Gamma-glutamyl transferases: A structural, mechanistic and physiological perspective

Abstract

Gamma glutamyl transferases (GGT) are highly conserved enzymes that occur from bacteria to humans. They remove terminal γ-glutamyl residue from peptides and amides. GGTs play an important role in the homeostasis of glutathione (a major cellular antioxidant) and in the detoxification of xenobiotics in mammals. They are implicated in diseases like diabetes, inflammation, neurodegenerative diseases and cardiovascular diseases. The physiological role of GGTs in bacteria is still unclear. Nothing is known about the basis for the strong conservation of the enzyme across the living system. The review focuses on the enzyme’s physiology, chemistry and structural properties of the enzyme with emphasis on the evolutionary relationships. The available data indicate that the members of the GGT family share common structural features but are functionally heterogenous.

Keywords

Gamma glutamyl transferase / Ntn hydrolase / structure / catalysis / function

References

[1] Anderson M E, Allison R D, Meister A (1982). Interconversion of leukotrienes catalyzed by purified gamma-glutamyl transpeptidase: concomitant formation of leukotriene D4 and gamma-glutamyl amino acids. Proc Natl Acad Sci USA, 79(4): 1088–1091

[2] Arendt C S, Hochstrasser M (1999). Eukaryotic 20S proteasome catalytic subunit propeptides prevent active site inactivation by N-terminal acetylation and promote particle assembly. EMBO J, 18(13): 3575–3585

[3] Benlloch M, Ortega A, Ferrer P, Segarra R, Obrador E, Asensi M, Carretero J, Estrela J M (2005). Acceleration of glutathione efflux and inhibition of gamma-glutamyltranspeptidase sensitize metastatic B16 melanoma cells to endothelium-induced cytotoxicity. J Biol Chem, 280(8): 6950–6959

[4] Boanca G, Sand A, Barycki J J (2006). Uncoupling the enzymatic and autoprocessing activities of Helicobacter pylori gamma-glutamyltranspeptidase. J Biol Chem, 281(28): 19029–19037

[5] Boanca G, Sand A, Okada T, Suzuki H, Kumagai H, Fukuyama K, Barycki J J (2007). Autoprocessing of Helicobacter pylori gamma-glutamyltranspeptidase leads to the formation of a threonine-threonine catalytic dyad. J Biol Chem, 282(1): 534–541

[6] Boanca G, Sand A, Okada T, Suzuki H, Kumagai H, Fukuyama K, Barycki J J (2007). Autoprocessing of Helicobacter pylori gamma-glutamyltranspeptidase leads to the formation of a threonine-threonine catalytic dyad. J Biol Chem, 282(1): 534–541

[7] Bochtler M, Ditzel L, Groll M, Huber R (1997). Crystal structure of heat shock locus V (HslV) from Escherichia coli. Proc Natl Acad Sci USA, 94(12): 6070–6074

[8] Bompard-Gilles C, Villeret V, Davies G J, Fanuel L, Joris B, Frère J M, Van Beeumen J (2000). A new variant of the Ntn hydrolase fold revealed by the crystal structure of L-aminopeptidase D-ala-esterase/amidase from Ochrobactrum anthropi. Structure, 8(2): 153–162

[9] Brannigan J A, Dodson G, Duggleby H J, Moody P C, Smith J L, Tomchick D R, Murzin A G (1995). A protein catalytic framework with an N-terminal nucleophile is capable of self-activation. Nature, 378(6555): 416–419

[10] Candela T, Fouet A (2006). Poly-gamma-glutamate in bacteria. Mol Microbiol, 60(5): 1091–1098

[11] Carter B Z, Shi Z Z, Barrios R, Lieberman M W (1998). gamma-glutamyl leukotrienase, a gamma-glutamyl transpeptidase gene family member, is expressed primarily in spleen. J Biol Chem, 273(43): 28277–28285

[12] Carter B Z, Wiseman A L, Orkiszewski R, Ballard K D, Ou C N, Lieberman M W (1997). Metabolism of leukotriene C4 in gamma-glutamyl transpeptidase-deficient mice. J Biol Chem, 272(19): 12305–12310

[13] Castonguay R, Lherbet C, Keillor J W (2003). Kinetic studies of rat kidney gamma-glutamyltranspeptidase deacylation reveal a general base-catalyzed mechanism. Biochemistry, 42(39): 11504–11513

[14] Chevalier C, Thiberge J M, Ferrero R L, Labigne A (1999). Essential role of Helicobacter pylori gamma-glutamyltranspeptidase for the colonization of the gastric mucosa of mice. Mol Microbiol, 31(5): 1359–1372

[15] Chikhi N, Holic N, Guellaen G, Laperche Y (1999). Gamma-glutamyl transpeptidase gene organization and expression: a comparative analysis in rat, mouse, pig and human species. Comp Biochem Physiol B Biochem Mol Biol, 122(4): 367–380

[16] Cook N D, Upperton K P, Challis B C, Peters T J (1987). The donor specificity and kinetics of the hydrolysis reaction of gamma-glutamyltransferase. Biochim Biophys Acta, 914(3): 240–245

[17] Duggleby H J, Tolley S P, Hill C P, Dodson E J, Dodson G, Moody P C (1995). Penicillin acylase has a single-amino-acid catalytic centre. Nature, 373(6511): 264–268

[18] Dunbar J A, Ogston S A, Ritchie A, Devgun M S, Hagart J, Martin B T (1985). Are problem drinkers dangerous drivers? An investigation of arrest for drinking and driving, serum gamma glutamyltranspeptidase activities, blood alcohol concentrations, and road traffic accidents: the Tayside Safe Driving Project. Br Med J (Clin Res Ed), 290(6471): 827–830

[19] Elce J S, Broxmeyer B (1976). γ-glutamyltransferase of rat kidney. Simultaneous assay of the hydrolysis and transfer reactions with (glutamate-14C)glutathione. Biochem J, 153(2): 223–232

[20] Elkins J M, Kershaw N J, Schofield C J (2005). X-ray crystal structure of ornithine acetyltransferase from the clavulanic acid biosynthesis gene cluster. Biochem J, 385(Pt 2): 565–573

[21] Galivan J, Ryan T J, Chave K, Rhee M, Yao R, Yin D (2000). Glutamyl hydrolase. pharmacological role and enzymatic characterization. Pharmacol Ther, 85(3): 207–215

[22] Gardell S J, Tate S S (1980). Affinity labeling of gamma-glutamyl transpeptidase by glutamine antagonists. Effects of the gamma-glutamyl transferase and proteinase activities. FEBS Lett, 122(2): 171–174

[23] Gardell S J, Tate S S (1983). Effects of bile acids and their glycine conjugates on gamma-glutamyl transpeptidase. J Biol Chem, 258(10): 6198–6201

[24] Gjerde H, Sakshaug J, Mørland J (1986). Heavy drinking among Norwegian male drunken drivers: a study of gamma-glutamyltransferase. Alcohol Clin Exp Res, 10(2): 209–212

[25] Gouet P, Courcelle E, Stuart D I, Métoz F (1999). ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics, 15(4): 305–308

[26] Gounni A S, Spanel-Borowski K, Palacios M, Heusser C, Moncada S, Lobos E (2001). Pulmonary inflammation induced by a recombinant Brugia malayi gamma-glutamyl transpeptidase homolog: involvement of humoral autoimmune responses. Mol Med, 7(5): 344–354

[27] Guo H C, Xu Q, Buckley D, Guan C (1998). Crystal structures of Flavobacterium glycosylasparaginase. An N-terminal nucleophile hydrolase activated by intramolecular proteolysis. J Biol Chem, 273(32): 20205–20212

[28] Han L, Hiratake J, Tachi N, Suzuki H, Kumagai H, Sakata K (2006). Gamma-(monophenyl)phosphono glutamate analogues as mechanism-based inhibitors of gamma-glutamyl transpeptidase. Bioorg Med Chem, 14(17): 6043–6054

[29] Hanigan M H (1995). Expression of gamma-glutamyl transpeptidase provides tumor cells with a selective growth advantage at physiological concentrations of cyst(e)ine. Carcinogenesis, 16(2): 181–185

[30] Hashimoto Y, Futamura A, Nakarai H, Nakahara K (2001). Relationship between response of gamma-glutamyl transpeptidase to alcohol drinking and risk factors for coronary heart disease. Atherosclerosis, 158(2): 465–470

[31] Heisterkamp N, Rajpert-De Meyts E, Uribe L, Forman H J, Groffen J (1991). Identification of a human gamma-glutamyl cleaving enzyme related to, but distinct from, gamma-glutamyl transpeptidase. Proc Natl Acad Sci USA, 88(14): 6303–6307

[32] Hinchman C A, Matsumoto H, Simmons T W, Ballatori N (1991). Intrahepatic conversion of a glutathione conjugate to its mercapturic acid. Metabolism of 1-chloro-2,4-dinitrobenzene in isolated perfused rat and guinea pig livers. J Biol Chem, 266(33): 22179–22185

[33] Huseby N E (1977). Purification and some properties of gamma-glutamyltransferase from human liver. Biochim Biophys Acta, 483(1): 46–56

[34] Ikeda Y, Fujii J, Anderson M E, Taniguchi N, Meister A (1995). Involvement of Ser-451 and Ser-452 in the catalysis of human gamma-glutamyl transpeptidase. J Biol Chem, 270(38): 22223–22228

[35] Ikeda Y, Fujii J, Taniguchi N, Meister A (1995). Expression of an active glycosylated human gamma-glutamyl transpeptidase mutant that lacks a membrane anchor domain. Proc Natl Acad Sci USA, 92(1): 126–130

[36] Ikeda Y, Taniguchi N (2005). Gene expression of gamma-glutamyltranspeptidase. Methods Enzymol, 401: 408–425

[37] Inoue M, Hiratake J, Suzuki H, Kumagai H, Sakata K (2000). Identification of catalytic nucleophile of Escherichia coli gamma-glutamyltranspeptidase by gamma-monofluorophosphono derivative of glutamic acid: N-terminal thr-391 in small subunit is the nucleophile. Biochemistry, 39(26): 7764–7771

[38] Ishikawa T, Hasegawa S, Kasai T, Obata Y (1967). Changes in amino acid composition during germination of soybean Part IV Identification of α- and γ-glutamylaspartic acid. Agric Biol Chem, 31(4): 490–493

[39] Isupov M N, Obmolova G, Butterworth S, Badet-Denisot M A, Badet B, Polikarpov I, Littlechild J A, Teplyakov A (1996). Substrate binding is required for assembly of the active conformation of the catalytic site in Ntn amidotransferases: evidence from the 1.8 A crystal structure of the glutaminase domain of glucosamine 6-phosphate synthase. Structure, 4(7): 801–810

[40] Karkowsky A M, Bergamini M V W, Orlowski M (1976). Kinetic studies of sheep kidney gamma-glutamyl transpeptidase. J Biol Chem, 251(15): 4736–4743

[41] Kasai T, Ohmiya A, Sakamura S (1982). γ-Glutamyltranspeptidases in the metabolism of γ-glutamyl peptides in plants. Phytochemistry, 21(6): 1233–1239

[42] Kawasaki Y, Ogawa T, Sasaoka K (1982). Occurrence and some properties of a novel γ-glutamyl transpeptidase responsible for the synthesis of γ-L-glutamyl-D-alanine in pea seedlings. Biochim Biophys Acta, 716(2): 194–200

[43] Kean E A, Hare E R (1980). γ-Glutamyl transpeptidase of the ackee plant. Phytochemistry, 19(2): 194–203

[44] Keillor J W, Castonguay R, Lherbet C (2005). Gamma-glutamyl transpeptidase substrate specificity and catalytic mechanism. Methods Enzymol, 401: 449–467

[45] Keillor J W, Menard A, Castonguay R, Lherbet C, Rivard C (2004). Pre-steady-state kinetic studies of rat kidney γ-glutamyl transpeptidase confirm its ping-pong mechanism. J Phys Org Chem, 17(67): 529–536

[46] Kim J H, Krahn J M, Tomchick D R, Smith J L, Zalkin H (1996). Structure and function of the glutamine phosphoribosylpyrophosphate amidotransferase glutamine site and communication with the phosphoribosylpyrophosphate site. J Biol Chem, 271(26): 15549–15557

[47] Kim Y, Yoon K H, Khang Y, Turley S, Hol W G (2000). The 2.0 A crystal structure of cephalosporin acylase. Structure, 8(10): 1059–1068

[48] Kimura K, Itoh Y (2003). Characterization of poly-gamma-glutamate hydrolase encoded by a bacteriophage genome: possible role in phage infection of Bacillus subtilis encapsulated with poly-gamma-glutamate. Appl Environ Microbiol, 69(5): 2491–2497

[49] Kimura K, Tran L S, Uchida I, Itoh Y (2004). Characterization of Bacillus subtilis gamma-glutamyltransferase and its involvement in the degradation of capsule poly-gamma-glutamate. Microbiology, 150(Pt 12): 4115–4123

[50] King J B, West M B, Cook P F, Hanigan M H (2009). A novel, species-specific class of uncompetitive inhibitors of γ-glutamyl transpeptidase. J Biol Chem, 284(14): 9059–9065

[51] Kumar R S, Brannigan J A, Prabhune A A, Pundle A V, Dodson G G, Dodson E J, Suresh C G (2006). Structural and functional analysis of a conjugated bile salt hydrolase from Bifidobacterium longum reveals an evolutionary relationship with penicillin V acylase. J Biol Chem, 281(43): 32516–32525

[52] Lee D H, Ha M H, Kim J H, Christiani D C, Gross M D, Steffes M, Blomhoff R, Jacobs D R Jr (2003). Gamma-glutamyltransferase and diabetes—a 4 year follow-up study. Diabetologia, 46(3): 359–364

[53] Lee Y S, Kim H W, Park S S (2000). The role of alpha-amino group of the N-terminal serine of beta subunit for enzyme catalysis and autoproteolytic activation of glutaryl 7-aminocephalosporanic acid acylase. J Biol Chem, 275(50): 39200–39206

[54] Leustek T, Martin M N, Bick J A, Davies J P (2000). Pathways and regulation of sulfur metabolism revealed through molecular and genetic studies. Annu Rev Plant Physiol Plant Mol Biol, 51(1): 141–165

[55] Lherbet C, Keillor J W (2004). Probing the stereochemistry of the active site of gamma-glutamyl transpeptidase using sulfur derivatives of l-glutamic acid. Org Biomol Chem, 2(2): 238–245

[56] Lherbet C, Keillor J W (2004). Probing the stereochemistry of the active site of gamma-glutamyl transpeptidase using sulfur derivatives of l-glutamic acid. Org Biomol Chem, 2(2): 238–245

[57] Li Y, Chen J, Jiang W, Mao X, Zhao G, Wang E (1999). In vivo post-translational processing and subunit reconstitution of cephalosporin acylase from Pseudomonas sp. 130. Eur J Biochem, 262(3): 713–719

[58] Lieberman M W, Wiseman A L, Shi Z Z, Carter B Z, Barrios R, Ou C N, Chévez-Barrios P, Wang Y, Habib G M, Goodman J C, Huang S L, Lebovitz R M, Matzuk M M (1996). Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-deficient mice. Proc Natl Acad Sci USA, 93(15): 7923–7926

[59] Lieberman M W, Wiseman A L, Shi Z Z, Carter B Z, Barrios R, Ou C N, Chévez-Barrios P, Wang Y, Habib G M, Goodman J C, Huang S L, Lebovitz R M, Matzuk M M (1996). Growth retardation and cysteine deficiency in gamma-glutamyl transpeptidase-deficient mice. Proc Natl Acad Sci USA, 93(15): 7923–7926

[60] London R E, Gabel S A (2001). Development and evaluation of a boronate inhibitor of gamma-glutamyl transpeptidase. Arch Biochem Biophys, 385(2): 250–258

[61] Löwe J, Stock D, Jap B, Zwickl P, Baumeister W, Huber R (1995). Crystal structure of the 20S proteasome from the archaeon T. acidophilum at 3.4 A resolution. Science, 268(5210): 533–539

[62] Martin M N, Slovin J P (2000). Purified gamma-glutamyl transpeptidases from tomato exhibit high affinity for glutathione and glutathione S-conjugates. Plant Physiol, 122(4): 1417–1426

[63] Mathew M W, Chen Y, Wickham S (2013). Novel insights into eukaryotic γ-glutamyl transpeptidase 1from the crystal structure of the glutamate-bound human enzyme. J Biol Chem, (In press)

[64] Mayatepek E, Okun J G, Meissner T, Assmann B, Hammond J, Zschocke J, Lehmann W D (2004). Synthesis and metabolism of leukotrienes in gamma-glutamyl transpeptidase deficiency. J Lipid Res, 45(5): 900–904

[65] Mehdi K, Thierie J, Penninckx M J (2001). gamma-Glutamyl transpeptidase in the yeast Saccharomyces cerevisiae and its role in the vacuolar transport and metabolism of glutathione. Biochem J, 359(Pt 3): 631–637

[66] Meister A (1973). On the enzymology of amino acid transport. Science, 180(4081): 33–39

[67] Ménard A, Castonguay R, Lherbet C, Rivard C, Roupioz Y, Keillor J W (2001). Nonlinear free energy relationship in the general-acid-catalyzed acylation of rat kidney gamma-glutamyl transpeptidase by a series of gamma-glutamyl anilide substrate analogues. Biochemistry, 40(42): 12678–12685

[68] Mesiter A, Anderson M E (1973). Glutathione. Annu Rev Biochem, 52(1): 711–760

[69] Michalska K, Brzezinski K, Jaskolski M (2005). Crystal structure of isoaspartyl aminopeptidase in complex with L-aspartate. J Biol Chem, 280(31): 28484–28491

[70] Minami H, Suzuki H, Kumagai H (2003). A mutant Bacillus subtilis gamma-glutamyltranspeptidase specialized in hydrolysis activity. FEMS Microbiol Lett, 224(2): 169–173

[71] Minami H, Suzuki H, Kumagai H (2004). Gamma-glutamyltranspeptidase, but not YwrD, is important in utilization of extracellular glutathione as a sulfur source in Bacillus subtilis. J Biol Chem, 186: 1213–1214

[72] Nakayama R, Kumagai H, Tochikura T (1984). Gamma-glutamyltranspeptidase from Proteus mirabilis: localization and activation by phospholipids. J Bacteriol, 160(3): 1031–1036

[73] Nemesánszky E, Lott J A (1985). Gamma-glutamyltransferase and its isoenzymes: progress and problems. Clin Chem, 31(6): 797–803

[74] Niederau C, Niederau M, Strohmeyer G, Bertling L, Sonnenberg A (1990). Does acute consumption of large alcohol amounts lead to pancreatic injury? A prospective study of serum pancreatic enzymes in 300 drunken drivers. Digestion, 45(2): 115–120

[75] Niida S, Kawahara M, Ishizuka Y, Ikeda Y, Kondo T, Hibi T, Suzuki Y, Ikeda K, Taniguchi N (2004). Gamma-glutamyltranspeptidase stimulates receptor activator of nuclear factor-kappaB ligand expression independent of its enzymatic activity and serves as a pathological bone-resorbing factor. J Biol Chem, 279(7): 5752–5756

[76] Obrador E, Carretero J, Ortega A, Medina I, Rodilla V, Pellicer J A, Estrela J M (2002). Gamma-glutamyl transpeptidase overexpression increases metastatic growth of B16 melanoma cells in the mouse liver. Hepatology, 35(1): 74–81

[77] Oertli M, Noben M, Engler D B, Semper R P, Reuter S, Maxeiner J, Gerhard M, Taube C, Müller A (2013). Helicobacter pylori γ-glutamyl transpeptidase and vacuolating cytotoxin promote gastric persistence and immune tolerance. Proc Natl Acad Sci USA, 110(8): 3047–3052

[78] Ogawa Y, Hosoyama H, Hamano M, Motai H (1991). Purification and properties of gamma-glutamyltranspeptidase from Bacillus subtilis (natto). Agric Biol Chem, 55(12): 2971–2977

[79] Okada T, Suzuki H, Wada K, Kumagai H, Fukuyama K (2006). Crystal structures of gamma-glutamyltranspeptidase from Escherichia coli, a key enzyme in glutathione metabolism, and its reaction intermediate. Proc Natl Acad Sci USA, 103(17): 6471–6476

[80] Okada T, Suzuki H, Wada K, Kumagai H, Fukuyama K (2006). Crystal structures of gamma-glutamyltranspeptidase from Escherichia coli, a key enzyme in glutathione metabolism, and its reaction intermediate. Proc Natl Acad Sci USA, 103(17): 6471–6476

[81] Okada T, Suzuki H, Wada K, Kumagai H, Fukuyama K (2007). Crystal structure of the gamma-glutamyltranspeptidase precursor protein from Escherichia coli. Structural changes upon autocatalytic processing and implications for the maturation mechanism. J Biol Chem, 282(4): 2433–2439

[82] Ortega A L, Carretero J, Obrador E, Gambini J, Asensi M, Rodilla V, Estrela J M (2003). Tumor cytotoxicity by endothelial cells. Impairment of the mitochondrial system for glutathione uptake in mouse B16 melanoma cells that survive after in vitro interaction with the hepatic sinusoidal endothelium. J Biol Chem, 278(16): 13888–13897

[83] Pei J, Grishin N V (2003). Peptidase family U34 belongs to the superfamily of N-terminal nucleophile hydrolases. Protein Sci, 12(5): 1131–1135

[84] Pompella A, De Tata V, Paolicchi A, Zunino F (2006). Expression of gamma-glutamyltransferase in cancer cells and its significance in drug resistance. Biochem Pharmacol, 71(3): 231–238

[85] Rawlings N D, Morton F R, Barrett A J (2006). MEROPS: the peptidase database. Nucleic Acids Res, 34(Suppl 1): D270–D272

[86] Saridakis V, Christendat D, Thygesen A, Arrowsmith C H, Edwards A M, Pai E F (2002). Crystal structure of Methanobacterium thermoautotrophicum conserved protein MTH1020 reveals an NTN-hydrolase fold. Proteins, 48(1): 141–143

[87] Scouller K, Conigrave K M, Macaskill P, Irwig L, Whitfield J B (2000). Should we use carbohydrate-deficient transferrin instead of gamma-glutamyltransferase for detecting problem drinkers? A systematic review and metaanalysis. Clin Chem, 46(12): 1894–1902

[88] Sharath B, Prabhune AA, Suresh CG, Wilkinson AJ, Brannigan JA (2010). Crystal structure of Gamma Glutamyl Transferase from Bacillus subtilis. Protein Data Bank deposit ID 2v36

[89] Shaw L M, London J W, Fetterolf D, Garfinkel D (1977). Gamma-Glutamyltransferase: kinetic properties and assay conditions when gamma-glutamyl-4-nitroanilide and its 3-carboxy derivative are used as donor substrates. Clin Chem, 23(1): 79–85

[90] Shaw L M, London J W, Petersen L E (1978). Isolation of gamma-glutamyltransferase from human liver, and comparison with the enzyme from human kidney. Clin Chem, 24(6): 905–915

[91] Shaw L M, Strømme J H, London J L, Theodorsen L (1983). International Federation of Clinical Chemistry. Scientific Committee, Analytical Section. Expert Panel on Enzymes. IFCC methods for measurement of enzymes. Part 4. IFCC methods for gamma-glutamyltransferase ((gamma-glutamyl)-peptide: amino acid gamma-glutamyltransferase, EC 2.3.2.2). IFCC Document, Stage 2, Draft 2, 1983-01 with a view to an IFCC Recommendation. Clin Chim Acta, 135(3): 315F–338F

[92] Sherwood R F, Melton R G, Alwan S M, Hughes P (1985). Purification and properties of carboxypeptidase G2 from Pseudomonas sp. strain RS-16. Use of a novel triazine dye affinity method. Eur J Biochem, 148(3): 447–453

[93] Sian J, Dexter D T, Lees A J, Daniel S, Jenner P, Marsden C D (1994). Glutathione-related enzymes in brain in Parkinson’s disease. Ann Neurol, 36(3): 356–361

[94] Singh J C, Chander J, Singh S, Singh G, Atal C K (1986). gamma-Glutamyl transpeptidase: a novel biochemical marker in inflammation. Biochem Pharmacol, 35(21): 3753–3760

[95] Smith T K, Ikeda Y, Fujii J, Taniguchi N, Meister A (1995). Different sites of acivicin binding and inactivation of gamma-glutamyl transpeptidases. Proc Natl Acad Sci USA, 92(6): 2360–2364

[96] Smith T K, Meister A (1994). Active deglycosylated mammalian gamma-glutamyl transpeptidase. FASEB J, 8(9): 661–664

[97] Storozhenko S, Belles-Boix E, Babiychuk E, Hérouart D, Davey M W, Slooten L, Van Montagu M, Inzé D, Kushnir S (2002). Gamma-glutamyl transpeptidase in transgenic tobacco plants. Cellular localization, processing, and biochemical properties. Plant Physiol, 128(3): 1109–1119

[98] Stromme J H, Theodorsen L (1976). Gamma-glutamyltransferase: Substrate inhibition, kinetic mechanism, and assay conditions. Clin Chem, 22(4): 417–421

[99] Suresh C G, Pundle A V, SivaRaman H, Rao K N, Brannigan J A, McVey C E, Verma C S, Dauter Z, Dodson E J, Dodson G G (1999). Penicillin V acylase crystal structure reveals new Ntn-hydrolase family members. Nat Struct Biol, 6(5): 414–416

[100] Suzuki H, Hashimoto W, Kumagai H (1993). Escherichia coli K-12 can utilize an exogenous gamma-glutamyl peptide as an amino acid source, for which gamma-glutamyltranspeptidase is essential. J Bacteriol, 175(18): 6038–6040

[101] Suzuki H, Kumagai H (2002). Autocatalytic processing of gamma-glutamyltranspeptidase. J Biol Chem, 277(45): 43536–43543

[102] Suzuki H, Kumagai H, Tochikura T (1986). Gamma-glutamyltranspeptidase from Escherichia coli K-12: formation and localization. J Bacteriol, 168(3): 1332–1335

[103] Suzuki H, Kumagai H, Tochikura T (1986). Gamma-glutamyltranspeptidase from Escherichia coli K-12: purification and properties. J Bacteriol, 168(3): 1325–1331

[104] Suzuki H, Miwa C, Ishihara S, Kumagai H (2004). A single amino acid substitution converts gamma-glutamyltranspeptidase to a class IV cephalosporin acylase (glutaryl-7-aminocephalosporanic acid acylase). Appl Environ Microbiol, 70(10): 6324–6328

[105] Szasz G (1969). A kinetic photometric method for serum gamma-glutamyl transpeptidase. Clin Chem, 15(2): 124–136

[106] Takahashi H, Hirose K, Watanabe H (2004). Necessity of meningococcal gamma-glutamyl aminopeptidase for Neisseria meningitidis growth in rat cerebrospinal fluid (CSF) and CSF-like medium. J Bacteriol, 186(1): 244–247

[107] Takahashi H, Watanabe H (2004). Post-translational processing of Neisseria meningitidis gamma-glutamyl aminopeptidase and its association with inner membrane facing to the cytoplasmic space. FEMS Microbiol Lett, 234(1): 27–35

[108] Tanaka T O, Hirata T, Futamura K, et al (1993). Purification and characterization of poly (γ-glutamic acid) hydrolase from a filamentous fungus, Myrothecium sp. TM 4222. Biosci Biotechnol Biochem, 57(12): 2148–2153

[109] Taniguchi N, Ikeda Y (1998). gamma-Glutamyl transpeptidase: catalytic mechanism and gene expression. Adv Enzymol Relat Areas Mol Biol, 72: 239–278

[110] Tate S S, Meister A (1974). Interaction of gamma-glutamyl transpeptidase with amino acids, dipeptides, and derivatives and analogs of glutathione. J Biol Chem, 249(23): 7593–7602

[111] Tate S S, Meister A (1974). Stimulation of the hydrolytic activity and decrease of the transpeptidase activity of gamma-glutamyl transpeptidase by maleate; identity of a rat kidney maleate-stimulated glutaminase and gamma-glutamyl transpeptidase. Proc Natl Acad Sci USA, 71(9): 3329–3333

[112] Tate S S, Meister A (1977). Affinity labeling of gamma-glutamyl transpeptidase and location of the gamma-glutamyl binding site on the light subunit. Proc Natl Acad Sci USA, 74(3): 931–935

[113] Tate S S, Meister A (1978). Serine-borate complex as a transition-state inhibitor of gamma-glutamyl transpeptidase. Proc Natl Acad Sci USA, 75(10): 4806–4809

[114] Tate S S, Meister A (1985). gamma-Glutamyl transpeptidase from kidney. Methods Enzymol, 113: 400–419

[115] Thompson G A, Meister A (1977). Interrelationships between the binding sites for amino acids, dipeptides, and gamma-glutamyl donors in gamma-glutamyl transpeptidase. J Biol Chem, 252(19): 6792–6798

[116] Thompson G A, Meister A (1980). Modulation of gamma-glutamyl transpeptidase activities by hippurate and related compounds. J Biol Chem, 255(5): 2109–2113

[117] Thompson J D, Higgins D G, Gibson T J (1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res, 22(22): 4673–4680

[118] Toller I M, Neelsen K J, Steger M, Hartung M L, Hottiger M O, Stucki M, Kalali B, Gerhard M, Sartori A A, Lopes M, Müller A (2011). Carcinogenic bacterial pathogen Helicobacter pylori triggers DNA double-strand breaks and a DNA damage response in its host cells. Proc Natl Acad Sci USA, 108(36): 14944–14949

[119] Volcani B E, Margalith P (1957). A new species (Flavobacterium polyglutamicum) which hydrolyzes the gamma-L-glutamyl bond in polypeptides. J Bacteriol, 74(5): 646–655

[120] Wada K, Irie M, Suzuki H, Fukuyama K (2010). Crystal structure of the halotolerant gamma-glutamyltranspeptidase from Bacillus subtilis in complex with glutamate reveals a unique architecture of the solvent-exposed catalytic pocket. FEBS J, 277(4): 1000–1009

[121] Webb E C (1992). Enzyme Nomenclature 1992 Recommendations of the Nomenclature Committee of the International Union of Biochemistry and Molecular Biology on the Nomenclature and Classification of Enzymes, International Union of Biochemistry and Molecular Biology. San Diego, Calif, USA: Academic Press, 6th edition

[122] Whitfield J B (2001). Gamma glutamyl transferase. Crit Rev Clin Lab Sci, 38(4): 263–355

[123] Whitfield J B, Pounder R E, Neale G, Moss D W (1972). Serum-glytamyl transpeptidase activity in liver disease. Gut, 13(9): 702–708

[124] Xu K, Strauch M A (1996). Identification, sequence, and expression of the gene encoding gamma-glutamyltranspeptidase in Bacillus subtilis. J Bacteriol, 178(14): 4319–4322

[125] Yamaguchi T, Takei N, Araki K, Ishii K, Nagano T, Ichikawa T, Kumanishi T, Nawa H (2000). Molecular characterization of a novel gamma-glutamyl transpeptidase homologue found in rat brain. J Biochem, 128(1): 101–106

[126] Yao R, Schneider E, Ryan T J, Galivan J (1996). Human gamma-glutamyl hydrolase: cloning and characterization of the enzyme expressed in vitro. Proc Natl Acad Sci USA, 93(19): 10134–10138

[127] Zhang H, Forman H J, Choi J (2005). Gamma-glutamyl transpeptidase in glutathione biosynthesis. Methods Enzymol, 401: 468–483

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