Plasmodium vivax invasion of human erythrocytes inhibited by antibodies directed against the Duffy binding protein

PLoS Medicine

Volumn 4, Issue 12, 2007, Pages 1940-1948

  Grimberg, Brian T ^a   Udomsangpetch, Rachanee ^b   Xainli, Jia ^a   McHenry, Amy ^c   Panichakul, Tasanee ^b   Sattabongkot, Jetsumon ^d   Cui, Liwang ^e   Bockarie, Moses ^f   Chitnis, Chetan ^g   Adams, John ^h   Zimmerman, Peter A ^a   King, Christopher L ^a,i  

^a CASE WESTERN RESERVE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b MAHIDOL UNIVERSITY   (Thailand)

^c UNIVERSITY OF NOTRE DAME   (United States)

^d ARMED FORCES RESEARCH INSTITUTE OF MEDICAL SCIENCES   (Thailand)

^e PENNSYLVANIA STATE UNIVERSITY   (United States)

^f PAPUA NEW GUINEA INSTITUTE OF MEDICAL RESEARCH   (Papua New Guinea)

^g INTERNATIONAL CENTRE FOR GENETIC ENGINEERING AND BIOTECHNOLOGY   (Italy)

^h UNIVERSITY OF SOUTH FLORIDA   (United States)

ⁱ Veterans Affairs Research Service   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DUFFY BINDING PROTEIN; IMMUNOGLOBULIN G; POLYCLONAL ANTIBODY; RECOMBINANT PROTEIN; CELL SURFACE RECEPTOR; DARC PROTEIN, HUMAN; DUFFY ANTIGEN BINDING PROTEIN, PLASMODIUM; MALARIA VACCINE; PARASITE ANTIGEN; PEPTIDE FRAGMENT; PROTOZOAL PROTEIN; PROTOZOON ANTIBODY;

ANTIGEN ANTIBODY COMPLEX; ARTICLE; BLOOD SAMPLING; ENZYME LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTE; FLOW CYTOMETRY; HOST PARASITE INTERACTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE MICROSCOPY; MALARIA; NONHUMAN; PARASITE; PARASITEMIA; PLASMODIUM; PLASMODIUM VIVAX; PROTEIN EXPRESSION; ANIMAL; BLOOD; BLOOD GROUP DUFFY SYSTEM; CELL CULTURE; FLUORESCENCE MICROSCOPY; IMMUNOLOGY; MALE; METABOLISM; MYANMAR; PAPUA NEW GUINEA; PARASITOLOGY; PATHOGENICITY; PLASMODIUM VIVAX MALARIA; RABBIT; THAILAND;

ANIMALS; ANTIBODIES, PROTOZOAN; ANTIGENS, PROTOZOAN; CELLS, CULTURED; DUFFY BLOOD-GROUP SYSTEM; ENZYME-LINKED IMMUNOSORBENT ASSAY; ERYTHROCYTES; FLOW CYTOMETRY; HUMANS; MALARIA VACCINES; MALARIA, VIVAX; MALE; MICROSCOPY, FLUORESCENCE; MYANMAR; PAPUA NEW GUINEA; PEPTIDE FRAGMENTS; PLASMODIUM VIVAX; PROTOZOAN PROTEINS; RABBITS; RECEPTORS, CELL SURFACE; RECOMBINANT PROTEINS; THAILAND;

EID: 38049050264     PISSN: 15491277     EISSN: 15491676     Source Type: Journal    
DOI: 10.1371/journal.pmed.0040337     Document Type: Article

References (51)

1. Mendis K, Sina BJ, Marchesini P, Carter R (2001) The neglected burden of Plasmodium vivax malaria. Am J Trop Med Hyg 64: 97-106.
2. Adams JH, Sim BK, Dolan SA, Fang X, Kaslow DC, et al. (1992) A family of erythrocyte binding proteins of malaria parasites. Proc Natl Acad Sci U S A 89: 7085-7089.
3. Baum J, Maier AG, Good RT, Simpson KM, Cowman AF (2005) Invasion by P. falciparum merozoites suggests a hierarchy of molecular interactions. PLoS Pathog 1: e37. doi:10.1371/journal.ppat.0010037.
4. Dolan SA, Miller LH, Wellems TE (1990) Evidence for a switching mechanism in the invasion of erythrocytes by Plasmodium falciparum. J Clin Invest 86: 618-624.
5. Miller LH, Haynes JD, McAuliffe FM, Shiroishi T, Durocher JR, et al. (1977) Evidence for differences in erythrocyte surface receptors for the malarial parasites, Plasmodium falciparum and Plasmodium knowlesi. J Exp Med 146: 277-281.
6. Rayner JC, Vargas-Serrato E, Huber CS, Galinski MR, Barnwell JW (2001) A Plasmodium falciparum homologue of Plasmodium vivax reticulocyte binding protein (PvRBP1) defines a trypsin-resistant erythrocyte invasion pathway. J Exp Med 194: 1571-1581.
7. Miller LH, Mason SJ, Clyde DF, McGinniss MH (1976) The resistance factor to Plasmodium vivax in blacks. The Duffy-blood-group genotype, FyFy. N Engl J Med 295: 302-304.
8. Miller LH, Mason SJ, Dvorak JA, McGinniss MH, Rothman IK (1975) Erythrocyte receptors for (Plasmodium knowlesi) malaria: Duffy blood group determinants. Science 189: 561-563.
9. Dvorak JA, Miller LH, Whitehouse WC, Shiroishi T (1975) Invasion of erythrocytes by malaria merozoites. Science 187: 748-750.
10. Welch SG, McGregor IA, Williams K (1977) The Duffy blood group and malaria prevalence in Gambian West Africans. Trans R Soc Trop Med Hyg 71: 295-296.
11. Zimmerman PA, Woolley I, Masinde GL, Miller SM, McNamara DT, et al. (1999) Emergence of FY*A(null) in a Plasmodium vivax-endemic region of Papua New Guinea. Proc Natl Acad Sci U S A 96: 13973-13977.
12. Kasehagen LJ, Mueller I, Kiniboro B, Bockarie MJ, Reeder JC, et al. (2007) Reduced Plasmodium vivax erythrocyte infection in PNG Duffy-negative heterozygotes. PLoS ONE 2: e336. doi:10.1371/journal.pone. 0000336.
13. Chaudhuri A, Polyakova J, Zbrzezna V, Williams K, Gulati S, et al. (1993) Cloning of glycoprotein D cDNA, which encodes the major subunit of the Duffy blood group system and the receptor for the Plasmodium vivax malaria parasite. Proc Natl Acad Sci U S A 90: 10793-10797.
14. Chaudhuri A, Zbrzezna V, Polyakova J, Pogo AO, Hesselgesser J, et al. (1994) Expression of the Duffy antigen in K562 cells. Evidence that it is the human erythrocyte chemokine receptor. J Biol Chem 269: 7835-7838.
15. Neote K, Mak JY, Kolakowski LF Jr, Schall TJ (1994) Functional and biochemical analysis of the cloned Duffy antigen: identity with the red blood cell chemokine receptor. Blood 84: 44-52.
16. Horuk R, Chitnis CE, Darbonne WC, Colby TJ, Rybicki A, et al. (1993) A receptor for the malarial parasite Plasmodium vivax: the erythrocyte chemokine receptor. Science 261: 1182-1184.
17. Murphy PM (2002) International Union of Pharmacology. XXX. Update on chemokine receptor nomenclature. Pharmacol Rev 54: 227-229.
18. Adams JH, Hudson DE, Torii M, Ward GE, Wellems TE, et al. (1990) The Duffy receptor family of Plasmodium knowlesi is located within the micronemes of invasive malaria merozoites. Cell 63: 141-153.
19. Fang XD, Kaslow DC, Adams JH, Miller LH (1991) Cloning of the Plasmodium vivax Duffy receptor. Mol Biochem Parasitol 44: 125-132.
20. Haynes JD, Dalton JP, Klotz FW, McGinniss MH, Hadley TJ, et al. (1988) Receptor-like specificity of a Plasmodium knowlesi malarial protein that binds to Duffy antigen ligands on erythrocytes. J Exp Med 167: 1873-1881.
21. 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: 340-350.
22. 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: 1531-1536.
23. Singh AP, Ozwara H, Kocken CH, Puri SK, Thomas AW, et al. (2005) Targeted deletion of Plasmodium knowlesi Duffy binding protein confirms its role in junction formation during invasion. Mol Microbiol 55: 1925-1934.
24. Singh AP, Puri SK, Chitnis CE (2002) Antibodies raised against receptorbinding domain of Plasmodium knowlesi Duffy binding protein inhibit erythrocyte invasion. Mol Biochem Parasitol 121: 21-31.
25. Singh S, Pandey K, Chattopadhayay R, Yazdani SS, Lynn A, et al. (2001) Biochemical, biophysical, and functional characterization of bacterially expressed and refolded receptor binding domain of Plasmodium vivax Duffy-binding protein. J Biol Chem 276: 17111-17116.
26. Tran TM, Moreno A, Yazdani SS, Chitnis CE, Barnwell JW, et al. (2005) Detection of a Plasmodium vivax erythrocyte binding protein by flow cytometry. Cytometry A 63: 59-66.
27. Russell BM, Udomsangpetch R, Rieckmann KH, Kotecka BM, Coleman RE, et al. (2003) Simple in vitro assay for determining the sensitivity of Plasmodium vivax isolates from fresh human blood to antimalarials in areas where P. vivax is endemic. Antimicrob Agents Chemother 47: 170-173.
28. Udomsangpetch R, Somsri S, Panichakul T, Chotivanich K, Sirichaisinthop J, et al. (2007) Short-term in vitro culture of field isolates of Plasmodium vivax using umbilical cord blood. Parasitol Int 56: 65-69.
29. World Health Organization (2000) Bench aids for the diagnosis of malaria infections. Geneva: World Health Organization. 12 p.
30. McNamara DT, Kasehagen LJ, Grimberg BT, Cole-Tobian J, Collins WE, et al. (2006) Diagnosing infection levels of four human malaria parasite species by a polymerase chain reaction/ligase detection reaction fluorescent microsphere-based assay. Am J Trop Med Hyg 74: 413-421.
31. Palmer CJ, Lindo JF, Klaskala WI, Quesada JA, Kaminsky R, et al. (1998) Evaluation of the OptiMAL test for rapid diagnosis of Plasmodium vivax and Plasmodium falciparum malaria. J Clin Microbiol 36: 203-206.
32. Mehlotra RK, Kasehagen LJ, Baisor M, Lorry K, Kazura JW, et al. (2002) Malaria infections are randomly distributed in diverse holoendemic areas of Papua New Guinea. Am J Trop Med Hyg 67: 555-562.
33. Cole-Tobian JL, Cortes A, Baisor M, Kastens W, Xainli J, et al. (2002) Age-acquired immunity to a Plasmodium vivax invasion ligand, the Duffy binding protein. J Infect Dis 186: 531-539.
34. Choe H, Moore MJ, Owens CM, Wright PL, Vasilieva N, et al. (2005) Sulphated tyrosines mediate association of chemokines and Plasmodium vivax Duffy binding protein with the Duffy antigen/receptor for chemokines (DARC). Mol Microbiol 55: 1413-1422.
35. Farzan M, Mirzabekov T, Kolchinsky P, Wyatt R, Cayabyab M, et al. (1999) Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96: 667-676.
36. Hans D, Pattnaik P, Bhattacharyya A, Shakri A, Yazdani S, et al. (2005) Mapping binding residues in the Plasmodium vivax domain that binds Duffy antigen during red cell invasion. Mol Microbiol 55: 1423-1434.
37. Tournamille C, Le Van Kim C, Gane P, Blanchard D, Proudfoot AE, et al. (1997) Close association of the first and fourth extracellular domains of the Duffy antigen/receptor for chemokines by a disulfide bond is required for ligand binding. J Biol Chem 272: 16274-16280.
38. Wasniowska K, Blanchard D, Janvier D, Wang ZX, Peiper SC, et al. (1996) Identification of the Fy6 epitope recognized by two monoclonal antibodies in the N-terminal extracellular portion of the Duffy antigen receptor for chemokines. Mol Immunol 33: 917-923.
39. Nichols ME, Rubinstein P, Barnwell J, Rodriguez de Cordoba S, Rosenfield RE (1987) A new human Duffy blood group specificity defined by a murine monoclonal antibody. Immunogenetics and association with susceptibility to Plasmodium vivax. J Exp Med 166: 776-785.
40. Pasvol G, Wilson RJ, Smalley ME, Brown J (1978) Separation of viable schizont-infected red cells of Plasmodium falciparum from human blood. Ann Trop Med Parasitol 72: 87-88.
41. VanBuskirk KM, Cole-Tobian JL, Baisor M, Sevova ES, Bockarie M, et al. (2004) Antigenic drift in the ligand domain of Plasmodium vivax Duffy binding protein confers resistance to inhibitory antibodies. J Infect Dis 190: 1556-1562.
42. John CC, O'Donnell RA, Sumba PO, Moormann AM, de Koning-Ward TF, et al. (2004) Evidence that invasion-inhibitory antibodies specific for the 19-kDa fragment of merozoite surface protein-1 (MSP-1 19) 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.
43. O'Donnell RA, de Koning-Ward TF, Burt RA, Bockarie M, Reeder JC, et al. (2001) Antibodies against merozoite surface protein (MSP)-1(19) are a major component of the invasion-inhibitory response in individuals immune to malaria. J Exp Med 193: 1403-1412.
44. Egan AF, Burghaus P, Druilhe P, Holder AA, Riley EM (1999) Human antibodies to the 19kDa C-terminal fragment of Plasmodium falciparum merozoite surface protein 1 inhibit parasite growth in vitro. Parasite Immunol 21: 133-139.
45. Hodder AN, Crewther PE, Anders RF (2001) Specificity of the protective antibody response to apical membrane antigen 1. Infect Immun 69: 3286-3294.
46. Garnham PCC (1966) Malaria parasites and other haemosporidia. Oxford: Blackwell Scientific Publications. 1114 p.
47. Golenda CF, Li J, Rosenberg R (1997) Continuous in vitro propagation of the malaria parasite Plasmodium vivax. Proc Natl Acad Sci U S A 94: 6786-6791.
48. Kitchen SF (1938) The infection of reticulocytes by Plasmodium vivax. Am J Trop Med 18: 347-353.
49. Mons B, Collins WE, Skinner JC, van der Star W, Croon JJ, et al. (1988) Plasmodium vivax: in vitro growth and reinvasion in red blood cells of Aotus nancymai. Exp Parasitol 66: 183-188.
50. Smeijsters LJ, Zijlstra NM, Franssen FF, Overdulve JP (1996) Simple, fast, and accurate fluorometric method to determine drug susceptibility of Plasmodium falciparum in 24-well suspension cultures. Antimicrob Agents Chemother 40: 835-838.
51. Soares IS, Rodrigues MM (2002) Immunogenic properties of the Plasmodium vivax vaccine candidate MSP1(19) expressed as a secreted non-glycosylated polypeptide from Pichia pastoris. Parasitology 124: 237-246.