Crystallographic and spectroscopic characterizations of Sulfolobus solfataricus TrxA1 provide insights into the determinants of thioredoxin fold stability
Crystallographic and spectroscopic characterizations of Sulfolobus solfataricus TrxA1 provide insights into the determinants of thioredoxin fold stability(301 views) Esposito L, Ruggiero A, Masullo M, Ruocco MR, Lamberti A, Arcari P, Zagari A, Vitagliano L
Istituto di Biostrutture e Bioimmagini, CNR, Via Mezzocannone 16, I-80134 Napoli, Italy
Dipartimento delle Scienze Biologiche, Sezione di Biostrutture, Università degli Studi di Napoli Federico II, Via Mezzocannone 16, I-80134 Napoli, Italy
Dipartimento di Studi delle Istituzioni e dei Sistemi Territoriali, Università degli Studi di Napoli Parthenope, Via Medina 40, 80133 Napoli, Italy
Dipartimento di Biochimica e Biotecnologie Mediche, Università degli Studi di Napoli Federico II, Via S. Pansini 5, I-80131 Napoli, Italy
CEINGE Biotecnologie Avanzate s.c.a r.l., Via Gaetano Salvatore 486, I-80145 Napoli, Italy
References: Arner, E.S., Holmgren, A., Physiological functions of thioredoxin and thioredoxin reductase (2000) Eur. J. Biochem., 267, pp. 6102-610
Brunger, A.T., Version of the crystallography and NMR system (2007) Nat. Protoc., 2, pp. 2728-2733
Capitani, G., Markovic-Housley, Z., DelVal, G., Morris, M., Jansonius, J.N., Crystal structures of two functionally different thioredoxins in spinach chloroplasts (2000) J. Mol. Biol., 302, pp. 135-154
Carvalho, A.P., Fernandes, P.A., Ramos, M.J., Similarities and differences in the thioredoxin superfamily (2006) Prog. Biophys. Mol. Biol., 91, pp. 229-248
Carvalho, A.T., Fernandes, P.A., Ramos, M.J., Determination of the DeltapKa between the active site cysteines of thioredoxin and DsbA (2006) J. Comput. Chem., 27, pp. 966-975
Cecere, F., Iuliano, A., Albano, F., Zappelli, C., Castellano, I., Diclofenac-induced apoptosis in the neuroblastoma cell line SH-SY5Y: possible involvement of the mitochondrial superoxide dismutase (2010) J. Biomed. Biotechnol., 2010, p. 801726
Chivers, P.T., Raines, R.T., General acid/base catalysis in the active site of Escherichia coli thioredoxin (1997) Biochemistry, 36, pp. 15810-15816
Chivers, P.T., Prehoda, K.E., Volkman, B.F., Kim, B.M., Markley, J.L., Microscopic pKa values of Escherichia coli thioredoxin (1997) Biochemistry, 36, pp. 14985-14991
Colas, P., Cohen, B., Jessen, T., Grishina, I., McCoy, J., Brent, R., Genetic selection of peptide aptamers that recognize and inhibit cyclin-dependent kinase 2 (1996) Nature, 380, pp. 548-550
Eriksson, A.E., Baase, W.A., Zhang, X.J., Heinz, D.W., Blaber, M., Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect (1992) Science, 255, pp. 178-183
Flocco, M.M., Mowbray, S.L., Strange bedfellows: interactions between acidic side-chains in proteins (1995) J. Mol. Biol., 254, pp. 96-105
Granata, V., Graziano, G., Ruggiero, A., Raimo, G., Masullo, M., Chemical denaturation of the elongation factor 1alpha isolated from the hyperthermophilic archaeon Sulfolobus solfataricus (2006) Biochemistry, 45, pp. 719-726
Grimaldi, P., Ruocco, M.R., Lanzotti, M.A., Ruggiero, A., Ruggiero, I., Characterisation of the components of the thioredoxin system in the archaeon Sulfolobus solfataricus (2008) Extremophiles, 12, pp. 553-562
Holmgren, A., Thioredoxin structure and mechanism: conformational changes on oxidation of the active-site sulfhydryls to a disulfide (1995) Structure, 3, pp. 239-243
Ibarra-Molero, B., Loladze, V.V., Makhatadze, G.I., Sanchez-Ruiz, J.M., Thermal versus guanidine-induced unfolding of ubiquitin. An analysis in terms of the contributions from charge-charge interactions to protein stability (1999) Biochemistry, 38, pp. 8138-8149
Ito, N., Komiyama, N.H., Fermi, G., Structure of deoxyhaemoglobin of the antarctic fish Pagothenia bernacchii with an analysis of the structural basis of the root effect by comparison of the liganded and unliganded haemoglobin structures (1995) J. Mol. Biol., 250, pp. 648-658
Jones, T.A., Zou, J.Y., Cowan, S.W., Kjeldgaard, M., Improved methods for building protein models in electron density maps and the location of errors in these models (1991) Acta Crystallogr. A, A47, pp. 110-119
Katti, S.K., LeMaster, D.M., Eklund, H., Crystal structure of thioredoxin from Escherichia coli at 1.68A resolution (1990) J. Mol. Biol., 212, pp. 167-184
Krissinel, E., Henrick, K., Inference of macromolecular assemblies from crystalline state (2007) J. Mol. Biol., 372, pp. 774-797
Kumar, S., Nussinov, R., How do thermophilic proteins deal with heat? (2001) Cell. Mol. Life Sci., 58, pp. 1216-1233
Kumar, S., Tsai, C.J., Nussinov, R., Factors enhancing protein thermostability (2000) Protein Eng., 13, pp. 179-191
Ladenstein, R., Ren, B., Protein disulfides and protein disulfide oxidoreductases in hyperthermophiles (2006) FEBS J., 273, pp. 4170-4185
LaVallie, E.R., DiBlasio, E.A., Kovacic, S., Grant, K.L., Schendel, P.F., A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. Coli cytoplasm (1993) Biotechnology (NY), 11, pp. 187-193
Leone, M., Di Lello, P., Ohlenschlager, O., Pedone, E.M., Bartolucci, S., Solution structure and backbone dynamics of the K18G/R82E Alicyclobacillus acidocaldarius thioredoxin mutant: a molecular analysis of its reduced thermal stability (2004) Biochemistry, 43, pp. 6043-6058
Lillig, C.H., Holmgren, A., Thioredoxin and related molecules-from biology to health and disease (2007) Antioxid. Redox Signal., 9, pp. 25-47
Makhatadze, G.I., Lopez, M.M., Richardson, J.M., Thomas, S.T., Anion binding to the ubiquitin molecule (1998) Protein Sci., 7, pp. 689-697
Maulik, N., Das, D.K., Emerging potential of thioredoxin and thioredoxin interacting proteins in various disease conditions (2008) Biochim. Biophys. Acta, 1780, pp. 1368-1382
Mazzarella, L., Vergara, A., Vitagliano, L., Merlino, A., Bonomi, G., High resolution crystal structure of deoxy hemoglobin from Trematomus bernacchii at different pH values: the role of histidine residues in modulating the strength of the root effect (2006) Proteins, 65, pp. 490-498
Mazzarella, L., Bonomi, G., Lubrano, M.C., Merlino, A., Riccio, A., Minimal structural requirements for root effect: crystal structure of the cathodic hemoglobin isolated from the antarctic fish Trematomus newnesi (2006) Proteins, 62, pp. 316-321
Ming, H., Kato, Y., Miyazono, K., Ito, K., Kamo, M., Crystal structure of thioredoxin domain of ST2123 from thermophilic archaea Sulfolobus tokodaii strain7 (2007) Proteins, 69, pp. 204-208
Moretto, N., Bolchi, A., Rivetti, C., Imbimbo, B.P., Villetti, G., Conformation-sensitive antibodies against alzheimer amyloid-beta by immunization with a thioredoxin-constrained B-cell epitope peptide (2007) J. Biol. Chem., 282, pp. 11436-11445
Pedone, E., Limauro, D., D'Alterio, R., Rossi, M., Bartolucci, S., Characterization of a multifunctional protein disulfide oxidoreductase from Sulfolobus solfataricus (2006) FEBS J., 273, pp. 5407-5420
Petsko, G.A., Structural basis of thermostability in hyperthermophilic proteins, or "there's more than one way to skin a cat" (2001) Methods Enzymol., 334, pp. 469-478
Ruggiero, A., Ruocco, M.R., Grimaldi, P., Arcari, P., Masullo, M., Crystallization and preliminary X-ray crystallographic analysis of Sulfolobus solfataricus thioredoxin reductase (2005) Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun., 61, pp. 906-909
Ruggiero, A., Masullo, M., Marasco, D., Ruocco, M.R., Grimaldi, P., The dimeric structure of Sulfolobus solfataricus thioredoxin A2 and the basis of its thermostability (2009) Proteins, 77, pp. 1004-1008
Ruggiero, A., Lanzotti, M.A., Ruocco, M.R., Grimaldi, P., Marasco, D., Crystallization and preliminary X-ray crystallographic analysis of two dimeric hyperthermostable thioredoxins isolated from Sulfolobus solfataricus (2009) Acta Crystallogr., Sect. F: Struct. Biol. Cryst. Commun., 65, pp. 604-607
Ruocco, M.R., Ruggiero, A., Masullo, L., Arcari, P., Masullo, M., A 35kDa NAD(P)H oxidase previously isolated from the archaeon Sulfolobus solfataricus is instead a thioredoxin reductase (2004) Biochimie, 86, pp. 883-892
Tang, G.W., Altman, R.B., Remote thioredoxin recognition using evolutionary conservation and structural dynamics (2011) Structure, 19, pp. 461-470
Arner, E. S., Holmgren, A., Physiological functions of thioredoxin and thioredoxin reductase (2000) Eur. J. Biochem., 267, pp. 6102-610
Brunger, A. T., Version of the crystallography and NMR system (2007) Nat. Protoc., 2, pp. 2728-2733
Carvalho, A. P., Fernandes, P. A., Ramos, M. J., Similarities and differences in the thioredoxin superfamily (2006) Prog. Biophys. Mol. Biol., 91, pp. 229-248
Carvalho, A. T., Fernandes, P. A., Ramos, M. J., Determination of the DeltapKa between the active site cysteines of thioredoxin and DsbA (2006) J. Comput. Chem., 27, pp. 966-975
Chivers, P. T., Raines, R. T., General acid/base catalysis in the active site of Escherichia coli thioredoxin (1997) Biochemistry, 36, pp. 15810-15816
Chivers, P. T., Prehoda, K. E., Volkman, B. F., Kim, B. M., Markley, J. L., Microscopic pKa values of Escherichia coli thioredoxin (1997) Biochemistry, 36, pp. 14985-14991
Eriksson, A. E., Baase, W. A., Zhang, X. J., Heinz, D. W., Blaber, M., Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect (1992) Science, 255, pp. 178-183
Flocco, M. M., Mowbray, S. L., Strange bedfellows: interactions between acidic side-chains in proteins (1995) J. Mol. Biol., 254, pp. 96-105
Jones, T. A., Zou, J. Y., Cowan, S. W., Kjeldgaard, M., Improved methods for building protein models in electron density maps and the location of errors in these models (1991) Acta Crystallogr. A, A47, pp. 110-119
Katti, S. K., LeMaster, D. M., Eklund, H., Crystal structure of thioredoxin from Escherichia coli at 1. 68A resolution (1990) J. Mol. Biol., 212, pp. 167-184
LaVallie, E. R., DiBlasio, E. A., Kovacic, S., Grant, K. L., Schendel, P. F., A thioredoxin gene fusion expression system that circumvents inclusion body formation in the E. Coli cytoplasm (1993) Biotechnology (NY), 11, pp. 187-193
Lillig, C. H., Holmgren, A., Thioredoxin and related molecules-from biology to health and disease (2007) Antioxid. Redox Signal., 9, pp. 25-47
Makhatadze, G. I., Lopez, M. M., Richardson, J. M., Thomas, S. T., Anion binding to the ubiquitin molecule (1998) Protein Sci., 7, pp. 689-697
Petsko, G. A., Structural basis of thermostability in hyperthermophilic proteins, or "there's more than one way to skin a cat" (2001) Methods Enzymol., 334, pp. 469-478
Ruocco, M. R., Ruggiero, A., Masullo, L., Arcari, P., Masullo, M., A 35kDa NAD (P) H oxidase previously isolated from the archaeon Sulfolobus solfataricus is instead a thioredoxin reductase (2004) Biochimie, 86, pp. 883-892
Tang, G. W., Altman, R. B., Remote thioredoxin recognition using evolutionary conservation and structural dynamics (2011) Structure, 19, pp. 461-470
Crystallographic and spectroscopic characterizations of Sulfolobus solfataricus TrxA1 provide insights into the determinants of thioredoxin fold stability
Structural characterizations of thioredoxins (Trxs) are important for their involvement in severe pathologies and for their stable scaffold. Here we report a combined structural and spectroscopic characterization of a Trx isolated from the hyperthermophilic archaeon Sulfolobus solfataricus (SsTrxA1). Thermal denaturation unveils that SsTrxA1 is endowed with a remarkable stability in the explored temperature range 50-105 degrees C. The structure of the oxidized form of SsTrxA1 determined at 1.9 angstrom resolution presents a number of peculiar features. Although the protein was crystallized in a slightly acid medium (pH 6.5) as many as ten intramolecular/intermolecular carboxyl-carboxylate interactions involving glutamic and aspartic acid side chains are found in three independent SsTrxA1 molecules present in the asymmetric unit. Surprisingly for a hyperthermostable protein, the structure of SsTrxA1 is characterized by the presence (a) of a very limited number of intramolecular salt bridges and (b) of a cavity nearby Cys52, a residue that is frequently a phenylananine in other members of the family. Chemical denaturation investigations carried out on SsTrxA1 and SsTrxA2 show that both proteins present a significant stability against guanidine hydrochloride, thus indicating that ionic interactions play a minor role in their stabilization. Compared to Trxs from mesophilic sources, SsTrxA1 displays a longer alpha-helix 1 and a shorter loop connecting this alpha-helix with beta-strand 2. As these features are shared with Trxs isolated from thermophilic sources, the shortening of this loop may be a general strategy adopted to stabilize this fold. This feature may be exploited for the design of hyperthermostable Inc scaffolds. (C) 2011 Elsevier Inc. All rights reserved.
Crystallographic and spectroscopic characterizations of Sulfolobus solfataricus TrxA1 provide insights into the determinants of thioredoxin fold stability
Crystallographic and spectroscopic characterizations of Sulfolobus solfataricus TrxA1 provide insights into the determinants of thioredoxin fold stability