Inhibition of GSH synthesis potentiates temozolomide-induced bystander effect in glioblastoma

Cancer Letters

Volumn 331, Issue 1, 2013, Pages 68-75

  Kohsaka, Shinji ^a   Takahashi, Kenta ^a   Wang, Lei ^a   Tanino, Mishie ^a   Kimura, Taichi ^a   Nishihara, Hiroshi ^a   Tanaka, Shinya ^a  

^a HOKKAIDO UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

Brain tumor; GBM; MGMT; Temozolomide

Indexed keywords

ANTIOXIDANT; CATALASE; GLUTATHIONE; MANGANESE SUPEROXIDE DISMUTASE; METHYLATED DNA PROTEIN CYSTEINE METHYLTRANSFERASE; TEMOZOLOMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BYSTANDER EFFECT; CELL DAMAGE; CELL DEATH; CELL STIMULATION; CELL STRAIN KMG4; CELL STRESS; CONTROLLED STUDY; CULTURE MEDIUM; CYTOTOXICITY; DRUG POTENTIATION; DRUG RESISTANCE; DRUG SENSITIVITY; FEMALE; GENE EXPRESSION; GLIOBLASTOMA; GLUTATHIONE METABOLISM; GLUTATHIONE SYNTHESIS INHIBITION; HUMAN; HUMAN CELL; IN VIVO STUDY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; TUMOR CELL LINE; TUMOR MODEL; TUMOR RESISTANCE; TUMOR VOLUME; UPREGULATION;

ANIMALS; ANTINEOPLASTIC AGENTS, ALKYLATING; APOPTOSIS; BLOTTING, WESTERN; BRAIN NEOPLASMS; BYSTANDER EFFECT; CATALASE; CELL PROLIFERATION; CULTURE MEDIA, CONDITIONED; DACARBAZINE; DNA METHYLATION; DNA MODIFICATION METHYLASES; DNA REPAIR ENZYMES; DRUG RESISTANCE, NEOPLASM; FEMALE; GLIOBLASTOMA; GLUTATHIONE; HUMANS; IMMUNOENZYME TECHNIQUES; MICE; MICE, INBRED BALB C; REAL-TIME POLYMERASE CHAIN REACTION; RNA, SMALL INTERFERING; SUPEROXIDE DISMUTASE; TUMOR CELLS, CULTURED; TUMOR SUPPRESSOR PROTEINS; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84873526155     PISSN: 03043835     EISSN: 18727980     Source Type: Journal    
DOI: 10.1016/j.canlet.2012.12.005     Document Type: Article

References (43)

1. Louis D.N., Ohgaki H., Wiestler O.D., Cavenee W.K., Burger P.C., Jouvet A., Scheithauer B.W., Kleihues P. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol. 2007, 114:97-109.
2. Van Meir E.G., Hadjipanayis C.G., Norden A.D., Shu H.K., Wen P.Y., Olson J.J. Exciting new advances in neuro-oncology: the avenue to a cure for malignant glioma. CA Cancer J. Clin. 2010, 60:166-193.
3. Stupp R., Mason W.P., van den Bent M.J., Weller M., Fisher B., Taphoorn M.J., Belanger K., Brandes A.A., Marosi C., Bogdahn U., Curschmann J., Janzer R.C., Ludwin S.K., Gorlia T., Allgeier A., Lacombe D., Cairncross J.G., Eisenhauer E., Mirimanoff R.O. Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. New Engl. J. Med. 2005, 352:987-996.
4. Mrugala M.M., Chamberlain M.C. Mechanisms of disease: temozolomide and glioblastoma - look to the future. Nat. Clin. Pract. Oncol. 2008, 5:476-486.
5. Cheng C.L., Johnson S.P., Keir S.T., Quinn J.A., Ali-Osman F., Szabo C., Li H., Salzman A.L., Dolan M.E., Modrich P., Bigner D.D., Friedman H.S. Poly(ADP-ribose) polymerase-1 inhibition reverses temozolomide resistance in a DNA mismatch repair-deficient malignant glioma xenograft. Mol. Cancer Ther. 2005, 4:1364-1368.
6. Trivedi R.N., Almeida K.H., Fornsaglio J.L., Schamus S., Sobol R.W. The role of base excision repair in the sensitivity and resistance to temozolomide-mediated cell death. Cancer Res. 2005, 65:6394-6400.
7. 6-alkylguanine-DNA alkyltransferase which confer significant resistance of human glial tumor xenografts to treatment with 1,3-bis(2-chloroethyl)-1-nitrosourea or temozolomide. Clin. Cancer Res. 2001, 7:421-428.
8. Hegi M.E., Diserens A.C., Gorlia T., Hamou M.F., de Tribolet N., Weller M., Kros J.M., Hainfellner J.A., Mason W., Mariani L., Bromberg J.E., Hau P., Mirimanoff R.O., Cairncross J.G., Janzer R.C., Stupp R. MGMT gene silencing and benefit from temozolomide in glioblastoma. New Engl. J. Med. 2005, 352:997-1003.
9. 6-methylguanine-DNA methyltransferase status in glioma: relationship between immunohistochemistry and methylation analysis. Am. J. Surg. Pathol. 2008, 32:1220-1227.
10. 6-alkylguanine-DNA-alkyltransferase: phase I safety, pharmacodynamic, and pharmacokinetic trial and evaluation in combination with temozolomide in patients with advanced solid tumors. Clin. Cancer Res. 2006, 12:1577-1584.
11. 6-alkylguanine DNA alkyltransferase inhibitors. Expert Opin. Invest. Drugs 2007, 16:1573-1584.
12. 6-benzylguanine for patients with recurrent or progressive malignant glioma. J. Clin. Oncol. 2005, 23:7178-7187.
13. 6-benzylguanine in adults with recurrent, temozolomide-resistant malignant glioma. J. Clin. Oncol. 2009, 27:1262-1267.
14. Kohsaka S., Wang L., Yachi K., Mahabir R., Narita T., Itoh T., Tanino M., Kimura T., Nishihara H., Tanaka S. STAT3 inhibition overcomes temozolomide resistance in glioblastoma by downregulating MGMT expression. Mol. Cancer Ther. 2012, 11:1289-1299.
15. Chhipa R.R., Bhat M.K. Bystander killing of breast cancer MCF-7 cells by MDA-MB-231 cells exposed to 5-fluorouracil is mediated via Fas. J. Cell. Biochem. 2007, 101:68-79.
16. Merle P., Morvan D., Caillaud D., Demidem A. Chemotherapy-induced bystander effect in response to several chloroethylnitrosoureas: an origin independent of DNA damage?. Anticancer Res. 2008, 28:21-27.
17. Gorman S., Tosetto M., Lyng F., Howe O., Sheahan K., O'Donoghue D., Hyland J., Mulcahy H., O'Sullivan J. Radiation and chemotherapy bystander effects induce early genomic instability events: telomere shortening and bridge formation coupled with mitochondrial dysfunction. Mutat. Res. 2009, 669:131-138.
18. Narayanan P.K., Goodwin E.H., Lehnert B.E. Alpha particles initiate biological production of superoxide anions and hydrogen peroxide in human cells. Cancer Res. 1997, 57:3963-3971.
19. Shao C., Folkard M., Prise K.M. Role of TGF-beta1 and nitric oxide in the bystander response of irradiated glioma cells. Oncogene 2008, 27:434-440.
20. Azzam E.I., de Toledo S.M., Little J.B. Direct evidence for the participation of gap junction-mediated intercellular communication in the transmission of damage signals from alpha-particle irradiated to nonirradiated cells. Proc. Natl. Acad Sci. USA 2001, 98:473-478.
21. Akagi T., Sasai K., Hanafusa H. Refractory nature of normal human diploid fibroblasts with respect to oncogene-mediated transformation. Proc. Natl. Acad Sci. USA 2003, 100:13567-13572.
22. Kohsaka S., Sasai K., Takahashi K., Akagi T., Tanino M., Kimura T., Nishihara H., Tanaka S. A population of BJ fibroblasts escaped from Ras-induced senescence susceptible to transformation. Biochem. Biophys. Res. Commun. 2011, 410:878-884.
23. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
24. Qian B.Z., Pollard J.W. Macrophage diversity enhances tumor progression and metastasis. Cell 2010, 141:39-51.
25. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
26. Weigert A., Tzieply N., von Knethen A., Johann A.M., Schmidt H., Geisslinger G., Brune B. Tumor cell apoptosis polarizes macrophages role of sphingosine-1-phosphate. Mol. Biol. Cell 2007, 18:3810-3819.
27. Johann A.M., Weigert A., Eberhardt W., Kuhn A.M., Barra V., von Knethen A., Pfeilschifter J.M., Brune B. Apoptotic cell-derived sphingosine-1-phosphate promotes HuR-dependent cyclooxygenase-2 mRNA stabilization and protein expression. J. Immunol. 2008, 180:1239-1248.
28. Trachootham D., Alexandre J., Huang P. Targeting cancer cells by ROS-mediated mechanisms: a radical therapeutic approach?. Nat. Rev. 2009, 8:579-591.
29. Ramanathan B., Jan K.Y., Chen C.H., Hour T.C., Yu H.J., Pu Y.S. Resistance to paclitaxel is proportional to cellular total antioxidant capacity. Cancer Res. 2005, 65:8455-8460.
30. Lenehan P.F., Gutierrez P.L., Wagner J.L., Milak N., Fisher G.R., Ross D.D. Resistance to oxidants associated with elevated catalase activity in HL-60 leukemia cells that overexpress multidrug-resistance protein does not contribute to the resistance to daunorubicin manifested by these cells. Cancer Chemother. Pharmacol. 1995, 35:377-386.
31. Reya T., Morrison S.J., Clarke M.F., Weissman I.L. Stem cells, cancer, and cancer stem cells. Nature 2001, 414:105-111.
32. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
33. Galli R., Binda E., Orfanelli U., Cipelletti B., Gritti A., De Vitis S., Fiocco R., Foroni C., Dimeco F., Vescovi A. Isolation and characterization of tumorigenic, stem-like neural precursors from human glioblastoma. Cancer Res. 2004, 64:7011-7021.
34. Kemper K., Sprick M.R., de Bree M., Scopelliti A., Vermeulen L., Hoek M., Zeilstra J., Pals S.T., Mehmet H., Stassi G., Medema J.P. The AC133 epitope, but not the CD133 protein, is lost upon cancer stem cell differentiation. Cancer Res. 2010, 70:719-729.
35. Wan F., Zhang S., Xie R., Gao B., Campos B., Herold-Mende C., Lei T. The utility and limitations of neurosphere assay, CD133 immunophenotyping and side population assay in glioma stem cell research. Brain Pathol. 2010, 20:877-889.
36. Ogden A.T., Waziri A.E., Lochhead R.A., Fusco D., Lopez K., Ellis J.A., Kang J., Assanah M., McKhann G.M., Sisti M.B., McCormick P.C., Canoll P., Bruce J.N. Identification of A2B5+CD133 tumor-initiating cells in adult human gliomas. Neurosurgery 2008, 62:505-514; discussion 514-505.
37. Lathia J.D., Gallagher J., Heddleston J.M., Wang J., Eyler C.E., Macswords J., Wu Q., Vasanji A., McLendon R.E., Hjelmeland A.B., Rich J.N. Integrin alpha 6 regulates glioblastoma stem cells. Cell Stem Cell 2010, 6:421-432.
38. Read T.A., Fogarty M.P., Markant S.L., McLendon R.E., Wei Z., Ellison D.W., Febbo P.G., Wechsler-Reya R.J. Identification of CD15 as a marker for tumor-propagating cells in a mouse model of medulloblastoma. Cancer Cell. 2009, 15:135-147.
39. Son M.J., Woolard K., Nam D.H., Lee J., Fine H.A. SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 2009, 4:440-452.
40. Esteller M., Garcia-Foncillas J., Andion E., Goodman S.N., Hidalgo O.F., Vanaclocha V., Baylin S.B., Herman J.G. Inactivation of the DNA-repair gene MGMT and the clinical response of gliomas to alkylating agents. New Engl. J. Med. 2000, 343:1350-1354.
41. 6-methylguanine-DNA methyltransferase and survival in inoperable newly diagnosed glioblastoma patients treated with neoadjuvant temozolomide. J. Clin. Oncol. 2007, 25:1470-1475.
42. Martinez R., Schackert G., Yaya-Tur R., Rojas-Marcos I., Herman J.G., Esteller M. Frequent hypermethylation of the DNA repair gene MGMT in long-term survivors of glioblastoma multiforme. J. Neurooncol. 2007, 83:91-93.
43. Natsume A., Ishii D., Wakabayashi T., Tsuno T., Hatano H., Mizuno M., Yoshida J. IFN-beta down-regulates the expression of DNA repair gene MGMT and sensitizes resistant glioma cells to temozolomide. Cancer Res. 2005, 65:7573-7579.