UbcH7 regulates 53BP1 stability and DSB repair

Proceedings of the National Academy of Sciences of the United States of America

Volumn 111, Issue 49, 2014, Pages 17456-17461

  Han, Xiangzi ^a   Zhang, Lei ^a   Chung, Jinsil ^a   Pozo, Franklin Mayca ^a   Tran, Amanda ^a   Seachrist, Darcie D ^a   Jacobberger, James W ^a   Keri, Ruth A ^a   Gilmore, Hannah ^b   Zhang, Youwei ^a  

^a CASE WESTERN RESERVE UNIVERSITY   (United States)

^b UNIVERSITY HOSPITALS OF CLEVELAND   (United States)

Author keywords

53BP1; DNA damage response; DSB repair; Protein degradation; UbcH7

Indexed keywords

BINDING PROTEIN; P53 BINDING PROTEIN 1; UBIQUITIN CONJUGATING ENZYME; UBIQUITIN CONJUGATING ENZYME H7; UNCLASSIFIED DRUG; CAMPTOTHECIN; PROTEASOME; SIGNAL PEPTIDE; SMALL INTERFERING RNA; TP53BP1 PROTEIN, HUMAN; UBE2L3 PROTEIN, HUMAN; UBIQUITIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CELL STRESS; CONTROLLED STUDY; DNA DAMAGE; DNA END JOINING REPAIR; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; PROTEIN DEPLETION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; REGULATORY MECHANISM; SENSITIVITY ANALYSIS; CELL SURVIVAL; CHEMISTRY; DNA REPAIR; GENE EXPRESSION REGULATION; HEK293 CELL LINE; HUMAN; METABOLISM; PHOSPHORYLATION; PROGNOSIS; TUMOR CELL LINE;

CAMPTOTHECIN; CELL LINE, TUMOR; CELL SURVIVAL; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DNA REPAIR; GENE EXPRESSION REGULATION, NEOPLASTIC; HEK293 CELLS; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROGNOSIS; PROTEASOME ENDOPEPTIDASE COMPLEX; RNA, SMALL INTERFERING; UBIQUITIN; UBIQUITIN-CONJUGATING ENZYMES;

EID: 84918562574     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1408538111     Document Type: Article

References (44)

1. Harper JW, Elledge SJ (2007) The DNA damage response: Ten years after. Mol Cell 28(5):739-745
2. Zimmermann M, Lottersberger F, Buonomo SB, Sfeir A, de Lange T (2013) 53BP1 regulates DSB repair using Rif1 to control 5' end resection. Science 339(6120):700-704
3. Chapman JR, et al. (2013) RIF1 is essential for 53BP1-dependent nonhomologous end joining and suppression of DNA double-strand break resection. Mol Cell 49(5): 858-871
4. Di Virgilio M, et al. (2013) Rif1 prevents resection of DNA breaks and promotes immunoglobulin class switching. Science 339(6120):711-715
5. Feng L, Fong KW, Wang J, Wang W, Chen J (2013) RIF1 counteracts BRCA1-mediated end resection during DNA repair. J Biol Chem 288(16):11135-11143
6. Escribano-Díaz C, et al. (2013) A cell cycle-dependent regulatory circuit composed of 53BP1-RIF1 and BRCA1-CtIP controls DNA repair pathway choice. Mol Cell 49(5): 872-883
7. Panier S, Boulton SJ (2014) Double-strand break repair: 53BP1 comes into focus. Nat Rev Mol Cell Biol 15(1):7-18
8. Goodarzi AA, Jeggo PA (2013) The repair and signaling responses to DNA doublestrand breaks. Adv Genet 82:1-45
9. Saberi A, et al. (2007) RAD18 and poly(ADP-ribose) polymerase independently suppress the access of nonhomologous end joining to double-strand breaks and facilitate homologous recombination-mediated repair. Mol Cell Biol 27(7):2562-2571
10. McGlynn P, Lloyd RG (2002) Recombinational repair and restart of damaged replication forks. Nat Rev Mol Cell Biol 3(11):859-870
11. Tang J, et al. (2013) Acetylation limits 53BP1 association with damaged chromatin to promote homologous recombination. Nat Struct Mol Biol 20(3):317-325
12. Bouwman P, et al. (2010) 53BP1 loss rescues BRCA1 deficiency and is associated with triple-negative and BRCA-mutated breast cancers. Nat Struct Mol Biol 17(6):688-695
13. Bunting SF, et al. (2010) 53BP1 inhibits homologous recombination in Brca1-deficient cells by blocking resection of DNA breaks. Cell 141(2):243-254
14. Cao L, et al. (2009) A selective requirement for 53BP1 in the biological response to genomic instability induced by Brca1 deficiency. Mol Cell 35(4):534-541
15. Neboori HJ, et al. (2012) Low p53 binding protein 1 (53BP1) expression is associated with increased local recurrence in breast cancer patients treated with breast-conserving surgery and radiotherapy. Int J Radiat Oncol Biol Phys 83(5):e677-e683
16. Jaspers JE, et al. (2013) Loss of 53BP1 causes PARP inhibitor resistance in Brca1- mutated mouse mammary tumors. Cancer Discov 3(1):68-81
17. Oplustilova L, et al. (2012) Evaluation of candidate biomarkers to predict cancer cell sensitivity or resistance to PARP-1 inhibitor treatment. Cell Cycle 11(20):3837-3850
18. Squatrito M, Vanoli F, Schultz N, Jasin M, Holland EC (2012) 53BP1 is a haploinsufficient tumor suppressor and protects cells from radiation response in glioma. Cancer Res 72(20):5250-5260
19. Takeyama K, et al. (2008) Integrative analysis reveals 53BP1 copy loss and decreased expression in a subset of human diffuse large B-cell lymphomas. Oncogene 27(3): 318-322
20. Ausborn NL, et al. (2013) 53BP1 expression is a modifier of the prognostic value of lymph node ratio and CA 19-9 in pancreatic adenocarcinoma. BMC Cancer 13:155
21. Messick TE, Greenberg RA (2009) The ubiquitin landscape at DNA double-strand breaks. J Cell Biol 187(3):319-326
22. Jackson SP, Durocher D (2013) Regulation of DNA damage responses by ubiquitin and SUMO. Mol Cell 49(5):795-807
23. Zhang Y, Hunter T (2014) Roles of Chk1 in cell biology and cancer therapy. Int J Cancer 134(5):1013-1023
24. Zhang YW, et al. (2005) Genotoxic stress targets human Chk1 for degradation by the ubiquitin-proteasome pathway. Mol Cell 19(5):607-618
25. Whitcomb EA, Dudek EJ, Liu Q, Taylor A (2009) Novel control of S phase of the cell cycle by ubiquitin-conjugating enzyme H7. Mol Biol Cell 20(1):1-9
26. Robinson PA, et al. (1995) A human ubiquitin conjugating enzyme, L-UBC, maps in the Alzheimer's disease locus on chromosome 14q24.3. Mamm Genome 6(10):725-731
27. Moynihan TP, et al. (1996) Characterization of a human ubiquitin-conjugating enzyme gene UBE2L3. Mamm Genome 7(7):520-525
28. Nuber U, Schwarz S, Kaiser P, Schneider R, Scheffner M (1996) Cloning of human ubiquitin-conjugating enzymes UbcH6 and UbcH7 (E2-F1) and characterization of their interaction with E6-AP and RSP5. J Biol Chem 271(5):2795-2800
29. Brzovic PS, et al. (2003) Binding and recognition in the assembly of an active BRCA1/ BARD1 ubiquitin-ligase complex. Proc Natl Acad Sci USA 100(10):5646-5651
30. Gudjonsson T, et al. (2012) TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes. Cell 150(4):697-709
31. Cimprich KA, Cortez D (2008) ATR: An essential regulator of genome integrity. Nat Rev Mol Cell Biol 9(8):616-627
32. Pringa E, Meier I, Müller U, Martinez-Noel G, Harbers K (2000) Disruption of the gene encoding the ubiquitin-conjugating enzyme UbcM4 has no effect on proliferation and in vitro differentiation of mouse embryonic stem cells. Biochim Biophys Acta 1494(1-2):75-82
33. Zhang YW, et al. (2009) The F box protein Fbx6 regulates Chk1 stability and cellular sensitivity to replication stress. Mol Cell 35(4):442-453
34. Pierce AJ, Johnson RD, Thompson LH, Jasin M (1999) XRCC3 promotes homologydirected repair of DNA damage in mammalian cells. Genes Dev 13(20):2633-2638
35. Callen E, et al. (2013) 53BP1 mediates productive and mutagenic DNA repair through distinct phosphoprotein interactions. Cell 153(6):1266-1280
36. Stewart CF (2001) Topoisomerase I interactive agents. Cancer Chemother Biol Response Modif 19:85-128
37. Bailly C (2000) Topoisomerase I poisons and suppressors as anticancer drugs. Curr Med Chem 7(1):39-58
38. Moudry P, et al. (2012) Nucleoporin NUP153 guards genome integrity by promoting nuclear import of 53BP1. Cell Death Differ 19(5):798-807
39. Moudry P, et al. (2012) Ubiquitin-activating enzyme UBA1 is required for cellular response to DNA damage. Cell Cycle 11(8):1573-1582
40. Butler LR, et al. (2012) The proteasomal de-ubiquitinating enzyme POH1 promotes the double-strand DNA break response. EMBO J 31(19):3918-3934
41. Liu C, et al. (2013) RNF168 forms a functional complex with RAD6 during the DNA damage response. J Cell Sci 126(Pt 9):2042-2051
42. Sørensen CS, et al. (2005) The cell-cycle checkpoint kinase Chk1 is required for mammalian homologous recombination repair. Nat Cell Biol 7(2):195-201
43. Zhang D, Zaugg K, Mak TW, Elledge SJ (2006) A role for the deubiquitinating enzyme USP28 in control of the DNA-damage response. Cell 126(3):529-542
44. Grotsky DA, et al. (2013) BRCA1 loss activates cathepsin L-mediated degradation of 53BP1 in breast cancer cells. J Cell Biol 200(2):187-202.