A New Theoretical Approach to Biological Self-assembly

Overview

Journal Biophys Rev

Publisher Springer

Specialty Biophysics

Date 2017 May 17

PMID 28510109

Citations 14

Authors

Masahiro Kinoshita

Affiliations

Soon will be listed here.

Abstract

Upon biological self-assembly, the number of accessible translational configurations of water in the system increases considerably, leading to a large gain in water entropy. It is important to calculate the solvation entropy of a biomolecule with a prescribed structure by accounting for the change in water-water correlations caused by solute insertion. Modeling water as a dielectric continuum is not capable of capturing the physical essence of the water entropy effect. As a reliable tool, we propose a hybrid of the angle-dependent integral equation theory combined with a multipolar water model and a morphometric approach. Using our methods wherein the water entropy effect is treated as the key factor, we can elucidate a variety of processes such as protein folding, cold, pressure, and heat denaturating of a protein, molecular recognition, ordered association of proteins such as amyloid fibril formation, and functioning of ATP-driven proteins.

Citing Articles

Solvation, geometry, and assembly of the tobacco mosaic virus.

Spirandelli I, Evans M PNAS Nexus. 2025; 4(3):pgaf065.

PMID: 40065976 PMC: 11891515. DOI: 10.1093/pnasnexus/pgaf065.

Accelerated amyloid fibril formation at the interface of liquid-liquid phase-separated droplets by depletion interactions.

Yamaguchi K, Mima J, Nakajima K, Sakuta H, Yoshikawa K, Goto Y Protein Sci. 2025; 34(2):e5163.

PMID: 39876094 PMC: 11774873. DOI: 10.1002/pro.5163.

Free-energy decomposition of salt effects on the solubilities of small molecules and the role of excluded-volume effects.

Hervo-Hansen S, Lin D, Kasahara K, Matubayasi N Chem Sci. 2024; 15(2):477-489.

PMID: 38179544 PMC: 10763565. DOI: 10.1039/d3sc04617f.

Physical pictures of rotation mechanisms of F- and V-ATPases: Leading roles of translational, configurational entropy of water.

Yasuda S, Hayashi T, Murata T, Kinoshita M Front Mol Biosci. 2023; 10:1159603.

PMID: 37363397 PMC: 10288849. DOI: 10.3389/fmolb.2023.1159603.

Enhanced enzymatic activity exerted by a packed assembly of a single type of enzyme.

Dinh H, Nakata E, Mutsuda-Zapater K, Saimura M, Kinoshita M, Morii T Chem Sci. 2021; 11(34):9088-9100.

PMID: 34094190 PMC: 8161546. DOI: 10.1039/d0sc03498c.

References

Snir Y, Kamien R . Helical tubes in crowded environments. Phys Rev E Stat Nonlin Soft Matter Phys. 2007; 75(5 Pt 1):051114. DOI: 10.1103/PhysRevE.75.051114. View

Yasuda S, Yoshidome T, Oshima H, Kodama R, Harano Y, Kinoshita M . Effects of side-chain packing on the formation of secondary structures in protein folding. J Chem Phys. 2010; 132(6):065105. DOI: 10.1063/1.3319509. View

Hansen-Goos H, Roth R, Mecke K, Dietrich S . Solvation of proteins: linking thermodynamics to geometry. Phys Rev Lett. 2007; 99(12):128101. DOI: 10.1103/PhysRevLett.99.128101. View

Mishima H, Yasuda S, Yoshidome T, Oshima H, Harano Y, Ikeguchi M . Characterization of experimentally determined native-structure models of a protein using energetic and entropic components of free-energy function. J Phys Chem B. 2012; 116(27):7776-86. DOI: 10.1021/jp301541z. View

Yoshidome T, Harano Y, Kinoshita M . Pressure effects on structures formed by entropically driven self-assembly: illustration for denaturation of proteins. Phys Rev E Stat Nonlin Soft Matter Phys. 2009; 79(1 Pt 1):011912. DOI: 10.1103/PhysRevE.79.011912. View

Harano Y, Kinoshita M . Translational-entropy gain of solvent upon protein folding. Biophys J. 2005; 89(4):2701-10. PMC: 1366771. DOI: 10.1529/biophysj.104.057604. View

Kinoshita M . Molecular origin of the hydrophobic effect: analysis using the angle-dependent integral equation theory. J Chem Phys. 2008; 128(2):024507. DOI: 10.1063/1.2823733. View

Oshima H, Yasuda S, Yoshidome T, Ikeguchi M, Kinoshita M . Crucial importance of the water-entropy effect in predicting hot spots in protein-protein complexes. Phys Chem Chem Phys. 2011; 13(36):16236-46. DOI: 10.1039/c1cp21597c. View

Yoshidome T, Kinoshita M . Physical origin of hydrophobicity studied in terms of cold denaturation of proteins: comparison between water and simple fluids. Phys Chem Chem Phys. 2012; 14(42):14554-66. DOI: 10.1039/c2cp41738c. View

10.

Ellis R, Minton A . Cell biology: join the crowd. Nature. 2003; 425(6953):27-8. DOI: 10.1038/425027a. View

11.

Harano Y, Yoshidome T, Kinoshita M . Molecular mechanism of pressure denaturation of proteins. J Chem Phys. 2008; 129(14):145103. DOI: 10.1063/1.2991176. View

12.

Yoshidome T, Ito Y, Ikeguchi M, Kinoshita M . Rotation mechanism of F1-ATPase: crucial importance of the water entropy effect. J Am Chem Soc. 2011; 133(11):4030-9. DOI: 10.1021/ja109594y. View

13.

Oshima H, Yoshidome T, Amano K, Kinoshita M . A theoretical analysis on characteristics of protein structures induced by cold denaturation. J Chem Phys. 2009; 131(20):205102. DOI: 10.1063/1.3265985. View

14.

Karino Y, Matubayasi N . Communication: Free-energy analysis of hydration effect on protein with explicit solvent: equilibrium fluctuation of cytochrome c. J Chem Phys. 2011; 134(4):041105. DOI: 10.1063/1.3535560. View

15.

Amano K, Yoshidome T, Iwaki M, Suzuki M, Kinoshita M . Entropic potential field formed for a linear-motor protein near a filament: Statistical-mechanical analyses using simple models. J Chem Phys. 2010; 133(4):045103. DOI: 10.1063/1.3462279. View

16.

Kinoshita M . Importance of translational entropy of water in biological self-assembly processes like protein folding. Int J Mol Sci. 2009; 10(3):1064-1080. PMC: 2672019. DOI: 10.3390/ijms10031064. View

17.

Imai T, Harano Y, Kinoshita M, Kovalenko A, Hirata F . Theoretical analysis on changes in thermodynamic quantities upon protein folding: essential role of hydration. J Chem Phys. 2007; 126(22):225102. DOI: 10.1063/1.2743962. View

18.

Kodama R, Roth R, Harano Y, Kinoshita M . Morphometric approach to thermodynamic quantities of solvation of complex molecules: extension to multicomponent solvent. J Chem Phys. 2011; 135(4):045103. DOI: 10.1063/1.3617247. View

19.

Yoshidome T, Ito Y, Matubayasi N, Ikeguchi M, Kinoshita M . Structural characteristics of yeast F1-ATPase before and after 16-degree rotation of the γ subunit: theoretical analysis focused on the water-entropy effect. J Chem Phys. 2012; 137(3):035102. DOI: 10.1063/1.4734298. View

20.

Kinoshita M . Roles of translational motion of water molecules in sustaining life. Front Biosci (Landmark Ed). 2009; 14(9):3419-54. DOI: 10.2741/3463. View