P2 receptor-mediated signaling in spherical bushy cells of the mammalian cochlear nucleus

Journal of Neurophysiology

Volumn 102, Issue 3, 2009, Pages 1821-1833

  Milenkovic, Ivan ^a   Rinke, Ilka ^a,b   Witte, Mirko ^a   Dietz, Beatrice ^a   Rübsamen, Rudolf ^a  

^a UNIVERSITY OF LEIPZIG   (Germany)

^b MAX PLANCK INSTITUTE OF NEUROBIOLOGY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE 5' O (3 THIOTRIPHOSPHATE); CALCIUM ION; PROTEIN KINASE C; PURINERGIC P2X2 RECEPTOR; PURINERGIC P2Y1 RECEPTOR;

ADAPTATION; ANIMAL TISSUE; ARTICLE; AUDITORY STIMULATION; CALCIUM SIGNALING; COCHLEAR NUCLEUS; CONTROLLED STUDY; ENZYME ACTIVITY; GERBIL; NERVE CELL EXCITABILITY; NONHUMAN; POTASSIUM CONDUCTANCE; PRIORITY JOURNAL; SOUND DETECTION;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; ANIMALS; ANIMALS, NEWBORN; BIOPHYSICS; CALCIUM; COCHLEAR NUCLEUS; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC STIMULATION; ENZYME INHIBITORS; FLUOROMETRY; FURA-2; GENE EXPRESSION REGULATION; GERBILLINAE; LYSINE; MEMBRANE POTENTIALS; NEURONS; PATCH-CLAMP TECHNIQUES; RECEPTORS, PURINERGIC P2; SIGNAL TRANSDUCTION; THIONUCLEOTIDES; VESICULAR GLUTAMATE TRANSPORT PROTEIN 1;

EID: 70349293680     PISSN: 00223077     EISSN: 15221598     Source Type: Journal    
DOI: 10.1152/jn.00186.2009     Document Type: Article

References (129)

1. Abbracchio MP, Burnstock G, Verkhratsky A, Zimmermann H. Purinergic signalling in the nervous system: an overview. Trends Neurosci 32: 19-29, 2009.
2. Allen Brain Atlas [Internet]. Seattle (WA): Allen Institute for Brain Science. © 2008. Available from: http://www.brain-map.org.
3. Amadio S, Vacca F, Martorana A, Sancesario G, Volonte C. P2Y1 receptor switches to neurons from glia in juvenile versus neonatal rat cerebellar cortex. BMC Dev Biol 7: 77, 2007.
4. Atkinson L, Batten TF, Deuchars J. P2X(2) receptor immunoreactivity in the dorsal vagal complex and area postrema of the rat. Neuroscience 99: 683-696, 2000. (Pubitemid 30682420)
5. Backoff PM, Shadduck Palombi P, Caspary DM. Gamma-aminobutyric acidergic and glycinergic inputs shape coding of amplitude modulation in the chinchilla cochlear nucleus. Hear Res 134: 77-88, 1999.
6. Bazwinsky I, Hartig W, Rubsamen R. Characterization of cochlear nucleus principal cells of Meriones unguiculatus and Monodelphis domestica by use of calcium-binding protein immunolabeling. J Chem Neuroanat 35: 158-174, 2008. (Pubitemid 50009021)
7. Bianchi BR, Lynch KJ, Touma E, Niforatos W, Burgard EC, Alexander KM, Park HS, Yu H, Metzger R, Kowaluk E, Jarvis MF, van Biesen T. Pharmacological characterization of recombinant human and rat P2X receptor subtypes. Eur J Pharmacol 376: 127-138, 1999. (Pubitemid 29320178)
8. Bischofberger J, Engel D, Li L, Geiger JR, Jonas P. Patch-clamp recording from mossy fiber terminals in hippocampal slices. Nat Protoc 1: 2075-2081, 2006. (Pubitemid 46773330)
9. Boland LM, Jackson KA. Protein kinase C inhibits Kv1.1 potassium channel function. Am J Physiol 277: C100-C110, 1999.
10. Bowser DN, Khakh BS. ATP excites interneurons and astrocytes to increase synaptic inhibition in neuronal networks. J Neurosci 24: 8606-8620, 2004.
11. Brawer JR, Morest DK. Relations between auditory nerve endings and cell types in the cat's anteroventral cochlear nucleus seen with the Golgi method and Nomarski optics. J Comp Neurol 160: 491-506, 1975.
12. Brawer JR, Morest DK, Kane EC. The neuronal architecture of the cochlear nucleus of the cat. J Comp Neurol 155: 251-300, 1974.
13. Brew HM, Forsythe ID. Two voltage-dependent K+ conductances with complementary functions in postsynaptic integration at a central auditory synapse. J Neurosci 15: 8011-8022, 1995.
14. Brown P, Dale N. Modulation of K(+) currents in Xenopus spinal neurons by p2y receptors: a role for ATP and ADP in motor pattern generation. J Physiol 540: 843-850, 2002. (Pubitemid 35190157)
15. Burnstock G. Purinergic nerves. Pharmacol Rev 24: 509-581, 1972.
16. Burnstock G. Cotransmission. Curr Opin Pharmacol 4: 47-52, 2004.
17. Burnstock G. Physiology and pathophysiology of purinergic neurotransmission. Physiol Rev 87: 659-797, 2007.
18. Camaioni E, Boyer JL, Mohanram A, Harden TK, Jacobson KA. Deoxyadenosine bisphosphate derivatives as potent antagonists at P2Y1 receptors. J Med Chem 41: 183-190, 1998. (Pubitemid 28114360)
19. Caminos E, Vale C, Lujan R, Martinez-Galan JR, Juiz JM. Developmental regulation and adult maintenance of potassium channel proteins (Kv 1.1 and Kv 1.2) in the cochlear nucleus of the rat. Brain Res 1056: 118-131, 2005. (Pubitemid 41557699)
20. Cao XJ, Shatadal S, Oertel D. Voltage-sensitive conductances of bushy cells of the Mammalian ventral cochlear nucleus. J Neurophysiol 97: 3961-3975, 2007. (Pubitemid 47080631)
21. Caspary DM, Backoff PM, Finlayson PG, Palombi PS. Inhibitory inputs modulate discharge rate within frequency receptive fields of anteroventral cochlear nucleus neurons. J Neurophysiol 72: 2124-2133, 1994.
22. Chen ZP, Levy A, Lightman SL. Activation of specific ATP receptors induces a rapid increase in intracellular calcium ions in rat hypothalamic neurons. Brain Res 641: 249-256, 1994. (Pubitemid 24101291)
23. Chung SK, Reinhart PH, Martin BL, Brautigan D, Levitan IB. Protein kinase activity closely associated with a reconstituted calcium-activated potassium channel. Science 253: 560-562, 1991. (Pubitemid 21917188)
24. Communi D, Motte S, Boeynaems JM, Pirotton S. Pharmacological characterization of the human P2Y4 receptor. Eur J Pharmacol 317: 383-389, 1996a. (Pubitemid 27014046)
25. Communi D, Parmentier M, Boeynaems JM. Cloning, functional expression and tissue distribution of the human P2Y6 receptor. Biochem Biophys Res Commun 222: 303-308, 1996b. (Pubitemid 26335011)
26. 2+ channel subtypes at cell bodies and synaptic terminals of rat anterioventral cochlear bushy neurones. J Physiol 512: 365-376, 1998.
27. Egan TM, Khakh BS. Contribution of calcium ions to P2X channel responses. J Neurosci 24: 3413-3420, 2004.
28. Evans RJ, Lewis C, Buell G, Valera S, North RA, Surprenant A. Pharmacological characterization of heterologously expressed ATP-gated cation channels (P2x purinoceptors). Mol Pharmacol 48: 178-183, 1995.
29. Fields RD, Burnstock G. Purinergic signalling in neuron-glia interactions. Nat Rev Neurosci 7: 423-436, 2006.
30. Florenzano F, Viscomi MT, Cavaliere F, Volonte C, Molinari M. Cerebellar lesion up-regulates P2X1 and P2X2 purinergic receptors in precerebellar nuclei. Neuroscience 115: 425-434, 2002. (Pubitemid 35284759)
31. Francis HW, Manis PB. Effects of deafferentation on the electrophysiology of ventral cochlear nucleus neurons. Hear Res 149: 91-105, 2000. (Pubitemid 30734429)
32. Franke H, Grummich B, Hartig W, Grosche J, Regenthal R, Edwards RH, Illes P, Krugel U. Changes in purinergic signaling after cerebral injury - involvement of glutamatergic mechanisms? Int J Dev Neurosci 24: 123-132, 2006. (Pubitemid 43294618)
33. Franke H, Illes P. Involvement of P2 receptors in the growth and survival of neurons in the CNS. Pharmacol Ther 109: 297-324, 2006. (Pubitemid 43132815)
34. Friauf E, Lohmann C. Development of auditory brainstem circuitry. Activity-dependent and activity-independent processes. Cell Tissue Res 297: 187-195, 1999. (Pubitemid 29366463)
35. Fries JE, Wheeler-Schilling TH, Guenther E, Kohler K. Expression of P2Y1, P2Y2, P2Y4, and P2Y6 receptor subtypes in the rat retina. Invest Ophthalmol Vis Sci 45: 3410-3417, 2004. (Pubitemid 39298556)
36. Gai Y, Carney LH. Influence of inhibitory inputs on rate and timing of responses in the anteroventral cochlear nucleus. J Neurophysiol 99: 1077-1095, 2008.
37. Garcia MM, Edward R, Brennan GB, Harlan RE. Deafferentation-induced changes in protein kinase C expression in the rat cochlear nucleus. Hear Res 147: 113-124, 2000. (Pubitemid 30658059)
38. Garcia MM, Harlan RE. Protein kinase C in central auditory pathways of the rat. J Comp Neurol 385: 1-25, 1997. (Pubitemid 27329816)
39. Gerevich Z, Muller C, Illes P. Metabotropic P2Y1 receptors inhibit P2X3 receptor-channels in rat dorsal root ganglion neurons. Eur J Pharmacol 521: 34-38, 2005. (Pubitemid 41427787)
40. Grigg JJ, Brew HM, Tempel BL. Differential expression of voltage-gated potassium channel genes in auditory nuclei of the mouse brainstem. Hear Res 140: 77-90, 2000.
41. 2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440-3450, 1985.
42. Hackney CM, Osen KK, Kolston J. Anatomy of the cochlear nuclear complex of guinea pig. Anat Embryol (Berl) 182: 123-149, 1990. (Pubitemid 20265199)
43. Hartig W, Riedel A, Grosche J, Edwards RH, Fremeau RT Jr, Harkany T, Brauer K, Arendt T. Complementary distribution of vesicular glutamate transporters 1 and 2 in the nucleus accumbens of rat: relationship to calretinin-containing extrinsic innervation and calbindin-immunoreactive neurons. J Comp Neurol 465: 1-10, 2003. (Pubitemid 37075676)
44. Hartig W, Singer A, Grosche J, Brauer K, Ottersen OP, Bruckner G. Perineuronal nets in the rat medial nucleus of the trapezoid body surround neurons immunoreactive for various amino acids, calcium-binding proteins and the potassium channel subunit Kv3.1b. Brain Res 899: 123-133, 2001. (Pubitemid 32324153)
45. Housley GD, Jagger DJ, Greenwood D, Raybould NP, Salih SG, Jarlebark LE, Vlajkovic SM, Kanjhan R, Nikolic P, Munoz DJ, Thorne PR. Purinergic regulation of sound transduction and auditory neurotransmission. Audiol Neurootol 7: 55-61, 2002. (Pubitemid 34253013)
46. Housley GD, Kanjhan R, Raybould NP, Greenwood D, Salih SG, Jarlebark L, Burton LD, Setz VC, Cannell MB, Soeller C, Christie DL, Usami S, Matsubara A, Yoshie H, Ryan AF, Thorne PR. Expression of the P2X(2) receptor subunit of the ATP-gated ion channel in the cochlea: implications for sound transduction and auditory neurotransmission. J Neurosci 19: 8377-8388, 1999. (Pubitemid 30226757)
47. Hu HZ, Gao N, Zhu MX, Liu S, Ren J, Gao C, Xia Y, Wood JD. Slow excitatory synaptic transmission mediated by P2Y1 receptors in the guineapig enteric nervous system. J Physiol 550: 493-504, 2003. (Pubitemid 36889307)
48. Huang LC, Ryan AF, Cockayne DA, Housley GD. Developmentally regulated expression of the P2X3 receptor in the mouse cochlea. Histochem Cell Biol 125: 681-692, 2006. (Pubitemid 43780175)
49. Illes P, Ribeiro JA. Neuronal P2 receptors of the central nervous system. Curr Top Med Chem 4: 831-838, 2004. (Pubitemid 38854841)
50. Jo YH, Schlichter R. Synaptic corelease of ATP and GABA in cultured spinal neurons. Nat Neurosci 2: 241-245, 1999. (Pubitemid 30491294)
51. Jones TA, Leake PA, Snyder RL, Stakhovskaya O, Bonham B. Spontaneous discharge patterns in cochlear spiral ganglion cells before the onset of hearing in cats. J Neurophysiol 98: 1898-1908, 2007.
52. Kaczmarek LK, Bhattacharjee A, Desai R, Gan L, Song P, von Hehn CA, Whim MD, Yang B. Regulation of the timing of MNTB neurons by short-term and long-term modulation of potassium channels. Hear Res 206: 133-145, 2005. (Pubitemid 41080064)
53. Kanjhan R, Housley GD, Burton LD, Christie DL, Kippenberger A, Thorne PR, Luo L, Ryan AF. Distribution of the P2X2 receptor subunit of the ATP-gated ion channels in the rat central nervous system. J Comp Neurol 407: 11-32, 1999. (Pubitemid 29161990)
54. Kanjhan R, Housley GD, Thorne PR, Christie DL, Palmer DJ, Luo L, Ryan AF. Localization of ATP-gated ion channels in cerebellum using P2x2R subunit-specific antisera. Neuroreport 7: 2665-2669, 1996. (Pubitemid 26403036)
55. King BF, Townsend-Nicholson A, Burnstock G. Metabotropic receptors for ATP and UTP: exploring the correspondence between native and recombinant nucleotide receptors. Trends Pharmacol Sci 19: 506-514, 1998a. (Pubitemid 29008540)
56. King BF, Wildman SS, Ziganshina LE, Pintor J, Burnstock G. Effects of extracellular pH on agonism and antagonism at a recombinant P2X2 receptor. Br J Pharmacol 121: 1445-1453, 1997. (Pubitemid 27317559)
57. King M, Housley GD, Raybould NP, Greenwood D, Salih SG. Expression of ATP-gated ion channels by Reissner's membrane epithelial cells. Neuroreport 9: 2467-2474, 1998b. (Pubitemid 28387132)
58. Kitzes LM, Kageyama GH, Semple MN, Kil J. Development of ectopic projections from the ventral cochlear nucleus to the superior olivary complex induced by neonatal ablation of the contralateral cochlea. J Comp Neurol 353: 341-363, 1995.
59. Kopp-Scheinpflug C, Dehmel S, Dorrscheidt GJ, Rubsamen R. Interaction of excitation and inhibition in anteroventral cochlear nucleus neurons that receive large endbulb synaptic endings. J Neurosci 22: 11004-11018, 2002. (Pubitemid 36005177)
60. Kopp-Scheinpflug C, Fuchs K, Lippe WR, Tempel BL, Rubsamen R. Decreased temporal precision of auditory signaling in Kcna1-null mice: an electrophysiological study in vivo. J Neurosci 23: 9199-9207, 2003. (Pubitemid 37243821)
61. Kuznetsova MS, Higgs MH, Spain WJ. Adaptation of firing rate and spike-timing precision in the avian cochlear nucleus. J Neurosci 28: 11906-11915, 2008.
62. Lagostena L, Mammano F. Intracellular calcium dynamics and membrane conductance changes evoked by Deiters' cell purinoceptor activation in the organ of Corti. Cell Calcium 29: 191-198, 2001. (Pubitemid 32184390)
63. Lalo U, Voitenko N, Kostyuk P. Iono- and metabotropically induced purinergic calcium signalling in rat neocortical neurons. Brain Res 799: 285-291, 1998. (Pubitemid 28351259)
64. Lazarowski ER, Boucher RC, Harden TK. Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol Pharmacol 64: 785-795, 2003.
65. Lazarowski ER, Watt WC, Stutts MJ, Boucher RC, Harden TK. Pharmacological selectivity of the cloned human P2U-purinoceptor: potent activation by diadenosine tetraphosphate. Br J Pharmacol 116: 1619-1627, 1995.
66. Leake PA, Hradek GT, Chair L, Snyder RL. Neonatal deafness results in degraded topographic specificity of auditory nerve projections to the cochlear nucleus in cats. J Comp Neurol 497: 13-31, 2006. (Pubitemid 43844565)
67. Leao RN, Svahn K, Berntson A, Walmsley B. Hyperpolarization-activated (I) currents in auditory brainstem neurons of normal and congenitally deaf mice. Eur J Neurosci 22: 147-157, 2005. (Pubitemid 41059980)
68. Lippe WR. Rhythmic spontaneous activity in the developing avian auditory system. J Neurosci 14: 1486-1495, 1994.
69. Manis PB, Marx SO. Outward currents in isolated ventral cochlear nucleus neurons. J Neurosci 11: 2865-2880, 1991.
70. McKay SM, Oleskevich S. The role of spontaneous activity in development of the endbulb of Held synapse. Hear Res 230: 53-63, 2007. (Pubitemid 47058842)
71. Milenkovic I, Weick M, Wiedemann P, Reichenbach A, Bringmann A. P2Y receptor-mediated stimulation of Muller glial cell DNA synthesis: dependence on EGF and PDGF receptor transactivation. Invest Ophthalmol Vis Sci 44: 1211-1220, 2003. (Pubitemid 36297842)
72. Milenkovic I, Witte M, Turecek R, Heinrich M, Reinert T, Rubsamen R. Development of chloride-mediated inhibition in neurons of the anteroventral cochlear nucleus of gerbil (Meriones unguiculatus). J Neurophysiol 98: 1634-1644, 2007. (Pubitemid 47435907)
73. Moran-Jimenez MJ, Matute C. Immunohistochemical localization of the P2Y(1) purinergic receptor in neurons and glial cells of the central nervous system. Brain Res Mol Brain Res 78: 50-58, 2000. (Pubitemid 30417485)
74. Morest DK, Hutson KA, Kwok S. Cytoarchitectonic atlas of the cochlear nucleus of the chinchilla, Chinchilla laniger. J Comp Neurol 300: 230-248, 1990. (Pubitemid 20361331)
75. Mori M, Heuss C, Gahwiler BH, Gerber U. Fast synaptic transmission mediated by P2X receptors in CA3 pyramidal cells of rat hippocampal slice cultures. J Physiol 535: 115-123, 2001. (Pubitemid 32782729)
76. Nakagawa T, Akaike N, Kimitsuki T, Komune S, Arima T. ATP-induced current in isolated outer hair cells of guinea pig cochlea. J Neurophysiol 63: 1068-1074, 1990. (Pubitemid 20188871)
77. Nieber K, Poelchen W, Illes P. Role of ATP in fast excitatory synaptic potentials in locus coeruleus neurones of the rat. Br J Pharmacol 122: 423-430, 1997. (Pubitemid 27429716)
78. Nikolic P, Housley GD, Luo L, Ryan AF, Thorne PR. Transient expression of P2X(1) receptor subunits of ATP-gated ion channels in the developing rat cochlea. Brain Res Dev Brain Res 126: 173-182, 2001. (Pubitemid 32204436)
79. Nikolic P, Housley GD, Thorne PR. Expression of the P2X7 receptor subunit of the adenosine 5′-triphosphate-gated ion channel in the developing and adult rat cochlea. Audiol Neurootol 8: 28-37, 2003. (Pubitemid 36098750)
80. North RA. Molecular physiology of P2X receptors. Physiol Rev 82: 1013-1067, 2002.
81. Oertel D. Synaptic responses and electrical properties of cells in brain slices of the mouse anteroventral cochlear nucleus. J Neurosci 3: 2043-2053, 1983. (Pubitemid 14233765)
82. Oertel D. The role of timing in the brain stem auditory nuclei of vertebrates. Annu Rev Physiol 61: 497-519, 1999. (Pubitemid 29143181)
83. Osen KK. Cytoarchitecture of the cochlear nuclei in the cat. J Comp Neurol 136: 453-484, 1969.
84. Ostapoff EM, Feng JJ, Morest DK. A physiological and structural study of neuron types in the cochlear nucleus. II. Neuron types and their structural correlation with response properties. J Comp Neurol 346: 19-42, 1994. (Pubitemid 2118685)
85. Pankratov Y, Castro E, Miras-Portugal MT, Krishtal O. A purinergic component of the excitatory postsynaptic current mediated by P2X receptors in the CA1 neurons of the rat hippocampus. Eur J Neurosci 10: 3898-3902, 1998. (Pubitemid 29073944)
86. Parekh AB, Putney JW Jr. Store-operated calcium channels. Physiol Rev 85: 757-810, 2005.
87. Parks TN. Effects of early deafness on development of brain stem auditory neurons. Ann Otol Rhinol Laryngol Suppl 168: 37-43, 1997.
88. Poelchen W, Sieler D, Wirkner K, Illes P. Co-transmitter function of ATP in central catecholaminergic neurons of the rat. Neuroscience 102: 593-602, 2001. (Pubitemid 32175096)
89. Ralevic V, Burnstock G. Receptors for purines and pyrimidines. Pharmacol Rev 50: 413-492, 1998.
90. Rathouz M, Trussell L. Characterization of outward currents in neurons of the avian nucleus magnocellularis. J Neurophysiol 80: 2824-2835, 1998. (Pubitemid 29029215)
91. Raybould NP, Housley GD. Variation in expression of the outer hair cell P2X receptor conductance along the guinea-pig cochlea. J Physiol 498: 717-727, 1997.
92. Robertson D, Paki B. A role for purinergic receptors at the inner hair cell-afferent synapse? Audiol Neurootol 7: 62-67, 2002. (Pubitemid 34253014)
93. Rouiller EM, Ryugo DK. Intracellular marking of physiologically characterized cells in the ventral cochlear nucleus of the cat. J Comp Neurol 225: 167-186, 1984.
94. Ruan HZ, Burnstock G. Localisation of P2Y1 and P2Y4 receptors in dorsal root, nodose and trigeminal ganglia of the rat. Histochem Cell Biol 120: 415-426, 2003. (Pubitemid 38005361)
95. Rubel EW, Fritzsch B. Auditory system development: primary auditory neurons and their targets. Annu Rev Neurosci 25: 51-101, 2002. (Pubitemid 34748012)
96. 2+ by P2Y1 receptors may depend on the developmental stage of cultured rat striatal neurons. J Cell Physiol 209: 81-93, 2006.
97. Rubio ME, Soto F. Distinct localization of P2X receptors at excitatory postsynaptic specializations. J Neurosci 21: 641-653, 2001. (Pubitemid 32107453)
98. Rubsamen R, Schafer M. Ontogenesis of auditory fovea representation in the inferior colliculus of the Sri Lankan rufous horseshoe bat, Rhinolophus rouxi. J Comp Physiol [A] 167: 757-769, 1990.
99. Ryugo DK, Sento S. Synaptic connections of the auditory nerve in cats: relationship between endbulbs of held and spherical bushy cells. J Comp Neurol 305: 35-48, 1991.
100. Schwarz DW, Puil E. Firing properties of spherical bushy cells in the anteroventral cochlear nucleus of the gerbil. Hear Res 114: 127-138, 1997. (Pubitemid 28007862)
101. Sergeeva OA, Klyuch BP, Fleischer W, Eriksson KS, Korotkova TM, Siebler M, Haas HL. P2Y receptor-mediated excitation in the posterior hypothalamus. Eur J Neurosci 24: 1413-1426, 2006. (Pubitemid 44401664)
102. Silinsky EM. On the association between transmitter secretion and the release of adenine nucleotides from mammalian motor nerve terminals. J Physiol 247: 145-162, 1975.
103. Simon J, Webb TE, King BF, Burnstock G, Barnard EA. Characterisation of a recombinant P2Y purinoceptor. Eur J Pharmacol 291: 281-289, 1995.
104. Song P, Yang Y, Barnes-Davies M, Bhattacharjee A, Hamann M, Forsythe ID, Oliver DL, Kaczmarek LK. Acoustic environment determines phosphorylation state of the Kv3.1 potassium channel in auditory neurons. Nat Neurosci 8: 1335-1342, 2005. (Pubitemid 41630421)
105. Stam JC, Michiels F, van der Kammen RA, Moolenaar WH, Collard JG. Invasion of T-lymphoma cells: cooperation between Rho family GTPases and lysophospholipid receptor signaling. EMBO J 17: 4066-4074, 1998. (Pubitemid 28333990)
106. Studeny S, Torabi A, Vizzard MA. P2X2 and P2X3 receptor expression in postnatal and adult rat urinary bladder and lumbosacral spinal cord. Am J Physiol Regul Integr Comp Physiol 289: R1155-R1168, 2005. (Pubitemid 41397066)
107. Sugasawa M, Erostegui C, Blanchet C, Dulon D. ATP activates nonselective cation channels and calcium release in inner hair cells of the guinea-pig cochlea. J Physiol 491: 707-718, 1996. (Pubitemid 26107244)
108. Tokuyama Y, Hara M, Jones EM, Fan Z, Bell GI. Cloning of rat and mouse P2Y purinoceptors. Biochem Biophys Res Commun 211: 211-218, 1995.
109. Tonazzini I, Trincavelli ML, Storm-Mathisen J, Martini C, Bergersen LH. Co-localization and functional cross-talk between A1 and P2Y1 purine receptors in rat hippocampus. Eur J Neurosci 26: 890-902, 2007. (Pubitemid 47274605)
110. Tritsch NX, Yi E, Gale JE, Glowatzki E, Bergles DE. The origin of spontaneous activity in the developing auditory system. Nature 450: 50-55, 2007. (Pubitemid 350070568)
111. Trussell LO. Synaptic mechanisms for coding timing in auditory neurons. Annu Rev Physiol 61: 477-496, 1999.
112. Unsworth CD, Johnson RG. Acetylcholine and ATP are coreleased from the electromotor nerve terminals of Narcine brasiliensis by an exocytotic mechanism. Proc Natl Acad Sci USA 87: 553-557, 1990. (Pubitemid 20051408)
113. Vohringer C, Schafer R, Reiser G. A chimeric rat brain P2Y1 receptor tagged with green-fluorescent protein: high-affinity ligand recognition of adenosine diphosphates and triphosphates and selectivity identical to that of the wild-type receptor. Biochem Pharmacol 59: 791-800, 2000. (Pubitemid 30081702)
114. von Kugelgen I. Pharmacological profiles of cloned mammalian P2Y-receptor subtypes. Pharmacol Ther 110: 415-432, 2006.
115. von Kugelgen I, Starke K. Noradrenaline-ATP co-transmission in the sympathetic nervous system. Trends Pharmacol Sci 12: 319-324, 1991.
116. von Kugelgen I, Wetter A. Molecular pharmacology of P2Y-receptors. Naunyn Schmiedebergs Arch Pharmacol 362: 310-323, 2000.
117. Waldo GL, Harden TK. Agonist binding and Gq-stimulating activities of the purified human P2Y1 receptor. Mol Pharmacol 65: 426-436, 2004.
118. Walsh EJ, McGee J. Rhythmic discharge properties of caudal cochlear nucleus neurons during postnatal development in cats. Hear Res 36: 233-247, 1988. (Pubitemid 18280228)
119. Watano T, Calvert JA, Vial C, Forsythe ID, Evans RJ. P2X receptor subtype-specific modulation of excitatory and inhibitory synaptic inputs in the rat brainstem. J Physiol 558: 745-757, 2004. (Pubitemid 39199102)
120. Weick M, Cherkas PS, Hartig W, Pannicke T, Uckermann O, Bringmann A, Tal M, Reichenbach A, Hanani M. P2 receptors in satellite glial cells in trigeminal ganglia of mice. Neuroscience 120: 969-977, 2003. (Pubitemid 36966649)
121. Welford LA, Cusack NJ, Hourani SM. The structure-activity relationships of ectonucleotidases and of excitatory P2-purinoceptors: evidence that dephosphorylation of ATP analogues reduces pharmacological potency. Eur J Pharmacol 141: 123-130, 1987.
122. Werner P, Seward EP, Buell GN, North RA. Domains of P2X receptors involved in desensitization. Proc Natl Acad Sci USA 93: 15485-15490, 1996. (Pubitemid 27009625)
123. White TD. Direct detection of depolarisation-induced release of ATP from a synaptosomal preparation. Nature 267: 67-68, 1977.
124. Woolf NK, Ryan AF. The development of auditory function in the cochlea of the mongolian gerbil. Hear Res 13: 277-283, 1984. (Pubitemid 14111265)
125. Wu SH, Oertel D. Intracellular injection with horseradish peroxidase of physiologically characterized stellate and bushy cells in slices of mouse anteroventral cochlear nucleus. J Neurosci 4: 1577-1588, 1984. (Pubitemid 14058674)
126. Xiang Z, Bo X, Burnstock G. P2X receptor immunoreactivity in the rat cochlea, vestibular ganglion and cochlear nucleus. Hear Res 128: 190-196, 1999. (Pubitemid 29083260)
127. Yao ST, Barden JA, Finkelstein DI, Bennett MR, Lawrence AJ. Comparative study on the distribution patterns of P2X(1)-P2X(6) receptor immunoreactivity in the brainstem of the rat and the common marmoset (Callithrix jacchus): association with catecholamine cell groups. J Comp Neurol 427: 485-507, 2000.
128. Zhou J, Nannapaneni N, Shore S. Vessicular glutamate transporters 1 and 2 are differentially associated with auditory nerve and spinal trigeminal inputs to the cochlear nucleus. J Comp Neurol 500: 777-787, 2007. (Pubitemid 46067789)
129. Zimmermann H. Biochemistry, localization and functional roles of ectonucleotidases in the nervous system. Prog Neurobiol 49: 589-618, 1996. (Pubitemid 26343246)