Transverse lipid organization dictates bending fluctuations in model plasma membranes

Rickeard, Brett W.; Nguyen, Michael H. L.; DiPasquale, Mitchell; Yip, Caesar G; Baker, Hamilton; Heberle, Frederick A.; Zuo, Xiaobing; Kelley, Elizabeth G.; Nagao, Michihiro; Marquardt, Drew

doi:10.1039/c9nr07977g

Cited by 31 publications

(27 citation statements)

References 62 publications

(88 reference statements)

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“…There is evidence that a non-zero leaflet tension could explain the surprising increase in bending rigidity observed in asymmetric vesicles prepared with the phase transfer technique [67]. A similar asymmetry-induced increase in the bending modulus was also reported in vesicles prepared using cyclodextrin-mediated lipid exchange [101]. These observations suggest that asymmetric model membranes in vitro likely harbor differential stress irrespective of how they are prepared.…”

Section: Molecular Dynamics (Md) Simulations Used To Model Asymmetric Membranessupporting

confidence: 54%

Model Membrane Systems Used to Study Plasma Membrane Lipid Asymmetry

et al. 2021

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It is well known that the lipid distribution in the bilayer leaflets of mammalian plasma membranes (PMs) is not symmetric. Despite this, model membrane studies have largely relied on chemically symmetric model membranes for the study of lipid–lipid and lipid–protein interactions. This is primarily due to the difficulty in preparing stable, asymmetric model membranes that are amenable to biophysical studies. However, in the last 20 years, efforts have been made in producing more biologically faithful model membranes. Here, we review several recently developed experimental and computational techniques for the robust generation of asymmetric model membranes and highlight a new and particularly promising technique to study membrane asymmetry.

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Section: Molecular Dynamics (Md) Simulations Used To Model Asymmetric Membranessupporting

confidence: 54%

Model Membrane Systems Used to Study Plasma Membrane Lipid Asymmetry

et al. 2021

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“…We therefore directly estimate the effective bending modulus, κ, which contains the effects of internal lipid monolayer dissipation. These effects are highly sensitive to the differences in surfactant properties and environment 19 and can provide mechanistic insights into EVALI pathology.…”

Section: ■ Introductionmentioning

confidence: 99%

A Mechanical Mechanism for Vitamin E Acetate in E-cigarette/Vaping-Associated Lung Injury

DiPasquale¹,

Gbadamosi²,

Nguyen³

et al. 2020

Chem. Res. Toxicol.

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The outbreak of electronic-cigarette/vaping-associated lung injury (EVALI) has made thousands ill. This lung injury has been attributed to a physical interaction between toxicants from the vaping solution and the pulmonary surfactant. In particular, studies have implicated vitamin E acetate as a potential instigator of EVALI. Pulmonary surfactant is vital to proper respiration through the mechanical processes of adsorption and interface stability to achieve and maintain low surface tension at the air−liquid interface. Using neutron spin echo spectroscopy, we investigate the impact of vitamin E acetate on the mechanical properties of two lipid-only pulmonary surfactant mimics: pure 1,2-dipalmitoyl-sn-glycero-3-phosphocholine and a more comprehensive lipid mixture. It was found that increasing vitamin E acetate concentration nonlinearly increased membrane fluidity and area compressibility to a plateau. Softer membranes would promote adsorption to the air−liquid interface during inspiration as well as collapse from the interface during expiration. These findings indicate the potential for the failure of the pulmonary surfactant upon expiration, attributed to monolayer collapse. This collapse could contribute to the observed EVALI signs and symptoms, including shortness of breath and pneumonitis.

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“…Other applications of NSE involve the utilization of neutron isotope sensitivity to investigate the dynamics of selective features within lipid membranes. For example, Rickeard et al (2020) used asymmetric lipid membranes with one of their bilayer leaflets selectively deuterated to investigate the effect of asymmetry and leaflet coupling on membrane bending fluctuations. Surprisingly, they found that asymmetric membranes possessed a larger bending modulus than symmetric bilayers with the same average lipid composition, a result that was uniquely enabled by NSE.…”

Section: Neutron Spin Echomentioning

confidence: 99%

“…Results from neutron scattering experiments have produced new insights, not only with regard to the material properties of membranes (e.g., bending rigidity), but also pertaining to their physical properties and how they relate to biological function. These insights have led to a better understanding of proteinlipid interactions, lipid domain formation and size, and PM asymmetry (Clifton et al, 2013;Marquardt et al, 2015;Heberle et al, 2016;Nickels et al, 2017;Rickeard et al, 2020).…”

Section: Introductionmentioning

confidence: 99%

Biomembrane Structure and Material Properties Studied With Neutron Scattering

et al. 2021

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Cell membranes and their associated structures are dynamical supramolecular structures where different physiological processes take place. Detailed knowledge of their static and dynamic structures is therefore needed, to better understand membrane biology. The structure–function relationship is a basic tenet in biology and has been pursued using a range of different experimental approaches. In this review, we will discuss one approach, namely the use of neutron scattering techniques as applied, primarily, to model membrane systems composed of lipid bilayers. An advantage of neutron scattering, compared to other scattering techniques, is the differential sensitivity of neutrons to isotopes of hydrogen and, as a result, the relative ease of altering sample contrast by substituting protium for deuterium. This property makes neutrons an ideal probe for the study of hydrogen-rich materials, such as biomembranes. In this review article, we describe isotopic labeling studies of model and viable membranes, and discuss novel applications of neutron contrast variation in order to gain unique insights into the structure, dynamics, and molecular interactions of biological membranes. We specifically focus on how small-angle neutron scattering data is modeled using different contrast data and molecular dynamics simulations. We also briefly discuss neutron reflectometry and present a few recent advances that have taken place in neutron spin echo spectroscopy studies and the unique membrane mechanical data that can be derived from them, primarily due to new models used to fit the data.

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Transverse lipid organization dictates bending fluctuations in model plasma membranes

Abstract: Neutron spin-echo (NSE) spectroscopy to measure the bending fluctuations of large unilamellar vesicles having an asymmetric transbilayer distribution of high- and low-melting lipids. Image by Kayle Kathleen Marie Gorospe of the University of Windsor Science Meets Art program.

Cited by 31 publications

References 62 publications

Model Membrane Systems Used to Study Plasma Membrane Lipid Asymmetry

Model Membrane Systems Used to Study Plasma Membrane Lipid Asymmetry

A Mechanical Mechanism for Vitamin E Acetate in E-cigarette/Vaping-Associated Lung Injury

Biomembrane Structure and Material Properties Studied With Neutron Scattering

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