Glutathione efflux and cell death

Antioxidants and Redox Signaling

Volumn 17, Issue 12, 2012, Pages 1694-1713

  Franco, Rodrigo ^a   Cidlowski, John A ^b  

^a UNIVERSITY OF NEBRASKA LINCOLN   (United States)

^b NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLUTATHIONE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE;

ANTIOXIDANT ACTIVITY; CELL DEATH; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; OXIDATIVE STRESS; PRIORITY JOURNAL; REVIEW;

ANIMALS; BIOLOGICAL TRANSPORT; CELL DEATH; GLUTATHIONE; HUMANS; MODELS, BIOLOGICAL; SIGNAL TRANSDUCTION;

EID: 84867709011     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2012.4553     Document Type: Review

References (257)

1. Anathy V, Aesif SW, Guala AS, Havermans M, Reynaert NL, Ho YS, Budd RC, and Janssen-Heininger YM. Redox amplification of apoptosis by caspase-dependent cleavage of glutaredoxin 1 and S-glutathionylation of Fas. J Cell Biol 184: 241-252, 2009..
2. Anathy V, Roberson EC, Guala AS, Godburn KE, Budd RC, and Janssen-Heininger YM. Redox-based regulation of ap-optosis: S-glutathionylation as a regulatory mechanism to control cell death. Antioxid Redox Signal 16: 496-505, 2012..
3. Aon MA, Cortassa S, Maack C, and O'Rourke B. Sequential opening of mitochondrial ion channels as a function of glu-tathione redox thiol status. J Biol Chem 282: 21889-21900, 2007.. (Pubitemid 47195754)
4. Aoshiba K, Yasui S, Nishimura K, and Nagai A. Thiol depletion induces apoptosis in cultured lung fibroblasts. Am J Respir Cell Mol Biol 21: 54-64, 1999.. (Pubitemid 129508628)
5. Aoyama K, Matsumura N, Watabe M, and Nakaki T. Oxidative stress on EAAC1 is involved in MPTP-induced glutathione depletion and motor dysfunction. Eur J Neu-rosci 27: 20-30, 2008..
6. Appenzeller-Herzog C. Glutathione-and non-glutathione-based oxidant control in the endoplasmic reticulum. J Cell Sci 124: 847-855, 2011..
7. Aquilano K, Baldelli S, Cardaci S, Rotilio G, and Ciriolo MR. Nitric oxide is the primary mediator of cytotoxicity induced by GSH depletion in neuronal cells. J Cell Sci 124: 1043-1054, 2011..
8. Armstrong JS and Jones DP. Glutathione depletion enforces the mitochondrial permeability transition and causes cell death in Bcl-2 overexpressing HL60 cells. FASEB J 16: 1263-1265, 2002..
9. Armstrong JS, Steinauer KK, Hornung B, Irish JM, Lecane P, Birrell GW, Peehl DM, and Knox SJ. Role of glutathione depletion and reactive oxygen species generation in apop-totic signaling in a human B lymphoma cell line. Cell Death Differ 9: 252-263, 2002.. (Pubitemid 34223869)
10. Awasthi S, Singhal SS, Sharma R, Zimniak P, and Awasthi YC. Transport of glutathione conjugates and chemothera-peutic drugs by RLIP76 (RALBP1): a novel link between G-protein and tyrosine kinase signaling and drug resistance. Int J Cancer 106: 635-646, 2003.. (Pubitemid 36993386)
11. Bajt ML, Ho YS, Vonderfecht SL, and Jaeschke H. Reactive oxygen as modulator of TNF and fas receptor-mediated apoptosis in vivo: studies with glutathione peroxidase-deficient mice. Antioxid Redox Signal 4: 733-740, 2002.. (Pubitemid 35246935)
12. Ballatori N, Hammond CL, Cunningham JB, Krance SM, and Marchan R. Molecular mechanisms of reduced gluta-thione transport: role of the MRP/CFTR/ABCC and OATP/SLC21A families of membrane proteins. Toxicol Appl Pharmacol 204: 238-255, 2005.. (Pubitemid 40545229)
13. Ballatori N, Krance SM, Marchan R, and Hammond CL. Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology. Mol Aspects Med 30: 13-28, 2009..
14. Ballatori N, Krance SM, Notenboom S, Shi S, Tieu K, and Hammond CL. Glutathione dysregulation and the etiology and progression of human diseases. Biol Chem 390: 191-214, 2009..
15. Baltes S, Fedrowitz M, Tortos CL, Potschka H, and Loscher W. Valproic acid is not a substrate for P-glycoprotein or multidrug resistance proteins 1 and 2 in a number of in vitro and in vivo transport assays. J Pharmacol Exp Ther 320: 331-343, 2007.. (Pubitemid 46025748)
16. Barrett WC, DeGnore JP, Konig S, Fales HM, Keng YF, Zhang ZY, Yim MB, and Chock PB. Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38: 6699-6705, 1999..
17. Basu S, Keszler A, Azarova NA, Nwanze N, Perlegas A, Shiva S, Broniowska KA, Hogg N, and Kim-Shapiro DB. A novel role for cytochrome c: efficient catalysis of S-nitrosothiol formation. Free Radic Biol Med 48: 255-263, 2010..
18. Baudouin-Cornu P, Lagniel G, Kumar C, Huang ME, and Labarre J. Glutathione degradation is a key determinant of glutathione homeostasis. J Biol Chem 287: 4552-4561, 2012..
19. Beer SM, Taylor ER, Brown SE, Dahm CC, Costa NJ, Runswick MJ, and Murphy MP. Glutaredoxin 2 catalyzes the reversible oxidation and glutathionylation of mito-chondrial membrane thiol proteins: implications for mito-chondrial redox regulation and antioxidant DEFENSE. J Biol Chem 279: 47939-47951, 2004.. (Pubitemid 39540945)
20. Benhar M, Forrester MT, and Stamler JS. Protein deni-trosylation: enzymatic mechanisms and cellular functions. Nat Rev Mol Cell Biol 10: 721-732, 2009..
21. Benlloch M, Ortega A, Ferrer P, Segarra R, Obrador E, Asensi M, Carretero J, and Estrela JM. Acceleration of glutathione efflux and inhibition of gamma-glutamyltranspeptidase sensitize metastatic B16 melanoma cells to endothelium-induced cytotoxicity. J Biol Chem 280: 6950-6959, 2005.. (Pubitemid 40341251)
22. Biswas SK and Rahman I. Environmental toxicity, redox signaling and lung inflammation: the role of glutathione. Mol Aspects Med 30: 60-76, 2009..
23. Blair IA. Endogenous glutathione adducts. Curr Drug Me-tab 7: 853-872, 2006.. (Pubitemid 44873711)
24. Blair IA. Analysis of endogenous glutathione-adducts and their metabolites. Biomed Chromatogr 24: 29-38, 2010..
25. Blokzijl H, van Steenpaal A, Vander Borght S, Bok LI, Libbrecht L, Tamminga M, Geuken M, Roskams TA, Dijkstra G, Moshage H, Jansen PL, and Faber KN. Upre-gulation and cytoprotective role of epithelial multidrug resistance-associated protein 1 in inflammatory bowel disease. J Biol Chem 283: 35630-35637, 2008..
26. Bojes HK, Datta K, Xu J, Chin A, Simonian P, Nunez G, and Kehrer JP. Bcl-xL overexpression attenuates glutathione depletion in FL5.12 cells following interleukin-3 withdrawal. Biochem J 325 (Pt 2): 315-319, 1997..
27. Bortner CD and Cidlowski JA. The role of apoptotic volume decrease and ionic homeostasis in the activation and repression of apoptosis. Pflugers Arch 448: 313-318, 2004.. (Pubitemid 40895600)
28. Brechbuhl HM, Gould N, Kachadourian R, Riekhof WR, Voelker DR, and Day BJ. Glutathione transport is a unique function of the ATP-binding cassette protein ABCG2. J Biol Chem 285: 16582-16587, 2010..
29. Briz O, Romero MR, Martinez-Becerra P, Macias RI, Perez MJ, Jimenez F, San Martin FG, and Marin JJ. OATP8/1B3-mediated cotransport of bile acids and glutathione: an export pathway for organic anions from hepatocytes? J Biol Chem 281: 30326-30335, 2006.. (Pubitemid 44582086)
30. Broniowska KA, Keszler A, Basu S, Kim-Shapiro DB, and Hogg N. Cytochrome c-mediated formation of S-nitrosothiol in cells. Biochem J 442: 191-197, 2012..
31. Brown GC and Borutaite V. Regulation of apoptosis by the redox state of cytochrome c. Biochim Biophys Acta 1777: 877-881, 2008..
32. Bush JA, Ho VC, Mitchell DL, Tron VA, and Li G. Effect of N-acetylcysteine on UVB-induced apoptosis and DNA repair in human and mouse keratinocytes. Photochem Photo-biol 70: 329-333, 1999.. (Pubitemid 129555881)
33. Cazanave S, Berson A, Haouzi D, Vadrot N, Fau D, Grodet A, Letteron P, Feldmann G, El-Benna J, Fromenty B, Robin MA, and Pessayre D. High hepatic glutathione stores alleviate Fas-induced apoptosis in mice. J Hepatol 46: 858-868, 2007.. (Pubitemid 46546601)
34. Chanvorachote P, Nimmannit U, Wang L, Stehlik C, Lu B, Azad N, and Rojanasakul Y. Nitric oxide negatively regulates Fas CD95-induced apoptosis through inhibition of ubiquitin-proteasome-mediated degradation of FLICE inhibitory protein. J Biol Chem 280: 42044-42050, 2005.. (Pubitemid 43023173)
35. Chen CJ, Huang HS, and Chang WC. Depletion of phos-pholipid hydroperoxide glutathione peroxidase up-regulates arachidonate metabolism by 12S-lipoxygenase and cyclooxygenase 1 in human epidermoid carcinoma A431 cells. FASEB J 17: 1694-1696, 2003..
36. Chiang HS and Maric M. Lysosomal thiol reductase negatively regulates autophagy by altering glutathione synthesis and oxidation. Free Radic Biol Med 51: 688-699, 2011..
37. Chipuk JE and Green DR. How do BCL-2 proteins induce mitochondrial outer membrane permeabilization? Trends Cell Biol 18: 157-164, 2008..
38. Chrestensen CA, Starke DW, and Mieyal JJ. Acute cadmium exposure inactivates thioltransferase (Glutaredoxin), inhibits intracellular reduction of protein-glutathionyl-mixed disulfides, and initiates apoptosis. J Biol Chem 275: 26556-26565, 2000..
39. Circu ML and Aw TY. Glutathione and apoptosis. Free Radic Res 42: 689-706, 2008..
40. Circu ML and Aw TY. Reactive oxygen species, cellular redox systems, and apoptosis. Free Radic Biol Med 48: 749-762, 2010..
41. Circu ML, Stringer S, Rhoads CA, Moyer MP, and Aw TY. The role of GSH efflux in staurosporine-induced apoptosis in colonic epithelial cells. Biochem Pharmacol 77: 76-85, 2009..
42. Coffey RN, Watson RW, Hegarty NJ, O'Neill A, Gibbons N, Brady HR, and Fitzpatrick JM. Thiol-mediated apoptosis in prostate carcinoma cells. Cancer 88: 2092-2104, 2000.. (Pubitemid 30233211)
43. Cole SP and Deeley RG. Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol Sci 27: 438-446, 2006.. (Pubitemid 44051570)
44. Crack PJ, Taylor JM, Flentjar NJ, de Haan J, Hertzog P, Iannello RC, and Kola I. Increased infarct size and exacerbated apoptosis in the glutathione peroxidase-1 (Gpx-1) knockout mouse brain in response to ischemia/reperfusion injury. J Neurochem 78: 1389-1399, 2001.. (Pubitemid 32899770)
45. Cullen KV, Davey RA, and Davey MW. Verapamil-stimulated glutathione transport by the multidrug resistance-associated protein (MRP1) in leukaemia cells. Biochem Pharmacol 62: 417-424, 2001.. (Pubitemid 32607723)
46. Custodio JB, Cardoso CM, and Almeida LM. Thiol protecting agents and antioxidants inhibit the mitochondrial permeability transition promoted by etoposide: implications in the prevention of etoposide-induced apoptosis. Chem Biol Interact 140: 169-184, 2002.. (Pubitemid 34655538)
47. D'Alessio M, Cerella C, Amici C, Pesce C, Coppola S, Fa-nelli C, De Nicola M, Cristofanon S, Clavarino G, Berga-maschi A, Magrini A, Gualandi G, and Ghibelli L. Glutathione depletion up-regulates Bcl-2 in BSO-resistant cells. FASEB J 18: 1609-1611, 2004.. (Pubitemid 39561649)
48. D'Alessio M, Cerella C, De Nicola M, Bergamaschi A, Magrini A, Gualandi G, Alfonsi AM, and Ghibelli L. Apoptotic GSH extrusion is associated with free radical generation. Ann N Y Acad Sci 1010: 449-452, 2003.. (Pubitemid 38265024)
49. D'Alessio M, De Nicola M, Coppola S, Gualandi G, Pug-liese L, Cerella C, Cristofanon S, Civitareale P, Ciriolo MR, Bergamaschi A, Magrini A, and Ghibelli L. Oxidative Bax dimerization promotes its translocation to mitochondria independently of apoptosis. FASEB J 19: 1504-1506, 2005.. (Pubitemid 41279012)
50. Dalle-Donne I, Colombo G, Gagliano N, Colombo R, Giustarini D, Rossi R, and Milzani A. S-glutathiolation in life and death decisions of the cell. Free Radic Res 45: 3-15, 2011..
51. Dalton TP, Chen Y, Schneider SN, Nebert DW, and Shert-zer HG. Genetically altered mice to evaluate glutathione homeostasis in health and disease. Free Radic Biol Med 37: 1511-1526, 2004.. (Pubitemid 39349798)
52. Davis MA, Flaws JA, Young M, Collins K, and Colburn NH. Effect of ceramide on intracellular glutathione determines apoptotic or necrotic cell death of JB6 tumor cells. Toxicol Sci 53: 48-55, 2000.. (Pubitemid 30043602)
53. Deas O, Dumont C, Mollereau B, Metivier D, Pasquier C, Bernard-Pomier G, Hirsch F, Charpentier B, and Senik A. Thiol-mediated inhibition of FAS and CD2 apoptotic signaling in activated human peripheral T cells. Int Immunol 9: 117-125, 1997.. (Pubitemid 27062894)
54. Delgado-Esteban M, Almeida A, and Bolanos JP. D-Glucose prevents glutathione oxidation and mitochondrial damage after glutamate receptor stimulation in rat cortical primary neurons. J Neurochem 75: 1618-1624, 2000..
55. Denton D, Nicolson S, and Kumar S. Cell death by autop-hagy: facts and apparent artefacts. Cell Death Differ 19: 87-95, 2012..
56. Di Monte D, Sandy MS, and Smith MT. Increased efflux rather than oxidation is the mechanism of glutathione depletion by 1-methyl-4-phenyl-1, 2, 3, 6-tetrahydropyridine (MPTP). Biochem Biophys Res Commun 148: 153-160, 1987..
57. Di Stefano A, Frosali S, Leonini A, Ettorre A, Priora R, Di Simplicio FC, and Di Simplicio P. GSH depletion, protein S-glutathionylation and mitochondrial transmembrane potential hyperpolarization are early events in initiation of cell death induced by a mixture of isothiazolinones in HL60 cells. Biochim Biophys Acta 1763: 214-225, 2006..
58. Diaz-Hernandez JI, Almeida A, Delgado-Esteban M, Fernandez E, and Bolanos JP. Knockdown of glutamate-cysteine ligase by small hairpin RNA reveals that both catalytic and modulatory subunits are essential for the survival of primary neurons. J Biol Chem 280: 38992-39001, 2005.. (Pubitemid 41713849)
59. Dimmeler S, Haendeler J, Nehls M, and Zeiher AM. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta-converting enzyme (ICE)-like and cyste-ine protease protein (CPP)-32-like proteases. J Exp Med 185: 601-607, 1997.. (Pubitemid 27098145)
60. Dogan AL, Legrand O, Faussat AM, Perrot JY, and Marie JP. Evaluation and comparison of MRP1 activity with three fluorescent dyes and three modulators in leukemic cell lines. Leuk Res 28: 619-622, 2004.. (Pubitemid 38543199)
61. Drechsel DA, Liang LP, and Patel M. 1-methyl-4-phenylpyridinium-induced alterations of glutathione status in immortalized rat dopaminergic neurons. Toxicol Appl Pharmacol 220: 341-348, 2007.. (Pubitemid 46627847)
62. Ellison I and Richie JP, Jr. Mechanisms of glutathione dis-ulfide efflux from erythrocytes. Biochem Pharmacol 83: 164-169, 2012..
63. Estrela JM, Ortega A, and Obrador E. Glutathione in cancer biology and therapy. Crit Rev Clin Lab Sci 43: 143-181, 2006.. (Pubitemid 43860449)
64. Fadeel B and Orrenius S. Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. J Intern Med 258: 479-517, 2005.. (Pubitemid 41705391)
65. Faucher K, Rabinovitch-Chable H, Cook-Moreau J, Barriere G, Sturtz F, and Rigaud M. Overexpression of human GPX1 modifies Bax to Bcl-2 apoptotic ratio in human endothelial cells. Mol Cell Biochem 277: 81-87, 2005.. (Pubitemid 41236189)
66. Fernandes RS and Cotter TG. Apoptosis or necrosis: in-tracellular levels of glutathione influence mode of cell death. Biochem Pharmacol 48: 675-681, 1994.. (Pubitemid 24283836)
67. Fico A, Manganelli G, Cigliano L, Bergamo P, Abrescia P, Franceschi C, Martini G, and Filosa S. 2-deoxy-d-ribose induces apoptosis by inhibiting the synthesis and increasing the efflux of glutathione. Free Radic Biol Med 45: 211-217, 2008..
68. Filomeni G, Aquilano K, Civitareale P, Rotilio G, and Cir-iolo MR. Activation of c-Jun-N-terminal kinase is required for apoptosis triggered by glutathione disulfide in neuro-blastoma cells. Free Radic Biol Med 39: 345-354, 2005.. (Pubitemid 40910191)
69. Filomeni G, Aquilano K, Rotilio G, and Ciriolo MR. Anti-apoptotic response to induced GSH depletion: involvement of heat shock proteins and NF-kappaB activation. Antioxid Redox Signal 7: 446-455, 2005.. (Pubitemid 40279813)
70. Filomeni G, Rotilio G, and Ciriolo MR. Glutathione dis-ulfide induces apoptosis in U937 cells by a redox-mediated p38 MAP kinase pathway. FASEB J 17: 64-66, 2003..
71. Forman HJ, Zhang H, and Rinna A. Glutathione: overview of its protective roles, measurement, and biosynthesis. Mol Aspects Med 30: 1-12, 2009..
72. Fortenberry JD, Owens ML, and Brown LA. S-nitrosoglutathione enhances neutrophil DNA fragmentation and cell death. Am J Physiol 276: L435-L442, 1999.. (Pubitemid 29159532)
73. Franco R and Cidlowski JA. SLCO/OATP-like transport of glutathione in FasL-induced apoptosis: glutathione efflux is coupled to an organic anion exchange and is necessary for the progression of the execution phase of apoptosis. J Biol Chem 281: 29542-29557, 2006.. (Pubitemid 44536962)
74. Franco R and Cidlowski JA. Apoptosis and glutathione: beyond an antioxidant. Cell Death Differ 16: 1303-1314, 2009..
75. Franco R, DeHaven WI, Sifre M, Bortner CD, and Ci-dlowski JA. Glutathione depletion and disruption of in-tracellular ionic homeostasis regulate lymphoid cell apoptosis. J Biol Chem 283: 36071-36087, 2008..
76. Franco R, Panayiotidis MI, and Cidlowski JA. Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J Biol Chem 282: 30452-30465, 2007.. (Pubitemid 350035221)
77. Franco R, Schoneveld OJ, Pappa A, and Panayiotidis MI. The central role of glutathione in the pathophysiology of human diseases. Arch Physiol Biochem 113: 234-258, 2007..
78. Franklin CC, Krejsa CM, Pierce RH, White CC, Fausto N, and Kavanagh TJ. Caspase-3-dependent cleavage of the glutamate-l-cysteine ligase catalytic subunit during apop-totic cell death. Am J Pathol 160: 1887-1894, 2002.. (Pubitemid 34525668)
79. Franklin CC, Rosenfeld-Franklin ME, White C, Kavanagh TJ, and Fausto N. TGFbeta1-induced suppression of glutathi-one antioxidant defenses in hepatocytes: caspase-dependent post-translational and caspase-independent transcriptional regulatory mechanisms. FASEB J 17: 1535-1537, 2003..
80. Friesen C, Kiess Y, and Debatin KM. A critical role of gluta-thione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differ 11 Suppl 1: S73-S85, 2004.. (Pubitemid 39136800)
81. Furfaro AL, Macay JR, Marengo B, Nitti M, Parodi A, Fe-noglio D, Marinari UM, Pronzato MA, Domenicotti C, and Traverso N. Resistance of neuroblastoma GI-ME-N cell line to glutathione depletion involves Nrf2 and heme oxyge-nase-1. Free Radic Biol Med 52: 488-496, 2012..
82. Gallogly MM, Starke DW, and Mieyal JJ. Mechanistic and kinetic details of catalysis of thiol-disulfide exchange by glutaredoxins and potential mechanisms of regulation. Antioxid Redox Signal 11: 1059-1081, 2009..
83. Galluzzi L, Maiuri MC, Vitale I, Zischka H, Castedo M, Zitvogel L, and Kroemer G. Cell death modalities: classification and pathophysiological implications. Cell Death Differ 14: 1237-1243, 2007.. (Pubitemid 46969863)
84. Galluzzi L, Vitale I, Abrams JM, Alnemri ES, Baehrecke EH, Blagosklonny MV, Dawson TM, Dawson VL, El-Deiry WS, Fulda S, Gottlieb E, Green DR, Hengartner MO, Kepp O, Knight RA, Kumar S, Lipton SA, Lu X, Madeo F, Malorni W, Mehlen P, Nunez G, Peter ME, Piacentini M, Ru-binsztein DC, Shi Y, Simon HU, Vandenabeele P, White E, Yuan J, Zhivotovsky B, Melino G, and Kroemer G. Molecular definitions of cell death subroutines: recommendations of the Nomenclature Committee on Cell Death 2012. Cell Death Differ 19: 107-120, 2012..
85. Garcia-Nogales P, Almeida A, and Bolanos JP. Peroxyni-trite protects neurons against nitric oxide-mediated apoptosis. A key role for glucose-6-phosphate dehydrogenase activity in neuroprotection. J Biol Chem 278: 864-874, 2003.. (Pubitemid 36790760)
86. Garcia-Ruiz C, Fernandez-Checa JC, and Kaplowitz N. Bidirectional mechanism of plasma membrane transport of reduced glutathione in intact rat hepatocytes and membrane vesicles. J Biol Chem 267: 22256-22264, 1992..
87. Garcia TB, Oliveira KR, do Nascimento JL, Crespo-Lopez ME, Picanco-Diniz DL, Mota TC, and Herculano AM. Glutamate induces glutathione efflux mediated by gluta-mate/aspartate transporter in retinal cell cultures. Neu-rochem Res 36: 412-418, 2011..
88. Gendron MC, Schrantz N, Metivier D, Kroemer G, Ma-ciorowska Z, Sureau F, Koester S, and Petit PX. Oxidation of pyridine nucleotides during Fas-and ceramide-induced apoptosis in Jurkat cells: correlation with changes in mitochondria, glutathione depletion, intracellular acidification and caspase 3 activation. Biochem J 353: 357-367, 2001.. (Pubitemid 32096946)
89. Ghibelli L, Coppola S, Fanelli C, Rotilio G, Civitareale P, Scovassi AI, and Ciriolo MR. Glutathione depletion causes cytochrome c release even in the absence of cell commitment to apoptosis. FASEB J 13: 2031-2036, 1999.. (Pubitemid 29517633)
90. Ghibelli L, Fanelli C, Rotilio G, Lafavia E, Coppola S, Co-lussi C, Civitareale P, and Ciriolo MR. Rescue of cells from apoptosis by inhibition of active GSH extrusion. FASEB J 12: 479-486, 1998.. (Pubitemid 28146527)
91. Ghosh S, Pulinilkunnil T, Yuen G, Kewalramani G, An D, Qi D, Abrahani A, and Rodrigues B. Cardiomyocyte apo-ptosis induced by short-term diabetes requires mitochon-drial GSH depletion. Am J Physiol Heart Circ Physiol 289: H768-H776, 2005.. (Pubitemid 41129394)
92. Gouaze V, Andrieu-Abadie N, Cuvillier O, Malagarie-Cazenave S, Frisach MF, Mirault ME, and Levade T. Glutathione peroxidase-1 protects from CD95-induced apoptosis. J Biol Chem 277: 42867-42874, 2002.. (Pubitemid 35285663)
93. Gouaze V, Mirault ME, Carpentier S, Salvayre R, Levade T, and Andrieu-Abadie N. Glutathione peroxidase-1 over-expression prevents ceramide production and partially inhibits apoptosis in doxorubicin-treated human breast carcinoma cells. Mol Pharmacol 60: 488-496, 2001.. (Pubitemid 32781555)
94. Gould NS, Min E, Martin RJ, and Day BJ. CFTR is the primary known apical glutathione transporter involved in cigarette smoke-induced adaptive responses in the lung. Free Radic Biol Med 52: 1201-1206, 2012..
95. Green RM, Graham M, O'Donovan MR, Chipman JK, and Hodges NJ. Subcellular compartmentalization of glutathi-one: correlations with parameters of oxidative stress related to genotoxicity. Mutagenesis 21: 383-390, 2006.. (Pubitemid 44691127)
96. Guha P, Dey A, Sen R, Chatterjee M, Chattopadhyay S, and Bandyopadhyay SK. Intracellular GSH depletion triggered mitochondrial Bax translocation to accomplish resveratrol-induced apoptosis in the U937 cell line. J Pharmacol Exp Ther 336: 206-214, 2011..
97. Hagenbuch B and Meier PJ. Organic anion transporting poly-peptides of the OATP/SLC21 family: phylogenetic classification as OATP/SLCO superfamily, new nomenclature and molecular/functional properties. Pflugers Arch 447: 653-665, 2004.. (Pubitemid 38241451)
98. Hammond CL, Madejczyk MS, and Ballatori N. Activation of plasma membrane reduced glutathione transport in death receptor apoptosis of HepG2 cells. Toxicol Appl Pharmacol 195: 12-22, 2004.. (Pubitemid 38177495)
99. Hammond CL, Marchan R, Krance SM, and Ballatori N. Glutathione export during apoptosis requires functional multidrug resistance-associated proteins. J Biol Chem 282: 14337-14347, 2007.. (Pubitemid 47100459)
100. Han D, Hanawa N, Saberi B, and Kaplowitz N. Hydrogen peroxide and redox modulation sensitize primary mouse hepatocytes to TNF-induced apoptosis. Free Radic Biol Med 41: 627-639, 2006.. (Pubitemid 44080508)
101. Han YH, Kim SH, Kim SZ, and Park WH. Apoptosis in arsenic trioxide-treated Calu-6 lung cells is correlated with the depletion of GSH levels rather than the changes of ROS levels. J Cell Biochem 104: 862-878, 2008..
102. Han YH, Kim SZ, Kim SH, and Park WH. Apoptosis in pyrogallol-treated Calu-6 cells is correlated with the changes of intracellular GSH levels rather than ROS levels. Lung Cancer 59: 301-314, 2008.. (Pubitemid 351343831)
103. Hancock JT, Desikan R, and Neill SJ. Does the redox status of cytochrome C act as a fail-safe mechanism in the regulation of programmed cell death? Free Radic Biol Med 31: 697-703, 2001.. (Pubitemid 32777871)
104. Hansen JM, Zhang H, and Jones DP. Differential oxidation of thioredoxin-1, thioredoxin-2, and glutathione by metal ions. Free Radic Biol Med 40: 138-145, 2006.. (Pubitemid 41759411)
105. He C and Klionsky DJ. Regulation mechanisms and signaling pathways of autophagy. Annu Rev Genet 43: 67-93, 2009..
106. He YY, Huang JL, Ramirez DC, and Chignell CF. Role of reduced glutathione efflux in apoptosis of immortalized human keratinocytes induced by UVA. J Biol Chem 278: 8058-8064, 2003.. (Pubitemid 36800545)
107. Hentze H, Gantner F, Kolb SA, and Wendel A. Depletion of hepatic glutathione prevents death receptor-dependent apoptotic and necrotic liver injury in mice. Am J Pathol 156: 2045-2056, 2000.. (Pubitemid 30641772)
108. Hentze H, Schmitz I, Latta M, Krueger A, Krammer PH, and Wendel A. Glutathione dependence of caspase-8 activation at the death-inducing signaling complex. J Biol Chem 277: 5588-5595, 2002.. (Pubitemid 34968612)
109. Hirrlinger J and Dringen R. Multidrug resistance protein 1-mediated export of glutathione and glutathione dis-ulfide from brain astrocytes. Methods Enzymol 400: 395-409, 2005.. (Pubitemid 43052433)
110. Hirrlinger J, Konig J, Keppler D, Lindenau J, Schulz JB, and Dringen R. The multidrug resistance protein MRP1 mediates the release of glutathione disulfide from rat astrocytes during oxidative stress. J Neurochem 76: 627-636, 2001.. (Pubitemid 32097039)
111. Ho YS, Xiong Y, Ho DS, Gao J, Chua BH, Pai H, and Mieyal JJ. Targeted disruption of the glutaredoxin 1 gene does not sensitize adult mice to tissue injury induced by ischemia/reperfusion and hyperoxia. Free Radic Biol Med 43: 1299-1312, 2007.. (Pubitemid 47440124)
112. Hofken T, Linder D, Kleene R, Goke B, and Wagner AC. Membrane dipeptidase and glutathione are major components of pig pancreatic zymogen granules. Exp Cell Res 244: 481-490, 1998.. (Pubitemid 28507064)
113. Hu HL, Forsey RJ, Blades TJ, Barratt ME, Parmar P, and Powell Jr. Antioxidants may contribute in the fight against ageing: an in vitro model. Mech Ageing Dev 121: 217-230, 2000.. (Pubitemid 32115415)
114. Huang DC, Hahne M, Schroeter M, Frei K, Fontana A, Villunger A, Newton K, Tschopp J, and Strasser A. Activation of Fas by FasL induces apoptosis by a mechanism that cannot be blocked by Bcl-2 or Bcl-x(L). Proc Natl Acad Sci U S A 96: 14871-14876, 1999.. (Pubitemid 30019732)
115. Huang J, Lam GY, and Brumell JH. Autophagy signaling through reactive oxygen species. Antioxid Redox Signal 14: 2215-2231, 2011..
116. Huang KP and Huang FL. Glutathionylation of proteins by glutathione disulfide S-oxide. Biochem Pharmacol 64: 1049-1056, 2002.. (Pubitemid 35232280)
117. Huang Z, Pinto JT, Deng H, and Richie JP, Jr. Inhibition of caspase-3 activity and activation by protein glutathionyla-tion. Biochem Pharmacol 75: 2234-2244, 2008..
118. Iantomasi T, Favilli F, Marraccini P, Magaldi T, Bruni P, and Vincenzini MT. Glutathione transport system in human small intestine epithelial cells. Biochim Biophys Acta 1330: 274-283, 1997.. (Pubitemid 27522785)
119. Imai H and Nakagawa Y. Biological significance of phospho-lipid hydroperoxide glutathione peroxidase (PHGPx, GPx4) in mammalian cells. Free Radic Biol Med 34: 145-169, 2003.. (Pubitemid 36084320)
120. Inoue K, Akaike T, Miyamoto Y, Okamoto T, Sawa T, Otagiri M, Suzuki S, Yoshimura T, and Maeda H. Ni-trosothiol formation catalyzed by ceruloplasmin. Implication for cytoprotective mechanism in vivo. J Biol Chem 274: 27069-27075, 1999..
121. Jang JH and Surh YJ. Bcl-2 attenuation of oxidative cell death is associated with up-regulation of gamma-gluta-mylcysteine ligase via constitutive NF-kappaB activation. J Biol Chem 279: 38779-38786, 2004..
122. Johansson M and Lundberg M. Glutathionylation of beta-actin via a cysteinyl sulfenic acid intermediary. BMC Bio-chem 8: 26, 2007..
123. Jones DP. Redefining oxidative stress. Antioxid Redox Signal 8: 1865-1879, 2006.. (Pubitemid 44726359)
124. Jourd'heuil D, Jourd'heuil FL, and Feelisch M. Oxidation and nitrosation of thiols at low micromolar exposure to nitric oxide. Evidence for a free radical mechanism. J Biol Chem 278: 15720-15726, 2003.. (Pubitemid 36799683)
125. Jungas T, Motta I, Duffieux F, Fanen P, Stoven V, and Oj-cius DM. Glutathione levels and BAX activation during apoptosis due to oxidative stress in cells expressing wildtype and mutant cystic fibrosis transmembrane conductance regulator. J Biol Chem 277: 27912-27918, 2002.. (Pubitemid 34966738)
126. Kane DJ, Sarafian TA, Anton R, Hahn H, Gralla EB, Valentine JS, Ord T, and Bredesen DE. Bcl-2 inhibition of neural death: decreased generation of reactive oxygen species. Science 262: 1274-1277, 1993.. (Pubitemid 24036095)
127. Kayanoki Y, Fujii J, Islam KN, Suzuki K, Kawata S, Mat-suzawa Y, and Taniguchi N. The protective role of gluta-thione peroxidase in apoptosis induced by reactive oxygen species. J Biochem 119: 817-822, 1996.. (Pubitemid 26131786)
128. Kemp M, Go YM, and Jones DP. Nonequilibrium thermodynamics of thiol/disulfide redox systems: a perspective on redox systems biology. Free Radic Biol Med 44: 921-937, 2008..
129. Keppler D, Leier I, Jedlitschky G, and Konig J. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance protein MRP1 and its apical isoform MRP2. Chem Biol Interact 111-112: 153-161, 1998.. (Pubitemid 28271941)
130. Kern JC and Kehrer JP. Free radicals and apoptosis: relationships with glutathione, thioredoxin, and the BCL family of proteins. Front Biosci 10: 1727-1738, 2005.. (Pubitemid 40532954)
131. Keszler A, Zhang Y, and Hogg N. Reaction between nitric oxide, glutathione, and oxygen in the presence and absence of protein: How are S-nitrosothiols formed? Free Radic Biol Med 48: 55-64, 2010..
132. Kim JE and Tannenbaum SR. S-Nitrosation regulates the activation of endogenous procaspase-9 in HT-29 human colon carcinoma cells. J Biol Chem 279: 9758-9764, 2004.. (Pubitemid 38372573)
133. Kirkland RA and Franklin JL. Evidence for redox regulation of cytochrome C release during programmed neuronal death: antioxidant effects of protein synthesis and caspase inhibition. J Neurosci 21: 1949-1963, 2001.. (Pubitemid 32221379)
134. Kizhakkayil J, Thayyullathil F, Chathoth S, Hago A, Patel M, and Galadari S. Glutathione regulates caspase-dependent ceramide production and curcumin-induced apoptosis in human leukemic cells. Free Radic Biol Med 52: 1854-1864, 2012..
135. Kroemer G, Galluzzi L, Vandenabeele P, Abrams J, Al-nemri ES, Baehrecke EH, Blagosklonny MV, El-Deiry WS, Golstein P, Green DR, Hengartner M, Knight RA, Kumar S, Lipton SA, Malorni W, Nunez G, Peter ME, Tschopp J, Yuan J, Piacentini M, Zhivotovsky B, and Melino G. Classification of cell death: recommendations of the Nomenclature Committee on Cell Death 2009. Cell Death Differ 16: 3-11, 2009..
136. Kroemer G and Levine B. Autophagic cell death: the story of a misnomer. Nat Rev Mol Cell Biol 9: 1004-1010, 2008..
137. Kuipers I, Guala AS, Aesif SW, Konings G, Bouwman FG, Mariman EC, Wouters EF, Janssen-Heininger YM, and Reynaert NL. Cigarette smoke targets glutaredoxin 1, increasing s-glutathionylation and epithelial cell death. Am J Respir Cell Mol Biol 45: 931-937, 2011..
138. l'Hoste S, Chargui A, Belfodil R, Corcelle E, Duranton C, Rubera I, Poujeol C, Mograbi B, Tauc M, and Poujeol P. CFTR mediates apoptotic volume decrease and cell death by controlling glutathione efflux and ROS production in cultured mice proximal tubules. Am J Physiol Renal Physiol 298: F435-F453, 2010..
139. Laberge RM, Karwatsky J, Lincoln MC, Leimanis ML, and Georges E. Modulation of GSH levels in ABCC1 expressing tumor cells triggers apoptosis through oxidative stress. Biochem Pharmacol 73: 1727-1737, 2007.. (Pubitemid 46601409)
140. Lagadic-Gossmann D, Huc L, and Lecureur V. Alterations of intracellular pH homeostasis in apoptosis: origins and roles. Cell Death Differ 11: 953-961, 2004.. (Pubitemid 39232355)
141. Lai Y, Hickey RW, Chen Y, Bayir H, Sullivan ML, Chu CT, Kochanek PM, Dixon CE, Jenkins LW, Graham SH, Wat-kins SC, and Clark RS. Autophagy is increased after traumatic brain injury in mice and is partially inhibited by the antioxidant gamma-glutamylcysteinyl ethyl ester. J Cereb Blood Flow Metab 28: 540-550, 2008.. (Pubitemid 351304265)
142. Lampela O, Juffer AH, and Rauk A. Conformational analysis of glutathione in aqueous solution with molecular dynamics. J Phys Chem A 107: 9208-9220, 2003..
143. Lash LH. Mitochondrial glutathione transport: physiological, pathological and toxicological implications. Chem Biol Interact 163: 54-67, 2006.. (Pubitemid 44572210)
144. Lash LH, Putt DA, Xu F, and Matherly LH. Role of rat organic anion transporter 3 (Oat3) in the renal basolateral transport of glutathione. Chem Biol Interact 170: 124-134, 2007.. (Pubitemid 47552421)
145. Lavrik I, Golks A, and Krammer PH. Death receptor signaling. J Cell Sci 118: 265-267, 2005.. (Pubitemid 40277339)
146. Le Foll I and Duval DP. Programmed cell death induced by glutathione depletion in PC 12 cells is blocked by inhibitors of 12 lipoxygenase, but does not appear to be mediated through the formation of 12 HETE derivatives. Free Radic Biol Med 30: 793-802, 2001.. (Pubitemid 32248715)
147. Lee HR, Cho JM, Shin DH, Yong CS, Choi HG, Waka-bayashi N, and Kwak MK. Adaptive response to GSH depletion and resistance to L: -buthionine-(S, R)-sulfoximine: involvement of Nrf2 activation. Mol Cell Biochem 318: 23-31, 2008..
148. Lee JW, Ko YE, Lee IH, Lee HK, Kim HW, and Kim YH. Osmotic stress induces loss of glutathione and increases the sensitivity to oxidative stress in H9c2 cardiac myocytes. Free Radic Res 43: 262-271, 2009..
149. Lee SM, Koh HJ, Park DC, Song BJ, Huh TL, and Park JW. Cytosolic NADP(+)-dependent isocitrate dehydrogenase status modulates oxidative damage to cells. Free Radic Biol Med 32: 1185-1196, 2002.. (Pubitemid 34603355)
150. Lee TK, Hammond CL, and Ballatori N. Intracellular glu-tathione regulates taurocholate transport in HepG2 cells. Toxicol Appl Pharmacol 174: 207-215, 2001.. (Pubitemid 32747831)
151. Leier I, Jedlitschky G, Buchholz U, Center M, Cole SP, Deeley RG, and Keppler D. ATP-dependent glutathione disulphide transport mediated by the MRP gene-encoded conjugate export pump. Biochem J 314 (Pt 2): 433-437, 1996.. (Pubitemid 26075650)
152. Li L, Lee TK, Meier PJ, and Ballatori N. Identification of glutathione as a driving force and leukotriene C4 as a substrate for oatp1, the hepatic sinusoidal organic solute transporter. J Biol Chem 273: 16184-16191, 1998.. (Pubitemid 28311391)
153. Li L, Meier PJ, and Ballatori N. Oatp2 mediates bidirectional organic solute transport: a role for intracellular glu-tathione. Mol Pharmacol 58: 335-340, 2000.. (Pubitemid 30497477)
154. Liang H, Ran Q, Jang YC, Holstein D, Lechleiter J, McDonald-Marsh T, Musatov A, Song W, Van Remmen H, and Richardson A. Glutathione peroxidase 4 differentially regulates the release of apoptogenic proteins from mitochondria. Free Radic Biol Med 47: 312-320, 2009..
155. Lin DY, Ma WY, Duan SJ, Zhang Y, and Du LY. Real-time imaging of viable-apoptotic switch in GSNO-induced mouse thymocyte apoptosis. Apoptosis 11: 1289-1298, 2006.. (Pubitemid 44035940)
156. Liuzzi F, Fanelli C, Ciriolo MR, Cerella C, D'Alessio M, Denicola M, Magrini A, Bergamaschi A, and Ghibelli L. Rescue of cells from apoptosis by antioxidants occurs downstream from GSH extrusion. Ann N Y Acad Sci 1010: 441-445, 2003.. (Pubitemid 38265022)
157. Lou H and Kaplowitz N. Glutathione depletion down-regulates tumor necrosis factor alpha-induced NF-kappaB activity via IkappaB kinase-dependent and-independent mechanisms. J Biol Chem 282: 29470-29481, 2007.. (Pubitemid 350043388)
158. Lu Y and Cederbaum A. The mode of cisplatin-induced cell death in CYP2E1-overexpressing HepG2 cells: modulation by ERK, ROS, glutathione, and thioredoxin. Free Radic Biol Med 43: 1061-1075, 2007.. (Pubitemid 47302654)
159. Lubos E, Loscalzo J, and Handy DE. Glutathione peroxi-dase-1 in health and disease: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 15: 1957-1997, 2011..
160. Mahagita C, Grassl SM, Piyachaturawat P, and Ballatori N. Human organic anion transporter 1B1 (OATP1B1/OATP-C) and 1B3 (OATP1B3/OATP-8) function as bidirectional carriers and do not mediate GSH-bile acid co-transport. Am J Physiol Gastrointest Liver Physiol 293: G271-G278, 2007.. (Pubitemid 47105195)
161. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, Kane LS, Gow AJ, and Stamler JS. Fas-induced caspase denitrosylation. Science 284: 651-654, 1999.. (Pubitemid 29289591)
162. Mannick JB, Miao XQ, and Stamler JS. Nitric oxide inhibits Fas-induced apoptosis. J Biol Chem 272: 24125-24128, 1997.. (Pubitemid 27418605)
163. Mannick JB, Schonhoff C, Papeta N, Ghafourifar P, Szibor M, Fang K, and Gaston B. S-Nitrosylation of mitochondrial caspases. J Cell Biol 154: 1111-1116, 2001.. (Pubitemid 34286189)
164. Marchan R, Hammond CL, and Ballatori N. Multidrug resistance-associated protein 1 as a major mediator of basal and apoptotic glutathione release. Biochim Biophys Acta 1778: 2413-2420, 2008..
165. Marengo B, De Ciucis C, Verzola D, Pistoia V, Raffaghello L, Patriarca S, Balbis E, Traverso N, Cottalasso D, Pronzato MA, Marinari UM, and Domenicotti C. Mechanisms of BSO (L-buthionine-S, R-sulfoximine)-induced cytotoxic effects in neuroblastoma. Free Radic Biol Med 44: 474-482, 2008..
166. Mari M, Morales A, Colell A, Garcia-Ruiz C, and Fernan-dez-Checa JC. Mitochondrial glutathione, a key survival antioxidant. Antioxid Redox Signal 11: 2685-2700, 2009..
167. Martin HL and Teismann P. Glutathione-a review on its role and significance in Parkinson's disease. FASEB J 23: 3263-3272, 2009..
168. Matsumaru K, Ji C and Kaplowitz N. Mechanisms for sensitization to TNF-induced apoptosis by acute glutathi-one depletion in murine hepatocytes. Hepatology 37: 1425-1434, 2003.. (Pubitemid 36667323)
169. Mattson DM, Ahmad IM, Dayal D, Parsons AD, Aykin-Burns N, Li L, Orcutt KP, Spitz DR, Dornfeld KJ, and Simons AL. Cisplatin combined with zidovudine enhances cytotoxicity and oxidative stress in human head and neck cancer cells via a thiol-dependent mechanism. Free Radic Biol Med 46: 232-237, 2009..
170. McCall K. Genetic control of necrosis-another type of programmed cell death. Curr Opin Cell Biol 22: 882-888, 2010..
171. McNeely SC, Belshoff AC, Taylor BF, Fan TW, McCabe MJ, Jr., Pinhas AR, and States JC. Sensitivity to sodium arsenite in human melanoma cells depends upon susceptibility to arsenite-induced mitotic arrest. Toxicol Appl Pharmacol 229: 252-261, 2008..
172. Meister A. Glutathione biosynthesis and its inhibition. Methods Enzymol 252: 26-30, 1995..
173. Melino G, Bernassola F, Knight RA, Corasaniti MT, Nistico G, and Finazzi-Agro A. S-nitrosylation regulates apoptosis. Nature 388: 432-433, 1997..
174. Messmer UK, Lapetina EG, and Brune B. Nitric oxide-induced apoptosis in RAW 264.7 macrophages is antagonized by protein kinase C-and protein kinase A-activating compounds. Mol Pharmacol 47: 757-765, 1995..
175. Meurette O, Lefeuvre-Orfila L, Rebillard A, Lagadic-Goss-mann D, and Dimanche-Boitrel MT. Role of intracellular glutathione in cell sensitivity to the apoptosis induced by tumor necrosis factor {alpha}-related apoptosis-inducing ligand/anticancer drug combinations. Clin Cancer Res 11: 3075-3083, 2005.. (Pubitemid 40525214)
176. Mieyal JJ, Gallogly MM, Qanungo S, Sabens EA, and Shelton MD. Molecular mechanisms and clinical implications of reversible protein S-glutathionylation. Antioxid Redox Signal 10: 1941-1988, 2008..
177. Minich T, Riemer J, Schulz JB, Wielinga P, Wijnholds J, and Dringen R. The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and gluta-thione disulfide from brain astrocytes. J Neurochem 97: 373-384, 2006..
178. Mitchell DA, Morton SU, Fernhoff NB, and Marletta MA. Thioredoxin is required for S-nitrosation of procaspase-3 and the inhibition of apoptosis in Jurkat cells. Proc Natl Acad Sci U S A 104: 11609-11614, 2007.. (Pubitemid 47175060)
179. Mohr S, Hallak H, de Boitte A, Lapetina EG, and Brune B. Nitric oxide-induced S-glutathionylation and inactivation of glyceraldehyde-3-phosphate dehydrogenase. J Biol Chem 274: 9427-9430, 1999..
180. Monostori P, Wittmann G, Karg E, and Turi S. Determination of glutathione and glutathione disulfide in biological samples: an in-depth review. J Chromatogr B Analyt Technol Biomed Life Sci 877: 3331-3346, 2009..
181. Morgan MJ, Kim YS, and Liu ZG. TNFalpha and reactive oxygen species in necrotic cell death. Cell Res 18: 343-349, 2008.. (Pubitemid 351333898)
182. Mueller CF, Widder JD, McNally JS, McCann L, Jones DP, and Harrison DG. The role of the multidrug resistance protein-1 in modulation of endothelial cell oxidative stress. Circ Res 97: 637-644, 2005.. (Pubitemid 41416332)
183. Musallam L, Ethier C, Haddad PS, and Bilodeau M. EGF mediates protection against Fas-induced apoptosis by depleting and oxidizing intracellular GSH stocks. J Cell Physiol 198: 62-72, 2004.. (Pubitemid 38124458)
184. Nagai H, Matsumaru K, Feng G, and Kaplowitz N. Reduced glutathione depletion causes necrosis and sensitiza-tion to tumor necrosis factor-alpha-induced apoptosis in cultured mouse hepatocytes. Hepatology 36: 55-64, 2002.. (Pubitemid 34700762)
185. Nepravishta R, Sabelli R, Iorio E, Micheli L, Paci M, and Melino S. Oxidative species and S-glutathionyl conjugates in the apoptosis induction by allyl thiosulfate. FEBS J 279: 154-167, 2012..
186. Ng KH, Lim BG, and Wong KP. Sulfate conjugating and transport functions of MDCK distal tubular cells. Kidney Int 63: 976-986, 2003.. (Pubitemid 36315575)
187. Nomura K, Imai H, Koumura T, Kobayashi T, and Naka-gawa Y. Mitochondrial phospholipid hydroperoxide glu-tathione peroxidase inhibits the release of cytochrome c from mitochondria by suppressing the peroxidation of cardiolipin in hypoglycaemia-induced apoptosis. Biochem J 351: 183-193, 2000..
188. Nur E, Verwijs M, de Waart DR, Schnog JJ, Otten HM, Brandjes DP, Biemond BJ, and Elferink RP. Increased efflux of oxidized glutathione (GSSG) causes glutathione depletion and potentially diminishes antioxidant defense in sickle erythrocytes. Biochim Biophys Acta 1812: 1412-1417, 2011..
189. O'Neill AJ, O'Neill S, Hegarty NJ, Coffey RN, Gibbons N, Brady H, Fitzpatrick JM, and Watson RW. Glutathione depletion-induced neutrophil apoptosis is caspase 3 dependent. Shock 14: 605-609, 2000..
190. Oda T, Sadakata N, Komatsu N, and Muramatsu T. Specific efflux of glutathione from the basolateral membrane domain in polarized MDCK cells during ricin-induced apo-ptosis. J Biochem 126: 715-721, 1999.. (Pubitemid 29500392)
191. Ortega A, Ferrer P, Carretero J, Obrador E, Asensi M, Pel-licer JA, and Estrela JM. Down-regulation of glutathione and Bcl-2 synthesis in mouse B16 melanoma cells avoids their survival during interaction with the vascular endo-thelium. J Biol Chem 278: 39591-39599, 2003.. (Pubitemid 37248518)
192. Osbild S, Brault L, Battaglia E, and Bagrel D. Resistance to cisplatin and adriamycin is associated with the inhibition of glutathione efflux in MCF-7-derived cells. Anticancer Res 26: 3595-3600, 2006.. (Pubitemid 44701544)
193. Pan S and Berk BC. Glutathiolation regulates tumor necrosis factor-alpha-induced caspase-3 cleavage and apop-tosis: key role for glutaredoxin in the death pathway. Circ Res 100: 213-219, 2007.. (Pubitemid 46208721)
194. Pan Z, Voehringer DW, and Meyn RE. Analysis of redox regulation of cytochrome c-induced apoptosis in a cell-free system. Cell Death Differ 6: 683-688, 1999.. (Pubitemid 29366658)
195. Park HA, Khanna S, Rink C, Gnyawali S, Roy S, and Sen CK. Glutathione disulfide induces neural cell death via a 12-lipoxygenase pathway. Cell Death Differ 16: 1167-1179, 2009..
196. Perricone C, De Carolis C, and Perricone R. Glutathione: a key player in autoimmunity. Autoimmun Rev 8: 697-701, 2009..
197. Perrotton T, Trompier D, Chang XB, Di Pietro A, and Baubichon-Cortay H. (R)-and (S)-verapamil differentially modulate the multidrug-resistant protein MRP1. J Biol Chem 282: 31542-31548, 2007.. (Pubitemid 350044880)
198. Pias EK and Aw TY. Apoptosis in mitotic competent un-differentiated cells is induced by cellular redox imbalance independent of reactive oxygen species production. FASEB J 16: 781-790, 2002.. (Pubitemid 34615126)
199. Pias EK and Aw TY. Early redox imbalance mediates hydroperoxide-induced apoptosis in mitotic competent un-differentiated PC-12 cells. Cell Death Differ 9: 1007-1016, 2002.. (Pubitemid 35023615)
200. Poole LB and Nelson KJ. Discovering mechanisms of signaling-mediated cysteine oxidation. Curr Opin Chem Biol 12: 18-24, 2008..
201. Qanungo S, Starke DW, Pai HV, Mieyal JJ, and Nieminen AL. Glutathione supplementation potentiates hypoxic ap-optosis by S-glutathionylation of p65-NFkappaB. J Biol Chem 282: 18427-18436, 2007.. (Pubitemid 47100260)
202. Rahman I, Kode A, and Biswas SK. Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1: 3159-3165, 2006..
203. Ran Q, Liang H, Gu M, Qi W, Walter CA, Roberts LJ, 2nd, Herman B, Richardson A, and Van Remmen H. Transgenic mice overexpressing glutathione peroxidase 4 are protected against oxidative stress-induced apoptosis. J Biol Chem 279: 55137-55146, 2004.. (Pubitemid 40066507)
204. Rana S and Dringen R. Gap junction hemichannel-mediated release of glutathione from cultured rat astro-cytes. Neurosci Lett 415: 45-48, 2007.. (Pubitemid 46356717)
205. Ray SD, Kamendulis LM, Gurule MW, Yorkin RD, and Corcoran GB. Ca2+ antagonists inhibit DNA fragmentation and toxic cell death induced by acetaminophen. FASEB J 7: 453-463, 1993.. (Pubitemid 23108560)
206. Rius M, Hummel-Eisenbeiss J, Hofmann AF, and Keppler D. Substrate specificity of human ABCC4 (MRP4)-mediated cotransport of bile acids and reduced glutathione. Am J Physiol Gastrointest Liver Physiol 290: G640-G649, 2006..
207. Rouzer CA, Scott WA, Griffith OW, Hamill AL, and Cohn ZA. Glutathione metabolism in resting and phago-cytizing peritoneal macrophages. J Biol Chem 257: 2002-2008, 1982.. (Pubitemid 12146167)
208. Rudin CM, Yang Z, Schumaker LM, VanderWeele DJ, Newkirk K, Egorin MJ, Zuhowski EG, and Cullen KJ. Inhibition of glutathione synthesis reverses Bcl-2-mediated cisplatin resistance. Cancer Res 63: 312-318, 2003.. (Pubitemid 36152486)
209. Ryter SW, Kim HP, Hoetzel A, Park JW, Nakahira K, Wang X, and Choi AM. Mechanisms of cell death in oxidative stress. Antioxid Redox Signal 9: 49-89, 2007.. (Pubitemid 44901874)
210. Sato T, Machida T, Takahashi S, Iyama S, Sato Y, Kur-ibayashi K, Takada K, Oku T, Kawano Y, Okamoto T, Ta-kimoto R, Matsunaga T, Takayama T, Takahashi M, Kato J, and Niitsu Y. Fas-mediated apoptosome formation is dependent on reactive oxygen species derived from mito-chondrial permeability transition in Jurkat cells. J Immunol 173: 285-296, 2004.. (Pubitemid 38797353)
211. Sawai H and Domae N. Transfer of Fas (CD95) protein from the cell surface to the surface of polystyrene beads coated with anti-Fas antibody clone CH-11. Eur J Histochem 54: e8, 2010..
212. Schafer FQ and Buettner GR. Redox environment of the cell as viewed through the redox state of the glutathione dis-ulfide/glutathione couple. Free Radic Biol Med 30: 1191-1212, 2001.. (Pubitemid 32463931)
213. Scherz-Shouval R, Shvets E, Fass E, Shorer H, Gil L, and Elazar Z. Reactive oxygen species are essential for autop-hagy and specifically regulate the activity of Atg4. EMBO J 26: 1749-1760, 2007.. (Pubitemid 46624042)
214. Schor NF, Rudin CM, Hartman AR, Thompson CB, Tyur-ina YY, and Kagan VE. Cell line dependence of Bcl-2-induced alteration of glutathione handling. Oncogene 19: 472-476, 2000.. (Pubitemid 30077350)
215. Schrammel A, Gorren AC, Schmidt K, Pfeiffer S, and Mayer B. S-nitrosation of glutathione by nitric oxide, peroxynitrite, and (*)NO/O(2)(*-). Free Radic Biol Med 34: 1078-1088, 2003..
216. Seiler A, Schneider M, Forster H, Roth S, Wirth EK, Culmsee C, Plesnila N, Kremmer E, Radmark O, Wurst W, Bornkamm GW, Schweizer U, and Conrad M. Glutathione peroxidase 4 senses and translates oxidative stress into 12/15-lipoxygenase dependent-and AIF-mediated cell death. Cell Metab 8: 237-248, 2008..
217. Sekine S, Mitsuki K, Ito K, Kugioka S, and Horie T. Sustained intrahepatic glutathione depletion causes proteasomal degradation of multidrug resistance-associated protein 2 in rat liver. Biochim Biophys Acta 1822: 980-987, 2012..
218. Shen S, Kepp O, and Kroemer G. The end of autophagic cell death? Autophagy 8, 2012..
219. Sies H. Glutathione and its role in cellular functions. Free Radic Biol Med 27: 916-921, 1999.. (Pubitemid 29507465)
220. Slater AF, Stefan C, Nobel I, van den Dobbelsteen DJ, and Orrenius S. Intracellular redox changes during apoptosis. Cell Death Differ 3: 57-62, 1996.. (Pubitemid 26072531)
221. Sreekumar PG, Spee C, Ryan SJ, Cole SP, Kannan R, and Hinton DR. Mechanism of RPE cell death in alpha-crystallin deficient mice: a novel and critical role for MRP1-mediated GSH efflux. PLoS One 7: e33420, 2012..
222. Staab CA, Alander J, Brandt M, Lengqvist J, Morgenstern R, Grafstrom RC, and Hoog JO. Reduction of S-nitrosoglutathione by alcohol dehydrogenase 3 is facilitated by substrate alcohols via direct cofactor recycling and leads to GSH-controlled formation of glutathione transferase inhibitors. Biochem J 413: 493-504, 2008..
223. Starke DW, Chock PB, and Mieyal JJ. Glutathione-thiyl radical scavenging and transferase properties of human glutaredoxin (thioltransferase). Potential role in redox signal transduction. J Biol Chem 278: 14607-14613, 2003.. (Pubitemid 36799782)
224. Stridh MH, Correa F, Nodin C, Weber SG, Blomstrand F, Nilsson M, and Sandberg M. Enhanced glutathione efflux from astrocytes in culture by low extracellular Ca2+ and curcumin. Neurochem Res 35: 1231-1238, 2010..
225. Stridh MH, Tranberg M, Weber SG, Blomstrand F, and Sandberg M. Stimulated efflux of amino acids and gluta-thione from cultured hippocampal slices by omission of extracellular calcium: likely involvement of connexin hemichannels. J Biol Chem 283: 10347-10356, 2008..
226. Stubauer G, Giuffre A, and Sarti P. Mechanism of S-nitrosothiol formation and degradation mediated by copper ions. J Biol Chem 274: 28128-28133, 1999..
227. Sullivan DM, Wehr NB, Fergusson MM, Levine RL, and Finkel T. Identification of oxidant-sensitive proteins: TNF-alpha induces protein glutathiolation. Biochemistry 39: 11121-11128, 2000..
228. Sumbayev VV. S-nitrosylation of thioredoxin mediates activation of apoptosis signal-regulating kinase 1. Arch Bio-chem Biophys 415: 133-136, 2003.. (Pubitemid 36687926)
229. Sze G, Kaplowitz N, Ookhtens M, and Lu SC. Bidirectional membrane transport of intact glutathione in Hep G2 cells. Am J Physiol 265: G1128-G1134, 1993..
230. Tao L and English AM. Protein S-glutathiolation triggered by decomposed S-nitrosoglutathione. Biochemistry 43: 4028-4038, 2004.. (Pubitemid 38437069)
231. Thomson SJ, Cox AG, Cuddihy SL, Pullar JM, and Hampton MB. Inhibition of receptor-mediated apoptosis upon Bcl-2 overexpression is not associated with increased antioxidant status. Biochem Biophys Res Commun 375: 145-150, 2008..
232. Trompier D, Chang XB, Barattin R, du Moulinet D'Hard-emare A, Di Pietro A, and Baubichon-Cortay H. Verapamil and its derivative trigger apoptosis through glutathione extrusion by multidrug resistance protein MRP1. Cancer Res 64: 4950-4956, 2004.. (Pubitemid 38924542)
233. Troyano A, Fernandez C, Sancho P, de Blas E, and Aller P. Effect of glutathione depletion on antitumor drug toxicity (apoptosis and necrosis) in U-937 human promonocytic cells. The role of intracellular oxidation. J Biol Chem 276: 47107-47115, 2001..
234. Troyano A, Sancho P, Fernandez C, de Blas E, Bernardi P, and Aller P. The selection between apoptosis and necrosis is differentially regulated in hydrogen peroxide-treated and glutathione-depleted human promonocytic cells. Cell Death Differ 10: 889-898, 2003.. (Pubitemid 36939699)
235. Tulpule K and Dringen R. Formaldehyde stimulates Mrp1-mediated glutathione deprivation of cultured astrocytes. J Neurochem 116: 626-635, 2011..
236. Vahrmeijer AL, Hoetelmans RW, Mulder GJ, Schutrups J, van Vlierberghe RL, van de Velde CJ, and van Dierendonck JH. Development of resistance to glutathione depletion-induced cell death in CC531 colon carcinoma cells: association with increased expression of bcl-2. Biochem Pharmacol 59: 1557-1562, 2000.. (Pubitemid 30229888)
237. Valko M, Morris H, and Cronin MT. Metals, toxicity and oxidative stress. Curr Med Chem 12: 1161-1208, 2005.. (Pubitemid 40655271)
238. Valverde M, Rojas E, Kala SV, Kala G, and Lieberman MW. Survival and cell death in cells constitutively unable to synthesize glutathione. Mutat Res 594: 172-180, 2006.. (Pubitemid 43170997)
239. van den Dobbelsteen DJ, Nobel CS, Schlegel J, Cotgreave IA, Orrenius S, and Slater AF. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J Biol Chem 271: 15420-15427, 1996.. (Pubitemid 26225311)
240. Van Luyn MJ, Muller M, Renes J, Meijer C, Scheper RJ, Nienhuis EF, Mulder NH, Jansen PL, and De Vries EG. Transport of glutathione conjugates into secretory vesicles is mediated by the multidrug-resistance protein 1. Int J Cancer 76: 55-62, 1998.. (Pubitemid 28164569)
241. Varghese J, Khandre NS, and Sarin A. Caspase-3 activation is an early event and initiates apoptotic damage in a human leukemia cell line. Apoptosis 8: 363-370, 2003.. (Pubitemid 36935208)
242. Voehringer DW and Meyn RE. Redox aspects of Bcl-2 function. Antioxid Redox Signal 2: 537-550, 2000..
243. Wang H, Li J, Follett PL, Zhang Y, Cotanche DA, Jensen FE, Volpe JJ, and Rosenberg PA. 12-Lipoxygenase plays a key role in cell death caused by glutathione depletion and ar-achidonic acid in rat oligodendrocytes. Eur J Neurosci 20: 2049-2058, 2004.. (Pubitemid 39331125)
244. Wang W and Ballatori N. Endogenous glutathione conjugates: occurrence and biological functions. Pharmacol Rev 50: 335-356, 1998..
245. Will Y, Kaetzel RS, Brown MK, Fraley TS, and Reed DJ. In vivo reversal of glutathione deficiency and susceptibility to in vivo dexamethasone-induced apoptosis by N-acetylcysteine and L-2-oxothiazolidine-4-carboxylic acid, but not ascorbic acid, in thymocytes from gamma-gluta-myltranspeptidase-deficient knockout mice. Arch Biochem Biophys 397: 399-406, 2002.. (Pubitemid 34852309)
246. Winterbourn CC and Hampton MB. Thiol chemistry and specificity in redox signaling. Free Radic Biol Med 45: 549-561, 2008..
247. Xu K and Thornalley PJ. Involvement of glutathione metabolism in the cytotoxicity of the phenethyl isothiocyanate and its cysteine conjugate to human leukaemia cells in vitro. Biochem Pharmacol 61: 165-177, 2001.. (Pubitemid 32121781)
248. Xu X, Chua CC, Kong J, Kostrzewa RM, Kumaraguru U, Hamdy RC, and Chua BH. Necrostatin-1 protects against glutamate-induced glutathione depletion and caspase-independent cell death in HT-22 cells. J Neurochem 103: 2004-2014, 2007.. (Pubitemid 350126615)
249. Yang J, Bogni A, Schuetz EG, Ratain M, Dolan ME, McLeod H, Gong L, Thorn C, Relling MV, Klein TE, and Altman RB. Etoposide pathway. Pharmacogenet Genomics 19: 552-553, 2009..
250. Yang Z, Wang ZE, Doulias PT, Wei W, Ischiropoulos H, Locksley RM, and Liu L. Lymphocyte development requires S-nitrosoglutathione reductase. J Immunol 185: 6664-6669, 2010..
251. Yuan H, Perry CN, Huang C, Iwai-Kanai E, Carreira RS, Glembotski CC, and Gottlieb RA. LPS-induced autophagy is mediated by oxidative signaling in cardiomyocytes and is associated with cytoprotection. Am J Physiol Heart Circ Physiol 296: H470-H479, 2009..
252. Yuan L and Kaplowitz N. Glutathione in liver diseases and hepatotoxicity. Mol Aspects Med 30: 29-41, 2009..
253. Zamzami N, Marzo I, Susin SA, Brenner C, Larochette N, Marchetti P, Reed J, Kofler R, and Kroemer G. The thiol crosslinking agent diamide overcomes the apoptosis-inhibitory effect of Bcl-2 by enforcing mitochondrial permeability transition. Oncogene 16: 1055-1063, 1998.. (Pubitemid 28107943)
254. Zhang H, Limphong P, Pieper J, Liu Q, Rodesch CK, Christians E, and Benjamin IJ. Glutathione-dependent reductive stress triggers mitochondrial oxidation and cyto-toxicity. FASEB J 26: 1442-1451, 2012..
255. Zhang Z, Liew CW, Handy DE, Zhang Y, Leopold JA, Hu J, Guo L, Kulkarni RN, Loscalzo J, and Stanton RC. High glucose inhibits glucose-6-phosphate dehydrogenase, leading to increased oxidative stress and beta-cell apopto-sis. FASEB J 24: 1497-1505, 2010..
256. Zhu J, Krom BP, Sanglard D, Intapa C, Dawson CC, Peters BM, Shirtliff ME, and Jabra-Rizk MA. Farnesol-induced apoptosis in Candida albicans is mediated by Cdr1-p extrusion and depletion of intracellular glutathione. PLoS One 6: e28830, 2011..
257. Zimmermann AK, Loucks FA, Schroeder EK, Bouchard RJ, Tyler KL, and Linseman DA. Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria. J Biol Chem 282: 29296-29304, 2007.. (Pubitemid 350043369)