Molecular determinants of mechanosensation in the muscle spindle

Banks, 2015, The innervation of the muscle spindle: a personal history, J Anat, 227, 115 Wu, 2021, Distinct subtypes of proprioceptive dorsal root ganglion neurons regulate adaptive proprioception in mice, Nat Commun, 12, 1026, 10.1038/s41467-021-21173-9 Oliver, 2021, Molecular correlates of muscle spindle and golgi tendon organ afferents, Nat Commun, 12, 1451, 10.1038/s41467-021-21880-3 Proske, 2012, The proprioceptive senses: their roles in signaling body shape, body position and movement, and muscle force, Physiol Rev, 92, 1651, 10.1152/physrev.00048.2011 Bewick, 2014, Mechanotransduction in the muscle spindle, Pflügers Archiv Szczot, 2021, The form and function of piezo2, Annu Rev Biochem, 90, 507, 10.1146/annurev-biochem-081720-023244 Woo, 2015, Piezo2 is the principal mechanotransduction channel for proprioception, Nat Neurosci, 18, 1756, 10.1038/nn.4162 Florez-Paz, 2016, A critical role for piezo2 channels in the mechanotransduction of mouse proprioceptive neurons, Sci Rep, 6, 1, 10.1038/srep25923 Ikeda, 2014, Merkel cells transduce and encode tactile stimuli to drive aβ-afferent impulses, Cell, 157, 664, 10.1016/j.cell.2014.02.026 Woo, 2014, Piezo2 is required for merkel-cell mechanotransduction, Nature, 509, 622, 10.1038/nature13251 Assaraf, 2020, Piezo2 expressed in proprioceptive neurons is essential for skeletal integrity, Nat Commun, 11, 3168, 10.1038/s41467-020-16971-6 Chesler, 2016, The role of piezo2 in human mechanosensation, N Engl J Med, 375, 1355, 10.1056/NEJMoa1602812 Cox, 2016, Removal of the mechanoprotective influence of the cytoskeleton reveals piezo1 is gated by bilayer tension, Nat Commun, 7, 10366, 10.1038/ncomms10366 Romero, 2020, A dietary fatty acid counteracts neuronal mechanical sensitization, Nat Commun, 11, 2997, 10.1038/s41467-020-16816-2 Hu, 2010, Evidence for a protein tether involved in somatic touch, EMBO J, 29, 855, 10.1038/emboj.2009.398 Jia, 2016, Regulation of piezo2 mechanotransduction by static plasma membrane tension in primary afferent neurons, J Biol Chem, 291, 9087, 10.1074/jbc.M115.692384 Poole, 2014, Tuning piezo ion channels to detect molecular-scale movements relevant for fine touch, Nat Commun, 5, 3520, 10.1038/ncomms4520 Qi, 2015, Membrane stiffening by stoml3 facilitates mechanosensation in sensory neurons, Nat Commun, 6, 8512, 10.1038/ncomms9512 Borbiro, 2015, Activation of trpv1 channels inhibits mechanosensitive piezo channel activity by depleting membrane phosphoinositides, Sci Signal, 8, ra15, 10.1126/scisignal.2005667 Eijkelkamp, 2013, A role for piezo2 in epac1-dependent mechanical allodynia, Nat Commun, 4, 1682, 10.1038/ncomms2673 Chang, 2020, Role of microtubules in piezo2 mechanotransduction of mouse merkel cells, J Neurophysiol, 124, 1824, 10.1152/jn.00502.2020 Dubin, 2017, Endogenous piezo1 can confound mechanically activated channel identification and characterization, Neuron, 94, 266, 10.1016/j.neuron.2017.03.039 Parpaite, 2021, Patch-seq of mouse drg neurons reveals candidate genes for specific mechanosensory functions, bioRxiv Lu, 2020, Tentonin 3/tmem150c senses blood pressure changes in the aortic arch, J Clin Invest, 130, 3671, 10.1172/JCI133798 Hong, 2016, Tentonin 3/tmem150c confers distinct mechanosensitive currents in dorsal-root ganglion neurons with proprioceptive function, Neuron, 91, 107, 10.1016/j.neuron.2016.05.029 Anderson, 2018, Tmem150c/tentonin3 is a regulator of mechano-gated ion channels, Cell Rep, 23, 701, 10.1016/j.celrep.2018.03.094 Simon, 2010, Amiloride-sensitive channels are a major contributor to mechanotransduction in mammalian muscle spindles, J Physiol, 588, 171, 10.1113/jphysiol.2009.182683 Hunt, 1978, Ionic basis of the receptor potential in primary endings of mammalian muscle spindles, J Gen Physiol, 71, 683, 10.1085/jgp.71.6.683 de Nooij, 2015, The pdz-domain protein whirlin facilitates mechanosensory signaling in mammalian proprioceptors, J Neurosci, 35, 3073, 10.1523/JNEUROSCI.3699-14.2015 Ciardo, 2016, Whirlin increases trpv1 channel expression and cellular stability, Biochim Biophys Acta Mol Cell Res, 1863, 115, 10.1016/j.bbamcr.2015.10.016 Lin, 2016, Evidence for the involvement of asic3 in sensory mechanotransduction in proprioceptors, Nat Commun, 7, 11460, 10.1038/ncomms11460 Bewick, 2005, Autogenic modulation of mechanoreceptor excitability by glutamate release from synaptic-like vesicles: evidence from the rat muscle spindle primary sensory ending, J Physiol, 562, 381, 10.1113/jphysiol.2004.074799 Wu, 2004, Vesicular glutamate transporter immunoreactivity in the central and peripheral endings of muscle-spindle afferents, Brain Res, 1011, 247, 10.1016/j.brainres.2004.03.047 Than, 2021, Vesicle-released glutamate is necessary to maintain muscle spindle afferent excitability but not dynamic sensitivity in adult mice, J Physiol, 599, 2953, 10.1113/JP281182 Zanato, 2014, Synthesis and biological evaluation of (−)-kainic acid analogues as phospholipase d-coupled metabotropic glutamate receptor ligands, Org Biomol Chem, 12, 9638, 10.1039/C4OB02002B Lund, 2010, Assessment of the potential role of muscle spindle mechanoreceptor afferents in chronic muscle pain in the rat masseter muscle, PLoS One, 5, e11131, 10.1371/journal.pone.0011131 Maksimovic, 2014, Epidermal merkel cells are mechanosensory cells that tune mammalian touch receptors, Nature, 509, 617, 10.1038/nature13250 Ranade, 2014, Piezo2 is the major transducer of mechanical forces for touch sensation in mice, Nature, 516, 121, 10.1038/nature13980 Hoffman, 2018, Merkel cells activate sensory neural pathways through adrenergic synapses, Neuron, 100, 1401, 10.1016/j.neuron.2018.10.034 Higashikawa, 2019, Merkel cells release glutamate following mechanical stimulation: implication of glutamate in the merkel cell-neurite complex, Front Cell Neurosci, 13, 10.3389/fncel.2019.00255 Chang, 2016, Merkel disc is a serotonergic synapse in the epidermis for transmitting tactile signals in mammals, Proc Natl Acad Sci Unit States Am, 113, E5491, 10.1073/pnas.1610176113 Vincent, 2015, Complex impairment of ia muscle proprioceptors following traumatic or neurotoxic injury, J Anat, 227, 221 Carrasco, 2017, Distribution of ttx-sensitive voltage-gated sodium channels in primary sensory endings of mammalian muscle spindles, J Neurophysiol, 117, 1690, 10.1152/jn.00889.2016 Kruse, 1991, Components of the dynamic response of mammalian muscle spindles that originate in the sensory terminals, Exp Brain Res, 86, 359, 10.1007/BF00228959 Shenton, 2014, A study of the expression of small conductance calcium-activated potassium channels (sk1-3) in sensory endings of muscle spindles and lanceolate endings of hair follicles in the rat, PLoS One, 9, 10.1371/journal.pone.0107073 Zheng, 2019, Deep sequencing of somatosensory neurons reveals molecular determinants of intrinsic physiological properties, Neuron, 103, 598, 10.1016/j.neuron.2019.05.039 Gerwin, 2019, Acetylcholine receptors in the equatorial region of intrafusal muscle fibres modulate mouse muscle spindle sensitivity, J Physiol, 597, 1993, 10.1113/JP277139 Zhang, 2014, Formation of cholinergic synapse-like specializations at developing murine muscle spindles, Dev Biol, 393, 227, 10.1016/j.ydbio.2014.07.011 Kim, 2020, Single-nucleus transcriptomics reveals functional compartmentalization in syncytial skeletal muscle cells, Nat Commun, 11, 1, 10.1038/s41467-020-20064-9 Gerwin, 2020, Impaired muscle spindle function in murine models of muscular dystrophy, J Physiol, 598, 1591, 10.1113/JP278563 Oki, 2019, The loss of slow skeletal muscle isoform of troponin t in spindle intrafusal fibers explains the pathophysiology of amish nemaline myopathy, J Physiol, 597, 3999, 10.1113/JP278119 Kröger, 2021, Muscle spindle function in healthy and diseased muscle, Skeletal Muscle, 11, 1, 10.1186/s13395-020-00258-x Wu, 2019, A role for sensory end organ-derived signals in regulating muscle spindle proprioceptor phenotype, J Neurosci, 39, 4252, 10.1523/JNEUROSCI.2671-18.2019