BRCA1 recruitment to transcriptional pause sites is required for R-loop-driven DNA damage repair

Molecular Cell

Volumn 57, Issue 4, 2015, Pages 636-647

  Hatchi, Elodie ^a,b   Skourti Stathaki, Konstantina ^c   Ventz, Steffen ^b,d   Pinello, Luca ^b,d   Yen, Angela ^e,f   Kamieniarz Gdula, Kinga ^c   Dimitrov, Stoil ^a,b   Pathania, Shailja ^a,b   McKinney, Kristine M ^a,b   Eaton, Matthew L ^e,f   Kellis, Manolis ^e,f   Hill, Sarah J ^a,b   Parmigiani, Giovanni ^b,d   Proudfoot, Nicholas J ^c   Livingston, David M ^a,b  

^a HARVARD MEDICAL SCHOOL   (United States)

^b DANA FARBER CANCER INSTITUTE   (United States)

^c UNIVERSITY OF OXFORD   (United Kingdom)

^d HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^e BROAD INSTITUTE OF MIT AND HARVARD   (United States)

^f MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BRCA1 PROTEIN; HISTONE H2AX; PROTEIN DERIVATIVE; SENATAXIN; UNCLASSIFIED DRUG; BRCA1 PROTEIN, HUMAN; RNA HELICASE; SETX PROTEIN, HUMAN;

ARTICLE; BINDING SITE; COMPLEX FORMATION; DNA DAMAGE; DNA REPAIR; GENETIC TRANSCRIPTION; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; PROTEIN BINDING; TRANSCRIPTION TERMINATION; BIOLOGICAL MODEL; GENETICS; HELA CELL LINE; METABOLISM; PHYSIOLOGY;

BRCA1 PROTEIN; DNA DAMAGE; DNA REPAIR; HELA CELLS; HUMANS; MODELS, GENETIC; RNA HELICASES; TRANSCRIPTION TERMINATION, GENETIC; TRANSCRIPTION, GENETIC;

EID: 84923848772     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2015.01.011     Document Type: Article

References (69)

1. Aguilera A. The connection between transcription and genomic instability. EMBO J. 2002, 21:195-201.
2. Aguilera A., García-Muse T. R loops: from transcription byproducts to threats to genome stability. Mol. Cell 2012, 46:115-124.
3. Alexandrov L.B., Nik-Zainal S., Wedge D.C., Aparicio S.A.J.R., Behjati S., Biankin A.V., Bignell G.R., Bolli N., Borg A., Børresen-Dale A.-L., et al. Signatures of mutational processes in human cancer. Nature 2013, 500:415-421. Australian Pancreatic Cancer Genome Initiative, ICGC Breast Cancer ConsortiumICGC Breast Cancer Consortium, ICGC MMML-Seq ConsortiumICGC MMML-Seq Consortium, ICGC PedBrainICGC PedBrain.
4. Alzu A., Bermejo R., Begnis M., Lucca C., Piccini D., Carotenuto W., Saponaro M., Brambati A., Cocito A., Foiani M., Liberi G. Senataxin associates with replication forks to protect fork integrity across RNA-polymerase-II-transcribed genes. Cell 2012, 151:835-846.
5. Anderson S.F., Schlegel B.P., Nakajima T., Wolpin E.S., Parvin J.D. BRCA1 protein is linked to the RNA polymerase II holoenzyme complex via RNA helicase A. Nat. Genet. 1998, 19:254-256.
6. Beale R.C.L., Petersen-Mahrt S.K., Watt I.N., Harris R.S., Rada C., Neuberger M.S. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes: correlation with mutation spectra invivo. J.Mol. Biol. 2004, 337:585-596.
7. Becherel O.J., Yeo A.J., Stellati A., Heng E.Y.H., Luff J., Suraweera A.M., Woods R., Fleming J., Carrie D., McKinney K., et al. Senataxin plays an essential role with DNA damage response proteins in meiotic recombination and gene silencing. PLoS Genet. 2013, 9:e1003435.
8. Bennett C.B., Westmoreland T.J., Verrier C.S., Blanchette C.A.B., Sabin T.L., Phatnani H.P., Mishina Y.V., Huper G., Selim A.L., Madison E.R., et al. Yeast screens identify the RNA polymerase II CTD and SPT5 as relevant targets of BRCA1 interaction. PLoS ONE 2008, 3:e1448.
9. Bhatia V., Barroso S.I., García-Rubio M.L., Tumini E., Herrera-Moyano E., Aguilera A. BRCA2 prevents R-loop accumulation and associates with TREX-2 mRNA export factor PCID2. Nature 2014, 511:362-365.
10. Bochar D.A., Wang L., Beniya H., Kinev A., Xue Y., Lane W.S., Wang W., Kashanchi F., Shiekhattar R. BRCA1 is associated with a human SWI/SNF-related complex: linking chromatin remodeling to breast cancer. Cell 2000, 102:257-265.
11. Boulé J.-B., Zakian V.A. The yeast Pif1p DNA helicase preferentially unwinds RNA DNA substrates. Nucleic Acids Res. 2007, 35:5809-5818.
12. Burns M.B., Lackey L., Carpenter M.A., Rathore A., Land A.M., Leonard B., Refsland E.W., Kotandeniya D., Tretyakova N., Nikas J.B., et al. APOBEC3B is an enzymatic source of mutation in breast cancer. Nature 2013, 494:366-370.
13. Cantor S.B., Bell D.W., Ganesan S., Kass E.M., Drapkin R., Grossman S., Wahrer D.C., Sgroi D.C., Lane W.S., Haber D.A., Livingston D.M. BACH1, a novel helicase-like protein, interacts directly with BRCA1 and contributes to its DNA repair function. Cell 2001, 105:149-160.
14. Cerritelli S.M., Crouch R.J. Ribonuclease H: the enzymes in eukaryotes. FEBS J. 2009, 276:1494-1505.
15. Chan K., Sterling J.F., Roberts S.A., Bhagwat A.S., Resnick M.A., Gordenin D.A. Base damage within single-strand DNA underlies invivo hypermutability induced by a ubiquitous environmental agent. PLoS Genet. 2012, 8:e1003149.
16. Chan Y.A., Hieter P., Stirling P.C. Mechanisms of genome instability induced by RNA-processing defects. Trends Genet. 2014, 30:245-253.
17. Consortium T.E.P. An integrated encyclopedia of DNA elements in the human genome. Nature 2012, 489:57-74. ENCODE Project Consortium.
18. Daniel J.A., Nussenzweig A. The AID-induced DNA damage response in chromatin. Mol. Cell 2013, 50:309-321.
19. Davidson L., Muniz L., West S. 3' end formation of pre-mRNA and phosphorylation of Ser2 on the RNA polymerase II CTD are reciprocally coupled in human cells. Genes Dev. 2014, 28:342-356.
20. Gaillard H., Herrera-Moyano E., Aguilera A. Transcription-associated genome instability. Chem. Rev. 2013, 113:8638-8661.
21. Gallardo M., Luna R., Erdjument-Bromage H., Tempst P., Aguilera A. Nab2p and the Thp1p-Sac3p complex functionally interact at the interface between transcription and mRNA metabolism. J.Biol. Chem. 2003, 278:24225-24232.
22. Gan W., Guan Z., Liu J., Gui T., Shen K., Manley J.L., Li X. R-loop-mediated genomic instability is caused by impairment of replication fork progression. Genes Dev. 2011, 25:2041-2056.
23. Gardini A., Baillat D., Cesaroni M., Shiekhattar R. Genome-wide analysis reveals a role for BRCA1 and PALB2 in transcriptional co-activation. EMBO J. 2014, 33:890-905.
24. Ginno P.A., Lott P.L., Christensen H.C., Korf I., Chédin F. R-loop formation is a distinctive characteristic of unmethylated human CpG island promoters. Mol. Cell 2012, 45:814-825.
25. Gorski J.J., Savage K.I., Mulligan J.M., McDade S.S., Blayney J.K., Ge Z., Harkin D.P. Profiling of the BRCA1 transcriptome through microarray and ChIP-chip analysis. Nucleic Acids Res. 2011, 39:9536-9548.
26. Hamperl S., Cimprich K.A. The contribution of co-transcriptional RNA:DNA hybrid structures to DNA damage and genome instability. DNA Repair (Amst.) 2014, 19:84-94.
27. Helmrich A., Ballarino M., Tora L. Collisions between replication and transcription complexes cause common fragile site instability at the longest human genes. Mol. Cell 2011, 44:966-977.
28. Hill S.J., Rolland T., Adelmant G., Xia X., Owen M.S., Dricot A., Zack T.I., Sahni N., Jacob Y., Hao T., et al. Systematic screening reveals a role for BRCA1 in the response to transcription-associated DNA damage. Genes Dev. 2014, 28:1957-1975.
29. Huen M.S.Y., Sy S.M.H., Chen J. BRCA1 and its toolbox for the maintenance of genome integrity. Nat. Rev. Mol. Cell Biol. 2010, 11:138-148.
30. Huertas P., Aguilera A. Cotranscriptionally formed DNA:RNA hybrids mediate transcription elongation impairment and transcription-associated recombination. Mol. Cell 2003, 12:711-721.
31. Huppert J.L., Bugaut A., Kumari S., Balasubramanian S. G-quadruplexes: the beginning and end of UTRs. Nucleic Acids Res. 2008, 36:6260-6268.
32. Iacovoni J.S., 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.
33. Kawai S., Amano A. BRCA1 regulates microRNA biogenesis via the DROSHA microprocessor complex. J.Cell Biol. 2012, 197:201-208.
34. Kim N., Jinks-Robertson S. Transcription as a source of genome instability. Nat. Rev. Genet. 2012, 13:204-214.
35. Kleiman F.E., Manley J.L. Functional interaction of BRCA1-associated BARD1 with polyadenylation factor CstF-50. Science 1999, 285:1576-1579.
36. Kleiman F.E., Wu-Baer F., Fonseca D., Kaneko S., Baer R., Manley J.L. BRCA1/BARD1 inhibition of mRNA 3' processing involves targeted degradation of RNA polymerase II. Genes Dev. 2005, 19:1227-1237.
37. Li X., Manley J.L. Cotranscriptional processes and their influence on genome stability. Genes Dev. 2006, 20:1838-1847.
38. Mischo H.E., Gómez-González B., Grzechnik P., Rondón A.G., Wei W., Steinmetz L., Aguilera A., Proudfoot N.J. Yeast Sen1 helicase protects the genome from transcription-associated instability. Mol. Cell 2011, 41:21-32.
39. Mullan P.B., Quinn J.E., Harkin D.P. The role of BRCA1 in transcriptional regulation and cell cycle control. Oncogene 2006, 25:5854-5863.
40. Nik-Zainal S., Alexandrov L.B., Wedge D.C., Van Loo P., Greenman C.D., Raine K., Jones D., Hinton J., Marshall J., Stebbings L.A., et al. Mutational processes molding the genomes of 21 breast cancers. Cell 2012, 149:979-993. Breast Cancer Working Group of the International Cancer Genome Consortium.
41. Nik-Zainal S., Wedge D.C., Alexandrov L.B., Petljak M., Butler A.P., Bolli N., Davies H.R., Knappskog S., Martin S., Papaemmanuil E., et al. Association of a germline copy number polymorphism of APOBEC3A and APOBEC3B with burden of putative APOBEC-dependent mutations in breast cancer. Nat. Genet. 2014, 46:487-491.
42. Nojima T., Dienstbier M., Murphy S., Proudfoot N.J., Dye M.J. Definition of RNA polymerase II CoTC terminator elements in the human genome. Cell Rep. 2013, 3:1080-1092.
43. Pathania S., Nguyen J., Hill S.J., Scully R., Adelmant G.O., Marto J.A., Feunteun J., Livingston D.M. BRCA1 is required for postreplication repair after UV-induced DNA damage. Mol. Cell 2011, 44:235-251.
44. Paull T.T., Rogakou E.P., Yamazaki V., Kirchgessner C.U., Gellert M., Bonner W.M. A critical role for histone H2AX in recruitment of repair factors to nuclear foci after DNA damage. Curr. Biol. 2000, 10:886-895.
45. Paull T.T., Cortez D., Bowers B., Elledge S.J., Gellert M. Direct DNA binding by Brca1. Proc. Natl. Acad. Sci. USA 2001, 98:6086-6091.
46. Pleasance E.D., Cheetham R.K., Stephens P.J., McBride D.J., Humphray S.J., Greenman C.D., Varela I., Lin M.-L., Ordóñez G.R., Bignell G.R., et al. A comprehensive catalogue of somatic mutations from a human cancer genome. Nature 2010, 463:191-196.
47. Roberts S.A., Sterling J., Thompson C., Harris S., Mav D., Shah R., Klimczak L.J., Kryukov G.V., Malc E., Mieczkowski P.A., et al. Clustered mutations in yeast and in human cancers can arise from damaged long single-strand DNA regions. Mol. Cell 2012, 46:424-435.
48. Savage K.I., Gorski J.J., Barros E.M., Irwin G.W., Manti L., Powell A.J., Pellagatti A., Lukashchuk N., McCance D.J., McCluggage W.G., et al. Identification of a BRCA1-mRNA splicing complex required for efficient DNA repair and maintenance of genomic stability. Mol. Cell 2014, 54:445-459.
49. Savage K.I., Matchett K.B., Barros E.M., Cooper K.M., Irwin G.W., Gorski J.J., Orr K.S., Vohhodina J., Kavanagh J.N., Madden A.F., et al. BRCA1 deficiency exacerbates estrogen-induced DNA damage and genomic instability. Cancer Res. 2014, 74:2773-2784.
50. Savolainen L., Helleday T. Transcription-associated recombination is independent of XRCC2 and mechanistically separate from homology-directed DNA double-strand break repair. Nucleic Acids Res. 2009, 37:405-412.
51. Scully R., Anderson S.F., Chao D.M., Wei W., Ye L., Young R.A., Livingston D.M., Parvin J.D. BRCA1 is a component of the RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. USA 1997, 94:5605-5610.
52. Silver D.P., Livingston D.M. Mechanisms of BRCA1 tumor suppression. Cancer Discov 2012, 2:679-684.
53. Skourti-Stathaki K., Proudfoot N.J. A double-edged sword: R loops as threats to genome integrity and powerful regulators of gene expression. Genes Dev. 2014, 28:1384-1396.
54. Skourti-Stathaki K., Proudfoot N.J., Gromak N. Human senataxin resolves RNA/DNA hybrids formed at transcriptional pause sites to promote Xrn2-dependent termination. Mol. Cell 2011, 42:794-805.
55. Skourti-Stathaki K., Kamieniarz-Gdula K., Proudfoot N.J. R-loops induce repressive chromatin marks over mammalian gene terminators. Nature 2014, 516:436-439.
56. Steinmetz E.J., Warren C.L., Kuehner J.N., Panbehi B., Ansari A.Z., Brow D.A. Genome-wide distribution of yeast RNA polymerase II and its control by Sen1 helicase. Mol. Cell 2006, 24:735-746.
57. Stirling P.C., Chan Y.A., Minaker S.W., Aristizabal M.J., Barrett I., Sipahimalani P., Kobor M.S., Hieter P. R-loop-mediated genome instability in mRNA cleavage and polyadenylation mutants. Genes Dev. 2012, 26:163-175.
58. Suraweera A., Lim Y., Woods R., Birrell G.W., Nasim T., Becherel O.J., Lavin M.F. Functional role for senataxin, defective in ataxia oculomotor apraxia type 2, in transcriptional regulation. Hum. Mol. Genet. 2009, 18:3384-3396.
59. Tardat M., Brustel J., Kirsh O., Lefevbre C., Callanan M., Sardet C., Julien E. The histone H4 Lys 20 methyltransferase PR-Set7 regulates replication origins in mammalian cells. Nat. Cell Biol. 2010, 12:1086-1093.
60. Thorvaldsdóttir H., Robinson J.T., Mesirov J.P. Integrative Genomics Viewer (IGV): high-performance genomics data visualization and exploration. Brief. Bioinform. 2013, 14:178-192.
61. Tutt A., Ashworth A. The relationship between the roles of BRCA genes in DNA repair and cancer predisposition. Trends Mol. Med. 2002, 8:571-576.
62. Ursic D., Himmel K.L., Gurley K.A., Webb F., Culbertson M.R. The yeast SEN1 gene is required for the processing of diverse RNA classes. Nucleic Acids Res. 1997, 25:4778-4785.
63. Ursic D., Chinchilla K., Finkel J.S., Culbertson M.R. Multiple protein/protein and protein/RNA interactions suggest roles for yeast DNA/RNA helicase Sen1p in transcription, transcription-coupled DNA repair and RNA processing. Nucleic Acids Res. 2004, 32:2441-2452.
64. Venkitaraman A.R. Cancer suppression by the chromosome custodians, BRCA1 and BRCA2. Science 2014, 343:1470-1475.
65. White E., Kamieniarz-Gdula K., Dye M.J., Proudfoot N.J. AT-rich sequence elements promote nascent transcript cleavage leading to RNA polymerase II termination. Nucleic Acids Res. 2013, 41:1797-1806.
66. Wimberly H., Shee C., Thornton P.C., Sivaramakrishnan P., Rosenberg S.M., Hastings P.J. R-loops and nicks initiate DNA breakage and genome instability in non-growing Escherichia coli. Nat. Commun. 2013, 4:2115.
67. Yarden R.I., Brody L.C. BRCA1 interacts with components of the histone deacetylase complex. Proc. Natl. Acad. Sci. USA 1999, 96:4983-4988.
68. Yüce Ö., West S.C. Senataxin, defective in the neurodegenerative disorder ataxia with oculomotor apraxia 2, lies at the interface of transcription and the DNA damage response. Mol. Cell. Biol. 2013, 33:406-417.
69. Zhu Q., Pao G.M., Huynh A.M., Suh H., Tonnu N., Nederlof P.M., Gage F.H., Verma I.M. BRCA1 tumour suppression occurs via heterochromatin-mediated silencing. Nature 2011, 477:179-184.