A novel mechanism for nicotinic potentiation of glutamatergic synapses

Journal of Neuroscience

Volumn 34, Issue 6, 2014, Pages 2051-2064

  Halff, Andrew W ^a   Gómez Varela, David ^a,b   John, Danielle ^a   Berg, Darwin K ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MAX PLANCK INSTITUTE OF EXPERIMENTAL MEDICINE   (Germany)

Author keywords

FRAP; GluA1; Hippocampus; nAChR; Nicotine; Plasticity

Indexed keywords

AMPA RECEPTOR; BUNGAROTOXIN RECEPTOR; GLUTAMATE RECEPTOR 1; GLUTAMATE RECEPTOR 2; NEUROTRANSMITTER; NICOTINE; POSTSYNAPTIC DENSITY PROTEIN 95; PROTEIN ZO1; SHORT HAIRPIN RNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CALCIUM SIGNALING; CELL CULTURE; CONTROLLED STUDY; DENDRITIC SPINE; EMBRYO; EXOCYTOSIS; FEMALE; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GLUTAMATERGIC TRANSMISSION; HIPPOCAMPAL CA1 REGION; MALE; MOUSE; NICOTINIC POTENTIATION; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE; SYNAPTIC POTENTIAL; SYNAPTIC TRANSMISSION;

FRAP; GLUA1; HIPPOCAMPUS; NACHR; NICOTINE; PLASTICITY;

ANIMALS; ANIMALS, NEWBORN; EXCITATORY POSTSYNAPTIC POTENTIALS; FEMALE; GLUTAMIC ACID; HIPPOCAMPUS; MALE; MICE; MICE, INBRED C57BL; NICOTINE; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; SYNAPSES;

EID: 84893461885     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2795-13.2014     Document Type: Article

References (77)

1. Ashby MC, Maier SR, Nishimune A, Henley JM (2006) Lateral diffusion drives constitutive exchange of AMPA receptors at dendritic spines and is regulated by spine morphology. J Neurosci 26: 7046-7055. CrossRef Medline
2. Atallah BV, Scanziani M (2009) Instantaneous modulation of gamma oscillation frequency by balancing excitation with inhibition. Neuron 62: 566-577. CrossRef Medline
3. Bats C, Groc L, Choquet D (2007) The interaction between Stargazin and PSD-95 regulates AMPA receptor surface trafficking. Neuron 53: 719-734. CrossRef Medline
4. 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 alpha 7 nicotinic receptor. Proc Natl Acad Sci U S A 90: 6971-6975. CrossRef Medline
5. Bliss TV, Collingridge GL (1993) A synaptic model of memory: long-term potentiation in the hippocampus. Nature 361: 31-39. CrossRef Medline
6. Borgdorff AJ, Choquet D (2002) Regulation of AMPA receptor lateral movements. Nature 417: 649-653. CrossRef Medline
7. Campbell NR, Fernandes CC, Halff AW, Berg DK (2010) Endogenous signaling through alpha7-containing nicotinic receptors promotes maturation and integration of adult-born neurons in the hippocampus. J Neurosci 30: 8734-8744. CrossRef Medline
8. Chang KT, Berg DK (2001) Voltage-gated channels block nicotinic regulation of CREB phosphorylation and gene expression in neurons. Neuron 32: 855-865. CrossRef Medline
9. Chen L, Chetkovich DM, Petralia RS, Sweeney NT, Kawasaki Y, Wenthold RJ, Bredt DS, Nicoll RA (2000) Stargazin regulates synaptic targeting of AMPA receptors by two distinct mechanisms. Nature 408: 936-943. CrossRef Medline
10. Conroy WG, Liu Z, Nai Q, Coggan JS, Berg DK (2003) PDZ-containing proteins provide a functional postsynaptic scaffold for nicotinic receptors in neurons. Neuron 38: 759-771. CrossRef Medline
11. Dajas-Bailador F, Wonnacott S (2004) Nicotinic acetylcholine receptors and the regulation of neuronal signalling. Trends Pharmacol Sci 25: 317-324. CrossRef Medline
12. Dani JA, Ji D, Zhou FM (2001) Synaptic plasticity and nicotine addiction. Neuron 31: 349-352. CrossRef Medline
13. De Biasi M, Dani JA (2011) Reward, addiction, withdrawal to nicotine. Annu Rev Neurosci 34: 105-130. CrossRef Medline
14. Descarries L, Gisiger V, Steriade M (1997) Diffuse transmission by acetylcholine in the CNS. Prog Neurobiol 53: 603-625. CrossRef Medline
15. De Simoni A, Griesinger CB, Edwards FA (2003) Development of rat CA1 neurones in acute versus organotypic slices: role of experience in synaptic morphology and activity. J Physiol 550: 135-147. CrossRef Medline
16. Ehrlich I, Malinow R (2004) Postsynaptic density 95 controls AMPA receptor incorporation during long-term potentiation and experience-driven synaptic plasticity. J Neurosci 24: 916-927. CrossRef Medline
17. Elias GM, Funke L, Stein V, Grant SG, Bredt DS, Nicoll RA (2006) Synapsespecific and developmentally regulated targeting of AMPA receptors by a family of MAGUK scaffolding proteins. Neuron 52: 307-320. CrossRef Medline
18. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG, Fine A (2001) Ultrastructural distribution of the 7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21: 7993-8003. Medline
19. Farías GG, Vallés AS, Colombres M, Godoy JA, Toledo EM, Lukas RJ, Barrantes FJ, Inestrosa NC (2007) Wnt-7a induces presynaptic colocalization of alpha 7-nicotinic acetylcholine receptors and adenomatous polyposis coli in hippocampal neurons. J Neurosci 27: 5313-5325. CrossRef Medline
20. Feldman DE (2012) The spike-timing dependence of plasticity. Neuron 75: 556-571. CrossRef Medline
21. Fernandes CC, Berg DK, Gómez-Varela D (2010) Lateral mobility of nicotinic acetylcholine receptors on neurons is determined by receptor composition, local domain, and cell type. J Neurosci 30: 8841-8851. CrossRef Medline
22. Fujii S, Ji Z, Morita N, Sumikawa K (1999) Acute and chronic nicotine exposure differentially facilitate the induction of LTP. Brain Res 846: 137-143. CrossRef Medline
23. Galan A, Laird JM, Cervero F (2004) In vivo recruitment by painful stimuli of AMPA receptor subunits to the plasma membrane of spinal cord neurons. Pain 112: 315-323. CrossRef Medline
24. Goetze B, Grunewald B, Baldassa S, Kiebler M (2004) Chemically controlled formation of a DNA/calcium phosphate coprecipitate: application for transfection of mature hippocampal neurons. J Neurobiol 60: 517-525. CrossRef Medline
25. Gómez-Varela D, Schmidt M, Schoellerman J, Peters EC, Berg DK (2012) PMCA2 via PSD-95 controls calcium signaling by α7-containing nicotinic acetylcholine receptors on aspiny interneurons. J Neurosci 32: 6894-6905. CrossRef Medline
26. Gray R, Rajan AS, Radcliffe KA, Yakehiro M, Dani JA (1996) Hippocampal synaptic transmission enhanced by low concentrations of nicotine. Nature 383: 713-716. CrossRef Medline
27. Greenberg ME, Thompson MA, Sheng M (1992) Calcium regulation of immediate early gene transcription. J Physiol Paris 86: 99-108. CrossRef Medline
28. Gu Z, Lamb PW, Yakel JL (2012) Cholinergic coordination of presynaptic and postsynaptic activity induces timing-dependent hippocampal synaptic plasticity. J Neurosci 32: 12337-12348. CrossRef Medline
29. Hayashi Y, Shi SH, Esteban JA, Piccini A, Poncer JC, Malinow R (2000) Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction. Science 287: 2262-2267. CrossRef Medline
30. Heine M, Groc L, Frischknecht R, Béïque JC, Lounis B, Rumbaugh G, Huganir RL, Cognet L, Choquet D (2008) Surface mobility of postsynaptic AMPARs tunes synaptic transmission. Science 320: 201-205. CrossRef Medline
31. Hu M, Lie QS, Chang KT, Berg DK (2002) Nicotinic regulation of CREB activation in hippocampal neurons by glutamatergic and nonglutamatergic pathways. Mol Cell Neurosci 21: 616-625. CrossRef Medline
32. Hukkanen J, Jacob P 3rd, Benowitz NL (2005) Metabolism and disposition kinetics of nicotine. Pharmacol Rev 57: 79-115. CrossRef Medline
33. Isaac JT, Nicoll RA, Malenka RC (1995) Evidence for silent synapses: implications for the expression of LTP. Neuron 15: 427-434. CrossRef Medline
34. Ji D, Lape R, Dani JA (2001) Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity. Neuron 31: 131-141. CrossRef Medline
35. Kawai H, Zago W, Berg DK (2002) Nicotinic alpha 7 receptor clusters on hippocampal GABAergic neurons: regulation by synaptic activity and neurotrophins. J Neurosci 22: 7903-7912. Medline
36. Kenney JW, Gould TJ (2008) Modulation of hippocampus-dependent learning and synaptic plasticity by nicotine. Mol Neurobiol 38: 101-121. CrossRef Medline
37. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26: 2000-2009. CrossRef Medline
38. Levin ED, Conners CK, Silva D, Hinton SC, Meck WH, March J (1998) Transdermal nicotine effects on attention. Psychopharmacology (Berl) 140: 135-141. CrossRef Medline
39. Liao D, Hessler NA, Malinow R (1995) Activation of postsynaptically silent synapses during pairing-induced LTP in CA1 region of hippocampal slice. Nature 375: 400-404. CrossRef Medline
40. Lois C, Hong EJ, Pease S, Brown EJ, Baltimore D (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295: 868-872. CrossRef Medline
41. Lozada AF, Wang X, Gounko NV, Massey KA, Duan J, Liu Z, Berg DK (2012a) Glutamatergic synapse formation is promoted byα7-containing nicotinic acetylcholine receptors. J Neurosci 32: 7651-7661. CrossRef Medline
42. Lozada AF, Wang X, Gounko NV, Massey KA, Duan J, Liu Z, Berg DK (2012b) Induction of dendritic spines by β2-containing nicotinic receptors. J Neurosci 32: 8391-8400. CrossRef Medline
43. Lu W, Shi Y, Jackson AC, Bjorgan K, During MJ, Sprengel R, Seeburg PH, Nicoll RA (2009) Subunit composition of synaptic AMPA receptors revealed by a single-cell genetic approach. Neuron 62: 254-268. CrossRef Medline
44. Maggi L, Le Magueresse C, Changeux JP, Cherubini E (2003) Nicotine activates immature "silent" connections in the developing hippocampus. Proc Natl Acad Sci U S A 100: 2059-2064. CrossRef Medline
45. Makino H, Malinow R (2009) AMPA receptor incorporation into synapses during LTP: the role of lateral movement and exocytosis. Neuron 64: 381-390. CrossRef Medline
46. Makino H, Malinow R (2011) Compartmentalized versus global synaptic plasticity on dendrites controlled by experience. Neuron 72: 1001-1011. CrossRef Medline
47. Malinow R, Malenka RC (2002) AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 25: 103-126. CrossRef Medline
48. Mansvelder HD, McGehee DS (2002) Cellular and synaptic mechanisms of nicotine addiction. J Neurobiol 53: 606-617. CrossRef Medline
49. Mayford M, Siegelbaum SA, Kandel ER (2012) Synapses and memory storage. Cold Spring Harb Perspect Biol 4: pi: a005751. Medline
50. McGehee DS, Heath MJ, Gelber S, Devay P, Role LW (1995) Nicotine enhancement of fast excitatory synaptic transmission in CNS by presynaptic receptors. Science 269: 1692-1696. CrossRef Medline
51. Miesenböck G, De Angelis DA, Rothman JE (1998) Visualizing secretion and synaptic transmission with pH-sensitive green fluorescent proteins. Nature 394: 192-195. CrossRef Medline
52. Mondin M, Labrousse V, Hosy E, Heine M, Tessier B, Levet F, Poujol C, Blanchet C, Choquet D, Thoumine O (2011) Neurexin-neuroligin adhesions capture surface-diffusing AMPA receptors through PSD-95 scaffolds. J Neurosci 31: 13500-13515. CrossRef Medline
53. Neff RA 3rd, Conroy WG, Schoellerman JD, Berg DK (2009) Synchronous and asynchronous transmitter release at nicotinic synapses are differentially regulated by postsynaptic PSD-95 proteins. J Neurosci 29: 15770-15779. CrossRef Medline
54. Nicoll RA, Malenka RC (1999) Expression mechanisms underlying NMDA receptor-dependent long-term potentiation. Ann N Y Acad Sci 868: 515-525. CrossRef Medline
55. Opazo P, Choquet D (2011) A three-step model for the synaptic recruitment of AMPA receptors. Mol Cell Neurosci 46: 1-8. CrossRef Medline
56. Opazo P, Labrecque S, Tigaret CM, Frouin A, Wiseman PW, De Koninck P, Choquet D (2010) CaMKII triggers the diffusional trapping of surface AMPARs through phosphorylation of stargazin. Neuron 67: 239-252. CrossRef Medline
57. Opazo P, Sainlos M, Choquet D (2012) Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol 22: 453-460. CrossRef Medline
58. Passafaro M, Sala C, Niethammer M, Sheng M (1999) Microtubule binding by CRIPT and its potential role in the synaptic clustering of PSD-95. Nat Neurosci 2: 1063-1069. CrossRef Medline
59. Peeke SC, Peeke HV (1984) Attention, memory and cigarette smoking. Psycopharmacology (Berl) 84: 205-215. CrossRef Medline
60. Pepeu G, Giovannini MG (2004) Changes in acetylcholine extracellular levels during cognitive processes. Learn Mem 11: 21-27. CrossRef Medline
61. Petrini EM, Lu J, Cognet L, Lounis B, Ehlers MD, Choquet D (2009) Endocytic trafficking and recycling maintain a pool of mobile surface AMPA receptors required for synaptic potentiation. Neuron 63: 92-105. CrossRef Medline
62. Placzek AN, Zhang TA, Dani JA (2009) Nicotinic mechanisms influencing synaptic plasticity in the hippocampus. Acta Pharmacol Sin 30: 752-760. CrossRef Medline
63. Qin XF, An DS, Chen IS, Baltimore D (2003) Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc Natl Acad Sci U S A 100: 183-188. CrossRef Medline
64. Rose JE, Mukhin AG, Lokitz SJ, Turkington TG, Herskovic J, Behm FM, Garg S, Garg PK (2010) Kinetics of brain nicotine accumulation in dependent and nondependent smokers assessed with PET and cigarettes containing 11C-nicotine. Proc Natl Acad Sci U S A 107: 5190-5195. CrossRef Medline
65. Sans N, Vissel B, Petralia RS, Wang YX, Chang K, Royle GA, Wang CY, O'Gorman S, Heinemann SF, Wenthold RJ (2003) Aberrant formation of glutamate receptor complexes in hippocampal neurons of mice lacking the GluR2 AMPA receptor subunit. J Neurosci 23: 9367-9373. Medline
66. Séguéla 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. Medline
67. Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76: 823-847. CrossRef Medline
68. Shi S, Hayashi Y, Esteban JA, Malinow R (2001) Subunit-specific rules governing AMPA receptor trafficking to synapses in hippocampal pyramidal neurons. Cell 105: 331-343. CrossRef Medline
69. Stoppini L, Buchs PA, Muller D (1991) A simple method for organotypic cultures of nervous tissue. J Neurosci 37: 173-182.
70. Tanaka H, Hirano T (2012) Visualization of subunit-specific delivery of glutamate receptors to postsynaptic membrane during hippocampal long-term potentiation. Cell Rep 1: 291-298. CrossRef Medline
71. Thiel CM, Fink GR (2008) Effects of the cholinergic agonist nicotine on reorienting of visual and special attention and top-down attentional control. Neuroscience 152: 381-390. CrossRef Medline
72. Umbriaco D, Garcia S, Beaulieu C, Descarries L (1995) Relational features of acetylcholine, noradrenaline, serotonin and GABA axon terminals in the stratum radiatum of adult rat hippocampus (CA1). Hippocampus 5: 605-620. CrossRef Medline
73. Wada E, Wada K, Boulter J, Deneris E, Heinemann S, Patrick J, Swanson LW (1989) Distribution of alpha2, alpha3, alpha4, and beta2 neuronal nicotinic receptor subunit mRNAs in the central nervous system: a hybridization histochemical study in the rat. J Comp Neurol 284: 314-335. CrossRef Medline
74. Whitlock JR, Heynen AJ, Shuler MG, Bear MF (2006) Learning induces long-term potentiation in the hippocampus. Science 313: 1093-1097. CrossRef Medline
75. Woods G, Zito K (2008) Preparation of gene gun bullets and biolistic transfection of neurons in slice culture. J Vis Exp 12: pii: 675.
76. Yakel JL (2012) Nicotinic ACh receptors in the hippocampus: role in excitability and plasticity. Nicotine Tob Res 14: 1249-1257. CrossRef Medline
77. Zarei MM, Radcliffe KA, Chen D, Patrick JW, Dani JA (1999) Distributions of nicotinic acetylcholine receptor alpha7 and beta2 subunits on cultured hippocampal neurons. Neuroscience 88: 755-764. CrossRef Medline