RARE PLASMODIUM FALCIPARUM MEROZOITE SURFACE PROTEIN 1 19-KDA (MSP-119) HAPLOTYPES IDENTIFIED IN MALI USING HIGH-THROUGHPUT GENOTYPING METHODS

SHANNON L. TAKALA Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Fogarty International Center, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali

Search for other papers by SHANNON L. TAKALA in
Current site
Google Scholar
PubMed
Close
,
DAVID L. SMITH Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Fogarty International Center, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali

Search for other papers by DAVID L. SMITH in
Current site
Google Scholar
PubMed
Close
,
MAHAMADOU A. THERA Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Fogarty International Center, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali

Search for other papers by MAHAMADOU A. THERA in
Current site
Google Scholar
PubMed
Close
,
DRISSA COULIBALY Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Fogarty International Center, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali

Search for other papers by DRISSA COULIBALY in
Current site
Google Scholar
PubMed
Close
,
OGOBARA K. DOUMBO Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Fogarty International Center, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali

Search for other papers by OGOBARA K. DOUMBO in
Current site
Google Scholar
PubMed
Close
, and
CHRISTOPHER V. PLOWE Center for Vaccine Development, University of Maryland School of Medicine, Baltimore, Maryland; Fogarty International Center, National Institutes of Health, Bethesda, Maryland; Malaria Research and Training Center, University of Bamako, Bamako, Mali

Search for other papers by CHRISTOPHER V. PLOWE in
Current site
Google Scholar
PubMed
Close
Restricted access

Genetic diversity in malaria vaccine antigens may compromise malaria vaccine efficacy, so it is important to understand this diversity and the processes that generate it. By applying new high-throughput genotyping methods to a large sample of infections from Mali (N = 1369), seven new 19-kDa merozoite surface protein 1 (MSP-119) haplotypes were identified. Herein we report the sequences of these new haplotypes and discuss their possible origins. Although they are present in < 1% of the samples examined, the existence of these rare haplotypes reveals a greater degree of diversity at this locus than previously reported and highlights the potential for Plasmodium to evolve under selective pressure from the immune system and from such interventions as vaccines and drugs.

Author Notes

  • 1

    Escalante AA, Lal AA, Ayala FJ, 1998. Genetic polymorphism and natural selection in the malaria parasite Plasmodium falciparum.Genetics 149 :189–202.

  • 2

    Blackman MJ, Heidrich HG, Donachie S, McBride JS, Holder AA, 1990. A single fragment of a malaria merozoite surface protein remains on the parasite during red cell invasion and is the target of invasion-inhibiting antibodies. J Exp Med 172 :379–382.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Holder AA, Blackman MJ, Burghaus PA, Chappel JA, Ling IT, McCallum-Deighton N, Shai S, 1992. A malaria merozoite surface protein (MSP1)—structure, processing and function. Mem Inst Oswaldo Cruz 87 :37–42.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 4

    Branch OH, Udhayakumar V, Hightower AW, Oloo AJ, Hawley WA, Nahlen BL, Bloland PB, Kaslow DC, Lal AA, 1998. A longitudinal investigation of IgG and IgM antibody responses to the merozoite surface protein-1 19-kiloDalton domain of Plasmodium falciparum in pregnant women and infants: associations with febrile illness, parasitemia, and anemia. Am J Trop Med Hyg 58 :211–219.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 5

    Branch OH, Oloo AJ, Nahlen BL, Kaslow D, Lal AA, 2000. Anti-merozoite surface protein-1 19-kDa IgG in mother-infant pairs naturally exposed to Plasmodium falciparum: subclass analysis with age, exposure to asexual parasitemia, and protection against malaria. V. The Asembo Bay Cohort Project. J Infect Dis 181 :1746–1752.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 6

    Egan AF, Morris J, Barnish G, Allen S, Greenwood BM, Kaslow DC, Holder AA, Riley EM, 1996. Clinical immunity to Plasmodium falciparum malaria is associated with serum antibodies to the 19-kDa C-terminal fragment of the merozoite surface antigen, PfMSP-1. J Infect Dis 173 :765–769.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 7

    John CC, O’Donnell RA, Sumba PO, Moormann AM, Koning-Ward TF, King CL, Kazura JW, Crabb BS, 2004. Evidence that invasion-inhibitory antibodies specific for the 19-kDa fragment of merozoite surface protein-1 (MSP-119) can play a protective role against blood-stage Plasmodium falciparum infection in individuals in a malaria endemic area of Africa. J Immunol 173 :666–672.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 8

    Okech BA, Corran PH, Todd J, Joynson-Hicks A, Uthaipibull C, Egwan TG, Holder AA, Riley EM, 2004. Fine specificity of serum antibodies to Plasmodium falciparum merozoite surface protein, PfMSP-1(19), predicts protection from malaria infection and high-density parasitemia. Infect Immun 72 :1557–1567.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Riley EM, Allen SJ, Wheeler JG, Blackman MJ, Bennett S, Takacs B, Schonfeld HJ, Holder AA, Greenwood BM, 1992. Naturally acquired cellular and humoral immune responses to the major merozoite surface antigen (PfMSP1) of Plasmodium falciparum are associated with reduced malaria morbidity. Parasite Immunol 14 :321–337.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Miller LH, Roberts T, Shahabuddin M, McCutchan TF, 1993. Analysis of sequence diversity in the Plasmodium falciparum merozoite surface protein-1 (MSP-1). Mol Biochem Parasitol 59 :1–14.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 11

    Da Silveira LA, Ribeiro WL, Kirchgatter K, Wunderlich G, Matsuoka H, Tanabe K, Ferreira MU, 2001. Sequence diversity and linkage disequilibrium within the Merozoite Surface Protein-1 (MSP-1) locus of Plasmodium falciparum: a longitudinal study in Brazil. J Eukaryot Microbiol 48 :433–439.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Ferreira MU, Ribeiro WL, Tonon AP, Kawamoto F, Rich SM, 2003. Sequence diversity and evolution of the malaria vaccine candidate merozoite surface protein-1 (MSP-1) of Plasmodium falciparum.Gene 304 :65–75.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Qari SH, Shi YP, Goldman IF, Nahlen BL, Tibayrenc M, Lal AA, 1998. Predicted and observed alleles of Plasmodium falciparum merozoite surface protein-1 (MSP-1), a potential malaria vaccine antigen. Mol Biochem Parasitol 92 :241–252.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Sakihama N, Kimura M, Hirayama K, Kanda T, Na-Bangchang K, Jongwutiwes S, Conway D, Tanabe K, 1999. Allelic recombination and linkage disequilibrium within MSP-1 of Plasmodium falciparum, the malignant human malaria parasite. Gene 230 :47–54.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Gupta S, Swinton J, Anderson RM, 1994. Theoretical studies of the effects of heterogeneity in the parasite population on the transmission dynamics of malaria. Proc R Soc Lond B Biol Sci 256 :231–238.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 16

    Gupta S, Ferguson NM, Anderson RM, 1997. Vaccination and the population structure of antigenically diverse pathogens that exchange genetic material. Proc R Soc Lond B Biol Sci 264 :1435–1443.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 17

    Lipsitch M, 1997. Vaccination against colonizing bacteria with multiple serotypes. Proc Natl Acad Sci USA 94 :6571–6576.

  • 18

    Lythgoe KA, 2002. Effects of acquired immunity and mating strategy on the genetic structure of parasite populations. Am Nat 159 :519–529.

  • 19

    McLean AR, 1995. Vaccination, evolution and changes in the efficacy of vaccines: a theoretical framework. Proc Biol Sci 261 :389–393.

  • 20

    Genton B, Betuela I, Felger I, Al-Yaman F, Anders RF, Saul A, Rare L, Baisor M, Lorry K, Brown GV, Pye D, Irving DO, Smith TA, Beck HP, Alpers MP, 2002. A recombinant blood-stage malaria vaccine reduces Plasmodium falciparum density and exerts selective pressure on parasite populations in a phase 1-2b trial in Papua New Guinea. J Infect Dis 185 :820–827.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 21

    Takala SL, Coulibaly D, Thera MA, Dicko A, Smith DL, Guindo AB, Kone AK, Traore K, Ouattara A, Djimde AA, Sehdev PS, Lyke KE, Diallo DA, Doumbo OK, Plowe CV, 2007. Dynamics of polymorphism in a malaria vaccine antigen at a vaccine-testing site in Mali. PLoS Med 4 :e93.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 22

    Takala SL, Smith DL, Stine OC, Coulibaly D, Thera MA, Doumbo OK, Plowe CV, 2006. A high-throughput method for quantifying alleles and haplotypes of the malaria vaccine candidate Plasmodium falciparum merozoite surface protein-1 19kDa. Malar J 5 :31.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 23

    Vijay KS, Ranjan S, Saxena V, Rajesh V, Roy SK, Kochar D, Ranjan A, Das A, 2005. Plasmodium falciparum: genetic diversity of C-terminal region of MSP-1 in isolates from Indian sub-continent. Exp Parasitol 110 :384–388.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 24

    Conway DJ, Roper C, Oduola AM, Arnot DE, Kremsner PG, Grobusch MP, Curtis CF, Greenwood BM, 1999. High recombination rate in natural populations of Plasmodium falciparum.Proc Natl Acad Sci USA 96 :4506–4511.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 25

    Tibayrenc M, Kjellberg F, Arnaud J, Oury B, Breniere SF, Darde ML, Ayala FJ, 1991. Are eukaryotic microorganisms clonal or sexual? A population genetics vantage. Proc Natl Acad Sci USA 88 :5129–5133.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 26

    McCutchan TF, Lal AA, do Rosario V, Waters AP, 1992. Two types of sequence polymorphism in the circumsporozoite gene of Plasmodium falciparum.Mol Biochem Parasitol 50 :37–45.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 27

    Chang SP, Case SE, Gosnell WL, Hashimoto A, Kramer KJ, Tam LQ, Hashiro CQ, Nikaido CM, Gibson HL, Lee-Ng CT, Barr PJ, Yokota BT, Hut GS, 1996. A recombinant baculovirus 42-kilodalton C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 protects Aotus monkeys against malaria. Infect Immun 64 :253–261.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 28

    Stoute JA, Gombe J, Withers MR, Siangla J, McKinney D, Onyango M, Cummings JF, Milman J, Tucker K, Soisson L, Stewart VA, Lyon JA, Angov E, Leach A, Cohen J, Kester KE, Ockenhouse CF, Holland CA, Diggs CL, Wittes J, Gray HD Jr, 2007. Phase 1 randomized double-blind safety and immunogenicity trial of Plasmodium falciparum malaria merozoite surface protein FMP1 vaccine, adjuvanted with AS02A, in adults in western Kenya 1. Vaccine 25 (1):176–184. Epub 2005 Dec 7.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 29

    Holder AA, Lockyer MJ, Odink KG, Sandhu JS, Riveros-Moreno V, Nicholls SC, Hillman Y, Davey LS, Tizard ML, Schwarz RT, 1985. Primary structure of the precursor to the three major surface antigens of Plasmodium falciparum merozoites. Nature 317 :270–273.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 30

    Tanabe K, Mackay M, Goman M, Scaife JG, 1987. Allelic dimorphism in a surface antigen gene of the malaria parasite Plasmodium falciparum.J Mol Biol 195 :273–287.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 31

    Chang SP, Kramer KJ, Yamaga KM, Kato A, Case SE, Siddiqui WA, 1988. Plasmodium falciparum: gene structure and hydropathy profile of the major merozoite surface antigen (gp195) of the Uganda-Palo Alto isolate. Exp Parasitol 67 :1–11.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 32

    Jongwutiwes S, Tanabe K, Kanbara H, 1993. Sequence conservation in the C-terminal part of the precursor to the major merozoite proteins (MSP-1) of Plasmodium falciparum from field isolates. Mol Biochem Parasitol 59 :95–100.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 33

    Kang Y, Long CA, 1995. Sequence heterogeneity of the C-terminal, Cys-rich region of the merozoite surface protein-1 (MSP-1) in field samples of Plasmodium falciparum.Mol Biochem Parasitol 73 :103–110.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 34

    Lalitha PV, Malhotra P, Chattopadhyay R, Chauhan VS, 1999. Plasmodium falciparum: variations in the C-terminal cysteine-rich region of the merozoite surface protein-1 in field samples among Indian isolates. Exp Parasitol 92 :12–18.

    • PubMed
    • Search Google Scholar
    • Export Citation
Past two years Past Year Past 30 Days
Abstract Views 55 55 14
Full Text Views 316 1 0
PDF Downloads 37 0 0
 
 
 
 
Affiliate Membership Banner
 
 
Research for Health Information Banner
 
 
CLOCKSS
 
 
 
Society Publishers Coalition Banner
Save