Mannosylglycerate stabilizes staphylococcal nuclease with restriction of slow β-sheet motions

Protein Science

Volumn 21, Issue 8, 2012, Pages 1126-1137

  Pais, Tiago M ^a   Lamosa, Pedro ^a   Matzapetakis, Manolis ^a   Turner, David L ^a   Santos, Helena ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

Author keywords

NMR; Osmolytes; Protein dynamics; Protein stabilization; Proton deuterium exchange

Indexed keywords

GLYCERIC ACID; MANNOSYLGLYCERATE; NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; BETA SHEET; ENZYME STABILITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FOLDING; PROTEIN UNFOLDING; STAPHYLOCOCCUS; THERMOSTABILITY;

EXCIPIENTS; GLYCERIC ACIDS; MANNOSE; MICROCOCCAL NUCLEASE; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; STAPHYLOCOCCUS AUREUS; THERMODYNAMICS;

EID: 84863795258     PISSN: 09618368     EISSN: 1469896X     Source Type: Journal    
DOI: 10.1002/pro.2100     Document Type: Article

References (56)

1. Brown AD, Simpson JR (1972) Water relations of sugar-tolerant yeasts: the role of intracellular polyols. J Gen Microbiol 72:589-591.
2. Brown AD (1976) Microbial water stress. Bacteriological Rev 40:803-846.
3. Santos H, Lamosa P, Faria TQ, Borges N, Neves C (2007) The physiological role, biosynthesis and mode of action of compatible solutes from (hyper)thermophiles. In: Gerday C, Glansdorff N, Eds. Physiology and biochemistry of extremophiles. ASM Publishers: Washington, D.C. pp 86-103.
4. Faria TQ, Mingote A, Siopa F, Ventura R, Maycock C, Santos H (2008) Design of new enzyme stabilizers inspired by glycosides of hyperthermophilic microorganisms. Carbohydr Res 343:3025-3033.
5. Faria TQ, Lima JC, Bastos M, Macanita AL, Santos H (2004) Protein stabilization by osmolytes from hyperthermophiles: effect of mannosylglycerate on the thermal unfolding of recombinant nuclease a from Staphylococcus aureus studied by picosecond time-resolved fluorescence and calorimetry. J Biol Chem 279:48680-48691. (Pubitemid 39625744)
6. Nozaki Y, Tanford C (1963) The solubility of amino acids and related compounds in aqueous urea solutions. J Biol Chem 238:4074-4081.
7. Nozaki Y, Tanford C (1970) The solubility of amino acids, diglycine, and triglycine in aqueous guanidine hydrochloride solutions. J Biol Chem 245:1648-1652.
8. Arakawa T, Timasheff SN (1985) The stabilization of proteins by osmolytes. Biophys J 47:411-414.
9. Auton M, Bolen DW (2004) Additive transfer free energies of the peptide backbone unit that are independent of the model compound and the choice of concentration scale. Biochemistry 43:1329-1342. (Pubitemid 38176532)
10. Liu Y, Bolen DW (1995) The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemistry 34:12884-12891.
11. Timasheff SN (1992) Water as ligand: preferential binding and exclusion of denaturants in protein unfolding. Biochemistry 31:9857-9864.
12. Pais TM, Lamosa P, Garcia-Moreno B, Turner DL, Santos H (2009) Relationship between protein stabilization and protein rigidification induced by mannosylglycerate. J Mol Biol 394:237-250.
13. Wang A, Robertson AD, Bolen DW (1995) Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry 34:15096-15104.
14. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules 1. Theory and range of validity. J Am Chem Soc 104:4546-4559.
15. Lipari G, Szabo A (1982) Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules 2. Analysis of experimental results. J Am Chem Soc 104:4559-4570.
16. Hvidt A, Nielsen SO (1966) Hydrogen exchange in proteins. Adv Protein Chem 21:287-386.
17. Lamosa P, Turner DL, Ventura R, Maycock C, Santos H (2003) Protein stabilization by compatible solutes. Effect of diglycerol phosphate on the dynamics of Desulfovibrio gigas rubredoxin studied by NMR. Eur J Biochem 270:4606-4614. (Pubitemid 37487229)
18. Tanford C (1970) Protein denaturation. C. Theoretical models for the mechanism of denaturation. Adv Protein Chem 24:1-95.
19. Schellman JA (1987) The thermodynamic stability of proteins. Annu Rev Biophys Biophys Chem 16:115-137.
20. Bai Y, Sosnick TR, Mayne L, Englander SW (1995) Protein folding intermediates: native-state hydrogen exchange. Science 269:192-197.
21. Mayo SL, Baldwin RL (1993) Guanidinium chloride induction of partial unfolding in amide proton exchange in RNase A. Science 262:873-876. (Pubitemid 24014074)
22. Nicholson LK, Kay LE, Baldisseri DM, Arango J, Young PE, Bax A, Torchia DA (1992) Dynamics of methyl groups in proteins as studied by proton-detected 13C NMR spectroscopy. Application to the leucine residues of staphylococcal nuclease. Biochemistry 31:5253-5263.
23. Cordier F, Caffrey M, Brutscher B, Cusanovich MA, Marion D, Blackledge M (1998) Solution structure, rotational diffusion anisotropy and local backbone dynamics of Rhodobacter capsulatus cytochrome c2. J Mol Biol 281:341-361. (Pubitemid 28360598)
24. Dosset P, Hus JC, Blackledge M, Marion D (2000) Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J Biomol NMR 16: 23-28. (Pubitemid 30114721)
25. d'Auvergne EJ, Gooley PR (2008) Optimisation of NMR dynamic models I. Minimisation algorithms and their performance within the model-free and Brownian rotational diffusion spaces. J Biomol NMR 40:107-119.
26. d'Auvergne EJ, Gooley PR (2008) Optimisation of NMR dynamic models II. A new methodology for the dual optimisation of the model-free parameters and the Brownian rotational diffusion tensor. J Biomol NMR 40:121-133.
27. Linderstrøm-Lang K (1955) The pH-dependence of the deuterium exchange of insulin. Biochim Biophys Acta 18:308.
28. Bédard S, Mayne LC, Peterson RW, Wand AJ, Englander SW (2008) The foldon substructure of staphylococcal nuclease. J Mol Biol 376:1142-1154.
29. Bai Y, Milne JS, Mayne L, Englander SW (1993) Primary structure effects on peptide group hydrogen exchange. Proteins 17:75-86. (Pubitemid 23261059)
30. Pace CN, Shirley BA, McNutt M, Gajiwala K (1996) Forces contributing to the conformational stability of proteins. Faseb J 10:75-83. (Pubitemid 26035509)
31. Myers JK, Pace CN, Scholtz JM (1995) Denaturant m-values and heat-capacity changes - relation to changes in accessible surface-areas of protein unfolding. Protein Sci 4:2138-2148.
32. Lee AL, Flynn PF, Wand AJ (1999) Comparison of H-2 and C-13 NMR relaxation techniques for the study of protein methyl group dynamics in solution. J Am Chem Soc 121:2891-2902. (Pubitemid 29165526)
33. Yang DW, Kay LE (1996) Contributions to conformational entropy arising from bond vector fluctuations measured from NMR-derived order parameters: application to protein folding. J Mol Biol 263:369-382.
34. Li Z, Raychaudhuri S, Wand AJ (1996) Insights into the local residual entropy of proteins provided by NMR relaxation. Protein Sci 5:2647-2650. (Pubitemid 26424878)
35. 2+ binding by calbindin D9k. J Am Chem Soc 115:9832-9833.
36. Englander SW, Kallenbach NR (1983) Hydrogen-exchange and structural dynamics of proteins and nucleic-acids. Q Rev Biophys 16:521-655.
37. Watson E, Matousek WM, Irimies EL, Alexandrescu AT (2007) Partially folded states of staphylococcal nuclease highlight the conserved structural hierarchy of OB-fold proteins. Biochemistry 46:9484-9494. (Pubitemid 47291955)
38. Zhang O, Kay LE, Shortle D, Forman-Kay JD (1997) Comprehensive NOE characterization of a partially folded large fragment of staphylococcal nuclease D131D, using NMR methods with improved resolution. J Mol Biol 272:9-20. (Pubitemid 27395533)
39. Wooll JO, Wrabl JO, Hilser VJ (2000) Ensemble modulation as an origin of denaturant-independent hydrogen exchange in proteins. J Mol Biol 301:247-256.
40. Mello CC, Barrick D (2003) Measuring the stability of partly folded proteins using TMAO. Protein Sci 12: 1522-1529. (Pubitemid 36759355)
41. Wang Y, Shortle D (1995) The equilibrium folding pathway of staphylococcal nuclease: Identification of the most stable chain-chain interactions by NMR and CD spectroscopy. Biochemistry 34:15895-15905.
42. Walkenhorst WF, Edwards JA, Markley JL, Roder H (2002) Early formation of a beta hairpin during folding of staphylococcal nuclease H124L as detected by pulsed hydrogen exchange. Protein Sci 11:82-91. (Pubitemid 34024760)
43. Shortle D, Abeygunawardana C (1993) NMR analysis of the residual structure in the denatured state of an unusual mutant of staphylococcal nuclease. Structure 1:121-134.
44. Green SM, Shortle D (1993) Patterns of nonadditivity between pairs of stability mutations in staphylococcal nuclease. Biochemistry 32:10131-10139. (Pubitemid 23312442)
45. Carra JH, Privalov PL (1995) Energetics of denaturation and m-values of staphylococcal nuclease mutants. Biochemistry 34:2034-2041.
46. Chen J, Lu Z, Sakon J, Stites WE (2000) Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability. J Mol Biol 303:125-130.
47. Calhoun DB, Englander SW (1985) Internal protein motions, concentrated glycerol, and hydrogen exchange studied in myoglobin. Biochemistry 24:2095-2100. (Pubitemid 15018541)
48. Santoro MM, Bolen DW (1988) Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27:8063-8068.
49. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOE assignment using the new software CANDID and the torsion angle dynamics algorithm DYANA. J Mol Biol 319:209-227. (Pubitemid 34729497)
50. Herrmann T, Güntert P, Wüthrich K (2002) Protein NMR structure determination with automated NOEidentification in the NOESY spectra using the new software ATNOS. J Biomol NMR 24:171-189. (Pubitemid 36113646)
51. Güntert P, Mumenthaler C, Wüthrich K (1997) Torsion angle dynamics for NMR structure calculation with the new program DYANA. J Mol Biol 273:283-298.
52. Nederveen AJ, Doreleijers JF, Vranken W, Miller Z, Spronk CA, Nabuurs SB, Guntert P, Livny M, Markley JL, Nilges M, Ulrich EL, Kaptein R, Bonvin AM (2005) RECOORD: a recalculated coordinate database of 500+ proteins from the PDB using restraints from the Bio- MagResBank. Proteins 59:662-672. (Pubitemid 40695843)
53. 13C longitudinal and transverse relaxation rates measured in the same protein sample. J Am Chem Soc 123:6164-6169.
54. Woessner DE (1962) Spin relaxation processes in a two-proton system undergoing anisotropic reorientation. J Chem Phys 36:1-4.
55. Palmer AG, III, Hochstrasser RA, Millar DP, Rance M, Wright PE (1993) Characterization of amino-acid sidechain dynamics in a zinc-finger peptide using C-13 NMR-spectroscopy and time-resolved fluorescence spectroscopy. J Am Chem Soc 115:6333-6345.
56. Koradi R, Billeter M, Wüthrich K (1996) MOLMOL: a program for display and analysis of macromolecular structures. J Mol Graph 14:51-32.