Controlling the mechanoelasticity of model biomembranes with room-temperature ionic liquids

Rotella, Chiara; Kumari, Pallavi; Rodriguez, Brian J.; Jarvis, Suzanne P.; Benedetto, Antonio

doi:10.1007/s12551-018-0424-5

Cited by 13 publications

(23 citation statements)

References 32 publications

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“…5 ). The same group has also shown that ILs can affect the mechano-elasticity of phospholipid bilayers (Rotella et al 2018 ; Kumari et al 2020 ). Variation in the Young’s modulus of MDA-MB-231 cells has been observed after incubation in [C n mim]-based ILs (Fig.…”

Section: Mechanisms Of Action Of Ilsmentioning

confidence: 99%

“…5 ). The same group has also shown that ILs can affect the mechano-elasticity of phospholipid bilayers (Rotella et al 2018 ; Kumari et al 2020 ).…”

Section: Mechanisms Of Action Of Ilsmentioning

confidence: 99%

“…At low doses, (i) IL-cations insert into the lipid structure of phospholipids bilayers in a time scale of few nanoseconds; (ii) this insertion process is driven by the electrostatic attraction force between the positively charged imidazolium ring of the IL-cation with one of the electronegative oxygen atom in the lipid head, (iii) and it is stabilized by Van der Waals forces between the tail of the IL-cation and the tails of the phospholipid, which are both hydrophobic; (iv) the location of the IL-cation is always in the region between the heads and the tails of the phospholipids, and (v) it stays almost always in the outer leaflet region; (vi) the insertion process will reach a dynamical equilibrium with the amount of IL-cations in the order of 1-to-7 IL per 10 phospholipids; and (vii) it is not fully reversible. Furthermore, by AFM, we have shown that ILs dispersed at low doses at the bilayer-water interface are able to change the mechano-elasticity of phospholipid bilayers without affecting their overall structure and stability (Rotella et al 2018 ), and that this holds also at cell level (Benedetto and Ballone 2018a ) affecting cell migration and adhesion (Kumari et al 2020 ). In this context, more specifically, we have shown that sub-toxic doses of imidazolium ILs are able to enhance cell migration in human breast cancer cell line MDA-MB-231 by reducing the elasticity and the penetration resistance of the cellular lipid membrane (Fig.…”

Section: Introductionmentioning

confidence: 99%

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Mechanisms of action of ionic liquids on living cells: the state of the art

2020

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Ionic liquids (ILs) are a relatively new class of organic electrolytes composed of an organic cation and either an organic or inorganic anion, whose melting temperature falls around room-temperature. In the last 20 years, the toxicity of ILs towards cells and micro-organisms has been heavily investigated with the main aim to assess the risks associated with their potential use in (industrial) applications, and to develop strategies to design greener ILs. Toxicity, however, is synonym with affinity, and this has stimulated, in turn, a series of biophysical and chemical-physical investigations as well as few biochemical studies focused on the mechanisms of action (MoAs) of ILs, key step in the development of applications in bio-nanomedicine and bio-nanotechnology. This review has the intent to present an overview of the state of the art of the MoAs of ILs, which have been the focus of a limited number of studies but still sufficient enough to provide a first glimpse on the subject. The overall picture that emerges is quite intriguing and shows that ILs interact with cells in a variety of different mechanisms, including alteration of lipid distribution and cell membrane viscoelasticity, disruption of cell and nuclear membranes, mitochondrial permeabilization and dysfunction, generation of reactive oxygen species, chloroplast damage (in plants), alteration of transmembrane and cytoplasmatic proteins/enzyme functions, alteration of signaling pathways, and DNA fragmentation. Together with our earlier review work on the biophysics and chemical-physics of IL-cell membrane interactions (Biophys. Rev. 9:309, 2017), we hope that the present review, focused instead on the biochemical aspects, will stimulate a series of new investigations and discoveries in the still new and interdisciplinary field of “ILs, biomolecules, and cells.”

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Section: Mechanisms Of Action Of Ilsmentioning

confidence: 99%

“…5 ). The same group has also shown that ILs can affect the mechano-elasticity of phospholipid bilayers (Rotella et al 2018 ; Kumari et al 2020 ).…”

Section: Mechanisms Of Action Of Ilsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Mechanisms of action of ionic liquids on living cells: the state of the art

2020

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“…Due to the importance of the interaction with the cell membrane, model biomembranes (such as phospholipid bilayers) can be artificially reconstructed in order to use surface techniques for a deep investigation, for example atomic force microscopy (AFM), − neutron scattering, X-rays, ,, quartz crystal balance, nanoplasmonics, electrochemical impedance measurements, and molecular dynamic simulations. − ILs were shown to be capable of strongly interacting with supported phospholipid structures to create defects and perturbations, including structural rearrangement and fluidification, formation of holes, and complete disintegration of the assemblies . Morphological and structural rearrangement of phospholipid bilayers on mica upon interaction with ILs was recently observed by Rotella et al, by means of AFM-based imaging and indentation analysis. These results are relevant since they demonstrate that ILs are able to markedly interact with the lipid system and, in particular, with simplified models of the cell membrane.…”

Section: Introductionmentioning

confidence: 99%

Imidazolium-Based Ionic Liquids Affect Morphology and Rigidity of Living Cells: An Atomic Force Microscopy Study

2018

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The study of the toxicity, biocompatibility, and environmental sustainability of room-temperature ionic liquids (ILs) is still in its infancy. Understanding the impact of ILs on living organisms, especially from the aquatic ecosystem, is urgent, since large amounts of these substances are starting to be employed as solvents in industrial chemical processes, and on the other side, evidence of toxic effects of ILs on microorganisms and single cells have been observed. To date, the toxicity of ILs has been investigated by means of macroscopic assays aimed at characterizing the effective concentrations (like the EC) that cause the death of a significant fraction of the population of microorganisms and cells. These studies allow us to identify the cell membrane as the first target of the IL interaction, whose effectiveness was correlated to the lipophilicity of the cation, i.e., to the length of the lateral alkyl chain. Our study aimed at investigating the molecular mechanisms underpinning the interaction of ILs with living cells. To this purpose, we carried out a combined topographic and mechanical analysis by atomic force microscopy of living breast metastatic cancer cells (MDA-MB-231) upon interaction with imidazolium-based ILs. We showed that ILs are able to induce modifications of the overall rigidity (effective Young's modulus) and morphology of the cells. Our results demonstrate that ILs act on the physical properties of the outer cell layer (the membrane linked to the actin cytoskeleton), already at concentrations below the EC. These potentially toxic effects are stronger at higher IL concentrations, as well as with longer lateral chains in the cation.

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“… 52 − 54 , 58 − 66 It has been shown, in this context, that IL cations, dispersed at low doses at the water–bilayer interface, diffuse into the lipid region of the bilayer, 61 , 62 causing variations in the lipid dynamics 63 , 64 and bilayer mechanoelasticity. 45 , 62 , 65 , 66 …”

Section: Introductionmentioning

confidence: 99%

Absorption of the [bmim][Cl] Ionic Liquid in DMPC Lipid Bilayers across Their Gel, Ripple, and Fluid Phases

Benedetto

Kelley

2022

J. Phys. Chem. B

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Lipid bilayers are a key component of cell membranes and play a crucial role in life and in bio-nanotechnology. As a result, controlling their physicochemical properties holds the promise of effective therapeutic strategies. Ionic liquids (ILs)—a vast class of complex organic electrolytes—have shown a high degree of affinity with lipid bilayers and can be exploited in this context. However, the chemical physics of IL absorption and partitioning into lipid bilayers is yet to be fully understood. This work focuses on the absorption of the model IL [bmim][Cl] into 1,2-dimyristoyl- sn -glycero-3-phosphocholine (DMPC) lipid bilayers across their gel, ripple, and fluid phases. Here, by small-angle neutron scattering, we show that (i) the IL cations are absorbed in the lipid bilayer in all its thermodynamic phases and (ii) the amount of IL inserted into the lipid phase increased with increasing temperature, changing from three to four IL cations per 10 lipids with increasing temperature from 10 °C in the gel phase to 40 °C in the liquid phase, respectively. An explicative hypothesis, based on the entropy gain coming from the IL hydration water, is presented to explain the observed temperature trend. The ability to control IL absorption with temperature can be used as a handle to tune the effect of ILs on biomembranes and can be exploited in bio-nanotechnological applications.

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Controlling the mechanoelasticity of model biomembranes with room-temperature ionic liquids

Cited by 13 publications

References 32 publications

Mechanisms of action of ionic liquids on living cells: the state of the art

Mechanisms of action of ionic liquids on living cells: the state of the art

Imidazolium-Based Ionic Liquids Affect Morphology and Rigidity of Living Cells: An Atomic Force Microscopy Study

Absorption of the [bmim][Cl] Ionic Liquid in DMPC Lipid Bilayers across Their Gel, Ripple, and Fluid Phases

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