Novel insights into eukaryotic y-glutamyltranspeptidase 1 from the crystal structure of the glutamate-bound human enzyme

Journal of Biological Chemistry

Volumn 288, Issue 44, 2013, Pages 31902-31913

  West, Matthew B ^a   Chen, Yunyu ^a   Wickham, Stephanie ^a   Heroux, Ann ^b   Cahill, Kyle ^a   Hanigan, Marie H ^a,c   Mooers, Blaine H M ^a,c  

^a UNIVERSITY OF OKLAHOMA COLLEGE OF MEDICINE   (United States)

^b UNIVERSITY OF OKLAHOMA   (United States)

^c BROOKHAVEN NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVE SITE ARCHITECTURE; CARDIO-VASCULAR DISEASE; CATALYTIC BEHAVIOR; CATALYTIC NUCLEOPHILES; CATALYTIC RESIDUE; OPEN CONFORMATION; STRUCTURAL MODELING; SUBSTRATE BINDING;

AMINO ACIDS; CHLORINE COMPOUNDS; DISEASE CONTROL; ENZYMES; MAMMALS; NUCLEOPHILES;

DISEASES;

GAMMA GLUTAMYLTRANSFERASE; GAMMA GLUTAMYLTRANSFERASE 1; GLUTAMIC ACID; UNCLASSIFIED DRUG;

ARTICLE; CATALYSIS; CONTROLLED STUDY; CRYSTAL STRUCTURE; ENZYME ACTIVE SITE; ENZYME BINDING; ENZYME CONFORMATION; ENZYME PURIFICATION; HUMAN; NONHUMAN; NUCLEOTIDE SEQUENCE; PICHIA PASTORIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; SITE DIRECTED MUTAGENESIS;

ANOMALOUS DIFFRACTION; ENZYME STRUCTURE; GAMMA-GLUTAMYLPEPTIDYLTRANSFERASE; GAMMA-GLUTAMYLTRANSFERASE; GAMMA-GLUTAMYLTRANSPEPTIDASE; GLYCOPROTEIN; HYDROLASES; OXIDATIVE STRESS; PROTEASE; THREONINE PEPTIDASE;

CATALYTIC DOMAIN; CRYSTALLOGRAPHY, X-RAY; GAMMA-GLUTAMYLTRANSFERASE; GLUTAMIC ACID; HUMANS; PROTEIN STRUCTURE, SECONDARY; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84887107305     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.498139     Document Type: Article

References (57)

1. Lieberman, M. W., and 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., and Matzuk, M. M. (1996) Growth retardation and cysteine deficiency in γ-glutamyl transpeptidase-deficient mice. Proc. Natl. Acad. Sci. U.S.A. 93, 7923-7926 (Pubitemid 26277140)
2. Hanigan, M. H., and Ricketts, W. A. (1993) Extracellular glutathione is a source of cysteine for cells that express γ-glutamyl transpeptidase. Biochemistry 32, 6302-6306 (Pubitemid 23196889)
3. Cooper, A. J., and Hanigan, M. H. (2010) Enzymes involved in processing glutathione conjugates. in Comprehensive Toxicology: Biotransformation (Guengerich, F. P., ed) pp. 323-365, Elsevier, New York
4. Rojas, E., Valverde, M., Kala, S. V., Kala, G., and Lieberman, M. W. (2000) Accumulation of DNA damage in the organs of mice deficient in γ-glutamyltranspeptidase. Mutat. Res. 447, 305-316 (Pubitemid 30177177)
5. Wickham, S., and West., M. B., Cook, P. F., and Hanigan, M. H. (2011) γ-Glutamyl compounds. Substrate specificity of γ-glutamyl transpeptidase enzymes. Anal. Biochem. 414, 208-214
6. Lowry, M. H., and McAllister., B. P., Jean, J. C, Brown, L. A., and Hughey., R. P., Cruikshank, W. W., Amar, S., Lucey, E. C, Braun, K., Johnson, P., Wight, T. N, and Joyce-Brady, M. (2008) Lung lining fluid glutathione attenuates IL-13-induced asthma. Am. J. Respir. Cell Mol. Biol. 38, 509-516 (Pubitemid 351758668)
7. Sian, J., and Dexter., D. T., Lees, A. J., Daniel, S., Jenner, P., and Marsden, C. D. (1994) Glutathione-related enzymes in brain in Parkinson's disease. Ann. Neurol. 36, 356-361 (Pubitemid 24280056)
8. Emdin, M., Pompella, A., and Paolicchi, A. (2005) γ- glutamyltransferase, atherosclerosis, and cardiovascular disease. Triggering oxidative stress within the plaque. Circulation 112, 2078-2080 (Pubitemid 41475797)
9. Diergaarde, B., Brand, R., Lamb, J., Cheong, S. Y., Stello, K., Barmada, M. M., Feingold, E., and Whitcomb, D. C. (2010) Pooling-based genomewide association study implicates γ-glutamyltransferase 1 (GGT1)genein pancreatic carcinogenesis. Pancreatology 10, 194-200
10. Hanigan, M. H, Gallagher, B. C, Townsend, D. M., and Gabarra, V. (1999) γ-Glutamyl transpeptidase accelerates tumor growth and increases the resistance of tumors to cisplatin in vivo. Carcinogenesis 20, 553-559 (Pubitemid 29151289)
11. Castellano, I., and Merlino, A. (2012) γ-Glutamyltranspeptidases. Sequence, structure, biochemical properties, and biotechnological applications. Cell. Mol. Life Sci. 69, 3381-3394
12. Earhart, R. H, Koeller, J. M., and Davis., T. E., Borden, E. C, McGovren, J. P., and Davis., H. L., and Tormey, D. C. (1983) Phase I trial and pharmacokinetics of acivicin administered by 72-hour infusion. Cancer Treat. Rep. 67, 683-692 (Pubitemid 13001715)
13. Fleishman, G., and Yap., H. Y., Murphy, W. K., and Bodey, G. (1983) Phase II trial of acivicin in advanced metastatic breast cancer. Cancer Treat. Rep. 67, 843-844 (Pubitemid 13007295)
14. Hidalgo, M., Rodriguez, G., Kuhn, J. G., Brown, T., Weiss, G., MacGovren, J. P., Von Hoff, D. D., and Rowinsky, E. K. (1998) A Phase I and pharmacological study of the glutamine antagonist acivicin with the amino acid solution aminosyn in patients with advanced solid malignancies. Clin. Cancer Res. 4, 2763-2770 (Pubitemid 28523503)
15. King, J. B., and West., M. B., Cook, P. F., and Hanigan, M. H. (2009) A novel, species-specific class of uncompetitive inhibitors of γ-glutamyl transpeptidase. J. Biol. Chem. 284, 9059-9065
16. Wickham, S., Regan, N, and West., M. B., Kumar, V. P., Thai, J., Li, P. K., and Cook., P. F., and Hanigan, M. H. (2012) Divergent effects of compounds on the hydrolysis and transpeptidation reactions of γ-glutamyl transpeptidase. J. Enzyme Inhib. Med. Chem. 27, 476-489
17. Wickham, S., Regan, N, and West., M. B., Thai, J., Cook, P. F., and Terzyan., S. S., Li, P. K., and Hanigan, M. H. (2013) Inhibition of human γ-glutamyl transpeptidase. Development of more potent, physiologically relevant, uncompetitive inhibitors. Biochem. J. 450, 547-557
18. Duggleby, H. J., and Tolley., S. P., Hill, C. P., Dodson, E. J., Dodson, G., and Moody, P. C. (1995) Penicillin acylase has a single-amino-acid catalytic centre. Nature 373, 264-268
19. Oinonen, C, and Rouvinen, J. (2000) Structural comparison of Ntn-hydrolases. Protein Sci. 9, 2329-2337 (Pubitemid 32105715)
20. Castonguay, R., Halim, D., Morin, M., Furtos, A., Lherbet, C, Bonneil, E., Thibault, P., and Keillor, J. W. (2007) Kinetic characterization and identification of the acylation and glycosylation sites of recombinant human γ-glutamyltranspeptidase. Biochemistry 46, 12253-12262 (Pubitemid 350022380)
21. Ekici, O. D., Paetzel, M., and Dalbey, R. E. (2008) Unconventional serine proteases. Variations on the catalytic Ser/His/Asp triad configuration. Protein Sci. 17, 2023-2037
22. Elce, J. S., and Broxmeyer, B. (1976) γ-Glutamyltransferase of rat-kidney. simultaneous assay of hydrolysis and transfer-reactions with [glutamate-C-14]glutathione. Biochem. J. 153, 223-232
23. Curthoys, N. P., and Hughey, R. P. (1979) Characterization and physiological-function of rat renal γ-glutamyl-transpeptidase. Enzyme 24, 383-403 (Pubitemid 10202809)
24. Thompson, G. A., and Meister, A. (1976) Hydrolysis and transfer reactions catalyzed by γ-glutamyl transpeptidase. Evidence for separate substrate sites and for high affinity of L-cystine. Biochem. Biophys. Res. Commun. 71, 32-36
25. Allison, R. D. (1985) γ-Glutamyl transpeptidase. Kinetics and mechanism. Methods Enzymol. 113, 419-437
26. Taniguchi, N, and Ikeda, Y. (1998) γ-Glutamyl transpeptidase. Catalytic mechanism and gene expression. Adv. Enzymol. Relat. Areas Mol. Biol. 72, 239-278
27. Morrow, A. L., Williams, K., Sand, A., Boanca, G., and Barycki, J. J. (2007) Characterization of Helicobacter pylori γ-glutamyltranspeptidase reveals the molecular basis for substrate specificity and a critical role for the tyrosine 433-containing loop in catalysis. Biochemistry 46, 13407-13414 (Pubitemid 350136379)
28. Okada, T., Suzuki, H, Wada, K., Kumagai, H, and Fukuyama, K. (2006) Crystal structures of γ-glutamyltranspeptidase from Escherichia coli, a key enzyme in glutathione metabolism, and its reaction intermediate. Proc. Natl. Acad. Sci. U.S.A. 103, 6471-6476
29. Wada, K., Irie, M., Suzuki, H., and Fukuyama, K. (2010) Crystal structure of the halotolerant γ-glutamyltranspeptidase from Bacillus subtilis in complex with glutamate reveals a unique architecture of the solvent-exposed catalytic pocket. FEBS J. 277, 1000-1009
30. Suzuki, H., Kumagai, H., and Tochikura, T. (1986) γ-Glutamyl- transpeptidase from Escherichia coli K-12. Purification and properties. J. Bacteriol. 168, 1325-1331 (Pubitemid 17226822)
31. Ikeda, Y., Fujii, J., Anderson, M. E., Taniguchi, N, and Meister, A. (1995) Involvement of Ser-451 and Ser-452 in the catalysis of human γ-glutamyl transpeptidase. J. Biol. Chem. 270, 22223-22228
32. Minami, H., Suzuki, H., and Kumagai, H. (2003) Salt-tolerant γ-glutamyltranspeptidase from Bacillus subtilis 168 with glutaminase activity. Enzyme Microb. Technol. 32, 431-438, http://dx.doi.org/10.1016/S0141- 0229(02)00314-9 (Pubitemid 36136062)
33. Boanca, G., Sand, A., and Barycki, J. J. (2006) Uncoupling the enzymatic and autoprocessing activities of Helicobacter pylori γ- glutamyltranspeptidase. J. Biol. Chem. 281, 19029-19037 (Pubitemid 44035406)
34. Rajpert-De Meyts, E., Heisterkamp, N, and Groffen, J. (1988) Cloning and nucleotide sequence of human γ-glutamyl transpeptidase. Proc. Natl. Acad. Sci. U.S.A. 85, 8840-8844 (Pubitemid 19001801)
35. West, M. B., and Segu., Z. M., Feasley, C. L., Kang, P., Klouckova, I., Li, C, and Novotny., M. V., West, C. M., Mechref, Y., and Hanigan, M. H. (2010) Analysis of site-specific glycosylation of renal and hepatic γ-glutamyl transpeptidase from normal human tissue. J. Biol. Chem. 285, 29511-29524
36. West, M. B., Wickham, S., Quinalty, L. M., and Pavlovicz., R. E., Li, C, and Hanigan, M. H. (2011) Autocatalytic cleavage of human γ-glutamyl transpeptidase is highly dependent on N-glycosylation at asparagine 95. J. Biol. Chem. 286, 28876-28888
37. Suzuki, H, and Kumagai, H. (2002) Autocatalytic processing of γ-glutamyltranspeptidase. J. Biol. Chem. 277, 43536-43543
38. Kinlough, C. L., and Poland., P. A., Bruns, J. B., and Hughey, R. P. (2005) γ-Glutamyltranspeptidase. Disulfide bridges, propeptide cleavage, and activation in the endoplasmic reticulum. Methods Enzymol. 401, 426-449 (Pubitemid 43052407)
39. West, M. B., Wickham, S., Parks, E. E., and Sherry., D. M., and Hanigan, M. H. (2013) Human GGT2 does not autocleave into a functional enzyme. A cautionary tale for interpretation of microarray data on redox signaling. Antioxid. Redox Signal. 10.1089/ars.2012.4997
40. Kabsch, W. (2010) XDS. Acta Crystallogr. D Biol. Crystallogr. 66, 125-132
41. Vagin, A., and Teplyakov, A. (2010) Molecular replacement with MOL-REP. Acta Crystallogr. D Biol. Crystallogr. 66, 22-25
42. Adams, P. D., and Afonine., P. V., Bunkóczi, G., Chen, V. B., and Davis., I. W., Echols, N., Headd, J. J., and Hung., L. W., Kapral, G. J., Grosse-Kunstleve, R. W., McCoy, A. J., Moriarty, N. W., Oeffner, R., Read, R. J., Richardson, D. C, Richardson, J. S., Terwilliger, T. C, and Zwart, P. H. (2010) PHENIX. A comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213-221
43. Emsley, P., Lohkamp, B., Scott, W. G., and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501
44. Thorn, A., and Sheldrick, G. M. (2011) ANODE. Anomalous and heavyatom density calculation. J. Appl. Crystallogr. 44, 1285-1287
45. Thompson, J. D., and Higgins., D. G., and 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, 4673-4680 (Pubitemid 24354800)
46. Gouet, P., Courcelle, E., Stuart, D. I., and Métoz, F. (1999) ESPript. Analysis of multiple sequence alignments in PostScript. Bioinformatics 15, 305-308 (Pubitemid 29213756)
47. Kabsch, W., and Sander, C (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22, 2577-2637
48. Krissinel, E., and Henrick, K. (2007) Inference of macromolecular assemblies from crystalline state. J. Mol. Biol. 372, 774-797 (Pubitemid 47321791)
49. Boanca, G., Sand, A., Okada, T., Suzuki, H., Kumagai, H., Fukuyama, K., and Barycki, J. J. (2007) Autoprocessing of Helicobacterpylori γ-glutamyltranspeptidase leads to the formation of a threonine-threonine catalytic dyad. J. Biol. Chem. 282, 534-541 (Pubitemid 47086261)
50. Okada, T., Suzuki, H, Wada, K., Kumagai, H, and Fukuyama, K. (2007) Crystal structure of the γ-glutamyltranspeptidase precursor protein from Escherichia coli. Structural changes upon autocatalytic processing and implications for the maturation mechanism. J. Biol. Chem. 282, 2433-2439 (Pubitemid 47076749)
51. Hu, X., and Legler., P. M., Khavrutskii, I., Scorpio, A., Compton, J. R., and Robertson., K. L., Friedlander, A. M., and Wallqvist, A. (2012) Probing the donor and acceptor substrate specificity of the γ-glutamyl transpeptidase. Biochemistry 51, 1199-1212
52. Laskowski, R. A., and Swindells, M. B. (2011) LigPlot+. Multiple ligandprotein interaction diagrams for drug discovery. J. Chem. Inf. Model. 51, 2778-2786
53. Shapovalov, M. V., Dunbrack, R. L. Jr. (2011) A smoothed backbone-dependent rotamer library for proteins derived from adaptive kernel density estimates and regressions. Structure 19, 844-858
54. Lodola, A., Branduardi, D., De Vivo, M., Capoferri, L., Mor, M., Piomelli, D., and Cavalli, A. (2012) A catalytic mechanism for cysteine N-terminal nucleophile hydrolases, as revealed by free energy simulations. PLoS One 7, e32397
55. Ikeda, Y., Fujii, J., and Taniguchi, N (1996) Effects of substitutions of the conserved histidine residues in human γ-glutamyl transpeptidase. J. Biochem. 119, 1166-1170 (Pubitemid 26202632)
56. Ikeda, Y., Fujii, J., and Taniguchi, N (1993) Significance of Arg-107 and Glu-108 in the catalytic mechanism of human γ-glutamyl transpeptidase. Identification by site-directed mutagenesis. J. Biol. Chem. 268, 3980-3985 (Pubitemid 23072929)
57. Chen, V. B., and Arendall., W. B., 3rd, Headd, J. J., Keedy, D. A., Immormino, R. M., Kapral, G. J., Murray, L. W., Richardson, J. S., and Richardson, D. C. (2010) MolProbity. All-atom structure validation for macromolecular crystallography. Acta Crystallogr. D Biol. Crystallogr. 66, 12-21