Evidence for the role of lipid rafts and sphingomyelin in Ca2+-gating of Transient Receptor Potential channels in trigeminal sensory neurons and peripheral nerve terminals

Sághy, Éva; Szöke, Éva; Payrits, Maja; Helyes, Zsuzsanna; Börzsei, Rita; Erostyák, János; Jánosi, Tibor Z.; Sétáló, György; Szolcsányi, Janós

doi:10.1016/j.phrs.2015.07.028

Cited by 85 publications

(105 citation statements)

References 75 publications

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“…Annexin A6 possesses a calcium-dependent membrane-binding domain in its C terminus (Cornely et al, 2011) (Gerke et al, 2005) that interacts with phosphotidylserine groups on the inner plasma membrane, a region rich in cholesterol and termed lipid rafts (Lizarbe et al, 2013). Previous in vitro studies demonstrated Annexin A6 to be a membrane scaffold that links membrane microdomains to the cytoskeleton (Cornely et al, 2011) (Saghy et al, 2015), a likely role that it is also playing in chick sensory neurons given our data. Furthermore, lipid biogenesis plays a key role in the formation of sensory nerves; for example, both rat and mouse trigeminal nerves have axonal membranes enriched in lipid rafts (Benes et al, 1973) (Gnanasekaran et al, 2011).…”

Section: Discussionsupporting

confidence: 64%

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Shah

Schiffmacher

Taneyhill

2017

Developmental Biology

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Cranial sensory ganglia are components of the peripheral nervous system that possess a significant somatosensory role and include neurons within the trigeminal and epibranchial nerve bundles. Although it is well established that these ganglia arise from interactions between neural crest and neurogenic placode cells, the molecular basis of ganglia assembly is still poorly understood. Members of the Annexin protein superfamily play key roles in sensory nervous system development throughout metazoans. Annexin A6 is expressed in chick trigeminal and epibranchial placode cell-derived neuroblasts and neurons, but its function in cranial ganglia formation has not been elucidated. To this end, we interrogated the role of Annexin A6 using gene perturbation studies in the chick embryo. Our data reveal that placode cell-derived neuroblasts with reduced Annexin A6 levels ingress and migrate normally to the ganglionic anlage, where neural crest cell corridors correctly form around them. Strikingly, while Annexin A6-depleted placode cell-derived neurons still express mature neuronal markers, they fail to form two long processes, which are considered morphological features of mature neurons, and no longer innervate their designated targets due to the absence of this bipolar morphology. Moreover, overexpression of Annexin A6 causes some placode cell-derived neurons to form extra protrusions alongside these bipolar processes. These data demonstrate that the molecular program associated with neuronal maturation is distinct from that orchestrating changes in neuronal morphology, and, importantly, reveal Annexin A6 to be a key membrane scaffolding protein during sensory neuron membrane biogenesis. Collectively, our results provide novel insight into mechanisms underscoring morphological changes within placode cell-derived neurons that are essential for cranial gangliogenesis.

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Section: Discussionsupporting

confidence: 64%

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Shah

Schiffmacher

Taneyhill

2017

Developmental Biology

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“…Cholesterol also acts as a negative modulator of TRPM3 suppressing its constitutive and stimulated activity [121]. However, a recent study reported opposite results, with TRPM8 activity reduced after disruption of lipid rafts in trigeminal neurons, and TRPM3 activation not affected by cholesterol depletion [122]. Thus, further studies are needed to clarify whether the discrepancies reported are due to different experimental conditions or determined by the cellular context.…”

Section: Sphingolipids Cholesterol and Steroidsmentioning

confidence: 99%

Lipids as central modulators of sensory TRP channels

Ciardo

Ferrer-Montiel

2017

Biochimica et Biophysica Acta (BBA) - Biomembranes

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The transient receptor potential (TRP) ion channel family is involved in a diversity of physiological processes including sensory and homeostatic functions, as well as muscle contraction and vasomotor control. Their dysfunction contributes to the etiology of several diseases, being validated as therapeutic targets. These ion channels may be activated by physical or chemical stimuli and their function is highly influenced by signaling molecules activated by extracellular signals. Notably, as integral membrane proteins, lipid molecules also modulate their membrane location and function either by direct interaction with the channel structure or by modulating the physico-chemical properties of the cellular membrane. This lipid-based modulatory effect is being considered an alternative and promising approach to regulate TRP channel dysfunction in diseases. Here, we review the current progress in this exciting field highlighting a complex channel regulation by a large diversity of lipid molecules and suggesting some diseases that may benefit from a membrane lipid therapy. This article is part of a Special Issue entitled: Membrane Lipid Therapy: Drugs Targeting Biomembranes edited by Pablo V. Escribá.

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“…This phenomenon allows us to imagine that some interaction between pm‐AuNRs and sugar‐containing molecules anchored to the plasma membrane, e. g., gangliosides, inositol phospholipids, etc., might create conditions favorable for sustained photothermal ion channel activation . In fact, it was recently reported that the activation of the ion channel, transient receptor potential vanilloid type I (TRPV1), was affected by the integrity of lipid rafts, in which some gangliosides are localized . We are now investigating the interaction of pm‐AuNRs with GUVs bearing a lipid raft‐localizing ganglioside.…”

Section: Resultsmentioning

confidence: 99%

Colloidal Stability of Lipid/Protein‐Coated Nanomaterials in Salt and Sucrose Solutions

et al. 2018

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Considering the importance of surface chemistry in the colloidal stabilization of gold nanorods (AuNRs), we designed AuNRs in two physiologically relevant, salt and salt‐free aqueous solutions to validate its role in colloidal stability. Here, we show that AuNRs coated with cationic lipid/lipid‐binding protein composite materials is stable in both phosphate‐buffered saline (PBS) and sucrose solution (200 mM), but not in deionized water. Salting‐in effects of proteins explain the relatively better stability of AuNRs in PBS than in deionized water. Sucrose‐assisted stabilization of the AuNRs was associated with a decrease in their zeta potential and tended to diminish without the cationic lipid, which would be attributed to an electrostatic interaction between sucrose and the cationic lipid. Given that sucrose solution is often used for cell‐sized liposome studies, our finding will enable nanomaterial‐membrane interaction analyses in live cell and cell‐free systems with identical nanomaterials.

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Evidence for the role of lipid rafts and sphingomyelin in Ca2+-gating of Transient Receptor Potential channels in trigeminal sensory neurons and peripheral nerve terminals

Cited by 85 publications

References 75 publications

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Annexin A6 controls neuronal membrane dynamics throughout chick cranial sensory gangliogenesis

Lipids as central modulators of sensory TRP channels

Colloidal Stability of Lipid/Protein‐Coated Nanomaterials in Salt and Sucrose Solutions

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