Structural and denaturation studies of two mutants of a cold adapted superoxide dismutase point to the importance of electrostatic interactions in protein stability
Structural and denaturation studies of two mutants of a cold adapted superoxide dismutase point to the importance of electrostatic interactions in protein stability(642 views) Merlino A, Russo Krauss I, Castellano I, Ruocco MR, Capasso A, De Vendittis E, Rossi B, Sica F
Dipartimento di Scienze Chimiche, Università di Napoli Federico II, Complesso Universitario di Monte sant'Angelo, I-80126 Napoli, Italy
Istituto di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 16, I-80134 Napoli, Italy
Stazione Zoologica Anton Dohrn, Villa Comunale, I-80121 Napoli, Italy
Dipartimento di Medicina Molecolare e Biotecnologie Mediche, Università di Napoli Federico II, Via S. Pansini 5, I-80131 Napoli, Italy
Istituto Nazionale di Biostrutture e Biosistemi, Consorzio Interuniversitario, Viale Medaglie d'Oro 305, I-00136 Roma, Italy
References: D'Amico, S., Collins, T., Marx, J.C., Feller, G., Gerday, C., Psychrophilic microorganisms: Challenges for life (2006) EMBO Rep., 7, pp. 385-38
Feller, G., Life at low temperatures: Is disorder the driving force? (2007) Extremophiles, 11, pp. 211-216
Marx, J.C., Blaise, V., Collins, T., D'Amico, S., Delille, D., Gratia, E., Hoyoux, A., Gerday, C., A perspective on cold enzymes: Current knowledge and frequently asked questions (2004) Cell. Mol. Biol. (Noisy-le-grand), 50, pp. 643-655
Huston, A.L., Haeggstrom, J.Z., Feller, G., Cold adaptation of enzymes: Structural, kinetic and microcalorimetric characterizations of an aminopeptidase from the Arctic psychrophile Colwellia psychrerythraea and of human leukotriene A(4) hydrolase (2008) Biochim. Biophys. Acta, 1784, pp. 1865-1872
Siddiqui, K.S., Cavicchioli, R., Cold-adapted enzymes (2006) Annual Review of Biochemistry, 75, pp. 403-433. , DOI 10.1146/annurev.biochem.75.103004.142723
De Vendittis, E., Castellano, I., Cotugno, R., Ruocco, M.R., Raimo, G., Masullo, M., Adaptation of model proteins from cold to hot environments involves continuous and small adjustments of average parameters related to amino acid composition (2008) Journal of Theoretical Biology, 250 (1), pp. 156-171. , DOI 10.1016/j.jtbi.2007.09.006, PII S0022519307004249
Merlino, A., Russo Krauss, I., Castellano, I., De Vendittis, E., Rossi, B., Conte, M., Vergara, A., Sica, F., Structure and flexibility in cold-adapted iron superoxide dismutases: The case of the enzyme isolated from Pseudoalteromonas haloplanktis (2010) J. Struct. Biol., 172, pp. 343-352
Castellano, I., Di Maro, A., Ruocco, M.R., Chambery, A., Parente, A., Di Martino, M.T., Parlato, G., De Vendittis, E., Psychrophilic superoxide dismutase from Pseudoalteromonas haloplanktis: Biochemical characterization and identification of a highly reactive cysteine residue (2006) Biochimie, 88 (10), pp. 1377-1389. , DOI 10.1016/j.biochi.2006.04.005, PII S0300908406000551
Miller, A.F., Superoxide dismutases: Ancient enzymes and new insights (2012) FEBS Lett., 586, pp. 585-595
Perry, J.J., Shin, D.S., Getzoff, E.D., Tainer, J.A., The structural biochemistry of the superoxide dismutases (2010) Biochim. Biophys. Acta, 1804, pp. 245-262
Castellano, I., Ruocco, M.R., Cecere, F., Di Maro, A., Chambery, A., Michniewicz, A., Parlato, G., De Vendittis, E., Glutathionylation of the iron superoxide dismutase from the psychrophilic eubacterium Pseudoalteromonas haloplanktis (2008) Biochim. Biophys. Acta, 1784, pp. 816-826
Parge, H.E., Getzoff, E.D., Scandella, C.S., Crystallographic characterization of recombinant human CuZn superoxide dismutase (1986) Journal of Biological Chemistry, 261 (34), pp. 16215-16218
McRee, D.E., Redford, S.M., Getzoff, E.D., Lepock, J.R., Hallewell, R.A., Tainer, J.A., Changes in crystallographic structure and thermostability of a Cu,Zn superoxide dismutase mutant resulting from the removal of a buried cysteine (1990) J. Biol. Chem., 265, pp. 14234-14241
Russo Krauss, I., Merlino, A., Vergara, A., Sica, F., An overview of biological macromolecule crystallization (2013) Int. J. Mol. Sci., 14, pp. 11643-11691
Merlino, A., Krauss, I.R., Castellano, I., De Vendittis, E., Vergara, A., Sica, F., Crystallization and preliminary X-ray diffraction studies of a psychrophilic iron superoxide dismutase from Pseudoalteromonas haloplanktis (2008) Protein and Peptide Letters, 15 (4), pp. 415-418. , http://docstore.ingenta.com/cgi-bin/ds_deliver/1/u/d/ISIS/44188690.1/ben/ ppl/2008/00000015/00000004/art00017/AD8EFBDF6FAC2CBA121067526311180442B08F628F. pdf?link=http://www.ingentaconnect.com/error/delivery&format=pdf, DOI 10.2174/092986608784246533
Lah, M.S., Dixon, M.M., Pattridge, K.A., Stallings, W.C., Fee, J.A., Ludwig, M.L., Structure-function in Escherichia coli iron superoxide dismutase: Comparisons with the manganese enzyme from Thermus thermophilus (1995) Biochemistry, 34, pp. 1646-1660
Otwinowski, Z., Minor, W., Processing of X-ray diffraction data collected in oscillation mode (1997) Methods in Enzymology, 276, pp. 307-326. , DOI 10.1016/S0076-6879(97)76066-X
Brunger, A.T., Adams, P.D., Clore, G.M., Delano, W.L., Gros, P., Grosse-Kunstleve, R.W., Jiang, J.S., Warren, G.L., Crystallography & NMR system: A new software suite for macromolecular structure determination (1998) Acta Crystallogr. D Biol. Crystallogr., 54 (PART 5), pp. 905-921
Murshudov, G.N., Vagin, A.A., Dodson, E.J., Refinement of macromolecular structures by the maximum-likelihood method (1997) Acta Crystallographica Section D: Biological Crystallography, 53 (3), pp. 240-255. , DOI 10.1107/S0907444996012255
Jones, T.A., Bergdoll, M., Kjeldgaard, M., O: A macromolecule modeling environment (1990) Crystallogr Model Methods Mol Des, [Pap Symp], pp. 189-199. , C. Bugg, S. Ealick, Springer-Verlag Press
Emsley, P., Lohkamp, B., Scott, W.G., Cowtan, K., Features and development of Coot (2010) Acta Crystallogr. D Biol. Crystallogr., 66 (PART 4), pp. 486-501
Laskowski, R.A., Macarthur, M.W., Moss, M.D., Thorton, J.M., PROCHECK: A program to check the stereochemical quality of protein structure (1993) J. Appl. Crystallogr., 26, pp. 283-291
McCord, J.M., Fridovich, I., Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) (1969) J. Biol. Chem., 244, pp. 6049-6055
Dello Russo, A., Rullo, R., Nitti, G., Masullo, M., Bocchini, V., Iron superoxide dismutase from the archaeon Sulfolobus solfataricus: Average hydrophobicity and amino acid weight are involved in the adaptation of proteins to extreme environments (1997) Biochimica et Biophysica Acta - Protein Structure and Molecular Enzymology, 1343 (1), pp. 23-30. , DOI 10.1016/S0167-4838(97)00105-2, PII S0167483897001052
Tierney, D.L., Fee, J.A., Ludwig, M.L., Penner-Hahn, J.E., X-ray absorption spectroscopy of the iron site in Escherichia coli Fe(III) superoxide dismutase (1995) Biochemistry, 34, pp. 1661-1668
Vathyam, S., Byrd, R.A., Miller, A.F., Mapping the effects of metal ion reduction and substrate analog binding to Fe-superoxide dismutase by NMR spectroscopy (2000) Magn. Reson. Chem., 38, pp. 536-542
Struvay, C., Feller, G., Optimization to low temperature activity in psychrophilic enzymes (2012) Int. J. Mol. Sci., 13, pp. 11643-11665
Pedersen, H.L., Willassen, N.P., Leiros, I., The first structure of a cold-adapted superoxide dismutase (SOD): Biochemical and structural characterization of iron SOD from Aliivibrio salmonicida (2009) Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun., 65, pp. 84-92
DiDonato, M., Craig, L., Huff, M.E., Thayer, M.M., Cardoso, R.M.F., Kassmann, C.J., Lo, T.P., Tainer, J.A., ALS mutants of human superoxide dismutase form fibrous aggregates via framework destabilization (2003) Journal of Molecular Biology, 332 (3), pp. 601-615. , DOI 10.1016/S0022-2836(03)00889-1
Mizuno, K., Whittaker, M.M., Bachinger, H.P., Whittaker, J.W., Calometric studies on the tight binding metal interactions of Escherichia coli manganese superoxide dismutase (2004) Journal of Biological Chemistry, 279 (26), pp. 27339-27344. , DOI 10.1074/jbc.M400813200
Ludwig, M.L., Metzger, A.L., Pattridge, K.A., Stallings, W.C., Manganese superoxide dismutase from Thermus thermophilus. A structural model refined at 1.8 A resolution (1991) J. Mol. Biol., 219, pp. 335-358
Vance, C.K., Miller, A.-F., Spectroscopic comparisons of the pH dependencies of Fe-substituted (Mn)superoxide dismutase and Fe-superoxide dismutase (1998) Biochemistry, 37 (16), pp. 5518-5527. , DOI 10.1021/bi972580r
De Vendittis, A., Amato, M., Mickniewicz, A., Parlato, G., De Angelis, A., Castellano, I., Rullo, R., De Vendittis, E., Regulation of the properties of superoxide dismutase from the dental pathogenic microorganism Streptococcus mutans by iron- and manganese-bound co-factor (2010) Mol. Biosyst., 6, pp. 1973-1982
De Vendittis, A., Marco, S., Di Maro, A., Chambery, A., Albino, A., Masullo, M., Michniewicz, A., Rullo, R., Properties of a putative cambialistic superoxide dismutase from the aerotolerant bacterium Streptococcus thermophilus strain LMG 18311 (2012) Protein Pept. Lett., 19, pp. 333-344
Zavodszky, P., Kardos, J., Svingor, A., Petsko, G.A., Adjustment of conformational flexibility is a key event in the thermal adaptation of proteins (1998) Proceedings of the National Academy of Sciences of the United States of America, 95 (13), pp. 7406-7411. , DOI 10.1073/pnas.95.13.7406
Bae, E., Phillips Jr., G.N., Structures and analysis of highly homologous psychrophilic, mesophilic, and thermophilic adenylate kinases (2004) Journal of Biological Chemistry, 279 (27), pp. 28202-28208. , DOI 10.1074/jbc.M401865200
Georlette, D., Damien, B., Blaise, V., Depiereux, E., Uversky, V.N., Gerday, C., Feller, G., Structural and functional adaptations to extreme temperatures in psychrophilic, mesophilic, and thermophilic DNA ligases (2003) Journal of Biological Chemistry, 278 (39), pp. 37015-37023. , DOI 10.1074/jbc.M305142200
Unsworth, L.D., Van Der Oost, J., Koutsopoulos, S., Hyperthermophilic enzymes - Stability, activity and implementation strategies for high temperature applications (2007) FEBS Journal, 274 (16), pp. 4044-4056. , DOI 10.1111/j.1742-4658.2007.05954.x
Shin, D.S., Didonato, M., Barondeau, D.P., Hura, G.L., Hitomi, C., Berglund, J.A., Getzoff, E.D., Tainer, J.A., Superoxide dismutase from the eukaryotic thermophile Alvinella pompejana: Structures, stability, mechanism, and insights into amyotrophic lateral sclerosis (2009) J. Mol. Biol., 385, pp. 1534-1555
Myers, J.K., Pace, C.N., Scholtz, J.M., Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding (1995) Protein Sci., 4, pp. 2138-2148
O'Brien, E.P., Dima, R.I., Brooks, B., Thirumalai, D., Interactions between hydrophobic and ionic solutes in aqueous guanidinium chloride and urea solutions: Lessons for protein denaturation mechanism (2007) Journal of the American Chemical Society, 129 (23), pp. 7346-7353. , DOI 10.1021/ja069232+
Granata, V., Del Vecchio, P., Barone, G., Shehi, E., Fusi, P., Tortora, P., Graziano, G., Guanidine-induced unfolding of the Sso7d protein from the hyperthermophilic archaeon Sulfolobus solfataricus (2004) International Journal of Biological Macromolecules, 34 (3), pp. 195-201. , DOI 10.1016/j.ijbiomac.2004.04.002, PII S0141813004000200
Marx, J. C., Blaise, V., Collins, T., D'Amico, S., Delille, D., Gratia, E., Hoyoux, A., Gerday, C., A perspective on cold enzymes: Current knowledge and frequently asked questions (2004) Cell. Mol. Biol. (Noisy-le-grand), 50, pp. 643-655
Huston, A. L., Haeggstrom, J. Z., Feller, G., Cold adaptation of enzymes: Structural, kinetic and microcalorimetric characterizations of an aminopeptidase from the Arctic psychrophile Colwellia psychrerythraea and of human leukotriene A (4) hydrolase (2008) Biochim. Biophys. Acta, 1784, pp. 1865-1872
Siddiqui, K. S., Cavicchioli, R., Cold-adapted enzymes (2006) Annual Review of Biochemistry, 75, pp. 403-433. , DOI 10. 1146/annurev. biochem. 75. 103004. 142723
Miller, A. F., Superoxide dismutases: Ancient enzymes and new insights (2012) FEBS Lett., 586, pp. 585-595
Perry, J. J., Shin, D. S., Getzoff, E. D., Tainer, J. A., The structural biochemistry of the superoxide dismutases (2010) Biochim. Biophys. Acta, 1804, pp. 245-262
Parge, H. E., Getzoff, E. D., Scandella, C. S., Crystallographic characterization of recombinant human CuZn superoxide dismutase (1986) Journal of Biological Chemistry, 261 (34), pp. 16215-16218
McRee, D. E., Redford, S. M., Getzoff, E. D., Lepock, J. R., Hallewell, R. A., Tainer, J. A., Changes in crystallographic structure and thermostability of a Cu, Zn superoxide dismutase mutant resulting from the removal of a buried cysteine (1990) J. Biol. Chem., 265, pp. 14234-14241
Lah, M. S., Dixon, M. M., Pattridge, K. A., Stallings, W. C., Fee, J. A., Ludwig, M. L., Structure-function in Escherichia coli iron superoxide dismutase: Comparisons with the manganese enzyme from Thermus thermophilus (1995) Biochemistry, 34, pp. 1646-1660
Brunger, A. T., Adams, P. D., Clore, G. M., Delano, W. L., Gros, P., Grosse-Kunstleve, R. W., Jiang, J. S., Warren, G. L., Crystallography & NMR system: A new software suite for macromolecular structure determination (1998) Acta Crystallogr. D Biol. Crystallogr., 54 (PART 5), pp. 905-921
Murshudov, G. N., Vagin, A. A., Dodson, E. J., Refinement of macromolecular structures by the maximum-likelihood method (1997) Acta Crystallographica Section D: Biological Crystallography, 53 (3), pp. 240-255. , DOI 10. 1107/S0907444996012255
Jones, T. A., Bergdoll, M., Kjeldgaard, M., O: A macromolecule modeling environment (1990) Crystallogr Model Methods Mol Des, [Pap Symp], pp. 189-199. , C. Bugg, S. Ealick, Springer-Verlag Press
Laskowski, R. A., Macarthur, M. W., Moss, M. D., Thorton, J. M., PROCHECK: A program to check the stereochemical quality of protein structure (1993) J. Appl. Crystallogr., 26, pp. 283-291
McCord, J. M., Fridovich, I., Superoxide dismutase. An enzymic function for erythrocuprein (hemocuprein) (1969) J. Biol. Chem., 244, pp. 6049-6055
Tierney, D. L., Fee, J. A., Ludwig, M. L., Penner-Hahn, J. E., X-ray absorption spectroscopy of the iron site in Escherichia coli Fe (III) superoxide dismutase (1995) Biochemistry, 34, pp. 1661-1668
Pedersen, H. L., Willassen, N. P., Leiros, I., The first structure of a cold-adapted superoxide dismutase (SOD): Biochemical and structural characterization of iron SOD from Aliivibrio salmonicida (2009) Acta Crystallogr. Sect. F: Struct. Biol. Cryst. Commun., 65, pp. 84-92
Ludwig, M. L., Metzger, A. L., Pattridge, K. A., Stallings, W. C., Manganese superoxide dismutase from Thermus thermophilus. A structural model refined at 1. 8 A resolution (1991) J. Mol. Biol., 219, pp. 335-358
Vance, C. K., Miller, A. -F., Spectroscopic comparisons of the pH dependencies of Fe-substituted (Mn) superoxide dismutase and Fe-superoxide dismutase (1998) Biochemistry, 37 (16), pp. 5518-5527. , DOI 10. 1021/bi972580r
Unsworth, L. D., Van Der Oost, J., Koutsopoulos, S., Hyperthermophilic enzymes - Stability, activity and implementation strategies for high temperature applications (2007) FEBS Journal, 274 (16), pp. 4044-4056. , DOI 10. 1111/j. 1742-4658. 2007. 05954. x
Shin, D. S., Didonato, M., Barondeau, D. P., Hura, G. L., Hitomi, C., Berglund, J. A., Getzoff, E. D., Tainer, J. A., Superoxide dismutase from the eukaryotic thermophile Alvinella pompejana: Structures, stability, mechanism, and insights into amyotrophic lateral sclerosis (2009) J. Mol. Biol., 385, pp. 1534-1555
Myers, J. K., Pace, C. N., Scholtz, J. M., Denaturant m values and heat capacity changes: Relation to changes in accessible surface areas of protein unfolding (1995) Protein Sci., 4, pp. 2138-2148
O'Brien, E. P., Dima, R. I., Brooks, B., Thirumalai, D., Interactions between hydrophobic and ionic solutes in aqueous guanidinium chloride and urea solutions: Lessons for protein denaturation mechanism (2007) Journal of the American Chemical Society, 129 (23), pp. 7346-7353. , DOI 10. 1021/ja069232+
Structural and denaturation studies of two mutants of a cold adapted superoxide dismutase point to the importance of electrostatic interactions in protein stability
A peculiar feature of the psychrophilic iron superoxide dismutase from Pseudoalteromonas haloplanktis (PhSOD) is the presence in its amino acid sequence of a reactive cysteine (Cys57). To define the role of this residue, a structural characterization of the effect of two PhSOD mutations, C57S and C57R, was performed. Thermal and denaturant-induced unfolding of wild type and mutant PhSOD followed by circular dichroism and fluorescence studies revealed that C -> R substitution alters the thermal stability and the resistance against denaturants of the enzyme, whereas C57S only alters the stability of the protein against urea. The crystallographic data on the C57R mutation suggest an involvement of the Arg side chain in the formation of salt bridges on protein surface. These findings support the hypothesis that the thermal resistance of PhSOD relies on optimization of charge-charge interactions on its surface. Our study contributes to a deeper understanding of the denaturation mechanism of superoxide dismutases, suggesting the presence of a structural dimeric intermediate between the native state and the unfolded state. This hypothesis is supported by the crystalline and solution data on the reduced form of the enzyme. (C) 2014 Elsevier B.V. All rights reserved.
Structural and denaturation studies of two mutants of a cold adapted superoxide dismutase point to the importance of electrostatic interactions in protein stability
Structural and denaturation studies of two mutants of a cold adapted superoxide dismutase point to the importance of electrostatic interactions in protein stability