Biology of charged particles

Cancer Journal

Volumn 15, Issue 4, 2009, Pages 271-284

  Blakely, Eleanor A ^a   Chang, Polly Y ^b  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

^b SRI INTERNATIONAL   (United States)

Author keywords

Carbon ions; Charged particles; Heavy ion radiobiology; High linear energy transfer effects; Mechanisms underlying particle effects; Particle radiotherapy; Particle treatment planning; Protons; Translational biology

Indexed keywords

ARGON; CARBON; HELIUM; NEON; PROTON; SILICON; URANIUM;

CANCER CELL; CELL SURVIVAL; CHARGED PARTICLE; DRUG MECHANISM; HARDER GLAND; ION THERAPY; LINEAR ENERGY TRANSFER; MAMMARY GLAND; MATERIAL STATE; NONHUMAN; OXYGEN ENHANCEMENT RATIO; PHOTON; PHYSICAL MODEL; PRIORITY JOURNAL; RADIATION DEPTH DOSE; RADIATION DOSE FRACTIONATION; RELATIVE BIOLOGIC EFFECTIVENESS; REVIEW; SECOND CANCER; SKIN DEFECT; TREATMENT PLANNING; TUMOR MODEL;

DOSE-RESPONSE RELATIONSHIP, RADIATION; GENOMICS; HEALTH PHYSICS; HUMANS; IONS; NEOPLASMS; PARTICLE SIZE; PROTEOMICS; PROTONS; RELATIVE BIOLOGICAL EFFECTIVENESS; TRANSLATIONAL RESEARCH;

EID: 69549090258     PISSN: 15289117     EISSN: 1540336X     Source Type: Journal    
DOI: 10.1097/PPO.0b013e3181b666c5     Document Type: Review

References (142)

1. Rutherford E, Chadwick J, and Ellis CD. Radiations From Radioactive Substances. Cambridge: University Press; 1930.
2. Hall E. Protons for radiotherapy: a 1946 proposal. Lancet Oncol. 2009;10:196.
3. Welsh JS. Basics of particle therapy: introduction to hadrons. Am J Clin Oncol. 2008;31:493-495.
4. Weinburg S. A model of leptons. Phys Rev Lett. 1967;19:1264-1266.
5. Ashikawa JK, Sondhaus CA, Tohias CA, et al. Acute effects of high-energy protons and alpha particles in mice. Radiat Res. 1967;7:312-324.
6. Hall EJ, Kellerer AM, Rossi HH, et al. The relative biological effectiveness of 160 MeV protons. II. Biological data and their interpretation in terms of microdosimetry. Int J Radiat Oncol Biol Phys. 1978;4:1009-1013.
7. Raju MR, Amols HI, Bain E, et al. A heavy particle comparative study. Part III: OER and RBE. Br J Radiol. 1978;51:712-719. (Pubitemid 9019162)
8. Raju MR, Amols HI, Dicello JF, et al. A heavy particle comparative study. Part I: depth-dose distributions. Br J Radiol. 1978;51:699-703. (Pubitemid 9019160)
9. Raju MR, Bain E, Carpenter SG, et al. A heavy particle comparative study. Part II: cell survival versus depth. Br J Radiol. 1978;51:704-711. (Pubitemid 9019161)
10. Raju MR, Carpenter SG. A heavy particle comparative study. Part IV: acute and late reactions. Br J Radiol. 1978;51:720-727. (Pubitemid 9019163)
11. Robertson JB, Williams JR, Schmidt RA, et al. Radiobiological studies of a high-energy modulated proton beam utilizing cultured mammalian cells. Cancer. 1975;35:1664-1677.
12. Tepper J, Verhey L, Goitein M, et al. In vivo determinations of RBE in a high energy modulated proton beam using normal tissue reactions and fractionated dose schedules. Int J Radiat Oncol Biol Phys. 1977;2:1115-1122. (Pubitemid 8247876)
13. Tobias CA, Anger HO, Lawrence JH. Radiological use of high energy deuterons and alpha particles. Am J Roentgenol Radium Ther Nucl Med. 1952;67:1-27.
14. Falkmer S, Larsson B, Stenson S. Effects of single dose proton irradiation of normal skin and Vx2 carcinoma in rabbit ears: a comparative investigation with protons and roentgen rays. Acta radiol. 1959;52:217-234.
15. Larsson B. Blood vessel changes following local irradiation of the brain with high-energy protons. Acta Soc Med Ups. 1960;65:51-71.
16. Larsson B, Graffman S, Jung B. Fixation of carbon-11 in the cells of proton-irradiated blood. Nature. 1965;207:543-544.
17. Stenson S. Weight change and mortality of rats after abdominal proton and roentgen irradiation. A comparative investigation. Acta Radiol Ther Phys Biol. 1969;8:423-432.
18. Stenson S. Effects of proton and roentgen radiation on the rectum of the rat. Acta Radiol Ther Phys Biol. 1969;8:263-278.
19. Ueno Y, Grigoriev YG. The RBE of protons with energy greater than 126 MeV. Br J Radiol. 1969;42:475.
20. Wainson AA, Lomanov MF, Shmakova NL, et al. The RBE of accelerated protons in different parts of the Bragg curve. Br J Radiol. 1972;45:525-529.
21. Sayeg JA, Birge AC, Beam CA, et al. The effects of accelerated carbon nuclei and other radiations on the survival of haploid yeast. II. Biological experiments. Radiat Res. 1959;10:449-461.
22. Tobias CA, Todd PW. Heavy charged particles in cancer therapy. Natl Cancer Inst Monogr. 1967;24:1-21.
23. Tobias CA, Lyman JT, Chatterjee A, et al. Radiological physics characteristics of the extracted heavy ion beams of the bevatron. Science. 1971;174:1131-1134.
24. Tobias CA, Lyman JT, Lawrence JH. Some considerations of physical and biological factors in radiotherapy with high-LET radiations including heavy particles, pi mesons, and fast neutrons. Prog At Med. 1971;3:167-218.
25. Tobias CA. Pretherapeutic investigations with accelerated heavy ions. Radiology. 1973;108:145-158.
26. White MG, Isaila M, Prelec K, et al. Acceleration of nitrogen ions to 7.4 Gev in the Princeton Particle accelerator. Science. 1971;174:1121-1123.
27. Grunder HA, Hartsough WD, Lofgren EJ. Acceleration of heavy ions at the Bevatron. Science. 1971;174:1128-1129.
28. Ghiorso A, Grunder H, Hartsough W, et al. The bevalac: an economical facility for very high energetic heavy particle research. IEEE Trans Nucl Sci NS. 1973;20:155.
29. Tobias CA, Tobias I. People and Particles. San Francisco: San Francisco Press Inc.; 1997.
30. Llacer J, Schmidt JB, Tobias CA. Characterization of fragmented heavy-ion beams using a three-stage telescope detector: detector configuration and instrumentation. Med Phys. 1990;17:158-162. (Pubitemid 20140132)
31. Llacer J, Schmidt JB, Tobias CA. Characterization of fragmented heavy-ion beams using a three-stage telescope detector: measurements of 670-MeV/amu 20Ne beams. Med Phys. 1990;17:151-157. (Pubitemid 20140131)
32. Castro JR, Petti PL, Daftari IK, et al. Clinical gain from improved beam delivery systems. Radiat Environ Biophys. 1992;31:233-240.
33. Ludewigt B. Beam spreading methods. In: Linz U, Chapman J, Hall E, eds. Ion Beams in Tumor Therapy. Weinbheim, Germany: Chapman and Hall; 1995.
34. Renner TR, Chu WT. Wobbler facility for biomedical experiments. Med Phys. 1987;14:825-834.
35. ICRU. International Commission on Radiation Units and Measurements. North Carolina: Oxford University Press; 1986.
36. IAEA/ICRU. Relative Biological Effectiveness in Ion Beam Therapy. 2008; TRS 461.
37. Linz U, ed. Ion Beams in Tumor Therapy. Weinheim: Chapman and Hall; 1995.
38. Raju MR. Heavy-Particle Radiotherapy. New York: Academic Press; 1980.
39. Skarsgard L, ed. Pion and Heavy Ion Radiotherapy. Amsterdam: Elsevier Biomedical; 1983.
40. Blakely EA, Ngo FQH, Curtis SB, et al. Heavy-ion radiobiology: cellular studies. Adv Radiat Biol. 1984;11:195-389.
41. Leith JT, Ainsworth J, Alpen E. Heavy ion radiobiology: normal tissue studies. Adv Radiat Biol. 1983;10:191.
42. Belli M, Cera F, Cherubini R, et al. Inactivation and mutation induction in V79 cells by low energy protons: re-evaluation of the results at the LNL facility. Int J Radiat Biol. 1993;63:331-337. (Pubitemid 23076215)
43. Wambersie A, Hendry JH, Andreo P, et al. The RBE issues in ion-beam therapy: conclusions of a joint IAEA/ICRU working group regarding quantities and units. Radiat Prot Dosimetry. 2006;122:463-470. (Pubitemid 47090504)
44. Paganetti H, Niemierko A, Ancukiewicz M, et al. Relative biological effectiveness (RBE) values for proton beam therapy. Int J Radiat Oncol Biol Phys. 2002;53:407-421. (Pubitemid 34522107)
45. Paganetti H. Significance and implementation of RBE variations in proton beam therapy. Technol Cancer Res Treat. 2003;2:413-426. (Pubitemid 37362998)
46. Gerweck LE, Kozin SV. Relative biological effectiveness of proton beams in clinical therapy. Radiother Oncol. 1999;50:135-142.
47. Tilly N, Johansson J, Isacsson U, et al. The influence of RBE variations in a clinical proton treatment plan for a hypopharynx cancer. Phys Med Biol. 2005;50:2765-2777. (Pubitemid 40771010)
48. Paganetti H. Interpretation of proton relative biological effectiveness using lesion induction, lesion repair, and cellular dose distribution. Med Phys. 2005;32:2548-2556. (Pubitemid 41197192)
49. Curtis SB. Lethal and potentially lethal lesions induced by radiation - a unified repair model. Radiat Res. 1986;106:252-270.
50. Dicello JF. Absorption characteristics of protons and photons in tissue. Technol Cancer Res Treat. 2007;6(4 Suppl):25-29.
51. Endo S, Takada M, Onizuka Y, et al. Microdosimetric evaluation of secondary particles in a phantom produced by carbon 290 MeV/nucleon ions at HIMAC. J Radiat Res (Tokyo). 2007;48:397-406. (Pubitemid 47451251)
52. Uzawa A, Ando K, Koike S, et al. Comparison of biological effectiveness of carbon-ion beams in Japan and Germany. Int J Radiat Oncol Biol Phys. 2009;73:1545-1551.
53. Deleted in proof.
54. Lyman JT. Computer modeling of heavy charged-particle beams. In: LD Skarsgard, ed. Pion and Heavy Ion Radiotherapy: Preclinical and Clinical Studies. Amsterdam: Elsevier; 1983:139-148.
55. Tobias CA, Blakely EA, Ngo FQH, et al. The repair-misrepair model of cell survival. In: Meyn RE, Withers HR, eds. Radiation Biology and Cancer. New York: Raven; 1980:195-230.
56. Furusawa Y, Fukutsu K, Aoki M, et al. Inactivation of aerobic and hypoxic cells from three different cell lines by accelerated (3)He-, (12)C- and (20)Ne-ion beams. Radiat Res. 2000;154:485-496. (Pubitemid 30836536)
57. Kanai T, Endo M, Minohara S, et al. Biophysical characteristics of HIMAC clinical irradiation system for heavy-ion radiation therapy. Int J Radiat Oncol Biol Phys. 1999;44:201-210. (Pubitemid 29186209)
58. Kraft G. Tumor therapy with heavy charged particles. Prog Particle Nuclear Phys. 2000;45:S473-S544. (Pubitemid 32076531)
59. Kraft G, Scholz M, Bechthold U. Tumor therapy and track structure. Radiat Environ Biophys. 1999;38:229-237.
60. Weyrather WK, Debus J. Particle beams for cancer therapy. Clin Oncol. 2003;15:S23-S28.
61. Weyrather WK, Kraft G. RBE of carbon ions: experimental data and the strategy of RBE calculation for treatment planning. Radiother Oncol. 2004;73(Suppl 2):S161-S169. (Pubitemid 41219141)
62. Weyrather WK, Ritter S, Scholz M, et al. RBE for carbon track-segment irradiation in cell lines of differing repair capacity. Int J Radiat Biol. 1999;75:1357-1364.
63. Tobias CA, et al. Tracks in Condensed Systems. Proceedings Sixth International Congress of Radiation Research. In: 6th International Congress of Radiation Research. Tokyo, Japan: Japanese Association for Radaition Research; 1979.
64. Chatterjee A, Maccabee HD, Tobias CA. Radial cutoff LET and radial cutoff dose calculations for heavy charged particles in water. Radiat Res. 1973;54:479-494.
65. Chatterjee A, Holly WR. Computer simulation of initial events in the biochemical mechanisms of DNA damage. Adv Radiat Biol. 1993;17:181-226.
66. Wilson W, Toburen LH, Miller JH, et al. Cross sections used in proton track simulations. In: Workshop on Electronic and Ionic Collision Cross Sections needed in the modeling of Radiation Interactions with Matter. Argonne, IL: Argonne National Laboratory; 1984.
67. Charlton DE, Goodhead DT, Wilson WE, et al. Energy deposition in cylindrical volumes; 1) protons energy 0.3-4.0
68. Wilson WE, Miller JH, Nikjpoo H. PITTS: a code for positive ion track structure. In: Varma MN, Chatterjee A, eds.Computational Approaches in Molecular Biology - Monte Carlo Methods. New York: Plenum Press; 1993.
69. Cucinotta FA, Nikjoo H, Goodhead DT. Model for radial dependence of frequency distributions for energy imparted in nanometer volumes from HZE particles. Radiat Res. 2000;153:459-468. (Pubitemid 30185401)
70. Chatterjee A, Holley WR. Biochemical mechanisms and clusters of damage for high-LET radiation. Adv Space Res. 1992;12:33-43.
71. Ngo FQH. Effects on mammalian cells of fractionated heavy-ion doses. In: L. Skarsgard, ed. Pion and Heavy-Ion Radiotherapy: Preclinical and Clinical Studies. New York: Elsevier Science Publishing; 1982.
72. Bohrnsen G, Weber KJ, Scholz M. Measurement of biological effects of high-energy carbon ions at low doses using a semi-automated cell detection system. Int J Radiat Biol. 2002;78:259-266 (Pubitemid 34293345)
73. Andreo P. On the clinical spatial resolution achievable with protons and heavier charged particle radiotherapy beams. Phys Med Biol. 2009;54:N205-N215.
74. Kanai T, Furusawa Y, Fukutsu K, et al. Irradiation of mixed beam and design of spread-out Bragg peak for heavy-ion radiotherapy. Radiat Res. 1997;147:78-85. (Pubitemid 27014450)
75. Kellerer AM, Rossi HH. A generalized formation of dual radiation action. Radiat Res. 1978;75:471-488.
76. Zaider M, Rossi HH. The synergistic effects of different radiations. Radiat Res. 1980;83:732-739.
77. Kase Y, Kanai T, Matsumoto Y, et al. Microdosimetric measurements and estimation of human cell survival for heavy-ion beams. Radiat Res. 2006;166:629-638. (Pubitemid 44477716)
78. Scholz M, Kraft G. The physical and radiobiological basis of the local effect model: a response to the commentary by R. Katz. Radiat Res. 2004;161:612-620. (Pubitemid 40754232)
79. Combs SE, Bohl J, Elsässer T, et al. Radiobiological evaluation and correlation with the local effect model (LEM) of carbon ion radiation therapy and temozolomide in glioblastoma cell lines. Int J Radiat Biol. 2009;85:126-137.
80. Elsasser T, Kramer M, Scholz M. Accuracy of the local effect model for the prediction of biologic effects of carbon ion beams in vitro and in vivo. Int J Radiat Oncol Biol Phys. 2008;71:866-872.
81. Elsasser T, Scholz M. Cluster effects within the local effect model. Radiat Res. 2007;167:319-329. (Pubitemid 351292544)
82. Gemmel A, Hasch B, Ellerbrock M, et al. Biological dose optimization with multiple ion fields. Phys Med Biol. 2008;53:6991-7012.
83. Kase Y, Kanai T, Matsufuji N, et al. Biophysical calculation of cell survival probabilities using amorphous track structure models for heavy-ion irradiation. Phys Med Biol. 2008;53:37-59.
84. Kramer M, et al. Treatment planning for scanned ion beams. Radiother Oncol. 2004;73:S80-S85. (Pubitemid 41219121)
85. Kramer M, Scholz M. Rapid calculation of biological effects in ion radiotherapy. Phys Med Biol. 2006;51:1959-1970.
86. Scholz M, Matsufuji N, Kanai T. Test of the local effect model using clinical data: tumour control probability for lung tumours after treatment with carbon ion beams. Radiat Prot Dosimetry. 2006;122:478-479. (Pubitemid 47090507)
87. Tobias CM. Failla Memorial Lecture: the future of heavy ion science in biology and medicine. Radiat Res. 1985;103:1-33.
88. Xu XG, Bednarz B, Paganetti H. A review of dosimetry studies on external-beam radiation treatment with respect to second cancer induction. Phys Med Biol. 2008;53:R193-R241. (Pubitemid 352020053)
89. National Council for Radiation Protection and Measurements. Information Needed to Make Radiation Protection Recommendations for Space Missions Beyond Low-Earth Orbit. Report # 153. Bethesda, MD: National Council for Radiation Protection and Measurements; 2006.
90. Goldberg Z, Schwietert CW, Lehnert B, et al. Effects of low-dose ionizing radiation on gene expression in human skin biopsies. Int J Radiat Oncol Biol Phys. 2004;58:567-574. (Pubitemid 38142485)
91. Costes S, Streuli CH, Barcellos-Hoff MH. Quantitative image analysis of laminin immunoreactivity in skin basement membrane irradiated with 1 GeV/nucleon iron particles. Radiat Res. 2000;154:389-397. (Pubitemid 30749647)
92. Leith JT, Lewinsky BS, Schilling WA. Modification of the response of mouse skin to x-irradiation by bleomycin treatment. Radiat Res. 1975;61:100-109.
93. Leith JT, McDonald M, Howard J. Residual skin damage in rats 1 year after exposure to X rays or accelerated heavy ions. Radiat Res. 1982;89:209-213. (Pubitemid 12207935)
94. Leith JT, Powers-Risius P, Woodruff KH, et al. Response of the skin of hamsters to fractionated irradiation with X rays or accelerated carbon ions. Radiat Res. 1981;88:565-576. (Pubitemid 12242616)
95. Leith JT, Lewinsky BS, Schilling WA. Comparison of skin responses of mice after single or fractionated exposure to cyclotron-accelerated helium ions and 230 kv x-irradiation. Radiat Res. 1975;62:195-215.
96. Blakely EA, Tobias CA, Ngo FQH, et al. Comparison of helium and heavy ion beams for therapy based on cellular radiobiological data. Int J Radiat Oncol Biol Phys. 1978;4(suppl 2):93-94. Abstract.
97. Blakely EA, Tobias CA, Yang TCH, et al. Inactivation of human kidney cells by high-energy monoenergetic heavy-ion beams. Radiat Res. 1979;80:122-160.
98. Blakely EA, Tobias CA, Ngo FQH, et al. In: Pirruccecllo MC, Tobias CA, eds. Biological and Medical Research With Accelerated Heavy Ions at the Bevalac. Lawrence Berkeley Laboratory, LBL 11220; 1980: 73-86.
99. Lucke-Huhle C, Blakely EA, Chang PY, et al. Drastic G2 arrest in mammalian cells after irradiation with heavy-ion beams. Radiat Res. 1979;79:97-112.
100. Ngo FQH, Blakely EA, Tobias CA. Sequential exposures of mammalian cells to low- and high-LET radiations: I: lethal effects following x-ray and neon-ion irradiation. Radiat Res. 1981;87:59-78.
101. Roots R, Yang TC, Craise L, et al. Rejoining capacity of DNA breaks induced by accelerated carbon and neon ions in the spread Bragg peak. Int J Radiat Biol. 1980;38:203-210.
102. Chapman JD, Blakely EA, Smith KC, et al. Radiobiological characterization of the inactivating events produced in mammalian cells by helium and heavy ions. Int J Radiat Oncol Biol Phys. 1977;3:97-102.
103. Curtis SB, Schilling WA, Tenforde TS, et al. Survival of oxygenated and hypoxic tumor cells in the extended-peak regions of heavy charged-particle beams. Radiat Res. 1982;90:292-309.
104. Yang TCH, Blakely EA, Chatterjee A, et al. Response of cultured mammalian cells to accelerated krypton particles. Life Sci Space Res. 1977;87:511-520.
105. Goldstein LS, Phillips TL, Ross GY. Biological effects of accelerated heavy ions: II: fractionated irradiation of intestinal crypt cells. Radiat Res. 1981;86:529-541.
106. Leith JT, Woodruff KH, Howard J, Lyman JT, et al. Early and late effects of accelerated charged particles on normal tissues. Int J Radiat Oncol Biol Phys. 1977;3:103-108. (Pubitemid 8344735)
107. Blakely E, Castro JR. Assessment of acute and late effects to high-LET radiation. Proceedings of National Institute of Radiological Sciences: International Seminar on the Application of Heavy Ion accelerator to Radiation Therapy of Cancer, nirs-m-103/himac-008. National Institute of Radiological Research, Chiba, Japan, 1994:149-157.
108. Field SB. An historical survey of radiobiology and radiotherapy with fast neutrons. Curr Top Radiat Res.1976;11:1-86.
109. Burns FJ, Albert RE. Dose response for skin tumors induced by single and split doses of argon ions. In: Pirruccello MC, Tobias CA, eds. Biological and Medical Research with Accelerated Heavy Ions. Berkeley, CA: Lawrence Berkeley Laboratory, LBL11220; 1980.
110. Burns FJ, et al. High-LET radiation-induced malignant and benign tumors in rat skin. In: Suzuki M, ed. Risk Evaluation of Cosmic-Ray Exposure in Long-Term Nammed Space Mission. Tokyo: Kodansha Scientific Ltd.; 1999:109-119.
111. Burns FJ, Zhao P, Xu G, et al. Fibroma induction in rat skin following single or multiple doses of 1.0 GeV/nucleon 56Fe ions from the Brookhaven Alternating Gradient Synchrotron (AGS). Phys Med. 2001;17(Suppl 1):194-195. (Pubitemid 32823679)
112. Heimbach RD, Burns FJ, Albert RE. An evaluation by alpha-particle Bragg peak radiation of the critical depth in the rat skin for tumor induction. Radiat Res. 1969;39:332-344.
113. Ayala MN, Soderberg PG. Vitamin E can protect against ultraviolet radiation-induced cataract in albino rats. Ophthalmic Res. 2004;36:264-269.
114. Karslioglu I, Ertekin MV, Koçer I, et al. Protective role of intramuscularly administered vitamin E on the levels of lipid peroxidation and the activities of antioxidant enzymes in the lens of rats made cataractous with gamma-irradiation. Eur J Ophthalmol. 2004;14:478-485. (Pubitemid 40136573)
115. Fry RJ, Powers-Risius P, Alpen EL, et al. High-LET radiation carcinogenesis. Adv Space Res. 1983;3:241-248.
116. Alpen EL, Powers-Risius P, Curtis SB, et al. Fluence-based relative biological effectiveness for charged particle carcinogenesis in mouse Harderian gland. Adv Space Res. 1994;14:573-581.
117. Curtis SB, Townsend LW, Wilson JW, et al. Fluence-related risk coefficients using the Harderian gland data as an example. Adv Space Res. 1992;12:407-416.
118. Curtis SB, Nealy JE, Wilson JW. Risk cross sections and their application to risk estimation in the galactic cosmic-ray environment. Radiat Res. 1995;141:57-65.
119. NCRP, Fluence-Based and Microdosimetric Event-based Methods for Radiation Protection in Space, in NCRP Report # 137. National Council for Radiation Protection and Measurements: Bethesda, MD, 2001.
120. Dicello JF, Christian A, Cucinotta FA, et al. In vivo mammary tumourigenesis in the Sprague-Dawley rat and microdosimetric correlates. Phys Med Biol. 2004;49:3817-3830. (Pubitemid 39206459)
121. Tubiana M. Can we reduce the incidence of second primary malignancies occurring after radiotherapy? A critical review. Radiother Oncol. 2009;91:4-15; discussion 1-3.
122. Ianzini F, Mackey M, Mitotic catastophe. In: Gewirtz DA, Holt SE, Grant S, eds. Apoptosis, Senescence and Cancer. 2nd ed. Totowa, New Jersey: Humana Press; 2007:73-91.
123. Mizushima N, Levine B, Cuervo AM, et al. Autophagy fights disease through cellular self-digestion. Nature. 2008;451:1069-1075. (Pubitemid 351317450)
124. Pirtoli L, Cevenini G, Tini P, et al. The prognostic role of beclin 1 protein expression in high-grade gliomas. Autophagy.
125. Fournier C, Wiese C, Taucher-Scholz G. Accumulation of the cell cycle regulators TP53 and CDKN1A (p21) in human fibroblasts after exposure to low- and high-LET radiation. Radiat Res. 2004;161:675-684. (Pubitemid 39149576)
126. Jakob B, Scholz M, Taucher-Scholz G. Biological imaging of heavy charged-particle tracks. Radiat Res. 2003;159:676-684. (Pubitemid 36539248)
127. Chang PY, Bjornstad KA, Rosen CJ, et al. Effects of iron ions, protons and X rays on human lens cell differentiation. Radiat Res. 2005;164(4 Pt 2):531-539.
128. Iwadate Y, Mizoe J, 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. 2001;50:803-808. (Pubitemid 32515335)
129. 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 (Tokyo). 2007;48:317-325.
130. Hamada N, Hara T, Omura-Minamisawa M, et al. Energetic heavy ions overcome tumor radioresistance caused by overexpression of Bcl-2. Radiother Oncol. 2008;89:231-236.
131. Ma J, Ye L, Da M, et al. Heavy ion irradiation increases apoptosis and STAT-3 expression, led to the cells arrested at G2/M phase in human hepatoma SMMC-7721 cells. Mol Cell Biochem. 2009;328:17-23.
132. Yamamoto N, Ikeda C, Yakushiji T, et al. Genetic effects of X-ray and carbon ion irradiation in head and neck carcinoma cell lines. Bull Tokyo Dent Coll. 2007;48:177-185.
133. Higo M, Uzawa K, Kawata T, et al. Enhancement of SPHK1 in vitro by carbon ion irradiation in oral squamous cell carcinoma. Int J Radiat Oncol Biol Phys. 2006;65:867-875. (Pubitemid 43795824)
134. Fushimi K, Uzawa K, Ishigami T, et al. Susceptible genes and molecular pathways related to heavy ion irradiation in oral squamous cell carcinoma cells. Radiother Oncol. 2008;89:237-244.
135. Matsumoto Y, Iwakawa M, Furusawa Y, et al. Gene expression analysis in human malignant melanoma cell lines exposed to carbon beams. Int J Radiat Biol. 2008;84:299-314.
136. Imadome K, Iwakawa M, Nojiri K, et al. Upregulation of stress-response genes with cell cycle arrest induced by carbon ion irradiation in multiple murine tumors models. Cancer Biol Ther. 2008;7:208-217. (Pubitemid 351590425)
137. Nojiri K, Iwakawa M, Ichikawa Y, et al. The proangiogenic factor ephrin-A1 is up-regulated in radioresistant murine tumor by irradiation. Exp Biol Med (Maywood). 2009;234:112-122.
138. Bigelow A, Garty G, Funayama T, et al. Expanding the question-answering potential of single-cell microbeams at RARAF, USA. J Radiat Res (Tokyo). 2009;50(Suppl A):A21-A28.
139. Gerardi S. Ionizing radiation microbeam facilities for radiobiological studies in Europe. J Radiat Res (Tokyo). 2009;50(Suppl A):A13-A20.
140. Matsumoto H, Tomita M, Otsuka K, et al. A new paradigm in radioadaptive response developing from microbeam research. J Radiat Res (Tokyo). 2009;50(Suppl A):A67-A79.
141. Prise KM, Schettino G, Vojnovic B, et al. Microbeam studies of the bystander response. J Radiat Res (Tokyo). 2009;50(Suppl A):A1-A6.
142. Voss KO, Fournier C, Taucher-Scholz G. Heavy ion microprobes: a unique tool for bystander research and other radiobiological applications. New J Phys. 2008;10:075011.