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Population genetic analysis of Plasmodium vivax vir genes in Pakistan

  • Sylvatrie-Danne Dinzouna-Boutamba (Department of Parasitology and Tropical Medicine, School of Medicine, Kyungpook National University) ;
  • Zin Moon (Department of Parasitology and Tropical Medicine, School of Medicine, Kyungpook National University) ;
  • Sanghyun Lee (Department of Parasitology and Tropical Medicine, School of Medicine, Kyungpook National University) ;
  • Sahib Gul Afridi (Department of Biochemistry, Abdul Wali Khan University Mardan) ;
  • Huong Giang Le (Department of Parasitology and Tropical Medicine, Department of Convergence Medical Science, and Institute of Health Science, Gyeongsang National University College of Medicine) ;
  • Yeonchul Hong (Department of Parasitology and Tropical Medicine, School of Medicine, Kyungpook National University) ;
  • Byoung-Kuk Na (Department of Parasitology and Tropical Medicine, Department of Convergence Medical Science, and Institute of Health Science, Gyeongsang National University College of Medicine) ;
  • Youn-Kyoung Goo (Department of Parasitology and Tropical Medicine, School of Medicine, Kyungpook National University)
  • Received : 2024.05.08
  • Accepted : 2024.06.21
  • Published : 2024.08.31

Abstract

Plasmodium vivax variant interspersed repeats (vir) refer to the key protein used for escaping the host immune system. Knowledge in the genetic variation of vir genes can be used for the development of vaccines or diagnostic methods. Therefore, we evaluated the genetic diversity of the vir genes of P. vivax populations of several Asian countries, including Pakistan, which is a malaria-endemic country experiencing a significant rise in malaria cases in recent years. We analyzed the genetic diversity and population structure of 4 vir genes (vir 4, vir 12, vir 21, and vir 27) in the Pakistan P. vivax population and compared these features to those of the corresponding vir genes in other Asian countries. In Pakistan, vir 4 (S=198, H=9, Hd=0.889, Tajima's D value=1.12321) was the most genetically heterogenous, while the features of vir 21 (S=8, H=7, Hd=0.664, Tajima's D value =-0.63763) and vir 27 (S =25, H =11, Hd =0.682, Tajima's D value=-2.10836) were relatively conserved. Additionally, vir 4 was the most genetically diverse among Asian P. vivax populations, although within population diversity was low. Meanwhile, vir 21 and vir 27 among all Asian populations were closely related genetically. Our findings on the genetic diversity of vir genes and its relationships between populations in diverse geographical locations contribute toward a better understanding of the genetic characteristics of vir. The high level of genetic diversity of vir 4 suggests that this gene can be a useful genetic marker for understanding the P. vivax population structure. Longitudinal genetic diversity studies of vir genes in P. vivax isolates obtained from more diverse geographical areas are needed to better understand the function of vir genes and their use for the development of malaria control measures, such as vaccines.

Keywords

Acknowledgement

This work was supported by the National Research Foundation of Korea (NRF) grant (NRF-2024M3A9H5043141). We are grateful to all blood donors and the supportive laboratory personnel who contributed in samples collection and diagnosis in the Pakistan.

References

  1. World Health Organization. World Malaria Report 2022. World Health Organization. Geneva, Switzerland. 2022.
  2. Fernandez-Becerra C, Pein O, de Oliveira TR, Yamamoto MM, Cassola AC, et al. Variant proteins of Plasmodium vivax are not clonally expressed in natural infections. Mol Microbiol 2005;58(3):648-658. https://doi.org/10.1111/j.1365-2958.2005.04850.x
  3. del Portillo HA, Lanzer M, Rodriguez-Malaga S, Zavala F, Fernandez-Becerra C. Variant genes and the spleen in Plasmodium vivax malaria. Int J Parasitol 2004;34(13-14):1547-1554. https://doi.org/10.1016/j.ijpara.2004.10.012
  4. Pasternak ND, Dzikowski R. PfEMP1: an antigen that plays a key role in the pathogenicity and immune evasion of the malaria parasite Plasmodium falciparum. Int J Biochem Cell Biol 2009;41(7):1463-1466. https://doi.org/10.1016/j.biocel.2008.12.012
  5. Fernandez-Becerra C, Yamamoto MM, Vencio RZ, Lacerda M, Rosanas-Urgell A, et al. Plasmodium vivax and the importance of the subtelomeric multigene vir superfamily. Trends Parasitol 2009;25(1):44-51. https://doi.org/10.1016/j.pt.2008.09.012
  6. Arevalo-Herrera M, Chitnis C, Herrera S. Current status of Plasmodium vivax vaccine. Hum Vaccin 2010;6(1):124-132. https://doi.org/10.4161/hv.6.1.9931
  7. Bull PC, Abdi AI. The role of PfEMP1 as targets of naturally acquired immunity to childhood malaria: prospects for a vaccine. Parasitology 2016;143(2):171-186. https://doi.org/10.1017/S0031182015001274
  8. Oliveira TR, Fernandez-Becerra C, Jimenez MC, Del Portillo HA, Soares IS. Evaluation of the acquired immune responses to Plasmodium vivax VIR variant antigens in individuals living in malaria-endemic areas of Brazil. Malar J 2006;5:83. https://doi.org/10.1186/1475-2875-5-83
  9. Lee S, Choi YK, Goo YK. Humoral and cellular immune response to Plasmodium vivax VIR recombinant and synthetic antigens in individuals naturally exposed to P. vivax in the Republic of Korea. Malar J 2021;20(1):288. https://doi.org/10.1186/s12936-021-03810-2
  10. Na BK, Kim TS, Lin K, Baek MC, Chung DI, et al. Genetic polymorphism of vir genes of Plasmodium vivax in Myanmar. Parasitol Int 2021;80:102233. https://doi.org/10.1016/j.parint.2020.102233
  11. Son UH, Dinzouna-Boutamba SD, Lee S, Yun HS, Kim JY, et al. Diversity of vir genes in Plasmodium vivax from endemic regions in the Republic of Korea: an initial evaluation. Korean J Parasitol 2017;55(2):149-158. https://doi.org/10.3347/kjp.2017.55.2.149
  12. Gupta P, Pande V, Das A, Singh V. Genetic polymorphisms in VIR genes among Indian Plasmodium vivax populations. Korean J Parasitol 2014;52(5):557-564. https://doi.org/10.3347/kjp.2014.52.5.557
  13. Gupta P, Das A, Singh OP, Ghosh SK, Singh V. Assessing the genetic diversity of the vir genes in Indian Plasmodium vivax population. Acta Trop 2012;124(2):133-139. https://doi.org/10.1016/j.actatropica.2012.07.002
  14. Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, et al. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 1993;61(2):315-320. https://doi.org/10.1016/0166-6851(93)90077-b
  15. Librado P, Rozas J. DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 2009;25(11):1451-1452. https://doi.org/10.1093/bioinformatics/btp187
  16. Leigh JW, Bryant D. PopART: full-feature software for haplotype network construction. Methods Ecol Evol 2015;6(9):1110-1116. https://doi.org/10.1111/2041-210X.12410
  17. Goo YK. Vivax malaria and the potential role of the subtelomeric multigene vir superfamily. Microorganisms 2022;10(6):1083. https://doi.org/10.3390/microorganisms10061083
  18. Fernandez-Becerra C, Bernabeu M, Castellanos A, Correa BR, Obadia T, et al. Plasmodium vivax spleen-dependent genes encode antigens associated with cytoadhesion and clinical protection. Proc Natl Acad Sci U S A 2020;117(23):13056-13065. https://doi.org/10.1073/pnas.1920596117
  19. Wesolowski A, Taylor AR, Chang HH, Verity R, Tessema S, et al. Mapping malaria by combining parasite genomic and epidemiologic data. BMC Med 2018;16(1):190. https://doi.org/10.1186/s12916-018-1181-9
  20. Bonnell E, Pasquier E, Wellinger RJ. Telomere replication: solving multiple end replication problems. Front Cell Dev Biol 2021;9:668171. https://doi.org/10.3389/fcell.2021.668171
  21. Eckshtain-Levi N, Weisberg AJ, Vinatzer BA. The population genetic test Tajima's D identifies genes encoding pathogen-associated molecular patterns and other virulence-related genes in Ralstonia solanacearum. Mol Plant Pathol 2018;19(9):2187-2192. https://doi.org/10.1111/mpp.12688
  22. Hudson RR, Kaplan NL. Deleterious background selection with recombination. Genetics 1995;141(4):1605-1617. https://doi.org/10.1093/genetics/141.4.1605
  23. Fantin RF, Coelho CH, Berhe AD, Magalhaes LMD, Pereira DB, et al. Immunological characterization of a VIR protein family member (VIR-14) in Plasmodium vivax-infected subjects from different epidemiological regions in Africa and South America. PLoS Negl Trop Dis 2023;17(4):e0011229. https://doi.org/10.1371/journal.pntd.0011229