Heterogeneous genetic diversity pattern in Plasmodium vivax genes encoding merozoite surface proteins (MSP) -7E, -7F and -7L

Malaria Journal

Volumn 13, Issue 1, 2014, Pages

  Garzón Ospina, Diego ^a,b   Forero Rodríguez, Johanna ^a   Patarroyo, Manuel A ^a,b  

^a FUNDACIÓN INSTITUTO DE INMUNOLOGÍA DE COLOMBIA FIDIC   (Colombia)

^b UNIVERSIDAD DEL ROSARIO   (Colombia)

Author keywords

Genetic diversity; msp 7; Natural selection; Plasmodium vivax; Selective sweep

Indexed keywords

MEMBRANE PROTEIN; MEROZOITE SURFACE PROTEIN 7E; MEROZOITE SURFACE PROTEIN 7F; MEROZOITE SURFACE PROTEIN 7L; UNCLASSIFIED DRUG; MEROZOITE SURFACE PROTEIN 7, PLASMODIUM; PROTOZOAL DNA; PROTOZOAL PROTEIN;

AMINO ACID SEQUENCE; ARTICLE; BALANCING SELECTION; BLOOD SAMPLING; DNA SEQUENCE; GENE EXPRESSION; GENE LINKAGE DISEQUILIBRIUM; GENE MUTATION; GENETIC CODE; GENETIC DISTANCE; GENETIC VARIABILITY; GENOTYPE; MOLECULAR EVOLUTION; NATURAL SELECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PLASMODIUM CYNOMOLGI; PLASMODIUM VIVAX; SELECTIVE SWEEP; SPECIES DIFFERENCE; CHEMISTRY; CLUSTER ANALYSIS; COLOMBIA; GENETICS; HUMAN; ISOLATION AND PURIFICATION; MEROZOITE; MOLECULAR GENETICS; PARASITOLOGY; PLASMODIUM VIVAX MALARIA; SEQUENCE HOMOLOGY;

CLUSTER ANALYSIS; COLOMBIA; DNA, PROTOZOAN; GENETIC VARIATION; HUMANS; MALARIA, VIVAX; MEMBRANE PROTEINS; MEROZOITES; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMODIUM VIVAX; PROTOZOAN PROTEINS; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY;

EID: 84924296302     PISSN: None     EISSN: 14752875     Source Type: Journal    
DOI: 10.1186/1475-2875-13-495     Document Type: Article

References (72)

1. Singh J, Purohit B, Desai A, Savardekar L, Shanbag P, Kshirsagar N: Clinical Manifestations, treatment, and outcome of hospitalized patients with Plasmodium vivax malaria in two Indian States: A Retrospective Study. Malar Res Treat 2013, 2013:341862.
2. Jain V, Agrawal A, Singh N: Malaria in a tertiary health care facility of Central India with special reference to severe vivax: implications for malaria control. Pathog Glob Health 2013, 107:299-304.
3. Pacheco MA, Battistuzzi FU, Junge RE, Cornejo OE, Williams CV, Landau I, Rabetafika L, Snounou G, Jones-Engel L, Escalante AA: Timing the origin of human malarias: the lemur puzzle. BMC Evol Biol 2011, 11:299.
4. Carlton JM, Adams JH, Silva JC, Bidwell SL, Lorenzi H, Caler E, Crabtree J, Angiuoli SV, Merino EF, Amedeo P, Cheng Q, Coulson RM, Crabb BS, Del Portillo HA, Essien K, Feldblyum TV, Fernandez-Becerra C, Gilson PR, Gueye AH, Guo X, Kang'a S, Kooij TW, Korsinczky M, Meyer EV, Nene V, Paulsen I, White O, Ralph SA, Ren Q, Sargeant TJ, et al: Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature 2008, 455:757-763.
5. Iyer J, Gruner AC, Renia L, Snounou G, Preiser PR: Invasion of host cells by malaria parasites: a tale of two protein families. Mol Microbiol 2007, 65:231-249.
6. Chitnis CE, Blackman MJ: Host cell invasion by malaria parasites. Parasitol Today 2000, 16:411-415.
7. Rodriguez LE, Urquiza M, Ocampo M, Curtidor H, Suarez J, Garcia J, Vera R, Puentes A, Lopez R, Pinto M, Rivera Z, Patarroyo ME: Plasmodium vivax MSP-1 peptides have high specific binding activity to human reticulocytes. Vaccine 2002, 20:1331-1339.
8. Urquiza M, Rodriguez LE, Suarez JE, Guzman F, Ocampo M, Curtidor H, Segura C, Trujillo E, Patarroyo ME: Identification of Plasmodium falciparum MSP-1 peptides able to bind to human red blood cells. Parasite Immunol 1996, 18:515-526.
9. Kauth CW, Woehlbier U, Kern M, Mekonnen Z, Lutz R, Mucke N, Langowski J, Bujard H: Interactions between merozoite surface proteins 1, 6, and 7 of the malaria parasite Plasmodium falciparum. J Biol Chem 2006, 281:31517-31527.
10. Pachebat JA, Ling IT, Grainger M, Trucco C, Howell S, Fernandez-Reyes D, Gunaratne R, Holder AA: The 22 kDa 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, 117:83-89.
11. Trucco C, Fernandez-Reyes D, Howell S, Stafford WH, Scott-Finnigan TJ, Grainger M, Ogun SA, Taylor WR, Holder AA: 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 2001, 112:91-101.
12. Garzon-Ospina D, Cadavid LF, Patarroyo MA: Differential expansion of the merozoite surface protein (msp)-7 gene family in Plasmodium species under a birth-and-death model of evolution. Mol Phylogenet Evol 2010, 55:399-408.
13. Garcia Y, Puentes A, Curtidor H, Cifuentes G, Reyes C, Barreto J, Moreno A, Patarroyo ME: Identifying merozoite surface protein 4 and merozoite surface protein 7 Plasmodium falciparum protein family members specifically binding to human erythrocytes suggests a new malarial parasite-redundant survival mechanism. J Med Chem 2007, 50:5665-5675.
14. Kadekoppala M, O'Donnell RA, Grainger M, Crabb BS, Holder AA: Deletion of the Plasmodium falciparum merozoite surface protein 7 gene impairs parasite invasion of erythrocytes. Eukaryot Cell 2008, 7:2123-2132.
15. Tewari R, Ogun SA, Gunaratne RS, Crisanti A, Holder AA: Disruption of Plasmodium berghei merozoite surface protein 7 gene modulates parasite growth in vivo. Blood 2005, 105:394-396.
16. Mello K, Daly TM, Morrisey J, Vaidya AB, Long CA, Bergman LW: A multigene family that interacts with the amino terminus of Plasmodium MSP-1 identified using the yeast two-hybrid system. Eukaryot Cell 2002, 1:915-925.
17. Chen JH, Jung JW, Wang Y, Ha KS, Lu F, Lim CS, Takeo S, Tsuboi T, Han ET: Immunoproteomics profiling of blood stage Plasmodium vivax infection by high-throughput screening assays. J Proteome Res 2010, 9:6479-6489.
18. Wang L, Crouch L, Richie TL, Nhan DH, Coppel RL: Naturally acquired antibody responses to the components of the Plasmodium falciparum merozoite surface protein 1 complex. Parasite Immunol 2003, 25:403-412.
19. Woehlbier U, Epp C, Hackett F, Blackman MJ, Bujard H: Antibodies against multiple merozoite surface antigens of the human malaria parasite Plasmodium falciparum inhibit parasite maturation and red blood cell invasion. Malar J 2010, 9:77.
20. Mello K, Daly TM, Long CA, Burns JM, Bergman LW: Members of the merozoite surface protein 7 family with similar expression patterns differ in ability to protect against Plasmodium yoelii malaria. Infect Immun 2004, 72:1010-1018.
21. Garzon-Ospina D, Lopez C, Forero-Rodriguez J, Patarroyo MA: Genetic diversity and selection in three Plasmodium vivax merozoite surface protein 7 (Pvmsp-7) genes in a Colombian population. PLoS One 2012, 7:e45962.
22. Garzon-Ospina D, Romero-Murillo L, Tobon LF, Patarroyo MA: Low genetic polymorphism of merozoite surface proteins 7 and 10 in Colombian Plasmodium vivax isolates. Infect Genet Evol 2011, 11:528-531.
23. Roy SW, Weedall GD, da Silva RL, Polley SD, Ferreira MU: Sequence diversity and evolutionary dynamics of the dimorphic antigen merozoite surface protein-6 and other Msp genes of Plasmodium falciparum. Gene 2009, 443:12-21.
24. Tetteh KK, Stewart LB, Ochola LI, Amambua-Ngwa A, Thomas AW, Marsh K, Weedall GD, Conway DJ: Prospective identification of malaria parasite genes under balancing selection. PLoS One 2009, 4:e5568.
25. Bozdech Z, Mok S, Hu G, Imwong M, Jaidee A, Russell B, Ginsburg H, Nosten F, Day NP, White NJ, Carlton JM, Preiser PR: The transcriptome of Plasmodium vivax reveals divergence and diversity of transcriptional regulation in malaria parasites. Proc Natl Acad Sci U S A 2008, 105:16290-16295.
26. Sawai H, Otani H, Arisue N, Palacpac N, de Oliveira ML, Pathirana S, Handunnetti S, Kawai S, Kishino H, Horii T, Tanabe K: Lineage-specific positive selection at the merozoite surface protein 1 (msp1) locus of Plasmodium vivax and related simian malaria parasites. BMC Evol Biol 2010, 10:52.
27. Tanabe K, Escalante A, Sakihama N, Honda M, Arisue N, Horii T, Culleton R, Hayakawa T, Hashimoto T, Longacre S, Pathirana S, Handunnetti S, Kishino H: Recent independent evolution of msp1 polymorphism in Plasmodium vivax and related simian malaria parasites. Mol Biochem Parasitol 2007, 156:74-79.
28. Imwong M, Pukrittayakamee S, Gruner AC, Renia L, Letourneur F, Looareesuwan S, White NJ, Snounou G: Practical PCR genotyping protocols for Plasmodium vivax using Pvcs and Pvmsp1. Malar J 2005, 4:20.
29. ORF Finder (Open Reading Frame Finder). [http://www.ncbi.nlm.nih.gov/projects/gorf/]
30. Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
31. Abascal F, Zardoya R, Posada D: ProtTest: selection of best-fit models of protein evolution. Bioinformatics 2005, 21:2104-2105.
32. Neafsey DE, Galinsky K, Jiang RH, Young L, Sykes SM, Saif S, Gujja S, Goldberg JM, Young S, Zeng Q, Chapman SB, Dash AP, Anvikar AR, Sutton PL, Birren BW, Escalante AA, Barnwell JW, Carlton JM: The malaria parasite Plasmodium vivax exhibits greater genetic diversity than Plasmodium falciparum. Nat Genet 2012, 44:1046-1050.
33. Suyama M, Torrents D, Bork P: PAL2NAL: robust conversion of protein sequence alignments into the corresponding codon alignments. Nucleic Acids Res 2006, 34:W609-612.
34. Jorda J, Kajava AV: T-REKS: identification of Tandem REpeats in sequences with a K-meanS based algorithm. Bioinformatics 2009, 25:2632-2638.
35. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009, 25:1451-1452.
36. Depaulis F, Veuille M: Neutrality tests based on the distribution of haplotypes under an infinite-site model. Mol Biol Evol 1998, 15:1788-1790.
37. Zhang J, Rosenberg HF, Nei M: Positive Darwinian selection after gene duplication in primate ribonuclease genes. Proc Natl Acad Sci U S A 1998, 95:3708-3713.
38. Nei M, Kumar S: Molecular evolution and phylogenetics. Oxford New York: Oxford University Press; 2000.
39. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 2011, 28:2731-2739.
40. Delport W, Poon AF, Frost SD, Kosakovsky Pond SL: Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26:2455-2457.
41. Pond SL, Frost SD, Grossman Z, Gravenor MB, Richman DD, Brown AJ: Adaptation to different human populations by HIV-1 revealed by codonbased analyses. PLoS Comput Biol 2006, 2:e62.
42. Kosakovsky Pond SL, Frost SD: Not so different after all: a comparison of methods for detecting amino acid sites under selection.Mol Biol Evol 2005, 22:1208-1222.
43. Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL: Detecting individual sites subject to episodic diversifying selection. PLoS Genet 2012, 8:e1002764.
44. Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K: FUBAR: a fast, unconstrained bayesian approximation for inferring selection. Mol Biol Evol 2013, 30:1196-1205.
45. Jukes TH, Cantor CR: Evolution of protein molecules. In Mammalian Protein Metabolism. Edited by Munro HN. New York: Academic Press; 1969.
46. Kelly JK: A test of neutrality based on interlocus associations. Genetics 1997, 146:1197-1206.
47. Kosakovsky Pond SL, Posada D, Gravenor MB, Woelk CH, Frost SD: Automated phylogenetic detection of recombination using a genetic algorithm. Mol Biol Evol 2006, 23:1891-1901.
48. Rozas J, Gullaud M, Blandin G, Aguade M: DNA variation at the rp49 gene region of Drosophila simulans: evolutionary inferences from an unusual haplotype structure. Genetics 2001, 158:1147-1155.
49. Hudson RR, Kaplan NL: Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 1985, 111:147-164.
50. Martin DP, Lemey P, Lott M, Moulton V, Posada D, Lefeuvre P: RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 2010, 26:2462-2463.
51. Tachibana S, Sullivan SA, Kawai S, Nakamura S, Kim HR, Goto N, Arisue N, Palacpac NM, Honma H, Yagi M, Tougan T, Katakai Y, Kaneko O, Mita T, Kita K, Yasutomi Y, Sutton PL, Shakhbatyan R, Horii T, Yasunaga T, Barnwell JW, Escalante AA, Carlton JM, Tanabe K: Plasmodium cynomolgi genome sequences provide insight into Plasmodium vivax and the monkey malaria clade. Nat Genet 2012, 44:1051-1055.
52. Mongui A, Perez-Leal O, Soto SC, Cortes J, Patarroyo MA: Cloning, expression, and characterisation of a Plasmodium vivax MSP7 family merozoite surface protein. Biochem Biophys Res Commun 2006, 351:639-644.
53. Figtree M, Pasay CJ, Slade R, Cheng Q, Cloonan N, Walker J, Saul A: Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA 1 and MSP 1 genes. Mol Biochem Parasitol 2000, 108:53-66.
54. Mascorro CN, Zhao K, Khuntirat B, Sattabongkot J, Yan G, Escalante AA, Cui L: Molecular evolution and intragenic recombination of the merozoite surface protein MSP-3alpha from the malaria parasite Plasmodium vivax in Thailand. Parasitology 2005, 131:25-35.
55. Gomez A, Suarez CF, Martinez P, Saravia C, Patarroyo MA: High polymorphism in Plasmodium vivax merozoite surface protein-5 (MSP5). Parasitology 2006, 133:661-672.
56. Putaporntip C, Udomsangpetch R, Pattanawong U, Cui L, Jongwutiwes S: Genetic diversity of the Plasmodium vivax merozoite surface protein-5 locus from diverse geographic origins. Gene 2010, 456:24-35.
57. Nurminsky D: Selective sweep. Georgetown, Tex. New York, N.Y: Landes Bioscience/Eurekah.com; Kluwer Academic/Plenum Publishers; 2005.
58. Putaporntip C, Jongwutiwes S, Ferreira MU, Kanbara H, Udomsangpetch R, Cui L: Limited global diversity of the Plasmodium vivax merozoite surface protein 4 gene. Infect Genet Evol 2009, 9:821-826.
59. Martinez P, Suarez CF, Gomez A, Cardenas PP, Guerrero JE, Patarroyo MA: High level of conservation in Plasmodium vivax merozoite surface protein 4 (PvMSP4). Infect Genet Evol 2005, 5:354-361.
60. Pacheco MA, Elango AP, Rahman AA, Fisher D, Collins WE, Barnwell JW, Escalante AA: Evidence of purifying selection on merozoite surface protein 8 (MSP8) and 10 (MSP10) in Plasmodium spp. Infect Genet Evol 2012, 12:978-986.
61. Forero-Rodriguez J, Garzon-Ospina D, Patarroyo MA: Low genetic diversity and functional constraint in loci encoding Plasmodium vivax P12 and P38 proteins in the Colombian population. Malar J 2014, 13:58.
62. Forero-Rodriguez J, Garzon-Ospina D, Patarroyo MA: Low genetic diversity in the locus encoding the Plasmodium vivax P41 protein in Colombia's parasite population. Malar J 2014, 13:388.
63. Chenet SM, Pacheco MA, Bacon DJ, Collins WE, Barnwell JW, Escalante AA: The evolution and diversity of a low complexity vaccine candidate, merozoite surface protein 9 (MSP-9), in Plasmodium vivax and closely related species. Infect Genet Evol 2013, 20:239-248.
64. Pacheco MA, Ryan EM, Poe AC, Basco L, Udhayakumar V, Collins WE, Escalante AA: Evidence for negative selection on the gene encoding rhoptry-associated protein 1 (RAP-1) in Plasmodium spp. Infect Genet Evol 2010, 10:655-661.
65. Carlton JM, Das A, Escalante AA: Genomics, population genetics and evolutionary history of Plasmodium vivax. Adv Parasitol 2013, 81:203-222.
66. Slatkin M, Wiehe T: Genetic hitch-hiking in a subdivided population. Genet Res 1998, 71:155-160.
67. Nurminsky DI: Genes in sweeping competition. Cell Mol Life Sci 2001, 58:125-134.
68. Perez-Tris J, Hellgren O, Krizanauskiene A, Waldenstrom J, Secondi J, Bonneaud C, Fjeldsa J, Hasselquist D, Bensch S: Within-host speciation of malaria parasites. PLoS One 2007, 2:e235.
69. Sutherland CJ, Tanomsing N, Nolder D, Oguike M, Jennison C, Pukrittayakamee S, Dolecek C, Hien TT, do Rosario VE, Arez AP, Pinto J, Michon P, Escalante AA, Nosten F, Burke M, Lee R, Blaze M, Otto TD, Barnwell JW, Pain A, Williams J, White NJ, Day NP, Snounou G, Lockhart PJ, Chiodini PL, Imwong M, Polley SD: Two nonrecombining sympatric forms of the human malaria parasite Plasmodium ovale occur globally. J Infect Dis 2010, 201:1544-1550.
70. Mu J, Joy DA, Duan J, Huang Y, Carlton J, Walker J, Barnwell J, Beerli P, Charleston MA, Pybus OG, Su XZ: Host switch leads to emergence of Plasmodium vivax malaria in humans. Mol Biol Evol 2005, 22:1686-1693.
71. Burge C, Karlin S: Prediction of complete gene structures in human genomic DNA. J Mol Biol 1997, 268:78-94.
72. Rice BL, Acosta MM, Pacheco MA, Carlton JM, Barnwell JW, Escalante AA: The origin and diversification of the merozoite surface protein 3 (msp3) multi-gene family in Plasmodium vivax and related parasites. Mol Phylogenet Evol 2014, 78C:172-184.