Isolation and Characterization of the MSP1 Genes from Plasmodium malariae and Plasmodium ovale

Larry Birkenmeyer Infectious Diseases Research and Development, Abbott Diagnostics, Abbott Laboratories, Abbott Park, Illinois

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A. Scott Muerhoff Infectious Diseases Research and Development, Abbott Diagnostics, Abbott Laboratories, Abbott Park, Illinois

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George J. Dawson Infectious Diseases Research and Development, Abbott Diagnostics, Abbott Laboratories, Abbott Park, Illinois

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Suresh M. Desai Infectious Diseases Research and Development, Abbott Diagnostics, Abbott Laboratories, Abbott Park, Illinois

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The merozoite surface protein 1 (MSP1) is the principal surface antigen of the blood stage form of the Plasmodium parasite. Antibodies recognizing MSP1 are frequently detected following Plasmodium infection, making this protein a significant component of malaria vaccines and diagnostic tests. Although the MSP1 gene sequence has been reported for Plasmodium falciparum and Plasmodium vivax, this gene has not been identified for the other two major human-infectious species, Plasmodium malariae and Plasmodium ovale. MSP1 genes from these two species were isolated from Cameroon blood donor samples. The genes are similar in size to known MSP1 genes and encode proteins with interspecies conserved domains homologous to those identified in other Plasmodium species. Sequence and phylogenetic analysis of all available Plasmodium MSP1 amino acid sequences clearly shows that the Po and Pm MSP1 sequences are truly unique within the Plasmodium genus and not simply Pf or Pv variants.

Author Notes

*Address correspondence to Larry Birkenmeyer, Abbott Diagnostics, Infectious Diseases R&D, Dept. 09NB, Bldg. AP20, 100 Abbott Park Road, Abbott Park, IL 60064-6015. E-mail: larry.birkenmeyer@abbott.com

Authors' addresses: Larry Birkenmeyer, A. Scott Muerhoff, George Dawson, and Suresh M. Desai, Abbott Diagnostics, Infectious Diseases R&D, Abbott Park, IL, E-mails: larry.birkenmeyer@abbott.com, scott.muerhoff@abbott.com, george.dawson@abbott.com, and suresh.desai@abbott.com.

  • 1.

    Korenromp E, Miller J, Nahlen B, Wardlaw T, Young M, 2005. World Malaria Report. Available at: http://rbm.who.int/wmr2005/html/toc.htm.

  • 2.

    Collins WE, Barnwell JW, 2009. Plasmodium knowlesi: finally being recognized. J Infect Dis 199: 11071108.

  • 3.

    Lysenko AJ, Beljaev AE, 1969. An analysis of the geographical distribution of Plasmodium ovale. Bull World Health Organ 40: 383394.

  • 4.

    Mueller I, Zimmerman PA, Reeder JC, 2007. Plasmodium malariae and Plasmodium ovale–the “bashful” malaria parasites. Trends Parasitol 23: 278283.

    • Search Google Scholar
    • Export Citation
  • 5.

    Cox-Singh J, Davis TM, Lee KS, Shamsul SS, Matusop A, Ratnam S, Rahman HA, Conway DJ, Singh B, 2008. Plasmodium knowlesi malaria in humans is widely distributed and potentially life threatening. Clin Infect Dis 46: 165171.

    • Search Google Scholar
    • Export Citation
  • 6.

    White NJ, 2008. Plasmodium knowlesi: the fifth human malaria parasite. Clin Infect Dis 46: 172173.

  • 7.

    Florens L, Washburn MP, Raine JD, Anthony RM, Grainger M, Haynes JD, Moch JK, Muster N, Sacci JB, Tabb DL, Witney AA, Wolters D, Wu Y, Gardner MJ, Holder AA, Sinden RE, Yates JR, Carucci DJ, 2002. A proteomic view of the Plasmodium falciparum life cycle. Nature 419: 520526.

    • Search Google Scholar
    • Export Citation
  • 8.

    Fandeur T, Volney B, Peneau C, de Thoisy B, 2000. Monkeys of the rainforest in French Guiana are natural reservoirs for P. brasilianum/P. malariae malaria. Parasitology 120:1121.

    • Search Google Scholar
    • Export Citation
  • 9.

    Gerold P, Schofield L, Blackman MJ, Holder AA, Schwarz RT, 1996. Structural analysis of the glycosyl-phosphatidylinositol membrane anchor of the merozoite surface proteins-1 and -2 of Plasmodium falciparum. Mol Biochem Parasitol 75: 131143.

    • Search Google Scholar
    • Export Citation
  • 10.

    Blackman MJ, 2000. Proteases involved in erythrocyte invasion by the malaria parasite: function and potential as chemotherapeutic targets. Curr Drug Targets 1: 5983.

    • Search Google Scholar
    • Export Citation
  • 11.

    Blackman MJ, Whittle H, Holder AA, 1991. Processing of the Plasmodium falciparum major merozoite surface protein-1: identification of a 33-kilodalton secondary processing product which is shed prior to erythrocyte invasion. Mol Biochem Parasitol 49: 3544.

    • Search Google Scholar
    • Export Citation
  • 12.

    O'Dea KP, McKean PG, Harris A, Brown KN, 1995. Processing of the Plasmodium chabaudi chabaudi AS merozoite surface protein 1 in vivo and in vitro. Mol Biochem Parasitol 72:111119.

    • Search Google Scholar
    • Export Citation
  • 13.

    Blackman MJ, Dennis ED, Hirst EM, Kocken CH, Scott-Finnigan TJ, Thomas AW, 1996. Plasmodium knowlesi: secondary processing of the malaria merozoite surface protein-1. Exp Parasitol 83: 229239.

    • Search Google Scholar
    • Export Citation
  • 14.

    Tolle R, Fruh K, Doumbo O, Koita O, N'Diaye M, Fischer A, Dietz K, Bujard H, 1993. A prospective study of the association between the human humoral immune response to Plasmodium falciparum blood stage antigen gp190 and control of malarial infections. Infect Immun 61: 4047.

    • Search Google Scholar
    • Export Citation
  • 15.

    Egan AF, Chappel JA, Burghaus PA, Morris JS, McBride JS, Holder AA, Kaslow DC, Riley EM, 1995. Serum antibodies from malaria-exposed people recognize conserved epitopes formed by the two epidermal growth factor motifs of MSP1(19), the carboxy-terminal fragment of the major merozoite surface protein of Plasmodium falciparum. Infect Immun 63: 456466.

    • Search Google Scholar
    • Export Citation
  • 16.

    Faber BW, Remarque EJ, Morgan WD, Kocken CH, Holder AA, Thomas AW, 2007. Malaria vaccine-related benefits of a single protein comprising Plasmodium falciparum apical membrane antigen 1 domains I and II fused to a modified form of the 19-kilodalton C-terminal fragment of merozoite surface protein 1. Infect Immun 75: 59475955.

    • Search Google Scholar
    • Export Citation
  • 17.

    Stowers AW, Cioce V, Shimp RL, Lawson M, Hui G, Muratova O, Kaslow DC, Robinson R, Long CA, Miller LH, 2001. Efficacy of two alternate vaccines based on Plasmodium falciparum merozoite surface protein 1 in an Aotus challenge trial. Infect Immun 69: 15361546.

    • Search Google Scholar
    • Export Citation
  • 18.

    Kim S, Ahn HJ, Kim TS, Nam HW, 2003. ELISA detection of vivax malaria with recombinant multiple stage-specific antigens and its application to survey of residents in endemic areas. Korean J Parasitol 41: 203207.

    • Search Google Scholar
    • Export Citation
  • 19.

    Kitchen AD, Lowe PH, Lalloo K, Chiodini PL, 2004. Evaluation of a malarial antibody assay for use in the screening of blood and tissue products for clinical use. Vox Sang 87: 150155.

    • Search Google Scholar
    • Export Citation
  • 20.

    Walker-Abbey A, Djokam RR, Eno A, Leke RF, Titanji VP, Fogako J, Sama G, Thuita LH, Beardslee E, Snounou G, Zhou A, Taylor DW, 2005. Malaria in pregnant Cameroonian women: the effect of age and gravidity on submicroscopic and mixed-species infections and multiple parasite genotypes. Am J Trop Med Hyg 72: 229235.

    • Search Google Scholar
    • Export Citation
  • 21.

    Mangold KA, Manson RU, Koay ES, Stephens L, Regner M, Thomson RB Jr, Peterson LR, Kaul KL, 2005. Real-time PCR for detection and identification of Plasmodium spp. J Clin Microbiol 43: 24352440.

    • Search Google Scholar
    • Export Citation
  • 22.

    Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ, 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 33893402.

    • Search Google Scholar
    • Export Citation
  • 23.

    Sambrook J, Russell DW, 2001. Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.

  • 24.

    Genetics Computer Group, 2005. Wisconsin Package Version 11.0. San Diego, CA: Accelrys Inc.

  • 25.

    Tamura K, Dudley J, Nei M, Kumar S, 2007. MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24: 15961599.

    • Search Google Scholar
    • Export Citation
  • 26.

    Nei M, Gojobori T, 1986. Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3: 418426.

    • Search Google Scholar
    • Export Citation
  • 27.

    Eisenhaber B, Bork P, Eisenhaber F, 1999. Prediction of potential GPI-modification sites in proprotein sequences. J Mol Biol 292: 741758.

  • 28.

    Bendtsen JD, Nielsen H, von Heijne G, Brunak S, 2004. Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783795.

  • 29.

    Jones DT, Taylor WR, Thornton JM, 1992. The rapid generation of mutation data matrices from protein sequences. Comput Appl Biosci 8: 275282.

    • Search Google Scholar
    • Export Citation
  • 30.

    Felsenstein J, 1985. Confidence limits on phylogenies: an approach using the bootstrap. Evolution 39: 783791.

  • 31.

    Win TT, Jalloh A, Tantular IS, Tsuboi T, Ferreira MU, Kimura M, Kawamoto F, 2004. Molecular analysis of Plasmodium ovale variants. Emerg Infect Dis 10: 12351240.

    • Search Google Scholar
    • Export Citation
  • 32.

    Tanabe K, Escalante A, Sakihama N, Honda M, Arisue N, Horii T, Culleton R, Hayakawa T, Hashimoto T, Longacre S, Pathirana S, Handunnetti S, Kishino H, 2007. Recent independent evolution of msp1 polymorphism in Plasmodium vivax and related simian malaria parasites. Mol Biochem Parasitol 156: 7479.

    • Search Google Scholar
    • Export Citation
  • 33.

    Blackman MJ, Ling IT, Nicholls SC, Holder AA, 1991. Proteolytic processing of the Plasmodium falciparum merozoite surface protein-1 produces a membrane-bound fragment containing two epidermal growth factor-like domains. Mol Biochem Parasitol 49: 2933.

    • Search Google Scholar
    • Export Citation
  • 34.

    Deleersnijder W, Hendrix D, Bendahman N, Hanegreefs J, Brijs L, Hamers-Casterman C, Hamers R, 1990. Molecular cloning and sequence analysis of the gene encoding the major merozoite surface antigen of Plasmodium chabaudi chabaudi IP-PC1. Mol Biochem Parasitol 43: 231244.

    • Search Google Scholar
    • Export Citation
  • 35.

    Zhong H, Fan JY, Yang S, Davidson EA, 1999. Cloning and characterization of the merozoite surface antigen 1 gene of Plasmodium berghei. Am J Trop Med Hyg 60: 994999.

    • Search Google Scholar
    • Export Citation
  • 36.

    Koussis K, Withers-Martinez C, Yeoh S, Child M, Hackett F, Knuepfer E, Juliano L, Woehlbier U, Bujard H, Blackman MJ, 2009. A multifunctional serine protease primes the malaria parasite for red blood cell invasion. EMBO J 28: 725735.

    • Search Google Scholar
    • Export Citation
  • 37.

    Withers-Martinez C, Jean L, Blackman MJ, 2004. Subtilisin-like proteases of the malaria parasite. Mol Microbiol 53: 5563.

  • 38.

    Harris PK, Yeoh S, Dluzewski AR, O'Donnell RA, Withers-Martinez C, Hackett F, Bannister LH, Mitchell GH, Blackman MJ, 2005. Molecular identification of a malaria merozoite surface sheddase. PLoS Pathog 1: 241251.

    • Search Google Scholar
    • Export Citation
  • 39.

    Naik RS, Branch OH, Woods AS, Vijaykumar M, Perkins DJ, Nahlen BL, Lal AA, Cotter RJ, Costello CE, Ockenhouse CF, Davidson EA, Gowda DC, 2000. Glycosylphosphatidylinositol anchors of Plasmodium falciparum: molecular characterization and naturally elicited antibody response that may provide immunity to malaria pathogenesis. J Exp Med 192: 15631576.

    • Search Google Scholar
    • Export Citation
  • 40.

    Udenfriend S, Kodukula K, 1995. How glycosylphosphatidylinositol-anchored membrane proteins are made. Annu Rev Biochem 64: 563591.

  • 41.

    Hughes AL, 1992. Positive selection and interallelic recombination at the merozoite surface antigen-1 (MSA-1) locus of Plasmodium falciparum. Mol Biol Evol 9: 381393.

    • Search Google Scholar
    • Export Citation
  • 42.

    Leclerc MC, Hugot JP, Durand P, Renaud F, 2004. Evolutionary relationships between 15 Plasmodium species from new and old world primates (including humans): an 18S rDNA cladistic analysis. Parasitology 129: 677684.

    • Search Google Scholar
    • Export Citation
  • 43.

    Ollomo B, Durand P, Prugnolle F, Douzery E, Arnathau C, Nkoghe D, Leroy E, Renaud F, 2009. A new malaria agent in African hominids. PLoS Pathog 5: e1000446.

  • 44.

    Perkins SL, Schall JJ, 2002. A molecular phylogeny of malarial parasites recovered from cytochrome b gene sequences. J Parasitol 88: 972978.

    • Search Google Scholar
    • Export Citation
  • 45.

    Rich SM, Leendertz FH, Xu G, LeBreton M, Djoko CF, Aminake MN, Takang EE, Diffo JL, Pike BL, Rosenthal BM, Formenty P, Boesch C, Ayala FJ, Wolfe ND, 2009. The origin of malignant malaria. Proc Natl Acad Sci USA 106: 1490214907.

    • Search Google Scholar
    • Export Citation
  • 46.

    Van de Peer Y, Baldauf SL, Doolittle WF, Meyer A, 2000. An updated and comprehensive rRNA phylogeny of (crown) eukaryotes based on rate-calibrated evolutionary distances. J Mol Evol 51: 565576.

    • Search Google Scholar
    • Export Citation
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