Advertisement

Frontiers in Biology

, Volume 13, Issue 3, pp 168–179 | Cite as

CBP/p300: intramolecular and intermolecular regulations

  • Yongming XueEmail author
  • Hong Wen
  • Xiaobing ShiEmail author
Review
  • 54 Downloads

Abstract

Background

CREB binding protein (CBP) and its close paralogue p300 are transcriptional coactivators with intrinsic acetyltransferase activity. Both CBP/p300 play critical roles in development and diseases. The enzymatic and biological functions of CBP/p300 are tightly regulated by themselves and by external factors. However, a comprehensive up-to-date review of the intramolecular and intermolecular regulations is lacking.

Objective

To summarize the molecular mechanisms regulating CBP/p300s functions.

Methods

A systematic literature search was conducted using the PubMed (https://doi.org/www.ncbi.nlm.nih.gov/pubmed/) for literatures published during 1985–2018. Keywords “CBP regulation” or “p300 regulation” were used for the search.

Results

The functions of CBP/p300, especially their acetyltransferase activity and chromatin association, are regulated both intramolecularly by their autoinhibitory loop (AIL), bromodomain, and PHD-RING region and intermolecularly by their interacting partners. The intramolecular mechanisms equip CBP/p300 with the capability of self-regulation while the intermolecular mechanisms allow them to respond to various cell signaling pathways.

Conclusion

Investigations into those regulation mechanisms are crucial to our understanding of CBP/p300s role in development and pathogenesis. Pharmacological interventions targeting these regulatory mechanisms have therapeutic potentials.

Keywords

p300 CBP histone acetylation autoacetylation HAT 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Notes

Acknowledgments

We thank members of the Shi laboratory for discussions. This work was supported in part by grants from NIH/NCI (CA204020) and Leukemia & Lymphoma Society (1339-17) to X.S.. X.S. is a Scientific Advisory Board member of EpiCypher.

References

  1. Arany Z, Sellers W R, Livingston D M, Eckner R (1994). E1Aassociated p300 and CREB-associated CBP belong to a conserved family of coactivators. Cell, 77(6): 799–800PubMedCrossRefGoogle Scholar
  2. Bannister A J, Kouzarides T (1996). The CBP co-activator is a histone acetyltransferase. Nature, 384(6610): 641–643PubMedCrossRefGoogle Scholar
  3. Berk A J (2005). Recent lessons in gene expression, cell cycle control, and cell biology from adenovirus. Oncogene, 24(52): 7673–7685PubMedCrossRefGoogle Scholar
  4. Best J L, Amezcua C A, Mayr B, Flechner L, Murawsky C M, Emerson B, Zor T, Gardner K H, Montminy M (2004). Identification of small-molecule antagonists that inhibit an activator: coactivator interaction. Proc Natl Acad Sci USA, 101(51): 17622–17627PubMedCrossRefGoogle Scholar
  5. Black J C, Choi J E, Lombardo S R, Carey M (2006). A mechanism for coordinating chromatin modification and preinitiation complex assembly. Mol Cell, 23(6): 809–818PubMedCrossRefGoogle Scholar
  6. Block K M, Wang H, Szabó L Z, Polaske NW, Henchey L K, Dubey R, Kushal S, László C F, Makhoul J, Song Z, Meuillet E J, Olenyuk B Z (2009). Direct inhibition of hypoxia-inducible transcription factor complex with designed dimeric epidithiodiketopiperazine. J Am Chem Soc, 131(50): 18078–18088PubMedPubMedCentralCrossRefGoogle Scholar
  7. Bose D A, Donahue G, Reinberg D, Shiekhattar R, Bonasio R, Berger S L (2017). RNA Binding to CBP Stimulates Histone Acetylation and Transcription. Cell 168, 135–149 e122Google Scholar
  8. Bowers E M, Yan G, Mukherjee C, Orry A, Wang L, Holbert M A, Crump N T, Hazzalin C A, Liszczak G, Yuan H, Larocca C, Saldanha S A, Abagyan R, Sun Y, Meyers D J, Marmorstein R, Mahadevan L C, Alani R M, Cole P A (2010). Virtual ligand screening of the p300/CBP histone acetyltransferase: identification of a selective small molecule inhibitor. Chem Biol, 17(5): 471–482PubMedPubMedCentralCrossRefGoogle Scholar
  9. Ceschin D G, Walia M, Wenk S S, Duboé C, Gaudon C, Xiao Y, Fauquier L, Sankar M, Vandel L, Gronemeyer H (2011). Methylation specifies distinct estrogen-induced binding site repertoires of CBP to chromatin. Genes Dev, 25(11): 1132–1146PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chakravarti D, La Morte V J, Nelson MC, Nakajima T, Schulman I G, Juguilon H, Montminy M, Evans RM (1996). Role of CBP/P300 in nuclear receptor signalling. Nature, 383(6595): 99–103PubMedCrossRefGoogle Scholar
  11. Chakravarti D, Ogryzko V, Kao H Y, Nash A, Chen H, Nakatani Y, Evans R M (1999). A viral mechanism for inhibition of p300 and PCAF acetyltransferase activity. Cell, 96(3): 393–403PubMedCrossRefGoogle Scholar
  12. Chan H M, La Thangue N B (2001). p300/CBP proteins: HATs for transcriptional bridges and scaffolds. J Cell Sci, 114(Pt 13): 2363–2373PubMedGoogle Scholar
  13. Chen C C, Carson J J, Feser J, Tamburini B, Zabaronick S, Linger J, Tyler J K (2008). Acetylated lysine 56 on histone H3 drives chromatin assembly after repair and signals for the completion of repair. Cell, 134(2): 231–243PubMedPubMedCentralCrossRefGoogle Scholar
  14. Chen, J., and Li, Q. (2011). Life and death of transcriptional co-activator p300. Epigenetics: official journal of the DNA Methylation Society 6, 957–961.CrossRefGoogle Scholar
  15. Chen Y J, Wang Y N, Chang W C (2007). ERK2-mediated C-terminal serine phosphorylation of p300 is vital to the regulation of epidermal growth factor-induced keratin 16 gene expression. J Biol Chem, 282 (37): 27215–27228PubMedCrossRefGoogle Scholar
  16. Chevillard-Briet M, Trouche D, Vandel L (2002). Control of CBP coactivating activity by arginine methylation. EMBO J, 21(20): 5457–5466PubMedPubMedCentralCrossRefGoogle Scholar
  17. Chrivia J C, Kwok R P, Lamb N, Hagiwara M, Montminy M R, Goodman R H (1993). Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature, 365(6449): 855–859PubMedCrossRefGoogle Scholar
  18. Conery A R, Centore R C, Neiss A, Keller P J, Joshi S, Spillane K L, Sandy P, Hatton C, Pardo E, Zawadzke L (2016). Bromodomain inhibition of the transcriptional coactivators CBP/EP300 as a therapeutic strategy to target the IRF4 network in multiple myeloma. eLife, 5: e10483PubMedPubMedCentralCrossRefGoogle Scholar
  19. Contreras-Martos S, Piai A, Kosol S, Varadi M, Bekesi A, Lebrun P, Volkov A N, Gevaert K, Pierattelli R, Felli I C, Tompa P (2017). Linking functions: an additional role for an intrinsically disordered linker domain in the transcriptional coactivator CBP. Sci Rep, 7(1): 4676PubMedPubMedCentralCrossRefGoogle Scholar
  20. Dancy B M, Cole P A (2015). Protein lysine acetylation by p300/CBP. Chem Rev, 115(6): 2419–2452PubMedPubMedCentralCrossRefGoogle Scholar
  21. Das C, Lucia MS, Hansen K C, Tyler J K (2009). CBP/p300-mediated acetylation of histone H3 on lysine 56. Nature, 459(7243): 113–117PubMedPubMedCentralCrossRefGoogle Scholar
  22. Das C, Roy S, Namjoshi S, Malarkey C S, Jones D N, Kutateladze T G, Churchill M E, Tyler J K (2014). Binding of the histone chaperone ASF1 to the CBP bromodomain promotes histone acetylation. Proc Natl Acad Sci USA, 111(12): E1072–E1081PubMedCrossRefGoogle Scholar
  23. Debes J D, Sebo T J, Lohse C M, Murphy L M, Haugen D A, Tindall D J (2003). p300 in prostate cancer proliferation and progression. Cancer Res, 63(22): 7638–7640PubMedGoogle Scholar
  24. Delvecchio M, Gaucher J, Aguilar-Gurrieri C, Ortega E, Panne D (2013). Structure of the p300 catalytic core and implications for chromatin targeting and HAT regulation. Nat Struct Mol Biol, 20(9): 1040–1046PubMedCrossRefGoogle Scholar
  25. Dyson H J, Wright P E (2016). Role of Intrinsic Protein Disorder in the Function and Interactions of the Transcriptional Coactivators CREBbinding Protein (CBP) and p300. J Biol Chem, 291(13): 6714–6722PubMedPubMedCentralCrossRefGoogle Scholar
  26. Eckner R, Ewen M E, Newsome D, Gerdes M, DeCaprio J A, Lawrence J B, Livingston D M (1994). Molecular cloning and functional analysis of the adenovirus E1A-associated 300-kD protein (p300) reveals a protein with properties of a transcriptional adaptor. Genes Dev, 8(8): 869–884PubMedCrossRefGoogle Scholar
  27. Fonte C, Grenier J, Trousson A, Chauchereau A, Lahuna O, Baulieu E E, Schumacher M, Massaad C (2005). Involvement of betacatenin and unusual behavior of CBP and p300 in glucocorticosteroid signaling in Schwann cells. Proc Natl Acad Sci USA, 102(40): 14260–14265PubMedCrossRefGoogle Scholar
  28. Fryer C J, Lamar E, Turbachova I, Kintner C, Jones K A (2002). Mastermind mediates chromatin-specific transcription and turnover of the Notch enhancer complex. Genes Dev, 16(11): 1397–1411PubMedPubMedCentralCrossRefGoogle Scholar
  29. Ghosh S, Taylor A, Chin M, Huang H R, Conery A R, Mertz J A, Salmeron A, Dakle P J, Mele D, Cote A, Jayaram H, Setser J W, Poy F, Hatzivassiliou G, DeAlmeida-Nagata D, Sandy P, Hatton C, Romero F A, Chiang E, Reimer T, Crawford T, Pardo E, Watson V G, Tsui V, Cochran A G, Zawadzke L, Harmange J C, Audia J E, Bryant B M, Cummings R T, Magnuson S R, Grogan J L, Bellon S F, Albrecht B K, Sims R J 3rd, Lora J M (2016). Regulatory T Cell Modulation by CBP/EP300 Bromodomain Inhibition. J Biol Chem, 291(25): 13014–13027PubMedPubMedCentralCrossRefGoogle Scholar
  30. Giotopoulos G, Chan WI, Horton S J, Ruau D, Gallipoli P, Fowler A, Crawley C, Papaemmanuil E, Campbell P J, Göttgens B, Van Deursen J M, Cole P A, Huntly B J (2016). The epigenetic regulators CBP and p300 facilitate leukemogenesis and represent therapeutic targets in acute myeloid leukemia. Oncogene, 35(3): 279–289PubMedCrossRefGoogle Scholar
  31. Girdwood D, Bumpass D, Vaughan O A, Thain A, Anderson L A, Snowden A W, Garcia-Wilson E, Perkins N D, Hay R T (2003). P300 transcriptional repression is mediated by SUMO modification. Mol Cell, 11(4): 1043–1054PubMedCrossRefGoogle Scholar
  32. Goodman R H, Smolik S (2000). CBP/p300 in cell growth, transformation, and development. Genes Dev, 14(13): 1553–1577PubMedGoogle Scholar
  33. Hamamori Y, Sartorelli V, Ogryzko V, Puri P L, Wu H Y, Wang J Y, Nakatani Y, Kedes L (1999). Regulation of histone acetyltransferases p300 and PCAF by the bHLH protein twist and adenoviral oncoprotein E1A. Cell, 96(3): 405–413PubMedCrossRefGoogle Scholar
  34. Hammitzsch A, Tallant C, Fedorov O, O’Mahony A, Brennan P E, Hay D A, Martinez F O, Al-Mossawi M H, de Wit J, Vecellio M, Wells C, Wordsworth P, Müller S, Knapp S, Bowness P (2015). CBP30, a selective CBP/p300 bromodomain inhibitor, suppresses human Th17 responses. Proc Natl Acad Sci USA, 112(34): 10768–10773PubMedCrossRefGoogle Scholar
  35. Hansson M L, Popko-Scibor A E, Saint Just Ribeiro M, Dancy B M, Lindberg M J, Cole P A, Wallberg A E (2009). The transcriptional coactivator MAML1 regulates p300 autoacetylation and HAT activity. Nucleic Acids Res, 37(9): 2996–3006PubMedPubMedCentralCrossRefGoogle Scholar
  36. Heintzman N D, Stuart R K, Hon G, Fu Y, Ching CW, Hawkins R D, Barrera L O, Van Calcar S, Qu C, Ching K A, Wang W, Weng Z, Green R D, Crawford G E, Ren B (2007). Distinct and predictive chromatin signatures of transcriptional promoters and enhancers in the human genome. Nat Genet, 39(3): 311–318PubMedCrossRefGoogle Scholar
  37. Hong L, Schroth G P, Matthews H R, Yau P, Bradbury E M (1993). Studies of the DNA binding properties of histone H4 amino terminus. Thermal denaturation studies reveal that acetylation markedly reduces the binding constant of the H4 “tail” to DNA. J Biol Chem, 268(1): 305–314PubMedGoogle Scholar
  38. Horton S J, Giotopoulos G, Yun H, Vohra S, Sheppard O, Bashford-Rogers R, Rashid M, Clipson A, Chan W I, Sasca D, Yiangou L, Osaki H, Basheer F, Gallipoli P, Burrows N, Erdem A, Sybirna A, Foerster D, Zhao W, Sustic T, Petrunkina Harrison A, Laurenti E, Okosun J, Hodson D, Wright P, Smith K G, Maxwell P, Fitzgibbon J, Du M Q, Adams D J, Huntly B J P (2017). Early loss of Crebbp confers malignant stem cell properties on lymphoid progenitors. Nat Cell Biol, 19(9): 1093–1104PubMedPubMedCentralCrossRefGoogle Scholar
  39. Horwitz G A, Zhang K, McBrian M A, Grunstein M, Kurdistani S K, Berk A J (2008). Adenovirus small e1a alters global patterns of histone modification. Science, 321(5892): 1084–1085PubMedPubMedCentralCrossRefGoogle Scholar
  40. Huang W C, Chen C C (2005). Akt phosphorylation of p300 at Ser-1834 is essential for its histone acetyltransferase and transcriptional activity. Mol Cell Biol, 25(15): 6592–6602PubMedPubMedCentralCrossRefGoogle Scholar
  41. Jang E R, Choi J D, Jeong G, Lee J S (2010). Phosphorylation of p300 by ATM controls the stability of NBS1. Biochem Biophys Res Commun, 397(4): 637–643PubMedCrossRefGoogle Scholar
  42. Jiang Y, Ortega-Molina A, Geng H, Ying H Y, Hatzi K, Parsa S, McNally D, Wang L, Doane A S, Agirre X, Teater M, Meydan C, Li Z, Poloway D, Wang S, Ennishi D, Scott D W, Stengel K R, Kranz J E, Holson E, Sharma S, Young J W, Chu C S, Roeder R G, Shaknovich R, Hiebert S W, Gascoyne R D, Tam W, Elemento O, Wendel H G, Melnick A M (2017). CREBBP Inactivation Promotes the Development of HDAC3-Dependent Lymphomas. Cancer Discov, 7(1): 38–53PubMedCrossRefGoogle Scholar
  43. Jin Q, Yu L R, Wang L, Zhang Z, Kasper L H, Lee J E, Wang C, Brindle P K, Dent S Y, Ge K (2011). Distinct roles of GCN5/PCAFmediated H3K9ac and CBP/p300-mediated H3K18/27ac in nuclear receptor transactivation. EMBO J, 30(2): 249–262PubMedCrossRefGoogle Scholar
  44. Kalkhoven E (2004). CBP and p300: HATs for different occasions. Biochem Pharmacol, 68(6): 1145–1155PubMedCrossRefGoogle Scholar
  45. Karanam B, Jiang L, Wang L, Kelleher N L, Cole P A (2006). Kinetic and mass spectrometric analysis of p300 histone acetyltransferase domain autoacetylation. J Biol Chem, 281(52): 40292–40301PubMedCrossRefGoogle Scholar
  46. Kasper L H, Boussouar F, Ney P A, Jackson C W, Rehg J, van Deursen J M, Brindle P K (2002). A transcription-factor-binding surface of coactivator p300 is required for haematopoiesis. Nature, 419(6908): 738–743PubMedCrossRefGoogle Scholar
  47. Kasper L H, Fukuyama T, Biesen M A, Boussouar F, Tong C, de Pauw A, Murray P J, van Deursen J M, Brindle P K (2006). Conditional knockout mice reveal distinct functions for the global transcriptional coactivators CBP and p300 in T-cell development. Mol Cell Biol, 26(3): 789–809PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kawasaki H, Eckner R, Yao T P, Taira K, Chiu R, Livingston D M, Yokoyama K K (1998). Distinct roles of the co-activators p300 and CBP in retinoic-acid-induced F9-cell differentiation. Nature, 393 (-): 284–289PubMedCrossRefGoogle Scholar
  49. Kim T K, Hemberg M, Gray J M, Costa A M, Bear D M, Wu J, Harmin D A, Laptewicz M, Barbara-Haley K, Kuersten S, Markenscoff-Papadimitriou E, Kuhl D, Bito H, Worley P F, Kreiman G, Greenberg M E (2010). Widespread transcription at neuronal activity-regulated enhancers. Nature, 465(7295): 182–187PubMedPubMedCentralCrossRefGoogle Scholar
  50. Korzus E (2017). Rubinstein-Taybi Syndrome and Epigenetic Alterations. Adv Exp Med Biol, 978: 39–62PubMedCrossRefGoogle Scholar
  51. Kouzarides T (2007). Chromatin modifications and their function. Cell, 128(4): 693–705PubMedCrossRefGoogle Scholar
  52. Kraus W L, Manning E T, Kadonaga J T (1999). Biochemical analysis of distinct activation functions in p300 that enhance transcription initiation with chromatin templates. Mol Cell Biol, 19(12): 8123–8135PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kung A L, Rebel V I, Bronson R T, Ch’ng L E, Sieff C A, Livingston D M, Yao T P (2000). Gene dose-dependent control of hematopoiesis and hematologic tumor suppression by CBP. Genes Dev, 14(3): 272–277PubMedPubMedCentralGoogle Scholar
  54. Kung A L, Zabludoff S D, France D S, Freedman S J, Tanner E A, Vieira A, Cornell-Kennon S, Lee J, Wang B, Wang J, Memmert K, Naegeli H U, Petersen F, Eck M J, Bair K W, Wood A W, Livingston D M (2004). Small molecule blockade of transcriptional coactivation of the hypoxia-inducible factor pathway. Cancer Cell, 6 (1): 33–43PubMedCrossRefGoogle Scholar
  55. Kuo H Y, Chang C C, Jeng J C, Hu H M, Lin D Y, Maul G G, Kwok R P, Shih H M (2005). SUMO modification negatively modulates the transcriptional activity of CREB-binding protein via the recruitment of Daxx. Proc Natl Acad Sci USA, 102(47): 16973–16978PubMedCrossRefGoogle Scholar
  56. Kwok R P, Lundblad J R, Chrivia J C, Richards J P, Bächinger H P, Brennan R G, Roberts S G, Green M R, Goodman R H (1994). Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature, 370(6486): 223–226PubMedCrossRefGoogle Scholar
  57. Lasko L M, Jakob C G, Edalji R P, Qiu W, Montgomery D, Digiammarino E L, Hansen T M, Risi R M, Frey R, Manaves V, Shaw B, Algire M, Hessler P, Lam L T, Uziel T, Faivre E, Ferguson D, Buchanan F G, Martin R L, Torrent M, Chiang G G, Karukurichi K, Langston JW, Weinert B T, Choudhary C, de Vries P, Van Drie J H, McElligott D, Kesicki E, Marmorstein R, Sun C, Cole P A, Rosenberg S H, Michaelides MR, Lai A, Bromberg K D (2017). Discovery of a selective catalytic p300/CBP inhibitor that targets lineage-specific tumours. Nature, 550(7674): 128–132PubMedPubMedCentralGoogle Scholar
  58. Lau O D, Kundu T K, Soccio R E, Ait-Si-Ali S, Khalil E M, Vassilev A, Wolffe A P, Nakatani Y, Roeder R G, Cole P A (2000). HATs off: selective synthetic inhibitors of the histone acetyltransferases p300 and PCAF. Mol Cell, 5(3): 589–595PubMedCrossRefGoogle Scholar
  59. Lee Y H, Coonrod S A, Kraus W L, Jelinek M A, Stallcup M R (2005). Regulation of coactivator complex assembly and function by protein arginine methylation and demethylimination. Proc Natl Acad Sci USA, 102(10): 3611–3616PubMedCrossRefGoogle Scholar
  60. Liu X, Wang L, Zhao K, Thompson P R, Hwang Y, Marmorstein R, Cole P A (2008). The structural basis of protein acetylation by the p300/CBP transcriptional coactivator. Nature, 451(7180): 846–850PubMedCrossRefGoogle Scholar
  61. Madison D L, Yaciuk P, Kwok R P, Lundblad J R (2002). Acetylation of the adenovirus-transforming protein E1A determines nuclear localization by disrupting association with importin-alpha. J Biol Chem, 277(41): 38755–38763PubMedCrossRefGoogle Scholar
  62. Martincorena I, Campbell P J (2015). Somatic mutation in cancer and normal cells. Science, 349(6255): 1483–1489PubMedCrossRefGoogle Scholar
  63. Mayr B, Montminy M (2001). Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat Rev Mol Cell Biol, 2 (8): 599–609PubMedCrossRefGoogle Scholar
  64. Michaelides MR, Kluge A, Patane M, Van Drie J H, Wang C, Hansen T M, Risi R M, Mantei R, Hertel C, Karukurichi K, Nesterov A, McElligott D, de Vries P, Langston JW, Cole P A, Marmorstein R, Liu H, Lasko L, Bromberg K D, Lai A, Kesicki E A (2017). Discovery of Spiro Oxazolidinediones as Selective, Orally Bioavailable Inhibitors of p300/CBP Histone Acetyltransferases. ACS Med Chem Lett, 9(1): 28–33PubMedPubMedCentralCrossRefGoogle Scholar
  65. Morin R D, Mendez-Lago M, Mungall A J, Goya R, Mungall K L, Corbett R D, Johnson N A, Severson T M, Chiu R, Field M, Jackman S, Krzywinski M, Scott DW, Trinh D L, Tamura-Wells J, Li S, Firme M R, Rogic S, Griffith M, Chan S, Yakovenko O, Meyer I M, Zhao E Y, Smailus D, Moksa M, Chittaranjan S, Rimsza L, Brooks-Wilson A, Spinelli J J, Ben-Neriah S, Meissner B, Woolcock B, Boyle M, McDonald H, Tam A, Zhao Y, Delaney A, Zeng T, Tse K, Butterfield Y, Birol I, Holt R, Schein J, Horsman D E, Moore R, Jones S J, Connors J M, Hirst M, Gascoyne R D, Marra MA (2011). Frequent mutation of histone-modifying genes in non-Hodgkin lymphoma. Nature, 476(7360): 298–303PubMedPubMedCentralCrossRefGoogle Scholar
  66. Mullighan C G, Zhang J, Kasper L H, Lerach S, Payne-Turner D, Phillips L A, Heatley S L, Holmfeldt L, Collins-Underwood J R, Ma J, Buetow K H, Pui C H, Baker S D, Brindle P K, Downing J R (2011). CREBBP mutations in relapsed acute lymphoblastic leukaemia. Nature, 471(7337): 235–239PubMedPubMedCentralCrossRefGoogle Scholar
  67. Nguyen U T, Bittova L, Müller M M, Fierz B, David Y, Houck-Loomis B, Feng V, Dann G P, Muir T W (2014). Accelerated chromatin biochemistry using DNA-barcoded nucleosome libraries. Nat Methods, 11(8): 834–840PubMedPubMedCentralCrossRefGoogle Scholar
  68. Ogryzko V V, Schiltz R L, Russanova V, Howard B H, Nakatani Y (1996). The transcriptional coactivators p300 and CBP are histone acetyltransferases. Cell, 87(5): 953–959PubMedCrossRefGoogle Scholar
  69. Oike Y, Takakura N, Hata A, Kaname T, Akizuki M, Yamaguchi Y, Yasue H, Araki K, Yamamura K, Suda T (1999). Mice homozygous for a truncated form of CREB-binding protein exhibit defects in hematopoiesis and vasculo-angiogenesis. Blood, 93(9): 2771–2779PubMedGoogle Scholar
  70. Park S, Martinez-Yamout M A, Dyson H J, Wright P E (2013). The CH2 domain of CBP/p300 is a novel zinc finger. FEBS Lett, 587(16): 2506–2511PubMedPubMedCentralCrossRefGoogle Scholar
  71. Park S, Stanfield R L, Martinez-Yamout MA, Dyson H J, Wilson I A, Wright P E (2017). Role of the CBP catalytic core in intramolecular SUMOylation and control of histone H3 acetylation. Proc Natl Acad Sci USA, 114(27): E5335–E5342PubMedCrossRefGoogle Scholar
  72. Pasqualucci L, Dominguez-Sola D, Chiarenza A, Fabbri G, Grunn A, Trifonov V, Kasper L H, Lerach S, Tang H, Ma J, Rossi D, Chadburn A, Murty V V, Mullighan C G, Gaidano G, Rabadan R, Brindle P K, Dalla-Favera R (2011). Inactivating mutations of acetyltransferase genes in B-cell lymphoma. Nature, 471(7337): 189–195PubMedPubMedCentralCrossRefGoogle Scholar
  73. Peifer M, Fernández-Cuesta L, Sos M L, George J, Seidel D, Kasper L H, Plenker D, Leenders F, Sun R, Zander T, Menon R, Koker M, Dahmen I, Müller C, Di Cerbo V, Schildhaus H U, Altmüller J, Baessmann I, Becker C, de Wilde B, Vandesompele J, Böhm D, Ansén S, Gabler F, Wilkening I, Heynck S, Heuckmann J M, Lu X, Carter S L, Cibulskis K, Banerji S, Getz G, Park K S, Rauh D, Grütter C, Fischer M, Pasqualucci L, Wright G, Wainer Z, Russell P, Petersen I, Chen Y, Stoelben E, Ludwig C, Schnabel P, Hoffmann H, Muley T, Brockmann M, Engel-Riedel W, Muscarella L A, Fazio V M, Groen H, Timens W, Sietsma H, Thunnissen E, Smit E, Heideman D A, Snijders P J, Cappuzzo F, Ligorio C, Damiani S, Field J, Solberg S, Brustugun O T, Lund- Iversen M, Sänger J, Clement J H, Soltermann A, Moch H, Weder W, Solomon B, Soria J C, Validire P, Besse B, Brambilla E, Brambilla C, Lantuejoul S, Lorimier P, Schneider P M, Hallek M, Pao W, Meyerson M, Sage J, Shendure J, Schneider R, Büttner R, Wolf J, Nürnberg P, Perner S, Heukamp L C, Brindle P K, Haas S, Thomas R K (2012). Integrative genome analyses identify key somatic driver mutations of small-cell lung cancer. Nat Genet, 44 (10): 1104–1110PubMedPubMedCentralCrossRefGoogle Scholar
  74. Perissi V, Dasen J S, Kurokawa R, Wang Z, Korzus E, Rose D W, Glass C K, Rosenfeld M G (1999). Factor-specific modulation of CREB-binding protein acetyltransferase activity. Proc Natl Acad Sci USA, 96(7): 3652–3657PubMedCrossRefGoogle Scholar
  75. Petrij F, Giles R H, Dauwerse H G, Saris J J, Hennekam R C, Masuno M, Tommerup N, van Ommen G J, Goodman R H, Peters D J (1995). Rubinstein-Taybi syndrome caused by mutations in the transcriptional co-activator CBP. Nature, 376(6538): 348–351PubMedCrossRefGoogle Scholar
  76. Picaud S, Fedorov O, Thanasopoulou A, Leonards K, Jones K, Meier J, Olzscha H, Monteiro O, Martin S, Philpott M, Tumber A, Filippakopoulos P, Yapp C, Wells C, Che K H, Bannister A, Robson S, Kumar U, Parr N, Lee K, Lugo D, Jeffrey P, Taylor S, Vecellio ML, Bountra C, Brennan P E, O’Mahony A, Velichko S, Müller S, Hay D, Daniels D L, Urh M, La Thangue N B, Kouzarides T, Prinjha R, Schwaller J, Knapp S (2015). Generation of a Selective Small Molecule Inhibitor of the CBP/p300 Bromodomain for Leukemia Therapy. Cancer Res, 75(23): 5106–5119PubMedPubMedCentralCrossRefGoogle Scholar
  77. Plotnikov A N, Yang S, Zhou T J, Rusinova E, Frasca A, Zhou M M (2014). Structural insights into acetylated-histone H4 recognition by the bromodomain-PHD finger module of human transcriptional coactivator CBP. Structure, 22(2): 353–360PubMedCrossRefGoogle Scholar
  78. Rack J G M, Lutter T, Kjæreng Bjerga G E, Guder C, Ehrhardt C, Värv S, Ziegler M, Aasland R (2014). The PHD finger of p300 influences its ability to acetylate histone and non-histone targets. J Mol Biol, 426(24): 3960–3972PubMedCrossRefGoogle Scholar
  79. Radhakrishnan I, Pérez-Alvarado G C, Parker D, Dyson H J, Montminy M R, Wright P E (1997). Solution structure of the KIX domain of CBP bound to the transactivation domain of CREB: a model for activator:coactivator interactions. Cell, 91(6): 741–752PubMedCrossRefGoogle Scholar
  80. Rebel V I, Kung A L, Tanner E A, Yang H, Bronson R T, Livingston D M (2002). Distinct roles for CREB-binding protein and p300 in hematopoietic stem cell self-renewal. Proc Natl Acad Sci USA, 99 (23): 14789–14794PubMedCrossRefGoogle Scholar
  81. Roe J S, Mercan F, Rivera K, Pappin D J, Vakoc C R (2015). BET Bromodomain Inhibition Suppresses the Function of Hematopoietic Transcription Factors in Acute Myeloid Leukemia. Mol Cell, 58(6): 1028–1039PubMedPubMedCentralCrossRefGoogle Scholar
  82. Rojas J R, Trievel R C, Zhou J, Mo Y, Li X, Berger S L, Allis C D, Marmorstein R (1999). Structure of Tetrahymena GCN5 bound to coenzyme A and a histone H3 peptide. Nature, 401(6748): 93–98PubMedCrossRefGoogle Scholar
  83. Roth S Y, Allis C D (1996). Histone acetylation and chromatin assembly: a single escort, multiple dances? Cell, 87(1): 5–8PubMedCrossRefGoogle Scholar
  84. Saint Just Ribeiro M, Hansson M L, Wallberg A E (2007). A proline repeat domain in the Notch co-activator MAML1 is important for the p300-mediated acetylation of MAML1. Biochem J, 404(2): 289–298PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sanchez R, Zhou M M (2011). The PHD finger: a versatile epigenome reader. Trends Biochem Sci, 36(7): 364–372PubMedPubMedCentralGoogle Scholar
  86. Schiltz R L, Mizzen C A, Vassilev A, Cook R G, Allis C D, Nakatani Y (1999). Overlapping but distinct patterns of histone acetylation by the human coactivators p300 and PCAF within nucleosomal substrates. J Biol Chem, 274(3): 1189–1192PubMedCrossRefGoogle Scholar
  87. Shi X, Hong T, Walter K L, Ewalt M, Michishita E, Hung T, Carney D, Peña P, Lan F, Kaadige M R, Lacoste N, Cayrou C, Davrazou F, Saha A, Cairns B R, Ayer D E, Kutateladze T G, Shi Y, Côté J, Chua K F, Gozani O (2006). ING2 PHD domain links histone H3 lysine 4 methylation to active gene repression. Nature, 442(7098): 96–99PubMedPubMedCentralCrossRefGoogle Scholar
  88. Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie J R, Peterson C L (2006). Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science, 311(5762): 844–847PubMedCrossRefGoogle Scholar
  89. Solomon B D, Bodian D L, Khromykh A, Mora G G, Lanpher B C, Iyer R K, Baveja R, Vockley J G, Niederhuber J E (2015). Expanding the phenotypic spectrum in EP300-related Rubinstein- Taybi syndrome. Am J Med Genet A, 167A(5): 1111–1116PubMedCrossRefGoogle Scholar
  90. Stein R W, Corrigan M, Yaciuk P, Whelan J, Moran E (1990). 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, 64 (9): 4421–4427PubMedPubMedCentralGoogle Scholar
  91. Szerlong H J, Prenni J E, Nyborg J K, Hansen J C (2010). Activatordependent p300 acetylation of chromatin in vitro: enhancement of transcription by disruption of repressive nucleosome-nucleosome interactions. J Biol Chem, 285(42): 31954–31964PubMedPubMedCentralCrossRefGoogle Scholar
  92. Tanaka Y, Naruse I, Hongo T, Xu M, Nakahata T, Maekawa T, Ishii S (2000). Extensive brain hemorrhage and embryonic lethality in a mouse null mutant of CREB-binding protein. Mech Dev, 95(1-2): 133–145PubMedCrossRefGoogle Scholar
  93. Tanaka Y, Naruse I, Maekawa T, Masuya H, Shiroishi T, Ishii S (1997). Abnormal skeletal patterning in embryos lacking a single Cbp allele: a partial similarity with Rubinstein-Taybi syndrome. Proc Natl Acad Sci USA, 94(19): 10215–10220PubMedCrossRefGoogle Scholar
  94. Tang Z, Chen W Y, Shimada M, Nguyen U T, Kim J, Sun X J, Sengoku T, McGinty R K, Fernandez J P, Muir T W, Roeder R G (2013). SET1 and p300 act synergistically, through coupled histone modifications, in transcriptional activation by p53. Cell, 154(2): 297–310PubMedPubMedCentralCrossRefGoogle Scholar
  95. Tessarz P, Kouzarides T (2014). Histone core modifications regulating nucleosome structure and dynamics. Nat Rev Mol Cell Biol, 15(11): 703–708PubMedCrossRefGoogle Scholar
  96. Thompson P R, Kurooka H, Nakatani Y, Cole P A (2001). Transcriptional coactivator protein p300. Kinetic characterization of its histone acetyltransferase activity. J Biol Chem, 276(36): 33721–33729PubMedCrossRefGoogle Scholar
  97. Thompson P R, Wang D, Wang L, Fulco M, Pediconi N, Zhang D, An W, Ge Q, Roeder R G, Wong J, Levrero M, Sartorelli V, Cotter R J, Cole P A (2004). Regulation of the p300 HAT domain via a novel activation loop. Nat Struct Mol Biol, 11(4): 308–315PubMedCrossRefGoogle Scholar
  98. Trievel R C, Rojas J R, Sterner D E, Venkataramani R N, Wang L, Zhou J, Allis C D, Berger S L, Marmorstein R (1999). Crystal structure and mechanism of histone acetylation of the yeast GCN5 transcriptional coactivator. Proc Natl Acad Sci USA, 96(16): 8931–8936PubMedCrossRefGoogle Scholar
  99. Tse C, Sera T, Wolffe A P, Hansen J C (1998). Disruption of higherorder folding by core histone acetylation dramatically enhances transcription of nucleosomal arrays by RNA polymerase III. Mol Cell Biol, 18(8): 4629–4638PubMedPubMedCentralCrossRefGoogle Scholar
  100. Vempati R K, Jayani R S, Notani D, Sengupta A, Galande S, Haldar D (2010). p300-mediated acetylation of histone H3 lysine 56 functions in DNA damage response in mammals. J Biol Chem, 285 (37): 28553–28564PubMedPubMedCentralCrossRefGoogle Scholar
  101. Visel A, Blow M J, Li Z, Zhang T, Akiyama J A, Holt A, Plajzer-Frick I, Shoukry M, Wright C, Chen F, Afzal V, Ren B, Rubin E M, Pennacchio L A (2009). ChIP-seq accurately predicts tissuespecific activity of enhancers. Nature, 457(7231): 854–858PubMedPubMedCentralCrossRefGoogle Scholar
  102. Vo N, Goodman R H (2001). CREB-binding protein and p300 in transcriptional regulation. J Biol Chem, 276(17): 13505–13508PubMedCrossRefGoogle Scholar
  103. Wan W, You Z, Xu Y, Zhou L, Guan Z, Peng C, Wong C C L, Su H, Zhou T, Xia H (2017). mTORC1 Phosphorylates Acetyltransferase p300 to Regulate Autophagy and Lipogenesis. Molecular cell 68, 323–335 e326.Google Scholar
  104. Wang F, Marshall C B, Ikura M (2013a). Transcriptional/epigenetic regulator CBP/p300 in tumorigenesis: structural and functional versatility in target recognition. Cell Mol Life Sci, 70(21): 3989–4008PubMedCrossRefGoogle Scholar
  105. Wang Q E, Han C, Zhao R, Wani G, Zhu Q, Gong L, Battu A, Racoma I, Sharma N, Wani A A (2013b). p38 MAPK- and Aktmediated p300 phosphorylation regulates its degradation to facilitate nucleotide excision repair. Nucleic Acids Res, 41(3): 1722–1733PubMedCrossRefGoogle Scholar
  106. Wang Z, Zang C, Cui K, Schones D E, Barski A, Peng W, Zhao K (2009). Genome-wide mapping of HATs and HDACs reveals distinct functions in active and inactive genes. Cell, 138(5): 1019–1031PubMedPubMedCentralCrossRefGoogle Scholar
  107. Whyte P, Williamson N M, Harlow E (1989). Cellular targets for transformation by the adenovirus E1A proteins. Cell, 56(1): 67–75PubMedCrossRefGoogle Scholar
  108. Xu L, Cheng A, Huang M, Zhang J, Jiang Y, Wang C, Li F, Bao H, Gao J, Wang N, Liu J, Wu J, Wong C C L, Ruan K (2017). Structural insight into the recognition of acetylated histone H3K56ac mediated by the bromodomain of CREB-binding protein. FEBS J, 284(20): 3422–3436PubMedCrossRefGoogle Scholar
  109. Xu W, Chen H, Du K, Asahara H, Tini M, Emerson B M, Montminy M, Evans RM (2001). A transcriptional switch mediated by cofactor methylation. Science, 294(5551): 2507–2511PubMedCrossRefGoogle Scholar
  110. Yao T P, Oh S P, Fuchs M, Zhou N D, Ch’ng L E, Newsome D, Bronson R T, Li E, Livingston D M, Eckner R (1998). Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell, 93(3): 361–372PubMedCrossRefGoogle Scholar
  111. Yee S P, Branton P E (1985). Detection of cellular proteins associated with human adenovirus type 5 early region 1A polypeptides. Virology, 147(1): 142–153PubMedCrossRefGoogle Scholar
  112. Yuan L W, Soh J W, Weinstein I B (2002). Inhibition of histone acetyltransferase function of p300 by PKCdelta. Biochim Biophys Acta, 1592(2): 205–211PubMedCrossRefGoogle Scholar
  113. Zeng L, Zhang Q, Gerona-Navarro G, Moshkina N, Zhou M M (2008). Structural basis of site-specific histone recognition by the bromodomains of human coactivators PCAF and CBP/p300. Structure, 16(4): 643–652PubMedPubMedCentralCrossRefGoogle Scholar
  114. Zhang J, Vlasevska S, Wells V A, Nataraj S, Holmes A B, Duval R, Meyer S N, Mo T, Basso K, Brindle P K, Hussein S, Dalla-Favera R, Pasqualucci L (2017a). The CREBBP Acetyltransferase Is a Haploinsufficient Tumor Suppressor in B-cell Lymphoma. Cancer Discov, 7(3): 322–337PubMedPubMedCentralCrossRefGoogle Scholar
  115. Zhang R, Erler J, Langowski J (2017b). Histone Acetylation Regulates Chromatin Accessibility: Role of H4K16 in Inter-nucleosome Interaction. Biophys J, 112(3): 450–459PubMedCrossRefGoogle Scholar
  116. Zhong J, Ding L, Bohrer L R, Pan Y, Liu P, Zhang J, Sebo T J, Karnes R J, Tindall D J, van Deursen J, Huang H (2014). p300 acetyltransferase regulates androgen receptor degradation and PTENdeficient prostate tumorigenesis. Cancer Res, 74(6): 1870–1880PubMedPubMedCentralCrossRefGoogle Scholar
  117. Zhu P, Li G (2016). Structural insights of nucleosome and the 30-nm chromatin fiber. Curr Opin Struct Biol, 36: 106–115PubMedCrossRefGoogle Scholar
  118. Zucconi B E, Luef B, Xu W, Henry R A, Nodelman I M, Bowman G D, Andrews A J, Cole P A (2016). Modulation of p300/CBP Acetylation of Nucleosomes by Bromodomain Ligand I-CBP112. Biochemistry, 55(27): 3727–3734PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Higher Education Press and Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of Epigenetics and Molecular Carcinogenesis, Center for Cancer EpigeneticsThe University of Texas MD Anderson Cancer CenterHoustonUSA
  2. 2.Genetics and Epigenetics Graduate ProgramThe University of Texas MD Anderson Cancer Center UTHealth Graduate School of Biomedical SciencesHoustonUSA
  3. 3.Center for EpigeneticsVan Andel Research InstituteGrand RapidsUSA

Personalised recommendations