Piezo2 in Cutaneous and Proprioceptive Mechanotransduction in Vertebrates

Anderson, Evan O.; Schneider, Eve R.; Bagriantsev, Sviatoslav N.

doi:10.1016/bs.ctm.2016.11.002

Cited by 32 publications

(18 citation statements)

References 78 publications

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“…Interestingly, single-channel activity of reconstituted Piezo1 does not substantially decay after mechanical stimulation, suggesting that inactivation in cells may require additional components not present in the tested bilayer ( Syeda et al, 2016 ). Aside from post-translational modifications, these components could include lipids and transmembrane or intracellular proteins, such as components of the cytoskeleton ( Anderson et al, 2017 ; Borbiro and Rohacs, 2017 ; Murthy et al, 2017 ; Wu et al, 2017a ). We propose that TMEM150C influences at least one such component, leading to changes in mechano-evoked responses in the Piezos and TREK-1.…”

Section: Discussionmentioning

confidence: 99%

“…These neurons can convert mechanical stimulation into ionic current due to the presence of mechano-gated ion channels, including nonselective excitatory channels, such as by Piezo2, and potassium-selective inhibitory channels, such as TREK-1 (K 2P 2.1) ( Alloui et al, 2006 ; Ranade et al, 2015 ). Activity of these channels is regulated through alternative splicing, interaction with the cytoskeleton, signaling pathways, and the lipid composition of the plasma membrane ( Anderson et al, 2017 ; Borbiro and Rohacs, 2017 ; Murthy et al, 2017 ; Szczot et al, 2017 ). Despite recent advances, proteins and pathways involved in regulation of mechano-sensitivity remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

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TMEM150C/Tentonin3 Is a Regulator of Mechano-gated Ion Channels

et al. 2018

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SUMMARY Neuronal mechano-sensitivity relies on mechanogated ion channels, but pathways regulating their activity remain poorly understood. TMEM150C was proposed to mediate mechano-activated current in proprioceptive neurons. Here, we studied functional interaction of TMEM150C with mechano-gated ion channels from different classes (Piezo2, Piezo1, and the potassium channel TREK-1) using two independent methods of mechanical stimulation. We found that TMEM150C significantly prolongs the duration of the mechano-current produced by all three channels, decreases apparent activation threshold in Piezo2, and induces persistent current in Piezo1. We also show that TMEM150C is co-expressed with Piezo2 in trigeminal neurons, expanding its role beyond proprioceptors. Finally, we cloned TMEM150C from the trigeminal neurons of the tactile-foraging domestic duck and showed that it functions similarly to the mouse ortholog, demonstrating evolutionary conservation among vertebrates. Our studies reveal TMEM150C as a general regulator of mechano-gated ion channels from different classes.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

TMEM150C/Tentonin3 Is a Regulator of Mechano-gated Ion Channels

et al. 2018

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“…Both Piezo1 and Piezo2 are nonselective cation channels with ~42% identity and the structure and mechanogating properties of both Piezo1 and Piezo2 have been elucidated recently [ 102 , 103 , 104 ]. They function as mechanotransducers in several somatic cells [ 24 , 105 , 106 , 107 , 108 , 109 ], while only Piezo2 functions as a transducer in LTMRs (see below).…”

Section: Putative Mechanosensitive Ion Channelsmentioning

confidence: 99%

“…Although this review is focused on the periphery of the nervous system, the occurrence of putative mechanoproteins in cutaneous mechanoreceptors has been mostly studied in parallel with LTMR neurons (see [ 21 , 105 , 109 ]). For this reason, a reference to DRG neurons will be included ( Figure 4 ).…”

Section: Putative Mechanoproteins In Mechanoreceptorsmentioning

confidence: 99%

Peripheral Mechanobiology of Touch—Studies on Vertebrate Cutaneous Sensory Corpuscles

Cobo

García‐Piqueras

García‐Mesa

et al. 2020

IJMS

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The vertebrate skin contains sensory corpuscles that are receptors for different qualities of mechanosensitivity like light brush, touch, pressure, stretch or vibration. These specialized sensory organs are linked anatomically and functionally to mechanosensory neurons, which function as low-threshold mechanoreceptors connected to peripheral skin through Aβ nerve fibers. Furthermore, low-threshold mechanoreceptors associated with Aδ and C nerve fibers have been identified in hairy skin. The process of mechanotransduction requires the conversion of a mechanical stimulus into electrical signals (action potentials) through the activation of mechanosensible ion channels present both in the axon and the periaxonal cells of sensory corpuscles (i.e., Schwann-, endoneurial- and perineurial-related cells). Most of those putative ion channels belong to the degenerin/epithelial sodium channel (especially the family of acid-sensing ion channels), the transient receptor potential channel superfamilies, and the Piezo family. This review updates the current data about the occurrence and distribution of putative mechanosensitive ion channels in cutaneous mechanoreceptors including primary sensory neurons and sensory corpuscles.

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“…For example, mice that lack TREK2, a hyperpolarizing background K + channel, have reduced mechanical thresholds (measured by von Frey) compared to WT controls ( Pereira et al, 2014 ). Another possible candidate is the Piezo 2 channel, shown to be important for mechanically induced currents in cultured sensory neurons ( Coste et al, 2010 ) and in mechanical nociception in rodents and humans ( Maksimovic et al, 2014 ; Ranade et al, 2014 ; Woo et al, 2014 ; Chesler et al, 2016 ; Anderson et al, 2017 ). Future studies are needed to determine whether CD137L has differential effects on these channels, thus helping to elucidate the underlying mechanisms regarding CD137L’s pro-nociceptive effects.…”

Section: Discussionmentioning

confidence: 99%

Contribution of CD137L to Sensory Hypersensitivity in a Murine Model of Neuropathic Pain

Wakley¹,

Leeming²,

Malon³

et al. 2018

eNeuro

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CD137L (4-1BBL) is a costimulatory molecule whose signaling can promote monocyte/macrophage functions; however, CD137L-mediated microglial response and its role in neuropathic pain remain unknown. We investigated CD137L following peripheral nerve injury-induced neuropathic pain using a spinal nerve L5 transection (L5Tx) murine model in both sexes. First, C57BL/6_CD137L knock-out (KO) mice displayed decreased mechanical and diminished heat hypersensitivity compared to wild-type (WT) controls, beginning on day 3 to up to day 35 post-L5Tx. Purified anti-mouse CD137L neutralizing monoclonal antibody (0.1 or 0.5 µg) was also used to identify CD137L’s window of action in BALB/c mice. Anti-CD137L antibody was intrathecally administered either from day 0 (before surgery) to day 7 (early treatment), or from day 6 to 13 post-L5Tx (late treatment), and nociceptive thresholds were assessed before surgery to up to day 35 post-surgery. Early treatment with anti-CD137L reduced L5Tx-induced mechanical but not heat hypersensitivity, while later treatment did not alter either sensitivity. Pro- versus anti-inflammatory responses within the lumbar spinal cord following L5Tx were further evaluated via quantitative real-time PCR (qRT-PCR) and immunohistochemistry (IHC) in time-course studies. Following L5Tx, female CD137L KO mice did not show increased iNOS mRNA and had reduced numbers of IL-1β+ cells compared to WT. At 21 d post-surgery, CD137L KO mice had higher total numbers of arginase (Arg)-1+ cells and Arg-1+ microglia. Altogether, results indicate that spinal cord CD137L contributes to the development of peripheral nerve injury-induced neuropathic pain, which may be in part mediated through CD137L’s modulation of the pro- and anti-inflammatory balance within the spinal cord.

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Piezo2 in Cutaneous and Proprioceptive Mechanotransduction in Vertebrates

Cited by 32 publications

References 78 publications

TMEM150C/Tentonin3 Is a Regulator of Mechano-gated Ion Channels

TMEM150C/Tentonin3 Is a Regulator of Mechano-gated Ion Channels

Peripheral Mechanobiology of Touch—Studies on Vertebrate Cutaneous Sensory Corpuscles

Contribution of CD137L to Sensory Hypersensitivity in a Murine Model of Neuropathic Pain

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