Emerging roles for chromatin as a signal integration and storage platform

Nature Reviews Molecular Cell Biology

Volumn 14, Issue 4, 2013, Pages 211-224

  Badeaux, Aimee I ^a   Shi, Yang ^a  

^a BOSTON CHILDREN S HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AURORA B KINASE; BMI1 PROTEIN; BRM PROTEIN; CHECKPOINT KINASE 1; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIN DEPENDENT KINASE 1; CYCLIN DEPENDENT KINASE 2; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3B; HETEROCHROMATIN PROTEIN 1; HISTONE; HISTONE ACETYLTRANSFERASE; HISTONE DEACETYLASE 3; HISTONE H3; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; JANUS KINASE 2; MITOGEN ACTIVATED PROTEIN KINASE P38; MYOD PROTEIN; PHOSPHATIDYLINOSITOL 3 KINASE; POSITIVE TRANSCRIPTION ELONGATION FACTOR B; PROTEIN KINASE B; PROTEIN KINASE C ALPHA; PYRUVATE KINASE; RNA POLYMERASE II; SIRTUIN 1; TRANSCRIPTION FACTOR CLOCK; TRANSCRIPTION FACTOR EZH2; TRANSCRIPTION FACTOR FKHR; UNINDEXED DRUG; CHROMATIN;

CARBOXY TERMINAL SEQUENCE; CELL CYCLE REGULATION; CELL DIFFERENTIATION; CELL DIVISION; CHROMATIN; CHROMOSOME CONDENSATION; CHROMOSOME SEGREGATION; DNA DAMAGE; DNA METHYLATION; DNA REPLICATION; EPIGENETICS; EXTRACELLULAR MATRIX; GENE EXPRESSION; GENETIC TRANSCRIPTION; HISTONE METHYLATION; HISTONE MODIFICATION; HUMAN; MOLECULAR DOCKING; MOLECULAR INTERACTION; NONHUMAN; NUCLEOSOME; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION ELONGATION; ANIMAL; GENETIC EPIGENESIS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PROTEIN PROCESSING;

CELL COMMUNICATION; CHROMATIN; EPIGENESIS, GENETIC; HISTONES; HUMANS; METHYLATION; MODELS, GENETIC; SIGNAL TRANSDUCTION; ANIMALS; DNA METHYLATION; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL;

EID: 84875424617     PISSN: 14710072     EISSN: 14710080     Source Type: Journal    
DOI: 10.1038/nrm3545     Document Type: Review

References (133)

1. Slattery, M. et al. Cofactor binding evokes latent differences in DNA binding specificity between Hox proteins. Cell 147, 1270-1282 (2011).
2. Stark, G. & Darnell, J. The JAK-STAT pathway at twenty. Immunity 36, 503-514 (2012).
3. Kodadek, T., Sikder, D. & Nalley, K. Keeping transcriptional activators under control. Cell 127, 261-264 (2006). (Pubitemid 44572383)
4. Young, N. et al. High throughput characterization of combinatorial histone codes. Mol. Cell Proteom. 8, 2266-2284 (2009).
5. Strahl, B. & Allis, C. The language of covalent histone modifications. Nature 403, 41-45 (2000). (Pubitemid 30038513)
6. Cheung, P., Allis, C. & Sassone-Corsi, P. Signaling to chromatin through histone modifications. Cell 103, 263-271 (2000).
7. Greer, E. et al. Transgenerational epigenetic inheritance of longevity in Caenorhabditis elegans. Nature 479, 365-436 (2011).
8. Schreiber, S. & Bernstein, B. Signaling network model of chromatin. Cell 111, 771-778 (2002). (Pubitemid 36106399)
9. Bao, Y. Chromatin response to DNA double-strand break damage. Epigenomics 3, 307-328 (2011).
10. Conaway, J. W. Introduction to theme "Chromatin, epigenetics, and transcription". Annu. Rev. Biochem. 81, 61-64 (2012).
11. Greer, E. & Shi, Y. Histone methylation: a dynamic mark in health, disease and inheritance. Nature Rev. Genet. 13, 343-400 (2012).
12. Spitale, R., Tsai, M.-C. & Chang, H. RNA templating the epigenome: long noncoding RNAs as molecular scaffolds. Epigenetics 6, 539-582 (2011).
13. Iberg, A. et al. Arginine methylation of the histone H3 tail impedes effector binding. J. Biol. Chem. 283, 3006-3016 (2008).
14. Guccione, E. et al. Methylation of histone H3R2 by PRMT6 and H3K4 by an MLL complex are mutually exclusive. Nature 449, 933-940 (2007).
15. Hyllus, D. et al. PRMT6-mediated methylation of R2 in histone H3 antagonizes H3 K4 trimethylation. Genes Dev. 21, 3369-3449 (2007).
16. Eustermann, S. et al. Combinatorial readout of histone H3 modifications specifies localization of ATRX to heterochromatin. Nature Struct. Mol. Biol. 18, 777-859 (2011).
17. Qiu, Y. et al. Combinatorial readout of unmodified H3R2 and acetylated H3K14 by the tandem PHD finger of MOZ reveals a regulatory mechanism for HOXA9 transcription. Genes Dev. 26, 1376-1467 (2012).
18. Suganuma, T. & Workman, J. Signals and combinatorial functions of histone modifications. Annu. Rev. Biochem. 80, 473-572 (2011).
19. Taverna, S., Li, H., Ruthenburg, A., Allis, C. & Patel, D. How chromatin-binding modules interpret histone modifications: lessons from professional pocket pickers. Nature Struct. Mol. Biol. 14, 1025-1065 (2007).
20. Ruthenburg, A. et al. Recognition of a mononucleosomal histone modification pattern by BPTF via multivalent interactions. Cell 145, 692-706 (2011).
21. Alabert, C. & Groth, A. Chromatin replication and epigenome maintenance. Nature Rev. Mol. Cell Biol. 13, 153-167 (2012).
22. Ripperger, J. & Merrow, M. Perfect timing: epigenetic regulation of the circadian clock. FEBS Lett. 585, 1406-1411 (2011).
23. Zee, B., Levin, R., Dimaggio, P. & Garcia, B. Global turnover of histone post-translational modifications and variants in human cells. Epigenetics Chromatin 3, 22 (2010).
24. Barth, T. & Imhof, A. Fast signals and slow marks: the dynamics of histone modifications. Trends Biochem. Sci 35, 618-644, 2010.
25. Banerjee, T. & Chakravarti, D. A peek into the complex realm of histone phosphorylation. Mol. Cell. Biol. 31, 4858-4931 (2011).
26. Baek, S. When signaling kinases meet histones and histone modifiers in the nucleus. Mol. Cell 42, 274-358 (2011).
27. Wei, Y., Yu, L., Bowen, J., Gorovsky, M. & Allis, C. Phosphorylation of histone H3 is required for proper chromosome condensation and segregation. Cell 97, 99-208 (1999).
28. Cheung, P. et al. Synergistic coupling of histone H3 phosphorylation and acetylation in response to epidermal growth factor stimulation. Mol. Cell 5, 905-920 (2000).
29. Thomson, S., Clayton, A. & Mahadevan, L. Independent dynamic regulation of histone phosphorylation and acetylation during immediate-early gene induction. Mol. Cell 8, 1231-1272 (2001).
30. Vicent, G. et al. Induction of progesterone target genes requires activation of Erk and Msk kinases and phosphorylation of histone H3. Mol. Cell 24, 367-448 (2006).
31. Zippo, A. et al. Histone crosstalk between H3S10ph and H4K16ac generates a histone code that mediates transcription elongation. Cell 138, 1122-1136 (2009).
32. Dawson, M. et al. JAK2 phosphorylates histone H3Y41 and excludes HP1α from chromatin. Nature 461, 819-822 (2009).
33. Liokatis, S. et al. Phosphorylation of histone H3 Ser10 establishes a hierarchy for subsequent intramolecular modification events. Nature Struct. Mol. Biol. 19, 819-823 (2012).
34. Metzger, E. et al. Phosphorylation of histone H3T6 by PKCβI controls demethylation at histone H3K4. Nature 464, 792-798 (2010).
35. Lau, P. & Cheung, P. Histone code pathway involving H3 S28 phosphorylation and K27 acetylation activates transcription and antagonizes polycomb silencing. Proc. Natl Acad. Sci. USA 108, 2801-2807 (2011).
36. Yang, W. et al. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis. Cell 150, 685-696 (2012).
37. Avraham, R. & Yarden, Y. Feedback regulation of EGFR signalling: decision making by early and delayed loops. Nature Rev. Mol. Cell Biol. 12, 104-121 (2011).
38. Xiong, S., Salazar, G., Patrushev, N. & Alexander, R. FoxO1 mediates an autofeedback loop regulating SIRT1 expression. J. Biol. Chem. 286, 5289-5388 (2011).
39. Latham, J., Chosed, R., Wang, S. & Dent, S. Chromatin signaling to kinetochores: transregulation of Dam1 methylation by histone H2B ubiquitination. Cell 146, 709-728 (2011).
40. Lu, C. & Thompson, C. Metabolic regulation of epigenetics. Cell Metab. 16, 9-17 (2012).
41. Melvin, A. & Rocha, S. Chromatin as an oxygen sensor and active player in the hypoxia response. Cell. Signal. 24, 35-78 (2012).
42. Zhou, X. et al. Hypoxia induces trimethylated H3 lysine 4 by inhibition of JARID1A demethylase. Cancer Res. 70, 4214-4235 (2010).
43. Chowdhury, R. et al. The oncometabolite 2-hydroxyglutarate inhibits histone lysine demethylases. EMBO Rep. 12, 463-469 (2011).
44. Lu, C. et al. IDH mutation impairs histone demethylation and results in a block to cell differentiation. Nature 483, 474-478 (2012).
45. Shimazu, T. et al. Suppression of oxidative stress by β-hydroxybutyrate, an endogenous histone deacetylase inhibitor. Science 339, 211-214 (2013).
46. Fujiki, R. et al. GlcNAcylation of a histone methyltransferase in retinoic-acid-induced granulopoiesis. Nature 459, 455-464 (2009).
47. Fujiki, R. et al. GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature 480, 557-617 (2011).
48. Hanover, J., Krause, M. & Love, D. Bittersweet memories: linking metabolism to epigenetics through O-GlcNAcylation. Nature Rev. Mol. Cell Biol. 13, 312-333 (2012).
49. Kaelin, W. Jr. Cancer and altered metabolism: potential importance of hypoxia-inducible factor and 2-oxoglutarate-dependent dioxygenases. Cold Spring Harb. Symp. Quant. Biol. 76, 335-345 (2011).
50. Sassone-Corsi, P. Physiology. When metabolism and epigenetics converge. Science 339, 148-150 (2013).
51. Yang, X.-J. & Seto, E. Lysine acetylation: codified crosstalk with other posttranslational modifications. Mol. Cell 31, 449-510 (2008).
52. Cha, T.-L. et al. Akt-mediated phosphorylation of EZH2 suppresses methylation of lysine 27 in histone H3. Science 310, 306-310 (2005). (Pubitemid 41457195)
53. Nacerddine, K. et al. Akt-mediated phosphorylation of Bmi1 modulates its oncogenic potential, E3 ligase activity, and DNA damage repair activity in mouse prostate cancer. J. Clin. Invest. 122, 1920-1952 (2012).
54. Huang, W.-C. & Chen, C.-C. Akt phosphorylation of p300 at Ser-1834 is essential for its histone acetyltransferase and transcriptional activity. Mol. Cell. Biol. 25, 6592-7194 (2005).
55. Bird, A. DNA methylation patterns and epigenetic memory. Genes Dev. 16, 6-21 (2002). (Pubitemid 34049633)
56. Estθve, P.-O. et al. A methylation and phosphorylation switch between an adjacent lysine and serine determines human DNMT1 stability. Nature Struct. Mol. Biol. 18, 42-50 (2011).
57. Hervouet, E. et al. Disruption of Dnmt1/PCNA/UHRF1 interactions promotes tumorigenesis from human and mice glial cells. PLoS ONE 5, e11333 (2010).
58. Arita, K., Ariyoshi, M., Tochio, H., Nakamura, Y. & Shirakawa, M. Recognition of hemi-methylated DNA by the SRA protein UHRF1 by a base-flipping mechanism. Nature 455, 818-821 (2008).
59. Avvakumov, G. et al. Structural basis for recognition of hemi-methylated DNA by the SRA domain of human UHRF1. Nature 455, 822-825 (2008).
60. Hashimoto, H. et al. The SRA domain of UHRF1 flips 5-methylcytosine out of the DNA helix. Nature 455, 826-829 (2008).
61. Hennessy, B., Smith, D., Ram, P., Lu, Y. & Mills, G. Exploiting the PI3K/AKT pathway for cancer drug discovery. Nature Rev. Drug Discov. 4, 988-1992 (2005).
62. Bernstein, B. et al. A bivalent chromatin structure marks key developmental genes in embryonic stem cells. Cell 125, 315-326 (2006).
63. Svotelis, A. et al. H3K27 demethylation by JMJD3 at a poised enhancer of anti-apoptotic gene BCL2 determines ERα ligand dependency. EMBO J. 30, 3947-3961 (2011).
64. Creyghton, M. et al. Histone H3K27ac separates active from poised enhancers and predicts developmental state. Proc. Natl Acad. Sci. USA 107, 21931-21936 (2010).
65. Visel, A. et al. ChIP-seq accurately predicts tissue-specific activity of enhancers. Nature 457, 854-858 (2009).
66. Hargreaves, D. & Crabtree, G. ATP-dependent chromatin remodeling: genetics, genomics and mechanisms. Cell Res. 21, 396-420 (2011).
67. Forcales, S. et al. Signal-dependent incorporation of MyoD-BAF60c into Brg1-based SWI/SNF chromatin-remodelling complex. EMBO J. 31, 301-317 (2012).
68. Palacios, D. et al. TNF/p38α/polycomb signaling to Pax7 locus in satellite cells links inflammation to the epigenetic control of muscle regeneration. Cell Stem Cell 7, 455-524 (2010).
69. Bedford, M. & Clarke, S. Protein arginine methylation in mammals: who, what, and why. Mol. Cell 33, 1-13 (2009).
70. Zhao, Q. et al. PRMT5-mediated methylation of histone H4R3 recruits DNMT3A, coupling histone and DNA methylation in gene silencing. Nature Struct. Mol. Biol. 16, 304-315 (2009).
71. Liu, F. et al. JAK2V617F-mediated phosphorylation of PRMT5 downregulates its methyltransferase activity and promotes myeloproliferation. Cancer Cell 19, 283-377 (2011).
72. Levy, D. et al. Lysine methylation of the NF-κB subunit RelA by SETD6 couples activity of the histone methyltransferase GLP at chromatin to tonic repression of NF-κB signaling. Nature Immunol. 12, 29-65 (2011).
73. Day, J. & Sweatt, J. Epigenetic mechanisms in cognition. Neuron 70, 813-842 (2011).
74. Maze, I., Noh, K.-M. & Allis, C. Histone regulation in the CNS: basic principles of epigenetic plasticity. Neuropsychopharmacology 38, 3-22 (2012).
75. West, A. & Greenberg, M. Neuronal activity-regulated gene transcription in synapse development and cognitive function. Cold Spring Harb. Persp. Biol. 3, a005744 (2011).
76. Okuno, H. Regulation and function of immediate-early genes in the brain: beyond neuronal activity markers. Neurosci. Res. 69, 175-261 (2011).
77. Tagami, H., Ray-Gallet, D., Almouzni, G. & Nakatani, Y. Histone H3.1 and H3.3 complexes mediate nucleosome assembly pathways dependent or independent of DNA synthesis. Cell 116, 51-112 (2004).
78. Michod, D. et al. Calcium-dependent dephosphorylation of the histone chaperone DAXX regulates H3.3 loading and transcription upon neuronal activation. Neuron 74, 122-157 (2012).
79. Ng, R. & Gurdon, J. Epigenetic memory of an active gene state depends on histone H3.3 incorporation into chromatin in the absence of transcription. Nature Cell Biol. 10, 102-111 (2008).
80. Su, D. et al. Structural basis for recognition of H3K56-acetylated histone H3-H4 by the chaperone Rtt106. Nature 483, 104-111 (2012).
81. Chang, Y. et al. MPP8 mediates the interactions between DNA methyltransferase Dnmt3a and H3K9 methyltransferase GLP/G9a. Nature Commun. 2, 533 (2011).
82. Fischle, W., Wang, Y. & Allis, C. Binary switches and modification cassettes in histone biology and beyond. Nature 425, 475-484 (2003).
83. Nicodeme, E. et al. Suppression of inflammation by a synthetic histone mimic. Nature 468, 1119-1123 (2010).
84. Marazzi, I. et al. Suppression of the antiviral response by an influenza histone mimic. Nature 483, 428-433 (2012).
85. Chin, H. et al. Automethylation of G9a and its implication in wider substrate specificity and HP1 binding. Nucleic Acids Res. 35, 7313-7336 (2007).
86. Sampath, S. et al. Methylation of a histone mimic within the histone methyltransferase G9a regulates protein complex assembly. Mol. Cell 27, 596-1204 (2007).
87. Tachibana, M. et al. Histone methyltransferases G9a and GLP form heteromeric complexes and are both crucial for methylation of euchromatin at H3-K9. Genes Dev. 19, 815-826 (2005).
88. Kim, H. et al. p53 requires an intact C-terminal domain for DNA binding and transactivation. J. Mol. Biol. 415, 843-897 (2012).
89. Huang, J. et al. p53 is regulated by the lysine demethylase LSD1. Nature 449, 105-113 (2007).
90. Chuikov, S. et al. Regulation of p53 activity through lysine methylation. Nature 432, 353-413 (2004).
91. West, L. & Gozani, O. Regulation of p53 function by lysine methylation. Epigenomics 3, 361-370 (2011).
92. Kruse, J.-P. & Gu, W. Modes of p53 regulation. Cell 137, 609-631 (2009).
93. Cui, G. et al. PHF20 is an effector protein of p53 double lysine methylation that stabilizes and activates p53. Nature Struct. Mol. Biol. 19, 916-924 (2012).
94. Badeaux, A. et al. Loss of the methyl lysine effector protein PHF20 impacts the expression of genes regulated by the lysine acetyltransferase MOF. J. Biol. Chem. 287, 429-466 (2012).
95. Park, S. et al. Identification of Akt interaction protein PHF20/TZP that transcriptionally regulates p53. J. Biol. Chem. 287, 11151-11214 (2012).
96. Brookes, E. & Pombo, A. Modifications of RNA polymerase II are pivotal in regulating gene expression states. EMBO Rep, 10, 1213-1219, 2009.
97. Levine, M. Paused RNA polymerase II as a developmental checkpoint. Cell 145, 502-513 (2011).
98. Hsin, J.-P., Sheth, A. & Manley, J. RNAP II CTD phosphorylated on threonine-4 is required for histone mRNA 3? end processing. Science 334, 683-689 (2011).
99. Mayer, A. et al. CTD tyrosine phosphorylation impairs termination factor recruitment to RNA polymerase II. Science 336, 1723-1728 (2012).
100. Ranuncolo, S., Ghosh, S., Hanover, J., Hart, G. & Lewis, B. Evidence of the involvement of O-GlcNAc-modified human RNA polymerase II CTD in transcription in vitro and in vivo. J. Biol. Chem. 287, 23549-23561 (2012).
101. Sims, R. et al. The C-terminal domain of RNA polymerase II is modified by site-specific methylation. Science 332, 99-202 (2011).
102. Yang, Y. et al. TDRD3 is an effector molecule for arginine-methylated histone marks. Mol. Cell 40, 1016-1023 (2010).
103. Canani, R. et al. Epigenetic mechanisms elicited by nutrition in early life. Nutr. Res. Rev. 24, 198-403 (2011).
104. Symonds, M., Sebert, S., Hyatt, M. & Budge, H. Nutritional programming of the metabolic syndrome. Nature Rev. Endocrinol. 5, 604-614 (2009).
105. Walker, C. & Ho, S.-M. Developmental reprogramming of cancer susceptibility. Nature Rev. Cancer 12, 479-565 (2012).
106. Trollope, A. et al. Stress, epigenetic control of gene expression and memory formation. Exp. Neurol. 233, 3-14 (2012).
107. Zovkic, I. & Sweatt, J. Epigenetic mechanisms in learned fear: implications for PTSD. Neuropsychopharmacology 38, 77-93 (2012).
108. Kantojδrvi, K. et al. Analysis of 9p24 and 11p12-13 regions in autism spectrum disorders: rs1340513 in the JMJD2C gene is associated with ASDs in Finnish sample. Psychiatr. Genet. 20, 102-108 (2010).
109. Wang, K.-S., Liu, X., Zhang, Q., Wu, L.-Y. & Zeng, M. Genome-wide association study identifies 5q21 and 9p24.1 (KDM4C) loci associated with alcohol withdrawal symptoms. J. Neural Transm. 119, 425-433 (2012).
110. Iwase, S. et al. The X-linked mental retardation gene SMCX/JARID1C defines a family of histone H3 lysine 4 demethylases. Cell 128, 1077-1088 (2007). (Pubitemid 46437259)
111. Ounap, K. et al. A novel c.2T C mutation of the KDM5C/JARID1C gene in one large family with X-linked intellectual disability. Eur. J. Med. Genet. 55, 178-184 (2012).
112. Kleefstra, T. et al. Disruption of an EHMT1-associated chromatin-modification module causes intellectual disability. Am. J. Hum. Genet. 91, 73-82 (2012).
113. O'Roak, B. et al. Sporadic autism exomes reveal a highly interconnected protein network of de novo mutations. Nature 485, 246-250 (2012).
114. Laumonnier, F. et al. Mutations in PHF8 are associated with X linked mental retardation and cleft lip/cleft palate. J. Med. Genet. 42, 780-786 (2005). (Pubitemid 41475255)
115. Ong, C.-T. & Corces, V. Enhancer function: new insights into the regulation of tissue-specific gene expression. Nature Rev. Genet. 12, 283-293 (2011).
116. Boeke, J. et al. Phosphorylation of SU(VAR)3-9 by the chromosomal kinase JIL-1. PLoS ONE 5, e10042 (2010).
117. Chi, Y. et al. Identification of CDK2 substrates in human cell lysates. Genome Biol. 9, R149 (2008).
118. Liu, H. et al. Phosphorylation of MLL by ATR is required for execution of mammalian S-phase checkpoint. Nature 467, 343-346 (2010).
119. Wu, S. et al. Dynamic regulation of the PR-Set7 histone methyltransferase is required for normal cell cycle progression. Genes Dev. 24, 2531-2542 (2010).
120. Spektor, T., Congdon, L., Veerappan, C. & Rice, J. The UBC9 E2 SUMO conjugating enzyme binds the PR-Set7 histone methyltransferase to facilitate target gene repression. PLoS ONE 6, e22785 (2011).
121. Chen, S. et al. Cyclin-dependent kinases regulate epigenetic gene silencing through phosphorylation of EZH2. Nature Cell Biol. 12, 1108-1122 (2010).
122. Wei, Y. et al. CDK1-dependent phosphorylation of EZH2 suppresses methylation of H3K27 and promotes osteogenic differentiation of human mesenchymal stem cells. Nature Cell Biol. 13, 87-181 (2011).
123. Baba, A. et al. PKA-dependent regulation of the histone lysine demethylase complex PHF2-ARID5B. Nature Cell Biol. 13, 668-743 (2011).
124. Liu, W. et al. PHF8 mediates histone H4 lysine 20 demethylation events involved in cell cycle progression. Nature 466, 508-512 (2010).
125. Feng, Q. et al. Biochemical control of CARM1 enzymatic activity by phosphorylation. J. Biol. Chem. 284, 36167-36241 (2009).
126. Higashimoto, K., Kuhn, P., Desai, D., Cheng, X. & Xu, W. Phosphorylation-mediated inactivation of coactivator-associated arginine methyltransferase 1. Proc. Natl Acad. Sci. USA 104, 12318-12323 (2007). (Pubitemid 47206135)
127. Estθve P. O. et al. Regulation of DNMT1 stability through SET7-mediated lysine methylation in mammalian cells. Proc. Natl Acad. Sci. USA 106, 5076-5081 (2009
128. Lee, B. & Muller M. T. SUMOylation enhances DNA methyltransferase 1 activity. Biochem. J. 421, 449-461 (2009
129. Sugiyama Y. et al. The DNA-binding activity of mouse DNA methyltransferase 1 is regulated by phosphorylation with casein kinase 1δ/. Biochem J. 427, 489-497 (2010
130. Lavoie G. & St-Pierre Y. Phosphorylation of human DNMT1: implication of cyclin-dependent kinases. Biochem. Biophys. Res. Commun. 409, 187-192 (2011
131. Bourachot, B., Yaniv, M. & Muchardt, C. Growth inhibition by the mammalian SWI-SNF subunit Brm is regulated by acetylation. EMBO J. 22, 6505-6515 (2003). (Pubitemid 38009598)
132. Galisson, F. et al. A novel proteomics approach to identify SUMOylated proteins and their modification sites in human cells. Mol Cell Proteomics 10, M110.004796 (2011).
133. Hsiao, H.-H., Meulmeester, E., Frank, B., Melchior, F. & Urlaub, H. "ChopNSpice, " a mass spectrometric approach that allows identification of endogenous small ubiquitin-like modifier-conjugated peptides. Mol. Cell Proteom. 8, 2664-2675 (2009).