Decreasing GSH and increasing ROS in chemosensitivity gliomas with IDH1 mutation

Tumor Biology

Volumn 36, Issue 2, 2015, Pages 655-662

  Shi, Jinlong ^a   Sun, Baolan ^a   Shi, Wei ^a   Zuo, Hao ^a   Cui, Daming ^b   Ni, Lanchun ^a   Chen, Jian ^a  

^a NANTONG UNIVERSITY   (China)

^b TONGJI UNIVERSITY SCHOOL OF MEDICINE   (China)

Author keywords

Chemotherapy; Gliomas; Glutathione; Isocitrate dehydrogenase 1; Reactive oxygen species

Indexed keywords

CISPLATIN; GLUTATHIONE; ISOCITRATE DEHYDROGENASE 1; MUTANT PROTEIN; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; TEMOZOLOMIDE; DACARBAZINE; IDH1 PROTEIN, HUMAN; ISOCITRATE DEHYDROGENASE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CARCINOGENICITY; CHEMOSENSITIVITY; CONTROLLED STUDY; FEMALE; GENE MUTATION; GENE OVEREXPRESSION; GLIOBLASTOMA; GLIOBLASTOMA CELL LINE; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; SITE DIRECTED MUTAGENESIS; WILD TYPE; ANALOGS AND DERIVATIVES; BIOSYNTHESIS; CELL PROLIFERATION; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; GLIOMA; METABOLISM; MUTATION; PATHOLOGY; PROGNOSIS;

CELL PROLIFERATION; CISPLATIN; DACARBAZINE; GENE EXPRESSION REGULATION, NEOPLASTIC; GLIOMA; HUMANS; ISOCITRATE DEHYDROGENASE; MUTATION; PROGNOSIS; REACTIVE OXYGEN SPECIES;

EID: 84925536048     PISSN: 10104283     EISSN: 14230380     Source Type: Journal    
DOI: 10.1007/s13277-014-2644-z     Document Type: Article

References (53)

1. Jemal A, Siegel R, Ward E, Hao Y, Xu J, Thun MJ. Cancer statistics, 2009. CA Cancer J Clin. 2009;59(4):225–49.
2. Su Y, Li G, Zhang X, Gu J, Zhang C, Tian Z, et al. JSI-124 inhibits glioblastoma multiforme cell proliferation through G(2)/M cell cycle arrest and apoptosis augment. Cancer Biol Ther. 2008;7(8):1243–9.
3. Yin D, Wakimoto N, Xing H, Lu D, Huynh T, Wang X, et al. Cucurbitacin B markedly inhibits growth and rapidly affects the cytoskeleton in glioblastoma multiforme. Int J Cancer. 2008;123(6):1364–75.
4. Jeon JY, An JH, Kim SU, Park HG, Lee MA. Migration of human neural stem cells toward an intracranial glioma. Exp Mol Med. 2008;40(1):84–91.
5. Georgescu MM, Kirsch KH, Akagi T, Shishido T, Hanafusa H. The tumor-suppressor activity of PTEN is regulated by its carboxyl-terminal region. Proc Natl Acad Sci U S A. 1999;96(18):10182–7.
6. Parsons DW, Jones S, Zhang X, Lin JC, Leary RJ, Angenendt P, et al. An integrated genomic analysis of human glioblastoma multiforme. Science. 2008;321(5897):1807–12.
7. Sonoda Y, Kumabe T, Nakamura T, Saito R, Kanamori M, Yamashita Y, et al. Analysis of IDH1 and IDH2 mutations in Japanese glioma patients. Cancer Sci. 2009;100(10):1996–8.
8. Yan H, Parsons DW, Jin G, McLendon R, Rasheed BA, Yuan W, et al. IDH1 and IDH2 mutations in gliomas. N Engl J Med. 2009;360(8):765–73.
9. Weller M, Felsberg J, Hartmann C, Berger H, Steinbach JP, Schramm J, et al. Molecular predictors of progression-free and overall survival in patients with newly diagnosed glioblastoma: a prospective translational study of the German Glioma Network. J Clin Oncol. 2009;27(34):5743–50.
10. +-dependent IDH activity in glioblastoma. Acta Neuropathol. 2010;119(4):487–94.
11. Dubbink HJ, Taal W, van Marion R, Kros JM, van Heuvel I, Bromberg JE, et al. IDH1 mutations in low-grade astrocytomas predict survival but not response to temozolomide. Neurology. 2009;73(21):1792–5.
12. Metellus P, Coulibaly B, Colin C, de Paula AM, Vasiljevic A, Taieb D, et al. Absence of IDH mutation identifies a novel radiologic and molecular subtype of WHO grade II gliomas with dismal prognosis. Acta Neuropathol. 2010;120(6):719–29.
13. Yan W, Zhang W, You G, Bao Z, Wang Y, Liu Y, et al. Correlation of IDH1 mutation with clinicopathologic factors and prognosis in primary glioblastoma: a report of 118 patients from China. PLoS One. 2012;7(1):e30339.
14. Xie F, Tang JJ, Wang X, Liu YH, Mao Q. Correlation between IDH1 mutation and prognosis in supratentorial high-grade astrocytomas. Sichuan Da Xue Xue Bao Yi Xue Ban. 2013;44(2):184–7. 192.
15. Bujko M, Kober P, Matyja E, Nauman P, Dyttus-Cebulok K, Czeremszynska B. Prognostic value of IDH1 mutations identified with PCR-RFLP assay in glioblastoma patients. Mol Diagn Ther. 2010;14(3):163–9.
16. Hartmann C, Hentschel B, Tatagiba M, Schramm J, Schnell O, Seidel C, et al. Molecular markers in low-grade gliomas: predictive or prognostic? Clin Cancer Res. 2011;17(13):4588–99.
17. Houillier C, Wang X, Kaloshi G, Mokhtari K, Guillevin R, Laffaire J, et al. IDH1 or IDH2 mutations predict longer survival and response to temozolomide in low-grade gliomas. Neurology. 2010;75(17):1560–6.
18. van den Bent MJ, Dubbink HJ, Marie Y, Brandes AA, Taphoorn MJ, Wesseling P, et al. IDH1 and IDH2 mutations are prognostic but not predictive for outcome in anaplastic oligodendroglial tumors: a report of the European Organization for Research and Treatment of Cancer Brain Tumor Group. Clin Cancer Res. 2010;16(5):1597–604.
19. Sasaki M, Knobbe CB, Itsumi M, Elia AJ, Harris IS, Chio II, et al. d-2-Hydroxyglutarate produced by mutant IDH1 perturbs collagen maturation and basement membrane function. Genes Dev. 2012;26(18):2038–49.
20. Mohrenz IV, Antonietti P, Pusch S, Capper D, Balss J, Voigt S, et al. Isocitrate dehydrogenase 1 mutant R132H sensitizes glioma cells to BCNU-induced oxidative stress and cell death. Apoptosis. 2013;18:1416–25.
21. Kim J, Kim JI, Jang HS, Park JW, Park KM. Protective role of cytosolic NADP(+)-dependent isocitrate dehydrogenase, IDH1, in ischemic pre-conditioned kidney in mice. Free Radic Res. 2011;45(7):759–66.
22. Geisbrecht BV, Gould SJ. The human PICD gene encodes a cytoplasmic and peroxisomal NADP(+)-dependent isocitrate dehydrogenase. J Biol Chem. 1999;274(43):30527–33.
23. Duran M, Kamerling JP, Bakker HD, van Gennip AH, Wadman SK. l-2-Hydroxyglutaric aciduria: an inborn error of metabolism? J Inherit Metab Dis. 1980;3(4):109–12.
24. Chuang JI, Chang TY, Liu HS. Glutathione depletion-induced apoptosis of Ha-ras-transformed NIH3T3 cells can be prevented by melatonin. Oncogene. 2003;22(9):1349–57.
25. Ghibelli L, Fanelli C, Rotilio G, Lafavia E, Coppola S, Colussi C, et al. Rescue of cells from apoptosis by inhibition of active GSH extrusion. FASEB J. 1998;12(6):479–86.
26. Guha P, Dey A, Sen R, Chatterjee M, Chattopadhyay S, Bandyopadhyay SK. Intracellular GSH depletion triggered mitochondrial Bax translocation to accomplish resveratrol-induced apoptosis in the U937 cell line. J Pharmacol Exp Ther. 2011;336(1):206–14.
27. Gottesman MM, Fojo T, Bates SE. Multidrug resistance in cancer: role of ATP-dependent transporters. Nat Rev Cancer. 2002;2(1):48–58.
28. Kretz-Remy C, Arrigo AP. Gene expression and thiol redox state. Methods Enzymol. 2002;348:200–15.
29. Juan ME, Wenzel U, Daniel H, Planas JM. Resveratrol induces apoptosis through ROS-dependent mitochondria pathway in HT-29 human colorectal carcinoma cells. J Agric Food Chem. 2008;56(12):4813–8.
30. Mardis ER, Ding L, Dooling DJ, Larson DE, McLellan MD, Chen K, et al. Recurring mutations found by sequencing an acute myeloid leukemia genome. N Engl J Med. 2009;361(11):1058–66.
31. Guo C, Pirozzi CJ, Lopez GY, Yan H. Isocitrate dehydrogenase mutations in gliomas: mechanisms, biomarkers and therapeutic target. Curr Opin Neurol. 2011;24(6):648–52.
32. Lin CJ, Lee CC, Shih YL, Lin CH, Wang SH, Chen TH, et al. Inhibition of mitochondria- and endoplasmic reticulum stress-mediated autophagy augments temozolomide-induced apoptosis in glioma cells. PLoS One. 2012;7(6):e38706.
33. Kohsaka S, Takahashi K, Wang L, Tanino M, Kimura T, Nishihara H, et al. Inhibition of GSH synthesis potentiates temozolomide-induced bystander effect in glioblastoma. Cancer Lett. 2013;331(1):68–75.
34. Oliva CR, Moellering DR, Gillespie GY, Griquer CE, et al. Acquisition of chemoresistance in gliomas is associated with increased mitochondrial coupling and decreased ROS production. PLoS One. 2011;6(9):e24665.
35. Schweyer S, Soruri A, Heintze A, Rzdzun HJ, Favvazi A. The role of reactive oxygen species in cisplatin-induced apoptosis in human malignant testicular germ cell lines. Int J Oncol. 2004;25(6):1671–6.
36. Yu ZY, Liang YG, Xiao H, Shan YJ, Dong B, Huang R. Melissoidesin G, a diterpenoid purified from Isodon melissoides, induces leukemic-cell apoptosis through induction of redox imbalance and exhibits synergy with other anticancer agents. Int J Cancer. 2007;121(9):2084–94.
37. Das GC, Bacsi A, Shrivastav M, Hazra TK, Boldogh I. Enhanced gamma-glutamylcysteine synthetase activity decreases drug-induced oxidative stress levels and cytotoxicity. Mol Carcinog. 2006;45(9):635–47.
38. Li S, Chou AP, Chen W, Chen R, Deng Y, Phillips HS, et al. Overexpression of isocitrate dehydrogenase mutant proteins renders glioma cells more sensitive to radiation. Neuro Oncol. 2013;15(1):57–68.
39. Zhao S, Lin Y, Xu W, Jiang W, Zha Z, Wang P, et al. Glioma-derived mutations in IDH1 dominantly inhibit IDH1 catalytic activity and induce HIF-1alpha. Science. 2009;324(5924):261–5.
40. Dang L, White DW, Gross S, Bennett BD, Bittinger MA, Driggers EM, et al. Cancer-associated IDH1 mutations produce 2-hydroxyglutarate. Nature. 2009;462(7274):739–44.
41. Szatrowski TP, Nathan CF. Production of large amounts of hydrogen peroxide by human tumor cells. Cancer Res. 1991;51(3):794–8.
42. Hu Y, Rosen DG, Zhou Y, Feng L, Yang G, Liu J, et al. Mitochondrial manganese-superoxide dismutase expression in ovarian cancer: role in cell proliferation and response to oxidative stress. J Biol Chem. 2005;280(47):39485–92.
43. Toyokuni S. Oxidative stress and cancer: the role of redox regulation. Biotherapy. 1998;11(2–3):147–54.
44. Kondo S, Toyokuni S, Iwasa Y, Tanaka T, Onodera H, Hiai H, et al. Persistent oxidative stress in human colorectal carcinoma, but not in adenoma. Free Radic Biol Med. 1999;27(3–4):401–10.
45. Devi GS, Prasad MH, Saraswathi I, Raghu D, Rao DN, Reddy PP. Free radicals antioxidant enzymes and lipid peroxidation in different types of leukemias. Clin Chim Acta. 2000;293(1–2):53–62.
46. Hileman EA, Achanta G, Huang P. Superoxide dismutase: an emerging target for cancer therapeutics. Expert Opin Ther Targets. 2001;5(6):697–710.
47. Lyss G, Knorre A, Schmidt TJ, Pahl HL, Merfort I. The anti-inflammatory sesquiterpene lactone helenalin inhibits the transcription factor NF-kappaB by directly targeting p65. J Biol Chem. 1998;273(50):33508–16.
48. Ghantous A, Gali-Muhtasib H, Vuorela H, Saliba NA, Darwiche N. What made sesquiterpene lactones reach cancer clinical trials? Drug Discov Today. 2010;15(15–16):668–78.
49. Sharma V, Joseph C, Ghosh S, Agarwal A, Mishra MK, Sen E. Kaempferol induces apoptosis in glioblastoma cells through oxidative stress. Mol Cancer Ther. 2007;6(9):2544–53.
50. Pramanik KC, Boreddy SR, Srivastava SK. Role of mitochondrial electron transport chain complexes in capsaicin mediated oxidative stress leading to apoptosis in pancreatic cancer cells. PLoS One. 2011;6(5):e20151.
51. Sun J, McKallip RJ. Plumbagin treatment leads to apoptosis in human K562 leukemia cells through increased ROS and elevated TRAIL receptor expression. Leuk Res. 2011;35(10):1402–8.
52. Franco R, Panayiotidis MI, Cidlowski JA. Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J Biol Chem. 2007;282(42):30452–65.
53. Sun Y, St Clair DK, Xu Y, Crooks PA, St Clair WH. A NADPH oxidase-dependent redox signaling pathway mediates the selective radiosensitization effect of parthenolide in prostate cancer cells. Cancer Res. 2010;70(7):2880–90.