Plasma membrane glutathione transporters and their roles in cell physiology and pathophysiology

Molecular Aspects of Medicine

Volumn 30, Issue 1-2, 2009, Pages 13-28

  Ballatori, Nazzareno ^a   Krance, Suzanne M ^a   Marchan, Rosemarie ^a   Hammond, Christine L ^a  

^a UNIVERSITY OF ROCHESTER SCHOOL OF MEDICINE AND DENTISTRY   (United States)

Author keywords

Apoptosis; Cell proliferation and differentiation; Glutathione; Glutathione transporters; Multidrug resistance associated proteins; Signaling; Thiol redox status; Xenobiotic export

Indexed keywords

BILE SALT; BILIRUBIN; CYCLIC NUCLEOTIDE; GLUCURONIC ACID; GLUTATHIONE; GLUTATHIONE DERIVATIVE; GLUTATHIONE DISULFIDE; METAL COMPLEX; MULTIDRUG RESISTANCE PROTEIN; MULTIDRUG RESISTANCE PROTEIN 1; MULTIDRUG RESISTANCE PROTEIN 2; MULTIDRUG RESISTANCE PROTEIN 5; S NITROSOGLUTATHIONE; STEROID; THIOL; TRANSMEMBRANE CONDUCTANCE REGULATOR; TRIPEPTIDE; XENOBIOTIC AGENT;

APOPTOSIS; AUTOIMMUNE DISEASE; CATABOLISM; CELL DEGENERATION; CELL DIFFERENTIATION; CELL FUNCTION; CELL LEVEL; CELL MATURATION; CELL MEMBRANE; CELL MOTION; CELL PROLIFERATION; CHOLESTEROL TRANSPORT; COMPLEX FORMATION; CONJUGATE; CONJUGATION; DEGENERATIVE DISEASE; HOMEOSTASIS; HUMAN; INFLAMMATION; LIVER CELL; MAMMAL CELL; NONHUMAN; OXIDATION; OXIDATION REDUCTION REACTION; OXIDATION REDUCTION STATE; PATHOPHYSIOLOGY; PEPTIDE SYNTHESIS; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN TRANSPORT; REGULATORY MECHANISM; REVIEW; SIGNAL TRANSDUCTION; STEM CELL; SYNTHESIS;

ANIMALS; APOPTOSIS; CELL MEMBRANE; CELL PROLIFERATION; HUMANS; MEMBRANE TRANSPORT PROTEINS; MODELS, BIOLOGICAL;

MAMMALIA;

EID: 65049090568     PISSN: 00982997     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mam.2008.08.004     Document Type: Review

References (225)

1. Alexander R.L., Bates D.J., Wright M.W., King S.B., and Morrow C.S. Modulation of nitrated lipid signaling by multidrug resistance protein 1 (MRP1): glutathione conjugation and MRP1-mediated efflux inhibit nitrolinoleic acid-induced, PPARgamma-dependent transcription activation. Biochemistry 45 (2006) 7889-7896
2. Anderson C.P., Tsai J.M., Meek W.E., Liu R.M., Tang Y., Forman H.J., and Reynolds C.P. Depletion of glutathione by buthionine sulfoxine is cytotoxic for human neuroblastoma cell lines via apoptosis. Exp. Cell. Res. 246 1 (1999) 183-192
3. Anselmo A.N., and Cobb M.H. Protein kinase function and glutathionylation. Biochem. J. 381 (2004) e1-2
4. Aracena P., Sánchez G., Donoso P., Hamilton S.L., and Hidalgo C. S-Glutathionylation decreases Mg2+ inhibition and S-nitrosylation enhances Ca2+ activation of RyR1 channels. J. Biol. Chem. 278 44 (2003) 42927-42935
5. Ardite E., Barbera J.A., Roca J., and Fernandez-Checa J.C. Glutathione depletion impairs myogenic differentiation of murine skeletal muscle C2C12 cells through sustained NF-kappaB activation. Am. J. Pathol. 165 (2004) 719-728
6. Arrigo A.P. Gene expression and the thiol redox state. Free Radical Biol. Med. 27 (1999) 936-944
7. Atsmon J., Freeman M.L., Meredith M.J., Sweetman B.J., and Roberts L.J. Conjugation of 9-deoxy-{up triangle, filled}9,{up triangle, filled}12(E)-prostaglandin D2 with intracellular glutathione and enhancement of its antiproliferative activity by glutathione depletion. Cancer Res. 50 (1990) 1879-1885
8. Bakos E., Evers R., Sinko E., Varadi A., Borst P., and Sarkadi B. Interactions of the human multidrug resistance proteins MRP1 and MRP2 with organic anions. Mol. Pharmacol. 57 4 (2000) 760-768
9. Ballatori N. Glutathione mercaptides as transport forms of metals. Adv. Pharmacol. 27 (1994) 271-298
10. Ballatori N. Transport of toxic metals by molecular mimicry. Environ. Health Perspect. 110 Suppl. 5 (2002) 689-694
11. Ballatori N., and Dutczak W.J. Identification and characterization of high and low affinity transport systems for reduced glutathione in liver cell canalicular membranes. J. Biol. Chem. 269 31 (1994) 19731-19737
12. Ballatori N., and Truong A.T. Relation between biliary glutathione excretion and bile acid-independent bile flow. Am. J. Physiol. 256 1 Pt 1 (1989) G22-G30
13. Ballatori N., and Truong A.T. Glutathione as a primary osmotic driving force in hepatic bile formation. Am. J. Physiol. 263 5 Pt 1 (1992) G617-G624
14. Ballatori N., Moseley R.H., and Boyer J.L. Sodium gradient-dependent l-glutamate transport is localized to the canalicular domain of liver plasma membranes. Studies in rat liver sinusoidal and canalicular membrane vesicles. J. Biol. Chem. 261 (1986) 6216-6221
15. Ballatori N., Jacob R., and Boyer J.L. Intrabiliary glutathione hydrolysis - a source of glutamate in bile. J. Biol. Chem. 261 (1986) 7860-7865
16. Ballatori N., Jacob R., Barrett C., and Boyer J.L. Biliary catabolism of glutathione and differential reabsorption of its amino acid constituents. Am. J. Physiol. 254 (1988) G1-G7
17. Ballatori N., Truong A.T., Ma A.K., and Boyer J.L. Determinants of glutathione efflux and biliary GSH/GSSG ratio in perfused rat liver. Am. J. Physiol. 256 (1989) G482-G490
18. Ballatori N., Gatmaitan Z., and Truong A.T. Impaired biliary excretion and whole body elimination of methylmercury in rats with a congenital defect in biliary glutathione excretion. Hepatology 22 (1995) 1469-1473
19. Ballatori N., Hammond C.L., Cunningham J.B., Krance S.M., and Marchan R. Molecular mechanisms of reduced glutathione transport: role of the MRP/CFTR/ABCC and OATP/SLC21A families of membrane proteins. Toxicol. Appl. Pharmacol. 204 3 (2005) 238-255
20. Bánhegyi G., Csala M., Nagy G., Sorrentino V., Fulceri R., and Benedetti A. Evidence for the transport of glutathione through ryanodine receptor channel type 1. Biochem. J. 376 Pt 3 (2003) 807-812
21. Barrett W.C., DeGnore J.P., Konig S., Fales H.M., Keng Y.F., Zhang Z.Y., Yim M.B., and Chock P.B. Regulation of PTP1B via glutathionylation of the active site cysteine 215. Biochemistry 38 (1999) 6699-6705
22. Beaver J.P., and Waring P. A decrease in intracellular glutathione concentration precedes the onset of apoptosis in murine thymocytes. Eur. J. Cell Biol. 68 1 (1995) 47-54
23. Beck K., Hayashi K., Dang K., Hayashi M., and Boyd C.D. Analysis of ABCC6 (MRP6) in normal human tissues. Histochem. Cell Biol. 123 4-5 (2005) 517-528
24. Belinsky M.G., Bain L.J., Balsara B.B., Testa J.R., and Kruh G.D. Characterization of MOAT-C and MOAT-D, new members of the MRP/cMOAT subfamily of transporter proteins. J. Natl. Cancer Inst. 90 (1998) 1735-1741
25. Benard O., and Balasubramanian K.A. Modulation of glutathione level during butyrate-induced differentiation in human colon derived HT-29 cells. Mol. Cell Biochem. 170 (1997) 109-114
26. Benlloch M., Ortega A., Ferrer P., Segarra R., Obrador E., Asensi M., Carretero J., and Estrela J.M. Acceleration of glutathione efflux and inhibition of gamma-glutamyltranspeptidase sensitize metastatic B16 melanoma cells to endothelium-induced cytotoxicity. J. Biol. Chem. 280 8 (2005) 6950-6959
27. Blackburn R.V., Spitz D.R., Liu X., Galoforo S.S., Sim J.E., Ridnour L.A., Chen J.C., Davis B.H., Corry P.M., and Lee Y.J. Metabolic oxidative stress activates signal transduction and gene expression during glucose deprivation in human tumor cells. Free Radical Biol. Med. 26 (1999) 419-430
28. Bojes H.K., Datta K., Xu J., Chin A., Simonian P., Nunez G., and Kehrer J.P. Bcl-xL overexpression attenuates glutathione depletion in FL5.12 cells following interleukin-3 withdrawal. Biochem. J. 325 Pt 2 (1997) 315-319
29. Borst P., and Oude Elferink R.P.J. Mammalian ABC transporters in health and disease. Ann. Rev. Biochem. 71 (2002) 537-592
30. Borst P., Evers R., Kool M., and Wijnholds J. A family of drug transporters: the multidrug resistance-associated proteins. J. Natl. Cancer Inst. 92 16 (2000) 1295-1302
31. Borst P., de Wolf C., and van de Wetering K. Multidrug resistance-associated proteins 3, 4, and 5. Eur. J. Physiol. 453 (2007) 661-673
32. Buchler M., Konig J., Brom M., Kartenbeck J., Spring H., Horie T., and Keppler D. CDNA cloning of the hepatocyte canalicular isoform of the multidrug resistance protein, cMrp, reveals a novel conjugate export pump deficient in hyperbilirubinemic mutant rats. J. Biol. Chem. 271 25 (1996) 15091-15098
33. Celli A., Que F.G., Gores G.J., and LaRusso N.F. Glutathione depletion is associated with decreased Bcl-2 expression and increased apoptosis in cholangiocytes. Am. J. Physiol. 275 4 Pt 1 (1998) G749-G757
34. Chai Y.C., Hoppe G., and Sears J. Reversal of protein S-glutathiolation by glutaredoxin in the retinal pigment epithelium. Exp. Eye Res. 76 (2003) 155-159
35. Chenais B., Andriollo M., Guiraud P., Belhoussine R., and Jeannesson P. Oxidative stress involvement in chemically induced differentiation of K562 cells. Free Radical Biol. Med. 28 (2000) 18-27
36. Chiarugi P., and Cirri P. Redox regulation of protein tyrosine phosphatases during receptor tyrosine kinase signal transduction. Trends Biochem. Sci. 28 (2003) 509-514
37. Chiba T., Takahashi S., Sato N., Ishii S., and Kikuchi K. Fas-mediated apoptosis is modulated by intracellular glutathione in human T-cells. Eur. J. Immunol. 26 5 (1996) 1164-1169
38. Chu X.Y., Strauss J.R., Mariano M.A., Li J., Newton D.J., Cai X., Wang R.W., Yabut J., Hartley D.P., Evans D.C., and Evers R. Characterization of mice lacking the multidrug resistance protein MRP2 (ABCC2). J. Pharmacol. Exp. Ther. 317 2 (2006) 579-589
39. Cole S.P., and Deeley R.G. Transport of glutathione and glutathione conjugates by MRP1. Trends Pharmacol. Sci. 27 (2006) 438-446
40. Cole S.P., Bhardwaj G., Gerlach J.H., Mackie J.E., Grant C.E., Almquist K.C., Stewart A.J., Kurz E.U., Duncan A.M., and Deeley R.G. Overexpression of a transporter gene in a multidrug-resistant human lung cancer cell line. Science 258 5088 (1992) 1650-1654
41. Conseil G., Deeley R.G., and Cole S.P. Polymorphisms of MRP1 (ABCC1) and related ATP-dependent drug transporters. Pharmacogenet. Genomics 15 8 (2005) 523-533
42. Csala M., Fulceri R., Mandl J., Benedetti A., and Bánhegyi G. Ryanodine receptor channel-dependent glutathione transport in the sarcoplasmic reticulum of skeletal muscle. Biochem. Biophys. Res. Commun. 287 3 (2001) 696-700
43. Cui Y., Konig J., Buchholz J.K., Spring H., Leier I., and Keppler D. Drug resistance and ATP-dependent conjugate transport mediated by the apical multidrug resistance protein, MRP2, permanently expressed in human and canine cells. Mol. Pharmacol. 55 5 (1999) 929-937
44. Dalle-Donne I., Rossi R., Giustarini D., Colombo R., and Milzani A. S-glutathionylation in protein redox regulation. Free Radical Biol. Med. 43 (2007) 883-898
45. Davison K., Cote S., Mader S., and Miller W.H. Glutathione depletion overcomes resistance to arsenic trioxide in arsenic-resistant cell lines. Leukemia 17 (2003) 931-940
46. Debbas V., Arai R.J., Ferderbar S., Schindler F., Stern A., and Monteiro H.P. Regulation of p21Waf1 expression and TNFalpha biosynthesis by glutathione modulators in PMA induced-THP1 differentiation: involvement of JNK and ERK pathways. Biochem. Biophys. Res. Commun. 363 (2007) 965-970
47. Deeley R.G., Westlake C., and Cole S.P. Transmembrane transport of endo- and xenobiotics by mammalian ATP-binding cassette multidrug resistance proteins. Physiol. Rev. 86 (2006) 849-899
48. Denk G.U., Soroka C.J., Takeyama Y., Chen W.S., Schuetz J.D., and Boyer J.L. Multidrug resistance-associated protein 4 is up-regulated in liver but down-regulated in kidney in obstructive cholestasis in the rat. J. Hepatol. 40 (2004) 585-591
49. Devadas S., Hinshaw J.A., Zaritskaya L., and Williams M.S. Fas-stimulated generation of reactive oxygen species or exogenous oxidative stress sensitize cells to Fas-mediated apoptosis. Free Radical Biol. Med. 35 6 (2003) 648-661
50. Dietrich J., Han R., Yang Y., Mayer-Proschel M., and Noble M. CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J. Biol. 5 (2006) 22
51. Dijkstra M., Kuipers F., Havinga R., Smit E.P., and Vonk R.J. Bile secretion of trace elements in rats with a congenital defect in hepatobiliary transport of glutathione. Pediatr. Res. 28 4 (1990) 339-343
52. Dinkova-Kostova A.T., Holtzclaw W.D., Cole R.N., Itoh K., Wakabayashi N., Katoh Y., Yamamoto M., and Talalay P. Direct evidence that sulfhydryl groups of Keap1 are the sensors regulating induction of phase 2 enzymes that protect against carcinogens and oxidants. Proc. Natl. Acad. Sci. USA 99 (2002) 11908-11913
53. Dreuw A., Hermanns H.M., Heise R., Joussen S., Rodríguez F., Marquardt Y., Jugert F., Merk H.F., Heinrich P.C., and Baron J.M. Interleukin-6-type cytokines upregulate expression of multidrug resistance-associated proteins in NHEK and dermal fibroblasts. J. Invest. Dermatol. 124 1 (2005) 28-37
54. Duan D.Y., Liu L.L., Bozeat N., Huang Z.M., Xiang S.Y., Wang G.L., Ye L., and Hume J.R. Functional role of anion channels in cardiac diseases. Acta Pharmacol. Sinica 26 3 (2005) 265-278
55. Ellerby L.M., Ellerby H.M., Park S.M., Holleran A.L., Murphy A.N., Fiskum G., Kane D.J., Testa M.P., Kayalar C., and Bredesen D.E. Shift of the cellular oxidation-reduction potential in neural cells expressing Bcl-2. J. Neurochem. 67 3 (1996) 1259-1267
56. Englund G., Rorsman F., Rönnblom A., Karlbom U., Lazorova L., Gråsjö J., Kindmark A., and Artursson P. Regional levels of drug transporters along the human intestinal tract: co-expression of ABC and SLC transporters and comparison with Caco-2 cells. Eur. J. Pharm. Sci. 29 3-4 (2006) 269-277
57. Esposito F., Agosti V., Morrone G., Morra F., Cuomo C., Russo T., Venuta S., and Cimino F. Inhibition of the differentiation of human myeloid cell lines by redox changes induced through glutathione depletion. Biochem. J. 301 Pt 3 (1994) 649-653
58. Evers R., de Haas M., Sparidans R., Beijnen J., Wielinga P.R., Lankelma J., and Borst P. Vinblastine and sulfinpyrazone export by the multidrug resistance protein MRP2 is associated with glutathione export. Br. J. Cancer 83 3 (2000) 375-383
59. Fadeel B., and Orrenius S. Apoptosis: a basic biological phenomenon with wide-ranging implications in human disease. J. Int. Med. 258 6 (2005) 479-517
60. Fernandez-Checa J.C., and Kaplowitz N. Hepatic mitochondrial glutathione: transport and role in disease and toxicity. Toxicol. Appl. Pharmacol. 204 3 (2005) 263-273
61. Fernandez-Checa J.C., Takikawa H., Horie T., Ookhtens M., and Kaplowitz N. Canalicular transport of reduced glutathione in normal and mutant Eisai hyperbilirubinemic rats. J. Biol. Chem. 267 3 (1992) 1667-1673
62. Fidelus R.K., Ginouves P., Lawrence D., and Tsan M.F. Modulation of intracellular glutathione concentrations alters lymphocyte activation and proliferation. Exp. Cell Res. 170 2 (1987) 269-275
63. Filomeni G., Rotilio G., and Ciriolo M.R. Disulfide relays and phosphorylative cascades: partners in redox-mediated signaling pathways. Cell Death Differen. 12 (2005) 1555-1563
64. Forman H.J., Fukuto J.M., and Torres M. Redox signaling: thiol chemistry defines which reactive oxygen and nitrogen species can act as second messengers. Am. J. Physiol. Cell Physiol. 287 (2004) C246-C256
65. Franco R., and Cidlowski J.A. 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 40 (2006) 29542-29557
66. Franco R., Panayiotidis M.I., and Cidlowski J.A. Glutathione depletion is necessary for apoptosis in lymphoid cells independent of reactive oxygen species formation. J. Biol. Chem. 282 42 (2007) 30452-30465
67. Fratelli M., Goodwin L.O., Orom U.A., Lombardi S., Tonelli R., Mengozzi M., and Ghezzi P. Gene expression profiling reveals a signaling role of glutathione in redox regulation. Proc. Natl. Acad. Sci. USA 102 (2005) 13998-14003
68. Frey I.M., Rubio-Aliaga I., Siewert A., Sailer D., Drobyshev A., Beckers J., de Angelis M.H., Aubert J., Bar Hen A., Fiehn O., Eichinger H.M., and Daniel H. Profiling at mRNA, protein, and metabolite levels reveals alterations in renal amino acid handling and glutathione metabolism in kidney tissue of Pept2-/- mice. Physiol. Genomics 28 3 (2007) 301-310
69. Friesen C., Kiess Y., and Debatin K.M. A critical role of glutathione in determining apoptosis sensitivity and resistance in leukemia cells. Cell Death Differen. 1 Suppl. 1 (2004) S73-S85
70. Gao L., Kim K.J., Yankaskas J.R., and Forman H.J. Abnormal glutathione transport in cystic fibrosis airway epithelia. Am. J. Physiol. 277 (1999) L113-L118
71. Gao L., Broughman J.R., Iwamoto T., Tomich J.M., Venglarik C.J., and Forman H.J. Synthetic chloride channel restores glutathione secretion in cystic fibrosis airway epithelia. Am. J. Physiol. Lung Cell Mol. Physiol. 281 1 (2001) L24-L30
72. Gekeler V., Ise W., Sanders K.H., Ulrich W.R., and Beck J. The leukotriene LTD4 receptor antagonist MK571 specifically modulates MRP associated multidrug resistance. Biochem. Biophys. Res. Commun. 208 1 (1995) 345-352
73. Ghezzi P. Regulation of protein function by glutathionylation. Free Radical Res. 39 (2005) 573-580
74. Ghezzi P., and Di Simplicio P. Glutathionylation pathways in drug response. Curr. Opin. Pharmacol. 7 4 (2007) 398-403
75. Ghezzi P., Bonetto V., and Fratelli M. Thiol-disulfide balance: from the concept of oxidative stress to that of redox regulation. Antioxid. Redox Signal. 7 (2005) 964-972
76. Ghibelli L., Coppola S., Rotilio G., Lafavia E., Maresca V., and Ciriolo M.R. Non-oxidative loss of glutathione in apoptosis via GSH extrusion. Biochem. Biophys. Res. Commun. 216 (1995) 313-320
77. Ghibelli L., Fanelli C., Rotilio G., Lafavia E., Coppola S., Colussi C., Civitareale P., and Ciriolo M.R. Rescue of cells from apoptosis by inhibition of active GSH extrusion. FASEB J. 12 (1998) 479-486
78. Giustarini D., Rossi R., Milzani A., Colombo R., and Dalle-Donne I. S-glutathionylation: from redox regulation of protein functions to human diseases. J. Cell. Mol. Med. 8 (2004) 201-212
79. Hall A.G. Review: the role of glutathione in the regulation of apoptosis. Eur. J. Clin. Invest. 29 (1999) 238-245
80. Hammond C.L., Lee T.K., and Ballatori N. Novel roles for glutathione in gene expression, cell death, and membrane transport of organic solutes. J. Hepatol. 34 6 (2001) 946-954
81. Hammond C.L., Madejczyk M.S., and Ballatori N. Activation of plasma membrane reduced glutathione transport in death receptor apoptosis of HepG2 cells. Toxicol. Appl. Pharmacol. 195 1 (2004) 12-22
82. Hammond C.L., Marchan R., Krance S.M., and Ballatori N. Glutathione export during apoptosis requires functional multidrug resistance-associated proteins. J. Biol. Chem. 282 (2007) 14337-14347
83. Hansen J.M., Carney E.W., and Harris C. Altered differentiation in rat and rabbit limb bud micromass cultures by glutathione modulating agents. Free Radical Biol. Med. 31 (2001) 1582-1592
84. Haouzi D., Lekehal M., Tinel M., Vadrot N., Caussanel L., Lettéron P., Moreau A., Feldmann G., Fau D., and Pessayre D. Prolonged, but not acute, glutathione depletion promotes Fas-mediated mitochondrial permeability transition and apoptosis in mice. Hepatology 33 (2001) 1181-1188
85. He Y.Y., Huang J.L., Ramirez D.C., and Chignell C.F. Role of reduced glutathione efflux in apoptosis of immortalized human keratinocytes induced by UVA. J. Biol. Chem. 278 10 (2003) 8058-8064
86. Henmi K., Tsuboi S., Demura T., Fukuda H., Iwabuchi M., and Ogawa K.I. A possible role of glutathione and glutathione disulfide in tracheary element differentiation in the cultured mesophyll cells of Zinnia elegans. Plant Cell Physiol. 42 (2001) 673-676
87. Hihnala S., Kujala M., Toppari J., Kere J., Holmberg C., and Höglund P. Expression of SLC26A3, CFTR and NHE3 in the human male reproductive tract: role in male subfertility caused by congenital chloride diarrhoea. Mol. Hum. Reprod. 12 2 (2006) 107-111
88. Hinchman C.A., and Ballatori N. Glutathione-degrading capacities of liver and kidney in different species. Biochem. Pharmacol. 40 5 (1990) 1131-1135
89. Hinchman C.A., and Ballatori N. Glutathione conjugation and conversion to mercapturic acids can occur as an intrahepatic process. J. Toxicol. Environ. Health 41 (1994) 387-409
90. Hinchman C.A., Matsumoto H., Simmons T.W., and Ballatori N. Intrahepatic conversion of a glutathione conjugate to its mercapturic acid. J. Biol. Chem. 266 (1991) 22179-22185
91. Hinchman C.A., Truong A.T., and Ballatori N. Hepatic uptake of intact glutathione S-conjugate, inhibition by organic anions, and sinusoidal catabolism. Am. J. Physiol. 265 (1993) G547-G554
92. Hinchman C.A., Rebbeor J.F., and Ballatori N. Efficient hepatic uptake and concentrative biliary excretion of a mercapturic acid. Am. J. Physiol. 275 (1998) G612-G619
93. Huh Y.J., Kim J.M., Kim H., Song H., So H., Lee S.Y., Kwon S.B., Kim H.J., Kim H.H., Lee S.H., Choi Y., Chung S.C., Jeong D.W., and Min B.M. Regulation of osteoclast differentiation by the redox-dependent modulation of nuclear import of transcription factors. Cell Death Differen. 13 7 (2005) 1138-1146
94. Iemata M., Takarada T., Hinoi E., Taniura H., and Yoneda Y. Suppression by glutamate of proliferative activity through glutathione depletion mediated by the cystine/glutamate antiporter in mesenchymal C3H10T1/2 stem cells. J. Cell. Physiol. 213 (2007) 721-729
95. Ignarro L.J. Nitric oxide. A novel signal transduction mechanism for transcellular communication. Hypertension 16 (1990) 477-483
96. Ikuma M., and Welsh M.J. Regulation of CFTR Cl-channel gating by ATP binding and hydrolysis. Proc. Natl. Acad. Sci. USA 97 (2000) 8675-8680
97. Ilias A., Urban Z., Seidl T.L., Le Saux O., Sinko E., Boyd C.D., Sarkadi B., and Varadi A. Loss of ATP-dependent transport activity in pseudoxanthoma elasticum-associated mutants of human ABCC6 (MRP6). J. Biol. Chem. 277 (2002) 16860-16867
98. Jansen P.L., Peters W.H., and Lamers W.H. Hereditary chronic conjugated hyperbilirubinemia in mutant rats caused by defective hepatic anion transport. Hepatology 5 4 (1985) 573-579
99. Jedlitschky G., Leier I., Buchholz U., Center M., and Keppler D. ATP-dependent transport of glutathione S-conjugates by the multidrug resistance-associated protein. Cancer Res. 54 18 (1994) 4833-4836
100. Jedlitschky G., Hoffmann U., and Kroemer H.K. Structure and function of the MRP2 (ABCC2) protein and its role in drug disposition. Exp. Opin. Drug Metab. Toxicol. 2 3 (2006) 351-366
101. Jun J.H., Lee S.H., Kwak H.B., Lee Z.H., Seo S.B., Woo K.M., Ryoo H.M., Kim G.S., and Baek J.H. N-acetylcysteine stimulates osteoblastic differentiation of mouse calvarial cells. J. Cell. Biochem. 103 4 (2008) 1246-1255
102. Kang Y.J., Feng Y., and Hatcher E.L. Glutathione stimulates A549 cell proliferation in glutamine-deficient culture: the effect of glutamate supplementation. J. Cell. Physiol. 161 (1994) 589-596
103. Kawabe T., Chen Z.S., Wada M., Uchiumi T., Ono M., Akiyama S., and Kuwano M. Enhanced transport of anticancer agents and leukotriene C4 by the human canalicular multispecific organic anion transporter (cMOAT/MRP2). FEBS Lett. 456 2 (1999) 327-331
104. Keppler D., Leier I., and Jedlitschky G. Transport of glutathione conjugates and glucuronides by the multidrug resistance proteins MRP1 and MRP2. Biol. Chem. 378 (1997) 787-791
105. Kim K.Y., Rhim T., Choi I., and Kim S.S. N-acetylcysteine induces cell cycle arrest in hepatic stellate cells through its reducing activity. J. Biol. Chem. 276 (2001) 40591-40598
106. Kim J.M., Kim H., Kwon S.B., Lee S.Y., Chung S.C., Jeong D.W., and Min B.M. Intracellular glutathione status regulates mouse bone marrow monocyte-derived macrophage differentiation and phagocytic activity. Biochem. Biophys. Res. Commun. 325 (2004) 101-108
107. Klein M., Mamnun Y.M., Eggmann T., Schuller C., Wolfger H., Martinoia E., and Kuchler K. The ATP-binding cassette (ABC) transporter Bpt1p mediates vacuolar sequestration of glutathione conjugates in yeast. FEBS Lett. 520 (2002) 63-67
108. Kogan I., Ramjeesingh M., Huan L.J., Wang Y., and Bear C.E. Perturbation of the pore of the cystic fibrosis transmembrane conductance regulator (CFTR) inhibits its ATPase activity. J. Biol. Chem. 276 (2001) 11575-11581
109. Kogan I., Ramjeesingh M., Li C., Kidd J.F., Wang Y., Leslie E.M., Cole S.P., and Bear C.E. CFTR directly mediates nucleotide-regulated glutathione flux. EMBO J. 22 (2003) 1981-1989
110. Koike K., Kawabe T., Tanaka T., Toh S., Uchiumi T., Wada M., Akiyama S., Ono M., and Kuwano M. A canalicular multispecific organic anion transporter (cMOAT) antisense cDNA enhances drug sensitivity in human hepatic cancer cells. Cancer Res. 57 24 (1997) 5475-5479
111. Kolberg A., Rosa T.G., Puhl M.T., Scola G., a Janner D., Maslinkiewicz A., Lagranha D.J., Heck T.G., Curi R., and de Bittencourt Jr. P.I. Low expression of MRP1/GS-X pump ATPase in lymphocytes of Walker 256 tumour-bearing rats is associated with cyclopentenone prostaglandin accumulation and cancer immunodeficiency. Cell. Biochem. Funct. 24 1 (2006) 23-39
112. König J., Nies A.T., Cui Y., Leier I., and Keppler D. Conjugate export pumps of the multidrug resistance protein (MRP) family: localization, substrate specificity, and MRP2-mediated drug resistance. Biochim. Biophys. Acta 1461 2 (1999) 377-394
113. Kool M., de Haas M., Scheffer G.L., Scheper R.J., van Eijk M.J., Juijn J.A., Baas F., and Borst P. Analysis of expression of cMOAT (MRP2), MRP3, MRP4, and MRP5, homologues of the multidrug resistance-associated protein gene (MRP1), in human cancer cell lines. Cancer Res. 57 (1997) 3537-3547
114. Krause M.S., Oliveira Jr. L.P., Silveira E.M., Vianna D.R., Rossato J.S., Almeida B.S., Rodrigues M.F., Fernandes A.J., Costa J.A., Curi R., and de Bittencourt Jr. P.I. MRP1/GS-X pump ATPase expression: is this the explanation for the cytoprotection of the heart against oxidative stress-induced redox imbalance in comparison to skeletal muscle cells?. Cell. Biochem. Funct. 25 (2007) 23-32
115. Kruh G.D., Guo Y., Hopper-Borge E., Belinsky M.G., and Chen Z. ABCC10, ABCC11, and ABCC12. Pflugers Arch. 453 (2007) 675-684
116. Kruh G.D., Belinsky M.G., Gallo J.M., and Lee K. Physiological and pharmacological functions of Mrp2, Mrp3 and Mrp4 as determined from recent studies on gene-disrupted mice. Cancer Metastasis Rev. 26 1 (2007) 5-14
117. Kurisu H., Kamisaka K., Koyo T., Yamasuge S., Igarashi H., Maezawa H., Uesugi T., and Tagaya O. Organic anion transport study in mutant rats with autosomal recessive conjugated hyperbilirubinemia. Life Sci. 49 14 (1991) 1003-1011
118. Laberge R.M., Karwatsky J., Lincoln M.C., Leimanis M.L., and Georges E. Modulation of GSH levels in ABCC1 expressing tumor cells triggers apoptosis through oxidative stress. Biochem. Pharmacol. 73 11 (2007) 1727-1737
119. Lacueva J., Perez-Ramos M., Soto J.L., Oliver I., Andrada E., Medrano J., Perez-Vazquez T., Arroyo A., Carrato A., Ferragut J.A., and Calpena R. Multidrug resistance-associated protein (MRP1) gene is strongly expressed in gastric carcinomas. Analysis by immunohistochemistry and real-time quantitative RT-PCR. Histopathology 46 4 (2005) 389-395
120. Lai L., and Tan T.M. Role of glutathione in the multidrug resistance protein 4 (MRP4/ABCC4)-mediated efflux of cAMP and resistance to purine analogues. Biochem. J. 361 (2002) 497-503
121. Lash L.H. Role of glutathione transport processes in kidney function. Toxicol. Appl. Pharmacol. 204 3 (2005) 329-342
122. Lash L.H. Mitochondrial glutathione transport: physiological, pathological and toxicological implications. Chem. Biol. Interact. 163 1-2 (2006) 54-67
123. Lautier D., Canitrot Y., Deeley R.G., and Cole S.P. Multidrug resistance mediated by the multidrug resistance protein (MRP) gene. Biochem. Pharmacol. 52 7 (1996) 967-977
124. Lee K., Belinsky M.G., Bell D.W., Testa J.R., and Kruh G.D. Isolation of MOAT-B, a widely expressed multidrug resistance-associated protein/canalicular multispecific organic anion transporter-related transporter. Cancer Res. 58 (1998) 2741-2747
125. Lee K., Klein-Szanto A.J., and Kruh G.D. Analysis of the MRP4 drug resistance profile in transfected NIH3T3 cells. J. Natl. Cancer Inst. 92 (2000) 1934-1940
126. Leier I., Jedlitschky G., Buchholz U., Cole S.P., Deeley R.G., and Keppler D. The MRP gene encodes an ATP-dependent export pump for leukotriene C4 and structurally related conjugates. J. Biol. Chem. 269 45 (1994) 27807-27810
127. Leslie E.M., Ito K., Upadhyaya P., Hecht S.S., Deeley R.G., and Cole S.P. Transport of the beta-O-glucuronide conjugate of the tobacco-specific carcinogen 4-(methylnitrosamino)-1-(3-pyridyl)-1-butanol (NNAL) by the multidrug resistance protein 1 (MRP1). Requirement for glutathione or a non-sulfur-containing analog. J. Biol. Chem. 276 30 (2001) 27846-27854
128. Leslie E.M., Deeley R.G., and Cole S.P. Toxicological relevance of the multidrug resistance protein 1, MRP1 (ABCC1) and related transporters. Toxicology 167 1 (2001) 3-23
129. Leslie E.M., Bowers R.J., Deeley R.G., and Cole S.P. Structural requirements for functional interaction of glutathione tripeptide analogs with the human multidrug resistance protein 1 (MRP1). J. Pharmacol. Exp. Ther. 304 2 (2003) 643-653
130. Leslie E.M., Deeley R.G., and Cole S.P. Multidrug resistance proteins: a role of P-glycoprotein, MRP1, MRP2, and BCRP (ABCG2) in tissue defense. Toxicol. Appl. Pharmacol. 204 (2005) 216-237
131. Li C., Ramjeesingh M., Wang W., Garami E., Hewryk M., Lee D., Rommens J.M., Galley K., and Bear C.E. ATPase activity of the cystic fibrosis transmembrane conductance regulator. J. Biol. Chem. 271 (1996) 28463-28468
132. Li L., Lee T.K., and Ballatori N. Functional re-evaluation of the putative glutathione transporters, RcGshT and RsGshT. Yale J. Biol. Med. 70 (1997) 301-310
133. Li L., Lee T.K., Meier P.J., 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 26 (1998) 16184-16191
134. Lillig C.H., Berndt C., and Holmgren A. Glutaredoxin systems. Biochim. Biophys. Acta. 1780 11 (2008) 1304-1317
135. Lind C., Gerdes R., Hamnell Y., Schuppe-Koistinen I., von Lowenhielm H.B., Holmgren A., and Cotgreave I.A. Identification of S-glutathionylated cellular proteins during oxidative stress and constitutive metabolism by affinity purification and proteomic analysis. Arch. Biochem. Biophys. 406 (2002) 229-240
136. Linsdell P., and Hanrahan J.W. Glutathione permeability of CFTR. Am. J. Physiol. 275 (1998) C323-C326
137. Linsdell P., and Hanrahan J.W. Substrates of multidrug resistance-associated proteins block the cystic fibrosis transmembrane conductance regulator chloride channel. Br. J. Pharmacol. 126 (1999) 1471-1477
138. Loe D.W., Almquist K.C., Deeley R.G., and Cole S.P. Multidrug resistance protein (MRP)-mediated transport of leukotriene C4 and chemotherapeutic agents in membrane vesicles. Demonstration of glutathione-dependent vincristine transport. J. Biol. Chem. 271 16 (1996) 9675-9682
139. Loe D.W., Stewart R.K., Massey T.E., Deeley R.G., and Cole S.P. ATP-dependent transport of aflatoxin B1 and its glutathione conjugates by the product of the multidrug resistance protein (MRP) gene. Mol. Pharmacol. 51 6 (1997) 1034-1041
140. Loe D.W., Deeley R.G., and Cole S.P. Characterization of vincristine transport by the M(r) 190,000 multidrug resistance protein (MRP): evidence for cotransport with reduced glutathione. Cancer Res. 58 22 (1998) 5130-5136
141. Loe D.W., Deeley R.G., and Cole S.P. Verapamil stimulates glutathione transport by the 190-kDa multidrug resistance protein 1 (MRP1). J. Pharmacol. Exp. Ther. 293 2 (2000) 530-538
142. Lorico A., Rappa G., Finch R.A., Yang D., Flavell R.A., and Sartorelli A.C. Disruption of the murine MRP (multidrug resistance protein) gene leads to increased sensitivity to etoposide (VP-16) and increased levels of glutathione. Cancer Res. 57 (1997) 5238-5242
143. Mahagita C., Grassl S.M., Piyachaturawat P., and Ballatori N. Human organic anion transporter 1B1 and 1B3 function as bidirectional carriers and do not mediate GSH-bile acid cotransport. Am. J. Physiol. Gastrointest. Liver Physiol. 293 1 (2007) G271-G278
144. Mao Q., Deeley R.G., and Cole S.P. Functional reconstitution of substrate transport by purified multidrug resistance protein MRP1 (ABCC1) in phospholipid vesicles. J. Biol. Chem. 275 44 (2000) 34166-34172
145. Marchan, R., Hammond, C.L., Ballatori, N., in press. Multidrug resistance-associated protein 1 as a major mediator of basal and apoptotic glutathione release. Biochim. Biophys. Acta.
146. Mayer M., and Noble M. N-acetyl-l-cysteine is a pluripotent protector against cell death and enhancer of trophic factor-mediated cell survival in vitro. Proc. Natl. Acad. Sci. USA 91 (1994) 7496-7500
147. McAleer M.A., Breen M.A., White N.L., and Matthews N. PABC11 (also known as MOAT-C and MRP5), a member of the ABC family of proteins, has anion transporter activity but does not confer multidrug resistance when overexpressed in human embryonic kidney 293 cells. J. Biol. Chem. 274 33 (1999) 23541-23548
148. McCarthy V.A., and Harris A. The CFTR gene and regulation of its expression. Pediatr. Pulmonol. 40 1 (2005) 1-8
149. Meister A., and Anderson M.E. Glutathione. Annu. Rev. Biochem. 52 (1983) 711-760
150. Meister A., and Tate S.S. Glutathione and related γ-glutamyl compounds: biosynthesis and utilization. Ann. Rev. Biochem. 45 (1976) 559-604
151. Merad-Boudia M., Nicole A., Santiard-Baron D., Saille C., and Ceballos-Picot I. Mitochondrial impairment as an early event in the process of apoptosis induced by glutathione depletion in neuronal cells: relevance to Parkinson's disease. Biochem. Pharmacol. 56 5 (1998) 645-655
152. Meredith M.J., Cusick C.L., Soltaninassab S., Sekhar K.S., Lu S., and Freeman M.L. Expression of Bcl-2 increases intracellular glutathione by inhibiting methionine-dependent GSH efflux. Biochem. Biophys. Res. Commun. 248 3 (1998) 458-463
153. Minich T., Riemer J., Schulz J.B., Wielinga P., Wijnholds J., and Dringen R. The multidrug resistance protein 1 (Mrp1), but not Mrp5, mediates export of glutathione and glutathione disulfide from brain astrocytes. J. Neurochem. 97 2 (2006) 373-384
154. Morales M.M., Carroll T.P., Morita T., Schwiebert E.M., Devuyst O., Wilson P.D., Lopes A.G., Stanton B.A., Dietz H.C., Cutting G.R., and Guggino W.B. Both the wild type and a functional isoform of CFTR are expressed in kidney. Am. J. Physiol. 270 6 Pt 2 (1996) F1038-F1048
155. Morrow C.S., Peklak-Scott C., Bishwokarma B., Kute T.E., Smitherman P.K., and Townsend A.J. Multidrug resistance protein 1 (MRP1, ABCC1) mediates resistance to mitoxantrone via glutathione-dependent drug efflux. Mol. Pharmacol. 69 4 (2006) 1499-1505
156. Mueller C.F., Widder J.D., McNally J.S., McCann L., Jones D.P., and Harrison D.G. The role of the multidrug resistance protein-1 in modulation of endothelial cell oxidative stress. Circ. Res. 97 7 (2005) 637-644
157. Mylona P., Glazier J.D., Greenwood S.L., Sides M.K., and Sibley C.P. Expression of the cystic fibrosis (CF) and multidrug resistance (MDR1) genes during development and differentiation in the human placenta. Mol. Hum. Reprod. 2 9 (1996) 693-698
158. Nies A.T., and Keppler D. The apical conjugate efflux pump ABCC2 (MRP2). Pflugers Arch. 453 5 (2007) 643-659
159. Ortega A., Ferrer P., Carretero J., Obrador E., Asensi M., Pellicer J.A., and Estrela J.M. Down-regulation of glutathione and Bcl-2 synthesis in mouse B16 melanoma cells avoids their survival during interaction with the vascular endothelium. J. Biol. Chem. 278 41 (2003) 39591-39599
160. Oude Elferink R.P., de Haan J., Lambert K.J., Hagey L.R., Hofmann A.F., and Jansen P.L. Selective hepatobiliary transport of nordeoxycholate side chain conjugates in mutant rats with a canalicular transport defect. Hepatology 9 6 (1989) 861-865
161. Paranjpe A., Cacalano N.A., Hume W.R., and Jewett A. N-acetylcysteine protects dental pulp stromal cells from HEMA-induced apoptosis by inducing differentiation of the cells. Free Radical Biol. Med. 43 (2007) 1394-1408
162. Parasassi T., Brunelli R., Bracci-Laudiero L., Greco G., Gustafsson A.C., Krasnowska E.K., Lundeberg J., Lundeberg T., Pittaluga E., Romano M.C., and Serafino A. Differentiation of normal and cancer cells induced by sulfhydryl reduction: biochemical and molecular mechanisms. Cell Death Differen. 12 (2005) 1285-1296
163. Patrizio P., and Salameh W.A. Expression of the cystic fibrosis transmembrane conductance regulator (CFTR) mRNA in normal and pathological adult human epididymis. J. Reprod. Fertil. Suppl. 53 (1998) 261-270
164. Paulusma C.C., van Geer M.A., Evers R., Heijn M., Ottenhoff R., Borst P., and Oude Elferink R.P. Canalicular multispecific organic anion transporter/multidrug resistance protein 2 mediates low-affinity transport of reduced glutathione. Biochem. J. 338 Pt 2 (1999) 393-401
165. Qian Y.M., Song W.C., Cui H., Cole S.P., and Deeley R.G. Glutathione stimulates sulfated estrogen transport by multidrug resistance protein 1. J. Biol. Chem. 276 9 (2001) 6404-6411
166. Rappa G., Lorico A., Flavell R.A., and Sartorelli A.C. Evidence that the multidrug resistance protein (MRP) functions as a co-transporter of glutathione and natural product toxins. Cancer Res. 57 23 (1997) 5232-5237
167. Rebbeor J.F., Connolly G.C., Dumont M.E., and Ballatori N. ATP-Dependent transport of reduced glutathione in yeast secretory vesicles. Biochem. J. 334 (1998) 723-729
168. Rebbeor J.F., Connolly G.C., Dumont M.E., and Ballatori N. ATP-Dependent transport of reduced glutathione on YCF1, the yeast orthologue of mammalian multidrug resistance associated proteins. J. Biol. Chem. 273 (1998) 33449-33454
169. Rebbeor J.F., Connolly G.C., Henson J.H., Boyer J.L., and Ballatori N. ATP-dependent GSH and glutathione S-conjugate transport in skate liver: role of an Mrp functional homologue. Am. J. Physiol. 279 (2000) G417-G425
170. Rebbeor J.F., Connolly G.C., and Ballatori N. Inhibition of Mrp2- and Ycf1p-mediated transport by reducing agents: evidence for GSH transport on rat Mrp2. Biochim. Biophys. Acta 1559 2 (2002) 171-178
171. Reed J.C. Apoptosis-based therapies. Nat. Rev. Drug Discov. 1 2 (2002) 111-121
172. Renes J., de Vries E.G., Nienhuis E.F., Jansen P.L., and Muller M. ATP- and glutathione-dependent transport of chemotherapeutic drugs by the multidrug resistance protein MRP1. Br. J. Pharmacol. 126 3 (1999) 681-688
173. Reynaert N.L., Ckless K., Guala A.S., Wouters E.F., van der Vliet A., and Janssen-Heininger Y.M. In situ detection of S-glutathionylated proteins following glutaredoxin-1 catalyzed cysteine derivatization. Biochim. Biophys. Acta 1760 (2006) 380-387
174. Rius M., Nies A.T., Hummel-Eisenbeiss J., Jedlitschky G., and Keppler D. Cotransport of reduced glutathione with bile salts by MRP4 (ABCC4) localized to the basolateral hepatocyte membrane. Hepatology 38 2 (2003) 374-384
175. Rius M., Hummel-Eisenbeiss J., Hofmann A.F., and Keppler D. Substrate specificity of human ABCC4 (MRP4)-mediated cotransport of bile acids and reduced glutathione. Am. J. Phys. 290 (2006) G640-G649
176. Rius M., Hummel-Eisenbeiss J., and Keppler D. ATP-dependent transport of leukotrienes B4 and C4 by the multidrug resistance protein ABCC4 (MRP4). J. Pharmacol. Exp. Ther. 324 (2008) 86-94
177. Ronaldson, P.T., Bendayan, R., 2008. HIV-1 viral envelope glycoprotein gp120 produces oxidative stress and regulates the functional expression of multidrug resistance protein-1 (Mrp1) in glial cells. J. Neurochem. (Epub ahead of print).
178. Roum J.H., Buhl R., McElvaney N.G., Borok Z., and Crystal R.G. Systemic deficiency of glutathione in cystic fibrosis. J. Appl. Physiol. 75 (1993) 2419-2424
179. Salerno M., and Garnier-Suillerot A. Kinetics of glutathione and daunorubicin efflux from multidrug resistance protein overexpressing small-cell lung cancer cells. Eur. J. Pharmacol. 421 1 (2001) 1-9
180. Salmeen A., and Barford D. Functions and mechanisms of redox regulation of cysteine-based phosphatases. Antioxid. Redox Signal. 7 (2005) 560-577
181. Sauer H., Wartenberg M., and Hescheler J. Reactive oxygen species as intracellular messengers during cell growth and differentiation. Cell Physiol. Biochem. 11 (2001) 173-186
182. Scheffer G.L., Kool M., de Haas M., de Vree J.M., Pijnenborg A.C., Bosman D.K., Elferink R.P., van der Valk P., Borst P., and Scheper R.J. Tissue distribution and induction of human multidrug resistant protein 3. Lab Invest. 82 2 (2002) 193-201
183. Schneider E., Yamazaki H., Sinha B.K., and Cowan K.H. Buthionine sulphoximine-mediated sensitisation of etoposide-resistant human breast cancer MCF7 cells overexpressing the multidrug resistance-associated protein involves increased drug accumulation. Br. J. Cancer 71 4 (1995) 738-743
184. Schuetz E.G., Strom S., Yasuda K., Lecureur V., Assem M., Brimer C., Lamba J., Kim R.B., Ramachandran V., Komoroski B.J., Venkataramanan R., Cai H., Sinal C.J., Gonzalez F.J., and Schuetz J.D. Disrupted bile acid homeostasis reveals an unexpected interaction among nuclear hormone receptors, transporters, and cytochrome P450. J. Biol. Chem. 276 (2001) 39411-39418
185. Sen C.K. Cellular thiols and redox-regulated signal transduction. Curr. Top. Cell. Regul. 36 (2000) 1-30
186. Serrano M.A., Macias R.I., Briz O., Monte M.J., Blazquez A.G., Williamson C., Kubitz R., and Marin J.J. Expression in human trophoblast and choriocarcinoma cell lines, BeWo, Jeg-3 and JAr of genes involved in the hepatobiliary-like excretory function of the placenta. Placenta 28 2-3 (2007) 107-117
187. Sharma K.G., Mason D.L., Liu G., Rea P.A., Bachhawat A.K., and Michaelis S. Localization, regulation, and substrate transport properties of Bpt1p, a Saccharomyces cerevisiae MRP-type ABC transporter. Eukaryot. Cell 1 (2002) 391-400
188. Shaw J.P., and Chou I.N. Elevation of intracellular glutathione content associated with mitogenic stimulation of quiescent fibroblasts. J. Cell. Physiol. 129 (1986) 193-198
189. Shelton M.D., and Mieyal J.J. Regulation by reversible S-glutathionylation: molecular targets implicated in inflammatory diseases. Mol. Cells 25 3 (2008) 332-346
190. Sies H., Wahlländer A., Waydhas C., Soboll S., and Höberle D. Functions of intracellular glutathione in hepatic hydroperoxide and drug metabolism and the role of extracellular glutathione. Adv. Enzyme Regul. 18 (1980) 303-320
191. Simmons T.W., Hinchman C.A., and Ballatori N. Polarity of hepatic glutathione and glutathione S-conjugate efflux, and intraorgan mercapturic acid formation in the skate. Biochem. Pharmacol. 42 (1991) 2221-2228
192. Simmons T.W., Anders M.W., and Ballatori N. Cysteine and S-(1,2-dichlorovinyl)-l-cysteine transport in rat liver canalicular membrane vesicles: potential reabsorption mechanisms for biliary metabolites of glutathione and its S-conjugates. J. Pharmacol. Exp. Ther. 262 (1992) 1182-1188
193. Smith J., Ladi E., Mayer-Proschel M., and Noble M. Redox state is a central modulator of the balance between self-renewal and differentiation in a dividing glial precursor cell. Proc. Natl. Acad. Sci. USA 97 (2000) 10032-10037
194. Staal F.J., Roederer M., and Herzenberg L.A. Intracellular thiols regulate activation of nuclear factor kappa B and transcription of human immunodeficiency virus. Proc. Natl. Acad. Sci. USA 87 (1990) 9943-9947
195. Staal F.J., Anderson M.T., Staal G.E., Herzenberg L.A., and Gitler C. Redox regulation of signal transduction: tyrosine phosphorylation and calcium influx. Proc. Natl. Acad. Sci. USA 91 (1994) 3619-3622
196. Strong T.V., Boehm K., and Collins F.S. Localization of cystic fibrosis transmembrane conductance regulator mRNA in the human gastrointestinal tract by in situ hybridization. J. Clin. Invest. 93 1 (1994) 347-354
197. Suthanthiran M., Anderson M.E., Sharma V.K., and Meister A. Glutathione regulates activation-dependent DNA synthesis in highly purified normal human T lymphocytes stimulated via the CD2 and CD3 antigens. Proc. Natl. Acad. Sci. USA 87 (1990) 3343-3347
198. Suzuki H., and Sugiyama Y. Excretion of GSSG and glutathione conjugates mediated by MRP1 and cMOAT/MRP2. Sem. Liver Dis. 18 (1998) 359-376
199. Suzuki Y.J., Forman H.J., and Sevanian A. Oxidants as stimulators of signal transduction. Free Radical Biol. Med. 22 (1997) 269-285
200. Taipalensuu J., Törnblom H., Lindberg G., Einarsson C., Sjöqvist F., Melhus H., Garberg P., Sjöström B., Lundgren B., and Artursson P. Correlation of gene expression of ten drug efflux proteins of the ATP-binding cassette transporter family in normal human jejunum and in human intestinal epithelial Caco-2 cell monolayers. J. Pharmacol. Exp. Ther. 299 1 (2001) 164-170
201. Toh S., Wada M., Uchiumi T., Inokuchi A., Makino Y., Horie Y., Adachi Y., Sakisaka S., and Kuwano M. Genomic structure of the canalicular multispecific organic anion-transporter gene (MRP2/cMOAT) and mutations in the ATP-binding-cassette region in Dubin-Johnson syndrome. Am. J. Hum. Genet. 64 3 (1999) 739-746
202. Torky A.R., Stehfest E., Viehweger K., Taege C., and Foth H. Immuno-histochemical detection of MRPs in human lung cells in culture. Toxicology 207 3 (2005) 437-450
203. Townsend D.M. S-glutathionylation: indicator of cell stress and regulator of the unfolded protein response. Mol. Interv. 7 6 (2007) 313-324
204. Trauner M., Nathanson M.H., Mennone A., Rydberg S.A., and Boyer J.L. Nitric oxide donors stimulate bile flow and glutathione disulfide excretion independent of guanosine 3′, 5′-cyclic [corrected] monophosphate in the isolated perfused rat liver. Hepatology 25 2 (1997) 263-269
205. Trompier D., Chang X.B., Barattin R., t D'Hardemare 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 (2004) 4950-4956
206. van Aubel R.A., Koenderink J.B., Peters J.G., Van Os C.H., and Russel F.G. Mechanisms and interaction of vinblastine and reduced glutathione transport in membrane vesicles by the rabbit multidrug resistance protein Mrp2 expressed in insect cells. Mol. Pharmacol. 56 4 (1999) 714-719
207. van den Dobbelsteen D.J., Nobel C.S., Schlegel J., Cotgreave I.A., Orrenius S., and Slater A.F. Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J. Biol. Chem. 271 (1996) 15420-15427
208. Vanhoefer U., Cao S., Minderman H., Toth K., Skenderis II B.S., Slovak M.L., and Rustum Y.M. D, l-buthionine-(S, R)-sulfoximine potentiates in vivo the therapeutic efficacy of doxorubicin against multidrug resistance protein-expressing tumors. Clin. Cancer Res. 2 12 (1996) 1961-1968
209. Velsor L.W., van Heeckeren A., and Day B.J. Antioxidant imbalance in the lungs of cystic fibrosis transmembrane conductance regulator protein mutant mice. Am. J. Physiol. Lung Cell. Mol. Physiol. 281 (2001) L31-L38
210. Versantvoort C.H., Bagrij T., Wright K.A., and Twentyman P.R. On the relationship between the probenecid-sensitive transport of daunorubicin or calcein and the glutathione status of cells overexpressing the multidrug resistance-associated protein (MRP). Int. J. Cancer 63 6 (1995) 855-862
211. Vlachaki M.T., and Meyn R.E. ASTRO research fellowship: the role of BCL-2 and glutathione in an antioxidant pathway to prevent radiation-induced apoptosis. Int. J. Radiat. Oncol. Biol. Phys. 42 (1998) 185-190
212. Voehringer D.W. BCL-2 and glutathione: alterations in cellular redox state that regulate apoptosis sensitivity. Free Radical Biol. Med. 27 (1999) 945-950
213. Wada M., Toh S., Taniguchi K., Nakamura T., Uchiumi T., Kohno K., Yoshida I., Kimura A., Sakisaka S., Adachi Y., and Kuwano M. Mutations in the canilicular multispecific organic anion transporter (cMOAT) gene, a novel ABC transporter, in patients with hyperbilirubinemia II/Dubin-Johnson syndrome. Hum. Mol. Genet. 7 2 (1998) 203-207
214. Wang X. The expanding role of mitochondria in apoptosis. Genes Dev. 15 22 (2001) 2922-2933
215. Wang W., and Ballatori N. Endogenous glutathione conjugates: occurrence and biological functions. Pharmacol. Rev. 50 3 (1998) 335-356
216. Watts R.N., Hawkins C., Ponka P., and Richardson D.R. Nitrogen monoxide (NO)-mediated iron release from cells is linked to NO-induced glutathione efflux via multidrug resistance-associated protein 1. Proc. Natl. Acad. Sci. USA 103 20 (2006) 7670-7675
217. Widder J.D., Guzik T.J., Mueller C.F., Clempus R.E., Schmidt H.H., Dikalov S.I., Griendling K.K., Jones D.P., and Harrison D.G. Role of the multidrug resistance protein-1 in hypertension and vascular dysfunction caused by angiotensin II. Arterioscler. Thromb. Vasc. Biol. 27 (2007) 762-768
218. Wijnholds J., Mol C.A., van Deemter L., de Haas M., Scheffer G.L., Baas F., Beijnen J.H., Scheper R.J., Hatse S., De Clercq E., Balzarini J., and Borst P. Multidrug-resistance protein 5 is a multispecific organic anion transporter able to transport nucleotide analogs. Proc. Natl. Acad. Sci. USA 97 13 (2000) 7476-7481
219. Yi J.-R., Lu S., Fernandez-Checa J., and Kaplowitz N. Expression cloning of a rat hepatic reduced glutathione transporter with canalicular characteristics. J. Clin. Invest. 93 (1994) 1841-1845
220. Yi J.-R., Lu S., Fernandez-Checa J., and Kaplowitz N. Expression cloning of the cDNA for a polypeptide associated with rat hepatic sinusoidal reduced glutathione transport: characteristics and comparison with the canalicular transporter. Proc. Natl. Acad. Sci. USA 92 (1995) 1495-1499
221. Zaman G.J., Lankelma J., van Tellingen O., Beijnen J., Dekker H., Paulusma C., Oude Elferink R.P., Baas F., and Borst P. Role of glutathione in the export of compounds from cells by the multidrug-resistance-associated protein. Proc. Natl. Acad. Sci. USA 92 17 (1995) 7690-7694
222. Zelcer N., Reid G., Wielinga P., Kuil A., van der Heijden I., Schuetz J.D., and Borst P. Steroid and bile acid conjugates are substrates of human multidrug-resistance protein (MRP) 4 (ATP-binding cassette C4). Biochem. J. 371 Pt 2 (2003) 361-367
223. Ziegler D.M. Role of reversible oxidation-reduction of enzyme thiols-disulfides in metabolic regulation. Annu. Rev. Biochem. 54 (1985) 305-329
224. Zimmermann C., Gutmann H., Hruz P., Gutzwiller J.P., Beglinger C., and Drewe J. Mapping of multidrug resistance gene 1 and multidrug resistance-associated protein isoform 1 to 5 mRNA expression along the human intestinal tract. Drug Metab. Dispos. 33 2 (2005) 219-224
225. Zimmermann A.K., Loucks F.A., Schroeder E.K., Bouchard R.J., Tyler K.L., and Linseman D.A. Glutathione binding to the Bcl-2 homology-3 domain groove: a molecular basis for Bcl-2 antioxidant function at mitochondria. J. Biol. Chem. 282 40 (2007) 29296-29304