Epigenetics & Chromatin | |
Parasite epigenetics and immune evasion: lessons from budding yeast | |
Krassimir Y Yankulov1  Daniel CB Jeffery1  Roxanne Oshidari1  Brandon A Wyse1  | |
[1] Department of Molecular and Cellular Biology, University of Guelph, Guelph, ON N1G 2 W1, Canada | |
关键词: Epigenetic switch; Gene silencing; Telomere position effect; Allelic exclusion; Antigenic variation; | |
Others : 805037 DOI : 10.1186/1756-8935-6-40 |
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received in 2013-08-30, accepted in 2013-11-11, 发布年份 2013 | |
【 摘 要 】
The remarkable ability of many parasites to evade host immunity is the key to their success and pervasiveness. The immune evasion is directly linked to the silencing of the members of extended families of genes that encode for major parasite antigens. At any time only one of these genes is active. Infrequent switches to other members of the gene family help the parasites elude the immune system and cause prolonged maladies. For most pathogens, the detailed mechanisms of gene silencing and switching are poorly understood. On the other hand, studies in the budding yeast Saccharomyces cerevisiae have revealed similar mechanisms of gene repression and switching and have provided significant insights into the molecular basis of these phenomena. This information is becoming increasingly relevant to the genetics of the parasites. Here we summarize recent advances in parasite epigenetics and emphasize the similarities between S. cerevisiae and pathogens such as Plasmodium, Trypanosoma, Candida, and Pneumocystis. We also outline current challenges in the control and the treatment of the diseases caused by these parasites and link them to epigenetics and the wealth of knowledge acquired from budding yeast.
【 授权许可】
2013 Wyse et al.; licensee BioMed Central Ltd.
【 预 览 】
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20140708072126839.pdf | 498KB | download | |
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Figure 1. | 108KB | Image | download |
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【 参考文献 】
- [1]Deitsch KW, Lukehart SA, Stringer JR: Common strategies for antigenic variation by bacterial, fungal and protozoan pathogens. Nat Rev Microbiol 2009, 7(7):493-503.
- [2]Filler SG: Candida-host cell receptor-ligand interactions. Curr Opin Microbiol 2006, 9(4):333-339.
- [3]Morrison LJ, Marcello L, McCulloch R: Antigenic variation in the African trypanosome: molecular mechanisms and phenotypic complexity. Cell Microbiol 2009, 11(12):1724-1734.
- [4]Vink C, Rudenko G, Seifert HS: Microbial antigenic variation mediated by homologous DNA recombination. FEMS Microbiol Rev 2011. doi: 10.1111/j.1574-6976.2011.00321.x
- [5]Cushion MT, Stringer JR: Stealth and opportunism: alternative lifestyles of species in the fungal genus Pneumocystis. Annu Rev Microbiol 2010, 64:431-452.
- [6]Jain N, Fries BC: Antigenic and phenotypic variations in fungi. Cell Microbiol 2009, 11(12):1716-1723.
- [7]Scherf A, Lopez-Rubio JJ, Riviere L: Antigenic variation in Plasmodium falciparum. Annu Rev Microbiol 2008, 62:445-470.
- [8]Scherf A, Riviere L, Lopez-Rubio JJ: SnapShot: var gene expression in the malaria parasite. Cell 2008, 134(1):190.
- [9]Kirkman LA, Deitsch KW: Antigenic variation and the generation of diversity in malaria parasites. Curr Opin Microbiol 2012, 15(4):456-462.
- [10]Mwakalinga SB, Wang CW, Bengtsson DC, Turner L, Dinko B, Lusingu JP, Arnot DE, Sutherland CJ, Theander TG, Lavstsen T: Expression of a type B RIFIN in Plasmodium falciparum merozoites and gametes. Malar J 2012, 11:429. BioMed Central Full Text
- [11]Domergue R, Castano I, De Las PA, Zupancic M, Lockatell V, Hebel JR, Johnson D, Cormack BP: Nicotinic acid limitation regulates silencing of Candida adhesins during UTI. Science 2005, 308(5723):866-870.
- [12]Prucca CG, Slavin I, Quiroga R, Elias EV, Rivero FD, Saura A, Carranza PG, Lujan HD: Antigenic variation in Giardia lamblia is regulated by RNA interference. Nature 2008, 456(7223):750-754.
- [13]Prucca CG, Lujan HD: Antigenic variation in Giardia lamblia. Cell Microbiol 2009, 11(12):1706-1715.
- [14]Nash TE, Banks SM, Alling DW, Merritt JW Jr, Conrad JT: Frequency of variant antigens in Giardia lamblia. Exp Parasitol 1990, 71(4):415-421.
- [15]Ottaviani A, Gilson E, Magdinier F: Telomeric position effect: from the yeast paradigm to human pathologies? Biochimie 2008, 90(1):93-107.
- [16]Yankulov K: Dare to challenge the silence? Telomeric gene silencing revisited. Nucleus 2011, 2(6):513-516.
- [17]Rusche LN, Rine J: Switching the mechanism of mating type switching: a domesticated transposase supplants a domesticated homing endonuclease. Genes Dev 2010, 24(1):10-14.
- [18]Keely SP, Renauld H, Wakefield AE, Cushion MT, Smulian AG, Fosker N, Fraser A, Harris D, Murphy L, Price C, Quail MA, Seeger K, Sharp S, Tindal CJ, Warren T, Zuiderwijk E, Barrell BG, Stringer JR, Hall N: Gene arrays at Pneumocystis carinii telomeres. Genetics 2005, 170(4):1589-1600.
- [19]Sunkin SM, Stringer JR: Translocation of surface antigen genes to a unique telomeric expression site in Pneumocystis carinii. Mol Microbiol 1996, 19(2):283-295.
- [20]Robinson NP, Burman N, Melville SE, Barry JD: Predominance of duplicative VSG gene conversion in antigenic variation in African trypanosomes. Mol Cell Biol 1999, 19(9):5839-5846.
- [21]Figueiredo LM, Cross GA, Janzen CJ: Epigenetic regulation in African trypanosomes: a new kid on the block. Nat Rev Microbiol 2009, 7(7):504-513.
- [22]Rudenko G: Epigenetics and transcriptional control in African trypanosomes. Essays Biochem 2010, 48(1):201-219.
- [23]Hughes K, Wand M, Foulston L, Young R, Harley K, Terry S, Ersfeld K, Rudenko G: A novel ISWI is involved in VSG expression site downregulation in African trypanosomes. EMBO J 2007, 26(9):2400-2410.
- [24]Figueiredo LM, Janzen CJ, Cross GA: A histone methyltransferase modulates antigenic variation in African trypanosomes. PLoS Biol 2008, 6(7):e161.
- [25]Portugal S, Carret C, Recker M, Armitage AE, Gonçalves LA, Epiphanio S, Sullivan D, Roy C, Newbold CI, Drakesmith H, Mota MM: Host-mediated regulation of superinfection in malaria. Nat Med 2011, 17(6):732-737.
- [26]Recker M, Buckee CO, Serazin A, Kyes S, Pinches R, Christodoulou Z, Springer AL, Gupta S, Newbold CI: Antigenic variation in Plasmodium falciparum malaria involves a highly structured switching pattern. PLoS Pathog 2011, 7(3):e1001306.
- [27]Recker M, Nee S, Bull PC, Kinyanjui S, Marsh K, Newbold C, Gupta S: Transient cross-reactive immune responses can orchestrate antigenic variation in malaria. Nature 2004, 429(6991):555-558.
- [28]Scherf A, Hernandez-Rivas R, Buffet P, Bottius E, Benatar C, Pouvelle B, Gysin J, Lanzer M: Antigenic variation in malaria: in situ switching, relaxed and mutually exclusive transcription of var genes during intra-erythrocytic development in Plasmodium falciparum. EMBO J 1998, 17(18):5418-5426.
- [29]Horrocks P, Pinches R, Christodoulou Z, Kyes SA, Newbold CI: Variable var transition rates underlie antigenic variation in malaria. Proc Natl Acad Sci USA 2004, 101(30):11129-11134.
- [30]Dzikowski R, Li F, Amulic B, Eisberg A, Frank M, Patel S, Wellems TE, Deitsch KW: Mechanisms underlying mutually exclusive expression of virulence genes by malaria parasites. EMBO Rep 2007, 8(10):959-965.
- [31]Frank M, Dzikowski R, Amulic B, Deitsch K: Variable switching rates of malaria virulence genes are associated with chromosomal position. Mol Microbiol 2007, 64(6):1486-1498.
- [32]Deitsch KW, Calderwood MS, Wellems TE: Malaria: cooperative silencing elements in var genes. Nature 2001, 412(6850):875-876.
- [33]Voss TS, Healer J, Marty AJ, Duffy MF, Thompson JK, Beeson JG, Reeder JC, Crabb BS, Cowman AF: A var gene promoter controls allelic exclusion of virulence genes in Plasmodium falciparum malaria. Nature 2006, 439(7079):1004-1008.
- [34]Voss TS, Tonkin CJ, Marty AJ, Thompson JK, Healer J, Crabb BS, Cowman AF: Alterations in local chromatin environment are involved in silencing and activation of subtelomericvar genes in Plasmodium falciparum. Mol Microbiol 2007, 66(1):139-150.
- [35]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: Telomeric heterochromatin propagation and histone acetylation control mutually exclusive expression of antigenic variation genes in malaria parasites. Cell 2005, 121(1):25-36.
- [36]Lopez-Rubio JJ, Gontijo AM, Nunes MC, Issar N, Hernandez Rivas R, Scherf A: 5′ flanking region of var genes nucleate histone modification patterns linked to phenotypic inheritance of virulence traits in malaria parasites. Mol Microbiol 2007, 66(6):1296-1305.
- [37]Chookajorn T, Dzikowski R, Frank M, Li F, Jiwani AZ, Hartl DL, Deitsch KW: Epigenetic memory at malaria virulence genes. Proc Natl Acad Sci USA 2007, 104(3):899-902.
- [38]Malmquist NA, Moss TA, Mecheri S, Scherf A, Fuchter MJ: Small-molecule histone methyltransferase inhibitors display rapid antimalarial activity against all blood stage forms in Plasmodium falciparum. Proc Natl Acad Sci USA 2012, 109(41):16708-16713.
- [39]Jiang L, Mu J, Zhang Q, Ni T, Srinivasan P, Rayavara K, Yang W, Turner L, Lavstsen T, Theander TG, Peng W, Wei G, Jing Q, Wakabayashi Y, Bansal A, Luo Y, Ribeiro JM, Scherf A, Aravind L, Zhu J, Zhao K, Miller LH: PfSETvs methylation of histone H3K36 represses virulence genes in Plasmodium falciparum. Nature 2013, 499(7457):223-227.
- [40]Duraisingh MT, Voss TS, Marty AJ, Duffy MF, Good RT, Thompson JK, Freitas-Junior LH, Scherf A, Crabb BS, Cowman AF: Heterochromatin silencing and locus repositioning linked to regulation of virulence genes in Plasmodium falciparum. Cell 2005, 121(1):13-24.
- [41]Ralph SA, Scheidig-Benatar C, Scherf A: Antigenic variation in Plasmodium falciparum is associated with movement of var loci between subnuclear locations. Proc Natl Acad Sci USA 2005, 102(15):5414-5419.
- [42]Epp C, Li F, Howitt CA, Chookajorn T, Deitsch KW: Chromatin associated sense and antisense noncoding RNAs are transcribed from the var gene family of virulence genes of the malaria parasite Plasmodium falciparum. RNA 2009, 15(1):116-127.
- [43]Gunasekera AM, Patankar S, Schug J, Eisen G, Kissinger J, Roos D, Wirth DF: Widespread distribution of antisense transcripts in the Plasmodium falciparum genome. Mol Biochem Parasitol 2004, 136(1):35-42.
- [44]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: Genome-wide discovery and verification of novel structured RNAs in Plasmodium falciparum. Genome Res 2008, 18(2):281-292.
- [45]Broadbent KM, Park D, Wolf AR, Van Tyne D, Sims JS, Ribacke U, Volkman S, Duraisingh M, Wirth D, Sabeti PC, Rinn JL: A global transcriptional analysis of Plasmodium falciparum malaria reveals a novel family of telomere-associated lncRNAs. Genome Biol 2011, 12(6):R56. BioMed Central Full Text
- [46]Baum J, Papenfuss AT, Mair GR, Janse CJ, Vlachou D, Waters AP, Cowman AF, Crabb BS, de Koning-Ward TF: Molecular genetics and comparative genomics reveal RNAi is not functional in malaria parasites. Nucleic Acids Res 2009, 37(11):3788-3798.
- [47]Raabe CA, Sanchez CP, Randau G, Robeck T, Skryabin BV, Chinni SV, Kube M, Reinhardt R, Ng GH, Manickam R, Kuryshev VY, Lanzer M, Brosius J, Tang TH, Rozhdestvensky TS: A global view of the nonprotein-coding transcriptome in Plasmodium falciparum. Nucleic Acids Res 2009, 38(2):608-617.
- [48]Ralph SA, Bischoff E, Mattei D, Sismeiro O, Dillies MA, Guigon G, Coppee JY, David PH, Scherf A: Transcriptome analysis of antigenic variation in Plasmodium falciparum–var silencing is not dependent on antisense RNA. Genome Biol 2005, 6(11):R93. BioMed Central Full Text
- [49]De Las PA, Pan SJ, Castano I, Alder J, Cregg R, Cormack BP: Virulence-related surface glycoproteins in the yeast pathogen Candida glabrata are encoded in subtelomeric clusters and subject to RAP1- and SIR-dependent transcriptional silencing. Genes Dev 2003, 17(18):2245-2258.
- [50]Rosas-Hernandez LL, Juarez-Reyes A, Arroyo-Helguera OE, De Las PA, Pan SJ, Cormack BP, Castano I: yKu70/yKu80 and Rif1 regulate silencing differentially at telomeres in Candida glabrata. Eukaryot Cell 2008, 7(12):2168-2178.
- [51]Kulakova L, Singer SM, Conrad J, Nash TE: Epigenetic mechanisms are involved in the control of Giardia lamblia antigenic variation. Mol Microbiol 2006, 61(6):1533-1542.
- [52]Yankulov K: Dynamics and stability: epigenetic conversions in position effect variegation. Biochem Cell Biol 2013, 91(1):6-13.
- [53]Rusche LN, Kirchmaier AL, Rine J: The establishment, inheritance, and function of silenced chromatin in Saccharomyces cerevisiae. Annu Rev Biochem 2003, 72:481-516.
- [54]Rehman MA, Yankulov K: The dual role of autonomously replicating sequences as origins of replication and as silencers. Curr Genet 2009, 55(4):357-363.
- [55]Feuerhahn S, Iglesias N, Panza A, Porro A, Lingner J: TERRA biogenesis, turnover and implications for function. FEBS Lett 2010, 584(17):3812-3818.
- [56]Yang X, Figueiredo LM, Espinal A, Okubo E, Li B: RAP1 is essential for silencing telomeric variant surface glycoprotein genes in Trypanosoma brucei. Cell 2009, 137(1):99-109.
- [57]Alsford S, Kawahara T, Isamah C, Horn D: A sirtuin in the African trypanosome is involved in both DNA repair and telomeric gene silencing but is not required for antigenic variation. Mol Microbiol 2007, 63(3):724-736.
- [58]Tonkin CJ, Carret CK, Duraisingh MT, Voss TS, Ralph SA, Hommel M, Duffy MF, Silva LM, Scherf A, Ivens A, Speed TP, Beeson JG, Cowman AF: Sir2 paralogues cooperate to regulate virulence genes and antigenic variation in Plasmodium falciparum. PLoS Biol 2009, 7(4):e84.
- [59]Taddei A, Gasser SM: Structure and function in the budding yeast nucleus. Genetics 2012, 192(1):107-129.
- [60]Kirchmaier AL, Rine J: DNA replication-independent silencing in S. cerevisiae. Science 2001, 291(5504):646-650.
- [61]Maillet L, Gaden F, Brevet V, Fourel G, Martin SG, Dubrana K, Gasser SM, Gilson E: Ku-deficient yeast strains exhibit alternative states of silencing competence. EMBO Rep 2001, 2(3):203-210.
- [62]Fourel G, Lebrun E, Gilson E: Protosilencers as building blocks for heterochromatin. Bioessays 2002, 24(9):828-835.
- [63]Fourel G, Magdinier F, Gilson E: Insulator dynamics and the setting of chromatin domains. Bioessays 2004, 26(5):523-532.
- [64]Fourel G, Revardel E, Koering CE, Gilson E: Cohabitation of insulators and silencing elements in yeast subtelomeric regions. EMBO J 1999, 18(9):2522-2537.
- [65]Power P, Jeffery D, Rehman MA, Chatterji A, Yankulov K: Sub-telomeric core X and Y’ elements in S. cerevisiae suppress extreme variations in gene silencing. PLoS One 2011, 6(3):e17523.
- [66]Pryde FE, Louis EJ: Limitations of silencing at native yeast telomeres. EMBO J 1999, 18(9):2538-2550.
- [67]Gilson E, Geli V: How telomeres are replicated. Nat Rev Mol Cell Biol 2007, 8(10):825-838.
- [68]Smargiasso N, Gabelica V, Damblon C, Rosu F, De Pauw E, Teulade-Fichou MP, Rowe JA, Claessens A: Putative DNA G-quadruplex formation within the promoters of Plasmodium falciparum var genes. BMC Genomics 2009, 10:362. BioMed Central Full Text
- [69]Gallegos-Garcia V, Pan SJ, Juarez-Cepeda J, Ramirez-Zavaleta CY, Martin-del-Campo MB, Martinez-Jimenez V, Castano I, Cormack B, De Las PA: A novel downstream regulatory element cooperates with the silencing machinery to repress EPA1 expression in Candida glabrata. Genetics 2012, 190(4):1285-1297.
- [70]Juarez-Reyes A, Ramirez-Zavaleta CY, Medina-Sanchez L, De Las PA, Castano I: A protosilencer of subtelomeric gene expression in Candida glabrata with unique properties. Genetics 2012, 190(1):101-111.
- [71]Flueck C, Bartfai R, Niederwieser I, Witmer K, Alako BT, Moes S, Bozdech Z, Jenoe P, Stunnenberg HG, Voss TS: A major role for the Plasmodium falciparum ApiAP2 protein PfSIP2 in chromosome end biology. PLoS Pathog 2010, 6(2):e1000784.
- [72]Renauld H, Aparicio OM, Zierath PD, Billington BL, Chhablani SK, Gottschling DE: Silent domains are assembled continuously from the telomere and are defined by promoter distance and strength, and by SIR3 dosage. Genes Dev 1993, 7(7A):1133-1145.
- [73]Aparicio OM, Gottschling DE: Overcoming telomeric silencing: a trans-activator competes to establish gene expression in a cell cycle-dependent way. Genes Dev 1994, 8(10):1133-1146.
- [74]Ahmad K, Henikoff S: Modulation of a transcription factor counteracts heterochromatic gene silencing in Drosophila. Cell 2001, 104(6):839-847.
- [75]Fastman Y, Noble R, Recker M, Dzikowski R: Erasing the epigenetic memory and beginning to switch–the onset of antigenic switching of var genes in Plasmodium falciparum. PLoS One 2012, 7(3):e34168.
- [76]Ma B, Pan SJ, Domergue R, Rigby T, Whiteway M, Johnson D, Cormack BP: High-affinity transporters for NAD + precursors in Candida glabrata are regulated by Hst1 and induced in response to niacin limitation. Mol Cell Biol 2009, 29(15):4067-4079.
- [77]Meneghini MD, Wu M, Madhani HD: Conserved histone variant H2A.Z protects euchromatin from the ectopic spread of silent heterochromatin. Cell 2003, 112(5):725-736.
- [78]Hoeijmakers WA, Salcedo-Amaya AM, Smits AH, Francoijs KJ, Treeck M, Gilberger TW, Stunnenberg HG, Bartfai R: H2A.Z/H2B.Z double-variant nucleosomes inhabit the AT-rich promoter regions of the Plasmodium falciparum genome. Mol Microbiol 2013, 87(5):1061-1073.
- [79]Talbert PB, Henikoff S: Chromatin-based transcriptional punctuation. Genes Dev 2009, 23(9):1037-1041.
- [80]Siegel TN, Hekstra DR, Kemp LE, Figueiredo LM, Lowell JE, Fenyo D, Wang X, Dewell S, Cross GA: Four histone variants mark the boundaries of polycistronic transcription units in Trypanosoma brucei. Genes Dev 2009, 23(9):1063-1076.
- [81]Nguyen AT, Zhang Y: The diverse functions of Dot1 and H3K79 methylation. Genes Dev 2011, 25(13):1345-1358.
- [82]Wagner EJ, Carpenter PB: Understanding the language of Lys36 methylation at histone H3. Nat Rev Mol Cell Biol 2012, 13(2):115-126.
- [83]Schwartz L, Brown GV, Genton B, Moorthy VS: A review of malaria vaccine clinical projects based on the WHO rainbow table. Malar J 2012, 11:11. BioMed Central Full Text
- [84]La Greca F, Magez S: Vaccination against trypanosomiasis: can it be done or is the trypanosome truly the ultimate immune destroyer and escape artist? Hum Vaccin 2011, 7(11):1225-1233.
- [85]Seder RA, Chang LJ, Enama ME, Zephir KL, Sarwar UN, Gordon IJ, Holman LA, James ER, Billingsley PF, Gunasekera A, Richman A, Chakravarty S, Manoj A, Velmurugan S, Li M, Ruben AJ, Li T, Eappen AG, Stafford RE, Plummer SH, Hendel CS, Novik L, Costner PJ, Mendoza FH, Saunders JG, Nason MC, Richardson JH, Murphy J, Davidson SA, Richie TL, et al.: Protection against malaria by intravenous immunization with a nonreplicating sporozoite vaccine. Science 2013, 341(6152):1359-1365.
- [86]Prusty D, Mehra P, Srivastava S, Shivange AV, Gupta A, Roy N, Dhar SK: Nicotinamide inhibits Plasmodium falciparum Sir2 activity in vitro and parasite growth. FEMS Microbiol Lett 2008, 282(2):266-272.
- [87]Castano I, Pan SJ, Zupancic M, Hennequin C, Dujon B, Cormack BP: Telomere length control and transcriptional regulation of subtelomericadhesins in Candida glabrata. Mol Microbiol 2005, 55(4):1246-1258.
- [88]Doheny JG, Mottus R, Grigliatti TA: Telomeric position effect–a third silencing mechanism in eukaryotes. PLoS One 2008, 3(12):e3864.
- [89]Wallace JA, Orr-Weaver TL: Replication of heterochromatin: insights into mechanisms of epigenetic inheritance. Chromosoma 2005, 114(6):389-402.
- [90]Tabancay AP Jr, Forsburg SL: Eukaryotic DNA replication in a chromatin context. Curr Top Dev Biol 2006, 76:129-184.
- [91]Osborne EA, Hiraoka Y, Rine J: Symmetry, asymmetry, and kinetics of silencing establishment in Saccharomyces cerevisiae revealed by single-cell optical assays. Proc Natl Acad Sci USA 2011, 108(4):1209-1216.
- [92]Xu EY, Bi X, Holland MJ, Gottschling DE, Broach JR: Mutations in the nucleosome core enhance transcriptional silencing. Mol Cell Biol 2005, 25(5):1846-1859.
- [93]Smith CM, Haimberger ZW, Johnson CO, Wolf AJ, Gafken PR, Zhang Z, Parthun MR, Gottschling DE: Heritable chromatin structure: mapping “memory” in histones H3 and H4. Proc Natl Acad Sci USA 2002, 99(4):16454-16461.
- [94]Pillus L, Rine J: Epigenetic inheritance of transcriptional states in S. cerevisiae. Cell 1989, 59(4):637-647.
- [95]Xu EY, Zawadzki KA, Broach JR: Single-cell observations reveal intermediate transcriptional silencing states. Mol Cell 2006, 23(2):219-229.
- [96]Jeffery DC, Wyse BA, Rehman MA, Brown GW, You Z, Oshidari R, Masai H, Yankulov KY: Analysis of epigenetic stability and conversions in Saccharomyces cerevisiae reveals a novel role of CAF-I in position-effect variegation. Nucleic Acids Res 2013, 41(18):8475-8488.
- [97]Alabert C, Groth A: Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 2012, 13(3):153-167.
- [98]Coleman BI, Ribacke U, Manary M, Bei AK, Winzeler EA, Wirth DF, Duraisingh MT: Nuclear repositioning precedes promoter accessibility and is linked to the switching frequency of a Plasmodium falciparum invasion gene. Cell Host Microbe 2012, 12(6):739-750.