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Molecular and Cellular Biology

Recruitment of RBM6 to DNA Double-Strand Breaks Fosters Homologous Recombination Repair

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Pages 130-142 | Received 13 Jun 2022, Accepted 01 Feb 2023, Published online: 20 Mar 2023

REFERENCES

  • Jackson SP, Bartek J. The DNA-damage response in human biology and disease. Nature. 2009;461:1071–1078. doi:10.1038/nature08467.
  • Blackford AN, Jackson SP. ATM, ATR, and DNA-PK: the Trinity at the heart of the DNA damage response. Mol Cell. 2017;66:801–817. doi:10.1016/j.molcel.2017.05.015.
  • Lord CJ, Ashworth A. PARP inhibitors: synthetic lethality in the clinic. Science. 2017;355:1152–1158. doi:10.1126/science.aam7344.
  • Tubbs A, Nussenzweig A. Endogenous DNA damage as a source of genomic instability in cancer. Cell. 2017;168:644–656.
  • Machour FE, Ayoub N. Transcriptional regulation at DSBs: mechanisms and consequences. Trends Genet. 2020;36:981–997. doi:10.1016/j.tig.2020.01.001.
  • Kulkarni A, Wilson DM. 3rd. The involvement of DNA-damage and -repair defects in neurological dysfunction. Am J Hum Genet. 2008;82:539–566. doi:10.1016/j.ajhg.2008.01.009.
  • Morio T. Recent advances in the study of immunodeficiency and DNA damage response. Int J Hematol. 2017;106:357–365. doi:10.1007/s12185-017-2263-8.
  • Alt FW, Schwer B. DNA double-strand breaks as drivers of neural genomic change, function, and disease. DNA Repair. 2018;71:158–163. doi:10.1016/j.dnarep.2018.08.019.
  • Bednarski JJ, Sleckman BP. At the intersection of DNA damage and immune responses. Nat Rev Immunol. 2019;19:231–242. doi:10.1038/s41577-019-0135-6.
  • Shrivastav M, De Haro LP, Nickoloff JA. Regulation of DNA double-strand break repair pathway choice. Cell Res. 2008;18:134–147. doi:10.1038/cr.2007.111.
  • Jasin M, Rothstein R. Repair of strand breaks by homologous recombination. Cold Spring Harb Perspect Biol. 2013;5:a012740. doi:10.1101/cshperspect.a012740.
  • Clouaire T, Legube G. DNA double strand break repair pathway choice: a chromatin based decision? Nucleus. 2015;6:107–113. doi:10.1080/19491034.2015.1010946.
  • Sfeir A, Symington LS. Microhomology-mediated end joining: a back-up survival mechanism or dedicated pathway? Trends Biochem Sci. 2015;40:701–714. doi:10.1016/j.tibs.2015.08.006.
  • Bhargava R, Onyango DO, Stark JM. Regulation of single-strand annealing and its role in genome maintenance. Trends Genet. 2016;32:566–575. doi:10.1016/j.tig.2016.06.007.
  • Ceccaldi R, Rondinelli B, D’Andrea AD. Repair pathway choices and consequences at the double-strand break. Trends Cell Biol. 2016;26:52–64. doi:10.1016/j.tcb.2015.07.009.
  • Hustedt N, Durocher D. The control of DNA repair by the cell cycle. Nat Cell Biol. 2016;19:1–9. doi:10.1038/ncb3452.
  • Scully R, Panday A, Elango R, Willis NA. DNA double-strand break repair-pathway choice in somatic mammalian cells. Nat Rev Mol Cell Biol. 2019;20:698–714. doi:10.1038/s41580-019-0152-0.
  • Aleksandrov R, Hristova R, Stoynov S, Gospodinov A. The chromatin response to double-strand DNA breaks and their repair. Cells. 2020;9:1853. doi:10.3390/cells9081853.
  • Li S, Kuhne WW, Kulharya A, Hudson FZ, Ha K, Cao Z, Dynan WS. Involvement of p54(nrb), a PSF partner protein, in DNA double-strand break repair and radioresistance. Nucleic Acids Res. 2009;37:6746–6753. doi:10.1093/nar/gkp741.
  • Paulsen RD, Soni DV, Wollman R, Hahn AT, Yee MC, Guan A, Hesley JA, Miller SC, Cromwell EF, Solow-Cordero DE, et al. A genome-wide siRNA screen reveals diverse cellular processes and pathways that mediate genome stability. Mol Cell. 2009;35:228–239. doi:10.1016/j.molcel.2009.06.021.
  • Salton M, Lerenthal Y, Wang SY, Chen DJ, Shiloh Y. Involvement of Matrin 3 and SFPQ/NONO in the DNA damage response. Cell Cycle. 2010;9:1568–1576. doi:10.4161/cc.9.8.11298.
  • Adamson B, Smogorzewska A, Sigoillot FD, King RW, Elledge SJ. A genome-wide homologous recombination screen identifies the RNA-binding protein RBMX as a component of the DNA-damage response. Nat Cell Biol. 2012;14:318–328. doi:10.1038/ncb2426.
  • Mastrocola AS, Kim SH, Trinh AT, Rodenkirch LA, Tibbetts RS. The RNA-binding protein fused in sarcoma (FUS) functions downstream of poly(ADP-ribose) polymerase (PARP) in response to DNA damage. J Biol Chem. 2013;288:24731–24741.
  • Montecucco A, Biamonti G. Pre-mRNA processing factors meet the DNA damage response. Front Genet. 2013;4:102.
  • Khoury-Haddad H, Guttmann-Raviv N, Ipenberg I, Huggins D, Jeyasekharan AD, Ayoub N. PARP1-dependent recruitment of KDM4D histone demethylase to DNA damage sites promotes double-strand break repair. Proc Natl Acad Sci USA. 2014;111:E728–E737.
  • Zoabi M, Nadar-Ponniah PT, Khoury-Haddad H, Usaj M, Budowski-Tal I, Haran T, Henn A, Mandel-Gutfreund Y, Ayoub N. RNA-dependent chromatin localization of KDM4D lysine demethylase promotes H3K9me3 demethylation [Research Support, Non-U.S. Gov’t]. Nucleic Acids Res. 2014;42:13026–13038. doi:10.1093/nar/gku1021.
  • Khoury-Haddad H, Nadar-Ponniah PT, Awwad S, Ayoub N. The emerging role of lysine demethylases in DNA damage response: dissecting the recruitment mode of KDM4D/JMJD2D to DNA damage sites [Research Support, Non-U.S. Gov’t]. Cell Cycle. 2015;14:950–958. doi:10.1080/15384101.2015.1014147.
  • Naro C, Bielli P, Pagliarini V, Sette C. The interplay between DNA damage response and RNA processing: the unexpected role of splicing factors as gatekeepers of genome stability. Front Genet. 2015;6:142.
  • Giono LE, Nieto Moreno N, Cambindo Botto AE, Dujardin G, Munoz MJ, Kornblihtt AR. The RNA response to DNA damage. J Mol Biol. 2016;428:2636–2651.
  • Kai M. Roles of RNA-binding proteins in DNA damage response. Int J Mol Sci. 2016;17:310. doi:10.3390/ijms17030310.
  • Abu-Zhayia ER, Khoury-Haddad H, Guttmann-Raviv N, Serruya R, Jarrous N, Ayoub N. A role of human Rnase P subunits, Rpp29 and Rpp21, in homology directed-repair of double-strand breaks. Sci Rep. 2017;7:1002. doi:10.1038/s41598-017-01185-6.
  • Hawley BR, Lu WT, Wilczynska A, Bushell M. The emerging role of RNAs in DNA damage repair. Cell Death Differ. 2017;24:580–587. doi:10.1038/cdd.2017.16.
  • Kochan JA, Desclos ECB, Bosch R, Meister L, Vriend LEM, van Attikum H, Krawczyk PM. Meta-analysis of DNA double-strand break response kinetics. Nucleic Acids Res. 2017;45:12625–12637. doi:10.1093/nar/gkx1128.
  • Marchesini M, Ogoti Y, Fiorini E, Aktas Samur A, Nezi L, D’Anca M, Storti P, Samur MK, Ganan-Gomez I, Fulciniti MT, et al. ILF2 is a regulator of RNA splicing and DNA damage response in 1q21-amplified multiple myeloma. Cancer Cell. 2017;32:88–100 e106. doi:10.1016/j.ccell.2017.05.011.
  • Milek M, Imami K, Mukherjee N, Bortoli F, Zinnall U, Hazapis O, Trahan C, Oeffinger M, Heyd F, Ohler U, et al. DDX54 regulates transcriptome dynamics during DNA damage response. Genome Res. 2017;27:1344–1359. doi:10.1101/gr.218438.116.
  • Nishida K, Kuwano Y, Nishikawa T, Masuda K, Rokutan K. RNA binding proteins and genome integrity. Int J Mol Sci. 2017;18:1341. doi:10.3390/ijms18071341.
  • Abu-Zhayia ER, Awwad SW, Ben-Oz BM, Khoury-Haddad H, Ayoub N. CDYL1 fosters double-strand break-induced transcription silencing and promotes homology-directed repair. J Mol Cell Biol. 2018;10:341–357. doi:10.1093/jmcb/mjx050.
  • Bishara LA, Machour FE, Awwad SW, Ayoub N. NELF complex fosters BRCA1 and RAD51 recruitment to DNA damage sites and modulates sensitivity to PARP inhibition. DNA Repair. 2021;97:103025. doi:10.1016/j.dnarep.2020.103025.
  • Awwad SW, Abu-Zhayia ER, Guttmann-Raviv N, Ayoub N. NELF-E is recruited to DNA double-strand break sites to promote transcriptional repression and repair. EMBO Rep. 2017;18:745–764. doi:10.15252/embr.201643191.
  • Jang Y, Elsayed Z, Eki R, He S, Du KP, Abbas T, Kai M. Intrinsically disordered protein RBM14 plays a role in generation of RNA:DNA hybrids at double-strand break sites. Proc Natl Acad Sci USA. 2020;117:5329–5338. doi:10.1073/pnas.1913280117.
  • Gardiner M, Toth R, Vandermoere F, Morrice NA, Rouse J. Identification and characterization of FUS/TLS as a new target of ATM. Biochem J. 2008;415:297–307.
  • Levone BR, Lenzken SC, Antonaci M, Maiser A, Rapp A, Conte F, Reber S, Mechtersheimer J, Ronchi AE, Muhlemann O, et al. FUS-dependent liquid-liquid phase separation is important for DNA repair initiation. J Cell Biol. 2021;220:e202008030.
  • Krietsch J, Caron MC, Gagne JP, Ethier C, Vignard J, Vincent M, Rouleau M, Hendzel MJ, Poirier GG, Masson JY. PARP activation regulates the RNA-binding protein NONO in the DNA damage response to DNA double-strand breaks. Nucleic Acids Res. 2012;40:10287–10301. doi:10.1093/nar/gks798.
  • Bechara EG, Sebestyen E, Bernardis I, Eyras E, Valcarcel J. RBM5, 6, and 10 differentially regulate NUMB alternative splicing to control cancer cell proliferation. Mol Cell. 2013;52:720–733. doi:10.1016/j.molcel.2013.11.010.
  • Machour FE, Abu-Zhayia ER, Awwad SW, Bidany-Mizrahi T, Meinke S, Bishara LA, Heyd F, Aqeilan RI, Ayoub N. RBM6 splicing factor promotes homologous recombination repair of double-strand breaks and modulates sensitivity to chemotherapeutic drugs. Nucleic Acids Res. 2021;49:11708–11727. doi:10.1093/nar/gkab976.
  • Dinant C, de Jager M, Essers J, van Cappellen WA, Kanaar R, Houtsmuller AB, Vermeulen W. Activation of multiple DNA repair pathways by sub-nuclear damage induction methods. J Cell Sci. 2007;120:2731–2740. doi:10.1242/jcs.004523.
  • Iacovoni JS, Caron P, Lassadi I, Nicolas E, Massip L, Trouche D, Legube G. High-resolution profiling of gammaH2AX around DNA double strand breaks in the mammalian genome. embo J. 2010;29:1446–1457. doi:10.1038/emboj.2010.38.
  • Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, et al. ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science. 2007;316:1160–1166. doi:10.1126/science.1140321.
  • Bennetzen MV, Larsen DH, Bunkenborg J, Bartek J, Lukas J, Andersen JS. Site-specific phosphorylation dynamics of the nuclear proteome during the DNA damage response. Mol Cell Proteomics. 2010;9:1314–1323. doi:10.1074/mcp.M900616-MCP200.
  • Elia AE, Boardman AP, Wang DC, Huttlin EL, Everley RA, Dephoure N, Zhou C, Koren I, Gygi SP, Elledge SJ. Quantitative proteomic atlas of ubiquitination and acetylation in the DNA damage response. Mol Cell. 2015;59:867–881. doi:10.1016/j.molcel.2015.05.006.
  • Schlam-Babayov S, Bensimon A, Harel M, Geiger T, Aebersold R, Ziv Y, Shiloh Y. Phosphoproteomics reveals novel modes of function and inter-relationships among PIKKs in response to genotoxic stress. embo J. 2021;40:e104400.
  • Sousa FG, Matuo R, Soares DG, Escargueil AE, Henriques JA, Larsen AK, Saffi J. PARPs and the DNA damage response. Carcinogenesis. 2012;33:1433–1440. doi:10.1093/carcin/bgs132.
  • Tallis M, Morra R, Barkauskaite E, Ahel I. Poly(ADP-ribosyl)ation in regulation of chromatin structure and the DNA damage response. Chromosoma. 2014;123:79–90. doi:10.1007/s00412-013-0442-9.
  • Khadka P, Hsu JK, Veith S, Tadokoro T, Shamanna RA, Mangerich A, Croteau DL, Bohr VA. Differential and concordant roles for Poly(ADP-Ribose) Polymerase 1 and Poly(ADP-Ribose) in regulating WRN and RECQL5 activities. Mol Cell Biol. 2015;35:3974–3989. doi:10.1128/MCB.00427-15.
  • Spegg V, Altmeyer M. Biomolecular condensates at sites of DNA damage: more than just a phase. DNA Repair. 2021;106:103179. doi:10.1016/j.dnarep.2021.103179.
  • Pinder J, Salsman J, Dellaire G. Nuclear domain ‘knock-in’ screen for the evaluation and identification of small molecule enhancers of CRISPR-based genome editing. Nucleic Acids Res. 2015;43:9379–9392. doi:10.1093/nar/gkv993.
  • Abu-Zhayia ER, Bishara LA, Machour FE, Barisaac AS, Ben-Oz BM, Ayoub N. CDYL1-dependent decrease in lysine crotonylation at DNA double-strand break sites functionally uncouples transcriptional silencing and repair. Mol Cell. 2022;82:1940–1955 e1947. doi:10.1016/j.molcel.2022.03.031.
  • Smith R, Sellou H, Chapuis C, Huet S, Timinszky G. CHD3 and CHD4 recruitment and chromatin remodeling activity at DNA breaks is promoted by early poly(ADP-ribose)-dependent chromatin relaxation. Nucleic Acids Res. 2018;46:6087–6098. doi:10.1093/nar/gky334.
  • Aravind L, Walker DR, Koonin EV. Conserved domains in DNA repair proteins and evolution of repair systems. Nucleic Acids Res. 1999;27:1223–1242. doi:10.1093/nar/27.5.1223.
  • Robert-Paganin J, Rety S, Leulliot N. Regulation of DEAH/RHA helicases by G-patch proteins. Biomed Res Int. 2015;2015:931857. doi:10.1155/2015/931857.
  • Patel A, Lee HO, Jawerth L, Maharana S, Jahnel M, Hein MY, Stoynov S, Mahamid J, Saha S, Franzmann TM, et al. A liquid-to-solid phase transition of the ALS protein FUS accelerated by disease mutation. Cell. 2015;162:1066–1077. doi:10.1016/j.cell.2015.07.047.
  • Klaric JA, Wust S, Panier S. New faces of old friends: emerging new roles of RNA-binding proteins in the DNA double-strand break response. Front Mol Biosci. 2021;8:668821. doi:10.3389/fmolb.2021.668821.

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