Activation of α7 nicotinic acetylcholine receptors protects potentiated synapses from depotentiation during theta pattern stimulation in the hippocampal CA1 region of rats

Neuropharmacology

Volumn 105, Issue , 2016, Pages 378-387

  Galvez, Bryan ^a   Gross, Noah ^a   Sumikawa, Katumi ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

ACh; Depotentiation; GluN2A; Hippocampus; LTP; Nicotine; 7 nicotinic acetylcholine receptor

Indexed keywords

BUNGAROTOXIN RECEPTOR; CASPASE 3; CASPASE 3 INHIBITOR; F ACTIN; GLUTAMATE RECEPTOR 1; JASPAMIDE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2A; NICOTINE; NICOTINIC RECEPTOR BLOCKING AGENT; ACTIN; AMPA RECEPTOR; CASP3 PROTEIN, RAT; DEPSIPEPTIDE; GLUTAMATE RECEPTOR IONOTROPIC, AMPA 1; NEUROPROTECTIVE AGENT; NICOTINIC AGENT;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME ACTIVITY; HIPPOCAMPAL CA1 REGION; INTERNALIZATION; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MALE; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN PHOSPHORYLATION; PROTEIN STABILITY; RAT; RECEPTOR DOWN REGULATION; SIGNAL TRANSDUCTION; SYNAPSE; THETA RHYTHM; AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; DRUG EFFECTS; IN VITRO STUDY; SPRAGUE DAWLEY RAT;

ACTINS; ALPHA7 NICOTINIC ACETYLCHOLINE RECEPTOR; ANIMALS; CA1 REGION, HIPPOCAMPAL; CASPASE 3; DEPSIPEPTIDES; IN VITRO TECHNIQUES; LONG-TERM POTENTIATION; MALE; NEUROPROTECTIVE AGENTS; NICOTINE; NICOTINIC AGONISTS; NICOTINIC ANTAGONISTS; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, AMPA; RECEPTORS, N-METHYL-D-ASPARTATE; SYNAPSES; THETA RHYTHM;

EID: 84958544325     PISSN: 00283908     EISSN: 18737064     Source Type: Journal    
DOI: 10.1016/j.neuropharm.2016.02.008     Document Type: Article

References (84)

1. M. Alkondon, E.F. Pereira, and E.X. Albuquerque alpha-bungarotoxin- and methyllycaconitine-sensitive nicotinic receptors mediate fast synaptic transmission in interneurons of rat hippocampal slices Brain Res. 810 1998 257 263
2. M. Alkondon, E. Pereira, L. Almeida, W. Randall, and E. Albuquerque Nicotine at concentrations found in cigarette smokers activates and desensitizes nicotinic acetylcholine receptors in CA1 interneurons of rat hippocampus Neuropharmacology 39 2000 2726 2739
3. M. Alkondon, and E.X. Albuquerque Nicotinic acetylcholine receptor alpha7 and alpha4beta2 subtypes differentially control GABAergic input to CA1 neurons in rat hippocampus J. Neurophysiol. 86 2001 3043 3055
4. A. Arai, J. Larson, and G. Lynch Anoxia reveals a vulnerable period in the development of long-term potentiation Brain Res. 511 1990 353 357
5. M. Barros, M. Ramirez, and E. Reis Participation of hippocampal nicotinic receptors in acquisition, consolidation and retrieval of memory for one trial inhibitory avoidance in rats Neuroscience 126 2004 651 656
6. A. Bellot, B. Guivernau, M. Tajes, M. Bosch-Morató, V. Valls-Comamala, and F.J. Muñoz The structure and function of actin cytoskeleton in mature glutamatergic dendritic spines Brain Res. 1573 2014 1 16
7. T.A. Benke, A. Lüthi, J.T.R. Isaac, and G.L. Collingridge Modulation of AMPA receptor unitary conductance by synaptic activity Nature 393 1998 793 797
8. T.V. Bliss, and G.L. Collingridge A synaptic model of memory: long-term potentiation in the hippocampus Nature 361 1993 31 39
9. M. Bosch, J. Castro, T. Saneyoshi, H. Matsuno, M. Sur, and Y. Hayashi Structural and molecular remodeling of dendritic spine substructures during long-term potentiation Neuron 82 2014 444 459
10. L.Y. Chen, C.S. Rex, M.S. Casale, C.M. Gall, and G. Lynch Changes in synaptic morphology accompany actin signaling during LTP J. Neurosci. 27 2007 5363 5372
11. G.L. Collingridge, J.T. Isaac, and Y.T. Wang Receptor trafficking and synaptic plasticity Nat. Rev. Neurosci. 5 2004 952 962
12. S. Deiana, B. Platt, and G. Riedel The cholinergic system and spatial learning Behav. Brain Res. 221 2011 389 411
13. J.Y. Delgado, and T.J. O'dell Long-term potentiation persists in an occult state following mGluR-dependent depotentiation Neuropharmacology 48 2005 936 948
14. A. Dityatev, M. Schachner, and P. Sonderegger The dual role of the extracellular matrix in synaptic plasticity and homeostasis Nat. Rev. Neurosci. 11 2010 735 746
15. P. Dutar, M. Bassant, M. Senut, and Y. Lamour The septohippocampal pathway: structure and function of a central cholinergic system Physiol. Rev. 75 1995 393 427
16. R. Fabian-Fine, P. Skehel, M.L. Errington, H.A. Davies, E. Sher, M.G. Stewart, and A. Fine Ultrastructural distribution of the alpha7 nicotinic acetylcholine receptor subunit in rat hippocampus J. Neurosci. 21 2001 7993 8003
17. C.J. Frazier, Y.D. Rollins, C.R. Breese, S. Leonard, R. Freedman, and T.V. Dunwiddie Acetylcholine activates an alpha-bungarotoxin-sensitive nicotinic current in rat hippocampal interneurons, but not pyramidal cells J. Neurosci. 18 1998 1187 1195
18. C.J. Frazier, A.V. Buhler, J.L. Weiner, and T.V. Dunwiddie Synaptic potentials mediated via alpha-bungarotoxin-sensitive nicotinic acetylcholine receptors in rat hippocampal interneurons J. Neurosci. 18 1998 8228 8235
19. 2+ permeability of nicotinic acetylcholine receptors Cell Calcium 35 2004 1 8
20. S. Fujii, K. Saito, H. Miyakawa, K. Ito, and H. Kato Reversal of long-term potentiation (depotentiation) induced by tetanus stimulation of the input to CA1 neurons of guinea pig hippocampal slices Brain Res. 555 1991 112 122
21. S. Fujii, Z. Ji, N. Morita, and K. Sumikawa Acute and chronic nicotine exposure differentially facilitate the induction of LTP Brain Res. 846 1999 137 143
22. S. Fujii, and K. Sumikawa Nicotine accelerates reversal of long-term potentiation and enhances long-term depression in the rat hippocampal CA1 region Brain Res. 894 2001 340 346
23. Y. Fukazawa, Y. Saitoh, F. Ozawa, Y. Ohta, K. Mizuno, and K. Inokuchi Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo Neuron 38 2002 447 460
24. Z. Gu, and J.L. Yakel Timing-dependent septal cholinergic induction of dynamic hippocampal synaptic plasticity Neuron 71 2011 155 165
25. X. Guan, S. Nakauchi, and K. Sumikawa Nicotine reverses consolidated long-term potentiation in the hippocampal CA1 region Brain Res. 1078 2006 80 91
26. Y. Hayashi, S.H. Shi, J.A. Esteban, A. Piccini, J.C. Poncer, and R. Malinow Driving AMPA receptors into synapses by LTP and CaMKII: requirement for GluR1 and PDZ domain interaction Science 287 2000 2262 2267
27. K. He, A. Lee, L. Song, P.O. Kanold, and H.-K. Lee AMPA receptor subunit GluR1 (GluA1) serine-845 site is involved in synaptic depression but not in spine shrinkage associated with chemical long-term depression J. Neurophysiol. 105 2011 1897 1907
28. C. Huang, Y. Liang, and K. Hsu Characterization of the mechanism underlying the reversal of long term potentiation by low frequency stimulation at hippocampal CA1 synapses J. Biol. Chem. 276 2001 48108 48117
29. D. Ji, R. Lape, and J.A. Dani Timing and location of nicotinic activity enhances or depresses hippocampal synaptic plasticity Neuron 31 2001 131 141
30. A. Jouvenceau, J. Billard, U. Haditsch, I.M. Mansuy, and P. Dutar Different phosphatase-dependent mechanisms mediate long-term depression and depotentiation of long-term potentiation in mouse hippocampal CA1 area Eur. J. Neurosci. 18 2003 1279 1285
31. J.W. Kenney, M.D. Adoff, D.S. Wilkinson, and T.J. Gould The effects of acute, chronic, and withdrawal from chronic nicotine on novel and spatial object recognition in male C57BL/6J mice Psychopharmacology 217 2011 353 365
32. E.A. Kramár, and G. Lynch Developmental and regional differences in the consolidation of long-term potentiation Neuroscience 118 2003 387 398
33. E.A.A. Kramár, B. Lin, C.S. Rex, C.M. Gall, and G. Lynch Integrin-driven actin polymerization consolidates long-term potentiation Proc. Natl. Acad. Sci. U. S. A. 103 2006 5579 5584
34. C. Lang, A. Barco, L. Zablow, E.R. Kandel, S.A. Siegelbaum, and S.S. Zakharenko Transient expansion of synaptically connected dendritic spines upon induction of hippocampal long-term potentiation Proc. Natl. Acad. Sci. U. S. A. 101 2004 16665 16670
35. J. Larson, P. Xiao, and G. Lynch Reversal of LTP by theta frequency stimulation Brain Res. 600 1993 97 102
36. H.-K. Lee, M. Barbarosie, K. Kameyama, M.F. Bear, and R.L. Huganir Regulation of distinct AMPA receptor phosphorylation sites during bidirectional synaptic plasticity Nature 405 2000 955 959
37. H.-K.K. Lee, K. Takamiya, K. He, L. Song, and R.L. Huganir Specific roles of AMPA receptor subunit GluR1 (GluA1) phosphorylation sites in regulating synaptic plasticity in the CA1 region of hippocampus J. Neurophysiol. 103 2010 479 489
38. R. Li, F.-S.S. Huang, A.-K.K. Abbas, and Holger Wigstrom Role of NMDA receptor subtypes in different forms of NMDA-dependent synaptic plasticity BMC Neurosci. 8 2007 55
39. Z. Li, J. Jo, J.-M. Jia, S.-C. Lo, D.J. Whitcomb, S. Jiao, K. Cho, and M. Sheng Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization Cell 141 2010 859 871
40. Y.-C. Liang, C.-C. Huang, and K.-S. Hsu A role of p38 mitogen-activated protein kinase in adenosine A1 receptor-mediated synaptic depotentiation in area CA1 of the rat hippocampus Mol. Brain 1 2008 13
41. Qs Liu, and D.K. Berg Actin filaments and the opposing actions of CaM kinase II and calcineurin in regulating alpha7-containing nicotinic receptors on chick ciliary ganglion neurons J. Neurosci. 19 1999 10280 10288
42. L. Liu, T.P. Wong, M.F. Pozza, K. Lingenhoehl, Y. Wang, M. Sheng, Y.P. Auberson, and Y.T. Wang Role of NMDA receptor subtypes in governing the direction of hippocampal synaptic plasticity Science 304 2004 1021 1024
43. W. Lu, and K.W. Roche Posttranslational regulation of AMPA receptor trafficking and function Curr. Opin. Neurobiol. 22 2012 470 479
44. G. Lynch, C.S. Rex, and C.M. Gall LTP consolidation: substrates, explanatory power, and functional significance Neuropharmacology 52 2007 12 23
45. R.C. Malenka, and M.F. Bear LTP and LTD: an embarrassment of riches Neuron 44 2004 5 21
46. H.-Y.Y. Man, Y. Sekine-Aizawa, and R.L. Huganir Regulation of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor trafficking through PKA phosphorylation of the Glu receptor 1 subunit Proc. Natl. Acad. Sci. U. S. A. 104 2007 3579 3584
47. E.O. Mann, and S.A. Greenfield Novel modulatory mechanisms revealed by the sustained application of nicotine in the guinea-pig hippocampus in vitro J. Physiol. 551 2003 539 550
48. F. Marrosu, C. Portas, M. Mascia, M. Casu, M. Fà, M. Giagheddu, A. Imperato, and G. Gessa Microdialysis measurement of cortical and hippocampal acetylcholine release during sleep-wake cycle in freely moving cats Brain Res. 671 1995 329 332
49. P.V. Massey, B.E. Johnson, P.R. Moult, Y.P. Auberson, M.W. Brown, E. Molnar, G.L. Collingridge, and Z.I. Bashir Differential roles of NR2A and NR2B-containing NMDA receptors in cortical long-term potentiation and long-term depression J. Neurosci. 24 2004 7821 7828
50. M. Matsuzaki, N. Honkura, G.C.R. Ellis-Davies, and H. Kasai Structural basis of long-term potentiation in single dendritic spines Nature 429 2004 761 766
51. J.L. McGaugh Memory-a century of consolidation Science 287 2000 248 251
52. D.S. McGehee, and L.W. Role Presynaptic ionotropic receptors Curr. Opin. Neurobiol. 6 1996 342 349
53. A.R. McQuiston, and D.V. Madison Nicotinic receptor activation excites distinct subtypes of interneurons in the rat hippocampus J. Neurosci. 19 1999 2887 2896
54. H. Monyer, N. Burnashev, D.J. Laurie, B. Sakmann, and P.H. Seeburg Developmental and regional expression in the rat brain and functional properties of four NMDA receptors Neuron 12 1994 529 540
55. L. Nadel, A. Hupbach, R. Gomez, and K. Newman-Smith Memory formation, consolidation and transformation Neurosci. Biobehav. Rev. 36 2012 1640 1645
56. S. Nakauchi, R.J. Brennan, J. Boulter, and K. Sumikawa Nicotine gates long-term potentiation in the hippocampal CA1 region via the activation of alpha2∗nicotinic ACh receptors Eur. J. Neurosci. 25 2007 2666 2681
57. S. Nakauchi, and K. Sumikawa Endogenous ACh suppresses LTD induction and nicotine relieves the suppression via different nicotinic ACh receptor subtypes in the mouse hippocampus Life Sci. 111 2014 62 68
58. S. Nabavi, R. Fox, C. Proulx, John Lin, R. Tsien, and R. Malinow Engineering a memory with LTD and LTP Nature 511 2014 348 352
59. T. O'Dell, and E. Kandel Low-frequency stimulation erases LTP through an NMDA receptor-mediated activation of protein phosphatases Learn. Mem. 1 1994 129 139
60. M.C. Oh, V.A. Derkach, E.S. Guire, and T.R. Soderling Extrasynaptic membrane trafficking regulated by GluR1 serine 845 phosphorylation primes AMPA receptors for long-term potentiation J. Biol. Chem. 281 2006 752 758
61. K.-I. Okamoto, T. Nagai, A. Miyawaki, and Y. Hayashi Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity Nat. Neurosci. 7 2004 1104 1112
62. M. Orsetti, F. Casamenti, and G. Pepeu Enhanced acetylcholine release in the hippocampus and cortex during acquisition of an operant behavior Brain Res. 724 1996 89 96
63. S. Peineau, C. Taghibiglou, C. Bradley, T.P. Wong, L. Liu, J. Lu, E. Lo, D. Wu, E. Saule, T. Bouschet, P. Matthews, J.T. Isaac, Z.A. Bortolotto, Y.T. Wang, and G.L. Collingridge LTP inhibits LTD in the hippocampus via regulation of GSK3beta Neuron 53 2007 703 717
64. Y. Peng, J. Zhao, Q.-H.H. Gu, R.-Q.Q. Chen, Z. Xu, J.-Z.Z. Yan, S.-H.H. Wang, S.-Y.Y. Liu, Z. Chen, and W. Lu Distinct trafficking and expression mechanisms underlie LTP and LTD of NMDA receptor-mediated synaptic responses Hippocampus 20 2010 646 658
65. M.W. Quick, and R.A.J. Lester Desensitization of neuronal nicotinic receptors J. Neurobiol. 53 2002 457 478
66. B. Ramachandran, and J.U. Frey Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro J. Neurosci. 29 2009 12167 12173
67. C.S. Rex, L.Y. Chen, A. Sharma, J. Liu, A.H. Babayan, C.M. Gall, and G. Lynch Different Rho GTPase-dependent signaling pathways initiate sequential steps in the consolidation of long-term potentiation J. Cell Biol. 186 2009 85 97
68. J.D. Shepherd, and R.L. Huganir The cell biology of synaptic plasticity: AMPA receptor trafficking Annu. Rev. Cell Dev. Biol. 23 2007 613 643
69. R.D. Shoop, N. Yamada, and D.K. Berg Cytoskeletal links of neuronal acetylcholine receptors containing alpha 7 subunits J. Neurosci. 20 2000 4021 4029
70. U. Staubli, D. Chun, and G. Lynch Time-dependent reversal of long-term potentiation by an integrin antagonist J. Neurosci. 18 1998 3460 3469
71. S.N. Sudweeks, and J.L. Yakel Functional and molecular characterization of neuronal nicotinic ACh receptors in rat CA1 hippocampal neurons J. Physiol. 527 Pt 3 2000 515 528
72. N. Wanaverbecq, A. Semyanov, I. Pavlov, M.C. Walker, and D.M. Kullmann Cholinergic axons modulate GABAergic signaling among hippocampal interneurons via postsynaptic alpha 7 nicotinic receptors J. Neurosci. 27 2007 5683 5693
73. R.G. Wiley, T.N. Oeltmann, and D.A. Lappi Immunolesioning: selective destruction of neurons using immunotoxin to rat NGF receptor Brain Res. 562 1991 149 153
74. D.G. Winder, and J.D. Sweatt Roles of serine/threonine phosphatases in hippocampel synaptic plasticity Nat. Rev. Neurosci. 2 2001 461 474
75. Y. Yamazaki, N. Hamaue, and K. Sumikawa Nicotine compensates for the loss of cholinergic function to enhance long-term potentiation induction Brain Res. 946 2002 148 152
76. Y. Yamazaki, Y. Jia, N. Hamaue, and K. Sumikawa Nicotine-induced switch in the nicotinic cholinergic mechanisms of facilitation of long-term potentiation induction Eur. J. Neurosci. 22 2005 845 860
77. Y. Yamazaki, T. Sugihara, J.-I. Goto, K. Chida, H. Fujiwara, K. Kaneko, S. Fujii, and K. Mikoshiba Role of inositol 1,4,5-trisphosphate receptors in the postsynaptic expression of guinea pig hippocampal mossy fiber depotentiation Brain Res. 1387 2011 19 28
78. H. Yang, M.J. Courtney, P. Martinsson, and D. Manahan-Vaughan Hippocampal long-term depression is enhanced, depotentiation is inhibited and long-term potentiation is unaffected by the application of a selective c-Jun N-terminal kinase inhibitor to freely behaving rats Eur. J. Neurosci. 33 2011 1647 1655
79. Y. Yang, X.B. Wang, M. Frerking, and Q. Zhou Spine expansion and stabilization associated with long-term potentiation J. Neurosci. 28 2008 5740 5751
80. R. Yuste, and T. Bonhoeffer Morphological changes in dendritic spines associated with long-term synaptic plasticity Annu. Rev. Neurosci. 24 2001 1071 1089
81. J. Zhang, and D.K. Berg Reversible inhibition of GABAA receptors by alpha7-containing nicotinic receptors on the vertebrate postsynaptic neurons J. Physiol. 579 2007 753 763
82. L. Zhang, K. Meng, Y. Li, and T. Han NR2A-containing NMDA receptors are required for L-LTP induction and depotentiation in CA1 region of hippocampal slices Eur. J. Neurosci. 29 2009 2137 2144
83. Q. Zhou, K.J. Homma, and M.M. Poo Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses Neuron 44 2004 749 757
84. Y. Zhu, D. Pak, Y. Qin, S.G. McCormack, M.J. Kim, J.P. Baumgart, V. Velamoor, Y.P. Auberson, P. Osten, Aelst, L. van, M. Sheng, and J. Zhu Rap2-JNK removes synaptic AMPA receptors during depotentiation Neuron 46 2005 905 916