Radiotherapy targeting cancer stem cells: Current views and future perspectives

Anticancer Research

Volumn 33, Issue 3, 2013, Pages 747-754

  Ogawa, Kazuhiko ^a   Yoshioka, Yasuo ^a   Isohashi, Fumiaki ^a   Seo, Yuji ^a   Yoshida, Ken ^b   Yamazaki, Hideya ^c  

^a OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b OSAKA MEDICAL COLLEGE   (Japan)

^c KYOTO PREFECTURAL UNIVERSITY OF MEDICINE   (Japan)

Author keywords

Cancer stem cells; Radioresistance; Radiotherapy; Review; Therapeutic targets

Indexed keywords

ALDEHYDE DEHYDROGENASE; ATM PROTEIN; AUTOPHAGY PROTEIN 5; BECLIN 1; BETA CATENIN; BMI1 PROTEIN; BONE MORPHOGENETIC PROTEIN; CANCER TESTIS ANTIGEN; CD133 ANTIGEN; CHECKPOINT KINASE 1; CHECKPOINT KINASE 2; COPPER 64 DIACETYL BIS(N4 METHYTHIOSEMICARBAZONE); EPIDERMAL GROWTH FACTOR RECEPTOR; HERMES ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; MITOGEN ACTIVATED PROTEIN KINASE; NOTCH RECEPTOR; OCTAMER TRANSCRIPTION FACTOR 4; PROTEIN KINASE C DELTA; RADIOPHARMACEUTICAL AGENT; REACTIVE OXYGEN METABOLITE; SIRTUIN 1; SONIC HEDGEHOG PROTEIN; STAT3 PROTEIN; TELOMERASE; TRANSCRIPTION FACTOR SLUG; TRANSCRIPTION FACTOR SNAIL; UNCLASSIFIED DRUG; UNINDEXED DRUG; VASCULAR ENDOTHELIAL CADHERIN; WNT PROTEIN;

CANCER PROGNOSIS; CANCER RADIOTHERAPY; CANCER STEM CELL; CELL FATE; CELL RENEWAL; DNA DAMAGE; DNA END JOINING REPAIR; DNA REPAIR; EPITHELIAL MESENCHYMAL TRANSITION; GAMMA KNIFE RADIOSURGERY; GLIOBLASTOMA; GLIOMA; HUMAN; ION THERAPY; OUTCOME ASSESSMENT; PRIORITY JOURNAL; RADIOSENSITIVITY; REVIEW; SIGNAL TRANSDUCTION; STEM CELL NICHE;

ANIMALS; ANTIGENS, CD; BIOLOGICAL MARKERS; DNA REPAIR; GLYCOPROTEINS; HUMANS; NEOPLASMS; NEOPLASTIC STEM CELLS; PEPTIDES; RADIATION TOLERANCE; REACTIVE OXYGEN SPECIES;

EID: 84875896209     PISSN: 02507005     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (67)

1. Seaberg RM and van der Kooy D: Stem and progenitor cells: the premature desertion of rigorous definitions. Trends Neurosci 26: 125-131, 2003.
2. Lapidot T, Sirard C, Vormoor J, Murdoch B, Hoang T, Caceres- Cortes J, Minden M, Paterson B, Caligiuri MA and Dick JE: A cell initiating human acute myeloid leukaemia after transplantation into SCID mice. Nature 367: 645-648 1994.
3. Koch U, Krause M and Baumann M: Cancer stem cells at the crossroads of current cancer therapy failures - radiation oncology perspective. Semin Cancer Biol 20: 116-124, 2010.
4. Piccirillo SG, Reynolds BA, Zanetti N, Lamorte G, Binda E, Broggi G, Brem H, Olivi A, Dimeco F and Vescovi AL: Bone morphogenetic proteins inhibit the tumorigenic potential of human brain tumour-initiating cells. Nature 444: 761-765, 2006.
5. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, Hung SC, Chang YL, Tsai ML, Lee YY, Ku HH and Chiou SH: Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS One 3: e2637, 2008.
6. Wang J, Wakeman TP, Lathia JD, Hjelmeland AB, Wang XF, White RR, Rich JN and Sullenger BA: Notch promotes radioresistance of glioma stem cells. Stem Cells 28: 17-28, 2010.
7. Phillips TM, McBride WH and Pajonk F: The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785, 2006.
8. Kurrey NK, Jalgaonkar SP, Joglekar AV, Ghanate AD, Chaskar PD, Doiphode RY and Bapat SA: Snail and slug mediate radioresistance and chemoresistance by antagonizing p53- mediated apoptosis and acquiring a stem-like phenotype in ovarian cancer cells. Stem Cells 27: 2059-2068, 2009.
9. Chen MS, Woodward WA, Behbod F, Peddibhotla S, Alfaro MP, Buchholz TA and Rosen JM: Wnt/beta-catenin mediates radiation resistance of Sca1+ progenitors in an immortalized mammary gland cell line. J Cell Sci 120: 468-477, 2007.
10. Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA and Rosen JM: Wnt/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci USA 104: 618-623, 2007.
11. Liu ZG, Liu L, Xu LH, Yi W, Tao YL, Tu ZW, Li MZ, Zeng MS and Xia YF: BMI-1 induces radioresistance in MCF-7 mammary carcinoma cells. Oncol Rep 27: 1116-1122, 2012.
12. Facchino S, Abdouh M, Chatoo W and Bernier G: BMI1 confers radioresistance to normal and cancerous neural stem cells through recruitment of the DNA damage response machinery. J Neurosci 30: 10096-10111, 2010.
13. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, Dewhirst MW, Bigner DD and Rich JN: Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760, 2006.
14. Yin H and Glass J: The phenotypic radiation resistance of CD44+/CD24(-or low) breast cancer cells is mediated through the enhanced activation of ATM signaling. PLoS One 6: e24080, 2011.
15. D'Andrea FP, Safwat A, Kassem M, Gautier L, Overgaard J and Horsman MR: Cancer stem cell overexpression of nicotinamide N-methyltransferase enhances cellular radiation resistance. Radiother Oncol 99: 373-378, 2011.
16. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, Qian D, Lam JS, Ailles LE, Wong M, Joshua B, Kaplan MJ, Wapnir I, Dirbas FM, Somlo G, Garberoglio C, Paz B, Shen J, Lau SK, Quake SR, Brown JM, Weissman IL and Clarke MF: Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783, 2009.
17. Svendsen A, Verhoeff JJ, Immervoll H, Brogger JC, Kmiecik J, Poli A, Netland IA, Prestegarden L, Planaguma J, Torsvik A, Kjersem AB, Sakariassen PO, Heggdal JI, Van Furth WR, Bjerkvig R, Lund-Johansen M, Enger PO, Felsberg J, Brons NH, Tronstad KJ, Waha A and Chekenya M: Expression of the progenitor marker NG2/CSPG4 predicts poor survival and resistance to ionising radiation in glioblastoma. Acta Neuropathol 122: 495-510, 2011.
18. Jamal M, Rath BH, Williams ES, Camphausen K and Tofilon PJ: Microenvironmental regulation of glioblastoma radioresponse. Clin Cancer Res 16: 6049-6059, 2010.
19. Lomonaco SL, Finniss S, Xiang C, Decarvalho A, Umansky F, Kalkanis SN, Mikkelsen T and Brodie C: The induction of autophagy by gamma-radiation contributes to the radioresistance of glioma stem cells. Int J Cancer 125: 717-722, 2009.
20. Kim MJ, Kim RK, Yoon CH, An S, Hwang SG, Suh Y, Park MJ, Chung HY, Kim IG and Lee SJ: Importance of PKCδ signaling in fractionated-radiation- induced expansion of glioma-initiating cells and resistance to cancer treatment. J Cell Sci 124: 3084-3094, 2011.
21. Liu S and Wicha MS: Targeting breast cancer stem cells. J Clin Oncol 28: 4006-4012, 2010.
22. Blazek ER, Foutch JL and Maki G: Daoy medulloblastoma cells that express CD133 are radioresistant relative to CD133- cells, and the CD133+ sector is enlarged by hypoxia. Int J Radiat Oncol Biol Phys 67: 1-5, 2007.
23. Kim HM, Haraguchi N, Ishii H, Ohkuma M, Okano M, Mimori K, Eguchi H, Yamamoto H, Nagano H, Sekimoto M, Doki Y and Mori M: Increased CD13 expression reduces reactive oxygen species, promoting survival of liver cancer stem cells via an epithelialmesenchymal transition-like phenomenon. Ann Surg Oncol 19: S539-548, 2012.
24. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, Hamou MF, de Tribolet N, Regli L, Wick W, Kouwenhoven MC, Hainfellner JA, Heppner FL, Dietrich PY, Zimmer Y, Cairncross JG, Janzer RC, Domany E, Delorenzi M, Stupp R and Hegi ME: 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: 3015-3024, 2008.
25. Tamura K, Aoyagi M, Wakimoto H, Ando N, Nariai T, Yamamoto M and Ohno K: Accumulation of CD133-positive glioma cells after high-dose irradiation by gamma knife surgery plus external beam radiation. J Neurosurg 113: 310-318, 2010.
26. Saigusa S, Tanaka K, Toiyama Y, Yokoe T, Okugawa Y, Kawamoto A, Yasuda H, Morimoto Y, Fujikawa H, Inoue Y, Miki C and Kusunoki M: Immunohistochemical features of CD133 expression: Association with resistance to chemoradiotherapy in rectal cancer. Oncol Rep 24: 345-350, 2010.
27. Shien K, Toyooka S, Ichimura K, Soh J, Furukawa M, Maki Y, Muraoka T, Tanaka N, Ueno T, Asano H, Tsukuda K, Yamane M, Oto T, Kiura K and Miyoshi S: Prognostic impact of cancer stem cell-related markers in non-small cell lung cancer patients treated with induction chemoradiotherapy. Lung Cancer 77: 162-167, 2012.
28. de Jong MC, Pramana J, van der Wal JE, Lacko M, Peutz-Kootstra CJ, de Jong JM, Takes RP, Kaanders JH, van der Laan BF, Wachters J, Jansen JC, Rasch CR, van Velthuysen ML, Grenman R, Hoebers FJ, Schuuring E, van den Brekel MW and Begg AC: CD44 expression predicts local recurrence after radiotherapy in larynx cancer. Clin Cancer Res 16: 5329-5338, 2010.
29. Chiou SH, Kao CL, Chen YW, Chien CS, Hung SC, Lo JF, Chen YJ, Ku HH, Hsu MT and Wong TT: Identification of CD133- positive radioresistant cells in atypical teratoid/rhabdoid tumor. PLoS One 3: e2090, 2008.
30. Kao CL, Huang PI, Tsai PH, Tsai ML, Lo JF, Lee YY, Chen YJ, Chen YW and Chiou SH: Resveratrol-induced apoptosis and increased radiosensitivity in CD133-positive cells derived from atypical teratoid/rhabdoid tumor. Int J Radiat Oncol Biol Phys 74: 219-228, 2009.
31. Lagadec C, Vlashi E, Della Donna L, Meng Y, Dekmezian C, Kim K and Pajonk F: Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 12: R13, 2010.
32. Zeng J, Aziz K, Chettiar ST, Aftab BT, Armour M, Gajula R, Gandhi N, Salih T, Herman JM, Wong J, Rudin CM, Tran PT and Hales RK: Hedgehog Pathway Inhibition radiosensitizes non-small cell lung cancers. Int J Radiat Oncol Biol Phys doi:pii: S0360-3016(12)03664-4, 2012.
33. Ponnurangam S, Mammen JM, Ramalingam S, He Z, Zhang Y, Umar S, Subramaniam D and Anant S: Honokiol in combination with radiation targets Notch signaling to inhibit colon cancer stem cells. Mol Cancer Ther 11: 963-972, 2012.
34. Yu S, Zhang R, Liu F, Wang H, Wu J and Wang Y: Notch inhibition suppresses nasopharyngeal carcinoma by depleting cancer stemlike side population cells. Oncol Rep 28: 561-566, 2012.
35. Croker AK and Allan AL: Inhibition of aldehyde dehydrogenase (ALDH) activity reduces chemotherapy and radiation resistance of stem-like ALDHhiCD44+ human breast cancer cells. Breast Cancer Res Treat 133: 75-87, 2012.
36. Chen YC, Chang CJ, Hsu HS, Chen YW, Tai LK, Tseng LM, Chiou GY, Chang SC, Kao SY, Chiou SH and Lo WL: Inhibition of tumorigenicity and enhancement of radiochemosensitivity in head and neck squamous cell cancer-derived ALDH1-positive cells by knockdown of Bmi-1. Oral Oncol 46: 158-165, 2010.
37. Zhang M, Atkinson RL and Rosen JM: Selective targeting of radiation-resistant tumor-initiating cells. Proc Natl Acad Sci USA 107: 3522-3527, 2010.
38. Hsu HS, Huang PI, Chang YL, Tzao C, Chen YW, Shih HC, Hung SC, Chen YC, Tseng LM and Chiou SH: Cucurbitacin I inhibits tumorigenic ability and enhances radiochemosensitivity in nonsmall cell lung cancer-derived CD133-positive cells. Cancer 117: 2970-2985, 2011.
39. Kang KB, Zhu C, Wong YL, Gao Q, Ty A and Wong MC: Gefitinib radiosensitizes stem-like glioma cells: inhibition of epidermal growth factor receptor-AKT-DNA-PK signaling, accompanied by inhibition of DNA double-strand break repair. Int J Radiat Oncol Biol Phys 83: e43-52, 2012.
40. Chen YW, Chen KH, Huang PI, Chen YC, Chiou GY, Lo WL, Tseng LM, Hsu HS, Chang KW and Chiou SH: Cucurbitacin I suppressed stem-like property and enhanced radiation-induced apoptosis in head and neck squamous carcinoma - derived CD44(+)ALDH1(+) cells. Mol Cancer Ther 9: 2879-2892, 2010.
41. Song CW, Lee H, Dings RP, Williams B, Powers J, Santos TD, Choi BH and Park HJ: Metformin kills and radiosensitizes cancer cells and preferentially kills cancer stem cells. Sci Rep 2: 362. doi: 10.1038/srep00362, 2012.
42. Evers P, Lee PP, DeMarco J, Agazaryan N, Sayre JW, Selch M and Pajonk F: Irradiation of the potential cancer stem cell niches in the adult brain improves progression-free survival of patients with malignant glioma. BMC Cancer 10: 384, 2010.
43. Gupta T, Nair V, Paul SN, Kannan S, Moiyadi A, Epari S and Jalali R: Can irradiation of potential cancer stem-cell niche in the subventricular zone influence survival in patients with newly diagnosed glioblastoma? J Neurooncol 109: 195-203, 2012.
44. Yawata T, Nakai E, Park KC, Chihara T, Kumazawa A, Toyonaga S, Masahira T, Nakabayashi H, Kaji T and Shimizu K: Enhanced expression of cancer testis antigen genes in glioma stem cells. Mol Carcinog 49: 532-544, 2010.
45. Zhuang W, Li B, Long L, Chen L, Huang Q and Liang Z: Induction of autophagy promotes differentiation of glioma-initiating cells and their radiosensitivity. Int J Cancer 129: 2720-2731, 2011.
46. Zhang X, Komaki R, Wang L, Fang B and Chang JY: Treatment of radioresistant stem-like esophageal cancer cells by an apoptotic gene-armed, telomerase-specific oncolytic adenovirus. Clin Cancer Res 14: 2813-2823, 2008.
47. Chang CJ, Hsu CC, Yung MC, Chen KY, Tzao C, Wu WF, Chou HY, Lee YY, Lu KH, Chiou SH and Ma HI: Enhanced radiosensitivity and radiation-induced apoptosis in glioma CD133-positive cells by knockdown of SirT1 expression. Biochem Biophys Res Commun 380: 236-242, 2009.
48. Vlashi E, Kim K, Lagadec C, Donna LD, McDonald JT, Eghbali M, Sayre JW, Stefani E, McBride W and Pajonk F: In vivo imaging, tracking, and targeting of cancer stem cells. J Natl Cancer Inst 101: 350-359, 2009.
49. Cui X, Oonishi K, Tsujii H, Yasuda T, Matsumoto Y, Furusawa Y, Akashi M, Kamada T and Okayasu R: Effects of carbon ion beam on putative colon cancer stem cells and its comparison with X-rays. Cancer Res 71: 3676-3687, 2011.
50. Kamlah F, Hanze J, Arenz A, Seay U, Hasan D, Juricko J, Bischoff B, Gottschald OR, Fournier C, Taucher-Scholz G, Scholz M, Seeger W, Engenhart-Cabillic R and Rose F: Comparison of the effects of carbon ion and photon irradiation on the angiogenic response in human lung adenocarcinoma cells. Int J Radiat Oncol Biol Phys 80: 1541-1549, 2011.
51. Yoshii Y, Furukawa T, Kiyono Y, Watanabe R, Mori T, Yoshii H, Asai T, Okazawa H, Welch MJ and Fujibayashi Y: Internal radiotherapy with copper-64-diacetyl-bis (N4-methylthiosemicarbazone) reduces CD133+ highly tumorigenic cells and metastatic ability of mouse colon carcinoma. Nucl Med Biol 38: 151-157, 2011.
52. Dirks PB: Brain tumor stem cells: bringing order to the chaos of brain cancer. J Clin Oncol 26: 2916-2924, 2008.
53. Leung C, Lingbeek M, Shakhova O, Liu J, Tanger E, Saremaslani P, Van Lohuizen M and Marino S: BMI1 is essential for cerebellar development and is overexpressed in human medulloblastomas. Nature 428: 337-341, 2004.
54. Gilbertson RJ and Rich JN: Making a tumour's bed: Glioblastoma stem cells and the vascular niche. Nat Rev Cancer 7: 733-736, 2007.
55. Moore KA and Lemischka IR: Stem cells and their niches. Science 311: 1880-1885, 2006.
56. Jin L, Hope KJ, Zhai Q, Smadja-Joffe F and Dick JE: Targeting of CD44 eradicates human acute myeloid leukemic stem cells. Nat Med 12: 1167-1174, 2006.
57. Krause DS, Lazarides K, von Andrian UH and Van Etten RA: Requirement for CD44 in homing and engraftment of BCRABL- expressing leukemic stem cells. Nat Med 12: 1175-1180, 2006.
58. Calabrese C, Poppleton H, Kocak M, Hogg TL, Fuller C, Hamner B, Oh EY, Gaber MW, Finklestein D, Allen M, Frank A, Bayazitov IT, Zakharenko SS, Gajjar A, Davidoff A and Gilbertson RJ: A perivascular niche for brain tumor stem cells. Cancer Cell 11: 69-82, 2007.
59. Gage FH, Coates PW, Palmer TD, Kuhn HG, Fisher LJ, Suhonen JO, Peterson DA, Suhr ST and Ray J: Survival and differentiation of adult neuronal progenitor cells transplanted to the adult brain. Proc Natl Acad Sci USA 92: 11879-11883, 1995
60. Reynolds BA and Weiss S: Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 255: 1707-1710, 1992.
61. Takebe N, Harris PJ, Warren RQ and Ivy SP: Targeting cancer stem cells by inhibiting Wnt, Notch, and Hedgehog pathways. Nat Rev Clin Oncol 8: 97-106, 2011.
62. Shigdar S, Lin J, Yu Y, Pastuovic M, Wei M and Duan W: RNA aptamer against a cancer stem cell marker epithelial cell adhesion molecule. Cancer Sci 102: 991-998, 2011.
63. Ogawa K, Ishiuchi S, Inoue O, Yoshii Y, Saito A, Watanabe T, Iraha S, Toita T, Kakinohana Y, Ariga T, Kasuya G and Murayama S: Phase II trial of radiotherapy after hyperbaric oxygenation with multiagent chemotherapy (procarbazine, nimustine, and vincristine) for high-grade gliomas: Long-term results. Int J Radiat Oncol Biol Phys 82: 732-738, 2012.
64. Brown JM: Tumor hypoxia in cancer therapy. Methods Enzymol 435: 297-321, 2007.
65. Eyler CE and Rich JN: Survival of the fittest: Cancer stem cells in therapeutic resistance and angiogenesis. J Clin Oncol 26: 2839-2845, 2008.
66. Tsurumi C, Esser N, Firat E, Gaedicke S, Follo M, Behe M, Elsasser-Beile U, Grosu AL, Graeser R and Niedermann G: Non-invasive in vivo imaging of tumor-associated CD133/prominin. PLoS One 5: e15605, 2010.
67. Niyazi M, Maihoefer C, Krause M, Rodel C, Budach W and Belka C: Radiotherapy and new drugs new side effects? Radiat Oncol 6: 177, 2011.