• 1.

    Mendis K, Sina BJ, Marchesini P, Carter R, 2001. The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64: 97106.

  • 2.

    Genton B, D'Acremont V, Rare L, Baea K, Reeder JC, Alpers MP, Muller I, 2008. Plasmodium vivax and mixed infections are associated with severe malaria in children: a prospective cohort study from Papua New Guinea. PLoS Med 5: 881889.

    • Search Google Scholar
    • Export Citation
  • 3.

    Tjitra E, Anstey NM, Sugiarto P, Warikar N, Kenangalem E, Karyana M, Lampah DA, Price RN, 2008. Multidrug–resistant Plasmodium vivax associated with severe and fatal malaria: a prospective study in Papua, Indonesia. PLoS Med 5: 890899.

    • Search Google Scholar
    • Export Citation
  • 4.

    Barnwell JW, Nichols ME, Rubinstein P, 1989. In vitro evaluation of the role of the Duffy blood group in erythrocyte invasion by Plasmodium vivax. J Exp Med 169: 17951802.

    • Search Google Scholar
    • Export Citation
  • 5.

    Adams JH, Sim BK, Dolan SA, Fang X, Kaslow DC, Miller LH, 1992. A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci USA 89: 70857089.

    • Search Google Scholar
    • Export Citation
  • 6.

    Wertheimer SP, Barnwell JW, 1989. Plasmodium vivax interaction with the human Duffy blood group glycoprotein: identification of a parasite receptor like protein. Exp Parasitol 69: 340350.

    • Search Google Scholar
    • Export Citation
  • 7.

    Horuk R, Chitnis CE, Darbonne WC, Colby TJ, Rybicki A, Hadley TJ, Miller LH, 1993. A receptor for the malarial parasite Plasmodium vivax. The erythrocyte chemokine receptor. Science 261: 11821184.

    • Search Google Scholar
    • Export Citation
  • 8.

    Barnwell JW, Galinski MR, 1995. Plasmodium vivax: a glimpse into the unique and shared biology of the merozoite. Ann Trop Med Parasitol 89: 113120.

    • Search Google Scholar
    • Export Citation
  • 9.

    Ryan JR, Stoute JA, Amon J, Dunton RF, Mtalib R, Koros J, Owour B, Luckhart SH, Wirtz RA, Barnwell JW, Rosenberg R, 2006. Evidence for transmission of Plasmodium vivax among a Duffy antigen negative population in western Kenya. Am J Trop Med Hyg 75: 575581.

    • Search Google Scholar
    • Export Citation
  • 10.

    Menard D, Barnadas C, Bouchier C, Henry-Halldin C, Ratsimbasoa A, Thonier V, Carod JF, Domarle O, Colin Y, Bertrand O, Picot K, King CL, Grimberg BT, Mercereau-Puijalon O, Zimmerman PA, 2010. Plasmodium vivax clinical malaria is commonly observed in Duffy-negative Malagasy people. Proc Natl Acad Sci USA 107: 59675971.

    • Search Google Scholar
    • Export Citation
  • 11.

    Adam H, Hudson DE, Torii M, Ward GE, Wellems TE, Aikawa M, Miller LH, 1990. The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 63: 141153.

    • Search Google Scholar
    • Export Citation
  • 12.

    Chitnis CE, Miller LH, 1994. Identification of the erythrocyte binding domains of Plasmodium vivax and Plasmodium knowlesi proteins involved in erythrocyte invasion. J Exp Med 180: 497506.

    • Search Google Scholar
    • Export Citation
  • 13.

    Chitnis CE, Chaudhuri A, Horuk R, Pogo AO, Miller LH, 1996. The domain on the Duffy blood group antigen for binding Plasmodium vivax and P. knowlesi malarial parasites to erythrocytes. J Exp Med 184: 15311536.

    • Search Google Scholar
    • Export Citation
  • 14.

    Ranjan A, Chitnis CE, 1999. Mapping regions containing binding residues within functional domains of Plasmodium vivax and Plasmodium knowlesi erythrocyte–binding proteins. Proc Natl Acad Sci USA 96: 1406714072.

    • Search Google Scholar
    • Export Citation
  • 15.

    Singh SK, Singh AP, Pandey S, Yazdani SS, Chitnis CE, Sharma A, 2003. Definition of structural elements in Plasmodium vivax and P. knowlesi Duffy–binding domains necessary for erythrocyte invasion. Biochem J 374: 193198.

    • Search Google Scholar
    • Export Citation
  • 16.

    Tsuboi T, Kappe SH, Al-Yaman F, Prickett MD, Alpers M, Adams JH, 1994. Natural variation within the principal adhesion domain of the Plasmodium vivax Duffy binding protein. Infect Immun 62: 55815586.

    • Search Google Scholar
    • Export Citation
  • 17.

    Ampudia E, Patarroyo MA, Patarroyo ME, Murillo LA, 1996. Genetic polymorphism of the Duffy receptor binding domain of Plasmodium vivax in Colombian wild isolates. Mol Biochem Parasitol 78: 269272.

    • Search Google Scholar
    • Export Citation
  • 18.

    Xainli J, Adams JH, King CL, 2000. The erythrocyte binding motif of Plasmodium vivax Duffy binding protein is highly polymorphic and functionally conserved in isolates from Papua New Guinea. Mol Biochem Parasitol 111: 253260.

    • Search Google Scholar
    • Export Citation
  • 19.

    Cole-Tobian J, King CL, 2003. Diversity and natural selection in Plasmodium vivax Duffy binding protein gene. Mol Biochem Parasitol 127: 121132.

    • Search Google Scholar
    • Export Citation
  • 20.

    Babaeekho L, Zakeri S, Djadid ND, 2009. Genetic mapping of the Duffy binding protein (DBP) ligand domain of Plasmodium vivax from unstable malaria region in the Middle East. Am J Trop Med Hyg 80: 112118.

    • Search Google Scholar
    • Export Citation
  • 21.

    Michon P, Fraser T, Adams JH, 2000. Naturally acquired and vaccine-elicited antibodies block erythrocyte cytoadherence of the Plasmodium vivax Duffy binding protein. Infect Immun 68: 31643171.

    • Search Google Scholar
    • Export Citation
  • 22.

    Cole-Tobian JL, Cortes A, Baisor M, Kastens W, Xainli J, Bockarie M, Adams JH, King CL, 2002. Age-acquired immunity to a Plasmodium vivax invasion ligand, the Duffy binding protein. J Infect Dis 186: 531539.

    • Search Google Scholar
    • Export Citation
  • 23.

    Xainli J, Cole-Tobian JL, Baisor M, Kastens W, Bockarie M, Yazdani SS, Chitnis CE, Adams JH, King CL, 2003. Epitope-specific humoral immunity to Plasmodium vivax Duffy binding protein. Infect Immun 71: 25082515.

    • Search Google Scholar
    • Export Citation
  • 24.

    Xainli J, Baiso M, Kastens W, Bockarie M, Adams JH, King CL, 2002. Age-dependent cellular immune responses to Plasmodium vivax Duffy binding protein in humans. J Immunol 169: 32003207.

    • Search Google Scholar
    • Export Citation
  • 25.

    Cole-Tobian JL, Michon P, Biasor M, Richards JS, Beeson JG, Mueller I, King CL, 2009. Strain-specific Duffy binding protein antibodies correlate with protection against infection with homologous compared to heterologous Plasmodiun vivax strains in Papua New Guinean children. Infect Immun 77: 40094017.

    • Search Google Scholar
    • Export Citation
  • 26.

    Ceravolo IP, Souza-Silva FA, Fontes CJ, Braga EM, Madureira AP, Krettli AU, Souza JM, Brito CF, Adams JH, Carvalho LH, 2008. Inhibitory properties of the antibody response to Plasmodium vivax Duffy binding protein in an area with unstable malaria transmission. Scand J Immunol 67: 270278.

    • Search Google Scholar
    • Export Citation
  • 27.

    Ceravolo IP, Sanchez BA, Sousa TN, Guerra BM, Soares IS, Braga EM, McHenry AM, Adams JH, Brito CF, Carvalho LH, 2009. Naturally acquired inhibitory antibodies to Plasmodium vivax Duffy binding protein are short-lived and allele-specific following a single malaria infection. Clin Exp Immunol 156: 502510.

    • Search Google Scholar
    • Export Citation
  • 28.

    Souza-Silva FA, da Silva-Nunes M, Sanchez BA, Ceravolo IP, Malafronte RS, Brito CF, Ferreira MU, Carvalho LH, 2010. Naturally acquired antibodies to Plasmodium vivax Duffy binding protein (DBP) in rural Brazilian Amazon. Am J Trop Med Hyg 82: 185193.

    • Search Google Scholar
    • Export Citation
  • 29.

    Michon PA, Arevalo-Herrera M, Fraser T, Herrera S, Adams JH, 1998. Serologic responses to recombinant Plasmodium vivax Duffy binding protein in a Colombian village. Am J Trop Med Hyg 59: 597599.

    • Search Google Scholar
    • Export Citation
  • 30.

    Fraser T, Michon P, Barnwell JW, Noe AR, Al-Yaman F, Kaslow DC, Adams JH, 1997. Expression and serologic activity of a soluble recombinant Plasmodium vivax Duffy binding protein. Infect Immun 65: 27722777.

    • Search Google Scholar
    • Export Citation
  • 31.

    Singh S, Pandey K, Chattopadhayay R, Yazdani SS, Lynn A, Bharadwaj A, Ranjan A, Chitnis C, 2001. Biochemical, biophysical, and functional characterization of bacterially expressed and refolded receptor binding domain of Plasmodium vivax Duffy-binding protein. J Biol Chem 276: 1711117116.

    • Search Google Scholar
    • Export Citation
  • 32.

    Grimberg BT, Udomsangpetch R, Xainli J, McHenry A, Panichakul T, Sattabongkot J, Cui L, Bockarie M, Chitnis CE, Adams J, Zimmerman PA, King CHL, 2007. Vivax invasion of human erythrocytes inhibited by antibodies directed against the Duffy binding protein. PLoS Med 4: 19401947.

    • Search Google Scholar
    • Export Citation
  • 33.

    Ceravolo IP, Bruna-Romero O, Braga EM, Fontes CJ, Brito CF, Souza JM, Krettli AU, Adams JH, Carvalho LH, 2005. Anti-Plasmodium vivax Duffy binding protein antibodies measure exposure to malaria in the Brazilian Amazon. Am Trop Med Hyg 72: 675681.

    • Search Google Scholar
    • Export Citation
  • 34.

    Zakeri S, Najafabadi ST, Zare A, Djadid ND, 2002. Detection of malaria parasites by nested PCR in south–eastern, Iran: evidence of highly mixed infections in Chahbahar district. Malar J 1: 2.

    • Search Google Scholar
    • Export Citation
  • 35.

    Snounou G, Viriyakosol S, Zhu XP, Jarra W, Pinheiro L, do Rosario VE, Thaithong S, Brown KN, 1993. High sensitivity of detection of human malaria parasites by the use of nested polymerase chain reaction. Mol Biochem Parasitol 61: 315320.

    • Search Google Scholar
    • Export Citation
  • 36.

    Hedman K, Lappalainen M, Seppaia I, Makela O, 1989. Recent primary Toxoplasma infection indicated by a low avidity of specific IgG. J Infect Dis 159: 736740.

    • Search Google Scholar
    • Export Citation
  • 37.

    Suárez-mutis MC, Cuervo P, Leoratti FM, Moraes-Avila SL, Ferreira AW, Fernandes O, Coura JR, 2007. Cross sectional study reveals a high percentage of asymptomatic Plasmodium vivax infection in the Amazon Rio Negro area, Brazil Rev. Inst Med Trop Sao Paulo 49: 159164.

    • Search Google Scholar
    • Export Citation
  • 38.

    Baum J, Thomas AW, Conway DJ, 2003. Evidence for diversifying selection on erythrocyte-binding antigens of Plasmodium falciparum and P. vivax. Genetics 163: 13271336.

    • Search Google Scholar
    • Export Citation
  • 39.

    Kho WG, Chung JY, Sim EJ, Kim DW, Chung WC, 2001. Analysis of polymorphic regions of Plasmodium vivax Duffy binding protein of Korean isolates. Korean J Parasitol 39: 143150.

    • Search Google Scholar
    • Export Citation
  • 40.

    Sousa TN, Ceravolo IP, Frnandes Fontes CJ, Couto A, Carvalho LH, Brito CF, 2006. The pattern of major polymorphisms in the Duffy binding protein ligand domain from the Brazilian Amazon area. Mol Biochem Parasitol 146: 251254.

    • Search Google Scholar
    • Export Citation
  • 41.

    Egan A, Waterfall M, Pinder M, Holder A, Riley E, 1997. Characterization of human T- and B-cell epitopes in the C terminus of Plasmodium falciparum merozoite surface protein 1: evidence for poor T-cell recognition of polypeptides with numerous disulfide bonds. Infect Immun 65: 30243031.

    • Search Google Scholar
    • Export Citation
  • 42.

    Quin SJ, Seixas EM, Cross CA, Berg M, Lindo V, Stockinger B, Langhorne J, 2001. Low CD4+ T cell responses to the C-terminal region of the malaria merozoite surface protein-1 may be attributed to processing within distinct MHC class II pathways. Eur J Immunol 31: 7281.

    • Search Google Scholar
    • Export Citation
  • 43.

    Ferreira MU, Kimura EA, Souza JM, Katzin AM, 1996. The isotype composition and avidity of naturally acquired anti-Plasmodium falciparum antibodies: differential patterns in clinically immune Africans and Amazonians patients. Am J Trop Med Hyg 55: 315323.

    • Search Google Scholar
    • Export Citation
  • 44.

    Soares IS, Barnwell JW, Ferreira MU, Gomes Da Cunha M, Laurino JP, Castilho BA, Rodrigues MM, 1999. A Plasmodium vivax vaccine candidate displays limited allele polymorphism, which doses not restrict recognition by antibodies. Mol Med 5: 459470.

    • Search Google Scholar
    • Export Citation
  • 45.

    Aikawa M, Miller LH, Johnson J, Rabbege J, 1978. Erythrocyte entry by malaria parasites. A moving junction between erythrocyte and parasite. J Cell Biol 77: 7282.

    • Search Google Scholar
    • Export Citation
  • 46.

    Cowman A, Crabb B, 2006. Invasion of red blood cells by malaria parasites. Cell 124: 755766.

Past two years Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 245 147 3
PDF Downloads 58 32 1
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 

 

 

 

Antibody Responses and Avidity of Naturally Acquired Anti-Plasmodium vivax Duffy Binding Protein (PvDBP) Antibodies in Individuals from an Area with Unstable Malaria Transmission

View More View Less
  • Malaria and Vector Research Group (MVRG), Biotechnology Research Center (BRC), Pasteur Institute of Iran, Tehran, Iran
Restricted access

Plasmodium vivax remains an important cause of morbidity outside Africa, and no effective vaccine is available against this parasite. The P. vivax Duffy binding protein (PvDBP) is essential during merozoite invasion into erythrocytes, and it is a target for protective immunity against malaria. This investigation was designed to evaluate naturally acquired antibodies to two variant forms of PvDBP-II antigen (DBP-I and -VI) in malaria individuals (N = 85; median = 22 years) who were living in hypoendemic areas in Iran. The two PvDBP-II variants were expressed in Escherichia coli, and immunoglobulin G (IgG) isotype composition and avidity of naturally acquired antibodies to these antigens were measured using enzyme-linked immunosorbent assay (ELISA). Results showed that almost 32% of the studied individuals had positive antibody responses to the two PvDBP-II variants, and the prevalence of responders did not differ significantly (P > 0.05; χ2 test). The IgG-positive samples exhibited 37.03% and 40.8% high-avidity antibodies for PvDBP-I and PvDBP-VI variants, respectively. Furthermore, high-avidity IgG1 antibody was found in 39.1% of positive sera for each examined variant antigen. The avidity of antibodies for both PvDBP variant antigens and the prevalence of responders with high- and intermediate-avidity IgG, IgG1, and IgG3 antibodies were similar in patients (P > 0.05; χ2 test). Moreover, the prevalence of IgG antibody responses to the two variants significantly increased with exposure and host age. To sum up, the results provided additional data in our understanding of blood-stage immunity to PvDBP, supporting the rational development of an effective blood-stage vaccine based on this antigen.

Author Notes

*Address correspondence to Sedigheh Zakeri, Malaria and Vector Research Group (MVRG), Biotechnology Research Centre (BRC), Pasteur Institute of Iran, PO Box 1316943551, Tehran, Iran. E-mail: zakeris@pasteur.ac.ir

Financial support: This work was financially supported through Research Grant No. 264 from Pasteur Institute of Iran (to S.Z.).

Authors' address: Sedigheh Zakeri, Laleh Babaeekhou, Akram Abouie Mehrizi, Maryamm Abbasi, and Navid Dinparast Djadid, Malaria and Vector Research Group (MVRG), Biotechnology Research Center (BRC), Pasteur Institute of Iran, Tehran, Iran, E-mails: zakeris@pasteur.ac.ir, lamid21@yahoo.com, abouei@gmail.com, abasi313@gmail.com and navid@pasteur.ac.ir.

Reprint requests: Sedigheh Zakeri, Malaria and Vector Research Group (MVRG), Biotechnology Research Centre (BCR), Pasteur Institute of Iran, PO Box 1316943551, Tehran, Iran, E-mails: zakeris@pasteur.ac.ir and zakeris@yahoo.com.

Save