Presynaptic α7 nicotinic acetylcholine receptors enhance hippocampal mossy fiber glutamatergic transmission via PKA activation

Journal of Neuroscience

Volumn 34, Issue 1, 2014, Pages 124-133

  Cheng, Qing ^a   Yakel, Jerrel L ^a  

^a NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

4 CHLORO N (3 QUINUCLIDINYL) BENZAMIDE; BUNGAROTOXIN RECEPTOR; CALCIUM; CYCLIC AMP DEPENDENT PROTEIN KINASE; NICOTINE; UNCLASSIFIED DRUG;

ACTION POTENTIAL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM CURRENT; COGNITION; ELECTROPHYSIOLOGY; EXCITATORY POSTSYNAPTIC POTENTIAL; GLUTAMATERGIC TRANSMISSION; HIPPOCAMPAL CA3 REGION; HIPPOCAMPAL MOSSY FIBER; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; MALE; MOUSE; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP TECHNIQUE; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

EID: 84891412137     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.2973-13.2014     Document Type: Article

References (85)

1. Adams CE, Broide RS, Chen Y, Winzer-Serhan UH, Henderson TA, Leslie FM, Freedman R (2002) Development of the alpha7 nicotinic cholinergic receptor in rat hippocampal formation. Brain Res Dev Brain Res 139:175-187. CrossRef Medline
2. Albuquerque EX, Pereira EF, Alkondon M, Rogers SW (2009) Mammalian nicotinic acetylcholine receptors: from structure to function. Physiol Rev 89:73-120. CrossRef Medline
3. Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus: I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86. CrossRef Medline
4. Bancila V, Cordeiro JM, Bloc A, Dunant Y (2009) Nicotine-induced and depolarisation-induced glutamate release from hippocampus mossy fibre synaptosomes: two distinct mechanisms. J Neurochem 110:570-580. CrossRef Medline
5. Barrantes GE, Murphy CT, Westwick J, Wonnacott S (1995) Nicotine increases intracellular calcium in rat hippocampal neurons via voltagegated calcium channels. Neurosci Lett 196:101-104. CrossRef Medline
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 alpha 7 nicotinic receptor. Proc Natl Acad Sci U S A 90:6971-6975. CrossRef Medline
7. Bischofberger J, Engel D, Frotscher M, Jonas P (2006) Timing and efficacy of transmitter release at mossy fiber synapses in the hippocampal network. Pflugers Arch 453:361-372. CrossRef Medline
8. Bitner RS, Bunnelle WH, Anderson DJ, Briggs CA, Buccafusco J, Curzon P, Decker MW, Frost JM, Gronlien JH, Gubbins E, Li J, Malysz J, Markosyan S, Marsh K, Meyer MD, Nikkel AL, Radek RJ, Robb HM, Timmermann D, et al. (2007) Broad-spectrum efficacy across cognitive domains by alpha7 nicotinic acetylcholine receptor agonism correlates with activation of ERK1/2 and CREB phosphorylation pathways. J Neurosci 27:10578-10587. CrossRef Medline
9. Bodnar AL, Cortes-Burgos LA, Cook KK, Dinh DM, Groppi VE, Hajos M, Higdon NR, Hoffmann WE, Hurst RS, Myers JK, Rogers BN, Wall TM, Wolfe ML, Wong E (2005) Discovery and structure-activity relationship of quinuclidine benzamides as agonists of alpha7 nicotinic acetylcholine receptors. J Med Chem 48:905-908. CrossRef Medline
10. Bürli T, Baer K, Ewers H, Sidler C, Fuhrer C, Fritschy JM (2010) Single particle tracking of alpha7 nicotinic AChR in hippocampal neurons reveals regulated confinement at glutamatergic and GABAergic perisynaptic sites. PLoS One 5:e11507. CrossRef Medline
11. Caiati MD, Safiulina VF, Fattorini G, Sivakumaran S, Legname G, Cherubini E (2013) PrPC controls via protein kinase A the direction of synaptic plasticity in the immature hippocampus. J Neurosci 33:2973-2983. CrossRef Medline
12. Castillo PE, Schoch S, Schmitz F, Südhof TC, Malenka RC (2002) RIM1alpha is required for presynaptic long-term potentiation. Nature 415:327-330. CrossRef Medline
13. Conti AC, Maas JW Jr, Muglia LM, Dave BA, Vogt SK, Tran TT, Rayhel EJ, Muglia LJ (2007) Distinct regional and subcellular localization of adenylyl cyclases type 1 and 8 in mouse brain. Neuroscience 146:713-729. CrossRef Medline
14. Contractor A, Swanson G, Heinemann SF (2001) Kainate receptors are involved in short-and long-term plasticity at mossy fiber synapses in the hippocampus. Neuron 29:209-216. CrossRef Medline
15. Couey JJ, Meredith RM, Spijker S, Poorthuis RB, Smit AB, Brussaard AB, Mansvelder HD (2007) Distributed network actions by nicotine increase the threshold for spike-timing-dependent plasticity in prefrontal cortex. Neuron 54:73-87. CrossRef Medline
16. del Barrio L, Egea J, León R, Romero A, Ruiz A, Montero M, Alvarez J, López MG (2011) Calcium signalling mediated through alpha7 and nonalpha7 nAChR stimulation is differentially regulated in bovine chromaffin cells to induce catecholamine release. Br J Pharmacol 162:94-110. CrossRef Medline
17. de Leon J, Diaz FJ (2005) A meta-analysis of worldwide studies demonstrates an association between schizophrenia and tobacco smoking behaviors. Schizophr Res 76:135-157. CrossRef Medline
18. Dickinson JA, Kew JN, Wonnacott S (2008) Presynaptic alpha 7-and beta 2-containing nicotinic acetylcholine receptors modulate excitatory amino acid release from rat prefrontal cortex nerve terminals via distinct cellular mechanisms. Mol Pharmacol 74:348-359. CrossRef Medline
19. Fabian-Fine R, Skehel P, Errington ML, Davies HA, Sher E, Stewart MG, Fine A (2001) Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus. J Neurosci 21:7993-8003. Medline
20. Fayuk D, Yakel JL (2004) Regulation of nicotinic acetylcholine receptor channel function by acetylcholinesterase inhibitors in rat hippocampal CA1 interneurons. Mol Pharmacol 66:658-666. CrossRef Medline
21. Fayuk D, Yakel JL (2007) Dendritic Ca2+ signalling due to activation of alpha 7-containing nicotinic acetylcholine receptors in rat hippocampal neurons. J Physiol 582:597-611. CrossRef Medline
22. Fernandes C, Hoyle E, Dempster E, Schalkwyk LC, Collier DA (2006) Performance deficit of alpha7 nicotinic receptor knock-out mice in a delayed matching-to-place task suggests a mild impairment of working/episodiclike memory. Genes Brain Behav 5:433-440. CrossRef Medline
23. Fucile S (2004) Ca2+ permeability of nicotinic acetylcholine receptors. Cell Calcium 35:1-8. CrossRef Medline
24. Garduño J, Galindo-Charles L, Jiménez-Rodriguez J, Galarraga E, Tapia D, Mihailescu S, Hernandez-Lopez S (2012) Presynaptic alpha4beta2 nicotinic acetylcholine receptors increase glutamate release and serotonin neuron excitability in the dorsal raphe nucleus. J Neurosci 32:15148-15157. CrossRef Medline
25. Gilbert D, Lecchi M, Arnaudeau S, Bertrand D, Demaurex N (2009) Local and global calcium signals associated with the opening of neuronal alpha7 nicotinic acetylcholine receptors. Cell Calcium 45:198-207. CrossRef Medline
26. Gómez-Varela D, Schmidt M, Schoellerman J, Peters EC, Berg DK (2012) PMCA2 via PSD-95 controls calcium signaling by alpha7-containing nicotinic acetylcholine receptors on aspiny interneurons. J Neurosci 32: 6894-6905. CrossRef Medline
27. 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
28. Grybko MJ, Hahm ET, Perrine W, Parnes JA, Chick WS, Sharma G, Finger TE, Vijayaraghavan S (2011) A transgenic mouse model reveals fast nicotinic transmission in hippocampal pyramidal neurons. Eur J Neurosci 33:1786-1798. CrossRef Medline
29. 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
30. Hernandez CM, Kayed R, Zheng H, Sweatt JD, Dineley KT (2010) Loss of alpha7 nicotinic receptors enhances beta-amyloid oligomer accumulation, exacerbating early-stage cognitive decline and septohippocampal pathology in a mouse model of Alzheimer's disease. J Neurosci 30:2442-2453. CrossRef Medline
31. Hurst RS, Hajós M, Raggenbass M, Wall TM, Higdon NR, Lawson JA, Rutherford-Root KL, Berkenpas MB, Hoffmann WE, Piotrowski DW, Groppi VE, Allaman G, Ogier R, Bertrand S, Bertrand D, Arneric SP (2005) A novel positive allosteric modulator of the alpha7 neuronal nicotinic acetylcholine receptor: in vitro and in vivo characterization. J Neurosci 25:4396-4405. CrossRef Medline
32. Jackson MB, Konnerth A, Augustine GJ (1991) Action potential broadening and frequency-dependent facilitation of calcium signals in pituitary nerve terminals. Proc Natl Acad Sci U S A 88:380-384. CrossRef Medline
33. Jindrichova M, Lansdell SJ, Millar NS (2012) Changes in temperature have opposing effects on current amplitude in alpha7 and alpha4beta2 nicotinic acetylcholine receptors. PLoS One 7:e32073. CrossRef Medline
34. Jones S, Sudweeks S, Yakel JL (1999) Nicotinic receptors in the brain: correlating physiology with function. Trends Neurosci 22:555-561. CrossRef Medline
35. Kaeser-Woo YJ, Younts TJ, Yang X, Zhou P, Wu D, Castillo PE, Südhof TC (2013) Synaptotagmin-12 phosphorylation by cAMP-dependent protein kinase is essential for hippocampal mossy fiber LTP. J Neurosci 33:9769-9780. CrossRef Medline
36. Kamiya H, Shinozaki H, Yamamoto C (1996) Activation of metabotropic glutamate receptor type 2/3 suppresses transmission at rat hippocampal mossy fibre synapses. J Physiol 493:447-455. Medline
37. Kolomeets NS, Orlovskaya DD, Rachmanova VI, Uranova NA (2005) Ultrastructural alterations in hippocampal mossy fiber synapses in schizophrenia: a postmortem morphometric study. Synapse 57:47-55. CrossRef Medline
38. Kolomeets NS, Orlovskaya DD, Uranova NA (2007) Decreased numerical density of CA3 hippocampal mossy fiber synapses in schizophrenia. Synapse 61:615-621. CrossRef Medline
39. Lambe EK, Picciotto MR, Aghajanian GK (2003) Nicotine induces glutamate release from thalamocortical terminals in prefrontal cortex. Neuropsychopharmacology 28:216-225. CrossRef Medline
40. Lee KJ, Queenan BN, Rozeboom AM, Bellmore R, Lim ST, Vicini S, Pak DT (2013) Mossy fiber-CA3 synapses mediate homeostatic plasticity in mature hippocampal neurons. Neuron 77:99-114. CrossRef Medline
41. Léna C, Changeux JP (1997) Role of Ca2+ ions in nicotinic facilitation of GABA release in mouse thalamus. J Neurosci 17:576-585. Medline
42. Léránth C, Frotscher M (1987) Cholinergic innervation of hippocampal GAD-and somatostatin-immunoreactive commissural neurons. J Comp Neurol 261:33-47. CrossRef Medline
43. Leranth C, Frotscher M (1989) Organization of the septal region in the rat brain: cholinergic-GABAergic interconnections and the termination of hippocampo-septal fibers. J Comp Neurol 289:304-314. CrossRef Medline
44. Levin ED, Wilson W, Rose JE, McEvoy J (1996) Nicotine-haloperidol interactions and cognitive performance in schizophrenics. Neuropsychopharmacology 15:429-436. CrossRef Medline
45. Levin ED, Bradley A, Addy N, Sigurani N (2002) Hippocampal alpha 7 and alpha 4 beta 2 nicotinic receptors and working memory. Neuroscience 109:757-765. CrossRef Medline
46. Levin ED, McClernon FJ, Rezvani AH (2006) Nicotinic effects on cognitive function: behavioral characterization, pharmacological specification, and anatomic localization. Psychopharmacology 184:523-539. CrossRef Medline
47. Levin ED, Petro A, Rezvani AH, Pollard N, Christopher NC, Strauss M, Avery J, Nicholson J, Rose JE (2009) Nicotinic alpha7-or beta2-containing receptor knockout: effects on radial-arm maze learning and long-term nicotine consumption in mice. Behav Brain Res 196:207-213. CrossRef Medline
48. Lonart G, Südhof TC (1998) Region-specific phosphorylation of rabphilin in mossy fiber nerve terminals of the hippocampus. J Neurosci 18:634-640. Medline
49. Lonart G, Janz R, Johnson KM, Südhof TC (1998) Mechanism of action of rab3A in mossy fiber LTP. Neuron 21:1141-1150. CrossRef Medline
50. Maggi L, Sola E, Minneci F, Le Magueresse C, Changeux JP, Cherubini E (2004) Persistent decrease in synaptic efficacy induced by nicotine at Schaffer collateral-CA1 synapses in the immature rat hippocampus. J Physiol 559:863-874. CrossRef Medline
51. Magleby KL, Zengel JE (1976) Long term changes in augmentation, potentiation, and depression of transmitter release as a function of repeated synaptic activity at the frog neuromuscular junction. J Physiol 257:471-494. Medline
52. Maouche K, Medjber K, Zahm JM, Delavoie F, Terryn C, Coraux C, Pons S, Cloëz-Tayarani I, Maskos U, Birembaut P, Tournier JM (2013) Contribution of alpha7 nicotinic receptor to airway epithelium dysfunction under nicotine exposure. Proc Natl Acad Sci U S A 110:4099-4104. CrossRef Medline
53. 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
54. Mellor J, Nicoll RA, Schmitz D (2002) Mediation of hippocampal mossy fiber long-term potentiation by presynaptic Ih channels. Science 295:143-147. CrossRef Medline
55. Menegon A, Bonanomi D, Albertinazzi C, Lotti F, Ferrari G, Kao HT, Benfenati F, Baldelli P, Valtorta F (2006) Protein kinase A-mediated synapsin I phosphorylation is a central modulator of Ca2+-dependent synaptic activity. J Neurosci 26:11670-11681. CrossRef Medline
56. Nashmi R, Lester HA (2006) CNS localization of neuronal nicotinic receptors. J Mol Neurosci 30:181-184. CrossRef Medline
57. Neher E, Sakaba T (2008) Multiple roles of calcium ions in the regulation of neurotransmitter release. Neuron 59:861-872. CrossRef Medline
58. Newhouse PA, Potter A, Singh A (2004) Effects of nicotinic stimulation on cognitive performance. Curr Opin Pharmacol 4:36-46. CrossRef Medline
59. Nicoll RA, SchmitzD (2005) Synaptic plasticity at hippocampal mossy fibre synapses. Nat Rev Neurosci 6:863-876. CrossRef Medline
60. Nott A, Levin ED (2006) Dorsal hippocampal alpha7 and alpha4beta2 nicotinic receptors and memory. Brain Res 1081:72-78. CrossRef Medline
61. Pelkey KA, Topolnik L, Yuan XQ, Lacaille JC, McBain CJ (2008) Statedependent cAMP sensitivity of presynaptic function underlies meta-plasticity in a hippocampal feedforward inhibitory circuit. Neuron 60:980-987. CrossRef Medline
62. Rodríguez-Moreno A, Sihra TS (2004) Presynaptic kainate receptor facilitation of glutamate release involves protein kinase A in the rat hippocampus. J Physiol 557:733-745. CrossRef Medline
63. Rodríguez-Moreno A, Sihra TS (2011) Metabotropic actions of kainate receptors in the control of glutamate release in the hippocampus. Adv Exp Med Biol 717:39-48. CrossRef Medline
64. Ruiz A, Fabian-Fine R, Scott R, Walker MC, Rusakov DA, Kullmann DM (2003) GABAA receptors at hippocampal mossy fibers. Neuron 39:961-973. CrossRef Medline
65. Schmitz D, Mellor J, Nicoll RA (2001) Presynaptic kainate receptor mediation of frequency facilitation at hippocampal mossy fiber synapses. Science 291:1972-1976. CrossRef Medline
66. Séguéla P, Wadiche J, Dineley-Miller K, Dani JA, Patrick JW (1993) Molecular cloning, functional properties, and distribution of rat brain alpha 7: a nicotinic cation channel highly permeable to calcium. J Neurosci 13:596-604. Medline
67. Sharma G, Vijayaraghavan S (2003) Modulation of presynaptic store calcium induces release of glutamate and postsynaptic firing. Neuron 38: 929-939. CrossRef Medline
68. Sharma G, Grybko M, Vijayaraghavan S (2008) Action potentialindependent and nicotinic receptor-mediated concerted release of multiple quanta at hippocampal CA3-mossy fiber synapses. J Neurosci 28: 2563-2575. CrossRef Medline
69. Szabo SI, Zelles T, Vizi ES, Lendvai B (2008) The effect of nicotine on spiking activity and Ca2+dynamics of dendritic spines in rat CA1 pyramidal neurons. Hippocampus 18:376-385. CrossRef Medline
70. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann CI, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improvedGCaMPcalcium indicators. Nat Methods 6:875-881. CrossRef Medline
71. Timmermann DB, Grønlien JH, Kohlhaas KL, Nielsen EØ, Dam E, Jørgensen TD, Ahring PK, Peters D, Holst D, Christensen JK, Malysz J, Briggs CA, Gopalakrishnan M, Olsen GM (2007) An allosteric modulator of the alpha7 nicotinic acetylcholine receptor possessing cognition-enhancing properties in vivo. J Pharmacol Exp Ther 323:294-307. CrossRef Medline
72. Torborg CL, Nakashiba T, Tonegawa S, McBain CJ (2010) Control of CA3 output by feedforward inhibition despite developmental changes in the excitation-inhibition balance. J Neurosci 30:15628-15637. CrossRef Medline
73. Tu B, Gu Z, Shen JX, Lamb PW, Yakel JL (2009) Characterization of a nicotine-sensitive neuronal population in rat entorhinal cortex. J Neurosci 29:10436-10448. CrossRef Medline
74. Turner TJ (2004) Nicotine enhancement of dopamine release by a calciumdependent increase in the size of the readily releasable pool of synaptic vesicles. J Neurosci 24:11328-11336. CrossRef Medline
75. Vogt KE, RegehrWG (2001) Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21:75-83. Medline
76. Weisskopf MG, Nicoll RA (1995) Presynaptic changes during mossy fibre LTP revealed by NMDA receptor-mediated synaptic responses. Nature 376:256-259. CrossRef Medline
77. Weisskopf MG, Castillo PE, Zalutsky RA, Nicoll RA (1994) Mediation of hippocampal mossy fiber long-term potentiation by cyclic AMP. Science 265:1878-1882. CrossRef Medline
78. Welsby PJ, Rowan MJ, Anwyl R (2009) Intracellular mechanisms underlying the nicotinic enhancement of LTP in the rat dentate gyrus. Eur J Neurosci 29:65-75. CrossRef Medline
79. Wozny C, Maier N, Fidzinski P, Breustedt J, Behr J, Schmitz D (2008) Differential cAMP signaling at hippocampal output synapses. J Neurosci 28:14358-14362. CrossRef Medline
80. Xia Z, Storm DR (2005) The role of calmodulin as a signal integrator for synaptic plasticity. Nat Rev Neurosci 6:267-276. CrossRef Medline
81. Yaguchi T, Nagata T, Nishizaki T (2009) Dilinoleoylphosphatidylcholine ameliorates scopolamine-induced impairment of spatial learning and memory by targeting alpha7 nicotinic ACh receptors. Life Sci 84:263-266. CrossRef Medline
82. Young JW, Crawford N, Kelly JS, Kerr LE, Marston HM, Spratt C, Finlayson K, Sharkey J (2007) Impaired attention is central to the cognitive deficits observed in alpha 7 deficient mice. Eur Neuropsychopharmacol 17:145-155. CrossRef Medline
83. Zhao Y, Araki S, Wu J, Teramoto T, Chang YF, Nakano M, Abdelfattah AS, Fujiwara M, Ishihara T, Nagai T, Campbell RE (2011) An expanded palette of genetically encoded Ca(2)(+) indicators. Science 333:1888-1891. CrossRef Medline
84. Zhong C, Du C, Hancock M, Mertz M, Talmage DA, Role LW (2008) Presynaptic type III neuregulin 1 is required for sustained enhancement of hippocampal transmission by nicotine and for axonal targeting of alpha7 nicotinic acetylcholine receptors. J Neurosci 28:9111-9116. CrossRef Medline
85. Zucker RS, Regehr WG (2002) Short-term synaptic plasticity. Annu Rev Physiol 64:355-405. CrossRef Medline