PDZ protein mediated activity-dependent LTP/LTD developmental switch at rat retinocollicular synapses.
The insertion of amino-3-hydroxy-5-methyl-4-isoxazole propionic acid (AMPA) receptors into the plasma membrane and removal via internalization are essential for regulating synaptic strength, which underlies the basic mechanism of learning and memory. The retinocollicular pathway undergoes synaptic refinement during development and shows a wide variety of long-term synaptic changes; however, still little is known about its underlying molecular regulation. Here we report a rapid developmental long-term potentiation (LTP)/long-term depression (LTD) switch and its intracellular mechanism at the rat retinocollicular pathway from postnatal day 5 (P5) to P14. Before P9, neurons always exhibited LTP, whereas LTD was observed only after P10. Blockade of GluR2/3-glutamate receptor-interacting protein (GRIP)/AMPA-receptor-binding protein (ABP)/protein interacting with C kinase 1 (PICK1) interactions with pep2-SVKI could sustain the LTP after P10. This suggests that the LTP/LTD switch relied on PDZ protein activities. Selective interruption of GluR2/3-PICK1 binding by pep2-EVKI blocked the long-lasting effects of both LTP and LTD, suggesting a role for PICK1 in the maintenance of long-term synaptic plasticity. Interestingly, synaptic expression of GRIP increased more than twofold from P7 to P11, whereas ABP and PICK1 expression levels remained stable. Blockade of spontaneous retinal input suppressed this increase and abolished the LTP/LTD switch. These results suggest that the increased GRIP synaptic expression may be a key regulatory factor in mediating the activity-dependent developmental LTP/LTD switch, whereas PICK1 may be required for both LTP and LTD to maintain their long-term effects.
Xue
Lei
L
NINDS, National Institutes of Health, Porter Neuroscience Research Center, Bethesda, MD 20892, USA. xuel@ninds.nih.gov
Zhang
Fan
F
Chen
Xianhua
X
Lin
Junji
J
Shi
Jian
J
D000367:Age Factors; D000818:Animals; D000831:Animals, Newborn; D002352:Carrier Proteins / Q000378:metabolism; D003598:Cytoskeletal Proteins; D005071:Evoked Potentials; D019706:Excitatory Postsynaptic Potentials; D066298:In Vitro Techniques; D036341:Intercellular Signaling Peptides and Proteins; D047908:Intracellular Signaling Peptides and Proteins; D007700:Kinetics; D017774:Long-Term Potentiation / Q000187:drug effects; D036881:Long-Term Synaptic Depression / Q000187:drug effects; D009419:Nerve Tissue Proteins / Q000378:metabolism*; D009687:Nuclear Proteins / Q000378:metabolism; D009842:Oligopeptides / Q000494:pharmacology; D054731:PDZ Domains; D051381:Rats; D017207:Rats, Sprague-Dawley; D018091:Receptors, AMPA / Q000378:metabolism; D016194:Receptors, N-Methyl-D-Aspartate / Q000378:metabolism; D055351:Retinal Neurons / Q000187:drug effects / Q000378:metabolism*; D013477:Superior Colliculi / Q000187:drug effects / Q000254:growth & development / Q000378:metabolism*; D013569:Synapses / Q000187:drug effects / Q000378:metabolism*; D009435:Synaptic Transmission / Q000187:drug effects
D002352:Carrier Proteins; D003598:Cytoskeletal Proteins; C491308:Grip1 protein, rat; C118486:Grip2 protein, rat; D036341:Intercellular Signaling Peptides and Proteins; D047908:Intracellular Signaling Peptides and Proteins; D009419:Nerve Tissue Proteins; D009687:Nuclear Proteins; D009842:Oligopeptides; C498298:PICK1 protein, rat; D018091:Receptors, AMPA; D016194:Receptors, N-Methyl-D-Aspartate; C104723:glutamate receptor ionotropic, AMPA 3; C104722:glutamate receptor ionotropic, AMPA 2
J Neurophysiol. 1999 Aug;82(2):526-32
10444652
Acta Med Okayama. 2008 Feb;62(1):21-8
18323868
Neuron. 1999 Jan;22(1):179-87
10027300
Trends Neurosci. 2002 Nov;25(11):578-88
12392933
J Neurosci. 2001 Aug 1;21(15):5417-28
11466413
Cell. 1996 Dec 27;87(7):1327-38
8980238
Nature. 1986 Feb 27-Mar 5;319(6056):774-6
2869411
Nat Neurosci. 2000 Mar;3(3):211-6
10700251
J Neurosci. 2007 Dec 12;27(50):13649-54
18077676
EMBO J. 2005 Sep 21;24(18):3266-78
16138078
Neuron. 2004 Sep 30;44(1):5-21
15450156
J Neurosci. 2000 Jun 15;20(12):RC81
10827202
Neuron. 1998 Aug;21(2):347-57
9728916
Proc Natl Acad Sci U S A. 2002 May 14;99(10):7096-101
12011465
Neuron. 2003 Dec 18;40(6):1147-60
14687549
Neuron. 2000 Nov;28(2):499-510
11144359
J Neurosci. 1982 Jan;2(1):32-48
7054394
Neuron. 2003 Feb 20;37(4):625-38
12597860
J Neurosci. 1992 Apr;12(4):1212-32
1313491
J Comp Neurol. 1991 Apr 22;306(4):697-707
2071701
Nature. 1992 Jun 25;357(6380):686-9
1377360
Nat Neurosci. 2005 Aug;8(8):1043-50
16025109
Neuron. 2000 Dec;28(3):873-86
11163273
Neuron. 2006 Mar 16;49(6):845-60
16543133
Annu Rev Neurosci. 1989;12:13-31
2648947
J Neurosci. 1999 Aug 15;19(16):6930-41
10436050
Nature. 1993 Jan 7;361(6407):31-9
8421494
Vis Neurosci. 1999 May-Jun;16(3):491-501
10349970
J Comp Neurol. 2006 Feb 10;494(5):738-51
16374812
J Neurosci. 2007 Dec 12;27(50):13903-8
18077702
Neuron. 2003 Oct 9;40(2):361-79
14556714
Neuron. 2000 Aug;27(2):313-25
10985351
Neuropharmacology. 2007 Jan;52(1):71-6
16899258
J Neurophysiol. 1998 Feb;79(2):555-66
9463421
Neuron. 2000 Oct;28(1):103-14
11086987
J Neurosci. 2006 Dec 6;26(49):12647-55
17151267
Nat Neurosci. 2001 Mar;4(3):235-6
11224537
J Biol Chem. 2001 Oct 26;276(43):40025-32
11498531
J Neurosci. 2006 Mar 1;26(9):2380-90
16510715
Eur J Neurosci. 2006 Jun;23(11):3043-50
16819993
Annu Rev Neurosci. 2002;25:103-26
12052905
Neuron. 2001 Jan;29(1):157-69
11182088
J Neurosci. 2002 May 1;22(9):3493-503
11978826
Proc Natl Acad Sci U S A. 2001 Sep 25;98(20):11725-30
11573007
Curr Opin Neurobiol. 1994 Jun;4(3):389-99
7919934
Eur J Neurosci. 2004 Sep;20(5):1331-40
15341604
Annu Rev Neurosci. 2000;23:649-711
10845078
Mol Cell Neurosci. 2008 Jun;38(2):189-202
18417360
J Neurosci. 1986 Dec;6(12):3692-705
3794796
J Neurosci. 1997 Aug 15;17(16):6264-76
9236237
Eur J Neurosci. 2002 May;15(9):1421-32
12028352
J Neurosci. 2000 Oct 1;20(19):7258-67
11007883
Science. 1995 Mar 10;267(5203):1510-2
7878472
Nature. 1997 Mar 20;386(6622):279-84
9069286
Cell. 1998 Jan 23;92(2):279-89
9458051
J Neurosci. 2008 Jan 2;28(1):292-303
18171946
Nat Neurosci. 2002 Feb;5(2):155-61
11788834
J Neurosci. 2008 May 28;28(22):5752-5
18509036
Neuron. 1996 Feb;16(2):333-44
8789948
Trends Neurosci. 1993 Dec;16(12):521-7
7509523
J Neurophysiol. 1992 Apr;67(4):841-51
1350308
Neuron. 1998 Sep;21(3):581-91
9768844
J Neurosci. 2004 Dec 8;24(49):11098-107
15590926
J Neurosci. 2005 Feb 2;25(5):1291-303
15689567
J Neurosci Methods. 2006 Nov 15;158(1):30-6
16797717
Neuron. 2005 Aug 4;47(3):407-21
16055064
J Neurosci. 1997 Apr 1;17(7):2469-76
9065507
BMC Neurosci. 2007 Jul 26;8:55
17655746
J Neurosci. 1985 Aug;5(8):2240-53
2991484
Nat Neurosci. 1999 Nov;2(11):972-7
10526335
Neuropharmacology. 2007 Jan;52(1):60-70
16904707