Regulation of hepatic glutathione synthesis: Current concepts and controversies

FASEB Journal

Volumn 13, Issue 10, 1999, Pages 1169-1183

  Lu, Shelly C ^a  

^a UNIVERSITY OF SOUTHERN CALIFORNIA   (United States)

Author keywords

Antioxidant; Cysteine availability; Detoxification; glutamylcysteine synthetase

Indexed keywords

ANTIOXIDANT; CYCLOHEXIMIDE; CYSTEINE; CYSTINE; DACTINOMYCIN; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; METHIONINE; SULFUR AMINO ACID;

ANIMAL TISSUE; ANTIOXIDANT ACTIVITY; CELL MEMBRANE TRANSPORT; CELL PROLIFERATION; DIABETES MELLITUS; DRUG RESISTANCE; ENZYME ACTIVITY; GENE EXPRESSION; GLUTATHIONE METABOLISM; HORMONAL REGULATION; LIVER METABOLISM; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; REVIEW; TUMOR CELL LINE;

ANIMALIA; MAMMALIA;

EID: 0033067354     PISSN: 08926638     EISSN: None     Source Type: Journal    
DOI: 10.1096/fasebj.13.10.1169     Document Type: Review

References (124)

1. DeLeve, L., and Kaplowitz, N. (1991) Glutathione metabolism and its role in hepatotoxicity. Pharmacol. Ther. 52, 287-305
2. Hwang, C., Sinsky, A. J., and Lodish, H. F. (1992) Oxidized redox state of glutathione in the endoplasmic reticulum. Science 257, 1496-1502
3. Meredith, M. J., and Reed, D. J. (1982) Status of the mitochondrial pool of glutathione in the isolated hepatocyte. J. Biol. Chem. 257, 3747-3753
4. Meister, A. (1988) Glutathione. In The Liver: Biology and Pathobiology, Second Edition (Aria, I. M., Jakoby, W. B., Popper, H., Schachter, D., and Shafritz, D. A., eds) pp. 401-417, Raven Press, New York
5. Suthanthiran, M., Anderson, M. E., Sharma, V. K., and Meister A. (1990) 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, 3343-3347
6. Hutter, D. E., Till, B. G., and Greene, J. J. (1997) Redox state changes in density-dependent regulation of proliferation. Exp. Cell Res. 232, 435-438
7. Fernández-Checa, J., Lu, S. C., Ookhtens, M., DeLeve, L., Runnegar, M., Yoshida, H., Saiki, H., Kannan, R., Garcia-Ruiz, C., Kuhlenkamp, J. F., and Kaplowitz, N. (1992) The Regulation of Hepatic Glutathione. In Hepatic Annion Transport and Bile Secretion: Physiology and Pathophysiology (Tavoloni, N., and Berk, P. D., eds) pp. 363-395, Marcel Dekker, New York
8. Fernández-Checa, J., Kaplowitz, N., Garcia-Ruiz, C., Colell, A., Miranda, M., Mai, M., Ardite, E., and Morales, A. (1997) GSH transport in mitochondria: defense against TNF-induced oxidative stress and alcohol-induced defect. Am. J. Physiol. 273, G7-G17
9. Ookhtens, M., and Kaplowitz, N. (1998) Role of the liver in interorgan homeostasis of glutathione and cyst(e)ine. Sem. Liver Dis. 18, 313-329
10. Yan, N., and Meister, A. (1990) Amino acid sequence of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 265, 1588-1593
11. Huang, C., Anderson, M. E., and Meister, A. (1993) Amino acid sequence and function of the light subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 268, 20578-20583
12. Gipp, J. J., Chang, C., and Mulcahy, R. T. (1992) Cloning and nucleotide sequence of a full-length cDNA for human liver γ-glutamylcysteine synthetase. Biochem. Biophys. Res. Commun. 185, 29-35
13. Gipp, J. J., Bailey, H. H., and Mulcahy, R. T. (1995) Cloning and sequence of the cDNA for the light subunit of human liver γ-glutamylcysteine synthetase and relative mRNA levels for heavy and light subunits in human normal tissues. Biochem. Biophys Res. Commun. 206, 584-589
14. Seelig, G. F., Simondsen, R. P., and Meister, A. (1984) Reversible dissociation of γ-glutamylcysteine synthetase into two subunits. J. Biol. Chem. 259, 9345-9347
15. Huang, C., Chang, L., Anderson, M. E., and Meister, A. (1993) Catalytic and regulatory properties of the heavy subunit of rat kidney γ-glutamylcysteine synthetase. J. Biol. Chem. 268, 19675-19680
16. Chang, L. S. (1996) The functional involvement of Lys-38 in the heavy subunit of rat kidney γ-glutamylcysteine synthetase: chemical modification and mutagenesis studies. J. Prot. Chem. 15, 321-326
17. Huang, C. S., Moore, W. R., and Meister, A. (1988) On the active site thiol of γ-glutamylcysteine synthetase: relationship to catalysis, inhibition, and regulation. Proc. Natl. Acad. Sci. USA 85, 2464-2468
18. Misra, I., and Griffith, O. W. (1998) Expression and purification of human γ-glutamylcysteine synthetase. Protein Exp. Purif. 13, 268-276
19. Lu, S. C., Ge, J., Kuhlenkamp, J., and Kaplowitz, N. (1992) Insulin and glucocorticoid dependence of hepatic γ-glutamylcysteine synthetase and GSH synthesis in the rat: studies in cultured hepatocytes and in vivo. J. Clin. Invest. 90, 524-532
20. Oppenheimer, L., Wellner, V. P., Griffith, O. W., and Meister, A. (1979) Glutathione synthetase. Purification from rat kidney and mapping of the substrate binding sites. J. Biol. Chem. 254, 5184-5190
21. Huang, C. S., He, W., Meister, A., and Anderson, M. E. (1995) Amino acid sequence of rat kidney glutathione synthetase. Proc. Natl. Acad. Sci. USA 92, 1232-1236
22. Snoke, J. E., Yanan, S., and Bloch, K. (1953) Synthesis of glutathione from γ-glutamylcysteine. J. Biol. Chem. 201, 573-86
23. Yanari, S., Snoke, J. E., and Bloch, K. (1953) Energy source in glutathione biosynthesis. J. Biol. Chem. 201, 561-571
24. Grant, C. M., MacIver, F. H., and Dawes, I. W. (1997) Glutathione synthetase is dispensable for growth under both normal and oxidative stress conditions in the yeast Saccharomyces cerevisiae due to an accumulation of the dipeptide γ-glutamylcysteine. Mol. Biol. Cell 8, 1699-1707
25. Bannai, S., Ishii, T., Takada, A., and Noriko, T. (1989) Regulation of glutathione level by amino acid transport. In Glutathione Centennial (Taniguchi, N., Higashi, T., Sakamoto, Y., and Meister, A., eds) pp. 407-421, Academic Press, San Diego
26. Kilberg, M. S. (1982) Amino acid transport in isolated rat hepatocytes. J. Membr. Biol. 69, 1-12
27. Takada, A., and Bannai, S. (1984) Transport of cystine in isolated rat hepatocytes in primary culture. J. Biol. Chem. 259, 2441-2445
28. Tateishi, N., Higashi, T., Shinya, S., Naruse, A., and Sakamoto Y. (1974) Studies on the regulation of glutathione level in rat liver. J. Biochem. 75, 93-103
29. Tateishi, N., and Sakamoto, Y. (1983) Nutritional significance of glutathione in rat liver. In Glutathione: Storage, Transport and Turnover in Mammals (Sakamoto, Y., et al., eds) pp. 13-38, Scientific Socoetu Press, Tokyo
30. Bannai, S. (1984) Transport of cystine and cysteine in mammalian cells. Biochim. Biophys. Acta 779, 289-306
31. Kilberg, M. S., Christensen, H. N., and Handlogten, M. E. (1979) Cysteine as a system-specific substrate for transport system ASC in rat hepatocytes. Biochem. Biophys. Res. Commun. 88, 744-751
32. Gazzola, G. C., Dall'Asta, V., and Guidotti, G. G. (1980) The transport of neutral amino acids in cultured human fibroblasts. J. Biol. Chem. 255, 929-396
33. Bannai, S., and Kitamura, E. (1981 ) Role of proton dissociation in the transport of cystine and glutamate in human diploid fibroblasts in culture. J. Biol. Chem. 256, 5770-5772
34. Bannai, S. (1986) Exchange of cystine and glutamate across plasma membrane of human fibroblasts. J. Biol. Chem. 261, 2256-2263
35. Bannai, S., Takada, A., Kasuga, H., and Tateishi, N. (1986) Induction of cystine transport activity in isolated rat hepatocytes by sulfobromophthalein and other electrophilic agents. Hepatohgy 6, 1361-1368
36. Aw, T. Y., Ookhtens, M., and Kaplowitz, N. (1986) Mechanism of inhibition of glutathione efflux by methionine from isolated rat hepatocytes. Am. J. Physiol. 251, G354-G361
37. Lu, S. C., and Huang, H. Y. (1994) Comparison of sulfur amino acid utilization for GSH synthesis between HepG2 cells and cultured rat hepatocytes. Biochem. Pharmacol. 47, 859-869
38. Tateishi, N., and Sakamoto, Y. (1989) Regulation of glutathione level in primary cultured hepatocytes. In Glutathione Centennial (Taniguchi, N., Higashi, T., Sakamoto, Y., et al., eds) pp. 57-71, Academic Press, San Diego
39. +-independent neutral amino acid transport systems in primary cultures of rat hepatocytes. J. Biol. Chem. 257, 12006-12011
40. Tarver, H., and Schmidt, C. L. A. (1939) The conversion of methionine to cystine: experiments with radioactive sulfur. J. Biol. Chem. 130, 67-80
41. Finkelstein, J. D. (1990) Methionine metabolism in mammals. J. Nutr. Biochem. 1, 228-237
42. Neuhauser-Berthold, M., Kuhfus, A., and Bassler, K. H. (1988) Utilization of glutathione disulfide as cysteine source during long-term parenteral nutrition in the growing rat. Metabolism 37, 796-801
43. Mato, J. M., Alvarez, L., Corrales, F. J, and Pajares, M. A. (1994) S-adenosylmethionine and the liver. In The Liver: Biology and Pathobiology, Third edition (Arias, I. M., Boyer, J. L., Fausto, N., Jakoby, W. B., Schachter, D. A., and Shafritz, D. A., eds) pp. 461-470, Raven Press, New York
44. Beatty, P. W., and Reed, D. J. (1980) Involvement of the cystathionine pathway in the biosynthesis of glutathione by isolated rat hepatocytes. Arch. Biochem. Biophys. 204, 80-87
45. Reed, D. J., and Beatty, P. W. (1980) Biosynthesis and regulation of glutathione: toxicological implications. In Review of Biochemical Toxicology (Hodgson, E, Bend, J. R., and Philpot, R. N., eds) pp. 213-241, Elsevier North Holland, New York
46. Shan, X., Aw, T. Y., Shapira, R., and Jones, D. (1989) Oxygen dependence of glutathione synthesis in hepatocytes. Toxicol. Appl. Pharmacol. 101, 261-270
47. Finkelstein, J. D., Kyle, W. E., Harris, B. J., and Martin, J. J. (1982) Methionine metabolism in mammals: concentration of metabolites in rat tissues. J. Nutr. 112, 1011-1018
48. Cooper, A. J. L. (1983) Biochemistry of sulfur-containing amino acids. Annu. Rev. Biochem. 52, 187-222
49. Horowitz, J. H., Rypins, E. B., Henderson, J. M., Heymsfield, S. B., Moffitt, S. D., Bain, R. P., Chawla, R. K., Bleier J. C., and Rudman, D. (1981) Evidence for impairment of transsulfuration pathway in cirrhosis. Gastroenterotogy 81, 668-675
50. Lu, S. C. (1998) Methionine adenosyltransferase and liver disease: it's all about SAM. Gastroenterology 114, 403-407
51. Vendemiale, G., Altomare, E., Trizio, T., Le Grazie, C., Di Padova, C., Salerna, M. T., Carrieri, V., and Albano, O. (1989) Effect of oral S-adenosyl-L-methionine on hepatic glutathione in patients with liver disease. Scand. J. Gastroenterol. 24, 407-415
52. Mato, J. M., Camara, J., Ortiz, P., Rodés, J., and Spanish Collaborative Group for the Study of Alcoholic Liver Cirrhosis. (1997) S-Adenosylmethionine in the treatment of alcoholic liver cirrhosis: results from a multicentric, placebo-controlled, randomized, double-blind clinical trial. Hepatology 26, A489 (abstr.)
53. Mulcahy, R. T., Bailey, H. H., and Gipp, J. J. (1994) Up-regulation of γ-glutamylcysteine synthetase activity in melphalan-resistant human multiple myeloma cells expressing increased glutathione levels. Cancer Chemother. Pharmacol. 34, 67-71
54. Mulcahy, R. T., Untawale, S., and Gipp, J. J. (1994) Transcriptional up-regulation of γ-glutamylcysteine synthetase gene expression in melphalan-resistant human prostate carcinoma cells. Mol. Pharmacol. 46, 909-914
55. Mulcahy, R. T., Bailey, H. H., and Gipp, J. J. (1995) Transfection of complementary DNAs for the heavy and light subunits of human γ-glutamylcysteine synthetase results in an elevation of intracellular glutathione and resistance to melphalan. Cancer Res. 55, 4771-4775
56. Godwin, A. K., Meister, A., O'Dwyer, P. J., Huang, C. S., Hamilton, T. C., and Anderson, M. E. (1992) High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc. Natl. Acad. Sci. USA 89, 3070-3074
57. Kuo, M. T., Bao, J. J., Furuichi, M., Yamane, Y., Gomi, A., Savaraj, N., Masuzawa, T., and Ishikawa, T. (1998) Frequent coexpression of MRP/GS-X pump and γ-glutamylcysteine synthetase mRNA in drug-resistant cells, untreated tumor cells and normal mouse tissues. Biochem. Pharmacol. 55, 605-615
58. Oguri, T., Fujiwara, Y., Isobe, T., Katoh, O., Watanabe, H., and Yamakido, M. (1998) Expression of γ-glutamylcysteine synthetase (γ-GCS) and multidrug resistance-associated protein (MRP), but not human canalicular multispecific organic anion transporter (cMOAT), genes correlates with exposure of human lung cancers to platinum drugs. Br. J. Cancer 77, 1089-1096
59. Ishikawa, T., Bao, J. J., Yamane, Y., Akimaru, K., Frindrich, K., Wright, C. D., and Kuo, M. T. (1996) Coordinated induction of MRP/GS-X pump and γ-glutamylcysteine synthetase by heavy metals in human leukemia cells. J. Biol. Chem. 271, 14981-14988
60. Woods, J. S., and Ellis, M. E., (1995) Up-regulation of glutathione synthesis in rat kidney by methyl mercury. Relationship to mercury-induced oxidative stress. Biochem. Pharmacol. 50, 1719-1724
61. Shi, M. M., Kugelman, A., Iwamoto, T., Tian, L., and Forman, H. J. (1994) Quinone-induced oxidative stress elevates glutathione and induces γ-glutamylcysteine synthetase activity in rat lung epithelial L2 cells. J. Biol. Chem. 269, 26512-26317
62. Liu, R. M., Hu, H., Robison, T. W., and Forman, H. J. (1996) Differential enhancement of γ-glutamyl transpeptidase and γ-glutamylcysteine synthetase by tert-butylhydroquinone in rat lung epithelial L2 cells. Am. J. Resp. Cell Mol. Biol. 14, 186-191
63. Mulcahy, R. T., Wartman, M. A., Bailey, H. H., and Gipp, J. J. (1997) Constitutive and β-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase heavy subunit gene is regulated by a distal antioxidant response element/ TRE sequence. J. Biol. Chem. 272, 7445-7454
64. Morales, A., García-Ruiz, C., Miranda, M., Marí, M., Colell, A., Ardite, E., Fernández-Checa, J. C. (1997) Tumor necrosis factor increases hepatocellular glutathione by transcriptional regulation of the heavy subunit chain of γ-glutamylcysteine synthetase. J. Biol. Chem. 272, 30371-30379
65. Cai, J., Huang, Z., and Lu, S. C. (1997) Differential regulation of γ-glutamylcysteine synthetase heavy and light subunit gene expression. Biochem. J. 326, 167-172
66. Cai, J., Sun, W., and Lu, S. C. (1995) Hormonal and cell density regulation of hepatic γ-glutamylcysteine synthetase gene expression. Mol. Pharmacol. 48, 212-218
67. Lu, S. C., and Ge, J. (1992) Loss of suppression of GSH synthesis under low cell density in primary cultures of rat hepatocytes. Am. J. Physiol. 263, C1181-C1189
68. Huang, Z., Li, H., Cai, J., Kuhlenkamp, J., Kaplowitz, N., and Lu, S. C. (1998) Changes in glutathione homeostasis during liver regeneration in the rat. Hepatology 27, 147-153
69. Liu, R. M., Vasiliou, V., Zhu, H., Duh, J. L., Tabor, M. W., Puga, A., Nebert, D. W., Sainsbury, M., and Shertzer, H. G. (1994) Regulation of [Ah]gene battery enzymes and glutathione levels by 5,10-dihydroindeno[1,2-b]indole in mouse hepatoma cell lines. Carcinogenesis 15, 2347-2352
70. Kondo, T., Yoshida, K., Urata, Y., Goto, S., Gasa, S., and Taniguchi, N. (1993) γ-Glutamylcysteine synthetase and active transport of glutathione S-conjugate are responsive to heat shock in K562 erythroid cells. J. Biol. Chem. 268, 20366-20372
71. Borroz, K. I., Buetler, T. M., and Eaton, D. L. (1994) Modulation of γ-glutamylcysteine synthetase large subunit mRNA expression by butylated hydroxyanisole. Toxicol. Appl. Pharmacol. 126, 150-155
72. Sekhar, K. R., Long, M., Long, J., Xu, Z. Q., Summar, M. L., and Freeman, M. L. (1997) Alteration of transcriptional and post-transcriptional expression of gamma-glutamylcysteine synthetase by diethyl maleate. Radiation Res. 147, 592-297
73. Urata, Y., Yamamoto, H., Goto, S., Tsushima, H., Akazawa, S., Yamashita, S., Nagataki, S., and Kondo, T. (1996) Long exposure to high glucose concentration impairs the responsive expression of γ-glutamylcysteine synthetase by interleukin-1β and tumor necrosis factor-α in mouse endothelial cells. J. Biol. Chem. 271, 15146-15152
74. Kuo, P. C., Abe, K. Y., and Schroeder, R. A. (1996) Interleukin-l-induced nitric oxide production modulates glutathione synthesis in cultured rat hepatocytes. Am. J. Physiol. 271, C851-C862
75. Chen, Y., Saari, J. T., and Kang, Y. J. (1995) Expression of γ-glutamylcysteine synthetase in the liver of copper-deficient rats. Proc. Soc. Exp. Biol. Med. 210, 102-106
76. Rahman, I., Bel, A., Mulier, B., Lawson, M. F., Harrison, D. J., MacNee, W., and Smith, C. A. (1996) Transcriptional regulation of γ-glutamylcysteine synthetase heavy subunit by oxidants in human alveolar epithelial cells. Biochem. Biophys. Res. Commun. 229, 832-837
77. Rahman, I., Smith, C. A., Lawson, M. F., Harrison, D. J., and MacNee, W. (1996) Induction of γ-glutamylcysteine synthetase by cigarette smoke is associated with AP-1 in human alveolar epithelial cells. FEBS Lett. 396, 21-25
78. Lu, S. C., Cai, J., Kuhlenkamp, J., Sun, W., Takikawa, H., Takenaka, O., Horie, T., Yi, J., and Kaplowitz, N. (1996) Alterations in glutathione homeostasis in mutant Eisai hyperbilirubinemic rats. Hepatology 24, 253-258
79. Gomi, A., Masuzawa, T., Ishikawa, T., and Kuo, M. T. (1997) Post-transcriptional regulation of MRP/GS-Xpump and γ-glutamylcysteine synthetase expression by 1-(4-amino-2-methyl-5-pyrimidinyl) methyl-3-(2-chloroethyl)-3-nilrosourea and by cycloheximide in human glioma cells. Biochem. Biophys. Res. Commun. 239, 51-56
80. Tomonari, A., Nishio, K., Kurokawa, H., Fukumoto, H., Fukuoka, K., Iwamoto, Y., Usuda, J., Suzuki, T., Itakura, M., and Saijo, N. (1997) Proximal 5-flanking sequence of the human γ-glutamylcysteine synthetase heavy subunit gene is involved in cisplatin-induced transcriptional up-regulation in a lung cancer cell line SBC-3. Biochem. Biophys. Res. Commun. 236, 616-621
81. Sekhar, K R., Meredith, M. J., Kerr, L. D., Soltaninassab, S. R., Spitz, D. R., Xu, Z. Q., and Freeman, M. L. (1997) Expression of glutathione and γ-glutamylcysteine synthetase mRNA is Jun dependent. Biochem. Biophys. Res. Commun. 234, 588-593
82. Tian, L., Shi, M. M., and Forman, H. J. (1997) Increased transcription of the regulatory subunit of γ-glutamylcysteine synthetase in rat lung epithelial L2 cells exposed to oxidative stress or glutathione depletion. Arch. Biochem. Biophys. 342, 126-133
83. Galloway, D. C., Blake, D. G., Shepherd, A. G., and McLellan, L. I. (1997) Regulation of human γ-glutamylcysteine synthetase: co-ordinate induction of the catalytic and regulatory subunits in HepG2 cells. Biochem J. 328, 99-104
84. Yao, K. S., Godwin, A. K., Johnson, S. W., Ozols, R. F., O'Dwyer, P. J., and Hamilton, T. C. (1995) Evidence for altered regulation of γ-glutamylcysteine synthetase gene expression among cisplatin-sensitive and cisplatin-resistant human ovarian cancer cell lines. Cancer Res. 55, 4367-4374
85. Teshigawara, M., Matsumoto, S., Tsuboi, S., and Ohmori, S. (1995) Changes in levels of glutathione and related compounds and activities of glutathione-related enzymes during liver regeneration. Res. Exp. Med. 195, 55-60
86. 1 is a potent inhibitor of glutathione synthesis in the lung epithelial cell line A549: transcriptional effect on the GSH rate-limiting enzyme, γ-glutamylcysteine synthetase. Am. J. Resp. Cell. Mol. Biol. 17, 599-607
87. Rahman, I., Smith, C. A. D., Antonicelli, F., and MacNee, W. (1998) Characterization of γ-glutamylcysteine synthetase-heavy subunit promoter: a critical role for AP-1. FEBS Lett. 427, 129-133
88. Morales, A., Miranda, M., Sanchez-Reyes, A., Colell, A., Biete, A., and Fernández-Checa, J. C. (1998) Transcriptional regulation of the heavy subunit chain of γ-glutamylcysteine synthetase by ionizing radiation. FEBS Lett. 427, 15-20
89. Shimizu, T., Iwanaga, M., Yasunaga, A., Urata, Y., Goto, S., Shibata, S., and Kondo, T. (1998) Protective role of glutathione synthesis on radiation-induced DNA damage in rabbit brain. Cell. Mol. Neurobiol. 18, 299-310
90. Iwanaga, M., Mori, K., Iida, T., Urata, Y., Matsuo, T., Wasunaga, A., Shibata, S., and Kondo, T. (1998) Nuclear factor kappa B dependent induction of gamina-glutamylcysteine synthetase by ionizing radiation in T98G human glioblastoma cells. Free Rad. Biol. Med. 24, 1256-1268
91. Tanaka, T., Uchiumi, T., Kohno, K., Tomonari, A., Nishio, K., Saijo, N., Kondo, T., and Kuwano, M. (1998) Glutathione homeostasis in human hepatic cells: overexpression of γ-glutamylcysteine synthetase gene in cell lines resistant to buthionine sulfoximine, an inhibitor of glutathione synthesis. Biochem. Biophys. Res. Commun. 246, 398-403
92. Yamane, Y., Furuichi, M., Song, R., Van, N. T., Mulcahy, R. T., Ishikawa, T., and Kuo, M. T. (1998) Expression of multidrug resistance protein/GS-X pump and γ-glutamylcysteine synthetase genes is regulated by oxidative stress. J. Biol. Chem. 273, 31075-31085
93. Liu, R. M., Gao, L., Choi, J., and Forman, H. J. (1998) γ-Glutamylcysteine synthetase: mRNA stabilization and independent subunit transcription by 4-hydroxy-2-nonenal. Am. J. Physiol. 275, L861-L869
94. Tipnis, S. R., Blake, D. G., Shepherd, G., and McLellan, L. I. (1999) Overexpression of the regulatory subunit of γ-glutamylcysteine synthetase in HeLa cells increases γ-glutamylcysteine synthetase activity and confers drug resistance. Biochem. J. 337, 559-566
95. Kuo, P. C., Abe, K. Y., and Schroeder, R. A. (1996) Interleukin-l-induced nitric oxide production modulates glutathione synthesis in cultured rat hepatocytes. Am. J. Physiol. 40, C851-C862
96. Moellering, D., McAndrew, J., Patel, R. P., Cornwell, T., Lincoln, T., Cao, X., Messina, J. L., Forman, H. J., Jo, H., and Darley-Usmar, V. M. (1998) Nitric oxide-dependent induction of glutathione synthesis through increased expression of γ-glutamylcysteine synthetase. Arch. Biochem. Biophys. 358, 74-82
97. Moinova, H. R., and Mulcahy, R. T. (1998) An electrophile responsive element (EpRE) regulates β-naphthoflavone induction of the human γ-glutamylcysteine synthetase regulatory subunit gene. J. Biol. Chem. 273, 14683-14689
98. Mulcahy, R. T., and Gipp, J. J. (1995) Identification of a putative antioxidant response element in the 5′-flanking region of the human γ-glutamylcysteine synthetase heavy subunit gene. Biochem. Biophys. Res. Commun. 209, 227-233
99. Wild, A. C., Gipp, J. J., Mulcahy, R. T. (1998) Overlapping antioxidant response element and PMA response element sequences mediate basal and β-naphthoflavone-induced expression of the human γ-glutamylcysteine synthetase catalytic subunit gene, Biochem. J. 332, 373-381
100. Rahman, I., Bel, A., Mulier, B., Donaldson, K., and MacNee, W. (1998) Differential regulation of glutathione by oxidants and dexamethasone in alveolar epithelial cells. Am. J. Physiol. 275, L80-L86
101. Nakamura, T., Yoshimoto, K., Nakayama, Y., Tomita, Y., and Ichihara, A. (1993) Reciprocal modulation of growth and differentiated functions of mature rat hepatocytes in primary culture by cell-cell contact and cell membranes. Proc. Natl. Acad. Sci. USA 80, 7229-7233
102. Shaw, J. P., and Chou, I. (1986) Elevation of intracellular glutathione content associated with mitogenic stimulation of quiescent fibroblasts. J. Cell. Physiol. 129, 193-198
103. Messina, J. P., and Lawrence, D. A. (1989) Cell cycle progression of glutathione-depleted human peripheral blood mononuclear cells is inhibited at S phase. J. Immunol. 143, 1974-1981
104. Iwata, S., Hori, T., Sato, N., Ueda-Taniguchi, Y., Yamabe, T., Nakamura, H., Masutani, H., and Yodoi, Y. (1994) Thiolmediated redox regulation of lymphocyte proliferation. Possible involvement of adult T cell leukemia-derived factor and glutathione in transferrin receptor expression. J. Immunol. 152, 5633-5642
105. Poot, M., Teubert, H., Rabinovitch, P. S., and Kavanagh, T. J. (1995) De novo synthesis of glutathione is required for both entry into and progression through the cell cycle. J. Cell. Physiol. 163, 555-560
106. o. J. Cell. Physiol. 81, 91-96
107. Lee, F. Y. F., Siemann, D. W., Allalunis-Turner, M. J., and Keng, P. C. (1988) Glutathione contents in human and rodent tumor cells in various phases of the cell cycle. Cancer Res. 48, 3661-3665
108. Holmgren, A. (1981) Regulation of ribonucleotide reductase. Curr. Top. Cell. Regul. 19, 47-76
109. Kijima, H., Tsuchida, T., Kondo, H., Iida, T., Oshika, Y., Nakamura, M., Scanlon, K. J., Kondo, T., and Tamaoki, N. (1998) Hammerhead ribozymes against γ-glutamylcysteine synthetase mRNA down-regulate intracellular glutathione concentration of mouse islet cells. Biochem. Biophys. Res. Commun. 247, 697-703
110. Lu, S. C., Kuhlenkamp, J., Garcia-Ruiz, C., and Kaplowitz, N. (1991) Hormone-mediated down-regulation of hepatic GSH synthesis in the rat. J. Clin. Invest. 88, 260-269
111. Estrela, J. M., Gil, F., Vila, J. M., and Viña, J. (1988) α-Adrenergic modulation of glutathione metabolism in isolated rat hepatocytes. Am. J. Physiol. 255, E801-E805
112. Hirota, M., Inoue, M., Ando, Y., Hirayama, K., Morino, Y., Sakamoto, K., Mon, K., and Agaki, M. (1989) Inhibition of stress-induced gastric injury in the rat by glutathione. Gastroenterology 97, 853-859
113. Lew, H., Pyke, S., and Quintanilha, A. (1985) Changes in the glutathione status of plasma, liver and muscle following exhaustive exercise in rats. Fed. Eur. Biochem. Soc. 185, 262-266
114. Lu, S. C., Garcia-Ruiz, C., Kuhlenkamp, J., Ookhtens, M., Salas-Prato, M., and Kaplowitz, N. (1990) Hormonal regulation of GSH efflux. J. Biol. Chem. 265, 16088-16095
115. Hidalgo, J., Garvey, J. S., and Armario, A. (1990) On the metallothionein, glutathione and cysteine relationship in rat liver. J. Pharm. Exp. Ther. 255, 554-564
116. Sun, W., Huang, Z., and Lu, S. C. (1996) Regulation of γ-glutamylcysteine synthetase by protein phosphorylation. Bioehem. J. 320, 321-328
117. Lauterburg, B. H., and Mitchell, J. R. (1982) Toxic doses of acetaminophen suppress hepatic glutathione synthesis in rats. Hepatology, 2, 8-12
118. Lefrançois-Martinez, A., Diaz-Guerra, M.J., Vallet, V., Kahn, A., and Antoine, B. (1994) Glucose-dependent regulation of the L-pyruvate kinase gene in a hepatoma cell line is independent of insulin and cyclic AMP. FASEB J. 8, 89-96
119. Vaulont, S., and Kahn, A. (1994) Transcriptional control of metabolic regulation genes by carbohydrates. FASEB J. 8, 28-35
120. Ghibelli, L., Coppola, S., Rotilio, G., Lafavia, E., Maresca, V., and Ciriolo, M. R. (1995) Non-oxidative loss of glutathione in apoptosis via GSH extrusion. Biochem. Biophys. Res. Commun. 216, 313-320
121. Van den Dobbelsteen, D. J., Nobel, C. S. I., Schlegel, J., Cotgreave, I. A., Orrenius, S., and Slater, A. F. G. (1996) Rapid and specific efflux of reduced glutathione during apoptosis induced by anti-Fas/APO-1 antibody. J. Biol. Chem. 271, 15420-15427
122. Kohno, T., Yamada, Y., Hata, T., Mori, H., Yamamura, M., Tomonaga, M., Urata, Y., Goto, S., and Kondo, T. (1996) Relation of oxidative stress and glutathione synthesis to CD95 (Fas/APO-1 )-mediated apoptosis of adult T cell leukemia cells. J. Immunol. 156, 4722-4728
123. Delneste, Y., Jeannin, P., Sebille, E., Aubry, J. P., and Bonnefoy, J. Y. (1996) Thiols prevent Fas (CD95)-mediated T cell apoptosis by down-regulating membrane Fas expression. Eur. J. Immunol. 26, 2981-2988
124. Cotgreave, I. A., and Gerdes, R. C. (1998) Recent trends in glutathione biochemistry - glutathione-protein interactions: a molecular link between oxidative stress and cell proliferation? Biochem. Biophys. Res. Commun. 242, 1-9