Gamma-glutamyl transpeptidase gene organization and expression: A comparative analysis in rat, mouse, pig and human species

Comparative Biochemistry and Physiology - B Biochemistry and Molecular Biology

Volumn 122, Issue 4, 1999, Pages 367-380

  Chikhi, Naïma ^a   Holic, Nathalie ^a   Guellaen, Georges ^a   Laperche, Yannick ^a  

^a HENRI MONDOR HOSPITAL   (France)

Author keywords

Comparative study; Gamma glutamyl transpeptidase; Gene organization; Gene regulation; Glutathione; Multiple promoters; Oxidative stress; Sequence analysis

Indexed keywords

COMPLEMENTARY DNA; GAMMA GLUTAMYLTRANSFERASE; GLUTATHIONE; MESSENGER RNA;

AMINO ACID SEQUENCE; EXON; GENE CONTROL; GENE EXPRESSION; GENE SEQUENCE; GENE STRUCTURE; GENETIC TRANSCRIPTION; HUMAN; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROMOTER REGION; RAT; REVIEW; SEQUENCE ANALYSIS; SPECIES DIFFERENCE; SWINE;

SUS SCROFA;

EID: 0032899255     PISSN: 03050491     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0305-0491(99)00013-9     Document Type: Review

References (113)

1. Ayoubi TA, Van De Ven WJ. Regulation of gene expression by alternative promoters. FASEB J 1996;10:453-60.
2. Ballatori N. Glutathione mercaptides as transport forms of metals. Adv Pharmacol 1994;27:271-98.
3. Ballatori N, Lieberman MW. Accelerated methylmercury elimination in gamma-glutamyl transpeptidase deficient mice. Am J Pathol 1998;152:1049-55.
4. Barouki R, Finidori J, Chobert MN, Aggerbeck M, Laperche Y, Hanoune J. Biosynthesis and processing of gamma-glutamyl transpeptidase in hepatoma tissue culture cells. J Biol Chem 1984;259:7970-4.
5. Bergelson S, Pinkus R, Daniel V. Intracellular glutathione levels regulate Fos/Jun induction and activation of glutathione-S-transferase-gene expression. Cancer Res 1994;54:36-40.
6. Brouillet A, Darbouy M, Okamoto T, Chobert MN, Lahuna O, Garlatti M, Goodspeed D, Laperche Y. Functional characterization of the rat gamma-glutamyl transpeptidase promoter that is expressed and regulated in the liver and hepatoma cells. J Biol Chem 1994;269:14878-84.
7. Brouillet A, Holic N, Chobert MN, Laperche Y. The gamma-glutamyl transpeptidase gene is transcribed from a different promoter in rat hepatocytes and biliary cells. Am J Pathol 1998;152:1039-48.
8. Bulle F, Mattei MG, Siegrist S, Pawlak A, Passage E, Chobert MN, Laperche Y, Guellaen G. Assignment of the human gamma-glutamyl transferase gene to the long arm of chromosome 22. Hum Genet 1987;6:283-6.
9. Busachi C, Mebis J, Broeckaert L, Desmet V. Histochemistry of gammaglutamyl transpeptidase in human liver biopsies. Pathol Res Pract 1981;172:99-108.
10. Carter BZ, Wiseman AL, Orkiszewski R, Ballard KD, Ou CN, Lieberman MW. Metabolism of leukotriene C4 in gamma-glutamyl transpeptidase-deficient mice. J Biol Chem 1997;272:12305-10.
11. Chobert MN, Grondin G, Brouillet A, Laperche Y, Beaudoin AR. Control of gamma-glutamyl transpeptidase expression by glucocorticoids in the rat pancreas. Correlation with granule formation. J Biol Chem 1996;271:12431-7.
12. Chobert MN, Lahuna O, Lebargy F, Kurauchi O, Darbouy M, Bernaudin JF, Guellaen G, Barouki R, Laperche Y. Tissue-specific expression of two gammaglutamyl transpeptidase mRNAs with alternative 5′ ends encoded by a single copy gene in the rat. J Biol Chern 1990;265:2352-7.
13. Choie DD, Longnecker DS, del Campo AA. Acute and chronic cisplatin nephropathy in rats. Lab Invest 1981;44:397-402.
14. Collins JE, Mungall AJ, Badcock KL, Fay JM, Dunham I. The organization of the gamma-glutamyl transferase genes and other low copy repeats in human chromosome 22q11 [published erratum appears in Genome Res 1997;7(9):94-21]. Genome Res 1997;7:522-31.
15. Coloma Pitot HC. Characterization and sequence of a cDNA clone of gamma-glutamyltranspeptidase. Nucleic Acids Res 1986;14:1393-403.
16. Courtay C, Heisterkamp N, Siest G, Groffen J. Expression of multiple gamma-glutamyltransferase genes in man. Biochem J 1994;297:503-8.
17. Courtay C, Oster T, Michelet F, Visvikis A, Diederich M, Wellman M, Siest C. Gamma-glutamyltransferase: nucleotide sequence of the human pancreatic cDNA. Evidence for a ubiquitous gamma-glutamyltransferase polypeptide in human tissues. Biochem Pharmacol 1992;43:2527-33.
18. Curthoys NP, Hughey RP. Characterization and physiological function of rat renal gamma-glutamyltranspeptidase. Enzyme 1979;24:383-403.
19. Darbouy M, Chobert MN, Lahuna O, Okamoto T, Bonvalet JP, Farman N, Laperche Y. Tissue-specific expression of multiple gamma-glutamyl transpeptidase mRNAs in rat epithelia. Am J Physiol 1991;261:1130-7.
20. Diederich M, Wellman M, Siest G. Localization of a regulatory region on the 5′-untranslated region of human hepatoma HepG2 gamma-glutamyltransferase mRNA and response to dexamethasone and antisense oligonucleotide treatment. FEBS Lett 1994;356:307-10.
21. Diederich M, Wellman M, Visvikis A, Puga A, Siest G. The 5′ untranslated region of the human gamma-glutamyl transferase mRNA contains a tissue-specific active translational enhancer. FEBS Lett 1993;332:88-92.
22. Farber E, Sarma DS. Hepatocarcinogenesis: a dynamic cellular perspective. Lab Invest 1987;56:4-22.
23. Finidori J, Laperche Y, Haguenauer-Tsapis R, Barouki R, Guellaen G, Hanoune J. In vitro biosynthesis and membrane insertion of gamma-glutamyl transpeptidase. J Biol Chem 1984;259:4687-90.
24. Forman HJ, Skelton DC. Protection of alveolar macrophages from hyperoxia by gamma-glutamyl transpeptidase. Am J Physiol 1990;259:L102-7.
25. Gerber MA, Thung SN. Enzyme patterns in human hepatocellular carcinoma. Am J Pathol 1980;98:395-400.
26. Germain L, Blouin MJ, Marceau N. Biliary epithelial and hepatocytic cell lineage relationships in embryonic rat liver as determined by the differential expression of cytokeratins, alpha-fetoprotein, albumin, and cell surface-exposed components. Cancer Res 1988;48:4909-18.
27. Godwin AK, Meister A, O'Dwyer PJ, Huang CS, Hamilton TC, Anderson ME. High resistance to cisplatin in human ovarian cancer cell lines is associated with marked increase of glutathione synthesis. Proc Natl Acad Sci USA 1992;89:3070-4.
28. Goodspeed DC, Dunn TJ, Miller CD, Pitot HC. Human gamma-glutamyl transpeptidase cDNA: comparison of hepatoma and kidney mRNA in the human and rat. Gene 1989;76:1-9.
29. Griffiths SA, Good VM, Gordon LA, Hudson EA, Barrett MC, Munks RJ, Manson MM. Characterization of a promoter for gamma-glutamyl transpeptidase activated in rat liver in response to aflatoxin B1 and ethoxyquin. Mol Carcinogen 1995;14:251-62.
30. Habib GM, Carter BZ, Sepulveda AR, Shi ZZ, Wan DF, Lebovitz RM, Lieberman MW. Identification of a sixth promoter that directs the transcription of gamma-glutamyl transpeptidase type III RNA in mouse. J Biol Chem 1995;270:13711-5.
31. Hamilton TC, Winker MA, Louie KG, Batist G, Behrens BC, Tsuruo T, Grotzinger KR, McKoy WM, Young RC, Ozols RF. Augmentation of adriamycin, melphalan, and cisplatin cytotoxicity in drug-resistant and sensitive human ovarian carcinoma cell lines by buthionine sulfoximine mediated glutathione depletion. Biochem Pharmacol 1985;34:2583-6.
32. Hanigan MR. Expression of gamma-glutamy transpeptidase provides turnor cells with a selective growth advantage at physiologic concentrations of cyst(e)ine. Carcinogenesis 1995;16:181-5.
33. Hanigan MR. gamma-Glutamyl transpeptidase, a glutathionase: its expression and function in carcinogenesis. Chem Biol Interact 1998;111-112:333-42.
34. Hanigan MH, Frierson HF Jr. Immunohistochemical detection of gamma-glutamyl transpeptidase in normal human tissue. Histochem Cytochem 1996;44:1101-8.
35. Hanigan MR, Gallagher BC, Taylor PT, Large MK. Inhibition of gamma-glutamyl transpeptidase activity by acivicin in vivo protects the kidney from cisplastin-induced toxicity. Cancer Res 1994;54:5925-9.
36. Hanigan MH, Pitot HC. Gamma-glutamyl transpeptidase-its role in hepatocarcinogenesis. Carcinogenesis 1985;6:165-72.
37. Hanigan MH, Ricketts WA. Extracellular glutathione is a source of cysteine cells that express gamma-glutamyl transpeptidase. Biochemistry 1993;32:6302-6.
38. Harding CO, Williams P, Wagner E, Chang DS, Wild K, Colwell RE, Wolff JA. Mice with genetic gamma-glutamyl transpeptidase deficiency exhibit glutathionuria, severe growth failure, reduced life spans and infertility. Biol Chem 1997;272:12560-7.
39. Heisterkamp N, Rajpert-De Meyts E, Uribe L, Forman HJ, Groffen J. Identification of a human gamma-glutamyl cleaving enzyme related to, but distinct from, gamma-glutamyl transpeptidase. Proc Natl Acad Sci USA 1991;88:6303-7.
40. Hirai S, Yaniv M. Jun DNA-binding is modulated by mutations between the leucines or by direct interaction of fos with the TGACTCA sequence. Nat New Biol 1989;1:181-91.
41. Hsu MH, Chirala SS, Wakil SJ. Human fatty-acid synthase gene. Evidence for the presence of two promoters and their functional interaction. J Biol Chem 1996;271:13584-92.
42. Iannocone PM, Kozuimi J. Pattern and rate of disappearance of gamma-glutamyl transpeptidase activity in fetal and neonatal rat livers. Histochem Cytochem 1983;31:1312-6.
43. Ikeda Y, Fujii J, Anderson ME, Taniguchi N, Meister A. Involvement of Ser-451 and Ser-452 in the catalysis of human gamma-glutamyl transpeptidase. Biol Chem 1995;270:22223-8.
44. Ikeda Y, Fujii J, Taniguchi N, Meister A. Human gamma-glutamyl transpeptidase mutants involving conserved aspartate residues and. the unique cysteine residue of the light subunit. J Biol Chem 1995;270:12471-5.
45. Ishikawa T, Li ZS, Lu YP, Rea PA. The CS-X pump in plant, yeast and animal cells: Structure, function and gene expression. Biosci Rep 1997;17:189-207.
46. Ishiye M, Niwa M. Nucleotide sequence and expression in Escherichia coli of the cephalosporin acylase gene of a Pseudomonas strain. Biochim Biophys Acta 1992;1132:233-9.
47. Javahery R, Khachi A, Lo K, Zenzie-Gregory B, Smale ST. DNA sequence requirements for transcriptional initiator activity in mammalian cells. Mol Cell Biol 1994;14:116-27.
48. Joyce-Brady M, Oakes SM, Wuthrich D, Laperche Y. Three alternative promoters of the rat gamma-glutamyl transferase gene are active in developing lung and are differentially regulated by oxygen after birth. J Clin Invest 1996;97:1774-9.
49. Kaplowitz N, Aw TY, Ookhtens M. he regulation of hepatic glutathione. Annu Rev Pharmacol Toxicol 1985;25:715-44.
50. Kozak M. An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 1991;115:887-903.
51. Kugelman A, Choy HA, Liu R, Shi MM, Gozal E, Forman HJ. gammaGlutamyl transpeptidase is increased by oxidative stress in rat alveolar L2 epithelial cells. Am Respir Cell Mol Biol 1994;11:586-92.
52. Kurauchi O, Lahuna O, Darbouy M, Aggerbeck M, Chobert MN, Laperche Y. Organization of the 5′ end of the rat gamma-glutamyl transpeptidase gene: structure of a promoter active in the kidney. Biochemistry 1991;30:1618-23.
53. Lahuna O, Brouillet A, Chobert MN, Darbouy M, Okamoto T, Laperche Y. Identification of a second promoter which drives the expression of gammaglutamyl transpeptidase in rat kidney and epididymis. Biochemistry 1992;31:9190-6.
54. Lan ZJ, Palladino MA, Rudolph DB, Labus JC, Hinton BT. Identification, expression, and regulation of the transcriptional factor polyomavirus enhancer activator 3, and its putative role in regulating the expression of gammaglutamyl transpeptidase mRNA-W in the rat epididymis. Biol Reprod 1997;57:186-93.
55. Laperche Y, Bulle F, Aissani T, Chobert MN, Aggerbeck M, Hanoune J, Guellaen G. Molecular cloning and nucleotide sequence of rat kidney gamma-glutamyl transpeptidase cDNA [published erratum appears in Proc Natl Acad Sci USA 1989;86(9):31-59]. Proc Natl Acad Sci USA 1986;83:937-41.
56. 35S-labeled RNA probes. Lab Invest 1990;62:731-5.
57. Leh H. Organisation moléculaire et étude des promoteurs de la gammaglutamyl transpeptidase humaine. Thesis, Biologie et santé, Nancy I, Nancy, 1997, 134pp.
58. Leh H, Chikhi N, Ichino K, Guellaen G, Wellman M, Siest G, Visvikis A. An intronic promoter controls the expression of truncated human gammaglutamyltransferase mRNAs. FEBS Lett 1998;434:51-6.
59. Leh H, Courtay C, Gerardin P, Wellman M, Siest G, Visvikis A. Cloning and expression of a novel type (III) of human gamma-glutamyltransferase truncated mRNA. FEBS Lett 1996;394:258-62.
60. Lenardo MJ, Baltimore D. NF-kappa B: a pleiotropic mediator of inducible and tissue-specific gene control. Cell 1989;58:227-9.
61. Lieberman MW, Barrios R, Carter BZ, Habib GM, Lebovitz RM, Rajagopalan S, Sepulveda AR, Shi ZZ, Wan DR. gamma-Glutamyl transpeptidase. What does the organization and expression of a multipromoter gene tell us about its functions? Am J Pathol 1995;147:1175-85.
62. Lieberman MW, Wiseman AL, Shi ZZ, Carter BZ, Barrios R, Ou CN, Chevez-Barrios P, Wang Y, Habib GM, Goodman JC, Huang SL, Lebovitz RM, Matzuk MM. Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-defident mice. Proc Natl Acad Sci USA 1996;93:7923-6.
63. Liu RM, Hu H, Robison TW, Forman HJ. Increased gamma-glutamylcysteine synthetase and gamma-glutamyl transpeptidase activities enhance resistance of rat lung epithelial L2 cells to quinone toxicity. Am J Respir Cell Mol Biol 1996;14:192-7.
64. Liu RM, Shi MM, Giulivi C, Forman HJ. Quinones increase gamma-glutamyl transpeptidase expression by multiple mechanisms in rat lung epithelial cells. Am J Physiol 1998;274:L330-6.
65. Mandel HG, Manson MM, Judah DJ, Simpson JL, Green JA, Forrester LM, Wolf CR, Neal GE. Metabolic basis for the protective effect of the antioxidant ethoxyquin on aflatoxin B1 hepatocarcinogenesis in the rat. Cancer Res 1987;47:5218-993.
66. Marathe GV, Nash B, Haschemeyer H, Tate SS. Ultrastructural localization ofg-glutamyl transpeptidase in rat kidney and jejunum. FEBS Lett 1979;107:436-40.
67. Markey CM, Rudolph DB, Labus JC, Hinton BT. Oxidative stress differentially regulates the expression of gamma- glutamyl transpeptidase mRNAs in the initial segment of the rat epididymis. J Androl 1998;19:92-9.
68. Meister A. New developments in glutathione metabolism and their potential application in therapy. Hepatology 1984;4:739-42.
69. Mitchell PJ, Wang C, Tjian R. Positive and negative regulation of transcription in vitro: enhancer-binding protein AP-2 is inhibited by SV40 T antigen. Cell 1987;50:847-61.
70. Nomura S, Lahuna O, Suzuki T, Brouillet A, Chobert MN, Laperche Y. A specific distal promoter controls gamma-glutamyl transpeptidase gene expression in undifferentiated rat transformed liver cells. Biochem J 1997;326:311-20.
71. Oakes SM, Takahashi Y, Williams MC, Joyce-Brady M. Ontogeny of gamma-glutamyltransferase in the rat lung. Am J Physiol 1997;272:L739-44.
72. Okarnoto T, Darbouy M, Brouillet A, Lahuna O, Chobert MN, Laperche Y. Expression of the rat gamma-glutamyl transpeptidase gene from a specific promoter in the small intestine and in hepatoma cells. Biochemistry 1994;33:11536-43.
73. Palladino MA, Hinton BT. Developmental regulation of expression of multiple gamma-glutamyl transpeptidase mRNAs in the postnatal rat epididymis. Biochem Biophys Res Commun 1994;198:554-9.
74. Palladino MA, Hinton BT. Expression of multiple gamma-glutamyl transpeptidase messenger ribonucleic acid transcripts in the adult rat epididymis is differentially regulated by androgens and testicular factors in a region-specific manner. Endocrinology 1994;135:1146-56.
75. Palladino MA, Laperche Y, Hinton BT. Multiple forms of gamma-glutamyl transpeptidase messenger ribonucleic acid are expressed in the adult rat testis and epididymis. Biol Reprod 1994;50:320-8.
76. Papandrikopoulou A, Frey A, Gassen HG. Cloning and expression of gamma-glutamyl transpeptidase from isolated porcine brain capillaries. Eur J Biochem 1989;183:693-8.
77. Pawlak A, Cohen EH, Octave JN, Schweickhardt R, Wu SJ, Bulle F, Chikhi N, Baik JH, Siegrist S, Guellaen G. An alternatively processed mRNA specific for gamma-glutamyl transpeptidase in human tissues. J Biol Chem 1990;265:3256-62.
78. Pawlak A, Lahuna O, Bulle F, Suzuki A, Ferry N, Siegrist S, Chikhi N, Chobert MN, Guellaen G, Laperche Y. gamma-Glutamyl transpeptidase: a single copy gene in the rat and a multigene family in the human genome. J Biol Chem 1988;263:9913-6.
79. Pawlak A, Wu SJ, Bulle F, Suzuki A, Chikhi N, Ferry N, Baik JH, Siegrist S, Guellaen G. Different gamma-glutamyl transpeptidase mRNAs are expressed in human liver and kidney. Biochem Biophys Res Commun 1989;164:912-28.
80. Peltz SW, Brewer G, Bernstein P, Hart PA, Ross J. Regulation of mRNA turnover in eukaryotic cells. Crit Rev Eukaryotic Gene Expr 1991;1:99-126.
81. Power CA, Griffiths SA, Simpson JL, Laperche Y, Guellaen G, Manson MM. Induction of gamma-glutamyl transpeptidase mRNA by aflatoxin B1 and ethoxyquin in rat liver. Carcinogenesis 1987;8:737-40.
82. Rabito CA, Kreisberg JI, Wight D. Alkaline phosphatase and gammaglutamyl transpeptidase as polarization markers during the organization of LLC-PK1 cells into an epithelial membrane. J Biol Chem 1984;259:574-82.
83. Rajagopalan S, Park JH, Patel PD, Lebovitz RM, Lieberman MW. Cloning and analysis of the rat gamma-glutamyltransferase gene. J Biol Chem 1990;265:11721-5.
84. Rajpert-De Meyts E, Heisterkamp N, Groffen J. Cloning and nucleotide sequence of human gamma-glutamyl transpeptidase. Proc Natl Acad Sci USA 1988;85:8840-4.
85. Reed DJ, Fariss MW. Glutathione depletion and susceptibility. Pharmacol Rev 1984;36:25S-33.
86. Ritter JK, Chen F, Sheen YY, Tran HM, Kimura S, Yeatman MT, Owens IS. A novelcomplex locus UGT1 encodes human bilirubin, phenol, and other UDP-glucuronosyltransferase isozymes with identical carboxyl termini. Biol Chem 1992;267:3257-61.
87. Rudolph DB, Hinton BT. Stability and transcriptional regulation of gamma-glutamyl transpeptidase mRNA expression in the initial segment of the rat epididymis. J Androl 1997;18:501-12.
88. 2-induced changes in lung and storage pool thiols in mice: effect of superoxide dismutase. J Appl Physiol 1993;74:989-97.
89. Rushmore TH, Morton MR, Pickett CB. The antioxidant responsive element. Activation by oxidative stress and identification of the DNA consensus sequence required for functional activity. J Biol Chem 1991;266:11632-9.
90. Sakamuro D, Yamazoe M, Matsuda Y, Kangawa K, Taniguchi N, Matsuo H, Yoshikawa H, Ogasawara N. The primary structure of human gamma-glutamyl transpeptidase. Gene 1988;73:1-9.
91. Scambler PJ. Deletions of human chromosome 22 and associated birth defects. Curr Opin Genet Dev 1993;3:432-7.
92. Schaffner DL, Barrios R, Massey C, Banez EI, Ou CN, Rajagopalan S, Aguilar-Cordova E, Lebovitz RM, Overbeek PA, Lieberman MW. Targeting of the rasT24 oncogene to the proximal convoluted tubules in transgenic mice results in hyperplasia and polycystic kidneys. Am J Pathol 1993;142:1051-60.
93. Schudy A, Bangsow T, Flach R, Trost C, Schepelmann S, Weber P, Knupfer E, Gassen HG. Organization of the 5′-end of the porcine gamma-glutamyl transpeptidase gene and identification of three different mRNAs in the kidney. Biochem Biophys Res Commun 1996;229:693-700.
94. Semenza G. Anchoring and biosynthesis of stalked brush border membrane proteins: glycosidases and peptidases of enterocytes and renal tubuli. Annu Rev Cell Biol 1986;2:255-313.
95. Sen CK, Packer L. Antioxidant and redox regulation of gene transcription. FASEB J 1996;10:709-20.
96. Sepulveda AR, Huang SL, Lebovitz RM, Lieberman MW. A 346-base pair region of the mouse gamma-glutamyl transpeptidase type II promoter contains sufficient cis-acting elements for kidney-restricted expression in transgenic mice. Biol Chem 1997;272:11959-67.
97. Shi NIM, Kugelman A, Iwamoto T, Tian L, Forman HJ. Quinone-induced oxidative stress elevates glutathione and induces gamma-glutamylcysteine synthetase activity in rat lung epithelial L2 cells. J Biol Chem 1994;269:26512-7.
98. Shi ZZ, Habib GM, Lebovitz RM, Lieberman MW. Cloning of cDNA and genomic structure of the mouse gamma-glutamyl transpeptidase-encoding gene. Gene 1995;167:233-7.
99. Siegrist S, Laperche Y, Chobert MN, Bulle F, Nakhasi HL, Guellaen G. Regulation of mouse mammary-gland gamma-glutamyltranspeptidase mRNA during pregnancy, lactation and weaning. Biochem J 1990;267:621-4.
100. Sierra-Rivera E, Meredith NU, Summar ML, Smith NW, Voorhees GJ, Stoffel CM, Freeman ML. Genes regulating glutathione concentrations in X-ray-transformed rat embryo fibroblasts: changes in gamma-glutamylcysteine synthetase and gamma-glutamyltranspeptidase expression. Carcinogenesis 1994;15:1301-7.
101. Smith TK, Meister A. Chemical modification of active site residues in gamma-glutamyl transpeptidase. Aspartate 422 and cysteine 453. J Biol Chem 1995;270:12476-80.
102. Speisky H, Shackel N, Varghese G, Wade D, Israel Y. Role of hepatic gamma-glutamyltransferase in the degradation of circulating glutathione: studies in the intact guinea pig perfused liver. Hepatology 1990;11:843-9.
103. Stauffer JK, Colbert MC, Ciejek-Baez E. Nonconservative utilization of aldolase A alternative promoters. J Biol Chem 1990;265:11773-82.
104. Suzuki T, Okuno H, Yoshida T, Endo T, Nishina H, Iba H. Difference in transcriptional regulatory function between c-Fos and Fra-2. Nucleic Acids Res 1991;19:5537-42.
105. Tacchini L, Pogliaghi G, Radice L, Anzon E, Bernelli-Zazzera A. Differential activation of heat-shock and oxidation-specific stress genes in chemically induced oxidative stress. Biochem J 1995;309:453-9.
106. Tate SS, Meister A. Affinity labeling of gamma-glutamyl transpeptidase and location of the gamma-glutamyl binding site on the light subunit. Proc Natl Acad Sci USA 1977;74:931-5.
107. Tate SS, Meister A. gamma-Glutamyl transpeptidase: catalytic, structural and functional aspects. Mol Cell Biochem 1981;39:357-68.
108. Tenhunen J, Salminen M, Jalanko A, Ukkonen S, Ulmanen I. Structure of the rat catechol-O-methyltransferase gene: separate promoters are used to produce mRNAs for soluble and membrane-bound forms of the enzyme. DNA Cell Biol 1993;12:253-63.
109. Verdi JM, Campagnoni AT. Translational regulation by steroids. Identification of a steroid modulatory element in the S-untranslated region of the myelin basic protein messenger RNA. Biol Chem 1990;265:20314-20.
110. Wapnir RA, Mancusi VJ, Goldstein LA. Comparative ontogenesis of gamma-glutamyl transpeptidase in rat tissues. Experientia 1982;38:647-8.
111. Wetmore LA, Gerard C, Drazen JM. Human lung expresses unique gamma-glutamyl transpeptidase transcripts. Proc Natl Acad Sci USA 1993;90:7461-5.
112. Wilhelm D, Bender K, Knebel A, Angel P. The level of intracellular glutathione is a key regulator for the induction of stress-activated signal transduction pathways including Jun N-terminal protein kinases and p38 kinase by alkylating agents. Mol Cell Biol 1997;17:4792-800.
113. Wolff JEA, Belloni-Olivi L, Bressler JP, Goldstein GW. Glutamyl transpeptidase activity in brain microvessels exhibits regional heterogeneity. J Neurochem 1992;58:909-15.