Ionic basis of a mechanotransduction current in adult rat dorsal root ganglion neurons
Tóm tắt
Sensory mechanical transduction – necessary for hearing, proprioception, and the senses of touch and pain – remains poorly understood. In somatosensation, even the basic properties of the mechanically sensitive excitatory ionic currents that are assumed to mediate mechanical transduction are largely undescribed. We have recorded, from the soma of rat dorsal root ganglion (DRG) neurons in vitro, whole-cell ionic currents induced by the impact of a piezo-electrically driven glass probe. This transient mechanically activated current was observed in virtually all DRG neurons tested. In ion substitution experiments the current could be carried nonselectively by most cations, including divalent and organic cations, but not by chloride or sulfate ions. In addition, the mechanically activated current carried by monovalent cations was consistently blocked by millimolar concentrations of external calcium or magnesium. Based on these results, the transient mechanical transduction current observed in somatosensory neurons in vitro is mediated by large-pore mechanically gated channels nonselective for cations but impermeable to anions.
Tài liệu tham khảo
Jordt SE, McKemy DD, Julius D: Lessons from peppers and peppermint: the molecular logic of thermosensation. Curr Opin Neurobiol 2003, 13: 487–492. 10.1016/S0959-4388(03)00101-6
Wood JN: Recent advances in understanding molecular mechanisms of primary afferent activation. Gut 2004, 53 Suppl 2: ii9–12.
Cho H, Shin J, Shin CY, Lee SY, Oh U: Mechanosensitive ion channels in cultured sensory neurons of neonatal rats. J Neurosci 2002, 22: 1238–1247.
Viana F, de la Pena E, Pecson B, Schmidt RF, Belmonte C: Swelling-activated calcium signalling in cultured mouse primary sensory neurons. Eur J Neurosci 2001, 13: 722–734. 10.1046/j.0953-816x.2000.01441.x
Alessandri-Haber N, Yeh JJ, Boyd AE, Parada CA, Chen X, Reichling DB, Levine JD: Hypotonicity induces TRPV4-mediated nociception in rat. Neuron 2003, 39: 497–511. 10.1016/S0896-6273(03)00462-8
McCarter GC, Reichling DB, Levine JD: Mechanical transduction by rat dorsal root ganglion neurons in vitro. Neurosci Lett 1999, 273: 179–182. 10.1016/S0304-3940(99)00665-5
Drew LJ, Wood JN, Cesare P: Distinct mechanosensitive properties of capsaicin-sensitive and -insensitive sensory neurons. J Neurosci 2002, 22: RC228.
Drew LJ, Rohrer DK, Price MP, Blaver KE, Cockayne DA, Cesare P, Wood JN: Acid-sensing ion channels ASIC2 and ASIC3 do not contribute to mechanically activated currents in mammalian sensory neurones. J Physiol 2004, 556: 691–710. 10.1113/jphysiol.2003.058693
Di Castro A, Drew LJ, Wood JN, Cesare P: Modulation of sensory neuron mechanotransduction by PKC- and nerve growth factor-dependent pathways. Proc Natl Acad Sci U S A 2006, 103: 4699–4704. 10.1073/pnas.0508005103
Takahashi A, Gotoh H: Mechanosensitive whole-cell currents in cultured rat somatosensory neurons. Brain Res 2000, 869: 225–230. 10.1016/S0006-8993(00)02366-0
Crawford AC, Evans MG, Fettiplace R: The actions of calcium on the mechano-electrical transducer current of turtle hair cells. J Physiol 1991, 434: 369–398.
Ricci AJ, Fettiplace R: The effects of calcium buffering and cyclic AMP on mechano-electrical transduction in turtle auditory hair cells. J Physiol 1997, 501 ( Pt 1): 111–124. 10.1111/j.1469-7793.1997.111bo.x
Dwyer TM, Adams DJ, Hille B: The permeability of the endplate channel to organic cations in frog muscle. J Gen Physiol 1980, 75: 469–492. 10.1085/jgp.75.5.469
Krishtal OA, Pidoplichko VI: Receptor for protons in the membrane of sensory neurons. Brain Res 1981, 214: 150–154. 10.1016/0006-8993(81)90446-7
Krishtal OA, Marchenko SM, Obukhov AG: Cationic channels activated by extracellular ATP in rat sensory neurons. Neuroscience 1988, 27: 995–1000. 10.1016/0306-4522(88)90203-5
Oh U, Hwang SW, Kim D: Capsaicin activates a nonselective cation channel in cultured neonatal rat dorsal root ganglion neurons. J Neurosci 1996, 16: 1659–1667.
Gold MS, Dastmalchi S, Levine JD: Co-expression of nociceptor properties in dorsal root ganglion neurons from the adult rat in vitro. Neuroscience 1996, 71: 265–275. 10.1016/0306-4522(95)00433-5
Cesare P, McNaughton P: A novel heat-activated current in nociceptive neurons and its sensitization by bradykinin. Proc Natl Acad Sci USA 1996, 93: 15435–15439. 10.1073/pnas.93.26.15435
Reichling DB, Levine JD: Heat transduction in rat sensory neurons by calcium-dependent activation of a cation channel. Proc Natl Acad Sci USA 1997, 94: 7006–7011. 10.1073/pnas.94.13.7006
Caterina MJ, Schumacher MA, Tominaga M, Rosen TA, Levine JD, Julius D: The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 1997, 389: 816–824. 10.1038/39807
Michaelis M, Blenk KH, Janig W, Vogel C: Development of spontaneous activity and mechanosensitivity in axotomized afferent nerve fibers during the first hours after nerve transection in rats. J Neurophysiol 1995, 74: 1020–1027.
Handwerker HO, Kilo S, Reeh PW: Unresponsive afferent nerve fibres in the sural nerve of the rat. J Physiol 1991, 435: 229–242.
Kress M, Koltzenburg M, Reeh PW, Handwerker HO: Responsiveness and functional attributes of electrically localized terminals of cutaneous C-fibers in vivo and in vitro. J Neurophysiol 1992, 68: 581–595.
Schmelz M, Schmidt R, Ringkamp M, Handwerker HO, Torebjork HE: Sensitization of insensitive branches of C nociceptors in human skin. J Physiol 1994, 480 ( Pt 2): 389–394.
Harper AA, Lawson SN: Electrical properties of rat dorsal root ganglion neurones with different peripheral nerve conduction velocities. J Physiol (Lond) 1985, 359: 47–63.
Harper AA, Lawson SN: Conduction velocity is related to morphological cell type in rat dorsal root ganglion neurones. J Physiol (Lond) 1985, 359: 31–46.
Gale JE, Marcotti W, Kennedy HJ, Kros CJ, Richardson GP: FM1–43 dye behaves as a permeant blocker of the hair-cell mechanotransducer channel. J Neurosci 2001, 21: 7013–7025.
Meyers JR, MacDonald RB, Duggan A, Lenzi D, Standaert DG, Corwin JT, Corey DP: Lighting up the senses: FM1–43 loading of sensory cells through nonselective ion channels. J Neurosci 2003, 23: 4054–4065.
Gillespie PG, Walker RG: Molecular basis of mechanosensory transduction. Nature 2001, 413: 194–202. 10.1038/35093011
Walker RG, Willingham AT, Zuker CS: A Drosophila mechanosensory transduction channel. Science 2000, 287: 2229–2234. 10.1126/science.287.5461.2229
Kim J, Chung YD, Park DY, Choi S, Shin DW, Soh H, Lee HW, Son W, Yim J, Park CS, Kernan MJ, Kim C: A TRPV family ion channel required for hearing in Drosophila. Nature 2003, 424: 81–84. 10.1038/nature01733
Sidi S, Friedrich RW, Nicolson T: NompC TRP channel required for vertebrate sensory hair cell mechanotransduction. Science 2003, 301: 96–99. 10.1126/science.1084370
Gong Z, Son W, Chung YD, Kim J, Shin DW, McClung CA, Lee Y, Lee HW, Chang DJ, Kaang BK, Cho H, Oh U, Hirsh J, Kernan MJ, Kim C: Two interdependent TRPV channel subunits, inactive and Nanchung, mediate hearing in Drosophila. J Neurosci 2004, 24: 9059–9066. 10.1523/JNEUROSCI.1645-04.2004
Corey DP, Garcia-Anoveros J, Holt JR, Kwan KY, Lin SY, Vollrath MA, Amalfitano A, Cheung EL, Derfler BH, Duggan A, Geleoc GS, Gray PA, Hoffman MP, Rehm HL, Tamasauskas D, Zhang DS: TRPA1 is a candidate for the mechanosensitive transduction channel of vertebrate hair cells. Nature 2004, 432: 723–730. 10.1038/nature03066
O'Hagan R, Chalfie M, Goodman MB: The MEC-4 DEG/ENaC channel of Caenorhabditis elegans touch receptor neurons transduces mechanical signals. Nat Neurosci 2005, 8: 43–50. 10.1038/nn1362
Gold MS, Reichling DB, Shuster MJ, Levine JD: Hyperalgesic agents increase a tetrodotoxin-resistant Na+ current in nociceptors. Proc Natl Acad Sci U S A 1996, 93: 1108–1112. 10.1073/pnas.93.3.1108
Hille B: Ionic channels of excitable membranes. 3rd edition. Sunderland, Mass., Sinauer Associates; 2001:xviii, 814.