP3 malaria vaccine constructs. PLoS One 6: e28165.
25. Sirima SB, Cousens S, Druilhe P, (2011) Protection against malaria by MSP3 candidate vaccine. The New England journal of medicine 365: 1062-1064.
26. Lima-Junior JC, Jiang J, Rodrigues-da-Silva RN, Banic DM, Tran TM, et al. (2011) B cell epitope mapping and characterization of naturally acquired antibodies to the Plasmodium vivax merozoite surface protein-3alpha (PvMSP-3alpha) in malaria exposed individuals from Brazilian Amazon. Vaccine 29: 1801-1811.
27. Lima-Junior JC, Rodrigues-da-Silva RN, Banic DM, Jiang J, Singh B, et al. (2012) Influence of HLA-DRB1 and HLA-DQB1 alleles on IgG antibody response to the P. vivax MSP-1, MSP-3alpha and MSP-9 in individuals from Brazilian endemic area. PLoS One 7: e36419.
28. Mourao LC, Morais CG, Bueno LL, Jimenez MC, Soares IS, et al. (2012) Naturally acquired antibodies to Plasmodium vivax blood-stage vaccine candidates (PvMSP-1(1)(9) and PvMSP-3alpha(3)(5)(9)(-)(7)(9)(8) and their relationship with hematological features in malaria patients from the Brazilian Amazon. Microbes and infection/Institut Pasteur 14: 730-739.
29. 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.
30. 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: 757-763.
31. Gardner MJ, Hall N, Fung E, White O, Berriman M, et al. (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419: 498-511.
32. Pain A, Bohme 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.
33. Saul A, Battistutta D, (1990) Analysis of the sequences flanking the translational start sites of Plasmodium falciparum. Mol Biochem Parasitol 42: 55-62.
34. Waters AP, Higgins DG, McCutchan TF, (1993) Evolutionary relatedness of some primate models of Plasmodium. Molecular biology and evolution 10: 914-923.
35. Singh S, Soe S, Weisman S, Barnwell JW, Perignon JL, et al. (2009) A conserved multi-gene family induces cross-reactive antibodies effective in defense against Plasmodium falciparum. PLoS ONE 4: e5410.
36. David PH, Hudson DE, Hadley TJ, Klotz FW, Miller 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.
37. Barnwell JW, Galinski MR, DeSimone SG, Perler F, Ingravallo P, (1999) Plasmodium vivax, P. cynomolgi, and P. knowlesi: identification of homologue proteins associated with the surface of merozoites. Exp Parasitol 91: 238-249.
38. Ji YE, Mericle BL, Rehkopf DH, Anderson JD, Feagin JE, (1996) The Plasmodium falciparum 6 kb element is polycistronically transcribed. Molecular and biochemical parasitology 81: 211-223.
39. Balu B, Blair PL, Adams JH, (2009) Identification of the transcription initiation site reveals a novel transcript structure for Plasmodium falciparum maebl. Experimental parasitology 121: 110-114.
40. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS biology 1: E5.
41. Scherf A, Lopez-Rubio JJ, Riviere L, (2008) Antigenic variation in Plasmodium falciparum. Annual review of microbiology 62: 445-470.
42. Harvey KL, Gilson PR, Crabb BS, (2012) A model for the progression of receptor-ligand interactions during erythrocyte invasion by Plasmodium falciparum. International journal for parasitology 42: 567-573.
43. Foth BJ, Zhang N, Chaal BK, Sze SK, Preiser PR, et al. (2011) Quantitative time-course profiling of parasite and host cell proteins in the human malaria parasite Plasmodium falciparum. Molecular & cellular proteomics: MCP 10: M110 006411.
44. 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.
45. 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. Molecular microbiology 43: 1401-1411.
46. Pfahler JM, Galinski MR, Barnwell JW, Lanzer M, (2006) Transient transfection of Plasmodium vivax blood stage parasites. Molecular and biochemical parasitology 149: 99-101.
47. Akinyi S, Hanssen E, Meyer EV, Jiang J, Korir CC, et al. (2012) A 95 kDa protein of Plasmodium vivax and P. cynomolgi visualized by three-dimensional tomography in the caveola-vesicle complexes (Schuffner's dots) of infected erythrocytes is a member of the PHIST family. Molecular microbiology 84: 816-831.
48. 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.
49. Roussilhon C, Oeuvray C, Muller-Graf C, Tall A, Rogier C, et al. (2007) Long-term clinical protection from falciparum malaria is strongly associated with IgG3 antibodies to merozoite surface protein 3. PLoS medicine 4: e320.
50. Druilhe P, Spertini F, Soesoe D, Corradin G, Mejia P, et al. (2005) A malaria vaccine that elicits in humans antibodies able to kill Plasmodium falciparum. PLoS medicine 2: e344.
51. 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.
52. 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.
53. Zakeri S, Barjesteh H, Djadid ND, (2006) Merozoite surface protein-3alpha is a reliable marker for population genetic analysis of Plasmodium vivax. Malar J 5: 53.
54. Cui L, Mascorro CN, Fan Q, Rzomp KA, Khuntirat B, et al. (2003) Genetic diversity and multiple infections of Plasmodium vivax malaria in Western Thailand. Am J Trop Med Hyg 68: 613-619.
55. Ord R, Polley S, Tami A, Sutherland CJ, (2005) High sequence diversity and evidence of balancing selection in the Pvmsp3alpha gene of Plasmodium vivax in the Venezuelan Amazon. Mol Biochem Parasitol 144: 86-93.
56. Bruce MC, Galinski MR, Barnwell JW, Snounou G, Day KP (1999) Polymorphism at the merozoite surface protein-3alpha locus of Plasmodium vivax: global and local diversity. 518-525 p.
57. Aresha M, Sanath M, Deepika F, Renu W, Anura B, et al. (2008) Genotyping of Plasmodium vivax infections in Sri Lanka using Pvmsp-3alpha and Pvcs genes as markers: A preliminary report. Trop Biomed 25: 100-106.
58. Veron V, Legrand E, Yrinesi J, Volney B, Simon S, et al. (2009) Genetic diversity of msp3alpha and msp1_b5 markers of Plasmodium vivax in French Guiana. Malar J 8: 40.
59. Kosek M, Yori PP, Gilman RH, Calderon M, Zimic M, et al. (2012) High degree of Plasmodium vivax diversity in the Peruvian Amazon demonstrated by tandem repeat polymorphism analysis. Am J Trop Med Hyg 86: 580-586.
60. Ribeiro RS, Ladeira L, Rezende AM, Fontes CJ, Carvalho LH, et al. (2011) Analysis of the genetic variability of PvMSP-3alpha among Plasmodium vivax in Brazilian field isolates. Memorias do Instituto Oswaldo Cruz 106Suppl 1: 27-33.
61. Barnwell JW, Nichols ME, Rubinstein P, (1989) In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med 169: 1795-1802.
62. Campbell CC, Collins WE, Chin W, Roberts JM, Broderson JR, (1983) Studies of the Sal I strain of Plasmodium vivax in the squirrel monkey (Saimiri sciureus). J Parasitol 69: 598-601.
63. Galinski MR, Medina CC, Ingravallo P, Barnwell JW, (1992) A reticulocyte-binding protein complex of Plasmodium vivax merozoites. Cell 69: 1213-1226.
64. Livak KJ, Schmittgen TD, (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.
65. Nielsen H, Engelbrecht J, Brunak S, von Heijne G, (1997) Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10: 1-6.
66. Eisenhaber B, Bork P, Eisenhaber F, (1999) Prediction of potential GPI-modification sites in proprotein sequences. J Mol Biol 292: 741-758.