KATs in cancer: Functions and therapies

Oncogene

Volumn 34, Issue 38, 2015, Pages 4901-4913

  Farria, A ^a   Li, W ^a   Dent, S Y R ^a  

^a UNIVERSITY OF TEXAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACYLTRANSFERASE; ACYLTRANSFERASE INHIBITOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN BINDING PROTEIN INHIBITOR; HISTONE ACETYLTRANSFERASE GCN5; HISTONE ACETYLTRANSFERASE GCN5 INHIBITOR; HISTONE ACETYLTRANSFERASE PCAF; HISTONE ACETYLTRANSFERASE PCAF INHIBITOR; LYSINE; LYSINE ACETYLTRANSFERASE; PROTEIN; PROTEIN 300; PROTEIN 300 INHIBITOR; TAT INTERACTING PROTEIN 60KDA; TIP60 INHIBITOR; UNCLASSIFIED DRUG; ENZYME INHIBITOR; HISTONE ACETYLTRANSFERASE;

BREAST CANCER; CANCER GROWTH; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CHROMATIN; ENZYME ACTIVITY; ENZYME REGULATION; HISTONE ACETYLATION; HUMAN; LEUKEMIA; LUNG CANCER; NEOPLASM; PRIORITY JOURNAL; REVIEW; ANIMAL; ANTAGONISTS AND INHIBITORS; ENZYMOLOGY; METABOLISM; NEOPLASMS; PATHOLOGY;

ANIMALS; ENZYME INHIBITORS; HISTONE ACETYLTRANSFERASES; HUMANS; LYSINE; NEOPLASMS;

EID: 84941873904     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2014.453     Document Type: Review

References (192)

1. de Ruijter AJ, van Gennip AH, Caron HN, Kemp S, van Kuilenburg AB. Histone deacetylases (HDACs): characterization of the classical HDAC family. Biochem J 2003; 370: 737-749.
2. Haberland M, Montgomery RL, Olson EN. The many roles of histone deacetylases in development and physiology: implications for disease and therapy. Nat Rev Genet 2009; 10: 32-42.
3. Kim HJ, Bae SC. Histone deacetylase inhibitors: molecular mechanisms of action and clinical trials as anti-cancer drugs. Am J Transl Res 2011; 3: 166-179.
4. Kuo MH, Brownell JE, Sobel RE, Ranalli TA, Cook RG, Edmondson DG, et al. Transcription-linked acetylation by Gcn5p of histones H3 and H4 at specific lysines. Nature 1996; 383: 269-272.
5. Jin Q, Yu LR, Wang L, Zhang Z, Kasper LH, Lee JE, et al. Distinct roles of GCN5/PCAF-mediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J 2011; 30: 249-262.
6. Nakamura T, Blechman J, Tada S, Rozovskaia T, Itoyama T, Bullrich F, et al. huASH1 protein, a putative transcription factor encoded by a human homologue of the Drosophila ash1 gene, localizes to both nuclei and cell-cell tight junctions. Proc Natl Acad Sci USA 2000; 97: 7284-7289.
7. Kaeser MD, Aslanian A, Dong MQ, Yates JR 3rd, Emerson BM. BRD7, a novel PBAF-specific SWI/SNF subunit, is required for target gene activation and repression in embryonic stem cells. J Biol Chem 2008; 283: 32254-32263.
8. Brownell JE, Zhou J, Ranalli T, Kobayashi R, Edmondson DG, Roth SY, et al. Tetrahymena histone acetyltransferase A: a homolog to yeast Gcn5p linking histone acetylation to gene activation. Cell 1996; 84: 843-851.
9. Haynes SR, Dollard C, Winston F, Beck S, Trowsdale J, Dawid IB. The bromodomain: a conserved sequence found in human, Drosophila and yeast proteins. Nucleic Acids Res 1992; 20: 2603.
10. Dhalluin C, Carlson JE, Zeng L, He C, Aggarwal AK, Zhou MM. Structure and ligand of a histone acetyltransferase bromodomain. Nature 1999; 399: 491-496.
11. Zeng L, Zhou MM. Bromodomain: an acetyl-lysine binding domain. FEBS Lett 2002; 513: 124-128.
12. Filippakopoulos P, Picaud S, Mangos M, Keates T, Lambert JP, Barsyte-Lovejoy D, et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 2012; 149: 214-231.
13. Asangani IA, Dommeti VL, Wang X, Malik R, Cieslik M, Yang R, et al. Therapeutic targeting of BET bromodomain proteins in castration-resistant prostate cancer. Nature 2014; 510: 278-282.
14. Patel AJ, Liao CP, Chen Z, Liu C, Wang Y, Le LQ. BET bromodomain inhibition triggers apoptosis of NF1-associated malignant peripheral nerve sheath tumors through Bim induction. Cell Rep 2014; 6: 81-92.
15. Bandopadhayay P, Bergthold G, Nguyen B, Schubert S, Gholamin S, Tang Y, et al. BET bromodomain inhibition of MYC-amplified medulloblastoma. Clin Cancer Res 2014; 20: 912-925.
16. Zou Z, Huang B, Wu X, Zhang H, Qi J, Bradner J, et al. Brd4 maintains constitutively active NF-kappaB in cancer cells by binding to acetylated RelA. Oncogene 2014; 33: 2395-2404.
17. Santillan DA, Theisler CM, Ryan AS, Popovic R, Stuart T, Zhou MM, et al. Bromodomain and histone acetyltransferase domain specificities control mixed lineage leukemia phenotype. Cancer Res 2006; 66: 10032-10039.
18. French CA, Miyoshi I, Kubonishi I, Grier HE, Perez-Atayde AR, Fletcher JA. BRD4-NUT fusion oncogene: a novel mechanism in aggressive carcinoma. Cancer Res 2003; 63: 304-307.
19. French CA, Ramirez CL, Kolmakova J, Hickman TT, Cameron MJ, Thyne ME, et al. BRD-NUT oncoproteins: a family of closely related nuclear proteins that block epithelial differentiation and maintain the growth of carcinoma cells. Oncogene 2008; 27: 2237-2242.
20. Grayson AR, Walsh EM, Cameron MJ, Godec J, Ashworth T, Ambrose JM, et al. MYC, a downstream target of BRD-NUT, is necessary and sufficient for the blockade of differentiation in NUT midline carcinoma. Oncogene 2014; 33: 1736-1742.
21. Delmore JE, Issa GC, Lemieux ME, Rahl PB, Shi J, Jacobs HM, et al. BET bromodomain inhibition as a therapeutic strategy to target c-Myc. Cell 2011; 146: 904-917.
22. Mertz JA, Conery AR, Bryant BM, Sandy P, Balasubramanian S, Mele DA, et al. Targeting MYC dependence in cancer by inhibiting BET bromodomains. Proc Natl Acad Sci USA 2011; 108: 16669-16674.
23. Lange M, Kaynak B, Forster UB, Tonjes M, Fischer JJ, Grimm C, et al. Regulation of muscle development by DPF3, a novel histone acetylation and methylation reader of the BAF chromatin remodeling complex. Genes Dev 2008; 22: 2370-2384.
24. Zeng L, Zhang Q, Li S, Plotnikov AN, Walsh MJ, Zhou MM. Mechanism and regulation of acetylated histone binding by the tandem PHD finger of DPF3b. Nature 2010; 466: 258-262.
25. Li Y, Wen H, Xi Y, Tanaka K, Wang H, Peng D, et al. AF9 YEATS domain links histone acetylation to Dot1L H3K9 methylation. Cell 2014; 159: 558-571.
26. Bernt KM, Zhu N, Sinha AU, Vempati S, Faber J, Krivtsov AV, et al. MLL-rearranged leukemia is dependent on aberrant H3K79 methylation by DOT1L. Cancer Cell 2011; 20: 66-78.
27. Bhoumik A, Ronai Z. ATF2: a transcription factor that elicits oncogenic or tumor suppressor activities. Cell Cycle 2008; 7: 2341-2345.
28. Endo M, Su L, Nielsen TO. Activating transcription factor 2 in mesenchymal tumors. Hum Pathol 2014; 45: 276-284.
29. Lv G, Hu Z, Tie Y, Du J, Fu H, Gao X, et al. MicroRNA-451 regulates activating transcription factor 2 expression and inhibits liver cancer cell migration. Oncology Rep 2014; 32: 1021-1028.
30. Shah M, Bhoumik A, Goel V, Dewing A, Breitwieser W, Kluger H, et al. A role for ATF2 in regulating MITF and melanoma development. PLoS Genet 2010; 6: e1001258.
31. Butler JS, Koutelou E, Schibler AC, Dent SY. Histone-modifying enzymes: regulators of developmental decisions and drivers of human disease. Epigenomics 2012; 4: 163-177.
32. McMahon SB, Van Buskirk HA, Dugan KA, Copeland TD, Cole MD. The novel ATM-related protein TRRAP is an essential cofactor for the c-Myc and E2F oncoproteins. Cell 1998; 94: 363-374.
33. McMahon SB, Wood MA, Cole MD. The essential cofactor TRRAP recruits the histone acetyltransferase hGCN5 to c-Myc. Mol Cell Biol 2000; 20: 556-562.
34. Dang CV. c-Myc target genes involved in cell growth, apoptosis, and metabolism. Mol Cell Biol 1999; 19: 1-11.
35. Flinn EM, Wallberg AE, Hermann S, Grant PA, Workman JL, Wright AP. Recruitment of Gcn5-containing complexes during c-Myc-dependent gene activation. Structure and function aspects. J Biol Chem 2002; 277: 23399-23406.
36. Liu X, Tesfai J, Evrard YA, Dent SY, Martinez E. c-Myc transformation domain recruits the human STAGA complex and requires TRRAP and GCN5 acetylase activity for transcription activation. J Biol Chem 2003; 278: 20405-20412.
37. Kenneth NS, Ramsbottom BA, Gomez-Roman N, Marshall L, Cole PA, White RJ. TRRAP and GCN5 are used by c-Myc to activate RNA polymerase III transcription. Proc Natl Acad Sci USA 2007; 104: 14917-14922.
38. Zhang N, Ichikawa W, Faiola F, Lo SY, Liu X, Martinez E. MYC interacts with the human STAGA coactivator complex via multivalent contacts with the GCN5 and TRRAP subunits. Biochim Biophys Acta 2014; 1839: 395-405.
39. Patel JH, Du Y, Ard PG, Phillips C, Carella B, Chen CJ, et al. The c-MYC oncoprotein is a substrate of the acetyltransferases hGCN5/PCAF and TIP60. Mol Cell Biol 2004; 24: 10826-10834.
40. Chen L, Wei T, Si X, Wang Q, Li Y, Leng Y, et al. Lysine acetyltransferase GCN5 potentiates the growth of non-small cell lung cancer via promotion of E2F1, cyclin D1, and cyclin E1 expression. J Biol Chem 2013; 288: 14510-14521.
41. Lu Q, Kamps MP. Heterodimerization of Hox proteins with Pbx1 and oncoprotein E2a-Pbx1 generates unique DNA-binding specifities at nucleotides predicted to contact the N-terminal arm of the Hox homeodomain-demonstration of Hox-dependent targeting of E2a-Pbx1 in vivo. Oncogene 1997; 14: 75-83.
42. Holmlund T, Lindberg MJ, Grander D, Wallberg AE. GCN5 acetylates and regulates the stability of the oncoprotein E2A-PBX1 in acute lymphoblastic leukemia. Leukemia 2013; 27: 578-585.
43. Chen J, Luo Q, Yuan Y, Huang X, Cai W, Li C, et al. Pygo2 associates with MLL2 histone methyltransferase and GCN5 histone acetyltransferase complexes to augment Wnt target gene expression and breast cancer stem-like cell expansion. Mol Cell Biol 2010; 30: 5621-5635.
44. Wang YL, Faiola F, Xu M, Pan S, Martinez E. Human ATAC is a GCN5/PCAFcontaining acetylase complex with a novel NC2-like histone fold module that interacts with the TATA-binding protein. J Biol Chem 2008; 283: 33808-33815.
45. Krebs AR, Karmodiya K, Lindahl-Allen M, Struhl K, Tora L. SAGA and ATAC histone acetyl transferase complexes regulate distinct sets of genes and ATAC defines a class of p300-independent enhancers. Mol Cell 2011; 44: 410-423.
46. Yang XJ, Ogryzko VV, Nishikawa J, Howard BH, Nakatani Y. A p300/CBPassociated factor that competes with the adenoviral oncoprotein E1A. Nature 1996; 382: 319-324.
47. Nagy Z, Riss A, Fujiyama S, Krebs A, Orpinell M, Jansen P, et al. The metazoan ATAC and SAGA coactivator HAT complexes regulate different sets of inducible target genes. Cell Mol Life Sci 2010; 67: 611-628.
48. Xu W, Edmondson DG, Roth SY. Mammalian GCN5 and P/CAF acetyltransferases have homologous amino-terminal domains important for recognition of nucleosomal substrates. Mol Cell Biol 1998; 18: 5659-5669.
49. Nagy Z, Tora L. Distinct GCN5/PCAF-containing complexes function as coactivators and are involved in transcription factor and global histone acetylation. Oncogene 2007; 26: 5341-5357.
50. Yamauchi T, Yamauchi J, Kuwata T, Tamura T, Yamashita T, Bae N, et al. Distinct but overlapping roles of histone acetylase PCAF and of the closely related PCAFB/GCN5 in mouse embryogenesis. Proc Natl Acad Sci USA 2000; 97: 11303-11306.
51. Xu W, Edmondson DG, Evrard YA, Wakamiya M, Behringer RR, Roth SY. Loss of Gcn5l2 leads to increased apoptosis and mesodermal defects during mouse development. Nat Genet 2000; 26: 229-232.
52. Sakaguchi K, Herrera JE, Saito S, Miki T, Bustin M, Vassilev A, et al. DNA damage activates p53 through a phosphorylation-acetylation cascade. Genes Dev 1998; 12: 2831-2841.
53. Liu L, Scolnick DM, Trievel RC, Zhang HB, Marmorstein R, Halazonetis TD, et al. p53 sites acetylated in vitro by PCAF and p300 are acetylated in vivo in response to DNA damage. Mol Cell Biol 1999; 19: 1202-1209.
54. Lin R, Tao R, Gao X, Li T, Zhou X, Guan KL, et al. Acetylation stabilizes ATP-citrate lyase to promote lipid biosynthesis and tumor growth. Mol Cell 2013; 51: 506-518.
55. Malatesta M, Steinhauer C, Mohammad F, Pandey DP, Squatrito M, Helin K. Histone acetyltransferase PCAF is required for Hedgehog-Gli-dependent transcription and cancer cell proliferation. Cancer Res 2013; 73: 6323-6333.
56. Nye MD, Almada LL, Fernandez-Barrena MG, Marks DL, Elsawa SF, Vrabel A, et al. The transcription factor GLI1 interacts with SMAD proteins to modulate transforming growth factor beta-induced gene expression in a p300/CREB-binding protein-associated factor (PCAF)-dependent manner. J Biol Chem 2014; 289: 15495-15506.
57. Gong AY, Eischeid AN, Xiao J, Zhao J, Chen D, Wang ZY, et al. miR-17-5p targets the p300/CBP-associated factor and modulates androgen receptor transcriptional activity in cultured prostate cancer cells. BMC Cancer 2012; 12: 492.
58. Ge X, Jin Q, Zhang F, Yan T, Zhai Q. PCAF acetylates {beta}-catenin and improves its stability. Mol Biol Cell 2009; 20: 419-427.
59. Chrivia JC, Kwok RP, Lamb N, Hagiwara M, Montminy MR, Goodman RH. Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 1993; 365: 855-859.
60. Stein RW, Corrigan M, Yaciuk P, Whelan J, Moran E. Analysis of E1A-mediated growth regulation functions: binding of the 300-kilodalton cellular product correlates with E1A enhancer repression function and DNA synthesis-inducing activity. J Virol 1990; 64: 4421-4427.
61. Arany Z, Sellers WR, Livingston DM, Eckner R. E1A-associated p300 and CREBassociated CBP belong to a conserved family of coactivators. Cell 1994; 77: 799-800.
62. Shi D, Pop MS, Kulikov R, Love IM, Kung AL, Grossman SR. CBP and p300 are cytoplasmic E4 polyubiquitin ligases for p53. Proc Natl Acad Sci USA 2009; 106: 16275-16280.
63. Zhong J, Ding L, Bohrer LR, Pan Y, Liu P, Zhang J, et al. p300 acetyltransferase regulates androgen receptor degradation and PTEN-deficient prostate tumorigenesis. Cancer Res 2014; 74: 1870-1880.
64. Bedford DC, Kasper LH, Fukuyama T, Brindle PK. Target gene context influences the transcriptional requirement for the KAT3 family of CBP and p300 histone acetyltransferases. Epigenetics 2010; 5: 9-15.
65. Rebel VI, Kung AL, Tanner EA, Yang H, Bronson RT, Livingston DM. Distinct roles for CREB-binding protein and p300 in hematopoietic stem cell self-renewal. Proc Natl Acad Sci USA 2002; 99: 14789-14794.
66. Chen R, Xu M, Hogg RT, Li J, Little B, Gerard RD, et al. The acetylase/deacetylase couple CREB-binding protein/sirtuin 1 controls hypoxia-inducible factor 2 signaling. J Biol Chem 2012; 287: 30800-30811.
67. Gu J, Milligan J, Huang LE. Molecular mechanism of hypoxia-inducible factor 1alpha -p300 interaction. A leucine-rich interface regulated by a single cysteine. J Biol Chem 2001; 276: 3550-3554.
68. Ianculescu I, Wu DY, Siegmund KD, Stallcup MR. Selective roles for cAMP response element-binding protein binding protein and p300 protein as coregulators for androgen-regulated gene expression in advanced prostate cancer cells. J Biol Chem 2012; 287: 4000-4013.
69. Santer FR, Hoschele PP, Oh SJ, Erb HH, Bouchal J, Cavarretta IT, et al. Inhibition of the acetyltransferases p300 and CBP reveals a targetable function for p300 in the survival and invasion pathways of prostate cancer cell lines. Mol Cancer Ther 2011; 10: 1644-1655.
70. Miller RW, Rubinstein JH. Tumors in Rubinstein-Taybi syndrome. Am J Med Genet 1995; 56: 112-115.
71. Zimmer SN, Lemieux ME, Karia BP, Day C, Zhou T, Zhou Q, et al. Mice heterozygous for CREB binding protein are hypersensitive to gamma-radiation and invariably develop myelodysplastic/myeloproliferative neoplasm. Exp Hematol 2012; 40: 295-306 e5.
72. Gui Y, Guo G, Huang Y, Hu X, Tang A, Gao S, et al. Frequent mutations of chromatin remodeling genes in transitional cell carcinoma of the bladder. Nat Genet 2011; 43: 875-878.
73. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, et al. Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature 2011; 471: 189-195.
74. Mullighan CG, Zhang J, Kasper LH, Lerach S, Payne-Turner D, Phillips LA, et al. CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature 2011; 471: 235-239.
75. Ionov Y, Matsui S, Cowell JK. A role for p300/CREB binding protein genes in promoting cancer progression in colon cancer cell lines with microsatellite instability. Proc Natl Acad Sci USA 2004; 101: 1273-1278.
76. Wang F, Marshall CB, Ikura M. Transcriptional/epigenetic regulator CBP/p300 in tumorigenesis: structural and functional versatility in target recognition. Cell Mol Life Sci 2013; 70: 3989-4008.
77. Pattabiraman DR, Sun J, Dowhan DH, Ishii S, Gonda TJ. Mutations in multiple domains of c-Myb disrupt interaction with CBP/p300 and abrogate myeloid transforming ability. Mol Cancer Res 2009; 7: 1477-1486.
78. Pattabiraman DR, McGirr C, Shakhbazov K, Barbier V, Krishnan K, Mukhopadhyay P, et al. Interaction of c-Myb with p300 is required for the induction of acute myeloid leukemia (AML) by human AML oncogenes. Blood 2014; 123: 2682-2690.
79. Gao Y, Geng J, Hong X, Qi J, Teng Y, Yang Y, et al. Expression of p300 and CBP is associated with poor prognosis in small cell lung cancer. Int J Clin Exp Pathol 2014; 7: 760-767.
80. Liao ZW, Zhou TC, Tan XJ, Song XL, Liu Y, Shi XY, et al. High expression of p300 is linked to aggressive features and poor prognosis of nasopharyngeal carcinoma. J Transl Med 2012; 10: 110.
81. Rotte A, Bhandaru M, Cheng Y, Sjoestroem C, Martinka M, Li G. Decreased expression of nuclear p300 is associated with disease progression and worse prognosis of melanoma patients. PLoS One 2013; 8: e75405.
82. Takeuchi A, Shiota M, Tatsugami K, Yokomizo A, Tanaka S, Kuroiwa K, et al. p300 mediates cellular resistance to doxorubicin in bladder cancer. Mol Med Rep 2012; 5: 173-176.
83. Lee SO, Chun JY, Nadiminty N, Lou W, Feng S, Gao AC. Interleukin-4 activates androgen receptor through CBP/p300. Prostate 2009; 69: 126-132.
84. Yoshida M, Miyoshi I, Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci USA 1982; 79: 2031-2035.
85. Bex F, Yin MJ, Burny A, Gaynor RB. Differential transcriptional activation by human T-cell leukemia virus type 1 Tax mutants is mediated by distinct interactions with CREB binding protein and p300. Mol Cell Biol 1998; 18: 2392-2405.
86. Suzuki T, Uchida-Toita M, Yoshida M. Tax protein of HTLV-1 inhibits CBP/p300- mediated transcription by interfering with recruitment of CBP/p300 onto DNA element of E-box or p53 binding site. Oncogene 1999; 18: 4137-4143.
87. Eckner R, Ludlow JW, Lill NL, Oldread E, Arany Z, Modjtahedi N, et al. Association of p300 and CBP with simian virus 40 large T antigen. Mol Cell Biol 1996; 16: 3454-3464.
88. Valls E, de la Cruz X, Martinez-Balbas MA. The SV40 T antigen modulates CBP histone acetyltransferase activity. Nucleic Acids Res 2003; 31: 3114-3122.
89. Ahuja D, Saenz-Robles MT, Pipas JM. SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation. Oncogene 2005; 24: 7729-7745.
90. Saenz Robles MT, Shivalila C, Wano J, Sorrells S, Roos A, Pipas JM. Two independent regions of simian virus 40 T antigen increase CBP/p300 levels, alter patterns of cellular histone acetylation, and immortalize primary cells. J Virol 2013; 87: 13499-13509.
91. Patel D, Huang SM, Baglia LA, McCance DJ. The E6 protein of human papillomavirus type 16 binds to and inhibits co-activation by CBP and p300. EMBO J 1999; 18: 5061-5072.
92. Arany Z, Newsome D, Oldread E, Livingston DM, Eckner R. A family of transcriptional adaptor proteins targeted by the E1A oncoprotein. Nature 1995; 374: 81-84.
93. Ferrari R, Pellegrini M, Horwitz GA, Xie W, Berk AJ, Kurdistani SK. Epigenetic reprogramming by adenovirus e1a. Science 2008; 321: 1086-1088.
94. Inuzuka H, Gao D, Finley LW, Yang W, Wan L, Fukushima H, et al. Acetylationdependent regulation of Skp2 function. Cell 2012; 150: 179-193.
95. Ikura T, Ogryzko VV, Grigoriev M, Groisman R, Wang J, Horikoshi M, et al. Involvement of the TIP60 histone acetylase complex in DNA repair and apoptosis. Cell 2000; 102: 463-473.
96. Fuchs M, Gerber J, Drapkin R, Sif S, Ikura T, Ogryzko V, et al. The p400 complex is an essential E1A transformation target. Cell 2001; 106: 297-307.
97. Kimura A, Horikoshi M. Tip60 acetylates six lysines of a specific class in core histones in vitro. Genes Cells 1998; 3: 789-800.
98. Legube G, Linares LK, Lemercier C, Scheffner M, Khochbin S, Trouche D. Tip60 is targeted to proteasome-mediated degradation by Mdm2 and accumulates after UV irradiation. EMBO J 2002; 21: 1704-1712.
99. Sun Y, Jiang X, Chen S, Fernandes N, Price BD. A role for the Tip60 histone acetyltransferase in the acetylation and activation of ATM. Proc Natl Acad Sci USA 2005; 102: 13182-13187.
100. Sun Y, Jiang X, Price BD. Tip60: connecting chromatin to DNA damage signaling. Cell Cycle 2010; 9: 930-936.
101. Sun Y, Jiang X, Xu Y, Ayrapetov MK, Moreau LA, Whetstine JR, et al. Histone H3 methylation links DNA damage detection to activation of the tumour suppressor Tip60. Nat Cell Biol 2009; 11: 1376-1382.
102. Kusch T, Florens L, Macdonald WH, Swanson SK, Glaser RL, Yates JR 3rd, et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions. Science 2004; 306: 2084-2087.
103. Van Den Broeck A, Nissou D, Brambilla E, Eymin B, Gazzeri S. Activation of a Tip60/E2F1/ERCC1 network in human lung adenocarcinoma cells exposed to cisplatin. Carcinogenesis 2012; 33: 320-325.
104. Sykes SM, Mellert HS, Holbert MA, Li K, Marmorstein R, Lane WS, et al. Acetylation of the p53 DNA-binding domain regulates apoptosis induction. Mol Cell 2006; 24: 841-851.
105. Tang Y, Luo J, Zhang W, Gu W. Tip60-dependent acetylation of p53 modulates the decision between cell-cycle arrest and apoptosis. Mol Cell 2006; 24: 827-839.
106. Jiang Z, Kamath R, Jin S, Balasubramani M, Pandita TK, Rajasekaran B. Tip60-mediated acetylation activates transcription independent apoptotic activity of Abl. Mol Cancer 2011; 10: 88.
107. Brady ME, Ozanne DM, Gaughan L, Waite I, Cook S, Neal DE, et al. Tip60 is a nuclear hormone receptor coactivator. J Biol Chem 1999; 274: 17599-17604.
108. Gaughan L, Brady ME, Cook S, Neal DE, Robson CN. Tip60 is a co-activator specific for class I nuclear hormone receptors. J Biol Chem 2001; 276: 46841-46848.
109. Gaughan L, Logan IR, Cook S, Neal DE, Robson CN. Tip60 and histone deacetylase 1 regulate androgen receptor activity through changes to the acetylation status of the receptor. J Biol Chem 2002; 277: 25904-25913.
110. Jeong KW, Kim K, Situ AJ, Ulmer TS, An W, Stallcup MR. Recognition of enhancer element-specific histone methylation by TIP60 in transcriptional activation. Nat Struct Mol Biol 2011; 18: 1358-1365.
111. Xiao H, Chung J, Kao HY, Yang YC. Tip60 is a co-repressor for STAT3. J Biol Chem 2003; 278: 11197-11204.
112. Zhao H, Jin S, Gewirtz AM. The histone acetyltransferase TIP60 interacts with c-Myb and inactivates its transcriptional activity in human leukemia. J Biol Chem 2012; 287: 925-934.
113. Chevillard-Briet M, Quaranta M, Grezy A, Mattera L, Courilleau C, Philippe M, et al. Interplay between chromatin-modifying enzymes controls colon cancer progression through Wnt signaling. Hum Mol Genet 2014; 23: 2120-2131.
114. Gorrini C, Squatrito M, Luise C, Syed N, Perna D, Wark L, et al. Tip60 is a haplo-insufficient tumour suppressor required for an oncogene-induced DNA damage response. Nature 2007; 448: 1063-1067.
115. Harris AW, Pinkert CA, Crawford M, Langdon WY, Brinster RL, Adams JM. The E mu-myc transgenic mouse. A model for high-incidence spontaneous lymphoma and leukemia of early B cells. J Exp Med 1988; 167: 353-371.
116. Halkidou K, Gnanapragasam VJ, Mehta PB, Logan IR, Brady ME, Cook S, et al. Expression of Tip60, an androgen receptor coactivator, and its role in prostate cancer development. Oncogene 2003; 22: 2466-2477.
117. ME LL, Vidal F, Gallardo D, Diaz-Fuertes M, Rojo F, Cuatrecasas M, et al. New p53 related genes in human tumors: significant downregulation in colon and lung carcinomas. Oncol Rep 2006; 16: 603-608.
118. Mattera L, Escaffit F, Pillaire MJ, Selves J, Tyteca S, Hoffmann JS, et al. The p400/Tip60 ratio is critical for colorectal cancer cell proliferation through DNA damage response pathways. Oncogene 2009; 28: 1506-1517.
119. Chen G, Cheng Y, Tang Y, Martinka M, Li G. Role of Tip60 in human melanoma cell migration, metastasis, and patient survival. J Invest Dermatol 2012; 132: 2632-2641.
120. Miyamoto N, Izumi H, Noguchi T, Nakajima Y, Ohmiya Y, Shiota M, et al. Tip60 is regulated by circadian transcription factor clock and is involved in cisplatin resistance. J Biol Chem 2008; 283: 18218-18226.
121. Shiota M, Yokomizo A, Masubuchi D, Tada Y, Inokuchi J, Eto M, et al. Tip60 promotes prostate cancer cell proliferation by translocation of androgen receptor into the nucleus. Prostate 2010; 70: 540-554.
122. Duong MT, Akli S, Macalou S, Biernacka A, Debeb BG, Yi M, et al. Hbo1 is a cyclin E/CDK2 substrate that enriches breast cancer stem-like cells. Cancer Res 2013; 73: 5556-5568.
123. Borrow J, Stanton VP Jr, Andresen JM, Becher R, Behm FG, Chaganti RS, et al. The translocation t(8;16)(p11;p13) of acute myeloid leukaemia fuses a putative acetyltransferase to the CREB-binding protein. Nat Genet 1996; 14: 33-41.
124. Kitabayashi I, Aikawa Y, Nguyen LA, Yokoyama A, Ohki M. Activation of AML1-mediated transcription by MOZ and inhibition by the MOZ-CBP fusion protein. EMBO J 2001; 20: 7184-7196.
125. Rauh D, Fischer F, Gertz M, Lakshminarasimhan M, Bergbrede T, Aladini F, et al. An acetylome peptide microarray reveals specificities and deacetylation substrates for all human sirtuin isoforms. Nat Commun 2013; 4: 2327.
126. Choudhary C, Kumar C, Gnad F, Nielsen ML, Rehman M, Walther TC, et al. Lysine acetylation targets protein complexes and co-regulates major cellular functions. Science 2009; 325: 834-840.
127. Martinez-Balbas MA, Bauer UM, Nielsen SJ, Brehm A, Kouzarides T. Regulation of E2F1 activity by acetylation. EMBO J 2000; 19: 662-671.
128. Okumura K, Mendoza M, Bachoo RM, DePinho RA, Cavenee WK, Furnari FB. PCAF modulates PTEN activity. J Biol Chem 2006; 281: 26562-26568.
129. Thevenet L, Mejean C, Moniot B, Bonneaud N, Galeotti N, Aldrian-Herrada G, et al. Regulation of human SRY subcellular distribution by its acetylation/deacetylation. EMBO J 2004; 23: 3336-3345.
130. Li M, Luo J, Brooks CL, Gu W. Acetylation of p53 inhibits its ubiquitination by Mdm2. J Biol Chem 2002; 277: 50607-50611.
131. Yu X, Guo ZS, Marcu MG, Neckers L, Nguyen DM, Chen GA, et al. Modulation of p53, ErbB1, ErbB2, and Raf-1 expression in lung cancer cells by depsipeptide FR901228. J Natl Cancer Inst 2002; 94: 504-513.
132. Scroggins BT, Robzyk K, Wang D, Marcu MG, Tsutsumi S, Beebe K, et al. An acetylation site in the middle domain of Hsp90 regulates chaperone function. Mol Cell 2007; 25: 151-159.
133. Hallows WC, Yu W, Denu JM. Regulation of glycolytic enzyme phosphoglycerate mutase-1 by Sirt1 protein-mediated deacetylation. J Biol Chem2012; 287: 3850-3858.
134. Schwer B, Bunkenborg J, Verdin RO, Andersen JS, Verdin E. Reversible lysine acetylation controls the activity of the mitochondrial enzyme acetyl-CoA synthetase 2. Proc Natl Acad Sci USA 2006; 103: 10224-10229.
135. Zhao S, Xu W, Jiang W, Yu W, Lin Y, Zhang T, et al. Regulation of cellular metabolism by protein lysine acetylation. Science 2010; 327: 1000-1004.
136. Khan O, La Thangue NB. HDAC inhibitors in cancer biology: emerging mechanisms and clinical applications. Immunol Cell Biol 2012; 90: 85-94.
137. Kalac M, Scotto L, Marchi E, Amengual J, Seshan VE, Bhagat G, et al. HDAC inhibitors and decitabine are highly synergistic and associated with unique gene-expression and epigenetic profiles in models of DLBCL. Blood 2011; 118: 5506-5516.
138. Santoro F, Botrugno OA, Dal Zuffo R, Pallavicini I, Matthews GM, Cluse L, et al. A dual role for Hdac1: oncosuppressor in tumorigenesis, oncogene in tumor maintenance. Blood 2013; 121: 3459-3468.
139. Grant PA, Duggan L, Cote J, Roberts SM, Brownell JE, Candau R, et al. Yeast Gcn5 functions in two multisubunit complexes to acetylate nucleosomal histones: characterization of an Ada complex and the SAGA (Spt/Ada) complex. Genes Dev 1997; 11: 1640-1650.
140. Balasubramanian R, Pray-Grant MG, Selleck W, Grant PA, Tan S. Role of the Ada2 and Ada3 transcriptional coactivators in histone acetylation. J Biol Chem 2002; 277: 7989-7995.
141. Thompson PR, Wang D, Wang L, Fulco M, Pediconi N, Zhang D, et al. Regulation of the p300 HAT domain via a novel activation loop. Nat Struct Mol Biol 2004; 11: 308-315.
142. Sun B, Guo S, Tang Q, Li C, Zeng R, Xiong Z, et al. Regulation of the histone acetyltransferase activity of hMOF via autoacetylation of Lys274. Cell Res 2011; 21: 1262-1266.
143. Santos-Rosa H, Valls E, Kouzarides T, Martinez-Balbas M. Mechanisms of P/CAF auto-acetylation. Nucleic Acids Res 2003; 31: 4285-4292.
144. Herrera JE, Bergel M, Yang XJ, Nakatani Y, Bustin M. The histone acetyltransferase activity of human GCN5 and PCAF is stabilized by coenzymes. J Biol Chem 1997; 272: 27253-27258.
145. Chimenti F, Bizzarri B, Maccioni E, Secci D, Bolasco A, Chimenti P, et al. A novel histone acetyltransferase inhibitor modulating Gcn5 network: cyclopentylidene- [4-(4′-chlorophenyl)thiazol-2-yl)hydrazone. J Med Chem 2009; 52: 530-536.
146. Trisciuoglio D, Ragazzoni Y, Pelosi A, Desideri M, Carradori S, Gabellini C, et al. CPTH6, a thiazole derivative, induces histone hypoacetylation and apoptosis in human leukemia cells. Clin Cancer Res 2012; 18: 475-486.
147. Secci D, Carradori S, Bizzarri B, Bolasco A, Ballario P, Patramani Z, et al. Synthesis of a novel series of thiazole-based histone acetyltransferase inhibitors. Bioorg Med Chem 2014; 22: 1680-1689.
148. Lau OD, Kundu TK, Soccio RE, Ait-Si-Ali S, Khalil EM, Vassilev A, et al. HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol Cell 2000; 5: 589-595.
149. Balasubramanyam K, Swaminathan V, Ranganathan A, Kundu TK. Small molecule modulators of histone acetyltransferase p300. J Biol Chem2003; 278: 19134-19140.
150. Sung B, Pandey MK, Ahn KS, Yi T, Chaturvedi MM, Liu M, et al. Anacardic acid (6-nonadecyl salicylic acid), an inhibitor of histone acetyltransferase, suppresses expression of nuclear factor-kappaB-regulated gene products involved in cell survival, proliferation, invasion, and inflammation through inhibition of the inhibitory subunit of nuclear factor-kappaBalpha kinase, leading to potentiation of apoptosis. Blood 2008; 111: 4880-4891.
151. Ghizzoni M, Boltjes A, Graaf C, Haisma HJ, Dekker FJ. Improved inhibition of the histone acetyltransferase PCAF by an anacardic acid derivative. Bioorg Med Chem 2010; 18: 5826-5834.
152. Saadat N, Gupta SV. Potential role of garcinol as an anticancer agent. J Oncol 2012; 2012: 647206.
153. Balasubramanyam K, Altaf M, Varier RA, Swaminathan V, Ravindran A, Sadhale PP, et al. Polyisoprenylated benzophenone, garcinol, a natural histone acetyltransferase inhibitor, represses chromatin transcription and alters global gene expression. J Biol Chem 2004; 279: 33716-33726.
154. Arif M, Pradhan SK, Thanuja GR, Vedamurthy BM, Agrawal S, Dasgupta D, et al. Mechanism of p300 specific histone acetyltransferase inhibition by small molecules. J Med Chem 2009; 52: 267-277.
155. Ye X, Yuan L, Zhang L, Zhao J, Zhang CM, Deng HY. Garcinol, an acetyltransferase inhibitor, suppresses proliferation of breast cancer cell line MCF-7 promoted by 17beta-estradiol. Asian Pac J Cancer Prev 2014; 15: 5001-5007.
156. Ahmad A, Wang Z, Ali R, Maitah MY, Kong D, Banerjee S, et al. Apoptosis-inducing effect of garcinol is mediated by NF-kappaB signaling in breast cancer cells. J Cell Biochem 2010; 109: 1134-1141.
157. Ahmad A, Sarkar SH, Bitar B, Ali S, Aboukameel A, Sethi S, et al. Garcinol regulates EMT and Wnt signaling pathways in vitro and in vivo, leading to anticancer activity against breast cancer cells. Mol Cancer Ther 2012; 11: 2193-2201.
158. Yu SY, Liao CH, Chien MH, Tsai TY, Lin JK, Weng MS. Induction of p21(Waf1/Cip1) by garcinol via downregulation of p38-MAPK signaling in p53-independent H1299 lung cancer. J Agric Food Chem 2014; 62: 2085-2095.
159. Ahmad A, Wang Z, Wojewoda C, Ali R, Kong D, Maitah MY, et al. Garcinol-induced apoptosis in prostate and pancreatic cancer cells is mediated by NF- kappaB signaling. Front Biosci 2011; 3: 1483-1492.
160. Sethi G, Chatterjee S, Rajendran P, Li F, Shanmugam MK, Wong KF, et al. Inhibition of STAT3 dimerization and acetylation by garcinol suppresses the growth of human hepatocellular carcinoma in vitro and in vivo. Mol Cancer 2014; 13: 66.
161. Li F, Shanmugam MK, Chen L, Chatterjee S, Basha J, Kumar AP, et al. Garcinol, a polyisoprenylated benzophenone modulates multiple proinflammatory signaling cascades leading to the suppression of growth and survival of head and neck carcinoma. Cancer Prev Res 2013; 6: 843-854.
162. Stimson L, Rowlands MG, Newbatt YM, Smith NF, Raynaud FI, Rogers P, et al. Isothiazolones as inhibitors of PCAF and p300 histone acetyltransferase activity. Mol Cancer Ther 2005; 4: 1521-1532.
163. Zheng Y, Balasubramanyam K, Cebrat M, Buck D, Guidez F, Zelent A, et al. Synthesis and evaluation of a potent and selective cell-permeable p300 histone acetyltransferase inhibitor. J Am Chem Soc 2005; 127: 17182-17183.
164. Marcu MG, Jung YJ, Lee S, Chung EJ, Lee MJ, Trepel J, et al. Curcumin is an inhibitor of p300 histone acetylatransferase. Med Chem 2006; 2: 169-174.
165. Balasubramanyam K, Varier RA, Altaf M, Swaminathan V, Siddappa NB, Ranga U, et al. Curcumin, a novel p300/CREB-binding protein-specific inhibitor of acetyltransferase, represses the acetylation of histone/nonhistone proteins and histone acetyltransferase-dependent chromatin transcription. J Biol Chem 2004; 279: 51163-51171.
166. Shah S, Prasad S, Knudsen KE. Targeting pioneering factor and hormone receptor cooperative pathways to suppress tumor progression. Cancer Res 2012; 72: 1248-1259.
167. Teiten MH, Gaascht F, Cronauer M, Henry E, Dicato M, Diederich M. Anti-proliferative potential of curcumin in androgen-dependent prostate cancer cells occurs through modulation of the Wingless signaling pathway. Int J Oncol 2011; 38: 603-611.
168. Emami KH, Nguyen C, Ma H, Kim DH, Jeong KW, Eguchi M, et al. A small molecule inhibitor of beta-catenin/CREB-binding protein transcription [corrected]. Proc Natl Acad Sci USA 2004; 101: 12682-12687.
169. Gang EJ, Hsieh YT, Pham J, Zhao Y, Nguyen C, Huantes S, et al. Small-molecule inhibition of CBP/catenin interactions eliminates drug-resistant clones in acute lymphoblastic leukemia. Oncogene 2014; 33: 2169-2178.
170. Lu H, Li Y, Shu M, Tang J, Huang Y, Zhou Y, et al. Hypoxia-inducible factor-1alpha blocks differentiation of malignant gliomas. FEBS J 2009; 276: 7291-7304.
171. Bowers EM, Yan G, Mukherjee C, Orry A, Wang L, Holbert MA, et al. Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem Biol 2010; 17: 471-482.
172. Gao XN, Lin J, Ning QY, Gao L, Yao YS, Zhou JH, et al. A histone acetyltransferase p300 inhibitor C646 induces cell cycle arrest and apoptosis selectively in AML1- ETO-positive AML cells. PLoS One 2013; 8: e55481.
173. Yan G, Eller MS, Elm C, Larocca CA, Ryu B, Panova IP, et al. Selective inhibition of p300 HAT blocks cell cycle progression, induces cellular senescence, and inhibits the DNA damage response in melanoma cells. J Invest Dermatol 2013; 133: 2444-2452.
174. Liu Y, Wang L, Predina J, Han R, Beier UH, Wang LC, et al. Inhibition of p300 impairs Foxp3(+) T regulatory cell function and promotes antitumor immunity. Nat Med 2013; 19: 1173-1177.
175. Ravindra KC, Selvi BR, Arif M, Reddy BA, Thanuja GR, Agrawal S, et al. Inhibition of lysine acetyltransferase KAT3B/p300 activity by a naturally occurring hydroxynaphthoquinone, plumbagin. J Biol Chem 2009; 284: 24453-24464.
176. Tohyama S, Tomura A, Ikeda N, Hatano M, Odanaka J, Kubota Y, et al. Discovery and characterization of NK13650s, naturally occurring p300-selective histone acetyltransferase inhibitors. J Org Chem 2012; 77: 9044-9052.
177. Yin S, Kaluz S, Devi NS, Jabbar AA, de Noronha RG, Mun J, et al. Arylsulfonamide KCN1 inhibits in vivo glioma growth and interferes with HIF signaling by disrupting HIF-1alpha interaction with cofactors p300/CBP. Clin Cancer Res 2012; 18: 6623-6633.
178. Yang H, Pinello CE, Luo J, Li D, Wang Y, Zhao LY, et al. Small-molecule inhibitors of acetyltransferase p300 identified by high-throughput screening are potent anticancer agents. Mol Cancer Ther 2013; 12: 610-620.
179. Kushal S, Lao BB, Henchey LK, Dubey R, Mesallati H, Traaseth NJ, et al. Protein domain mimetics as in vivo modulators of hypoxia-inducible factor signaling. Proc Natl Acad Sci USA 2013; 110: 15602-15607.
180. Hao J, Ao A, Zhou L, Murphy CK, Frist AY, Keel JJ, et al. Selective small molecule targeting beta-catenin function discovered by in vivo chemical genetic screen. Cell Rep 2013; 4: 898-904.
181. Xie X, Piao L, Bullock BN, Smith A, Su T, Zhang M, et al. Targeting HPV16 E6-p300 interaction reactivates p53 and inhibits the tumorigenicity of HPV-positive head and neck squamous cell carcinoma. Oncogene 2014; 33: 1037-1046.
182. Ghizzoni M, Wu J, Gao T, Haisma HJ, Dekker FJ, George Zheng Y. 6-alkylsalicylates are selective Tip60 inhibitors and target the acetyl-CoA binding site. Eur J Med Chem 2012; 47: 337-344.
183. Sun Y, Jiang X, Chen S, Price BD. Inhibition of histone acetyltransferase activity by anacardic acid sensitizes tumor cells to ionizing radiation. FEBS Lett 2006; 580: 4353-4356.
184. Kobayashi J, Kato A, Ota Y, Ohba R, Komatsu K. Bisbenzamidine derivative, pentamidine represses DNA damage response through inhibition of histone H2A acetylation. Mol Cancer 2010; 9: 34.
185. Coffey K, Blackburn TJ, Cook S, Golding BT, Griffin RJ, Hardcastle IR, et al. Characterisation of a Tip60 specific inhibitor, NU9056, in prostate cancer. PLoS One 2012; 7: e45539.
186. Gao C, Bourke E, Scobie M, Famme MA, Koolmeister T, Helleday T, et al. Rational design and validation of a Tip60 histone acetyltransferase inhibitor. Sci Rep 2014; 4: 5372.
187. Prinjha RK, Witherington J, Lee K. Place your BETs: the therapeutic potential of bromodomains. Trends Pharmacol Sci 2012; 33: 146-153.
188. Loven J, Hoke HA, Lin CY, Lau A, Orlando DA, Vakoc CR, et al. Selective inhibition of tumor oncogenes by disruption of super-enhancers. Cell 2013; 153: 320-334.
189. Gao L, Schwartzman J, Gibbs A, Lisac R, Kleinschmidt R, Wilmot B, et al. Androgen receptor promotes ligand-independent prostate cancer progression through c-Myc upregulation. PLoS One 2013; 8: e63563.
190. Filippakopoulos P, Knapp S. Targeting bromodomains: epigenetic readers of lysine acetylation. Nat Rev Drug Discov 2014; 13: 337-356.
191. Fiskus W, Sharma S, Qi J, Valenta JA, Schaub LJ, Shah B, et al. Highly active combination of BRD4 antagonist and histone deacetylase inhibitor against human acute myelogenous leukemia cells. Mol Cancer Ther 2014; 13: 1142-1154.
192. Kurdistani SK. Histone modifications as markers of cancer prognosis: a cellular view. Br J Cancer 2007; 97: 1-5.