Influence of osmolytes on protein and water structure: A step to understanding the mechanism of protein stabilization

Journal of Physical Chemistry B

Volumn 117, Issue 39, 2013, Pages 11502-11508

  Bruździak, Piotr ^a   Panuszko, Aneta ^a   Stangret, Janusz ^a  

^a GDANSK UNIVERSITY OF TECHNOLOGY   (Poland)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ENZYMES; MOLECULES; OXYGEN; STABILIZATION;

ENERGETIC CHARACTERISTICS; HEN EGG WHITE LYSOZYME; HYDRATION WATER; N ,N-DIMETHYLGLYCINE; N-METHYLGLYCINE; PROTEIN MOLECULES; PROTEIN STABILIZATION; WATER STRUCTURE;

PROTEINS;

AMINE; AMINO ACID; BETAINE; EGG PROTEIN; GLYCINE; LYSOZYME; METHYLAMINE; OXYGEN; SARCOSINE; TRIMETHYLOXAMINE; WATER;

ANIMAL; ARTICLE; CALORIMETRY; CHEMISTRY; CHICKEN; FEMALE; INFRARED SPECTROSCOPY; PROTEIN DENATURATION; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; SOLUTION AND SOLUBILITY; TRANSITION TEMPERATURE;

AMINES; AMINO ACIDS; ANIMALS; BETAINE; CALORIMETRY; CHICKENS; EGG PROTEINS; FEMALE; GLYCINE; METHYLAMINES; MURAMIDASE; OXYGEN; PROTEIN DENATURATION; PROTEIN STABILITY; PROTEIN STRUCTURE, SECONDARY; SARCOSINE; SOLUTIONS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; TRANSITION TEMPERATURE; WATER;

EID: 84885145262     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp404780c     Document Type: Article

References (64)

1. Yancey, P. H.; Clark, M. E.; Hand, S. C.; Bowlus, R. D.; Somero, G. N. Living with Water Stress: Evolution of Osmolyte Systems Science 1982, 217, 1214-1222
2. Yancey, P. H.; Somero, G. N. Counteraction of Urea Destabilization of Protein Structure by Methylamine Osmoregulatory Compounds of Elasmobranch Fishes Biochem. J. 1979, 183, 317-323
3. Arakawa, T.; Ejima, D.; Kita, Y.; Tsumoto, K. Small Molecule Pharmacological Chaperones: From Thermodynamic Stabilization to Pharmaceutical Drugs Biochim. Biophys. Acta, Proteins Proteomics 2006, 1764, 1677-1687
4. Arakawa, T.; Prestrelski, S. J.; Kenney, W. C.; Carpenter, J. F. Factors Affecting Short-term and Long-term Stabilities of Proteins Adv. Drug Delivery Rev. 2001, 46, 307-326
5. Srirangsan, P.; Kawai, K.; Hamada-Sato, N.; Watanabe, M.; Suzuki, T. Stabilizing Effects of Sucrose-Polymer Formulations on the Activities of Freeze-Dried Enzyme Mixtures of Alkaline Phosphatase, Nucleoside Phosphorylase and Xanthine Oxidase Food Chem. 2011, 125, 1188-1193
6. Rajan, R. S.; Tsumoto, K.; Tokunaga, M.; Tokunaga, H.; Kita, Y.; Arakawa, T. Chemical and Pharmacological Chaperones: Application for Recombinant Protein Production and Protein Folding Diseases Curr. Med. Chem. 2011, 18, 1-15
7. Ohtake, S. O. S.; Martin, R.; Saxena, A.; Pham, B.; Chiueh, G.; Osorio, M.; Kopecko, D.; Xu, D. Q.; Lechuga-Ballesteros, D.; Truong-Le, V. Room Temperature Stabilization of Oral, Live Attenuated Salmonella enterica Serovar Typhi-Vectored Vaccines Vaccine 2011, 29, 2761-2771
8. Mueller-Dieckmann, C.; Kauffmann, B.; Weiss, M. S. Trimethylamine N -oxide as a Versatile Cryoprotective Agent in Macromolecular Crystallography Appl. Crystallogr. 2011, 44, 433-436
9. Martins, J. M.; Neves, J. A.; Freitas, A.; Tirapicos, J. L. Betaine Supplementation Affects the Cholesterol but not the Lipid Profile of Pigs Eur. J. Lipid Sci. Technol. 2010, 112, 295-303
10. Khan, S. H.; Ahmad, N.; Ahmad, F.; Kumar, R. Naturally Occurring Organic Osmolytes: From Cell Physiology to Disease Prevention IUBMB Life 2010, 62, 891-895
11. Bartolini, M.; Andrisano, V. Strategies for the Inhibition of Protein Aggregation in Human Diseases ChemBioChem 2010, 11, 1018-1035
12. Athawale, M. V.; Sarupria, S.; Garde, S. Enthalpy-Entropy Contributions to Salt and Osmolyte Effects on Molecular-Scale Hydrophobic Hydration and Interactions J. Phys. Chem. B 2008, 112, 5661-5670
13. Athawale, M. V.; Dordick, J. S.; Garde, S. Osmolyte Trimethylamine- N -oxide does not Affect the Strength of Hydrophobic Interactions: Origin of Osmolyte Compatibility Biophys. J. 2005, 89, 858-866
14. Maclagan, R.; Malardier-Jugroot, C.; Whitehead, M. A.; Lever, M. Theoretical Studies of the Interaction of Water with Compensatory and Noncompensatory Solutes for Proteins J. Phys. Chem. A 2004, 108, 2514-2519
15. Sharp, K. A.; Madan, B.; Manas, E.; Vanderkooi, J. M. Water Structure Changes Induced by Hydrophobic and Polar Solutes Revealed by Simulations and Infrared Spectroscopy J. Chem. Phys. 2001, 114, 1791-1796
16. Panuszko, A.; Bruździak, P.; Zielkiewicz, J.; Wyrzykowski, D.; Stangret, J. Effects of Urea and Trimethylamine- N -oxide on the Properties of Water and the Secondary Structure of Hen Egg White Lysozyme J. Phys. Chem. B 2009, 113, 14797-14809
17. Panuszko, A.; Wojciechowski, M.; Bruździak, P.; Rakowska, P. W.; Stangret, J. Characteristics of Hydration Water Around Hen Egg Lysozyme as the Protein Model in Aqueous Solution. FTIR Spectroscopy and Molecular Dynamics Simulation Phys. Chem. Chem. Phys. 2012, 14, 15765-15773
18. Leung, K.; Rempe, S. B. Ab Initio Molecular Dynamics Study of Glycine Intramolecular Proton Transfer in Water J. Chem. Phys. 2005, 122, 18405-18418
19. Sun, J.; Bousquet, D.; Forbert, H.; Marx, D. Glycine in Aqueous Solution: Solvation Shells, Interfacial Water, and Vibrational Spectroscopy from Ab Initio Molecular Dynamics J. Chem. Phys. 2010, 133, 114508-114517
20. Alagona, G.; Ghio, C.; Kollman, P. A. Monte-Carlo Simulation Studies of the Solvation of Ions.2. Glycine Zwitterion THEOCHEM: J. Mol. Struct. 1988, 43, 385-392
21. Campo, M. G. Molecular Dynamics Simulation of Glycine Zwitterion in Aqueous Solution J. Chem. Phys. 2006, 125, 114511-114518
22. Parsons, M. T.; Koga, Y. Hydration Number of Glycine in Aqueous Solution: An Experimental Estimate J. Chem. Phys. 2005, 123, 234504-234509
23. Ide, M.; Maeda, Y.; Kitano, H. Effect of Hydrophobicity of Amino Acids on the Structure of Water J. Phys. Chem. B 1997, 101, 7022-7026
24. Hayashi, Y.; Katsumoto, Y.; Oshige, I.; Ornori, S.; Yasuda, A. Comparative Study of Urea and Betaine Solutions by Dielectric Spectroscopy: Liquid Structures of a Protein Denaturant and Stabilizer J. Phys. Chem. B 2007, 111, 11858-11863
25. Sironi, M.; Fornili, A.; Fornili, S. L. Water Interaction with Glycine Betaine: A Hybrid QM/MM Molecular Dynamics Simulation Phys. Chem. Chem. Phys. 2001, 3, 1081-1085
26. Civera, M.; Fornili, A.; Sironi, M.; Fornili, S. L. Molecular Dynamics Simulation of Aqueous Solutions of Glycine Betaine Chem. Phys. Lett. 2003, 367, 238-244
27. Rosgen, J.; Jackson-Atogi, R. Volume Exclusion and H-Bonding Dominate the Thermodynamics and Solvation of Trimethylamine- N -oxide in Aqueous Urea J. Am. Chem. Soc. 2012, 134, 3590-3597
28. Zou, Q.; Bennion, B. J.; Dagget, V.; Murphy, K. P. The Molecular Mechanism of Stabilization of Proteins by TMAO and its Ability to Counteract the Effects of Urea J. Am. Chem. Soc. 2002, 124, 1192-1202
29. Bennion, B. J.; Daggett, V. Counteraction of Urea-Induced Protein Denaturation by TMAO: A Chemical Chaperone at Atomic Resolution Proc. Natl. Acad. Sci. U.S.A. 2004, 101, 6433-6438
30. Daggett, V. Protein Folding-Simulation Chem. Rev. 2006, 106, 1898-1916
31. Paul, S.; Patey, G. N. Structure and Interaction in Aqueous Urea-Trimethylamine- N -oxide Solutions J. Am. Chem. Soc. 2007, 129, 4476-4482
32. Baskakov, I.; Bolen, D. W. Forcing Thermodynamically Unfolded Proteins to Fold J. Biol. Chem. 1998, 273, 4831-4834
33. Bolen, D. W.; Baskakov, I. The Osmophobic Effect: Natural Selection of a Thermodynamic Force in Protein Folding J. Mol. Biol. 2001, 310, 955-963
34. Liu, Y.; Bolen, D. W. The Peptide Backbone Plays a Dominant Role in Protein Stabilization by Naturally Occurring Osmolytes Biochemistry 1995, 34, 12884-12891
35. Hovagimyan, K. G.; Gerig, J. T. Interactions of Trimethylamine- N -oxide and Water with Cyclo-Alanylglycine J. Phys. Chem. B 2005, 109, 24142-24151
36. Schellman, J. A. Protein Stability in Mixed Solvents: A Balance of Contact Interaction and Excluded Volume Biophys. J. 2003, 85, 108-125
37. Wang, A.; Bolen, D. W. A Naturally Occurring Protective System in Urea-Rich Cells: Mechanism of Osmolyte Protection of Proteins against Urea Denaturation Biochemistry 1997, 36, 9101-9108
38. Timasheff, S. N. Water as Ligand: Preferential Binding and Exclusion of Denaturants in Protein Unfolding Biochemistry 1992, 31, 9857-9864
39. Paul, S.; Patey, G. N. Why tert -Butyl Alcohol Associates in Aqueous Solution but Trimethylamine- N -oxide does not J. Phys. Chem. B 2006, 110, 10514-10518
40. 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. 1993, 22, 67-97
41. Foglia, F.; Carullo, P.; Del Vecchio, P. The Effect of Trimethylamine- N -oxide on RNase a Stability J. Therm. Anal. Cal. 2008, 91, 67-72
42. Street, T. O.; Bolen, D. W.; Rose, G. D. A Molecular Mechanism for Osmolyte-Induced Protein Stability Proc. Natl. Acad. Sci. U.S.A. 2006, 103, 13997-14002
43. Samuelsson, L. M.; Bedford, J. J.; Smith, R. A. J.; Leader, J. P. A Comparison of the Counteracting Effects of Glycine Betaine and TMAO on the Activity of RNase A in Aqueous Urea Solution Comp. Biochem. Physiol. A 2005, 141, 22-28
44. Makhatadze, G. I.; Clore, G. M.; Gronenborn, A. M.; Privalov, P. L. Thermodynamics of Unfolding of the all Beta-Sheet Protein Interleukin-1-beta Biochemistry 1994, 33, 9327-9332
45. Santoro, M. M.; Liu, Y. F.; Khan, S. M. A.; Hou, L. X.; Bolen, D. W. Increased Thermal Stability of Proteins in the Presence of Naturally Occurring Osmolytes Biochemistry 1992, 31, 5278-5283
46. Panuszko, A.; Śmiechowski, M.; Stangret, J. Fourier Transform Infrared Spectroscopic and Theoretical Study of Water Interactions with Glycine and its N -Methylated Derivatives J. Chem. Phys. 2011, 134, 115104-115104
47. Zhang, J.; Yan, Y. B. Probing Conformational Changes of Proteins by Quantitative Second-Derivative Infrared Spectroscopy Anal. Biochem. 2005, 340, 89-98
48. Natalello, A.; Ami, D.; Brocca, S.; Lotti, M.; Doglia, S. M. Secondary Structure, Conformational Stability and Glycosylation of a Recombinant Candida rugosa Lipase Studied by Fourier-Transform Infrared Spectroscopy Biochem. J. 2005, 385, 511-517
49. Vogel, R.; Siebert, F. Vibrational Spectroscopy as a Tool for Probing Protein Function Curr. Opin. Chem. Biol. 2000, 4, 518-523
50. Arrondo, J. L. R.; Goni, F. M. Structure and Dynamics of Membrane Proteins as Studied by Infrared Spectroscopy Progr. Biochem. Mol. Biol. 1999, 72, 367-405
51. Oberg, K. A.; Fink, A. L. A New Attenuated Total Reflectance Fourier Transform Infrared Spectroscopy Method for the Study of Proteins in Solution Anal. Biochem. 1998, 256, 92-106
52. Arrondo, J. L. R.; Muga, A.; Castresana, J.; Goni, F. M. Quantitative Studies of the Structure of Proteins in Solution by Fourier-Transform Infrared Spectroscopy Progr. Biochem. Mol. Biol. 1993, 59, 23-56
53. Susi, H.; Byler, D. M. Protein Structure by Fourier Transform Infrared Spectroscopy: Second Derivative Spectra Biochem. Biophys. Res. Commun. 1983, 115, 391-397
54. Susi, H. Infrared Spectroscopy-Conformation Methods Enzymol. 1972, 26, 455-472
55. Tsuboi, M. Application of Infrared Spectroscopy to Structure Studies of Nucleic Acids Appl. Spectrosc. Rev. 1970, 3, 45-90
56. Śmiechowski, M.; Stangret, J. Vibrational Spectroscopy of Semiheavy Water (HDO) as a Probe of Solute Hydration Pure Appl. Chem. 2010, 82, 1869-1887
57. Gojło, E.; Śmiechowski, M.; Panuszko, A.; Stangret, J. Hydration of Carboxylate Anions: Infrared Spectroscopy of Aqueous Solutions J. Phys. Chem. B 2009, 113, 8128-8136
58. Luthra, S.; Kalonia, D. S.; Pikal, M. J. Effect of Hydration on the Secondary Structure of Lyophilized Proteins as Measured by Fourier Transform Infrared (FTIR) Spectroscopy J. Pharm. Sci. 2007, 96, 2910-2921
59. Śmiechowski, M.; Gojło, E.; Stangret, J. Hydration of Simple Carboxylic Acids from Infrared Spectra of HDO and Theoretical Calculations J. Phys. Chem. B 2011, 115, 4834-4842
60. 2 Aqueous Solutions Spectrosc. Lett. 1988, 21, 369-381
61. Stangret, J.; Gampe, T. Hydration Sphere of Tetrabutylammonium Cation. FTIR Studies of HDO Spectra J. Phys. Chem. B 1999, 103, 3778-3783
62. Stangret, J.; Gampe, T. Ionic Hydration Behavior Serived From Infrared Spectra in HDO J. Phys. Chem. A 2002, 106, 5393-5402
63. Kristiansson, O.; Eriksson, A.; Lindgren, J. Hydration of Ions in Aqueous Solutions Studied by Infrared Spectroscopy. II. Application J. Acta Chem. Scand. A 1984, 38A, 613-618
64. Badger, R. M.; Bauer, S. H. Spectroscopic Studies of the Hydrogen Bond. II. The Shift of the O[Single Bond]H Vibrational Frequency in the Formation of the Hydrogen Bond J. Chem. Phys. 1937, 5, 839-851