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Molecular evolution and intragenic recombination of the merozoite surface protein MSP-3α from the malaria parasite Plasmodium vivax in Thailand

Published online by Cambridge University Press:  24 March 2005

C. N. MASCORRO
Affiliation:
Department of Entomology, The Pennsylvania State University, 501 ASI Building, University Park, PA 16802, USA
K. ZHAO
Affiliation:
Department of Entomology, The Pennsylvania State University, 501 ASI Building, University Park, PA 16802, USA
B. KHUNTIRAT
Affiliation:
Department of Entomology, AFRIMS, 315/6 Rajvithi Road, Bangkok 10499, Thailand
J. SATTABONGKOT
Affiliation:
Department of Entomology, AFRIMS, 315/6 Rajvithi Road, Bangkok 10499, Thailand
G. YAN
Affiliation:
Department of Biological Sciences, State University of New York at Buffalo, NY 14260, USA
A. A. ESCALANTE
Affiliation:
School of Life Sciences, Arizona State University, Tempe AZ 85287, USA
L. CUI
Affiliation:
Department of Entomology, The Pennsylvania State University, 501 ASI Building, University Park, PA 16802, USA

Abstract

The merozoite surface antigens of malaria parasites are prime anti-morbidity/mortality vaccine candidates. However, their highly polymorphic nature requires extensive surveys of parasite populations to validate vaccine designs. Previous studies have found 3 molecular types (A, B and C) of the Plasmodium vivax merozoite surface protein 3α (PvMSP-3α) among parasite field populations. Here we analysed complete PvMSP-3α sequences from 17 clinical P. vivax isolates from Thailand and found that the nucleotide diversity was as high as that from samples widely separated by time and space. The polymorphic sites were not randomly distributed but concentrated in the N-terminal Ala-rich domain (block 2A), which is partially deleted in type B and C sequences. The size variations among type A sequences were due to small indels occurring in block 2A, whereas type B and C sequences were uniform in length with each type having a different large deletion. Analysis of synonymous and non-synonymous substitutions suggested that different selection forces were operating on different regions of the molecule. The numerous recombination sites detected within the Ala-rich domain suggested that intragenic recombination was at least partially responsible for the observed genetic diversity of the PvMSP-3α gene. Phylogenetic analysis failed to link any alleles to a specific geographical origin, even when different domains of PvMSP-3α were used for analysis. The highly polymorphic nature and lack of geographical clustering of isolates suggest that more systematic investigations of the PvMSP-3α gene are needed to explore its evolution and vaccine potential.

Type
Research Article
Copyright
© 2005 Cambridge University Press

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References

REFERENCES

ANDERSON, T. J., HAUBOLD, B., WILLIAMS, J. T., ESTRADA-FRANCO, J. G., RICHARDSON, L., MOLLINEDO, R., BOCKARIE, M., MOKILI, J., MHARAKURWA, S., FRENCH, N., WHITWORTH, J., VELEZ, I. D., BROCKMAN, A. H., NOSTEN, F., FERREIRA, M. U. & DAY, K. P. ( 2000). Microsatellite markers reveal a spectrum of population structures in the malaria parasite Plasmodium falciparum. Molecular Biology and Evolution 17, 14671482.CrossRefGoogle Scholar
BERZINS, K. ( 2002). Merozoite antigens involved in invasion. In Malaria Immunology (ed. Perlmann, P. & Troye-Blomberg, M.), pp. 125143. Karger, Basel, Switzerland.CrossRef
BRUCE, M. C., GALINSKI, M. R., BARNWELL, J. W., DONNELLY, C. A., WALMSLEY, M., ALPERS, M. P., WALLIKER, D. & DAY, K. P. ( 2000). Genetic diversity and dynamics of Plasmodium falciparum and P. vivax populations in multiply infected children with asymptomatic malaria infections in Papua New Guinea. Parasitology 121, 257272.Google Scholar
BRUCE, M. C., GALINSKI, M. R., BARNWELL, J. W., SNOUNOU, G. & DAY, K. ( 1999). Polymorphism at the merozoite surface protein-3α locus of Plasmodium vivax: global diversity. American Journal of Tropical Medicine and Hygiene 61, 518525.CrossRefGoogle Scholar
COLE-TOBIAN, J. & KING, C. L. ( 2003). Diversity and natural selection in Plasmodium vivax Duffy binding protein gene. Molecular and Biochemical Parasitology 127, 121132.CrossRefGoogle Scholar
CONWAY, D. J., CAVANAGH, D. R., TANABE, K., ROPER, C., MIKES, Z. S., SAKIHAMA, N., BOJANG, K. A., ODUOLA, A. M., KREMSNER, P. G., ARNOT, D. E., GREENWOOD, B. M. & MCBRIDE, J. S. ( 2000). A principal target of human immunity to malaria identified by molecular population genetic and immunological analyses. Nature Medicine 6, 689692.CrossRefGoogle Scholar
CUI, L., MASCORRO, C. N., RZOMP, K. A., FAN, Q., KHUNTIRAT, B., ZHOU, G., CHEN, H., YAN, G. & SATTABONGKOT, J. ( 2003 a). Genetic diversity and multiple infections of Plasmodium vivax malaria in western Thailand. American Journal of Tropical Medicine and Hygiene 68, 613619.Google Scholar
CUI, L., ESCALANTE, A. A., IMWONG, M. & SNOUNOU, G. ( 2003 b). The genetic diversity of Plasmodium vivax populations. Trends in Parasitology 19, 220226.Google Scholar
ESCALANTE, A. A., LAL, A. A. & AYALA, F. J. ( 1998). Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics 149, 189202.Google Scholar
ESCALANTE, A. A., CORNEJO, O. E., ROJAS, A., UDHAYAKUMAR, V. & LAL, A. A. ( 2004). Assessing the effect of natural selection in malaria parasites. Trends in Parasitology 20, 388395.CrossRefGoogle Scholar
FELGER, I., MARSHAL, V. M., REEDER, J. C., HUNT, J. A., MGONE, C. S. & BECK, H. P. ( 1997). Sequence diversity and molecular evolution of the merozoite surface antigen 2 of Plasmodium falciparum. Journal of Molecular Evolution 45, 154160.CrossRefGoogle Scholar
FERREIRA, M. U., RIBEIRO, W. L., TONON, A. P., KAWAMOTO, F. & RICH, S. ( 2003). Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum. Gene 304, 6574.CrossRefGoogle Scholar
FIGTREE, M., PASAY, C. J., SLADE, R., CHENG, Q., CLOONAN, N., WALKER, J. & SAUL, A. ( 2000). Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA 1 and MSP 1 genes. Molecular and Biochemical Parasitology 108, 5366.CrossRefGoogle Scholar
FU, Y. X. & LI, W. H. ( 1993). Statistical tests of neutrality of mutations. Genetics 133, 693709.Google Scholar
GALINSKI, M. R., CORREDOR-MEDINA, C., POVOA, M., CROSBY, J., INGRAVALLO, P. & BARNWELL, J. W. ( 1999). Plasmodium vivax merozoite surface protein-3 contains coiled-coil motifs in an alanine-rich central domain. Molecular and Biochemical Parasitology 101, 131147.CrossRefGoogle Scholar
GALINSKI, M. R., INGRAVALLO, P., CORREDOR-MEDINA, C., AL-KHEDERY, B., POVOA, M. & BARNWELL, J. W. ( 2001). Plasmodium vivax merozoite surface proteins-3β and -3γ share structural similarities with P. vivax merozoite surface protein-3α and define a new gene family. Molecular and Biochemical Parasitology 115, 4153.Google Scholar
HISAEDA, H., SAUL, A., REECE, J. J., KENNEDY, M. C., LONG, C. A., MILLER, L. H. & STOWERS, A. W. ( 2002). Merozoite surface protein 3 and protection against malaria in Aotus nancymai monkeys. Journal of Infectious Diseases 185, 657664.CrossRefGoogle Scholar
HUBER, W., FELGER, I., MATILE, H., LIPPS, H. J., STEIGER, S. & BECK, H.-P. ( 1997). Limited sequence polymorphism in the Plasmodium falciparum merozoite surface protein 3. Molecular and Biochemical Parasitology 87, 231234.CrossRefGoogle Scholar
KUMAR, S., TAMURA, K., JAKOBSEN, I. B. & NEI, M. ( 2001). MEGA2: Molecular Evolutionary Genetics Analysis software. Bioinformatics 17, 12441245.CrossRefGoogle Scholar
MENDIS, K. N., SINA, B. J., MARCHESINI, P. & CARTER, R. ( 2001). The neglected burden of Plasmodium vivax malaria. American Journal of Tropical Medicine and Hygiene 64, 97106.CrossRefGoogle Scholar
MCCOLL, D. J. & ANDERS, R. F. ( 1997). Conservation of structural motifs and antigenic diversity in the Plasmodium falciparum merozoite surface protein-3 (MSP-3). Molecular and Biochemical Parasitology 90, 2131.CrossRefGoogle Scholar
MCCOLL, D. J., SILVA, A., FOLEY, M., KUN, J. F. J., FAVALORO, J. M., THOMPSON, J. K., MARSHALL, V. M., COPPEL, R. L., KEMP, D. J. & ANDERS, R. F. ( 1994). Molecular variation in a novel polymorphic antigen associated with Plasmodium falciparum merozoites. Molecular and Biochemical Parasitology 68, 5367.CrossRefGoogle Scholar
MUELLER, I., KAIOK, J., REEDER, J. C. & CORTES, A. ( 2002). The population structure of Plasmodium falciparum and Plasmodium vivax during an epidemic of malaria in the eastern highlands of Papua New Guinea. American Journal of Tropical Medicine and Hygiene 67, 459464.CrossRefGoogle Scholar
OEUVRAY, C., BOUHARON-TAYOUN, H., GRAS-MASSE, H., BOTTIUS, E., KAIDOH, T., AIKAWA, M., FILGUEIRA, M. C., TARTAR, A. & DRUILHE, P. ( 1994). Merozoite surface protein-3: a malaria protein inducing antibodies that promote Plasmodium falciparum killing by cooperation with blood monocytes. Blood 84, 15941602.Google Scholar
OKENU, D. M. N., THOMAS, A. W. & CONWAY, D. J. ( 2000). Allelic lineages of the merozoite surface protein 3 gene in Plasmodium reichenowi and Plasmodium falciparum. Molecular and Biochemical Parasitology 109, 185188.CrossRefGoogle Scholar
PUTAPORNTIP, C., JONGWUTIWES, S., SAKIHAMA, N., FERREIRA, M. U., KHO, W. G., KANEKO, A., KANBARA, H., HATTORI, T. & TANABE, K. ( 2002). Mosaic organization and heterogeneity in frequency of allelic recombination of the Plasmodium vivax merozoite surface protein-1 locus. Proceedings of the National Academy of Sciences, USA 99, 1634816353.CrossRefGoogle Scholar
PUTAPORNTIP, C., JONGWUTIWES, S., TIA, T., FERREIRA, M. U., KANBARA, H. & TANABE, K. ( 2001). Diversity in the thrombospondin-related adhesive protein gene (TRAP) of Plasmodium vivax. Gene 268, 97104.Google Scholar
RAYNER, J. C., CORREDOR, V., FELDMAN, D., INGRAVALLO, P., IDERABDULLAH, F., GALINSKI, M. R. & BARNWELL, J. W. ( 2002). Extensive polymorphism in the Plasmodium vivax merozoite surface coat protein MSP-3α is limited to specific domains. Parasitology 125, 393405.CrossRefGoogle Scholar
RAYNER, J. C., HUBER, C. S., FELDMAN, D., INGRAVALLO, P., GALINSKI, M. R. & BARNWELL, J. W. ( 2004). Plasmodium vivax merozoite surface protein PvMSP-3b is radically polymorphic through mutation and large insertions and deletions. Infection, Genetics and Evolution 4, 309319.CrossRefGoogle Scholar
RICHIE, T. L. & SAUL, A. ( 2002). Progress and challenges for malaria vaccines. Nature, London 415, 694701.CrossRefGoogle Scholar
ROZAS, J., SANCHEZ-DELBARRIO, J. C., MESSEGUER, X. & ROZAS, R. ( 2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 24962497.CrossRefGoogle Scholar
SAITOU, N. & NEI, M. ( 1987). The neighbor-joining method: a new method for reconstructing phylogenetic tree. Molecular Biology and Evolution 4, 406425.Google Scholar
SAKIHAMA, N., KANEKO, A., HATTORI, T. & TANABE, K. ( 2001). Limited recombination events in merozoite surface protein-1 alleles of Plasmodium falciparum on islands. Gene 279, 4148.CrossRefGoogle Scholar
SATTABONGKOT, J., TSUBOI, T., ZOLLNER, G. E., SIRICHAISINTHOP, J. & CUI, L. ( 2004). Plasmodium vivax transmission: chances for control? Trends in Parasitology 20, 192198.Google Scholar
TAJIMA, F. ( 1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585595.Google Scholar
TAKALA, S., BRANCH, O., ESCALANTE, A. A., KARIUKI, S., WOOTTON, J. & LAL, A. A. ( 2002). Evidence for intragenic recombination in Plasmodium falciparum: identification of a novel allele family in block 2 of merozoite surface protein-1: Asembo Bay Area Cohort Project XIV. Molecular and Biochemical Parasitology 125, 163171.CrossRefGoogle Scholar
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. ( 1997). The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 48764882.CrossRefGoogle Scholar
XAINLI, J., ADAMS, J. H. & KING, C. L. ( 2000). The erythrocytic binding motif of Plasmodium vivax Duffy binding protein is highly polymorphic and functionally conserved in isolates from Papua New Guinea. Molecular and Biochemical Parasitology 111, 253260.CrossRefGoogle Scholar
ZHOU, G., SIRICHAISINTHOP, J., SATTABONGKOT, J., JONES, J., BJØRNSTAD, O. N., YAN, G. & CUI, L. ( 2005). Spatio-temporal distribution of falciparum and vivax malaria in Thailand. American Journal of Tropical Medicine and Hygiene (in the Press)Google Scholar