Irradiation With Carbon Ion Beams Induces Apoptosis, Autophagy, and Cellular Senescence in a Human Glioma-Derived Cell Line

International Journal of Radiation Oncology Biology Physics

Volumn 76, Issue 1, 2010, Pages 229-241

  Jinno Oue, Atsushi ^a,b   Shimizu, Nobuaki ^a,b   Hamada, Nobuyuki ^a,b,c   Wada, Seiichi ^a,b,c   Tanaka, Atsushi ^a,b   Shinagawa, Masahiko ^a,b   Ohtsuki, Takahiro ^a,b   Mori, Takahisa ^a,b   Saha, Manujendra N ^a,b   Hoque, Ariful S ^a,b   Islam, Salequl ^a,b   Kogure, Kimitaka ^a   Funayama, Tomoo ^c   Kobayashi, Yasuhiko ^a,b,c   Hoshino, Hiroo ^a,b  

^a GUNMA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b Development Center for Targeted and Minimally Invasive Diagnosis and Treatment   (Japan)

^c Quantum Beam Science Directorate   (Japan)

Author keywords

Apoptosis; Autophagy; Cellular senescence; Glioma; Heavy ion beam; p53

Indexed keywords

APOPTOSIS; APOPTOTIC CELLS; AUTOPHAGY; BIOLOGICAL RESPONSE; CARBON ION BEAMS; CELL LINES; CELLULAR SENESCENCE; GALACTOSIDASES; GLIOMA CELL LINES; GLIOMA CELLS; HOECHST; INDUCED APOPTOSIS; KINASE INHIBITORS; LIGHT CHAIN; MEMBRANE-BOUND; MONODANSYLCADAVERINE; RESIDUAL FRACTION; SOUTHERN BLOT HYBRIDIZATION; TELOMERE LENGTH; TUMOR SUPPRESSORS; WESTERN BLOTTING;

AMINO ACIDS; BEAM PLASMA INTERACTIONS; CELL CULTURE; CELL DEATH; CHROMOSOMES; INERTIAL CONFINEMENT FUSION; ION BEAMS; ION BOMBARDMENT; RADIATION; SIMULATED ANNEALING;

HEAVY IONS;

BETA GALACTOSIDASE; CARBON; DANSYLCADAVERINE; MICROTUBULE ASSOCIATED PROTEIN; MICROTUBULE ASSOCIATED PROTEIN LIGHT CHAIN 3; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; AUTOPHAGY; CANCER RADIOTHERAPY; CELL AGING; CELL LINE; GLIOMA; HUMAN; HUMAN CELL; ION THERAPY; PRIORITY JOURNAL; RADIATION DOSE; SOUTHERN BLOTTING; WESTERN BLOTTING;

APOPTOSIS; AUTOPHAGY; BETA-GALACTOSIDASE; CARBON; CELL AGING; CELL LINE, TUMOR; COLONY-FORMING UNITS ASSAY; CYCLIN-DEPENDENT KINASE INHIBITOR P21; GLIOMA; HEAVY IONS; HUMANS; MICROTUBULE-ASSOCIATED PROTEINS; TELOMERE; TUMOR SUPPRESSOR PROTEIN P53;

EID: 72049102608     PISSN: 03603016     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ijrobp.2009.08.054     Document Type: Article

References (40)

1. Kramer M., Weyrather W.K., and Scholz M. The increased biological effectiveness of heavy charged particles: From radiobiology to treatment planning. Technol Cancer Res Treat 2 (2003) 427-436
2. Tsujii H., Mizoe J., Kamada T., et al. Overview of clinical experiences on carbon ion radiotherapy at NIRS. Radiother Oncol 73 (2004) S41-S49
3. Hamada N. Recent insights into the biological action of heavy-ion radiation. J Radiat Res 50 (2009) 1-9
4. Iwadate Y., Mizoe J.-E., Osaka Y., et al. High linear energy transfer carbon radiation effectively kills cultured glioma cells with either mutant or wild-type p53. Int J Radiat Oncol Biol Phys 50 (2001) 803-808
5. Tsuboi K., Moritake T., Tsuchida Y., et al. Cell cycle checkpoint and apoptosis induction in glioblastoma cells and fibroblasts irradiated with carbon beam. J Radiat Res 48 (2007) 317-325
6. Wada S., Kobayashi Y., Funayama T., et al. Detection of DNA damage in individual cells induced by heavy-ion irradiation with a non-denaturing comet assay. J Radiat Res 43 (2002) S153-S156
7. Ito H., Daido S., Kanzawa T., et al. Radiation-induced autophagy is associated with LC3 and its inhibition sensitizes malignant glioma cells. Int J Oncol 26 (2005) 1401-1410
8. Suzuki M., and Boothman D.A. Stress-induced premature senescence (SIPS)-influence of SIPS on radiotherapy. J Radiat Res 49 (2008) 105-112
9. Hamada N., Funayama T., Wada S., et al. LET-dependent survival of irradiated normal human fibroblasts and their descendents. Radiat Res 166 (2006) 24-30
10. Biederbick A., Kern H.F., and Elasser H.P. Monodansylcadaverine (MDC) is a specific in vivo marker for autophagic vacuoles. Eur J Cell Biol 66 (1995) 3-14
11. Munafo D.B., and Colombo M.I. A novel assay to study autophagy: Regulation of autophagosome vacuole size by amino acid deprivation. J Cell Sci 114 (2001) 3619-3629
12. Seglen P.O., and Gordon P.B. 3-Methyladenine: Specific inhibitor of autophagic/lysosomal protein degradation in isolated rat hepatocytes. Proc Natl Acad Sci U S A 79 (1982) 1889-1892
13. Kabeya Y., Mizushima N., Ueno T., et al. LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO J 19 (2000) 5720-5728
14. Dimri G.P., Lee X., Basile G., et al. A biomarker that identifies senescent human cells in culture and in aging skin. in vivo. Proc Natl Acad Sci U S A 26 (1995) 9363-9367
15. Bancroft J.D. An introduction to histochemical techniques (1967), Butterworths, London p148-175
16. Baur J.A., Wright W.E., and Shay J.W. Analysis of mammalian telomere position effect. Methods Mol Biol 287 (2004) 121-136
17. Gozuacilk D., and Kimchi A. Autophagy as a cell death and tumor suppressor mechanism. Oncogene 23 (2004) 2891-2896
18. Ben-Porath I., and Weinberg R.A. The signals and pathways activating cellular senescence. Int J Biochem Cell Biol 37 (2005) 961-976
19. Mathon N.F., and Lloyd A.C. Cell senescence and cancer. Nat Rev Cancer 1 (2001) 203-213
20. Toussaint O., Medrano E.E., and von Zglinicki T. Cellular and molecular mechanisms of stress-induced premature senescence (SIPS) of human diploid fibroblasts and melanocytes. Exp Gerontol 35 (2000) 927-945
21. Kurz D.J., Decary S., Hong Y., et al. Senescence-associated β-galactosidase reflects an increase in lysosomal mass during replicative ageing of human endothelial cells. J Cell Sci 113 (2000) 3613-3622
22. Brunk U.T., and Terman A. Lipofuscin: Mechanisms of age-related accumulation and influence on cell function. Free Radic Biol Med 33 (2002) 611-619
23. Van Meir E.G., Kikuchi T., Tada M., et al. Analysis of the p53 gene and its expression in human glioblastoma cells. Cancer Res 54 (1994) 649-652
24. Xin M.G., Zhang J., Block E.R., et al. Senescence-enhanced oxidative stress is associated with deficiency of mitochondrial cytochrome c oxidase in vascular endothelial cells. Mech Ageing Dev 124 (2003) 911-919
25. Halliwell B., and Whiteman M. Measuring reactive species and oxidative damage in vivo and in cell culture: How should you do it and what do the results mean?. Br J Pharmacol 142 (2004) 231-235
26. Maiuri M.C., Zalckvar E., Kimchi A., et al. Self-eating and self-killing: Crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol 8 (2007) 741-752
27. Jones K., Elemore L., Jackson-Cook C., et al. p53-Dependent accelerated senescence induced by ionizing radiation in breast tumour cells. Int J Radiat Biol 81 (2005) 445-458
28. Flint J., Craddock C.F., Villegas A., et al. Healing of broken human chromosomes by the addition of telomeric repeats. Am J Hum Genet 55 (1994) 505-512
29. Sgura A., Antoccia A., Berardinelli F., et al. Telomere length in mammalian cells exposed to low- and high-LET radiations. Radiat Prot Dosim 122 (2006) 176-179
30. Hande M.P., Lansdorp P.M., and Natarajan A.T. Induction of telomerase activity by in vivo X-irradiation of mouse splenocytes and its possible role in chromosome healing. Mutat Res 404 (1998) 205-214
31. Hyeon Joo O., Hande M.P., Lansdorp P.M., et al. Induction of telomerase activity and chromosome aberrations in human tumour cell lines following X-irradiation. Mutat Res 401 (1998) 121-131
32. Ayouaz A., Raynaud C., Heride C., et al. Telomeres: Hallmarks of radiosensitivity. Biochimie 90 (2008) 60-72
33. Mirzayans R., Scott A., Cameron M., et al. Induction of accelerated senescence by gamma radiation in human solid tumor-derived cell lines expressing wild-type TP53. Radiat Res 163 (2005) 53-62
34. Suzuki K., Mori I., Nakayama Y., et al. Radiation-induced senescence-like growth arrest requires TP53 function but not telomere shortening. Radiat Res 155 (2001) 248-253
35. Sugrue M.M., Shin D.Y., Lee S.W., et al. Wild-type p53 triggers a rapid senescence program in human tumor cells lacking functional p53. Proc Natl Acad Sci U S A 94 (1997) 9648-9653
36. waf1/cip1 in senescence-like terminal proliferation arrest induced in human tumor cells by chemotherapeutic drugs. Oncogene 18 (1999) 4808-4818
37. von Zglinicki T., Saretzki G., and Ladhoff J. Human cell senescence as a DNA damage response. Mech Ageing Dev 126 (2005) 111-117
38. Kurz T., Terman A., and Brunk U.T. The role of oxidative stress and lysosomal iron. Arch Biochem Biophys 462 (2007) 220-230
39. Mizoe J.E., Tsujii H., Hasegawa A., et al. Phase I/II clinical trial of carbon ion radiotherapy for malignant gliomas: Combined X-ray radiotherapy, chemotherapy, and carbon ion radiotherapy. Int J Radiat Oncol Biol Phys 69 (2007) 390-396
40. Tsujii H., Mizoe J.E., Kamada T., et al. Overview of clinical experiences on carbon ion radiotherapy at NIRS. Radiother Oncol 73 Suppl 2 (2004) S41-S49