cAMP-Dependent Synaptic Plasticity at the Hippocampal Mossy Fiber Terminal.

LTP PKA cAMP forskolin-induced potentiation mossy fiber synapse synaptic plasticity

Journal

Frontiers in synaptic neuroscience
ISSN: 1663-3563
Titre abrégé: Front Synaptic Neurosci
Pays: Switzerland
ID NLM: 101548972

Informations de publication

Date de publication:
2022
Historique:
received: 24 01 2022
accepted: 23 02 2022
entrez: 21 4 2022
pubmed: 22 4 2022
medline: 22 4 2022
Statut: epublish

Résumé

Cyclic adenosine monophosphate (cAMP) is a crucial second messenger involved in both pre- and postsynaptic plasticity in many neuronal types across species. In the hippocampal mossy fiber (MF) synapse, cAMP mediates presynaptic long-term potentiation and depression. The main cAMP-dependent signaling pathway linked to MF synaptic plasticity acts via the activation of the protein kinase A (PKA) molecular cascade. Accordingly, various downstream putative synaptic PKA target proteins have been linked to cAMP-dependent MF synaptic plasticity, such as synapsin, rabphilin, synaptotagmin-12, RIM1a, tomosyn, and P/Q-type calcium channels. Regulating the expression of some of these proteins alters synaptic release probability and calcium channel clustering, resulting in short- and long-term changes to synaptic efficacy. However, despite decades of research, the exact molecular mechanisms by which cAMP and PKA exert their influences in MF terminals remain largely unknown. Here, we review current knowledge of different cAMP catalysts and potential downstream PKA-dependent molecular cascades, in addition to non-canonical cAMP-dependent but PKA-independent cascades, which might serve as alternative, compensatory or competing pathways to the canonical PKA cascade. Since several other central synapses share a similar form of presynaptic plasticity with the MF, a better description of the molecular mechanisms governing MF plasticity could be key to understanding the relationship between the transcriptional and computational levels across brain regions.

Identifiants

pubmed: 35444523
doi: 10.3389/fnsyn.2022.861215
pmc: PMC9013808
doi:

Types de publication

Journal Article Review

Langues

eng

Pagination

861215

Informations de copyright

Copyright © 2022 Shahoha, Cohen, Ben-Simon and Ashery.

Déclaration de conflit d'intérêts

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Références

J Neurosci. 2021 Jan 27;41(4):711-725
pubmed: 33268547
Nature. 1997 Jun 19;387(6635):810-4
pubmed: 9194562
Cell. 2003 Oct 3;115(1):49-60
pubmed: 14532002
Neuron. 2012 Oct 4;76(1):70-81
pubmed: 23040807
Neuron. 2008 Feb 28;57(4):536-45
pubmed: 18304483
PLoS One. 2014 Jun 24;9(6):e100252
pubmed: 24959857
Br J Pharmacol. 2018 Apr;175(7):994-1003
pubmed: 29338070
Curr Opin Neurobiol. 1999 Jun;9(3):305-13
pubmed: 10395573
Annu Rev Physiol. 1992;54:489-505
pubmed: 1314043
Cell. 1994 Oct 7;79(1):69-79
pubmed: 7923379
Nat Commun. 2021 May 18;12(1):2912
pubmed: 34006874
Neuron. 2006 Aug 3;51(3):303-15
pubmed: 16880125
Neuroscience. 2007 May 11;146(2):713-29
pubmed: 17335981
Nat Rev Neurosci. 2007 Aug;8(8):597-609
pubmed: 17637801
Sci Rep. 2018 Jan 30;8(1):1866
pubmed: 29382930
Neuromolecular Med. 2013 Jun;15(2):351-63
pubmed: 23519441
Neuron. 1996 Apr;16(4):797-803
pubmed: 8607997
J Neurosci. 2006 Jun 28;26(26):7071-81
pubmed: 16807336
Elife. 2019 Sep 19;8:
pubmed: 31535974
Biochem Pharmacol. 1986 Dec 15;35(24):4349-57
pubmed: 2878666
J Neurochem. 2021 Feb;156(3):270-272
pubmed: 33274445
Front Neuroanat. 2010 Dec 20;4:149
pubmed: 21191478
Hippocampus. 2005;15(6):691-6
pubmed: 15986406
Cell. 2018 Aug 9;174(4):1015-1030.e16
pubmed: 30096299
J Neurosci. 2012 Sep 19;32(38):13189-99
pubmed: 22993435
Neuron. 2020 Aug 5;107(3):509-521.e7
pubmed: 32492366
Nature. 2007 Jan 11;445(7124):168-76
pubmed: 17151600
iScience. 2020 Apr 24;23(4):101025
pubmed: 32283526
J Neurosci. 2019 Oct 16;39(42):8209-8216
pubmed: 31619489
Front Synaptic Neurosci. 2013 Oct 17;5:8
pubmed: 24146648
J Neurosci. 2004 Dec 15;24(50):11368-80
pubmed: 15601943
Proc Natl Acad Sci U S A. 1996 Nov 12;93(23):13304-9
pubmed: 8917586
Curr Opin Neurobiol. 2020 Aug;63:198-209
pubmed: 32663762
Semin Cell Dev Biol. 2011 Jun;22(4):387-92
pubmed: 21827866
Annu Rev Pharmacol Toxicol. 2001;41:145-74
pubmed: 11264454
Neurosignals. 2009;17(1):5-22
pubmed: 18948702
Neuropharmacology. 1995 Nov;34(11):1573-9
pubmed: 8606805
J Physiol. 2020 May;598(9):1649-1654
pubmed: 30735245
Genes Cells. 1996 Jul;1(7):615-32
pubmed: 9078389
Behav Brain Res. 2012 Jan 1;226(1):56-65
pubmed: 21907247
Neuron. 2006 Nov 9;52(3):497-510
pubmed: 17088215
J Neurophysiol. 2009 Dec;102(6):3251-9
pubmed: 19776361
Science. 1998 Dec 18;282(5397):2275-9
pubmed: 9856955
Learn Mem. 1997 Jul-Aug;4(2):230-43
pubmed: 10456066
Neuron. 2013 Oct 30;80(3):675-90
pubmed: 24183019
Neuron. 2003 Jul 17;39(2):327-41
pubmed: 12873388
Elife. 2021 Jun 01;10:
pubmed: 34061025
PLoS Biol. 2021 Jun 21;19(6):e3001149
pubmed: 34153028
Cell Mol Life Sci. 2001 Jan;58(1):94-116
pubmed: 11229820
J Cell Biol. 2005 Sep 26;170(7):1113-25
pubmed: 16186257
Prog Brain Res. 2007;163:43-61
pubmed: 17765711
Cell. 2020 Dec 10;183(6):1682-1698.e24
pubmed: 33232692
Cell. 1995 Dec 29;83(7):1211-22
pubmed: 8548807
J Neurosci Res. 1998 Aug 1;53(3):269-78
pubmed: 9698155
Proc Natl Acad Sci U S A. 1980 Dec;77(12):7492-6
pubmed: 6111794
eNeuro. 2017 Sep 25;4(5):
pubmed: 28948210
Curr Opin Pharmacol. 2007 Feb;7(1):77-85
pubmed: 17085074
J Neurosci. 2000 Nov 15;20(22):8279-89
pubmed: 11069934
J Neurosci. 2007 Dec 5;27(49):13420-9
pubmed: 18057200
Proc Natl Acad Sci U S A. 2021 Mar 2;118(9):
pubmed: 33622791
Mol Brain. 2013 Jan 22;6:5
pubmed: 23339575
Elife. 2016 Oct 25;5:
pubmed: 27780032
Int J Mol Sci. 2020 Apr 26;21(9):
pubmed: 32357495
Elife. 2016 Dec 02;5:
pubmed: 27911261
Biochem J. 2013 Nov 1;455(3):359-65
pubmed: 24112109
Arch Neurol. 2004 May;61(5):641-4
pubmed: 15148138
J Biol Chem. 2017 Jul 21;292(29):12220-12231
pubmed: 28546426
J Cell Biol. 1983 May;96(5):1337-54
pubmed: 6404910
J Neurosci. 2013 Jun 5;33(23):9769-80
pubmed: 23739973
J Neurosci. 2007 Oct 31;27(44):12025-32
pubmed: 17978044
J Neurochem. 2021 Feb;156(3):324-336
pubmed: 33037623
Proc Natl Acad Sci U S A. 1980 Nov;77(11):6912-6
pubmed: 6256770
J Comp Neurol. 1981 Jan 1;195(1):51-86
pubmed: 7204652
Nature. 1997 Aug 7;388(6642):590-3
pubmed: 9252190
Nature. 2002 Jan 17;415(6869):327-30
pubmed: 11797010
J Allergy Clin Immunol. 2006 Jan;117(1):18-24; quiz 25
pubmed: 16387578
J Neurosci. 2009 Sep 2;29(35):10974-8
pubmed: 19726655
Nature. 1997 Aug 7;388(6642):593-8
pubmed: 9252191
Cell Rep. 2020 Feb 25;30(8):2594-2602.e3
pubmed: 32101738
Curr Opin Struct Biol. 2019 Feb;54:179-188
pubmed: 30986753
Science. 1988 Jun 17;240(4859):1667-9
pubmed: 2454509
Ann N Y Acad Sci. 1998 Dec 15;861:31-7
pubmed: 9928236
Nat Rev Neurosci. 2008 Jan;9(1):65-75
pubmed: 18094707
Nat Rev Neurosci. 2011 Dec 20;13(1):7-21
pubmed: 22183436
Front Syst Neurosci. 2013 Oct 30;7:74
pubmed: 24198767
Proc Natl Acad Sci U S A. 2003 Jul 22;100(15):8975-80
pubmed: 12815098
Neuron. 2008 Dec 26;60(6):980-7
pubmed: 19109906
Curr Opin Neurobiol. 2005 Jun;15(3):266-74
pubmed: 15919191
Elife. 2016 Apr 26;5:e14997
pubmed: 27113915
Front Cell Neurosci. 2014 Feb 04;8:28
pubmed: 24550783
J Neurochem. 2013 Sep;126(5):565-78
pubmed: 23692284
J Physiol. 2007 Jun 15;581(Pt 3):961-70
pubmed: 17379642
Neuropharmacology. 1998 Dec;37(12):1445-58
pubmed: 9886667
J Neurosci. 2015 Apr 22;35(16):6544-53
pubmed: 25904804
Mol Brain. 2012 May 14;5:14
pubmed: 22583753
Science. 1990 Jun 29;248(4963):1619-24
pubmed: 2114039
J Physiol. 1999 Jul 15;518 ( Pt 2):497-506
pubmed: 10381595
Front Synaptic Neurosci. 2013 Jan 11;4:9
pubmed: 23335896
Vitam Horm. 2010;82:65-85
pubmed: 20472133
Nat Cell Biol. 2002 Aug;4(8):E203-6
pubmed: 12149635
J Physiol. 2018 Feb 15;596(4):703-716
pubmed: 29218821
Synapse. 2011 Sep;65(9):945-54
pubmed: 21360593
Neuron. 2001 Apr;30(1):183-96
pubmed: 11343654
Sci Signal. 2013 Jun 25;6(281):ra51
pubmed: 23800469
J Biol Chem. 1999 Dec 31;274(53):37815-20
pubmed: 10608844
Physiol Rev. 2007 Jul;87(3):965-1010
pubmed: 17615394
Neuron. 2008 Jan 10;57(1):108-20
pubmed: 18184568
Annu Rev Pharmacol Toxicol. 2010;50:355-75
pubmed: 20055708
Trends Neurosci. 2009 May;32(5):275-82
pubmed: 19307030
J Physiol. 1993 Dec;472:615-63
pubmed: 7908327
Neuron. 1998 Feb;20(2):305-15
pubmed: 9491991
Cell Rep. 2020 Feb 11;30(6):2006-2017.e3
pubmed: 32049027
Front Synaptic Neurosci. 2018 Oct 30;10:33
pubmed: 30425632
Chem Soc Rev. 2013 Jan 7;42(1):305-41
pubmed: 23023210
Neuron. 1998 Nov;21(5):1141-50
pubmed: 9856469
J Biol Chem. 2005 Nov 25;280(47):39253-9
pubmed: 16203731
Nat Rev Mol Cell Biol. 2012 Oct;13(10):646-58
pubmed: 22992589
Gene. 2016 Feb 15;577(2):101-8
pubmed: 26687711
Neuron. 2017 Aug 16;95(4):928-943.e3
pubmed: 28817805
J Neurosci. 1997 Nov 15;17(22):8687-94
pubmed: 9348337
J Neurosci. 1998 May 1;18(9):3386-403
pubmed: 9547246
Biochim Biophys Acta. 2003 Feb 17;1593(2-3):141-9
pubmed: 12581858
J Neurosci. 1999 Oct 15;19(20):9090-7
pubmed: 10516326
Mol Neurobiol. 2003 Feb;27(1):99-106
pubmed: 12668903
Trends Neurosci. 2011 Oct;34(10):515-25
pubmed: 21788086
Sci Rep. 2017 Aug 4;7(1):7351
pubmed: 28779099
J Neurosci. 1998 Jan 15;18(2):634-40
pubmed: 9425005
J Neurosci. 2003 Oct 29;23(30):9710-8
pubmed: 14585998
Neuron. 1999 Aug;23(4):787-98
pubmed: 10482244
J Neurophysiol. 2016 Jun 1;115(6):2997-3007
pubmed: 26961099
PLoS Biol. 2006 Jul;4(8):e261
pubmed: 16895441
J Neurophysiol. 2018 Sep 1;120(3):1264-1273
pubmed: 29897859
Neuropsychopharmacology. 2006 Dec;31(12):2660-8
pubmed: 16407894
J Neurosci. 2011 Apr 20;31(16):6041-52
pubmed: 21508229
Science. 1994 Sep 23;265(5180):1878-82
pubmed: 7916482
Neuron. 1994 Feb;12(2):261-9
pubmed: 8110457
Cell Rep. 2015 Jul 21;12(3):396-404
pubmed: 26166572
EMBO J. 2006 Jun 21;25(12):2856-66
pubmed: 16763567
Protein Sci. 2018 Aug;27(8):1364-1391
pubmed: 29893445
J Biol Chem. 2001 Aug 31;276(35):32480-8
pubmed: 11431472
Neuron. 2017 Dec 6;96(5):1033-1040.e3
pubmed: 29103807
Nat Neurosci. 2017 Oct 26;20(11):1434-1447
pubmed: 29073641
J Biol Chem. 2014 Apr 4;289(14):10126-39
pubmed: 24567337
Proc Natl Acad Sci U S A. 2018 Jul 10;115(28):7434-7439
pubmed: 29946034
Proc Natl Acad Sci U S A. 2004 Feb 24;101(8):2578-83
pubmed: 14983051
J Cell Biol. 2007 Jan 1;176(1):113-24
pubmed: 17190793
J Neurosci. 1999 Jul 15;19(14):5834-46
pubmed: 10407024
J Biol Chem. 2011 Jan 14;286(2):1181-8
pubmed: 21030594
Eur J Neurosci. 2004 Apr;19(7):1895-905
pubmed: 15078563
Proc Natl Acad Sci U S A. 2003 Oct 14;100(21):12450-5
pubmed: 14519849
Proc Natl Acad Sci U S A. 2007 Feb 13;104(7):2519-24
pubmed: 17284589
Nat Neurosci. 2014 Feb;17(2):269-79
pubmed: 24336151
Nature. 2002 Jan 17;415(6869):321-6
pubmed: 11797009
Neuron. 2011 Jan 27;69(2):304-16
pubmed: 21262468
FEBS Lett. 2018 Nov;592(21):3516-3531
pubmed: 29993122
eNeuro. 2021 Mar 11;8(2):
pubmed: 33593734
J Speech Hear Disord. 1965 May;30:184-6
pubmed: 14281431
Neurosci Lett. 1996 Mar 22;207(1):70-2
pubmed: 8710213
Proc Natl Acad Sci U S A. 2008 Sep 30;105(39):15130-5
pubmed: 18815362
Nature. 1998 Dec 3;396(6710):474-7
pubmed: 9853756
Neuron. 1998 Oct;21(4):837-45
pubmed: 9808469
Neuron. 2016 Feb 17;89(4):683-94
pubmed: 26889809
J Neurophysiol. 1998 Apr;79(4):2181-90
pubmed: 9535977
Cold Spring Harb Perspect Biol. 2012 Feb 01;4(2):
pubmed: 22147943
Proc Natl Acad Sci U S A. 1989 Oct;86(20):8108-12
pubmed: 2510160
Biochem Biophys Res Commun. 1969 Jul 23;36(2):328-36
pubmed: 4308081
Neuron. 2003 Jul 17;39(2):309-25
pubmed: 12873387
J Neurosci. 2007 Sep 26;27(39):10434-44
pubmed: 17898215
Proc Natl Acad Sci U S A. 2008 Sep 23;105(38):14680-5
pubmed: 18799741
J Neurosci. 1994 Feb;14(2):523-37
pubmed: 8301352
Cold Spring Harb Perspect Biol. 2011 Jan 01;3(1):a004143
pubmed: 21123395
J Chem Neuroanat. 2011 Jan;41(1):43-54
pubmed: 21094251
Genome Biol. 2007;8(12):R264
pubmed: 18076763
J Neurosci. 1998 May 1;18(9):3186-94
pubmed: 9547227
Neuroscience. 2000;98(3):407-27
pubmed: 10869836
Neuron. 2005 Feb 3;45(3):327-9
pubmed: 15694316
J Cell Sci. 2006 Jul 15;119(Pt 14):2912-20
pubmed: 16787939
Prog Neurobiol. 2009 Dec;89(4):334-42
pubmed: 19770022
Science. 2007 Feb 16;315(5814):961-6
pubmed: 17303747
Cell Commun Signal. 2010 Jun 25;8:15
pubmed: 20579354
J Physiol. 2009 Jan 15;587(1):101-13
pubmed: 19001039
J Gen Physiol. 1972 Nov;60(5):558-69
pubmed: 4345439
Cell. 2011 Jan 21;144(2):282-95
pubmed: 21241895
Science. 2014 Feb 7;343(6171):665-70
pubmed: 24503854

Auteurs

Meishar Shahoha (M)

Faculty of Life Sciences, School of Neurobiology, Biochemistry and Biophysics, Tel Aviv University, Tel Aviv, Israel.
Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel.

Ronni Cohen (R)

Faculty of Life Sciences, School of Neurobiology, Biochemistry and Biophysics, Tel Aviv University, Tel Aviv, Israel.
Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel.

Yoav Ben-Simon (Y)

Department of Neurophysiology, Vienna Medical University, Vienna, Austria.

Uri Ashery (U)

Faculty of Life Sciences, School of Neurobiology, Biochemistry and Biophysics, Tel Aviv University, Tel Aviv, Israel.
Sagol School of Neuroscience, Tel Aviv University, Tel Aviv, Israel.

Classifications MeSH