Carbon-ion beam irradiation kills X-ray-resistant p53-null cancer cells by inducing mitotic catastrophe

PLoS ONE

Volumn 9, Issue 12, 2014, Pages

  Amornwichet, Napapat ^a,b   Oike, Takahiro ^a,c   Shibata, Atsushi ^d   Ogiwara, Hideaki ^c   Tsuchiya, Naoto ^c   Yamauchi, Motohiro ^e   Saitoh, Yuka ^a   Sekine, Ryota ^d   Isono, Mayu ^f   Yoshida, Yukari ^f   Ohno, Tatsuya ^f   Kohno, Takashi ^c   Nakano, Takashi ^a   Fei, Peiwen ^g  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b CHULALONGKORN UNIVERSITY   (Thailand)

^c NATIONAL CANCER CENTER RESEARCH INSTITUTE   (Japan)

^d GUNMA UNIVERSITY   (Japan)

^e NAGASAKI UNIVERSITY   (Japan)

^f GUNMA UNIVERSITY HEAVY ION MEDICAL CENTER   (Japan)

^g UNIVERSITY OF HAWAII CANCER CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS; ARTICLE; CANCER CELL DESTRUCTION; CELL DEATH; CELL KILLING; CELL SURVIVAL; CHROMOSOME ABERRATION; CONTROLLED STUDY; DNA REPAIR; DOUBLE STRANDED DNA BREAK; G2 PHASE CELL CYCLE CHECKPOINT; HCT116 CELL LINE; HUMAN; HUMAN CELL; INTERMETHOD COMPARISON; ION THERAPY; M PHASE CELL CYCLE CHECKPOINT; MITOSIS; MITOTIC CATASTROPHE; RADIOSENSITIVITY; TUMOR SUPPRESSOR GENE; X IRRADIATION; DEFICIENCY; GENETICS; IONIZING RADIATION; METABOLISM; PHOSPHORYLATION; RADIATION RESPONSE; TUMOR CELL LINE;

HISTONE; PROTEIN P53;

APOPTOSIS; CELL LINE, TUMOR; DNA BREAKS, DOUBLE-STRANDED; G2 PHASE CELL CYCLE CHECKPOINTS; HCT116 CELLS; HEAVY ION RADIOTHERAPY; HISTONES; HUMANS; M PHASE CELL CYCLE CHECKPOINTS; PHOSPHORYLATION; RADIATION, IONIZING; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84919800356     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0115121     Document Type: Article

References (36)

1. Schulz-Ertner D, Tsujii H (2007) Particle radiation therapy using proton and heavier ion beams. J Clin Oncol 25: 953-964.
2. Loeffler JS, Durante M (2013) Charged particle therapy-optimization, challenges and future directions. Nat Rev Clin Oncol 10: 411-424.
3. Yamada S (2014) Postoperative Recurrence of Rectal Cancer. In: Tsujii H, Kamada T, Shirai T, Noda K, Tsuji H, Karasawa K, editors. Carbon-Ion Radiotherapy: Principles, Practices, and Treatment Planning. Tokyo: Springer. pp. 203-209.
4. Ciatto S, Pacini P (1982) Radiation therapy for recurrences of carcinoma of the rectum and sigmoid after surgery. Acta Radiol Oncol 21: 105-109.
5. Mak RH, Doran E, Muzikansky A, Kang J, Neal JW, et al. (2011) Outcomes after combined modality therapy for EGFR-mutant and wild-type locally advanced NSCLC. Oncologist 16: 886-895.
6. Torres-Roca JF (2012) A molecular assay of tumor radiosensitivity: A roadmap towards biology-based personalized radiation therapy. Per Med 9: 547-557.
7. Ishikawa H, Mitsuhashi N, Sakurai H, Maebayashi K, Niibe H (2001) The effects of P53 status and human papillomavirus infection on the clinical outcome of patients with stage IIIB cervical carcinoma treated with radiation therapy alone. Cancer 91: 80-89.
8. Huerta S, Hrom J, Gao X, Saha D, Anthony T, et al. (2010) Tissue microarray constructs to predict a response to chemoradiation in rectal cancer. Dig Liver Dis 42: 679-684.
9. Giono LE, Manfredi JJ (2006) The p53 tumor suppressor participates in multiple cell cycle checkpoints. J Cell Physiol 209: 13-20.
10. Takahashi T, Fukawa T, Hirayama R, Yoshida Y, Musha A, et al. (2010) In vitro interaction of high-LET heavy-ion irradiation and chemotherapeutic agents in two cell lines with different radiosensitivities and different p53 status. Anticancer Res 30: 1961-1967.
11. Huerta S, Gao X, Dineen S, Kapur P, Saha D, et al. (2013) Role of p53, Bax, p21, and DNA-PKcs in radiation sensitivity of HCT-116 cells and xenografts. Surgery 154: 143-151.
12. Maalouf M, Alphonse G, Colliaux A, Beuve M, Trajkovic-Bodennec S, et al. (2009) Different mechanisms of cell death in radiosensitive and radioresistant p53 mutated head and neck squamous cell carcinoma cell lines exposed to carbon-ions and x-rays. Int J Radiat Oncol Biol Phys 74: 200-209.
13. Yamakawa N, Takahashi A, Mori E, Imai Y, Furusawa Y, et al. (2008) High LET radiation enhances apoptosis in mutated p53 cancer cells though Caspase-9 activation. Cancer Sci 99: 1455-1460.
14. Takahashi A, Matsumoto H, Yuki K, Yasumoto J, Kajiwara A, et al. (2004) High-LET radiation enhanced apoptosis but not necrosis regardless of p53 status. Int J Radiat Oncol Biol Phys 60: 591- 597.
15. Takahashi A, Ohnishi K, Ota I, Asakawa I, Tomamoto T, et al. (2001) p53-dependent thermal enhancement of cellular sensitivity in human spuamous cell carcinomas in relation to LET. Int J Radiat Biol 77: 1043-1051.
16. Bunz F, Dutriaux A, Lengauer C, Waldman T, Zhou S, et al. (1998) Requirement for p53 and p21 to sustain G2 arrest after DNA damage. Science 282: 1497-1501.
17. Kurioka D, Takeshita F, Tsuta K, Sakamoto H, Watanabe S, et al. (2014) NEK9-dependent proliferation of cancer cells lacking functional p53. Sci Rep 4: 6111.
18. Yamauchi M, Suzuki K, Oka Y, Suzuki M, Kondo H, et al. (2011) Mode of ATM-dependent suppression of chromosome translocation. Biochem Biophys Res Commun 416: 111-108.
19. Oike T, Ogiwara H, Torikai K, Nakano T, Yokota J, et al. (2012) Garcinol, a histone acetyltransferase inhibitor, radiosensitizes cancer cells by inhibiting non-homologous end joining. Int J Radiat Oncol Biol Phys 84: 815-821.
20. Oike T, Ogiwara H, Tominaga Y, Ito K, Ando O, et al. (2013) A synthetic lethality-based strategy to treat cancers harboring a genetic deficiency in the chromatin remodeling factor BRG1. Cancer Res 73: 5508- 5518.
21. Sawai Y, Murata H, Horii M, Koto K, Matsui T, et al. (2013) Effectiveness of sulforaphane as a radiosensitizer for murine osteosarcoma cells. Oncol Rep 29: 941-945.
22. Russo AL, Kwon HC, Burgan WE, Carter D, Beam K, et al. (2009) In vitro and in vivo radiosensitization of glioblastoma cells by the poly (ADP-ribose) polymerase inhibitor E7016. Clin Cancer Res 15: 607-612.
23. Di-Micco R, Sulli G, Dobreva M, Liontos M, Botrugno OA, et al. (2011) Interplay between oncogeneinduced DNA damage response and heterochromatin in senescence and cancer. Nat Cell Biol 13: 292- 302.
24. Nakajima Nl, Brunton H, Watanabe R, Shrikhande A, Hirayama R, et al. (2013) Visualisation of yH2AX foci caused by heavy ion particle traversal; distinction between core track versus non-track damage. PLoS One 8: e70107.
25. Bullock AN, Fersht AR (2001) Rescuing the function of mutant p53. Nat Rev Cancer 1: 68-76.
26. Wouters BG (2009) Cell death after irradiation: how, when and why cells die. In: Joiner M and van der Kogel A, editors. Basic Clinical Radiobiology. 4th ed. London: Hodder Education. pp. 27-40.
27. Hall EJ, Giaccia AJ (2006) DNA strand breaks and chromosomal aberrations. In: McAllister L ed. Radiobiology for the radiologist. 6th ed. Philadelphia: Lippincott Williams & Wilkins. pp. 16-29.
28. Lobrich M, Shibata A, Beucher A, Fisher A, Ensminger M, et al. (2010) cH2AX foci analysis for monitoring DNA double-strand break repair: Strengths, limitations and optimization. Cell Cycle 9: 662- 669.
29. Shibata A, Conrad S, Birraux J, Geuting V, Barton O, et al. (2011) Factors determining DNA doublestrand break repair pathway choice in G2 phase. EMBO J 30: 1079-1092.
30. Bucher N and Britten CD (2008) G2 checkpoint abrogation and checkpoint kinase-1 targeting in the treatment of cancer. Br J Cancer 98: 523-528.
31. Deckbar D, Jeggo PA, Lobrich M (2011) Understanding the limitations of radiation-induced cell cycle checkpoints. Crit Rev Biochem Mol Biol 46: 271-283.
32. Lukas C, Savic V, Bekker-Jensen S, Doil C, Neumann B, et al. (2011) 53BP1 nuclear bodies form around DNA lesions generated by mitotic transmission of chromosomes under replication stress. Nat Cell Biol 13: 243-253.
33. Harrigan JA, Belotserkovskaya R, Coates J, Dimitrova DS, Polo SE, et al. (2011) Replication stress induces 53BP1-containing OPT domains in G1 cells. J Cell Biol 193: 97-108.
34. Giunta S, Belotserkovskaya R, Jackson SP (2010) DNA damage signaling in response to doublestrand breaks during mitosis. J Cell Biol 190: 197-207.
35. Terato H, Ide H (2004) Clustered DNA damage induced by heavy ion particles. Biol Sci Space 18: 206- 215.
36. Oishi T, Sasaki A, Hamada N, Ishiuchi S, Funayama T, et al. (2008) Proliferation and cell death of human glioblastoma cells after carbon-ion beam exposure: Morphologic and morphometric analyses. Neuropathology 28: 408-416.