H2A.Z demarcates intergenic regions of the Plasmodium falciparum epigenome that are dynamically marked by H3K9ac and H3K4me3

PLoS Pathogens

Volumn 6, Issue 12, 2010, Pages

  Bártfai, Richárd ^a   Hoeijmakers, Wieteke A M ^a   Salcedo Amaya, Adriana M ^a   Smits, Arne H ^a   Janssen Megens, Eva ^a   Kaan, Anita ^a   Treeck, Moritz ^b,d   Gilberger, Tim Wolf ^b,c   Franc ̧oijs, Kees Jan ^a   Stunnenberg, Hendrik G ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^c MCMASTER UNIVERSITY   (Canada)

^d STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2A; HISTONE H2A.Z; HISTONE H3; PROTEIN H3K4ME3; PROTEIN H3K9AC; UNCLASSIFIED DRUG; HISTONE; SPACER DNA;

ARTICLE; EPIGENETICS; GENE AMPLIFICATION; GENE EXPRESSION; GENE SEQUENCE; GENOME; NONHUMAN; NUCLEOSOME; PLASMODIUM FALCIPARUM; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTOZOAL GENETICS; TROPHOZOITE; ACETYLATION; DNA SEQUENCE; ERYTHROCYTE; GENETIC VARIABILITY; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; METHODOLOGY; METHYLATION; PARASITOLOGY;

PLASMODIUM FALCIPARUM;

ACETYLATION; DNA, INTERGENIC; EPIGENOMICS; ERYTHROCYTES; GENETIC VARIATION; GENOME, PROTOZOAN; HISTONES; HUMANS; METHYLATION; PLASMODIUM FALCIPARUM; SEQUENCE ANALYSIS, DNA;

EID: 78651238244     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1001223     Document Type: Article

References (72)

1. Lasonder E, Ishihama Y, Andersen JS, Vermunt AM, Pain A, et al. (2002) Analysis of the Plasmodium falciparum proteome by high-accuracy mass spectrometry. Nature 419: 537-542.
2. 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.
3. Le Roch KG, Zhou Y, 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.
4. Otto TD, Wilinski D, Assefa S, Keane TM, Sarry LR, et al. (2010) New insights into the blood-stage transcriptome of Plasmodium falciparum using RNA-Seq. Mol Microbiol 76: 12-24.
5. Sims JS, Militello KT, Sims PA, Patel VP, Kasper JM, et al. (2009) Patterns of gene-specific and total transcriptional activity during the Plasmodium falciparum intraerythrocytic developmental cycle. Eukaryot Cell 8: 327-338.
6. Shock JL, Fischer KF, DeRisi JL (2007) Whole-genome analysis of mRNA decay in Plasmodium falciparum reveals a global lengthening of mRNA half-life during the intraerythrocytic development cycle. Genome Biol 8: R134.
7. Le Roch KG, Johnson JR, Florens L, Zhou Y, Santrosyan A, et al. (2004) Global analysis of transcript and protein levels across the Plasmodium falciparum life cycle. Genome Res 14: 2308-2318.
8. Mair GR, Braks JA, Garver LS, Wiegant JC, Hall N, et al. (2006) Regulation of sexual development of Plasmodium by translational repression. Science 313: 667-669.
9. Coleman BI, Duraisingh MT (2008) Transcriptional control and gene silencing in Plasmodium falciparum. Cell Microbiol 10: 1935-1946.
10. 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.
11. De Silva EK, Gehrke AR, Olszewski K, Leon I, Chahal JS, et al. (2008) Specific DNA-binding by apicomplexan AP2 transcription factors. Proc Natl Acad Sci U S A 105: 8393-8398.
12. Yuda M, Iwanaga S, Shigenobu S, Mair GR, Janse CJ, et al. (2009) Identification of a transcription factor in the mosquito-invasive stage of malaria parasites. Mol Microbiol 71: 1402-1414.
13. Yuda M, Iwanaga S, Shigenobu S, Kato T, Kaneko I (2010) Transcription factor AP2-Sp and its target genes in malarial sporozoites. Mol Microbiol 75: 854-863.
14. Bernstein BE, Meissner A, Lander ES (2007) The mammalian epigenome. Cell 128: 669-681.
15. Choi SW, Keyes MK, Horrocks P (2006) LC/ESI-MS demonstrates the absence of 5-methyl-29-deoxycytosine in Plasmodium falciparum genomic DNA. Mol Biochem Parasitol 150: 350-352.
16. Baum J, Papenfuss AT, Mair GR, Janse CJ, Vlachou D, et al. (2009) Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res 37: 3788-3798.
17. Epp C, Li F, Howitt CA, Chookajorn T, Deitsch KW (2008) Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum. RNA.
18. Raabe CA, Sanchez CP, Randau G, Robeck T, Skryabin BV, et al. (2010) A global view of the nonprotein-coding transcriptome in Plasmodium falciparum. Nucleic Acids Res 38: 608-617.
19. Militello KT, Patel V, Chessler AD, Fisher JK, Kasper JM, et al. (2005) RNA polymerase II synthesizes antisense RNA in Plasmodium falciparum. RNA 11: 365-370.
20. Miao J, Fan Q, Cui L, Li J (2006) The malaria parasite Plasmodium falciparum histones: organization, expression, and acetylation. Gene 369: 53-65.
21. 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.
22. Gissot M, Kim K (2008) How epigenomics contributes to the understanding of gene regulation in Toxoplasma gondii. J Biol Chem 55: 476-480.
23. Hakimi MA, Deitsch KW (2007) Epigenetics in Apicomplexa: control of gene expression during cell cycle progression, differentiation and antigenic variation. Curr Opin Microbiol 10: 357-362.
24. Salcedo-Amaya AM, van Driel MA, Alako BT, Trelle MB, van den Elzen AM, et al. (2009) Dynamic histone H3 epigenome marking during the intraerythrocytic cycle of Plasmodium falciparum. Proc Natl Acad Sci U S A 106: 9655-9660.
25. Salcedo-Amaya AM, Hoeijmakers WA, Bartfai R, Stunnenberg HG (2010) Malaria: could its unusual epigenome be the weak spot? Int J Biochem Cell Biol 42: 781-784.
26. 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.
27. 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.
28. 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.
29. Kozarewa I, Ning Z, Quail MA, Sanders MJ, Berriman M, et al. (2009) Amplification-free Illumina sequencing-library preparation facilitates improved mapping and assembly of (G+C)-biased genomes. Nat Methods 6: 291-295.
30. Ponts N, Harris EY, Prudhomme J, Wick I, Eckhardt-Ludka C, et al. (2010) Nucleosome landscape and control of transcription in the human malaria parasite. Genome Res 20: 228-238.
31. Westenberger SJ, Cui L, Dharia N, Winzeler E (2009) Genome-wide nucleosome mapping of Plasmodium falciparum reveals histone-rich coding and histone-poor intergenic regions and chromatin remodeling of core and subtelomeric genes. BMC Genomics 10: 610.
32. Zlatanova J, Thakar A (2008) H2A.Z: view from the top. Structure 16: 166-179.
33. Newlon CS, Theis JF (2002) DNA replication joins the revolution: whole-genome views of DNA replication in budding yeast. Bioessays 24: 300-304.
34. Aggarwal BD, Calvi BR (2004) Chromatin regulates origin activity in Drosophila follicle cells. Nature 430: 372-376.
35. Lucas I, Palakodeti A, Jiang Y, Young DJ, Jiang N, et al. (2007) High-throughput mapping of origins of replication in human cells. EMBO Rep 8: 770-777.
36. Unnikrishnan A, Gafken PR, Tsukiyama T (2010) Dynamic changes in histone acetylation regulate origins of DNA replication. Nat Struct Mol Biol 17: 430-437.
37. Vogelauer M, Rubbi L, Lucas I, Brewer BJ, Grunstein M (2002) Histone acetylation regulates the time of replication origin firing. Mol Cell 10: 1223-1233.
38. Burke TW, Cook JG, Asano M, Nevins JR (2001) Replication factors MCM2 and ORC1 interact with the histone acetyltransferase HBO1. J Biol Chem 276: 15397-15408.
39. Iizuka M, Stillman B (1999) Histone acetyltransferase HBO1 interacts with the ORC1 subunit of the human initiator protein. J Biol Chem 274: 23027-23034.
40. Miotto B, Struhl K (2010) HBO1 histone acetylase activity is essential for DNA replication licensing and inhibited by Geminin. Mol Cell 37: 57-66.
41. Dzikowski R, Deitsch KW (2009) Genetics of antigenic variation in Plasmodium falciparum. Curr Genet 55: 103-110.
42. Flueck C, Bartfai R, Niederwieser I, Witmer K, Alako BT, et al. (2010) A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology. PLoS Pathog 6: e1000784.
43. Chaal BK, Gupta AP, Wastuwidyaningtyas BD, Luah YH, Bozdech Z (2010) Histone deacetylases play a major role in the transcriptional regulation of the Plasmodium falciparum life cycle. PLoS Pathog 6: e1000737.
44. t Hoen PA, Ariyurek Y, Thygesen HH, Vreugdenhil E, Vossen RH, et al. (2008) Deep sequencing-based expression analysis shows major advances in robustness, resolution and inter-lab portability over five microarray platforms. Nucleic Acids Res 36: e141.
45. Quail MA, Kozarewa I, Smith F, Scally A, Stephens PJ, et al. (2008) A large genome center's improvements to the Illumina sequencing system. Nat Methods 5: 1005-1010.
46. Talbert PB, Henikoff S (2010) Histone variants-ancient wrap artists of the epigenome. Nat Rev Mol Cell Biol 11: 264-275.
47. Raisner RM, Hartley PD, Meneghini MD, Bao MZ, Liu CL, et al. (2005) Histone variant H2A.Z marks the 59 ends of both active and inactive genes in euchromatin. Cell 123: 233-248.
48. Jin C, Zang C, Wei G, Cui K, Peng W, et al. (2009) H3.3/H2A.Z double variant-containing nucleosomes mark 'nucleosome-free regions' of active promoters and other regulatory regions. Nat Genet 41: 941-945.
49. Lowell JE, Kaiser F, Janzen CJ, Cross GA (2005) Histone H2AZ dimerizes with a novel variant H2B and is enriched at repetitive DNA in Trypanosoma brucei. J Cell Sci 118: 5721-5730.
50. Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, et al. (2009) Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 23: 1063-1076.
51. Millar CB, Xu F, Zhang K, Grunstein M (2006) Acetylation of H2AZ Lys 14 is associated with genome-wide gene activity in yeast. Genes Dev 20: 711-722.
52. Bonenfant D, Coulot M, Towbin H, Schindler P, van Oostrum J (2006) Characterization of histone H2A and H2B variants and their post-translational modifications by mass spectrometry. Mol Cell Proteomics 5: 541-552.
53. Ishibashi T, Dryhurst D, Rose KL, Shabanowitz J, Hunt DF, et al. (2009) Acetylation of vertebrate H2A.Z and its effect on the structure of the nucleosome. Biochemistry 48: 5007-5017.
54. Meneghini MD, Wu M, Madhani HD (2003) Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 112: 725-736.
55. Altaf M, Auger A, Covic M, Cote J (2009) Connection between histone H2A variants and chromatin remodeling complexes. Biochem Cell Biol 87: 35-50.
56. Eirin-Lopez J, Ausio J (2007) H2A.Z-Mediated Genome-Wide Chromatin Specialization. Curr Genomics 8: 59-66.
57. Kobor MS, Venkatasubrahmanyam S, Meneghini MD, Gin JW, Jennings JL, et al.(2004) A protein complex containing the conserved Swi2/Snf2-related ATPase Swr1p deposits histone variant H2A.Z into euchromatin. PLoS Biol 2: E131.
58. Krogan NJ, Keogh MC, Datta N, Sawa C, Ryan OW, et al. (2003) A Snf2 family ATPase complex required for recruitment of the histone H2A variant Htz1. Mol Cell 12: 1565-1576.
59. Shia WJ, Li B, Workman JL (2006) SAS-mediated acetylation of histone H4 Lys 16 is required for H2A.Z incorporation at subtelomeric regions in Saccharo-myces cerevisiae. Genes Dev 20: 2507-2512.
60. Barski A, Cuddapah S, Cui K, Roh TY, Schones DE, et al. (2007) High- resolution profiling of histone methylations in the human genome. Cell 129: 823-837.
61. Sarcinella E, Zuzarte PC, Lau PN, Draker R, Cheung P (2007) Monoubiqui-tylation of H2A.Z distinguishes its association with euchromatin or facultative heterochromatin. Mol Cell Biol 27: 6457-6468.
62. Downs JA, Allard S, Jobin-Robitaille O, Javaheri A, Auger A, et al. (2004) Binding of chromatin-modifying activities to phosphorylated histone H2A at DNA damage sites. Mol Cell 16: 979-990.
63. Sun ZW, Allis CD (2002) Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature 418: 104-108.
64. Li B, Carey M, Workman JL (2007) The role of chromatin during transcription. Cell 128: 707-719.
65. Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, et al. (2005) Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122: 517-527.
66. Cui L, Fan Q, Miao J (2008) Histone lysine methyltransferases and demethylases in Plasmodium falciparum. Int J Parasitol 38: 1083-1097.
67. Jenuwein T (2001) Re-SET-ting heterochromatin by histone methyltransferases. Trends Cell Biol 11: 266-273.
68. Pinskaya M, Morillon A (2009) Histone H3 lysine 4 di-methylation: a novel mark for transcriptional fidelity? Epigenetics 4: 302-306.
69. Vermeulen M, Mulder KW, Denissov S, Pijnappel WW, van Schaik FM, et al. (2007) Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 131: 58-69.
70. Crabb BS, Rug M, Gilberger TW, Thompson JK, Triglia T, et al. (2004) Transfection of the human malaria parasite Plasmodium falciparum. Methods Mol Biol 270: 263-276.
71. Gilberger TW, Thompson JK, Reed MB, Good RT, Cowman AF (2003) The cytoplasmic domain of the Plasmodium falciparum ligand EBA-175 is essential for invasion but not protein trafficking. J Cell Biol 162: 317-327.
72. Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows- Wheeler transform. Bioinformatics 25: 1754-1760.