Structural plasticity of staphylococcal nuclease probed by perturbation with pressure and pH

Proteins: Structure, Function and Bioinformatics

Volumn 79, Issue 4, 2011, Pages 1293-1305

  Kitahara, Ryo ^a   Hata, Kazumi ^b   Maeno, Akihiro ^b   Akasaka, Kazuyuki ^b   Chimenti, Michael S ^c,f   Garcia Moreno, E Bertrand ^c   Schroer, Martin A ^d   Jeworrek, Christoph ^d   Tolan, Metin ^d   Winter, Roland ^d   Roche, Julien ^e   Roumestand, Christian ^e   Montet de Guillen, Karine ^e   Royer, Catherine A ^e  

^a RITSUMEIKAN UNIVERSITY   (Japan)

^b KINKI UNIVERSITY   (Japan)

^c JOHNS HOPKINS UNIVERSITY   (United States)

^d TU DORTMUND UNIVERSITY   (Germany)

^e UNIV MONTPELLIER   (France)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Conformational dynamics; NMR; Pressure; Protein electrostatics; SAXS

Indexed keywords

LYSINE; NUCLEASE; STAPHYLOCOCCUS NUCLEASE; UNCLASSIFIED DRUG;

ARTICLE; ATMOSPHERIC PRESSURE; HETERONUCLEAR SINGLE QUANTUM COHERENCE; HYDROPHOBICITY; HYDROSTATIC PRESSURE; IONIZATION; MOLECULAR DYNAMICS; MOLECULAR PROBE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PH; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PROTEIN VARIANT; STAPHYLOCOCCUS; STRUCTURE ANALYSIS; X RAY CRYSTALLOGRAPHY;

AMINO ACID SUBSTITUTION; DEUTERIUM EXCHANGE MEASUREMENT; HYDROGEN-ION CONCENTRATION; LYSINE; MICROCOCCAL NUCLEASE; MODELS, MOLECULAR; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PRESSURE; PROTEIN CONFORMATION; PROTEIN UNFOLDING; SCATTERING, SMALL ANGLE; STATIC ELECTRICITY; X-RAY DIFFRACTION;

EID: 79952490338     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.22966     Document Type: Article

References (53)

1. Stites WE, Gittis AG, Lattman EE, Shortle D. In a staphylococcal nuclease mutant the side-chain of a lysine replacing valine 66 is fully buried in the hydrophobic core. J Mol Biol 1991; 221: 7-14.
2. Baran KL, Chimenti MS, Schlessman JL, Fitch CA, Herbst KJ, Garcia-Moreno BE. Electrostatic effects in a network of polar and ionizable groups in staphylococcal nuclease. J Mol Biol 2008; 379: 1045-1062.
3. Garcia-Moreno B, Dwyer JJ, Gittis AG, Lattman EE, Spencer DS, Stites WE. Experimental measurement of the effective dielectric in the hydrophobic core of a protein. Biophys Chem 1997; 64: 211-224.
4. Castaneda CA, Fitch CA, Majumdar A, Khangulov V, Schlessman JL, Garcia-Moreno BE. Molecular determinants of the pK(a) values of Asp and Glu residues in staphylococcal nuclease. Proteins 2009; 77: 570-588.
5. Chimenti MS, Castaneda CA, Majumdar A, Garcia-Moreno B. Structural origins of high apparent dielectric constants experienced by ionizable groups in the hydrophobic core of a protein. J Mol Biol 2010; doi10.1016.2010.10.001.
6. Fitch CA, Karp DA, Lee KK, Stites WE, Lattman EE, Garcia-Moreno EB. Experimental pK(a) values of buried residues: analysis with continuum methods and role of water penetration. Biophys J 2002; 82: 3289-3304.
7. Isom DG, Cannon BR, Castaneda CA, Robinson A, Garcia-Moreno B. High tolerance for ionizable residues in the hydrophobic interior of proteins. Proc Natl Acad Sci USA 2008; 105: 17784-17788.
8. Karp DA, Gittis AG, Stahley MR, Fitch CA, Stites WE, Garcia-Moreno EB. High apparent dielectric constant inside a protein reflects structural reorganization coupled to the ionization of an internal Asp. Biophys J 2007; 92: 2041-2053.
9. Karp DA, Stahley MR, Garcia-Moreno B. Conformational consequences of ionization of Lys, Asp, and Glu buried at position 66 in staphylococcal nuclease. Biochemistry 2010; 49: 4138-4146.
10. Takayama Y, Castaneda CA, Chimenti M, Garcia-Moreno B, Iwahara J. Direct evidence for deprotonation of a lysine side chain buried in the hydrophobic core of a protein. J Am Chem Soc 2008; 130: 6714-6715.
11. Zheng Z, Sosnick TR. Protein vivisection reveals elusive intermediates in folding. J Mol Biol 2010; 397: 777-788.
12. Royer CA. Revisiting volume changes in pressure-induced protein unfolding. Biochim Biophys Acta 2002; 1595: 201-209.
13. Silva JL, Foguel D, Royer CA. Pressure provides new insights into protein folding, dynamics and structure. Trends Biochem Sci 2001; 26: 612-618.
14. Brun L, Isom DG, Velu P, Garcia-Moreno B, Royer CA. Hydration of the folding transition state ensemble of a protein. Biochemistry 2006; 45: 3473-3480.
15. Mitra L, Hata K, Kono R, Maeno A, Isom D, Rouget JB, Winter R, Akasaka K, Garcia-Moreno B, Royer CA. V(i)-value analysis: a pressure-based method for mapping the folding transition state ensemble of proteins. J Am Chem Soc 2007; 129: 14108-14109.
16. Mitra L, Rouget JB, Garcia-Moreno B, Royer CA, Winter R. Towards a quantitative understanding of protein hydration and volumetric properties. Chemphyschem 2008; 9: 2715-2721.
17. Panick G, Malessa R, Winter R, Rapp G, Frye KJ, Royer CA. Structural characterization of the pressure-denatured state and unfolding/refolding kinetics of staphylococcal nuclease by synchrotron small-angle X-ray scattering and Fourier-transform infrared spectroscopy. J Mol Biol 1998; 275: 389-402.
18. Panick G, Vidugiris GJ, Malessa R, Rapp G, Winter R, Royer CA. Exploring the temperature-pressure phase diagram of staphylococcal nuclease. Biochemistry 1999; 38: 4157-4164.
19. Woenckhaus J, Kohling R, Thiyagarajan P, Littrell KC, Seifert S, Royer CA, Winter R. Pressure-jump small-angle X-ray scattering detected kinetics of staphylococcal nuclease folding. Biophys J 2001; 80: 1518-1523.
20. Lassalle MW, Yamada H, Morii H, Ogata K, Sarai A, Akasaka K. Filling a cavity dramatically increases pressure stability of the c-Myb R2 subdomain. Proteins 2001; 45: 96-101.
21. 15N NMR. Biochemistry 2001; 40: 8665-8671.
22. Akasaka K. Highly fluctuating protein structures revealed by variable-pressure nuclear magnetic resonance. Biochemistry 2003; 42: 10875-10885.
23. Akasaka K. Probing conformational fluctuation of proteins by pressure perturbation. Chem Rev 2006; 106: 1814-1835.
24. Bezsonova I, Korzhnev DM, Prosser RS, Forman-Kay JD, Kay LE. Hydration and packing along the folding pathway of SH3 domains by pressure-dependent NMR. Biochemistry 2006; 45: 4711-4719.
25. Korzhnev DM, Bezsonova I, Evanics F, Taulier N, Zhou Z, Bai Y, Chalikian TV, Prosser RS, Kay LE. Probing the transition state ensemble of a protein folding reaction by pressure-dependent NMR relaxation dispersion. J Am Chem Soc 2006; 128: 5262-5269.
26. Korzhnev DM, Kay LE. Probing invisible, low-populated states of protein molecules by relaxation dispersion NMR spectroscopy: an application to protein folding. Acc Chem Res 2008; 41: 442-451.
27. Kataoka M, Nishii I, Fujisawa T, Ueki T, Tokunaga F, Goto Y. Structural characterization of the molten globule and native states of apomyoglobin by solution X-ray scattering. J Mol Biol 1995; 249: 215-228.
28. Svergun DI, Koch MHJ. Small-angle scattering studies of biological macromolecules in solution. Rep Prog Phys 2003: 1735-1782.
29. Franke D, Svergun DI. DAMMIF, a program for rapid ab-initio shape determination in small-angle scattering. J Appl Cryst 2009; 42: 342-346.
30. Akasaka K. Highly fluctuating protein structures revealed by variable-pressure nuclear magnetic resonance. Biochemistry 2003; 42: 10875-10885.
31. Kohn JE, Millett IS, Jacob J, Zagrovic B, Dillon TM, Cingel N, Dothager RS, Seifert S, Thiyagarajan P, Sosnick TR, Hasan MZ, Pande VS, Ruczinski I, Doniach S, Plaxco KW. Random-coil behavior and the dimensions of chemically unfolded proteins. Proc Natl Acad Sci USA 2004; 101: 12491-12496.
32. Rouget JB, Schroer MA, Jeworrek C, Pühse M, Saldana JL, Bessin Y, Tolan M, Barrick D, Winter R, Royer CA. Unique features of the folding landscape of a repeat protein revealed by pressure perturbation. Biophys J 2010; 98: 2712-2721.
33. Kobashigawa Y, Sakurai M, Nitta K. Effect of hydrostatic pressure on unfolding of alpha-lactalbumin: volumetric equivalence of the molten globule and unfolded state. Protein Sci 1999; 8: 2765-2772.
34. 1H NMR spectroscopy. Proc Natl Acad Sci USA 1993; 90: 1776-1780.
35. Ruan K, Lange R, Bec N, Balny C. A stable partly denatured state of trypsin induced by high hydrostatic pressure. Biochem Biophys Res Commun 1997; 239: 150-154.
36. Damjanovic A, Schlessman JL, Fitch CA, Garcia AE, Garcia-Moreno EB. Role of flexibility and polarity as determinants of the hydration of internal cavities and pockets in proteins. Biophys J 2007; 93: 2791-2804.
37. Ghosh N, Cui Q. pKa of residue 66 in Staphylococal nuclease. I. Insights from QM/MM simulations with conventional sampling. J Phys Chem B 2008; 112: 8387-8397.
38. Zheng L, Chen M, Yang W. Random walk in orthogonal space to achieve efficient free-energy simulation of complex systems. Proc Natl Acad Sci USA 2008; 105: 20227-20232.
39. Ropars V, Bouguet-Bonnet S, Auguin D, Barthe P, Canet D, Roumestand C. Unraveling protein dynamics through fast spectral density mapping. J Biomol NMR 2007; 37: 159-177.
40. Barthe P, Ropars V, Roumestand C. DYNAMOF: a program for the dynamics analysis of relaxation data obtained at multiple magnetic fields. In: 2006. 513 p.
41. Bai Y, Milne JS, Mayne L, Englander SW. Primary structure effects on peptide group hydrogen exchange. Proteins 1993; 17: 75-86.
42. Yamada H, Nishikawa K, Honda M, Shimura T, Tabayashi K, Akasaka K. Pressure-resisting cell for high-pressure, high-resolution nuclear magnetic resonance measurements at very high magnetic fields. Rev Sci Instrum 2001; 72: 1463-1471.
43. Royer CA, Smith WR, Beechem JM. Analysis of binding in macromolecular complexes: a generalized numerical approach. Anal Biochem 1990; 191: 287-294.
44. Royer CA, Beechem JM. Numerical analysis of binding data: advantages, practical aspects, and implications. Methods Enzymol 1992; 210: 481-505.
45. Neumann RC, Jr., Kauzmann W, Zipp A. Pressure dependence of weak acid ionization in aqueous buffers. J Phys Chem 1973: 2687-2693.
46. Javid N, Vogtt K, Krywka C, Tolan M, Winter R. Protein-protein interactions in complex cosolvent solutions. ChemPhysChem 2007; 8: 679-689.
47. Krywka C, Sternemann C, Paulus M, Javid N, Winter R, Al-Sawalmih A, Yi S, Raabe D, Tolan M. The small-angle and wide-angle X-ray scattering set-up at beamline BL9 of DELTA. J Synchrotron Rad 2007; 14: 251.
48. Roth SV, Dohrmann R, Dommach M, Kuhlmann M, Kroger I, Gehrke R, Walter H, Schroer C, Lengeler B, Müller-Buschbaum P. Small-angle options of the upgraded ultrasmall-angle X-ray scattering beamline BW4 at HASYLAB. Rev Sci Instrum 2006; 77: 085106.
49. Krywka C, Sternemann C, Paulus M, Tolan M, Royer C, Winter R. Effect of osmolytes on pressure-induced unfolding of proteins: A high-pressure SAXS study. ChemPhysChem 2008; 9: 2809-2815.
50. Lindner P, Zemb T. Neutrons, X-rays and light: scattering methods applied to soft condensed matter. Amsterdam: Elsevier Science; 2002.
51. Svergun DI. Determination of regularization parameter in indirect-transform methods using perceptual criteria. J Appl Cryst 1992; 25: 495-503.
52. Kozin MB, Svergun DI. Automated matching of high- and low-resolution structural models. J Appl Cryst 2001; 34: 33-41.
53. Volkov VV, Svergun DI. Uniqueness of ab initio shape determination in small-angle scattering. J Appl Cryst 2003; 36: 860-864.