CD24-/low stem-like breast cancer marker defines the radiation-resistant cells involved in memorization and transmission of radiation-induced genomic instability

Oncogene

Volumn 32, Issue 2, 2013, Pages 251-258

  Bensimon, J ^a   Altmeyer Morel, S ^a   Benjelloun, H ^a   Chevillard, S ^a   Lebeau, J ^a  

^a INSTITUT DE RADIOPROTECTION ET DE SÛRETÉ NUCLÉAIRE   (France)

Author keywords

breast cancer stem cells; genomic instability; radiation effects

Indexed keywords

CD24 ANTIGEN;

APOPTOSIS; ARTICLE; BREAST CANCER; CANCER CELL; CANCER STEM CELL; CELL POPULATION; CELL PROLIFERATION; CELL SURVIVAL; CHROMOSOMAL INSTABILITY; GENOMIC INSTABILITY; HUMAN; HUMAN CELL; IRRADIATION; POLYPLOIDY; PRIORITY JOURNAL; PROGENY; PROTEIN EXPRESSION; RADIATION DOSE; RADIATION EXPOSURE; RADIOSENSITIVITY;

ANTIGENS, CD24; ANTIGENS, CD44; BREAST NEOPLASMS; CELL LINE, TUMOR; CHROMOSOME BREAKAGE; FEMALE; GENOMIC INSTABILITY; HUMANS; NEOPLASTIC STEM CELLS; POLYPLOIDY; RADIATION TOLERANCE; TUMOR MARKERS, BIOLOGICAL;

EID: 84872181159     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/onc.2012.31     Document Type: Article

References (39)

1. Little JB. Radiation-induced genomic instability. Int J Radiat Biol 1998; 74: 663-671. (Pubitemid 28566232)
2. Morgan WF, Day JP, Kaplan MI, McGhee EM, Limoli CL. Genomic instability induced by ionizing radiation. Radiat Res 1996; 146: 247-258. (Pubitemid 26320088)
3. Mothersill C, Seymour CB. Mechanisms and implications of genomic instability and other delayed effects of ionizing radiation exposure. Mutagenesis 1998; 13: 421-426. (Pubitemid 28458724)
4. Ponnaiya B, Cornforth MN, Ullrich RL. Induction of chromosomal instability in human mammary cells by neutrons and gamma rays. Radiat Res 1997; 147: 288-294. (Pubitemid 27114384)
5. Sudo H, Garbe J, Stampfer MR, Barcellos-Hoff MH, Kronenberg A. Karyotypic instability and centrosome aberrations in the progeny of finite life-span human mammary epithelial cells exposed to sparsely or densely ionizing radiation. Radiat Res 2008; 170: 23-32. (Pubitemid 351931184)
6. Suzuki K, Ojima M, Kodama S, Watanabe M. Delayed activation of DNA damage checkpoint and radiation-induced genomic instability. Mutat Res 2006; 597: 73-77.
7. Rosen JM, Jordan CT. The increasing complexity of the cancer stem cell paradigm. Science 2009; 324: 1670-1673.
8. Kai K, Arima Y, Kamiya T, Saya H. Breast cancer stem cells. Breast Cancer 2010; 17: 80-85.
9. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci USA 2003; 100: 3983-3988. (Pubitemid 36418143)
10. Sheridan C, Kishimoto H, Fuchs RK, Mehrotra S, Bhat-Nakshatri P, Turner CH et al. CD44+/CD24-breast cancer cells exhibit enhanced invasive properties: An early step necessary for metastasis. Breast Cancer Res 2006; 8: R59.
11. Shipitsin M, Campbell LL, Argani P, Weremowicz S, Bloushtain-Qimron N, Yao J et al. Molecular definition of breast tumor heterogeneity. Cancer Cell 2007; 11: 259-273. (Pubitemid 46349843)
12. Hwang-Verslues WW, Kuo WH, Chang PH, Pan CC, Wang HH, Tsai ST et al. Multiple lineages of human breast cancer stem/progenitor cells identified by profiling with stem cell markers. PLoS One 2009; 4: E8377.
13. Resetkova E, Reis-Filho JS, Jain RK, Mehta R, Thorat MA, Nakshatri H et al. Prognostic impact of ALDH1 in breast cancer: A story of stem cells and tumor microenvironment. Breast Cancer Res Treat 2010; 123: 97-108.
14. Yu F, Yao H, Zhu P, Zhang X, Pan Q, Gong C et al. let-7 regulates self renewal and tumorigenicity of breast cancer cells. Cell 2007; 131: 1109-1123. (Pubitemid 350235025)
15. Fillmore CM, Kuperwasser C. Human breast cancer cell lines contain stem-like cells that self-renew, give rise to phenotypically diverse progeny and survive chemotherapy. Breast Cancer Res 2008; 10: R25.
16. Nguyen NP, Almeida FS, Chi A, Nguyen LM, Cohen D, Karlsson U et al. Molecular biology of breast cancer stem cells: Potential clinical applications. Cancer Treat Rev 2010; 36: 485-491.
17. Pajonk F, Vlashi E, McBride WH. Radiation resistance of cancer stem cells: the 4 R's of radiobiology revisited. Stem Cells 2010; 28: 639-648.
18. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009; 458: 780-783.
19. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006; 98: 1777-1785. (Pubitemid 46017929)
20. Lagadec C, Vlashi E, Della Donna L, Meng Y, Dekmezian C, Kim K et al. Survival, self-renewing capacity and multi-lineage potency of breast cancer initiating cells during fractionated radiation treatment. Breast Cancer Res 2010; 12: R13.
21. Luce A, Courtin A, Levalois C, Altmeyer-Morel S, Romeo PH, Chevillard S et al. Death receptor pathways mediate targeted and non-targeted effects of ionizing radiations in breast cancer cells. Carcinogenesis 2009; 30: 432-439.
22. Gewirtz DA. Growth arrest and cell death in the breast tumor cell in response to ionizing radiation and chemotherapeutic agents which induce DNA damage. Breast Cancer Res Treat 2000; 62: 223-235.
23. Gewirtz DA, Sundaram S, Magnet KJ. Influence of topoisomerase II inhibitors and ionizing radiation on growth arrest and cell death pathways in the breast tumor cell. Cell Biochem Biophys 2000; 33: 19-31.
24. Olivier M, Bautista S, Valles H, Theillet C. Relaxed cell-cycle arrests and propagation of unrepaired chromosomal damage in cancer cell lines with wildtype p53. Mol Carcinog 1998; 23: 1-12. (Pubitemid 28441054)
25. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY et al. The epithelialmesenchymal transition generates cells with properties of stem cells. Cell 2008; 133: 704-715. (Pubitemid 351636299)
26. Ponti D, Costa A, Zaffaroni N, Pratesi G, Petrangolini G, Coradini D et al. Isolation and in vitro propagation of tumorigenic breast cancer cells with stem/progenitor cell properties. Cancer Res 2005; 65: 5506-5511. (Pubitemid 40911148)
27. Vlashi E, McBride WH, Pajonk F. Radiation responses of cancer stem cells. J Cell Biochem 2009; 108: 339-342.
28. Debeb BG, Xu W, Woodward WA. Radiation resistance of breast cancer stem cells: Understanding the clinical framework. J Mammary Gland Biol Neoplasia 2009; 14: 11-17.
29. Abraham BK, Fritz P, McClellan M, Hauptvogel P, Athelogou M, Brauch H. Prevalence of CD44+/CD24-/low cells in breast cancer may not be associated with clinical outcome but may favor distant metastasis. Clin Cancer Res 2005; 11: 1154-1159. (Pubitemid 40175765)
30. Giatromanolaki A, Sivridis E, Fiska A, Koukourakis MI. The CD44+/CD24-phenotype relates to 'triple-negative' state and unfavorable prognosis in breast cancer patients. Med Oncol 2011; 28: 745-752.
31. Baumann P, Cremers N, Kroese F, Orend G, Chiquet-Ehrismann R, Uede T et al. CD24 expression causes the acquisition of multiple cellular properties associated with tumor growth and metastasis. Cancer Res 2005; 65: 10783-10793. (Pubitemid 41715227)
32. Bircan S, Kapucuoglu N, Baspinar S, Inan G, Candir O. CD24 expression in ductal carcinoma in situ and invasive ductal carcinoma of breast: An immunohistochemistry-based pilot study. Pathol Res Pract 2006; 202: 569-576. (Pubitemid 44057770)
33. Kristiansen G, Winzer KJ, Mayordomo E, Bellach J, Schluns K, Denkert C et al. CD24 expression is a new prognostic marker in breast cancer. Clin Cancer Res 2003; 9: 4906-4913. (Pubitemid 37323297)
34. Aypar U, Morgan WF, Baulch JE. Radiation-induced genomic instability: Are epigenetic mechanisms the missing linkInt J Radiat Biol 2011; 87: 179-191.
35. Aypar U, Morgan WF, Baulch JE. Radiation-induced epigenetic alterations after low and high LET irradiations. Mutat Res 2011; 707: 24-33.
36. Lahtz C, Pfeifer GP. Epigenetic changes of DNA repair genes in cancer. J Mol Cell Biol 2011; 3: 51-58.
37. Bloushtain-Qimron N, Yao J, Snyder EL, Shipitsin M, Campbell LL, Mani SA et al. Cell type-specific DNA methylation patterns in the human breast. Proc Natl Acad Sci USA 2008; 105: 14076-14081.
38. Hernandez-Vargas H, Ouzounova M, Le Calvez-Kelm F, Lambert MP, McKay-Chopin S, Tavtigian SV et al. Methylome analysis reveals Jak-STAT pathway deregulation in putative breast cancer stem cells. Epigenetics 2011; 6: 428-439.
39. Rossi L, Challen GA, Sirin O, Lin KK, Goodell MA. Hematopoietic Stem Cell Characterization and Isolation. Methods Mol Biol 2011; 750: 47-59.