Exploring the unfolding mechanism of γ-glutamyltranspeptidases: The case of the thermophilic enzyme from Geobacillus thermodenitrificans

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1824, Issue 4, 2012, Pages 571-577

  Pica, Andrea ^a   Russo Krauss, Irene ^a   Castellano, Immacolata ^b   Rossi, Mosè ^b   La Cara, Francesco ^b   Graziano, Giuseppe ^c   Sica, Filomena ^a,d   Merlino, Antonello ^a,d  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

^c UNIVERSITY OF SANNIO   (Italy)

^d CNR   (Italy)

Author keywords

glutamyltranspeptidases; Chemical denaturation; Circular dichroism; Intermediate state; Protein stability; Thermal unfolding

Indexed keywords

GAMMA GLUTAMYLTRANSFERASE; GUANIDINE;

ARTICLE; CIRCULAR DICHROISM; ENZYME STABILITY; ENZYME STRUCTURE; FLUORESCENCE; GEOBACILLUS; GEOBACILLUS THERMODENITRIFICAN; NONHUMAN; PRIORITY JOURNAL; PROTEIN UNFOLDING; SPECTROSCOPY; TEMPERATURE;

AMINO ACID SUBSTITUTION; ANILINO NAPHTHALENESULFONATES; BACTERIAL PROTEINS; CIRCULAR DICHROISM; ENZYME STABILITY; FLUORESCENT DYES; GAMMA-GLUTAMYLTRANSFERASE; GEOBACILLUS; GUANIDINE; HYDROGEN-ION CONCENTRATION; HYDROPHOBIC AND HYDROPHILIC INTERACTIONS; MUTAGENESIS, SITE-DIRECTED; PROTEIN STRUCTURE, SECONDARY; PROTEIN UNFOLDING; SPECTROMETRY, FLUORESCENCE; TRANSITION TEMPERATURE;

GEOBACILLUS THERMODENITRIFICANS;

EID: 84857350575     PISSN: 15709639     EISSN: 18781454     Source Type: Journal    
DOI: 10.1016/j.bbapap.2012.01.014     Document Type: Article

References (40)

1. S.S. Tate, and A. Meister γ-glutamyltranspeptidase: catalytic, structural and functional aspects Mol. Cell. Biochem. 39 1981 357 368
2. M.W. Lieberman, A.L. Wiseman, Z.Z. Shi, B.Z. Carter, R. Barrios, C.N. Ou, P. Chevez-Barrios, Y. Wang, G.M. Habib, J.C. Goodman, S.L. Huang, R.M. Lebovitz, and M.M. Matzuk Growth retardation and cysteine deficiency in γ-glutamyltranspeptidase-deficient mice Proc. Natl. Acad. Sci. U. S. A. 93 1996 7923 7926
3. D.H. Lee, D.R. Jacobs Jr., M. Gross, C.I. Kiefe, J. Roseman, C.E. Lewis, and M. Steffes γ-glutamyltransferase is a predictor of incident diabetes and hypertension: the Coronary Artery Risk Development in Young Adults (CARDIA) Study Clin. Chem. 49 2003 1358 1366
4. A. Pompella, A. Corti, A. Paolicchi, C. Giommarelli, and F. Zunino γ-glutamyltransferase, redox regulation and cancer drug resistance Curr. Opin. Pharmacol. 7 2007 360 366
5. R. Barrios, Z.Z. Shi, S.V. Kala, A.L. Wiseman, S.E. Welty, G. Kala, A.A. Bahler, C.N. Ou, and M.W. Lieberman Oxygen-induced pulmonary injury in γ-glutamyltranspeptidase-deficient mice Lung 179 2001 319 330
6. J.C. Jean, Y. Liu, L.A. Brown, R.E. Marc, E. Klings, and M. Joyce-Brady γ-glutamyltransferase deficiency results in lung oxidant stress in normoxia Am. J. Physiol. Lung Cell. Mol. Physiol. 283 2002 L766 L776
7. M. Emdin, A. Pompella, and A. Paolicchi γ-glutamyltransferase, atherosclerosis, and cardiovascular disease: triggering oxidative stress within the plaque Circulation 112 2005 2078 2080
8. H. Zhang, and H.J. Forman Redox regulation of γ- glutamyltranspeptidase Am. J. Respir. Cell Mol. Biol. 41 2009 509 515
9. J. Sian, D.T. Dexter, A.J. Lees, S. Daniel, P. Jenner, and C.D. Marsden Glutathione-related enzymes in brain in Parkinson's disease Ann. Neurol. 36 1994 356 361
10. B. del Bello, A. Paolicchi, M. Comporti, A. Pompella, and E. Maellaro Hydrogen peroxide produced during γ-glutamyltranspeptidase activity is involved in prevention of apoptosis and maintainance of proliferation in U937 cells FASEB J. 13 1999 69 79
11. M. Djavaheri-Mergny, M.J. Accaoui, D. Rouillard, and J. Wietzerbin γ-glutamyltranspeptidase activity mediates NF-kappaB activation through lipid peroxidation in human leukemia U937 cells Mol. Cell. Biochem. 232 2002 103 111
12. H. Suzuki, and H. Kumagai Autocatalytic processing of γ-glutamyltranspeptidase J. Biol. Chem. 277 2002 43536 43543
13. G. Boanca, A. Sand, and J.J. Barycki Uncoupling the enzymatic and autoprocessing activities of Helicobacter pylori γ-glutamyltranspeptidase J. Biol. Chem. 281 2006 19029 19037
14. C.L. Kinlough, P.A. Poland, J.B. Bruns, and R.P. Hughey γ-glutamyltranspeptidase: disulfide bridges, propeptide cleavage, and activation in the endoplasmic reticulum Methods Enzymol. 401 2005 426 449
15. S.S. Tate, and A. Meister γ-glutamyltranspeptidase from kidney Methods Enzymol. 113 1985 400 419
16. H. Suzuki, S. Izuka, H. Minami, N. Miyakawa, S. Ishihara, and H. Kumagai Use of bacterial γ-glutamyltranspeptidase for enzymatic synthesis of gamma-d-glutamyl compounds Appl. Environ. Microbiol. 69 2003 6399 6404
17. G. Boanca, A. Sand, T. Okada, H. Suzuki, H. Kumagai, K. Fukuyama, and J.J. Barycki Autoprocessing of Helicobacter pylori γ- glutamyltranspeptidase leads to the formation of a threonine-threonine catalytic dyad J. Biol. Chem. 282 2007 534 541
18. T. Okada, H. Suzuki, K. Wada, H. Kumagai, and K. Fukuyama 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 2006 6471 6476
19. T. Okada, H. Suzuki, K. Wada, H. Kumagai, and K. Fukuyama 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 2007 2433 2439
20. K. Wada, J. Hiratake, M. Irie, T. Okada, C. Yamada, H. Kumagai, H. Suzuki, and K. Fukuyama Crystal structures of Escherichia coli γ-glutamyltranspeptidase in complex with azaserine and acivicin: novel mechanistic implication for inhibition by glutamine antagonists J. Mol. Biol. 380 2008 361 372
21. K. Wada, M. Irie, H. Suzuki, K. Fukuyama, 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 (2010) 1000-1009.
22. R.C. Lyu, H.Y. Hu, L.Y. Kuo, H.F. Lo, P.L. Ong, H.P. Chang, and L.L. Lin Role of the conserved Thr399 and Thr417 residues of Bacillus licheniformis γ-glutamyltranspeptidase as evaluated by mutational analysis Curr. Microbiol. 59 2009 101 106
23. J.C. Yang, W.C. Liang, Y.Y. Chen, M.C. Chi, H.F. Lo, H.L. Chen, L.L. Lin, Biophysical characterization of Bacillus licheniformis and Escherichia coli γ-glutamyltranspeptidases: A comparative analysis, Int J Biol Macromol 48 (2011) 414-422.
24. I. Castellano, A. Merlino, M. Rossi, F. La Cara, Biochemical and structural properties of gamma-glutamyl transpeptidase from Geobacillus thermodenitrificans: an enzyme specialized in hydrolase activity, Biochimie 92 (2010) 464-474.
25. H. Minami, H. Suzuki, and H. Kumagai A mutant Bacillus subtilis γ-glutamyltranspeptidase specialized in hydrolysis activity FEMS Microbiol. Lett. 224 2003 169 173
26. P.L. Ong, Y.F. Yao, Y.M. Weng, W.H. Hsu, and L.L. Lin Residues Arg114 and Arg337 are critical for the proper function of Escherichia coli γ-glutamyltranspeptidase Biochem. Biophys. Res. Commun. 366 2008 294 300
27. I. Castellano, A. Di Salle, A. Merlino, M. Rossi, F. La Cara, Gene cloning and protein expression of γ-glutamyltranspeptidases from Thermus thermophilus and Deinococcus radiodurans: comparison of molecular and structural properties with mesophilic counterparts, Extremophiles 15 (2011) 259-270.
28. H.P. Chang, W.C. Liang, R.C. Lyu, M.C. Chi, T.F. Wang, K.L. Su, H.C. Hung, L.L. Lin, Effects of C-terminal truncation on autocatalytic processing of Bacillus licheniformis γ-glutamyltranspeptidase, Biochemistry (Mosc) 75 (2010) 919-929.
29. W.H. Hsu, P.L. Ong, S.C. Chen, and L.L. Lin Contribution of Ser463 residue to the enzymatic and autoprocessing activities of Escherichia coli γ-glutamyltranspeptidase Indian J. Biochem. Biophys. 46 2009 281 288
30. C.P. Hung, J.C. Yang, J.H. Chen, M.C. Chi, and L.L. Lin Unfolding analysis of the mature and unprocessed forms of Bacillus licheniformis γ-glutamyltranspeptidase J. Biol. Phys. 37 2011 463 475
31. M.M. Bradford A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding Anal. Biochem. 72 1976 248 254
32. L. Whitmore, and B.A. Wallace DICHROWEB, an online server for protein secondary structure analyses from circular dichroism spectroscopic data Nucleic Acids Res. 32 2004 W668 W673
33. A. Merlino, I. Russo Krauss, I. Castellano, E. De Vendittis, B. Rossi, M. Conte, A. Vergara, F. Sica, Structure and flexibility in cold-adapted iron superoxide dismutases: the case of the enzyme isolated from Pseudoalteromonas haloplanktis, J Struct Biol 172 (2010) 343-352.
34. J.A. Rumfeldt, C. Galvagnion, K.A. Vassall, and E.M. Meiering Conformational stability and folding mechanisms of dimeric proteins Prog. Biophys. Mol. Biol. 98 2008 61 84
35. A. Merlino, I. Russo Krauss, B. Rossi, S. Marco, E. De Vendittis, A. Vergara, F. Sica, Identification of an active dimeric intermediate populated during the unfolding process of a cambialistic superoxide dismutase, Biochimie 94 (2012) 768-775.
36. S. D'Amico, J.C. Marx, C. Gerday, and G. Feller Activity-stability relationships in extremophilic enzymes J. Biol. Chem. 278 2003 7891 7896
37. P. Del Vecchio, G. Graziano, V. Granata, G. Barone, L. Mandrich, M. Rossi, and G. Manco Denaturing action of urea and guanidine hydrochloride towards two thermophilic esterases Biochem. J. 367 2002 857 863
38. S.L. Mayo, and R.L. Baldwin Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A Science 262 1993 873 876
39. P.K. Nandi, and D.R. Robinson Effects of urea and guanidine hydrochloride on peptide and nonpolar groups Biochemistry 23 1984 6661 6668
40. G. Graziano Contrasting the denaturing effect of guanidinium chloride with the stabilizing effect of guanidinium sulfate Phys. Chem. Chem. Phys. 13 2011 12008 12014