Natural Selection Maintains a Stable Polymorphism at the Circumsporozoite Protein Locus of Plasmodium Falciparum in a Low Endemic Area

Overview

Journal Infect Genet Evol

Specialties Biology
Genetics
Infectious Diseases

Date 2009 May 23

PMID 19460323

Citations 11

Authors

Chaturong Putaporntip

Somchai Jongwutiwes

Austin L Hughes

Affiliations

Soon will be listed here.

Abstract

Circumsporozoite protein gene sequences of Plasmodium falciparum were collected in 1996-1997 and in 2006-2007 from a single endemic area in Thailand. Repeat units were more similar within the same haplotype than between haplotypes, supporting the hypothesis that repeat arrays evolve by a process of concerted evolution. There was evidence that natural selection has favored amino acid changes in the Th2R and Th3R T-cell epitope regions. One haplotype in these epitopes, designated *5/*1, occurred in approximately 70% of sequences in both collection periods. The most common other haplotypes differed from *5/*1 by at least two amino acid replacements; and divergence in the epitopes was correlated with divergence in the repeats. These patterns are most consistent with balancing selection driven by interactions with the immune system of the vertebrate host, probably involving both T-cell recognition of the Th2R and Th3R epitopes and antibody responses to the repeats.

Citing Articles

Genetic variation of the circumsporozoite protein in parasite isolates from Homabay County in Kenya.

Maina M, Musundi S, Kuja J, Waweru H, Kiboi D, Kanoi B Front Parasitol. 2025; 3():1346017.

PMID: 39817167 PMC: 11732096. DOI: 10.3389/fpara.2024.1346017.

Genetic polymorphism of circumsporozoite protein of Plasmodium falciparum among Chinese migrant workers returning from Africa to Henan Province.

He Z, Zhang Q, Wang D, Hu Y, Zhou R, Qian D Malar J. 2022; 21(1):248.

PMID: 36030242 PMC: 9419638. DOI: 10.1186/s12936-022-04275-7.

Insights into the molecular diversity of Plasmodium vivax merozoite surface protein-3γ (pvmsp3γ), a polymorphic member in the msp3 multi-gene family.

Kuamsab N, Putaporntip C, Pattanawong U, Jongwutiwes S Sci Rep. 2020; 10(1):10977.

PMID: 32620822 PMC: 7335089. DOI: 10.1038/s41598-020-67222-z.

Genetic polymorphism of the N-terminal region in circumsporozoite surface protein of Plasmodium falciparum field isolates from Sudan.

Mohamed N, Ali Albsheer M, AbdElbagi H, Siddig E, Mohamed M, Ahmed A Malar J. 2019; 18(1):333.

PMID: 31570093 PMC: 6771110. DOI: 10.1186/s12936-019-2970-0.

Genetic polymorphism and natural selection of circumsporozoite surface protein in Plasmodium falciparum field isolates from Myanmar.

Le H, Kang J, Moe M, Jun H, Thai T, Lee J Malar J. 2018; 17(1):361.

PMID: 30314440 PMC: 6186114. DOI: 10.1186/s12936-018-2513-0.

References

Hughes A, Yeager M . Natural selection at major histocompatibility complex loci of vertebrates. Annu Rev Genet. 1999; 32:415-35. DOI: 10.1146/annurev.genet.32.1.415. View

Takahata N, Nei M . Allelic genealogy under overdominant and frequency-dependent selection and polymorphism of major histocompatibility complex loci. Genetics. 1990; 124(4):967-78. PMC: 1203987. DOI: 10.1093/genetics/124.4.967. View

Yang Z, Nielsen R . Estimating synonymous and nonsynonymous substitution rates under realistic evolutionary models. Mol Biol Evol. 2000; 17(1):32-43. DOI: 10.1093/oxfordjournals.molbev.a026236. View

Hughes M, Hughes A . Natural selection on Plasmodium surface proteins. Mol Biochem Parasitol. 1995; 71(1):99-113. DOI: 10.1016/0166-6851(95)00037-2. View

Hughes A . Circumsporozoite protein genes of malaria parasites (Plasmodium spp.): evidence for positive selection on immunogenic regions. Genetics. 1991; 127(2):345-53. PMC: 1204362. DOI: 10.1093/genetics/127.2.345. View

Escalante A, Cornejo O, Rojas A, Udhayakumar V, Lal A . Assessing the effect of natural selection in malaria parasites. Trends Parasitol. 2004; 20(8):388-95. DOI: 10.1016/j.pt.2004.06.002. View

Nei M, Gojobori T . Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol. 1986; 3(5):418-26. DOI: 10.1093/oxfordjournals.molbev.a040410. View

Sharma S, Pathak S . Malaria vaccine: a current perspective. J Vector Borne Dis. 2008; 45(1):1-20. View

Ballou W, Rothbard J, Wirtz R, Gordon D, Williams J, Gore R . Immunogenicity of synthetic peptides from circumsporozoite protein of Plasmodium falciparum. Science. 1985; 228(4702):996-9. DOI: 10.1126/science.2988126. View

10.

Saitou N, Nei M . The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987; 4(4):406-25. DOI: 10.1093/oxfordjournals.molbev.a040454. View

11.

Li W . Unbiased estimation of the rates of synonymous and nonsynonymous substitution. J Mol Evol. 1993; 36(1):96-9. DOI: 10.1007/BF02407308. View

12.

Jongwutiwes S, Tanabe K, Hughes M, Kanbara H, Hughes A . Allelic variation in the circumsporozoite protein of Plasmodium falciparum from Thai field isolates. Am J Trop Med Hyg. 1994; 51(5):659-68. DOI: 10.4269/ajtmh.1994.51.659. View

13.

Putaporntip C, Jongwutiwes S, Hughes A . Differential selective pressures on the merozoite surface protein 2 locus of Plasmodium falciparum in a low endemic area. Gene. 2008; 427(1-2):51-7. PMC: 3427789. DOI: 10.1016/j.gene.2008.09.009. View

14.

Good M, Pombo D, Quakyi I, Riley E, Houghten R, Menon A . Human T-cell recognition of the circumsporozoite protein of Plasmodium falciparum: immunodominant T-cell domains map to the polymorphic regions of the molecule. Proc Natl Acad Sci U S A. 1988; 85(4):1199-203. PMC: 279734. DOI: 10.1073/pnas.85.4.1199. View

15.

Hughes A . Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol Biol Evol. 1992; 9(3):381-93. DOI: 10.1093/oxfordjournals.molbev.a040730. View

16.

Arnot D . Malaria and the major histocompatibility complex. Parasitol Today. 1989; 5(5):138-42. DOI: 10.1016/0169-4758(89)90077-x. View

17.

Martin D, Williamson C, Posada D . RDP2: recombination detection and analysis from sequence alignments. Bioinformatics. 2004; 21(2):260-2. DOI: 10.1093/bioinformatics/bth490. View

18.

Rich S, Ayala F . Population structure and recent evolution of Plasmodium falciparum. Proc Natl Acad Sci U S A. 2000; 97(13):6994-7001. PMC: 34375. DOI: 10.1073/pnas.97.13.6994. View

19.

Tamura K, Dudley J, Nei M, Kumar S . MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol. 2007; 24(8):1596-9. DOI: 10.1093/molbev/msm092. View

20.

NUSSENZWEIG V, Nussenzweig R . Rationale for the development of an engineered sporozoite malaria vaccine. Adv Immunol. 1989; 45:283-334. DOI: 10.1016/s0065-2776(08)60695-1. View