Nicotinic α7 receptor clusters on hippocampal GABAergic neurons: Regulation by synaptic activity and neurotrophins

Journal of Neuroscience

Volumn 22, Issue 18, 2002, Pages 7903-7912

  Kawai, Hideki ^a   Zago, Wagner ^a   Berg, Darwin K ^a  

^a NEUROBIOLOGY SECTION   (United States)

Author keywords

Acetylcholine; BDNF; Bungarotoxin; Hippocampal; NGF; Nicotinic; Receptors

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; ALPHA BUNGAROTOXIN; BRAIN ANTIBODY; BRAIN DERIVED NEUROTROPHIC FACTOR ANTIBODY; BUNGAROTOXIN RECEPTOR; GENE PRODUCT; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR BLOCKING AGENT; NERVE GROWTH FACTOR ANTIBODY; NEUROTROPHIN; NICOTINIC RECEPTOR; TETRODOTOXIN; TUBOCURARINE CHLORIDE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CHOLINERGIC TRANSMISSION; DENDRITE; ELECTRIC ACTIVITY; GABAERGIC SYSTEM; GENE EXPRESSION; HIPPOCAMPUS; IMMUNOHISTOCHEMISTRY; INTERNEURON; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RECEPTOR BLOCKING; SIGNAL TRANSDUCTION; SYNAPSE;

EID: 0037107192     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.22-18-07903.2002     Document Type: Article

References (52)

1. Alkondon M, Albuquerque EX (2001) Nicotinic acetylcholine receptors α7 and α4β2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus. J Neurophysiol 86:3043-3055.
2. Alkondon M, Pereira EFR, Barbosa CTF, Albuquerque EX (1997a) Neuronal nicotinic acetylcholine receptor activation modulates γ-aminobutyric acid release from CA1 neurons of rat hippocampal slices. J Pharmacol Exp Ther 283:1396-1411.
3. Alkondon M, Pereira EFR, Cortes WS, Maelicke A, Albuquerque EX (1997b) Choline is a selective agonist of α7 nicotinic acetylcholine receptors in the rat brain neurons. Eur J Neurosci 9:2734-2742.
4. Alkondon M, Pereira EFR, Albuquerque EX (1998) α-Bungarotoxinand methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices. Brain Res 810:257-263.
5. Barrantes GE, Roger AT, Lindstrom J, Wonnacott S (1995) α-Bungarotoxin binding sites in rat hippocampal and cortical cultures: Initial characterization, colocalization with α7 subunits and upregulation by chronic nicotine treatment. Brain Res 672:228-236.
6. Bertrand D, Galzi JL, Devillers-Thiéry A, Bertrand S, Changeux JP (1993) Mutations at two distinct sites within the channel domain M2 alter calcium permeability of neuronal α7 nicotinic receptor. Proc Natl Acad Sci USA 90:6971-6975.
7. Bolton MM, Pittman AJ, Lo DC (2000) Brain-derived neurotrophic factor differentially regulates excitatory and inhibitory synaptic transmission in hippocampal cultures. J Neurosci 20:3221-3232.
8. Buhler AV, Dunwiddie TV (2001) Regulation of the activity of hippocampal stratum oriens interneurons by α7 nicotinic acetylcholine receptors. Neuroscience 106:55-67.
9. Buhler AV, Dunwiddie TV (2002) α7 Nicotinic acetylcholine receptors on GABAergic interneurons evoke dendritic and somatic inhibition of hippocampal neurons. J Neurophysiol 87:548-557.
10. Cline HT (2001) Dendritic arbor development and synaptogenesis. Curr Opin Neurobiol 11:118-126.
11. Descarries L (1998) The hypothesis of an ambient level of acetylcholine in the central nervous system. J Physiol (Paris) 92:215-220.
12. Descarries L, Gisiger V, Steriade M (1997) Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53:603-625.
13. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG, Fine A (2001) Ultrastructural distribution of the α7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21:7993-8003.
14. Fiala JC, Feinberg M, Popov V, Harris KM (1998) Synaptogenesis via dendritic filopodia in developing hippocampal area CA1. J Neurosci 18:8900-8911.
15. Frazier CJ, Buhler AV, Weiner JL, Dunwiddie TV (1998) Synaptic potentials mediated via a-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons. J Neurosci 18:8228-8235.
16. Freund TF, Buzsaki G (1996) Interneurons of the hippocampus. Hippocampus 6:347-470.
17. Frotscher M, Leranth C (1985) Cholinergic innervation of the rat hippocampus as revealed by choline acetyltransferase immunocytochemistry: A combined light and electron microscopic study. J Comp Neurol 239:237-246.
18. Fujii S, Ji Z, Sumikawa K (2000) Inactivation of α7 ACh receptors and activation of non-α7 ACh receptors both contribute to long term potentiation induction in the hippocampal CA1 region. Neurosci Lett 286:134-138.
19. Ganguly K, Schinder AF, Wong ST, Poo Mm (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105:521-532.
20. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383:713-716.
21. Hartmann M, Heumann R, Lessmann V (2001) Synaptic secretion of BDNF after high-frequency stimulation of glutamatergic synapses. EMBO J 20:5887-5897.
22. Hefft S, Hulo S, Bertrand D, Muller D (1999) Synaptic transmission at nicotinic acetylcholine receptors in rat hippocampal organotypic cultures and slices. J Physiol (Lond) 515:769-776.
23. Ji D, Dani JA (2000) Inhibition and disinhibition of pyramidal neurons by activation of nicotinic receptors on hippocampal interneurons. J Neurophysiol 83:2682-2690.
24. Ji D, Lape R, Dani JA (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31:131-141.
25. Jones S, Sudweeks S, Yakel JL (1999) Nicotinic receptors in the brain: Correlating physiology with function. Trends Neurosci 22:555-561.
26. Jontes JD, Smith SJ (2000) Filopodia, spines, and the generation of synaptic diversity. Neuron 27:11-14.
27. Kawai H, Berg DK (2001) Nicotinic acetylcholine receptors containing α7 subunits on rat cortical neurons do not undergo long-lasting inactivation even when up-regulated by chronic nicotine exposure. J Neurochem 78:1367-1378.
28. Kovalchuk Y, Hanse E, Kafitz KW, Konnerth A (2001) Postsynaptic induction of BDNF-mediated long-term potentiation. Science 295:1729-1734.
29. Lauterborn JC, Lynch G, Vanderklish P, Arai A, Gall CM (2000) Positive modulation of AMPA receptors increases neurotrophin expression by hippocampal and cortical neurons. J Neurosci 20:8-21.
30. Levy RB, Aoki C (2002) α7 Nicotinic acetylcholine receptors occur at postsynaptic densities of AMPA receptor-positive and -negative excitatory synapses in rat sensory cortex. J Neurosci 22:5001-5015.
31. Liu Y, Ford B, Mann MA, Fischbach GD (2001) Neuregulins increase α7 nicotinic acetylcholine receptors and enhance excitatory synaptic transmission in GABAergic interneurons of the hippocampus. J Neurosci 21:5660-5669.
32. Loeb JA, Fischbach GD (1997) Neurotrophic factors increase neuregulin expression in embryonic ventral spinal cord neurons. J Neurosci 17:1416-1424.
33. Loeb JA, Hmadcha A, Fischbach GD, Land SJ, Zakarian VL (2002) Neuregulin expression at neuromuscular synapses is modulated by synaptic activity and neurotrophic factors. J Neurosci 22:2206-2214.
34. Maggi L, Sher E, Cherubini E (2001) Regulation of GABA release by nicotinic acetylcholine receptors in the neonatal rat hippocampus. J Physiol (Lond) 536:89-100.
35. McAllister AK, Katz LC, Lo DC (1999) Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295-318.
36. McKinney M, Coyle JT, Hedreen JC (1983) Topographic analysis of the innervation of the rat neocortex and hippocampus by the basal forebrain cholinergic system. J Comp Neurol 217:103-121.
37. Murthy VN, Schikorski T, Stevens CF, Zhu Y (2001) Inactivity produces increases in neurotransmitter release and synapse size. Neuron 32:673-682.
38. Olbrich HG, Braak H (1985) Ratio of pyramidal cells versus non-pyramidal cells in sector CA1 of the human Ammon's horn. Anat Embryol 173:105-110.
39. Paysan J, Coggan JS, Conroy WG, Berg DK (2000) The neurofilament infrastructure of a developing presynaptic calyx. J Comp Neurol 425:284-294.
40. Peng X, Gerzanich V, Anand R, Wang F, Lindstrom J (1997) Chronic nicotine treatment up-regulates α3 and α7 acetylcholine receptor subtypes expressed by the human neuroblastoma cell line SH-SY5Y. Mol Pharmacol 51:776-784.
41. Radcliffe KA, Dani JA (1998) Nicotinic stimulation produces multiple forms of increased glutamatergic synaptic transmission. J Neurosci 18:7075-7083.
42. Rao A, Cha EM, Craig AM (2000) Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J Neurosci 20:8344-8353.
43. 125I]bungarotoxin binding and α7 nicotinic subunit immunoreactivity during the development of rat hippocampal neurons in culture. Neurosci Lett 222:179-182.
44. Schinder AF, Poo MM (2000) The neurotrophin hypothesis for synaptic plasticity. Trends Neurosci 23:639-645.
45. Schuman EM (1999) Neurotrophin regulation of synaptic transmission. Curr Opin Neurobiol 9:105-109.
46. Seguela P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain α7: A nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604.
47. Turrigiano GG, Nelson SB (2000) Hebb and homeostasis in neuronal plasticity. Curr Opin Neurobiol 10:358-364.
48. Turrini P, Casu MA, Wong TP, De Koninck Y, Ribeiro-Da-Silva A, Cuello AC (2001) Cholinergic nerve terminals establish classical synapses in the rat cerebral cortex: Synaptic pattern and age-related atrophy. Neuroscience 105:277-285.
49. Tyler WJ, Pozzo-Miller LD (2001) BDNF enhances quantal neurotransmitter release and increases the number of docked vesicles at the active zones of hippocampal excitatory synapses. J Neurosci 21:4249-4258.
50. Zafra F, Castren E, Thoenen H, Lindholm D (1991) Interplay between glutamate and gamma-aminobutyric acid transmitter systems in the physiological regulation of brain-derived neurotrophic factor and nerve growth factor synthesis in hippocampal neurons. Proc Natl Acad Sci USA 88:10037-10041.
51. Zarei MM, Radcliffe KA, Chen D, Patrick JW, Dani JA (1999) Distributions of nicotinic acetylcholine receptor α7 and β2 subunits on cultured hippocampal neurons. Neuroscience 88:755-764.
52. Zoli M, Jansson A, Sykova E, Agnati LF, Fuxe K (1999) Volume transmission in the CNS and its relevance for neuropsychopharmacology. Trends Pharmacol Sci 20:142-150.