Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations

Zhernenkov, Mikhail; Bolmatov, Dima; Soloviov, Dmytro; Zhernenkov, Kirill; Toperverg, B. P.; Cunsolo, Alessandro; Bosak, A.; Cai, Yong Q.

doi:10.1038/ncomms11575

Cited by 61 publications

(111 citation statements)

References 57 publications

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“…However, on a macroscopic scale the average distance between repeating structural units increases due to the increased amount of Chol and, thus, the S (Q, 0) peak shifts toward smaller Q values. In the presented data, the S (Q, 0) structure factor shows no bulk water peak at Q = 20 nm −1 , which is an indication that IXS spectra are mainly dominated by the lipid sample (39,40). The IXS spectra (SI Appendix, Figs.…”

Section: Significancementioning

confidence: 56%

Functional lipid pairs as building blocks of phase-separated membranes

Soloviov

Cai

Bolmatov

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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Biological membranes exhibit a great deal of compositional and phase heterogeneity due to hundreds of chemically distinct components. As a result, phase separation processes in cell membranes are extremely difficult to study, especially at the molecular level. It is currently believed that the lateral membrane heterogeneity and the formation of domains, or rafts, are driven by lipid–lipid and lipid–protein interactions. Nevertheless, the underlying mechanisms regulating membrane heterogeneity remain poorly understood. In the present work, we combine inelastic X-ray scattering with molecular dynamics simulations to provide direct evidence for the existence of strongly coupled transient lipid pairs. These lipid pairs manifest themselves experimentally through optical vibrational (a.k.a. phononic) modes observed in binary (1,2-dipalmitoyl-sn-glycero-3-phosphocholine [DPPC]–cholesterol) and ternary (DPPC–1,2-dioleoyl-sn-glycero-3-phosphocholine/1-palmitoyl-2-oleoyl-glycero-3-phosphocholine [DOPC/POPC]–cholesterol) systems. The existence of a phononic gap in these vibrational modes is a direct result of the finite size of patches formed by these lipid pairs. The observation of lipid pairs provides a spatial (subnanometer) and temporal (subnanosecond) window into the lipid–lipid interactions in complex mixtures of saturated/unsaturated lipids and cholesterol. Our findings represent a step toward understanding the lateral organization and dynamics of membrane domains using a well-validated probe with a high spatial and temporal resolution.

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Section: Significancementioning

confidence: 56%

Functional lipid pairs as building blocks of phase-separated membranes

Soloviov

Cai

Bolmatov

et al. 2020

Proc. Natl. Acad. Sci. U.S.A.

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“…Other recent studies have highlighted the existence of a complex collective THz dynamics of phospholipid membrane [22,23] and of an anomalous trend of the in-plane collective dynamics in crossing the main phase transition [24]. These anomalous vibrational dynamics were proven to be correlated with the formation of short-lived nanometer-scale lipid clusters that play a role in facilitating the passive molecular transport across the bilayer plane [24].…”

Section: Introductionmentioning

confidence: 98%

Molecular Dynamics of POPC Phospholipid Bilayers through the Gel to Fluid Phase Transition: An Incoherent Quasi-Elastic Neutron Scattering Study

Wanderlingh¹,

Branca²,

Crupi³

et al. 2017

Journal of Chemistry

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The microscopic dynamics for the gel and liquid-crystalline phase of highly aligned D 2 O-hydrated bilayers of 1-palmitoyl-oleoylsn-glycero-phosphocholine (POPC) were investigated in the temperature range from 248 to 273 K by using incoherent quasielastic neutrons scattering (QENS). We develop a model for describing the molecular motions of the liquid phase occurring in the 0.3 to 350 ps time range. Accordingly, the complex dynamics of hydrogen are described in terms of simple dynamical processes involving different parts of the phospholipid chain. The analysis of the data evidences the existence of three different motions: the fast motion of hydrogen vibrating around the carbon atoms, the intermediate motion of carbon atoms in the acyl chains, and the slower translational motion of the entire phospholipid molecule. The influence of the temperature on these dynamical processes is investigated. In particular, by going from gel to liquid-crystalline phase, we reveal an increase of the segmental motion mainly affecting the terminal part of the acyl chains and a change of the diffusional dynamics from a localized rattling-like motion to a confined diffusion.

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“…However, for a bilayer membrane in a pure water system, previous atomistic simulations ascribe the permeation events to the potential energy fluctuations of the membrane, 7 similar to some experimental views, namely, transient local perturbations and "lipid pores." 8,25 Thus, not only the membrane conformation but also its potential fluctuation should play a key role in the water transport. We thus further compare the fluctuations of the lipid-lipid potential energy for the salt-in and salt-out cases, where the standard deviations are presented in Fig.…”

Section: Resultsmentioning

confidence: 99%

“…7 To some extent, this point of view is in agreement with a newest experimental work that shows the evidence of the formation of short-lived nanometer-scale lipid clusters and transient pores, facilitating the passive molecular transport across the bilayer membrane. 8 Thus, conformation and energy fluctuations should play a key role in the membrane permeation.…”

Section: Introductionmentioning

confidence: 99%

Asymmetric osmotic water permeation through a vesicle membrane

Zhao

Fang

et al. 2017

The Journal of Chemical Physics

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Understanding the water permeation through a cell membrane is of primary importance for biological activities and a key step to capture its shape transformation in salt solution. In this work, we reveal the dynamical behaviors of osmotically driven transport of water molecules across a vesicle membrane by molecular dynamics simulations. Of particular interest is that the water transport in and out of vesicles is highly distinguishable given the osmotic force are the same, suggesting an asymmetric osmotic transportation. This asymmetric phenomenon exists in a broad range of parameter space such as the salt concentration, temperature, and vesicle size and can be ascribed to the similar asymmetric potential energy of lipid-ion, lipid-water, lipid-solution, lipid-lipid, and the lipid-lipid energy fluctuation. Specifically, the water flux has a linear increase with the salt concentration, similar to the prediction by Nernst-Planck equation or Fick's first law. Furthermore, due to the Arrhenius relation between the membrane permeability and temperature, the water flux also exhibits excellent Arrhenius dependence on the temperature. Meanwhile, the water flux shows a linear increase with the vesicle surface area since the flux amount across a unit membrane area should be a constant. Finally, we also present the anonymous diffusion behaviors for the vesicle itself, where transitions from normal diffusion at short times to subdiffusion at long times are identified. Our results provide significant new physical insights for the osmotic water permeation through a vesicle membrane and are helpful for future experimental studies.

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Revealing the mechanism of passive transport in lipid bilayers via phonon-mediated nanometre-scale density fluctuations

Cited by 61 publications

References 57 publications

Functional lipid pairs as building blocks of phase-separated membranes

Functional lipid pairs as building blocks of phase-separated membranes

Molecular Dynamics of POPC Phospholipid Bilayers through the Gel to Fluid Phase Transition: An Incoherent Quasi-Elastic Neutron Scattering Study

Asymmetric osmotic water permeation through a vesicle membrane

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