Small, clonally variant antigens expressed on the surface of the Plasmodium falciparum-infected erythrocyte are encoded by the rif gene family and are the target of human immune responses

Journal of Experimental Medicine

Volumn 190, Issue 10, 1999, Pages 1393-1403

  Fernandez, Victor ^a   Hommel, Marcel ^b   Chen, Qijun ^a   Hagblom, Per ^a   Wahlgren, Mats ^a,c  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LIVERPOOL SCHOOL OF TROPICAL MEDICINE   (United Kingdom)

^c KAROLINSKA INSTITUTE   (Sweden)

Author keywords

Antibodies; P. falciparum; rif gene family; Strain specific; Surface antigen

Indexed keywords

ANTISERUM; EPITOPE; MEMBRANE ANTIGEN; POLYPEPTIDE; TRYPSIN;

ANTIGEN EXPRESSION; ARTICLE; ERYTHROCYTE; IMMUNE RESPONSE; IMMUNOPRECIPITATION; MOLECULAR CLONING; MULTIGENE FAMILY; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTEIN EXPRESSION;

AMINO ACID SEQUENCE; ANIMALS; ANTIGENS, PROTOZOAN; ANTIGENS, SURFACE; ERYTHROCYTES; GENE EXPRESSION REGULATION; GENES, PROTOZOAN; HUMANS; MALARIA, FALCIPARUM; MEROZOITE SURFACE PROTEIN 1; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; PLASMODIUM FALCIPARUM;

EID: 0033571794     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.190.10.1393     Document Type: Article

References (42)

1. Miller, L.H., M.F. Good, and G. Milon. 1994. Malaria pathogenesis. Science. 264:1878-1883.
2. Baruch, D.I., B.L. Pasloske, H.B. Singh, X. Bi, X.C. Ma, M. Feldman, T.F. Taraschi, and R.J. Howard. 1995. Cloning the P. falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell. 82:77-87.
3. Smith, J.D., C.E. Chitnis, A.G. Craig, D.J. Roberts, D.E. Hudson-Taylor, D.S. Peterson, R. Pinches, C.I. Newbold, and L.H. Miller. 1995. Switches in expression of Plasmodium faldparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell. 82: 101-110.
4. Su, X., V.M. Heatwole, S.P. Werttheimer, F. Guinet, J.A. Herrfeldt, D.S. Peterson, J.A. Ravetch, and T.E. Wellems. 1995. The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell. 82:89-100.
5. Howard, R.J. 1988. Malarial proteins at the membrane of Plasmodium falciparum-infected erythrocytes and their involvement in cytoadherence to endothelial cells. Prog. Allergy. 41:98-147.
6. Forsyth, K.P., G. Philip, T. Smith, E. Kum, B. Southwell, and G.V. Brown. 1989. Diversity of antigens expressed on the surface of erythrocytes infected with mature Plasmodium falciparum parasites in Papua New Guinea. Am. J. Trop. Med. Hyg. 41:259-265.
7. Iqbal, J., P. Perlmann, and K. Berzins. 1993. Serological diversity of antigens expressed on the surface of erythrocytes infected with Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 87:583-588.
8. Barragan, A., P.G. Kremsner, W. Weiss, M. Wahlgren, and J. Carlson. 1998. Age-related buildup of humoral immunity against epitopes for rosette formation and agglutination in african areas of malaria endemicity. Infect. Immun. 66:4783-4787.
9. Marsh, K., and R.J. Howard. 1986. Antigens induced on erythrocytes by P. falciparum: expression of diverse and conserved determinants. Science. 231:150-153.
10. Newbold, C.I., R. Pinches, D.J. Roberts, and K. Marsh. 1992. Plasmodium falciparum: the human agglutinating antibody response to the infected red cell surface is predominantly variant specific. Exp. Parasitol. 75:281-292.
11. Bull, P.C., B.S. Lowe, M. Kortok, C.S. Molyneux, C.I. Newbold, and K. Marsh. 1998. Parasite antigens on the infected red cell surface are targets for naturally acquired immunity to malaria. Nat. Med. 4:358-360.
12. Bull, P.C., B.S. Lowe, M. Kortok, and K. Marsh. 1999. Antibody recognition of Plasmodium falciparum erythrocyte surface antigens in Kenya: evidence for rare and prevalent variants. Infect. Immun. 67:733-739.
13. Baruch, D.I., J.A. Gormley, C. Ma, R.J. Howard, and B.L. Pasloske. 1996. Plasmodium falciparum erythrocyte membrane protein 1 is a parasitized erythrocyte receptor for adherence to CD36, thrombospondin, and intercellular adhesion molecule 1. Proc. Natl. Acad. Sci. USA. 93:3497-3502.
14. Rowe, A., J.M. Moulds, C.I. Newbold, and L.H. Miller. 1997. P. falciparum resetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature. 388:292-295.
15. Chen, Q., A. Barragan, V. Fernandez, A. Sundström, M. Schlichtherle, A. Sahlen, J. Carlson, S. Datta, and M. Wahlgren. 1998. Identification of Plasmodium falciparum erythrocyte membrane protein 1 (PfEMP1) as the rosetting ligand of the malaria parasite P. falciparum. J. Exp. Med. 187:15-23.
16. Helmby, H., L. Cavelier, U. Petersson, and M. Wahlgren. 1993. Resetting Plasmodium falciparum-infected erythrocytes express unique strain-specific antigens on their surface. Infect. Immun. 61:284-288.
17. Stanley, H.A., and R.T. Reese. 1986. Plasmodium falciparum polypeptides associated with the infected erythrocyte plasma membrane. Proc. Natl. Acad. Sci. USA. 83:6093-6097.
18. Fernandez, V., C.J. Treutiger, G.B. Nash, and M. Wahlgren. 1998. Multiple adhesive phenotypes linked to rosetting-binding of erythrocytes in Plasmodium falciparum malaria. Infect. Immun. 66:2969-2975.
19. Aguiar, J.C., G.R. Albrecht, P. Cegielski, B.M. Greenwood, J.B. Jensen, G. Lallinger, A. Martinez, I.A. McGregor, J.N. Minjas, J. Neequaye, et al. 1992. Agglutination of Plasmodium falciparum-infected erythrocytes from east and west African isolates by human sera from distant geographic regions. Am. J. Trop. Med. Hyg. 47:621-632.
20. Carlson, J., G. Holmquist, D.W. Taylor, P. Perlmann, and M. Wahlgren. 1990. Antibodies to a histidine-rich protein (PfHRP1) disrupt spontaneously formed Plasmodium falciparum erythrocyte rosettes. Proc. Natl. Acad. Sci. USA. 87: 2511-2515.
21. Magowan, C., W. Wollish, L. Anderson, and J. Leech. 1988. Cytoadherence by Plasmodium falciparum-infected erythrocytes is correlated with the expression of a family of variable proteins on infected erythrocytes. J. Exp. Med. 168:1307-1320.
22. Scholander, C., C.J. Treutiger, K. Hultenby, and M. Wahlgren. 1996. Novel fibrillar structure confers adhesive property to malaria-infected erythrocytes. Nat. Med. 2:204-208.
23. Weber, J.L. 1988. Interspersed repetitive DNA from Plasmodium falciparum. Mol. Biochem. Parasitol. 29:117-124.
24. Gardner, M.J., H. Tettelin, D.J. Carucci, L.M. Cummings, L. Aravind, E.V. Koonin, S. Shallom, T. Mason, K. Yu, C. Fujii, et al. 1998. Chromosome 2 sequence of the human malaria parasite Plasmodium falciparum. Science. 282:1126-1132.
25. Howard, R.J., J.W. Barnwell, V. Kao, W.A. Daniel, and S.B. Aley. 1982. Radioiodination of new protein antigens on the surface of Plasmodium knowlesi schizont-infected erythrocytes. Mol. Biochem. Parasitol. 6:343-367.
26. Cheng, Q., N. Cloonan, K. Fischer, J. Thompson, G. Wayne, M. Lanzer, and A. Saul. 1998. stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol. Biochem. Parasitol. 97:161-176.
27. Biggs, B.-A., L. Gooze, K. Wycherley, W. Wollish, B. Southwell, J.H. Leech, and G.V. Brown. 1991. Antigenic variation in Plasmodium falciparum. Proc. Natl. Acad. Sci. USA. 88:9171-9174.
28. Roberts, D.J., A.G. Craig, A.R. Berendt, R. Pinches, G. Nash, K. Marsh, and C.I. Newbold. 1992. Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature. 357:689-692.
29. Thaithong, S., G.H. Beale, B. Fenton, J. McBride, V. Rosario, A. Walker, and D. Walliker. 1984. Clonal diversity in a single isolate of the malaria parasite Plasmodium falciparum. Trans. R. Soc. Trop. Med. Hyg. 78:242-245.
30. Conway, D.J., B.M. Greenwood, and J.S. McBride. 1991. The epidemiology of multiple-clone Plasmodium falciparum infections in Gambian patients. Parasitology. 103:1-6.
31. Cher, Q., V. Fernandez, A. Sundström, M. Schlichtherle, S. Data, P. Hagblom, and M. Wahlgren. 1998. Developmental selection of var gene expression in Plasmodium falciparum. Nature. 394:392-395.
32. Stimson, E., M. Virji, K. Makepeace, A. Dell, H.R. Morris, G. Payne, J.R. Saunders, M.P. Jennings, S. Barker, and M. Panico. 1995. Meningococcal pilin: a protein substituted with digalactosyl 2,4-diacetoamido-2,4,6-trideoxyhexose. Mol. Microbiol. 17:1201-1214.
33. Stimson, E., M. Virji, S. Barker, M. Panico, I. Blench, J.R. Saunders, G. Payne, E.R. Moxon, A. Dell, and H.R. Morris. 1996. Discovery of a novel protein modification: alpha-glycerophosphate is a substitute of meningococcal pilin. Biochem. J. 316:29-33.
34. Papanastasiou, P., M.J. McConville, J. Ralton, and P. Kohler. 1997. The variant-specific surface protein of Giardia, VSP4A1, is a glycosylated and palmitoylated protein. Biochem. J. 322:49-56.
35. Langreth, S.G., and E. Peterson. 1985. Pathogenicity, stability, and immunogenicity of a knobless clone of Plasmodium falciparum in Colombian owl monkeys. Infect. Immun. 47: 760-766.
36. Shirley, M.W., B.-A. Biggs, K.P. Forsyth, H.J. Brown, J.K. Thompson, G.V. Brown, and D.J. Kemp. 1990. Chromosome 9 from independent clones and isolates of Plasmodium falciparum undergoes subtelomeric deletions with similar breakpoints in vitro. Mol. Biochem. Parasitol. 40:137-145.
37. Scherf, A., R. Carter, C. Petersen, P. Alano, R. Nelson, M. Aikawa, D. Mattei, L. Pereira da Silva, and J. Leech. 1992. Gene inactivation of Pf11-1 of Plasmodium falciparum by chromosome breakage and healing: identification of a gametocyte-specific protein with a potential role in gametocytogenesis. EMBO (Eur. Mol. Biol. Organ.) J. 11:2293-2301.
38. Day, K.P., F. Karamalis, J. Thompson, D.A. Barnes, C. Peterson, H. Brown, G.V. Brown, and D.J. Kemp. 1993. Genes necessary for expression of a virulence determinant and for transmission of Plasmodium falciparum are located on a 0.3-megabase region of chromosome 9. Proc. Natl. Acad. Sci. USA. 90:8292-8296.
39. Treutiger, C.J., A. Heddini, V. Fernandez, W.A. Muller, and M. Wahlgren. 1997. PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nat. Med. 3:1405-1408.
40. van Schravendijk, M.R., E.P. Rock, K. Marsh, Y. Ito, M. Aikawa, J. Neequaye, D. Ofori-Adjei, R. Rodriguez, M.E. Patarroyo, and R.J. Howard. 1991. Characterization and localization of Plasmodium falciparum surface antigens on infected erythrocytes from west African patients. Blood. 78: 226-236.
41. Marsh, K., L. Otoo, R.J. Hayes, D.C. Carson, and B.M. Greenwood. 1989. Antibodies to blood stage antigens of Plasmodium falciparum in rural Gambians and their relation to protection against infection. Trans. R. Soc. Trop. Med. Hyg. 83:293-303.
42. O'Farrell, P.H. 1975. High resolution two dimensional electrophoresis of proteins. J. Biol. Chem. 250:4007-4021.