Molecular biology to radiation oncology: A model for translational research? Opportunities in basic and translational research

Radiation Research

Volumn 150, Issue 2, 1998, Pages 134-147

  Stone, Helen B ^a   Dewey, William C ^b   Wallace, Susan S ^c   Coleman, C Norman ^d  

^a NATIONAL CANCER INSTITUTE   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF VERMONT   (United States)

^d HARVARD RADIATION ONCOLOGY PROGRAM   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; CANCER RADIOTHERAPY; CANCER RESEARCH; CONFERENCE PAPER; CYTOPATHOGENIC EFFECT; DNA STRAND BREAKAGE; IONIZING RADIATION; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL;

EID: 0031853905     PISSN: 00337587     EISSN: None     Source Type: Journal    
DOI: 10.2307/3579849     Document Type: Conference Paper

References (122)

1. M. Jung and A. Dritschilo, Signal transduction and cellular responses to ionizing radiation. Semin. Radiat. Oncol. 6, 268-272 (1996).
2. Z. G. Liu, R. Baskaran, E. T. Lea-Chou, L. D. Wood, Y. Chen, M. Karin and J. Y. Wang, Three distinct signalling responses by murine fibroblasts to genotoxic stress. Nature 384, 273-276 (1996).
3. K. R. Blank, M. S. Rudoltz, G. D. Kao, R. J. Muschel and W. G. McKenna, The molecular regulation of apoptosis and implications for radiation oncology. Int. J. Radiat. Biol. 71, 455-466 (1997).
4. D. A. Liebermann, B. Hoffman and R. A. Steinman, Molecular controls of growth arrest and apoptosis: p53-dependent and independent pathways. Oncogene 11, 199-210 (1995).
5. C. Caelles, A. Helmberg and M. Karin, p53-dependent apoptosis in the absence of transcriptional activation of p53-target genes. Nature 370, 220-223 (1994).
6. A. Strasser, A. W. Harris, T. Jacks and S. Cory, DNA damage can induce apoptosis in proliferating lymphoid cells via p53-independent mechanisms inhibitable by Bcl-2. Cell 79, 329-339 (1994).
7. A. M. Chinnaiyan and V. M. Dixit, The cell-death machine. Curr. Biol. 6, 555-562 (1996).
8. G. M. Cohen, Caspases: The executioners of apoptosis. Biochem. J. 326, 1-16 (1997).
9. V. A. Soldatenkov, S. Prasad, V. Notario and A. Dritschilo, Radiation-induced apoptosis of Ewing's sarcoma cells: DNA fragmentation and proteolysis of poly(ADP-ribose) polymerase. Cancer Res. 55, 4240-4242 (1995).
10. V. Soldatenkov, V. Notario and A. Dritschilo, Expression of the human Bcl-2 increases resistance of Ewing's sarcoma cells to apoptosis and inhibits poly(ADP-ribose) polymerase cleavage induced by radiation. Int. J. Oncol. 9, 547-551 (1996).
11. E. White, Life, death and the pursuit of apoptosis. Genes Dev. 10, 1-15 (1996).
12. T. G. Graeber, C. Osmanian, T. Jacks, D. E. Housman, C. J. Koch, S. W. Lowe and A. J. Giaccia, Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature 379, 88-91 (1996).
13. S. Nagata, Apoptosis by death factor. Cell 88, 355-365 (1997).
14. D. L. Vaux and A. Strasser, The molecular biology of apoptosis. Proc. Natl. Acad. Sci. USA 93, 2239-2244 (1996).
15. R. E. Meyn, L. C. Stephens, N. R. Hunter, K. K. Ang and L. Milas, Reemergence of apoptotic cells between fractionated doses in irradiated murine tumors. Int. J. Radiat. Oncol. Biol. Phys. 30, 619-624 (1994).
16. S. H. Revell, Relationship between chromosome damage and cell death. In Radiation-induced Chromosome Damage in Man (T. Ishihara and M. S. Sasaki, Eds.), pp. 215-233. Alan R. Liss, New York, 1983.
17. R. E. Meyn, Apoptosis and response to radiation: Implications for radiation therapy. Oncology 11, 349-356 (1997).
18. W. C. Dewey, C. C. Ling and R. E. Meyn, Radiation-induced apoptosis: Relevance to radiotherapy. Int. J. Radiat. Oncol. Biol. Phys. 33, 781-796 (1995).
19. R. E. Meyn, L. C. Stephens, K. K. Ang, N. R. Hunter, W. A. Brock, L. Milas and L. J. Peters, Heterogeneity in the development of apoptosis in irradiated murine tumours of different histologies. Int. J. Radiat. Biol. 64, 583-591 (1993).
20. L. C. Stephens, N. R. Hunter, K. K. Ang, L. Milas and R. E. Meyn, Development of apoptosis in irradiated murine tumors as a function of time and dose. Radiat. Res. 135, 75-80 (1993).
21. A. J. Merritt, T. D. Allen, C. S. Potten and J. A. Hickman, Apoptosis in small intestinal epithelia from p53-null mice: Evidence for a delayed, p53-independent G2/M-associated cell death after γ-irradiation. Oncogens 14, 2759-2766 (1997).
22. L. Wang, Y. Cui, B. I. Lord, S. A. Roberts, C. S. Potten, J. H. Hendry and D. Scott, Gamma-ray-induced cell killing and chromosome abnormalities in the bone marrow of p53-deficient mice. Radiat. Res. 146, 259-266 (1996).
23. S. Murnane and J. L. Schwartz, Cell checkpoint and radiosensitivity. Nature 365, 22 (1993).
24. W. F. Morgan, J. P. Day, M. I. Kaplan, E. M. McGhee and C. L. Limoli, Genomic instability induced by ionizing radiation. Radiat. Res. 146, 247-258 (1996).
25. C. E. Canman and M. B. Kastan, Three paths to stress relief. Nature 384, 213-214 (1996).
26. P. Nurse, Ordering S phase and M phase in the cell cycle. Cell 79, 547-550 (1994).
27. D. O. Morgan, Principles of CDK regulation. Nature 374, 131-134 (1995).
28. R. W. King, R. J. Deshaies, J. M. Peters and M. W. Kirschner, How proteolysis drives the cell cycle. Science 274, 1652-1659 (1996).
29. R. A. Weinberg, The retinoblastoma protein and cell cycle control. Cell 81, 323-330 (1995).
30. C. J. Sherr, Cancer cell cycles. Science 274, 1672-1677 (1996).
31. B. Stillman, Cell cycle control of DNA replication. Science 274, 1659-1664 (1996).
32. 1-phase checkpoint by low-oxygen conditions is independent of p53 status. Mol. Cell. Biol. 14, 6264-6277 (1994).
33. J. P. Murnane, Cell cycle regulation in response to DNA damage in mammalian cells: A historical perspective. Cancer Metastasis Rev. 14, 17-29 (1995).
34. T. J. Jorgensen and Y. Shiloh, The ATM gene and the radiobiology of ataxia telangiectasia. Int. J. Radiat. Biol. 69, 527-537 (1996).
35. N. Zhang, P. Chen, K. K. Khanna, S. Scott, M. Gatei, S. Kozlov, D. Watters, K. Spring, T. Yen and M. F. Lavin, Isolation of full-length ATM cDNA and correction of the ataxia-telangiectasia cellular phenotype. Proc. Natl. Acad. Sci. USA 94, 8021-8026 (1997).
36. S. P. Jackson, Cancer predisposition. Ataxia-telangiectasia at the crossroads. Curr. Biol. 5, 1210-1212 (1995).
37. G. Chen and E. Y-H. P. Lee, The product of the ATM gene is a 370-kDa nuclear phosphoprotein. J. Biol. Chem. 271, 33693-33697 (1996).
38. S. M. Brown, Ataxia telangiectasia and cellular responses to DNA damage. Cancer Res. 57, 2313 (1997).
39. C. Barlow, S. Hirotsune, R. Paylor, M. Liyanage, M. Eckhaus, F. Collins, Y. Shiloh, J. N. Crawley, T. Ried, D. Tagle and A. Wynshaw-Boris, ATM-deficient mice: A paradigm of ataxia telangiectasia. Cell 86, 159-171 (1996).
40. M. Jung, A. Kondratyev, S. A. Lee, A. Dimtchev and A. Dritschilo, ATM gene product phosphorylates IγB-α. Cancer Res. 57, 24-27 (1997).
41. M. Jung, Y. Zhang, S. Lee and A. Dritschilo, Correction of radiation sensitivity in ataxia telangiectasia cells by a truncated IκB-α. Science 268, 1619-1621 (1995).
42. A. J. Levine. p53, the cellular gatekeeper for growth and division. Cell 88, 323-331 (1997).
43. H. Huang, C-Y. Li and J. B. Little, Abrogation of p53 function by transfection of HPV16 E6 gene does not enhance resistance of human tumour cells to ionizing radiation. Int. J. Radiat. Biol. 70, 151-160 (1996).
44. J. B. Little, Failla Memorial Lecture: Changing views of cellular radiosensitivity. Radiat. Res. 140, 299-312 (1994).
45. 2 delay. Cancer Res. 55, 1643-1648 (1995).
46. S. Fan, M. L. Smith, D. J. Rivet, D. Duba, Q. Zhan, K. W. Kohn, A. J. Fornace, Jr. and P. M. O'Connor, Disruption of p53 function sensitizes breast cancer MCF-7 cells to cisplatin and pentoxifylline. Cancer Res. 55, 1649-1654 (1995).
47. S. Fan, W. S. el-Deiry, I. Bae, J. Freeman, D. Jondle, K. Bhatia, A. J. Fornace, Jr., I. Magrath, K. W. Kohn and P. M. O'Connor, p53 gene mutations are associated with decreased sensitivity of human lymphoma cells to DNA damaging agents. Cancer Res. 54, 5824-5830 (1994).
48. D. G. Brachman, M. Beckett, D. Graves, D. Haraf, E. Vokes and R. R. Weichselbaum, p53 mutation does not correlate with radiosensitivity in 24 head and neck cancer cell lines. Cancer Res. 53, 3667-3669 (1993).
49. T. Waldman, Y. Zhang, L. Dillehay, J. Yu, K. Kinzler, B. Vogelstein and J. Williams, Cell-cycle arrest versus cell death in cancer therapy. Nat. Med. 3, 1034-1036 (1997).
50. waf1/Cip1 sensitizes tumors to radiation by an apoptosis-independent mechanism. Cancer Res. 57, 4703-4706 (1997).
51. L. H. Thompson, Evidence that mammalian cells possess homologous recombinational repair pathways. Mutat. Res. 363, 77-88 (1996).
52. S. M. Lewis, The mechanism of V(D)J joining: Lessons from molecular, immunological and comparative analyses. Adv. Immunol. 56, 27-150 (1994).
53. P. A. Jeggo, DNA-PK: At the cross-roads of biochemistry and genetics. Mutat. Res. 384, 1-14 (1997).
54. D. B. Roth, T. Lindahl and M. Gellert, Repair and recombination. How to make ends meet. Curr. Biol. 5, 496-499 (1995).
55. S. P. Lees-Miller, The DNA-dependent protein kinase, DNA-PK: 10 years and no ends in sight. Biochem. Cell Biol. 74, 503-512 (1996).
56. R. C. Getts and T. D. Stamato, Absence of a Ku-like DNA end binding activity in the xrs double-strand DNA repair-deficient mutant. J. Biol. Chem. 269, 15981-15984 (1994).
57. P. A. Jeggo, G. E. Taccioli and S. P. Jackson, Ménage à trois: Double strand break repair, V(D)J recombination and DNA-PK. BioEssays 17, 949-957 (1995).
58. M. Bogue and D. B. Roth, Mechanism of V(D)J recombination. Curr. Opin. Immunol. 8, 175-180 (1996).
59. C. U. Kirschgessner, C. K. Patil, J. W. Evans, C. A. Cuomo, L. M. Fried, T. Carter, M. A. Oettinger and J. M. Brown, DNA-dependent kinase (p350) as a candidate gene for the murine SCID defect. Science 267, 1178-1183 (1995).
60. T. Blunt, N. J. Finnie, G. E. Taccioli, G. C. M. Smith, J. Demengeot, T. M. Gottlieb, R. Mizuta, A. J. Varghese, F. W. Alt, P. A. Jeggo and S. P. Jackson, Defective DNA-dependent protein kinase activity is linked to V(D)J recombination and DNA repair defects associated with the murine seid mutation. Cell 80, 813-823 (1995).
61. A. Nussenzweig, C. Chen, V. da Costa Soares, M. Sanchez, K. Sokol, M. D. Nussenzweig and G. C. Li, Requirement for Ku80 in growth and immunoglobulin V(D)J recombination. Nature 382, 551-555 (1996).
62. G. E. Taccioli, T. M. Gottlieb, T. Blunt, A. Priestly, J. Demengeot, R. Mizuta, A. R. Lehmann, F. A. Alt, S. P. Jackson and P. A. Jeggo, Ku80: Product of the XRCC5 gene and its role in DNA repair and V(D)J recombination. Science 265, 1442-1445 (1994).
63. S. S. Wallace, DNA damages processed by base excision repair: Biological consequences. Int. J. Radiat. Biol. 66, 579-589 (1994).
64. S. S. Wallace, Oxidative damage to DNA and its repair. In Oxidative Stress and the Molecular Biology of Antioxidant Defenses (J. Scandalios, Ed.), pp. 49-90. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY, 1997.
65. S. Xanthoudakis, R. J. Smeyne, J. D. Wallace and T. Curran, The redox/DNA repair protein, Ref-1, is essential for early embryonic development in mice. Proc. Natl. Acad. Sci. USA 93, 8919-8923 (1996).
66. H. Gu, J. D. Marth, P. C. Orban, H. Mossmann and K. Rajewsky, Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265, 103-106 (1994).
67. J. F. Ward, The complexity of DNA damage: Relevance to biological consequences. Int. J. Radiat. Biol. 66, 427-432 (1994).
68. L. H. Thompson and P. A. Jeggo, Nomenclature of human genes involved in ionizing radiation sensitivity. Mutat. Res. 337, 131-134 (1995).
69. W. C. Dewey, H. H. Miller and D. B. Leeper, Chromosomal aberrations and mortality of x-irradiated mammalian cells: Emphasis on repair. Proc. Natl. Acad. Sci. USA 68, 667-671 (1971).
70. M. N. Cornforth and J. S. Bedford, A quantitative comparison of potentially lethal damage repair and the rejoining of interphase chromosome breaks in low passage normal human fibroblasts. Radiat. Res. 111, 385-405 (1987).
71. R. R. Weichselbaum, J. Nove and J. B. Little, Deficient recovery from potentially lethal radiation damage in ataxia telangiectasia and xeroderma pigmentosum. Nature 271, 261-262 (1978).
72. D. Kim, H. Ouyang, S. H. Yang, A. Nussenzweig, P. Burgman and G. C. Li, A constitutive heat shock element-binding factor is immunologically identical to the Ku autoantigen. J. Biol. Chem. 270, 15277-15284 (1995).
73. S. H. Yang, A. Nussenzweig, L. Li, D. Kim, H. Ouyang, P. Burgman and G. C. Li, Modulation of thermal induction of hsp70 expression by Ku autoantigen or its individual subunits. Mol. Cell. Biol. 16, 3799-3806 (1996).
74. R. B. Cary, S. R. Peterson, J. Wang, D. G. Bear, E. M. Bradbury and D. J. Chen, DNA looping by Ku and the DNA-dependent protein kinase. Proc. Natl. Acad. Sci. USA 94, 4267-4272 (1997).
75. D. Pang, S. Yoo, W. S. Dynan, M. Jung and A. Dritschilo, Ku proteins join DNA fragments as shown by atomic force microscopy. Cancer Res. 57, 1412-1415 (1997).
76. U. Kasid, A. Pfeifer, T. Brennan, M. Beckett, R. R. Weichselbaum, A. Dritschilo and G. E. Mark, Effect of antisense c-raf-1 on tumorigenicity and radiation sensitivity of a human squamous carcinoma. Science 243, 1354-1356 (1989).
77. V. A. Soldatenkov, A. Dritschilo, F. H. Wang, Z. Olah, W. B. Anderson and U. Kasid, Inhibition of Raf-1 protein kinase by antisense phosphorothioate oligodeoxyribonucleotide is associated with sensitization of human laryngeal squamous carcinoma cells to gamma radiation. Cancer J. Sci. Am. 3, 13-20 (1997).
78. R. K. Jain, Transport of molecules in the tumor interstitium: A review Cancer Res. 47, 3039-3051 (1987).
79. R. M. Sutherland, Cell and environment interactions in tumor microregions: The multicell spheroid model. Science 240, 177-184 (1988).
80. M. Höckel, K. Schlenger, M. Mitze, U. Schäffer and P. Vaupel, Hypoxia and radiation response in human tumors. Semin. Radiat. Oncol. 6, 3-9 (1996).
81. M. Nordsmark, M. Overgaard and J. Overgaard, Pretreatment oxygenation predicts radiation response in advanced squamous cell carcinoma of the head and neck. Radiother. Oncol. 41, 31-39 (1996).
82. R. Jain, Barriers to drug delivery in solid tumors. Sci. Am. 271, 58-65 (1994).
83. P. W. Vaupel, Oxygenation of solid tumors. In Drug Resistance in Oncology (B. A. Teicher, Ed.), pp. 59-85. Marcel Dekker, New York, 1993.
84. M. Höckel, K. Schlenger, B. Aral, M. Mitze, U. Schäffer and P. Vaupel, Association between tumor hypoxia and malignant progression in advanced cancer of the uterine cervix. Cancer Res. 56, 4509-4515 (1996).
85. J. M. Brown, SR 4233 (Tirapazamine): A new anticancer drug exploiting hypoxia in solid tumours. Br. J. Cancer 67, 1163-1170 (1993).
86. H. B. Stone, J. M. Brown, T. L. Phillips and R. M. Sutherland, Oxygen in human tumors: Correlations between methods of measurement and response to therapy. Radiat. Res. 136, 422-434 (1993).
87. J. Raleigh, M. Dewhirst and D. Thrall, Measuring tumor hypoxia. Semin. Radiat. Oncol. 6, 37-45 (1996).
88. 2 + M phases after irradiation of a solid tumor in vivo. Cancer Res. 39, 1891-1897 (1979).
89. D. J. Chaplin, P. L. Olive and R. E. Durand, Intermittent blood flow in a murine tumor: Radiobiological effects. Cancer Res. 47, 597-601 (1987).
90. C. A. Znati, M. Rosenstein, Y. Boucher, M. W. Epperly, W. D. Bloomer and R. K. Jain, Effect of radiation on interstitial fluid pressure and oxygenation in a human tumor xenograft. Cancer Res. 56, 964-968 (1996).
91. P. Vaupel, S. Frinak and M. O'Hara, Direct measurement of reoxygenation in malignant mammary tumors after a single large dose of irradiation. Adv. Exp. Med. Biol. 180, 773-782 (1984).
92. P. K. Narayanan, E. H. Goodwin and B. E. Lehnert, Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res. 57, 3963-3971 (1997).
93. S. M. Clutton, K. M. Townsend, C. Walker, J. D. Ansell and E. G. Wright, Radiation-induced genomic instability and persisting oxidative stress in primary bone marrow cultures. Carcinogenesis 17, 1633-1639 (1996).
94. D. Hanahan and J. Folkman, Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86, 353-364 (1996).
95. N. Weidner, J. Folkman, F. Pozza, P. Bevilacqua, E. N. Allred, D. H. Moore, S. Meli and G. Gasparini, Tumor angiogenesis: A new significant and independent prognostic indicator in early-stage breast carcinoma. J. Natl. Cancer Inst. 84, 1875-1887 (1992).
96. N. Weidner, P. R. Carroll, J. Flax, W. Blumenfeld and J. Folkman, Tumor angiogenesis correlates with metastasis in invasive prostate carcinoma. Am. J. Pathol. 143, 401-409 (1993).
97. M. Verheij, R. Bose, X. H. Lin, B. Yao, W. D. Jarvis, S. Grant, M. J. Birrer, E. Szabo, L. I. Zon, J. M. Kyriakis, A. Haimovitz-Friedman, Z. Fuks and R. N. Kolesnick, Requirement for ceramide-initiated SAPK/JNK signalling in stress-induced apoptosis. Nature 380, 75-79 (1996).
98. R. M. Sutherland, W. A. Ausserer, B. J. Murphy and K. R. Laderoute, Tumor hypoxia and heterogeneity: Challenges and opportunities for the future. Semin. Radiat. Oncol. 6, 59-70 (1996).
99. N. A. Hoffman, F. F. Gollin and K. H. Clifton, Acquired radioresistance of transplanted mammary adenocarcinoma in inbred mice after serial irradiation. Radiology 88, 568-575 (1967).
100. K. Kaneta and N. Muta, Radiosensitivity of the pre-irradiated Yoshida sarcoma. Nature 185, 858-859 (1960).
101. 95 radiation dose. Nature 211, 996-997 (1966).
102. K. Ando, S. Koike, M. Shikita, I. Hayata, H. Otsu and S. Satoh, Radiosensitivity of late recurrences following radiotherapy of murine fibrosarcomas. Radiat. Res. 113, 334-345 (1988).
103. W. K. Sinclair, X-ray-induced heritable damage (small colony formation) in cultured mammalian cells. Radiat. Res. 21, 584-611 (1964).
104. W. H. McBride, J. S. Economou, N. Kuber, J-H. Hong, C-S. Chiang, R. Syljuasen, S. T. Dougherty and G. J. Dougherty, Modification of tumor microenvironment by cytokine gene transfer. Acta Oncol. 34, 447-451 (1995).
105. 1 arrest by cell-substratum interactions. Cancer Res. 57, 1151-1156 (1997).
106. N. Boudreau, Z. Werb and M. J. Bissell, Suppression of apoptosis by basement membrane requires three-dimensional tissue organization and withdrawal from the cell cycle. Proc. Natl. Acad. Sci. USA 93, 3509-3513 (1996).
107. P. L. Olive and R. E. Durand, Drug and radiation resistance in spheroids: Cell contact and kinetics. Cancer Metastasis Rev. 13, 121-138 (1994).
108. Kip1 on resistance of tumor cells to anticancer agents. Nat. Med. 2, 1204-1210 (1996).
109. T. Gura, Cancer models. Systems for identifying new drugs are often faulty. Science 278, 1041-1042 (1997).
110. J. F. Fowler and T. J. Kinsella, The limiting radiosensitisation of tumours by S-phase sensitisers. Br. J. Cancer 74 (Suppl. 27), S294-S296 (1996).
111. H. R. Withers, The four R's of radiotherapy. Adv. Radiat. Biol. 5, 241-271 (1975).
112. L. H. Hartwell, P. Szanski, C. J. Roberts, A. W. Murray and S. H. Friend, Integrating genetic approaches into the discovery of anticancer drugs. Science 278, 1064-1068 (1997).
113. M. R. Grever, S. A. Schepartz and B. A. Chabner, The National Cancer Institute: Cancer drug discovery and development program. Semin. Oncol. 19, 622-638 (1992).
114. J. N. Weinstein, T. G. Myers, P. M. O'Connor, S. H. Friend, A. J. Fornace, Jr., K. W. Kohn, T. Fojo, S. E. Bates, L. V. Rubinstein, N. L. Anderson, J. K. Buolamwini, W. W. van Osdol, A. Monks, D. A. Scudiero, E. A. Sausville, D. W. Zaharevitz, B. Bunow, V. N. Viswanadhan, G. S. Johnson, R. E. Wittes and K. D. Paull, An information-intensive approach to the molecular pharmacology of cancer. Science 275, 343-349 (1997).
115. J. M. Brown, NCI's anticancer drug screening program may not be selecting for clinically active compounds. Oncol. Res. 9, 213-215 (1997).
116. L. H. Thompson and H. D. Suit, Proliferation kinetics of X-irradiated mouse L cells studied with time-lapse photography. II. Int. J. Radiat. Biol. 15, 347-362 (1969).
117. C. A. Vidair, C. H. Chen, C. C. Ling and W. C. Dewey, Apoptosis induced by X-irradiation of rec-myc cells is postmitotic and not predicted by the time after irradiation or behavior of sister cells. Cancer Res. 56, 4116-4118 (1996).
118. R. M. Sutherland and R. E. Durand, Radiation response of multi-cell spheroids - an in vitro tumour model. Curr. Top. Radiat. Res. Q. 11, 87-139 (1976).
119. L. Hlatky and E. L. Alpen, Two-dimensional diffusion limited system for cell growth. Cell Tissue Kinet. 18, 597-611 (1985).
120. M. G. Hollingshead, M. C. Alley, R. F. Camalier, B. J. Abbott, J. G. Mayo, L. Malspeis and M. R. Grever, In vivo cultivation of tumor cells in hollow fibers. Life Sci. 57, 131-141 (1995).
121. D. S. M. Cowan, K. O. Hicks and W. R. Wilson, Multicellular membranes as an in vitro model for extravascular diffusion in tumours. Br. J. Cancer 74 (Suppl. 27), S28-S31 (1996).
122. E. L. Gillette, S. L. McChesney, M. W. Dewhirst and R. J. Scott, Response of canine oral carcinomas to heat and radiation. Int. J. Radiat. Oncol. Biol. Phys. 13, 1861-1867 (1987).