Bcl2 inhibits recruitment of Mre11 complex to DNA double-strand breaks in response to high-linear energy transfer radiation

Nucleic Acids Research

Volumn 43, Issue 2, 2015, Pages 960-972

  Xie, Maohua ^a   Park, Dongkyoo ^a   You, Shuo ^a   Li, Rui ^a   Owonikoko, Taofeek K ^a   Wang, Ya ^a   Doetsch, Paul W ^a   Deng, Xingming ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; DNA BINDING PROTEIN; H2AFX PROTEIN, HUMAN; HISTONE; MRE11A PROTEIN, HUMAN; PROTEIN BCL 2; SIGNAL PEPTIDE; TP53BP1 PROTEIN, HUMAN;

ANTAGONISTS AND INHIBITORS; CELL LINE; CELL NUCLEUS; CHEMISTRY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; HOMOLOGOUS RECOMBINATION; HUMAN; IONIZING RADIATION; LINEAR ENERGY TRANSFER; METABOLISM; PROTEIN DOMAIN;

CELL LINE; CELL NUCLEUS; DNA; DNA BREAKS, DOUBLE-STRANDED; DNA REPAIR; DNA-BINDING PROTEINS; HISTONES; HOMOLOGOUS RECOMBINATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LINEAR ENERGY TRANSFER; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTO-ONCOGENE PROTEINS C-BCL-2; RADIATION, IONIZING;

EID: 84945200048     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gku1358     Document Type: Article

References (45)

1. Durante,M. and Cucinotta,F.A. (2008) Heavy ion carcinogenesis and human space exploration. Nat. Rev. Cancer, 8, 465-472.
2. Wang,H., Wang,X., Zhang,P. and Wang,Y. (2008) The Ku-dependent non-homologous end-joining but not other repair pathway is inhibited by high linear energy transfer ionizing radiation. DNA Repair, 7, 725-733.
3. Wang,H., Zhang,X., Wang,P., Yu,X., Essers,J., Chen,D., Kanaar,R., Takeda,S. and Wang,Y. (2010) Characteristics of DNA-binding proteins determine the biological sensitivity to high-linear energy transfer radiation. Nucleic Acids Res., 38, 3245-3251.
4. Asaithamby,A., Uematsu,N., Chatterjee,A., Story,M.D., Burma,S. and Chen,D.J. (2008) Repair of HZE-particle-induced DNA double-strand breaks in normal human fibroblasts. Radiat. Res., 169, 437-446.
5. Hada,M. and Georgakilas,A.G. (2008) Formation of clustered DNA damage after high-LET irradiation: a review. J. Radiat. Res., 49, 203-210.
6. Anderson,J.A., Harper,J.V., Cucinotta,F.A. and O'Neill,P. (2010) Participation of DNA-PKcs in DSB repair after exposure to highand low-LET radiation. Radiat. Res., 174, 195-205.
7. Williams,G.J., Lees-Miller,S.P. and Tainer,J.A. (2010) Mre11-Rad50-Nbs1 conformations and the control of sensing, signaling, and effector responses at DNA double-strand breaks. DNA Repair, 9, 1299-1306.
8. Williams,R.S.,Williams,J.S. and Tainer,J.A. (2007) Mre11-Rad50-Nbs1 is a keystone complex connecting DNA repair machinery, double-strand break signaling, and the chromatin template. Biochem. Cell Biol., 85, 509-520.
9. Paull,T.T. and Gellert,M. (1998) The 3to 5exonuclease activity of Mre 11 facilitates repair of DNA double-strand breaks. Mol. Cell, 1, 969-979.
10. Cannon,B., Kuhnlein,J., Yang,S.H., Cheng,A., Schindler,D., Stark,J.M., Russell,R. and Paull,T.T. (2013) Visualization of local DNA unwinding by Mre11/Rad50/Nbs1 using single-molecule FRET. Proc. Natl. Acad. Sci. U.S.A, 110, 18868-18873.
11. Cejka,P., Cannavo,E., Polaczek,P., Masuda-Sasa,T., Pokharel,S., Campbell,J.L. and Kowalczykowski,S.C. (2010) DNA end resection by Dna2-Sgs1-RPA and its stimulation by Top3-Rmi1 and Mre11-Rad50-Xrs2. Nature, 467, 112-116.
12. Ferretti,L.P., Lafranchi,L. and Sartori,A.A. (2013) Controlling DNA-end resection: a new task for CDKs. Front. Genet., 4, 99.
13. Wang,Q., Gao,F., May,W.S., Zhang,Y., Flagg,T. and Deng,X. (2008) Bcl2 negatively regulates DNA double-strand-break repair through a nonhomologous end-joining pathway. Mol. Cell, 29, 488-498.
14. Saintigny,Y., Dumay,A., Lambert,S. and Lopez,B.S. (2001) A novel role for the Bcl-2 protein family: specific suppression of the RAD51 recombination pathway. EMBO J., 20, 2596-2607.
15. Leatherbarrow,E.L., Harper,J.V., Cucinotta,F.A. and O'Neill,P. (2006) Induction and quantification of gamma-H2AX foci following low and high LET-irradiation. Int. J. Radiat. Biol., 82, 111-118.
16. Yuan,J. and Chen,J. (2009) N terminus of CtIP is critical for homologous recombination-mediated double-strand break repair. J. Biol. Chem., 284, 31746-31752.
17. Lee,J.H. and Paull,T.T. (2006) Purification and biochemical characterization of ataxia-telangiectasia mutated and Mre11/Rad50/Nbs1. Methods Enzymol., 408, 529-539.
18. Zheng,L., Kanagaraj,R., Mihaljevic,B., Schwendener,S., Sartori,A.A., Gerrits,B., Shevelev,I. and Janscak,P. (2009) MRE11 complex links RECQ5 helicase to sites of DNA damage. Nucleic Acids Res., 37, 2645-2657.
19. Sartori,A.A., Lukas,C., Coates,J., Mistrik,M., Fu,S., Bartek,J., Baer,R., Lukas,J. and Jackson,S.P. (2007) Human CtIP promotes DNA end resection. Nature, 450, 509-514.
20. Shibata,A., Moiani,D., Arvai,A.S., Perry,J., Harding,S.M., Genois,M.M., Maity,R., van Rossum-Fikkert,S., Kertokalio,A., Romoli,F. et al. (2014) DNA double-strand break repair pathway choice is directed by distinct MRE11 nuclease activities. Mol. Cell, 53, 7-18.
21. Paull,T.T. and Gellert,M. (2000) A mechanistic basis for Mre11-directed DNA joining at microhomologies. Proc. Natl. Acad. Sci. U.S.A., 97, 6409-6414.
22. Yu,Z., Vogel,G., Coulombe,Y., Dubeau,D., Spehalski,E., Hebert,J., Ferguson,D.O., Masson,J.Y. and Richard,S. (2012) The MRE11 GAR motif regulates DNA double-strand break processing and ATR activation. Cell Res., 22, 305-320.
23. Lee,J.H., Ghirlando,R., Bhaskara,V., Hoffmeyer,M.R., Gu,J. and Paull,T.T. (2003) Regulation of Mre11/Rad50 by Nbs1: effects on nucleotide-dependent DNA binding and association with ataxia-telangiectasia-like disorder mutant complexes. J. Biol. Chem., 278, 45171-45181.
24. Wang,H., Liu,S., Zhang,P., Zhang,S., Naidu,M., Wang,H. and Wang,Y. (2009) S-phase cells are more sensitive to high-linear energy transfer radiation. Int. J. Radiat. Oncol. Biol. Phys., 74, 1236-1241.
25. Huang,S., Okumura,K. and Sinicrope,F.A. (2009) BH3 mimetic obatoclax enhances TRAIL-mediated apoptosis in human pancreatic cancer cells. Clin. Cancer Res., 15, 150-159.
26. Cucinotta,F.A.,Wu,H., Shavers,M.R. and George,K. (2003) Radiation dosimetry and biophysical models of space radiation effects. Gravit. Space Biol. Bull, 16, 11-18.
27. Asaithamby,A. and Chen,D.J. (2011) Mechanism of cluster DNA damage repair in response to high-atomic number and energy particles radiation. Mutat. Res., 711, 87-99.
28. Asaithamby,A., Hu,B. and Chen,D.J. (2011) Unrepaired clustered DNA lesions induce chromosome breakage in human cells. Proc. Natl. Acad. Sci. U.S.A., 108, 8293-8298.
29. Laulier,C., Barascu,A., Guirouilh-Barbat,J., Pennarun,G., Chalony,C., Chevalier,F., Palierne,G., Bertrand,P., Verbavatz,J.M. and Lopez,B.S. (2011) Bcl-2 inhibits nuclear homologous recombination by localizing BRCA1 to the endomembranes. Cancer Res., 71, 3590-3602.
30. Hockenbery,D., Nunez,G., Milliman,C., Schreiber,R.D. and Korsmeyer,S.J. (1990) Bcl-2 is an inner mitochondrial membrane protein that blocks programmed cell death. Nature, 348, 334-336.
31. Nimonkar,A.V., Genschel,J., Kinoshita,E., Polaczek,P., Campbell,J.L., Wyman,C., Modrich,P. and Kowalczykowski,S.C. (2011) BLM-DNA2-RPA-MRN and EXO1-BLM-RPA-MRN constitute two DNA end resection machineries for human DNA break repair. Genes Dev., 25, 350-362.
32. de Jager,M., van Noort,J., van Gent,D.C., Dekker,C., Kanaar,R. and Wyman,C. (2001) Human Rad50/Mre11 is a flexible complex that can tether DNA ends. Mol. Cell, 8, 1129-1135.
33. Williams,R.S., Moncalian,G., Williams,J.S., Yamada,Y., Limbo,O., Shin,D.S., Groocock,L.M., Cahill,D., Hitomi,C., Guenther,G. et al. (2008) Mre11 dimers coordinate DNA end bridging and nuclease processing in double-strand-break repair. Cell, 135, 97-109.
34. Buis,J., Wu,Y., Deng,Y., Leddon,J., Westfield,G., Eckersdorff,M., Sekiguchi,J.M., Chang,S. and Ferguson,D.O. (2008) Mre11 nuclease activity has essential roles in DNA repair and genomic stability distinct from ATM activation. Cell, 135, 85-96.
35. Kelekar,A. and Thompson,C.B. (1998) Bcl-2-family proteins: the role of the BH3 domain in apoptosis. Trends Cell Biol., 8, 324-330.
36. Stracker,T.H. and Petrini,J.H. (2011) The MRE11 complex: starting from the ends. Nat. Rev. Mol. Cell. Biol., 12, 90-103.
37. Moore,S., Stanley,F.K. and Goodarzi,A.A. (2014) The repair of environmentally relevant DNA double strand breaks caused by high linear energy transfer irradiation-No simple task. DNA Repair, 17, 64-73.
38. Alloni,D., Campa,A., Belli,M., Esposito,G., Facoetti,A., Friedland,W., Liotta,M., Mariotti,L., Paretzke,H.G. and Ottolenghi,A. (2010) A Monte Carlo study of the radiation quality dependence of DNA fragmentation spectra. Radiat. Res., 173, 263-271.
39. Campa,A., Alloni,D., Antonelli,F., Ballarini,F., Belli,M., Dini,V., Esposito,G., Facoetti,A., Friedland,W., Furusawa,Y. et al. (2009) DNA fragmentation induced in human fibroblasts by 56Fe ions: experimental data and Monte Carlo simulations. Radiat. Res., 171, 438-445.
40. Paull,T.T. (2010) Making the best of the loose ends: Mre11/Rad50 complexes and Sae2 promote DNA double-strand break resection. DNA Repair, 9, 1283-1291.
41. Schlacher,K., Christ,N., Siaud,N., Egashira,A.,Wu,H. and Jasin,M. (2011) Double-strand break repair-independent role for BRCA2 in blocking stalled replication fork degradation by MRE11. Cell, 145, 529-542.
42. Schlacher,K., Wu,H. and Jasin,M. (2012) A distinct replication fork protection pathway connects Fanconi anemia tumor suppressors to RAD51-BRCA1/2. Cancer Cell, 22, 106-116.
43. Xie,M., Yen,Y., Owonikoko,T.K., Ramalingam,S.S., Khuri,F.R., Curran,W.J., Doetsch,P.W. and Deng,X. (2014) Bcl2 induces DNA replication stress by inhibiting ribonucleotide reductase. Cancer Res., 74, 212-223.
44. Pearson,C.G., Shikazono,N., Thacker,J. and O'Neill,P. (2004) Enhanced mutagenic potential of 8-oxo-7,8-dihydroguanine when present within a clustered DNA damage site. Nucleic Acids Res., 32, 263-270.
45. Kuhne,M., Rothkamm,K. and Lobrich,M. (2000) No dose-dependence of DNA double-strand break misrejoining following alpha-particle irradiation. Int. J. Radiat. Biol., 76, 891-900.