Clinical perspectives of cancer stem cell research in radiation oncology

Radiotherapy and Oncology

Volumn 108, Issue 3, 2013, Pages 388-396

  Bütof, Rebecca ^a   Dubrovska, Anna ^a   Baumann, Michael ^a  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

Author keywords

Cancer stem cells; Radiation oncology; Radiobiology

Indexed keywords

ANTINEOPLASTIC AGENT; DOUBLE STRANDED DNA;

BIOASSAY; CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER RESEARCH; CANCER RESISTANCE; CANCER STEM CELL; CANCER SURVIVAL; ESOPHAGEAL ADENOCARCINOMA; ESOPHAGUS CANCER; GENETIC HETEROGENEITY; GLIOBLASTOMA; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; METASTASIS; NONHUMAN; PRIORITY JOURNAL; PROGRESSION FREE SURVIVAL; RADIATION DOSE; RADICAL HYSTERECTOMY; RADIOSENSITIVITY; RECTUM CANCER; REVIEW; TREATMENT OUTCOME; UTERINE CERVIX CARCINOMA;

CANCER STEM CELLS; RADIATION ONCOLOGY; RADIOBIOLOGY;

ANIMALS; BRAIN NEOPLASMS; GLIOBLASTOMA; HEAD AND NECK NEOPLASMS; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; RADIATION TOLERANCE; RECTAL NEOPLASMS;

EID: 84887025650     PISSN: 01678140     EISSN: 18790887     Source Type: Journal    
DOI: 10.1016/j.radonc.2013.06.002     Document Type: Review

References (119)

1. M.F. Clarke, J.E. Dick, and P.B. Dirks Cancer stem cells - perspectives on current status and future directions: AACR Workshop on cancer stem cells Cancer Res 66 2006 9339 9344
2. M. Baumann, M. Krause, and R. Hill Exploring the role of cancer stem cells in radioresistance Nat Rev Cancer 8 2008 545 554
3. D. Dingli, and F. Michor Successful therapy must eradicate cancer stem cells Stem Cells 24 2006 2603 2610
4. M. Baumann, M. Krause, H. Thames, K. Trott, and D. Zips Cancer stem cells and radiotherapy Int J Radiat Biol 85 2009 391 402
5. U. Koch, M. Krause, and M. Baumann Cancer stem cells at the crossroads of current cancer therapy failures - radiation oncology perspective Semin Cancer Biol 20 2010 116 124
6. M. Krause, A. Yaromina, W. Eicheler, U. Koch, and M. Baumann Cancer stem cells: targets and potential biomarkers for radiotherapy Clin Cancer Res 17 2011 7224 7229
7. T.R. Munro, and C.W. Gilbert The relation between tumour lethal doses and the radiosensitivity of tumour cells Br J Radiol 34 1961 246 251
8. T.B. Brunner, L.A. Kunz-Schughart, P. Grosse-Gehling, and M. Baumann Cancer stem cells as a predictive factor in radiotherapy Semin Radiat Oncol 22 2012 151 174
9. R.P. Hill, and L. Milas The proportion of stem cells in murine tumors Int J Radiat Oncol Biol Phys 16 1989 513 518
10. M. Baumann, W. Dubois, and H.D. Suit Response of human squamous cell carcinoma xenografts of different sizes to irradiation: relationship of clonogenic cells, cellular radiation sensitivity in vivo, and tumor rescuing units Radiat Res 123 1990 325 330
11. M.R. Alison, W.R. Lin, S.M. Lim, and L.J. Nicholson Cancer stem cells: in the line of fire Cancer Treat Rev 38 2012 589 598
12. M. Baumann, M. Krause, and D. Zips Selective inhibition of the epidermal growth factor receptor tyrosine kinase by BIBX1382BS and the improvement of growth delay, but not local control, after fractionated irradiation in human FaDu squamous cell carcinoma in the nude mouse Int J Radiat Biol 79 2003 547 559
13. M. Krause, J. Prager, and X. Zhou EGFR-TK inhibition before radiotherapy reduces tumour volume but does not improve local control: differential response of cancer stem cells and nontumourigenic cells? Radiother Oncol 83 2007 316 325
14. A.T. Collins, P.A. Berry, C. Hyde, M.J. Stower, and N.J. Maitland Prospective identification of tumorigenic prostate cancer stem cells Cancer Res 65 2005 10946 10951
15. C.A. O'Brien, A. Pollett, S. Gallinger, and J.E. Dick A human colon cancer cell capable of initiating tumour growth in immunodeficient mice Nature 445 2007 106 110
16. M.E. Prince, R. Sivanandan, and A. Kaczorowski Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma Proc Natl Acad Sci USA 104 2007 973 978
17. S.K. Singh, C. Hawkins, and I.D. Clarke Identification of human brain tumour initiating cells Nature 432 2004 396 401
18. W. Jiang, J. Peng, Y. Zhang, W.C. Cho, and K. Jin The implications of cancer stem cells for cancer therapy Int J Mol Sci 13 2012 16636 16657
19. V.K. Srivastava, and J. Nalbantoglu Flow cytometric characterization of the DAOY medulloblastoma cell line for the cancer stem-like phenotype Cytometry A 73 2008 940 948
20. Peitzsch C, Kurth I, Kunz-Schughart LA, Baumann M, Dubrovska A. Discovery of the cancer stem cell related determinants of radioresistance. Radiat Oncol, 2013, submitted for publication [RO-S-13-00615].
21. C. Petersen, M. Baumann, H.H. Dubben, H. Arps, A. Melenkeit, and J. Helfrich Linear-quadratic analysis of tumour response to fractionated radiotherapy: a study on human squamous cell carcinoma xenografts Int J Radiat Biol 73 1998 197 205
22. H.D. Suit Radiation biology: the conceptual and practical impact on radiation therapy Radiat Res 94 1983 10 40
23. A. Yaromina, M. Krause, and H. Thames Pre-treatment number of clonogenic cells and their radiosensitivity are major determinants of local tumour control after fractionated irradiation Radiother Oncol 83 2007 304 310
24. D.L. Ball, R.J. Fisher, and B.H. Burmeister The complex relationship between lung tumor volume and survival in patients with non-small cell lung cancer treated by definitive radiotherapy: A prospective, observational prognostic factor study of the Trans-Tasman Radiation Oncology Group (TROG 9905) Radiother Oncol 106 2013 305 311
25. M. Baumann, T. Herrmann, and R. Koch Final results of the randomized phase III CHARTWEL-trial (ARO 97-1) comparing hyperfractionated-accelerated versus conventionally fractionated radiotherapy in non-small cell lung cancer (NSCLC) Radiother Oncol 100 2011 76 85
26. S.M. Bentzen, and H.D. Thames Tumor volume and local control probability: clinical data and radiobiological interpretations Int J Radiat Oncol Biol Phys 36 1996 247 251
27. H.H. Dubben, H.D. Thames, and H.P. Beck-Bornholdt Tumor volume: a basic and specific response predictor in radiotherapy Radiother Oncol 47 1998 167 174
28. M. Soliman, A. Yaromina, and S. Appold GTV differentially impacts locoregional control of non-small cell lung cancer (NSCLC) after different fractionation schedules: subgroup analysis of the prospective randomized CHARTWEL trial Radiother Oncol 106 2013 299 304
29. C.R. Johnson, H.D. Thames, D.T. Huang, and R.K. Schmidt-Ullrich The tumor volume and clonogen number relationship: tumor control predictions based upon tumor volume estimates derived from computed tomography Int J Radiat Oncol Biol Phys 33 1995 281 287
30. S. Bao, Q. Wu, and R.E. McLendon Glioma stem cells promote radioresistance by preferential activation of the DNA damage response Nature 444 2006 756 760
31. M. Ropolo, A. Daga, and F. Griffero Comparative analysis of DNA repair in stem and nonstem glioma cell cultures Mol Cancer Res 7 2009 383 392
32. K.J. Kim, K.H. Lee, and H.S. Kim The presence of stem cell marker-expressing cells is not prognostically significant in glioblastomas Neuropathology 31 2011 494 502
33. A. Murat, E. Migliavacca, and T. Gorlia Stem cell-related "self-renewal" signature and high epidermal growth factor receptor expression associated with resistance to concomitant chemoradiotherapy in glioblastoma J Clin Oncol 26 2008 3015 3024
34. R. Pallini, L. Ricci-Vitiani, and G.L. Banna Cancer stem cell analysis and clinical outcome in patients with glioblastoma multiforme Clin Cancer Res 14 2008 8205 8212
35. M.C. de Jong, J. Pramana, and J.E. van der Wal CD44 expression predicts local recurrence after radiotherapy in larynx cancer Clin Cancer Res 16 2010 5329 5338
36. M.I. Koukourakis, A. Giatromanolaki, V. Tsakmaki, V. Danielidis, and E. Sivridis Cancer stem cell phenotype relates to radio-chemotherapy outcome in locally advanced squamous cell head-neck cancer Br J Cancer 106 2012 846 853
37. J.K. Smit, H. Faber, and M. Niemantsverdriet Prediction of response to radiotherapy in the treatment of esophageal cancer using stem cell markers Radiother Oncol 107 2013 434 441
38. G.Y. Kwon, H. Ha, G. Ahn, S.Y. Park, S.J. Huh, and W. Park Role of CD24 protein in predicting metastatic potential of uterine cervical squamous cell carcinoma in patients treated with radiotherapy Int J Radiat Oncol Biol Phys 69 2007 1150 1156
39. C.O. Sung, W. Park, and Y.L. Choi Prognostic significance of CD24 protein expression in patients treated with adjuvant radiotherapy after radical hysterectomy for cervical squamous cell carcinoma Radiother Oncol 95 2010 359 364
40. T. Sprenger, L.C. Conradi, and T. Beissbarth Enrichment of CD133-expressing cells in rectal cancers treated with preoperative radiochemotherapy is an independent marker for metastasis and survival Cancer 119 2013 26 35
41. Q. Wang, Z.G. Chen, C.Z. Du, H.W. Wang, and L.Gu.J. Yan Cancer stem cell marker CD133+ tumour cells and clinical outcome in rectal cancer Histopathology 55 2009 284 293
42. A. Kawamoto, K. Tanaka, and S. Saigusa Clinical significance of radiation-induced CD133 expression in residual rectal cancer cells after chemoradiotherapy Exp Ther Med 3 2012 403 409
43. M. Svoboda, J. Sana, and P. Fabian MicroRNA expression profile associated with response to neoadjuvant chemoradiotherapy in locally advanced rectal cancer patients Radiat Oncol 7 2012 195
44. Y. Shimono, M. Zabala, and R.W. Cho Downregulation of miRNA-200c links breast cancer stem cells with normal stem cells Cell 138 2009 592 603
45. C.R. Schoof, E.L. Botelho, A. Izzotti, and R. Vasques Ldos MicroRNAs in cancer treatment and prognosis Am J Cancer Res 2 2012 414 433
46. P. Ramm, M. Bettscheider, and D. Beier 1H-nuclear magnetic resonance spectroscopy of glioblastoma cancer stem cells Stem Cells Dev 20 2011 2189 2195
47. C. Tsurumi, N. Esser, and E. Firat Non-invasive in vivo imaging of tumor-associated CD133/prominin PLoS One 5 2010 e15605
48. E. Vlashi, K. Kim, and C. Lagadec In vivo imaging, tracking, and targeting of cancer stem cells J Natl Cancer Inst 101 2009 350 359
49. I. Baccelli, and A. Trumpp The evolving concept of cancer and metastasis stem cells J Cell Biol 198 2012 281 293
50. P. Valent, D. Bonnet, and R. De Maria Cancer stem cell definitions and terminology: the devil is in the details Nat Rev Cancer 12 2012 767 775
51. J.E. Visvader, and G.J. Lindeman Cancer stem cells: current status and evolving complexities Cell Stem Cell 10 2012 717 728
52. M. Shibata, and M.M. Shen The roots of cancer: stem cells and the basis for tumor heterogeneity Bioessays 35 2013 253 260
53. N. Navin, J. Kendall, and J. Troge Tumour evolution inferred by single-cell sequencing Nature 472 2011 90 94
54. A. Sottoriva, I. Spiteri, D. Shibata, C. Curtis, and S. Tavare Single-molecule genomic data delineate patient-specific tumor profiles and cancer stem cell organization Cancer Res 73 2013 41 49
55. A. Kreso, C.A. O'Brien, and P. van Galen Variable clonal repopulation dynamics influence chemotherapy response in colorectal cancer Science 339 2013 543 548
56. S.A. Mani, W. Guo, and M.J. Liao The epithelial-mesenchymal transition generates cells with properties of stem cells Cell 133 2008 704 715
57. S. Pece, D. Tosoni, and S. Confalonieri Biological and molecular heterogeneity of breast cancers correlates with their cancer stem cell content Cell 140 2010 62 73
58. M. Krause, D. Zips, H.D. Thames, J. Kummermehr, and M. Baumann Preclinical evaluation of molecular-targeted anticancer agents for radiotherapy Radiother Oncol 80 2006 112 122
59. D. Zips, W. Eicheler, and P. Geyer Enhanced susceptibility of irradiated tumor vessels to vascular endothelial growth factor receptor tyrosine kinase inhibition Cancer Res 65 2005 5374 5379
60. C. Lagadec, E. Vlashi, L. Della Donna, C. Dekmezian, and F. Pajonk Radiation-induced reprogramming of breast cancer cells Stem Cells 30 2012 833 844
61. D.H. Nguyen, H.A. Oketch-Rabah, and I. Illa-Bochaca Radiation acts on the microenvironment to affect breast carcinogenesis by distinct mechanisms that decrease cancer latency and affect tumor type Cancer Cell 19 2011 640 651
62. M. Nishi, Y. Sakai, and H. Akutsu Induction of cells with cancer stem cell properties from nontumorigenic human mammary epithelial cells by defined reprogramming factors Oncogene 2013 http://dx.doi.org/10.1038/onc.2012.614 [Epub ahead of print].
63. S.M. Cabarcas, L.A. Mathews, and W.L. Farrar The cancer stem cell niche - there goes the neighborhood? Int J Cancer 129 2011 2315 2327
64. F. Hirschhaeuser, H. Menne, C. Dittfeld, J. West, W. Mueller-Klieser, and L.A. Kunz-Schughart Multicellular tumor spheroids: an underestimated tool is catching up again J Biotechnol 148 2010 3 15
65. S.F. Chen, Y.C. Chang, S. Nieh, C.L. Liu, C.Y. Yang, and Y.S. Lin Nonadhesive culture system as a model of rapid sphere formation with cancer stem cell properties PLoS One 7 2012 e31864
66. G. Zhang, L. Ma, Y.K. Xie, X.B. Miao, and C. Jin Esophageal cancer tumorspheres involve cancer stem-like populations with elevated aldehyde dehydrogenase enzymatic activity Mol Med Rep 6 2012 519 524
67. L.S. Piao, W. Hur, and T.K. Kim CD133+ liver cancer stem cells modulate radioresistance in human hepatocellular carcinoma Cancer Lett 315 2012 129 137
68. O. Al-Assar, R.J. Muschel, T.S. Mantoni, W.G. McKenna, and T.B. Brunner Radiation response of cancer stem-like cells from established human cell lines after sorting for surface markers Int J Radiat Oncol Biol Phys 75 2009 1216 1225
69. C. Dittfeld, A. Dietrich, and S. Peickert CD133 expression is not selective for tumor-initiating or radioresistant cell populations in the CRC cell line HCT-116 Radiother Oncol 94 2010 375 383
70. M. Baumann, W. DuBois, A. Pu, J. Freeman, and H.D. Suit Response of xenografts of human malignant gliomas and squamous cell carcinomas to fractionated irradiation Int J Radiat Oncol Biol Phys 23 1992 803 809
71. R.F. Kallman Rodent tumor models in experimental cancer therapy 1987 Pergamon Press 111 113 [chapter 5/27]
72. J. Overgaard Rodent tumor models in experimental cancer therapy 1987 Pergamon Press 128 132 [chapter 5/30]
73. H.D. Suit, and H. Thames Rodent tumor models in experimental cancer therapy 1987 Pergamon Press 138 148 [chapter 5/32]
74. K. Gurtner, Y. Deuse, and R. Butof Diverse effects of combined radiotherapy and EGFR inhibition with antibodies or TK inhibitors on local tumour control and correlation with EGFR gene expression Radiother Oncol 99 2011 323 330
75. A. Menegakis, W. Eicheler, A. Yaromina, H.D. Thames, M. Krause, and M. Baumann Residual DNA double strand breaks in perfused but not in unperfused areas determine different radiosensitivity of tumours Radiother Oncol 100 2011 137 144
76. A. Menegakis, A. Yaromina, and W. Eicheler Prediction of clonogenic cell survival curves based on the number of residual DNA double strand breaks measured by gammaH2AX staining Int J Radiat Biol 85 2009 1032 1041
77. Koch U, Höhne K, von Neubeck C, et al. Residual gH2AX foci predict local tumour control after radiotherapy. Radiat Oncol, 2013, submitted for publication [RO-D-13-00410].
78. M. Nordsmark, S.M. Bentzen, and V. Rudat Prognostic value of tumor oxygenation in 397 head and neck tumors after primary radiation therapy. An international multi-center study Radiother Oncol 77 2005 18 24
79. K. Toustrup, B.S. Sorensen, and M. Nordsmark Development of a hypoxia gene expression classifier with predictive impact for hypoxic modification of radiotherapy in head and neck cancer Cancer Res 71 2011 5923 5931
80. A. Yaromina, H. Thames, and X. Zhou Radiobiological hypoxia, histological parameters of tumour microenvironment and local tumour control after fractionated irradiation Radiother Oncol 96 2010 116 122
81. V. Quennet, A. Yaromina, and D. Zips Tumor lactate content predicts for response to fractionated irradiation of human squamous cell carcinomas in nude mice Radiother Oncol 81 2006 130 135
82. K.K. Ang, J. Harris, and R. Wheeler Human papillomavirus and survival of patients with oropharyngeal cancer N Engl J Med 363 2010 24 35
83. K.K. Ang, and E.M. Sturgis Human papillomavirus as a marker of the natural history and response to therapy of head and neck squamous cell carcinoma Semin Radiat Oncol 22 2012 128 142
84. T. Akimoto, N.R. Hunter, L. Buchmiller, K. Mason, K.K. Ang, and L. Milas Inverse relationship between epidermal growth factor receptor expression and radiocurability of murine carcinomas Clin Cancer Res 5 1999 2884 2890
85. J.G. Eriksen, T. Steiniche, and J. Overgaard The influence of epidermal growth factor receptor and tumor differentiation on the response to accelerated radiotherapy of squamous cell carcinomas of the head and neck in the randomized DAHANCA 6 and 7 study Radiother Oncol 74 2005 93 100
86. K. Iida, K. Nakayama, and M.T. Rahman EGFR gene amplification is related to adverse clinical outcomes in cervical squamous cell carcinoma, making the EGFR pathway a novel therapeutic target Br J Cancer 105 2011 420 427
87. E.P. Hui, F.L. Sung, and B.K. Yu Plasma osteopontin, hypoxia, and response to radiotherapy in nasopharyngeal cancer Clin Cancer Res 14 2008 7080 7087
88. J. Overgaard, J.G. Eriksen, M. Nordsmark, J. Alsner, and M.R. Horsman Plasma osteopontin, hypoxia, and response to the hypoxia sensitiser nimorazole in radiotherapy of head and neck cancer: results from the DAHANCA 5 randomised double-blind placebo-controlled trial Lancet Oncol 6 2005 757 764
89. M.R. Horsman, L.S. Mortensen, J.B. Petersen, M. Busk, and J. Overgaard Imaging hypoxia to improve radiotherapy outcome Nat Rev Clin Oncol 9 2012 674 687
90. D. Zips, K. Zophel, and N. Abolmaali Exploratory prospective trial of hypoxia-specific PET imaging during radiochemotherapy in patients with locally advanced head-and-neck cancer Radiother Oncol 105 2012 21 28
91. H.R. Withers Biologic basis for altered fractionation schemes Cancer 55 1985 2086 2095
92. H.R. Withers, J.M. Taylor, and B. Maciejewski The hazard of accelerated tumor clonogen repopulation during radiotherapy Acta Oncol 27 1988 131 146
93. W. Budach, D. Gioioso, A. Taghian, M. Stuschke, and H.D. Suit Repopulation capacity during fractionated irradiation of squamous cell carcinomas and glioblastomas in vitro Int J Radiat Oncol Biol Phys 39 1997 743 750
94. F. Hessel, M. Krause, and C. Petersen Repopulation of moderately well-differentiated and keratinizing GL human squamous cell carcinomas growing in nude mice Int J Radiat Oncol Biol Phys 58 2004 510 518
95. C. Petersen, D. Zips, and M. Krause Repopulation of FaDu human squamous cell carcinoma during fractionated radiotherapy correlates with reoxygenation Int J Radiat Oncol Biol Phys 51 2001 483 493
96. S. Dische, M. Saunders, A. Barrett, A. Harvey, D. Gibson, and M. Parmar A randomised multicentre trial of CHART versus conventional radiotherapy in head and neck cancer Radiother Oncol 44 1997 123 136
97. J. Overgaard, H.S. Hansen, and L. Specht Five compared with six fractions per week of conventional radiotherapy of squamous-cell carcinoma of head and neck: DAHANCA 6 and 7 randomised controlled trial Lancet 362 2003 933 940
98. R. Bütof, and M. Baumann Time in radiation oncology - keep it short! Radiother Oncol 106 2013 271 275
99. A.C. Begg, K. Haustermans, and A.A. Hart The value of pretreatment cell kinetic parameters as predictors for radiotherapy outcome in head and neck cancer: a multicenter analysis Radiother Oncol 50 1999 13 23
100. A. Trumpp, M. Essers, and A. Wilson Awakening dormant haematopoietic stem cells Nat Rev Immunol 10 2010 201 209
101. K. Ito, R. Bernardi, and A. Morotti PML targeting eradicates quiescent leukaemia-initiating cells Nature 453 2008 1072 1078
102. S.M. Bentzen Repopulation in radiation oncology: perspectives of clinical research Int J Radiat Biol 79 2003 581 585
103. O. Hansen, J. Overgaard, and H.S. Hansen Importance of overall treatment time for the outcome of radiotherapy of advanced head and neck carcinoma: dependency on tumor differentiation Radiother Oncol 43 1997 47 51
104. K. Gurtner, F. Hessel, and W. Eicheler Combined treatment of the immunoconjugate bivatuzumab mertansine and fractionated irradiation improves local tumour control in vivo Radiother Oncol 102 2012 444 449
105. P.D. Bos, X.H. Zhang, and C. Nadal Genes that mediate breast cancer metastasis to the brain Nature 459 2009 1005 1009
106. A.J. Minn, G.P. Gupta, and P.M. Siegel Genes that mediate breast cancer metastasis to lung Nature 436 2005 518 524
107. K.L. Andarawewa, S.V. Costes, and I. Fernandez-Garcia Lack of radiation dose or quality dependence of epithelial-to-mesenchymal transition (EMT) mediated by transforming growth factor beta Int J Radiat Oncol Biol Phys 79 2011 1523 1531
108. K.L. Andarawewa, A.C. Erickson, and W.S. Chou Ionizing radiation predisposes nonmalignant human mammary epithelial cells to undergo transforming growth factor beta induced epithelial to mesenchymal transition Cancer Res 67 2007 8662 8670
109. Y.C. Zhou, J.Y. Liu, and J. Li Ionizing radiation promotes migration and invasion of cancer cells through transforming growth factor-beta-mediated epithelial-mesenchymal transition Int J Radiat Oncol Biol Phys 81 2011 1530 1537
110. P. Friedl, J. Locker, E. Sahai, and J.E. Segall Classifying collective cancer cell invasion Nat Cell Biol 14 2012 777 783
111. A.A. Khalil, and P. Friedl Determinants of leader cells in collective cell migration Integr Biol (Camb) 2 2010 568 574
112. A. Allam, D. Gioioso, A. Taghian, M. Duffy, I.J. Fidler, and H.D. Suit Intrinsic radiation sensitivity: no correlation with the metastatic potential of human and murine tumor cell lines J Natl Cancer Inst 85 1993 1954 1957
113. H.D. Suit, R.S. Sedlacek, and E.L. Gillette Examination for a correlation between probabilities of development of distant metastasis and of local recurrence Radiology 95 1970 189 194
114. M. Baumann, H.D. Suit, and R.S. Sedlacek Metastases after fractionated radiation therapy of three murine tumor models Int J Radiat Oncol Biol Phys 19 1990 367 370
115. J. Ramsay, H.D. Suit, and R. Sedlacek Experimental studies on the incidence of metastases after failure of radiation treatment and the effect of salvage surgery Int J Radiat Oncol Biol Phys 14 1988 1165 1168
116. C. Moncharmont, A. Levy, and M. Gilormini Targeting a cornerstone of radiation resistance: cancer stem cell Cancer Lett 322 2012 139 147
117. X. Cui, K. Oonishi, and H. Tsujii Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays Cancer Res 71 2011 3676 3687
118. P. Metellus, I. Nanni-Metellus, and C. Delfino Prognostic impact of CD133 mRNA expression in 48 glioblastoma patients treated with concomitant radiochemotherapy: a prospective patient cohort at a single institution Ann Surg Oncol 18 2011 2937 2945
119. S.T. Avoranta, E.A. Korkeila, K.J. Syrjanen, S.O. Pyrhonen, and J.T. Sundstrom Lack of CD44 variant 6 expression in rectal cancer invasive front associates with early recurrence World J Gastroenterol 18 2012 4549 4556