Lamellar cells in Pacinian and Meissner corpuscles are touch sensors

Nikolaev, Yu. A.; Feketa, Viktor V.; Anderson, Evan O.; Schneider, Eve R.; Gracheva, Elena O.; Bagriantsev, Sviatoslav N.

doi:10.1126/sciadv.abe6393

Cited by 37 publications

(63 citation statements)

References 52 publications

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“…2). Despite functional diversity of sensory Schwann cells they possess one common feature which is their selective involvement in the transduction of mechanical stimuli, a feature that appears to be evolutionarily conserved 27 . Thus, we show that polymodal nociceptors require nociceptor Schwann cells for their mechanosensitivity, but not thermosensitivity.…”

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confidence: 99%

Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception

Ojeda-Alonso

Calvo-Enrique

Paricio-Montesinos

et al. 2022

Preprint

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That sensory neurons alone transduce mechanical stimuli was challenged by the discovery of nociceptive Schwann cells that can initiate pain. Consistent with the existence of inherently mechanosensitive sensory Schwann cells, we found that mechanosensory function of almost all nociceptors, including those signaling fast pain were critically dependent on sensory Schwann cells. Furthermore, in polymodal nociceptors, sensory Schwann cells signal mechanical, but not cold or heat pain. Terminal Schwann cells also surround mechanoreceptor nerve-endings forming Meissners corpuscles that signal vibrotactile touch, raising the possibility that touch sensation is also dependent on such cells. Using optogenetics we show that Meissner`s corpuscle Schwann cells are necessary for the detection and perception of vibrotactile stimuli. Our results show that sensory Schwann cells within diverse glio-neural mechanosensory end-organs are sensors for mechanical pain as well as touch perception. These results place specialized sensory Schwann cells at the center of somatic sensation to all types of mechanical stimuli.

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mentioning

confidence: 99%

Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception

Ojeda-Alonso

Calvo-Enrique

Paricio-Montesinos

et al. 2022

Preprint

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“…Thus, recently identified specialized Schwann cells that surround the peripheral endings of unmyelinated nociceptors may directly participate in the detection of noxious mechanical stimuli (Abdo et al, 2019). In addition, cells that form specialized sensory end-organs innervated by mechanoreceptors in birds were also recently shown to be mechanosensitive (Nikolaev et al, 2020). Using our global Tmem150c -/- mutant mice we wished to test whether loss of the TMEM150c protein had an impact on the mechanosensitive properties on functionally identified sensory neurons using ex vivo skin nerve preparations.…”

Section: Discussionmentioning

confidence: 99%

Lack of evidence for participation of TMEM150c/TENTONIN3 in sensory mechanotransduction

Ojeda-Alonso

Bégay

Garcia-Contreras

et al. 2022

Preprint

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The membrane protein TMEM150c has been proposed to form a mechanosensitive ion channel that is required for normal proprioceptor function. Here we examined whether expression of TMEM150c in neuroblastoma cells lacking Piezo1 is associated with the appearance of mechanosensitive currents. Using three different modes of mechanical stimuli, indentation, membrane stretch and substrate deflection we could not evoke mechanosensitive currents in cells expressing TMEM150c. We next asked if TMEM150c is necessary for the normal mechanosensitivity of cutaneous sensory neurons. We used an available mouse model in which the Tmem150c locus was disrupted through the insertion of a LacZ cassette with a splice acceptor that should lead to transcript truncation. Analysis of these mice indicated that ablation of the Tmem150c gene was not complete in sensory neurons of the dorsal root ganglia (DRG). Using a Crispr/cas9 strategy we made a second mouse model in which a large part of the Tmem150c gene was deleted and established that these Tmem150c-/- mice completely lack TMEM150c protein in the DRGs. We used an ex vivo skin nerve preparation to characterize the mechanosenstivity of mechanoreceptors and nociceptors in the glabrous skin of the Tmem150c-/- mice. We found no quantitative alterations in the physiological properties of any type of cutaneous sensory fiber in Tmem150c-/- mice. Since it has been claimed that TMEM150c is required for normal proprioceptor function we made a quantitative analysis of locomotion in Tmem150c-/- mice. Here again we found no indication that there was altered gait in Tmem150c-/- mice compared to wild type controls. In summary, we conclude that existing mouse models that have been used to investigate TMEM150c function in vivo are problematic. Furthermore, we could find no evidence that TMEM150c forms a mechanosensitive channel or that it is necessary for the normal mechanosensitivity of cutaneous sensory neurons.

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“…Nearly all TRP (transient receptor potential) families of ion channels have members with potential mechanosensory capacities ( Clapham et al, 2005 ; Samanta et al, 2018 ). Nevertheless, it has not been established whether these ion channels are mechanosensors or participate only when required for mechanosensation since some of them are insensitive to membrane stretch [see ( Nikolaev et al, 2020 )]. As far as we know, TRPV4 (vanilloid 4) is the only member of the TRP superfamily that has been detected in the lamellar cells of human digital Meissner ( Alonso-González et al, 2016 ).…”

Section: The Role Of the Lamellar Cells In Mechanotransductionmentioning

confidence: 99%

“…The most overwhelming putative role of lamellar cells in mechanosensation was provided recently by Nikolaev et al (2020) . They observed that the lamellar cells of Grandry’s corpuscles (assimilated to the lamellar cells within Meissner corpuscles) from duck bill skin detect tactile stimuli, thus, suggesting that also lamellar cells are touch sensors.…”

Section: The Role Of the Lamellar Cells In Mechanotransductionmentioning

confidence: 99%

The Lamellar Cells of Vertebrate Meissner and Pacinian Corpuscles: Development, Characterization, and Functions

et al. 2022

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Sensory corpuscles, or cutaneous end-organ complexes, are complex structures localized at the periphery of Aβ-axon terminals from primary sensory neurons that primarily work as low-threshold mechanoreceptors. Structurally, they consist, in addition to the axons, of non-myelinating Schwann-like cells (terminal glial cells) and endoneurial- and perineurial-related cells. The terminal glial cells are the so-called lamellar cells in Meissner and Pacinian corpuscles. Lamellar cells are variably arranged in sensory corpuscles as a “coin stack” in the Meissner corpuscles or as an “onion bulb” in the Pacinian ones. Nevertheless, the origin and protein profile of the lamellar cells in both morphotypes of sensory corpuscles is quite similar, although it differs in the expression of mechano-gated ion channels as well as in the composition of the extracellular matrix between the cells. The lamellar cells have been regarded as supportive cells playing a passive role in the process of genesis of the action potential, i.e., the mechanotransduction process. However, they express ion channels related to the mechano–electric transduction and show a synapse-like mechanism that suggest neurotransmission at the genesis of the electrical action potential. This review updates the current knowledge about the embryonic origin, development modifications, spatial arrangement, ultrastructural characteristics, and protein profile of the lamellar cells of cutaneous end-organ complexes focusing on Meissner and Pacinian morphotypes.

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Lamellar cells in Pacinian and Meissner corpuscles are touch sensors

Cited by 37 publications

References 52 publications

Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception

Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception

Lack of evidence for participation of TMEM150c/TENTONIN3 in sensory mechanotransduction

The Lamellar Cells of Vertebrate Meissner and Pacinian Corpuscles: Development, Characterization, and Functions

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