Paclitaxel combined with inhibitors of glucose and hydroperoxide metabolism enhances breast cancer cell killing via H2O2-mediated oxidative stress

Free Radical Biology and Medicine

Volumn 48, Issue 8, 2010, Pages 1024-1033

  Hadzic, Tanja ^a   Aykin Burns, Nükhet ^a   Zhu, Yueming ^a   Coleman, Mitchell C ^a   Leick, Katie ^a   Jacobson, Geraldine M ^a   Spitz, Douglas R ^a  

^a UNIVERSITY OF IOWA   (United States)

Author keywords

2 Deoxy d glucose; Breast cancer; Cancer vs normal cells; Chemosensitization; Free radicals; Hydroperoxide metabolism; Metabolic oxidative stress

Indexed keywords

BUTHIONINE SULFOXIMINE; DEOXYGLUCOSE; GLUCOSE; GLUTATHIONE; GLUTATHIONE DISULFIDE; HYDROGEN PEROXIDE; HYDROPEROXIDE; PACLITAXEL;

ANTINEOPLASTIC ACTIVITY; ARTICLE; BREAST CANCER; BREAST EPITHELIUM; CANCER CELL CULTURE; COMBINATION CHEMOTHERAPY; CONTROLLED STUDY; CYTOTOXICITY; DRUG EFFICACY; DRUG POTENTIATION; DRUG SELECTIVITY; FIBROBLAST; GLUCOSE METABOLISM; HUMAN; HUMAN CELL; MONOTHERAPY; OXIDATIVE STRESS; PRIORITY JOURNAL;

BREAST NEOPLASMS; BUTHIONINE SULFOXIMINE; CELL SURVIVAL; DEOXYGLUCOSE; DRUG SYNERGISM; FEMALE; FIBROBLASTS; GLUCOSE; HUMANS; HYDROGEN PEROXIDE; OXIDATIVE STRESS; PACLITAXEL; REACTIVE OXYGEN SPECIES; TUMOR CELLS, CULTURED;

EID: 77950518021     PISSN: 08915849     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2010.01.018     Document Type: Article

References (40)

1. Holmes F.A., Walters R.S., Theriault R.L., Forman A.D., Newton H., Yasuda H., Karin M., Kikugawa K. Phase II trial of taxol, active drug in the treatment of metastatic breast cancer. J. Natl. Cancer Inst. 1991, 83:1797-1805.
2. Liebmann J., Cook J.A., Fisher J., Teague D., Mitchell J.B. In vitro studies of taxol as a radiation sensitizer in human tumor cells. J. Natl. Cancer Inst. 1994, 86:441-446.
3. Glass-Marmor L., Beitner R. Taxol [paclitaxel] induces a detachment of phosphofructokinase from cytoskeleton of melanoma cells and decreases the levels of glucose-1,6-biphosphate, fructose-1,6-biphosphate and ATP. Eur. J. Pharmacol. 1999, 370:195-199.
4. Singh S.P., Gao Y., Singh L.D., Kunapuli S.P., Revindra R. Role of microtubules in glucose uptake by C6 glioma cells. Pharmacol. Toxicol. 1998, 83:83-89.
5. Orr G.A., Verdier-Pinard P., McDaid H., Horwitz S.B. Mechanisms of taxol resistance related to microtubules. Oncogene 2003, 22:7280-7295.
6. Alexandre J., Batteux F., Nicco C., Chereau C., Laurent A., Guillevin L., Weill B., Goldwasser F. Accumulation of hydrogen peroxide is an early and crucial step for paclitaxel-induced cancer cell death both in vitro and in vivo. Int. J. Cancer 2006, 119:41-48.
7. Swatrowski T.P., Nathan C.F. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991, 51:794-798.
8. Spitz D.R., Sim J.E., Ridnour L.A., Galoforo S.S., Lee Y.J. Glucose deprivation-induced oxidative stress in human tumor cells: a fundamental defect in metabolism?. Ann. N.Y. Acad. Sci. 2000, 899:349-362.
9. Andringa K.K., Coleman M.C., Aykin-Burns N., Hitchler M.J., Walsh S.A., Domann F.E., Spitz D.R. Inhibition of glutamate cysteine ligase activity sensitizes human breast cancer cells to the toxicity of 2-deoxy-d-glucose. Cancer Res. 2006, 66:1605-1610.
10. 2-resistant cell lines: do aldehydic by-products of lipid peroxidation contribute to oxidative stress?. Biochem. J. 1990, 267:453-459.
11. Anderson M.E. Handbook of Methods for Oxygen Radical Research 1985, 317-323. CRC Press, Boca Raton, FL. R.A. Greenwald (Ed.).
12. Griffith O.W. Determination of glutathione and glutathione disulfide using glutathione reductase and 2-vinylpyridine. Anal. Biochem. 1980, 106:207-212.
13. Lowry O.H., Rosebrough N.J., Farr A.L., Randall R.L. Protein measurements with the folin phenol reagent. J. Biol. Chem. 1951, 193:265-275.
14. Mavis R.D., Stellwagen E. Purification and subunit structure of glutathione reductase from baker's yeast. J. Biol. Chem. 1968, 243:809-814.
15. Alexandre J., Hu Y., Lu W., Pelicano H., Huang P. Novel action of paclitaxel against cancer cells: bystander effect mediated by reactive oxygen species. Cancer Res. 2007, 67:3512-3517.
16. Blackburn R.V., Spitz D.R., Liu S., Galoforo S.S., Sim J.E., Ridnour L.A., Chen J.C., Davis B.H., Corry P.M., Lee Y.L. Metabolic oxidative stress activates signal transduction and gene expression during glucose deprivation in human tumor cells. Free Radic. Biol. Med. 1999, 26:419-430.
17. Averill-Bates D.A., Przybytkowski E. The role of glucose in cellular defenses against cytotoxicity of hydrogen peroxide in CHO cells. Arch. Biochem. Biophys. 1994, 312:52-58.
18. Lin X., Zhang F., Bradbury C.M., Kaushal A., Li L., Spitz D.R., Aft R.L., Gius D. 2-Deoxy-d-glucose-induced cytotoxicity and radiosensitization in tumor cells are mediated via disruptions in thiol metabolism. Cancer Res. 2003, 63:3413-3418.
19. 2 mediate glucose deprivation-induced cytotoxicity and oxidative stress in human cancer cells. J. Biol. Chem. 2005, 11:4254-4263.
20. Simons A.L., Ahmad I.M., Mattson D.M., Dornfeld K.J., Spitz D.R. 2-Deoxy-d-glucose combined with cisplatin enhances cytotoxicity via metabolic oxidative stress in human head and neck cancer cells. Cancer Res. 2007, 67:3364-3370.
21. Kassim T., Rajni S., Rajesh K.T., Walter H.W., Shyam B., Michael A.T. Redox-regulation of Erk1/2-directed phosphatase by reactive oxygen species: role in signaling TPA-induced growth arrest in ML-1 cells. J. Cell. Physiol. 2008, 216:276-285.
22. Klees R.F., De Marco P.C., Salasznyk R.M., Ahuja D., Hogg M., Antoniotti S., Kamath L., Dordick J.S., Plopper G.E. Apocynin derivatives interrupt intracellular signaling resulting in decreased migration in breast cancer cells. J. Biomed. Biotechnol. 2006, 2:87246-87250.
23. Kallio A., Zheng A., Dahllund J., Heiskanen K.M., Härkönen P. Role of mitochondria in tamoxifen-induced rapid death of MCF-7 breast cancer cells. Apoptosis 2005, 10:1395-1410.
24. Varbiro G., Veres B., Gallyas F.J., Sumegi B. Direct effect of taxol on free radical formation and mitochondrial permeability transition. Free Radic. Biol. Med. 2001, 31:548-558.
25. Aft R.L., Zhang F.W., Gius D. Evaluation of 2-deoxy-d-glucose as a chemotherapeutic agent: mechanism of cell death. Br. J. Cancer 2002, 87:805-812.
26. Spitz D.R., Kinter M.T., Roberts R.J. The contribution of increased glutathione content to mechanisms of oxidative stress resistance in hydrogen peroxide resistant hamster fibroblasts. J. Cell. Physiol. 1995, 165:600-609.
27. Arrick B.A., Griffith O.W., Cerami A. Inhibition of glutathione synthesis as a chemotherapeutic strategy for trypanosomiasis. J. Exp. Med. 1981, 153:720-725.
28. Aykin-Burns N., Ahmad I.M., Zhu Y., Oberley L.W., Spitz D.R. Increased levels of superoxide and hydrogen peroxide mediate the differential susceptibility of cancer cells versus normal cells to glucose deprivation. Biochem. J. 2009, 418:29-37.
29. Kurtoglu M., Gao N., Shang J., Maher J.C., Lehrman M.A., Wangpaichitr M., Savaraj N., Lane A.N., Lampidis T.J. Under normoxia, 2-deoxy-d-glucose elicits cell death in select tumor types not by inhibition of glycolysis but by interfering with N-linked glycosylation. Mol. Cancer Ther. 2007, 6:3049-3058.
30. Hung, J.Y.; Hsu, Y.L.; Ni, W.C.; Tsai, Y.M.; Yang, C.J.; Kuo, P.L.; Huang, M.S. Oxidative and endoplasmic reticulum stress signaling are involved in dehydrocostuslactone-mediated apoptosis in human non-small cell lung cancer cells. Lung Cancer [Electronic publication ahead of print]. PMID 20004998.
31. Lee W.L., Wen T.N., Shiau J.Y., Shyur L.F. Differential proteomic profiling identifies novel molecular targets of paclitaxel and phytoagent deoxyelephantopin against mammary adenocarcinoma cells. J. Proteome Res. 2010, 9(1):237-253.
32. Bailey H.H. l-S,R-buthionine sulfoximine: historical development and clinical issues. Chem. Biol. Interact. 1998, 111-112:239-254.
33. Landau B.R., Lubs H.A. Animal responses to 2-deoxy-d-glucose administration. Proc. Soc. Exp. Biol. Med. 1958, 99:124-127.
34. Mohanti B.K., Rath G.K., Anantha N., Kannan V., Das B.S., Chandramouli B.A., Banerjee A.K., Das S., Jena A., Ravichandran R., Sahi U.P., Kumar R., Kapoor N., Kalia V.K., Dwarakanath B.S., Jain V. Improving cancer radiotherapy with 2-deoxy-d-glucose: phase I/II clinical trials on human cerebral gliomas. Int. J. Radiat. Oncol. Biol. Phys. 1996, 35:103-111.
35. Maschek G., Savaraj N., Priebe W., Braunschweiger P., Hamilton K., Tidmarsh G.F., De Young L.R., Lampidis T.J. 2-Deoxy-d-glucose increases the efficacy of adriamycin and paclitaxel in human osteosarcoma and non-small cell lung cancers in vivo. Cancer Res. 2004, 64:31-34.
36. 2 in vitro and in vivo and reduce menandione-induced DNA injury and cytotoxicity. Am. J. Physiol. 1995, 268:227-236.
37. Di Monaco M., Pizzini A., Gatto V., Leonardi L., Gallo M., Brignardello E., Boccuzzi G. Role of glucose-6-phosphate dehydrogenase inhibition in the antiproliferative effects of dehydroepiandrosterone on human breast cancer cells. Br. J. Cancer 1997, 75:589-592.
38. Berggren M.I., Husbeck B., Samulitis B., Baker A.F., Gallegos A., Powis G. Thioredoxin peroxidase-1 [peroxiredoxin-1] is increased in thioredoxin-1 transfected cells and results in enhanced protection against apoptosis caused by hydrogen peroxide but not by other agents including dexamethasone, etoposide, and doxorubicin. Arch. Biochem. Biophys. 2001, 392:103-109.
39. Nomura K., Imai H., Koumura T., Arai M., Nakagawa Y. Mitochondrial phospholipid hydroperoxide glutathione peroxidase suppresses apoptosis mediated by a mitochondrial death pathway. J. Biol. Chem. 1999, 274:29294-29302.
40. Tuttle S.W., Varnes M.E., Mitchell J.B., Biaglow J.E. Sensitivity to chemical oxidants and radiation in CHO cell lines deficient in oxidative pentose cycle activity. Int. J. Radiat. Oncol. Biol. Phys. 1992, 22:671-675.