The phenotypic radiation resistance of CD44 +/CD24 -or low breast cancer cells is mediated through the enhanced activation of ATM signaling

PLoS ONE

Volumn 6, Issue 9, 2011, Pages

  Yin, Hong ^a   Glass, Jonathan ^a  

^a LOUISIANA STATE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ATM PROTEIN; CD24 ANTIGEN; HERMES ANTIGEN; CELL CYCLE PROTEIN; DNA BINDING PROTEIN; MRE11A PROTEIN, HUMAN; NBN PROTEIN, HUMAN; NUCLEAR PROTEIN; PROTEIN SERINE THREONINE KINASE; TUMOR SUPPRESSOR PROTEIN;

ARTICLE; BREAST CANCER; CANCER CELL; CANCER CELL CULTURE; CANCER INITIATING CELL; CELL STRUCTURE; CELL SUBPOPULATION; DNA REPAIR; HUMAN; HUMAN CELL; NONHOMOLOGOUS END JOINING; PHENOTYPE; PROTEIN EXPRESSION; RADIOSENSITIVITY; SIGNAL TRANSDUCTION; BIOSYNTHESIS; BREAST TUMOR; CELL PROLIFERATION; CYTOLOGY; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; METABOLISM; METHODOLOGY; PHOSPHORYLATION; STEM CELL; TUMOR CELL LINE;

ANTIGENS, CD24; ANTIGENS, CD44; BREAST NEOPLASMS; CELL CYCLE PROTEINS; CELL LINE, TUMOR; CELL PROLIFERATION; DNA REPAIR; DNA-BINDING PROTEINS; FEMALE; FLOW CYTOMETRY; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; NUCLEAR PROTEINS; PHENOTYPE; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; STEM CELLS; TUMOR SUPPRESSOR PROTEINS;

EID: 80052841288     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0024080     Document Type: Article

References (43)

1. Ponti D, Zaffaroni N, Capelli C, Daidone MG, (2006) Breast cancer stem cells: an overview. Eur J Cancer 42: 1219-1224.
2. Woodward WA, Chen MS, Behbod F, Rosen JM, (2005) On mammary stem cells. J Cell Sci 118: 3585-3594.
3. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF, (2003) Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 100: 3983-3988.
4. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, et al. (2007) Molecular definition of breast tumor heterogeneity. Cancer Cell 11: 259-273.
5. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI, (2011) The CD44+/CD24- phenotype relates to 'triple-negative' state and unfavorable prognosis in breast cancer patients. Med Oncol 28: 745-752.
6. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, et al. (2005) Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 65: 5506-5511.
7. Fillmore CM, Kuperwasser C, (2008) Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 10: R25.
8. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, et al. (2006) CD44+/CD24- breast cancer cells exhibit enhanced invasive properties: an early step necessary for metastasis. Breast Cancer Res 8: R59.
9. Lou H, Dean M, (2007) Targeted therapy for cancer stem cells: the patched pathway and ABC transporters. Oncogene 26: 1357-1360.
10. Diehn M, Clarke MF, (2006) Cancer stem cells and radiotherapy: new insights into tumor radioresistance. J Natl Cancer Inst 98: 1755-1757.
11. Woodward WA, Chen MS, Behbod F, Alfaro MP, Buchholz TA, et al. (2007) WNT/beta-catenin mediates radiation resistance of mouse mammary progenitor cells. Proc Natl Acad Sci U S A 104: 618-623.
12. Chuthapisith S, Eremin J, El-Sheemey M, Eremin O, (2010) Breast cancer chemoresistance: emerging importance of cancer stem cells. Surg Oncol 19: 27-32.
13. Phillips TM, McBride WH, Pajonk F, (2006) The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 98: 1777-1785.
14. Lagadec C, Vlashi E, Della Donna L, Meng Y, Dekmezian C, et al. (2010) Survival and self-renewing capacity of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 12: R13.
15. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, et al. (2009) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458: 780-783.
16. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, et al. (2006) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444: 756-760.
17. Chiou SH, Kao CL, Chen YW, Chien CS, Hung SC, et al. (2008) Identification of CD133-positive radioresistant cells in atypical teratoid/rhabdoid tumor. PLoS ONE 3: e2090.
18. Karimi-Busheri F, Rasouli-Nia A, Mackey JR, Weinfeld M, (2010) Senescence evasion by MCF-7 human breast tumor-initiating cells. Breast Cancer Res 12: R31.
19. Jo M, Lester RD, Montel V, Eastman B, Takimoto S, et al. (2009) Reversibility of epithelial-mesenchymal transition (EMT) induced in breast cancer cells by activation of urokinase receptor-dependent cell signaling. J Biol Chem 284: 22825-22833.
20. Zou L, Hazan R, Roy P, (2009) Profilin-1 overexpression restores adherence junctions in MDA-MB-231 breast cancer cells in R-cadherin-dependent manner. Cell Motil Cytoskeleton.
21. Blick T, Widodo E, Hugo H, Waltham M, Lenburg ME, et al. (2008) Epithelial mesenchymal transition traits in human breast cancer cell lines. Clin Exp Metastasis 25: 629-642.
22. Rogakou EP, Boon C, Redon C, Bonner WM, (1999) Megabase chromatin domains involved in DNA double-strand breaks in vivo. J Cell Biol 146: 905-916.
23. Tian B, Yang Q, Mao Z, (2009) Phosphorylation of ATM by Cdk5 mediates DNA damage signalling and regulates neuronal death. Nat Cell Biol 11: 211-218.
24. Dave B, Chang J, (2009) Treatment resistance in stem cells and breast cancer. J Mammary Gland Biol Neoplasia 14: 79-82.
25. Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, et al. (2007) ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell 1: 555-567.
26. Morimoto K, Kim SJ, Tanei T, Shimazu K, Tanji Y, et al. (2009) Stem cell marker aldehyde dehydrogenase 1-positive breast cancers are characterized by negative estrogen receptor, positive human epidermal growth factor receptor type 2, and high Ki67 expression. Cancer Sci 100: 1062-1068.
27. Nakshatri H, (2010) Radiation resistance in breast cancer: are CD44+/CD24-/proteosome low/PKH26+ cells to blame? Breast Cancer Res 12: 105.
28. Sajithlal GB, Rothermund K, Zhang F, Dabbs DJ, Latimer JJ, et al. (2010) Permanently blocked stem cells derived from breast cancer cell lines. Stem Cells 28: 1008-1018.
29. Al-Assar O, Muschel RJ, Mantoni TS, McKenna WG, Brunner TB, (2009) Radiation response of cancer stem-like cells from established human cell lines after sorting for surface markers. Int J Radiat Oncol Biol Phys 75: 1216-1225.
30. Trosko JE, (2006) From adult stem cells to cancer stem cells: Oct-4 Gene, cell-cell communication, and hormones during tumor promotion. Ann N Y Acad Sci 1089: 36-58.
31. Murat A, Migliavacca E, Gorlia T, Lambiv WL, Shay T, et al. (2008) 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.
32. Milas L, Hittelman WN, (2009) Cancer stem cells and tumor response to therapy: current problems and future prospects. Semin Radiat Oncol 19: 96-105.
33. Diehn M, Cho RW, Clarke MF, (2009) Therapeutic implications of the cancer stem cell hypothesis. Semin Radiat Oncol 19: 78-86.
34. Patrawala L, Calhoun T, Schneider-Broussard R, Zhou J, Claypool K, et al. (2005) Side population is enriched in tumorigenic, stem-like cancer cells, whereas ABCG2+ and ABCG2- cancer cells are similarly tumorigenic. Cancer Res 65: 6207-6219.
35. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. (2008) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133: 704-715.
36. Lavin MF, (2008) Ataxia-telangiectasia: from a rare disorder to a paradigm for cell signalling and cancer. Nat Rev Mol Cell Biol 9: 759-769.
37. Lavin MF, Kozlov S, Gueven N, Peng C, Birrell G, et al. (2005) Atm and cellular response to DNA damage. Adv Exp Med Biol 570: 457-476.
38. Haince JF, Kozlov S, Dawson VL, Dawson TM, Hendzel MJ, et al. (2007) Ataxia telangiectasia mutated (ATM) signaling network is modulated by a novel poly(ADP-ribose)-dependent pathway in the early response to DNA-damaging agents. J Biol Chem 282: 16441-16453.
39. Matsuoka S, Ballif BA, Smogorzewska A, McDonald ER 3rd, Hurov KE, et al. (2007) ATM and ATR substrate analysis reveals extensive protein networks responsive to DNA damage. Science 316: 1160-1166.
40. Golding SE, Rosenberg E, Valerie N, Hussaini I, Frigerio M, et al. (2009) Improved ATM kinase inhibitor KU-60019 radiosensitizes glioma cells, compromises insulin, AKT and ERK prosurvival signaling, and inhibits migration and invasion. Mol Cancer Ther 8: 2894-2902.
41. Rainey MD, Charlton ME, Stanton RV, Kastan MB, (2008) Transient inhibition of ATM kinase is sufficient to enhance cellular sensitivity to ionizing radiation. Cancer Res 68: 7466-7474.
42. Li Y, Yang DQ, (2010) The ATM inhibitor KU-55933 suppresses cell proliferation and induces apoptosis by blocking Akt in cancer cells with overactivated Akt. Mol Cancer Ther 9: 113-125.
43. Hickson I, Zhao Y, Richardson CJ, Green SJ, Martin NM, et al. (2004) Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res 64: 9152-9159.