Beyond transcriptional silencing: Is methylcytosine a widely conserved eukaryotic DNA elimination mechanism?

BioEssays

Volumn 36, Issue 4, 2014, Pages 346-352

  Bracht, John R ^a  

^a PRINCETON UNIVERSITY   (United States)

Author keywords

Apoptosis; Epigenetics; Genome rearrangement; Methylcytosine; Oxytricha

Indexed keywords

CYTOSINE;

ARTICLE; DNA METHYLATION; EPIGENETIC REPRESSION; EUKARYOTE; GENE REARRANGEMENT; GENE SILENCING; HISTONE MODIFICATION; NONHUMAN; OXYTRICHA; STYLONYCHIA; TETRAHYMENA;

CILIOPHORA; EUKARYOTA; OXYTRICHA;

APOPTOSIS; EPIGENETICS; GENOME REARRANGEMENT; METHYLCYTOSINE; OXYTRICHA;

CILIOPHORA; CYTOSINE; DNA; DNA METHYLATION; EPIGENESIS, GENETIC; EUKARYOTIC CELLS; GENE EXPRESSION; HETEROCHROMATIN; HISTONES; OXYTRICHA; TETRAHYMENA;

EID: 84896738018     PISSN: 02659247     EISSN: 15211878     Source Type: Journal    
DOI: 10.1002/bies.201300123     Document Type: Article

References (58)

1. Bickle TA, Kruger DH. 1993. Biology of DNA restriction. Microbiol Rev 57: 434-50.
2. Law JA, Jacobsen SE. 2010. Establishing, maintaining and modifying DNA methylation patterns in plants and animals. Nat Rev Genet 11: 204-20.
3. Deaton AM, Bird A. 2011. CpG islands and the regulation of transcription. Genes Dev 25: 1010-22.
4. Bourc'his D, Bestor TH. 2004. Meiotic catastrophe and retrotransposon reactivation in male germ cells lacking Dnmt3L. Nature 431: 96-9.
5. Kato M, Miura A, Bender J, Jacobsen SE, et al. 2003. Role of CG and non-CG methylation in immobilization of transposons in Arabidopsis. Curr Biol 13: 421-6.
6. Zemach A, McDaniel IE, Silva P, Zilberman D. 2010. Genome-wide evolutionary analysis of eukaryotic DNA methylation. Science 328: 916-9.
7. Feng S, Cokus SJ, Zhang X, Chen PY, et al. 2010. Conservation and divergence of methylation patterning in plants and animals. Proc Natl Acad Sci USA 107: 8689-94.
8. Zemach A, Zilberman D. 2010. Evolution of eukaryotic DNA methylation and the pursuit of safer sex. Curr Biol 20: R780-5.
9. Coulondre C, Miller JH, Farabaugh PJ, Gilbert W. 1978. Molecular basis of base substitution hotspots in Escherichia coli. Nature 274: 775-80.
10. Parfrey LW, Lahr DJ, Knoll AH, Katz LA. 2011. Estimating the timing of early eukaryotic diversification with multigene molecular clocks. Proc Natl Acad Sci USA 108: 13624-9.
11. Bracht JR, Fang W, Goldman AD, Dolzhenko E, et al. 2013. Genomes on the edge: programmed genome instability in ciliates. Cell 152: 406-16.
12. Davis MC, Ward JG, Herrick G, Allis CD. 1992. Programmed nuclear death: apoptotic-like degradation of specific nuclei in conjugating Tetrahymena. Dev Biol 154: 419-32.
13. Liu ML, Yao MC. 2012. Role of ATG8 and autophagy in programmed nuclear degradation in Tetrahymena thermophila. Eukaryot Cell 11: 494-506.
14. Prescott DM. 2000. Genome gymnastics: unique modes of DNA evolution and processing in ciliates. Nat Rev Genet 1: 191-8.
15. Lauth MR, Spear BB, Heumann J, Prescott DM. 1976. DNA of ciliated protozoa - DNA-sequence diminution during macronuclear development of Oxytricha. Cell 7: 67-74.
16. Swart EC, Bracht JR, Magrini V, Minx P, et al. 2013. The Oxytricha trifallax macronuclear genome: a complex eukaryotic genome with 16, 000 tiny chromosomes. PLoS Biol 11: e1001473.
17. Williams K, Doak TG, Herrick G. 1993. Developmental precise excision of Oxytricha trifallax telomere-bearing elements and formation of circles closed by a copy of the flanking target duplication. EMBO J 12: 4593-601.
18. Dawson D, Buckley B, Cartinhour S, Myers R, et al. 1984. Elimination of germ-line tandemly repeated sequences from the somatic genome of the ciliate Oxytricha fallax. Chromosoma 90: 289-94.
19. Taverna SD, Coyne RS, Allis CD. 2002. Methylation of histone h3 at lysine 9 targets programmed DNA elimination in Tetrahymena. Cell 110: 701-11.
20. Liu Y, Taverna SD, Muratore TL, Shabanowitz J, et al. 2007. RNAi-dependent H3K27 methylation is required for heterochromatin formation and DNA elimination in Tetrahymena. Genes Dev 21: 1530-45.
21. Liu YF, Mochizuki K, Gorovsky MA. 2004. Histone H3 lysine 9 methylation is required for DNA elimination in developing macronuclei in Tetrahymena. Proc Natl Acad Sci USA 101: 1679-84.
22. Briggs SD, Bryk M, Strahl BD, Cheung WL, et al. 2001. Histone H3 lysine 4 methylation is mediated by Set1 and required for cell growth and rDNA silencing in Saccharomyces cerevisiae. Genes Dev 15: 3286-95.
23. Mochizuki K. 2010. DNA rearrangements directed by non-coding RNAs in ciliates. Wiley Interdiscip Rev RNA 1: 376-87.
24. Madireddi MT, Coyne RS, Smothers JF, Mickey KM, et al. 1996. Pdd1p, a novel chromodomain-containing protein, links heterochromatin assembly and DNA elimination in Tetrahymena. Cell 87: 75-84.
25. Nikiforov MA, Gorovsky MA, Allis CD. 2000. A novel chromodomain protein, pdd3p, associates with internal eliminated sequences during macronuclear development in Tetrahymena thermophila. Mol Cell Biol 20: 4128-34.
26. Coyne RS, Nikiforov MA, Smothers JF, Allis CD, et al. 1999. Parental expression of the chromodomain protein Pdd1p is required for completion of programmed DNA elimination and nuclear differentiation. Mol Cell 4: 865-72.
27. Smothers JF, Mizzen CA, Tubbert MM, Cook RG, et al. 1997. Pdd1p associates with germline-restricted chromatin and a second novel anlagen-enriched protein in developmentally programmed DNA elimination structures. Development 124: 4537-45.
28. Motl JA, Chalker DL. 2011. Zygotic expression of the double-stranded RNA binding motif protein Drb2p is required for DNA elimination in the ciliate Tetrahymena thermophila. Eukaryot Cell 10: 1648-59.
29. Verdel A, Vavasseur A, Le Gorrec M, Touat-Todeschini L. 2009. Common themes in siRNA-mediated epigenetic silencing pathways. Int J Dev Biol 53: 245-57.
30. Sienski G, Donertas D, Brennecke J. 2012. Transcriptional silencing of transposons by Piwi and maelstrom and its impact on chromatin state and gene expression. Cell 151: 964-80.
31. Klattenhoff C, Xi H, Li C, Lee S, et al. 2009. The Drosophila HP1 homolog Rhino is required for transposon silencing and piRNA production by dual-strand clusters. Cell 138: 1137-49.
32. Aravin AA, Sachidanandam R, Bourc'his D, Schaefer C, et al. 2008. A piRNA pathway primed by individual transposons is linked to de novo DNA methylation in mice. Mol Cell 31: 785-99.
33. Bracht JR, Perlman DH, Landweber LF. 2012. Cytosine methylation and hydroxymethylation mark DNA for elimination in Oxytricha trifallax. Genome Biol 13: R99.
34. Juranek S, Wieden HJ, Lipps HJ. 2003. De novo cytosine methylation in the differentiating macronucleus of the stichotrichous ciliate Stylonychia lemnae. Nucleic Acids Res 31: 1387-91.
35. Gorovsky MA, Hattman S, Pleger GL. 1973. (6 N)methyl adenine in the nuclear DNA of a eucaryote, Tetrahymena pyriformis. J Cell Biol 56: 697-701.
36. Cummings DJ, Tait A, Goddard JM. 1974. Methylated bases in DNA from Paramecium aurelia. Biochim Biophys Acta 374: 1-11.
37. Rae PM, Spear BB. 1978. Macronuclear DNA of the hypotrichous ciliate Oxytricha fallax. Proc Natl Acad Sci USA 75: 4992-6.
38. Ammermann D, Steinbruck G, Baur R, Wohlert H. 1981. Methylated bases in the DNA of the ciliate Stylonychia mytilus. Eur J Cell Biol 24: 154-6.
39. Salvini M, Durante M, Citti L, Nobili R. 1984. 5'-Methyl-cytosine in the macronuclear DNA of Blepharisma japonicum. Experientia 40: 1401-3.
40. Palacios G, Martin-Gonzalez A, Gutierrez JC. 1994. Macronuclear DNA demethylation is involved in the encystment process of the ciliate Colpoda inflata. Cell Biol Int 18: 223-8.
41. Tahiliani M, Koh KP, Shen Y, Pastor WA, et al. 2009. Conversion of 5-methylcytosine to 5-hydroxymethylcytosine in mammalian DNA by MLL partner TET1. Science 324: 930-5.
42. Shen L, Zhang Y. 2013. 5-Hydroxymethylcytosine: generation, fate, and genomic distribution. Curr Opin Cell Biol 25: 289-96.
43. Bulic A, Postberg J, Fischer A, Jonsson F, et al. 2013. A permissive chromatin structure is adopted prior to site-specific DNA demethylation of developmentally expressed genes involved in macronuclear differentiation. Epigenet Chromatin 6: 5.
44. Huang Y, Pastor WA, Shen Y, Tahiliani M, et al. 2010. The behaviour of 5-hydroxymethylcytosine in bisulfite sequencing. PLoS One 5: e8888.
45. Ng SF. 1989. Cytidine analogues and stomatogenic recovery in amicronucleate Paramecium tetraurelia and Paramecium jenningsi. J Protozool 36: 74-81.
46. Kwok FWK, Ng SF. 1989. 5-Azacytidine affects the programming of expression of the somatic nucleus of Paramecium. Development 105: 559-68.
47. Maercker C, Kortwig H, Nikiforov MA, Allis CD, et al. 1999. A nuclear protein involved in apoptotic-like DNA degradation in Stylonychia: implications for similar mechanisms in differentiating and starved cells. Mol Biol Cell 10: 3003-14.
48. Postberg J, Heyse K, Cremer M, Cremer T, et al. 2008. Spatial and temporal plasticity of chromatin during programmed DNA-reorganization in Stylonychia macronuclear development. Epigenet Chromatin 1: 3.
49. Cuozzo C, Porcellini A, Angrisano T, Morano A, et al. 2007. DNA damage, homology-directed repair, and DNA methylation. PLoS Genet 3: e110.
50. Fan W, Jin S, Tong T, Zhao H, et al. 2002. BRCA1 regulates GADD45 through its interactions with the OCT-1 and CAAT motifs. J Biol Chem 277: 8061-7.
51. Zhan Q, Chen IT, Antinore MJ, Fornace AJ, Jr. 1998. Tumor suppressor p53 can participate in transcriptional induction of the GADD45 promoter in the absence of direct DNA binding. Mol Cell Biol 18: 2768-78.
52. Lee B, Morano A, Porcellini A, Muller MT. 2012. GADD45alpha inhibition of DNMT1 dependent DNA methylation during homology directed DNA repair. Nucleic Acids Res 40: 2481-93.
53. Spruijt CG, Gnerlich F, Smits AH, Pfaffeneder T, et al. 2013. Dynamic readers for 5-(hydroxy)methylcytosine and its oxidized derivatives. Cell 152: 1146-59.
54. Ito S, Shen L, Dai Q, Wu SC, et al. 2011. Tet proteins can convert 5-methylcytosine to 5-formylcytosine and 5-carboxylcytosine. Science 333: 1300-3.
55. Lu E, Wolfe J. 2001. Lysosomal enzymes in the macronucleus of Tetrahymena during its apoptosis-like degradation. Cell Death Differ 8: 289-97.
56. Gopisetty G, Ramachandran K, Singal R. 2006. DNA methylation and apoptosis. Mol Immunol 43: 1729-40.
57. Kissil JL, Feinstein E, Cohen O, Jones PA, et al. 1997. DAP-kinase loss of expression in various carcinoma and B-cell lymphoma cell lines: possible implications for role as tumor suppressor gene. Oncogene 15: 403-7.
58. Chestnut BA, Chang Q, Price A, Lesuisse C, et al. 2011. Epigenetic regulation of motor neuron cell death through DNA methylation. J Neurosci 31: 16619-36.