Isolation of a highly reactive β-sheet-rich intermediate of lysozyme in a solvent-free liquid phase

Journal of Physical Chemistry B

Volumn 117, Issue 28, 2013, Pages 8400-8407

  Brogan, Alex P S ^a   Sharma, Kamendra P ^a   Perriman, Adam W ^a   Mann, Stephen ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CIRCULAR DICHROISM SPECTROSCOPY; DENATURATION; ENZYMES; SOLVENTS; STABILIZATION;

ANHYDROUS CONDITIONS; IRREVERSIBLE AGGREGATION; MOLECULAR CROWDING; REACTIVE INTERMEDIATE; SECONDARY STRUCTURES; SYNCHROTRON RADIATION CIRCULAR DICHROISM SPECTROSCOPY; TEMPERATURE-DEPENDENT CHANGES; THERMAL DENATURATIONS;

LIQUIDS;

EID: 84880541690     PISSN: 15206106     EISSN: 15205207     Source Type: Journal    
DOI: 10.1021/jp4041524     Document Type: Article

References (40)

1. Dill, K. A. Dominant Forces in Protein Folding Biochemistry 1990, 29, 7133-7155
2. Szilágyi, A.; Závodszky, P. Structural Differences Between Mesophilic, Moderately Thermophilic and Extremely Thermophilic Protein Subunits: Results of a Comprehensive Survey Structure 2000, 8, 493-504
3. Das, R.; Gerstein, M. The Stability of Thermophilic Proteins: a Study Based on Comprehensive Genome Comparison Funct. Integr. Genomics 2000, 1, 76-88
4. Xiao, L.; Honig, B. Electrostatic Contributions to the Stability of Hyperthermophilic Proteins J. Mol. Biol. 1999, 289, 1435-44
5. Dominguez De Maria, P. Nonsolvent Applications of Ionic Liquids in Biotransformations and Organocatalysis Angew. Chem., Int. Ed. 2008, 47, 6960
6. van Rantwijk, F.; Sheldon, R. A. Biocatalysis in Ionic Liquids Chem. Rev. 2007, 107, 2757-85
7. Pace, C. N.; Treviño, S.; Prabhakaran, E.; Scholtz, J. M. Protein Structure, Stability and Solubility in Water and Other Solvents Philos. Trans. R. Soc., B 2004, 359, 1225-34
8. Clark, D. S. Characteristics of Nearly Dry Enzymes in Organic Solvents: Implications for Biocatalysis in the Absence of Water Philos. Trans. R. Soc., B 2004, 359, 1299-307
9. Klibanov, A. M. Improving Enzymes by Using Them in Organic Solvents Nature 2001, 409, 241-246
10. Mattos, C.; Ringe, D. Proteins in Organic Solvents Curr. Opin. Struct. Biol. 2001, 11, 761-4
11. Rialdi, G.; Battistel, E. Thermodynamics of Proteins in Unusual Environments Biophys. Chem. 2007, 126, 65-79
12. Brovchenko, I.; Oleinikova, A. Which Properties of a Spanning Network of Hydration Water Enable Biological Functions? ChemPhysChem 2008, 9, 2695-702
13. Perriman, A. W.; Mann, S. Liquid Proteins-A New Frontier for Biomolecule-Based Nanoscience ACS Nano 2011, 5, 6085-6091
14. Perriman, A. W.; Coelfen, H.; Hughes, R. W.; Barrie, C. L.; Mann, S. Solvent-free Protein Liquids and Liquid Crystals Angew. Chem., Int. Ed. 2009, 48, 6242-6
15. Perriman, A. W.; Brogan, A. P. S.; Cölfen, H.; Tsoureas, N.; Owen, G. R.; Mann, S. Reversible Dioxygen Binding in Solvent-free Liquid Myoglobin Nat. Chem. 2010, 2, 622-626
16. Patil, A. J.; McGrath, N.; Barclay, J. E.; Evans, D. J.; Cölfen, H.; Manners, I.; Perriman, A. W.; Mann, S. Liquid Viruses by Nanoscale Engineering of Capsid Surfaces Adv. Mater. 2012, 24, 4557-63
17. Brogan, A. P. S.; Siligardi, G.; Hussain, R.; Perriman, A. W.; Mann, S. Hyper-thermal Stability and Unprecedented Re-folding of Solvent-free Liquid Myoglobin Chem. Sci. 2012, 3, 1839-1846
18. Gallat, F.-X.; Brogan, A. P. S.; Fichou, Y.; McGrath, N.; Moulin, M.; Härtlein, M.; Combet, J.; Wuttke, J.; Mann, S.; Zaccai, G. A Polymer Surfactant Corona Dynamically Replaces Water in Solvent-Free Protein Liquids and Ensures Macromolecular Flexibility and Activity J. Am. Chem. Soc. 2012, 132, 13168-13171
19. Frare, E.; Mossuto, M. F.; Laureto, P. P. de; Tolin, S.; Menzer, L.; Dumoulin, M.; Dobson, C. M.; Fontana, A. Characterization of Oligomeric Species on the Aggregation Pathway of Human Lysozyme J. Mol. Biol. 2009, 387, 17-27
20. Gu, Z.; Zhu, X.; Ni, S.; Su, Z.; Zhou, H.-M. Conformational Changes of Lysozyme Refolding Intermediates and Implications for Aggregation and Renaturation Int. J. Biochem. Cell Biol. 2004, 36, 795-805
21. Chiti, F.; Dobson, C. M. Amyloid Formation by Globular Proteins Under Native Conditions Nat. Chem. Biol. 2009, 5, 15-22
22. Buell, A. K.; Dhulesia, A.; Mossuto, M. F.; Cremades, N.; Kumita, J. R.; Dumoulin, M.; Welland, M. E.; Knowles, T. P. J.; Salvatella, X.; Dobson, C. M. Population of Nonnative States of Lysozyme Variants Drives Amyloid Fibril Formation J. Am. Chem. Soc. 2011, 133, 7737-43
23. Williams, M. A.; Thornton, J. M.; Goodfellow, J. M. Modelling Protein Unfolding: Hen Egg-white Lysozyme Protein Eng. 1997, 10, 895-903
24. Ahmad, F.; Contaxis, C. C.; Bigelow, C. C. Free Energy Changes in Lysozyme Denaturation J. Biol. Chem. 1983, 258, 7960-3
25. Yonezawa, Y.; Tanaka, S.; Kubota, T.; Wakabayashi, K.; Yutani, K.; Fujiwara, S. An Insight into the Pathway of the Amyloid Fibril Formation of Hen Egg White Lysozyme Obtained from a Small-angle X-ray and Neutron Scattering Study J. Mol. Biol. 2002, 323, 237-251
26. D'Amico, M.; Raccosta, S.; Cannas, M.; Martorana, V.; Manno, M. Existence of Metastable Intermediate Lysozyme Conformation Highlights the Role of Alcohols in Altering Protein Stability J. Phys. Chem. B 2011, 115, 4078-87
27. Sasahara, K.; Demura, M.; Nitta, K. Partially Unfolded Equilibrium State of Hen Lysozyme Studied by Circular Dichroism Spectroscopy Biochemistry 2000, 39, 6475-82
28. Whitmore, L.; Wallace, B. A. DICHROWEB, an Online Server for Protein Secondary Structure Analyses from Circular Dichroism Spectroscopic Data Nucleic Acids Res. 2004, 32, W668-73
29. Sreerama, N.; Woody, R. W. Estimation of Protein Secondary Structure from Circular Dichroism Spectra: Comparison of CONTIN, SELCON, and CDSSTR Methods with an Expanded Reference Set Anal. Biochem. 2000, 287, 252-60
30. Lees, J. G.; Miles, A. J.; Wien, F.; Wallace, B. A. A Reference Database for Circular Dichroism Spectroscopy Covering Fold and Secondary Structure Space Bioinformatics 2006, 22, 1955-62
31. Whitmore, L.; Wallace, B. A. Protein Secondary Structure Analyses from Circular Dichroism Spectroscopy: Methods and Reference Databases Biopolymers 2008, 89, 392-400
32. Pace, C. N. The Stability of Globular Proteins Crit. Rev. Biochem. 1975, 3, 1-43
33. Ahmad, F. On the Estimation of Stability Parameters from Heat-Induced Conformational Transition Curves of Proteins J. Iran. Chem. Soc. 2004, 1, 99-105
34. Taneja, S.; Ahmad, F. Increased Thermal Stability of Proteins in the Presence of Amino Acids Biochem. J. 1994, 303, 147-53
35. Sinha, A.; Yadav, S.; Ahmad, R.; Ahmad, F. A Possible Origin of Differences Between Calorimetric and Equilibrium Estimates of Stability Parameters of Proteins Biochem. J. 2000, 345, 711-717
36. Kline, S. R. Reduction and Analysis of SANS and USANS Data Using IGOR Pro J. Appl. Crystallogr. 2006, 39, 895-900
37. Stanley, C.; Krueger, S.; Parsegian, V. A.; Rau, D. C. Protein Structure and Hydration Probed by SANS and Osmotic Stress Biophy. J. 2008, 94, 2777-89
38. Hamill, A. C.; Wang, S.-C.; Lee, C. T. Probing Lysozyme Conformation with Light Reveals a New Folding Intermediate Biochemistry 2005, 44, 15139-15149
39. Sanchez-Ruiz, J. M. Protein Kinetic Stability Biophys. Chem. 2010, 148, 1-15
40. Fu, L.; Villette, S.; Petoud, S.; Fernandez-Alonso, F.; Saboungi, M.-L. H/D Isotope Effects in Protein Thermal Denaturation: The Case of Bovine Serum Albumin J. Phys. Chem. B 2011, 115, 1881-8