REVIEW

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

  • Sharath BALAKRISHNA ,
  • Asmita A. PRABHUNE
Expand
  • Division of Biochemical Sciences, National Chemical Laboratory, Dr. Homi Bhabha Road, Pune 411008, Maharashtra, India

Received date: 07 Oct 2013

Accepted date: 02 Dec 2013

Copyright

2014 Higher Education Press and Springer-Verlag Berlin Heidelberg

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.

Cite this article

Sharath BALAKRISHNA , Asmita A. PRABHUNE . Gamma-glutamyl transferases: A structural, mechanistic and physiological perspective[J]. Frontiers in Biology, 2014 , 9(1) : 51 -65 . DOI: 10.1007/s11515-014-1288-0

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

PMID

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

DOI

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

DOI

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

DOI

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

PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI

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

DOI PMID

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

DOI PMID

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

PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

PMID

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

PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

PMID

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

PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

PMID

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

DOI

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

PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

DOI PMID

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

PMID

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

DOI PMID

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

DOI PMID

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

PMID

Outlines

/