Nonhomologous end-joining repair plays a more important role than homologous recombination repair in defining radiosensitivity after exposure to High-LET radiation

Radiation Research

Volumn 182, Issue 3, 2014, Pages 338-344

  Takahashi, Akihisa ^a,b   Kubo, Makoto ^b   Ma, Hongyu ^b   Nakagawa, Akiko ^b   Yoshida, Yukari ^c   Isono, Mayu ^c   Kanai, Tatsuaki ^c   Ohno, Tatsuya ^c   Furusawa, Yoshiya ^d   Funayama, Tomoo ^e   Kobayashi, Yasuhiko ^e   Nakano, Takashi ^b,c  

^a GUNMA UNIVERSITY   (Japan)

^b GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^c GUNMA UNIVERSITY HEAVY ION MEDICAL CENTER   (Japan)

^d NATIONAL INSTITUTE OF RADIOLOGICAL SCIENCES   (Japan)

^e JAPAN ATOMIC ENERGY AGENCY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ARGON; CARBON; IRON; NEON;

ANIMAL CELL; ARTICLE; CELL SURVIVAL; DNA END JOINING REPAIR; EMBRYO; FIBROBLAST; HOMOLOGOUS RECOMBINATION; ION THERAPY; LINEAR ENERGY TRANSFER; MOUSE; NONHUMAN; PRIORITY JOURNAL; RADIATION EXPOSURE; RADIOSENSITIVITY; RADIOSENSITIZATION; RECOMBINATION REPAIR;

ANIMALS; CELL SURVIVAL; CELLS, CULTURED; DNA END-JOINING REPAIR; LINEAR ENERGY TRANSFER; MICE; RADIATION TOLERANCE; RECOMBINATIONAL DNA REPAIR;

EID: 84907365436     PISSN: 00337587     EISSN: 19385404     Source Type: Journal    
DOI: 10.1667/RR13782.1     Document Type: Article

References (48)

1. Ohnishi T, Mori E, Takahashi A. DNA double-strand breaks: their production, recognition, and repair in eukaryotes. Mutat Res 2009; 669:8-12.
2. Falk M, Lukasova E, Kozubek S. Higher-order chromatin structure in DSB induction, repair and misrepair. Mutat Res 2010; 704:88-100.
3. Chapman JR, Taylor MR, Boulton SJ. Playing the end game: DNA double-strand break repair pathway choice. Mol Cell 2012; 47:497-510.
4. Wang C, Lees-Miller SP. Detection and repair of ionizing radiation-induced DNA double strand breaks: new developments in nonhomologous end joining. Int J Radiat Oncol Biol Phys 2013; 86:440-9.
5. Jeggo PA, Geuting V, Löbrich M. The role of homologous recombination in radiation-induced double-strand break repair. Radiother Oncol 2011; 101:7-12.
6. Hall EJ, Giaccia AJ. Radiobiology for the radiologist. 7th ed. Philadelphia: Lippincott Williams & Wilkins; 2012.
7. Wouters BG, Begg AC. Irradiation-induced damage and the DNA damage response. In: Joiner M, van der Kogel A, editors. Basic clinical radiobiology. 4th ed. London: Hodder Arnold Publication; 2009. p. 11-26.
8. Kobayashi J, Antoccia A, Tauchi H, Matsuura S, Komatsu K. NBS1 and its functional role in the DNA damage response. DNA Repair 2004; 3:855-61.
9. Kanai T, Furusawa Y, Fukutsu K, Itsukaichi H, Eguchi-Kasai K, Ohara H. Irradiation of mixed beam and design of spread-out Bragg peak for heavy-ion radiotherapy. Radiat Res 1997; 147:78-85.
10. Suzuki M, Kase Y, Yamaguchi H, Kanai T, Ando K. Relative biological effectiveness for cell-killing effect on various human cell lines irradiated with heavy-ion medical accelerator in Chiba (HIMAC) carbon-ion beams. Int J Radiat Oncol Biol Phys 2000; 48:241-50.
11. Ando K, Kase Y. Biological characteristics of carbon-ion therapy. Int J Radiat Biol 2009; 85:715-28.
12. Hirayama R, Furusawa Y, Fukawa T, Ando K. Repair kinetics of DNA-DSB induced by X-rays or carbon ions under oxic and hypoxic conditions. J Radiat Res 2005; 46:325-32.
13. Takahashi A, Yamakawa N, Kirita T, Omori K, Ishioka N, Furusawa Y, et al. DNA damage recognition proteins localize along heavy ion induced tracks in the cell nucleus. J Radiat Res 2008; 49:645-52.
14. Takahashi A, Matsumoto H, Furusawa Y, Ohnishi K, Ishioka N, Ohnishi T. Apoptosis induced by high-LET radiations is not affected by cellular p53 gene status. Int J Radiat Biol 2005; 81:581-6.
15. Hamada N, Hara T, Omura-Minamisawa M, Funayama T, Sakashita T, Sora S, et al. The survival of heavy ion-irradiated Bcl-2 overexpressing radioresistant tumor cells and their progeny. Cancer Lett 2008; 268:76-81.
16. Hamada N, Imaoka T, Masunaga S, Ogata T, Okayasu R, Takahashi A, et al. Recent advances in the biology of heavy-ion cancer therapy. J Radiat Res 2010; 51:365-83.
17. Cui X, Oonishi K, Tsujii H, Yasuda T, Matsumoto Y, Furusawa Y, et al. Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays. Cancer Res 2011; 71:3676-87.
18. Akino Y, Teshima T, Kihara A, Kodera-Suzumoto Y, Inaoka M, Higashiyama S, et al. Carbon-ion beam irradiation effectively suppresses migration and invasion of human non-small-cell lung cancer cells. Int J Radiat Oncol Biol Phys 2009; 75:475-81.
19. Tsujii H, Kamada T. A review of update clinical results of carbon ion radiotherapy. Jpn J Clin Oncol 2012; 42:670-85.
20. Ohno T. Particle radiotherapy with carbon ion beams. EPMA J 2013; 4:9.
21. Mills KD, Ferguson DO, Essers J, Eckersdorff M, Kanaar R, Alt FW. Rad54 and DNA Ligase IV cooperate to maintain mammalian chromatid stability. Genes Dev 2004; 18:1283-92.
22. Ohno T, Kanai T, Yamada S, Yusa K, Tashiro M, Shimada H, et al. Carbon ion radiotherapy at the Gunma University Heavy Ion Medical Center: new facility set-up. Cancers 2011; 3:4046-60.
23. Funayama T, Wada S, Yokota Y, Fukamoto K, Sakashita T, Taguchi M, et al. Heavy-ion microbeam system at JAEATakasaki for microbeam biology. J Radiat Res 2008; 49:71-82.
24. Wang H, Wang X, Zhang P, Wang Y. The Ku-dependent nonhomologous end joining but not other repair pathway is inhibited by high linear energy transfer ionizing radiation. DNA Repair 2008; 7:725-33.
25. Wang H, Zhang X, Wang P, Yu X, Essers J, Chen D, et al. Characteristics of DNA-binding proteins determine the biological sensitivity to high-linear energy transfer radiation. Nucleic Acids Res 2010; 38:3245-51.
26. Aoki-Nakano M, Furusawa Y. Misrepair of DNA double-strand breaks after exposure to heavy-ion beams causes a peak in the LET-RBE relationship with respect to cell killing in DT40 cells. J Radiat Res 2013; 54:1029-35.
27. Weyrather WK, Ritter S, Scholz M, Kraft G. RBE for carbon track-segment irradiation in cell lines of differing repair capacity. Int J Radiat Biol 1999; 75:1357-64.
28. Okayasu R, Okada M, Okabe A, Noguchi M, Takakura K, Takahashi S. Repair of DNA damage induced by accelerated heavy ions in mammalian cells proficient and deficient in the non-homologous end-joining pathway. Radiat Res 2006; 165:59-67.
29. Lind BK, Persson LM, Edgren MR, Hedlö f I, Brahme A. Repairable-conditionally repairable damage model based on dual Poisson processes. Radiat Res 2003; 160:366-75.
30. Beucher A, Birraux J, Tchouandong L, Barton O, Shibata A, Conrad S, et al. ATM and Artemis promote homologous recombination of radiation-induced DNA double-strand breaks in G2. EMBO J 2009; 28:3413-27.
31. Shibata A, Conrad S, Birraux J, Geuting V, Barton O, Ismail A, et al. Factors determining DNA double-strand break repair pathway choice in G2 phase. EMBO J 2011; 30:1079-92.
32. Terato H, Tanaka R, Nakaarai Y, Nohara T, Doi Y, Iwai S, et al. Quantitative analysis of isolated and clustered DNA damage induced by gamma-rays, carbon ion beams, and iron ion beams. J Radiat Res 2008; 49:133-46.
33. Asaithamby A, Hu B, Chen DJ. Unrepaired clustered DNA lesions induce chromosome breakage in human cells. Proc Natl Acad Sci U S A 2011; 108:8293-8.
34. Li Y, Qian H, Wang Y, Cucinotta FA. A stochastic model of DNA fragments rejoining. PLoS One 2012; 7:e44293.
35. Mehnati P, Morimoto S, Yatagai F, Furusawa Y, Kobayashi Y, Wada S, et al. Exploration of "over kill effect" of high-LET Arand Fe-ions by evaluating the fraction of non-hit cell and interphase death. J Radiat Res 2005; 46:343-50.
36. Horsman MR, Bohm L, Margison GP, Milas L, Rosier JF, Safrany G, et al. Tumor radiosensitizers-current status of development of various approaches: report of an International Atomic Energy Agency meeting. Int J Radiat Oncol Biol Phys 2006; 64:551-61.
37. Nomiya T, Tsuji H, Maruyama K, Kamada T, Tsujii H. Up-todate results of carbon-ion radiotherapy for prostate cancer. J Radiat Res 2014; 55 Suppl 1:i28-9.
38. Yajima H, Fujisawa H, Nakajima NI, Hirakawa H, Jeggo PA, Okayasu R, et al. The complexity of DNA double strand breaks is a critical factor enhancing end-resection. DNA Repair 2013; 12:936-46.
39. Wang M, Wu W, Wu W, Rosidi B, Zhang L, Wang H, et al. PARP-1 and Ku compete for repair of DNA double strand breaks by distinct NHEJ pathways. Nucleic Acids Res 2006; 34:6170-82.
40. Simsek D, Jasin M. Alternative end-joining is suppressed by the canonical NHEJ component Xrcc4-ligase IV during chromosomal translocation formation. Nat Struct Mol Biol 2010; 17:410-6.
41. Malu S, Malshetty V, Francis D, Cortes P. Role of nonhomologous end joining in V (D) J recombination. Immunol Res 2012; 54:233-46.
42. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006; 444:756-60.
43. Hambardzumyan D, Squatrito M, Holland EC. Radiation resistance and stem-like cells in brain tumors. Cancer Cell 2006; 10:454-6.
44. Rich JN. Cancer stem cells in radiation resistance. Cancer Res 2007; 67:8980-4.
45. Nishikawa S, Ishii H, Haraguchi N, Kano I, Fukusumi K, Ohta K, et al. Genotoxic therapy stimulates error-prone DNA repair in dormant hepatocellular cancer stem cells. Exp Ther Med 2012; 3:959-62.
46. Okayasu R, Suetomi K, Ullrich RL. Wortmannin inhibits repair of DNA double-strand breaks in irradiated normal human cells. Radiat Res 1998; 149:440-5.
47. Oike T, Ogiwara H, Torikai K, Nakano T, Yokota J, Kohno T. Garcinol, a histone acetyltransferase inhibitor, radiosensitizes cancer cells by inhibiting non-homologous end joining. Int J Radiat Oncol Biol Phys 2012; 84:815-21.
48. Zhou X, Zhang X, Xie Y, Tanaka K, Wang B, Zhang H. DNAPKcs inhibition sensitizes cancer cells to carbon-ion irradiation via telomere capping disruption. PLoS One 2013; 8:e72641.