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Review Article

The relationship between cisplatin-induced reactive oxygen species, glutathione, and BCL-2 and resistance to cisplatin

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Pages 347-359 | Received 10 Sep 2009, Accepted 07 Jan 2010, Published online: 17 Feb 2010

References

  • Adams JM, Cory S. (2007). Bcl-2-regulated apoptosis: Mechanism and therapeutic potential. Curr Opin Immunol 19:488–496.
  • Aggarwal SK, Niroomand-Rad I. (1983). Effect of cisplatin on the plasma membrane phosphatase activities in ascites sarcoma-180 cells: A cytochemical study. J Histochem Cytochem 31:307–317.
  • Akaboshi M, Kawai K, Maki H, Akuta K, Ujeno Y, Miyahara T. (1992). The number of platinum atoms binding to DNA RNA and protein molecules of HeLa cells treated with cisplatin at its mean lethal concentration. Jpn J Cancer Res 83:522–526.
  • Armstrong JS, Jones DP. (2002). Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2 overexpressing HL60 cells. FASEB J 16:1263–1265.
  • Bakhshi A, Jensen J.P, Goldman P, Wright JJ, McBride OW, Epstein AL, Korsmeyer SJ. (1985). Cloning the chromosomal breakpoint of t(14;18) human lymphomas: Clustering around JH on chromosome 14 and near a transcriptional unit on 18. Cell 41:899–906.
  • Ballatori N, Krance SM, Marchan R, Hammond CL. (2009). Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology. Mol Aspects Med 30:13–28.
  • Beale PJ, Rogers P, Boxall F, Sharp SY, Kelland LR. (2000). BCL-2 family protein expression and platinum drug resistance in ovarian carcinoma. Br J Cancer 82:436–440.
  • Benlloch M, Ortega A, Ferrer P, Segarra R, Obrador E, Asensi M, Carretero J, Estrela JM. (2005). Acceleration of glutathione efflux and inhibition of gamma-glutamyltranspeptidase sensitize metastatic B16 melanoma cells to endothelium-induced cytotoxicity. J Biol Chem 280:6950–6959.
  • Berndtsson M, Hagg M, Panaretakis T, Havelka AM, Shoshan MC, Linder S. (2007). Acute apoptosis by cisplatin requires induction of reactive oxygen species but is not associated with damage to nuclear DNA. Int J Cancer 120:175–180.
  • Berners-Price SJ, Kuchel PW. (1990). Reaction of cis- and trans-[PtCl2(NH3)2] with reduced glutathione inside human red blood cells studied by 1H and 15N-[1H] DEPT NMR. J Inorg Biochem 38:327–345.
  • Boulikas T, Vougiouka M. (2003). Cisplatin and platinum drugs at the molecular level [review]. Oncol Rep 10:1663–1682.
  • Bragado P, Armesilla A, Silva A, Porras A. (2007). Apoptosis by cisplatin requires p53 mediated p38alpha MAPK activation through ROS generation. Apoptosis 12:1733–1742.
  • Brozovic A, Damrot J, Tsaryk R, Helbig L, Nikolova T, Hartig C, Osmak M, Roos WP, Kaina B, Fritz G. (2009). Cisplatin sensitivity is related to late DNA damage processing and checkpoint control rather than to the early DNA damage response. Mutat Res 670(1-2):32–41.
  • Brozovic A, Fritz G, Christmann M, Zisowsky J, Jaehde U, Osmak M, Kaina B. (2004). Long-term activation of SAPK/JNK p38 kinase and fas-L expression by cisplatin is attenuated in human carcinoma cells that acquired drug resistance. Int J Cancer 112:974–985.
  • Brozovic A, Majhen D, Roje V, Mikac N, Jakopec S, Fritz G, Osmak M, Ambriovic-Ristov A. (2008). alpha(v)beta(3) Integrin-mediated drug resistance in human laryngeal carcinoma cells is caused by glutathione-dependent elimination of drug-induced reactive oxidative species. Mol Pharmacol 74:298–306.
  • Brozovic A, Osmak M. (2007). Activation of mitogen-activated protein kinases by cisplatin and their role in cisplatin-resistance. Cancer Lett 251:1–16.
  • Buttke TM, Sandstrom PA. (1995). Redox regulation of programmed cell death in lymphocytes. Free Radic Res 22:389–397.
  • Byun SS, Kim SW, Choi H, Lee C, Lee E. (2005). Augmentation of cisplatin sensitivity in cisplatin-resistant human bladder cancer cells by modulating glutathione concentrations and glutathione-related enzyme activities. BJU Int 95:1086–1090.
  • Celli A, Que FG, Gores GJ, LaRusso NF. (1998). Glutathione depletion is associated with decreased Bcl-2 expression and increased apoptosis in cholangiocytes. Am J Physiol 275(4 Pt 1):G749–G757.
  • Chen ZX, Pervaiz S. (2007). Bcl-2 induces pro-oxidant state by engaging mitochondrial respiration in tumor cells. Cell Death Differ 14:1617–1627.
  • Cho HJ, Kim JK, Kim KD, Yoon HK, Cho MY, Park YP, Jeon JH, Lee ES, Byun SS, Lim HM, Song EY, Lim JS, Yoon DY, Lee HG, Choe YK. (2006). Upregulation of Bcl-2 is associated with cisplatin-resistance via inhibition of Bax translocation in human bladder cancer cells. Cancer Lett 237:56–66.
  • Cowley EA, Linsdell P. (2002). Oxidant stress stimulates anion secretion from the human airway epithelial cell line Calu-3: Implications for cystic fibrosis lung disease. J Physiol 543(Pt 1):201–209.
  • Custodio JB, Cardoso CM, Santos MS, Almeida LM, Vicente JA, Fernandes MA. (2009). Cisplatin impairs rat liver mitochondrial functions by inducing changes on membrane ion permeability: Prevention by thiol group protecting agents. Toxicology 259:18–24.
  • D’Alessio M, Cerella C, Amici C, Pesce C, Coppola S, Fanelli C, De Nicola M, Cristofanon S, Clavarino G, Bergamaschi A, Magrini A, Gualandi G, Ghibelli L. (2004). Glutathione depletion up-regulates Bcl-2 in BSO-resistant cells. FASEB J 18:1609–1611.
  • Danial NN. (2007). BCL-2 family proteins: Critical checkpoints of apoptotic cell death. Clin Cancer Res 13:7254–7263.
  • Daubeuf S, Balin D, Leroy P, Visvikis A. (2003). Different mechanisms for gamma-glutamyltransferase-dependent resistance to carboplatin and cisplatin. Biochem Pharmacol 66:595–604.
  • Daubeuf S, Leroy P, Paolicchi A, Pompella A, Wellman M, Galteau M.M, Visvikis A. (2002). Enhanced resistance of HeLa cells to cisplatin by overexpression of gamma-glutamyltransferase. Biochem Pharmacol 64:207–216.
  • Dickinson DA, Forman HJ. (2002). Cellular glutathione and thiols metabolism. Biochem Pharmacol 64:1019–1026.
  • Dimanche-Boitrel MT, Meurette O, Rebillard A, Lacour S. (2005). Role of early plasma membrane events in chemotherapy-induced cell death. Drug Resist Updat. 8(1-2), 5–14.
  • Estrela JM, Ortega A, Obrador E. (2006). Glutathione in cancer biology and therapy. Crit Rev Clin Lab Sci 43:143–181.
  • Filomeni G, Rotilio G, Ciriolo MR. (2002). Cell signalling and the glutathione redox system. Biochem Pharmacol 64:1057–1064.
  • Franco R, Cidlowski JA. (2009). Apoptosis and glutathione: Beyond an antioxidant. Cell Death Differ 16:1303–1314.
  • Franzini M, Corti A, Lorenzini E, Paolicchi A, Pompella A, De Cesare M, Perego P, Gatti L, Leone R, Apostoli P, Zunino F. (2006). Modulation of cell growth and cisplatin sensitivity by membrane gamma-glutamyltransferase in melanoma cells. Eur J Cancer 42:2623–2630.
  • Fuertes MA, Castilla J, Alonso C, Perez J.M. (2002). Novel concepts in the development of platinum antitumor drugs. Curr Med Chem Anticancer Agents 2:539–551.
  • Galanski M. (2006). Recent developments in the field of anticancer platinum complexes. Recent Pat Anticancer Drug Discov. 1:285–295.
  • Germain M, Shore GC. (2003). Cellular distribution of Bcl-2 family proteins. Sci STKE 2003(173):10.
  • Ghazal-Aswad S, Hogarth L, Hall AG, George M, Sinha DP, Lind M, Calvert AH, Sunter JP, Newell DR. (1996). The relationship between tumour glutathione concentration glutathione S-transferase isoenzyme expression and response to single agent carboplatin in epithelial ovarian cancer patients. Br J Cancer 74:468–473.
  • Giardino I, Edelstein D, Brownlee M. (1996). BCL-2 expression or antioxidants prevent hyperglycemia-induced formation of intracellular advanced glycation endproducts in bovine endothelial cells. J Clin Invest 97:1422–1428.
  • Giles GI. (2006). The redox regulation of thiol dependent signaling pathways in cancer. Curr Pharm Des 12:4427–4443.
  • Godwin AK, Meister A, O’Dwyer PJ, Huang CS, Hamilton TC, Anderson ME. (1992). High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci U S A 89:3070–3074.
  • Goto S, Kamada K, Soh Y, Ihara Y, Kondo T. (2002). Significance of nuclear glutathione S-transferase pi in resistance to anti-cancer drugs. Jpn J Cancer Res 93:1047–1056.
  • Grunicke H, Hofmann J. (1992). Cytotoxic and cytostatic effects of antitumor agents induced at the plasma membrane level. Pharmacol Ther 55:1–30.
  • Hanigan MH, Gallagher BC, Townsend DM, Gabarra V. (1999). Gamma-glutamyl transpeptidase accelerates tumor growth and increases the resistance of tumors to cisplatin in vivo. Carcinogenesis 20:553–559.
  • Hao XY, Bergh J, Brodin O, Hellman U, Mannervik B. (1994). Acquired resistance to cisplatin and doxorubicin in a small cell lung cancer cell line is correlated to elevated expression of glutathione-linked detoxification enzymes. Carcinogenesis 15:1167–1173.
  • Havelka AM, Berndtsson M, Olofsson MH, Shoshan MC, Linder S. (2007). Mechanisms of action of DNA-damaging anticancer drugs in treatment of carcinomas: Is acute apoptosis an “off-target” effect? Mini Rev Med Chem 7:1035–1039.
  • Herod JJ, Eliopoulos AG, Warwick J, Niedobitek G, Young LS, Kerr DJ. (1996). The prognostic significance of Bcl-2 and p53 expression in ovarian carcinoma. Cancer Res 56:2178–2184.
  • Hill JM, Loeb E, MacLellan A, Hill NO, Khan A, King JJ. (1975). Clinical studies of Platinum Coordination compounds in the treatment of various malignant diseases. Cancer Chemother Rep 59:647–659.
  • Hill JM, Speer RJ. (1982). Organo-platinum complexes as antitumor agents [review]. Anticancer Res 2:173–186.
  • Hill NO. (1979). Cis-platinum for cancer. N Engl J Med 301:47.
  • Hochman A, Liang H, Offen D, Melamed E, Sternin H. (2000). Developmental changes in antioxidant enzymes and oxidative damage in kidneys liver and brain of bcl-2 knockout mice. Cell Mol Biol (Noisy-le-grand) 46:41–52.
  • Hockenbery DM, Oltvai ZN, Yin XM, Milliman CL, Korsmeyer SJ. (1993). Bcl-2 functions in an antioxidant pathway to prevent apoptosis. Cell 75:241–251.
  • Hoffmann S, Spitkovsky D, Radicella J.P, Epe B, Wiesner R.J. (2004). Reactive oxygen species derived from the mitochondrial respiratory chain are not responsible for the basal levels of oxidative base modifications observed in nuclear DNA of Mammalian cells. Free Radic Biol Med 36:765–773.
  • Hopkins FG, Morgan EJ. (1936). Some relations between ascorbic acid and glutathione. Biochem J 30:1446–1462.
  • Hopkins FG, Morgan EJ. (1938). The influence of thiol-groups in the activity of dehydrogenases. Biochem J 32:611–620.
  • Huang HL, Fang LW, Lu SP, Chou CK, Luh TY, Lai MZ. (2003a). DNA-damaging reagents induce apoptosis through reactive oxygen species-dependent Fas aggregation. Oncogene 22:8168–8177.
  • Huang Z, Tong Y, Wang J, Huang Y. (2003b). NMR studies of the relationship between the changes of membrane lipids and the cisplatin-resistance of A549/DDP cells. Cancer Cell Int 3:5.
  • Inoue M, Sato EF, Nishikawa M, Park AM, Kira Y, Imada I, Utsumi K. (2003). Mitochondrial generation of reactive oxygen species and its role in aerobic life. Curr Med Chem 10:2495–2505.
  • Ise T, Shimizu T, Lee EL, Inoue H, Kohno K, Okada Y. (2005). Roles of volume-sensitive Cl− channel in cisplatin-induced apoptosis in human epidermoid cancer cells. J Membr Biol 205:139–145.
  • Ishikawa T. (1992). The ATP-dependent glutathione S-conjugate export pump. Trends Biochem Sci 17:463–468.
  • Ishikawa T, Wright CD, Ishizuka H. (1994). GS-X pump is functionally overexpressed in cis-diamminedichloroplatinum (II)-resistant human leukemia HL-60 cells and down-regulated by cell differentiation. J Biol Chem 269:29085–29093.
  • Jacobson MD. (1996). Reactive oxygen species and programmed cell death. Trends Biochem Sci 21:83–86.
  • Jing XB, Cai XB, Hu H, Chen SZ, Chen BM, Cai JY. (2007). Reactive oxygen species and mitochondrial membrane potential are modulated during CDDP-induced apoptosis in EC-109 cells. Biochem Cell Biol 85:265–271.
  • Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, Bredesen DE. (1993). Bcl-2 inhibition of neural death: Decreased generation of reactive oxygen species. Science 262:1274–1277.
  • Kim R, Emi M, Tanabe K, Toge T. (2004). Preclinical evaluation of antisense bcl-2 as a chemosensitizer for patients with gastric carcinoma. Cancer 101:2177–2186.
  • Kolfschoten GM, Pinedo HM, Scheffer PG, Schluper HM, Erkelens CA, Boven E. (2000). Development of a panel of 15 human ovarian cancer xenografts for drug screening and determination of the role of the glutathione detoxification system. Gynecol Oncol 76:362–368.
  • Komatsu M, Sumizawa T, Mutoh M, Chen ZS, Terada K, Furukawa T, Yang XL, Gao H, Miura N, Sugiyama T, Akiyama S. (2000). Copper-transporting P-type adenosine triphosphatase (ATP7B) is associated with cisplatin resistance. Cancer Res 60:1312–1316.
  • Konishi I, Nanbu K, Mandai M, Tsuruta Y, Kataoka N, Nagata Y, Mori T. (1998). Tumor response to neoadjuvant chemotherapy correlates with the expression of P-glycoprotein and PCNA but not GST-pi in the tumor cells of cervical carcinoma. Gynecol Oncol 70:365–371.
  • Kroemer G, Galluzzi L, Brenner C. (2007). Mitochondrial membrane permeabilization in cell death. Physiol Rev 87:99–163.
  • Kruidering M, Van de Water B, de Heer E, Mulder GJ, Nagelkerke JF. (1997). Cisplatin-induced nephrotoxicity in porcine proximal tubular cells: Mitochondrial dysfunction by inhibition of complexes I to IV of the respiratory chain. J Pharmacol Exp Ther 280:638–649.
  • Lacour S, Hammann A, Grazide S, Lagadic-Gossmann D, Athias A, Sergent O, Laurent G, Gambert P, Solary E, Dimanche-Boitrel MT. (2004). Cisplatin-induced CD95 redistribution into membrane lipid rafts of HT29 human colon cancer cells. Cancer Res 64:3593–3598.
  • Landriscina M, Maddalena F, Laudiero G, Esposito F. (2009). Adaptation to oxidative stress chemoresistance and cell survival. Antioxid Redox Signal 11:2701–2716.
  • Lee EL, Hasegawa Y, Shimizu T, Okada Y. (2008). IK1 channel activity contributes to cisplatin sensitivity of human epidermoid cancer cells. Am J Physiol Cell Physiol 294:C1398-C1406.
  • Lee M, Hyun DH, Marshall KA, Ellerby LM, Bredesen DE, Jenner P, Halliwell B. (2001). Effect of overexpression of BCL-2 on cellular oxidative damage, nitric oxide production, antioxidant defenses, and the proteasome. Free Radic Biol Med 31:1550–1559.
  • Levine B, Sinha S, Kroemer G. (2008). Bcl-2 family members: Dual regulators of apoptosis and autophagy. Autophagy 4:600–606.
  • Li F, Meng L, Zhou J, Xing H, Wang S, Xu G, Zhu H, Wang B, Chen G, Lu YP, Ma D. (2005). Reversing chemoresistance in cisplatin-resistant human ovarian cancer cells: A role of c-Jun NH2-terminal kinase 1. Biochem Biophys Res Commun 335:1070–1077.
  • Lin CS, Wang LS, Tsai CM, Wei YH. (2008). Low copy number and low oxidative damage of mitochondrial DNA are associated with tumor progression in lung cancer tissues after neoadjuvant chemotherapy. Interact Cardiovasc Thorac Surg 7:954–958.
  • Losert D, Pratscher B, Soutschek J, Geick A, Vornlocher H.P, Muller M, Wacheck V. (2007). Bcl-2 downregulation sensitizes nonsmall cell lung cancer cells to cisplatin but not to docetaxel. Anticancer Drugs 18:755–761.
  • Lu AL, Li X, Gu Y, Wright PM, Chang D.Y. (2001). Repair of oxidative DNA damage: Mechanisms and functions. Cell Biochem Biophys 35:141–170.
  • Lu SC, Ge JL. (1992). Loss of suppression of GSH synthesis at low cell density in primary cultures of rat hepatocytes. Am J Physiol 263(6 Pt 1):C1181–C1189.
  • Mandic A, Hansson J, Linder S, Shoshan MC. (2003). Cisplatin induces endoplasmic reticulum stress and nucleus-independent apoptotic signaling. J Biol Chem 278:9100–9106.
  • Markovic J, Borras C, Ortega A, Sastre J, Vina J, Pallardo FV. (2007). Glutathione is recruited into the nucleus in early phases of cell proliferation. J Biol Chem 282:20416–20424.
  • Martins NM, Santos NA, Curti C, Bianchi ML, Santos AC. (2008). Cisplatin induces mitochondrial oxidative stress with resultant energetic metabolism impairment membrane rigidification and apoptosis in rat liver. J Appl Toxicol 28:337–344.
  • Masuda H, Tanaka T, Takahama U. (1994). Cisplatin generates superoxide anion by interaction with DNA in a cell-free system. Biochem Biophys Res Commun 203:1175–1180.
  • Meijer C, Mulder NH, Hospers GA, Uges DR, de Vries EG. (1990). The role of glutathione in resistance to cisplatin in a human small cell lung cancer cell line. Br J Cancer 62:72–77.
  • Meister A. (1995). Glutathione metabolism. Methods Enzymol 251:3–7.
  • Meredith MJ, Cusick CL, Soltaninassab S, Sekhar KS, Lu S, Freeman ML. (1998). Expression of Bcl-2 increases intracellular glutathione by inhibiting methionine-dependent GSH efflux. Biochem Biophys Res Commun 248:458–463.
  • Meyer TE, Liang HQ, Buckley AR, Buckley DJ, Gout PW, Green EH, Bode AM. (1998). Changes in glutathione redox cycling and oxidative stress response in the malignant progression of NB2 lymphoma cells. Int J Cancer 77:55–63.
  • Michaud WA, Nichols AC, Mroz EA, Faquin WC, Clark JR, Begum S, Westra WH, Wada H, Busse PM, Ellisen LW, Rocco JW. (2009). Bcl-2 blocks cisplatin-induced apoptosis and predicts poor outcome following chemoradiation treatment in advanced oropharyngeal squamous cell carcinoma. Clin Cancer Res 15:1645–1654.
  • Mirkovic N, Voehringer DW, Story MD, McConkey DJ, McDonnell TJ, Meyn RE. (1997). Resistance to radiation-induced apoptosis in Bcl-2-expressing cells is reversed by depleting cellular thiols. Oncogene 15:1461–1470.
  • Miyajima A, Nakashima J, Yoshioka K, Tachibana M, Tazaki H, Murai M. (1997). Role of reactive oxygen species in cis-dichlorodiammineplatinum-induced cytotoxicity on bladder cancer cells. Br J Cancer 76:206–210.
  • Miyatake K, Gemba K, Ueoka H, Nishii K, Kiura K, Tabata M, Shibayama T, Takigawa N, Kawaraya M, Tanimoto M. (2003). Prognostic significance of mutant p53 protein P-glycoprotein and glutathione S-transferase-pi in patients with unresectable non-small cell lung cancer. Anticancer Res 23(3C):2829–2836.
  • Nichols TC, Guthridge JM, Karp DR, Molina H, Fletcher DR, Holers VM. (1998). Gamma-glutamyl transpeptidase, an ecto-enzyme regulator of intracellular redox potential is a component of TM4 signal transduction complexes. Eur J Immunol 28:4123–4129.
  • Nishimura T, Newkirk K, Sessions RB, Andrews PA, Trock BJ, Rasmussen AA, Montgomery EA, Bischoff EK, Cullen KJ. (1996). Immunohistochemical staining for glutathione S-transferase predicts response to platinum-based chemotherapy in head and neck cancer. Clin Cancer Res 2:1859–1865.
  • Nunez G, London L, Hockenbery D, Alexander M, McKearn J.P, Korsmeyer SJ. (1990). Deregulated Bcl-2 gene expression selectively prolongs survival of growth factor-deprived hemopoietic cell lines. J Immunol 144:3602–3610.
  • Osbild S, Brault L, Battaglia E, Bagrel D. (2006). Resistance to cisplatin and adriamycin is associated with the inhibition of glutathione efflux in MCF-7-derived cells. Anticancer Res 26(5A):3595–3600.
  • Paschen W. (2001). Dependence of vital cell function on endoplasmic reticulum calcium levels: Implications for the mechanisms underlying neuronal cell injury in different pathological states. Cell Calcium 29:1–11.
  • Paschen W. (2003). Endoplasmic reticulum: A primary target in various acute disorders and degenerative diseases of the brain. Cell Calcium 34:365–383.
  • Poulsen HE, Jensen BR, Weimann A, Jensen SA, Sorensen M, Loft S. (2000). Antioxidants DNA damage and gene expression. Free Radic Res 33(Suppl):S33–S39.
  • Previati M, Lanzoni I, Corbacella E, Magosso S, Guaran V, Martini A, Capitani S. (2006). Cisplatin-induced apoptosis in human promyelocytic leukemia cells. Int J Mol Med 18:511–516.
  • Rabik CA, Dolan ME. (2007). Molecular mechanisms of resistance and toxicity associated with platinating agents. Cancer Treat Rev 33:9–23.
  • Rahman I, MacNee W. (2000). Regulation of redox glutathione levels and gene transcription in lung inflammation: Therapeutic approaches. Free Radic Biol Med 28:1405–1420.
  • Rebillard A, Lagadic-Gossmann D, Dimanche-Boitrel MT. (2008). Cisplatin cytotoxicity: DNA and plasma membrane targets. Curr Med Chem 15:2656–2663.
  • Rudin CM, Hann CL, Peacock CD, Watkins DN. (2008). Novel systemic therapies for small cell lung cancer. J Natl Compr Canc Netw 6:315–322.
  • Rudin CM, Yang Z, Schumaker LM, VanderWeele DJ, Newkirk K, Egorin MJ, Zuhowski EG, Cullen KJ. (2003). Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res 63:312–318.
  • Sadowitz PD, Hubbard BA, Dabrowiak JC, Goodisman J, Tacka KA, Aktas MK, Cunningham MJ, Dubowy RL, Souid AK. (2002). Kinetics of cisplatin binding to cellular DNA and modulations by thiol-blocking agents and thiol drugs. Drug Metab Dispos 30:183–190.
  • Safaei R, Howell SB. (2005). Copper transporters regulate the cellular pharmacology and sensitivity to Pt drugs. Crit Rev Oncol Hematol 53:13–23.
  • Saitoh Y, Ouchida R, Kayasuga A, Miwa N. (2003). Anti-apoptotic defense of bcl-2 gene against hydroperoxide-induced cytotoxicity together with suppressed lipid peroxidation enhanced ascorbate uptake and upregulated Bcl-2 protein. J Cell Biochem 89:321–334.
  • Salles B, Calsou P. (1992). Involvement of glutathione in cis-platinum toxicity in Escherichia coli K12. Toxicology 72:341–350.
  • Satoh M, Kashihara N, Fujimoto S, Horike H, Tokura T, Namikoshi T, Sasaki T, Makino H. (2003). A novel free radical scavenger, edarabone, protects against cisplatin-induced acute renal damage in vitro and in vivo. J Pharmacol Exp Ther 305(3):1183–1190.
  • Satoh T, Nishida M, Tsunoda H, Kubo T. (2001). Expression of glutathione S-transferase pi (GST-pi) in human malignant ovarian tumors. Eur J Obstet Gynecol Reprod Biol 96:202–208.
  • Schafer FQ, Buettner GR. (2001). Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple. Free Radic Biol Med 30:1191–1212.
  • Scheel-Toellner D, Wang K, Craddock R, Webb PR, McGettrick HM, Assi LK, Parkes N, Clough LE, Gulbins E, Salmon M, Lord JM. (2004). Reactive oxygen species limit neutrophil life span by activating death receptor signaling. Blood 104:2557–2564.
  • Schweyer S, Soruri A, Heintze A, Radzun H.J, Fayyazi A. (2004). The role of reactive oxygen species in cisplatin-induced apoptosis in human malignant testicular germ cell lines. Int J Oncol 25:1671–1676.
  • Scorrano L, Oakes SA, Opferman JT, Cheng EH, Sorcinelli MD, Pozzan T, Korsmeyer SJ. (2003). BAX and BAK regulation of endoplasmic reticulum Ca2+: A control point for apoptosis. Science 300:135–139.
  • Sedletska Y, Giraud-Panis MJ, Malinge JM. (2005). Cisplatin is a DNA-damaging antitumour compound triggering multifactorial biochemical responses in cancer cells: Importance of apoptotic pathways. Curr Med Chem Anticancer Agents 5:251–265.
  • Sharma H, Sen S, Lo Muzio L, Mariggio A, Singh N. (2005). Antisense-mediated downregulation of anti-apoptotic proteins induces apoptosis and sensitizes head and neck squamous cell carcinoma cells to chemotherapy. Cancer Biol Ther 4:720–727.
  • Sharma R, Singhal SS, Srivastava SK, Bajpai KK, Frenkel EP, Awasthi S. (1993). Glutathione and glutathione linked enzymes in human small cell lung cancer cell lines. Cancer Lett 75:111–119.
  • Shimizu T, Lee EL, Ise T, Okada Y. (2008). Volume-sensitive Cl(−) channel as a regulator of acquired cisplatin resistance. Anticancer Res 28(1A):75–83.
  • Shimizu T, Numata T, Okada Y. (2004). A role of reactive oxygen species in apoptotic activation of volume-sensitive Cl(−) channel. Proc Natl Acad Sci U SA 101:6770–6773.
  • Siddik ZH. (2003). Cisplatin: Mode of cytotoxic action and molecular basis of resistance. Oncogene 22:7265–7279.
  • Slater AF, Nobel CS, Orrenius S. (1995). The role of intracellular oxidants in apoptosis. Biochim Biophys Acta 1271:59–62.
  • Soderdahl T, Enoksson M, Lundberg M, Holmgren A, Ottersen O.P, Orrenius S, Bolcsfoldi G, Cotgreave I.A. (2003). Visualization of the compartmentalization of glutathione and protein-glutathione mixed disulfides in cultured cells. FASEB J 17:124–126.
  • Stewart DJ. (2007). Mechanisms of resistance to cisplatin and carboplatin. Crit Rev Oncol Hematol 63:12–31.
  • Stewart JHT, Tran TL, Levi N, Tsai WS, Schrump DS, Nguyen DM. (2007). The essential role of the mitochondria and reactive oxygen species in cisplatin-mediated enhancement of fas ligand-induced apoptosis in malignant pleural mesothelioma. J Surg Res 141:120–131.
  • Surowiak P, Materna V, Kaplenko I, Spaczynski M, Dietel M, Lage H, Zabel M. (2005). Augmented expression of metallothionein and glutathione S-transferase pi as unfavourable prognostic factors in cisplatin-treated ovarian cancer patients. Virchows Arch 447:626–633.
  • Susnow N, Zeng L, Margineantu D, Hockenbery DM. (2009). Bcl-2 family proteins as regulators of oxidative stress. Semin Cancer Biol 19:42–49.
  • Suzuki T, Nishio K, Tanabe S. (2001). The MRP family and anticancer drug metabolism. Curr Drug Metab 2:367–377.
  • Thomenius MJ, Distelhorst CW. (2003). Bcl-2 on the endoplasmic reticulum: Protecting the mitochondria from a distance. J Cell Sci 116(Pt 22):4493–4499.
  • Torigoe T, Izumi H, Ishiguchi H, Yoshida Y, Tanabe M, Yoshida T, Igarashi T, Niina I, Wakasugi T, Imaizumi T, Momii Y, Kuwano M, Kohno K. (2005). Cisplatin resistance and transcription factors. Curr Med Chem Anticancer Agents 5:15–27.
  • Townsend DM, Tew KD. (2003). The role of glutathione-S-transferase in anti-cancer drug resistance. Oncogene 22:7369–7375.
  • Townsend D.M, Tew K.D, Tapiero H. (2003). The importance of glutathione in human disease. Biomed Pharmacother 57:145–155.
  • van der Zee AG, Hollema H, Suurmeijer AJ, Krans M, Sluiter WJ, Willemse PH, Aalders JG, de Vries EG. (1995). Value of P-glycoprotein, glutathione S-transferase pi, c-erbB-2, and p53 as prognostic factors in ovarian carcinomas. J Clin Oncol 13:70–78.
  • Van Houten B, Woshner V, Santos JH. (2006). Role of mitochondrial DNA in toxic responses to oxidative stress. DNA Repair (Amst) 5:145–152.
  • Vessey DA, Lee KH, Blacker KL. (1992). Characterization of the oxidative stress initiated in cultured human keratinocytes by treatment with peroxides. J Invest Dermatol 99:859–863.
  • Voehringer DW. (1999). BCL-2 and glutathione: Alterations in cellular redox state that regulate apoptosis sensitivity. Free Radic Biol Med 27:945–950.
  • Voehringer DW, Hirschberg DL, Xiao J, Lu Q, Roederer M, Lock CB, Herzenberg LA, Steinman L, Herzenberg LA. (2000). Gene microarray identification of redox and mitochondrial elements that control resistance or sensitivity to apoptosis. Proc Natl Acad Sci U S A 97:2680–2685.
  • Voehringer DW, Meyn RE. (1998). Reversing drug resistance in bcl-2-expressing tumor cells by depleting glutathione. Drug Resist Updat 1:345–351.
  • Voehringer DW, Meyn RE. (2000). Redox aspects of Bcl-2 function. Antioxid Redox Signal 2:537–550.
  • Warmann SW, Frank H, Heitmann H, Ruck P, Herberts T, Seitz G, Fuchs J. (2008). Bcl-2 gene silencing in pediatric epithelial liver tumors. J Surg Res 144:43–48.
  • Yang Z, Schumaker LM, Egorin MJ, Zuhowski EG, Guo Z, Cullen KJ. (2006). Cisplatin preferentially binds mitochondrial DNA and voltage-dependent anion channel protein in the mitochondrial membrane of head and neck squamous cell carcinoma: Possible role in apoptosis. Clin Cancer Res 12:5817–5825.
  • Yi X, Yin XM, Dong Z. (2003). Inhibition of Bid-induced apoptosis by Bcl-2. tBid insertion Bax translocation and Bax/Bak oligomerization suppressed. J Biol Chem 278:16992–16999.
  • Yip KW, Reed JC. (2008). Bcl-2 family proteins and cancer. Oncogene 27:6398–6406.
  • Zamble DB, Lippard SJ. (1995). Cisplatin and DNA repair in cancer chemotherapy. Trends Biochem Sci 20:435–439.

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