Relationship between Protein Stabilization and Protein Rigidification Induced by Mannosylglycerate

Journal of Molecular Biology

Volumn 394, Issue 2, 2009, Pages 237-250

  Pais, Tiago M ^a   Lamosa, Pedro ^a   Garcia Moreno, Bertrand ^b   Turner, David L ^a,c   Santos, Helena ^a  

^a INSTITUTO DE TECNOLOGIA QUÍMICA E BIOLÓGICA   (Portugal)

^b JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF SOUTHAMPTON   (United Kingdom)

Author keywords

chemical shift; dynamics; NMR; protein stabilization; staphylococcal nuclease

Indexed keywords

BACTERIAL ENZYME; GLYCERIC ACID; MANNOSYLGLYCERIC ACID; NITROGEN 15; NUCLEASE; UNCLASSIFIED DRUG; UREA;

ARTICLE; CONCENTRATION RESPONSE; CONTROLLED STUDY; DEUTERIUM HYDROGEN EXCHANGE; DIFFERENTIAL SCANNING CALORIMETRY; IONIC STRENGTH; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTON NUCLEAR MAGNETIC RESONANCE; TEMPERATURE SENSITIVITY; TRANSITION TEMPERATURE; VISCOSITY;

EID: 70350523594     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2009.09.012     Document Type: Article

References (60)

1. Nozaki Y., and Tanford C. The solubility of amino acids and related compounds in aqueous urea solutions. J. Biol. Chem. 238 (1963) 4074-4081
2. Nozaki Y., and Tanford C. The solubility of amino acids and related compounds in aqueous ethylene glycol solutions. J. Biol. Chem. 240 (1965) 3568-3575
3. Nozaki Y., and Tanford C. The solubility of amino acids, diglycine, and triglycine in aqueous guanidine hydrochloride solutions. J. Biol. Chem. 245 (1970) 1648-1652
4. Arakawa T., and Timasheff S.N. The stabilization of proteins by osmolytes. Biophys. J. 47 (1985) 411-414
5. Timasheff S.N. Water as ligand: preferential binding and exclusion of denaturants in protein unfolding. Biochemistry 31 (1992) 9857-9864
6. Timasheff S.N. The control of protein stability and association by weak interactions with water: how do solvents affect these processes?. Annu. Rev. Biophys. Biomol. Struct. 22 (1993) 67-97
7. Liu Y., and Bolen D.W. The peptide backbone plays a dominant role in protein stabilization by naturally occurring osmolytes. Biochemistry 34 (1995) 12884-12891
8. Auton M., and Bolen D.W. Additive transfer free energies of the peptide backbone unit that are independent of the model compound and the choice of concentration scale. Biochemistry 43 (2004) 1329-1342
9. Auton M., Holthauzen L.M., and Bolen D.W. Anatomy of energetic changes accompanying urea-induced protein denaturation. Proc. Natl Acad. Sci. USA 104 (2007) 15317-15322
10. Santos H., Lamosa P., Faria T.Q., Borges N., and Neves C. The physiological role, biosynthesis and mode of action of compatible solutes from (hyper)thermophiles. In: Gerday C., and Glandorf N. (Eds). Physiology and biochemistry of extremophiles (2007) 86-103
11. Faria T.Q., Mingote A., Siopa F., Ventura R., Maycock C., and Santos H. Design of new enzyme stabilizers inspired by glycosides of hyperthermophilic microorganisms. Carbohydr. Res. 343 (2008) 3025-3033
12. Pais T.M., Lamosa P., dos Santos W., LeGall J., Turner D.L., and Santos H. Structural determinants of protein stabilization by solutes. The importance of the hairpin loop in rubredoxins. FEBS J. 272 (2005) 999-1011
13. Razvi A., and Scholtz J.M. Lessons in stability from thermophilic proteins. Protein Sci. 15 (2006) 1569-1578
14. Petsko G.A. Structural basis of thermostability in hyperthermophilic proteins, or "there's more than one way to skin a cat". Methods Enzymol. 334 (2001) 469-478
15. Doan-Nguyen V., and Loria J.P. The effects of cosolutes on protein dynamics: the reversal of denaturant-induced protein fluctuations by trimethylamine N-oxide. Protein Sci. 16 (2007) 20-29
16. Lamosa P., Turner D.L., Ventura R., Maycock C., and Santos H. Protein stabilization by compatible solutes. Effect of diglycerol phosphate on the dynamics of Desulfovibrio gigas rubredoxin studied by NMR. Eur. J. Biochem. 270 (2003) 4606-4614
17. Wang A., Robertson A.D., and Bolen D.W. Effects of a naturally occurring compatible osmolyte on the internal dynamics of ribonuclease A. Biochemistry 34 (1995) 15096-15104
18. 15N resonances and secondary structure of the unligated enzyme as identified by three-dimensional NMR spectroscopy. Biochemistry 31 (1992) 911-920
19. 15N chemical shift assignments for the unligated enzyme and analysis of chemical shift changes that accompany formation of the nuclease-thymidine 3′,5′-bisphosphate-calcium ternary complex. Biochemistry 31 (1992) 921-936
20. 15N NMR relaxation study. J. Mol. Biol. 260 (1996) 570-587
21. 15N-NMR relaxation measurements. Eur. J. Biochem. 230 (1995) 1014-1024
22. Dosset P., Hus J.C., Blackledge M., and Marion D. Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data. J. Biomol. NMR 16 (2000) 23-28
23. Koradi R., Billeter M., and Wuthrich K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 14 (1996) 32-51
24. 2. J. Mol. Biol. 281 (1998) 341-361
25. Mandel A.M., Akke M., and Palmer III A.G. Backbone dynamics of Escherichia coli ribonuclease HI: correlations with structure and function in an active enzyme. J. Mol. Biol. 246 (1995) 144-163
26. Hwang T.L., Mori S., Shaka A.J., and van Zijl P.C. Application of phase-modulated CLEAN chemical EXchange spectroscopy (CLEANEX-PM) to detect water-protein proton exchange and intermolecular NOEs. J. Am. Chem. Soc. 119 (1997) 6203-6204
27. Jeener J., Meier B.H., Bachmann P., and Ernst R.R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 71 (1979) 4546-4553
28. Schwartz A.L., and Cutnell J.D. One- and two-dimensional NMR studies of exchanging amide protons in glutathione. J. Magn. Reson. 53 (1983) 398-411
29. Dobson C.M., Lian L.-Y., Redfield C., and Topping K.D. Measurement of hydrogen exchange rates using 2D NMR spectroscopy. J. Magn. Reson. 69 (1986) 201-209
30. Mori S., Abeygunawardana C., van Zijl P.C., and Berg J.M. Water exchange filter with improved sensitivity (WEX II) to study solvent-exchangeable protons. Application to the consensus zinc finger peptide CP-1. J. Magn. Reson., Ser. B 110 (1996) 96-101
31. Hwang T.L., van Zijl P.C., and Mori S. Accurate quantitation of water-amide proton exchange rates using the phase-modulated CLEAN chemical EXchange (CLEANEX-PM) approach with a fast-HSQC (FHSQC) detection scheme. J. Biomol. NMR 11 (1998) 221-226
32. Englander S.W., and Mayne L. Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Annu. Rev. Biophys. Biomol. Struct. 21 (1992) 243-265
33. Hvidt A., and Nielsen S.O. Hydrogen exchange in proteins. Adv. Protein Chem. 21 (1966) 287-386
34. Englander S.W., Sosnick T.R., Englander J.J., and Mayne L. Mechanisms and uses of hydrogen exchange. Curr. Opin. Struct. Biol. 6 (1996) 18-23
35. Bai Y., Milne J.S., Mayne L., and Englander S.W. Primary structure effects on peptide group hydrogen exchange. Proteins 17 (1993) 75-86
36. Rodriguez R., Chinea G., Lopez N., Pons T., and Vriend G. Homology modeling, model and software evaluation: three related resources. Bioinformatics 14 (1998) 523-528
37. Cohen F.E., and Kelly J.W. Therapeutic approaches to protein-misfolding diseases. Nature 426 (2003) 905-909
38. Davis-Searles P.R., Saunders A.J., Erie D.A., Winzor D.J., and Pielak G.J. Interpreting the effects of small uncharged solutes on protein-folding equilibria. Annu. Rev. Biophys. Biomol. Struct. 30 (2001) 271-306
39. Foord R.L., and Leatherbarrow R.J. Effect of osmolytes on the exchange rates of backbone amide protons in proteins. Biochemistry 37 (1998) 2969-2978
40. LeMaster D.M., Tang J., Paredes D.I., and Hernandez G. Enhanced thermal stability achieved without increased conformational rigidity at physiological temperatures: spatial propagation of differential flexibility in rubredoxin hybrids. Proteins 61 (2005) 608-616
41. Kamerzell T.J., and Middaugh C.R. The complex inter-relationships between protein flexibility and stability. J. Pharm. Sci. 97 (2008) 3494-3517
42. 15N relaxation and hydrogen-deuterium exchange studies of a hyperthermophilic enzyme highly active at 30 °C. Biochemistry 48 (2009) 2723-2739
43. Butterwick J.A., Patrick L.J., Astrof N.S., Kroenke C.D., Cole R., Rance M., and Palmer III A.G. Multiple time scale backbone dynamics of homologous thermophilic and mesophilic ribonuclease HI enzymes. J. Mol. Biol. 339 (2004) 855-871
44. 1H heteronuclear NMR relaxation analysis of oxidized and reduced forms of DsbA. J. Mol. Biol. 371 (2007) 703-716
45. Hernandez G., Jenney Jr. F.E., Adams M.W., and LeMaster D.M. Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature. Proc. Natl Acad. Sci. USA 97 (2000) 3166-3170
46. Liu Y., and Sturtevant J.M. The observed change in heat capacity accompanying the thermal unfolding of proteins depends on the composition of the solution and on the method employed to change the temperature of unfolding. Biochemistry 35 (1996) 3059-3062
47. Jacobs M.D., and Fox R.O. Staphylococcal nuclease folding intermediate characterized by hydrogen exchange and NMR spectroscopy. Proc. Natl Acad. Sci. USA 91 (1994) 449-453
48. Bédard S., Krishna M.M.G., Mayne L., and Englander S.W. Protein folding: independent unrelated pathways or predetermined pathway with optional errors. Proc. Natl Acad. Sci. USA 105 (2008) 7182-7187
49. Englander S.W., Mayne L., Bai Y., and Sosnick T.R. Hydrogen exchange: the modern legacy of Linderstrom-Lang. Protein Sci. 6 (1997) 1101-1109
50. Bédard S., Mayne L.C., Peterson R.W., Wand A.J., and Englander S.W. The foldon substructure of staphylococcal nuclease. J. Mol. Biol. 376 (2008) 1142-1154
51. Calhoun D.B., and Englander S.W. Internal protein motions, concentrated glycerol, and hydrogen exchange studied in myoglobin. Biochemistry 24 (1985) 2095-2100
52. Chen J., Lu Z., Sakon J., and Stites W.E. Increasing the thermostability of staphylococcal nuclease: implications for the origin of protein thermostability. J. Mol. Biol. 303 (2000) 125-130
53. Shortle D., and Meeker A.K. Residual structure in large fragments of staphylococcal nuclease: effects of amino acid substitutions. Biochemistry 28 (1989) 936-944
54. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28 (1989) 8972-8979
55. Piotto M., Saudek V., and Sklenar V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J. Biomol. NMR 2 (1992) 661-665
56. Markley J.L., Horsley W.J., and Klein M.P. Spin-lattice relaxation measurements in slowly relaxing complex spectra. J. Chem. Phys. 55 (1971) 3604-3605
57. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules 1. Theory and range validity. J. Am. Chem. Soc. 104 (1982) 4546-4559
58. Lipari G., and Szabo A. Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules 2. Analysis of experimental results. J. Am. Chem. Soc. 104 (1982) 4559-4570
59. 15N NMR relaxation measurements at two magnetic fields. J. Biomol. NMR 8 (1996) 273-284
60. Mori S., Wardana C.A., Johnson M.O., and van Zijl P.C. Improved sensitivity of HSQC spectra of exchanging protons at short interscan delays using a new Fast-HSQC (FHSQC) detection scheme that avoids water saturation. J. Magn. Reson., Ser B 108 (1995) 94-95