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Plasmodium vivax Duffy binding protein: a modular evolutionary proposal

Published online by Cambridge University Press:  16 April 2004

P. MARTINEZ ,
C. F. SUAREZ ,
P. P. CARDENAS  and
M. A. PATARROYO
P. MARTINEZ
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia Faculty of Science, Chemistry Department, Universidad Nacional de Colombia, Carrera 30, Calle 45, Bogota, Colombia
C. F. SUAREZ
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia
P. P. CARDENAS
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia Faculty of Science, Chemistry Department, Universidad Nacional de Colombia, Carrera 30, Calle 45, Bogota, Colombia
M. A. PATARROYO
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia Faculty of Science, Chemistry Department, Universidad Nacional de Colombia, Carrera 30, Calle 45, Bogota, Colombia
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Abstract

The population of malaria-causing parasites is characterized by great genetic diversity. Knowledge of the polymorphism generation mechanism is a central issue for developing effective vaccines against malaria and understanding the parasite population structure. Plasmodium vivax genetic diversity has been explained in terms of two major factors: natural selection and intragenic recombination. A modular organization was found within P. vivax Duffy binding protein in the present work. Four Colombian isolates have identical sequences to Salvador-1 strain amongst dpb regions III–VI analysed, suggesting a high identity between Central and South American isolates. Geographically clustered sectors, corresponding to cysteine-rich regions (II and VI), show a high sequence diversity that could reflect a possible immune response evasion mechanism; both positive and negative selection were detected in these regions. In contrast, other dbp gene regions display a non-geographical clustering pattern, lower sequence diversity and predominant negative selective pressure. Recombination was homogeneously detected all along the molecule. These findings suggest that diversification vs. homogenizing forces, drive dbp gene evolution and determine its mosaic region organization.

Keywords

Plasmodium vivaxgenetic diversityDuffy binding proteingeographical variationcysteine-rich motifsColombian isolates
Type
Research Article
Information
Parasitology , Volume 128 , Issue 4 , April 2004 , pp. 353 - 366
Copyright
© 2004 Cambridge University Press

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References

REFERENCES

ADAMS, J. H., BLAIR, P. L., KANEKO, O. & PETERSON, D. S. (2001). An expanding ebl family of Plasmodium falciparum. Trends in Parasitology 17, 297–299.CrossRefGoogle Scholar
ADAMS, J. H., SIM, B. K., DOLAN, S. A., FANG, X., KASLOW, D. C. & MILLER, L. H. (1992). A family of erythrocyte binding proteins of malaria parasites. Proceedings of the National Academy of Sciences, USA 89, 7085–7089.CrossRefGoogle Scholar
AMPUDIA, E., PATARROYO, M. A., PATARROYO, M. E. & MURILLO, L. A. (1996). Genetic polymorphism of the Duffy receptor binding domain of Plasmodium vivax in Colombian wild isolates. Molecular and Biochemical Parasitology 78, 269–272.CrossRefGoogle Scholar
BARNWELL, J. W. & GALINSKI, M. R. (1995). Plasmodium vivax: a glimpse into the unique and shared biology of the merozoite. Annals of Tropical Medicine and Parasitology 89, 113–120.CrossRefGoogle Scholar
BARNWELL, J. W., NICHOLS, M. E. & RUBINSTEIN, P. (1989). In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. Journal of Experimental Medicine 169, 1795–1802.CrossRefGoogle Scholar
CHITNIS, C. E. (2001). Molecular insights into receptors used by malaria parasites for erythrocyte invasion. Current Opinion in Hematology 8, 85–91.CrossRefGoogle Scholar
CHITNIS, C. E. & MILLER, L. H. (1994). Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. Journal of Experimental Medicine 180, 497–506.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, 121–132.CrossRefGoogle Scholar
COLE-TOBIAN, J. L., CORTES, A., BAISOR, M., KASTENS, W., XAINLI, J., BOCKARIE, M., ADAMS, J. H. & KING, C. L. (2002). Age-acquired immunity to a Plasmodium vivax invasion ligand, the duffy binding protein. Journal of Infectious Diseases 186, 531–539.CrossRefGoogle Scholar
COLLINS, D. W. & JUKES, T. H. (1994). Rates of transition and transversion in coding sequences since the human-rodent divergence. Genomics 20, 386–396.CrossRefGoogle Scholar
CUI, L., ESCALANTE, A. A., IMWONG, M. & SNOUNOU, G. (2003). The genetic diversity of Plasmodium vivax populations. Trends in Parasitology 19, 220–226.CrossRefGoogle Scholar
DAYHOFF, M. O., SCHWARTZ, R. M. & ORCUTT, B. C. (1978). A model of evolutionary change in proteins. In Atlas of Protein Sequence and Structure ( ed. Dayhoff, M. O.). National Biomedical Research Foundation. 5 (Suppl. 3e), 345–352.
ESCALANTE, A. A., GREBERT, H. M., ISEA, R., GOLDMAN, I. F., BASCO, L., MAGRIS, M., BISWAS, S., KARIUKI, S. & LAL, A. A. (2002). A study of genetic diversity in the gene encoding the circumsporozoite protein (CSP) of Plasmodium falciparum from different transmission areas-XVI. Asembo Bay Cohort Project. Molecular and Biochemical Parasitology 125, 83–90.CrossRefGoogle Scholar
ESCALANTE, A. A., LAL, A. A. & AYALA, F. J. (1998). Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics 149, 189–202.Google Scholar
FANG, X. D., KASLOW, D. C., ADAMS, J. H. & MILLER, L. H. (1991). Cloning of the Plasmodium vivax Duffy receptor. Molecular and Biochemical Parasitology 44, 125–132.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, 53–66.CrossRefGoogle Scholar
FITCH, W. (1971). Toward defining the course of evolution: minimum change for a specified tree topology. Systematic Zoology 20, 406–416.Google Scholar
FRASER, T., MICHON, P., BARNWELL, J. W., NOE, A. R., AL-YAMAN, F., KASLOW, D. C. & ADAMS, J. H. (1997). Expression and serologic activity of a soluble recombinant Plasmodium vivax Duffy binding protein. Infection and Immunity 65, 2772–2777.Google Scholar
FU, Y. X. & LI, W. H. (1993). Statistical tests of neutrality of mutations. Genetics 133, 693–709.Google Scholar
HILLIS, D. M. (1993). An empirical test of bootstrapping as a method for assessing confidence in phylogenetic analysis. Systematic Biology 42, 182–192.CrossRefGoogle Scholar
HUDSON, R. R. & KAPLAN, N. L. (1985). Statistical properties of the number of recombination events in the history of a sample of DNA sequences. Genetics 111, 147–164.Google Scholar
KHO, W. G., CHUNG, J. Y., SIM, E. J., KIM, D. W. & CHUNG, W. C. (2001). Analysis of polymorphic regions of Plasmodium vivax Duffy binding protein of Korean isolates. The Korean Journal of Parasitology 39, 143–150.CrossRefGoogle Scholar
KIM, T., KIM, Y. J., SONG, K. J., SONG, J. W., CHA, S. H., KIM, Y. K., SHIN, Y. K., SUH, I. B. & LIM, C. S. (2002). The molecular characteristics of circumsporozoite protein gene subtypes from Plasmodium vivax isolates in Republic of Korea. Parasitology Research 88, 1051–1054.CrossRefGoogle Scholar
KUMAR, S., TAMURA, K., JAKOBSEN, I. B. & NEI, M. (2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.CrossRefGoogle Scholar
KYTE, J. & DOOLITTLE, R. F. (1982). A simple method for displaying the hydropathic character of a protein. Journal of Molecular Biology 157, 105–132.CrossRefGoogle Scholar
LOMBARD, V., CAMON, E. B., PARKINSON, H. E., HINGAMP, P., STOESSER, G. & REDASCHI, N. (2002). EMBL-Align: a new public nucleotide and amino acid multiple sequence alignment database. Bioinformatics 18, 763–764.CrossRefGoogle Scholar
MANN, V. H., HUANG, T., CHENG, Q. & SAUL, A. (1994). Sequence variation in the circumsporozoite protein gene of Plasmodium vivax appears to be regionally biased. Molecular and Biochemical Parasitology 68, 45–52.CrossRefGoogle Scholar
MICHON, P., FRASER, T. & ADAMS, J. H. (2000). Naturally acquired and vaccine-elicited antibodies block erythrocyte cytoadherence of the Plasmodium vivax Duffy binding protein. Infection and Immunity 68, 3164–3171.CrossRefGoogle Scholar
MICHON, P., STEVENS, J. R., KANEKO, O. & ADAMS, J. H. (2002). Evolutionary relationships of conserved cysteine-rich motifs in adhesive molecules of malaria parasites. Molecular Biology and Evolution 19, 1128–1142.CrossRefGoogle Scholar
MILLER, L. H., MASON, S. J., CLYDE, D. F. & McGINNISS, M. H. (1976). The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. New England Journal of Medicine 295, 302–304.Google Scholar
NEI, M. & GOJOBORI, T. (1986). Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Molecular Biology and Evolution 3, 418–426.Google Scholar
NICHOLAS, K., NICHOLAS, H. B. JR. & DEERFIELD, D. W. II (1997). GeneDoc[ratio ]Analysis and Visualization of Genetic Variation. EMBNEW NEWS 4, 14.Google Scholar
OCAMPO, M., VERA, R., EDUARDO RODRIGUEZ, L., CURTIDOR, H., URQUIZA, M., SUAREZ, J., GARCIA, J., PUENTES, A., LOPEZ, R., TRUJILLO, M., TORRES, E. & ELKIN PATARROYO, M. (2002). Plasmodium vivax Duffy binding protein peptides specifically bind to reticulocytes. Peptides 23, 13–22.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, 16348–16353.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, 97–104.Google Scholar
QARI, S. H., GOLDMAN, I. F., POVOA, M. M., DI SANTI, S., ALPERS, M. P. & LAL, A. A. (1992). Polymorphism in the circumsporozoite protein of the human malaria parasite Plasmodium vivax. Molecular and Biochemical Parasitology 55, 105–113.CrossRefGoogle Scholar
RANJAN, A. & CHITNIS, C. E. (1999). Mapping regions containing binding residues within functional domains of Plasmodium vivax and Plasmodium knowlesi erythrocyte-binding proteins. Proceedings of the National Academy of Sciences, USA 96, 14067–14072.CrossRefGoogle 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-3alpha is limited to specific domains. Parasitology 125, 393–405.Google Scholar
REED, M. B., CARUANA, S. R., BATCHELOR, A. H., THOMPSON, J. K., CRABB, B. S. & COWMAN, A. F. (2000). Targeted disruption of an erythrocyte binding antigen in Plasmodium falciparum is associated with a switch toward a sialic acid-independent pathway of invasion. Proceedings of the National Academy of Sciences, USA 97, 7509–7514.CrossRefGoogle Scholar
ROZAS, J. & ROZAS, R. (1999). DnaSP version 3: an integrated program for molecular population genetics and molecular evolution analysis. Bioinformatics 15, 174–175.CrossRefGoogle Scholar
RZHETSKY, A. & NEI, M. (1993). Theoretical foundation of the minimum-evolution method of phylogenetic inference. Molecular Biology and Evolution 10, 1073–1095.Google Scholar
SINGH, S. K., SINGH, A. P., PANDEY, S., YAZDANI, S. S., CHITNIS, C. E. & SHARMA, A. (2003). Definition of structural elements in Plasmodium vivax and Plasmodium knowlesi Duffy binding domains necessary for erythrocyte invasion. The Biochemical Journal 374, 193–198.CrossRefGoogle Scholar
SUH, I. B., HOFFMAN, K. J., KIM, S. H., SONG, K. J., SONG, J. W., LEE, J. S. & LIM, C. S. (2001). The analysis of Plasmodium vivax Duffy receptor binding domain gene sequence from resurgent Korean isolates. Parasitology Research 87, 1007–1010.Google Scholar
SUZUKI, Y. & GOJOBORI, T. (1999). A method for detecting positive selection at single amino acid sites. Molecular Biology and Evolution 16, 1315–1328.CrossRefGoogle Scholar
TAJIMA, F. (1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
TAMURA, K. (1992). Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G+C-content biases. Molecular Biology and Evolution 9, 678–687.Google Scholar
THOMPSON, J. D., GIBSON, T. J., PLEWNIAK, F., JEANMOUGIN, F. & HIGGINS, D. G. (1997). The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Research 25, 4876–4882.CrossRefGoogle Scholar
TSUBOI, T., KAPPE, S. H., AL-YAMAN, F., PRICKETT, M. D., ALPERS, M. & ADAMS, J. H. (1994). Natural variation within the principal adhesion domain of the Plasmodium vivax duffy binding protein. Infection and Immunity 62, 5581–5586.Google Scholar
VERRA, F. & HUGHES, A. L. (2000). Evidence for ancient balanced polymorphism at the Apical Membrane Antigen-1 (AMA-1) locus of Plasmodium falciparum. Molecular and Biochemical Parasitology 105, 149–153.CrossRefGoogle Scholar
WERTHEIMER, S. P. & BARNWELL, J. W. (1989). Plasmodium vivax interaction with the human Duffy blood group glycoprotein: identification of a parasite receptor-like protein. Experimental Parasitology 69, 340–350.CrossRefGoogle Scholar
XAINLI, J., ADAMS, J. H. & KING, C. L. (2000). The erythrocyte 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, 253–260.CrossRefGoogle Scholar