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PMID: 9416608 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

Dynamics and unfolding pathways of a hyperthermophilic and a mesophilic rubredoxin.

Protein science : a publication of the Protein Society ·Vol. 6 ·No. 12 ·1997-12-00 ·Pages 2589-605

Lazaridis T, Lee I, Karplus M

Abstract

Molecular dynamics simulations in solution are performed for a rubredoxin from the hyperthermophilic archaeon Pyrococcus furiosus (RdPf) and one from the mesophilic organism Desulfovibrio vulgaris (RdDv). The two proteins are simulated at four temperatures: 300 K, 373 K, 473 K (two sets), and 500 K; the various simulations extended from 200 ps to 1,020 ps. At room temperature, the two proteins are stable, remain close to the crystal structure, and exhibit similar dynamic behavior; the RMS residue fluctuations are slightly smaller in the hyperthermophilic protein. An analysis of the average energy contributions in the two proteins is made; the results suggest that the intraprotein energy stabilizes RdPf relative to RdDv. At 373 K, the mesophilic protein unfolds rapidly (it begins to unfold at 300 ps), whereas the hyperthermophilic does not unfold over the simulation of 600 ps. This is in accord with the expected stability of the two proteins. At 473 K, where both proteins are expected to be unstable, unfolding behavior is observed within 200 ps and the mesophilic protein unfolds faster than the hyperthermophilic one. At 500 K, both proteins unfold; the hyperthermophilic protein does so faster than the mesophilic protein. The unfolding behavior for the two proteins is found to be very similar. Although the exact order of events differs from one trajectory to another, both proteins unfold first by opening of the loop region to expose the hydrophobic core. This is followed by unzipping of the beta-sheet. The results obtained in the simulation are discussed in terms of the factors involved in flexibility and thermostability.

MeSH Terms
Amino Acid Sequence Computer Simulation Crystallization Desulfovibrio vulgaris/chemistry Drug Stability Electrochemistry Hydrogen Bonding Models, Molecular Molecular Sequence Data Molecular Structure Molecular Weight Protein Folding Pyrococcus/chemistry Rubredoxins/chemistry Temperature Thermodynamics
Chemicals
Rubredoxins
Authors & Affiliations
3 authors, click to expand affiliations / ORCID
Lazaridis T
Department of Chemistry and Chemical Biology, Harvard University, Cambridge, Massacusetts 02138, USA.
Lee I
Karplus M
References (68)
68 references, click to expand
  1. Enthalpic contribution to protein stability: insights from atom-based calculations and statistical mechanics.
    Adv Protein Chem. 1995;47:231-306 PMID: 8561050
  2. Energetics of protein structure.
    Adv Protein Chem. 1995;47:307-425 PMID: 8561051
  3. NMR structure of HMfB from the hyperthermophile, Methanothermus fervidus, confirms that this archaeal protein is a histone.
    J Mol Biol. 1996 Jan 12;255(1):187-203 PMID: 8568866
  4. Determinants of enzyme thermostability observed in the molecular structure of Thermus aquaticus D-glyceraldehyde-3-phosphate dehydrogenase at 25 Angstroms Resolution.
    Biochemistry. 1996 Feb 27;35(8):2597-609 PMID: 8611563
  5. Temperature dependence of the redox potential of rubredoxin from Pyrococcus furiosus: a molecular dynamics study.
    Biochemistry. 1996 Oct 29;35(43):13772-9 PMID: 8901519
  6. Enhanced protein flexibility caused by a destabilizing amino acid replacement in BPTI.
    J Mol Biol. 1997 May 30;269(1):154-64 PMID: 9193007
  7. Dissecting contributions to the thermostability of Pyrococcus furiosus rubredoxin: beta-sheet chimeras.
    Biochemistry. 1997 Aug 26;36(34):10406-13 PMID: 9265620
  8. Purification, catalytic properties, and thermal stability of threo-Ds-3-isopropylmalate dehydrogenase coded by leuB gene from an extreme thermophile, Thermus thermophilus strain HB8.
    J Biochem. 1990 Sep;108(3):449-56 PMID: 2277037
  9. The structure of rubredoxin from Desulfovibrio desulfuricans strain 27774 at 1.5 A resolution.
    Proteins. 1990;8(4):352-64 PMID: 2091025
  10. Relation between stability, dynamics and enzyme activity in 3-phosphoglycerate kinases from yeast and Thermus thermophilus.
    J Mol Biol. 1991 Jul 20;220(2):531-8 PMID: 1856872
  11. Determinants of protein hyperthermostability: purification and amino acid sequence of rubredoxin from the hyperthermophilic archaebacterium Pyrococcus furiosus and secondary structure of the zinc adduct by NMR.
    Biochemistry. 1991 Nov 12;30(45):10885-95 PMID: 1932012
  12. The energy landscapes and motions of proteins.
    Science. 1991 Dec 13;254(5038):1598-603 PMID: 1749933
  13. Proline residues responsible for thermostability occur with high frequency in the loop regions of an extremely thermostable oligo-1,6-glucosidase from Bacillus thermoglucosidasius KP1006.
    J Biol Chem. 1991 Dec 25;266(36):24287-94 PMID: 1761534
  14. Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect.
    Science. 1992 Jan 10;255(5041):178-83 PMID: 1553543
  15. The folding of an enzyme. II. Substructure of barnase and the contribution of different interactions to protein stability.
    J Mol Biol. 1992 Apr 5;224(3):783-804 PMID: 1569557
  16. Crystalline ribonuclease A loses function below the dynamical transition at 220 K.
    Nature. 1992 Jun 4;357(6377):423-4 PMID: 1463484
  17. Effect of active site residues in barnase on activity and stability.
    J Mol Biol. 1992 Jun 5;225(3):585-9 PMID: 1602471
  18. Refinement of rubredoxin from Desulfovibrio vulgaris at 1.0 A with and without restraints.
    Acta Crystallogr B. 1992 Feb 1;48 ( Pt 1):42-59 PMID: 1616692
  19. Simulation of the thermal denaturation of hen egg white lysozyme: trapping the molten globule state.
    Biochemistry. 1992 Sep 1;31(34):7745-8 PMID: 1510961
  20. The structure of a thermally stable 3-phosphoglycerate kinase and a comparison with its mesophilic equivalent.
    Proteins. 1993 Mar;15(3):283-9 PMID: 8456097
  21. Modeling the structure of Pyrococcus furiosus rubredoxin by homology to other X-ray structures.
    Protein Sci. 1993 Apr;2(4):640-9 PMID: 8518735
  22. Investigations of the thermostability of rubredoxin models using molecular dynamics simulations.
    Protein Sci. 1993 Apr;2(4):650-65 PMID: 8518736
  23. Protein unfolding pathways explored through molecular dynamics simulations.
    J Mol Biol. 1993 Jul 20;232(2):600-19 PMID: 7688428
  24. Structural and genetic analysis of protein stability.
    Annu Rev Biochem. 1993;62:139-60 PMID: 8352587
  25. Step-wise mutation of barnase to binase. A procedure for engineering increased stability of proteins and an experimental analysis of the evolution of protein stability.
    J Mol Biol. 1993 Sep 20;233(2):305-12 PMID: 8377205
  26. Thermal motions and function of bacteriorhodopsin in purple membranes: effects of temperature and hydration studied by neutron scattering.
    Proc Natl Acad Sci U S A. 1993 Oct 15;90(20):9668-72 PMID: 8415760
  27. Influence of protein flexibility on the redox potential of rubredoxin: energy minimization studies.
    Proteins. 1993 Oct;17(2):152-60 PMID: 8265563
  28. Do salt bridges stabilize proteins? A continuum electrostatic analysis.
    Protein Sci. 1994 Feb;3(2):211-26 PMID: 8003958
  29. Characterization of the transition state of protein unfolding by use of molecular dynamics: chymotrypsin inhibitor 2.
    Proc Natl Acad Sci U S A. 1994 Oct 25;91(22):10430-4 PMID: 7937969
  30. The sequence of a subtilisin-type protease (aerolysin) from the hyperthermophilic archaeum Pyrobaculum aerophilum reveals sites important to thermostability.
    Protein Sci. 1994 Aug;3(8):1329-40 PMID: 7987227
  31. Protein stability parameters measured by hydrogen exchange.
    Proteins. 1994 Sep;20(1):4-14 PMID: 7824522
  32. Rubredoxin in crystalline state.
    Methods Enzymol. 1994;243:203-16 PMID: 7830611
  33. Structure of a hyperthermophilic tungstopterin enzyme, aldehyde ferredoxin oxidoreductase.
    Science. 1995 Mar 10;267(5203):1463-9 PMID: 7878465
  34. Are buried salt bridges important for protein stability and conformational specificity?
    Nat Struct Biol. 1995 Feb;2(2):122-8 PMID: 7749916
  35. Hyperthermophiles: taking the heat and loving it.
    Structure. 1995 Mar 15;3(3):251-4 PMID: 7788291
  36. Response of rubredoxin from Pyrococcus furiosus to environmental changes: implications for the origin of hyperthermostability.
    Biochemistry. 1995 Aug 8;34(31):9865-73 PMID: 7632687
  37. Solution structure and DNA-binding properties of a thermostable protein from the archaeon Sulfolobus solfataricus.
    Nat Struct Biol. 1994 Nov;1(11):808-19 PMID: 7634092
  38. Acid and thermal denaturation of barnase investigated by molecular dynamics simulations.
    J Mol Biol. 1995 Oct 6;252(5):672-708 PMID: 7563082
  39. Solution structure of the DNA-binding protein Sac7d from the hyperthermophile Sulfolobus acidocaldarius.
    Biochemistry. 1995 Oct 17;34(41):13289-304 PMID: 7577913
  40. Rubredoxin: a new electron transfer protein from Clostridium pasteurianum.
    Proc Natl Acad Sci U S A. 1965 Jul;54(1):193-9 PMID: 5216351
  41. Stereochemical basis of heat stability in bacterial ferredoxins and in haemoglobin A2.
    Nature. 1975 May 15;255(5505):256-9 PMID: 1143325
  42. Sequence and structure of D-glyceraldehyde 3-phosphate dehydrogenase from Bacillus stearothermophilus.
    Nature. 1977 Mar 24;266(5600):328-33 PMID: 193030
  43. Dynamic model of globular protein conformations based on NMR studies in solution.
    Nature. 1978 Sep 21;275(5677):247-8 PMID: 692702
  44. The structure of rubredoxin at 1.2 A resolution.
    J Mol Biol. 1979 Jul 5;131(3):509-22 PMID: 513127
  45. Thermal stability and protein structure.
    Biochemistry. 1979 Dec 11;18(25):5698-703 PMID: 518863
  46. Crystallographic refinement of rubredoxin at 1 x 2 A degrees resolution.
    J Mol Biol. 1980 Apr 15;138(3):615-33 PMID: 7411618
  47. A correlation between protein thermostability and resistance to proteolysis.
    Biochem J. 1982 Dec 1;207(3):641-4 PMID: 6819862
  48. 2D 1H and 3D 1H-15N NMR of zinc-rubredoxins: contributions of the beta-sheet to thermostability.
    Protein Sci. 1996 May;5(5):883-94 PMID: 8732760
  49. 2.0 A structure of indole-3-glycerol phosphate synthase from the hyperthermophile Sulfolobus solfataricus: possible determinants of protein stability.
    Structure. 1995 Dec 15;3(12):1295-306 PMID: 8747456
  50. Use of a minimum perturbation approach to predict TIM mutant structures.
    Protein Eng. 1995 Nov;8(11):1103-15 PMID: 8819976
  51. Enzyme thermostability and thermoactivity.
    Protein Eng. 1996 Aug;9(8):629-30 PMID: 8875639
  52. Correlation of hydrogen exchange behaviour and thermal stability of lysozyme.
    J Mol Biol. 1983 Aug 15;168(3):687-92 PMID: 6887252
  53. Quasi-harmonic method for studying very low frequency modes in proteins.
    Biopolymers. 1984 Jun;23(6):1099-112 PMID: 6733249
  54. Single amino acid replacements affecting the thermostability of kanamycin nucleotidyltransferase.
    Mol Gen Genet. 1986 Aug;204(2):355-8 PMID: 3020373
  55. Effect of anisotropy and anharmonicity on protein crystallographic refinement. An evaluation by molecular dynamics.
    J Mol Biol. 1986 Jul 20;190(2):227-54 PMID: 3795269
  56. Enhanced protein thermostability from site-directed mutations that decrease the entropy of unfolding.
    Proc Natl Acad Sci U S A. 1987 Oct;84(19):6663-7 PMID: 3477797
  57. Replacements of Pro86 in phage T4 lysozyme extend an alpha-helix but do not alter protein stability.
    Science. 1988 Feb 5;239(4840):631-5 PMID: 3277275
  58. Temperature adaptation of lactate dehydrogenase. Structural, functional and genetic aspects.
    Biophys Chem. 1988 Feb;29(1-2):171-9 PMID: 3282559
  59. Structure and stability of thermophilic enzymes. Studies on thermolysin.
    Biophys Chem. 1988 Feb;29(1-2):181-93 PMID: 3129040
  60. Polar hydrogen positions in proteins: empirical energy placement and neutron diffraction comparison.
    Proteins. 1988;4(2):148-56 PMID: 3227015
  61. Engineering protein thermal stability. Sequence statistics point to residue substitutions in alpha-helices.
    J Mol Biol. 1989 Mar 20;206(2):397-406 PMID: 2716053
  62. Thermitase, a thermostable subtilisin: comparison of predicted and experimental structures and the molecular cause of thermostability.
    Proteins. 1989;5(1):22-37 PMID: 2664764
  63. Dynamics of myoglobin: comparison of simulation results with neutron scattering spectra.
    Proc Natl Acad Sci U S A. 1990 Feb;87(4):1601-5 PMID: 2304919
  64. Comparison of the dynamics of myoglobin in different crystal forms.
    Biophys J. 1990 Feb;57(2):381-3 PMID: 2180490
  65. Structure of a thermostable disulfide-bridge mutant of phage T4 lysozyme shows that an engineered cross-link in a flexible region does not increase the rigidity of the folded protein.
    Biochemistry. 1990 Mar 13;29(10):2592-8 PMID: 2334683
  66. Extremely thermostable D-glyceraldehyde-3-phosphate dehydrogenase from the eubacterium Thermotoga maritima.
    Biochemistry. 1990 Aug 21;29(33):7584-92 PMID: 2271518
  67. Molecular dynamics simulations of rubredoxin from Clostridium pasteurianum: changes in structure and electrostatic potential during redox reactions.
    Proteins. 1995 Jun;22(2):154-67 PMID: 7567963
  68. The optimization of protein-solvent interactions: thermostability and the role of hydrophobic and electrostatic interactions.
    Protein Sci. 1995 Aug;4(8):1516-27 PMID: 8520477
Article Info
Journal
Protein science : a publication of the Protein Society
Abbr.
Protein Sci
ISSN
0961-8368
Published
1997-12-00
Pages
2589-605
Language
English
Region
United States
NLM ID
9211750
PMCID
PMC2143628
Subset
IM
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