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Positive diversifying selection on Plasmodium vivax RON2 protein

Published online by Cambridge University Press:  10 February 2012

JIANXIA TANG ,
YANG DAI ,
HONGWEI ZHANG ,
RICHARD L. CULLETON ,
YAOBO LIU ,
SONG ZHAO ,
XIAOTING WANG ,
XIAOHONG GUAN ,
OSAMU KANEKO  and
YINCHANG ZHU
JIANXIA TANG
Affiliation:
School of Basic Medical Science, Nanjing Medical University, Nanjing, Jiangsu, 210029, P. R. China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, Jiangsu Institute of Parasitic Diseases (JIPD), Meiyuan Yangxiang 117, Wuxi, Jiangsu, 214064, P. R. China
YANG DAI
Affiliation:
Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, Jiangsu Institute of Parasitic Diseases (JIPD), Meiyuan Yangxiang 117, Wuxi, Jiangsu, 214064, P. R. China
HONGWEI ZHANG
Affiliation:
Department of Sanitary Inspection, Henan Center of Disease Control and Prevention, Zhengzhou, Henan, 450003, P. R. China
RICHARD L. CULLETON
Affiliation:
Malaria Unit, Institute of Tropical Medicine (NEKKEN), Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan
YAOBO LIU
Affiliation:
Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, Jiangsu Institute of Parasitic Diseases (JIPD), Meiyuan Yangxiang 117, Wuxi, Jiangsu, 214064, P. R. China
SONG ZHAO
Affiliation:
Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, Jiangsu Institute of Parasitic Diseases (JIPD), Meiyuan Yangxiang 117, Wuxi, Jiangsu, 214064, P. R. China
XIAOTING WANG
Affiliation:
Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, Jiangsu Institute of Parasitic Diseases (JIPD), Meiyuan Yangxiang 117, Wuxi, Jiangsu, 214064, P. R. China
XIAOHONG GUAN
Affiliation:
School of Basic Medical Science, Nanjing Medical University, Nanjing, Jiangsu, 210029, P. R. China
OSAMU KANEKO
Affiliation:
Department of Protozoology, Institute of Tropical Medicine (NEKKEN) and the Global Center of Excellence Program, Nagasaki University, 1-12-4 Sakamoto, Nagasaki 852-8523, Japan
YINCHANG ZHU*
Affiliation:
School of Basic Medical Science, Nanjing Medical University, Nanjing, Jiangsu, 210029, P. R. China Key Laboratory on Technology for Parasitic Disease Prevention and Control, Ministry of Health, Jiangsu Institute of Parasitic Diseases (JIPD), Meiyuan Yangxiang 117, Wuxi, Jiangsu, 214064, P. R. China
*
*Corresponding author: Meiyuan Yangxiang 117, Wuxi, Jiangsu Province 214064, People's Republic of China. Tel: +86 510 8551 7721. Fax:+86 510 8551 0263. E-mail: [email protected]
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Summary

Plasmodium rhoptry neck protein 2 (RON2), which is released from the neck portion of the merozoite rhoptries and interacts with the microneme protein Apical Membrane Antigen 1 (AMA1), plays a crucial role in erythrocyte invasion. In this study, we sequenced the Plasmodium vivax RON2 gene from 19 P. vivax isolates collected in central China in order to establish whether this protein is under positive diversifying selection, which may occur as a result of protective host immune pressure†. In comparison with the P. vivax Sal-1 reference line, we found 10 amino acid substitutions dispersed throughout the open reading frame as well as indels caused by polymorphism in a repeat unit (21–23 repeats of (Q/E/K/N/H)(G/D)G(H/L/Y/P)G) in the second tandem repeat region located at amino acid positions 541–650. A McDonald-Kreitman test with RON2 sequences from the primate malaria parasite Plasmodium knowlesi, detected significant departure from neutrality in the PvRON2 3′ region (nucleotide positions 2668–6609). These results suggest that the PvRON2 gene has evolved under positive diversifying selection.

Keywords

Plasmodium vivaxRON2positive diversifying selectioncell invasion
Type
Research Article
Information
Parasitology , Volume 139 , Issue 6 , May 2012 , pp. 709 - 715
Copyright
Copyright © Cambridge University Press 2012

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References

REFERENCES

Alexander, D. L., Arastu-Kapur, S., Dubremetz, J. F. and Boothroyd, J. C. (2006). Plasmodium falciparum AMA1 binds a rhoptry neck protein homologous to TgRON4, a component of the moving junction in Toxoplasma gondii. Eukaryotic Cell 5, 1169–1173. doi:10.1128/EC.00040–06.CrossRefGoogle ScholarPubMed
Alexander, D. L., Mital, J., Ward, G. E., Bradley, P. and Boothroyd, J. C. (2005). Identification of the moving junction complex of Toxoplasma gondii: a collaboration between distinct secretory organelles. PLoS Pathogens 1, e17.CrossRefGoogle ScholarPubMed
Arévalo-Pinzón, G., Curtidor, H., Patiño, L. C. and Patarroyo, M. A. (2011). PvRON2, a new Plasmodium vivax rhoptry neck antigen. Malaria Journal 10, 60.CrossRefGoogle ScholarPubMed
Aurrecoechea, C., Brestelli, J., Brunk, B. P., Dommer, J., Fischer, S., Gajria, B., Gao, X., Gingle, A., Grant, G., Harb, O. S., Heiges, M., Innamorato, F., Iodice, J., Kissinger, J. C., Kraemer, E., Li, W., Miller, J. A., Nayak, V., Pennington, C., Pinney, d.f., Roos, D. S., Ross, C., Stoeckert, C. J. Jr, Treatman, C. and Wang, H. (2009). PlasmoDB: a functional genomic database for malaria parasites. Nucleic Acids Research 37, D539–543.CrossRefGoogle ScholarPubMed
Baum, J., Tonkin, C. J., Paul, A. S., Rug, M., Smith, B. J., Gould, S. B., Richard, D., Pollard, T. D. and Cowman, A. F. (2008). A malaria parasite forming regulates actin polymerization and localizes to the parasite-erythrocyte moving junction during invasion. Cell Host and Microbe 3, 188–198.CrossRefGoogle Scholar
Boothroyd, J. C. and Dubremetz, J. F. (2008). Kiss and split: the dual roles of Toxoplasma rhoptries. Nature Reviews Microbiology 6, 79–88.CrossRefGoogle Scholar
Cao, J., Kaneko, O., Thongkukiatkul, A., Tachibana, M., Otsuki, H., Gao, Q., Tsuboi, T. and Torii, M. (2009). Rhoptry neck protein RON2 forms a complex with microneme protein AMA1 in Plasmodium falciparum merozoites. Parasitology International 58, 29–35.CrossRefGoogle ScholarPubMed
Carlton, J. M., Adams, J. H., Silva, J. C., Bidwell, S. L., Lorenzi, H., Caler, E., Crabtree, J., Angiuoli, S. V., Merino, E. F., Amedeo, P., Cheng, Q., Coulson, R. M., Crabb, B. S., Del Portillo, H. A., Essien, K., Feldblyum, T. V., Fernandez-Becerra, C., Gilson, P. R., Gueye, A. H., Guo, X., Kang'a, S., Kooij, T. W., Korsinczky, M., Meyer, E. V., Nene, V., Paulsen, I., White, O., Ralph, S. A., Ren, Q., Sargeant, T. J., Salzberg, S. L., Stoeckert, C. J., Sullivan, S. A., Yamamoto, M. M., Hoffman, S. L., Wortman, J. R., Gardner, M. J., Galinski, M. R., Barnwell, J. W. and Fraser-Liggett, C. M. (2008). Comparative genomics of the neglected human malaria parasite Plasmodium vivax. Nature, London 455, 757–763.CrossRefGoogle ScholarPubMed
Curtidor, H., Patiño, L. C., Arévalo-Pinzón, G., Patarroyo, M. E. and Patarroyo, M. A. (2011). Identification of the Plasmodium falciparum rhoptry neck protein 5 (PfRON5). Gene 474, 22–8.CrossRefGoogle ScholarPubMed
Greenwood, B. M., Fidock, D. A., Kyle, D. E., Kappe, S. H., Alonso, P. L., Collins, F. H. and Duffy, P. E. (2008). Malaria: progress, perils, and prospects for eradication. Journal of Clinical Investigation 118, 1266–1276. doi:10.1172/JCI33996.CrossRefGoogle ScholarPubMed
von Heijne, G. (1992). Membrane protein structure prediction. Hydrophobicity analysis and the positive-inside rule. Journal of Molecular Biology 225, 487–94.CrossRefGoogle ScholarPubMed
Hirokawa, T., Boon-Chieng, S. and Mitaku, S. (1998). SOSUI: classification and secondary structure prediction system for membrane proteins. Bioinformatics 14, 378–379.CrossRefGoogle ScholarPubMed
Hofmann, K. and Stoffel, W. (1993). TMbase – A database of membrane spanning proteins segments. Biological Chemistry. Hoppe-Seyler 374, 166.Google Scholar
Hughes, A. L. and Nei, M. (1988). Pattern of nucleotide substitution at major histocompatibility complex class loci reveals overdominant selection. Nature, London 335, 167–170.CrossRefGoogle ScholarPubMed
Krogh, A., Larsson, B., von Heijne, G. and Sonnhammer, E. L. (2001). Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. Journal of Molecular Biology 305, 567–580.CrossRefGoogle ScholarPubMed
Lamarque, M., Besteiro, S., Papoin, J., Roques, M., Vulliez-Le Normand, B., Morlon-Guyot, J., Dubremetz, J. F., Fauquenoy, S., Tomavo, S., Faber, B. W., Kocken, C. H., Thomas, A. W., Boulanger, M. J., Bentley, G. A. and Lebrun, M. (2011). The RON2-AMA1 interaction is a critical step in moving junction-dependent invasion by apicomplexan parasites. PLoS Pathogens 7, e1001276. doi:10.1371/journal.ppat.1001276.CrossRefGoogle ScholarPubMed
Lebrun, M., Michelin, A., El Hajj, H., Poncet, J., Bradley, P. J., Vial, H. and Dubremetz, J. F. (2005). The rhoptry neck protein RON4 re-localizes at the moving junction during Toxoplasma gondii invasion. Cellular Microbiology 7, 1823–1833.CrossRefGoogle ScholarPubMed
McDonald, J. H. and Kreitman, M. (1991). Adaptive protein evolution at the Adh locus in Drosophila. Nature 351, 652–4.CrossRefGoogle ScholarPubMed
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 ScholarPubMed
Newman, A. M. and Cooper, J. B. (2007). XSTREAM: a practical algorithm for identification and architecture modeling of tandem repeats in protein sequences. BMC Bioinformatics 8, 382. doi:10.1186/1471-2105-8-382.CrossRefGoogle ScholarPubMed
Pain, A., Böhme, U., Berry, A. E., Mungall, K., Finn, R. D., Jackson, A. P., Mourier, T., Mistry, J., Pasini, E. M., Aslett, M. A., Balasubrammaniam, S., Borgwardt, K., Brooks, K., Carret, C., Carver, T. J., Cherevach, I., Chillingworth, T., Clark, T. G., Galinski, M. R., Hall, N., Harper, D., Harris, D., Hauser, H., Ivens, A., Janssen, C. S., Keane, T., Larke, N., Lapp, S., Marti, M., Moule, S., Meyer, I. M., Ormond, D., Peters, N., Sanders, M., Sanders, S., Sargeant, T. J., Simmonds, M., Smith, F., Squares, R., Thurston, S., Tivey, A. R., Walker, D., White, B., Zuiderwijk, E., Churcher, C., Quail, M. A., Cowman, A. F., Turner, C. M., Rajandream, M. A., Kocken, C. H., Thomas, A. W., Newbold, C. I., Barrell, B. G. and Berriman, M. (2008). The genome of the simian and human malaria parasite Plasmodium knowlesi. Nature, London 455, 799–803.CrossRefGoogle ScholarPubMed
Polley, S. D. and Conway, D. J. (2001). Strong diversifying selection on domains of the Plasmodium falciparum apical membrane antigen 1 gene. Genetics 158, 1505–1512.CrossRefGoogle ScholarPubMed
Price, R. N., Tjitr, E., Guerra, C. A., Yeung, S., White, N. J. and Anstey, N. M. (2007). Vivax malaria: neglected and not benign. American Journal of Tropical Medicine and Hygiene 77, 79–87.CrossRefGoogle Scholar
Richard, D., MacRaild, C. A., Riglar, D. T., Chan, J. A., Foley, M., Baum, J., Ralph, S. A., Norton, R. S. and Cowman, A. F. (2010). Interaction between Plasmodium falciparum apical membrane antigen 1 and the rhoptry neck protein complex defines a key step in the erythrocyte invasion process of malaria parasites. Journal of Biological Chemistry 285, 14815–22.CrossRefGoogle ScholarPubMed
Srinivasan, P., Beatty, W. L., Diouf, A., Herrera, R., Ambroggio, X., Moch, J.K., Tyler, J. S., Narum, D. L., Pierce, S. K., Boothroyd, J. C., Haynes, J. D. and Miller, L. H. (2011). Binding of Plasmodium merozoite proteins RON2 and AMA1 triggers commitment to invasion. Proceedings of the National Academy of Sciences, USA [Epub ahead of print].CrossRefGoogle Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. (1994). Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 4673–4680.CrossRefGoogle ScholarPubMed
Tonkin, M. L., Roques, M., Lamarque, M. H., Pugniére, M., Douguet, D., Crawford, J., Lebrun, M. and Boulanger, M. J. (2011). Host cell invasion by Apicomplexan parasites: Insights from the co-structure of AMA1 with RON2 peptide. Science 333, 463–467.CrossRefGoogle ScholarPubMed
Tufet-Bayona, M., Janse, C. J., Khan, S. M., Waters, A. P., Sinden, R. E. and Franke-Fayard, B. (2009). Localisation and timing of expression of putative Plasmodium berghei rhoptry proteins in merozoites and sporozoites. Molecular and Biochemical Parasitology 166, 22–31.CrossRefGoogle ScholarPubMed
Tusnády, G. E. and Simon, I. (2001). The HMMTOP transmembrane topology prediction server. Bioinformatics 17, 849–850.CrossRefGoogle ScholarPubMed
Tyler, J. S. and Boothroyd, J. C. (2011). The C-Terminus of Toxoplasma RON2 provides the crucial link between AMA1 and the host-associated invasion complex. PLoS Pathogens 7:e1001282. doi:10.1371/journal.ppat.1001282.CrossRefGoogle ScholarPubMed