Distinct subpopulations of head and neck cancer cells with different levels of intracellular reactive oxygen species exhibit diverse stemness, proliferation, and chemosensitivity

Cancer Research

Volumn 74, Issue 21, 2014, Pages 6291-6305

  Chang, Ching Wen ^a   Chen, Yu Syuan ^a   Chou, Shiu Huey ^b   Han, Chia Li ^c   Chen, Yu Ju ^c   Yang, Cheng Chieh ^a   Huang, Chih Yang ^d,e   Lo, Jeng Fan ^a,d,f  

^a NATIONAL YANG MING UNIVERSITY   (Taiwan)

^b FU JEN CATHOLIC UNIVERSITY   (Taiwan)

^c INSTITUTE OF CHEMISTRY   (Taiwan)

^d CHINA MEDICAL UNIVERSITY   (Taiwan)

^e ASIA UNIVERSITY   (Taiwan)

^f TAIPEI VETERANS GENERAL HOSPITAL   (Taiwan)

Author keywords

[No Author keywords available]

Indexed keywords

ALDEHYDE DEHYDROGENASE; CD133 ANTIGEN; CISPLATIN; GLUCOSE REGULATED PROTEIN 78; GLUCOSE TRANSPORTER 3; REACTIVE OXYGEN METABOLITE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER CELL LINE; CANCER RESISTANCE; CANCER STEM CELL; CARCINOGENICITY; CELL DEATH; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DRUG SENSITIVITY; FLOW CYTOMETRY; HEAD AND NECK SQUAMOUS CELL CARCINOMA; HUMAN; HUMAN CELL; MOUSE; NONHUMAN; ANIMAL; CYTOPLASM; DRUG EFFECTS; DRUG RESISTANCE; EPITHELIAL MESENCHYMAL TRANSITION; GENETICS; HEAD AND NECK TUMOR; METABOLISM; PATHOLOGY; SIGNAL TRANSDUCTION; SQUAMOUS CELL CARCINOMA; TUMOR CELL LINE;

ANIMALS; CARCINOMA, SQUAMOUS CELL; CELL DIFFERENTIATION; CELL LINE, TUMOR; CELL PROLIFERATION; CISPLATIN; CYTOPLASM; DRUG RESISTANCE, NEOPLASM; EPITHELIAL-MESENCHYMAL TRANSITION; HEAD AND NECK NEOPLASMS; HUMANS; MICE; NEOPLASTIC STEM CELLS; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84909606388     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-14-0626     Document Type: Article

References (52)

1. Medema JP. Cancer stem cells: the challenges ahead. Nat Cell Biol 2013;15:338-44.
2. Frank NY, Schatton T, Frank MH. The therapeutic promise of the cancer stem cell concept. J Clin Invest 2010;120:41-50.
3. Moore N, Lyle S. Quiescent, slow-cycling stem cell populations in cancer a review of the evidence and discussion of significance. J Oncol 2011;2011.
4. Koukourakis MI, Giatromanolaki A, Tsakmaki V, Danielidis V, Sivridis E. Cancer stem cell phenotype relates to radio-chemotherapy outcome in locally advanced squamous cell head-neck cancer. Br J Cancer 2012; 106:846-53.
5. Chang CW, Chen CC, Wu MJ, Chen YS, Chen CC, Sheu SJ, et al. Active component of antrodia cinnamomea mycelia targeting head and neck cancer initiating cells through exaggerated autophagic cell death. Evid Based Complement Alternat Med 2013;2013:946451.
6. Haddad RI, Shin DM. Recent advances in head and neck cancer. N Engl J Med 2008;359:1143-54.
7. Chiou SH, Yu CC, Huang CY, Lin SC, Liu CJ, Tsai TH, et al. Positive correlations of Oct-4 and Nanog in oral cancer stem-like cells and high-grade oral squamous cell carcinoma. Clin Cancer Res 2008; 14:4085-95.
8. Chen YS, Wu MJ, Huang CY, Lin SC, Chuang TH, Yu CC, et al. CD133/Src axis mediates tumor initiating property and epithelialmesenchymal transition of head and neck cancer. PLoS ONE 2011;6:e28053.
9. WuMJ, Jan CI, Tsay YG, Yu YH, Huang CY, Lin SC, et al. Elimination of head and neck cancer initiating cells through targeting glucose regulated protein78 signaling. Mol Cancer 2010;9:283.
10. Gupta SC, Hevia D, Patchva S, Park B, Koh W, Aggarwal BB. Upsides and downsides of reactive oxygen species for cancer: the roles of reactive oxygen species in tumorigenesis, prevention, and therapy. Antioxid Redox Signal 2012;16:1295-322.
11. Wang K, Zhang T, Dong Q, Nice EC, Huang C, Wei Y. Redox homeostasis: the linchpin in stem cell self-renewal and differentiation. Cell Death Dis 2013;4:e537.
12. Shi X, Zhang Y, Zheng J, Pan J. Reactive oxygen species in cancer stem cells. Antioxid Redox Signal 2012;16:1215-28.
13. Ogasawara MA, Zhang H. Redox regulation and its emerging roles in stem cells and stem-like cancer cells. Antioxid Redox Signal 2009;11: 1107-22.
14. Jang YY, Sharkis SJ. A low level of reactive oxygen species selects for primitive hematopoietic stem cells that may reside in the low-oxygenic niche. Blood 2007;110:3056-63.
15. Achuthan S, Santhoshkumar TR, Prabhakar J, Nair SA, Pillai MR. Druginduced senescence generates chemoresistant stemlike cells with low reactive oxygen species. J Biol Chem 2011;286:37813-29.
16. 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;458:780-3.
17. Trachootham D, Alexandre J, Huang P. Targeting cancer cells byROSmediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 2009;8:579-91.
18. Salnikov AV, Gladkich J, Moldenhauer G, Volm M, Mattern J, Herr I. CD133 is indicative for a resistance phenotype but does not represent a prognostic marker for survival of non-small cell lung cancer patients. Int J Cancer 2010;126:950-8.
19. Volm M, Mattern J. Expression of topoisomerase II, catalase, metallothionein and thymidylate-synthase in human squamous cell lung carcinomas and their correlation with doxorubicin resistance and with patients' smoking habits. Carcinogenesis 1992;13:1947-50.
20. Okumura K, Konishi A, Tanaka M, Kanazawa M, Kogawa K, Niitsu Y. Establishment of high-and low-invasion clones derived for a human tongue squamous cell carcinoma cell line SAS. J Cancer Res Clin Oncol 1996;122:243-8.
21. Barrett CW, Ning W, Chen X, Smith JJ, Washington MK, Hill KE, et al. Tumor suppressor function of the plasma glutathione peroxidase gpx3 in colitis-associated carcinoma. Cancer research 2013;73:1245-55.
22. Flavahan WA, Wu Q, Hitomi M, Rahim N, Kim Y, Sloan AE, et al. Brain tumor initiating cells adapt to restricted nutrition through preferential glucose uptake. Nat Neurosci 2013;16:1373-82.
23. Clay MR, Tabor M, Owen JH, Carey TE, Bradford CR, Wolf GT, et al. Single-marker identification of head and neck squamous cell carcinoma cancer stem cells with aldehyde dehydrogenase. Head Neck 2010;32:1195-201.
24. Le Belle JE, Orozco NM, Paucar AA, Saxe JP, Mottahedeh J, Pyle AD, et al. Proliferative neural stem cells have high endogenous ROS levels that regulate self-renewal and neurogenesis in a PI3K/Akt-dependant manner. Cell Stem Cell 2011;8:59-71.
25. Seale P, Asakura A, Rudnicki MA. The potential of muscle stem cells. Dev Cell 2001;1:333-42.
26. Colter DC, Sekiya I, Prockop DJ. Identification of a subpopulation of rapidly self-renewing and multipotential adult stem cells in colonies of humanmarrow stromal cells. Proc Natl Acad SciUS A 2001;98:7841-5.
27. Jones RJ, Collector MI, Barber JP, Vala MS, Fackler MJ, May WS, et al. Characterization of mouse lymphohematopoietic stem cells lacking spleen colony-forming activity. Blood 1996;88:487-91.
28. Gandarillas A, Davies D, Blanchard JM. Normal and c-Myc-promoted human keratinocyte differentiation both occur via a novel cell cycle involving cellular growth and endoreplication. Oncogene 2000;19: 3278-89.
29. Li L, Bhatia R. Stem cell quiescence. Clin Cancer Res 2011;17: 4936-41.
30. Lin C, Wang H. NADPH oxidase is involved in H2O2-induced differentiation of human promyelocytic leukaemia HL-60 cells. Cell Biol Int 2012;36:391-5.
31. Chou WC, Jie C, Kenedy AA, Jones RJ, Trush MA, Dang CV. Role of NADPH oxidase in arsenic-induced reactive oxygen species formation and cytotoxicity in myeloid leukemia cells. Proc Natl Acad Sci U S A 2004;101:4578-83.
32. Tsai LL, Yu CC, Chang YC, Yu CH, Chou MY. Markedly increased Oct4 and Nanog expression correlates with cisplatin resistance in oral squamous cell carcinoma. J Oral Pathol Med 2011;40:621-8.
33. Kobayashi CI, Suda T. Regulation of reactive oxygen species in stem cells and cancer stem cells. J Cell Physiol 2012;227:421-30.
34. Nagano O, Okazaki S, Saya H. Redox regulation in stem-like cancer cells by CD44 variant isoforms. Oncogene 2013;32:5191-8.
35. Klingelhoeffer C, Kammerer U, Koospal M, Muhling B, Schneider M, Kapp M, et al. Natural resistance to ascorbic acid induced oxidative stress is mainly mediated by catalase activity in human cancer cells and catalase-silencing sensitizes to oxidative stress. BMC Complement Altern Med 2012;12:61.
36. Zhu Z, Mukhina S, Zhu T, Mertani HC, Lee KO, Lobie PE. p44/42 MAP kinase-dependent regulation of catalase by autocrine human growth hormone protects human mammary carcinoma cells from oxidative stress-induced apoptosis. Oncogene 2005;24:3774-85.
37. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2013. CA Cancer J Clin 2013;63:11-30.
38. Maiti AK. Gene network analysis of oxidative stress-mediated drug sensitivity in resistant ovarian carcinoma cells. Pharmacogenomics J 2010;10:94-104.
39. Maiti AK. Genetic determinants of oxidative stress-mediated sensitization of drug-resistant cancer cells. Int J Cancer 2012;130:1-9.
40. Caraglia M, Giuberti G, Marra M, Addeo R, Montella L, Murolo M, et al. Oxidative stress and ERK1/2 phosphorylation as predictors of outcome in hepatocellular carcinoma patients treated with sorafenib plus octreotide LAR. Cell Death Dis 2011;2:e150.
41. Berlett BS, Stadtman ER. Protein oxidation in aging, disease, and oxidative stress. J Biol Chem 1997;272:20313-6.
42. Pervaiz S, Taneja R, Ghaffari S. Oxidative stress regulation of stem and progenitor cells. Antioxid Redox Signal 2009;11:2777-89.
43. Phillips TM, McBride WH, Pajonk F. The response of CD24(-/low)/ CD44+ breast cancer-initiating cells to radiation. J Natl Cancer Inst 2006;98:1777-85.
44. Li Z, Bao S, Wu Q, Wang H, Eyler C, Sathornsumetee S, et al. Hypoxiainducible factors regulate tumorigenic capacity of glioma stem cells. Cancer Cell 2009;15:501-13.
45. Bechtel W, Bauer G. Catalase protects tumor cells from apoptosis induction by intercellular ROS signaling. Anticancer Res 2009;29: 4541-57.
46. Gao MQ, Choi YP, Kang S, Youn JH, Cho NH. CD24+ cells from hierarchically organized ovarian cancer are enriched in cancer stem cells. Oncogene 2010;29:2672-80.
47. Dembinski JL, Krauss S. Characterization and functional analysis of a slow cycling stem cell-like subpopulation in pancreas adenocarcinoma. Clin Exp Metastasis 2009;26:611-23.
48. Bao S,WuQ, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006;444:756-60.
49. Dey-Guha I, Wolfer A, Yeh AC, G Albeck J, Darp R, Leon E, et al. Asymmetric cancer cell division regulated by AKT. Proc Natl Acad Sci U S A 2011;108:12845-50.
50. Yoneyama M, Kawada K, Gotoh Y, Shiba T, Ogita K. Endogenous reactive oxygen species are essential for proliferation of neural stem/ progenitor cells. Neurochem Int 2010;56:740-6.
51. Weinberg F, Hamanaka R, WheatonWW,Weinberg S, Joseph J, Lopez M, et al. Mitochondrial metabolism and ROS generation are essential for Kras-mediated tumorigenicity. Proc Natl Acad Sci U S A 2010; 107:8788-93.
52. Kim JJ, Tannock IF. Repopulation of cancer cells during therapy: an important cause of treatment failure. Nat Rev Cancer 2005;5:516-25.