3D architecture and a bicellular mechanism of touch detection in mechanosensory corpuscle

Nikolaev, Yury A.; Ziolkowski, Luke H.; Pang, Song; Li, Wei-Ping; Feketa, Viktor V.; Xu, C. Shan; Gracheva, Elena O.; Bagriantsev, Sviatoslav N.

doi:10.1126/sciadv.adi4147

Cited by 4 publications

(1 citation statement)

References 40 publications

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“…[242,312] Some ion channels such as Piezo1/2, transient receptor potential vanilloid 4 (TRPV4), TRPC, TACAN, and SWELL1, can transform their conformations under forces to facilitate ion influx and intracellular biochemical signals. [313] Particularly, Piezo1/2 are gaining the most investigations due to their versatile roles in many processes, [206] including immune response, [176] touch sensation, [314] cognitive functions, [315] gastrointestinal movements, [316] tendon adaptation to physical burden, [317] flow-induced vasodilation, [91] urination control of bladder, [318] and antigenic function of erythrocyte [319] (Figure 7). Mechanistically, it is now increasingly approved that forces from plasma membrane may directly open the Piezo 1 channel, [320,321] despite that forces from cytoskeleton and adhesions might contribute to this process.…”

Section: Other Molecular and Subcellular Mechanotransductionmentioning

confidence: 99%

A Hierarchical Mechanotransduction System: From Macro to Micro

Cao,

Tian,

Tian

et al. 2023

Advanced Science

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Mechanotransduction is a strictly regulated process whereby mechanical stimuli, including mechanical forces and properties, are sensed and translated into biochemical signals. Increasing data demonstrate that mechanotransduction is crucial for regulating macroscopic and microscopic dynamics and functionalities. However, the actions and mechanisms of mechanotransduction across multiple hierarchies, from molecules, subcellular structures, cells, tissues/organs, to the whole‐body level, have not been yet comprehensively documented. Herein, the biological roles and operational mechanisms of mechanotransduction from macro to micro are revisited, with a focus on the orchestrations across diverse hierarchies. The implications, applications, and challenges of mechanotransduction in human diseases are also summarized and discussed. Together, this knowledge from a hierarchical perspective has the potential to refresh insights into mechanotransduction regulation and disease pathogenesis and therapy, and ultimately revolutionize the prevention, diagnosis, and treatment of human diseases.

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Section: Other Molecular and Subcellular Mechanotransductionmentioning

confidence: 99%

A Hierarchical Mechanotransduction System: From Macro to Micro

Cao,

Tian,

Tian

et al. 2023

Advanced Science

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Structural and functional dissection of the Pacinian corpuscle reveals an active role of the inner core in touch detection

Ziolkowski,

Nikolaev,

Chikamoto

et al. 2024

Preprint

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SummaryPacinian corpuscles are rapidly adapting mechanoreceptor end-organs that detect transient touch and high-frequency vibration. In the prevailing model, these properties are determined by the outer core, which acts as a mechanical filter limiting static and low-frequency stimuli from reaching the afferent terminal—the sole site of touch detection in corpuscles. Here, we determine the detailed 3D architecture of corpuscular components and reveal their contribution to touch detection. We show that the outer core is dispensable for rapid adaptation and frequency tuning. Instead, these properties arise from the inner core, composed of gap junction-coupled lamellar Schwann cells (LSCs) surrounding the afferent terminal. By acting as additional touch sensing structures, LSCs potentiate mechanosensitivity of the terminal, which detects touch via fast-inactivating ion channels. We propose a model in which Pacinian corpuscle function is mediated by an interplay between mechanosensitive LSCs and the afferent terminal in the inner core.HighlightseFIB-SEM reveals detailed 3D architecture of the entire Pacinian (Herbst) corpuscleInner, not outer core mediates rapid adaptation and frequency tuningAfferent terminal detects touch via fast-inactivating ion channelsMechanosensitive lamellar Schwann cells tune afferent terminal sensitivity to touch

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Periarticular Proprioception: Analyzing the Three-Dimensional Structure of Corpuscular Mechanosensors in the Dorsal Part of the Scapholunate Ligament

Al Meklef,

Kacza,

Kremer

et al. 2024

Cells Tissues Organs

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Introduction Sensory nerve endings transmit mechanical stimuli into afferent neural signals and form the basis of proprioception, giving rise to the self-perception of dynamic stability of joints. We aimed to analyze the three-dimensional structure of periarticular corpuscular sensory nerve endings in a carpal ligament to enhance our understanding of their microstructure. Methods Two dorsal parts of the scapholunate ligament were excised from two human cadaveric wrist specimens. Consecutive cryosections were stained with immunofluorescence markers protein S100B, neurotrophin receptor p75 (p75), protein gene product 9.5 (PGP 9.5) and 4′ ,6-diamidino-2-phenylindole (DAPI). Three-dimensional images of sensory nerve endings were obtained using confocal laser scanning microscopy and subsequent analysis was performed using Imaris software. Results Ruffini endings were characterized by a PGP 9.5-positive central axon, with a median diameter of 4.63 µm and contained a median of 25 cells. The p75-positive capsule had a range in thickness of 0.94 µm and 15.5 µm, consisting of single to three layers of lamellar cells. Ruffini endings were significantly smaller in volume than Pacini corpuscles or Golgi-like endings. The latter contained a median of three intracorpuscular structures. Ruffini endings and Golgi-like endings presented a similar structural composition of their capsule and subscapular space. The central axon of Pacini corpuscles was surrounded by S100-positive cells forming the inner core which was significantly smaller than the outer core, which was immunoreactive for p75 and PGP 9.5. Conclusion This study reports new data regarding the intricate outer and intracorpuscular 3D morphology of periarticular sensory nerve endings, including the volume, number of cells and structural composition. These results may form a basis to differ between normal and pathological morphological changes in periarticular sensory nerve endings in future studies.

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3D architecture and a bicellular mechanism of touch detection in mechanosensory corpuscle

Cited by 4 publications

References 40 publications

A Hierarchical Mechanotransduction System: From Macro to Micro

A Hierarchical Mechanotransduction System: From Macro to Micro

Structural and functional dissection of the Pacinian corpuscle reveals an active role of the inner core in touch detection

Periarticular Proprioception: Analyzing the Three-Dimensional Structure of Corpuscular Mechanosensors in the Dorsal Part of the Scapholunate Ligament

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