Asymmetric kinetics of protein structural changes

Accounts of Chemical Research

Volumn 42, Issue 6, 2009, Pages 778-787

  Marchal, Stéphane ^a,b,c   Font, Josep ^d   Ribó, Marc ^e   Vilanova, Maria ^e   Phillips, Robert S ^f   Lange, Reinhard ^a,b,c   Torrent, Joan ^a,b,c  

^a INSERM   (France)

^b UNIV MONTPELLIER   (France)

^c PSL RESEARCH UNIVERSITY   (France)

^d UNIVERSITY OF SYDNEY   (Australia)

^e UNIVERSITY OF GIRONA   (Spain)

^f UNIVERSITY OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 67649200151     PISSN: 00014842     EISSN: None     Source Type: Journal    
DOI: 10.1021/ar800266r     Document Type: Article

References (42)

1. Greene, D. N.; Garcia, T.; Sutton, R. B.; Gernert, K. M.; Benian, G. M.; Oberhauser, A. F. Single-molecule force spectroscopy reveals a stepwise unfolding of Caenorhabditis elegans giant protein kinase domains. Biophys. J. 2008, 95, 1360-1370.
2. Dill, K. A.; Chan, H. S. From Levinthal to pathways to funnels. Nat. Struct. Biol. 1997, 4, 10-19.
3. Ballew, R. M.; Sabelko, J.; Gruebele, M. Direct observation of fast protein folding: the initial collapse of apomyoglobin. Proc. Natl Acad. Sci. U.S.A. 1996, 93, 5759-5764.
4. Callender, R. H.; Dyer, R. B.; Gilmanshin, R.; Woodruff, W. H. Fast events in protein folding: the time evolution of primary processes. Annu. Rev. Phys. Chem. 1998, 49, 173-202.
5. Huang, C. Y.; Getahun, Z.; Zhu, Y.; Klemke, J. W.; DeGrado, W. F.; Gai, F. Helix formation via conformation diffusion search. Proc. Natl Acad. Sci. U.S.A. 2002, 99, 2788-2793.
6. Kubelka, J.; Eaton, W. A.; Hofrichter, J. Experimental tests of villin subdomain folding simulations. J. Mol. Biol. 2003, 329, 625-630.
7. Tetreau, C.; Lavalette, D. Dominant features of protein reaction dynamics: conformational relaxation and ligand migration. Biochim. Biophys. Acta 2005, 1724, 411-424.
8. El Moustaine, D.; Perrier, V.; Smeller, L.; Lange, R.; Torrent, J. Full-length prion protein aggregates to amyloid fibrils and spherical particles by distinct pathways. FEBS J. 2008, 275, 2021-2031.
9. Wedemeyer, W. J.; Welker, E.; Scheraga, H. A. Proline cis-trans isomerization and protein folding. Biochemistry 2002, 41, 14637-14644.
10. Marchal, S.; Shehi, E.; Harricane, M. C.; Fusi, P.; Heitz, F.; Tortora, P.; Lange, R. Structural instability and fibrillar aggregation of non-expanded human ataxin-3 revealed under high pressure and temperature. J. Biol. Chem. 2003, 278, 31554- 31563.
11. Torrent, J.; Connelly, J. P.; Coll, M. G.; Ribo, M.; Lange, R.; Vilanova, M. Pressure versus heat-induced unfolding of ribonuclease A: the case of hydrophobic interactions within a chain-folding initiation site. Biochemistry 1999, 38, 15952- 15961.
12. Mombelli, E.; Afshar, M.; Fusi, P.; Mariani, M.; Tortora, P.; Connelly, J. P.; Lange, R. The role of phenylalanine 31 in maintaining the conformational stability of ribonuclease P2 from Sulfolobus solfataricus under extreme conditions of temperature and pressure. Biochemistry 1997, 36, 8733-8742.
13. Jacob, M.; Geeves, M.; Holtermann, G.; Schmid, F. X. Diffusional barrier crossing in a two-state protein folding reaction. Nat. Struct. Biol. 1999, 6, 923-926.
14. Torrent, J.; Font, J.; Herberhold, H.; Marchal, S.; Ribo, M.; Ruan, K.; Winter, R.; Vilanova, M.; Lange, R. The use of pressure-jump relaxation kinetics to study protein folding landscapes. Biochim. Biophys. Acta 2006, 1764, 489-496.
15. Pearson, D. S.; Holtermann, G.; Ellison, P.; Cremo, C.; Geeves, M. A. A novel pressure-jump apparatus for the microvolume analysis of protein-ligand and protein-protein interactions: its application to nucleotide binding to skeletalmuscle and smooth-muscle myosin subfragment-1. Biochem. J. 2002, 366, 643-651.
16. Phillips, R. S.; Miles, E. W.; Holtermann, G.; Goody, R. S. Hydrostatic pressure affects the conformational equilibrium of Salmonella typhimurium tryptophan synthase. Biochemistry 2005, 44, 7921-7928.
17. Kamatari, Y. O.; Yokoyama, S.; Tachibana, H.; Akasaka, K. Pressure-jump NMR study of dissociation and association of amyloid protofibrils. J. Mol. Biol. 2005, 349, 916-921.
18. Panick, G.; Winter, R. Pressure-induced unfolding/refolding of ribonuclease A: static and kinetic Fourier transform infrared spectroscopy study. Biochemistry 2000, 39, 1862-1869.
19. Torrent, J.; Marchal, S.; Ribo, M.; Vilanova, M.; Georges, C.; Dupont, Y.; Lange, R. Distinct unfolding and refolding pathways of ribonuclease a revealed by heating and cooling temperature jumps. Biophys. J. 2008, 94, 4056-4065.
20. Neira, J. L.; Rico, M. Folding studies on ribonuclease A, a model protein. Fold. Des. 1997, 2, R1-11.
21. Raines, R. T. Ribonuclease A. Chem. Rev. 1998, 98, 1045-1066.
22. Font, J.; Torrent, J.; Ribo, M.; Laurents, D. V.; Balny, C.; Vilanova, M.; Lange, R. Pressure-jump-induced kinetics reveals a hydration dependent folding/unfolding mechanism of ribonuclease A. Biophys. J. 2006, 91, 2264-2274.
23. Dodge, R. W.; Scheraga, H. A. Folding and unfolding kinetics of the proline-toalanine mutants of bovine pancreatic ribonuclease A. Biochemistry 1996, 35, 1548-1559.
24. Weber-Ban, E.; Hur, O.; Bagwell, C.; Banik, U.; Yang, L. H.; Miles, E. W.; Dunn, M. F. Investigation of allosteric linkages in the regulation of tryptophan synthase: the roles of salt bridges and monovalent cations probed by site-directed mutation, optical spectroscopy, and kinetics. Biochemistry 2001, 40, 3497- 3511.
25. Font, J.; Benito, A.; Lange, R.; Ribo, M.; Vilanova, M. The contribution of the residues from the main hydrophobic core of ribonuclease A to its pressure-folding transition state. Protein Sci. 2006, 15, 1000-1009.
26. Ribo, M.; Font, J.; Benito, A.; Torrent, J.; Lange, R.; Vilanova, M. Pressure as a tool to study protein-unfolding/refolding processes: the case of ribonuclease A. Biochim. Biophys. Acta 2006, 1764, 461-469.
27. Welker, E.; Maki, K.; Shastry, M. C.; Juminaga, D.; Bhat, R.; Scheraga, H. A.; Roder, H. Ultrarapid mixing experiments shed new light on the characteristics of the initial conformational ensemble during the folding of ribonuclease A. Proc. Natl Acad. Sci. U.S.A. 2004, 101, 17681-17686.
28. Miles, E. W. Tryptophan synthase: a multienzyme complex with an intramolecular tunnel. Chem. Rec. 2001, 1, 140-151.
29. Fan, Y. X.; McPhie, P.; Miles, E. W. Regulation of tryptophan synthase by temperature, monovalent cations, and an allosteric ligand. Evidence from Arrhenius plots, absorption spectra, and primary kinetic isotope effects. Biochemistry 2000, 39, 4692-4703.
30. Ngo, H.; Harris, R.; Kimmich, N.; Casino, P.; Niks, D.; Blumenstein, L.; Barends, T. R.; Kulik, V.; Weyand, M.; Schlichting, I.; Dunn, M. F. Synthesis and characterization of allosteric probes of substrate channeling in the tryptophan synthase bienzyme complex. Biochemistry 2007, 46, 7713-7727.
31. Ngo, H.; Kimmich, N.; Harris, R.; Niks, D.; Blumenstein, L.; Kulik, V.; Barends, T. R.; Schlichting, I.; Dunn, M. F. Allosteric regulation of substrate channeling in tryptophan synthase: modulation of the L-serine reaction in stage I of the betareaction by alpha-site ligands. Biochemistry 2007, 46, 7740-7753.
32. Peracchi, A.; Bettati, S.; Mozzarelli, A.; Rossi, G. L.; Miles, E. W.; Dunn, M. F. Allosteric regulation of tryptophan synthase: effects of pH, temperature, and alphasubunit ligands on the equilibrium distribution of pyridoxal 5'-phosphate-L-serine intermediates. Biochemistry 1996, 35, 1872-1880.
33. Ruvinov, S. B.; Ahmed, S. A.; McPhie, P.; Miles, E. W. Monovalent cations partially repair a conformational defect in a mutant tryptophan synthase alpha 2 beta 2 complex (beta-E109A). J. Biol. Chem. 1995, 270, 17333-17338.
34. Woehl, E.; Dunn, M. F. Mechanisms of monovalent cation action in enzyme catalysis: the tryptophan synthase alpha-, beta-, and alpha beta-reactions. Biochemistry 1999, 38, 7131-7141.
35. Woehl, E. U.; Dunn, M. F. Monovalent metal ions play an essential role in catalysis and intersubunit communication in the tryptophan synthase bienzyme complex. Biochemistry 1995, 34, 9466-9476.
36. Ahmed, S. A.; McPhie, P.; Miles, E. W. Mechanism of activation of the tryptophan synthase alpha2beta2 complex. Solvent effects of the co-substrate betamercaptoethanol. J. Biol. Chem. 1996, 271, 29100-29106.
37. Ahmed, S. A.; Miles, E. W. Aliphatic alcohols stabilize an alternative conformation of the tryptophan synthase alpha 2 beta 2 complex from Salmonella typhimurium. J. Biol. Chem. 1994, 269, 16486-16492.
38. Phillips, R. S.; McPhie, P.; Miles, E. W.; Marchal, S.; Lange, R. Quantitative effects of allosteric ligands and mutations on conformational equilibria in Salmonella typhimurium tryptophan synthase. Arch. Biochem. Biophys. 2008, 470, 8-19.
39. Phillips, R. S.; Miles, E. W.; McPhie, P.; Marchal, S.; Georges, C.; Dupont, Y.; Lange, R. Pressure and temperature jump relaxation kinetics of the conformational change in Salmonella typhimurium tryptophan synthase L-serine complex: large activation compressibility and heat capacity changes demonstrate the contribution of solvation. J. Am. Chem. Soc. 2008, 130, 13580-13588.
40. York, S. S. Kinetic spectroscopic studies of substrate and subunit interactions of tryptophan synthetase. Biochemistry 1972, 11, 2733-2740.
41. Raboni, S.; Mozzarelli, A.; Cook, P. F. Control of ionizable residues in the catalytic mechanism of tryptophan synthase from Salmonella typhimurium. Biochemistry 2007, 46, 13223-13234.
42. Lange, R.; Bec, N.; Mozhaev, V. V.; Frank, J. Fourth derivative UV-spectroscopy of proteins under high pressure. II. Application to reversible structural changes. Eur. Biophys. J. 1996, 24, 284-292.