journal article·2015-01Open access

Are coarse-grained models apt to detect protein thermal stability? The case of OPEP force field

Maria Kalimeri, Philippe Derreumaux, Fabio Sterpone

Abstract

We present the first investigation of the kinetic and thermodynamic stability of two homologous thermophilic and mesophilic proteins based on the coarse-grained model OPEP. The object of our investigation is a pair of G-domains of relatively large size, 200 amino acids each, with an experimental stability gap of about 40 K. The OPEP force field is able to maintain stable the fold of these relatively large proteins within the hundrend-nanosecond time scale without including external constraints. This makes possible to characterize the conformational landscape of the folded protein as well as to explore the unfolding. In agreement with all-atom simulations used as a reference, we show that the conformational landscape of the thermophilic protein is characterized by a larger number of substates with slower dynamics on the network of states and more resilient to temperature increase. Moreover, we verify the stability gap between the two proteins using replica-exchange simulations and estimate a difference between the melting temperatures of about 23 K, in fair agreement with experiment. The detailed investigation of the unfolding thermodynamics, allows to gain insight into the mechanism underlying the enhanced stability of the thermophile relating it to a smaller heat capacity of unfolding.
Source: europepmc · Quality: candidate unverified · Source record ↗

Research context

OpenAlex topics: Protein Structure and Dynamics · Enzyme Structure and Function · Spectroscopy and Quantum Chemical Studies

SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.

References (58)

Show source-provided references
1. Protein structure and the energetics of protein stability10.1021/cr960383c ↗
2. Hyperthermophilic enzymes: sources, uses, and molecular mechanisms for thermostability10.1128/MMBR.65.1.1-43.2001 ↗
3. Extremophiles as a source for novel enzymes10.1016/S1369-5274(03)00060-2 ↗
4. Protein stability and enzyme activity at extreme biological temperatures10.1088/0953-8984/22/32/323101 ↗
5. Thermophilic proteins: insight and perspective from in silico experiments10.1039/C1CS15199A ↗
6. Electrostatic contributions to the stability of hyperthermophilic proteins10.1006/jmbi.1999.2810 ↗
7. Ion pairs and the thermotolerance of proteins from hyperthermophiles: a “traffic rule” for hot roads10.1016/S0968-0004(01)01918-1 ↗
8. Quality matters: extension of clusters of residues with good hydrophobic contacts stabilize (hyper)thermophilic proteins10.1021/ci400568c ↗
9. How conformational flexibility stabilizes the hyperthermophilic elongation factor g-domain10.1021/jp407078z ↗
10. Reversible thermal unfolding of thermostable phosphoglycerate kinase. Thermostability associated with mean zero enthalpy change10.1016/0022-2836(77)90078-X ↗
11. Lessons in stability from thermophilic proteins10.1110/ps.062130306 ↗
12. The stability of Taq DNA polymerase results from a reduced entropic folding penalty; identification of other thermophilic proteins with similar folding thermodynamics10.1002/prot.24458 ↗
13. The opep protein model: from single molecules, amyloid formation, crowding and hydrodynamics to dna/rna systems10.1039/C4CS00048J ↗
14. Principles for designing ideal protein structures10.1038/nature11600 ↗
15. Rational stabilization of enzymes by computational redesign of surface charge-charge interactions10.1073/pnas.0808220106 ↗
16. A coarse-grained protein force field for folding and structure prediction10.1002/prot.21505 ↗
17. The coarse-grained opep force field for non-amyloid and amyloid proteins10.1021/jp301665f ↗
18. Importance of the ion-pair interactions in the opep coarse-grained force field: parametrization and validation10.1021/ct4003493 ↗
19. Understanding amyloid fibril nucleation and aÎ2 oligomer/drug interactions from computer simulations10.1021/ar4002075 ↗
20. Crystal structure of intact elongation factor EF-Tu from Escherichia coli in GDP conformation at 2.05Å̊ resolution10.1006/jmbi.1998.2387 ↗
21. The crystal structure of Sulfolobus solfataricus elongation factor 1a in complex with magnesium and gdp10.1021/bi0363331 ↗
22. Key role of proximal water in regulating thermostable proteins10.1021/jp805199c ↗
23. The effect of protein composition on hydration dynamics10.1039/c3cp44582h ↗
24. Use of the weighted histogram analysis method for the analysis of simulated and parallel tempering simulations10.1021/ct0502864 ↗
25. Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations10.1002/jcc.20065 ↗
26. Scalable molecular dynamics with namd10.1002/jcc.20289 ↗
27. Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features10.1002/bip.360221211 ↗
28. Hartigan · 1975
29. van Dongen · 2000
30. Schulten · 2000
31. Position-dependent diffusion coefficients and free energies from Bayesian analysis of equilibrium and replica molecular dynamics simulations10.1088/1367-2630/7/1/034 ↗
32. Computer simulations aimed at structure prediction of supersecondary motifs in proteins10.1002/prot.1135 ↗
33. Do ultrastable proteins from hyperthermophiles have high or low conformational rigidity?10.1073/pnas.97.7.2962 ↗
34. Millisecond time scale conformational flexibility in a hyperthermophile protein at ambient temperature10.1073/pnas.97.7.3166 ↗
35. Structural equilibrium fluctuations in mesophilic and thermophilic a-Amylase10.1016/S0006-3495(00)76413-7 ↗
36. Temperature dependence of the flexibility of thermophilic and mesophilic flavoenzymes of the nitroreductase fold10.1093/protein/gzp090 ↗
37. Bastian · 2009
38. Multi-basin dynamics of a protein in a crystal environment10.1016/S0167-2789(97)00090-0 ↗
39. Protein states and protein quakes10.1073/pnas.82.15.5000 ↗
40. The energy landscapes and motions of proteins10.1126/science.1749933 ↗
41. Energy landscapes: some new horizons10.1016/j.sbi.2009.12.011 ↗
42. Diffusion in a rough potential10.1073/pnas.85.7.2029 ↗
43. Diffusive dynamics of the reaction coordinate for protein folding funnels10.1063/1.471317 ↗
44. Coordinate-dependent diffusion in protein folding
45. How the diffusivity profile reduces the arbitrariness of protein folding free energies10.1063/1.3442716 ↗
46. A diffusion process-controlled Monte Carlo method for finding the global energy minimum of a polypeptide chain. I. Formulation and test on a hexadecapeptide10.1063/1.473525 ↗
47. Self-assembly of the beta 2-microglobulin NHVTLSQ peptide using a coarse-grained protein model reveals beta-barrel species10.1021/jp710592v ↗
48. Targeting the early steps of abeta16-22 protofibril disassembly by n-methylated inhibitors: a numerical study10.1002/prot.22254 ↗
49. Replica-exchange molecular dynamics method for protein folding10.1016/S0009-2614(99)01123-9 ↗
50. Stability against temperature of Sulfolobus solfataricus elongation factor 1a, a multi-domain protein10.1016/j.bbapap.2007.12.018 ↗
51. Thermostability of multidomain proteins: elongation factors EF-Tu from Escherichia coli and Bacillus stearothermophilus and their chimeric forms10.1110/ps.03272504 ↗
52. Assessing the quality of the opep coarse-grained force field10.1021/ct100646f ↗
53. How fast-folding proteins fold10.1126/science.1208351 ↗
54. The free energy landscape for hairpin folding in explicit water10.1073/pnas.201543998 ↗
55. Electrostatic contributions to the stability of a thermophilic cold shock protein10.1016/S0006-3495(03)75027-9 ↗
56. R Core Team · 2014
57. Bio3d: an R package for the comparative analysis of protein structures10.1093/bioinformatics/btl461 ↗
58. The igraph software package for complex network research