SETD2 is required for DNA double-strand break repair and activation of the p53-mediated checkpoint

eLife

Volumn 2014, Issue 3, 2014, Pages

  Carvalho, Sílvia ^a   Vítor, Alexandra C ^a   Sridhara, Sreerama Chaitanya ^a   Filipa, B Martins ^a   Ana, C Raposo ^a   Desterro, Joana M P ^a   Ferreira, João ^a   de Almeida, Sérgio Fernandes ^a  

^a UNIVERSITY OF LISBON   (Portugal)

Author keywords

[No Author keywords available]

Indexed keywords

HISTONE H2AX; HISTONE H3; HISTONE METHYLTRANSFERASE; PROTEIN P53; SETD2; UNCLASSIFIED DRUG; ATM PROTEIN; HISTONE LYSINE METHYLTRANSFERASE; PROTEIN BINDING; RAD51 PROTEIN; REPLICATION FACTOR A; SET2 PROTEIN, HUMAN; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN;

ARTICLE; CANCER CELL; CELL CYCLE; CELL SURVIVAL; CONTROLLED STUDY; DNA DAMAGE; DNA DAMAGE CHECKPOINT; DNA END JOINING REPAIR; DNA REPAIR; DOUBLE STRANDED DNA BREAK; FLOW CYTOMETRY; GENE EXPRESSION SYSTEM; GENE MUTATION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; KIDNEY CARCINOMA; RECOMBINATION REPAIR; REPORTER GENE; RNA INTERFERENCE; WESTERN BLOTTING; CELL CYCLE CHECKPOINT; GENETIC RECOMBINATION; GENETICS; KIDNEY TUMOR; METABOLISM; MUTATION; PATHOLOGY; SIGNAL TRANSDUCTION; TUMOR CELL LINE;

ATAXIA TELANGIECTASIA MUTATED PROTEINS; CARCINOMA, RENAL CELL; CELL CYCLE CHECKPOINTS; CELL LINE, TUMOR; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; HISTONE-LYSINE N-METHYLTRANSFERASE; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KIDNEY NEOPLASMS; MUTATION; PROTEIN BINDING; RAD51 RECOMBINASE; RECOMBINATION, GENETIC; RECOMBINATIONAL DNA REPAIR; REPLICATION PROTEIN A; SIGNAL TRANSDUCTION; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84899849011     PISSN: None     EISSN: 2050084X     Source Type: Journal    
DOI: 10.7554/eLife.02482     Document Type: Article

References (54)

1. Anantha RW, Vassin VM, Borowiec JA (2007) Sequential and synergistic modification of human RPA stimulates chromosomal DNA repair. J Biol Chem 282: 35910-35923
2. Banin S, Moyal L, Shieh S, Taya Y, Anderson CW, Chessa L, Smorodinsky NI, Prives C, Reiss Y, Shiloh Y, Ziv Y (1998) Enhanced phosphorylation of p53 by ATM in response to DNA damage. Science 281: 1674-1677
3. Bohm L, Briand G, Sautiere P, Crane-Robinson C (1981) Proteolytic digestion studies of chromatin core-histone structure. Identification of the limit peptides of histones H3 and H4. European journal of biochemistry / FEBS 119: 67-74
4. Bouwman P, Aly A, Escandell JM, Pieterse M, Bartkova J, van der Gulden H, Hiddingh S, Thanasoula M, Kulkarni A, Yang Q, Haffty BG, Tommiska J, Blomqvist C, Drapkin R, Adams DJ, Nevanlinna H, Bartek J, Tarsounas M, Ganesan S, Jonkers J (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 17: 688-695
5. Bunting SF, Callen E, Wong N, Chen HT, Polato F, Gunn A, Bothmer A, Feldhahn N, Fernandez-Capetillo O, Cao L, Xu X, Deng CX, Finkel T, Nussenzweig M, Stark JM, Nussenzweig A (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141: 243-254
6. Burden DA, Kingma PS, Froelich-Ammon SJ, Bjornsti MA, Patchan MW, Thompson RB, Osheroff N (1996) Topoisomerase II. etoposide interactions direct the formation of drug-induced enzyme-DNA cleavage complexes. J Biol Chem 271: 29238-29244
7. Cancer Genome Atlas Research N (2013) Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 499: 43-49
8. Canman CE, Lim DS, Cimprich KA, Taya Y, Tamai K, Sakaguchi K, Appella E, Kastan MB, Siliciano JD (1998) Activation of the ATM kinase by ionizing radiation and phosphorylation of p53. Science 281: 1677-1679
9. Carvalho S, Raposo AC, Martins FB, Grosso AR, Sridhara SC, Rino J, Carmo-Fonseca M, de Almeida SF (2013) Histone methyltransferase SETD2 coordinates FACT recruitment with nucleosome dynamics during transcription. Nucleic Acids Res 41: 2881-2893
10. Chapman JR, Taylor MR, Boulton SJ (2012) Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 47: 497-510
11. Dalgliesh GL, Furge K, Greenman C, Chen L, Bignell G, Butler A, Davies H, Edkins S, Hardy C, Latimer C, Teague J, Andrews J, Barthorpe S, Beare D, Buck G, Campbell PJ, Forbes S, Jia M, Jones D, Knott H, Kok CY, Lau KW, Leroy C, Lin ML, McBride DJ, Maddison M, Maguire S, McLay K, Menzies A, Mironenko T, Mulderrig L, Mudie L, O'Meara S, Pleasance E, Rajasingham A, Shepherd R, Smith R, Stebbings L, Stephens P, Tang G, Tarpey PS, Turrell K, Dykema KJ, Khoo SK, Petillo D, Wondergem B, Anema J, Kahnoski RJ, Teh BT, Stratton MR, Futreal PA (2010) Systematic sequencing of renal carcinoma reveals inactivation of histone modifying genes. Nature 463: 360-363
12. Daugaard M, Baude A, Fugger K, Povlsen LK, Beck H, Sørensen CS, Petersen NH, Sorensen PH, Lukas C, Bartek J, Lukas J, Rohde M, Jäättelä M (2012) LEDGF (p75) promotes DNA-end resection and homologous recombination. Nat Struct Mol Biol 19:803-10
13. de Almeida SF, Carmo-Fonseca M (2014) Reciprocal regulatory links between cotranscriptional splicing and chromatin. Semin Cell Dev Biol pii: S1084-9521(14)00038-X. doi: 10.1016/j.semcdb.2014.03.010. epub ahead of print
14. de Almeida SF, Garcia-Sacristan A, Custodio N, Carmo-Fonseca M (2010) A link between nuclear RNA surveillance, the human exosome and RNA polymerase II transcriptional termination. Nucleic acids research 38: 8015-8026
15. Duns G, van den Berg E, van Duivenbode I, Osinga J, Hollema H, Hofstra RM, Kok K (2010) Histone methyltransferase gene SETD2 is a novel tumor suppressor gene in clear cell renal cell carcinoma. Cancer Res 70: 4287-4291
16. Edmunds JW, Mahadevan LC, Clayton AL (2008) Dynamic histone H3 methylation during gene induction: HYPB/Setd2 mediates all H3K36 trimethylation. EMBO J 27: 406-420
17. Elbashir SM, Harborth J, Lendeckel W, Yalcin A, Weber K, Tuschl T (2001) Duplexes of 21-nucleotide RNAs mediate RNA interference in cultured mammalian cells. Nature 411: 494-498
18. Fontebasso AM, Schwartzentruber J, Khuong-Quang DA, Liu XY, Sturm D, Korshunov A, Jones DT, Witt H, Kool M, Albrecht S, Fleming A, Hadjadj D, Busche S, Lepage P, Montpetit A, Staffa A, Gerges N, Zakrzewska M, Zakrzewski K, Liberski PP, Hauser P, Garami M, Klekner A, Bognar L, Zadeh G, Faury D, Pfister SM, Jabado N, Majewski J (2013) Mutations in SETD2 and genes affecting histone H3K36 methylation target hemispheric high-grade gliomas. Acta neuropathologica 125: 659-669
19. Goldberg IH (1987) Free radical mechanisms in neocarzinostatin-induced DNA damage. Free radical biology & medicine 3: 41-54
20. Greenberg RA (2011) Histone tails: Directing the chromatin response to DNA damage. FEBS Lett 585: 2883-2890
21. Gurova KV, Hill JE, Razorenova OV, Chumakov PM, Gudkov AV (2004) p53 pathway in renal cell carcinoma is repressed by a dominant mechanism. Cancer Res 64: 1951-1958
22. Harper JW, Elledge SJ (2007) The DNA damage response: ten years after. Mol Cell 28: 739-745
23. Joseph CG, Hwang H, Jiao Y, Wood LD, Kinde I, Wu J, Mandahl N, Luo J, Hruban RH, Diaz LA, Jr., He TC, Vogelstein B, Kinzler KW, Mertens F, Papadopoulos N (2014) Exomic analysis of myxoid liposarcomas, synovial sarcomas, and osteosarcomas. Genes, chromosomes & cancer 53: 15-24
24. Kari V, Shchebet A, Neumann H, Johnsen SA (2011) The H2B ubiquitin ligase RNF40 cooperates with SUPT16H to induce dynamic changes in chromatin structure during DNA double-strand break repair. Cell Cycle 10:3495-504
25. Kastan MB, Bartek J (2004) Cell-cycle checkpoints and cancer. Nature 432: 316-323
26. Li F, Mao G, Tong D, Huang J, Gu L, Yang W, Li GM (2013) The histone mark H3K36me3 regulates human DNA mismatch repair through its interaction with MutSalpha. Cell 153: 590-600
27. Lieber MR (2010) The mechanism of double-strand DNA break repair by the nonhomologous DNA end-joining pathway. Annu Rev Biochem 79: 181-211
28. Luger K, Mader AW, Richmond RK, Sargent DF, Richmond TJ (1997) Crystal structure of the nucleosome core particle at 2.8 A resolution. Nature 389: 251-260
29. Lukas J, Lukas C, Bartek J (2011) More than just a focus: The chromatin response to DNA damage and its role in genome integrity maintenance. Nat Cell Biol 13: 1161-1169
30. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER, 3rd, Hurov KE, Luo J, Bakalarski CE, Zhao Z, Solimini N, Lerenthal Y, Shiloh Y, Gygi SP, Elledge SJ (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166
31. Moore, CW (1988) Internucleosomal cleavage and chromosomal degradation by bleomycin and phleomycin in yeast. Cancer Res 23: 6837-6843
32. Moynahan ME, Jasin M (2010) Mitotic homologous recombination maintains genomic stability and suppresses tumorigenesis. Nat Rev Mol Cell Biol 11: 196-207
33. Oliveira DV, Kato A, Nakamura K, Ikura T, Okada M, Kobayashi J, Yanagihara H, Saito Y, Tauchi H, Komatsu K (2014) Histone chaperone FACT regulates homologous recombination by chromatin remodeling through interaction with RNF20. J Cell Sci 127(Pt 4):763-72
34. Papamichos-Chronakis M, Peterson CL (2013) Chromatin and the genome integrity network. Nat Rev Genet 14: 62-75
35. Pei H, Zhang L, Luo K, Qin Y, Chesi M, Fei F, Bergsagel PL, Wang L, You Z, Lou Z (2011) MMSET regulates histone H4K20 methylation and 53BP1 accumulation at DNA damage sites. Nature 470: 124-128
36. Pierce AJ, Johnson RD, Thompson LH, Jasin M (1999) XRCC3 promotes homology-directed repair of DNA damage in mammalian cells. Genes Dev 13: 2633-2638
37. Rogakou EP, Pilch DR, Orr AH, Ivanova VS, Bonner WM (1998) DNA double-stranded breaks induce histone H2AX phosphorylation on serine 139. J Biol Chem 273: 5858-5868
38. San Filippo J, Sung P, Klein H (2008) Mechanism of eukaryotic homologous recombination. Annu Rev Biochem 77: 229-257
39. Sancar A, Lindsey-Boltz LA, Unsal-Kacmaz K, Linn S (2004) Molecular mechanisms of mammalian DNA repair and the DNA damage checkpoints. Annu Rev Biochem 73: 39-85
40. Sartori AA, Lukas C, Coates J, Mistrik M, Fu S, Bartek J, Baer R, Lukas J, Jackson SP (2007) Human CtIP promotes DNA end resection. Nature 450: 509-514
41. Sato Y, Yoshizato T, Shiraishi Y, Maekawa S, Okuno Y, Kamura T, Shimamura T, Sato-Otsubo A, Nagae G, Suzuki H, Nagata Y, Yoshida K, Kon A, Suzuki Y, Chiba K, Tanaka H, Niida A, Fujimoto A, Tsunoda T, Morikawa T, Maeda D, Kume H, Sugano S, Fukayama M, Aburatani H, Sanada M, Miyano S, Homma Y, Ogawa S (2013) Integrated molecular analysis of clear-cell renal cell carcinoma. Nat Genet 45: 860-867
42. Shao RG, Cao CX, Zhang H, Kohn KW, Wold MS, Pommier Y (1999) Replication-mediated DNA damage by camptothecin induces phosphorylation of RPA by DNA-dependent protein kinase and dissociates RPA:DNA-PK complexes. EMBO J 18: 1397-1406
43. Shieh SY, Ikeda M, Taya Y, Prives C (1997) DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91: 325-334
44. Shiotani B, Zou L (2009) Single-stranded DNA orchestrates an ATM-to-ATR switch at DNA breaks. Mol Cell 33: 547-558
45. Soria G, Polo SE, Almouzni G (2012) Prime, repair, restore: the active role of chromatin in the DNA damage response. Mol Cell 46: 722-734
46. Sperka T, Wang J, Rudolph KL (2012) DNA damage checkpoints in stem cells, ageing and cancer. Nat Rev Mol Cell Biol 13: 579-590
47. Stiff T, O'Driscoll M, Rief N, Iwabuchi K, Löbrich M, Jeggo PA (2004) ATM and DNA-PK function redundantly to phosphorylate H2AX after exposure to ionizing radiation. Cancer Res 64: 2390-6
48. Varela I, Tarpey P, Raine K, Huang D, Ong CK, Stephens P, Davies H, Jones D, Lin ML, Teague J, Bignell G, Butler A, Cho J, Dalgliesh GL, Galappaththige D, Greenman C, Hardy C, Jia M, Latimer C, Lau KW, Marshall J, McLaren S, Menzies A, Mudie L, Stebbings L, Largaespada DA, Wessels LF, Richard S, Kahnoski RJ, Anema J, Tuveson DA, Perez-Mancera PA, Mustonen V, Fischer A, Adams DJ, Rust A, Chan-on W, Subimerb C, Dykema K, Furge K, Campbell PJ, Teh BT, Stratton MR, Futreal PA (2011) Exome sequencing identifies frequent mutation of the SWI/SNF complex gene PBRM1 in renal carcinoma. Nature 469: 539-542
49. Waldmann T, Schneider R (2013) Targeting histone modifications--epigenetics in cancer. Curr Opin Cell Biol 25: 184-189
50. Ward IM, Chen J (2001) Histone H2AX is phosphorylated in an ATR-dependent manner in response to replicational stress. J Biol Chem 276:47759-62
51. Wyman C, Kanaar R (2006) DNA double-strand break repair: all's well that ends well. Annu Rev Genet 40: 363-383
52. Xie P, Tian C, An L, Nie J, Lu K, Xing G, Zhang L, He F (2008) Histone methyltransferase protein SETD2 interacts with p53 and selectively regulates its downstream genes. Cell Signal 20:1671-8
53. Yang X, Li L, Liang J, Shi L, Yang J, Yi X, Zhang D, Han X, Yu N, Shang Y (2013) Histone Acetyltransferase 1 Promotes Homologous Recombination in DNA Repair by Facilitating Histone Turnover. J Biol Chem 288:18271-82
54. Zhang J, Ding L, Holmfeldt L, Wu G, Heatley SL, Payne-Turner D, Easton J, Chen X, Wang J, Rusch M, Lu C, Chen SC, Wei L, Collins-Underwood JR, Ma J, Roberts KG, Pounds SB, Ulyanov A, Becksfort J, Gupta P, Huether R, Kriwacki RW, Parker M, McGoldrick DJ, Zhao D, Alford D, Espy S, Bobba KC, Song G, Pei D, Cheng C, Roberts S, Barbato MI, Campana D, Coustan-Smith E, Shurtleff SA, Raimondi SC, Kleppe M, Cools J, Shimano KA, Hermiston ML, Doulatov S, Eppert K, Laurenti E, Notta F, Dick JE, Basso G, Hunger SP, Loh ML, Devidas M, Wood B, Winter S, Dunsmore KP, Fulton RS, Fulton LL, Hong X, Harris CC, Dooling DJ, Ochoa K, Johnson KJ, Obenauer JC, Evans WE, Pui CH, Naeve CW, Ley TJ, Mardis ER, Wilson RK, Downing JR, Mullighan CG (2012) The genetic basis of early T-cell precursor acute lymphoblastic leukaemia. Nature 481: 157-163