Hostname: page-component-78c5997874-t5tsf Total loading time: 0 Render date: 2024-11-10T07:38:41.421Z Has data issue: false hasContentIssue false
  • English
  • Français

High polymorphism in Plasmodium vivax merozoite surface protein-5 (MSP5)

Published online by Cambridge University Press:  18 October 2006

A. GOMEZ ,
C. F. SUAREZ ,
P. MARTINEZ ,
C. SARAVIA  and
M. A. PATARROYO
A. GOMEZ
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia Universidad Nacional de Colombia, Carrera 30, Calle 45, Bogota, Colombia
C. F. SUAREZ
Affiliation:
Biomathematics Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia
P. MARTINEZ
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia
C. SARAVIA
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia
M. A. PATARROYO
Affiliation:
Molecular Biology Department, Fundacion Instituto de Inmunologia de Colombia, Carrera 50#26-00, Bogota, Colombia Universidad Nacional de Colombia, Carrera 30, Calle 45, Bogota, Colombia
Get access Rights & Permissions [Opens in a new window]

Abstract

A key issue relating to developing multi-component anti-malarial vaccines, lies in studying Plasmodium vivax surface proteins' genetic variation. The present work was aimed at amplifying, cloning and sequencing the gene encoding P. vivax merozoite surface protein 5 (PvMSP5) in samples obtained from infected patients from Colombian areas having varying malaria transmission rates.Nucleotide sequence data reported in this paper are available in the GenBank, EMBL and DDBJ databases under Accessions numbers DQ341586 to DQ341601. Our results have revealed that PvMSP5 is one of the P. vivax surface proteins having greater polymorphism, this being restricted to specific protein regions. The intron and exon II (which includes the GPI anchor and EGF-like domain) were both highly conserved when compared to exon I; exon I displayed the greatest variation and most of the recombination events occurred within it. No geographical grouping was observed. The Nei-Gojobori test revealed significant positive selection in the samples analysed here, whereas Tajima and Fu and Li tests presented a neutral selection pattern. The results reflected a localized variation pattern, recombination between PvMSP5 alleles and also functional and immune pressures, where stronger selective forces might be acting on exon I than on exon II, suggesting that the latter could be an important region to be included in an anti-malarial vaccine.

Keywords

antigenic diversitymerozoite surface protein 5 (MSP5)Plasmodium vivaxpolymorphismselection
Type
Research Article
Information
Parasitology , Volume 133 , Issue 6 , December 2006 , pp. 661 - 672
Copyright
2006 Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aguileta, G., Bielawski, J. P. and Yang, Z. ( 2004). Gene conversion and functional divergence in the beta-globin gene family. Journal of Molecular Evolution 59, 177–189.CrossRefGoogle Scholar
Applied-Biosystems ( 1993). Sequence Navigator v1.0.1. Foster City CA ( USA).
Babiker, H. A., Lines, J., Hill, W. G. and Walliker, D. ( 1997). Population structure of Plasmodium falciparum in villages with different malaria endemicity in east Africa. American Journal of Tropical Medicine and Hygiene 56, 141–147.CrossRefGoogle Scholar
Barnwell, J. W., Nichols, M. E. and 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
Benet, A., Tavul, L., Reeder, J. C. and Cortes, A. ( 2004). Diversity of Plasmodium falciparum vaccine candidate merozoite surface protein 4 (MSP4) in a natural population. Molecular and Biochemical Parasitology 134, 275–280.CrossRefGoogle Scholar
Black, C. G., Barnwell, J. W., Huber, C. S., Galinski, M. R. and Coppel, R. L. ( 2002). The Plasmodium vivax homologues of merozoite surface proteins 4 and 5 from Plasmodium falciparum are expressed at different locations in the merozoite. Molecular and Biochemical Parasitology 120, 215–224.CrossRefGoogle Scholar
Carvalho, L. J., Daniel-Ribeiro, C. T. and Goto, H. ( 2002). Malaria vaccine: candidate antigens, mechanisms, constraints and prospects. Scandinavian Journal of Immunology 56, 327–343.CrossRefGoogle Scholar
Conway, D. J., Roper, C., Oduola, A. M., Arnot, D. E., Kremsner, P. G., Grobusch, M. P., Curtis, C. F. and Greenwood, B. M. ( 1999). High recombination rate in natural populations of Plasmodium falciparum. Proceedings of the National Academy of Sciences, USA 96, 4506–4511.CrossRefGoogle Scholar
Cui, L., Escalante, A. A., Imwong, M. and Snounou, G. ( 2003 a). The genetic diversity of Plasmodium vivax populations. Trends in Parasitology 19, 220–226.Google Scholar
Cui, L., Mascorro, C. N., Fan, Q., Rzomp, K. A., Khuntirat, B., Zhou, G., Chen, H., Yan, G. and Sattabongkot, J. ( 2003 b). Genetic diversity and multiple infections of Plasmodium vivax malaria in Western Thailand. American Journal of Tropical Medicine and Hygiene 68, 613–619.Google Scholar
Dayhoff, M. O. ( 1978). Protein segment dictionary 78. In Atlas of Protein Sequence and Structure, Vol. 5 pp. VII 470. National Biomedical Research Foundation, Silver Spring, Md, USA.
Egan, A. F., Burghaus, P., Druilhe, P., Holder, A. A. and Riley, E. M. ( 1999). Human antibodies to the 19 kDa C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 inhibit parasite growth in vitro. Parasite Immunology 21, 133–139.CrossRefGoogle Scholar
Escalante, A. A., Lal, A. A. and Ayala, F. J. ( 1998). Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum. Genetics 149, 189–202.Google Scholar
Felger, I., Tavul, L., Kabintik, S., Marshall, V., Genton, B., Alpers, M. and Beck, H. P. ( 1994). Plasmodium falciparum: extensive polymorphism in merozoite surface antigen 2 alleles in an area with endemic malaria in Papua New Guinea. Experimental Parasitology 79, 106–116.CrossRefGoogle Scholar
Figtree, M., Pasay, C. J., Slade, R., Cheng, Q., Cloonan, N., Walker, J. and Saul, A. ( 2000). Plasmodium vivax synonymous substitution frequencies, evolution and population structure deduced from diversity in AMA1 and MSP1 genes. Molecular and Biochemical Parasitology 108, 53–56.CrossRefGoogle Scholar
Fitch, D. H., Mainone, C., Goodman, M. and Slightom, J. L. ( 1990). Molecular history of gene conversions in the primate fetal gamma-globin genes. Nucleotide sequences from the common gibbon, Hylobates lar. Journal of Biological Chemistry 265, 781–793.Google Scholar
Fitch, W. ( 1971). Toward defining the course of evolution: minimum change for a specified tree topology. Systematic Zoology 20, 406–416.Google Scholar
Fu, Y. X. and Li, W. H. ( 1993). Statistical tests of neutrality of mutations. Genetics 133, 693–709.Google Scholar
Gaur, D., Mayer, D. C. and Miller, L. H. ( 2004). Parasite ligand-host receptor interactions during invasion of erythrocytes by Plasmodium merozoites. International Journal for Parasitology 34, 1413–1429.CrossRefGoogle Scholar
Good, M. F. ( 2001). Towards a blood-stage vaccine for malaria: are we following all the leads? Nature Reviews, Immunology 1, 117–125.Google Scholar
Guttman, D. S. and Dykhuizen, D. E. ( 1994). Clonal divergence in Escherichia coli as a result of recombination, not mutation. Science 266, 1380–1383.CrossRefGoogle Scholar
Hillis, D. ( 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. and 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
Hughes, A. L. and Verra, F. ( 2001). Very large long-term effective population size in the virulent human malaria parasite Plasmodium falciparum. Proceedings of the Royal Society, Biological Sciences 268, 1855–1860.CrossRefGoogle Scholar
Hughes, M. K. and Hughes, A. L. ( 1995). Natural selection on Plasmodium surface proteins. Molecular and Biochemical Parasitology 71, 99–113.CrossRefGoogle Scholar
INS ( 2003). Datos de Vigilancia Epidemiológica: boletines de Enfermedades transmitidas por vectores. Instituto Nacional de Salud Colombia.
Jongwutiwes, S., Putaporntip, C., Friedman, R. and Hughes, A. L. ( 2002). The extent of nucleotide polymorphism is highly variable across a 3-kb region on Plasmodium falciparum chromosome 2. Molecular Biology and Evolution 9, 1585–1590.CrossRefGoogle Scholar
Kedzierski, L., Black, C. G. and Coppel, R. L. ( 2000). Immunization with recombinant Plasmodium yoelii merozoite surface protein 4/5 protects mice against lethal challenge. Infection and Immunity 68, 6034–6037.CrossRefGoogle Scholar
Kedzierski, L., Black, C. G., Goschnick, M. W., Stowers, A. W. and Coppel, R. L. ( 2002). Immunization with a combination of merozoite surface proteins 4/5 and 1 enhances protection against lethal challenge with Plasmodium yoelii. Infection and Immunity 70, 6606–6613.CrossRefGoogle Scholar
Kemp, D. J., Coppel, R. L. and Anders, R. F. ( 1987). Repetitive proteins and genes of malaria. Annual Review of Microbiology 41, 181–208.CrossRefGoogle Scholar
Kumar, S., Tamura, K., Jakobsen, I. B. and Nei, M. ( 2001). MEGA2: molecular evolutionary genetics analysis software. Bioinformatics 17, 1244–1245.CrossRefGoogle Scholar
Marshall, V. M., Silva, A., Foley, M., Cranmer, S., Wang, L., Mccoll, D. J., Kemp, D. J. and Coppel, R. L. ( 1997). A second merozoite surface protein (MSP-4) of Plasmodium falciparum that contains an epidermal growth factor-like domain. Infection and Immunity 65, 4460–4467.Google Scholar
Marshall, V. M., Tieqiao, W. and Coppel, R. L. ( 1998). Close linkage of three merozoite surface protein genes on chromosome 2 of Plasmodium falciparum. Molecular and Biochemical Parasitology 94, 13–25.CrossRefGoogle Scholar
Martinez, P., Suarez, C. F., Cardenas, P. P. and Patarroyo, M. A. ( 2004). Plasmodium vivax Duffy binding protein: a modular evolutionary proposal. Parasitology 128, 353–366.CrossRefGoogle Scholar
Martinez, P., Suarez, C. F., Gomez, A., Cardenas, P. P., Guerrero, J. E. and Patarroyo, M. A. ( 2005). High level of conservation in Plasmodium vivax merozoite surface protein 4 (PvMSP4). Infection, Genetics and Evolution 5, 354–361.CrossRefGoogle Scholar
Mascorro, C. N., Zhao, K., Khuntirat, B., Sattabongkot, J., Yan, G., Escalante, A. A. and Cui, L. ( 2005). Molecular evolution and intragenic recombination of the merozoite surface protein MSP-3alpha from the malaria parasite Plasmodium vivax in Thailand. Parasitology 131, 25–35.CrossRefGoogle Scholar
McVean, G., Awadalla, P. and Fearnhead, P. ( 2002). A coalescent-based method for detecting and estimating recombination from gene sequences. Genetics 160, 1231–1241.Google Scholar
Milne, I., Wright, F., Rowe, G., Marshall, D. F., Husmeier, D. and McGuire, G. ( 2004). TOPALi: software for automatic identification of recombinant sequences within DNA multiple alignments. Bioinformatics 20, 1806–1807.CrossRefGoogle Scholar
Miller, L. H., Mason, S. J., Clyde, D. F. and 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. and 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., Hb, N. and Deerfield, D. ( 1997). GeneDoc: analysis and visualization of genetic variation. EMBNEW.NEWS 4, 14.
Nielsen, R. ( 2005). Molecular signatures of natural selection. Annual Review of Genetics 39, 197–218.CrossRefGoogle Scholar
O'Donnell, R. A., De Koning-Ward, T. F., Burt, R. A., Bockarie, M., Reeder, J. C., Cowman, A. F. and Crabb, B. S. ( 2001). Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. Journal of Experimental Medicine 193, 1403–1412.CrossRefGoogle Scholar
Polson, H. E., Conway, D. J., Fandeur, T., Mercereau-Puijalon, O. and Longacre, S. ( 2005). Gene polymorphism of Plasmodium falciparum merozoite surface proteins 4 and 5. Molecular and Biochemical Parasitology 142, 110–115.CrossRefGoogle Scholar
Polley, S., MacRobert, L. and Sutherland, C. ( 2004). Vaccination for vivax malaria: targeting the invaders. Trends in Parasitology 20, 99–102.CrossRefGoogle Scholar
Putaporntip, C., Jongwutiwes, S., Sakihama, N., Ferreira, M. U., Kho, W. G., Kaneko, A., Kanbara, H., Hattori, T. and 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. and Tanabe, K. ( 2001). Diversity in the thrombospondin-related adhesive protein gene (TRAP) of Plasmodium vivax. Gene 268, 97–104.Google Scholar
Rainczuk, A., Scorza, T., Spithill, T. W. and Smooker, P. M. ( 2004). A bicistronic DNA vaccine containing apical membrane antigen 1 and merozoite surface protein 4/5 can prime humoral and cellular immune responses and partially protect mice against virulent Plasmodium chabaudi adami DS malaria. Infection and Immunity 72, 5565–5573.CrossRefGoogle Scholar
Rayner, J. C., Corredor, V., Feldman, D., Ingravallo, P., Iderabdullah, F., Galinski, M. R. and 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. and 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., Sanchez-Delbarrio, J. C., Messeguer, X. and Rozas, R. ( 2003). DnaSP, DNA polymorphism analyses by the coalescent and other methods. Bioinformatics 19, 2496–2497.CrossRefGoogle Scholar
Rzhetsky, A. and Nei, M. ( 1993). Theoretical foundation of the minimum-evolution method of phylogenetic inference. Molecular Biology and Evolution 10, 1073–1095.Google Scholar
Sim, B. K. ( 1995). EBA-175: an erythrocyte-binding ligand of Plasmodium falciparum. Parasitology Today 11, 213–217.CrossRefGoogle Scholar
Singh, S. K., Hora, R., Belrhali, H., Chitnis, C. E. and Sharma, A. ( 2006). Structural basis for Duffy recognition by the malaria parasite Duffy-binding-like domain. Nature, London 439, 741–744.CrossRefGoogle Scholar
Sitnikova, T. ( 1996). Bootstrap method of interior-branch test for phylogenetic trees. Mol Biol Evol 13, 605–611.CrossRefGoogle Scholar
Snewin, V. A., Herrera, M., Sanchez, G., Scherf, A., Langsley, G. and Herrera, S. ( 1991). Polymorphism of the alleles of the merozoite surface antigens MSA1 and MSA2 in Plasmodium falciparum wild isolates from Colombia. Molecular and Biochemical Parasitology 49, 265–275.CrossRefGoogle Scholar
Snow, R. W., Guerra, C. A., Noot, A. M., Myinme, H. Y. and Hay, S. I. ( 2005). The global distribution of clinical episodes of Plasmodium falciparum malaria. Nature, London 434, 214–217.CrossRefGoogle Scholar
Stowers, A. W., Cioce, V., Shimp, R. L., Lawson, M., Hui, G., Muratova, O., Kaslow, D. C., Robinson, R., Long, C. A. and Miller, L. H. ( 2001). Efficacy of two alternate vaccines based on Plasmodium falciparum merozoite surface protein 1 in an Aotus challenge trial. Infection and Immunity 69, 1536–1546.CrossRefGoogle Scholar
Tajima, F. ( 1989). Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123, 585–595.Google Scholar
Thompson, J. D., Gibson, T. J., Plewniak, F., Jeanmougin, F. and 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
Volkman, S. K., Barry, A. E., Lyons, E. J., Nielsen, K. M., Thomas, S. M., Choi, M., Thakore, S. S., Day, K. P., Wirth, D. F. and Hartl, D. L. ( 2001). Recent origin of Plasmodium falciparum from a single progenitor. Science 293, 482–484.CrossRefGoogle Scholar
Wang, L., Black, C. G., Marshall, V. M. and Coppel, R. L. ( 1999). Structural and antigenic properties of merozoite surface protein 4 of Plasmodium falciparum. Infection and Immunity 67, 2193–2200.Google Scholar
Wang, L., Goschnick, M. W. and Coppel, R. L. ( 2004). Oral immunization with a combination of Plasmodium yoelii merozoite surface proteins 1 and 4/5 enhances protection against lethal malaria challenge. Infection and Immunity 72, 6172–6175.CrossRefGoogle Scholar
WORLD HEALTH ORGANIZATION ( 2002). Epidemiological Bulletin. World Health Organization, Geneva.
Wu, T., Black, C. G., Wang, L., Hibbs, A. R. and Coppel, R. ( 1999). Lack of sequence diversity in the gene encoding merozoite surface protein 5 of Plasmodium falciparum. Molecular and Biochemical Parasitology 103, 243–250.CrossRefGoogle Scholar