Selective neuroinhibitory effects of taurine in slices of rat main olfactory bulb

Neuroscience

Volumn 124, Issue 4, 2004, Pages 929-944

  Belluzzi, O ^a   Puopolo, M ^b   Benedusi, M ^a   Kratskin, I ^c  

^a UNIVERSITY OF FERRARA   (Italy)

^b HARVARD MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

ACSF; AMPA; Artificial cerebrospinal fluid; GABAA receptors; Membrane electrical properties; Mitral tufted cells; Olfactory nerve evoked synaptic responses; Periglomerular cells; Presynaptic GABAB receptors

Indexed keywords

3 AMINOPROPYL(DIETHOXYMETHYL)PHOSPHINIC ACID; 4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID A RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR; 4 AMINOBUTYRIC ACID B RECEPTOR BLOCKING AGENT; 4 AMINOBUTYRIC ACID B RECEPTOR STIMULATING AGENT; BACLOFEN; BENZYL[3 [[1 (3,4 DICHLOROPHENYL)ETHYL]AMINO] 2 HYDROXYPROPYL]PHOSPHINIC ACID; BICUCULLINE; GLUTAMIC ACID; GLYCINE RECEPTOR ANTAGONIST; PICROTOXIN; RECEPTOR SUBUNIT; STRYCHNINE; TAURINE;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CHLORIDE CONDUCTANCE; CONCENTRATION RESPONSE; CONDUCTANCE; CONTROLLED STUDY; DRUG EFFECT; EXCITABILITY; INTERNEURON; MITRAL CELL; MOLECULAR MIMICRY; NERVE CELL; NERVE STIMULATION; NEUROTRANSMITTER RELEASE; NONHUMAN; OLFACTORY BULB; PATCH CLAMP; PRIORITY JOURNAL; RAT; SYNAPTIC INHIBITION; SYNAPTIC MEMBRANE;

ANIMALS; CELL MEMBRANE; DOSE-RESPONSE RELATIONSHIP, DRUG; ELECTRIC IMPEDANCE; GAMMA-AMINOBUTYRIC ACID; MEMBRANE POTENTIALS; NEURAL INHIBITION; NEURONS; OLFACTORY BULB; OLFACTORY NERVE; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; SYNAPTIC TRANSMISSION; TAURINE;

EID: 1542351157     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2003.12.032     Document Type: Article

References (88)

1. Aroniadou-Anderjaska V., Ennis M., Shipley M.T. Glomerular synaptic responses to olfactory nerve input in rat olfactory bulb slices. Neuroscience. 79:1997;425-434.
2. B heteroreceptors. J Neurophysiol. 84:2000;1194-1203.
3. Banay-Schwartz M., Lajtha A., Palkovits M. Changes with aging in the levels of amino acids in rat CNS structural elements I. glutamate and related amino acids. Neurochem Res. 14:1989;555-562.
4. Banay-Schwartz M., Lajtha A., Palkovits M. Changes with aging in the levels of amino acids in rat CNS structural elements Ii. taurine and small neutral amino acids. Neurochem Res. 14:1989;563-570.
5. Bardoni R., Magherini P.C., Belluzzi O. Excitatory synapses in the glomerular triad of frog olfactory bulb in vitro. Neuroreport. 7:1996;1851-1855.
6. Berkowicz D.A., Trombley P.Q., Shepherd G.M. Evidence for glutamate as the olfactory receptor cell neurotransmitter. J Neurophysiol. 71:1994;2557-2561.
7. Bianchi L., Colivicchi M.A., Bolam J.P., Della Corte L. The release of amino acids from rat neostriatum and substantia nigra in vivo A dual microdialysis probe analysis. Neuroscience. 87:1998;171-180.
8. B receptors. Trends Neurosci. 24:2001;277-282.
9. B receptors in the rat olfactory bulb. Neurosci Lett. 274:1999;195-198.
10. Bowery N.G., Hill D.R., Hudson A.L., Doble A., Middlemiss D.N., Shaw J., Turnbull M. Baclofen decreases neurotransmitter release in the mammalian CNS by an action at a novel GABA receptor. Nature. 283:1980;92-94.
11. B receptor site distribution in the rat central nervous system. Neuroscience. 20:1987;365-383.
12. Bufler J., Zufall F., Franke C., Hatt H. Patch-clamp recordings of spiking and nonspiking interneurons from rabbit olfactory bulb slices Gaba- and other transmitter receptors. J Comp Physiol A. 170:1992;153-159.
13. A receptors in mammalian brain in vitro. Eur J Pharmacol. 207:1991;9-16.
14. Cash D.J., Subbarao K. Channel opening of γ-aminobutyric acid receptor from rat brain Molecular mechanisms of the receptor response. Biochemistry. 26:1987;7562-7570.
15. Chao T.I., Kasa P., Wolff J.R. Distribution of astroglia in glomeruli of the rat main olfactory bulb Exclusion from the sensory subcompartment of neuropil. J Comp Neurol. 388:1997;191-210.
16. Chen X.-C., Pan Z.-L., Liu D.-S., Han X. Effect of taurine on human fetal neuron cells Proliferation and differentiation. Schaffer S., Lombardini J.B., Huxtable R.J. Taurine 3: cellular and regulatory mechanisms. 1998;397-403 Plenum Press, New York.
17. Chen W.R., Xiong W., Shepherd G.M. Analysis of relations between NMDA receptors and GABA release at olfactory bulb reciprocal synapses. Neuron. 25:2000;625-633.
18. B binding sites in the rat central nervous system A quantitative autoradiographic study. Neuroscience. 34:1990;341-357.
19. 14C]-taurine in eight areas of the rat central nervous system. Brain Res. 76:1974;447-459.
20. b receptors in the ca1 region of rat hippocampus. Neuropharmacology. 32:1993;1071-1073.
21. B receptors in rat hippocampal CA1 area. Brain Res. 864:2000;298-307.
22. Didier A., Ottersen O.P., Storm-Mathisen J. Differential subcellular distribution of glutamate and taurine in primary olfactory neurons. Neuroreport. 6:1994;145-148.
23. B-mediated action in the frog olfactory bulb makes odor responses more salient. Neuroscience. 97:2000;771-777.
24. Edwards F.A., Konnerth A., Sakmann B., Takahashi T. A thin slice preparation for patch clamp recordings from neurons of the mammalian central nervous system. Eur J Physiol. 414:1989;600-612.
25. Ennis M., Zimmer L.A., Shipley M.T. Olfactory nerve stimulation activates rat mitral cells via NMDA and non-NMDA receptors in vitro. Neuroreport. 7:1996;989-992.
26. Frederickson R.C., Neuss M., Morzorati S.L., McBride W.J. A comparison of the inhibitory effects of taurine and GABA on identified Purkinje cells and other neurons in the cerebellar cortex of the rat. Brain Res. 145:1978;117-126.
27. A-receptor heterogeneity in the adult rat brain Differential regional and cellular distribution of seven major subunits. J Comp Neurol. 359:1995;154-194.
28. Gall C.M., Hendry S.H., Seroogy K.B., Jones E.G., Haycock J.W. Evidence for coexistence of GABA and dopamine in neurons of the rat olfactory bulb. J Comp Neurol. 266:1987;307-318.
29. Halász N. The vertebrate olfactory system. 1990;Académiai Kiadó Budapest. pp 118-150.
30. - conductance in substantia nigra dopamine neurons. Brain Res. 571:1992;103-108.
31. Huxtable R.J. Taurine in the central nervous system and the mammalian actions of taurine. Prog Neurobiol. 32:1989;471-533.
32. B receptors inhibit dendrodendritic transmission in the rat olfactory bulb. J Neurosci. 23:2003;2032-2039.
33. Jacobson I., Hamberger A. Veratridine-induced release in vivo and in vitro of amino acids in the rabbit olfactory bulb. Brain Res. 299:1984;103-112.
34. Kamisaki Y., Maeda K., Ishimura M., Omura H., Itoh T. Effects of taurine on depolarization-evoked release of amino acids from rat cortical synaptosomes. Brain Res. 627:1993;181-185.
35. Kamisaki Y., Wada K., Nakamoto K., Itoh T. Effects of taurine on GABA release from synaptosomes of rat olfactory bulb. Amino Acids. 10:1996;49-57.
36. Kasowski H.J., Kim H., Greer C.A. Compartmental organization of the olfactory bulb glomerulus. J Comp Neurol. 407:1999;261-274.
37. B-receptor subtypes assemble into functional heteromeric complexes. Nature. 396:1998;683-687.
38. Keller A., Yagodin S., Aroniadou-Anderjaska V., Zimmer L.A., Ennis M., Sheppard N.F. Jr, Shipley M.T. Functional organization of rat olfactory bulb glomeruli revealed by optical imaging. J Neurosci. 18:1998;2602-2612.
39. Kosaka T., Hataguchi Y., Hama K., Nagatsu I., Wu J.-Y. Coexistence immunoreactivities for glutamic acid decarboxylase and tyrosine hydroxylase in some neurons in the periglomerular region of the rat main olfactory bulb Possible coexistence of gamma-aminobutyric acid (gaba) and dopamine. Brain Res. 343:1985;166-171.
40. Kratskin I., Belluzzi O. Immunohistochemical localization of the taurine-synthesizing enzyme in the rat olfactory bulb. Chem Senses. 27:(A-):2002;46.
41. Kratskin I., Belluzzi O. Anatomy and neurochemistry of the olfactory bulb. Doty R.L. Handbook of olfaction and gustation. 2003;139-164 M. Dekker, New York.
42. Kratskin I.L., Rio J.P., Kenigfest N.B., Doty R.L., Repérant J. A light and electron microscopic study of taurine-like immunoreactivity in the main olfactory bulb of frogs. J Chem Neuroanat. 18:2000;87-101.
43. A receptor subunit messenger RNAs in the rat brain 2. olfactory bulb and cerebellum. J Neurosci. 12:1992;1063-1076.
44. Luskin M.B. Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron. 11:1993;173-189.
45. Maar T., Morán J., Schousboe A., Pasantes-Morales H. Taurine deficiency in dissociated mouse cerebellum cultures affects neuronal migration. Int J Neurosci. 13:1995;491-502.
46. A receptor channel complex. Semin Neurosci. 3:1991;219-230.
47. B receptors in the rat central nervous system. J Comp Neurol. 405:1999;299-321.
48. Margolis F.L. Carnosine in the primary olfactory pathway. Science. 184:1974;909-911.
49. McCool B.A., Botting S.K. Characterization of strychnine-sensitive glycine receptors in acutely isolated adult rat basolateral amygdala neurons. Brain Res. 859:2000;341-351.
50. McIlwain H., Bachelard H.S. Biochemistry and the central nervous system. 1985;Churchill Livingstone, Edinburgh. p. 30.
51. Miller R.J. Presynaptic receptors. Annu Rev Pharmacol Toxicol. 38:1998;201-227.
52. Misgeld U., Deisz R.A., Dodt H.U., Lux H.D. The role of chloride transport in postsynaptic inhibition of hippocampal neurons. Science. 232:1986;1413-1415.
53. Montague A.A., Greer C.A. Differential distribution of ionotropic glutamate receptor subunits in the rat olfactory bulb. J Comp Neurol. 405:1999;233-246.
54. Mori K. Membrane and synaptic properties of identified neurons in the olfactory bulb. Prog Neurobiol. 29:1987;275-320.
55. Mugnaini E., Wouterlood F.G., Dahl A.-L., Oertel W.H. Immunocytochemical identification of GABAergic neurons in the main olfactory bulb of the rat. Arch Ital Biol. 122:1984;83-113.
56. Namima M., Okamoto K., Sakai Y. Modulatory action of taurine on the release of GABA in cerebellar slices of the guinea pig. J Neurochem. 40:1983;1-9.
57. Neher E. Correction for liquid junction potentials in patch clamp experiments. Rudy B., Iverson L.E. Methods in enzymology: ion channels, Vol. 207. 1992;123-131 Academic Press, San Diego.
58. Newland C.F., Cull-Candy S.G. On the mechanism of action of picrotoxin on GABA receptor channels in dissociated sympathetic neurons of the rat. J Physiol (Lond). 447:1992;191-213.
59. B-mediated inhibition of transmission from the olfactory nerve to mitral cells in the rat olfactory bulb. Brain Res Bull. 35:1994;119-123.
60. - conductance of cerebellar Purkinje cell dendrites in vitro. Brain Res. 259:1983;319-323.
61. b receptors. Eur J Pharmacol. 187:1990;27-38.
62. Palacín M., Estévez R., Bertran J., Zorzano A. Molecular biology of mammalian plasma membrane amino acid transporters. Physiol Rev. 78:1998;969-1054.
63. B receptor-mediated inhibition of mitral/tufted cell activity in the rat olfactory bulb A whole-cell patch-clamp study in vitro. Neuroscience. 111:2002;241-250.
64. B receptors in the rat olfactory bulb. Soc Neurosci Abstr Program No. 706.16.
65. A receptor subunits in the rat CNS. J Comp Neurol. 326:1992;193-216.
66. Pinching A.J., Powell T.P.S. The neuropil of the glomeruli of the olfactory bulb. J Cell Sci. 9:1971;347-377.
67. Potapov A.A. Baclofen inhibition of synaptic transmission in frog olfactory bulb glomeruli. Neirofiziologia. 17:1985;834-837.
68. 3H taurine accumulation in the rat retina, pituitary, and brain. Glia. 37:2002;153-168.
69. Price J.L., Powell T.P.S. The synaptology of the granule cells of the olfactory bulb. J Cell Sci. 7:1970;125-155.
70. A receptor subunit for benzodiazepine pharmacology. Nature. 338:1989;582-585.
71. Puopolo M., Belluzzi O. Inhibitory synapses among interneurons in the glomerular layer of rat and frog olfactory bulbs. J Neurophysiol. 80:1998;344-349.
72. Puopolo M., Belluzzi O. Functional heterogeneity of periglomerular cells in the rat olfactory bulb. Eur J Neurosci. 10:1998;1073-1083.
73. Puopolo M., Kratskin I., Belluzzi O. Direct inhibitory effect of taurine on relay neurons of the rat olfactory bulb in vitro. Neuroreport. 9:1998;2319-2322.
74. 35S]-t-butyl-bicyclophosphorothionate (TBPS) to rat brain synaptic membranes. Neuropharmacology. 34:1995;1607-1613.
75. Ross C.D., Godfrey D.A., Parli J.A. Amino acid concentrations and selected enzyme activities in rat auditory, olfactory, and visual systems. Neurochem Res. 20:1995;1483-1490.
76. Schoppa N.E., Kinzie J.M., Sahara Y., Segerson T.P., Westbrook G.L. Dendrodendritic inhibition in the olfactory bulb is driven by NMDA receptors. J Neurosci. 18:1998;6790-6802.
77. Shepherd G.M., Greer C.A. Olfactory bulb. Shepherd G.M. The synaptic organization of the brain. 1998;159-203 Oxford University Press, New York.
78. Shipley M.T., Ennis M. Functional organization of olfactory system. J Neurobiol. 30:1996;123-176.
79. Solís J.M., Herranz A.S., Herreras O., Lerma J., del Rio M. Low chloride-dependent release of taurine by a furosemide-sensitive process in the in vivo rat hippocampus. Neuroscience. 24:1988;885-891.
80. Taber K.H., Lin C.T., Liu J.W., Thalmann R.H., Wu J.-Y. Taurine in hippocampus Localization and postsynaptic action. Brain Res. 386:1986;113-121.
81. Thompson S.M., Deisz R.A., Prince D.A. Relative contributions of passive equilibrium and active transport to the distribution of chloride in mammalian cortical neurons. J Neurophysiol. 60:1988;105-124.
82. Toida K., Kosaka K., Heizmann C.W., Kosaka T. Chemically defined neuron groups and their subpopulations in the glomerular layer of the rat main olfactory bulb Iii. structural features of calbindin d28k-immunoreactive neurons. J Comp Neurol. 392:1998;179-198.
83. Trombley P.Q., Shepherd G.M. Synaptic transmission and modulation in the olfactory bulb. Curr Opin Neurobiol. 3:1993;540-547.
84. Trombley P.Q., Shepherd G.M. Glycine exerts potent inhibitory actions on mammalian olfactory bulb neurons. J Neurophysiol. 71:1994;761-767.
85. Wachowiak M., Cohen L.B. Presynaptic inhibition of primary olfactory afferents mediated by different mechanisms in lobster and turtle. J Neurosci. 19:1999;8808-8817.
86. Wachowiak M., Heyward P.M., Puche A.C., Shipley M.T. Regulation of receptor neuron input to the mouse olfactory bulb mediated by suppression of presynaptic calcium influx. Chem Senses. 27:2002;A-89.
87. Wellis D.P., Kauer J.S. GABAergic and glutamatergic synaptic input to identified granule cells in salamander olfactory bulb. J Physiol (Lond). 475:1994;419-430.
88. Ye G.I., Tse A.C.O., Yung W.-H. Taurine inhibits rat substantia nigra pars reticulata neurons by activation of GABA- and glycine-linked chloride conductance. Brain Res. 749:1997;175-179.