Effects of pressure on the dynamics of an oligomeric protein from deep-sea hyperthermophile

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 45, 2015, Pages 13886-13891

  Shrestha, Utsab R ^a   Bhowmik, Debsindhu ^a   Copley, John R D ^b   Tyagi, Madhusudan ^b,c   Leão, Juscelino B ^b   Chu, Xiang Qiang ^a  

^a WAYNE STATE UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^c UNIVERSITY OF MARYLAND   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HEN EGG WHITE LYSOZYME; HYDROGEN; INORGANIC PYROPHOSPHATASE; PROTEIN; UNCLASSIFIED DRUG; ARCHAEAL PROTEIN; BIOPOLYMER;

ARTICLE; CONFORMATIONAL TRANSITION; ENERGY; ENZYME ACTIVITY; ENZYME DENATURATION; FOURIER TRANSFORMATION; HYPERBARISM; HYPERTHERMOPHILE; MOLECULAR DYNAMICS; NEUTRON SCATTERING; NONHUMAN; PRIORITY JOURNAL; SPECTROMETER; TEMPERATURE; CHEMISTRY; ENZYMOLOGY; MARINE BIOLOGY; PRESSURE; THERMOCOCCUS;

ARCHAEAL PROTEINS; BIOPOLYMERS; MARINE BIOLOGY; PRESSURE; THERMOCOCCUS;

EID: 84946780138     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1514478112     Document Type: Article

References (75)

1. Orengo CA, Todd AE, Thornton JM (1999) From protein structure to function. Curr Opin Struct Biol 9(3):374-382.
2. Frauenfelder H, et al. (2009) A unified model of protein dynamics. Proc Natl Acad Sci USA 106(13):5129-5134.
3. Henzler-Wildman K, Kern D (2007) Dynamic personalities of proteins. Nature 450(7172): 964-972.
4. Parak F, Knapp EW (1984) A consistent picture of protein dynamics. Proc Natl Acad Sci USA 81(22):7088-7092.
5. Frauenfelder H, Parak F, Young RD (1988) Conformational substates in proteins. Annu Rev Biophys Biophys Chem 17:451-479.
6. Frauenfelder H, Leeson DT (1998) The energy landscape in non-biological and biological molecules. Nat Struct Biol 5(9):757-759.
7. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254(5038):1598-1603.
8. Austin RH, Beeson KW, Eisenstein L, Frauenfelder H, Gunsalus IC (1975) Dynamics of ligand binding to myoglobin. Biochemistry 14(24):5355-5373.
9. Onuchic JN, Luthey-Schulten Z, Wolynes PG (1997) Theory of protein folding: The energy landscape perspective. Annu Rev Phys Chem 48:545-600.
10. Hofmann C, Aartsma TJ, Michel H, Köhler J (2003) Direct observation of tiers in the energy landscape of a chromoprotein: A single-molecule study. Proc Natl Acad Sci USA 100(26):15534-15538.
11. Kitao A, Hayward S, Go N (1998) Energy landscape of a native protein: Jumpingamong-minima model. Proteins 33(4):496-517.
12. Milanesi L, et al. (2012) Measurement of energy landscape roughness of folded and unfolded proteins. Proc Natl Acad Sci USA 109(48):19563-19568.
13. Henzler-Wildman KA, et al. (2007) A hierarchy of timescales in protein dynamics is linked to enzyme catalysis. Nature 450(7171):913-916.
14. Chu XQ, et al. (2010) Experimental evidence of logarithmic relaxation in single-particle dynamics of hydrated protein molecules. Soft Matter 6(12):2623-2627.
15. Lagi M, Baglioni P, Chen SH (2009) Logarithmic decay in single-particle relaxation of hydrated lysozyme powder. Phys Rev Lett 103(10):108102.
16. Mulder FAA, Hon B, Mittermaier A, Dahlquist FW, Kay LE (2002) Slow internal dynamics in proteins: Application of NMR relaxation dispersion spectroscopy to methyl groups in a cavity mutant of T4 lysozyme. J Am Chem Soc 124(7):1443-1451.
17. Gabel F, et al. (2002) Protein dynamics studied by neutron scattering. Q Rev Biophys 35(4):327-367.
18. Calandrini V, Kneller GR (2008) Influence of pressure on the slow and fast fractional relaxation dynamics in lysozyme: A simulation study. J Chem Phys 128(6):065102.
19. Chu XQ, et al. (2009) Proteins remain soft at lower temperatures under pressure. J Phys Chem B 113(15):5001-5006.
20. Filabozzi A, et al. (2010) Elastic incoherent neutron scattering as a probe of high pressure induced changes in protein flexibility. Biochim Biophys Acta 1804(1):63-67.
21. Heremans K, Smeller L (1998) Protein structure and dynamics at high pressure. Biochim Biophys Acta 1386(2):353-370.
22. Mamontov E, O'Neill H, Zhang Q, Chathoth SM (2013) Temperature dependence of the internal dynamics of a protein in an aqueous solvent: Decoupling from the solvent viscosity. Chem Phys 424:12-19.
23. Tilton RF, Jr, Dewan JC, Petsko GA (1992) Effects of temperature on protein structure and dynamics: X-ray crystallographic studies of the protein ribonuclease-A at nine different temperatures from 98 to 320 K. Biochemistry 31(9):2469-2481.
24. Dhindsa GK, TyagiM, Chu XQ (2014) Temperature-dependent dynamics of dry and hydrated β-casein studied by quasielastic neutron scattering. J Phys Chem B 118(37):10821-10829.
25. Day R, Bennion BJ, Ham S, Daggett V (2002) Increasing temperature accelerates protein unfolding without changing the pathway of unfolding. J Mol Biol 322(1):189-203.
26. Khechinashvili NN, Janin J, Rodier F (1995) Thermodynamics of the temperatureinduced unfolding of globular proteins. Protein Sci 4(7):1315-1324.
27. Meersman F, et al. (2010) Consistent picture of the reversible thermal unfolding of hen egg-white lysozyme from experiment andmolecular dynamics. Biophys J 99(7):2255-2263.
28. Frauenfelder H, et al. (1990) Proteins and pressure. J Phys Chem 94(3):1024-1037.
29. Mozhaev VV, Heremans K, Frank J, Masson P, Balny C (1996) High pressure effects on protein structure and function. Proteins 24(1):81-91.
30. Gross M, Jaenicke R (1994) Proteins under pressure: The influence of high hydrostatic pressure on structure, function and assembly of proteins and protein complexes. Eur Biophys J 221(2):617-630.
31. Li H, Yamada H, Akasaka K (1999) Effect of pressure on the tertiary structure and dynamics of folded basic pancreatic trypsin inhibitor. Biophys J 77(5):2801-2812.
32. Boonyaratanakornkit BB, Park CB, Clark DS (2002) Pressure effects on intra-And intermolecular interactions within proteins. Biochim Biophys Acta 1595(1-2):235-249.
33. Roche J, et al. (2012) Cavities determine the pressure unfolding of proteins. Proc Natl Acad Sci USA 109(18):6945-6950.
34. Prehoda KE, Mooberry ES, Markley JL (1998) Pressure denaturation of proteins: Evaluation of compressibility effects. Biochemistry 37(17):5785-5790.
35. Hillson N, Onuchic JN, García AE (1999) Pressure-induced protein-folding/unfolding kinetics. Proc Natl Acad Sci USA 96(26):14848-14853.
36. Daniel I, Oger P, Winter R (2006) Origins of life and biochemistry under high-pressure conditions. Chem Soc Rev 35(10):858-875.
37. Stetter KO (2006) Hyperthermophiles in the history of life. Philos Trans R Soc Lond B Biol Sci 361(1474):1837-1842, discussion 1842-1843.
38. Ohmae E, Murakami C, Gekko K, Kato C (2007) Pressure effects on enzyme functions. J Biol Macromol 7:23-29.
39. Hughes RC, et al. (2012) Inorganic pyrophosphatase crystals from Thermococcus thioreducens for X-ray and neutron diffraction. Acta Crystallogr Sect F Struct Biol Cryst Commun 68(Pt 12):1482-1487.
40. Byrne-Steele ML, Ng JD (2009) Expression, purification and preliminary X-ray analysis of proliferating cell nuclear antigen from the archaeon Thermococcus thioreducens. Acta Crystallogr Sect F Struct Biol Cryst Commun 65(Pt 9):906-909.
41. Chu XQ, et al. (2012) Dynamic behavior of oligomeric inorganic pyrophosphatase explored by quasielastic neutron scattering. J Phys Chem B 116(33):9917-9921.
42. Roh JH, et al. (2006) Influence of hydration on the dynamics of lysozyme. Biophys J 91(7):2573-2588.
43. Carrillo W, García-Ruiz A, Recio I, Moreno-Arribas MV (2014) Antibacterial activity of hen egg white lysozyme modified by heat and enzymatic treatments against oenological lactic acid bacteria and acetic acid bacteria. J Food Prot 77(10):1732-1739.
44. Matthyssens GE, Simons G, Kanarek L (1972) Study of the thermal-denaturationmechanism of hen egg-white lysozyme through proteolytic degradation. Eur J Biochem 26(4):449-454.
45. Hikima S, Hikima J-i, Rojtinnakorn J, Hirono I, Aoki T (2003) Characterization and function of kuruma shrimp lysozyme possessing lytic activity against Vibrio species. Gene 316:187-195.
46. Copley JRD, Cook JC (2003) The Disk Chopper Spectrometer at NIST: A new instrument for quasielastic neutron scattering studies. Chem Phys 292(2-3):477-485.
47. Meyer A, Dimeo RM, Gehring PM, Neumann DA (2003) The high-flux backscattering spectrometer at the NIST Center for Neutron Research. Rev Sci Instrum 74(5):2759-2777.
48. Nickels JD, et al. (2012) Dynamics of protein and its hydration water: Neutron scattering studies on fully deuterated GFP. Biophys J 103(7):1566-1575.
49. Fujiwara S, Plazanet M, Matsumoto F, Oda T (2011) Internal motions of actin characterized by quasielastic neutron scattering. Eur Biophys J 40(5):661-671.
50. Dellerue S, Petrescu A-J, Smith JC, Bellissent-Funel M-C (2001) Radially softening diffusive motions in a globular protein. Biophys J 81(3):1666-1676.
51. Volino F, Dianoux AJ (1980) Neutron incoherent scattering law for diffusion in a potential of spherical symmetry: General formalism and application to diffusion inside a sphere. Mol Phys 41(2):271-279.
52. Kneller GR (2005) Quasielastic neutron scattering and relaxation processes in proteins: Analytical and simulation-based models. Phys Chem Chem Phys 7(13):2641-2655.
53. Angell CA (1995) Formation of glasses from liquids and biopolymers. Science 267(5206): 1924-1935.
54. Etchegoin P (1998) Glassylike low-frequency dynamics of globular proteins. Phys Rev E Stat Phys Plasmas Fluids Relat Interdiscip Topics 58(1):845-848.
55. Iben IE, et al. (1989) Glassy behavior of a protein. Phys Rev Lett 62(16):1916-1919.
56. Green JL, Fan J, Angell CA (1994) The protein-glass analogy: Some insights from homopeptide comparisons. J Phys Chem 98(51):13780-13790.
57. Gotze W, Sjogren L (1992) Relaxation processes in supercooled liquids. Rep Prog Phys 55(3):241-376.
58. Chu XQ, Mamontov E, O'Neill H, Zhang Q (2013) Temperature dependence of logarithmic-like relaxational dynamics of hydrated tRNA. J Phys Chem Lett 4(6):936-942.
59. Chou K-C (1985) Low-frequency motions in protein molecules. β-Sheet and β-barrel. Biophys J 48(2):289-297.
60. Rasmussen BF, Stock AM, Ringe D, Petsko GA (1992) Crystalline ribonuclease A loses function below the dynamical transition at 220 K. Nature 357(6377):423-424.
61. Ringe D, Petsko GA (2003) The "glass transition" in protein dynamics: What it is, why it occurs, and how to exploit it. Biophys Chem 105(2-3):667-680.
62. Caliskan G, et al. (2006) Dynamic transition in tRNA is solvent induced. J Am Chem Soc 128(1):32-33.
63. Meinhold L, Smith JC, Kitao A, Zewail AH (2007) Picosecond fluctuating protein energy landscape mapped by pressure temperature molecular dynamics simulation. Proc Natl Acad Sci USA 104(44):17261-17265.
64. Calligari PA, et al. (2015) Adaptation of extremophilic proteins with temperature and pressure: Evidence from initiation factor 6. J Phys Chem B 119(25):7860-7873.
65. Zaccai G (2000) How soft is a protein? A protein dynamics force constant measured by neutron scattering. Science 288(5471):1604-1607.
66. Tehei M, Daniel R, Zaccai G (2006) Fundamental and biotechnological applications of neutron scattering measurements for macromolecular dynamics. Eur Biophys J 35(7):551-558.
67. Kamatari YO, et al. (2001) Response of native and denatured hen lysozyme to high pressure studied by 15N/1H NMR spectroscopy. Eur J Biochem 268(6):1782-1793.
68. Matthews BW (2012) Proteins under pressure. Proc Natl Acad Sci USA 109(18):6792-6793.
69. Refaee M, Tezuka T, Akasaka K, Williamson MP (2003) Pressure-dependent changes in the solution structure of hen egg-white lysozyme. J Mol Biol 327(4):857-865.
70. Dahlhoff E, Somero GN (1991) Pressure and temperature adaptation of cytosolic malate dehydrogenase of shallow and deep-living marine invertebrates: Evidence for high body temperatures in hydrothermal vent animals. J Exp Biol 159(1):473-487.
71. Rupley JA, Careri G (1991) Protein hydration and function. Adv Protein Chem 41:37-172.
72. Pikuta EV, et al. (2007) Thermococcus thioreducens sp. nov., a novel hyperthermophilic, obligately sulfur-reducing archaeon from a deep-sea hydrothermal vent. Int J Syst Evol Microbiol 57(Pt 7):1612-1618.
73. Chu XQ, Mamontov E, O'Neill H, Zhang Q (2012) Apparent decoupling of the dynamics of a protein from the dynamics of its aqueous solvent. J Phys Chem Lett 3(3):380-385.
74. Azuah RT, et al. (2009) DAVE: A comprehensive software suite for the reduction, visualization, and analysis of low energy neutron spectroscopic data. J Res Natl Inst Stand Technol 114(6):341-358.
75. Doster W, Cusack S, Petry W (1989) Dynamical transition of myoglobin revealed by inelastic neutron scattering. Nature 337(6209):754-756.