Class i histone deacetylases are major histone decrotonylases: Evidence for critical and broad function of histone crotonylation in transcription

Cell Research

Volumn 27, Issue 7, 2017, Pages 898-915

  Wei, Wei ^a   Liu, Xiaoguang ^a   Chen, Jiwei ^a   Gao, Shennan ^a   Lu, Lu ^a   Zhang, Huifang ^a   Ding, Guangjin ^a   Wang, Zhiqiang ^a   Chen, Zhongzhou ^b   Shi, Tieliu ^a   Li, Jiwen ^a   Yu, Jianjun ^c   Wong, Jiemin ^a  

^a EAST CHINA NORMAL UNIVERSITY   (China)

^b CHINA AGRICULTURAL UNIVERSITY   (China)

^c SHANGHAI JIAO TONG UNIVERSITY AFFILIATED SIXTH PEOPLE S HOSPITAL   (China)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE; HISTONE DEACETYLASE; HISTONE DEACETYLASE INHIBITOR; HYDROXAMIC ACID; LYSINE; MUTANT PROTEIN; NICOTINAMIDE; SIRTUIN; TRANSCRIPTION FACTOR; TRICHOSTATIN A;

ACETYLATION; ANIMAL; CELL LINE; DRUG EFFECTS; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETICS; HUMAN; METABOLISM; MOUSE;

ACETYLATION; ANIMALS; CELL LINE; GENE EXPRESSION; HISTONE DEACETYLASE INHIBITORS; HISTONE DEACETYLASES; HISTONES; HUMANS; HYDROXAMIC ACIDS; LYSINE; MICE; MUTANT PROTEINS; NIACINAMIDE; SIRTUINS; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 85021794655     PISSN: 10010602     EISSN: 17487838     Source Type: Journal    
DOI: 10.1038/cr.2017.68     Document Type: Article

References (54)

1. Roth SY, Denu JM, Allis CD. Histone acetyltransferases. Annu Rev Biochem 2001; 70:81-120.
2. Wolffe AP. Histone deacetylase: a regulator of transcription. Science 1996; 272:371-372.
3. Rousseaux S, Khochbin S. Histone acylation beyond acetylation: terra incognita in chromatin biology. Cell J 2015; 17:1-6.
4. Tan M, Luo H, Lee S, et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011; 146:1016-1028.
5. Olsen CA. Expansion of the lysine acylation landscape. Angew Chem Int Ed Engl 2012; 51:3755-3756.
6. Dai L, Peng C, Montellier E, et al. Lysine 2-hydroxyisobutyrylation is a widely distributed active histone mark. Nat Chem Biol 2014; 10:365-370.
7. Zhang K, Chen Y, Zhang Z, Zhao Y. Identification and verification of lysine propionylation and butyrylation in yeast core histones using PTMap software. J Proteome Res 2009; 8:900-906.
8. Xie Z, Dai J, Dai L, et al. Lysine succinylation and lysine malonylation in histones. Mol Cell Proteomics 2012; 11:100-107.
9. Sabari BR, Zhang D, Allis CD, Zhao Y. Metabolic regulation of gene expression through histone acylations. Nat Rev Mol Cell Biol 2017; 18:90-101.
10. Sabari BR, Tang Z, Huang H, et al. Intracellular crotonyl-CoA stimulates transcription through p300-catalyzed histone crotonylation. Mol Cell 2015; 58:203-215.
11. Li Y, Sabari BR, Panchenko T, et al. Molecular coupling of histone crotonylation and active transcription by AF9 YEATS domain. Mol Cell 2016; 62:181-193.
12. Xiong X, Panchenko T, Yang S, et al. Selective recognition of histone crotonylation by double PHD fingers of MOZ and DPF2. Nat Chem Biol 2016; 12:1111-1118.
13. Andrews FH, Shinsky SA, Shanle EK, et al. The Taf14 YEATS domain is a reader of histone crotonylation. Nat Chem Biol 2016; 12:396-398.
14. Li Y, Wen H, Xi Y, et al. AF9 YEATS domain links histone acetylation to DOT1L-mediated H3K79 methylation. Cell 2014; 159:558-571.
15. 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.
16. Zhao D, Guan H, Zhao S, et al. YEATS2 is a selective histone crotonylation reader. Cell Res 2016; 26:629-632.
17. Cheng Z, Tang Y, Chen Y, et al. Molecular characterization of propionyllysines in non-histone proteins. Mol Cell Proteomics 2009; 8:45-52.
18. Smith BC, Denu JM. Acetyl-lysine analog peptides as mechanistic probes of protein deacetylases. J Biol Chem 2007; 282:37256-37265.
19. Du J, Zhou Y, Su X, et al. Sirt5 is a NAD-dependent protein lysine demalonylase and desuccinylase. Science 2011; 334:806-809.
20. Park J, Chen Y, Tishkoff DX, et al. SIRT5-mediated lysine desuccinylation impacts diverse metabolic pathways. Mol Cell 2013; 50:919-930.
21. Rardin MJ, He W, Nishida Y, et al. SIRT5 regulates the mitochondrial lysine succinylome and metabolic networks. Cell Metab 2013; 18:920-933.
22. Tan M, Peng C, Anderson KA, et al. Lysine glutarylation is a protein posttranslational modification regulated by SIRT5. Cell Metab 2014; 19:605-617.
23. Feldman JL, Baeza J, Denu JM. Activation of the protein deacetylase SIRT6 by long-chain fatty acids and widespread deacylation by mammalian sirtuins. J Biol Chem 2013; 288:31350-31356.
24. Bao X, Wang Y, Li X, et al. Identification of 'erasers' for lysine crotonylated histone marks using a chemical proteomics approach. eLife 2014; 3. doi: 10.7554/eLife.02999
25. Madsen AS, Olsen CA. Profiling of substrates for zinc-dependent lysine deacylase enzymes: HDAC3 exhibits decrotonylase activity in vitro. Angew Chem Int Ed Engl 2012; 51:9083-9087.
26. Van der Veer E, Ho C, O'Neil C, et al. Extension of human cell lifespan by nicotinamide phosphoribosyltransferase. J Biol Chem 2007; 282:10841-10845.
27. Lin CY, Loven J, Rahl PB, et al. Transcriptional amplification in tumor cells with elevated c-Myc. Cell 2012; 151:56-67.
28. Loven J, Orlando DA, Sigova AA, et al. Revisiting global gene expression analysis. Cell 2012; 151:476-482.
29. Dey A, Chitsaz F, Abbasi A, Misteli T, Ozato K. The double bromodomain protein Brd4 binds to acetylated chromatin during interphase and mitosis. Proc Natl Acad Sci USA 2003; 100:8758-8763.
30. Filippakopoulos P, Picaud S, Mangos M, et al. Histone recognition and large-scale structural analysis of the human bromodomain family. Cell 2012; 149:214-231.
31. Kimura H, Tada M, Nakatsuji N, Tada T. Histone code modifications on pluripotential nuclei of reprogrammed somatic cells. Mol Cell Biol 2004; 24:5710-5720.
32. Moussaieff A, Rouleau M, Kitsberg D, et al. Glycolysis-mediated changes in acetyl-CoA and histone acetylation control the early differentiation of embryonic stem cells. Cell Metab 2015; 21:392-402.
33. Niwa H, Miyazaki J, Smith AG. Quantitative expression of Oct-3/4 defines differentiation, dedifferentiation or self-renewal of ES cells. Nat Genet 2000; 24:372-376.
34. Young RA. Control of the embryonic stem cell state. Cell 2011; 144:940-954.
35. Fang L, Zhang L, Wei W, et al. A methylation-phosphorylation switch determines Sox2 stability and function in ESC maintenance or differentiation. Mol Cell 2014; 55:537-551.
36. Li Y, Zhao D, Chen Z, Li H. YEATS domain: linking histone crotonylation to gene regulation. Transcription 2017; 8:9-14.
37. Zhang Y, Iratni R, Erdjument-Bromage H, Tempst P, Reinberg D. Histone deacetylases and SAP18, a novel polypeptide, are components of a human Sin3 complex. Cell 1997; 89:357-364.
38. Hassig CA, Fleischer TC, Billin AN, Schreiber SL, Ayer DE. Histone deacetylase activity is required for full transcriptional repression by mSin3A. Cell 1997; 89:341-347.
39. Laherty CD, Yang WM, Sun JM, Davie JR, Seto E, Eisenman RN. Histone deacetylases associated with the mSin3 corepressor mediate mad transcriptional repression. Cell 1997; 89:349-356.
40. Xue Y, Wong J, Moreno GT, Young MK, Cote J, Wang W. NURD, a novel complex with both ATP-dependent chromatin-remodeling and histone deacetylase activities. Mol Cell 1998; 2:851-861.
41. Zhang Y, LeRoy G, Seelig HP, Lane WS, Reinberg D. The dermatomyositis-specific autoantigen Mi2 is a component of a complex containing histone deacetylase and nucleosome remodeling activities. Cell 1998; 95:279-289.
42. Guenther MG, Lane WS, Fischle W, Verdin E, Lazar MA, Shiekhattar R. A core SMRT corepressor complex containing HDAC3 and TBL1, a WD40-repeat protein linked to deafness. Genes Dev 2000; 14:1048-1057.
43. Li J, Wang J, Wang J, et al. Both corepressor proteins SMRT and N-CoR exist in large protein complexes containing HDAC3. EMBO J 2000; 19:4342-4350.
44. Kaczmarska Z, Ortega E, Goudarzi A, et al. Structure of p300 in complex with acyl-CoA variants. Nat Chem Biol 2017; 13:21-29.
45. Yao TP, Oh SP, Fuchs M, et al. Gene dosage-dependent embryonic development and proliferation defects in mice lacking the transcriptional integrator p300. Cell 1998; 93:361-372.
46. Chelmicki T, Dundar F, Turley MJ, et al. MOF-associated complexes ensure stem cell identity and Xist repression. eLife 2014; 3:e02024.
47. Li X, Li L, Pandey R, et al. The histone acetyltransferase MOF is a key regulator of the embryonic stem cell core transcriptional network. Cell Stem Cell 2012; 11:163-178.
48. Shechter D, Dormann HL, Allis CD, Hake SB. Extraction, purification and analysis of histones. Nat Protoc 2007; 2:1445-1457.
49. Liu X, Gao Q, Li P, et al. UHRF1 targets DNMT1 for DNA methylation through cooperative binding of hemi-methylated DNA and methylated H3K9. Nat Commun 2013; 4:1563.
50. Yoon HG, Choi Y, Cole PA, Wong J. Reading and function of a histone code involved in targeting corepressor complexes for repression. Mol Cell Biol 2005; 25:324-335.
51. Millard CJ, Watson PJ, Celardo I, et al. Class I HDACs share a common mechanism of regulation by inositol phosphates. Mol Cell 2013; 51:57-67.
52. Schuetz A, Min J, Allali-Hassani A, et al. Human HDAC7 harbors a class IIa histone deacetylase-specific zinc binding motif and cryptic deacetylase activity. J Biol Chem 2008; 283:11355-11363.
53. Vannini A, Volpari C, Gallinari P, et al. Substrate binding to histone deacetylases as shown by the crystal structure of the HDAC8-substrate complex. EMBO Rep 2007; 8:879-884.
54. Liu XG, Wei W, Liu YT, et al. MOF as an evolutionarily conserved histone crotonyltransferase and transcriptional activation by histone acetyltransferase-deficient and crotonyltransferase-competent CBP/p300. Cell Discov 2017; 3:17016. doi:10.1038/celldisc.2017.16