Differential expression of histone H3 genes and selective association of the variant H3.7 with a specific sequence class in Stylonychia macronuclear development

Epigenetics and Chromatin

Volumn 7, Issue 1, 2014, Pages

  Forcob, Sakeh ^a   Bulic, Aneta ^a   Jönsson, Franziska ^a   Lipps, Hans J ^a   Postberg, Jan ^a  

^a UNIVERSITY OF WITTEN HERDECKE   (Germany)

Author keywords

Chromatin; Ciliates; H3; Histone variants; Macronucleus; Micronucleus; ncRNA; Piwi; Sexual reproduction

Indexed keywords

EID: 84893677070     PISSN: None     EISSN: 17568935     Source Type: Journal    
DOI: 10.1186/1756-8935-7-4     Document Type: Article

References (36)

1. DNA methylation and methyl-CpG binding proteins: developmental requirements and function. Bogdanovic O, Veenstra GJ, Chromosoma 2009 118 5 549 565 10.1007/s00412-009-0221-9 19506892
2. DNA methylation landscapes: provocative insights from epigenomics. Suzuki MM, Bird A, Nat Rev Genet 2008 9 6 465 476 10.1038/nrg2341 18463664 (Pubitemid 351693975)
3. Regulation of chromatin by histone modifications. Bannister AJ, Kouzarides T, Cell Res 2011 21 3 381 395 10.1038/cr.2011.22 21321607
4. Chromatin modifications and their function. Kouzarides T, Cell 2007 128 4 693 705 10.1016/j.cell.2007.02.005 17320507 (Pubitemid 46273577)
5. Marking histone H3 variants: how, when and why? Loyola A, Almouzni G, Trends Biochem Sci 2007 32 9 425 433 10.1016/j.tibs.2007.08.004 17764953 (Pubitemid 47369165)
6. Histone H3 variants and their potential role in indexing mammalian genomes: the "H3 barcode hypothesis" Hake SB, Allis CD, Proc Natl Acad Sci USA 2006 103 17 6428 6435 10.1073/pnas.0600803103 16571659
7. The histone variant H3.3 marks active chromatin by replication- independent nucleosome assembly. Ahmad K, Henikoff S, Mol Cell 2002 9 6 1191 1200 10.1016/S1097-2765(02)00542-7 12086617 (Pubitemid 34722299)
8. Histone variants in metazoan development. Banaszynski LA, Allis CD, Lewis PW, Dev Cell 2010 19 5 662 674 10.1016/j.devcel.2010.10.014 21074717
9. The histone H3.3 chaperone HIRA is essential for chromatin assembly in the male pronucleus. Loppin B, Bonnefoy E, Anselme C, Laurencon A, Karr TL, Couble P, Nature 2005 437 7063 1386 1390 10.1038/nature04059 16251970 (Pubitemid 41568687)
10. The double face of the histone variant H3.3. Szenker E, Ray-Gallet D, Almouzni G, Cell Res 2011 21 3 421 434 10.1038/cr.2011.14 21263457
11. Asymmetry in histone H3 variants and lysine methylation between paternal and maternal chromatin of the early mouse zygote. van der Heijden GW, Dieker JW, Derijck AA, Muller S, Berden JH, Braat DD, van der Vlag J, de Boer P, Mech Dev 2005 122 9 1008 1022 10.1016/j.mod.2005.04.009 15922569 (Pubitemid 41080025)
12. The evolutionary history of histone H3 suggests a deep eukaryotic root of chromatin modifying mechanisms. Postberg J, Forcob S, Chang WJ, Lipps HJ, BMC Evol Biol 2010 10 259 10.1186/1471-2148-10-259 20738881
13. Deposition and function of histone H3 variants in Tetrahymena thermophila. Cui B, Liu Y, Gorovsky MA, Mol Cell Biol 2006 26 20 7719 7730 10.1128/MCB.01139-06 16908532 (Pubitemid 44547718)
14. An unusual histone H3 specific for early macronuclear development in Euplotes crassus. Jahn CL, Ling Z, Tebeau CM, Klobutcher LA, Proc Natl Acad Sci U S A 1997 94 4 1332 1337 10.1073/pnas.94.4.1332 9037053 (Pubitemid 27087851)
15. Several highly divergent histone H3 genes are present in the hypotrichous ciliate Stylonychia lemnae. Bernhard D, FEMS Microbiol Lett 1999 175 1 45 50 10.1111/j.1574-6968.1999.tb13600.x 10361708 (Pubitemid 29246052)
16. Spatial and temporal plasticity of chromatin during programmed DNA-reorganization in Stylonychia macronuclear development. Postberg J, Heyse K, Cremer M, Cremer T, Lipps HJ, Epigenetics Chromatin 2008 1 1 3 10.1186/1756-8935-1-3 19014664
17. Evolution of DNA organization in hypotrichous ciliates. Prescott DM, Ann N Y Acad Sci 1999 870 301 313 10.1111/j.1749-6632.1999.tb08892.x 10415492 (Pubitemid 29349356)
18. The development of the macronucleus in the ciliated protozoan Stylonychia mytilus. Ammermann D, Steinbruck G, Berger LV, Hennig W, Chromosoma 1974 45 4 401 429 4209692
19. The DNA of ciliated protozoa. Prescott DM, Microbiol Rev 1994 58 2 233 267 8078435
20. A PIWI homolog is one of the proteins expressed exclusively during macronuclear development in the ciliate Stylonychia lemnae. Fetzer CP, Hogan DJ, Lipps HJ, Nucleic Acids Res 2002 30 20 4380 4386 10.1093/nar/gkf579 12384584 (Pubitemid 35277248)
21. A microarray analysis of developmentally regulated genes during macronuclear differentiation in the stichotrichous ciliate Stylonychia lemnae. Paschka AG, Horejschi V, Jonsson F, Lindecke A, Weier G, Kaltschmidt C, Lipps HJ, Gene 2005 359 81 90 16150557 (Pubitemid 41341401)
22. Nongenic, bidirectional transcription precedes and may promote developmental DNA deletion in Tetrahymena thermophila. Chalker DL, Yao MC, Genes Dev 2001 15 10 1287 1298 10.1101/gad.884601 11358871 (Pubitemid 32472756)
23. Piwi-interacting RNAs protect DNA against loss during Oxytricha genome rearrangement. Fang W, Wang X, Bracht JR, Nowacki M, Landweber LF, Cell 2012 151 6 1243 1255 10.1016/j.cell.2012.10.045 23217708
24. Mating of the stichotrichous ciliate Oxytricha trifallax induces production of a class of 27 nt small RNAs derived from the parental macronucleus. Zahler AM, Neeb ZT, Lin A, Katzman S, PLoS One 2012 7 8 42371 10.1371/journal.pone.0042371 22900016
25. snRNA and heterochromatin formation are involved in DNA excision during macronuclear development in stichotrichous ciliates. Juranek SA, Rupprecht S, Postberg J, Lipps HJ, Eukaryot Cell 2005 4 11 1934 1941 10.1128/EC.4.11.1934- 1941.2005 16278460 (Pubitemid 41636885)
26. RNA-directed epigenetic regulation of DNA rearrangements. Mochizuki K, Essays Biochem 2010 48 1 89 100 10.1042/bse0480089 20822488
27. Evolution of gene scrambling in ciliate micronuclear genes. Curtis EA, Landweber LF, Ann N Y Acad Sci 1999 870 349 350 10415495 (Pubitemid 29349364)
28. Scoring residue conservation. Valdar WS, Proteins 2002 48 2 227 241 10.1002/prot.10146 12112692 (Pubitemid 34743413)
29. Nucleosome dynamics and histone variants. Ray-Gallet D, Almouzni G, Essays Biochem 2010 48 1 75 87 10.1042/bse0480075 20822487
30. Transcriptionally inactive micronuclei, macronuclear anlagen and transcriptionally active macronuclei differ in histone composition in the hypotrichous ciliate Stylonychia lemnae. Schlegel M, Muller S, Ruder F, Büsen W, Chromosoma 1990 99 401 406 10.1007/BF01726691 (Pubitemid 20338093)
31. H3K64 trimethylation marks heterochromatin and is dynamically remodeled during developmental reprogramming. Daujat S, Weiss T, Mohn F, Lange UC, Ziegler-Birling C, Zeissler U, Lappe M, Schubeler D, Torres-Padilla ME, Schneider R, Nat Struct Mol Biol 2009 16 7 777 781 10.1038/nsmb.1629 19561610
32. Regulation of histone gene expression in budding yeast. Eriksson PR, Ganguli D, Nagarajavel V, Clark DJ, Genetics 2012 191 1 7 20 10.1534/genetics.112.140145 22555441
33. A unified phylogeny-based nomenclature for histone variants. Talbert PB, Ahmad K, Almouzni G, Ausio J, Berger F, Bhalla PL, Bonner WM, Cande WZ, Chadwick BP, Chan SW, et al. Epigenetics Chromatin 2012 5 7 10.1186/1756-8935-5-7 22650316
34. The use of RNAi to analyze gene function in spirotrichous ciliates. Paschka AG, Jönsson F, Maier V, Möllenbeck M, Paeschke K, Postberg J, Rupprecht S, Lipps HJ, Eur J Protistol 2003 39 4 449 454 10.1078/0932-4739-00019 (Pubitemid 38171075)
35. A permissive chromatin structure is adopted prior to site-specific DNA demethylation of developmentally expressed genes involved in macronuclear differentiation. Bulic A, Postberg J, Fischer A, Jonsson F, Reuter G, Lipps HJ, Epigenetics Chromatin 2013 6 1 5 10.1186/1756-8935-6-5 23497475
36. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S, Mol Biol Evol 2011 28 10 2731 2739 10.1093/molbev/msr121 21546353