Genetics of antigenic variation in Plasmodium falciparum

Current Genetics

Volumn 55, Issue 2, 2009, Pages 103-110

  Dzikowski, Ron ^a   Deitsch, Kirk W ^b  

^a HEBREW UNIVERSITY   (Israel)

^b WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Chromatin; Epigenetic memory; Gene regulation; Malaria; Nuclear organization; Transcription

Indexed keywords

HISTONE H3; PROTEIN VAR; PROTEIN VAR1CSA; PROTEIN VAR2CSA; PROTOZOAL DNA; PROTOZOAL PROTEIN; PROTOZOAL RNA; RNA POLYMERASE II; UNCLASSIFIED DRUG; UNTRANSLATED RNA;

ANTIGEN RECOGNITION; ANTIGENIC VARIATION; CELLULAR DISTRIBUTION; DNA SEQUENCE; EPIGENETICS; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE SILENCING; GENE STRUCTURE; GENETIC ASSOCIATION; HUMAN; IMMUNOLOGICAL MEMORY; INTRANUCLEAR SPACE; MALARIA; NONHUMAN; PLASMODIUM FALCIPARUM; PRIORITY JOURNAL; PROTOZOAL GENETICS; REGULATORY SEQUENCE; REVIEW; RNA TRANSCRIPTION; TRANSCRIPTION REGULATION;

ANIMALS; ANTIGENIC VARIATION; ANTIGENS, PROTOZOAN; CELL NUCLEUS; EPIGENESIS, GENETIC; HOST-PARASITE INTERACTIONS; HUMANS; MALARIA, FALCIPARUM; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; REGULATORY ELEMENTS, TRANSCRIPTIONAL;

PLASMODIUM FALCIPARUM; PROTOZOA;

EID: 67349177230     PISSN: 01728083     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00294-009-0233-2     Document Type: Review

References (65)

1. Amulic B, Salanti A, Lavstsen T, Nielsen MA, Deitsch KW (2009) An upstream open reading frame controls translation of var2csa, a gene implicated in placental malaria. PLoS Pathog 5:e1000256
2. Andersen AA, Panning B (2003) Epigenetic gene regulation by noncoding RNAs. Curr Opin Cell Biol 15:281-289
3. Aravind L, Iyer LM, Wellems TE, Miller LH (2003) Plasmodium biology: genomic gleanings. Cell 115:771-785
4. Baruch DI (1999) Adhesive receptors on malaria-parasitized red cells. Baillieres Best Pract Res Clin Haematol 12:747-761
5. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, Feldman M, Taraschi TF, Howard RJ (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
6. Blythe JE, Yam XY, Kuss C, Bozdech Z, Holder AA, Marsh K, Langhorne J, Preiser PR (2008) Plasmodium falciparum STEVOR proteins are highly expressed in patient isolates and located in the surface membranes of infected red blood cells and the apical tips of merozoites. Infect Immun 76:3329-3336
7. Calderwood MS, Gannoun-Zaki L, Wellems TE, Deitsch KW (2003) Plasmodium falciparum var genes are regulated by two regions with separate promoters, one upstream of the coding region and a second within the intron. J Biol Chem 278:34125-34132
8. Chang SC, Tucker T, Thorogood NP, Brown CJ (2006) Mechanisms of X-chromosome inactivation. Front Biosci 11:852-866
9. Chen Q, Fernandez V, Sundstrom A, Schlichtherle M, Datta S, Hagblom P, Wahlgren M (1998) Developmental selection of var gene expression in Plasmodium falciparum. Nature 394:392-395
10. Cheng Q, Cloonan N, Fischer K, Thompson J, Waine G, Lanzer M, Saul A (1998) stevor and rif are Plasmodium falciparum multicopy gene families which potentially encode variant antigens. Mol Biochem Parasitol 97:161-176
11. Chookajorn T, Dzikowski R, Frank M, Li F, Jiwani AZ, Hartl DL, Deitsch KW (2007) Epigenetic memory at malaria virulence genes. Proc Natl Acad Sci USA 104:899-902
12. Coleman BI, Duraisingh MT (2008) Transcriptional control and gene silencing in Plasmodium falciparum. Cell Microbiol 10:1935-1946
13. Cooke BM, Mohandas N, Coppel RL (2001) The malaria-infected red blood cell: Structural and functional changes. Adv Parasitol 50:1-86
14. Deitsch KW, Moxon ER, Wellems TE (1997) Shared themes of antigenic variation and virulence in bacterial, protozoal, and fungal infections. Microbiol Mol Biol Rev 61:281-293
15. Deitsch KW, Calderwood MS, Wellems TE (2001) Malaria. Cooperative silencing elements in var genes. Nature 412:875-876
16. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, Thompson JK, Freitas-Junior LH, Scherf A, Crabb BS, Cowman AF (2005) Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 121:13-24
17. Dzikowski R, Deitsch KW (2008) Active transcription is required for maintenance of epigenetic memory in the malaria parasite Plasmodium falciparum. J Mol Biol 382:288-297
18. Dzikowski R, Frank M, Deitsch K (2006) Mutually exclusive expression of virulence genes by malaria parasites is regulated independently of antigen production. PLoS Pathog 2:e22
19. Dzikowski R, Li F, Amulic B, Eisberg A, Frank M, Patel S, Wellems TE, Deitsch KW (2007) Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep 8:959-965
20. Eissenberg JC, Shilatifard A (2006) Leaving a mark: The many footprints of the elongating RNA polymerase II. Curr Opin Genet Dev 16:184-190
21. Epp C, Li F, Howitt CA, Chookajorn T, Deitsch KW (2008a) Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum. RNA 15:116-127
22. Epp C, Raskolnikov D, Deitsch KW (2008b) A regulatable transgene expression system for cultured Plasmodium falciparum parasites. Malar J 7:86
23. Frank M, Dzikowski R, Constantini D, Amulic B, Burdougo E, Deitsch K (2006) Strict pairing of var promoters and introns is required for var gene silencing in the malaria parasite Plasmodium falciparum. J Biol Chem 281:9942-9952
24. Frank M, Dzikowski R, Amulic B, Deitsch K (2007) Variable switching rates of malaria virulence genes are associated with chromosomal position. Mol Microbiol 64:1486-1498
25. Freitas-Junior LH, Hernandez-Rivas R, Ralph SA, Montiel-Condado D, Ruvalcaba-Salazar OK, Rojas-Meza AP, Mancio-Silva L, Leal-Silvestre RJ, Gontijo AM, Shorte S, Scherf A (2005) Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 121:25-36
26. Gardner MJ, Hall N, Fung E, White O, Berriman M, Hyman RW, Carlton JM, Pain A, Nelson KE, Bowman S, Paulsen IT, James K, Eisen JA, Rutherford K, Salzberg SL, Craig A, Kyes S, Chan MS, Nene V, Shallom SJ, Suh B, Peterson J, Angiuoli S, Pertea M, Allen J, Selengut J, Haft D, Mather MW, Vaidya AB, Martin DM, Fairlamb AH, Fraunholz MJ, Roos DS, Ralph SA, McFadden GI, Cummings LM, Subramanian GM, Mungall C, Venter JC, Carucci DJ, Hoffman SL, Newbold C, Davis RW, Fraser CM, Barrell B (2002) Genome sequence of the human malaria parasite Plasmodium falciparum. Nature 419:498-511
27. Glenister FK, Fernandez KM, Kats LM, Hanssen E, Mohandas N, Coppel RL, Cooke BM (2008) Functional alteration of red blood cells by a mega-dalton protein of Plasmodium falciparum. Blood 112:3939-3948
28. Hampsey M, Reinberg D (2003) Tails of intrigue: Phosphorylation of RNA polymerase II mediates histone methylation. Cell 113:429-432
29. Hodder AN, Maier AG, Rug M, Brown M, Hommel M, Pantic I, Puig-de-Morales-Marinkovic M, Smith B, Triglia T, Beeson J, Cowman AF (2008) Analysis of structure and function of the giant protein Pf332 in Plasmodium falciparum. Mol Microbiol 71:48-65
30. Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI (2004) Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci USA 101:11129-11134
31. Iyer JK, Amaladoss A, Genesan S, Preiser PR (2007) Variable expression of the 235 kDa rhoptry protein of Plasmodium yoelii mediate host cell adaptation and immune evasion. Mol Microbiol 65:333-346
32. Kraemer SM, Smith JD (2003) Evidence for the importance of genetic structuring to the structural and functional specialization of the Plasmodium falciparum var gene family. Mol Microbiol 50:1527-1538
33. Kyes SA, Rowe JA, Kriek N, Newbold CI (1999) Rifins: A second family of clonally variant proteins expressed on the surface of red cells infected with Plasmodium falciparum. Proc Natl Acad Sci USA 96:9333-9338
34. Kyes S, Horrocks P, Newbold C (2001) Antigenic variation at the infected red cell surface in malaria. Annu Rev Microbiol 55:673-707
35. Kyes SA, Christodoulou Z, Raza A, Horrocks P, Pinches R, Rowe JA, Newbold CI (2003) A well-conserved Plasmodium falciparum var gene shows an unusual stage-specific transcript pattern. Mol Microbiol 48:1339-1348
36. Kyes SA, Kraemer SM, Smith JD (2007) Antigenic variation in Plasmodium falciparum: Gene organization and regulation of the var multigene family. Eukaryot Cell 6:1511-1520
37. Lavazec C, Sanyal S, Templeton TJ (2007) Expression switching in the stevor and Pfmc-2TM superfamilies in Plasmodium falciparum. Mol Microbiol 64:1621-1634
38. Lavstsen T, Salanti A, Jensen ATR, Arnot DE, Theander TG (2003) Sub-grouping of Plasmodium falciparum 3D7 var genes based on sequence analysis of coding and non-coding regions. Malar J 2:27
39. Li F, Sonbuchner L, Kyes SA, Epp C, Deitsch KW (2008) Nuclear non-coding RNAs are transcribed from the centromeres of Plasmodium falciparum and are associated with centromeric chromatin. J Biol Chem 283:5692-5698
40. Llinas M, Deitsch KW, Voss TS (2008) Plasmodium gene regulation: Far more to factor in. Trends Parasitol 24:551-556
41. Lopez-Rubio JJ, Gontijo AM, Nunes MC, Issar N, Hernandez RR, Scherf A (2007a) 5′ flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol 66:1296-1305
42. Lopez-Rubio JJ, Riviere L, Scherf A (2007b) Shared epigenetic mechanisms control virulence factors in protozoan parasites. Curr Opin Microbiol 10:560-568
43. Meller VH, Wu KH, Roman G, Kuroda MI, Davis RL (1997) roX1 RNA paints the X chromosome of male Drosophila and is regulated by the dosage compensation system. Cell 88:445-457
44. Meller VH, Gordadze PR, Park Y, Chu X, Stuckenholz C, Kelley RL, Kuroda MI (2000) Ordered assembly of roX RNAs into MSL complexes on the dosage-compensated X chromosome in Drosophila. Curr Biol 10:136-143
45. Miller LH, Good MF, Milon G (1994) Malaria pathogenesis. Science 264:1878-1883
46. Mills JP, Diez-Silva M, Quinn DJ, Dao M, Lang MJ, Tan KS, Lim CT, Milon G, David PH, Mercereau-Puijalon O, Bonnefoy S, Suresh S (2007) Effect of plasmodial RESA protein on deformability of human red blood cells harboring Plasmodium falciparum. Proc Natl Acad Sci USA 104:9213-9217
47. Mok BW, Ribacke U, Rasti N, Kironde F, Chen Q, Nilsson P, Wahlgren M (2008) Default pathway of var2csa switching and translational repression in Plasmodium falciparum. PLoS ONE 3:e1982
48. Mourier T, Carret C, Kyes S, Christodoulou Z, Gardner PP, Jeffares DC, Pinches R, Barrell B, Berriman M, Griffiths-Jones S, Ivens A, Newbold C, Pain A (2008) Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res 18:281-292
49. Navarro M, Gull K (2001) A pol I transcriptional body associated with VSG mono-allelic expression in Trypanosoma brucei. Nature 414:759-763
50. Ralph SA, Scheidig-Benatar C, Scherf A (2005) Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. Proc Natl Acad Sci USA 102:5414-5419
51. Salanti A, Staalsoe T, Lavstsen T, Jensen ATR, Sowa MPK, Arnot DE, Hviid L, Theander TG (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Mol Microbiol 49:179-191
52. Salanti A, Dahlback M, Turner L, Nielsen MA, Barfod L, Magistrado P, Jensen AT, Lavstsen T, Ofori MF, Marsh K, Hviid L, Theander TG (2004) Evidence for the involvement of VAR2CSA in pregnancy-associated malaria. J Exp Med 200:1197-1203
53. Sam-Yellowe TY, Florens L, Johnson JR, Wang T, Drazba JA, Le Roch KG, Zhou Y, Batalov S, Carucci DJ, Winzeler EA, Yates JRIII (2004) A Plasmodium gene family encoding Maurer's cleft membrane proteins: structural properties and expression profiling. Genome Res 14:1052-1059
54. Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M (1998) Antigenic variation in malaria: In situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 17:5418-5426
55. Scherf A, Lopez-Rubio JJ, Riviere L (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62:445-470
56. Sharp S, Lavstsen T, Fivelman QL, Saeed M, McRobert L, Templeton TJ, Jensen ATR, Baker DA, Theander TG, Sutherland CJ (2006) Programmed transcription of the var gene family, but not of stevor, in Plasmodium falciparum gametocytes. Eukaryot Cell 5:1206-1214
57. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, Peterson DS, Pinches R, Newbold CI, Miller LH (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82:101-110
58. Staines HM, Alkhalil A, Allen RJ, De Jonge HR, Derbyshire E, Egee S, Ginsburg H, Hill DA, Huber SM, Kirk K, Lang F, Lisk G, Oteng E, Pillai AD, Rayavara K, Rouhani S, Saliba KJ, Shen C, Solomon T, Thomas SL, Verloo P, Desai SA (2007) Electrophysiological studies of malaria parasite-infected erythrocytes: Current status. Int J Parasitol 37:475-482
59. Su X, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JV, Peterson DS, Ravetch JV, Wellems TE (1995) A large and diverse gene family (var) encodes 200-350 kD proteins implicated in the antigenic variation and cytoadherence of Plasmodium falciparum - infected erythrocytes. Cell 82:89-100
60. Trimnell AR, Kraemer SM, Mukherjee S, Phippard DJ, Janes JH, Flamoe E, Su XZ, Awadalla P, Smith JD (2006) Global genetic diversity and evolution of var genes associated with placental and severe childhood malaria. Mol Biochem Parasitol 148:169-180
61. Viebig NK, Gamain B, Scheidig C, Lepolard C, Przyborski J, Lanzer M, Gysin J, Scherf A (2005) A single member of the Plasmodium falciparum var multigene family determines cytoadhesion to the placental receptor chondroitin sulphate A. EMBO Rep 6:775-781
62. Voss TS, Thompson JK, Waterkeyn J, Felger I, Weiss N, Cowman AF, Beck HP (2000) Genomic distribution and functional characterisation of two distinct and conserved Plasmodium falciparum var gene 5′ flanking sequences. Mol Biochem Parasitol 107:103-115
63. Voss TS, Kaestli M, Vogel D, Bopp S, Beck HP (2003) Identification of nuclear proteins that interact differentially with Plasmodium falciparum var gene promoters. Mol Microbiol 48:1593-1607
64. Voss TS, Healer J, Marty AJ, Duffy MF, Thompson JK, Beeson JG, Reeder JC, Crabb BS, Cowman AF (2006) A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 439:1004-1008
65. Winter G, Chen QJ, Flick K, Kremsner P, Fernandez V, Wahlgren M (2003) The 3D7var5.2 (var(COMMON)) type var gene family is commonly expressed in non-placental Plasmodium falciparum malaria. Mol Biochem Parasitol 127:179-191