Unique features of the folding landscape of a repeat protein revealed by pressure perturbation

Biophysical Journal

Volumn 98, Issue 11, 2010, Pages 2712-2721

  Rouget, Jean Baptiste ^a   Schroer, Martin A ^b   Jeworrek, Christoph ^b   Pühse, Matthias ^b   Saldana, Jean Louis ^a   Bessin, Yannick ^a   Tolan, Metin ^b   Barrick, Doug ^c   Winter, Roland ^b   Royer, Catherine A ^a  

^a CENTRE DE BIOCHIMIE STRUCTURALE   (France)

^b TU DORTMUND UNIVERSITY   (Germany)

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

Author keywords

[No Author keywords available]

Indexed keywords

EID: 77952990872     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2010.02.044     Document Type: Article

References (54)

1. Levy, Y., and J. N. Onuchic. 2006. Water mediation in protein folding and molecular recognition. Annu. Rev: Biophys. Biomol. Struct. 35:389-415.
2. Mitra, L., J. B. Rouget, ...,R. Winter. 2008. Towards a quantitative understanding of protein hydration and volumetric properties. ChemPhysChem. 9:2715-2721.
3. Royer, C. A. 2002. Revisiting volume changes in pressure-induced protein unfolding. Biochim. Biophys. Acta. 1595:201-209.
4. Royer, C. A., and R. Winter. 2008. Volumetric properties of proteins and the role of solvent in conformational dynamics. In Water and Biomolecules: Physical Chemistry of Life Phenomena. K. Kuwajima, editor. Springer, New York. 173-186.
5. Royer, C. A. 2008. The nature of the transition state ensemble and the mechanisms of protein folding: a review. Arch. Biochem. Biophys. 469:34-45.
6. Kauzmann, W. 1987. Thermodynamics of unfolding. Nature. 325:763-764.
7. Brun, L., D. G. Isom, ..., C. A. Royer. 2006. Hydration of the folding transition, state ensemble of a protein. Biochemistry. 45:3473-3480.
8. Mitra, L., N. Smolin, ...,R. Winter. 2006. Pressure perturbation calorimetric studies of the solvation properties and the thermal unfolding of proteins in solution- experiments and theoretical interpretation. Phys. Chem. Chem. Phys. 8:1249-1265.
9. Mitra, L., K. Hata, ...,C. A. Royer. 2007. V(i)-value analysis: a pressure-based method for mapping the folding transition state ensemble of proteins. J. Am. Chem. Soc. 129:14108-14109.
10. Panick, G., G. J. Vidugiris, ..., C. A. Royer. 1999. Exploring the temperature-pressure phase diagram of staphylococcal nuclease. Biochemistry. 38:41.57-4164.
11. Seemann, H., R. Winter, and C. A. Royer. 2001, Volume, expansivity and isothermal compressibility changes associated with, temperature and pressure unfolding of Staphylococcal nuclease. J. Mol. Biol. 307:1091-1102.
12. Vidugiris, G. J., J. L. Markley, and C. A. Royer. 1995. Evidence for a molten globule-like transition state in protein folding from determination of activation volumes. Biochemistry. 34:4909-4912.
13. Schweiker, K. L., V. W. Fitz, and G. I. Makhatadze. 2009. Universal convergence of the specific volume changes of globular proteins upon unfolding. Biochemistry. 48:10846-10851.
14. Zweifel, M. E., D. J. Leahy, ...,D. Barrick. 2003. Structure and stability of the ankyrin domain of the Drosophila Notch receptor. Protein Sci. 12:2622-2632.
15. Barrick, D., D. U. Ferreiro, and E. A. Komives. 2008. Folding landscapes of ankyrin repeat proteins: experiments meet theory. Curr. Opin. Struct. Biol. 18:27-34.
16. Bradley, C. M., and D. Barrick. 2006. The notch ankyrin domain folds via a discrete, centralized pathway. Structure. 14:1303-1312.
17. Mello, C. C., and D. Barrick. 2004. An experimentally determined protein folding energy landscape. Proc. Natl. Acad. Sci. USA. 101: 14102-14107.
18. Mello, C. C., C. M. Bradley, ...,D. Barrick. 2005. Experimental characterization of the folding kinetics of the notch ankyrin domain. J. Mol. Biol. 352:266-281.
19. Zweifel, M. E., and D. Barrick. 2001, Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 2. Solution, stability and cooperativity of unfolding. Biochemistry. 40:14357-14367.
20. Zweifel, M. E., and D. Barrick. 2001. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 1. Solution conformational and hydrodynamic properties. Biochemistry. 40:14344-14356.
21. Royer, C. A., W. R. Smith, and J. M. Beechem. 1990. Analysis of binding in macromolecular complexes: a generalized numerical approach. Anal. Biochem. 191:287-294.
22. Kataoka, M., I. Nishii, ..., Y. Goto. 1995. Structural characterization of the molten, globule and native states of apomyoglobin by solution x-ray scattering. J. Mol. Biol. 249:215-228.
23. Lindner, P., and T. Zemb. 2002. Neutrons, X-rays and Light: Scattering Methods Applied to Soft Condensed Matter. Elsevier Science, Amsterdam.
24. Svergun, D. I., and M. H. J. Koch. 2003. Small-angle scattering studies of biological macromolecules in solution. Rep. Prog. Phys. 66: 1735-1782.
25. Neumann, Jr., R. C., W. Kauzmann, and A. Zipp. 1973. Pressure dependence of weak acid ionization, in aqueous buffers. J. Phys. Chem. 77:2687-2693.
26. Javid, N., K. Vogtt, ...,R. Winter. 2007. Protein-protein interactions in complex cosolvent solutions. ChemPhysChem. 8:679-689.
27. Krywka, C., C. Sternemann, ...,M. Tolan. 2007. The small-angle and wide-angle x-ray scattering set-up at beamline BL9 of DELTA. J. Synchrotron Radiat. 14:244-251.
28. Roth, S. V., R. Döhrmann, ...,P. Muller-Buschbaum. 2006. Smallangle options of the upgraded ultrasmall-angle x-ray scattering beamline BW4 at HASYLAB. Rev. Sci. Instrum, 77:085106.
29. Krywka, C., C. Sternemann, ...,R. Winter. 2008. Effect of osmolytes on pressure-induced unfolding of proteins: a high-pressure SAXS study. ChemPhysChem. 9:2809-2815.
30. Guinier, A., and G. Fournet. 1955. Small Angle Scattering of X-rays. Wiley, New York.
31. Svergun, D. I. 1992. Determination of regularization parameter in indirect-transform methods using perceptual criteria. J. Appl. Crystallogr. 25:495-503.
32. Street, T. O., C. M. Bradley, and D. Barrick. 2007. Predicting coupling limits from an experimentally determined energy landscape. Proc Natl. Acad. Sci. USA. 104:4907-4912.
33. Zweifel, M. E., and D. Barrick. 2002. Relationships between the temperature dependence of solvent denaturation and the denaturant dependence of protein stability curves. Biophys. Chem. 101-102:221-237.
34. Hawley, S. A. 1971, Reversible pressure-temperature denaturation of chymotrypsinogen. Biochemistry. 10:2436-2442.
35. Herberhold, H., and R. Winter. 2002. Temperature- and pressureinduced unfolding and refolding of ubiquitin: a static and kinetic Fourier transform infrared spectroscopy study. Biochemistry. 41:2396-2401.
36. Lassalle, M. W., H. Yamada, and K. Akasaka. 2000. The pressuretemperature free energy-landscape of staphylococcal nuclease monitored by (1)H NMR. J. Mol. Biol. 298:293-302.
37. Meersman, F., L. Smeller, and K. Heremans. 2006. Protein stability and dynamics in the pressure-temperature plane. Biochim. Biophys. Acta. 1764:346-354.
38. Smeller, L., F. Meersman, and K. Heremans. 2006. Refolding studies using pressure: The folding landscape of lysozyme in the pressuretemperature plane. Biochim. Biophys. Acta. 1764:497-505.
39. Wiedersich, J., S. Köhler, ...,J. Friedrich. 2008. Temperature and pressure dependence of protein stability: The engineered fluorescein-binding lipocalin FluA shows an elliptic phase diagram. Prot: Natl. Acad. Sci. USA. 105:5756-5761.
40. Zipp, A., and W. Kauzmann. 1973. Pressure denaturation of metmyoglobin. Biochemistry. 12:4217-4228.
41. From, N. B., and B. E. Bowler. 1998. Urea denaturation of staphylococcal nuclease monitored by Fourier transform infrared spectroscopy. Biochemistry. 37:1623-1631.
42. Reinställer, D., H. Fabian, ...,D. Naumann. 1996. Refolding of thermally and urea-denatured ribonuclease A monitored by time-resolved FTIR spectroscopy. Biochemistry. 35:15822-15830.
43. Silva, J. L., and G. Weber. 1993. Pressure stability of proteins. Annu. Rev. Phys. Chem. 44:89-113.
44. Weber, G., and H. G. Drickamer. 1983. The effect of high pressure upon proteins and other biomolecules. Q. Rev. Biophys. 16:89-112.
45. Imamura, H., and M. Kato. 2009. Effect of pressure on helix-coil transition of an alanine-based peptide: an FTIR study. Proteins. 75:911-918.
46. Paschek, D., S. Gnanakaran, and A. E. Garcia. 2005. Simulations of the pressure and temperature unfolding of an a-helical peptide. Proc. Natl. Acad. Sci. USA, 102:6765-6770.
47. Kloss, E., N. Courtemanche, and D. Barrick. 2008. Repeat-protein folding: new insights into origins of cooperativity, stability, and topology. Arch. Biochem. Biophys. 469:83-99.
48. Takekiyo, T., N. Takeda, ...,Y. Taniguchi. 2007. Pressure stability of the α-helix structure in a de novo designed protein (α-1-α)(2) studied by FTIR spectroscopy. Biopolymers. 85:185-188.
49. Muñoz, V., and L. Serrano. 1997. Development of the multiple sequence approximation within the AGADIR model of α-helix formation: comparison with Zimm-Bragg and Lifson-Roig formalisms. Biopolymers. 41:495-509.
50. Marqusee, S., V. H. Robbins, and R. L. Baldwin. 1989. Unusually stable helix formation, in short alanine-based peptides. Proc. Natl. Acad. Sci. USA. 86:5286-5290.
51. Kitahara, R., C. Royer, ...,C. Roumestand. 2002. Equilibrium and pressure-jump relaxation studies of the conformational transitions of P13MTCP1, J. Mol. Biol. 320:609-628.
52. Pappenberger, G., C. Saudan, ...,T. Kiefhaber. 2000. Denaturantinduced movement of the transition, state of protein folding revealed by high-pressure stopped-flow measurements. Proc: Natl. Acad. Sci. USA. 97:17-22.
53. Vidugiris, G. J., D. M. Truckses, ...,C. A. Royer. 1996. High-pressure denaturation of staphylococcal nuclease proline-to-glycine substitution mutants. Biochemistry. 35:3857-3864.
54. Tripp, K. W., and D. Barrick. 2008. Rerouting the folding pathway of the Notch ankyrin domain by reshaping the energy landscape. J. Am. Chem. Soc.: 130:5681-5688.