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

Andrea Stirpe1, Rita Guzzi1, Hein Wijma2, Martin Ph. Verbeet2, Gerard W. Canters2, Luigi Sportelli1
1Dipartimento di Fisica e Unità INFM, Laboratorio di Biofisica Molecolare, Università della Calabria, Ponte P. Bucci-Cubo 31C, I-87036, Arcavacata di Rende (CS), Italy
2Gorleaus Laboratories, Metallo Protein Group, Leiden University, P.O. Box 9502, 2300 RA Leiden, The Netherlands

Tài liệu tham khảo

Kakutani, 1981, Purification and properties of a copper-containing nitrite reductase from a denitrifying bacterium, Alcaligenes faecalis strain S-6, J. Biochem. (Tokyo), 89, 453, 10.1093/oxfordjournals.jbchem.a133220 Strehlitz, 1996, A nitrite sensor based on a highly sensitive nitrite reductase mediator-coupled amperometric detection, Anal. Chem., 68, 807, 10.1021/ac950692n Sasaki, 1998, Application of nitrite reductase from Alcaligenes faecalis S-6 for nitrite measurement, Biosens. Bioelectron., 13, 1, 10.1016/S0956-5663(97)00100-0 Murphy, 1995, Structure of Alcaligenes faecalis nitrite reductase and a copper site mutant, M150E, that contains zinc, Biochemistry, 34, 12107, 10.1021/bi00038a003 Murphy, 1997, Structure of nitrite bound to copper-containing nitrite reductase from Alcaligenes faecalis, J. Biol. Chem., 272, 28455, 10.1074/jbc.272.45.28455 Kakutani, 1981, A blue protein as an inactivating factor for nitrite reductase from Alcaligenes faecalis strain S-6, J. Biochem. (Tokyo), 89, 463, 10.1093/oxfordjournals.jbchem.a133221 Adman, 1991, Copper protein structures, Adv. Protein Chem., 42, 145, 10.1016/S0065-3233(08)60536-7 Suzuki, 1999, Structure–function relationships of copper-containing nitrite reductases, Coord. Chem. Rev., 190–192, 245, 10.1016/S0010-8545(99)00069-7 Privalov, 1986, Scanning microcalorimetry in studying temperature-induced changes in proteins, Methods Enzymol., 131, 4, 10.1016/0076-6879(86)31033-4 1998 Savini, 1990, The role of copper in the stability of ascorbate oxidase towards denaturing agents, Eur. J. Biochem., 190, 491, 10.1111/j.1432-1033.1990.tb15600.x Agostinelli, 1995, Stability of Japanese-lacquer-tree (Rhus vernicifera) laccase to thermal and chemical denaturation: comparison with ascorbate oxidase, Biochem. J., 306, 697, 10.1042/bj3060697 Mei, 1997, Role of quaternary structure in the stability of dimeric proteins: the case of ascorbate oxidase, Biochemistry, 36, 10917, 10.1021/bi970614p Koroleva, 2001, Temperature-induced changes in copper centers and protein conformation of two fungal laccase from Coriolus hirsutus and Coriolus zonatus, Biochim. Biophys. Acta, 1547, 397, 10.1016/S0167-4838(01)00209-6 Clark, 1993, Folding of bacterial luciferase involves a non-native heterodimeric intermediate in equilibrium with the native enzyme and the unfolded subunits, J. Biol. Chem., 268, 10773, 10.1016/S0021-9258(18)82052-X Couthon, 1995, Reversible dissociation and unfolding of dimeric creatine kinase isoenzyme MM in guanidine hydrochloride and urea, Eur. J. Biochem., 234, 160, 10.1111/j.1432-1033.1995.160_c.x Thorolfsson, 2002, l-Phenylalanine binding and domain organization in human phenylalanine hydroxylase: a differential scanning calorimetry study, Biochemistry, 41, 7573, 10.1021/bi0160720 Sanchez-Ruiz, 1992, Theoretical analysis of Lumry–Eyring models in differential scanning calorimetry, Biophys. J., 61, 921, 10.1016/S0006-3495(92)81899-4 Kurganov, 1997, Analysis of differential scanning calorimetry data for proteins. Criteria of validity of one-step mechanism of irreversible protein denaturation, Biophys. Chem., 69, 125, 10.1016/S0301-4622(97)80552-2 Vogl, 1997, Thermodynamic stability of annexin V E17G: equilibrium parameters from an irreversible unfolding reaction, Biochemistry, 36, 1657, 10.1021/bi962163z Backmann, 1998, Thermodynamics and kinetics of unfolding of the thermostrimeric table adenylate kinase from the archaeon Sulfolobus acidocaldarius, J. Mol. Biol., 284, 817, 10.1006/jmbi.1998.2216 Steif, 1993, Subunit interactions provide a significant contribution to the stability of the dimeric four-α-helical-bundle protein ROP, Biochemistry, 32, 3867, 10.1021/bi00066a005 Cashikar, 1996, Unfolding pathway in red kidney bean acid phosphatase is dependent on ligand binding, J. Biol. Chem., 271, 4741, 10.1074/jbc.271.9.4741 Protasevich, 1997, Conformation and thermal denaturation of apocalmodulin: role of electrostatic mutations, Biochemistry, 36, 2017, 10.1021/bi962538g Panse, 2000, Unfolding thermodynamics of the tetrameric chaperone, SecB, Biochemistry, 39, 2362, 10.1021/bi992484l Edge, 1985, High-resolution differential scanning calorimetric analysis of the subunits of Escherichia coli aspartate transcarbamoylase, Biochemistry, 24, 5899, 10.1021/bi00342a032 Wijma, 2003, Reconstitution of the type-1 active site of the H145G/A variants of nitrite reductase by ligand insertion, Biochemistry, 42, 4075, 10.1021/bi027270+ Brenner, 1995, A quantitative test for copper using bicinchoninic acid, Anal. Biochem., 226, 80, 10.1006/abio.1995.1194 Hiller, 1997, Stability and dynamics in a hyperthermophilic protein with melting temperature close to 200 °C, Proc. Natl. Acad. Sci. U. S. A., 94, 11329, 10.1073/pnas.94.21.11329 Pfeil, 1997, Ferredoxin from the hyperthermophile Thermotoga maritima is stable beyond the boiling point of water, J. Mol. Biol., 272, 591, 10.1006/jmbi.1997.1278 Higgins, 2002, Exceptional stability of a [2Fe–2S] ferrodoxin from hyperthermophilic bacterium Aquifex aeolicus, Biochim. Biophys. Acta, 1599, 82, 10.1016/S1570-9639(02)00405-3 Nielsen, 2003, A proposed mechanism for the thermal denaturation of a recombinant Bacillus halmapalus α-amylase—The effect of calcium ions, Biochim. Biophys. Acta, 1652, 52, 10.1016/j.bbapap.2003.08.002 Ahern, 1985, The mechanisms of irreversible enzyme inactivation at 100 °C, Science (Washington), 228, 1280, 10.1126/science.4001942 Zale, 1986, Why does ribonuclease irreversibly inactivate at high temperatures?, Biochemistry, 25, 5432, 10.1021/bi00367a014 Sandberg, 2002, Effects of metal ligation and oxygen on the reversibility of the thermal denaturation of Pseudomonas aeruginosa azurin, Biochemistry, 41, 1060, 10.1021/bi0157621 Sandberg, 2003, Thermal denaturation of spinach plastocyanin: effect of copper site oxidation state and molecular oxygen, Biochemistry, 42, 10301, 10.1021/bi034371e Tigerstrom, 2004, Effects of a novel disulfide bond and engineered electrostatic interactions on the thermostability of azurin, Biochemistry, 43, 12563, 10.1021/bi048926x Freire, 1990, Calorimetrically determined dynamics of complex unfolding transitions in proteins, Annu. Rev. Biophys. Biophys. Chem., 19, 159, 10.1146/annurev.bb.19.060190.001111 Lepock, 1992, Influence of transition rates and scan rate on kinetic simulations of differential scanning calorimetry profiles of reversible and irreversible protein denaturation, Biochemistry, 31, 12706, 10.1021/bi00165a023 Davoodi, 1998, Scan-Rate dependence in protein calorimetry—the reversible transitions of Bacillus circulans xylanase and a disulfide-bridge mutant, Protein Sci., 7, 1538, 10.1002/pro.5560070707 Sanchez-Ruiz, 1988, Differential scanning calorimetry of the irreversible thermal denaturation of thermolysin, Biochemistry, 27, 1648, 10.1021/bi00405a039 Idakieva, 2005, Differential scanning calorimetry of the irreversible denaturation of Rapana thomasiana (marine snail, Gastropod) hemocyanin, Biochim. Biophys. Acta, 1748, 50, 10.1016/j.bbapap.2004.12.004 Lyubarev, 1998, Irreversible thermal denaturation of uridine phosphorylase from Escherichia coli K-12, Biophys. Chem., 70, 247, 10.1016/S0301-4622(97)00133-6 Fessas, 2001, Thermal unfolding of monomeric and dimeric β-lactoglobulins, Eur. J. Biochem., 268, 5439, 10.1046/j.0014-2956.2001.02484.x Plaza del Pino, 2000, Lower kinetic limit to protein thermal stability: a proposal regarding protein stability in vivo and its relation with misfolding diseases, Proteins, 40, 58, 10.1002/(SICI)1097-0134(20000701)40:1<58::AID-PROT80>3.0.CO;2-M La Rosa, 1995, Thermodynamics of the thermal unfolding of azurin, J. Phys. Chem., 99, 14864, 10.1021/j100040a041 Suzuki, 1993, Novel spectroscopic aspects of type I copper in hyphomicrobium nitrite reductase, Inorg. Chim. Acta, 208, 107, 10.1016/S0020-1693(00)82892-3 LaCroix, 1996, 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, 7755, 10.1021/ja961217p Han, 1993, Resonance Raman excitation profiles indicate multiple Cys→Cu charge transfer transitions in type 1 copper proteins, J. Am. Chem. Soc., 115, 4256, 10.1021/ja00063a048 Kukimoto, 1994, 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, 5246, 10.1021/bi00183a030 McGarvey, 1967, Electron spin resonance of transition metal complexes, vol. 3, 90 Milardi, 1998, Thermodynamics and kinetics of the thermal unfolding of plastocyanin, Eur. Biophys. J., 27, 273, 10.1007/s002490050134 Guzzi, 1999, A spectroscopic and calorimetric investigation on the thermal stability of the Cys3Ala/Cys26Ala azurin mutant, Biophys. J., 77, 1052, 10.1016/S0006-3495(99)76955-9 La Rosa, 2002, A model for the thermal unfolding of amicyanin, Eur. Biophys. J., 30, 559, 10.1007/s00249-001-0193-z Guzzi, 2004, Thermal stability of wild type and disulfide bridge containing mutant of poplar plastocyanin, Biophys. Chem., 112, 35, 10.1016/j.bpc.2004.07.002