Parasites, Hosts and Diseases

The Korea Society for Parasitology and Tropical Medicine (대한기생충학·열대의학회)
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Allelic Diversity and Geographical Distribution of the Gene Encoding Plasmodium falciparum Merozoite Surface Protein-3 in Thailand

  • Received : 2014.11.30
  • Accepted : 2015.02.25
  • Published : 2015.04.30
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Abstract

Merozoite surface proteins (MSPs) of malaria parasites play critical roles during the erythrocyte invasion and so are potential candidates for malaria vaccine development. However, because MSPs are often under strong immune selection, they can exhibit extensive genetic diversity. The gene encoding the merozoite surface protein-3 (MSP-3) of Plasmodium falciparum displays 2 allelic types, K1 and 3D7. In Thailand, the allelic frequency of the P. falciparum msp-3 gene was evaluated in a single P. falciparum population in Tak at the Thailand and Myanmar border. However, no study has yet looked at the extent of genetic diversity of the msp-3 gene in P. falciparum populations in other localities. Here, we genotyped the msp-3 alleles of 63 P. falciparum samples collected from 5 geographical populations along the borders of Thailand with 3 neighboring countries (Myanmar, Laos, and Cambodia). Our study indicated that the K1 and 3D7 alleles co-existed, but at different proportions in different Thai P. falciparum populations. K1 was more prevalent in populations at the Thailand-Myanmar and Thailand-Cambodia borders, whilst 3D7 was more prevalent at the Thailand-Laos border. Global analysis of the msp-3 allele frequencies revealed that proportions of K1 and 3D7 alleles of msp-3 also varied in different continents, suggesting the divergence of malaria parasite populations. In conclusion, the variation in the msp-3 allelic patterns of P. falciparum in Thailand provides fundamental knowledge for inferring the P. falciparum population structure and for the best design of msp-3 based malaria vaccines.

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References

  1. Miller LH, Baruch DI, Marsh K, Doumbo OK. The pathogenic basis of malaria. Nature 2002; 415: 673-679. https://doi.org/10.1038/415673a
  2. Murray CJ, Ortblad KF, Guinovart C, Lim SS, Wolock TM, Roberts DA, Dansereau EA, Graetz N, Barber RM, Brown JC, Wang H, Duber HC, Naghavi M, Dicker D, Dandona L, Salomon JA, Heuton KR, Foreman K, Phillips DE, Fleming TD, Flaxman AD, Phillips BK, Johnson EK, Coggeshall MS, Abd-Allah F, Abera SF, Abraham JP, Abubakar I, Abu-Raddad LJ, Abu-Rmeileh NM, Achoki T, Adeyemo AO, Adou AK, Adsuar JC, Agardh EE, Akena D, Al Kahbouri MJ, Alasfoor D, Albittar MI, Alcala-Cerra G, Alegretti MA, Alemu ZA, Alfonso-Cristancho R, Alhabib S, Ali R, Alla F, Allen PJ, Alsharif U, Alvarez E, Alvis-Guzman N, Amankwaa AA, Amare AT, Amini H, Ammar W, Anderson BO, Antonio CA, Anwari P, Arnlov J, Arsenijevic VS, Artaman A, Asghar RJ, Assadi R, Atkins LS, Badawi A, Balakrishnan K, Banerjee A, Basu S, Beardsley J, Bekele T, Bell ML, Bernabe E, Beyene TJ, Bhala N, Bhalla A, Bhutta ZA, Abdulhak AB, Binagwaho A, Blore JD, Basara BB, Bose D, Brainin M, Breitborde N, Castaneda-Orjuela CA, Catala-Lopez F, Chadha VK, Chang JC, Chiang PP, Chuang TW, Colomar M, Cooper LT, Cooper C, Courville KJ, Cowie BC, Criqui MH, Dandona R, Dayama A, De Leo D, Degenhardt L, Del Pozo-Cruz B, Deribe K, Des Jarlais DC, Dessalegn M, Dharmaratne SD, Dilmen U, Ding EL, Driscoll TR, Durrani AM, Ellenbogen RG, Ermakov SP, Esteghamati A, Faraon EJ, Farzadfar F, Fereshtehnejad SM, Fijabi DO, Forouzanfar MH, Fra Paleo U, Gaffikin L, Gamkrelidze A, Gankpe FG, Geleijnse JM, Gessner BD, Gibney KB, Ginawi IA, Glaser EL, Gona P, Goto A, Gouda HN, Gugnani HC, Gupta R, Gupta R, Hafezi-Nejad N, Hamadeh RR, Hammami M, Hankey GJ, Harb HL, Haro JM, Havmoeller R, Hay SI, Hedayati MT, Pi IB, Hoek HW, Hornberger JC, Hosgood HD, Hotez PJ, Hoy DG, Huang JJ, Iburg KM, Idrisov BT, Innos K, Jacobsen KH, Jeemon P, Jensen PN, Jha V, Jiang G, Jonas JB, Juel K, Kan H, Kankindi I, Karam NE, Karch A, Karema CK, Kaul A, Kawakami N, Kazi DS, Kemp AH, Kengne AP, Keren A, Kereselidze M, Khader YS, Khalifa SE, Khan EA, Khang YH, Khonelidze I, Kinfu Y, Kinge JM, Knibbs L, Kokubo Y, Kosen S, Defo BK, Kulkarni VS, Kulkarni C, Kumar K, Kumar RB, Kumar GA, Kwan GF, Lai T, Balaji AL, Lam H, Lan Q, Lansingh VC, Larson HJ, Larsson A, Lee JT, Leigh J, Leinsalu M, Leung R, Li Y, Li Y, De Lima GM, Lin HH, Lipshultz SE, Liu S, Liu Y, Lloyd BK, Lotufo PA, Machado VM, Maclachlan JH, Magis-Rodriguez C, Majdan M, Mapoma CC, Marcenes W, Marzan MB, Masci JR, Mashal MT, Mason-Jones AJ, Mayosi BM, Mazorodze TT, Mckay AC, Meaney PA, Mehndiratta MM, Mejia-Rodriguez F, Melaku YA, Memish ZA, Mendoza W, Miller TR, Mills EJ, Mohammad KA, Mokdad AH, Mola GL, Monasta L, Montico M, Moore AR, Mori R, Moturi WN, Mukaigawara M, Murthy KS, Naheed A, Naidoo KS, Naldi L, Nangia V, Narayan KM, Nash D, Nejjari C, Nelson RG, Neupane SP, Newton CR, Ng M, Nisar MI, Nolte S, Norheim OF, Nowaseb V, Nyakarahuka L, Oh IH, Ohkubo T, Olusanya BO, Omer SB, Opio JN, Orisakwe OE, Pandian JD, Papachristou C, Caicedo AJ, Patten SB, Paul VK, Pavlin BI, Pearce N, Pereira DM, Pervaiz A, Pesudovs K, Petzold M, Pourmalek F, Qato D, Quezada AD, Quistberg DA, Rafay A, Rahimi K, Rahimi-Movaghar V, Ur Rahman S, Raju M, Rana SM, Razavi H, Reilly RQ, Remuzzi G, Richardus JH, Ronfani L, Roy N, Sabin N, Saeedi MY, Sahraian MA, Samonte GM, Sawhney M, Schneider IJ, Schwebel DC, Seedat S, Sepanlou SG, Servan-Mori EE, Sheikhbahaei S, Shibuya K, Shin HH, Shiue I, Shivakoti R, Sigfusdottir ID, Silberberg DH, Silva AP, Simard EP, Singh JA, Skirbekk V, Sliwa K, Soneji S, Soshnikov SS, Sreeramareddy CT, Stathopoulou VK, Stroumpoulis K, Swaminathan S, Sykes BL, Tabb KM, Talongwa RT, Tenkorang EY, Terkawi AS, Thomson AJ, Thorne-Lyman AL, Towbin JA, Traebert J, Tran BX, Dimbuene ZT, Tsilimbaris M, Uchendu US, Ukwaja KN, Uzun SB, Vallely AJ, Vasankari TJ, Venketasubramanian N, Violante FS, Vlassov VV, Vollset SE, Waller S, Wallin MT, Wang L, Wang X, Wang Y, Weichenthal S, Weiderpass E, Weintraub RG, Westerman R, White RA, Wilkinson JD, Williams TN, Woldeyohannes SM, Wong JQ, Xu G, Yang YC, Yano Y, Yentur GK, Yip P, Yonemoto N, Yoon SJ, Younis M, Yu C, Jin KY, El Sayed Zaki M, Zhao Y, Zheng Y, Zhou M, Zhu J, Zou XN, Lopez AD, Vos T. Global, regional, and national incidence and mortality for HIV, tuberculosis, and malaria during 1990-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 2014; 384: 1005-1070. https://doi.org/10.1016/S0140-6736(14)60844-8
  3. Breman JG. The ears of the hippopotamus: manifestations, determinants, and estimates of the malaria burden. Am J Trop Med Hyg 2001; 64: 1-11.
  4. Cui L, Yan G, Sattabongkot J, Cao Y, Chen B, Chen X, Fan Q, Fang Q, Jongwutiwes S, Parker D, Sirichaisinthop J, Kyaw MP, Su XZ, Yang H, Yang Z, Wang B, Xu J, Zheng B, Zhong D, Zhou G. Malaria in the Greater Mekong Subregion: heterogeneity and complexity. Acta Trop 2012; 121: 227-239. https://doi.org/10.1016/j.actatropica.2011.02.016
  5. Noedl H, Se Y, Schaecher K, Smith BL, Socheat D, Fukuda MM, Artemisinin Resistance in Cambodia 1 (ARC1) Study Consortium. Evidence of artemisinin-resistant malaria in western Cambodia. N Engl J Med 2008; 359: 2619-2620. https://doi.org/10.1056/NEJMc0805011
  6. Phyo AP, Nkhoma S, Stepniewska K, Ashley EA, Nair S, McGready R, ler Moo C, Al-Saai S, Dondorp AM, Lwin KM, Singhasivanon P, Day NP, White NJ, Anderson TJ, Nosten F. Emergence of artemisinin-resistant malaria on the western border of Thailand: a longitudinal study. Lancet 2012; 379: 1960-1966. https://doi.org/10.1016/S0140-6736(12)60484-X
  7. Fairhurst RM, Nayyar GM, Breman JG, Hallett R, Vennerstrom JL, Duong S, Ringwald P, Wellems TE, Plowe CV, Dondorp AM. Artemisinin-resistant malaria: research challenges, opportunities, and public health implications. Am J Trop Med Hyg 2012; 87: 231-241. https://doi.org/10.4269/ajtmh.2012.12-0025
  8. Ellis RD, Sagara I, Doumbo O, Wu Y. Blood stage vaccines for Plasmodium falciparum: current status and the way forward. Hum Vaccin 2010; 6: 627-634. https://doi.org/10.4161/hv.6.8.11446
  9. Miller LH, Ackerman HC, Su XZ, Wellems TE. Malaria biology and disease pathogenesis: insights for new treatments. Nat Med 2013; 19: 156-167. https://doi.org/10.1038/nm.3073
  10. Anders RE, Adda CG, Foley M, Norton RS. Recombinant protein vaccines against the asexual blood stages of Plasmodium falciparum. Hum Vaccin 2010; 6: 39-53. https://doi.org/10.4161/hv.6.1.10712
  11. McColl DJ, Silva A, Foley M, Kun JF, Favaloro JM, Thompson JK, Marshall VM, Coppel RL, Kemp DJ, Anders RF. Molecular variation in a novel polymorphic antigen associated with Plasmodium falciparum merozoites. Mol Biochem Parasitol 1994; 68: 53-67. https://doi.org/10.1016/0166-6851(94)00149-9
  12. Oeuvray C, Bouharoun-Tayoun H, Grass-Masse H, Lepers JP, Ralamboranto L, Tartar A, Druilhe P. A novel merozoite surface antigen of Plasmodium falciparum (MSP-3) identified by cellular-antibody cooperative mechanism antigenicity and biological activity of antibodies. Mem Inst Oswaldo Cruz 1994; 89(Suppl 2): 77-80. https://doi.org/10.1590/S0074-02761994000600018
  13. Oeuvray C, Bouharoun-Tayoun H, Gras-Masse H, Bottius E, Kaidoh T, Aikawa M, Filgueira MC, Tartar A, Druilhe P. Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Blood 1994; 84: 1594-1602.
  14. Hisaeda H, Saul A, Reece JJ, Kennedy MC, Long CA, Miller LH, Stowers AW. Merozoite surface protein 3 and protection against malaria in Aotus nancymai monkeys. J Infect Dis 2002; 185: 657-664. https://doi.org/10.1086/339187
  15. Carvalho LJ, Oliveira SG, Theisen M, Alves FA, Andrade MC, Zanini GM, Brigido MC, Oeuvray C, Povoa MM, Muniz JA, Druilhe P, Daniel-Ribeiro CT. 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 2004; 59: 363-372. https://doi.org/10.1111/j.0300-9475.2004.01409.x
  16. Soe S, Theisen M, Roussilhon C, Aye KS, Druilhe P: 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 2004; 72: 247-252. https://doi.org/10.1128/IAI.72.1.247-252.2004
  17. Polley SD, Tetteh KK, Lloyd JM, Akpogheneta OJ, Greenwood BM, Bojang KA, Conway DJ. Plasmodium falciparum merozoite surface protein 3 is a target of allele-specific immunity and alleles are maintained by natural selection. J Infect Dis 2007; 195: 279-287. https://doi.org/10.1086/509806
  18. Osier FH, Polley SD, Mwangi T, Lowe B, Conway DJ, Marsh K. Naturally acquired antibodies to polymorphic and conserved epitopes of Plasmodium falciparum merozoite surface protein 3. Parasite Immunol 2007; 29: 387-394. https://doi.org/10.1111/j.1365-3024.2007.00951.x
  19. Audran R, Cachat M, Lurati F, Soe S, Leroy O, Corradin G, Druilhe P, Spertini F. Phase I malaria vaccine trial with a long synthetic peptide derived from the merozoite surface protein 3 antigen. Infect Immun 2005; 73: 8017-8026. https://doi.org/10.1128/IAI.73.12.8017-8026.2005
  20. Sirima SB, Nebie I, Ouedraogo A, Tiono AB, Konate AT, Gansane A, Derme AI, Diarra A, Ouedraogo A, Soulama I, Cuzzin-Ouattara N, Cousens S, Leroy O. Safety and immunogenicity of the Plasmodium falciparum merozoite surface protein-3 long synthetic peptide (MSP3-LSP) malaria vaccine in healthy, semi-immune adult males in Burkina Faso, West Africa. Vaccine 2007; 25: 2723-2732. https://doi.org/10.1016/j.vaccine.2006.05.090
  21. Lusingu JP, Gesase S, Msham S, Francis F, Lemnge M, Seth M, Sembuche S, Rutta A, Minja D, Segeja MD, Bosomprah S, Cousens S, Noor R, Chilengi R, Druilhe P. Satisfactory safety and immunogenicity of MSP3 malaria vaccine candidate in Tanzanian children aged 12-24 months. Malar J 2009; 8: 163. https://doi.org/10.1186/1475-2875-8-163
  22. Sirima SB, Tiono AB, Ouedraogo A, Diarra A, Ouedraogo AL, Yaro JB, Ouedraogo E, Gansane A, Bougouma EC, Konate AT, Kabore Y, Traore A, Chilengi R, Soulama I, Luty AJ, Druilhe P, Cousens S, Nebie I. Safety and immunogenicity of the malaria vaccine candidate MSP3 long synthetic peptide in 12-24 months-old Burkinabe children. PLoS One 2009; 4: e7549. https://doi.org/10.1371/journal.pone.0007549
  23. McColl DJ, Anders RF. Conservation of structural motifs and antigenic diversity in the Plasmodium falciparum merozoite surface protein-3 (MSP-3). Mol Biochem Parasitol 1997; 90: 21-31. https://doi.org/10.1016/S0166-6851(97)00130-8
  24. Huber W, Felger I, Matile H, Lipps HJ, Steiger S, Beck HP. Limited sequence polymorphism in the Plasmodium falciparum merozoite surface protein 3. Mol Biochem Parasitol 1997; 87: 231-234. https://doi.org/10.1016/S0166-6851(97)00067-4
  25. Jordan SJ, Branch OH, Castro JC, Oster RA, Rayner JC. Genetic diversity of the malaria vaccine candidate Plasmodium falciparum merozoite surface protein-3 in a hypoendemic transmission environment. Am J Trop Med Hyg 2009; 80: 479-486.
  26. Ebrahimzadeh A, Mohammadi S, Jamshidi A. Allelic forms of merozoite surface protein-3 in Plasmodium falciparum isolates from Southeast of Iran. Jundishapur J Microbiol 2014; 7: e9829.
  27. Soulama I, Bigoga JD, Ndiaye M, Bougouma EC, Quagraine J, Casimiro PN, Stedman TT, Sirima SB. Genetic diversity of polymorphic vaccine candidate antigens (apical membrane antigen-1, merozoite surface protein-3, and erythrocyte binding antigen-175) in Plasmodium falciparum isolates from western and central Africa. Am J Trop Med Hyg 2011; 84: 276-284. https://doi.org/10.4269/ajtmh.2011.10-0365
  28. Simpalipan P, Pattaradilokrat S, Siripoon N, Seugorn A, Kaewthamasorn M, Butcher RD, Harnyuttanakorn P. Diversity and population structure of Plasmodium falciparum in Thailand based on the spatial and temporal haplotype patterns of the C-terminal 19-kDa domain of merozoite surface protein-1. Malar J 2014; 13: 54. https://doi.org/10.1186/1475-2875-13-54
  29. Pumpaibool T, Arnathau C, Durand P, Kanchanakhan N, Siripoon N, Suegorn A, Sitthi-Amorn C, Renaud F, Harnyuttanakorn P. Genetic diversity and population structure of Plasmodium falciparum in Thailand, a low transmission country. Malar J 2009; 8: 155. https://doi.org/10.1186/1475-2875-8-155
  30. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B. Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 2002; 419: 498-511. https://doi.org/10.1038/nature01097
  31. Excoffier L, Lischer HE. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resour 2010; 10: 564-567. https://doi.org/10.1111/j.1755-0998.2010.02847.x
  32. Cui L, Yan G, Sattabongkot J, Chen B, Cao Y, Fan Q, Parker D, Sirichaisinthop J, Su XZ, Yang H, Yang Z, Wang B, Zhou G. Challenges and prospects for malaria elimination in the Greater Mekong Subregion. Acta Trop 2012; 121: 240-245. https://doi.org/10.1016/j.actatropica.2011.04.006
  33. Pattaradilokrat S, Mu J, Awadalla P, Su X. Genome diversity and applications in genetic studies of the human malaria parasites Plasmodium falciparum and Plasmodium vivax. In Carlton JM, Perkins SL, Deitsch KW eds, Malaria Parasites: Comparative Genomics, Evolution and Molecular Biology. Wymondham, UK. Caister Academic Press. 2013, p 59-90.
  34. Kuesap J, Chaijaroenkul W, Ketprathum K, Tattiyapong P, Na-Bangchang K. Evolution of genetic polymorphisms of Plasmodium falciparum merozoite surface protein (PfMSP) in Thailand. Korean J Parasitol 2014; 52: 105-109. https://doi.org/10.3347/kjp.2014.52.1.105
  35. Rungsihirunrat K, Chaijaroenkul W, Siripoon N, Seugorn A, Na-Bangchang K. Genotyping of polymorphic marker (MSP3alpha and MSP3beta) genes of Plasmodium vivax field isolates from malaria endemic of Thailand. Trop Med Int Health 2011; 16: 794-801. https://doi.org/10.1111/j.1365-3156.2011.02771.x
  36. James S, Moehle K, Renard A, Mueller MS, Vogel D, Zurbriggen R, Pluschke G, Robinson JA. Synthesis, solution structure and immune recognition of an epidermal growth factor-like domain from Plasmodium falciparum merozoite surface protein-1. Chem Biochem 2006; 7: 1943-1950.
  37. Pizarro JC, Chitarra V, Verger D, Holm I, Petres S, Dartevelle S, Nato F, Longacre S, Bentley GA. Crystal structure of a Fab complex formed with PfMSP1-19, the C-terminal fragment of merozoite surface protein 1 from Plasmodium falciparum: a malaria vaccine candidate. J Mol Biol 2003; 328: 1091-1103. https://doi.org/10.1016/S0022-2836(03)00376-0
  38. Kamolratanakul P, Dhanamun B, Lertmaharit S, Seublingwong T, Udomsangpetch R, Thaithong S. Epidemiological studies of malaria at Pong Nam Ron, eastern Thailand. Southeast Asian J Trop Med Public Health 1994; 25: 425-429.
  39. Wangroongsarb P, Sudathip P, Satimai W. Characteristics and malaria prevalence of migrant populations in malaria-endemic areas along the Thai-Cambodian border. Southeast Asian J Trop Med Public Health 2012; 43: 261-269.
  40. Bang G, Prieur E, Roussilhon C, Druilhe P. Pre-clinical assessment of novel multivalent MSP3 malaria vaccine constructs. PLoS One 2011; 6: e28165. https://doi.org/10.1371/journal.pone.0028165

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