Non-small cell lung cancer cells survived ionizing radiation treatment display cancer stem cell and epithelial-mesenchymal transition phenotypes

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Gomez Casal, Roberto ^a,b   Bhattacharya, Chitralekha ^a,b   Ganesh, Nandita ^a   Bailey, Lisa ^a   Basse, Per ^a,c   Gibson, Michael ^a,b   Epperly, Michael ^a,b   Levina, Vera ^a,b  

^a UNIVERSITY OF PITTSBURGH CANCER INSTITUTE   (United States)

^b Department of Medicine ^*  (United States)

^c UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Cancer stem cell; Epithelial mesenchymal transition; Ionizing radiation; Non small cell lung cancer

Indexed keywords

AXITINIB; BETA CATENIN; CD24 ANTIGEN; CD44V ANTIGEN; DASATINIB; NERVE CELL ADHESION MOLECULE; OCTAMER TRANSCRIPTION FACTOR 4; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SOX2; VIMENTIN;

ADHERENT CELL; ARTICLE; CANCER CELL; CANCER RADIOTHERAPY; CANCER STEM CELL; CELL SURVIVAL; CONTROLLED STUDY; EMBRYONIC STEM CELL; EPITHELIAL MESENCHYMAL TRANSITION; HUMAN; HUMAN CELL; IN VITRO STUDY; LUNG NON SMALL CELL CANCER; PHENOTYPE;

ANTIGENS, CD44; CARCINOMA, NON-SMALL-CELL LUNG; CELL LINE, TUMOR; EPITHELIAL-MESENCHYMAL TRANSITION; HUMANS; LUNG NEOPLASMS; NEOPLASTIC STEM CELLS; PHENOTYPE; RADIATION TOLERANCE; RECEPTOR, PLATELET-DERIVED GROWTH FACTOR BETA; TRANSCRIPTION FACTORS; UP-REGULATION;

EID: 84881496427     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-94     Document Type: Article

References (76)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. CA Cancer J Clin 2012, 62(1):10-29.
2. Parsons A, Daley A, Begh R, Aveyard P. Influence of smoking cessation after diagnosis of early stage lung cancer on prognosis: systematic review of observational studies with meta-analysis. BMJ 2010, 340:b5569.
3. Greco FA, Stroup SL, Gray JR, Hainsworth JD. Paclitaxel in combination chemotherapy with radiotherapy in patients with unresectable stage III non-small-cell lung cancer. J Clin Oncol 1996, 14(5):1642-1648.
4. Danesi R, Pasqualetti G, Giovannetti E, Crea F, Altavilla G, Del Tacca M, Rosell R. Pharmacogenomics in non-small-cell lung cancer chemotherapy. Advanced drug delivery reviews 2009, 61(5):408-417.
5. Reya T, Morrison SJ, Clarke MF, Weissman IL. Stem cells, cancer, and cancer stem cells. Nat Geosci 2001, 414(6859):105-111.
6. Reya T, Clevers H. Wnt signalling in stem cells and cancer. Nat Geosci 2005, 434(7035):843-850.
7. Clarke MF, Fuller M. Stem cells and cancer: two faces of eve. Cell 2006, 124(6):1111-1115.
8. Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A 2003, 100(7):3983-3988.
9. Dontu G, Abdallah WM, Foley JM, Jackson KW, Clarke MF, Kawamura MJ, Wicha MS. In vitro propagation and transcriptional profiling of human mammary stem/progenitor cells. Genes Dev 2003, 17(10):1253-1270.
10. Hermann PC, Huber SL, Herrler T, Aicher A, Ellwart JW, Guba M, Bruns CJ, Heeschen C. Distinct populations of cancer stem cells determine tumor growth and metastatic activity in human pancreatic cancer. Cell Stem Cell 2007, 1(3):313-323.
11. Ignatova TN, Kukekov VG, Laywell ED, Suslov ON, Vrionis FD, Steindler DA. Human cortical glial tumors contain neural stem-like cells expressing astroglial and neuronal markers in vitro. Glia 2002, 39(3):193-206.
12. Eramo A, Lotti F, Sette G, Pilozzi E, Biffoni M, Di Virgilio A, Conticello C, Ruco L, Peschle C, De Maria R. Identification and expansion of the tumorigenic lung cancer stem cell population. Cell Death Differ 2008, 15(3):504-514.
13. Levina V, Marrangoni AM, DeMarco R, Gorelik E, Lokshin AE. Drug-selected human lung cancer stem cells: cytokine network, tumorigenic and metastatic properties. PLoS ONE 2008, 3(8):e3077.
14. Gorelik E, Lokshin A, Levina V. Lung cancer stem cells as a target for therapy. Anticancer Agents Med Chem 2010, 10(2):164-171.
15. McDermott SP, Wicha MS. Targeting breast cancer stem cells. Mol Oncol 2010, 4(5):404-419.
16. Dean M, Fojo T, Bates S. Tumour stem cells and drug resistance. Nat Rev Cancer 2005, 5(4):275-284.
17. Bertolini G, Roz L, Perego P, Tortoreto M, Fontanella E, Gatti L, Pratesi G, Fabbri A, Andriani F, Tinelli S, et al. Highly tumorigenic lung cancer CD133+ cells display stem-like features and are spared by cisplatin treatment. Proc Natl Acad Sci U S A 2009, 106(38):16281-16286.
18. Jiang F, Qiu Q, Khanna A, Todd NW, Deepak J, Xing L, Wang H, Liu Z, Su Y, Stass SA, et al. Aldehyde dehydrogenase 1 is a tumor stem cell-associated marker in lung cancer. Mol Cancer Res 2009, 7(3):330-338.
19. Levina V, Marrangoni A, Wang T, Parikh S, Su Y, Herberman R, Lokshin A, Gorelik E. Elimination of human lung cancer stem cells through targeting of the stem cell factor-c-kit autocrine signaling loop. Cancer Res 2010, 70(1):338-346.
20. Zhang WC, Shyh-Chang N, Yang H, Rai A, Umashankar S, Ma S, Soh BS, Sun LL, Tai BC, Nga ME, et al. Glycine decarboxylase activity drives non-small cell lung cancer tumor-initiating cells and tumorigenesis. Cell 2012, 148(1-2):259-272.
21. Ho MM, Ng AV, Lam S, Hung JY. Side population in human lung cancer cell lines and tumors is enriched with stem-like cancer cells. Cancer Res 2007, 67(10):4827-4833.
22. Singh S, Trevino J, Bora-Singhal N, Coppola D, Haura E, Altiok S, Chellappan SP. EGFR/Src/Akt signaling modulates Sox2 expression and self-renewal of stem-like side-population cells in non-small cell lung cancer. Molecular cancer 2012, 11:73.
23. Chen YC, Hsu HS, Chen YW, Tsai TH, How CK, Wang CY, Hung SC, Chang YL, Tsai ML, Lee YY, et al. Oct-4 expression maintained cancer stem-like properties in lung cancer-derived CD133-positive cells. PLoS ONE 2008, 3(7):e2637.
24. Giangreco A, Lu L, Vickers C, Teixeira VH, Groot KR, Butler CR, Ilieva EV, George PJ, Nicholson AG, Sage EK, et al. beta-catenin determines upper airway progenitor cell fate and preinvasive squamous lung cancer progression by modulating epithelial-mesenchymal transition. J Pathol 2012, 226(4):575-587.
25. Teng Y, Wang X, Wang Y, Ma D. Wnt/beta-catenin signaling regulates cancer stem cells in lung cancer A549 cells. Biochem Biophys Res Commun 2010, 392(3):373-379.
26. Shien K, Toyooka S, Ichimura K, Soh J, Furukawa M, Maki Y, Muraoka T, Tanaka N, Ueno T, Asano H, et al. Prognostic impact of cancer stem cell-related markers in non-small cell lung cancer patients treated with induction chemoradiotherapy. Lung Cancer 2012, 77(1):162-167.
27. Singh A, Settleman J. EMT, cancer stem cells and drug resistance: an emerging axis of evil in the war on cancer. Oncogene 2010, 29(34):4741-4751.
28. Kong D, Li Y, Wang Z, Sarkar FH. Cancer stem cells and epithelial-to-mesenchymal transition (EMT)-phenotypic cells: are they cousins or twins?. Cancers (Basel) 2011, 3(1):716-729.
29. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, Zhou AY, Brooks M, Reinhard F, Zhang CC, Shipitsin M, et al. The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 2008, 133(4):704-715.
30. Scheel C, Weinberg RA. Cancer stem cells and epithelial-mesenchymal transition: concepts and molecular links. Semin Cancer Biol 2012, 22(5-6):396-403.
31. Wijnhoven BP, Dinjens WN, Pignatelli M. E-cadherin-catenin cell-cell adhesion complex and human cancer. The British journal of surgery 2000, 87(8):992-1005.
32. Scheel C, Eaton EN, Li SH, Chaffer CL, Reinhardt F, Kah KJ, Bell G, Guo W, Rubin J, Richardson AL, et al. Paracrine and autocrine signals induce and maintain mesenchymal and stem cell states in the breast. Cell 2011, 145(6):926-940.
33. Polyak K, Weinberg RA. Transitions between epithelial and mesenchymal states: acquisition of malignant and stem cell traits. Nat Rev Cancer 2009, 9(4):265-273.
34. Craene BD, Berx G. Regulatory networks defining EMT during cancer initiation and progression. Nat Rev Cancer 2012, 13(2):97-110.
35. Heddleston JM, Li Z, McLendon RE, Hjelmeland AB, Rich JN. The hypoxic microenvironment maintains glioblastoma stem cells and promotes reprogramming towards a cancer stem cell phenotype. Cell Cycle 2009, 8(20):3274-3284.
36. Salnikov AV, Liu L, Platen M, Gladkich J, Salnikova O, Ryschich E, Mattern J, Moldenhauer G, Werner J, Schemmer P, et al. Hypoxia induces EMT in low and highly aggressive pancreatic tumor cells but only cells with cancer stem cell characteristics acquire pronounced migratory potential. PLoS One 2012, 7(9):e46391.
37. Andarawewa KL, Erickson AC, Chou WS, Costes SV, Gascard P, Mott JD, Bissell MJ, Barcellos-Hoff MH. Ionizing radiation predisposes nonmalignant human mammary epithelial cells to undergo transforming growth factor beta induced epithelial to mesenchymal transition. Cancer Res 2007, 67(18):8662-8670.
38. Jung JW, Hwang SY, Hwang JS, Oh ES, Park S, Han IO. Ionising radiation induces changes associated with epithelial-mesenchymal transdifferentiation and increased cell motility of A549 lung epithelial cells. Eur J Cancer 2007, 43(7):1214-1224.
39. Zhou P, Du LF, Lv GQ, Yu XM, Gu YL, Li JP, Zhang C. Functional polymorphisms in CD166/ALCAM gene associated with increased risk for breast cancer in a Chinese population. Breast Cancer Res Treat 2011, 128(2):527-534.
40. Kawamoto A, Yokoe T, Tanaka K, Saigusa S, Toiyama Y, Yasuda H, Inoue Y, Miki C, Kusunoki M. Radiation induces epithelial-mesenchymal transition in colorectal cancer cells. Oncol Rep 2012, 27(1):51-57.
41. Kim H, Yoo SB, Sun P, Jin Y, Jheon S, Lee CT, Chung JH. Alteration of the E-cadherin/beta-catenin complex is an independent poor prognostic factor in lung adenocarcinoma. Korean journal of pathology 2013, 47(1):44-51.
42. Hall EJ. Radiation dose-rate: a factor of importance in radiobiology and radiotherapy. The British journal of radiology 1972, 45(530):81-97.
43. Denker SP, Barber DL. Cell migration requires both ion translocation and cytoskeletal anchoring by the Na-H exchanger NHE1. The Journal of cell biology 2002, 159(6):1087-1096.
44. Levina V, Marrangoni AM, Demarco R, Gorelik E, Lokshin AE. Multiple effects of TRAIL in human carcinoma cells: Induction of apoptosis, senescence, proliferation, and cytokine production. Exp Cell Res 2008, 314(7):1605-1616.
45. Jung MJ, Rho JK, Kim YM, Jung JE, Jin YB, Ko YG, Lee JS, Lee SJ, Lee JC, Park MJ. Upregulation of CXCR4 is functionally crucial for maintenance of stemness in drug-resistant non-small cell lung cancer cells. Oncogene 2013, 32(2):209-221.
46. Ball SG, Shuttleworth A, Kielty CM. Inhibition of platelet-derived growth factor receptor signaling regulates Oct4 and Nanog expression, cell shape, and mesenchymal stem cell potency. Stem Cells 2012, 30(3):548-560.
47. Gupta PB, Chaffer CL, Weinberg RA. Cancer stem cells: mirage or reality?. Nat Med 2009, 15(9):1010-1012.
48. Ofori-Acquah SF, King JA. Activated leukocyte cell adhesion molecule: a new paradox in cancer. Translational research: the journal of laboratory and clinical medicine 2008, 151(3):122-128.
49. Lugli A, Iezzi G, Hostettler I, Muraro MG, Mele V, Tornillo L, Carafa V, Spagnoli G, Terracciano L, Zlobec I. Prognostic impact of the expression of putative cancer stem cell markers CD133, CD166, CD44s, EpCAM, and ALDH1 in colorectal cancer. Br J Cancer 2010, 103(3):382-390.
50. Haynes BF, Liao HX, Patton KL. The transmembrane hyaluronate receptor (CD44): multiple functions, multiple forms. Cancer Cells 1991, 3(9):347-350.
51. Zoller M. CD44: can a cancer-initiating cell profit from an abundantly expressed molecule?. Nat Rev Cancer 2011, 11(4):254-267.
52. Misra S, Heldin P, Hascall VC, Karamanos NK, Skandalis SS, Markwald RR, Ghatak S. Hyaluronan-CD44 interactions as potential targets for cancer therapy. The FEBS journal 2011, 278(9):1429-1443.
53. Katoh M. WNT signaling in stem cell biology and regenerative medicine. Curr Drug Targets 2008, 9(7):565-570.
54. 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, et al. CD44 expression predicts local recurrence after radiotherapy in larynx cancer. Clin Cancer Res 2010, 16(21):5329-5338.
55. Calloni R, Cordero EA, Henriques JA, Bonatto D. Reviewing and updating the major molecular markers for stem cells. Stem Cells Dev 2013, 22(9):1455-1476.
56. Lagadec C, Vlashi E, Della Donna L, Dekmezian C, Pajonk F. Radiation-induced reprogramming of breast cancer cells. Stem Cells 2012, 30(5):833-844.
57. Tellez CS, Juri DE, Do K, Bernauer AM, Thomas CL, Damiani LA, Tessema M, Leng S, Belinsky SA. EMT and stem cell-like properties associated with miR-205 and miR-200 epigenetic silencing are early manifestations during carcinogen-induced transformation of human lung epithelial cells. Cancer Res 2011, 71(8):3087-3097.
58. Ouyang G, Wang Z, Fang X, Liu J, Yang CJ. Molecular signaling of the epithelial to mesenchymal transition in generating and maintaining cancer stem cells. Cell Mol Life Sci 2010, 67(15):2605-2618.
59. Thiery JP, Lim CT. Tumor dissemination: an EMT affair. Cancer Cell 2013, 23(3):272-273.
60. Lee HJ, Choe G, Jheon S, Sung SW, Lee CT, Chung JH. CD24, a novel cancer biomarker, predicting disease-free survival of non-small cell lung carcinomas: a retrospective study of prognostic factor analysis from the viewpoint of forthcoming (seventh) new TNM classification. J Thorac Oncol 2010, 5(5):649-657.
61. Kang KS, Choi YP, Gao MQ, Kang S, Kim BG, Lee JH, Kwon MJ, Shin YK, Cho NH. CD24(+) ovary cancer cells exhibit an invasive mesenchymal phenotype. Biochem Biophys Res Commun 2013, 432(2):333-338.
62. Yang J, Weinberg RA. Epithelial-mesenchymal transition: at the crossroads of development and tumor metastasis. Developmental cell 2008, 14(6):818-829.
63. Onder TT, Gupta PB, Mani SA, Yang J, Lander ES, Weinberg RA. Loss of E-cadherin promotes metastasis via multiple downstream transcriptional pathways. Cancer Res 2008, 68(10):3645-3654.
64. Hung JJ, Yang MH, Hsu HS, Hsu WH, Liu JS, Wu KJ. Prognostic significance of hypoxia-inducible factor-1alpha, TWIST1 and Snail expression in resectable non-small cell lung cancer. Thorax 2009, 64(12):1082-1089.
65. Martin A, Cano A. Tumorigenesis: twist1 links EMT to self-renewal. Nature cell biology 2010, 12(10):924-925.
66. Barnes RM, Firulli AB. A twist of insight - the role of twist-family bHLH factors in development. The International journal of developmental biology 2009, 53(7):909-924.
67. Zhuo WL, Wang Y, Zhuo XL, Zhang YS, Chen ZT. Short interfering RNA directed against TWIST, a novel zinc finger transcription factor, increases A549 cell sensitivity to cisplatin via MAPK/mitochondrial pathway. Biochem Biophys Res Commun 2008, 369(4):1098-1102.
68. Ansieau S, Morel AP, Hinkal G, Bastid J, Puisieux A. TWISTing an embryonic transcription factor into an oncoprotein. Oncogene 2010, 29(22):3173-3184.
69. Pallier K, Cessot A, Cote JF, Just PA, Cazes A, Fabre E, Danel C, Riquet M, Devouassoux-Shisheboran M, Ansieau S, et al. TWIST1 a new determinant of epithelial to mesenchymal transition in EGFR mutated lung adenocarcinoma. PLoS One 2012, 7(1):e29954.
70. Yang J, Mani SA, Donaher JL, Ramaswamy S, Itzykson RA, Come C, Savagner P, Gitelman I, Richardson A, Weinberg RA. Twist, a master regulator of morphogenesis, plays an essential role in tumor metastasis. Cell 2004, 117(7):927-939.
71. Ryu HS, Park Do J, Kim HH, Kim WH, Lee HS. Combination of epithelial-mesenchymal transition and cancer stem cell-like phenotypes has independent prognostic value in gastric cancer. Hum Pathol 2012, 4(4):520-528.
72. Cool J, DeFalco TJ, Capel B. Vascular-mesenchymal cross-talk through Vegf and Pdgf drives organ patterning. Proc Natl Acad Sci U S A 2011, 108(1):167-172.
73. Yokoyama Y, Mori S, Hamada Y, Hieda M, Kawaguchi N, Shaker M, Tao Y, Yoshidome K, Tsujimoto M, Matsuura N. Platelet-derived growth factor regulates breast cancer progression via beta-catenin expression. Pathobiology: journal of immunopathology, molecular and cellular biology 2011, 78(5):253-260.
74. Ellis PM, Al-Saleh K. Multitargeted anti-angiogenic agents and NSCLC: clinical update and future directions. Crit Rev Oncol Hematol 2012, 84(1):47-58.
75. Gnoni A, Marech I, Silvestris N, Vacca A, Lorusso V. Dasatinib: an anti-tumour agent via Src inhibition. Curr Drug Targets 2011, 12(4):563-578.
76. Montero JC, Seoane S, Ocana A, Pandiella A. Inhibition of SRC family kinases and receptor tyrosine kinases by dasatinib: possible combinations in solid tumors. Clin Cancer Res 2011, 17(17):5546-5552.