Calorimetric and spectroscopic investigations of the thermal denaturation of wild type nitrite reductase

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1752, Issue 1, 2005, Pages 47-55

  Stirpe, Andrea ^a   Guzzi, Rita ^a   Wijma, Hein ^b   Verbeet, Martin Ph ^b   Canters, Gerard W ^b   Sportelli, Luigi ^a  

^a UNIVERSITY OF CALABRIA   (Italy)

^b LEIDEN UNIVERSITY   (Netherlands)

Author keywords

Activation energy; Lumry Eyring model; Nitrite reductase; Thermal denaturation

Indexed keywords

COPPER; NITRITE REDUCTASE;

ALCALIGENES FAECALIS; ARTICLE; CALORIMETRY; CONFORMATION; DENATURATION; DIFFERENTIAL SCANNING CALORIMETRY; DISSOCIATION; ELECTRON; ENERGY; ENVIRONMENTAL FACTOR; ENZYME ACTIVITY; HEAT; KINETICS; MAGNETISM; NONHUMAN; PRIORITY JOURNAL; SIMULATION; SPECTROSCOPY; TEMPERATURE; THERMAL ANALYSIS; WILD TYPE;

ALCALIGENES FAECALIS; CALORIMETRY, DIFFERENTIAL SCANNING; COPPER; ELECTRON SPIN RESONANCE SPECTROSCOPY; ENZYME STABILITY; HEAT; NITRITE REDUCTASES; PROTEIN DENATURATION; THERMODYNAMICS;

ALCALIGENES FAECALIS;

EID: 24044512147     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2005.07.004     Document Type: Article

References (55)

1. T. Kakutani, H. Watanabe, K. Arima, and T. Beppu Purification and properties of a copper-containing nitrite reductase from a denitrifying bacterium, Alcaligenes faecalis strain S-6 J. Biochem. (Tokyo) 89 1981 453 461
2. B. Strehlitz, B. Grundig, W. Schumacher, P.M.H. Kroneck, K.D. Vorlop, and H. Kotte A nitrite sensor based on a highly sensitive nitrite reductase mediator-coupled amperometric detection Anal. Chem. 68 1996 807 816
3. S. Sasaki, I. Karube, N. Hirota, Y. Arikawa, N. Nishiyama, M. Kukimoto, S. Horinouchi, and T. Beppu Application of nitrite reductase from Alcaligenes faecalis S-6 for nitrite measurement Biosens. Bioelectron. 13 1998 1 5
4. M.E.P. Murphy, S. Turley, M. Kukimoto, M. Nishiyama, S. Horinouchi, H. Sasaki, M. Tanokura, and E.T. Adman Structure of Alcaligenes faecalis nitrite reductase and a copper site mutant, M150E, that contains zinc Biochemistry 34 1995 12107 12117
5. M.E.P. Murphy, S. Turley, and E.T. Adman Structure of nitrite bound to copper-containing nitrite reductase from Alcaligenes faecalis J. Biol. Chem. 272 1997 28455 28460
6. T. Kakutani, H. Watanabe, K. Arima, and T. Beppu A blue protein as an inactivating factor for nitrite reductase from Alcaligenes faecalis strain S-6 J. Biochem. (Tokyo) 89 1981 463 472
7. E.T. Adman Copper protein structures Adv. Protein Chem. 42 1991 145 197
8. S. Suzuki, K. Kataoka, K. Yamaguchi, T. Inoue, and Y. Kai Structure-function relationships of copper-containing nitrite reductases Coord. Chem. Rev. 190-192 1999 245 265
9. P.L. Privalov, and S.A. Putekhin Scanning microcalorimetry in studying temperature-induced changes in proteins Methods Enzymol. 131 1986 4 51
10. J.E. Ladbury B.Z. Chowdhry Biocalorimetry: Applications of Calorimetry in the Biological Sciences 1998 John Wiley Chichester
11. I. Savini, S. D'Alessio, A. Giartosio, L. Morpurgo, and L. Avigliano The role of copper in the stability of ascorbate oxidase towards denaturing agents Eur. J. Biochem. 190 1990 491 495
12. E. Agostinelli, L. Cervoni, A. Giartosio, and L. Morpurgo Stability of Japanese-lacquer-tree (Rhus vernicifera) laccase to thermal and chemical denaturation: comparison with ascorbate oxidase Biochem. J. 306 1995 697 702
13. G. Mei, A. Di Venere, M. Buganza, P. Vecchini, N. Rosato, and A. Finazzi-Agrò Role of quaternary structure in the stability of dimeric proteins: the case of ascorbate oxidase Biochemistry 36 1997 10917 10922
14. O.V. Koroleva, E.V. Stepanova, V.I. Binukov, V.P. Timofeev, and W. Pfeil Temperature-induced changes in copper centers and protein conformation of two fungal laccase from Coriolus hirsutus and Coriolus zonatus Biochim. Biophys. Acta 1547 2001 397 407
15. A.C. Clark, J.F. Sinclair, and T.O. Baldwin Folding of bacterial luciferase involves a non-native heterodimeric intermediate in equilibrium with the native enzyme and the unfolded subunits J. Biol. Chem. 268 1993 10773 10779
16. F. Couthon, E. Clottes, C. Ebel, and C. Vial Reversible dissociation and unfolding of dimeric creatine kinase isoenzyme MM in guanidine hydrochloride and urea Eur. J. Biochem. 234 1995 160 170
17. M. Thorolfsson, B. Ibarra-Molero, P. Fojan, S.B. Petersen, J.M. Sanchez-Ruiz, and A. Martinez l-Phenylalanine binding and domain organization in human phenylalanine hydroxylase: a differential scanning calorimetry study Biochemistry 41 2002 7573 7585
18. J.M. Sanchez-Ruiz Theoretical analysis of Lumry-Eyring models in differential scanning calorimetry Biophys. J. 61 1992 921 935
19. B.I. Kurganov, A.E. Lyubarev, J.M. Sanchez-Ruiz, and V.L. Shnyrov Analysis of differential scanning calorimetry data for proteins. Criteria of validity of one-step mechanism of irreversible protein denaturation Biophys. Chem. 69 1997 125 135
20. T. Vogl, C. Jatzke, and H.J. Hinz Thermodynamic stability of annexin V E17G: equilibrium parameters from an irreversible unfolding reaction Biochemistry 36 1997 1657 1668
21. J. Backmann, G. Schäfer, L. Wyns, and H. Bönish Thermodynamics and kinetics of unfolding of the thermostrimeric table adenylate kinase from the archaeon Sulfolobus acidocaldarius J. Mol. Biol. 284 1998 817 833
22. C. Steif, P. Weber, J. Flossdorf, G. Cesareni, M. Kokkinidis, and H.J. Hinz Subunit interactions provide a significant contribution to the stability of the dimeric four-α-helical-bundle protein ROP Biochemistry 32 1993 3867 3876
23. A.G. Cashikar, and N.M. Rao Unfolding pathway in red kidney bean acid phosphatase is dependent on ligand binding J. Biol. Chem. 271 1996 4741 4746
24. I. Protasevich, B. Ranjbar, V. Lobachov, A. Makarov, R. Gilli, C. Briand, D. Lafitte, and J. Haiech Conformation and thermal denaturation of apocalmodulin: role of electrostatic mutations Biochemistry 36 1997 2017 2024
25. V.G. Panse, C.P. Swaminathan, J.J. Aloor, A. Surolia, and R. Varadarajan Unfolding thermodynamics of the tetrameric chaperone, SecB Biochemistry 39 2000 2362 2369
26. V. Edge, N.M. Allewell, and J.M. Sturtevant High-resolution differential scanning calorimetric analysis of the subunits of Escherichia coli aspartate transcarbamoylase Biochemistry 24 1985 5899 5906
27. H.J. Wijma, M.J. Boulanger, A. Molon, M. Fittipaldi, M. Huber, M.E.P. Murphy, M.Ph. Verbeet, and G.W. Canters Reconstitution of the type-1 active site of the H145G/A variants of nitrite reductase by ligand insertion Biochemistry 42 2003 4075 4083
28. A.J. Brenner, and E.D. Harris A quantitative test for copper using bicinchoninic acid Anal. Biochem. 226 1995 80 84
29. R. Hiller, Z.H. Zhou, M.W.W. Adams, and S.W. Englander Stability and dynamics in a hyperthermophilic protein with melting temperature close to 200°C Proc. Natl. Acad. Sci. U. S. A. 94 1997 11329 11332
30. W. Pfeil, U. Gesierich, G.R. Kleemann, and R. Sterner Ferredoxin from the hyperthermophile Thermotoga maritima is stable beyond the boiling point of water J. Mol. Biol. 272 1997 591 596
31. C.L. Higgins, J. Meyer, and P. Wittung-Stafshede Exceptional stability of a [2Fe-2S] ferrodoxin from hyperthermophilic bacterium Aquifex aeolicus Biochim. Biophys. Acta 1599 2002 82 89
32. A.D. Nielsen, M.L. Pusey, C.C. Fuglsang, and P. Westh A proposed mechanism for the thermal denaturation of a recombinant Bacillus halmapalus α-amylase-The effect of calcium ions Biochim. Biophys. Acta 1652 2003 52 63
33. T.J. Ahern, and A.M. Klibanov The mechanisms of irreversible enzyme inactivation at 100°C Science (Washington) 228 1985 1280 1284
34. S.E. Zale, and A.M. Klibanov Why does ribonuclease irreversibly inactivate at high temperatures? Biochemistry 25 1986 5432 5444
35. A. Sandberg, J. Leckner, Y. Shi, F.P. Schwarz, and B.G. Karlsson Effects of metal ligation and oxygen on the reversibility of the thermal denaturation of Pseudomonas aeruginosa azurin Biochemistry 41 2002 1060 1069
36. A. Sandberg, D.J. Harrison, and B.G. Karlsson Thermal denaturation of spinach plastocyanin: effect of copper site oxidation state and molecular oxygen Biochemistry 42 2003 10301 10310
37. A. Tigerstrom, F.P. Schwarz, B.G. Karlsson, M. Okvist, C. Alvarez-Rua, D. Maeder, F.T. Robb, and L. Sjolin Effects of a novel disulfide bond and engineered electrostatic interactions on the thermostability of azurin Biochemistry 43 2004 12563 12574
38. E. Freire, W.W. van Osdol, O.L. Mayorga, and J.M. Sanchez-Ruiz Calorimetrically determined dynamics of complex unfolding transitions in proteins Annu. Rev. Biophys. Biophys. Chem. 19 1990 159 188
39. J.R. Lepock, K.P. Ritchie, M.C. Kolios, A.M. Rodahl, K.A. Heinz, and J. Kruuv Influence of transition rates and scan rate on kinetic simulations of differential scanning calorimetry profiles of reversible and irreversible protein denaturation Biochemistry 31 1992 12706 12712
40. J. Davoodi, W.W. Wakarchuk, W.K. Surewicz, and P.R. Carey Scan-Rate dependence in protein calorimetry-the reversible transitions of Bacillus circulans xylanase and a disulfide-bridge mutant Protein Sci. 7 1998 1538 1544
41. J.M. Sanchez-Ruiz, J.L. Lopez-Lacomba, M. Cortijo, and P.L. Mateo Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin Biochemistry 27 1988 1648 1652
42. K. Idakieva, K. Parvanova, and S. Todinova Differential scanning calorimetry of the irreversible denaturation of Rapana thomasiana (marine snail, Gastropod) hemocyanin Biochim. Biophys. Acta 1748 2005 50 56
43. A.E. Lyubarev, B.I. Kurganov, A.A. Burlakova, and V.N. Orlov Irreversible thermal denaturation of uridine phosphorylase from Escherichia coli K-12 Biophys. Chem. 70 1998 247 257
44. D. Fessas, S. Lametti, A. Schiraldi, and F. Bonomi Thermal unfolding of monomeric and dimeric β-lactoglobulins Eur. J. Biochem. 268 2001 5439 5448
45. I.M. Plaza del Pino, B. Ibarra-Molero, and J.M. Sanchez-Ruiz Lower kinetic limit to protein thermal stability: a proposal regarding protein stability in vivo and its relation with misfolding diseases Proteins 40 2000 58 70
46. C. La Rosa, D. Milardi, D. Grasso, R. Guzzi, and L. Sportelli Thermodynamics of the thermal unfolding of azurin J. Phys. Chem. 99 1995 14864 14870
47. S. Suzuki, T. Kohzuma, S. Shidara, K. Ohki, and T. Aida Novel spectroscopic aspects of type I copper in hyphomicrobium nitrite reductase Inorg. Chim. Acta 208 1993 107 109
48. L.B. LaCroix, S.E. Shadle, Y. Wang, B.A. Averill, B. Hedman, K.O. Hodgson, and E.I. Solomon Electronic structure of the perturbed blue copper site in nitrite reductase: spectroscopic properties, bonding, and implications for the entatic/rack state J. Am. Chem. Soc. 118 1996 7755 7768
49. J. Han, T.M. Loehr, Y. Lu, J.S. Valentine, B.A. Averill, and J. Sanders-Loehr Resonance Raman excitation profiles indicate multiple Cys → Cu charge transfer transitions in type 1 copper proteins J. Am. Chem. Soc. 115 1993 4256 4263
50. M. Kukimoto, M. Nishiyama, M.E.P. Murphy, S. Turley, E.T. Adman, S. Horinouchi, and T. Beppu X-ray structure and site directed mutagenesis of a nitrite reductase from Alcaligenes faecalis S-6: roles of two copper atoms in nitrite reduction Biochemistry 33 1994 5246 5252
51. B.R. McGarvey Electron spin resonance of transition metal complexes R. Carlin Transition Metal Chemistry vol. 3 1967 M. Dekker New York 90 201
52. D. Milardi, C. La Rosa, D. Grasso, R. Guzzi, L. Sportelli, and C. Fini Thermodynamics and kinetics of the thermal unfolding of plastocyanin Eur. Biophys. J. 27 1998 273 282
53. R. Guzzi, L. Sportelli, C. La Rosa, D. Milardi, D. Grasso, M.Ph. Verbeet, and G.W. Canters A spectroscopic and calorimetric investigation on the thermal stability of the Cys3Ala/Cys26Ala azurin mutant Biophys. J. 77 1999 1052 1063
54. C. La Rosa, D. Milardi, D. Grasso, M.Ph. Verbeet, G.W. Canters, L. Sportelli, and R. Guzzi A model for the thermal unfolding of amicyanin Eur. Biophys. J. 30 2002 559 570
55. R. Guzzi, L. Andolfi, S. Cannistraro, M.Ph. Verbeet, G.W. Canters, and L. Sportelli Thermal stability of wild type and disulfide bridge containing mutant of poplar plastocyanin Biophys. Chem. 112 2004 35 43