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Genetic Diversity and Natural Selection in 42 kDa Region of Plasmodium vivax Merozoite Surface Protein-1 from China-Myanmar Endemic Border

  • Zhou, Xia (Medical College of Soochow University) ;
  • Tambo, Ernest (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Key Laboratory of Parasite and Vector Biology, Ministry of Health) ;
  • Su, Jing (School of Life Science, Fudan University) ;
  • Fang, Qiang (Department of Microbiology and Parasitology, Bengbu Medical College) ;
  • Ruan, Wei (Department of Parasitic Disease Control and Prevention, Zhejiang Provincial Center for Disease Control and Prevention) ;
  • Chen, Jun-Hu (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Key Laboratory of Parasite and Vector Biology, Ministry of Health) ;
  • Yin, Ming-Bo (School of Life Science, Fudan University) ;
  • Zhou, Xiao-Nong (National Institute of Parasitic Diseases, Chinese Center for Disease Control and Prevention, WHO Collaborating Centre for Tropical Diseases, National Center for International Research on Tropical Diseases, Key Laboratory of Parasite and Vector Biology, Ministry of Health)
  • Received : 2017.03.19
  • Accepted : 2017.09.18
  • Published : 2017.10.31

Abstract

Plasmodium vivax merozoite surface protein-1 (PvMSP1) gene codes for a major malaria vaccine candidate antigen. However, its polymorphic nature represents an obstacle to the design of a protective vaccine. In this study, we analyzed the genetic polymorphism and natural selection of the C-terminal 42 kDa fragment within PvMSP1 gene ($PvMSP1_{42}$) from 77 P. vivax isolates, collected from imported cases of China-Myanmar border (CMB) areas in Yunnan province and the inland cases from Anhui, Yunnan, and Zhejiang province in China during 2009-2012. Totally, 41 haplotypes were identified and 30 of them were new haplotypes. The differences between the rates of non-synonymous and synonymous mutations suggest that $PvMSP1_{42}$ has evolved under natural selection, and a high selective pressure preferentially acted on regions identified of $PvMSP1_{33}$. Our results also demonstrated that $PvMSP1_{42}$ of P. vivax isolates collected on China-Myanmar border areas display higher genetic polymorphisms than those collected from inland of China. Such results have significant implications for understanding the dynamic of the P. vivax population and may be useful information towards China malaria elimination campaign strategies.

Keywords

References

  1. Yin JH, Zhou SS, Xia ZG, Wang RB, Qian YJ, Yang WZ, Zhou XN. Historical patterns of malaria transmission in China. Adv Parasitol 2014; 86: 1-19.
  2. Vogel G. The forgotten malaria. Science 2013; 342: 684-687. https://doi.org/10.1126/science.342.6159.684
  3. Mueller I, Galinski MR, Baird JK, Carlton JM, Kochar DK, Alonso PL, del Portillo HA. Key gaps in the knowledge of Plasmodium vivax, a neglected human malaria parasite. Lancet Infect Dis 2009; 9: 555-566. https://doi.org/10.1016/S1473-3099(09)70177-X
  4. Wang Y, Ma A, Chen SB, Yang YC, Chen JH, Yin MB. Genetic diversity and natural selection of three blood-stage 6-Cys proteins in Plasmodium vivax populations from the China-Myanmar endemic border. Infect Genet Evol 2014; 28: 167-174. https://doi.org/10.1016/j.meegid.2014.09.026
  5. Kassegne K, Abe EM, Chen JH, Zhou XN. Immunomic approaches for antigen discovery of human parasites. Expert Rev Proteomics 2016; 13: 1091-1101. https://doi.org/10.1080/14789450.2016.1252675
  6. Longley RJ, Sattabongkot J, Mueller I. Insights into the naturally acquired immune response to Plasmodium vivax malaria. Parasitology 2016; 143: 154-170. https://doi.org/10.1017/S0031182015000670
  7. Chen JH, Chen SB, Wang Y, Ju C, Zhang T, Xu B, Shen HM, Mo XJ, Molina DM, Eng M, Liang X, Gardner MJ, Wang R, Hu W. An immunomics approach for the analysis of natural antibody responses to Plasmodium vivax infection. Mol Biosyst 2015; 11: 2354-2363. https://doi.org/10.1039/C5MB00330J
  8. 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. https://doi.org/10.1021/pr100705g
  9. Dutta S, Kaushal DC, Ware LA, Puri SK, Kaushal NA, Narula A, Upadhyaya DS, Lanar DE. Merozoite surface protein 1 of Plasmodium vivax induces a protective response against Plasmodium cynomolgi challenge in rhesus monkeys. Infect Immun 2005; 73: 5936-5944. https://doi.org/10.1128/IAI.73.9.5936-5944.2005
  10. Putaporntip C, Jongwutiwes S, Sakihama N, Ferreira MU, Kho WG, Kaneko A, Kanbara H, Hattori T, Tanabe K. Mosaic organization and heterogeneity in frequency of allelic recombination of the Plasmodium vivax merozoite surface protein-1 locus. Proc Natl Acad Sci U S A 2002; 99: 16348-16353. https://doi.org/10.1073/pnas.252348999
  11. Zhang L, Zhou SS, Feng J, Fang W, Xia ZG. Malaria situation in the People' s Republic of China in 2015. Chin J Parasitol Parasit Dis 2015; 34: 477-481 (in Chinese).
  12. Zhou X, Huang JL, Njuabe MT, Li SG, Chen JH, Zhou XN. A molecular survey of febrile cases in malaria-endemic areas along China-Myanmar border in Yunnan province, People's Republic of China. Parasite 2014; 21: 27. https://doi.org/10.1051/parasite/2014030
  13. Aurrecoechea C, Brestelli J, Brunk BP, Dommer J, Fischer S, Gajria B, Gao X, Gingle A, Grant G, Harb OS, Heiges M, Innamorato F, Iodice J, Kissinger JC, Kraemer E, Li W, Miller JA, Nayak V, Pennington C, Pinney DF, Roos DS, Ross C, Stoeckert CJ Jr, Treatman C, Wang H. PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Res 2009; 37: 539-543.
  14. Larkin MA, Blackshields G, Brown NP, Chenna R, McGettigan PA, McWilliam H, Valentin F, Wallace IM, Wilm A, Lopez R, Thompson JD, Gibson TJ, Higgins DG. Clustal W and Clustal X version 2.0. Bioinformatics 2007; 23: 2947-2948. https://doi.org/10.1093/bioinformatics/btm404
  15. 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. https://doi.org/10.1093/molbev/msr121
  16. Rozas J, Sanchez-DelBarrio JC, Messeguer X, Rozas R. DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 2003; 19: 2496-2497. https://doi.org/10.1093/bioinformatics/btg359
  17. Thornton K. Recombination and the properties of Tajima's D in the context of approximate-likelihood calculation. Genetics 2005; 171: 2143-2148. https://doi.org/10.1534/genetics.105.043786
  18. Bandelt HJ, Forster P, Rohl A. Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 1999; 16: 37-48. https://doi.org/10.1093/oxfordjournals.molbev.a026036
  19. Zhang W, Sun Z. Random local neighbor joining: a new method for reconstructing phylogenetic trees. Mol Phylogenet Evol 2008; 47: 117-128. https://doi.org/10.1016/j.ympev.2008.01.019
  20. Chen SB, Wang Y, Kassegne K, Xu B, Shen HM, Chen JH. Wholegenome sequencing of a Plasmodium vivax clinical isolate exhibits geographical characteristics and high genetic variation in China-Myanmar border area. BMC Genomics 2017; 18: 131. https://doi.org/10.1186/s12864-017-3523-y
  21. 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. https://doi.org/10.1038/ng.2373
  22. Shen HM, Chen SB, Wang Y, Xu B, Abe EM, Chen JH. Genomewide scans for the identification of Plasmodium vivax genes under positive selection. Malar J 2017; 16: 238. https://doi.org/10.1186/s12936-017-1882-0
  23. Pearson RD, Amato R, Auburn S, Miotto O, Almagro-Garcia J, Amaratunga C, Suon S, Mao S, Noviyanti R, Trimarsanto H, Marfurt J, Anstey NM, William T, Boni MF, Dolecek C, Hien TT, White NJ, Michon P, Siba P, Tavul L, Harrison G, Barry A, Mueller I, Ferreira MU, Karunaweera N, Randrianarivelojosia M, Gao Q, Hubbart C, Hart L, Jeffery B, Drury E, Mead D, Kekre M, Campino S, Manske M, Cornelius VJ, MacInnis B, Rockett KA, Miles A, Rayner JC, Fairhurst RM, Nosten F, Price RN, Kwiatkowski DP. Genomic analysis of local variation and recent evolution in Plasmodium vivax. Nat Genet 2016; 48: 959-964. https://doi.org/10.1038/ng.3599
  24. Hupalo DN, Luo Z, Melnikov A, Sutton PL, Rogov P, Escalante A, Vallejo AF, Herrera S, Arevalo-Herrera M, Fan Q, Wang Y, Cui L, Lucas CM, Durand S, Sanchez JF, Baldeviano GC, Lescano AG, Laman M, Barnadas C, Barry A, Mueller I, Kazura JW, Eapen A, Kanagaraj D, Valecha N, Ferreira MU, Roobsoong W, Nguitragool W, Sattabonkot J, Gamboa D, Kosek M, Vinetz JM, Gonzalez-Ceron L, Birren BW, Neafsey DE, Carlton JM. Population genomics studies identify signatures of global dispersal and drug resistance in Plasmodium vivax. Nat Genet 2016; 48: 953-958. https://doi.org/10.1038/ng.3588
  25. Zhong D, Bonizzoni M, Zhou G, Wang G, Chen B, Vardo-Zalik A, Cui L, Yan G, Zheng B. Genetic diversity of Plasmodium vivax malaria in China and Myanmar. Infect Genet Evol 2011; 11: 1419-1425. https://doi.org/10.1016/j.meegid.2011.05.009
  26. Bastos MS, da Silva-Nunes M, Malafronte RS, Hoffmann EH, Wunderlich G, Moraes SL, Ferreira MU. Antigenic polymorphism and naturally acquired antibodies to Plasmodium vivax merozoite surface protein 1 in rural Amazonians. Clin Vaccine Immunol 2007; 14: 1249-1259. https://doi.org/10.1128/CVI.00243-07
  27. Parobek CM, Bailey JA, Hathaway NJ, Socheat D, Rogers WO, Juliano JJ. Differing patterns of selection and geospatial genetic diversity within two leading Plasmodium vivax candidate vaccine antigens. PLoS Negl Trop Dis 2014; 8: e2796. https://doi.org/10.1371/journal.pntd.0002796
  28. Moore SJ, Min X, Hill N, Jones C, Zaixing Z, Cameron MM. Border malaria in China: knowledge and use of personal protection by minority populations and implications for malaria control: a questionnaire-based survey. BMC Public Health 2008; 8: 344. https://doi.org/10.1186/1471-2458-8-344
  29. Zhang HW, Liu Y, Zhang SS, Xu BL, Li WD, Tang JH, Zhou SS, Huang F. Preparation of malaria resurgence in China: case study of vivax malaria re-emergence and outbreak in Huang-Huai Plain in 2006. Adv Parasitol 2014; 86: 205-230.
  30. Dias S, Longacre S, Escalante AA, Udagama-Randeniya PV. Genetic diversity and recombination at the C-terminal fragment of the merozoite surface protein-1 of Plasmodium vivax (PvMSP-1) in Sri Lanka. Infect Genet Evol 2011; 11: 145-156. https://doi.org/10.1016/j.meegid.2010.09.007
  31. Thakur A, Alam MT, Sharma YD. Genetic diversity in the C-terminal 42 kDa region of merozoite surface protein-1 of Plasmodium vivax (PvMSP-1(42)) among Indian isolates. Acta Trop 2008; 108: 58-63. https://doi.org/10.1016/j.actatropica.2008.08.011
  32. 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
  33. Zhou XN, Bergquist R, Tanner M. Elimination of tropical disease through surveillance and response. Infect Dis Poverty 2013; 2: 1. https://doi.org/10.1186/2049-9957-2-1
  34. Chen SB, Ju C, Chen JH, Zheng B, Huang F, Xiao N, Zhou X, Ernest T, Zhou XN. Operational research needs toward malaria elimination in China. Adv Parasitol 2014; 86: 109-133.

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