Energetic and dynamic analysis of transport of Na+ and K+ through a cyclic peptide nanotube in water and in lipid bilayers

Yeonho Song, Ji Hye Lee, Hoon Hwang, George C Schatz, Hyonseok Hwang

Research output: Contribution to journalArticle

5 Citations (Scopus)

Abstract

Potential of mean force (PMF) profiles and position-dependent diffusion coefficients of Na+ and K+ are calculated to elucidate the translocation of ions through a cyclic peptide nanotube, composed of 8 × cyclo[-(d-Leu-Trp)4-] rings, in water and in hydrated DMPC bilayers. The PMF profiles and PMF decomposition analysis for the monovalent cations show that favorable interactions of the cations with the CPN as well as the lipid bilayer and dehydration free energy penalties are two major competing factors which determine the free energy surface for ion transport through CPNs both in water and in lipid bilayers, and that the selectivity of CPNs to cations mainly arises from favorable interaction energies of cations with CPNs and lipid bilayers that are more dominant than the dehydration penalties. Calculations of the position-dependent diffusion coefficients and dynamic friction kernels of the cations indicate that the dehydration process along with the molecular rearrangements occurring outside the channel and the coupling of the ion motions with the chain-structured water movements inside the channel lead to a decrease of the diffusion coefficients far away from the channel entrance and also reduced coefficients inside the channel. The PMF and diffusivity profiles for Na+ and K+ reveal that the energetics of ion transport through the CPN are governed by global interactions of ions with all the components in the system, while the diffusivity of ions through the channel is mostly determined by local interactions of ions with the confined water molecules inside the channel. Comparison of Na+ and K+ ion distributions based on overdamped Brownian dynamics simulations based on the PMF and diffusivity profiles with the corresponding results from molecular dynamics shows good agreement, indicating accuracy of the Bayesian inference method for determining diffusion coefficients in this application. In addition, this work shows that position-dependent diffusion coefficients of ions are required to explain the dynamics and conductance of ions through the CPN properly.

Original languageEnglish
Pages (from-to)11912-11922
Number of pages11
JournalJournal of Physical Chemistry B
Volume120
Issue number46
DOIs
Publication statusPublished - Nov 23 2016

Fingerprint

Peptide Nanotubes
Cyclic Peptides
Lipid bilayers
Dynamic analysis
Nanotubes
peptides
lipids
nanotubes
Ions
Water
diffusion coefficient
water
ions
cations
Positive ions
dehydration
Cations
diffusivity
Dehydration
profiles

ASJC Scopus subject areas

  • Physical and Theoretical Chemistry
  • Surfaces, Coatings and Films
  • Materials Chemistry

Cite this

Energetic and dynamic analysis of transport of Na+ and K+ through a cyclic peptide nanotube in water and in lipid bilayers. / Song, Yeonho; Lee, Ji Hye; Hwang, Hoon; Schatz, George C; Hwang, Hyonseok.

In: Journal of Physical Chemistry B, Vol. 120, No. 46, 23.11.2016, p. 11912-11922.

Research output: Contribution to journalArticle

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AB - Potential of mean force (PMF) profiles and position-dependent diffusion coefficients of Na+ and K+ are calculated to elucidate the translocation of ions through a cyclic peptide nanotube, composed of 8 × cyclo[-(d-Leu-Trp)4-] rings, in water and in hydrated DMPC bilayers. The PMF profiles and PMF decomposition analysis for the monovalent cations show that favorable interactions of the cations with the CPN as well as the lipid bilayer and dehydration free energy penalties are two major competing factors which determine the free energy surface for ion transport through CPNs both in water and in lipid bilayers, and that the selectivity of CPNs to cations mainly arises from favorable interaction energies of cations with CPNs and lipid bilayers that are more dominant than the dehydration penalties. Calculations of the position-dependent diffusion coefficients and dynamic friction kernels of the cations indicate that the dehydration process along with the molecular rearrangements occurring outside the channel and the coupling of the ion motions with the chain-structured water movements inside the channel lead to a decrease of the diffusion coefficients far away from the channel entrance and also reduced coefficients inside the channel. The PMF and diffusivity profiles for Na+ and K+ reveal that the energetics of ion transport through the CPN are governed by global interactions of ions with all the components in the system, while the diffusivity of ions through the channel is mostly determined by local interactions of ions with the confined water molecules inside the channel. Comparison of Na+ and K+ ion distributions based on overdamped Brownian dynamics simulations based on the PMF and diffusivity profiles with the corresponding results from molecular dynamics shows good agreement, indicating accuracy of the Bayesian inference method for determining diffusion coefficients in this application. In addition, this work shows that position-dependent diffusion coefficients of ions are required to explain the dynamics and conductance of ions through the CPN properly.

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