Epigenetic regulation of a murine retrotransposon by a dual histone modification mark

PLoS Genetics

Volumn 6, Issue 4, 2010, Pages

  Brunmeir, Reinhard ^a   Lagger, Sabine ^a   Simboeck, Elisabeth ^a,c   Sawicka, Anna ^a   Egger, Gerda ^a   Hagelkruys, Astrid ^a   Zhang, Yu ^b,d   Matthias, Patrick ^b   Miller, Wolfgang J ^a   Seiser, Christian ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

^c CENTRE FOR GENOMIC REGULATION CRG   (Spain)

^d HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE 1; HISTONE H3; MITOGEN ACTIVATED PROTEIN KINASE; SERINE; TRICHOSTATIN A;

ACETYLATION; ANIMAL CELL; ARTICLE; CHROMATIN; DNA METHYLATION; DNA PACKAGING; ENZYME ACTIVATION; ENZYME INHIBITION; EPIGENETICS; FIBROBLAST; GENE EXPRESSION; GENE INACTIVATION; GENE SILENCING; GENOMICS; HOST; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN MODIFICATION; PROTEIN PHOSPHORYLATION; RETROPOSON; TRANSCRIPTION INITIATION; TRANSCRIPTION REGULATION; TRANSPOSON; ANIMAL; ANIMAL EMBRYO; GENE EXPRESSION REGULATION; GENETIC EPIGENESIS; GENETICS; METABOLISM; PHOSPHORYLATION;

EUKARYOTA; MURINAE;

ACETYLATION; ANIMALS; CHROMATIN; EMBRYO, MAMMALIAN; EPIGENESIS, GENETIC; GENE EXPRESSION REGULATION; HISTONE DEACETYLASES; HISTONES; MICE; PHOSPHORYLATION; RETROELEMENTS;

EID: 77952411179     PISSN: 15537390     EISSN: 15537404     Source Type: Journal    
DOI: 10.1371/journal.pgen.1000927     Document Type: Article

References (89)

1. Strahl BD, Allis CD (2000) The language of covalent histone modifications. Nature 403: 41-45.
2. Yang XJ, Seto E (2008) The Rpd3/Hda1 family of lysine deacetylases: from bacteria and yeast to mice and men. Nat Rev Mol Cell Biol 9: 206-218.
3. Wang Z, Zang C, Cui K, Schones DE, Barski A, et al. (2009) Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell 138: 1019-1031.
4. Marks P, Rifkind RA, Richon VM, Breslow R, Miller T, et al. (2001) Histone deacetylases and cancer: causes and therapies. Nat Rev Cancer 1: 194-202.
5. Shankar S, Srivastava RK (2008) Histone deacetylase inhibitors: mechanisms and clinical significance in cancer: HDAC inhibitor-induced apoptosis. Adv Exp Med Biol 615: 261-298.
6. Brunmeir R, Lagger S, Seiser C (2009) Histone deacetylase HDAC1/HDAC2- controlled embryonic development and cell differentiation. Int J Dev Biol 53: 275-289.
7. Ikegami K, Ohgane J, Tanaka S, Yagi S, Shiota K (2009) Interplay between DNA methylation, histone modification and chromatin remodeling in stem cells and during development. Int J Dev Biol 53: 203-214.
8. Lander ES, Linton LM, Birren B, Nusbaum C, Zody MC, et al. (2001) Initial sequencing and analysis of the human genome. Nature 409: 860-921.
9. Waterston RH, Lindblad-Toh K, Birney E, Rogers J, Abril JF, et al. (2002) Initial sequencing and comparative analysis of the mouse genome. Nature 420: 520-562.
10. Prak ET, Kazazian HH, Jr. (2000) Mobile elements and the human genome. Nat Rev Genet 1: 134-144.
11. Goodier JL, Kazazian HH, Jr. (2008) Retrotransposons revisited: the restraint and rehabilitation of parasites. Cell 135: 23-35.
12. Maksakova IA, Romanish MT, Gagnier L, Dunn CA, van de Lagemaat LN, et al. (2006) Retroviral elements and their hosts: insertional mutagenesis in the mouse germ line. PLoS Genet 2: e2. doi:10.1371/journal.pgen.0020002.
13. Maksakova IA, Mager DL, Reiss D (2008) Keeping active endogenous retroviral-like elements in check: the epigenetic perspective. Cell Mol Life Sci 65: 3329-3347.
14. Goff SP (2004) Retrovirus restriction factors. Mol Cell 16: 849-859.
15. Martens JH, O'Sullivan RJ, Braunschweig U, Opravil S, Radolf M, et al. (2005) The profile of repeat-associated histone lysine methylation states in the mouse epigenome. Embo J 24: 800-812.
16. Matsui T, Leung D, Miyashita H, Maksakova I, Miyachi H, et al. (2010) Proviral silencing in embryonic stem cells requires the histone methyltransferase ESET. Nature advance online publication doi:10.1038/nature08858.
17. Slotkin RK, Martienssen R (2007) Transposable elements and the epigenetic regulation of the genome. Nat Rev Genet 8: 272-285.
18. Cam HP, Chen ES, Grewal SI (2009) Transcriptional scaffolds for heterochromatin assembly. Cell 136: 610-614.
19. Malone CD, Hannon GJ (2009) Small RNAs as guardians of the genome. Cell 136: 656-668.
20. Obbard DJ, Finnegan DJ (2008) RNA interference: endogenous siRNAs derived from transposable elements. Curr Biol 18: R561-563.
21. Matzke M, Kanno T, Daxinger L, Huettel B, Matzke AJ (2009) RNA-mediated chromatin-based silencing in plants. Curr Opin Cell Biol 21: 367-376.
22. McClintock B (1984) The significance of responses of the genome to challenge. Science 226: 792-801.
23. Capy P, Gasperi G, Biemont C, Bazin C (2000) Stress and transposable elements: co-evolution or useful parasites? Heredity 85 (Pt 2): 101-106.
24. Panning B, Smiley JR (1993) Activation of RNA polymerase III transcription of human Alu repetitive elements by adenovirus type 5: requirement for the E1b 58-kilodalton protein and the products of E4 open reading frames 3 and 6. Mol Cell Biol 13: 3231-3244.
25. Liu WM, Chu WM, Choudary PV, Schmid CW (1995) Cell stress and translational inhibitors transiently increase the abundance of mammalian SINE transcripts. Nucleic Acids Res 23: 1758-1765.
26. Stribinskis V, Ramos KS (2006) Activation of human long interspersed nuclear element 1 retrotransposition by benzo(a)pyrene, an ubiquitous environmental carcinogen. Cancer Res 66: 2616-2620.
27. French NS, Norton JD (1997) Structure and functional properties of mouse VL30 retrotransposons. Biochim Biophys Acta 1352: 33-47.
28. Januchowski R, Dabrowski M, Ofori H, Jagodzinski PP (2007) Trichostatin A down-regulate DNA methyltransferase 1 in Jurkat T cells. Cancer Lett 246: 313-317.
29. You JS, Kang JK, Lee EK, Lee JC, Lee SH, et al. (2008) Histone deacetylase inhibitor apicidin downregulates DNA methyltransferase 1 expression and induces repressive histone modifications via recruitment of corepressor complex to promoter region in human cervix cancer cells. Oncogene 27: 1376-1386.
30. Schermelleh L, Spada F, Easwaran HP, Zolghadr K, Margot JB, et al. (2005) Trapped in action: direct visualization of DNA methyltransferase activity in living cells. Nat Methods 2: 751-756.
31. Ghoshal K, Datta J, Majumder S, Bai S, Kutay H, et al. (2005) 5-Azadeoxycytidine induces selective degradation of DNA methyltransferase 1 by a proteasomal pathway that requires the KEN box, bromo-adjacent homology domain, and nuclear localization signal. Mol Cell Biol 25: 4727-4741.
32. Gonzalgo ML, Jones PA (1997) Rapid quantitation of methylation differences at specific sites using methylation-sensitive single nucleotide primer extension (Ms- SNuPE). Nucleic Acids Res 25: 2529-2531.
33. Lane N, Dean W, Erhardt S, Hajkova P, Surani A, et al. (2003) Resistance of IAPs to methylation reprogramming may provide a mechanism for epigenetic inheritance in the mouse. Genesis 35: 88-93.
34. Lagger G, O'Carroll D, Rembold M, Khier H, Tischler J, et al. (2002) Essential function of histone deacetylase 1 in proliferation control and CDK inhibitor repression. Embo J 21: 2672-2681.
35. Peaston AE, Evsikov AV, Graber JH, de Vries WN, Holbrook AE, et al. (2004) Retrotransposons regulate host genes in mouse oocytes and preimplantation embryos. Dev Cell 7: 597-606.
36. Stocking C, Kozak CA (2008) Murine endogenous retroviruses. Cell Mol Life Sci 65: 3383-3398.
37. Davis CM, Constantinides PG, van der Riet F, van Schalkwyk L, Gevers W, et al. (1989) Activation and demethylation of the intracisternal A particle genes by 5-azacytidine. Cell Differ Dev 27: 83-93.
38. Walsh CP, Chaillet JR, Bestor TH (1998) Transcription of IAP endogenous retroviruses is constrained by cytosine methylation. Nat Genet 20: 116-117.
39. Tzavaras T, Eftaxia S, Tavoulari S, Hatzi P, Angelidis C (2003) Factors influencing the expression of endogenous reverse transcriptases and viral-like 30 elements in mouse NIH3T3 cells. Int J Oncol 23: 1237-1243.
40. Maksakova IA, Mager DL (2005) Transcriptional regulation of early transposon elements, an active family of mouse long terminal repeat retrotransposons. J Virol 79: 13865-13874.
41. Scholes DT, Banerjee M, Bowen B, Curcio MJ (2001) Multiple regulators of Ty1 transposition in Saccharomyces cerevisiae have conserved roles in genome maintenance. Genetics 159: 1449-1465.
42. Griffith JL, Coleman LE, Raymond AS, Goodson SG, Pittard WS, et al. (2003) Functional genomics reveals relationships between the retrovirus-like Ty1 element and its host Saccharomyces cerevisiae. Genetics 164: 867-879.
43. Aye M, Irwin B, Beliakova-Bethell N, Chen E, Garrus J, et al. (2004) Host factors that affect Ty3 retrotransposition in Saccharomyces cerevisiae. Genetics 168: 1159-1176.
44. Irwin B, Aye M, Baldi P, Beliakova-Bethell N, Cheng H, et al. (2005) Retroviruses and yeast retrotransposons use overlapping sets of host genes. Genome Res 15: 641-654.
45. Nyswaner KM, Checkley MA, Yi M, Stephens RM, Garfinkel DJ (2008) Chromatin-associated genes protect the yeast genome from Ty1 insertional mutagenesis. Genetics 178: 197-214.
46. Heidmann O, Heidmann T (1991) Retrotransposition of a mouse IAP sequence tagged with an indicator gene. Cell 64: 159-170.
47. Moran JV, Holmes SE, Naas TP, DeBerardinis RJ, Boeke JD, et al. (1996) High frequency retrotransposition in cultured mammalian cells. Cell 87: 917-927.
48. Esnault C, Heidmann O, Delebecque F, Dewannieux M, Ribet D, et al. (2005) APOBEC3G cytidine deaminase inhibits retrotransposition of endogenous retroviruses. Nature 433: 430-433.
49. Mietz JA, Fewell JW, Kuff EL (1992) Selective activation of a discrete family of endogenous proviral elements in normal BALB/c lymphocytes. Mol Cell Biol 12: 220-228.
50. Nilsson M, Bohm S (1994) Inducible and cell type-specific expression of VL30 U3 subgroups correlate with their enhancer design. J Virol 68: 276-288.
51. Noutsopoulos D, Markopoulos G, Koliou M, Dova L, Vartholomatos G, et al. (2007) Vanadium induces VL30 retrotransposition at an unusually high level: a possible carcinogenesis mechanism. J Mol Biol 374: 80-90.
52. Mahadevan LC, Willis AC, Barratt MJ (1991) Rapid histone H3 phosphorylation in response to growth factors, phorbol esters, okadaic acid, and protein synthesis inhibitors. Cell 65: 775-783.
53. Thomson S, Clayton AL, Hazzalin CA, Rose S, Barratt MJ, et al. (1999) The nucleosomal response associated with immediate-early gene induction is mediated via alternative MAP kinase cascades: MSK1 as a potential histone H3/HMG-14 kinase. Embo J 18: 4779-4793.
54. Cheung P, Tanner KG, Cheung WL, Sassone-Corsi P, Denu JM, et al. (2000) Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol Cell 5: 905-915.
55. Clayton AL, Rose S, Barratt MJ, Mahadevan LC (2000) Phosphoacetylation of histone H3 on c-fos- and c-jun-associated nucleosomes upon gene activation. Embo J 19: 3714-3726.
56. Li J, Gorospe M, Hutter D, Barnes J, Keyse SM, et al. (2001) Transcriptional induction of MKP-1 in response to stress is associated with histone H3 phosphorylation-acetylation. Mol Cell Biol 21: 8213-8224.
57. Hauser C, Schuettengruber B, Bartl S, Lagger G, Seiser C (2002) Activation of the mouse histone deacetylase 1 gene by cooperative histone phosphorylation and acetylation. Mol Cell Biol 22: 7820-7830.
58. Winter S, Simboeck E, Fischle W, Zupkovitz G, Dohnal I, et al. (2008) 14-3-3 proteins recognize a histone code at histone H3 and are required for transcriptional activation. Embo J 27: 88-99.
59. Kurdistani SK, Tavazoie S, Grunstein M (2004) Mapping global histone acetylation patterns to gene expression. Cell 117: 721-733.
60. Koch CM, Andrews RM, Flicek P, Dillon SC, Karaoz U, et al. (2007) The landscape of histone modifications across 1% of the human genome in five human cell lines. Genome Res 17: 691-707.
61. Fischer JJ, Toedling J, Krueger T, Schueler M, Huber W, et al. (2008) Combinatorial effects of four histone modifications in transcription and differentiation. Genomics 91: 41-51.
62. Glozak MA, Seto E (2007) Histone deacetylases and cancer. Oncogene 26: 5420-5432.
63. Kalkhoven E (2004) CBP and p300: HATs for different occasions. Biochem Pharmacol 68: 1145-1155.
64. He G, Margolis DM (2002) Counterregulation of chromatin deacetylation and histone deacetylase occupancy at the integrated promoter of human immunodeficiency virus type 1 (HIV-1) by the HIV-1 repressor YY1 and HIV-1 activator Tat. Mol Cell Biol 22: 2965-2973.
65. Lusic M, Marcello A, Cereseto A, Giacca M (2003) Regulation of HIV-1 gene expression by histone acetylation and factor recruitment at the LTR promoter. Embo J 22: 6550-6561.
66. Garrison BS, Yant SR, Mikkelsen JG, Kay MA (2007) Postintegrative gene silencing within the Sleeping Beauty transposition system. Mol Cell Biol 27: 8824-8833.
67. Branciforte D, Martin SL (1994) Developmental and cell type specificity of LINE-1 expression in mouse testis: implications for transposition. Mol Cell Biol 14: 2584-2592.
68. Dupressoir A, Heidmann T (1996) Germ line-specific expression of intracisternal A-particle retrotransposons in transgenic mice. Mol Cell Biol 16: 4495-4503.
69. Seifarth W, Frank O, Zeilfelder U, Spiess B, Greenwood AD, et al. (2005) Comprehensive analysis of human endogenous retrovirus transcriptional activity in human tissues with a retrovirus-specific microarray. J Virol 79: 341-352.
70. Ishihara H, Tanaka I, Wan H, Nojima K, Yoshida K (2004) Retrotransposition of limited deletion type of intracisternal A-particle elements in the myeloid leukemia Clls of C3H/He mice. J Radiat Res (Tokyo) 45: 25-32.
71. Costain WJ, Rasquinha I, Graber T, Luebbert C, Preston E, et al. (2006) Cerebral ischemia induces neuronal expression of novel VL30 mouse retrotransposons bound to polyribosomes. Brain Res 1094: 24-37.
72. Rauch TA, Zhong X, Wu X, Wang M, Kernstine KH, et al. (2008) Highresolution mapping of DNA hypermethylation and hypomethylation in lung cancer. Proc Natl Acad Sci U S A 105: 252-257.
73. Wilson AS, Power BE, Molloy PL (2007) DNA hypomethylation and human diseases. Biochim Biophys Acta 1775: 138-162.
74. Colmegna I, Garry RF (2006) Role of endogenous retroviruses in autoimmune diseases. Infect Dis Clin North Am 20: 913-929.
75. Song X, Sui A, Garen A (2004) Binding of mouse VL30 retrotransposon RNA to PSF protein induces genes repressed by PSF: effects on steroidogenesis and oncogenesis. Proc Natl Acad Sci U S A 101: 621-626.
76. Song X, Sun Y, Garen A (2005) Roles of PSF protein and VL30 RNA in reversible gene regulation. Proc Natl Acad Sci U S A 102: 12189-12193.
77. Miller WJ, McDonald JF, Nouaud D, Anxolabehere D (1999) Molecular domestication-more than a sporadic episode in evolution. Genetica 107: 197-207.
78. Espino PS, Li L, He S, Yu J, Davie JR (2006) Chromatin modification of the trefoil factor 1 gene in human breast cancer cells by the Ras/mitogen-activated protein kinase pathway. Cancer Res 66: 4610-4616.
79. Wiech NL, Fisher JF, Helquist P, Wiest O (2009) Inhibition of histone deacetylases: a pharmacological approach to the treatment of non-cancer disorders. Curr Top Med Chem 9: 257-271.
80. Rotili D, Simonetti G, Savarino A, Palamara AT, Migliaccio AR, et al. (2009) Non-cancer uses of histone deacetylase inhibitors: effects on infectious diseases and beta-hemoglobinopathies. Curr Top Med Chem 9: 272-291.
81. Li L, Feng T, Lian Y, Zhang G, Garen A, et al. (2009) Role of human noncoding RNAs in the control of tumorigenesis. Proc Natl Acad Sci U S A.
82. Yamaguchi T, Cubizolles F, Zhang Y, Reichert N, Kohler H, et al. Histone deacetylases 1 and 2 act in concert to promote the G1-to-S progression. Genes Dev 24: 455-469.
83. Todaro GJ, Green H (1963) Quantitative studies of the growth of mouse embryo cells in culture and their development into established lines. J Cell Biol 17: 299-313.
84. Puschendorf M, Stein P, Oakeley EJ, Schultz RM, Peters AH, et al. (2006) Abundant transcripts from retrotransposons are unstable in fully grown mouse oocytes. Biochem Biophys Res Commun 347: 36-43.
85. Carter AT, Norton JD, Avery RJ (1983) A novel approach to cloning transcriptionally active retrovirus-like genetic elements from mouse cells. Nucleic Acids Res 11: 6243-6254.
86. Eaton L, Norton JD (1990) Independent regulation of mouse VL30 retrotransposon expression in response to serum and oncogenic cell transformation. Nucleic Acids Res 18: 2069-2077.
87. Hodgson CP, Elder PK, Ono T, Foster DN, Getz MJ (1983) Structure and expression of mouse VL30 genes. Mol Cell Biol 3: 2221-2231.
88. Wicker T, Sabot F, Hua-Van A, Bennetzen JL, Capy P, et al. (2007) A unified classification system for eukaryotic transposable elements. Nat Rev Genet 8: 973-982.
89. Smit AF (1993) Identification of a new, abundant superfamily of mammalian LTR-transposons. Nucleic Acids Res 21: 1863-1872.