95
Views
15
CrossRef citations to date
0
Altmetric
Research Article

MOF Suppresses Replication Stress and Contributes to Resolution of Stalled Replication Forks

, , , , , , , , & ORCID Icon show all
Article: e00484-17 | Received 12 Sep 2017, Accepted 05 Dec 2017, Published online: 03 Mar 2023

REFERENCES

  • Mazouzi A, Velimezi G, Loizou JI. 2014. DNA replication stress: causes, resolution and disease. Exp Cell Res 329:85–93. https://doi.org/10.1016/j.yexcr.2014.09.030.
  • Zeman MK, Cimprich KA. 2014. Causes and consequences of replication stress. Nat Cell Biol 16:2–9. https://doi.org/10.1038/ncb2897.
  • Halazonetis TD, Gorgoulis VG, Bartek J. 2008. An oncogene-induced DNA damage model for cancer development. Science 319:1352–1355. https://doi.org/10.1126/science.1140735.
  • Groth A, Rocha W, Verreault A, Almouzni G. 2007. Chromatin challenges during DNA replication and repair. Cell 128:721–733. https://doi.org/10.1016/j.cell.2007.01.030.
  • Khurana S, Oberdoerffer P. 2015. Replication stress: a lifetime of epigenetic change. Genes (Basel) 6:858–877. https://doi.org/10.3390/genes6030858.
  • Alabert C, Groth A. 2012. Chromatin replication and epigenome maintenance. Nat Rev Mol Cell Biol 13:153–167. https://doi.org/10.1038/nrm3288.
  • Blow JJ, Ge XQ, Jackson DA. 2011. How dormant origins promote complete genome replication. Trends Biochem Sci 36:405–414. https://doi.org/10.1016/j.tibs.2011.05.002.
  • Branzei D, Foiani M. 2007. Interplay of replication checkpoints and repair proteins at stalled replication forks. DNA Repair (Amst) 6:994–1003. https://doi.org/10.1016/j.dnarep.2007.02.018.
  • Hunt CR, Ramnarain D, Horikoshi N, Iyengar P, Pandita RK, Shay JW, Pandita TK. 2013. Histone modifications and DNA double-strand break repair after exposure to ionizing radiations. Radiat Res 179:383–392. https://doi.org/10.1667/RR3308.2.
  • Papamichos-Chronakis M, Peterson CL. 2008. The Ino80 chromatin-remodeling enzyme regulates replisome function and stability. Nat Struct Mol Biol 15:338–345. https://doi.org/10.1038/nsmb.1413.
  • Rowbotham SP, Barki L, Neves-Costa A, Santos F, Dean W, Hawkes N, Choudhary P, Will WR, Webster J, Oxley D, Green CM, Varga-Weisz P, Mermoud JE. 2011. Maintenance of silent chromatin through replication requires SWI/SNF-like chromatin remodeler SMARCAD1. Mol Cell 42:285–296. https://doi.org/10.1016/j.molcel.2011.02.036.
  • Shimada K, Oma Y, Schleker T, Kugou K, Ohta K, Harata M, Gasser SM. 2008. Ino80 chromatin remodeling complex promotes recovery of stalled replication forks. Curr Biol 18:566–575. https://doi.org/10.1016/j.cub.2008.03.049.
  • Leung KH, Abou El Hassan M, Bremner R. 2013. A rapid and efficient method to purify proteins at replication forks under native conditions. Biotechniques 55:204–206. https://doi.org/10.2144/000114089.
  • Driscoll R, Hudson A, Jackson SP. 2007. Yeast Rtt109 promotes genome stability by acetylating histone H3 on lysine 56. Science 315:649–652. https://doi.org/10.1126/science.1135862.
  • Clemente-Ruiz M, Gonzalez-Prieto R, Prado F. 2011. Histone H3K56 acetylation, CAF1, and Rtt106 coordinate nucleosome assembly and stability of advancing replication forks. PLoS Genet 7:e1002376. https://doi.org/10.1371/journal.pgen.1002376.
  • Myung K, Pennaneach V, Kats ES, Kolodner RD. 2003. Saccharomyces cerevisiae chromatin-assembly factors that act during DNA replication function in the maintenance of genome stability. Proc Natl Acad Sci U S A 100:6640–6645. https://doi.org/10.1073/pnas.1232239100.
  • Krishnan V, Chow MZ, Wang Z, Zhang L, Liu B, Liu X, Zhou Z. 2011. Histone H4 lysine 16 hypoacetylation is associated with defective DNA repair and premature senescence in Zmpste24-deficient mice. Proc Natl Acad Sci U S A 108:12325–12330. https://doi.org/10.1073/pnas.1102789108.
  • Sharma GG, So S, Gupta A, Kumar R, Cayrou C, Avvakumov N, Bhadra U, Pandita RK, Porteus MH, Chen DJ, Cote J, Pandita TK. 2010. MOF and histone H4 acetylation at lysine 16 are critical for DNA damage response and double-strand break repair. Mol Cell Biol 30:3582–3595. https://doi.org/10.1128/MCB.01476-09.
  • Shogren-Knaak M, Ishii H, Sun JM, Pazin MJ, Davie JR, Peterson CL. 2006. Histone H4-K16 acetylation controls chromatin structure and protein interactions. Science 311:844–847. https://doi.org/10.1126/science.1124000.
  • Oppikofer M, Kueng S, Martino F, Soeroes S, Hancock SM, Chin JW, Fischle W, Gasser SM. 2011. A dual role of H4K16 acetylation in the establishment of yeast silent chromatin. EMBO J 30:2610–2621. https://doi.org/10.1038/emboj.2011.170.
  • Zhang R, Erler J, Langowski J. 2017. Histone acetylation regulates chromatin accessibility: role of H4K16 in inter-nucleosome interaction. Biophys J 112:450–459. https://doi.org/10.1016/j.bpj.2016.11.015.
  • Fraga MF, Ballestar E, Villar-Garea A, Boix-Chornet M, Espada J, Schotta G, Bonaldi T, Haydon C, Ropero S, Petrie K, Iyer NG, Perez-Rosado A, Calvo E, Lopez JA, Cano A, Calasanz MJ, Colomer D, Piris MA, Ahn N, Imhof A, Caldas C, Jenuwein T, Esteller M. 2005. Loss of acetylation at Lys16 and trimethylation at Lys20 of histone H4 is a common hallmark of human cancer. Nat Genet 37:391–400. https://doi.org/10.1038/ng1531.
  • Gupta A, Guerin-Peyrou TG, Sharma GG, Park C, Agarwal M, Ganju RK, Pandita S, Choi K, Sukumar S, Pandita RK, Ludwig T, Pandita TK. 2008. The mammalian ortholog of Drosophila MOF that acetylates histone H4 lysine 16 is essential for embryogenesis and oncogenesis. Mol Cell Biol 28:397–409. https://doi.org/10.1128/MCB.01045-07.
  • Gupta A, Hunt CR, Pandita RK, Pae J, Komal K, Singh M, Shay JW, Kumar R, Ariizumi K, Horikoshi N, Hittelman WN, Guha C, Ludwig T, Pandita TK. 2013. T-cell-specific deletion of Mof blocks their differentiation and results in genomic instability in mice. Mutagenesis 28:263–270. https://doi.org/10.1093/mutage/ges080.
  • Gupta A, Hunt CR, Hegde ML, Chakraborty S, Udayakumar D, Horikoshi N, Singh M, Ramnarain DB, Hittelman WN, Namjoshi S, Asaithamby A, Hazra TK, Ludwig T, Pandita RK, Tyler JK, Pandita TK. 2014. MOF phosphorylation by ATM regulates 53BP1-mediated double-strand break repair pathway choice. Cell Rep 8:177–189. https://doi.org/10.1016/j.celrep.2014.05.044.
  • Bhadra MP, Horikoshi N, Pushpavallipvalli SN, Sarkar A, Bag I, Krishnan A, Lucchesi JC, Kumar R, Yang Q, Pandita RK, Singh M, Bhadra U, Eissenberg JC, Pandita TK. 2012. The role of MOF in the ionizing radiation response is conserved in Drosophila melanogaster. Chromosoma 121:79–90. https://doi.org/10.1007/s00412-011-0344-7.
  • Horikoshi N, Kumar P, Sharma GG, Chen M, Hunt CR, Westover K, Chowdhury S, Pandita TK. 2013. Genome-wide distribution of histone H4 Lysine 16 acetylation sites and their relationship to gene expression. Genome Integr 4:3. https://doi.org/10.1186/2041-9414-4-3.
  • Pandita TK. 2013. Histone H4 lysine 16 acetylated isoform synthesis opens new route to biophysical studies. Proteomics 13:1546–1547. https://doi.org/10.1002/pmic.201300145.
  • Gupta A, Sharma GG, Young CS, Agarwal M, Smith ER, Paull TT, Lucchesi JC, Khanna KK, Ludwig T, Pandita TK. 2005. Involvement of human MOF in ATM function. Mol Cell Biol 25:5292–5305. https://doi.org/10.1128/MCB.25.12.5292-5305.2005.
  • Kumar R, Hunt CR, Gupta A, Nannepaga S, Pandita RK, Shay JW, Bachoo R, Ludwig T, Burns DK, Pandita TK. 2011. Purkinje cell-specific males absent on the first (mMof) gene deletion results in an ataxia-telangiectasia-like neurological phenotype and backward walking in mice. Proc Natl Acad Sci U S A 108:3636–3641. https://doi.org/10.1073/pnas.1016524108.
  • Valerio DG, Xu H, Chen CW, Hoshii T, Eisold ME, Delaney C, Cusan M, Deshpande AJ, Huang CH, Lujambio A, Zheng YG, Zuber J, Pandita TK, Lowe SW, Armstrong SA. 2017. Histone acetyltransferase activity of MOF is required for MLL-AF9 leukemogenesis. Cancer Res 77:1753–1762. https://doi.org/10.1158/0008-5472.CAN-16-2374.
  • Thomas T, Dixon MP, Kueh AJ, Voss AK. 2008. Mof (MYST1 or KAT8) is essential for progression of embryonic development past the blastocyst stage and required for normal chromatin architecture. Mol Cell Biol 28:5093–5105. https://doi.org/10.1128/MCB.02202-07.
  • Li X, Li L, Pandey R, Byun JS, Gardner K, Qin Z, Dou Y. 2012. The histone acetyltransferase MOF is a key regulator of the embryonic stem cell core transcriptional network. Cell Stem Cell 11:163–178. https://doi.org/10.1016/j.stem.2012.04.023.
  • Pandita RK, Sharma GG, Laszlo A, Hopkins KM, Davey S, Chakhparonian M, Gupta A, Wellinger RJ, Zhang J, Powell SN, Roti Roti JL, Lieberman HB, Pandita TK. 2006. Mammalian Rad9 plays a role in telomere stability, S- and G2-phase-specific cell survival, and homologous recombinational repair. Mol Cell Biol 26:1850–1864. https://doi.org/10.1128/MCB.26.5.1850-1864.2006.
  • Roy D, Zhang Z, Lu Z, Hsieh CL, Lieber MR. 2010. Competition between the RNA transcript and the nontemplate DNA strand during R-loop formation in vitro: a nick can serve as a strong R-loop initiation site. Mol Cell Biol 30:146–159. https://doi.org/10.1128/MCB.00897-09.
  • Aguilera A, Garcia-Muse T. 2012. R loops: from transcription byproducts to threats to genome stability. Mol Cell 46:115–124. https://doi.org/10.1016/j.molcel.2012.04.009.
  • Taipale M, Akhtar A. 2005. Chromatin mechanisms in Drosophila dosage compensation. Prog Mol Subcell Biol 38:123–149. https://doi.org/10.1007/3-540-27310-7_5.
  • Zhou Y, Paull TT. 2015. Direct measurement of single-stranded DNA intermediates in mammalian cells by quantitative polymerase chain reaction. Anal Biochem 479:48–50. https://doi.org/10.1016/j.ab.2015.03.025.
  • Moldovan GL, Pfander B, Jentsch S. 2007. PCNA, the maestro of the replication fork. Cell 129:665–679. https://doi.org/10.1016/j.cell.2007.05.003.
  • Mailand N, Gibbs-Seymour I, Bekker-Jensen S. 2013. Regulation of PCNA-protein interactions for genome stability. Nat Rev Mol Cell Biol 14:269–282. https://doi.org/10.1038/nrm3562.
  • Byun TS, Pacek M, Yee MC, Walter JC, Cimprich KA. 2005. Functional uncoupling of MCM helicase and DNA polymerase activities activates the ATR-dependent checkpoint. Genes Dev 19:1040–1052. https://doi.org/10.1101/gad.1301205.
  • Zou L, Elledge SJ. 2003. Sensing DNA damage through ATRIP recognition of RPA-ssDNA complexes. Science 300:1542–1548. https://doi.org/10.1126/science.1083430.
  • Lee J, Dunphy WG. 2013. The Mre11-Rad50-Nbs1 (MRN) complex has a specific role in the activation of Chk1 in response to stalled replication forks. Mol Biol Cell 24:1343–1353. https://doi.org/10.1091/mbc.E13-01-0025.
  • Tang J, Cho NW, Cui G, Manion EM, Shanbhag NM, Botuyan MV, Mer G, Greenberg RA. 2013. Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 20:317–325. https://doi.org/10.1038/nsmb.2499.
  • Taipale M, Rea S, Richter K, Vilar A, Lichter P, Imhof A, Akhtar A. 2005. hMOF histone acetyltransferase is required for histone H4 lysine 16 acetylation in mammalian cells. Mol Cell Biol 25:6798–6810. https://doi.org/10.1128/MCB.25.15.6798-6810.2005.
  • Helmrich A, Ballarino M, Tora L. 2011. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol Cell 44:966–977. https://doi.org/10.1016/j.molcel.2011.10.013.
  • Suka N, Luo K, Grunstein M. 2002. Sir2p and Sas2p opposingly regulate acetylation of yeast histone H4 lysine16 and spreading of heterochromatin. Nat Genet 32:378–383. https://doi.org/10.1038/ng1017.
  • Akhtar A, Becker PB. 2000. Activation of transcription through histone H4 acetylation by MOF, an acetyltransferase essential for dosage compensation in Drosophila. Mol Cell 5:367–375. https://doi.org/10.1016/S1097-2765(00)80431-1.
  • Fullgrabe J, Lynch-Day MA, Heldring N, Li W, Struijk RB, Ma Q, Hermanson O, Rosenfeld MG, Klionsky DJ, Joseph B. 2013. The histone H4 lysine 16 acetyltransferase hMOF regulates the outcome of autophagy. Nature 500:468–471. https://doi.org/10.1038/nature12313.
  • Sheikh BN, Bechtel-Walz W, Lucci J, Karpiuk O, Hild I, Hartleben B, Vornweg J, Helmstädter M, Sahyoun AH, Bhardwaj V, Stehle T, Diehl S, Kretz O, Voss AK, Thomas T, Manke T, Huber TB, Akhtar A. 2016. MOF maintains transcriptional programs regulating cellular stress response. Oncogene 35:2698–2710. https://doi.org/10.1038/onc.2015.335.
  • Boubakri H, de Septenville AL, Viguera E, Michel B. 2010. The helicases DinG, Rep and UvrD cooperate to promote replication across transcription units in vivo. EMBO J 29:145–157. https://doi.org/10.1038/emboj.2009.308.
  • Gan W, Guan Z, Liu J, Gui T, Shen K, Manley JL, Li X. 2011. R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev 25:2041–2056. https://doi.org/10.1101/gad.17010011.
  • Tuduri S, Crabbe L, Conti C, Tourriere H, Holtgreve-Grez H, Jauch A, Pantesco V, De Vos J, Thomas A, Theillet C, Pommier Y, Tazi J, Coquelle A, Pasero P. 2009. Topoisomerase I suppresses genomic instability by preventing interference between replication and transcription. Nat Cell Biol 11:1315–1324. https://doi.org/10.1038/ncb1984.
  • Drolet M, Phoenix P, Menzel R, Masse E, Liu LF, Crouch RJ. 1995. Overexpression of RNase H partially complements the growth defect of an Escherichia coli delta topA mutant: R-loop formation is a major problem in the absence of DNA topoisomerase I. Proc Natl Acad Sci U S A 92:3526–3530. https://doi.org/10.1073/pnas.92.8.3526.
  • Rondon AG, Jimeno S, Garcia-Rubio M, Aguilera A. 2003. Molecular evidence that the eukaryotic THO/TREX complex is required for efficient transcription elongation. J Biol Chem 278:39037–39043. https://doi.org/10.1074/jbc.M305718200.
  • Singh M, Hunt CR, Pandita RK, Kumar R, Yang CR, Horikoshi N, Bachoo R, Serag S, Story MD, Shay JW, Powell SN, Gupta A, Jeffery J, Pandita S, Chen BP, Deckbar D, Lobrich M, Yang Q, Khanna KK, Worman HJ, Pandita TK. 2013. Lamin a/c depletion enhances DNA damage-induced stalled replication fork arrest. Mol Cell Biol 33:1210–1222. https://doi.org/10.1128/MCB.01676-12.
  • Li X, Corsa CA, Pan PW, Wu L, Ferguson D, Yu X, Min J, Dou Y. 2010. MOF and H4 K16 acetylation play important roles in DNA damage repair by modulating recruitment of DNA damage repair protein Mdc1. Mol Cell Biol 30:5335–5347. https://doi.org/10.1128/MCB.00350-10.
  • Barbour L, Xiao W. 2003. Regulation of alternative replication bypass pathways at stalled replication forks and its effects on genome stability: a yeast model. Mutat Res 532:137–155. https://doi.org/10.1016/j.mrfmmm.2003.08.014.
  • Hoege C, Pfander B, Moldovan GL, Pyrowolakis G, Jentsch S. 2002. RAD6-dependent DNA repair is linked to modification of PCNA by ubiquitin and SUMO. Nature 419:135–141. https://doi.org/10.1038/nature00991.
  • Nam EA, Cortez D. 2011. ATR signalling: more than meeting at the fork. Biochem J 436:527–536. https://doi.org/10.1042/BJ20102162.
  • MacDougall CA, Byun TS, Van C, Yee MC, Cimprich KA. 2007. The structural determinants of checkpoint activation. Genes Dev 21:898–903. https://doi.org/10.1101/gad.1522607.
  • Mattoo AR, Pandita RK, Chakraborty S, Charaka V, Mujoo K, Hunt CR, Pandita TK. 2017. MCL-1 depletion impairs DNA double-strand break repair and reinitiation of stalled DNA replication forks. Mol Cell Biol 37:e00535-16. https://doi.org/10.1128/MCB.00535-16.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.