Cellular mechanosensing of texture features

The ways that cells feel and then enable us to do the same is important for everything from the earliest stages of development all the way through the selection of the right sweater for an interview. At the level of individual cells, a range of mechanisms exist that underlie sensing and responsiveness to mechanical signals, and these regulate a whole spectrum of physiological and pathological processes. Even stem cells that have yet to differentiate into a specific cell type feel their environment and choose different lineages in part according to what they feel, including substrate stiffness (1). This can go horribly wrong in cancer cells that undergo an epithelial-mesenchymal transition when sensing the stiffening tumor environment and, thereby, prime themselves for invasion and metastasis (2). For multicellular sensing, somatosensory neurons decode texture features by converting compression into action potentials that propagate through the body (3). These cellular mechanosensing phenomena all arise from a similar conserved mechanosensory machinery at the subcellular level that affects the membrane, cytoskeleton, and nucleus. Mechanosensitive transmembrane proteins, including binding receptors (e.g., integrin (4), cadherin (5)) and ion channels (6), integrate and transduce forces into biochemical signaling, which all contribute to cell sensing.

Among these components in the mechanosensitive machinery, mechanosensitive membrane proteins play essential roles. For example, cell-extracelluclar matrix interactions based on integrins determine the direction of durotaxis based on motor-clutch machinery that integrates mechanical stimuli with target stiffnesses for a cell (7). Memory about the cell microenvironment transduced through integrins is retained within cells, with cadherin antagonizing integrin and erasing cell memory (5). For multicellular organisms like us, feeling and memory comes more from mechanosensitive ion channels (e.g., piezo family, DEG/ENaC, transient receptor potential ion channels) in sensory cells (e.g., auditory receptor cells, hair cells, somatosensory neurons), which respond to forces such as vibration and stretch and provide us our rich sensory world (6). Mechanotransduction assays (e.g., immunofluorescence, atomic force microscopy, patch clamp, elastomeric pillars) are plentiful for monitoring such dynamic cellular behaviors, but there is still a lack of integrative understanding of how these factors combine to enable macroscale mechanosensing.

In this issue of Biophysical Journal, Mao et al. advance this field by providing an exciting mathematical model for cellular mechanosensing during texture perception (8). The model proposes that sensory cells transform texture patterns into action potentials through mechanically activated ion channels that interact with the periodicity of the roughness of surfaces that we touch (Fig. 1). Based on the model, mechanosensitive ion channels can be grouped functionally into slowly adapting channels and rapidly adapting channels, which play distinct roles in texture perception. Rapidly adapting channels sense dynamic sliding, while slowly adapting channels sense static touch, so that as a finger slides on a periodically textured surface, only textures with wavelengths within a limited range can be decoded into our temporal firing patterns. This tradeoff between texture wavelength, contact force, ion channel time constants, and touching speed provides a foundation for understanding our ranges of perception and constitutes a framework for learning much about how we feel.

Figure 1.

When a finger slides on a textured surface, the compression could be transferred to stress on the ion channels on somatosensory neurons, which generates action potentials and the tactile sensation

This is an exciting advance. Before Mao’s work (8), tactile signaling had only been studied at the level of afferent fibers, without extension to the cellular level (9). Mao et al. now contribute to the field with a cellular-level understanding of how tactile signals generated from different texture features arise and with an elegant theoretical model that enables us to predict how sensory cells translate mechanical stimuli into electrical signals, a powerful tool for investigating texture perception. With this tool in hand, ideas such as electronic skin and realistic haptic interfaces are now a step closer. However, the understanding of tactile sensation is far from conclusive. Tactile sensation includes a complex interplay between biomechanics, transduction channels, and neuronal biophysics. Although learning how these elements cooperate to achieve elaborate touch sensation needs further investigation, we now have a solid theoretical foundation to work from.

Editor: Guy Genin.