2025, Number 2
<< Back Next >>
Rev Educ Bioquimica 2025; 44 (2)
Modificaciones en las histonas: su importancia en la identificación y reparación del daño al DNA
González-Gutiérrez AM, Ortiz-Muñiz AR, García-Rodríguez MC, Cortés-Barberena E
Language: Spanish
References: 76
Page: 70-81
PDF size: 612.95 Kb.
ABSTRACT
The purpose of this review is to present relevant information regarding the main histone modifications that intervene in the detection and repair of damaged genetic material (known as DNA damage response, (DDR)). Genomic integrity is vital for cellular well-being. Cells have developed review and maintenance systems to ensure adequate protection of genetic information. The nuclear genome is organized into a complex of histones and deoxyribonucleic acid (DNA) called nucleosome; the adaptability of this structure allows access to the proteins necessary to carry out biological processes such as transcription, duplication, and DNA repair. Histone proteins can present chemical modifications that, alone or in combination with others, provide specific biological results; this is known as the 'histone code'. In recent years, the study of post-translational modifications (PTMs) in histone proteins and their connection with the network of pathways DDR has increased.
REFERENCES
Chatterjee N, Walker GC. Mechanisms of DNAdamage, repair and mutagenesis. Environ MolMutagen. 2017; 58(5):235-63.
Brown JS, Jackson SP. Ubiquitylation,neddylation and the DNA damage response. OpenBiol. 2015; 5(4):1-21.
Liu Y, Li Y, Lu X. Regulators in the DNAdamage response. Arch Biochem Biophys. 2016;594:18-25.
Koyama M, Kurumizaka H. Structural diversityof the nucleosome. J Biochem (Tokyo). 2018;163(2):85-95.
Corujo D, Buschbeck M. Post-translationalmodifications of H2A histone variants and their rolein cancer. Cancers. 2018; 10(3):1-25.
Vlijm R, Lee M, Jan L, Lusser A, Dekker C,Dekker NH. Nucleosome Assembly DynamicsInvolve Spontaneous Fluctuations in the Handed-ness of Tetrasomes. Cell. 2015; 10(2):216-25.
Prado F, Jimeno-González S, Reyes JC. Histoneavailability as a strategy to control gene expression.RNA Biol. 2016; 14(3):281-6.
Cheema MS, Ausió J. The structural determi-nants behind the epigenetic role of histone variants.Genes. 2015; 6(3):685-713.
Govaert E, Van Steendam K, Scheerlinck E,Vossaert L, Meert P, Stella M, et al. Extractinghistones for the specific purpose of label-free MS.Proteomics. 2016; 16(23):2937-44.
Jenuwein T, Allis CD. Translating the histonecode. Science. 2001; 293(5532):1074-80.
Sneppen K, Dodd IB. A simple histone codeopens many paths to epigenetics. PLoS ComputBiol. 2012; 8(8):1-10.
Oweis W, Padala P, Hassouna F, Cohen-KfirE, Gibbs DR, Todd EA, et al. Trans-binding mech-anism of ubiquitin-like protein activation revealed by a UBA5-UFM1 complex. Cell Rep. 2016; 16(12):3113-20.
Wei Y, Xu X. UFMylation: A unique &fashionable modification for life. GPB. 2016;14(3):140-6.
Roque A, Ponte I, Suau P. Post-translationalmodifications of the intrinsically disorderedterminal domains of histone H1: effects onsecondary structure and chromatin dynamics.Chromosoma. 2017; 126(1):83-91.
Izzo A, Schneider R. The role of linker histoneH1 modifications in the regulation of geneexpression and chromatin dynamics. BiochimBiophys Acta BBA-Gene Regul Mech. 2016;1859(3):486-95.
Bönisch C, Hake SB. Histone H2A variants innucleosomes and chromatin: more or less stable?Nucleic Acids Res. 2012; 40(21):10719-41.
Shaytán AK, Landsman D, Panchenko AR.Nucleosome adaptability conferred by sequence andstructural variations in histone H2A-H2B dimers.Curr Opin Struct Biol. 2015; 32:48-57.
Phillips EON, Gunjan A. Histone variants:The unsung guardians of the genome. DNA Repair.2022; 112:1-41.
Dhahri H, Saintilnord WN, Chandler D,Fondufe-Mittendorf YN. Beyond the UsualSuspects: Examining the Role of UnderstudiedHistone Variants in Breast Cancer. Int J Mol Sci.2024; 25(12):1-24.
Osakabe A, Molaro A. Histone renegades:Unusual H2A histone variants in plants and animals.Semin Cell Dev Biol. 2023; 15(135):35-42.
Jiang D, Borg M, Lorković ZJ, MontgomerySA, Osakabe A, Yelagandula R, et al. The evolutionand functional divergence of the histone H2B family in plants. PLoS Genet. 2020; 16(7):1-22.
Raman P, Rominger MC, Young JM, MolaroA, Tsukiyama T, Malik HS. Novel Classes andEvolutionary Turnover of Histone H2B Variants inthe Mammalian Germline. Mol Biol Evol. 2022;39(2):1-19.
Lai PM, Gong X, Chan KM. Roles of histoneH2B, H3 and H4 variants in cancer developmentand prognosis. Int J Mol Sci. 2024; 25(17):1-33.
Delaney K, Weiss N, Almouzni G. The cell-cycle choreography of H3 variants shapes thegenome. Mol Cell. 2023; 83(21):3773-86.
Trovato M, Patil V, Gehre M, Noh KM.Histone Variant H3.3 Mutations in Defining theChromatin Function in Mammals. Cells. 2020;9(12):1-22.
Ray-Gallet D, Almouzni G. H3–H4 histonechaperones and cancer. Curr Opin Genet Dev. 2022;73:1-8.
Talbert PB, Henikoff S. Histone variants at aglance. J Cell Sci. 2021; 134(6):1-10.
Chen D, Jin C. Histone variants inenvironmental-stress-induced DNA damage repair.Mutat Res Mutat Res. 2019; 780:55-60.
Ghiraldini FG, Filipescu, Dan, Bernstein,Emily. Solid tumours hijack the histone variantnetwork. Nat Rev Cancer. 2021; 21(4):257-75.
Rossetto D, Avvakumov N, Côté J. Histonephosphorylation A chromatin modification involvedin diverse nuclear events. Epigenetics. 2012;7(10):1098-108.
Song J, Wang H, Wang J, Leier A, Marquez-Lago T, Yang B, et al. PhosphoPredict: Abioinformatics tool for prediction of human kinase-specific phosphorylation substrates and sites byintegrating heterogeneous feature selection. SciRep. 2017; 7(6862):1-19.
Talasz H, Helliger W, Puschendorf B, LindnerH.In Vivo Phosphorylation of Histone H1 Variantsduring the Cell Cycle. Biochemistry. 1996;35(6):1761-7.
Hunt CR, Ramnarain D, Horikoshi N, IyengarP, Pandita RK, Shay JW, et al. Histone Modi-fications and DNA Double-Strand Break Repairafter Exposure to Ionizing Radiations. Radiat Res.2013; 179(4):383-92.
Lai SJ, Tu IF, Wu WL, Yang JT, Luk LYP,Lai MC, et al. Site-specific His/Asp phospho-proteomic analysis of prokaryotes reveals putativetargets for drug resistance. BMC Microbiol. 2017; 17(123):1-10.
Andrés M, García-Gomis D, Ponte I, Suau P,Roque A. Histone H1 Post-Translational Modi-fications: Update and Future Perspectives. Int J MolSci. 2020; 21(16):1-23.
Xie A, Odate S, Chandramouly G, Scully R.H2AX post-translational modifications in theionizing radiation response and homologous recom-bination. Cell Cycle. 2010; 9(17):3602-10.
Salzano M, Sanz-García M, Monsalve DM,Moura DS, Lazo PA. VRK1 chromatin kinase phos-phorylates H2AX and is required for foci formationinduced by DNA damage. Epigenetics. 2015;10(5):373-83.
Cook PJ, Ju BG, Telese F, Wang X, Glass CK,Rosenfeld MG. Tyrosine dephosphorylation ofH2AX modulates apoptosis and survival decisions.Nature. 2009; 458(7238):591-6.
Fernández-Capetillo O, Allis CD,Nussenzweig A. Phosphorylation of histone H2B atDNA double-strand breaks. J Exp Med. 2004;199(12):1671-7.
Rossetto D, Truman AW, Kron SJ, Côté J.Epigenetic modifications in double strand breakDNA damage signaling and repair. Clin Cancer Res.2010; 16(18):4543-52.
Tjeertes JV, Miller KM, Jackson SP. Screenfor DNA-damage-responsive histone modificationsidentifies H3K9Ac and H3K56Ac in human cells.EMBO J. 2009; 28(13):1878-89.
Lee JH, Kang BH, Jang H, Kim TW, Choi J,Kwak S, et al. AKT phosphorylates H3-threonine45 to facilitate termination of gene transcription inresponse to DNA damage. Nucleic Acids Res. 2015;43(9):4505-16.
Singh RK, Kabbaj MHM, Paik J, Gunjan A.Histone levels are regulated by phosphorylation andubiquitylation dependent proteolysis. Nat Cell Biol.2009; 11(8):925-33.
Hossain MB, Shifat R, Johnson DG, BedfordMT, Gabrusiewicz KR, Cortes-Santiago N, et al.TIE2-mediated tyrosine phosphorylation of H4regulates DNA damage response by recruitingABL1. Sci Adv. 2016; 2(4):1-11.
Millan-Zambrano G, Santos-Rosa H, PudduF, Robson SC, Jackson SP, Kouzarides T.Phosphorylation of Histone H4T80 triggers DNAdamage checkpoint recovery. Mol Cell. 2018;72(4):625-35.
Gong F, Miller KM. Histone methylation andthe DNA damage response. Mutat Res. 2019;780:37-47.
Taylor-Papadimitriou J, Burchell JM. HistoneMethylases and Demethylases Regulating Antag-onistic Methyl Marks: Changes Occurring inCancer. Cells. 2022; 11(7):1-26.
Wu X nan, Shi T tao, He Y hui, Wang F fei,Sang R, Ding J cheng, et al. Methylation oftranscription factor YY2 regulates its transcriptionalactivity and cell proliferation. Cell Discov. 2017;3:1-22.
Patel DJ. A structural perspective on readoutof epigenetic histone and DNA methylation marks.Cold Spring Harb Perspect Biol. 2016; 8(3):1-47.
Karagianni P, Tzioufas AG. Epigeneticperspectives on systemic autoimmune disease. JAutoinmmunity. 2019; 104:1-10.
Molina-Serrano D, Kyriakou D, Kirmizis A.Histone modifications as an intersection betweendiet and longevity. Front Genet. 2019; 10(192):1-18.
Chen Y, Zhu WG. Biological function andregulation of histone and non-histone lysinemethylation in response to DNA damage. ActaBiochim Biophys Sin. 2016; 48(7):603-16.
Peña PV, Hom RA, Hung T, Lin H, Kuo AJ,Wong RPC, et al. Histone H3K4me3 binding isrequired for the DNA repair and apoptotic activitiesof ING1 tumor suppressor. J Mol Biol. 2008;380(2):303-12.
Williamson EA, Wray JW, Bansal P, HromasR.Overview for the Histone Codes for DNA Repair.Prog Mol Biol Transl Sci. 2012; 110:207-27.
Giannattasio M, Lazzaro F, Plevani P, Muzi-Falconi M. The DNA damage checkpoint responserequires histone H2B ubiquitination by Rad6-Bre1and H3 methylation by Dot1. J Biol Chem. 2005;280:9879-86.
Ma Z, Wang W, Wang S, Zhao X, Ma Y, WuC, et al. Symmetrical dimethylation of H4R3: Abridge linking DNA damage and repair upon oxi-dative stress. Redox Biol. 2020; 37(101653):1-12.
Jacquet K, Fradet-Turcotte A, Avvakumov N,Lambert JP, Roques C, Pandita RK, et al. The TIP60complex regulates bivalent chromatin recognitionby 53BP1 through direct H4K20me binding andH2AK15 acetylation. Mol Cell. 2016; 62(3):409-21.
Botuyan MV, Lee J, Ward IM, Kim JE,Thompson JR, Chen J, et al. Structural basis for themethylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair. Cell. 2006; 127(7):1361-73.
Shan W, Jiang Y, Yu H, Huang Q, Liu L, GuoX, et al. HDAC2 overexpression correlates withaggressive clinicopathological features and DNA-damage response pathway of breast cancer. Am JCancer Res. 2017; 7(5):1213-26.
Li Y, Li Z, Dong L, Tang M, Zhang P, ZhangC, et al. Histone H1 acetylation at lysine 85regulates chromatin condensation and genomestability upon DNA damage. Nucleic Acids Res.2018; 46(15):7716-30.
Li XM, Zhao ZY, Yu X, Xia QD, Zhou P,Wang SG, et al. Exploiting E3 ubiquitin ligases toreeducate the tumor microenvironment for cancertherapy. Exp Hematol Oncol. 2023; 12(1):34.
Rajsbaum R, García-Sastre A. Unanchoredubiquitin in virus uncoating. Science. 2014;346(6208):427-8.
Zhang S, Zhang M, Jing Y, Yin X, Ma P,Zhang Z, et al. Deubiquitinase USP13 dictatesMCL1 stability and sensitivity to BH3 mimeticinhibitors. 2018; 9(1):1-12.
Thorslund T, Ripplinger A, Hoffmann S, WildT, Uckelmann M, Villumsen B, et al. Histone H1couples initiation and amplification of ubiquitinsignalling after DNA damage. Nature. 2015;527(7578):389-93.
Uckelmann M, Sixma TK. Histoneubiquitination in the DNA damage response. DNARepair. 2017; 56:92-101.
Dantuma NP, van Attikum H. Spatiotemporalregulation of posttranslational modifications in theDNA damage response. EMBO J. 2016; 35(1):6-23.
Gatti M, Pinato S, Maiolica A, Rocchio F,Prato MG, Aebersold R, et al. RNF168 promotesnoncanonical K27 ubiquitination to signal DNAdamage. Cell Rep. 2015; 10(2):226-38.
Smeenk G, van Attikum H. The chromatin re-sponse to DNA breaks: Leaving a mark on genomeintegrity. Annu Rev Biochem. 2013; 82:55-80.
Wright DE, Wang CY, Kao CF. Flickin’ theubiquitin switch: The role of H2B ubiquitylation indevelopment. Epigenetics. 2011; 6(10):1165-75.
Palazzo L, Daniels CM, Nettleship JE,Rahman N, McPherson RL, Ong SE, et al. ENPP1processes protein ADP-ribosylation in vitro. FEBSJ.2016; 283(18):3371-88.
Zha JJ, Tang Y, Wang YL. Role of mono‑ADP‑ribosylation histone modification (Review).Exp Ther Med. 2021; 21(6):1-8.
Huang H, Sabari BR, Garcia BA, Allis CD,Zhao Y. SnapShot: Histone modifications. Cell.2014; 159(2):458-458.e1.
Jiang X, Xu Y, Price BD. Acetylation ofH2AX on lysine 36 plays a key role in the DNAdouble-strand break repair pathway. FEBS Lett.2010; 584(13):2926-30.
Clouaire T, Rocher V, Lashgari A, Arnould C,Aguirrebengoa M, Biernacka A, et al. Comprehen-sive mapping of histone modifications at DNA double-strand breaks deciphers repair pathway chro- matin signatures. Mol Cell. 2018; 72(2):250-62.
Browman GD, Poirier MG. Post-translationalmodifications of histones that influence nucleosomedynamics. Chem Rev. 2014; 115(6):2274-95.
Chen CC, Carson JJ, Feser J, Tamburini B,Zabaronick S, Linger J, et al. Acetylated lysine 56on histone H3 drives chromatin assembly afterrepair, signaling for the completion of repair. Cell.2008; 134(2):231-43.