Artículo

Estamos trabajando para incorporar este artículo al repositorio
Consulte el artículo en la página del editor
Consulte la política de Acceso Abierto del editor

Abstract:

Opioid peptides have been detected in the auditory and vestibular efferent neurons where they colocalize with the major neurotransmitter, acetylcholine. We investigated the function of opioids to modulate neurotransmission mediated by hair cell's α9/α10-containing nicotinic acetylcholine receptors (α9/α10nAChRs). The endogenous opioid peptides, endomorphin-1 (mu agonist) and dynorphin B (kappa agonist), but not a delta agonist [D-Pen2,D-Pen-5]enkephalin, inhibited the acetylcholine-evoked currents in frog saccular hair cells and rat inner hair cells. This inhibition was noncompetitive, voltage-independent, and was accompanied by an acceleration of the rate of current decay. Selective mu- and kappa-opioid receptor antagonists did not block the inhibition, although partial reduction by naloxone was observed. All opioid antagonists tested also reduced the acetylcholine response. Endomorphin-1 and dynorphin B inhibited the acetylcholine-evoked currents in α9/α10-expressing Xenopus oocytes. Because oocytes lack opioid receptors, it provides strong evidence for the direct interaction of opioid peptides with α9/α10nAChR. Conclusion: α9/α10nAChR is a target for modulation by endomorphin-1 and dynorphin B, efferent cotransmitters in the inner ear.

Registro:

Documento: Artículo
Título:The α9/α10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear
Autor:Lioudyno, M.I.; Verbitsky, M.; Glowatzki, E.; Holt, J.C.; Boulter, J.; Zadina, J.E.; Elgoyhen, A.B.; Guth, P.S.
Filiación:Department of Pharmacology, Tulane University, New Orleans, LA 70112, United States
Instituto De Investigaciones En Ingeniería Genética Y Biología Molecular, Buenos Aires, 1428, Argentina
Center for Hearing Sciences, Department of Otolaryngology-Head and Neck Surgery, Johns Hopkins University School of Medicine, Baltimore, MD 21205, United States
UCLA Brain Research Institute, Hatos Research Center for Neuropharmacology, Los Angeles, CA 90095, United States
VA Medical Center, Department of Medicine, Tulane University School of Medicine, New Orleans, LA 70146, United States
Palabras clave:acetylcholine; delta opiate receptor agonist; dynorphin B; endomorphin 1; enkephalin[2,5 dextro penicillamine]; kappa opiate receptor agonist; kappa opiate receptor antagonist; mu opiate receptor agonist; mu opiate receptor antagonist; naloxone; nicotinic receptor; opiate peptide; acetylcholine; agents interacting with transmitter, hormone or drug receptors; dynorphin; dynorphin B; endomorphin 1; endorphin; enkephalin[2,5 dextro penicillamine]; isoprotein; nicotinic receptor; oligopeptide; opiate receptor; animal cell; animal tissue; article; competitive inhibition; controlled study; drug effect; electric current; electric potential; evoked response; female; frog; hair cell; inner ear; neurotransmission; nonhuman; oocyte; priority journal; protein expression; protein interaction; protein targeting; rat; reduction; sacculus; Xenopus; animal; chemistry; cochlea; cytology; drug antagonism; electric conductivity; frogs and toads; in vitro study; inner ear; metabolism; physiology; Sprague Dawley rat; synapse; vestibule; Xenopus laevis; Animalia; Anura; Acetylcholine; Animals; Anura; Cochlea; Dynorphins; Ear, Inner; Electric Conductivity; Endorphins; Enkephalin, D-Penicillamine (2,5)-; Hair Cells; Neurotransmitter Agents; Oligopeptides; Oocytes; Protein Isoforms; Rats; Rats, Sprague-Dawley; Receptors, Nicotinic; Receptors, Opioid; Saccule and Utricle; Synapses; Xenopus laevis
Año:2002
Volumen:20
Número:4
Página de inicio:695
Página de fin:711
DOI: http://dx.doi.org/10.1006/mcne.2002.1150
Título revista:Molecular and Cellular Neuroscience
Título revista abreviado:Mol. Cell. Neurosci.
ISSN:10447431
CODEN:MOCNE
CAS:acetylcholine, 51-84-3, 60-31-1, 66-23-9; dynorphin B, 85006-82-2; endomorphin 1, 189388-22-5; enkephalin[2,5 dextro penicillamine], 88373-73-3, 88381-29-7; naloxone, 357-08-4, 465-65-6; Acetylcholine, 51-84-3; Dynorphins, 74913-18-1; endomorphin 1; Endorphins; Enkephalin, D-Penicillamine (2,5)-, 88373-73-3; Neurotransmitter Agents; Oligopeptides; Protein Isoforms; Receptors, Nicotinic; Receptors, Opioid; rimorphin, 83335-41-5
Registro:https://bibliotecadigital.exactas.uba.ar/collection/paper/document/paper_10447431_v20_n4_p695_Lioudyno

Referencias:

  • Abou-Madi, L., Pontarotti, P., Tramu, G., Cupo, A., Eybalin, M., Coexistence of putative neuroactive substances in lateral olivocochlear neurons of rat and guinea pig (1987) Hear. Res., 30, pp. 135-146
  • Adams, P.R., Acetylcholine receptor kinetics (1981) J. Membr. Biol., 581, pp. 61-74
  • Akasu, T., Ohta, Y., Koketsu, K., Neuropeptides facilitate the desensitization of nicotinic acetylcholine-receptor in frog skeletal muscle endplate (1984) Brain Res., 290, pp. 342-347
  • Altschuler, R.A., Parakkal, M.H., Fex, J., Localization of enkephalin-like immunoreactivity in acetylcholinesterase-positive cells in the guinea-pig lateral superior olivary complex that project to the cochlea (1983) Neuroscience, 9, pp. 621-630
  • Altschuler, R.A., Fex, J., Parakkal, M.H., Eckenstein, F., Colocalization of enkephalin-like and choline acetyltransferase-like immunoreactivities in olivocochlear neurons of the guinea pig (1984) J. Histochem. Cytochem., 32, pp. 839-843
  • Altschuler, R.A., Parakkal, M.H., Rubio, J.A., Hoffman, D.W., Fex, J., Enkephalin-like immunoreactivity in the guinea pig organ of Corti: Ultrastructural and lesion studies (1984) Hear. Res., 16, pp. 17-31
  • Altschuler, R.A., Reeks, K.A., Fex, J., Hoffman, D.W., Lateral olivocochlear neurons contain both enkephalin and dynorphin immunoreactivities: Immunocytochemical colocalization studies (1988) J. Histochem. Cytochem., 36, pp. 797-801
  • Anderson, A.D., Troyanovskaya, M., Wackym, P.A., Differential expression of alpha2-7, alpha9 and beta2-4 nicotinic acetylcholine receptor subunit mRNA in the vestibular end-organs and Scarpa's ganglia of the rat (1997) Brain Res., 778, pp. 409-413
  • Andrianov, G.N., Ryzhova, I.V., Opioid peptides as possible neuromodulators of the afferent synaptic transmission in the frog semicircular canal (1999) Neuroscience, 93, pp. 801-806
  • Andrianov, G.N., Ryzhova, I.V., Effects of dalargin on excitation induced by L-glutamate agonists in the frog vestibular organs (2000) Neuroreport, 11, pp. 183-186
  • Arias, H.R., Binding sites for exogenous and endogenous noncompetitive inhibitors of the nicotinic acetylcholine receptor (1998) Biochim. Biophys. Acta, 1376, pp. 173-220
  • Athas, G.B., Norris, C.H., Guth, P.S., Garcia, M.M., Expression profiling of vestibular hair cells from the frog (1997) ARO Abstracts, 20, p. 37
  • Blanchet, C., Erostegui, C., Sugasawa, M., Dulon, D., Acetylcholine-induced potassium current of guinea pig outer hair cells: Its dependence on a calcium influx through nicotinic-like receptors (1996) J. Neurosci., 16, pp. 2574-2584
  • Boton, R., Dascal, N., Gillo, B., Lass, Y., Two calcium-activated chloride conductances in Xenopus laevis oocytes permeabilized with the ionophore A23187 (1989) J. Physiol. (London), 408, pp. 511-534
  • Boulter, J., Connolly, J., Deneris, E., Goldman, D., Heinemann, S., Patrick, J., Functional expression of two neuronal nicotinic acetylcholine receptors from cDNA clones identifies a gene family (1987) Proc. Natl. Acad. Sci. USA, 84, pp. 7763-7767
  • Burki, C., Felix, D., Ehrenberger, K., Enkephalin suppresses afferent cochlear neurotransmission (1993) O.R.L. J. Otorhinolaryngol. Relat. Spec., 55, pp. 3-6
  • Carpenter, M.B., Chang, L., Pereira, A.B., Hersh, L.B., Bruce, G., Wu, J.Y., Vestibular and cochlear efferent neurons in the monkey identified by immunocytochemical methods (1987) Brain. Res., 408, pp. 275-280
  • Chavkin, C., James, I.F., Goldstein, A., Dynorphin is a specific endogenous ligand of the kappa opioid receptor (1982) Science, 215, pp. 413-415
  • Dodson, H.C., Walliker, J.R., Frampton, S., Douek, E.E., Fourcin, A.J., Bannister, L.H., Structural alteration of hair cells in the contralateral ear resulting from extracochlear electrical stimulation (1986) Nature, 320, pp. 65-67
  • Elgoyhen, A.B., Johnson, D.S., Boulter, J., Vetter, D.E., Heinemann, S., Alpha 9: An acetylcholine receptor with novel pharmacological properties expressed in rat cochlear hair cells (1994) Cell, 79, pp. 705-715
  • Elgoyhen, A.B., Vetter, D.E., Katz, E., Rothlin, C.V., Heinemann, S.F., Boulter, J., α10: A determinant of nicotinic cholinergic receptor function in mammalian vestibular and cochlear mechanosensory hair cells (2001) Proc. Nat. Acad. Sci. USA, 98, pp. 3501-3506
  • Emmerling, M.R., Sobkowicz, H.M., Levenick, C.V., Scott, G.L., Slapnick, S.M., Rose, J.E., Biochemical and morphological differentiation of acetylcholinesterase-positive efferent fibers in the mouse cochlea (1990) J. Electron Microsc. Tech., 15, pp. 123-143
  • Erostegui, C., Norris, C.H., Bobbin, R.P., In vitro pharmacologic characterization of a cholinergic receptor on outer hair cells (1994) Hear. Res., 74, pp. 135-147
  • Evans, M.G., Acetylcholine activates two currents in guinea-pig outer hair cells (1996) J. Physiol., 491, pp. 563-578
  • Eybalin, M., Cupo, A.A., Pujol, R., Met-enkephalin characterization in the cochlea: High-performance liquid chromatography and immunoelectron microscopy (1984) Brain Res., 305, pp. 313-322
  • Eybalin, M., Abou-Madi, L., Rossier, J., Pujol, R., Electron microscopic localization of N-terminal proenkephalin (synenkephalin) immunostaining in the guinea pig organ of Corti (1985) Brain Res., 358, pp. 354-359
  • Eybalin, M., Pujol, R., Choline acetyltransferase (ChAT) immunoelectron microscopy distinguishes at least three types of efferent synapses in the organ of Corti (1987) Exp. Brain. Res., 65, pp. 261-270
  • Eybalin, M., Pujol, R., Bockaert, J., Opioid receptors inhibit the adenylate cyclase in guinea pig cochleas (1987) Brain Res., 421, pp. 336-342
  • Eybalin, M., Rebillard, G., Jarry, T., Cupo, A., Effect of noise level on the Met-enkephalin content of the guinea pig cochlea (1987) Brain Res., 418, pp. 189-192
  • Fex, J., Altschuler, R.A., Enkephalin-like immunoreactivity of olivocochlear nerve fibers in cochlea of guinea pig and cat (1981) Proc. Natl. Acad. Sci. USA, 78, pp. 1255-1259
  • Fuchs, P.A., Murrow, B.W., A novel cholinergic receptor mediates inhibition of chick cochlear hair cells (1992) Proc. R. Soc. Lond. B. Biol. Sci., 248, pp. 35-40
  • Fuchs, P.A., Synaptic transmission at vertebrate hair cells (1996) Curr. Opin. Neurobiol., 6, pp. 514-519
  • Fuxe, K., Agnati, L.F., Volume transmission in the brain. Novel mechanisms for neural transmission (1991) Advances in Neuroscience, 1. , Raven Press, New York
  • Gerzanich, V., Anand, R., Lindstrom, J., Homomers of alpha 8 and alpha 7 subunits of nicotinic receptors exhibit similar channel but contrasting binding site properties (1994) Mol. Pharmacol., 45, pp. 212-220
  • Giniatullin, R., Di Angelantonio, S., Marchetti, C., Sokolova, E., Khiroug, L., Nistri, A., Calcitonin gene-related peptide rapidly downregulates nicotinic receptor function and slowly raises intracellular Ca2+ in rat chromaffin cells in vitro (1999) J. Neurosci., 19, pp. 2945-2953
  • Glowatzki, E., Fuchs, P.A., Cholinergic synaptic inhibition of inner hair cells in the neonatal mammalian cochlea (2000) Science, 288, pp. 2366-2368
  • Guth, P.S., Norris, C.H., Bobbin, R.P., The pharmacology of transmission in the peripheral auditory system (1976) Pharmacol. Rev., 28, pp. 95-125
  • Guth, P.S., Perin, P., Norris, C.H., Valli, P., The vestibular hair cells: Posttransductional signal processing (1998) Prog. Neurobiol., 54, pp. 193-247
  • Hiel, H., Elgoyhen, A.B., Drescher, D.G., Morley, B.J., Expression of nicotinic acetylcholine receptor mRNA in the adult rat peripheral vestibular system (1996) Brain. Res., 738, pp. 347-352
  • Hoffman, D.W., Altschuler, R.A., Fex, J., High-performance liquid chromatographic identification of enkephalin-like peptides in the cochlea (1983) Hear. Res., 9, pp. 71-78
  • Hoffman, D.W., Rubio, J.A., Altschuler, R.A., Fex, J., Several distinct receptor binding enkephalins in olivocochlear fibers and terminals in the organ of Corti (1984) Brain. Res., 322, pp. 59-65
  • Hoffman, D.W., Zamir, N., Rubio, J.A., Altschuler, R.A., Fex, J., Proenkephalin and prodynorphin related neuropeptides in the cochlea (1985) Hear. Res., 17, pp. 47-50
  • Holt, J.C., Lioudyno, M., Athas, G., Garcia, M.M., Perin, P., Guth, P.S., The effect of proteolytic enzymes on the α9-nicotinic receptor-mediated response in isolated frog vestibular hair cells (2001) Hear. Res., 152, pp. 25-42
  • Hughes, J., Smith, T.W., Kosterlitz, H.W., Fothergill, L.A., Morgan, B.A., Morris, H.R., Identification of two related pentapeptides from the brain with potent opiate agonist activity (1975) Nature, 258, pp. 577-580
  • Inoue, M., Kuriyama, H., Somatostatin inhibits the nicotinic receptor-activated inward current in guinea pig chromaffin cells (1991) Biochem. Biophys. Res. Commun., 174, pp. 750-757
  • Itoh, H., Andoh, T., Watanabe, I., Sasaki, T., Kamiya, Y., Okumura, F., Dynorphins directly inhibit neuronal nicotinic acetylcholine receptors in PC12 cells (2000) Eur. J. Neurosci., 12, pp. 1253-1262
  • Iverfeldt, K., Serfozo, P., Diaz Arnesto, L., Bartfai, T., Differential release of coexisting neurotransmitters: Frequency dependence of the efflux of substance P, thyrotropin releasing hormone and [3H]serotonin from tissue slices of rat ventral spinal cord (1989) Acta. Physiol. Scand., 137, pp. 63-71
  • Ishiyama, A., Ishiyama, G., Baloh, R.W., Evans, C.J., Heroin-induced reversible profound deafness and vestibular dysfunction (2001) Addiction, 96, pp. 1363-1364
  • James, I.F., Chavkin, C., Goldstein, A., Preparation of brain membranes containing a single type of opioid receptor highly selective for dynorphin (1982) Proc. Natl. Acad. Sci. USA, 79, pp. 7570-7574
  • Katz, E., Verbitsky, M., Rothlin, C.V., Vetter, D.E., Heinemann, S.F., Elgoyhen, A.B., High calcium permeability and calcium block of the alpha9 nicotinic acetylcholine receptor (2000) Hear. Res., 141, pp. 117-128
  • Lehtosalo, J.I., Ylikoski, J., Eranko, L., Eranko, O., Panula, P., Immunohistochemical localization of unique enkephalin sequences contained in preproenkephalin A in the guinea pig cochlea (1984) Hear. Res., 16, pp. 101-107
  • Lenoir, M., Shnerson, A., Pujol, R., Cochlear receptor development in the rat with emphasis on synaptogenesis (1980) Anat. Embryol. (Berlin), 160, pp. 253-262
  • Liberman, M.C., Efferent synapses in the inner hair cell area of the cat cochlea: An electron microscopic study of serial sections (1980) Hear. Res., 3, pp. 189-204
  • Liberman, M.C., Dodds, L.W., Pierce, S., Afferent and efferent innervation of the cat cochlea: Quantitative analysis with light and electron microscopy (1990) J. Comp. Neurol., 301, pp. 443-460
  • Liberman, M.C., Olivocochlear efferents and protection from acoustic injury (2000) Synaptic Function in Hearing and Balance, , A symposium sponsered by The Johns Hopkins Center for Hearing and Balance. June 8-10
  • Lioudyno, M., Holt, J.C., Puri, A., Guth, P.S., The response to acetylcholine in the frog's saccule is differentially modulated by opioid receptor agonists, possible efferent co-transmitters (1999) 29th SFN Meeting, , Abstract 481.17
  • Lioudyno, M., Athas, G., Verbitsky, M., Elgoyhen, A.B., Zadina, J.E., Guth, P.S., Dynorphin and endomorphin-1 inhibit the acetylcholine evoked currents in hair cells (2000) 31st INRC Meeting, , Abstract Sun21: 44
  • Lioudyno, M.I., Verbitsky, M., Holt, J.C., Elgoyhen, A.B., Guth, P.S., Morphine inhibits an α9-acetylcholine nicotinic receptor-mediated responses by a mechanism which does not involve opioid receptors (2000) Hear. Res., 149, pp. 167-177
  • Merchan Perez, A., Gil-Loyzaga, P., Eybalin, M., Fernandez Mateos, P., Bartolome, M.V., Choline-acetyltransferase-like immunoreactivity in the organ of Corti of the rat during postnatal development (1994) Brain Res. Dev. Brain Res., 82, pp. 29-34
  • Miles, K., Greengard, P., Huganir, R.L., Calcitonin gene-related peptide regulates phosphorylation of the nicotinic acetylcholine receptor in rat myotubes (1989) Neuron, 2, pp. 1517-1524
  • Morley, B.J., Li, H.S., Hiel, H., Drescher, D.G., Elgoyhen, A.B., Identification of the subunits of the nicotinic cholinergic receptors in the rat cochlea using RT-PCR and in situ hybridization (1998) Brain Res. Mol. Brain Res., 53, pp. 78-87
  • Mulle, C., Benoit, P., Pinset, C., Roa, M., Changeux, J.P., Calcitonin gene-related peptide enhances the rate of desensitization of the nicotinic acetylcholine receptor in cultured mouse muscle cells (1988) Proc. Natl. Acad. Sci. USA, 85, pp. 5728-5732
  • Nicholls, D.G., (1995) Proteins, Transmitters and Synapses, , Blackwell Science, Cambridge, MA
  • Oka, K., Andoh, T., Watanabe, I., Kamiya, Y., Ito, H., Inhibition of the neuronal nicotinic receptor-mediated current by kappa opioid receptor agonists in PC12 cells (1998) Pflugers Arch., 436, pp. 887-893
  • Oliver, D., Klocker, N., Schuck, J., Baukrowitz, T., Ruppersberg, J.P., Fakler, B., Gating of Ca2+-activated K+ channels controls fast inhibitory synaptic transmission at auditory outer hair cells (2000) Neuron, 26, pp. 595-601
  • Park, H.J., Niedzielski, A.S., Wenthold, R.J., Expression of the nicotinic acetylcholine receptor subunit, alpha9, in the guinea pig cochlea (1997) Hear. Res., 112, pp. 95-105
  • Perachio, A.A., Kevetter, G.A., Identification of vestibular efferent neurons in the gerbil: Histochemical and retrograde labelling (1989) Exp. Brain. Res., 78, pp. 315-326
  • Polpathapee, S., Tuchinda, P., Chiwapong, S., Sensorineural hearing loss in a heroin addict (1984) J. Med. Assoc. Thai., 67, pp. 57-60
  • Popper, P., Christ, J., Wackym, P.A., (2001) Opiate Receptor Immunoreactivity in the Vestibular Epithelia in Rat, , ARO abstract 64
  • Popper, P., Wackym, P.A., Opioid peptides and receptors in the vestibular epithelia in rats (2001) 31st SFN Meeting, , abstract 298.28
  • Pujol, R., Lateral and medial efferents: A double neurochemical mechanism to protect and regulate inner and outer hair cell function in the cochlea (1994) Br. J. Audiol., 28, pp. 185-191
  • Ryan, A.F., Simmons, D.M., Watts, A.G., Swanson, L.W., Enkephalin mRNA production by cochlear and vestibular efferent neurons in the gerbil brainstem (1991) Exp. Brain. Res., 87, pp. 259-267
  • Safieddine, S., Prior, A.M., Eybalin, M., Choline acetyltransferase, glutamate decarboxylase, tyrosine hydroxylase, calcitonin gene-related peptide and opioid peptides coexist in lateral efferent neurons of rat and guinea-pig (1997) Eur. J. Neurosci., 9, pp. 356-367
  • Sahley, T.L., Kalish, R.B., Musiek, F.E., Hoffman, D.W., Effects of opioid drugs on auditory evoked potentials suggest a role of lateral olivocochlear dynorphins in auditory function (1991) Hear. Res., 55, pp. 133-142
  • Sahley, T.L., Nodar, R.H., Improvement in auditory function following pentazocine suggests a role for dynorphins in auditory sensitivity (1994) Ear. Hear., 15, pp. 422-431
  • Sahley, T.L., Musiek, F.E., Nodar, R.H., Naloxone blockade of (-)pentazocine-induced changes in auditory function (1996) Ear Hear., 17, pp. 341-353
  • Sahley, T.L., Nodar, R.H., A biochemical model of peripheral tinnitus(1) (2001) Hear. Res., 152, pp. 43-54
  • Scholtz, A.W., Kanonier, G., Schrott-Fischer, A., Immunohistochemical investigation of enkephalins in the human inner ear (1998) Hear. Res., 118, pp. 123-128
  • Schrattenholz, A., Pereira, E.F., Roth, U., Weber, K.H., Albuquerque, E.X., Maelicke, A., Agonist responses of neuronal nicotinic acetylcholine receptors are potentiated by a novel class of allosterically acting ligands (1996) Mol. Pharmacol., 49, pp. 1-6
  • Simmons, D.D., Mansdorf, N.B., Kim, J.H., Olivocochlear innervation of inner and outer hair cells during postnatal maturation: Evidence for a waiting period (1996) J. Comp. Neurol., 370, pp. 551-562
  • Simmons, D.D., Morley, B.J., Differential expression of the alpha 9 nicotinic acetylcholine receptor subunit in neonatal and adult cochlear hair cells (1998) Brain Res. Mol. Brain Res., 56, pp. 287-292
  • Simmons, L.K., Schuetze, S.M., Role, L.W., Substance P modulates single-channel properties of neuronal nicotinic acetylcholine receptors (1990) Neuron, 4, pp. 393-403
  • Stallcup, W.B., Patrick, J., Substance P enhances cholinergic receptor desensitization in a clonal nerve cell line (1980) Proc. Natl. Acad. Sci. USA, 77, pp. 634-638
  • Tohyama, Y., Senba, E., Yamashita, T., Kitajiri, M., Kuriyama, H., Kumazawa, T., Ohata, K., Tohyama, M., Coexistence of calcitonin gene-related peptide and enkephalin in single neurons of the lateral superior olivary nucleus of the guinea pig that project to the cochlea as lateral olivocochlear system (1990) Brain Res., 515, pp. 312-314
  • Valenta, D.C., Downing, J.E., Role, L.W., Peptide modulation of ACh receptor desensitization controls neurotransmitter release from chicken sympathetic neurons (1993) J. Neurophysiol., 69, pp. 928-942
  • Van Den Abbeele, T., Teulon, J., Huy, P.T., Two types of voltage-dependent potassium channels in outer hair cells from the guinea pig cochlea (1999) Am. J. Physiol., 277, pp. C913-C925
  • Vega, R., Soto, E., Opioid peptide receptors in the vestibular system (2000) 21st Barany Society Meeting in Uppsala, , Abstract P68
  • Vetter, D.E., Liberman, M.C., Mann, J., Barhanin, J., Boulter, J., Brown, M.C., Saffiote-Kolman, J., Elgoyhen, A.B., Role of α9 nicotinic ACh receptor subunits in the development and function of cochlear efferent innervation (1999) Neuron, 23, pp. 93-103
  • Xia, X.M., Fakler, B., Rivard, A., Wayman, G., Johnson-Pais, T., Keen, J.E., Ishii, T., Adelman, J.P., Mechanism of calcium gating in small-conductance calcium-activated potassium channels (1998) Nature, 395, pp. 503-507
  • Xiao, Y., Smith, R.D., Caruso, F.S., Kellar, K.J., Blockade of rat alpha3beta4 nicotinic receptor function by methadone, its metabolites, and structural analogs (2001) J. Pharmacol. Exp. Ther., 299, pp. 366-371
  • Yuhas, W.A., Fuchs, P.A., Apamin-sensitive, small-conductance, calcium-activated potassium channels mediate cholinergic inhibition of chick auditory hair cells (1999) J. Comp. Physiol., 185, pp. 455-462
  • Zadina, J.E., Hackler, L., Ge, L.J., Kastin, A.J., A potent and selective endogenous agonist for the mu-opiate receptor (1997) Nature, 386, pp. 499-502

Citas:

---------- APA ----------
Lioudyno, M.I., Verbitsky, M., Glowatzki, E., Holt, J.C., Boulter, J., Zadina, J.E., Elgoyhen, A.B.,..., Guth, P.S. (2002) . The α9/α10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear. Molecular and Cellular Neuroscience, 20(4), 695-711.
http://dx.doi.org/10.1006/mcne.2002.1150
---------- CHICAGO ----------
Lioudyno, M.I., Verbitsky, M., Glowatzki, E., Holt, J.C., Boulter, J., Zadina, J.E., et al. "The α9/α10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear" . Molecular and Cellular Neuroscience 20, no. 4 (2002) : 695-711.
http://dx.doi.org/10.1006/mcne.2002.1150
---------- MLA ----------
Lioudyno, M.I., Verbitsky, M., Glowatzki, E., Holt, J.C., Boulter, J., Zadina, J.E., et al. "The α9/α10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear" . Molecular and Cellular Neuroscience, vol. 20, no. 4, 2002, pp. 695-711.
http://dx.doi.org/10.1006/mcne.2002.1150
---------- VANCOUVER ----------
Lioudyno, M.I., Verbitsky, M., Glowatzki, E., Holt, J.C., Boulter, J., Zadina, J.E., et al. The α9/α10-containing nicotinic ACh receptor is directly modulated by opioid peptides, endomorphin-1, and dynorphin B, proposed efferent cotransmitters in the inner ear. Mol. Cell. Neurosci. 2002;20(4):695-711.
http://dx.doi.org/10.1006/mcne.2002.1150