Antigenic variation in malaria: In situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum

EMBO Journal

Volumn 17, Issue 18, 1998, Pages 5418-5426

  Scherf, A ^c   Hernandez Rivas, R ^c   Buffet, P ^c   Bottius, E ^c   Benatar, C ^c   Pouvelle, B ^a   Gysin, J ^a   Lanzer, M ^b  

^a TIMONE HOSPITAL   (France)

^b UNIVERSITY OF WÜRZBURG   (Germany)

^c INSTITUT PASTEUR   (France)

Author keywords

Allelic exclusion; Antigenic variation; In situ activation; Silencing; var genes

Indexed keywords

ANTIGENIC VARIATION; ARTICLE; GENE CONTROL; GENE EXPRESSION; GENE SWITCHING; GENETIC TRANSCRIPTION; MALARIA; MULTIGENE FAMILY; NONHUMAN; PATHOGENICITY; PHENOTYPE; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; TROPHOZOITE;

ADP-RIBOSYL CYCLASE; AMINO ACID SEQUENCE; ANIMALS; ANTIGENIC VARIATION; ANTIGENS, CD; ANTIGENS, CD38; ANTIGENS, DIFFERENTIATION; BRAIN; CELL ADHESION; CELL LINE; CHO CELLS; CHONDROITIN SULFATES; CRICETINAE; ENDOTHELIUM; ERYTHROCYTES; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENES, PROTOZOAN; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MEMBRANE GLYCOPROTEINS; MOLECULAR SEQUENCE DATA; NAD+ NUCLEOSIDASE; PLASMODIUM FALCIPARUM; RNA, MESSENGER; RNA, PROTOZOAN; SAIMIRI; TRANSCRIPTION, GENETIC;

PLASMODIUM FALCIPARUM;

EID: 0032530397     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.18.5418     Document Type: Article

References (51)

1. Ausubel, F., Brent, R., Kingston, R., Moore, D., Seidman, J., Smith, J. and Struhl, K. (1998) Current Protocols in Molecular Biology. John Wiley and Sons, Inc., New York, NY.
2. Baruch, D.I., Pasloske, B.L., Singh, H.B., Bi, X., Ma, X.C., Feldman, M., Taraschi, T.F. and Howard, R.J. (1995) Cloning of P.falciparum gene encoding PfEMP1, a malarial variant antigen and adherence receptor on the surface of parasitized human erythrocytes. Cell, 82, 77-87.
3. Baruch, D.I., Gormely, J.A., Ma, C., Howard, R.J. and Pasloske, B.L. (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.
4. Baruch, D.I., Ma, X.C. Singh, H.B., Bi, X., Pasloske, B.L. and Howard, R.J. (1997) Identification of a region of PfEMP1 that mediates adherence of Plasmodium falciparum infected erythrocytes to CD36: conserved function with variant sequence. Blood, 90, 3766-3775.
5. Berendt, A.R., Simmons, D.L., Tansey, J., Newbold, C.I. and Marsh, K. (1989) Intercellular adhesion molecule-1 is an endothelial cell adhesion receptor for Plasmodium falciparum. Nature, 341, 57-59.
6. Borst, P. and Greaves, D.R. (1987) Programmed gene rearrangements altering gene expression. Science, 235, 658-667.
7. Borst, P. and Rudenko, G. (1994) Antigenic variation in African trypanosomes. Science, 264, 1872-1873.
8. Borst, P., Bitter, W., McCulloch, R., Van Leeuwen, F. and Rudenko, G. (1995) Antigenic variation in malaria. Cell, 82, 1-4.
9. Carlson, J. and Wahlgren, M. (1992) Plasmodium falciparum erythrocyte rosetting is mediated by promiscuous lectin-like interactions. J. Exp. Med., 176, 1311-1317.
10. Carlson, J., Helmby, H., Hill, A.V. Brewster, D., Greenwood, B.M. and Wahlgren, M. (1990) Human cerebral malaria: association with erythrocyte rosetting and lack of anti-rosetting antibodies. Lancet, 336, 1457-1460.
11. Carlson, J., Ekre, H.P., Helmby, H., Gysin, J., Greenwood, B.M. and Wahlgren, M. (1992) Disruption of Plasmodium falciparum erythrocyte rosettes by standard heparin and heparin devoid of anticoagulant activity. Am. J. Trop. Med. Hyg., 46, 595-602.
12. Ceder, H. (1988) DNA methylation and gene activity. Cell, 53, 3-4.
13. Chen, Q., Barragan, A., Fernandez, Y. Sundstrom, A., Schlichtherle, M., Sahlen, A., Carlson, J., Datta, S. and Wahlgren, M. (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.
14. Darkin-Rattray, S.J. et al. (1996) Apicidin: a novel antiprotozoal agent that inhibits parasite histone deacetylase. Proc. Natl Acad. Sci. USA, 93, 13143-13147.
15. Deitsch, K.W., Moxon, E.R. and Wellems, T.E. (1997) Shared themes of antigenic variation and virulence in bacterial, protozoal and fungal infections. Micribiol. Mol. Biol. Rev., 61, 281-293.
16. Donelson, J.E. (1995) Mechanisms of antigenic variation in Borrelia hermsii and African trypanosomes. J. Biol. Chem., 270, 7783-7786.
17. Fernandez, V., Treutiger, C., Nash, G. and Wahlgren, M. (1998) Multiple adhesive phenotypes linked to rosetting-binding of erythrocytes in Plasmodium falciparum malaria. Infect. Immun., 66, 2969-2975.
18. Fischer, K., Horrocks, P., Preuss, M., Wiesner, J., Wunsch, S., Camargo, A.A. and Lanzer, M. (1997) Expression of var genes located within polymorphic subtelomeric domains of Plasmodium falciparum chromosomes. Mol. Cell. Biol., 17, 3679-3686.
19. Fried, M. and Duffy, P. (1996) Adherence of Plasmodium falciparum to chondroitin sulfate A in the human placenta. Science, 272, 1502-1504.
20. Gardner, J.P., Pinches, R.A., Roberts, D.J. and Newbold, C.I. (1996) Variant antigens and endothelial receptor adhesion in Plasmodium falciparum. Proc. Natl Acad. Scu. USA, 93, 3503-3508.
21. Gay, F., Robert, C., Pouvelle, B., Peyrol, S., Scherf, A. and Gysin, J. (1995) Isolation and characterization of brain microvascular endothelial cells from Saimiri monkeys. An in vitro model for sequestration of Plasmodium falciparum-infected erythrocytes. J. Immunol. Methods, 184, 15-28.
22. Gommers-Ampt, J.H., Van Leeuwen, F., de Beer, A.L., Vliegenthart, J.F., Dizdaroglu, M., Kowalak, J.A., Crain, P.F. and Borst, P. (1993) Beta-D-glucosyl-hydroxymethyluracil: a novel modified base present in the DNA of the parasitic protozoan T.brucei. Cell, 75, 1129-1136.
23. Gysin, J., Pouvelle, B., Le Tonqueze, M., Edelman, L. and Boffa, M.C. (1997) Chondroitin sulfate of thrombomodulin is an adhesion receptor for Plasmodium falciparum-infected erythrocytes. Mol. Biochem. Parasitol., 88, 267-271.
24. Hasler, T., Albrecht, G.R., Van Schravendijk, M.R., Aguiar, J.C., Morehead, K.E., Pasloske, B.L., Ma, C., Barnwell, J.W., Greenwood, B. and Howard, R.J. (1993) An improved microassay for Plasmodium falciparum cytoadherence using stable transformants of Chinese hamster ovary cells expressing CD36 or intercellular adhesion molecule-1. Am. J. Trop. Med. Hyg., 48, 332-347.
25. Hernandez-Rivas, R. and Scherf, A. (1997) Separation and mapping of chromosomes of parasitic protozoa. Mem. Inst. Oswaldo Cruz, 92, 815-819.
26. Hernandez-Rivas, R., Mattei, D., Sterkers, Y., Peterson, D.S., Wellems, T.E. and Scherf, A. (1997) Expressed var genes are found in Plasmodium falciparum subtelomeric regions. Mol. Cell. Biol., 17, 604-611.
27. Lanasley, G., Hyde, J.E., Goman, M. and Scaife, J.G. (1983) Cloning and characterisation of the rRNA genes from the human malaria parasite Plasmodium falciparum. Nucleic Acids Res., 11, 8703-8717.
28. Lanzer, M., de Bruin, D., Wertheimer, S.P. and Ravetch, J.V. (1994) Transcriptional and nucleosomal characterization of a subtelomeric gene cluster flanking a site of chromosomal rearrangements in Plasmodium falciparum. Nucleic Acids Res., 22, 4176-4182.
29. Miller, L.H., Good, M.F. and Milon, G. (1994) Malaria pathogenesis. Science, 264, 1878-1883.
30. Newbold, C. Warn, P., Black, G., Berendt, A., Craig, A., Snow, B., Msobo, M., Peshu, N. and Marsh, K. (1997) Receptor-specific adhesion and clinical disease in Plasmodium falciparum. Am. J. Trop. Med. Hyg., 57, 389-398.
31. Ockenhouse, C.F., Tandon, N.N., Magowan, C., Jamieson, G.A. and Chulay, J.D. (1989) Identification of a platelet membrane glycoprotein as a falciparum malaria sequestration receptor. Science, 243, 1469-1471.
32. Ockenhouse, C.F., Ho, M., Tandon, N.N., Van Seventer, G.A., Shaw, S., White, N.J., Jamieson, G.A., Chulay, J.D. and Webster, H.K. (1991) Molecular basis of sequestration in severe and uncomplicated Plasmodium falciparum malaria: differential adhesion of infected erythrocytes to CD36 and ICAM-1. J. Infect. Dis., 164, 163-169.
33. Ockenhouse, C.F. et al. (1992) Human vascular endothelial cell adhesion receptors for Plasmodium falciparum infected erythrocytes: roles for endothelial leukocyte adhesion molecule 1 and vascular cell adhesion molecule 1. J. Exp. Med., 176, 1183-1189.
34. Pollack, Y., Kogan, N. and Golenser, J. (1991) Plasmodium falciparum: evidence for a DNA methylation pattern. Exp. Parasitol., 72, 339-344.
35. Pouvelle, B., Meyer, P. Robert, C., Bardel, L. and Gysin, J. (1997) Chondroitin-4-sulfate impairs in vitro and in vivo cytoadherence of Plasmodium falciparum infected erythrocytes. Mol. Med., 3, 508-518.
36. Robert, C., Pouvelle, B., Meyer, P., Muanza, K., Fujioka, H., Aikawa, M., Scherf, A. and Gysin, J. (1995) Chondroitin-4-sulphate (proteoglycan), a receptor for Plasmodium falciparum-infected erythrocyte adherence on brain microvascular endothelial cells. Res. Immunol., 146, 383-393.
37. Roberts, D., Sherwood, J., Spitalnik, S., Patton, L., Howard, R., Dixit, V., Frazier, W., Miller, L. and Ginsburg, V. (1985) Thrombospondin binds faliciparum malaria parasitized erythrocytes and may mediate cytoadherence. Nature, 318, 64-66.
38. Roberts, D.J., Craig, A.G., Berendt, A.R., Pinches, R., Nash, G., Marsh, K. and Newbold, C.I. (1992) Rapid switching to multiple antigenic and adhesive phenotypes in malaria. Nature, 357, 689-692.
39. Rogerson, S.J., Chaiyaroj, S.C., Ng, K., Reeder, J.C. and Brown, G.V. (1995) Chondroitin sulfate A is a cell surface receptor for Plasmodium falciparum-infected erythrocytes. J. Exp. Med., 182, 15-20.
40. Rowe, J.A., Moulds, J.M., Newbold, C.I. and Miller, L.H. (1997) P.falciparum rosetting mediated by a parasite-variant erythrocyte membrane protein and complement-receptor 1. Nature, 388, 292-295.
41. Rubio, J.P., Thompson, J.K. and Cowman, A.F. (1996) The var genes of Plasmodium falciparum are located in the subtelomeric region of most chromosomes. EMBO J., 15, 4069-4077.
42. Scholander, C., Treutiger, C. Hultenby, K. and Wahlgren, M. (1996) Novel fibrillar structure confers adhesive property to malaria-infected erythrocytes. Nature Med., 2, 204-208.
43. Smith, J.D., Chitnis, C.E., Craig, A.G., Roberts, D.J., Hudson-Taylor, D.E., Peterson, D.S., Pinches, R., Newbold, C.I. and Miller, L.H. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell, 82, 101-110.
44. Su, X.Z., Heatwole, V.M., Wertheimer, S.P. Guinet, F., Herrfeldt, J.A., Peterson, D.S., Ravetch, J.A. and Wellems, T.E. (1995) The large diverse gene family var encodes proteins involved in cytoadherence and antigenic variation of Plasmodium falciparum-infected erythrocytes. Cell, 82, 89-100.
45. Thompson, J.K., Rubio, J.P., Caruana, S., Brockman, A., Wickham, M.E. and Cowman, A.F. (1997) The chromosomal organization of the Plasmodium falciparum var gene family is conserved. Mol. Biochem. Parasitol., 87, 49-60.
46. Trager, W. and Jensen, J.B. (1976) Human malaria parasites in continuous culture. Science, 193, 673-675.
47. Treutiger, C., Heddini, A., Fernandez, V., Muller, W.A. and Wahlgren, M. (1997) PECAM-1/CD31, an endothelial receptor for binding Plasmodium falciparum-infected erythrocytes. Nature Med., 3, 1405-1408.
48. Turner, G.D. et al. (1994) An immunohistochemical study of the pathology of fatal malaria. Evidence for widespread endothelial activation and a potential role for intercellular adhesion molecule-1 in cerebral sequestration. Am. J. Pathol., 145, 1057-1069.
49. Vanhamme, L. and Pays, E. (1995) Control of gene expression in trypanosomes. Microbiol. Rev., 59, 223-240.
50. Wellems, T.E. and Howard, R.J. (1986) Homologous genes encode two distinct histidine-rich proteins in a cloned isolate of Plasmodium falciparum. Proc. Natl Acad. Sci. USA, 83, 6065-6069.
51. Wolffe, A.P. (1996) Histone deacetylase: a regulator of transcription. Science, 272, 371-372.