The Expanding Constellation of Histone Post-Translational Modifications in the Epigenetic Landscape
Abstract
:1. Introduction
2. Acetylation
3. Non-Acetyl Acylation
4. Methylation
5. Citrullination
6. Phosphorylation
7. Ubiquitylation
8. Sumoylation
9. Glycosylation
10. ADP-Ribosylation
11. Biotinylation
12. Monoaminylation
13. Isomerization
14. Glycation
15. Lipidation
16. Formylation
17. Histone Tail Clip**
18. Conclusions
Funding
Institutional Review Board Statement
Informed Consent Statement
Conflicts of Interest
References
- Kornberg, R.D. Chromatin structure: A repeating unit of histones and DNA. Science 1974, 184, 868–871. [Google Scholar] [CrossRef] [PubMed]
- Kornberg, R.D.; Lorch, Y. Twenty-five years of the nucleosome, fundamental particle of the eukaryote chromosome. Cell 1999, 98, 285–294. [Google Scholar] [CrossRef] [Green Version]
- Arents, G.; Burlingame, R.W.; Wang, B.C.; Love, W.E.; Moudrianakis, E.N. The nucleosomal core histone octamer at 3.1 Å resolution: A tripartite protein assembly and a left-handed superhelix. Proc. Natl. Acad. Sci. USA 1991, 88, 10148–10152. [Google Scholar] [CrossRef] [Green Version]
- Luger, K.; Mäder, A.W.; Richmond, R.K.; Sargent, D.F.; Richmond, T.J. Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 1997, 389, 251–260. [Google Scholar] [CrossRef]
- Ausio, J.; Dong, F.; van Holde, K.E. Use of selectively trypsinized nucleosome core particles to analyze the role of the histone “tails” in the stabilization of the nucleosome. J. Mol. Biol. 1989, 206, 451–463. [Google Scholar] [CrossRef]
- Bednar, J.; Horowitz, R.A.; Grigoryev, S.A.; Carruthers, L.M.; Hansen, J.C.; Koster, A.J.; Woodcock, C.L. Nucleosomes, linker DNA, and linker histone form a unique structural motif that directs the higher-order folding and compaction of chromatin. Proc. Natl. Acad. Sci. USA 1998, 95, 14173–14178. [Google Scholar] [CrossRef] [Green Version]
- Bednar, J.; Garcia-Saez, I.; Boopathi, R.; Cutter, A.R.; Papai, G.; Reymer, A.; Syed, S.H.; Lone, I.N.; Tonchev, O.; Crucifix, C.; et al. Structure and Dynamics of a 197 bp Nucleosome in Complex with Linker Histone H1. Mol. Cell 2017, 66, 384–397. [Google Scholar] [CrossRef] [Green Version]
- Cavalieri, V.; Melfi, R.; Spinelli, G. Promoter activity of the sea urchin (Paracentrotus lividus) nucleosomal H3 and H2A and linker H1 {alpha}-histone genes is modulated by enhancer and chromatin insulator. Nucleic Acids Res. 2009, 37, 7407–7415. [Google Scholar] [CrossRef] [Green Version]
- Cavalieri, V.; Melfi, R.; Spinelli, G. The Compass-like locus, exclusive to the Ambulacrarians, encodes a 874 chromatin insulator binding protein in the Sea Urchin embryo. PLoS Genet. 2013, 9, e1003847. [Google Scholar] [CrossRef] [Green Version]
- Cavalieri, V.; Spinelli, G. Histone-mediated transgenerational epigenetics. In Transgenerational Epigenetics, 2nd ed.; Tollefsbol, T.O., Ed.; Elsevier: Amsterdam, The Netherlands, 2019; pp. 157–183. [Google Scholar]
- Cavalieri, V. Histones, Their Variants and Post-translational Modifications in Zebrafish Development. Front. Cell Dev. Biol. 2020, 8, 456. [Google Scholar] [CrossRef] [PubMed]
- Su, X.; Ren, C.; Freitas, M.A. Mass spectrometry-based strategies for characterization of histones and their posttranslational modifications. Expert Rev. Proteom. 2007, 4, 211–225. [Google Scholar] [CrossRef] [PubMed]
- Zhao, Y.; Garcia, B.A. Comprehensive Catalog of Currently Documented Histone Modifications. Cold Spring Harb. Perspect. Biol. 2015, 7, a025064. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, E.; Shilatifard, A. The chromatin signaling pathway: Diverse mechanisms of recruitment of histone-modifying enzymes and varied biological outcomes. Mol. Cell 2010, 40, 689e701. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cavalieri, V.; Spinelli, G. Environmental epigenetics in zebrafish. Epigenetics Chromatin 2017, 10, 46. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cavalieri, V. Model organisms and their application in environmental epigenetics. In Environmental Epigenetics in Toxicology and Public Health; Fry, R., Ed.; Elsevier: Amsterdam, The Netherlands, 2020; pp. 67–87. [Google Scholar]
- Fischle, W.; Wang, Y.; Allis, C.D. Binary switches and modification cassettes in histone biology and beyond. Nature 2003, 425, 475–479. [Google Scholar] [CrossRef] [PubMed]
- Oey, N.E.; Leung, H.W.; Ezhilarasan, R.; Zhou, L.; Beuerman, R.W.; VanDongen, H.M.; VanDongen, A.M. A Neuronal Activity-Dependent Dual Function Chromatin-Modifying Complex Regulates Arc Expression. eNeuro 2015, 2, ENEURO.0020-14.2015. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Turner, B.M. Reading signals on the nucleosome with a new nomenclature for modified histones. Nat. Struct. Mol. Biol. 2005, 12, 110–112. [Google Scholar] [CrossRef]
- Phillips, D.M.P. The presence of acetyl groups in histones. Biochem. J. 1963, 87, 258–263. [Google Scholar] [CrossRef] [Green Version]
- Allfrey, V.G.; Faulkner, R.; Mirsky, A.E. Acetylation and methylation of histones and their possible role in the regulation of RNA synthesis. Proc. Natl. Acad. Sci. USA 1964, 51, 786–794. [Google Scholar] [CrossRef] [Green Version]
- Berndsen, C.B.; Denu, J.M. Catalysis and substrate selection by histone/protein lysine acetyltransferases. Curr. Opin. Struct. Biol. 2008, 18, 682–689. [Google Scholar] [CrossRef] [Green Version]
- Richman, R.; Chicoine, L.G.; Collini, M.P.; Cook, R.G.; Allis, C.D. Micronuclei and the cytoplasm of growing Tetrahymena contain a histone acetylase activity which is highly specific for free histone H4. J. Cell Biol. 1988, 106, 1017–1026. [Google Scholar] [CrossRef] [Green Version]
- Parthun, M.R.; Widom, J.; Gottschling, D.E. The major cytoplasmic histone acetyltransferase in yeast: Links to chromatin replication and histone metabolism. Cell 1996, 87, 85–94. [Google Scholar] [CrossRef] [Green Version]
- Seto, E.; Yoshida, M. Erasers of histone acetylation: The histone deacetylase enzymes. Cold Spring Harb. Perspect. Biol. 2014, 6, a018713. [Google Scholar] [CrossRef] [Green Version]
- Thorne, A.W.; Kmiciek, D.; Mitchelson, K.; Sautiere, P.; Crane-Robinson, C. Patterns of histone acetylation. Eur. J. Biochem. 1990, 193, 701–713. [Google Scholar] [CrossRef]
- Kimura, A.; Horikoshi, M. How do histone acetyltransferases select lysine residues in core histones? FEBS Lett. 1998, 431, 131–133. [Google Scholar] [CrossRef] [Green Version]
- Grant, P.A.; Duggan, L.; Côté, J.; Roberts, S.M.; Brownell, J.E.; Candau, R.; Ohba, R.; Owen-Hughes, T.; Allis, C.D.; Winston, F. 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. [Google Scholar] [CrossRef] [Green Version]
- Workman, J.L.; Kingston, R.E. Alteration of nucleosome structure as a mechanism of transcriptional regulation. Annu. Rev. Biochem. 1998, 67, 545–579. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Shogren-Knaak, M. Histone H4–K16 acetylation controls chromatin structure and protein interactions. Science 2006, 311, 844–847. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allahverdi, A.; Yang, R.; Korolev, N.; Fan, Y.; Davey, C.A.; Liu, C.F.; Nordenskiöld, L. The effects of histone H4 tail acetylations on cation-induced chromatin folding and self-association. Nucleic Acids Res. 2011, 39, 1680–1691. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Collepardo-Guevara, R.; Portella, G.; Vendruscolo, M.; Frenkel, D.; Schlick, T.; Orozco, M. Chromatin unfolding by epigenetic modifications explained by dramatic impairment of internucleosome interactions: A multiscale computational study. J. Am. Chem. Soc. 2015, 137, 10205–10215. [Google Scholar] [CrossRef] [PubMed]
- Schubeler, D.; MacAlpine, D.M.; Scalzo, D.; Wirbelauer, C.; Kooperberg, C.; van Leeuwen, F.; Gottschling, D.E.; O’Neill, L.P.; Turner, B.M.; Delrow, J.; et al. The histone modification pattern of active genes revealed through genome-wide chromatin analysis of a higher eukaryote. Genes Dev. 2004, 18, 1263–1271. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cavalieri, V.; Spinelli, G. Ectopic hbox12 Expression Evoked by Histone Deacetylase Inhibition Disrupts Axial Specification of the Sea Urchin Embryo. PLoS ONE 2015, 10, e0143860. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Di Caro, V.; Cavalieri, V.; Melfi, R.; Spinelli, G. Constitutive promoter occupancy by the MBF-1 activator and chromatin modification of the developmental regulated sea urchin alpha-H2A histone gene. J. Mol. Biol. 2007, 365, 1285–1297. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.B.; Zang, C.Z.; Rosenfeld, J.A.; Schones, D.E.; Barski, A.; Cuddapah, S.; Cui, K.; Roh, T.Y.; Peng, W.; Zhang, M.Q.; et al. Combinatorial patterns of histone acetylations and methylations in the human genome. Nat. Genet. 2008, 40, 897–903. [Google Scholar] [CrossRef] [Green Version]
- Brower-Toland, B.; Wacker, D.A.; Fulbright, R.M.; Lis, J.T.; Kraus, W.L.; Wang, M.D. Specific contributions of histone tails and their acetylation to the mechanical stability of nucleosomes. J. Mol. Biol. 2005, 346, 135–146. [Google Scholar] [CrossRef]
- Chen, Y.; Sprung, R.; Tang, Y.; Ball, H.; Sangras, B.; Kim, S.C.; Falck, J.R.; Peng, J.; Gu, W.; Zhao, Y. Lysine propionylation and butyrylation are novel post-translational modifications in histones. Mol. Cell Proteom. 2007, 6, 812–819. [Google Scholar] [CrossRef] [Green Version]
- Tan, M.; Luo, H.; Lee, S.; **, F.; Yang, J.S.; Montellier, E.; Buchou, T.; Cheng, Z.; Rousseaux, S.; Rajagopal, N.; et al. Identification of 67 histone marks and histone lysine crotonylation as a new type of histone modification. Cell 2011, 146, 1016–1028. [Google Scholar] [CrossRef] [Green Version]
- Huang, H.; Zhang, D.; Wang, Y.; Perez-Neut, M.; Han, Z.; Zheng, Y.G.; Hao, Q.; Zhao, Y. Lysine benzoylation is a histone mark regulated by SIRT2. Nat. Commun. 2018, 9, 3374. [Google Scholar] [CrossRef] [Green Version]
- Dai, L.; Peng, C.; Montellier, E.; Lu, Z.; Chen, Y.; Ishii, H.; Debernardi, A.; Buchou, T.; Rousseaux, S.; **, F.; et al. Lysine 2-hydroxyisobutyrylation is a widely distributed active histone mark. Nat. Chem. Biol. 2014, 10, 365–370. [Google Scholar] [CrossRef]
- ** rate and DNA accessibility. Nucleic Acids Res. 2020, 48, 9538–9549. [Google Scholar] [CrossRef] [PubMed]
- Montellier, E.; Rousseaux, S.; Zhao, Y.; Khochbin, S. Histone crotonylation specifically marks the haploid male germ cell gene expression program: Post-meiotic male-specific gene expression. Bioessays 2012, 34, 187–193. [Google Scholar] [CrossRef] [PubMed]
- Kebede, A.F.; Nieborak, A.; Shahidian, L.Z.; Le Gras, S.; Richter, F.; Gomez, D.A.; Baltissen, M.P.; Meszaros, G.; Magliarelli, H.D.F.; Taudt, A.; et al. Histone propionylation is a mark of active chromatin. Nat. Struct. Mol. Biol. 2017, 24, 1048–1056. [Google Scholar] [CrossRef] [PubMed]
- Ren, X.; Zhou, Y.; Xue, Z.; Hao, N.; Li, Y.; Guo, X.; Wang, D.; Shi, X.; Li, H. Histone benzoylation serves as an epigenetic mark for DPF and YEATS family proteins. Nucleic Acids Res. 2021, 49, 114–126. [Google Scholar] [CrossRef] [PubMed]
- Zhang, D.; Tang, Z.; Huang, H.; Zhou, G.; Cui, C.; Weng, Y.; Liu, W.; Kim, S.; Lee, S.; Perez-Neut, M.; et al. Metabolic regulation of gene expression by histone lactylation. Nature 2019, 574, 575–580. [Google Scholar] [CrossRef]
- Cui, H.; ** of post-translational modifications on synaptic, nuclear, and histone proteins in the adult mouse brain. J. Proteome Res. 2009, 8, 4966–4982. [Google Scholar] [CrossRef] [PubMed]
- Wright, D.E.; Wang, C.Y.; Kao, C.F. Histone ubiquitylation and chromatin dynamics. Front. Biosci. 2012, 17, 1051–1078. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhao, J.; Wang, M.; Chang, L.; Yu, J.; Song, A.; Liu, C.; Huang, W.; Zhang, T.; Wu, X.; Shen, X.; et al. RYBP/YAF2-PRC1 complexes and histone H1-dependent chromatin compaction mediate propagation of H2AK119ub1 during cell division. Nat. Cell Biol. 2020, 22, 439–452. [Google Scholar] [CrossRef]
- Fierz, B.; Chatterjee, C.; McGinty, R.K.; Bar-Dagan, M.; Raleigh, D.P.; Muir, T.W. Histone H2B ubiquitylation disrupts local and higher-order chromatin compaction. Nat. Chem. Biol. 2011, 7, 113–119. [Google Scholar] [CrossRef]
- Dover, J.; Schneider, J.; Tawiah-Boateng, M.A.; Wood, A.; Dean, K.; Johnston, M.; Shilatifard, A. Methylation of histone H3 by COMPASS requires ubiquitination of histone H2B by Rad6. J. Biol. Chem. 2002, 277, 28368–28371. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ng, H.H.; Xu, R.M.; Zhang, Y.; Struhl, K. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J. Biol. Chem. 2002, 277, 34655–34657. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Minsky, N.; Shema, E.; Field, Y.; Schuster, M.; Segal, E.; Oren, M. Monoubiquitinated H2B is associated with the transcribed region of highly expressed genes in human cells. Nat. Cell Biol. 2008, 10, 483–488. [Google Scholar] [CrossRef] [PubMed]
- Kim, J.; Guermah, M.; McGinty, R.K.; Lee, J.S.; Tang, Z.; Milne, T.A.; Shilatifard, A.; Muir, T.W.; Roeder, R.G. RAD6-Mediated transcription-coupled H2B ubiquitylation directly stimulates H3K4 methylation in human cells. Cell 2009, 137, 459–471. [Google Scholar] [CrossRef] [Green Version]
- Krajewski, W.A.; Li, J.; Dou, Y. Effects of histone H2B ubiquitylation on the nucleosome structure and dynamics. Nucleic Acids Res. 2018, 46, 7631–7642. [Google Scholar] [CrossRef] [Green Version]
- Han, J.; Zhang, H.; Zhang, H.; Wang, Z.; Zhou, H.; Zhang, Z. A Cul4 E3 ubiquitin ligase regulates histone hand-off during nucleosome assembly. Cell 2013, 155, 817–829. [Google Scholar] [CrossRef] [Green Version]
- Ryu, H.Y.; Hochstrasser, M. Histone sumoylation and chromatin dynamics. Nucleic Acids Res. 2021, 49, 6043–6052. [Google Scholar] [CrossRef] [PubMed]
- Meulmeester, E.; Melchior, F. Cell biology: SUMO. Nature 2008, 452, 709–711. [Google Scholar] [CrossRef]
- Chandrasekharan, M.B.; Huang, F.; Sun, Z.W. Ubiquitination of histone H2B regulates chromatin dynamics by enhancing nucleosome stability. Proc. Natl. Acad. Sci. USA 2009, 106, 16686–16691. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Nathan, D.; Ingvarsdottir, K.; Sterner, D.E.; Bylebyl, G.R.; Dokmanovic, M.; Dorsey, J.A.; Whelan, K.A.; Krsmanovic, M.; Lane, W.S.; Meluh, P.B.; et al. Histone sumoylation is a negative regulator in Saccharomyces cerevisiae and shows dynamic interplay with positive-acting histone modifications. Genes Dev. 2006, 20, 966–976. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Dhall, A.; Weller, C.E.; Chu, A.; Shelton, P.M.M.; Chatterjee, C. Chemically sumoylated histone H4 stimulates intranucleosomal demethylation by the LSD1-CoREST complex. ACS Chem. Biol. 2017, 12, 2275–2280. [Google Scholar] [CrossRef]
- Jain, N.; Tamborrini, D.; Evans, B.; Chaudhry, S.; Wilkins, B.J.; Neumann, H. Interaction of RSC Chromatin Remodeling Complex with Nucleosomes Is Modulated by H3 K14 Acetylation and H2B SUMOylation In Vivo. iScience 2020, 23, 101292. [Google Scholar] [CrossRef] [PubMed]
- Kalocsay, M.; Hiller, N.J.; Jentsch, S. Chromosome-wide Rad51 spreading and SUMO-H2A.Z-dependent chromosome fixation in response to a persistent DNA double-strand break. Mol. Cell 2009, 33, 335–343. [Google Scholar] [CrossRef]
- Ohkuni, K.; Levy-Myers, R.; Warren, J.; Au, W.C.; Takahashi, Y.; Baker, R.E.; Basrai, M.A. N-terminal sumoylation of centromeric histone H3 variant Cse4 regulates Its proteolysis to prevent mislocalization to non-centromeric chromatin. G3 2018, 8, 1215–1223. [Google Scholar] [CrossRef] [Green Version]
- Ohkuni, K.; Suva, E.; Au, W.C.; Walker, R.L.; Levy-Myers, R.; Meltzer, P.S.; Baker, R.E.; Basrai, M.A. Deposition of centromeric histone H3 variant CENP-A/Cse4 into chromatin is facilitated by its C-terminal sumoylation. Genetics 2020, 214, 839–854. [Google Scholar] [CrossRef]
- Sakabe, K.; Wang, Z.; Hart, G.W. Beta-N-acetylglucosamine (O-GlcNAc) is part of the histone code. Proc. Natl. Acad. Sci. USA 2010, 107, 19915–19920. [Google Scholar] [CrossRef] [Green Version]
- Zhang, S.; Roche, K.; Nasheuer, H.P.; Lowndes, N.F. Modification of histones by sugar β-N-acetylglucosamine (GlcNAc) occurs on multiple residues, including histone H3 serine 10, and is cell cycle-regulated. J. Biol. Chem. 2011, 286, 37483–37495. [Google Scholar] [CrossRef] [Green Version]
- Kreppel, L.K.; Blomberg, M.A.; Hart, G.W. Dynamic glycosylation of nuclear and cytosolic proteins. Cloning and characterization of a unique O-GlcNAc transferase with multiple tetratricopeptide repeats. J. Biol. Chem. 1997, 272, 9308–9315. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Gao, Y.; Wells, L.; Comer, F.I.; Parker, G.J.; Hart, G.W. Dynamic O-glycosylation of nuclear and cytosolic proteins: Cloning and characterization of a neutral, cytosolic beta-N-acetylglucosaminidase from human brain. J. Biol. Chem. 2001, 276, 9838–9845. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Toleman, C.; Paterson, A.J.; Whisenhunt, T.R.; Kudlow, J.E. Characterization of the histone acetyltransferase (HAT) domain of a bifunctional protein with activable O-GlcNAcase and HAT activities. J. Biol. Chem. 2004, 279, 53665–53673. [Google Scholar] [CrossRef] [Green Version]
- Rao, F.V.; Schüttelkopf, A.W.; Dorfmueller, H.C.; Ferenbach, A.T.; Navratilova, I.; van Aalten, D.M. Structure of a bacterial putative acetyltransferase defines the fold of the human O-GlcNAcase C-terminal domain. Open Biol. 2013, 3, 130021. [Google Scholar] [CrossRef] [Green Version]
- He, Y.; Roth, C.; Turkenburg, J.P.; Davies, G.J. Three-dimensional structure of a Streptomyces sviceus GNAT acetyltransferase with similarity to the C-terminal domain of the human GH84 O-GlcNAcase. Acta Crystallogr. D Biol. Crystallogr. 2014, 70, 186–195. [Google Scholar] [CrossRef] [Green Version]
- Chalker, J.M.; Gunnoo, S.B.; Boutureira, O.; Gerstberger, S.C.; Fernandez-Gonzalez, M.; Bernardes, G.J.L.; Griffin, L.; Hailu, H.; Schofield, C.J.; Davis, B.G. Methods for converting cysteine to dehydroalanine on peptides and proteins. Chem. Sci. 2011, 2, 1666–1676. [Google Scholar] [CrossRef]
- Fernández-González, M.; Boutureira, O.; Bernardes, G.J.L.; Chalker, J.M.; Young, M.A.; Errey, J.C.; Davis, B.G. Site-selective chemoenzymatic construction of synthetic glycoproteins using endoglycosidases. Chem. Sci. 2010, 1, 709–715. [Google Scholar] [CrossRef]
- Lercher, L.; Raj, R.; Patel, N.A.; Price, J.; Mohammed, S.; Robinson, C.V.; Schofield, C.J.; Davis, B.G. Generation of a synthetic GlcNAcylated nucleosome reveals regulation of stability by H2A-Thr101 GlcNAcylation. Nat. Commun. 2015, 6, 7978. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raj, R.; Lercher, L.; Mohammed, S.; Davis, B.G. Synthetic Nucleosomes Reveal that GlcNAcylation Modulates Direct Interaction with the FACT Complex. Angew. Chem. Int. Ed. Engl. 2016, 55, 8918–8922. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Fujiki, R.; Hashiba, W.; Sekine, H.; Yokoyama, A.; Chikanishi, T.; Ito, S.; Imai, Y.; Kim, J.; He, H.H.; Igarashi, K.; et al. GlcNAcylation of histone H2B facilitates its monoubiquitination. Nature 2011, 480, 557–560. [Google Scholar] [CrossRef] [PubMed]
- Chen, Q.; Chen, Y.; Bian, C.; Fujiki, R.; Yu, X. TET2 promotes histone O-GlcNAcylation during gene transcription. Nature 2013, 493, 561–564. [Google Scholar] [CrossRef] [PubMed]
- Deplus, R.; Delatte, B.; Schwinn, M.K.; Defrance, M.; Méndez, J.; Murphy, N.; Dawson, M.A.; Volkmar, M.; Putmans, P.; Calonne, E.; et al. TET2 and TET3 regulate GlcNAcylation and H3K4 methylation through OGT and SET1/COMPASS. EMBO J. 2013, 32, 645–655. [Google Scholar] [CrossRef] [PubMed]
- Vella, P.; Scelfo, A.; Jammula, S.; Chiacchiera, F.; Williams, K.; Cuomo, A.; Roberto, A.; Christensen, J.; Bonaldi, T.; Helin, K.; et al. Tet proteins connect the O-linked N-acetylglucosamine transferase Ogt to chromatin in embryonic stem cells. Mol. Cell 2013, 49, 645–656. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.S.; Zhang, Z. O-linked N-acetylglucosamine transferase (OGT) interacts with the histone chaperone HIRA complex and regulates nucleosome assembly and cellular senescence. Proc. Natl. Acad. Sci. USA 2016, 113, E3213–E3220. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Smith, J.A.; Stocken, L.A. Identification of poly (ADP-ribose) covalently bound to histone F1 in vivo. Biochem. Biophys. Res. Commun. 1973, 54, 297–300. [Google Scholar] [CrossRef]
- Glowacki, G.; Braren, R.; Firner, K.; Nissen, M.; Kühl, M.; Reche, P.; Bazan, F.; Cetkovic-Cvrlje, M.; Leiter, E.; Haag, F.; et al. The family of toxin-related ecto-ADP-ribosyltransferases in humans and the mouse. Protein Sci. 2002, 11, 1657–1670. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Messner, S.; Altmeyer, M.; Zhao, H.; Pozivil, A.; Roschitzki, B.; Gehrig, P.; Rutishauser, D.; Huang, D.; Caflisch, A.; Hottiger, M.O. PARP1 ADP-ribosylates lysine residues of the core histone tails. Nucleic Acids Res. 2010, 38, 6350–6362. [Google Scholar] [CrossRef] [Green Version]
- Rulten, S.L.; Fisher, A.E.; Robert, I.; Zuma, M.C.; Rouleau, M.; Ju, L.; Poirier, G.; Reina-San-Martin, B.; Caldecott, K.W. PARP-3 and APLF function together to accelerate nonhomologous end-joining. Mol. Cell 2011, 41, 33–45. [Google Scholar] [CrossRef]
- Kleine, H.; Poreba, E.; Lesniewicz, K.; Hassa, P.O.; Hottiger, M.O.; Litchfield, D.W.; Shilton, B.H.; Lüscher, B. Substrate-assisted catalysis by PARP10 limits its activity to mono-ADP-ribosylation. Mol. Cell 2008, 32, 57–69. [Google Scholar] [CrossRef]
- Liszt, G.; Ford, E.; Kurtev, M.; Guarente, L. Mouse Sir2 homolog SIRT6 is a nuclear ADP-ribosyltransferase. J. Biol. Chem. 2005, 280, 21313–21320. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karch, K.R.; Langelier, M.F.; Pascal, J.M.; Garcia, B.A. The nucleosomal surface is the main target of histone ADP-ribosylation in response to DNA damage. Mol. Biosyst. 2017, 13, 2660–2671. [Google Scholar] [CrossRef] [PubMed]
- Boulikas, T. Poly(ADP-ribosylated) histones in chromatin replication. J. Biol. Chem. 1990, 265, 14638–14647. [Google Scholar] [CrossRef]
- Burzio, L.O.; Riquelme, P.T.; Koide, S.S. ADP ribosylation of rat liver nucleosomal core histones. J. Biol. Chem. 1979, 254, 3029–3037. [Google Scholar] [CrossRef]
- Huletsy, A.; de Murcia, G.; Muller, S.; Hengartner, M.; Ménard, L.; Lamarre, D.; Poirier, G.G. The effect of poly(ADP-ribosyl)ation on native and H1-depleted chromatin. A role of poly(ADP-ribosyl)ation on core nucleosome structure. J. Biol. Chem. 1989, 264, 8878–8886. [Google Scholar] [CrossRef]
- Stone, P.; Lorimer, W.; Kidwell, W. Properties of the complex between histone H1 and poly(ADP-ribose synthesised in HeLa cell nuclei. Eur. J. Biochem. 1977, 81, 9–18. [Google Scholar] [CrossRef] [PubMed]
- Boulikas, T. DNA strand breaks alter histone ADP-ribosylation. Proc. Natl. Acad. Sci. USA 1989, 86, 3499–3503. [Google Scholar] [CrossRef] [Green Version]
- Poirier, G.G.; de Murcia, G.; Jongstra-Bilen, J.; Niedergang, C.; Mandel, P. Poly(ADP-ribosyl)ation of polynucleosomes causes relaxation of chromatin structure. Proc. Natl. Acad. Sci. USA 1982, 79, 3423–3427. [Google Scholar] [CrossRef] [Green Version]
- De Murcia, G.; Huletsky, A.; Lamarre, D.; Gaudreau, A.; Pouyet, J.; Daune, M.; Poirier, G.G. Modulation of chromatin superstructure induced by poly(ADP-ribose) synthesis and degradation. J. Biol. Chem. 1986, 261, 7011–7017. [Google Scholar] [CrossRef]
- Petesch, S.J.; Lis, J.T. Activator-induced spread of poly(ADP-ribose) polymerase promotes nucleosome loss at Hsp70. Mol. Cell 2012, 45, 64–74. [Google Scholar] [CrossRef] [Green Version]
- Lehmann, M.; Pirinen, E.; Mirsaidi, A.; Kunze, F.A.; Richards, P.J.; Auwerx, J.; Hottiger, M.O. ARTD1-induced poly-ADP-ribose formation enhances PPARγ ligand binding and co-factor exchange. Nucleic Acids Res. 2015, 43, 129–142. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hymes, J.; Fleischhauer, K.; Wolf, B. Biotinylation of histones by human serum biotinidase: Assessment of biotinyl-transferase activity in sera from normal individuals and children with biotinidase deficiency. Biochem. Mol. Med. 1995, 56, 76–83. [Google Scholar] [CrossRef]
- Kothapalli, N.; Camporeale, G.; Kueh, A.; Chew, Y.C.; Oommen, A.M.; Griffin, J.B.; Zempleni, J. Biological functions of biotinylated histones. J. Nutr. Biochem. 2005, 16, 446–448. [Google Scholar] [CrossRef] [Green Version]
- Brenner, C. Catalysis in the nitrilase superfamily. Curr. Opin. Struct. Biol. 2002, 12, 775–782. [Google Scholar] [CrossRef]
- Narang, M.A.; Dumas, R.; Ayer, L.M.; Gravel, R.A. Reduced histone biotinylation in multiple carboxylase deficiency patients: A nuclear role for holocarboxylase synthetase. Hum. Mol. Genet. 2004, 13, 15–23. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Bao, B.; Pestinger, V.; Hassan, Y.I.; Borgstahl, G.E.; Kolar, C.; Zempleni, J. Holocarboxylase synthetase is a chromatin protein and interacts directly with histone H3 to mediate biotinylation of K9 and K18. J. Nutr. Biochem. 2011, 22, 470–475. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ballard, T.D.; Wolff, J.; Griffin, J.B.; Stanley, J.S.; van Calcar, S.; Zempleni, J. Biotinidase catalyzes debiotinylation of histones. Eur. J. Nutr. 2002, 41, 78–84. [Google Scholar] [CrossRef] [PubMed]
- Bailey, L.M.; Ivanov, R.A.; Wallace, J.C.; Polyak, S.W. Artifactual detection of biotin on histones by streptavidin. Anal. Biochem. 2008, 373, 71–77. [Google Scholar] [CrossRef] [PubMed]
- Kuroishi, T.; Rios-Avila, L.; Pestinger, V.; Wijeratne, S.S.; Zempleni, J. Biotinylation is a natural, albeit rare, modification of human histones. Mol. Genet. Metab. 2011, 104, 537–545. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Stanley, J.S.; Griffin, J.B.; Zempleni, J. Biotinylation of histones in human cells: Effects of cell proliferation. Eur. J. Biochem. 2001, 268, 5424–5429. [Google Scholar] [CrossRef]
- Smith, E.M.; Hoi, J.T.; Eissenberg, J.C.; Shoemaker, J.D.; Neckameyer, W.S.; Ilvarsonn, A.M.; Harshman, L.G.; Schlegel, V.L.; Zempleni, J. Feeding Drosophila a biotin-deficient diet for multiple generations increases stress resistance and lifespan and alters gene expression and histone biotinylation patterns. J. Nutr. 2007, 137, 2006–2012. [Google Scholar] [CrossRef] [Green Version]
- Pestinger, V.; Wijeratne, S.S.; Rodriguez-Melendez, R.; Zempleni, J. Novel histone biotinylation marks are enriched in repeat regions and participate in repression of transcriptionally competent genes. J. Nutr. Biochem. 2011, 22, 328–333. [Google Scholar] [CrossRef] [Green Version]
- Chew, Y.C.; West, J.T.; Kratzer, S.J.; Ilvarsonn, A.M.; Eissenberg, J.C.; Dave, B.J.; Klinkebiel, D.; Christman, J.K.; Zempleni, J. Biotinylation of histones represses transposable elements in human and mouse cells and cell lines and in Drosophila melanogaster. J. Nutr. 2008, 138, 2316–2322. [Google Scholar] [CrossRef] [Green Version]
- Camporeale, G.; Oommen, A.M.; Griffin, J.B.; Sarath, G.; Zempleni, J. K12-biotinylated histone H4 marks heterochromatin in human lymphoblastoma cells. J. Nutr. Biochem. 2007, 18, 760–768. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wijeratne, S.S.; Camporeale, G.; Zempleni, J. K12-biotinylated histone H4 is enriched in telomeric repeats from human lung IMR-90 fibroblasts. J. Nutr. Biochem. 2010, 21, 310–316. [Google Scholar] [CrossRef] [Green Version]
- Li, Y.; Hassan, Y.I.; Moriyama, H.; Zempleni, J. Holocarboxylase synthetase interacts physically with euchromatic histone-lysine N-methyltransferase, linking histone biotinylation with methylation events. J. Nutr. Biochem. 2013, 24, 1446–1452. [Google Scholar] [CrossRef] [Green Version]
- Filenko, N.A.; Kolar, C.; West, J.T. Smith SA, Hassan YI, Borgstahl GE, Zempleni, J., Lyubchenko YL. The role of histone H4 biotinylation in the structure of nucleosomes. PLoS ONE 2011, 6, e16299. [Google Scholar] [CrossRef] [Green Version]
- Singh, M.P.; Wijeratne, S.S.; Zempleni, J. Biotinylation of lysine 16 in histone H4 contributes toward nucleosome condensation. Arch. Biochem. Biophys. 2013, 529, 105–111. [Google Scholar] [CrossRef] [Green Version]
- Farrelly, L.A.; Thompson, R.E.; Zhao, S.; Lepack, A.E.; Lyu, Y.; Bhanu, N.V.; Zhang, B.; Loh, Y.E.; Ramakrishnan, A.; Vadodaria, K.C.; et al. Histone serotonylation is a permissive modification that enhances TFIID binding to H3K4me3. Nature 2019, 567, 535–539. [Google Scholar] [CrossRef]
- Lepack, A.E.; Werner, C.T.; Stewart, A.F.; Fulton, S.L.; Zhong, P.; Farrelly, L.A.; Smith, A.C.W.; Ramakrishnan, A.; Lyu, Y.; Bastle, R.M.; et al. Dopaminylation of histone H3 in ventral tegmental area regulates cocaine seeking. Science 2020, 368, 197–201. [Google Scholar] [CrossRef]
- Lindner, H.; Sarg, B.; Hoertnagl, B.; Helliger, W. The microheterogeneity of the mammalian H1(0) histone. Evidence for an age-dependent deamidation. J. Biol. Chem. 1998, 273, 13324–13330. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lorand, L.; Graham, R.M. Transglutaminases: Crosslinking enzymes with pleiotropic functions. Nat. Rev. Mol. Cell Biol. 2003, 4, 140–156. [Google Scholar] [CrossRef]
- Vermeulen, M.; Mulder, K.W.; Denissov, S.; Pijnappel, W.W.; van Schaik, F.M.; Varier, R.A.; Baltissen, M.P.; Stunnenberg, H.G.; Mann, M.; Timmers, H.T. Selective anchoring of TFIID to nucleosomes by trimethylation of histone H3 lysine 4. Cell 2007, 131, 58–69. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lauberth, S.M.; Nakayama, T.; Wu, X.; Ferris, A.L.; Tang, Z.; Hughes, S.H.; Roeder, R.G. H3K4me3 interactions with TAF3 regulate preinitiation complex assembly and selective gene activation. Cell 2013, 152, 1021–1036. [Google Scholar] [CrossRef] [Green Version]
- Zhao, J.; Chen, W.; Pan, Y.; Zhang, Y.; Sun, H.; Wang, H.; Yang, F.; Liu, Y.; Shen, N.; Zhang, X.; et al. Structural insights into the recognition of histone H3Q5 serotonylation by WDR5. Sci. Adv. 2021, 7, eabf4291. [Google Scholar] [CrossRef]
- Wysocka, J.; Swigut, T.; Milne, T.A.; Dou, Y.; Zhang, X.; Burlingame, A.L.; Roeder, R.G.; Brivanlou, A.H.; Allis, C.D. WDR5 associates with histone H3 methylated at K4 and is essential for H3 K4 methylation and vertebrate development. Cell 2005, 121, 859–872. [Google Scholar] [CrossRef] [Green Version]
- Wedemeyer, W.J.; Welker, E.; Scheraga, H.A. Proline cis-trans isomerization and protein folding. Biochemistry 2002, 41, 14637–14644. [Google Scholar] [CrossRef] [PubMed]
- Göthel, S.F.; Marahiel, M.A. Peptidyl-prolyl cis-trans isomerases, a superfamily of ubiquitous folding catalysts. Cell Mol. Life Sci. 1999, 55, 423–436. [Google Scholar] [CrossRef] [PubMed]
- Nelson, C.J.; Santos-Rosa, H.; Kouzarides, T. Proline isomerization of histone H3 regulates lysine methylation and gene expression. Cell 2006, 126, 905–916. [Google Scholar] [CrossRef] [Green Version]
- Yang, W.M.; Yao, Y.L.; Seto, E. The FK506-binding protein 25 functionally associates with histone deacetylases and with transcription factor YY1. EMBO J. 2001, 20, 4814–4825. [Google Scholar] [CrossRef] [Green Version]
- Howe, F.S.; Boubriak, I.; Sale, M.J.; Nair, A.; Clynes, D.; Grijzenhout, A.; Murray, S.C.; Woloszczuk, R.; Mellor, J. Lysine acetylation controls local protein conformation by influencing proline isomerization. Mol. Cell 2014, 55, 733–744. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tan, H.L.; Lim, K.K.; Yang, Q.; Fan, J.S.; Sayed, A.M.M.; Low, L.S.; Ren, B.; Lim, T.K.; Lin, Q.; Mok, Y.K.; et al. Prolyl isomerization of the CENP-A N-terminus regulates centromeric integrity in fission yeast. Nucleic Acids Res. 2018, 46, 1167–1179. [Google Scholar] [CrossRef] [PubMed]
- Furuchi, T.; Sakurako, K.; Katane, M.; Sekine, M.; Homma, H. The role of protein L-isoaspartyl/D-aspartyl O-methyltransferase (PIMT) in intracellular signal transduction. Chem. Biodivers. 2010, 7, 1337–1348. [Google Scholar] [CrossRef] [PubMed]
- Young, A.L.; Carter, W.G.; Doyle, H.A.; Mamula, M.J.; Aswad, D.W. Structural integrity of histone H2B in vivo requires the activity of protein L-isoaspartate O-methyltransferase a putative protein repair enzyme. J. Biol. Chem. 2001, 276, 37161–37165. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Young, G.W.; Hoofring, S.A.; Mamula, M.J.; Doyle, H.A.; Bunick, G.J.; Hu, Y.; Aswad, D.W. Protein L-isoaspartyl methyltransferase catalyzes in vivo racemization of Aspartate-25 in mammalian histone H2B. J. Biol. Chem. 2005, 280, 26094–26098. [Google Scholar] [CrossRef] [Green Version]
- Qin, Z.; Zhu, J.X.; Aswad, D.W. The D-isoAsp-25 variant of histone H2B is highly enriched in active chromatin: Potential role in the regulation of gene expression? Amino Acids 2016, 48, 599–603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maillard, L.C. Action des acidesamines sur les sucres: Formation des melanoidines par voie methodique. CR Acad. Sci. Paris 1912, 154, 66–68. [Google Scholar]
- Ansari, N.A.; Chaudhary, D.K.; Dash, D. Modification of histone by glyoxal: Recognition of glycated histone containing advanced glycation adducts by serum antibodies of type 1 diabetes patients. Glycobiology 2018, 28, 207–213. [Google Scholar] [CrossRef]
- Hellwig, M.; Henle, T. Baking, ageing, diabetes: A short history of the Maillard reaction. Angew. Chem. Int. Ed. Engl. 2014, 53, 10316–10329. [Google Scholar] [CrossRef]
- Galligan, J.J.; Wepy, J.A.; Streeter, M.D.; Kingsley, P.J.; Mitchener, M.M.; Wauchope, O.R.; Beavers, W.N.; Rose, K.L.; Wang, T.; Spiegel, D.A.; et al. Methylglyoxal-derived posttranslational arginine modifications are abundant histone marks. Proc. Natl. Acad. Sci. USA 2018, 115, 9228–9233. [Google Scholar] [CrossRef] [Green Version]
- Zheng, Q.; Omans, N.D.; Leicher, R.; Osunsade, A.; Agustinus, A.S.; Finkin-Groner, E.; D’Ambrosio, H.; Liu, B.; Chandarlapaty, S.; Liu, S.; et al. Reversible histone glycation is associated with disease-related changes in chromatin architecture. Nat. Commun. 2019, 10, 1289. [Google Scholar] [CrossRef] [Green Version]
- Ashraf, J.M.; Rabbani, G.; Ahmad, S.; Hasan, Q.; Khan, R.H.; Alam, K.; Choi, I. Glycation ofH1 histone by 3-deoxyglucosone: Effects on protein structure and generation of different advanced glycation end products. PLoS ONE 2015, 10, e0130630. [Google Scholar]
- Rahmanpour, R.; Bathaie, S.Z. Histone H1 structural changes and its interaction with DNA in the presence of high glucose concentration in vivo and in vitro. J. Biomol. Struct. Dyn. 2011, 28, 575–586. [Google Scholar] [CrossRef]
- Zheng, Q.; Osunsade, A.; David, Y. Protein arginine deiminase 4 antagonizes methylglyoxal-induced histone glycation. Nat. Commun. 2020, 11, 3241. [Google Scholar] [CrossRef]
- Uchida, K. 4-Hydroxy-2-nonenal: A product and mediator of oxidative stress. Prog. Lipid Res. 2003, 42, 318–343. [Google Scholar] [CrossRef]
- Lee, S.H.; Blair, I.A. Characterization of 4-oxo-2-nonenal as a novel product of lipid peroxidation. Chem. Res. Toxicol. 2000, 13, 698–702. [Google Scholar] [CrossRef] [PubMed]
- Galligan, J.J.; Rose, K.L.; Beavers, W.N.; Hill, S.; Tallman, K.A.; Tansey, W.P.; Marnett, L.J. Stable histone adduction by 4-oxo-2-nonenal: A potential link between oxidative stress and epigenetics. J. Am. Chem. Soc. 2014, 136, 11864–11866. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Geib, T.; Iacob, C.; Jribi, R.; Fernandes, J.; Benderdour, M.; Sleno, L. Identification of 4-hydroxynonenal-modified proteins in human osteoarthritic chondrocytes. J. Proteom. 2021, 232, 104024. [Google Scholar] [CrossRef]
- Drake, J.; Petroze, R.; Castegna, A.; Ding, Q.; Keller, J.N.; Markesbery, W.R.; Lovell, M.A.; Butterfield, D.A. 4-Hydroxynonenal oxidatively modifies histones: Implications for Alzheimer’s disease. Neurosci. Lett. 2004, 356, 155–158. [Google Scholar] [CrossRef] [PubMed]
- Pellicanò, M.; Picone, P.; Cavalieri, V.; Carrotta, R.; Spinelli, G.; Di Carlo, M. The sea urchin embryo: A model to study Alzheimer’s beta amyloid induced toxicity. Arch. Biochem. Biophys. 2009, 483, 120–126. [Google Scholar] [CrossRef] [PubMed]
- Jiang, T.; Zhou, X.; Taghizadeh, K.; Dong, M.; Dedon, P.C. N-formylation of lysine in histone proteins as a secondary modification arising from oxidative DNA damage. Proc. Natl. Acad. Sci. USA 2007, 104, 60–65. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Walport, L.J.; Hopkinson, R.J.; Schofield, C.J. Mechanisms of human histone and nucleic acid demethylases. Curr. Opin. Chem. Biol. 2012, 16, 525–534. [Google Scholar] [CrossRef]
- Edrissi, B.; Taghizadeh, K.; Dedon, P.C. Quantitative analysis of histone modifications: Formaldehyde is a source of pathological n(6)-formyllysine that is refractory to histone deacetylases. PLoS Genet. 2013, 9, e1003328. [Google Scholar] [CrossRef] [Green Version]
- Wang, T.; Zhou, Q.; Li, F.; Yu, Y.; Yin, X.; Wang, J. Genetic Incorporation of N(ε)-Formyllysine, a New Histone Post-translational Modification. Chembiochem 2015, 16, 1440–1442. [Google Scholar] [CrossRef]
- Wisniewski, J.R.; Zougman, A.; Mann, M. Nepsilon-formylation of lysine is a widespread post-translational modification of nuclear proteins occurring at residues involved in regulation of chromatin function. Nucleic Acids Res. 2008, 36, 570–577. [Google Scholar] [CrossRef]
- Eickbush, T.H.; Watson, D.K.; Moudrianakis, E.N. A chromatin-bound proteolytic activity with unique specificity for histone H2A. Cell 1976, 9, 785–792. [Google Scholar] [CrossRef]
- Allis, C.D.; Bowen, J.K.; Abraham, G.N.; Glover, C.V.; Gorovsky, M.A. Proteolytic processing of histone H3 in chromatin: A physiologically regulated event in Tetrahymena micronuclei. Cell 1980, 20, 55–64. [Google Scholar] [CrossRef]
- Azad, G.K.; Swagatika, S.; Kumawat, M.; Kumawat, R.; Tomar, R.S. Modifying chromatin by histone tail clip**. J. Mol. Biol. 2018, 430, 3051–3067. [Google Scholar] [CrossRef] [PubMed]
- Santos-Rosa, H.; Kirmizis, A.; Nelson, C.; Bartke, T.; Saksouk, N.; Cote, J.; Kouzarides, T. Histone H3 tail clip** regulates gene expression. Nat. Struct. Mol. Biol. 2009, 16, 17–22. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Allis, C.D.; Wiggins, J.C. Proteolytic processing of micronuclear H3 and histone phosphorylation during conjugation in Tetrahymena thermophila. Exp. Cell Res. 1984, 153, 287–298. [Google Scholar] [CrossRef]
- Herrera-Solorio, A.M.; Vembar, S.S.; MacPherson, C.R.; Lozano-Amado, D.; Meza, G.R.; Xoconostle-Cazares, B.; Martins, R.M.; Chen, P.; Vargas, M.; Scherf, A.; et al. Clipped histone H3 is integrated into nucleosomes of DNA replication genes in the human malaria parasite Plasmodium falciparum. EMBO Rep. 2019, 20, e46331. [Google Scholar] [CrossRef] [PubMed]
- Duncan, E.M.; Muratore-Schroeder, T.L.; Cook, R.G.; Garcia, B.A.; Shabanowitz, J.; Hunt, D.F.; Allis, C.D. Cathepsin L proteolytically processes histone H3 during mouse embryonic stem cell differentiation. Cell 2008, 135, 284–294. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, K.; Punj, V.; Kim, J.M.; Lee, S.; Ulmer, T.S.; Lu, W.; Rice, J.C.; An, W. MMP-9 facilitates selective proteolysis of the histone H3 tail at genes necessary for proficient osteoclastogenesis. Genes Dev. 2016, 30, 208–219. [Google Scholar] [CrossRef] [Green Version]
- Duarte, L.F.; Young, A.R.; Wang, Z.; Wu, H.A.; Panda, T.; Kou, Y.; Kapoor, A.; Hasson, D.; Mills, N.R.; Ma’ayan, A.; et al. Histone H3.3 and its proteolytically processed form drive a cellular senescence programme. Nat. Commun. 2014, 5, 5210. [Google Scholar] [CrossRef] [Green Version]
- Cavalieri, V.; Bernardo, M.D.; Spinelli, G. Regulatory sequences driving expression of the sea urchin Otp homeobox gene in oral ectoderm cells. Gene Expr. Patterns 2007, 7, 124–130. [Google Scholar] [CrossRef] [PubMed]
- Biswas, M.; Voltz, K.; Smith, J.C.; Langowski, J. Role of histone tails in structural stability of the nucleosome. PLoS Comput. Biol. 2011, 7, e1002279. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Guyon, J.R.; Narlikar, G.J.; Sif, S.; Kingston, R.E. Kingston, Stable remodeling of tailless nucleosomes by the human SWI– SNF complex. Mol. Cell Biol. 1999, 19, 2088–2097. [Google Scholar] [CrossRef] [Green Version]
- Vogler, C.; Huber, C.; Waldmann, T.; Ettig, R.; Braun, L.; Izzo, A.; Daujat, S.; Chassignet, I.; Lopez-Contreras, A.J.; Fernandez-Capetillo, O.; et al. Histone H2A C-terminus regulates chromatin dynamics, remodeling, and histone H1 binding. PLoS Genet. 2010, 6, e1001234. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Iwasaki, W.; Miya, Y.; Horikoshi, N.; Osakabe, A.; Taguchi, H.; Tachiwana, H.; Shibata, T.; Kagawa, W.; Kurumizaka, H. Contribution of histone N-terminal tails to the structure and stability of nucleosomes. FEBS Open Bio 2013, 3, 363–369. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, H.; Wang, C.; Lee, S.; Deng, Y.; Wither, M.; Oh, S.; Ning, F.; Dege, C.; Zhang, Q.; Liu, X.; et al. Clip** of arginine-methylated histone tails by JMJD5 and JMJD7. Proc. Natl. Acad. Sci. USA 2017, 114, E7717–E7726. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Liu, H.; Wang, C.; Lee, S.; Ning, F.; Wang, Y.; Zhang, Q.; Chen, Z.; Zang, J.; Nix, J.; Dai, S.; et al. Specific Recognition of Arginine Methylated Histone Tails by JMJD5 and JMJD7. Sci. Rep. 2018, 8, 3275. [Google Scholar] [CrossRef] [PubMed]
- Studitsky, V.M.; Kassavetis, G.A.; Geiduschek, E.P.; Felsenfeld, G. Mechanism of transcription through the nucleosome by eukaryotic RNA polymerase. Science 1997, 278, 1960–1963. [Google Scholar] [CrossRef]
- Bal, W.; Lukszo, J.; Bialkowski, K.; Kasprzak, K.S. Interactions of Nickel(II) with histones: Interactions of Nickel(II) with CH3CO-Thr-Glu-Ser-His-His-Lys-NH2, a peptide modeling the potential metal binding site in the "C-Tail" region of histone H2A. Chem. Res. Toxicol. 1998, 11, 1014–1023. [Google Scholar] [CrossRef]
- Bal, W.; Liang, R.; Lukszo, J.; Lee, S.H.; Dizdaroglu, M.; Kasprzak, K.S. Ni(II) specifically cleaves the C-terminal tail of the major variant of histone H2A and forms an oxidative damage-mediating complex with the cleaved-off octapeptide. Chem. Res. Toxicol. 2000, 13, 616–624. [Google Scholar] [CrossRef] [PubMed]
- Karaczyn, A.A.; Bal, W.; North, S.L.; Bare, R.M.; Hoang, V.M.; Fisher, R.J.; Kasprzak, K.S. The octapeptidic end of the C-terminal tail of histone H2A is cleaved off in cells exposed to carcinogenic nickel(II). Chem. Res. Toxicol. 2003, 16, 1555–1559. [Google Scholar] [CrossRef]
- Usachenko, S.I.; Bavykin, S.G.; Gavin, I.M.; Bradbury, E.M. Rearrangement of the histone H2A C-terminal domain in the nucleosome. Proc. Natl. Acad. Sci. USA 1994, 91, 6845–6849. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Karaczyn, A.A.; Cheng, R.Y.; Buzard, G.S.; Hartley, J.; Esposito, D.; Kasprzak, K.S. Truncation of histone H2A’s C-terminal tail, as is typical for Ni(II)-assisted specific peptide bond hydrolysis, has gene expression altering effects. Ann. Clin. Lab. Sci. 2009, 39, 251–262. [Google Scholar] [PubMed]
- Lindner, H.; Sarg, B.; Grunicke, H.; Helliger, W. Age-dependent deamidation of H1(0) histones in chromatin of mammalian tissues. J. Cancer Res. Clin. Oncol. 1999, 125, 182–186. [Google Scholar] [CrossRef]
- Wondrak, G.T.; Cervantes-Laurean, D.; Jacobson, E.L.; Jacobson, M.K. Histone carbonylation in vivo and in vitro. Biochem. J. 2000, 351, 769–777. [Google Scholar] [CrossRef]
- Dixit, K.; Khan, M.A.; Sharma, Y.D.; Moinuddin; Alam, K. Physicochemical studies on peroxynitrite-modified H3 histone. Int. J. Biol. Macromol. 2010, 46, 20–26. [Google Scholar] [CrossRef]
- Unoki, M.; Masuda, A.; Dohmae, N.; Arita, K.; Yoshimatsu, M.; Iwai, Y.; Fukui, Y.; Ueda, K.; Hamamoto, R.; Shirakawa, M.; et al. Lysyl 5-hydroxylation, a novel histone modification, by Jumonji domain containing 6 (JMJD6). J. Biol. Chem. 2013, 288, 6053–6062. [Google Scholar] [CrossRef] [Green Version]
- Paulsen, C.E.; Carroll, K.S. Cysteine-mediated redox signaling: Chemistry, biology, and tools for discovery. Chem. Rev. 2013, 113, 4633–4679. [Google Scholar] [CrossRef]
- De Luca, A.; Moroni, N.; Serafino, A.; Primavera, A.; Pastore, A.; Pedersen, J.Z.; Petruzzelli, R.; Farrace, M.G.; Pierimarchi, P.; Moroni, G.; et al. Treatment of doxorubicin-resistant MCF7/Dx cells with nitric oxide causes histone glutathionylation and reversal of drug resistance. Biochem. J. 2011, 440, 175–183. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Tessarz, P.; Santos-Rosa, H.; Robson, S.C.; Sylvestersen, K.B.; Nelson, C.J.; Nielsen, M.L.; Kouzarides, T. Glutamine methylation in histone H2A is an RNA-polymerase-I-dedicated modification. Nature 2014, 505, 564–568. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cebrià-Costa, J.P.; Pascual-Reguant, L.; Gonzalez-Perez, A.; Serra-Bardenys, G.; Querol, J.; Cosín, M.; Verde, G.; Cigliano, R.A.; Sanseverino, W.; Segura-Bayona, S.; et al. LOXL2-mediated H3K4 oxidation reduces chromatin accessibility in triple-negative breast cancer cells. Oncogene 2020, 39, 79–121. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Strahl, B.D.; Allis, C.D. The language of covalent histone modifications. Nature 2000, 403, 41–44. [Google Scholar] [CrossRef] [PubMed]
- Henikoff, S.; Shilatifard, A. Histone modification: Cause or cog? Trends Genet. 2011, 27, 389–396. [Google Scholar] [CrossRef]
- Ernst, J.; Kellis, M. Discovery and characterization of chromatin states for systematic annotation of the human genome. Nat. Biotechnol. 2010, 28, 817–825. [Google Scholar] [CrossRef] [Green Version]
- Voigt, P.; LeRoy, G.; Drury, W.J., 3rd; Zee, B.M.; Son, J.; Beck, D.B.; Young, N.L.; Garcia, B.A.; Reinberg, D. Asymmetrically modified nucleosomes. Cell 2012, 151, 181–193. [Google Scholar] [CrossRef] [Green Version]
- Voigt, P.; Tee, W.W.; Reinberg, D. A double take on bivalent promoters. Genes Dev. 2013, 27, 1318–1338. [Google Scholar] [CrossRef] [Green Version]
- Dion, M.; Kaplan, T.; Friedman, N.; Rando, O.J. Dynamics of replication-independent histone turnover in budding yeast. Science 2007, 315, 1405–1408. [Google Scholar] [CrossRef]
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations. |
© 2021 by the author. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
Share and Cite
Cavalieri, V. The Expanding Constellation of Histone Post-Translational Modifications in the Epigenetic Landscape. Genes 2021, 12, 1596. https://doi.org/10.3390/genes12101596
Cavalieri V. The Expanding Constellation of Histone Post-Translational Modifications in the Epigenetic Landscape. Genes. 2021; 12(10):1596. https://doi.org/10.3390/genes12101596
Chicago/Turabian StyleCavalieri, Vincenzo. 2021. "The Expanding Constellation of Histone Post-Translational Modifications in the Epigenetic Landscape" Genes 12, no. 10: 1596. https://doi.org/10.3390/genes12101596