Transient alteration of cellular redox buffering before irradiation triggers apoptosis in head and neck carcinoma stem and non-stem cells

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Boivin, Anthony ^a,b   Hanot, Maité ^a,b   Malesys, Céline ^a,b   Maalouf, Mira ^a,b   Rousson, Robert ^c   Rodriguez Lafrasse, Claire ^a,b,c   Ardail, Dominique ^a,b,c  

^a UNIVERSITÉ LYON 1   (France)

^b UNIVERSITÉ CLAUDE BERNARD LYON 1   (France)

^c HOSPICES CIVILS DE LYON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

APOPTOSIS SIGNAL REGULATING KINASE 1; BUTHIONINE SULFOXIMINE; FUMARIC ACID DIMETHYL ESTER; GLUTATHIONE; SMALL INTERFERING RNA; STRESS ACTIVATED PROTEIN KINASE; BUFFER; FUMARIC ACID DERIVATIVE; MAP3K5 PROTEIN, HUMAN; PROTEIN BAX;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CANCER RADIOTHERAPY; CANCER STEM CELL; CANCER SURVIVAL; CELL DEATH; CELL ISOLATION; CELL VIABILITY; CONTROLLED STUDY; FEMALE; FLOW CYTOMETRY; HEAD AND NECK CARCINOMA; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IN VITRO GENE TRANSFER; IN VIVO STUDY; MITOCHONDRION; MOUSE; NICK END LABELING; NONHUMAN; OUTCOME ASSESSMENT; OXIDATION REDUCTION STATE; PROTEIN DEPLETION; RADIOSENSITIVITY; SINGLE DRUG DOSE; SQUAMOUS CELL CARCINOMA; TREATMENT OUTCOME; TUMOR VOLUME; WESTERN BLOTTING; ADAPTATION; CARCINOMA; DRUG ANTAGONISM; DRUG EFFECT; HEAD AND NECK TUMOR; HUMAN; METABOLISM; OXIDATION REDUCTION REACTION; PATHOLOGY; RADIATION EXPOSURE; TUMOR CELL LINE;

ADAPTATION, PHYSIOLOGICAL; APOPTOSIS; BCL-2-ASSOCIATED X PROTEIN; BUFFERS; BUTHIONINE SULFOXIMINE; CARCINOMA; CELL LINE, TUMOR; FUMARATES; GLUTATHIONE; HEAD AND NECK NEOPLASMS; HUMANS; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MAP KINASE KINASE KINASE 5; NEOPLASMS, SQUAMOUS CELL; NEOPLASTIC STEM CELLS; OXIDATION-REDUCTION;

EID: 79251613647     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0014558     Document Type: Article

References (63)

1. Pisani P, Bray F, Parkin DM (2002) Estimates of the world-wide prevalence of cancer for 25 sites in the adult population. Int J Cancer 97: 72-81.
2. Chin D, Boyle GM, Porceddu S, Theile DR, Parsons PG, et al. (2006) Head and neck cancer: past, present and future. Expert Rev Anticancer Ther 6: 1111-1118.
3. Mazeron R, Tao Y, Lusinchi A, Bourhis J (2009) Current concepts of management in radiotherapy for head and neck squamous-cell cancer. Oral Oncol 45: 402-408.
4. Alphonse G, Aloy MT, Broquet P, Gerard JP, Louisot P, et al. (2002) Ceramide induces activation of the mitochondrial/caspases pathway in Jurkat and SCC61 cells sensitive to gamma-radiation but activation of this sequence is defective in radioresistant SQ20B cells. Int J Radiat Biol 78: 821-35.
5. Maalouf M, Alphonse G, Colliaux A, Beuve M, Trajkovic-Bodennec S, et al. (2009) Different mechanisms of cell death in radiosensitive and radioresistant p53 mutated head and neck squamous cell carcinoma cell lines exposed to carbon ions and x-rays. Int J Radiat Oncol Biol Phys 74: 200-9.
6. Alphonse G, Bionda C, Aloy MT, Ardail D, Rousson R, et al. (2004) Overcoming resistance to gamma-rays in squamous carcinoma cells by polydrug elevation of ceramide levels. Oncogene 23: 2703-15.
7. Toyokuni S, Okamoto K, Yodoi J, Hiai H (1995) Persistent oxidative stress in cancer. FEBS Lett 358: 1-3.
8. Szatrowski TP, Nathan CF (1991) Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res 51: 794-798.
9. Behrend L, Henderson G, Zwacka RM (2003) Reactive oxygen species in oncogenic transformation. Biochem Soc Trans 31: 1441-1444.
10. Wu WS (2006) The signaling mechanism of ROS in tumor progression. Cancer Metastasis Rev 25: 695-705.
11. Pelicano H, Carney D, Huang P (2004) ROS stress in cancer cells and therapeutic implications. Drug Resist Updat 7: 97-110.
12. Inci E, Civelek S, Seven A, Inci F, Korkut N, et al. (2003) Laryngeal cancer: in relation to oxidative stress. Tohoku J Exp Med 200: 17-23.
13. Pervaiz S, Clement MV (2004) Tumor intracellular redox status and drug resistance-serendipity or a causal relationship? Curr Pharm Des 10: 1969-1977.
14. Bionda C, Hadchity E, Alphonse G, Chapet O, Rousson R, et al. (2007) Radioresistance of human carcinoma cells is correlated to a defect in raft membrane clustering. Free Radic Biol Med 43: 681-94.
15. Pantano C, Reynaert NL, Van der Vliet A, Janssen-Heininger YM (2006) Redox-sensitive kinases of the nuclear factor-kappaB signaling pathway. Antioxid Redox Signal 8: 1791-806.
16. Kaspar JW, Niture SK, Jaiswal AK (2009) Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic Biol Med 47: 1304-9.
17. Jaiswal AK (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Radic Biol Med 36: 1199-207.
18. Forman HJ, Zhang H, Rinna A (2009) Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30: 1-12.
19. Castro B, Alonso-Varona A, del Olmo M, Bilbao P, Palomares T (2002) Role of gamma-glutamyltranspeptidase on the response of poorly and moderately differentiated rhabdomyosarcoma cell lines to buthionine sulfoximine-induced inhibition of glutathione synthesis. Anticancer Drugs 13: 281-91.
20. Lippitz BE, Halperin EC, Griffith OW, Colvin OM, Honore G, et al. (1990) Lbuthionine sulfoximine -mediated radiosensitization in experimental interstitial radiotherapy of intracerebral D-54 MG glioma xenografts in athymic mice. Neurosurgery 26: 255-60.
21. Miura M, Sasaki T (1991) Role of glutathione in the intrinsic radioresistance of cell lines from a mouse squamous cell carcinoma. Radiat Res 126: 229-36.
22. Leung SW, Mitchell JB, al-Nabulsi I, Friedman N, Newsome J, et al. (1993) Effect of L-buthionine sulfoximine on the radiation response of human renal carcinoma cell lines. Cancer 71: 2276-85.
23. Mirkovic N, Voehringer DW, Story MD, McConkey DJ, McDonnell TJ, et al. (1997) Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 15: 1461-70.
24. Li L, Steinauer KK, Dirks AJ, Husbeck B, Gibbs I, et al. (2003) Radiationinduced cyclooxygenase 2 up-regulation is dependent on redox status in prostate cancer cells. Radiat Res 160: 617-21.
25. Maeda H, Hori S, Ohizumi H, Segawa T, Kakehi Y, et al. (2004) Effective treatment of advanced solid tumors by combination of arsenic trioxide and Lbuthionine sulfoximine. Cell Death Differ 11: 737-46.
26. Andringa KK, Coleman MC, Aykin-Burns N, Hitchler MJ, Walsh SA, et al. (2006) Inhibition of glutamate cysteine ligase activity sensitizes human breast cancer cells to the toxicity of 2-Deoxy-D-glucose. Cancer Res 66: 1605-10.
27. Magwere T, Myatt SS, Burchill SA (2008) Manipulation of oxidative stress to induce cell death in Ewing's sarcoma family of tumours. Eur J Cancer 44: 2276-87.
28. Palomares T, Caramés M, García-Alonso I, Alonso-Varona A (2009) Glutathione modulation reverses the growth-promoting effect of growth factors, improving the 5-fluorouracil antitumour response in WiDr colon cancer cells. Anticancer Res 29: 3957-65.
29. Lewis-Wambi JS, Swaby R, Kim H, Jordan VC (2009) Potential of l-buthionine sulfoximine to enhance the apoptotic action of estradiol to reverse acquired antihormonal resistance in metastatic breast cancer. J Steroid Biochem Mol Biol 114: 33-9.
30. Vahrmeijer AL, van Dierendonck JH, Schutrups J, van de Velde CJ, Mulder GJ (1999) Potentiation of the cytostatic effect of melphalan on colorectal cancer hepatic metastases by infusion of buthionine sulfoximine (BSO) in the rat: enhanced tumor glutathione depletion by infusion of BSO in the hepatic artery. Cancer Chemother Pharmacol 44: 111-6.
31. Palomares T, Bilbao P, del Olmo M, Castro B, Calle Y, et al. (1999) In vitro and in vivo comparison between the effects of treatment with adenosine triphosphate and treatment with buthionine sulfoximine on chemosensitization and tumour growth of B16 melanoma. Melanoma Res 9: 233-42.
32. Wick W, Stock J, Seyfried J, Baumgart J, Wüllner U, et al. (2002) CD95/CD95 ligand-independent potentiation of treosulfan cytotoxicity by BSO in malignant glioma cells in vitro and in vivo. Int J Oncol 21: 213-20.
33. O'Dwyer PJ, Hamilton TC, LaCreta FP, Gallo JM, Kilpatrick D, et al. (1996) Phase I trial of buthionine sulfoximine in combination with melphalan in patients with cancer. J Clin Oncol 14: 249-56.
34. Bailey HH, Ripple G, Tutsch KD, Arzoomanian RZ, Alberti D, et al. (1997) Phase I study of continuous-infusion L-S,R-buthionine sulfoximine with intravenous melphalan. J Natl Cancer Inst 89: 1789-96.
35. Trachootham D, Alexandre J, Huang P (2009) Targeting cancer cells by ROSmediated mechanisms: a radical therapeutic approach? Nat Rev Drug Discov 8: 579-91.
36. Al-Hajj M, Clarke MF (2004) Self-renewal and solid tumor stem cells. Oncogene 23: 7274-7282.
37. Dingli D, Michor F (2006) Successful therapy must eradicate cancer stem cells. Stem Cells 24: 2603-2610.
38. Prince ME, Sivanandan R, Kaczorowski A, Wolf GT, Kaplan MJ, et al. (2007) Identification of a subpopulation of cells with cancer stem cell properties in head and neck squamous cell carcinoma. Proc Natl Acad Sci U S A 104: 973-8.
39. Fujisawa T, Takeda K, Ichijo H (2007) ASK family proteins in stress response and disease. Mol biotechnol 37: 13-18.
40. Estrela JM, Ortega A, Obrador E (2006) Glutathione in cancer biology and therapy. Crit Rev clin Lab Sci 43: 143-81.
41. Mrowietz U, Asadullah K (2005) Dimethylfumarate for psoriasis: more than a dietary curiosity. Trends Mol Med 11: 43-8.
42. Gu B, DeAngelis LM (2005) Enhanced cytotoxicity of bioreductive antitumor agents with dimethyl fumarate in human glioblastoma cells. Anticancer Drugs 16: 167-74.
43. Odom RY, Dansby MY, Rollins-Hairston AM, Jackson KM, Kirlin WG (2009) Phytochemical induction of cell cycle arrest by glutathione oxidation and reversal by N-acetylcysteine in human colon carcinoma cells. Nutr Cancer 61: 332-9.
44. Nelson KC, Carlson JL, Newman ML, Sternberg P, Jr., Jones DP, et al. (1999) Effect of dietary inducer dimethylfumarate on glutathione in cultured human retinal pigment epithelial cells. Invest Ophtalmol Vis Sci 40: 1927-35.
45. Biaglow JE, Ayene IS, Koch CJ, Donahue J, Stamato TD, et al. (2003) Radiation response of cells during altered protein thiol redox. Radiat Res 159: 484-94.
46. Dethlefsen LA, Lehman CM, Biaglow JE, Peck VM (1988) Toxic effects of acute glutathione depletion by buthionine sulfoximine and dimethylfumarate on murine mammary carcinoma cells. Radiat Res 114: 215-24.
47. Lehnert S, Greene D, Batist G (1990) Radiation response of drug-resistant variants of a human breast cancer cell line: the effect of glutathione depletion. Radiat Res 124: 208-15.
48. Tobiume K, Matsuzawa A, Takahashi T, Nishitoh H, Morita K, et al. (2001) ASK1 is required for sustained activations of JNK/p38 MAP kinases and apoptosis. EMBO Rep 2: 222-8.
49. Matsuzawa A, Nishitoh H, Tobiume K, Takeda K, Ichijo H (2002) Physiological roles of ASK1-mediated signal transduction in oxidative stress- and endoplasmic reticulum stress-induced apoptosis: advanced findings from ASK1 knockout mice. Antioxid Redox Signal 4: 415-25.
50. Matsukawa J, Matsuzawa A, Takeda K, Ichijo H (2004) The ASK1-MAP kinase cascades in mammalian stress response. J Biochem 136: 261-5.
51. Sumbayev VV, Yasinska IM (2005) Regulation of MAP kinase-dependent apoptotic pathway: implication of reactive oxygen and nitrogen species. Arch Biochem Biophys 436: 406-12.
52. Chen CL, Lin CF, Chang WT, Huang WC, Teng CF, et al. (2008) Ceramide induces p38 MAPK and JNK activation through a mechanism involving a thioredoxin-interacting protein-mediated pathway. Blood 111: 4365-74.
53. Dhanasekaran DN, Reddy EP (2008) JNK signaling in apoptosis. Oncogene 27: 6245-51.
54. Roos WP, Kaina B (2006) DNA damage-induced cell death by apoptosis. Trends Mol Med 12: 440-450.
55. Schwartz JL, Rotmensch J, Giovanazzi S, Cohen MB, Weichselbaum RR (1988) Faster repair of DNA double-strand breaks in radioresistant human tumor cells. Int J Radiat Oncol Biol Phys 15: 907-912.
56. Prince ME, Ailles LE (2008) Cancer stem cells in head and neck squamous cell cancer. J Clin Oncol 26: 2871-5.
57. Graziano A, d'Aquino R, Tirino V, Desiderio V, Rossi A, et al. (2008) The stem cell hypothesis in head and neck cancer. J Cell Biochem 103: 408-12.
58. 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: 780-3.
59. Orta T, Eady JJ, Peacock JH, Steel GG (1995) Glutathione manipulation and the radiosensitivity of human tumour and fibroblast cell lines. Int J Radiat Biol 68: 413-9.
60. Gigante M, Toffoli G, Bertola A, Biscontin G, Dassie A, et al. (2003) Radiosensitivity in multidrug resistant and cisplatin-resistant human carcinoma cell lines. Am J Clin Oncol 26: 73-9.
61. Bernier J, Bentzen SM, Vermorken JB (2009) Molecular Therapy in head and neckoncology. Nat Rev Clin Oncol 6: 266-77.
62. Lo Russo L, Lo Muzio L (2009) Combination chemotherapy for head and neck cancer: The addition of Bcl-2 inhibitors. Curr Opin Investig Drugs 10: 1325-33.
63. Thomas SM, Grandis JR (2009) The Current States of Head and Neck Cancer Gene Therapy. Hum Gen Ther 20: 1565-1575.