Recruitment of PfSET2 by RNA Polymerase II to Variant Antigen Encoding Loci Contributes to Antigenic Variation in P. falciparum

PLoS Pathogens

Volumn 10, Issue 1, 2014, Pages

  Ukaegbu, Uchechi E ^a   Kishore, Sandeep P ^a   Kwiatkowski, Dacia L ^a   Pandarinath, Chethan ^a,c   Dahan Pasternak, Noa ^b,d   Dzikowski, Ron ^b   Deitsch, Kirk W ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

^b HEBREW UNIVERSITY OF JERUSALEM   (Israel)

^c STANFORD UNIVERSITY   (United States)

^d UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ERYTHROCYTE MEMBRANE PROTEIN 1, PLASMODIUM FALCIPARUM; HISTONE LYSINE METHYLTRANSFERASE; HISTONE METHYLTRANSFERASE; MESSENGER RNA; PARASITE ANTIGEN; PROTOZOAL PROTEIN; PROTOZOAL RNA; RNA POLYMERASE II;

ANTIGENIC VARIATION; GENETIC EPIGENESIS; GENETICS; HUMAN; IMMUNOLOGY; PHYSIOLOGY; PLASMODIUM FALCIPARUM;

ANTIGENIC VARIATION; ANTIGENS, PROTOZOAN; EPIGENESIS, GENETIC; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; PLASMODIUM FALCIPARUM; PROTOZOAN PROTEINS; RNA POLYMERASE II; RNA, MESSENGER; RNA, PROTOZOAN;

EID: 84893803102     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003854     Document Type: Article

References (64)

1. Jiang L, Lopez-Barragan MJ, Jiang H, Mu J, Gaur D, et al. (2010) Epigenetic control of the variable expression of a Plasmodium falciparum receptor protein for erythrocyte invasion. Proc Natl Acad Sci U S A 107: 2224-2229.
2. Cortes A, Carret C, Kaneko O, Yim Lim BY, Ivens A, et al. (2007) Epigenetic silencing of Plasmodium falciparum genes linked to erythrocyte invasion. PLoS Pathog 3: e107.
3. Crowley VM, Rovira-Graells N, Ribas dP, Cortes A, (2011) Heterochromatin formation in bistable chromatin domains controls the epigenetic repression of clonally variant Plasmodium falciparum genes linked to erythrocyte invasion. Mol Microbiol 80: 391-406.
4. Comeaux CA, Coleman BI, Bei AK, Whitehurst N, Duraisingh MT, (2011) Functional analysis of epigenetic regulation of tandem RhopH1/clag genes reveals a role in Plasmodium falciparum growth. Mol Microbiol 80: 378-390.
5. Chookajorn T, Dzikowski R, Frank M, Li F, Jiwani AZ, et al. (2007) Epigenetic memory at malaria virulence genes. Proc Natl Acad Sci U S A 104: 899-902.
6. Lopez-Rubio JJ, Mancio-Silva L, Scherf A, (2009) Genome-wide analysis of heterochromatin associates clonally variant gene regulation with perinuclear repressive centers in malaria parasites. Cell Host Microbe 5: 179-190.
7. Lopez-Rubio JJ, Riviere L, Scherf A, (2007) Shared epigenetic mechanisms control virulence factors in protozoan parasites. Curr Opin Microbiol 10: 560-568.
8. Flueck C, Bartfai R, Volz J, Niederwieser I, Salcedo-Amaya AM, et al. (2009) Plasmodium falciparum heterochromatin protein 1 marks genomic loci linked to phenotypic variation of exported virulence factors. PLoS Pathog 5: e1000569.
9. Cui L, Fan Q, Cui L, Miao J, (2008) Histone lysine methyltransferases and demethylases in Plasmodium falciparum. Int J Parasitol 38: 1083-1097.
10. Tonkin CJ, Carret CK, Duraisingh MT, Voss TS, Ralph SA, et al. (2009) Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 7: e84.
11. Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, et al. (2005) Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium faiciparum. Cell 121: 13-24.
12. Suganuma T, Workman JL, (2011) Signals and combinatorial functions of histone modifications. Annu Rev Biochem 80: 473-499.
13. Suganuma T, Workman JL, (2008) Crosstalk among Histone Modifications. Cell 135: 604-607.
14. Wagner EJ, Carpenter PB, (2012) Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 13: 115-126.
15. Klose RJ, Kallin EM, Zhang Y, (2006) JmjC-domain-containing proteins and histone demethylation. Nat Rev Genet 7: 715-727.
16. Sun XJ, Wei J, Wu XY, Hu M, Wang L, et al. (2005) Identification and characterization of a novel human histone H3 lysine 36-specific methyltransferase. J Biol Chem 280: 35261-35271.
17. Kizer KO, Phatnani HP, Shibata Y, Hall H, Greenleaf AL, et al. (2005) A novel domain in Set2 mediates RNA polymerase II interaction and couples histone H3 K36 methylation with transcript elongation. Mol Cell Biol 25: 3305-3316.
18. Li B, Howe L, Anderson S, Yates JR III, Workman JL, (2003) The Set2 histone methyltransferase functions through the phosphorylated carboxyl-terminal domain of RNA polymerase II. J Biol Chem 278: 8897-8903.
19. Xiao T, Hall H, Kizer KO, Shibata Y, Hall MC, et al. (2003) Phosphorylation of RNA polymerase II CTD regulates H3 methylation in yeast. Genes Dev 17: 654-663.
20. Cheung V, Chua G, Batada NN, Landry CR, Michnick SW, et al. (2008) Chromatin- and transcription-related factors repress transcription from within coding regions throughout the Saccharomyces cerevisiae genome. PLoS Biol 6: e277.
21. Li B, Jackson J, Simon MD, Fleharty B, Gogol M, et al. (2009) Histone H3 lysine 36 dimethylation (H3K36me2) is sufficient to recruit the Rpd3s histone deacetylase complex and to repress spurious transcription. J Biol Chem 284: 7970-7976.
22. Jiang L, Mu J, Zhang Q, Ni T, Srinivasan P, et al. (2013) PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 499: 223-227.
23. Kishore SP, Perkins SL, Templeton TJ, Deitsch KW, (2009) An unusual recent expansion of the C-terminal domain of RNA polymerase II in primate malaria parasites features a motif otherwise found only in mammalian polymerases. J Mol Evol 68: 706-714.
24. Cunningham D, Fonager J, Jarra W, Carret C, Preiser P, et al. (2009) Rapid changes in transcription profiles of the Plasmodium yoelii yir multigene family in clonal populations: lack of epigenetic memory? PLoS ONE 4: e4285.
25. Scherf A, Lopez-Rubio JJ, Riviere L, (2008) Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 62: 445-470.
26. Shechter D, Dormann HL, Allis CD, Hake SB, (2007) Extraction, purification and analysis of histones. Nat Protoc 2: 1445-1457.
27. Epp C, Li F, Howitt CA, Chookajorn T, Deitsch KW, (2009) 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.
28. 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.
29. 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.
30. Nkrumah LJ, Muhle RA, Moura PA, Ghosh P, Hatfull GF, et al. (2006) Efficient site-specific integration in Plasmodium falciparum chromosomes mediated by mycobacteriophage Bxb1 integrase. Nat Methods 3: 615-621.
31. Salanti A, Staalsoe T, Lavstsen T, Jensen ATR, Sowa MPK, et al. (2003) Selective upregulation of a single distinctly structured var gene in chondroitin sulphate A-adhering Plasmodium falciparum involved in pregnancy-associated malaria. Molecular Microbiology 49: 179-191.
32. Dzikowski R, Templeton TJ, Deitsch K, (2006) Variant antigen gene expression in malaria. Cell Microbiol 8: 1371-1381.
33. Hampsey M, Reinberg D, (2003) Tails of intrigue: phosphorylation of RNA polymerase II mediates histone methylation. Cell 113: 429-432.
34. Bischoff E, Vaquero C, (2010) In silico and biological survey of transcription-associated proteins implicated in the transcriptional machinery during the erythrocytic development of Plasmodium falciparum. BMC Genomics 11: 34.
35. Issar N, Ralph SA, Mancio-Silva L, Keeling C, Scherf A, (2009) Differential sub-nuclear localisation of repressive and activating histone methyl modifications in P. falciparum. Microbes Infect 11: 403-407.
36. Trelle MB, Salcedo-Amaya AM, Cohen AM, Stunnenberg HG, Jensen ON, (2009) Global histone analysis by mass spectrometry reveals a high content of acetylated lysine residues in the malaria parasite Plasmodium falciparum. J Proteome Res 8: 3439-3450.
37. Cui L, Miao J, (2010) Chromatin-mediated epigenetic regulation in the malaria parasite Plasmodium falciparum. Eukaryot Cell 9: 1138-1149.
38. Kishore SP, Stiller JW, Deitsch KW, (2013) Horizontal gene transfer of epigenetic machinery and evolution of parasitism in the malaria parasite Plasmodium falciparum and other apicomplexans. BMC Evol Biol 13: 37.
39. Vojnic E, Simon B, Strahl BD, Sattler M, Cramer P, (2006) Structure and carboxyl-terminal domain (CTD) binding of the Set2 SRI domain that couples histone H3 Lys36 methylation to transcription. J Biol Chem 281: 13-15.
40. Chapman RD, Heidemann M, Hintermair C, Eick D, (2008) Molecular evolution of the RNA polymerase II CTD. Trends Genet 24: 289-296.
41. Egloff S, Dienstbier M, Murphy S, (2012) Updating the RNA polymerase CTD code: adding gene-specific layers. Trends Genet 28: 333-341.
42. Le Roch KG, Zhou YY, Blair PL, Grainger M, Moch JK, et al. (2003) Discovery of gene function by expression profiling of the malaria parasite life cycle. Science 301: 1503-1508.
43. Bozdech Z, Llinas M, Pulliam BL, Wong ED, Zhu J, et al. (2003) The transcriptome of the intraerythrocytic developmental cycle of Plasmodium falciparum. PLoS Biol 1: E5.
44. Kyes S, Christodoulou Z, Pinches R, Kriek N, Horrocks P, et al. (2007) Plasmodium falciparum var gene expression is developmentally controlled at the level of RNA polymerase II-mediated transcription initiation. Mol Microbiol 63: 1237-1247.
45. Baruch DI, Pasloske BL, Singh HB, Bi X, Ma XC, et al. (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.
46. Smith JD, Chitnis CE, Craig AG, Roberts DJ, Hudson-Taylor DE, et al. (1995) Switches in expression of Plasmodium falciparum var genes correlate with changes in antigenic and cytoadherent phenotypes of infected erythrocytes. Cell 82: 101-110.
47. Su X, Heatwole VM, Wertheimer SP, Guinet F, Herrfeldt JV, et al. (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.
48. Enderes C, Kombila D, Dal Bianco M, Dzikowski R, Kremsner P, et al. (2011) Var Gene promoter activation in clonal Plasmodium falciparum isolates follows a hierarchy and suggests a conserved switching program that is independent of genetic background. J Infect Dis 204: 1620-1631.
49. Fastman Y, Noble R, Recker M, Dzikowski R, (2012) Erasing the epigenetic memory and beginning to switch-the onset of antigenic switching of var genes in Plasmodium falciparum. PLoS ONE 7: e34168.
50. Epp C, Raskolnikov D, Deitsch KW, (2008) A regulatable transgene expression system for cultured Plasmodium falciparum parasites. Malar J 7: 86.
51. 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.
52. Bancells C, Deitsch KW, (2013) A molecular switch in the efficiency of translation reinitiation controls expression of var2csa, a gene implicated in pregnancy associated malaria. Mol Microbiol [epub ahead of print].
53. Frank M, Dzikowski R, Constantini D, Amulic B, Burdougo E, et al. (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.
54. Dzikowski R, Li F, Amulic B, Eisberg A, Frank M, et al. (2007) Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep 8: 959-965.
55. 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.
56. 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. Journal of Biological Chemistry 278: 34125-34132.
57. Gannoun-Zaki L, Jost A, Mu JB, Deitsch KW, Wellems TE, (2005) A silenced Plasmodium falciparum var promoter can be activated in vivo through spontaneous deletion of a silencing element in the intron. Eukaryotic Cell 4: 490-492.
58. Gudipati RK, Villa T, Boulay J, Libri D, (2008) Phosphorylation of the RNA polymerase II C-terminal domain dictates transcription termination choice. Nat Struct Mol Biol 15: 786-794.
59. Broadbent KM, Park D, Wolf AR, Van Tyne D, Sims JS, et al. (2011) A global transcriptional analysis of Plasmodium falciparum malaria reveals a novel family of telomere-associated lncRNAs. Genome Biol 12: R56.
60. Sierra-Miranda M, Delgadillo DM, Mancio-Silva L, Vargas M, Villegas-Sepulveda N, et al. (2012) Two long non-coding RNAs generated from subtelomeric regions accumulate in a novel perinuclear compartment in Plasmodium falciparum. Mol Biochem Parasitol 185: 36-47.
61. Kyes SA, Christodoulou Z, Raza A, Horrocks P, Pinches R, et al. (2003) A well-conserved Plasmodium falciparum var gene shows an unusual stage-specific transcript pattern. Molecular Microbiology 48: 1339-1348.
62. Swamy L, Amulic B, Deitsch KW, (2011) Plasmodium falciparum var gene silencing is determined by cis DNA elements that form stable and heritable interactions. Eukaryot Cell 10: 530-539.
63. Avraham I, Schreier J, Dzikowski R, (2012) Insulator-like pairing elements regulate silencing and mutually exclusive expression in the malaria parasite Plasmodium falciparum. Proc Natl Acad Sci U S A 109: E3678-E3686.
64. Mok BW, Ribacke U, Rasti N, Kironde F, Chen Q, et al. (2008) Default Pathway of var2csa switching and translational repression in Plasmodium falciparum. PLoS ONE 3: e1982.