Molecular force transduction by ion channels – diversity and unifying principles

Abstract

SummaryCells perceive force through a variety of molecular sensors, of which the mechanosensitive ion channels are the most efficient and act the fastest. These channels apparently evolved to prevent osmotic lysis of the cell as a result of metabolite accumulation and/or external changes in osmolarity. From this simple beginning, nature developed specific mechanosensitive enzymes that allow us to hear, maintain balance, feel touch and regulate many systemic variables, such as blood pressure. For a channel to be mechanosensitive it needs to respond to mechanical stresses by changing its shape between the closed and open states. In that way, forces within the lipid bilayer or within a protein link can do work on the channel and stabilize its state. Ion channels have the highest turnover rates of all enzymes, and they can act as both sensors and effectors, providing the necessary fluxes to relieve osmotic pressure, shift the membrane potential or initiate chemical signaling. In this Commentary, we focus on the common mechanisms by which mechanical forces and the local environment can regulate membrane protein structure, and more specifically, mechanosensitive ion channels.

Piezo Proteins: Regulators of Mechanosensation and Other Cellular Processes

“…In proteoliposomes, Piezo1 conducts K ϩ and Na ϩ without preference, but whether purified Piezo1 conducts divalent ions and/or retains mechanosensitivity is unclear (3). Perhaps mechanosensitivity depends on the interaction with a regulator protein, such as stomatin-like protein 3 (STOML3), which interacts with both Piezo1 and Piezo2 and positively regulates channel activity (12), or it could be an intrinsic property of the channel, similar to that reported for the bacterial mechanogated channels MscS and MscL (29) and the eukaryotic twopore potassium channels of the TREK group (30,31). When compared side-by-side, Piezo1 activation requires a similar change in membrane tension as MscL (13), suggesting that lipid tension alone is, in principle, sufficient to gate Piezo1.…”

Genome-wide identification of MscS like gene family in Cicer arietinum using bioinformatics approach

“…MscS or MSL gene families are a group of membrane proteins that are capable of responding to membrane stimuli including touch, gravity, osmotic pressure and stress (Fasano et al, 2002;Edwards et al, 2012). They are also known as mechanosensitive ion channels or stress-gated ion channels (Sukharev and Sachs 2012;Gottlieb and Sachs 2012). In addition to the mechanical stimuli, they also respond to development process signals such as lateral roots development, damages to the cell wall, pollen tube development and plant-pathogen interactions (Anishkin and Sukharev 2009; Cox et al, 2015).…”

The Arabidopsis Synaptotagmin1 Is Enriched in Endoplasmic Reticulum-Plasma Membrane Contact Sites and Confers Cellular Resistance to Mechanical Stresses

“…Currently, two nonmutually exclusive mechanosensing models, namely, the ion channel and the tensegrity models, coexist in the plant literature. In the ion channel model, plant homologs of the bacterial mechanosensitive channel of small conductance and putative stretch-activated Ca 2+ -permeable channels are gated in response to mechanical forces and trigger a signaling cascade through the rapid influx of extracellular Ca 2+ toward the cytosol (Arnadóttir and Chalfie, 2010;Jensen and Haswell, 2012;Sukharev and Sachs, 2012;Kurusu et al, 2013). In the tensegrity model, plant cells operate as selfsupporting structures stabilized by a dynamic prestress state in which all elements are in isometric tension (Fuller, 1961).…”