Membrane dipole potential is sensitive to cholesterol stereospecificity: Implications for receptor function

Bandari, Suman; Chakraborty, Hirak; Covey, Douglas F.; Chattopadhyay, Amitabha

doi:10.1016/j.chemphyslip.2014.09.001

Cited by 38 publications

(32 citation statements)

References 49 publications

(85 reference statements)

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“…In addition, we recently showed that the requirement of cholesterol for receptor function is diastereospecific, but not enantiospecific (Jafurulla et al, 2014). This difference in sterol stereospecificity for receptor function appears to be related to membrane dipole potential (Bandari et al, 2014). We have also shown by coarse-grain molecular dynamics simulations that membrane cholesterol has higher occupancy in certain sites on the serotonin1A receptor (Sengupta and Chattopadhyay, 2012).…”

Section: Resultsmentioning

confidence: 69%

Molecular rheology of neuronal membranes explored using a molecular rotor: Implications for receptor function

Pal

Chakraborty

Bandari

et al. 2016

Chemistry and Physics of Lipids

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The role of membrane cholesterol as a crucial regulator in the structure and function of membrane proteins and receptors is well documented. However, there is a lack of consensus on the mechanism for such regulation. We have previously shown that the function of an important neuronal receptor, the serotonin1A receptor, is modulated by cholesterol in hippocampal membranes. With an overall objective of addressing the role of 3 membrane physical properties in receptor function, we measured the viscosity of hippocampal membranes of varying cholesterol content using a meso-substituted fluorophore (BODIPY-C12) based on the BODIPY probe. BODIPY-C12 acts as a fluorescent molecular rotor and allows measurement of hippocampal membrane viscosity through its characteristic viscosity-sensitive fluorescence depolarization. A striking feature of our results is that specific agonist binding by the serotonin1A receptor exhibits close correlation with hippocampal membrane viscosity, implying the importance of global membrane properties in receptor function. We envision that our results are important in understanding GPCR regulation by the membrane environment, and is relevant in the context of diseases in which GPCR signaling plays a major role and are characterized by altered membrane fluidity.Abbreviations: 2-AS, 2-(9-anthroyloxy)stearic acid; 12-AS, 12-(9-anthroyloxy)stearic acid; BODIPY, 4,4-difluoro-4-bora-3a,4a-diaza-s-indacene; GPCR, G protein-coupled receptor; 8-12-PC, 1-palmitoyl-2-(12-doxyl)stearoyl-sn-glycero-3-phosphocholine; DMPC, 1,2-dimyristoyl-sn-glycero-3-phosphocholine; DOPC, 1,2-dioleoylsn-glycero-3-phosphocholine; MβCD, methyl-β-cyclodextrin; Tempo-PC, 1,2-dioleoyl-snglycero-3-phosphotempocholine Keywords: Molecular rotor; hippocampal membrane; viscosity; cholesterol; neuronal receptor IntroductionBiological membranes are complex, highly organized, two-dimensional, supramolecular assemblies of a diverse variety of lipids and proteins. The function of membranes is to allow cellular compartmentalization, and impart an identity to individual cells and organelles, besides providing an appropriate environment for proper functioning of membrane proteins. Interestingly, cellular membranes in the nervous system are characterized by very high concentration and remarkable diversity of lipids, and these are correlated with increased complexity in the function of the nervous system (Sastry, 1985;Wenk, 2005). In this context, cholesterol represents an important lipid since brain cholesterol has been implicated in a number of neurological disorders (Chattopadhyay and Paila, 2007;Martín et al., 2014), some of which share a common etiology of defective cholesterol 4 metabolism in the brain (Porter and Herman, 2011). More importantly, the function of neuronal receptors depends on cholesterol (Pucadyil and Chattopadhyay, 2006;Allen et al., 2007;Paila and Chattopadhyay, 2010;Jafurulla and Chattopadhyay, 2013), which affects neurotransmission, resulting in mood and anxiety disorders (Papakostas et al., 2004). In spite of ...

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Section: Resultsmentioning

confidence: 69%

Molecular rheology of neuronal membranes explored using a molecular rotor: Implications for receptor function

Pal

Chakraborty

Bandari

et al. 2016

Chemistry and Physics of Lipids

Self Cite

View full text Add to dashboard Cite

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“…important as the transmembrane potential particularly as this may 259 also include aspects of molecular stereospecificity in their properties 260 as reported by Bandari et al[5]. This latter work was relatively recent 261 but promises to be very important in our understanding of membrane 262 function.263 6.…”

mentioning

confidence: 82%

“…It's 422 worth emphasising some recent work from the group of Chattopadhyay 423 (see[5]), however as they offer some exciting evidence of the possibility424 that chiral selective interactions based on different optical isomers. This is 425 could be enormously important as it may offer a profound change in our 426 understanding of the nature of many types of lipid-protein interactions 427 associated with the membrane dipole potential.428 10.…”

mentioning

confidence: 98%

The electrical interplay between proteins and lipids in membranes

Richens

Lane

Bramble

et al. 2015

Biochimica et Biophysica Acta (BBA) - Biomembranes

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All molecular interactions that are relevant to cellular and molecular structures are electrical in nature but manifest in a rich variety of forms that each has its own range and influences on the net effect of how molecular species interact. This article outlines how electrical interactions between the protein and lipid membrane components underlie many of the activities of membrane function. Particular emphasis is placed on spatially localised behaviour in membranes involving modulation of protein activity and microdomain structure. The interactions between membrane lipids and membrane proteins together with their role within cell biology represent an enormous body of work. Broad conclusions are not easy given the complexities of the various systems and even consensus with model membrane systems containing two or three lipid types is difficult. By defining two types of broad lipid-protein interaction, respectively Type I as specific and Type II as more non-specific and focussing on the electrical interactions mostly in the extra-membrane regions it is possible to assemble broad rules or a consensus of the dominant features of the interplay between these two fundamentally important classes of membrane component. This article is part of a special issue entitled: Lipid-protein interactions.

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“…2B). Likewise, the probe di-8-ANEPPS, is known to undergo shift in the fluorescence excitation spectrum in linear response to dipole potential changes in the lipid environment, which in turn, is dependent on the electric field in the membrane environment (16)(17)(18). The dipole potential originates from the nonrandom arrangement of molecular dipoles (i.e., water, carbonyl-groups and lipid head-groups) at the membrane interface (19).…”

Section: Bacterial Membrane Vesicle (Mv) Fusion Increases the Fluiditmentioning

confidence: 99%

Lipid Specificity of the Fusion of Bacterial Extracellular Vesicles with the Host Membrane

Prince

Tiwari

Mandal

et al. 2019

Preprint

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Bacterial membrane vesicles (MVs) facilitate long-distance delivery of virulence factors crucial for pathogenicity. The entry and trafficking mechanisms of virulence factors inside host cells is recently emerging, however, if bacterial MVs modulate the physicochemical properties of the host lipid membrane remains unknown. Here we quantitatively show that bacterial MV interaction increases the fluidity, dipole potential and elasticity of a biologically relevant multi-component host model membrane. The presence of lipids containing head-groups such as phosphatidylcholine, phosphatidylglycerol and phosphatidylinositol and a moderate acyl chain length of C16 helps the MV interaction. While significant binding of bacterial MVs to the raft-like lipid membranes with phase separated regions of the membrane was observed, however, the elevated levels of cholesterol tend to hinder the interaction of bacterial MVs. We further quantify the change in excess Gibbs free energy of mixing of bacterial MVs with host lipid membranes driving the modulation of host membrane parameters.

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Membrane dipole potential is sensitive to cholesterol stereospecificity: Implications for receptor function

Cited by 38 publications

References 49 publications

Molecular rheology of neuronal membranes explored using a molecular rotor: Implications for receptor function

Molecular rheology of neuronal membranes explored using a molecular rotor: Implications for receptor function

The electrical interplay between proteins and lipids in membranes

Lipid Specificity of the Fusion of Bacterial Extracellular Vesicles with the Host Membrane

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