Transient Receptor Potential Channels in Mechanosensing and Cell Volume Regulation

doi:10.1016/S0076-6879(07)28010-3

Methods in Enzymology

Volume 428, 2007, Pages 183-207

https://doi.org/10.1016/S0076-6879(07)28010-3 Get rights and content

Abstract

Transient receptor potential (TRP) channels are unique cellular sensors responding to a wide variety of extra‐ and intracellular signals, including mechanical and osmotic stress. In recent years, TRP channels from multiple subfamilies have been added to the list of mechano‐ and/or osmosensitive channels, and it is becoming increasingly apparent that Ca²⁺ influx via TRP channels plays a crucial role in the response to mechanical and osmotic perturbations in a wide range of cell types. Although the events translating mechanical and osmotic stimuli into regulation of TRP channels are still incompletely understood, the specific mechanisms employed vary between different TRP isoforms, and probably include changes in the tension and/or curvature of the lipid bilayer, changes in the cortical cytoskeleton, and signaling events such as lipid metabolism and protein phosphorylation/dephosphorylation. This chapter describes candidate mechanosensitive channels from mammalian TRP subfamilies, discusses inherent and technical issues potentially confounding evaluation of mechano‐ and/or osmosensitivity, and presents methods relevant to the study of TRP channel regulation by mechanical and osmotic stimuli and involvement in cell volume regulation.

Section snippets

INTRODUCTION

Transient receptor potential (TRP) channels are unique cellular sensors, the important roles of which include the detection of mechanical forces and of changes in cell volume or intra‐ or extracellular osmolarity. Based on sequence homology, mammalian TRP channels are divided into six subfamilies: TRPC (canonical), TRPV (vanilloid), TRPM (melastatin), TRPP (polycystin), TRPML (mucolipin), and TRPA (ankyrin). Most TRPs are polymodal channels activated by multiple physical and chemical stimuli

GENERAL MECHANISMS OF MECHANO‐ OR OSMOSENSING BY MEMBRANE PROTEINS

Membrane transport proteins appear to sense mechanical forces and/or changes in osmolarity by a number of fundamental mechanisms. These are outlined in Fig. 10.1 and discussed later, focusing on the mechanisms relevant to ion channels in general and TRP channels in particular (for reviews on general mechanisms of mechanotransduction, see Hamill and Martinac, 2001, Kung, 2005, Nicolson, 2005, Perozo 2006). Any channel embedded in a lipid bilayer is exposed to negative and positive pressures

TRP CHANNELS IN MECHANO‐ AND OSMOSENSING

The ability of cells to sense mechanical stimuli is fundamental to such essential physiological functions as embryonic development, hearing, touch sensitivity, and control of kidney function, vascular tone, and muscle stretch (see, e.g., Hamill and Martinac, 2001, Kung, 2005). Multiple TRP channels from various subfamilies have been shown to be sensitive to various forms of mechanical stress, including fluid shear stress, and increased membrane tension resulting from membrane stretch (Liedtke

TRP CHANNELS IN CELL VOLUME REGULATION

Cell volume perturbations occur under physiological and pathophysiological conditions in a wide range of cell types, and the ability to regulate cell volume is fundamental to cell function and survival. Following osmotic cell shrinkage or swelling, most cell types are able to regulate their volume in processes termed regulatory volume increase or regulatory volume decrease (RVD), respectively (Hoffmann and Pedersen, 2006, Lang et al., 1998). Obviously, to establish that a given channel actually

EXPERIMENTAL PROCEDURES

This section describes the foundations and practical procedures for selected methods useful in the evaluation of mechano‐ and osmosensitivity, as well as of transporter effects on [Ca²⁺]_i cell volume. Standard patch clamp procedures have been described extensively elsewhere (see, e.g., Hille, 2001, Sakmann and Neher, 1995) and are not detailed here.

ACKNOWLEDGMENTS

We thank Dr. Greg Owsianik (Leuven) for his help with Fig. 10.1. Work in the authors' laboratories is supported by the Danish National Research Council (SFP, Grants 21‐04‐0507 and 272‐05‐0305) and Human Frontiers Science Programme (HFSP Research Grant Ref. RGP 32/2004), the Belgian Federal Government, the Flemish Government, and the Onderzoeksraad KU Leuven (GOA 2004/07, F.W.O. G. 0136.00; F.W.O. G.0172.03, Interuniversity Poles of Attraction Program, Prime Ministers Office IUAP Nr.3P4/23,

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Squishy matters – Corneal mechanobiology in health and disease
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The cornea, as a dynamic and responsive tissue, constantly interacts with mechanical forces in order to maintain its structural integrity, barrier function, transparency and refractive power. Cells within the cornea sense and respond to various mechanical forces that fundamentally regulate their morphology and fate in development, homeostasis and pathophysiology. Corneal cells also dynamically regulate their extracellular matrix (ECM) with ensuing cell-ECM crosstalk as the matrix serves as a dynamic signaling reservoir providing biophysical and biochemical cues to corneal cells. Here we provide an overview of mechanotransduction signaling pathways then delve into the recent advances in corneal mechanobiology, focusing on the interplay between mechanical forces and responses of the corneal epithelial, stromal, and endothelial cells. We also identify species-specific differences in corneal biomechanics and mechanotransduction to facilitate identification of optimal animal models to study corneal wound healing, disease, and novel therapeutic interventions. Finally, we identify key knowledge gaps and therapeutic opportunities in corneal mechanobiology that are pressing for the research community to address especially pertinent within the domains of limbal stem cell deficiency, keratoconus and Fuchs’ endothelial corneal dystrophy. By furthering our understanding corneal mechanobiology, we can contextualize discoveries regarding corneal diseases as well as innovative treatments for them.
PIEZO channels and newcomers in the mammalian mechanosensitive ion channel family
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Citation Excerpt :
Although MS ion channels appeared very early during evolution (Cox et al., 2018), the lack of sequence conservation between procaryotes and eucaryotes has delayed the discovery of the channels responsible for mechanotransduction in animal kingdom (Arnadóttir and Chalfie, 2010; Chalfie, 2009; Gillespie and Walker, 2001; Hamill and Martinac, 2001; Kung, 2005; Ranade et al., 2015; Sukharev and Sachs, 2012). Several MS ion channels have been identified in the past, ranging from the two-pore domain potassium channels (K2P) to the non-selective cation channels from the transient receptor potential (TRP) channel family (Al-Sheikh and Kang, 2020a, 2020b; Brohawn et al., 2014a, 2014b; Douguet and Honoré, 2019; Liedtke et al., 2000; Liedtke, 2006; Pedersen and Nilius, 2007). Among TRP channels, NompC/TRPN (NO Mechanoreceptor Potential C) has been demonstrated fulfilling the criteria of being a MS ion channel involved in a variety of mechanosensation-related behaviors such as locomotion, touch, and sound across different species, including C. elegans, Drosophila, and zebrafish (Jin et al., 2017; Yan et al., 2013; Zhang et al., 2015), as well as touch-taste sensation in Octopus (van Giesen et al., 2020).
Many ion channels have been described as mechanosensitive according to various criteria. Most broadly defined, an ion channel is called mechanosensitive if its activity is controlled by application of a physical force. The last decade has witnessed a revolution in mechanosensory physiology at the molecular, cellular, and system levels, both in health and in diseases. Since the discovery of the PIEZO proteins as prototypical mechanosensitive channel, many proteins have been proposed to transduce mechanosensory information in mammals. However, few of these newly identified candidates have all the attributes of bona fide, pore-forming mechanosensitive ion channels. In this perspective, we will cover and discuss new data that have advanced our understanding of mechanosensation at the molecular level.
TRPV2 channel inhibitors attenuate fibroblast differentiation and contraction mediated by keratinocyte-derived TGF-β1 in an in vitro wound healing model of rats
2018, Journal of Dermatological Science
Keratinocytes release several factors that are involved in wound contracture and scar formation. We previously reported that a three-dimensional reconstruction model derived from rat skin represents a good wound healing model.
We characterized the role of transient receptor potential (TRP) channels in the release of transforming growth factor (TGF)-β1 from keratinocytes and the differentiation of fibroblasts to identify possible promising pharmacological approaches to prevent scar formation and contractures.
The three-dimensional culture model was made from rat keratinocytes seeded on a collagen gel in which dermal fibroblasts had been embedded.
Among the TRP channel inhibitors tested, the TRPV2 inhibitors SKF96365 and tranilast attenuated most potently keratinocyte-dependent and — independent collagen gel contraction due to TGF-β signaling as well as TGF-β1 release from keratinocytes and α-smooth muscle actin production in myofibroblasts. Besides the low amounts detected in normal dermis, TRPV2 mRNA and protein levels were increased after fibroblasts were embedded in the gel. TRPV2 was also expressed in the epidermis and keratinocyte layers of the model. Both inhibitors and TRPV2 siRNA attenuated the intracellular increase of Ca²⁺ induced by the TRPV agonist 2-aminoethoxydiphenyl borate in TGF-β1-pretreated fibroblasts.
This is the first study to show that compounds targeting TRPV2 channels ameliorate wound contraction through the inhibition of TGF-β1 release and the differentiation of dermal fibroblasts in a culture model.
The effect of diminished metabolic acidosis on thermoregulatory response during exercise
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Chapter Ten - Transient Receptor Potential Channels in Mechanosensing and Cell Volume Regulation

Abstract

Section snippets

INTRODUCTION

GENERAL MECHANISMS OF MECHANO‐ OR OSMOSENSING BY MEMBRANE PROTEINS

TRP CHANNELS IN MECHANO‐ AND OSMOSENSING

TRP CHANNELS IN CELL VOLUME REGULATION

EXPERIMENTAL PROCEDURES

ACKNOWLEDGMENTS

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Cell

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Cell. Mol. Life Sci.

J. Biol. Chem.

J. Biol. Chem.

J. Biol. Chem.

Am. J. Physiol.

Biophys. J.

Nat. Neurosci.

J. Physiol. (Lond.)

J. Physiol.

Cell Calcium

Nat. Rev. Mol. Cell Biol.

Annu. Rev. Physiol.

Structure

Nat. Cell Biol.

J. Cell Biol.

Mechanisms of stretch‐induced muscle damage in normal and dystrophic muscle: Role of ionic changes

J. Physiol.

Swelling‐induced arachidonic acid release via the 85‐kDa cPLA2 in human neuroblastoma cells

J. Neurophysiol.

TRPV4 exhibits a functional role in cell‐volume regulation

J. Cell Sci.

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J. Physiol.

A sensor for intracellular ionic strength

Proc. Natl. Acad. Sci. USA

3′ UTR seed matches, but not overall identity, are associated with RNAi off‐targets

Nat. Methods

ERM proteins and merlin: Integrators at the cell cortex

Nat. Rev. Mol. Cell. Biol.

A phospholipid sensor controls mechanogating of the K+ channel TREK‐1

EMBO J.

Evidence that TRPC1 (transient receptor potential canonical 1) forms a Ca2+‐permeable channel linked to the regulation of cell volume in liver cells obtained using small interfering RNA targeted against TRPC1

Biochem. J.

Transient receptor potential vanilloid 1 is required for intrinsic osmoreception in organum vasculosum lamina terminalis neurons and for normal thirst responses to systemic hyperosmolality

J. Neurosci.

TRPV4 and the mammalian kidney

Pflüg. Arch. Eur. J. Physiol.

OSM‐9, a novel protein with structural similarity to channels, is required for olfaction, mechanosensation, and olfactory adaptation in Caenorhabditis elegans

J. Neurosci.

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J. Physiol.

TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells

Nature

PACSINs bind to the TRPV4 cation channel: PACSIN 3 modulates the subcellular localization of TRPV4

J. Biol. Chem.

Internal Ca2+ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue

J. Cell Biol.

Osmotic stress and the cytoskeleton: the R(h)ole of Rho GTPases

Acta Physiol. (Oxf.)

Cation channels of the transient receptor potential superfamily: Their role in physiological and pathophysiological processes of smooth muscle cells

Pharmacol. Ther.

Critical role for transient receptor potential channel TRPM4 in myogenic constriction of cerebral arteries

Circ. Res.

Off‐target effects by siRNA can induce toxic phenotype

RNA

Evidence that the glucose transporter serves as a water channel in J774 macrophages

Proc. Natl. Acad. Sci. USA

Functional role of TRPC proteins in native systems: Implications from knockout and knock‐down studies

J. Physiol.

WNK kinases influence TRPV4 channel function and localization

Am. J. Physiol. Renal Physiol.

A phospholipid sensor controls mechanogating of the K⁺ channel TREK‐1

Evidence that TRPC1 (transient receptor potential canonical 1) forms a Ca²⁺‐permeable channel linked to the regulation of cell volume in liver cells obtained using small interfering RNA targeted against TRPC1

Internal Ca²⁺ release in yeast is triggered by hypertonic shock and mediated by a TRP channel homologue