Guidance molecules in synapse formation and plasticity.
A major goal of modern neuroscience research is to understand the cellular and molecular processes that control the formation, function, and remodeling of chemical synapses. In this article, we discuss the numerous studies that implicate molecules initially discovered for their functions in axon guidance as critical regulators of synapse formation and plasticity. Insights from these studies have helped elucidate basic principles of synaptogenesis, dendritic spine formation, and structural and functional synapse plasticity. In addition, they have revealed interesting dual roles for proteins and cellular mechanisms involved in both axon guidance and synaptogenesis. Much like the dual involvement of morphogens in early cell fate induction and axon guidance, many guidance-related molecules continue to play active roles in controlling the location, number, shape, and strength of neuronal synapses during development and throughout the lifetime of the organism. This article summarizes key findings that link axon guidance molecules to specific aspects of synapse formation and plasticity and discusses the emerging relationship between the molecular and cellular mechanisms that control both axon guidance and synaptogenesis.
Shen
Kang
K
Department of Biology, Howard Hughes Medical Institute, Stanford University, Stanford, California 94305, USA.
Cowan
Christopher W
CW
D000199:Actins / Q000502:physiology; D000818:Animals; D019208:Brain-Derived Neurotrophic Factor / Q000502:physiology; D055495:Neurogenesis / Q000502:physiology*; D009473:Neuronal Plasticity / Q000502:physiology*; D009474:Neurons / Q000502:physiology* / Q000648:ultrastructure; D020813:Receptor, trkB / Q000502:physiology; D013569:Synapses / Q000502:physiology* / Q000648:ultrastructure
D000199:Actins; D019208:Brain-Derived Neurotrophic Factor; D020813:Receptor, trkB
Neuron. 1996 Jul;17(1):91-102
8755481
Mol Cell Neurosci. 1998 Aug;11(5-6):247-59
9698392
Cell. 1996 Jul 12;86(1):35-46
8689685
Cell. 2000 Mar 3;100(5):525-35
10721990
Neuron. 2008 Jul 31;59(2):253-60
18667153
Nat Rev Neurosci. 2009 Apr;10(4):262-71
19300445
Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13438-43
10557339
Synapse. 2003 Dec 1;50(3):171-80
14515334
Neuron. 1990 Jan;4(1):61-85
2310575
J Neurosci. 2001 Jun 15;21(12):4249-58
11404410
J Biol Chem. 2009 Jun 5;284(23):15857-66
19332546
Neuron. 2003 Jul 17;39(2):255-67
12873383
Neuron. 2007 Nov 21;56(4):640-56
18031682
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7265-70
17440041
Mol Cell Neurosci. 2007 Dec;36(4):425-34
17826176
Nat Neurosci. 2007 Mar;10(3):301-10
17310244
J Neurosci. 2007 Jul 11;27(28):7508-19
17626212
Cell. 2007 Aug 24;130(4):704-16
17719547
Science. 2007 Oct 5;318(5847):103-6
17916735
Neuron. 2003 May 8;38(3):389-401
12741987
Neuron. 2003 May 8;38(3):447-60
12741991
Annu Rev Cell Dev Biol. 2007;23:263-92
17539753
Hippocampus. 2003;13(1):1-20
12625453
J Neurosci. 2005 Apr 13;25(15):3774-86
15829629
Neuron. 2003 Jan 23;37(2):263-74
12546821
Nat Neurosci. 2007 Jan;10(1):67-76
17143272
Neuron. 2005 Apr 21;46(2):205-17
15848800
Epilepsia. 2009 Apr;50(4):629-45
18657176
Brain Res. 2002 Nov 22;956(1):67-73
12426047
J Cell Biol. 2003 Dec 22;163(6):1313-26
14691139
Neuron. 2007 Jan 18;53(2):217-32
17224404
J Neurosci. 1999 Jun 1;19(11):4314-24
10341235
J Cell Biol. 2007 Sep 24;178(7):1295-307
17875741
Nature. 2008 Oct 2;455(7213):669-73
18776887
Proc Natl Acad Sci U S A. 2009 Aug 4;106(31):13058-63
19625617
Neuron. 2003 Jul 17;39(2):241-54
12873382
J Neurosci. 2007 Dec 19;27(51):14205-15
18094260
Nat Neurosci. 2004 Jan;7(1):33-40
14699416
Science. 2002 Jun 7;296(5574):1864-9
12052960
J Neurosci. 2008 Dec 10;28(50):13592-608
19074033
Neuron. 2001 Dec 20;32(6):1041-56
11754836
Proc Natl Acad Sci U S A. 2001 Dec 4;98(25):14702-7
11724927
Neuron. 2008 Mar 13;57(5):719-29
18341992
J Neurosci. 2005 Apr 6;25(14):3613-20
15814792
Nature. 2004 Jun 17;429(6993):761-6
15190253
Neuron. 2002 Jul 3;35(1):121-33
12123613
Exp Neurol. 2003 Jul;182(1):142-50
12821384
Neuron. 1999 Oct;24(2):401-14
10571233
Science. 2008 Mar 21;319(5870):1683-7
18309046
Cell. 2000 Dec 8;103(6):945-56
11136979
Nat Neurosci. 2009 Oct;12(10):1285-92
19734893
Neuron. 2009 May 28;62(4):510-25
19477153
J Neurosci. 2007 Mar 7;27(10):2513-24
17344389
Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10444-10449
16801538
Nat Neurosci. 2008 Feb;11(2):160-9
18193042
Nature. 2006 Jan 19;439(7074):283-9
16421561
J Neurosci. 1999 Jun 15;19(12):4972-83
10366630
Neuron. 2003 Nov 13;40(4):807-21
14622584
Annu Rev Biochem. 2003;72:609-42
12676795
Nat Neurosci. 2004 Apr;7(4):357-63
15034585
Philos Trans R Soc Lond B Biol Sci. 1986 Nov 12;314(1165):1-340
22462104
Neural Dev. 2009 May 23;4:18
19463192
J Neurosci. 2006 Mar 29;26(13):3474-81
16571754
J Neurosci. 2006 Nov 22;26(47):12152-64
17122040
J Neurosci. 2006 Oct 18;26(42):10813-25
17050720
J Neurosci. 2007 May 9;27(19):5127-38
17494698
Neuron. 1996 Jun;16(6):1137-45
8663990
Neuron. 2008 Jul 10;59(1):56-69
18614029
Proc Natl Acad Sci U S A. 1995 Sep 12;92(19):8856-60
7568031
Nat Rev Neurosci. 2004 Jan;5(1):24-34
14708001
Science. 2002 Jan 18;295(5554):491-5
11799243
Neuron. 1999 Sep;24(1):127-41
10677032
Prog Brain Res. 2006;157:15-24
17167900
J Neurosci. 2008 Mar 12;28(11):2753-65
18337405
Nature. 2002 Dec 19-26;420(6917):788-94
12490942
J Neurosci. 2008 Jul 2;28(27):7006-12
18596174
Nat Cell Biol. 2002 Aug;4(8):583-91
12134159
Nat Neurosci. 2003 Feb;6(2):153-60
12496762
Eur J Neurosci. 2006 May;23(9):2247-54
16706833
J Biol Chem. 2008 Feb 29;283(9):5918-27
18096705
Nature. 2009 Dec 24;462(7276):1065-9
20010807
J Neurobiol. 2005 Sep 15;64(4):417-34
16041756
Proc Natl Acad Sci U S A. 2009 Jul 28;106(30):12524-9
19592509
Nat Neurosci. 2004 Oct;7(10):1104-12
15361876
Nat Neurosci. 2006 Jun;9(6):798-806
16680164
Neuron. 2002 Jul 3;35(1):77-89
12123610
Mol Cell Neurosci. 2004 Jul;26(3):429-40
15234347
J Neurosci. 2007 Mar 14;27(11):3017-29
17360925
J Neurosci. 2007 Oct 17;27(42):11279-88
17942722
Dev Biol. 2006 Apr 1;292(1):34-45
16466709
Curr Opin Neurobiol. 2006 Feb;16(1):95-101
16361095
Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6856-61
10823894
Learn Mem. 2004 Mar-Apr;11(2):172-8
15054132
J Neurosci. 1998 Nov 1;18(21):8900-11
9786995
Neurobiol Learn Mem. 2008 Mar;89(3):312-23
17942328
Prog Neurobiol. 2003 Oct;71(2-3):249-67
14687984
Nature. 1996 Jun 20;381(6584):706-9
8649517
Nat Neurosci. 2002 Nov;5(11):1117-8
12389031
Science. 1998 Jul 31;281(5377):706-9
9685266
Curr Opin Cell Biol. 2003 Oct;15(5):621-32
14519398
Nat Neurosci. 2008 Sep;11(9):1035-43
19160501
Neuron. 2007 Jul 5;55(1):53-68
17610817