본문 바로가기
KERD
논문KCI 등재

Transcriptional regulation and chromatin dynamics at DNA double-strand breaks

2

조회

0

다운로드

0

인용

0

참고문헌

주제분류생화학

초록

In eukaryotic cells, DNA damage can occur at any time and at any chromatin locus, including loci at which active transcription is taking place. DNA double-strand breaks affect chromatin integrity and elicit a DNA damage response to facilitate repair of the DNA lesion. Actively transcribed genes near DNA lesions are transiently suppressed by crosstalk between DNA damage response factors and polycomb repressive complexes. Epigenetic modulation of the chromatin environment also contributes to efficient DNA damage response signaling and transcriptional repression. On the other hand, RNA transcripts produced in the G1 phase, as well as the active chromatin context of the lesion, appear to drive homologous recombination repair. Here, we discuss how the ISWI family of chromatin remodeling factors coordinates the DNA damage response and transcriptional repression, especially in transcriptionally active regions, highlighting the direct modulation of the epigenetic environment.

Abstract

In eukaryotic cells, DNA damage can occur at any time and at any chromatin locus, including loci at which active transcription is taking place. DNA double-strand breaks affect chromatin integrity and elicit a DNA damage response to facilitate repair of the DNA lesion. Actively transcribed genes near DNA lesions are transiently suppressed by crosstalk between DNA damage response factors and polycomb repressive complexes. Epigenetic modulation of the chromatin environment also contributes to efficient DNA damage response signaling and transcriptional repression. On the other hand, RNA transcripts produced in the G1 phase, as well as the active chromatin context of the lesion, appear to drive homologous recombination repair. Here, we discuss how the ISWI family of chromatin remodeling factors coordinates the DNA damage response and transcriptional repression, especially in transcriptionally active regions, highlighting the direct modulation of the epigenetic environment.

참고문헌 (84)

  1. Capozzo, I., "Express or repress? The transcriptional dilemma of damaged chromatin", FEBS J, 284, pp.2133~2147 (2017)
  2. Clouaire, T., "A Snapshot on the Cis Chromatin Response to DNA Double-Strand Breaks", Trends Genet, 35, pp.330~345 (2019)
  3. Marnef, A., "Transcription-Coupled DNA Double-Strand Break Repair : Active Genes Need Special Care", J. Mol. Biol, 429, pp.1277~1288 (2017)
  4. Clapier, C. R., "The biology of chromatin remodeling complexes", Annu. Rev. Biochem, 78, pp.273~304 (2009)
  5. Jackson, S. P., "The DNA-damage response in human biology and disease", Nature, 461, pp.1071~1078 (2009)
  6. Rogakou, E. P., "DNA doublestranded breaks induce histone H2AX phosphorylation on serine 139", J. Biol. Chem, 273, pp.5858~5868 (1998)
  7. Stucki, M., "MDC1 directly binds phosphorylated histone H2AX to regulate cellular responses to DNA double-strand breaks", Cell, 123, pp.1213~1226 (2005)
  8. Lukas, C., "Mdc1 couples DNA double-strand break recognition by Nbs1 with its H2AX-dependent chromatin retention", EMBO J, 23, pp.2674~2683 (2004)
  9. Lou, Z., "MDC1 maintains genomic stability by participating in the amplification of ATM-dependent DNA damage signals", Mol. Cell, 21, pp.187~200 (2006)
  10. Rogakou, E. P., "Megabase chromatin domains involved in DNA double-strand breaks in vivo", J. Cell Biol, 146, pp.905~916 (1999)
  11. Thorslund, T., "Histone H1 couples initiation and amplification of ubiquitin signalling after DNA damage", Nature, 527, pp.389~393 (2015)
  12. Doil, C., "RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins", Cell, 136, pp.435~446 (2009)
  13. Stewart, G. S., "The RIDDLE syndrome protein mediates a ubiquitindependent signaling cascade at sites of DNA damage", Cell, 136, pp.420~434 (2009)
  14. Fradet-Turcotte, A., "53BP1 is a reader of the DNA-damage-induced H2A Lys 15 ubiquitin mark", Nature, 499, pp.50~54 (2013)
  15. Acs, K., "The AAA-ATPase VCP", p97 promotes 53BP1 recruitment by removing L3MBTL1 from DNA double-strand breaks, 2011, pp.18, 1345~1350
  16. Sobhian, B., "RAP80 targets BRCA1 to specific ubiquitin structures at DNA damage sites", Science, 316, pp.1198~1202 (2007)
  17. Kim, H., "Ubiquitin-binding protein RAP80 mediates BRCA1-dependent DNA damage response", Science, 316, pp.1202~1205 (2007)
  18. Wang, B., "Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response", Science, 316, pp.1194~1198 (2007)
  19. Escribano-Diaz, C., "A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice", Mol. Cell, 49, pp.872~883 (2013)
  20. Chapman, J. R., "RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection", Mol. Cell, 49, pp.858~871 (2013)
  21. Di Virgilio, M., "Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching", Science, 339, pp.711~715 (2013)
  22. Zimmermann, M., "53BP1regulates DSB repair using Rif1 to control 5’ end resection", Science, 339, pp.700~704 (2013)
  23. Bunting, S. F., "53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks", Cell, 141, pp.243~254 (2010)
  24. Bouwman, P., "53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers", Nat. Struct. Mol. Biol, 17, pp.688~695 (2010)
  25. Chen, L., "Cell cycle-dependent complex formation of BRCA1.CtIP.MRN is important for DNA double-strand break repair", J. Biol. Chem, 283, pp.7713~7720 (2008)
  26. Lafranchi, L., "APC", C(Cdh1)controls CtIP stability during the cell cycle and in response to DNA damage, 2014, pp.33, 2860~2879
  27. Clouaire, T., "DNA double strand break repair pathway choice: a chromatin based decision?", Nucl. (Calcutta), 6, pp.107~113 (2015)
  28. Nakamura, K., "H4K20me0 recognition by BRCA1-BARD1 directs homologous recombination to sister chromatids", Nat. Cell Biol, 21, pp.311~318 (2019)
  29. Wu, W., "Interaction of BARD1 and HP1 Is Required for BRCA1 Retention at Sites of DNA Damage", Cancer Res, 75, pp.1311~1321 (2015)
  30. Shanbhag, N. M., "ATM-dependent chromatin changes silence transcription in cis to DNA double-strand breaks", Cell, 141, pp.970~981 (2010)
  31. Uckelmann, M., "Histone ubiquitination in the DNA damage response", DNA Repair(Amst. ), 56, pp.92~101 (2017)
  32. Tamburri, S., "Histone H2AK119 Mono-Ubiquitination Is Essential for Polycomb-Mediated Transcriptional Repression", Mol. Cell, 77, pp.840~856 (2020)
  33. Schuettengruber, B., "Genome Regulation by Polycomb and Trithorax : 70 Years and Counting", Cell, 171, pp.34~57 (2017)
  34. Wang, H., "Role of histone H2A ubiquitination in Polycomb silencing", Nature, 431, pp.873~878 (2004)
  35. Ui, A., "Transcriptional elongation factor ENL phosphorylated by ATM recruits polycomb and switches offtranscription for DSB repair", Mol. Cell, 58, pp.468~482 (2015)
  36. Cook, P. J., "Tyrosine dephosphorylation of H2AX modulates apoptosis and survival decisions", Nature, 458, pp.591~596 (2009)
  37. Ji, J. H., "De novo phosphorylation of H2AX by WSTF regulates transcriptioncoupled homologous recombination repair", Nucleic Acids Res, 47, pp.6299~6314 (2019)
  38. Sanchez, A., "BMI1-UBR5 axis regulates transcriptional repression at damaged chromatin", Proc. Natl Acad. Sci. USA, 113, pp.11243~11248 (2016)
  39. de Vivo, A., "The OTUD5-UBR5 complex regulates FACT-mediated transcription at damaged chromatin", Nucleic Acids Res, 47, pp.729~746 (2019)
  40. Kakarougkas, A., "Requirement for PBAF in transcriptional repression and repair at DNA breaks in actively transcribed regions of chromatin", Mol. Cell, 55, pp.723~732 (2014)
  41. Hu, K., "ATM-Dependent Recruitment of BRD7 is required for Transcriptional Repression and DNA Repair at DNA Breaks Flanking Transcriptional Active Regions", Adv. Sci. (Weinh. ), 7, pp.2000157~ (2020)
  42. Gagne, J. P., "Proteome-wide identification of poly(ADP-ribose) binding proteins and poly(ADP-ribose)-associated protein complexes", Nucleic Acids Res, 36, pp.6959~6976 (2008)
  43. Jungmichel, S., "Proteome-wide identification of poly(ADP-Ribosyl)ation targets in different genotoxic stress responses", Mol. Cell, 52, pp.272~285 (2013)
  44. Ahel, D., "Poly(ADP-ribose)-dependent regulation of DNA repair by the chromatin remodeling enzyme ALC1", Science, 325, pp.1240~1243 (2009)
  45. Haince, J. F., "PARP1-dependent kinetics of recruitment of MRE11 and NBS1proteins to multiple DNA damage sites", J. Biol. Chem, 283, pp.1197~1208 (2008)
  46. Smeenk, G., "Poly(ADP-ribosyl)ation links the chromatin remodeler SMARCA5", SNF2H to RNF168-dependent DNA damage signaling, 2013, pp.126, 889~903
  47. Chou, D. M., "A chromatin localization screen reveals poly (ADP ribose)-regulated recruitment of the repressive polycomb and NuRD complexes to sites of DNA damage", Proc. Natl Acad. Sci. USA, 107, pp.18475~18480 (2010)
  48. Rona, G., "PARP1-dependent recruitment of the FBXL10-RNF68-RNF2 ubiquitin ligase to sites of DNA damage controls H2A", Z loading. Elife, 7, pp.e38771~ (2018)
  49. Gong, F., "Screen identifies bromodomain protein ZMYND8 in chromatin recognition of transcription-associated DNA damage that promotes homologous recombination", Genes Dev, 29, pp.197~211 (2015)
  50. Gong, F., "Histone demethylase KDM5A regulates the ZMYND8-NuRD chromatin remodeler to promote DNA repair", J. Cell Biol, 216, pp.1959~1974 (2017)
  51. Awwad, S. W., "NELF-E is recruited to DNA double-strand break sites to promote transcriptional repression and repair", EMBO Rep, 18, pp.745~764 (2017)
  52. Dong, C., "Screen identifies DYRK1B network as mediator of transcription repression on damaged chromatin", Proc. Natl Acad. Sci. U. S. A, 117, pp.17019~17030 (2020)
  53. Abu-Zhayia, E. R., "CDYL1 fosters double-strand break-induced transcription silencing and promotes homology-directed repair", J. Mol. Cell. Biol, 10, pp.341~357 (2018)
  54. Pankotai, T., "DNAPKcs-dependent arrest of RNA polymerase II transcription in the presence of DNA breaks", Nat. Struct. Mol. Biol, 19, pp.276~282 (2012)
  55. Caron, P., "WWP2 ubiquitylates RNA polymerase II for DNA-PK-dependent transcription arrest and repair at DNA breaks", Genes Dev, 33, pp.684~704 (2019)
  56. Steurer, B., "DNA damage-induced transcription stress triggers the genomewide degradation of promoter-bound Pol II", Nat. Commun, 13, pp.3624~ (2022)
  57. Iannelli, F., "A damaged genome’s transcriptional landscape through multilayered expression profiling around in situ-mapped DNA double-strand breaks", Nat. Commun, 8, pp.15656~ (2017)
  58. Pessina, F., "Functional transcription promoters at DNA double-strand breaks mediate RNA-driven phase separation of damage-response factors", Nat. Cell Biol, 21, pp.1286~1299 (2019)
  59. Marteijn, J. A., "Understanding nucleotide excision repair and its roles in cancer and ageing", Nat. Rev. Mol. Cell Biol, 15, pp.465~481 (2014)
  60. Chaurasia, P., "Preferential repair of DNA double-strand break at the active gene in vivo", J. Biol. Chem, 287, pp.36414~36422 (2012)
  61. Wei, L., "DNA damage during the G0", G1 phase triggers RNA-templated, Cockayne syndrome B-dependent homologous recombination, 2015, pp.112, E3495~E3504
  62. Teng, Y., "ROS-induced R loops trigger a transcription-coupled but BRCA1", 2-independent homologous recombination pathway through CSB, 2018, pp.9, 4115~
  63. Yasuhara, T., "Human Rad52 Promotes XPG-Mediated R-loop Processing to Initiate Transcription-Associated Homologous Recombination Repair", Cell, 175, pp.558~570.e511 (2018)
  64. Cohen, S., "A POLD3", BLM dependent pathway handles DSBs in transcribed chromatin upon excessive RNA : DNA hybrid accumulation, 2022, pp.13, 2012~
  65. Aymard, F., "Transcriptionally active chromatin recruits homologous recombination at DNA double-strand breaks", Nat. Struct. Mol. Biol, 21, pp.366~374 (2014)
  66. Clouaire, T., "Comprehensive Mapping of Histone Modifications at DNA Double-Strand Breaks Deciphers Repair Pathway Chromatin Signatures", Mol. Cell, 72, pp.250~262.e256 (2018)
  67. Aymard, F., "Genome-wide mapping of long-range contacts unveils clustering of DNA double-strand breaks at damaged active genes", Nat. Struct. Mol. Biol, 24, pp.353~361 (2017)
  68. Clapier, C. R., "Mechanisms of action and regulation of ATP-dependent chromatin-remodelling complexes", Nat. Rev. Mol. Cell Biol, 18, pp.407~422 (2017)
  69. Lans, H., "ATP-dependent chromatin remodeling in the DNA-damage response", Epigenetics Chromatin, 5, pp.4~ (2012)
  70. Price, B. D., "Chromatin remodeling at DNA double-strand breaks", Cell, 152, pp.1344~1354 (2013)
  71. Meisenberg, C., "Repression of Transcription at DNA Breaks Requires Cohesin throughout Interphase and Prevents Genome Instability", Mol. Cell, 73, pp.212~223 (2019)
  72. Lai, A. Y., "Cancer biology and NuRD : a multifaceted chromatin remodelling complex", Nat. Rev. Cancer, 11, pp.588~596 (2011)
  73. Min, S., "The chromatin remodeler RSF1 coordinates epigenetic marks for transcriptional repression and DSB repair", Nucleic Acids Res, 49, pp.12268~12283 (2021)
  74. Min, S., "ATM-dependent chromatin remodeler Rsf-1 facilitates DNA damage checkpoints and homologous recombination repair", Cell Cycle, 13, pp.666~677 (2014)
  75. Pessina, F., "The RSF1 histone-remodelling factor facilitates DNA double-strand break repair by recruiting centromeric and Fanconi Anaemia proteins", PLoS Biol, 12, pp.e1001856~ (2014)
  76. Helfricht, A., "Remodeling and spacing factor 1(RSF1)deposits centromere proteins at DNA double-strand breaks to promote non-homologous end-joining", Cell Cycle, 12, pp.3070~3082 (2013)
  77. Helfricht, A., "Remodeling and spacing factor 1(RSF1) : a rising star in DNA repair", Epigenomics, 6, pp.261~265 (2014)
  78. Lee, H. S., "Spatiotemporal coordination of the RSF1-PLK1-Aurora B cascade establishes mitotic signaling platforms", Nat. Commun, 12, pp.5931~ (2021)
  79. Lee, H. S., "The chromatin remodeler RSF1 controls centromeric histone modifications to coordinate chromosome segregation", Nat. Commun, 9, pp.3848~ (2018)
  80. Lee, H. S., "The chromatin remodeller RSF1 is essential for PLK1 deposition and function at mitotic kinetochores", Nat. Commun, 6, pp.7904~ (2015)
  81. Min, S., "Chromatin-remodeling factor, RSF1, controls p53-mediated transcription in apoptosis upon DNA strand breaks", Cell Death Dis, 9, pp.1079~ (2018)
  82. Marnef, A., "R-loops as Janus-faced modulators of DNA repair", Nat. Cell Biol, 23, pp.305~313 (2021)
  83. Xu, Y., "Histone H2A.Z controls a critical chromatin remodeling step required for DNA double-strand break repair", Mol. Cell, 48, pp.723~733 (2012)
  84. Xu, Y., "The p400 ATPase regulates nucleosome stability and chromatin ubiquitination during DNA repair", J. Cell Biol, 191, pp.31~43 (2010)

관련 논문AI추천

이 간행물의 다른 논문 (191건)