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

Abstract Previous work identified nociceptive Schwann cells that can initiate pain. Consistent with the existence of inherently mechanosensitive sensory Schwann cells, we found that in mice, the mechanosensory function of almost all nociceptors, including those signaling fast pain, were dependent on...

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Main Authors: Julia Ojeda-Alonso, Laura Calvo-Enrique, Ricardo Paricio-Montesinos, Rakesh Kumar, Ming-Dong Zhang, James F. A. Poulet, Patrik Ernfors, Gary R. Lewin
Format: Article
Language:English
Published: Nature Portfolio 2024-02-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-44845-8
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author Julia Ojeda-Alonso
Laura Calvo-Enrique
Ricardo Paricio-Montesinos
Rakesh Kumar
Ming-Dong Zhang
James F. A. Poulet
Patrik Ernfors
Gary R. Lewin
author_facet Julia Ojeda-Alonso
Laura Calvo-Enrique
Ricardo Paricio-Montesinos
Rakesh Kumar
Ming-Dong Zhang
James F. A. Poulet
Patrik Ernfors
Gary R. Lewin
author_sort Julia Ojeda-Alonso
collection DOAJ
description Abstract Previous work identified nociceptive Schwann cells that can initiate pain. Consistent with the existence of inherently mechanosensitive sensory Schwann cells, we found that in mice, the mechanosensory function of almost all nociceptors, including those signaling fast pain, were dependent on sensory Schwann cells. In polymodal nociceptors, sensory Schwann cells signal mechanical, but not cold or heat pain. Terminal Schwann cells also surround mechanoreceptor nerve-endings within the Meissner’s corpuscle and in hair follicle lanceolate endings that both signal vibrotactile touch. Within Meissner´s corpuscles, two molecularly and functionally distinct sensory Schwann cells positive for Sox10 and Sox2 differentially modulate rapidly adapting mechanoreceptor function. Using optogenetics we show that Meissner’s corpuscle Schwann cells are necessary for the perception of low threshold vibrotactile stimuli. These results show that sensory Schwann cells within diverse glio-neural mechanosensory end-organs are sensors for mechanical pain as well as necessary for touch perception.
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spelling doaj.art-ee91562559af4c1c81fde4fe01d888242024-03-05T19:43:07ZengNature PortfolioNature Communications2041-17232024-02-0115111410.1038/s41467-024-44845-8Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociceptionJulia Ojeda-Alonso0Laura Calvo-Enrique1Ricardo Paricio-Montesinos2Rakesh Kumar3Ming-Dong Zhang4James F. A. Poulet5Patrik Ernfors6Gary R. Lewin7Molecular Physiology of Somatic Sensation, Max Delbrück Center for Molecular MedicineDepartment of Medical Biochemistry and Biophysics, Division of Molecular Neurobiology, Karolinska InstitutetNeural Circuits and Behavior, Max Delbrück Center for Molecular MedicineDepartment of Medical Biochemistry and Biophysics, Division of Molecular Neurobiology, Karolinska InstitutetDepartment of Medical Biochemistry and Biophysics, Division of Molecular Neurobiology, Karolinska InstitutetNeural Circuits and Behavior, Max Delbrück Center for Molecular MedicineDepartment of Medical Biochemistry and Biophysics, Division of Molecular Neurobiology, Karolinska InstitutetMolecular Physiology of Somatic Sensation, Max Delbrück Center for Molecular MedicineAbstract Previous work identified nociceptive Schwann cells that can initiate pain. Consistent with the existence of inherently mechanosensitive sensory Schwann cells, we found that in mice, the mechanosensory function of almost all nociceptors, including those signaling fast pain, were dependent on sensory Schwann cells. In polymodal nociceptors, sensory Schwann cells signal mechanical, but not cold or heat pain. Terminal Schwann cells also surround mechanoreceptor nerve-endings within the Meissner’s corpuscle and in hair follicle lanceolate endings that both signal vibrotactile touch. Within Meissner´s corpuscles, two molecularly and functionally distinct sensory Schwann cells positive for Sox10 and Sox2 differentially modulate rapidly adapting mechanoreceptor function. Using optogenetics we show that Meissner’s corpuscle Schwann cells are necessary for the perception of low threshold vibrotactile stimuli. These results show that sensory Schwann cells within diverse glio-neural mechanosensory end-organs are sensors for mechanical pain as well as necessary for touch perception.https://doi.org/10.1038/s41467-024-44845-8
spellingShingle Julia Ojeda-Alonso
Laura Calvo-Enrique
Ricardo Paricio-Montesinos
Rakesh Kumar
Ming-Dong Zhang
James F. A. Poulet
Patrik Ernfors
Gary R. Lewin
Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
Nature Communications
title Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
title_full Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
title_fullStr Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
title_full_unstemmed Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
title_short Sensory Schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
title_sort sensory schwann cells set perceptual thresholds for touch and selectively regulate mechanical nociception
url https://doi.org/10.1038/s41467-024-44845-8
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