OGT Mediated Histone H2B S112 GlcNAcylation Regulates DNA Damage Response

Panfei Wang^{a, b, d, #},
Changmin Peng^{a, b, d, #},
Xia Liu^{c, d, #},
Hailong Liu^b,
Yali Chen^b,
Li Zheng^d,
Baolin Han^{c
, ,},
Huadong Pei^{a, b
, ,}

a.
Key Laboratory of Industrial Fermentation Microbiology, Ministry of Education, Tianjin Industrial Microbiology Key Lab, College of Biotechnology, Tianjin University of Science and Technology, Tianjin 300457, China
b.
State Key Laboratory of Proteomics, Beijing Proteome Research Center, Beijing Institute of Radiation Medicine, Beijing 100850, China
c.
Department of Radiotherapy, Tianjin Baodi Hospital, Baodi Clinical College of Tianjin Medical University, Tianjin 301800, China
d.
School of Nursing and Medical Technology, Jianghan University, Wuhan 430056, China

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Corresponding author: E-mail address: tjhanbaolin@163.com (Baolin Han); E-mail address: peihuadong@hotmail.com (Huadong Pei)

These authors contributed equally to this work.

摘要

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Abstract: O-GlcNAcylation is an important post-translational modification and has been implicated in many fundamental cellular processes. Recent studies showed that O-linked N-acetylglucosamine (GlcNAc) transferase (OGT) mediated O-GlcNAcylation of histone H2B Ser 112 (H2B S112 GlcNAcylation) plays an important role in gene transcription. However, the role of this histone modification in DNA damage response has not been studied yet. In this study, we found that OGT and OGT mediated H2B S112 GlcNAcylation are involved in DNA damage response for maintaining genomic stability and are required for resistance to many DNA-damaging and replication stress-inducing agents. OGT mediated H2B S112 GlcNAcylation increased locally upon the induction of double-strand breaks (DSBs), and depletion of OGT or overexpression of H2B S112A mutant impaired homologous recombination (HR) and nonhomologous end-joining (NHEJ). Mechanistically, H2B S112 GlcNAcylation could bind Nijmegen breakage syndrome 1 (NBS1) and regulate NBS1 foci formation. Taken together, our results demonstrate a new function of histone O-GlcNAcylation in DNA damage response (DDR).
- OGT /
- H2B S112 GlcNAcylation /
- DNA damage response /
- NBS1
These authors contributed equally to this work.
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参考文献(46)

[1]	Al-Hakim, A., Escribano-Diaz, C., Landry, M.C. et al. The ubiquitous role of ubiquitin in the DNA damage response DNA Repair (Amst), 9 (2010),pp. 1229-1240
[2]	Celeste, A., Petersen, S., Romanienko, P.J. et al. Genomic instability in mice lacking histone H2AX Science, 296 (2002),pp. 922-927
[3]	Chapman, J.R., Jackson, S.P. Phospho-dependent interactions between NBS1 and MDC1 mediate chromatin retention of the MRN complex at sites of DNA damage EMBO Rep., 9 (2008),pp. 795-801
[4]	Chen, Q., Chen, Y., Bian, C. et al. TET2 promotes histone O-GlcNAcylation during gene transcription Nature, 493 (2013),pp. 561-564
[5]	Cotney, J., Leng, J., Yin, J. et al. The evolution of lineage-specific regulatory activities in the human embryonic limb Cell, 154 (2013),pp. 185-196
[6]	Desai-Mehta, A., Cerosaletti, K.M., Concannon, P. Distinct functional domains of nibrin mediate Mre11 binding, focus formation, and nuclear localization Mol. Cell. Biol., 21 (2001),pp. 2184-2191
[7]	Difilippantonio, S., Nussenzweig, A. The NBS1-ATM connection revisited Cell Cycle, 6 (2007),pp. 2366-2370
[8]	Falck, J., Coates, J., Jackson, S.P. Conserved modes of recruitment of ATM, ATR and DNA-PKcs to sites of DNA damage Nature, 434 (2005),pp. 605-611
[9]	Fattah, F., Lee, E.H., Weisensel, N. et al. Ku regulates the non-homologous end joining pathway choice of DNA double-strand break repair in human somatic cells PLoS Genet., 6 (2010),p. e1000855
[10]	Faucher, D., Wellinger, R.J. Methylated H3K4, a transcription-associated histone modification, is involved in the DNA damage response pathway PLoS Genet., 6 (2010),p. e1001082
[11]	FitzGerald, J.E., Grenon, M., Lowndes, N.F. 53BP1: function and mechanisms of focal recruitment Biochem. Soc. Trans., 37 (2009),pp. 897-904
[12]	Fnu, S., Williamson, E.A., De Haro, L.P. et al. Methylation of histone H3 lysine 36 enhances DNA repair by nonhomologous end-joining Proc. Natl. Acad. Sci. USA, 108 (2011),pp. 540-545
[13]	Fuchs, G., Shema, E., Vesterman, R. et al. RNF20 and USP44 regulate stem cell differentiation by modulating H2B monoubiquitylation Mol. Cell, 46 (2012),pp. 662-673
[14]	Fujiki, R., Hashiba, W., Sekine, H. et al. GlcNAcylation of histone H2B facilitates its monoubiquitination Nature, 480 (2011),pp. 557-560
[15]	Ginjala, V., Nacerddine, K., Kulkarni, A. et al. BMI1 is recruited to DNA breaks and contributes to DNA damage-induced H2A ubiquitination and repair Mol. Cell. Biol., 31 (2011),pp. 1972-1982
[16]	Goodarzi, A.A., Jeggo, P.A. The repair and signaling responses to DNA double-strand breaks Adv. Genet., 82 (2013),pp. 1-45
[17]	Greer, E.L., Shi, Y. Histone methylation: a dynamic mark in health, disease and inheritance Nat. Rev. Genet., 13 (2012),pp. 343-357
[18]	Harper, J.W., Elledge, S.J. The DNA damage response: ten years after Mol. Cell, 28 (2007),pp. 739-745
[19]	Hart, G.W., Housley, M.P., Slawson, C. Cycling of O-linked beta-N-acetylglucosamine on nucleocytoplasmic proteins Nature, 446 (2007),pp. 1017-1022
[20]	Hu, R., Wang, E., Peng, G. et al. Zinc finger protein 668 interacts with Tip60 to promote H2AX acetylation after DNA damage Cell Cycle, 12 (2013),pp. 2033-2041
[21]	Huen, M.S., Grant, R., Manke, I. et al. Cell, 131 (2007),pp. 901-914
[22]	Ikura, T., Tashiro, S., Kakino, A. et al. DNA damage-dependent acetylation and ubiquitination of H2AX enhances chromatin dynamics Mol. Cell. Biol., 27 (2007),pp. 7028-7040
[23]	Jackson, S.P., Bartek, J. The DNA-damage response in human biology and disease Nature, 461 (2009),pp. 1071-1078
[24]	Kartikasari, A.E., Zhou, J.X., Kanji, M.S. et al. The histone demethylase Jmjd3 sequentially associates with the transcription factors Tbx3 and Eomes to drive endoderm differentiation EMBO J., 32 (2013),pp. 1393-1408
[25]	Keum, Y.S., Kim, H.G., Bode, A.M. et al. UVB-induced COX-2 expression requires histone H3 phosphorylation at Ser10 and Ser28 Oncogene, 32 (2013),pp. 444-452
[26]	Kolas, N.K., Chapman, J.R., Nakada, S. et al. Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase Science, 318 (2007),pp. 1637-1640
[27]	Kusch, T., Florens, L., Macdonald, W.H. et al. Acetylation by Tip60 is required for selective histone variant exchange at DNA lesions Science, 306 (2004),pp. 2084-2087
[28]	Love, D.C., Hanover, J.A. The hexosamine signaling pathway: deciphering the “O-GlcNAc code” Sci. STKE, 2005 (2005)
[29]	Lukas, C., Melander, F., Stucki, M. et al. Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention EMBO J., 23 (2004),pp. 2674-2683
[30]	Mailand, N., Bekker-Jensen, S., Faustrup, H. et al. RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins Cell, 131 (2007),pp. 887-900
[31]	Mallette, F.A., Mattiroli, F., Cui, G. et al. RNF8- and RNF168-dependent degradation of KDM4A/JMJD2A triggers 53BP1 recruitment to DNA damage sites EMBO J., 31 (2012),pp. 1865-1878
[32]	Marteijn, J.A., Bekker-Jensen, S., Mailand, N. et al. Nucleotide excision repair-induced H2A ubiquitination is dependent on MDC1 and RNF8 and reveals a universal DNA damage response J. Cell Biol., 186 (2009),pp. 835-847
[33]	Melander, F., Bekker-Jensen, S., Falck, J. et al. Phosphorylation of SDT repeats in the MDC1 N terminus triggers retention of NBS1 at the DNA damage-modified chromatin J. Cell Biol., 181 (2008),pp. 213-226
[34]	Rogakou, E.P., Pilch, D.R., Orr, A.H. et al. DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139 J. Biol. Chem., 273 (1998),pp. 5858-5868
[35]	Rothbart, S.B., Dickson, B.M., Ong, M.S. et al. Multivalent histone engagement by the linked tandem Tudor and PHD domains of UHRF1 is required for the epigenetic inheritance of DNA methylation Genes Dev., 27 (2013),pp. 1288-1298
[36]	Sakabe, K., Wang, Z., Hart, G.W. Beta-N-acetylglucosamine (O-GlcNAc) is part of the histone code Proc. Natl. Acad. Sci. USA, 107 (2010),pp. 19915-19920
[37]	Shrivastav, M., De Haro, L.P., Nickoloff, J.A. Regulation of DNA double-strand break repair pathway choice Cell Res., 18 (2008),pp. 134-147
[38]	Spycher, C., Miller, E.S., Townsend, K. et al. Constitutive phosphorylation of MDC1 physically links the MRE11-RAD50-NBS1 complex to damaged chromatin J. Cell Biol., 181 (2008),pp. 227-240
[39]	Wang, Z., Gucek, M., Hart, G.W. Cross-talk between GlcNAcylation and phosphorylation: site-specific phosphorylation dynamics in response to globally elevated O-GlcNAc Proc. Natl. Acad. Sci. USA, 105 (2008),pp. 13793-13798
[40]	Wyman, C., Kanaar, R. DNA double-strand break repair: all's well that ends well Annu. Rev. Genet., 40 (2006),pp. 363-383
[41]	Xu, Q., Yang, C., Du, Y. et al. AMPK regulates histone H2B O-GlcNAcylation Nucleic Acids Res., 42 (2014),pp. 5594-5604
[42]	Yang, W., Xia, Y., Hawke, D. et al. PKM2 phosphorylates histone H3 and promotes gene transcription and tumorigenesis Cell, 150 (2012),pp. 685-696
[43]	You, Z., Chahwan, C., Bailis, J. et al. ATM activation and its recruitment to damaged DNA require binding to the C terminus of Nbs1 Mol. Cell. Biol., 25 (2005),pp. 5363-5379
[44]	Zhang, F., Yu, X. WAC, a functional partner of RNF20/40, regulates histone H2B ubiquitination and gene transcription Mol. Cell, 41 (2011),pp. 384-397
[45]	Zhang, Z., Jones, A., Joo, H.Y. et al. USP49 deubiquitinates histone H2B and regulates cotranscriptional pre-mRNA splicing Genes Dev., 27 (2013),pp. 1581-1595
[46]	Zhong, J., Martinez, M., Sengupta, S. et al. Quantitative phosphoproteomics reveals crosstalk between phosphorylation and O-GlcNAc in the DNA damage response pathway Proteomics, 15 (2015),pp. 591-607