Neuronal Cytoskeleton in Intellectual Disability: From Systems Biology and Modeling to Therapeutic Opportunities.
Boolean modeling
GTPase signaling
actin cytoskeleton
intellectual disability
microtubules
neuronal networks
pharmacological modulation
protein:protein interaction network
small Rho GTPases
systems biology
Journal
International journal of molecular sciences
ISSN: 1422-0067
Titre abrégé: Int J Mol Sci
Pays: Switzerland
ID NLM: 101092791
Informations de publication
Date de publication:
07 Jun 2021
07 Jun 2021
Historique:
received:
05
05
2021
revised:
25
05
2021
accepted:
04
06
2021
entrez:
2
7
2021
pubmed:
3
7
2021
medline:
27
7
2021
Statut:
epublish
Résumé
Intellectual disability (ID) is a pathological condition characterized by limited intellectual functioning and adaptive behaviors. It affects 1-3% of the worldwide population, and no pharmacological therapies are currently available. More than 1000 genes have been found mutated in ID patients pointing out that, despite the common phenotype, the genetic bases are highly heterogeneous and apparently unrelated. Bibliomic analysis reveals that ID genes converge onto a few biological modules, including cytoskeleton dynamics, whose regulation depends on Rho GTPases transduction. Genetic variants exert their effects at different levels in a hierarchical arrangement, starting from the molecular level and moving toward higher levels of organization, i.e., cell compartment and functions, circuits, cognition, and behavior. Thus, cytoskeleton alterations that have an impact on cell processes such as neuronal migration, neuritogenesis, and synaptic plasticity rebound on the overall establishment of an effective network and consequently on the cognitive phenotype. Systems biology (SB) approaches are more focused on the overall interconnected network rather than on individual genes, thus encouraging the design of therapies that aim to correct common dysregulated biological processes. This review summarizes current knowledge about cytoskeleton control in neurons and its relevance for the ID pathogenesis, exploiting in silico modeling and translating the implications of those findings into biomedical research.
Identifiants
pubmed: 34200511
pii: ijms22116167
doi: 10.3390/ijms22116167
pmc: PMC8201358
pii:
doi:
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : Fondazione Telethon
ID : GGP20039
Références
Neuropsychopharmacology. 2012 Jan;37(1):196-212
pubmed: 21937981
Am J Hum Genet. 2017 Nov 2;101(5):768-788
pubmed: 29100089
Expert Opin Drug Discov. 2015 Jun;10(6):615-29
pubmed: 25891144
J Neurochem. 2010 Dec;115(6):1309-21
pubmed: 21044075
J Neurosci. 2008 May 21;28(21):5422-32
pubmed: 18495876
Am J Hum Genet. 2014 Dec 4;95(6):721-8
pubmed: 25480035
J Med Genet. 2019 Sep;56(9):567-573
pubmed: 30842223
Hum Mol Genet. 2020 Jul 29;29(12):1950-1968
pubmed: 31943058
J Med Genet. 1998 Oct;35(10):801-5
pubmed: 9783701
J Biol Chem. 2007 May 4;282(18):13692-702
pubmed: 17360713
Nat Rev Mol Cell Biol. 2009 May;10(5):332-43
pubmed: 19373241
Nature. 1998 Sep 10;395(6698):194-8
pubmed: 9744280
J Cell Biol. 2007 Jul 30;178(3):503-16
pubmed: 17664338
Nat Genet. 1998 Jun;19(2):134-9
pubmed: 9620768
Biol Psychiatry. 2011 May 1;69(9):898-901
pubmed: 21237447
Nature. 2006 Aug 17;442(7104):814-7
pubmed: 16862120
Nat Genet. 2013 Jun;45(6):639-47
pubmed: 23603762
Neural Plast. 2016;2016:8051861
pubmed: 27795858
Am J Hum Genet. 2001 Aug;69(2):261-8
pubmed: 11431708
J Cell Biol. 1997 Mar 24;136(6):1307-22
pubmed: 9087445
Curr Biol. 2016 Apr 4;26(7):849-61
pubmed: 26948876
Front Cell Neurosci. 2014 Mar 27;8:81
pubmed: 24733999
Elife. 2017 Sep 26;6:
pubmed: 28949297
Neuron. 2002 Feb 28;33(5):741-50
pubmed: 11879651
J Cell Biol. 1999 Dec 27;147(7):1519-32
pubmed: 10613909
J Biol Chem. 1998 Feb 6;273(6):3470-5
pubmed: 9452470
Neuropharmacology. 2011 Jul-Aug;61(1-2):305-12
pubmed: 21569781
Neuroscience. 2019 Apr 15;404:423-444
pubmed: 30742961
EMBO J. 2005 Feb 9;24(3):473-86
pubmed: 15660133
Nature. 2013 Jan 17;493(7432):411-5
pubmed: 23263185
Nature. 2010 Nov 25;468(7323):533-8
pubmed: 21107423
Am J Med Genet A. 2021 May;185(5):1575-1581
pubmed: 33638601
Nature. 2011 Oct 26;478(7370):483-9
pubmed: 22031440
J Biol Chem. 2007 Dec 7;282(49):35666-78
pubmed: 17932039
J Biol Chem. 1982 Apr 25;257(8):4166-70
pubmed: 6461652
J Biol Chem. 1996 Aug 23;271(34):20246-9
pubmed: 8702756
EMBO J. 2018 Dec 14;37(24):
pubmed: 30266824
Neuron. 2004 Jun 24;42(6):947-59
pubmed: 15207239
Proc Natl Acad Sci U S A. 2007 Apr 24;104(17):7265-70
pubmed: 17440041
Proc Natl Acad Sci U S A. 2007 Jan 9;104(2):636-41
pubmed: 17202256
Science. 2011 Sep 9;333(6048):1456-8
pubmed: 21778362
J Cell Biol. 2007 Jul 2;178(1):107-19
pubmed: 17606869
Sci Rep. 2017 Nov 27;7(1):16407
pubmed: 29180826
J Neurosci. 2014 Sep 3;34(36):11929-47
pubmed: 25186741
Nat Cell Biol. 2006 Jan;8(1):17-26
pubmed: 16341208
J Mol Biol. 2006 May 26;359(1):35-46
pubmed: 16616186
J Biol Chem. 2003 May 23;278(21):19220-9
pubmed: 12626503
Mol Biol Cell. 2012 Nov;23(22):4383-92
pubmed: 23015759
J Cell Sci. 2013 Mar 1;126(Pt 5):1122-33
pubmed: 23321640
Cell Mol Neurobiol. 2021 Feb 11;:
pubmed: 33575839
Am J Hum Genet. 2015 Sep 3;97(3):493-500
pubmed: 26340335
Proc Natl Acad Sci U S A. 2010 Mar 30;107(13):5875-80
pubmed: 20231446
Mol Psychiatry. 2015 Sep;20(9):1069-78
pubmed: 25311365
Transl Psychiatry. 2017 Dec 11;7(12):1278
pubmed: 29225346
J Mol Biol. 1977 Sep 25;115(3):465-83
pubmed: 563468
J Cell Biol. 2017 Aug 7;216(8):2533-2550
pubmed: 28642362
EMBO Rep. 2004 Feb;5(2):154-60
pubmed: 14749719
Am J Hum Genet. 2017 Sep 7;101(3):466-477
pubmed: 28886345
Am J Hum Genet. 2020 Nov 5;107(5):963-976
pubmed: 33157009
Neurobiol Aging. 1994;15 Suppl 2:S87-9
pubmed: 7700471
Sci Transl Med. 2014 Oct 1;6(256):256ra135
pubmed: 25273096
Hum Mol Genet. 2011 Jul 1;20(13):2585-90
pubmed: 21498477
Glia. 2020 May;68(5):947-962
pubmed: 31743496
Science. 1996 Jul 12;273(5272):245-8
pubmed: 8662509
Hum Mol Genet. 2017 Sep 15;26(18):3520-3530
pubmed: 28641386
Physiol Rev. 2001 Apr;81(2):871-927
pubmed: 11274346
Hum Mol Genet. 2012 Oct 1;21(19):4270-85
pubmed: 22763239
Trends Neurosci. 1995 Apr;18(4):196-201
pubmed: 7778191
Mol Psychiatry. 2018 Apr;23(4):973-984
pubmed: 28397838
Glia. 2003 Dec;44(3):264-74
pubmed: 14603467
Neuroscience. 2020 Jul 15;439:125-136
pubmed: 31356900
J Neurosci. 2001 Apr 1;21(7):2361-72
pubmed: 11264310
Curr Biol. 2013 Mar 18;23(6):529-34
pubmed: 23453953
Annu Rev Genet. 2011;45:81-104
pubmed: 21910631
Nat Neurosci. 2007 Jan;10(1):67-76
pubmed: 17143272
Sci Rep. 2013;3:1224
pubmed: 23390575
J Cell Biol. 1997 Nov 3;139(3):797-807
pubmed: 9348295
J Neurosci. 2005 Nov 16;25(46):10627-36
pubmed: 16291935
Neuron. 1998 Sep;21(3):593-606
pubmed: 9768845
Eur J Clin Chem Clin Biochem. 1993 Aug;31(8):477-89
pubmed: 8218579
J Neurosci. 2000 Apr 1;20(7):2459-69
pubmed: 10729326
Small GTPases. 2014;5:e29769
pubmed: 24987837
Proc Natl Acad Sci U S A. 2004 May 18;101(20):7618-23
pubmed: 15128949
Mol Biol Cell. 2010 Jan 1;21(1):165-76
pubmed: 19889835
Int J Biol Macromol. 2019 Feb 1;122:1080-1089
pubmed: 30218739
Nature. 1998 Apr 30;392(6679):923-6
pubmed: 9582072
J Inherit Metab Dis. 2009 Oct;32(5):618-29
pubmed: 19731074
J Neurosci. 2013 Jul 17;33(29):11932-48
pubmed: 23864681
Expert Rev Mol Med. 2019 Jan 30;20:e7
pubmed: 30698126
Nat Cell Biol. 2000 Sep;2(9):637-44
pubmed: 10980705
Genes Cells. 2008 Mar;13(3):285-94
pubmed: 18298802
Cell Mol Life Sci. 2011 May;68(9):1633-43
pubmed: 20976519
J Biol Chem. 2001 Jun 1;276(22):18977-83
pubmed: 11279039
Nature. 1997 Jun 12;387(6634):725-9
pubmed: 9192900
Neuron. 2019 Jun 19;102(6):1199-1210.e6
pubmed: 31078368
PLoS Biol. 2007 Apr;5(4):e63
pubmed: 17341134
Cells. 2020 Mar 31;9(4):
pubmed: 32244264
Neurosci Lett. 2018 Aug 24;682:32-38
pubmed: 29885454
Nature. 2017 Nov 9;551(7679):227-231
pubmed: 29088697
J Med Genet. 2016 Nov;53(11):735-742
pubmed: 27418539
Neuropsychopharmacology. 2012 Apr;37(5):1152-63
pubmed: 22157810
Hum Mutat. 2016 Apr;37(4):354-8
pubmed: 26751395
EMBO J. 2003 Aug 15;22(16):4190-201
pubmed: 12912917
Annu Rev Med. 1997;48:353-74
pubmed: 9046968
Nat Struct Biol. 2003 Dec;10(12):1058-63
pubmed: 14578936
J Neurosci. 1999 Jun 1;19(11):4314-24
pubmed: 10341235
Nature. 2002 Aug 15;418(6899):790-3
pubmed: 12181570
Trends Cell Biol. 1997 Dec;7(12):479-84
pubmed: 17709011
Neurosci Biobehav Rev. 2014 Nov;47:735-52
pubmed: 25155242
J Neurosci. 2014 Sep 3;34(36):12168-81
pubmed: 25186760
Proc Natl Acad Sci U S A. 2001 Jan 30;98(3):1261-6
pubmed: 11158627
J Neurosci Res. 1992 Dec;33(4):505-12
pubmed: 1484385
World J Biol Psychiatry. 2020 Oct 6;:1-11
pubmed: 32914658
Cell Rep. 2019 Feb 19;26(8):2037-2051.e6
pubmed: 30784587
Hum Genet. 2015 Jan;134(1):97-109
pubmed: 25326669
Mol Cell Neurosci. 2003 Aug;23(4):574-86
pubmed: 12932438
Curr Biol. 2005 Nov 8;15(21):1961-7
pubmed: 16271875
Proc Natl Acad Sci U S A. 2011 Aug 30;108(35):14449-54
pubmed: 21844371
J Biol Chem. 2007 Jul 20;282(29):21497-506
pubmed: 17537723
Biol Open. 2013 Mar 15;2(3):277-82
pubmed: 23519094
Cell. 2001 Oct 19;107(2):209-21
pubmed: 11672528
Bioinform Biol Insights. 2015 Oct 27;9(Suppl 1):21-7
pubmed: 26523118
Dev Cell. 2015 Jul 27;34(2):152-67
pubmed: 26166300
Exp Cell Res. 2013 Sep 10;319(15):2368-74
pubmed: 23769912
J Neurosci. 2010 Mar 10;30(10):3589-99
pubmed: 20219993
Proc Natl Acad Sci U S A. 2021 Mar 9;118(10):
pubmed: 33649238
Oncogene. 1995 Oct 5;11(7):1271-81
pubmed: 7478547
Nat Rev Mol Cell Biol. 2013 Jan;14(1):7-12
pubmed: 23212475
Am J Med Genet A. 2020 Apr;182(4):792-797
pubmed: 31953988
Neuron. 2009 Jan 15;61(1):85-100
pubmed: 19146815
Nat Rev Neurosci. 2020 Dec;21(12):682-694
pubmed: 33046886
Arch Dis Child. 2002 Jan;86(1):54-6
pubmed: 11806886
Cereb Cortex. 2000 Oct;10(10):1038-44
pubmed: 11007554
Genes Dev. 2004 Apr 15;18(8):862-76
pubmed: 15078817
EMBO J. 2007 Sep 5;26(17):3888-99
pubmed: 17690689
Medicine (Baltimore). 2020 Aug 14;99(33):e21632
pubmed: 32872024
Neuropharmacology. 2009 Jan;56(1):73-80
pubmed: 18644395
J Neurosci. 2003 Apr 15;23(8):3343-52
pubmed: 12716942
J Biol Chem. 2015 Nov 27;290(48):28613-22
pubmed: 26453304
Am J Hum Genet. 2018 Feb 1;102(2):309-320
pubmed: 29394990
Nature. 1998 Jun 25;393(6687):805-9
pubmed: 9655397
Nat Rev Neurosci. 2009 May;10(5):319-32
pubmed: 19377501
Mol Cell Neurosci. 2002 Aug;20(4):579-94
pubmed: 12213441
Brain. 2003 Jul;126(Pt 7):1537-44
pubmed: 12805098
Brain Struct Funct. 2016 Jun;221(5):2427-42
pubmed: 26026482
Nucleic Acids Res. 2009 Jan;37(Database issue):D793-6
pubmed: 18842627
J Neurosci. 2016 Sep 21;36(38):9792-804
pubmed: 27656019
FEBS Lett. 2002 Jun 19;521(1-3):14-8
pubmed: 12067717
Nat Genet. 1998 Sep;20(1):25-30
pubmed: 9731525
Nat Genet. 2000 Oct;26(2):247-50
pubmed: 11017088
J Theor Biol. 2003 Jul 7;223(1):1-18
pubmed: 12782112
Mol Cell. 1998 Jan;1(2):183-92
pubmed: 9659915
J Cell Biol. 2010 May 17;189(4):619-29
pubmed: 20457765
Mol Genet Metab. 2017 Jun;121(2):127-137
pubmed: 28495044
JAMA Psychiatry. 2016 Mar;73(3):275-83
pubmed: 26817790
Nat Genet. 2000 May;25(1):25-9
pubmed: 10802651
Sci Rep. 2015 Jul 24;5:12434
pubmed: 26207352
Development. 2018 Oct 2;145(19):
pubmed: 30177526
Genome Biol. 2002;3(5):reviews3007
pubmed: 12049672
Mol Autism. 2021 Jan 13;12(1):1
pubmed: 33436060
J Neurosci. 2008 Jan 2;28(1):264-78
pubmed: 18171944
Proc Natl Acad Sci U S A. 2003 Oct 28;100(22):12923-8
pubmed: 14534328
Sci Rep. 2016 Oct 07;6:34877
pubmed: 27713499
J Biol Chem. 2004 Jan 2;279(1):713-9
pubmed: 14570905
Am J Hum Genet. 2013 Aug 8;93(2):368-83
pubmed: 23871722
Nat Neurosci. 2007 Jul;10(7):880-886
pubmed: 17529984
Am J Med Genet A. 2014 Sep;164A(9):2294-9
pubmed: 24898194
Exp Brain Res. 2017 Jun;235(6):1645-1655
pubmed: 28299411
Sci Transl Med. 2013 Apr 24;5(182):182ra53
pubmed: 23616120
J Neurosci. 1998 Apr 1;18(7):2423-36
pubmed: 9502803
Mol Biol Cell. 2007 Nov;18(11):4327-42
pubmed: 17699587
Annu Rev Biophys Biomol Struct. 2007;36:451-77
pubmed: 17477841
FEBS Lett. 2015 Dec 21;589(24 Pt B):3795-806
pubmed: 26545494
J Med Genet. 2014 Jul;51(7):487-94
pubmed: 24812067
CNS Spectr. 2008 Jul;13(7):598-605
pubmed: 18622364
Cell. 1995 Oct 20;83(2):171-6
pubmed: 7585934
Biochem Biophys Res Commun. 2019 Sep 3;516(4):1204-1210
pubmed: 31296385
Neurobiol Learn Mem. 2019 Dec;166:107070
pubmed: 31445077
Science. 1999 Mar 26;283(5410):2083-5
pubmed: 10092231
J Cell Biol. 1998 Apr 20;141(2):431-41
pubmed: 9548721
Neuron. 1995 Apr;14(4):763-71
pubmed: 7536426
Pediatrics. 2014 Oct;134(4):e1149-62
pubmed: 25180280
Nat Rev Mol Cell Biol. 2013 Jul;14(7):405-15
pubmed: 23778968
Nature. 1998 Jun 25;393(6687):809-12
pubmed: 9655398
Cell. 2003 Feb 21;112(4):453-65
pubmed: 12600310
J Mol Neurosci. 2019 Jul;68(3):321-330
pubmed: 31127536
Genes Dev. 1996 Apr 1;10(7):816-25
pubmed: 8846918
Cell. 2002 Jan 25;108(2):233-46
pubmed: 11832213
Am J Hum Genet. 2001 Jun;68(6):1497-500
pubmed: 11326334
J Am Acad Child Adolesc Psychiatry. 2005 Nov;44(11):1137-44
pubmed: 16239862
Mol Syndromol. 2012 Apr;2(3-5):202-212
pubmed: 22670141
J Clin Invest. 2014 Apr;124(4):1468-82
pubmed: 24614104
J Neurosci. 2006 Feb 1;26(5):1418-28
pubmed: 16452665
Hum Mol Genet. 2016 Mar 1;25(5):892-902
pubmed: 26721934
Genes Dev. 2012 Aug 1;26(15):1743-57
pubmed: 22810622
J Cell Biol. 1994 Aug;126(3):801-10
pubmed: 8045941
Front Neurosci. 2014 Oct 22;8:338
pubmed: 25374504
Mol Microbiol. 1997 Jun;24(5):1061-70
pubmed: 9220012
Genome Med. 2017 May 30;9(1):43
pubmed: 28554332
Mol Cell. 2009 Sep 24;35(6):841-55
pubmed: 19782033
Proc Natl Acad Sci U S A. 2006 Jul 5;103(27):10444-10449
pubmed: 16801538
Am J Med Genet A. 2003 Aug 1;120A(4):509-17
pubmed: 12884430
Cell. 2011 Mar 4;144(5):810-23
pubmed: 21376239
J Neurochem. 2013 Jul;126(2):165-82
pubmed: 23574039
Neurol Genet. 2017 May 26;3(3):e148
pubmed: 28589176
J Med Genet. 2013 Dec;50(12):819-22
pubmed: 24065355
J Cell Biol. 2000 Aug 7;150(3):567-80
pubmed: 10931868
J Neurosci. 2007 Aug 29;27(35):9439-50
pubmed: 17728457
Brain Res. 2011 Jul 5;1399:79-95
pubmed: 21645877
Trends Neurosci. 2016 Jul;39(7):433-440
pubmed: 27233682
J Neurosci. 2013 Oct 2;33(40):15767-78
pubmed: 24089484
Biopolymers. 2017 Nov 27;:
pubmed: 29178143
Physiol Rev. 2013 Jan;93(1):269-309
pubmed: 23303910
Small GTPases. 2018 May 4;9(3):224-229
pubmed: 27572055
J Neurosci. 2019 Nov 20;39(47):9306-9315
pubmed: 31597723
J Neurosci. 2008 Nov 19;28(47):12368-82
pubmed: 19020030
Nature. 1984 Nov 15-21;312(5991):237-42
pubmed: 6504138
Curr Biol. 2002 Oct 1;12(19):1704-10
pubmed: 12361576
Mol Cell Endocrinol. 2016 Jul 5;429:50-61
pubmed: 27040307
Stem Cell Reports. 2018 Apr 10;10(4):1251-1266
pubmed: 29526735
ACS Chem Neurosci. 2017 Jan 18;8(1):5-7
pubmed: 28095679
Nature. 2011 Apr 7;472(7341):100-4
pubmed: 21423166
PLoS Genet. 2017 Apr 28;13(4):e1006746
pubmed: 28453519
Nat Genet. 2011 Jun;43(6):601-6
pubmed: 21552264
Genet Med. 2021 Mar;23(3):543-554
pubmed: 33149277
Neuron. 2014 Oct 22;84(2):292-309
pubmed: 25374356
Traffic. 2007 Jan;8(1):12-20
pubmed: 17229312
Science. 1999 Aug 6;285(5429):895-8
pubmed: 10436159
PLoS One. 2016 Feb 05;11(2):e0148634
pubmed: 26849555
Nat Med. 2008 Aug;14(8):843-8
pubmed: 18568033
J Cell Biol. 1999 May 31;145(5):1009-26
pubmed: 10352018
EMBO J. 1998 Dec 1;17(23):6932-41
pubmed: 9843499
Genome Res. 2003 Nov;13(11):2498-504
pubmed: 14597658
Hum Mol Genet. 1999 Aug;8(8):1387-96
pubmed: 10400985
Nature. 1994 Sep 29;371(6496):419-23
pubmed: 8090221
J Child Neurol. 2010 Jul;25(7):892-7
pubmed: 20097664
Cell Rep. 2015 Jun 9;11(9):1400-1413
pubmed: 26027926
Development. 2016 Feb 1;143(3):449-60
pubmed: 26718007
Cancer Res. 2005 Apr 15;65(8):3092-9
pubmed: 15833838
Neuron. 2016 Jan 6;89(1):37-53
pubmed: 26687838
Hum Mol Genet. 2012 Jan 15;21(2):268-86
pubmed: 21989057
J Physiol. 2018 Jul;596(14):2773-2782
pubmed: 29380377
BMC Med Genet. 2020 Feb 12;21(1):31
pubmed: 32050918
Hum Mutat. 2014 Jan;35(1):41-4
pubmed: 24115387
J Neurosci. 2004 Mar 10;24(10):2481-95
pubmed: 15014124
Seizure. 2018 Jul;59:38-40
pubmed: 29734022
Nucleic Acids Res. 2021 Jan 8;49(D1):D325-D334
pubmed: 33290552
Drug Discov Today. 2014 Apr;19(4):510-9
pubmed: 24508819
Trends Cell Biol. 2013 Dec;23(12):644-51
pubmed: 23988427
Eur Neuropsychopharmacol. 2015 Jun;25(6):889-901
pubmed: 25890884
Glia. 2018 Jun;66(6):1244-1262
pubmed: 29076603
J Cell Biol. 2006 Feb 27;172(5):759-69
pubmed: 16492808
Behav Brain Res. 2010 Sep 1;212(1):78-83
pubmed: 20362628
Stem Cells Transl Med. 2016 Jul;5(7):860-9
pubmed: 27160703
Nat Commun. 2016 Nov 08;7:13316
pubmed: 27824329
J Mol Med (Berl). 1999 Jun;77(6):469-80
pubmed: 10475062
Curr Opin Neurobiol. 2009 Apr;19(2):146-53
pubmed: 19523814
Mol Cell. 2002 Jan;9(1):73-83
pubmed: 11804587
Cold Spring Harb Perspect Biol. 2016 Aug 01;8(8):
pubmed: 26988969
J Cell Biol. 2008 Feb 11;180(3):619-32
pubmed: 18268107
Nature. 1995 May 25;375(6529):338-40
pubmed: 7753201
Biol Psychiatry. 2017 Feb 1;81(3):179-192
pubmed: 27587266
J Hum Genet. 2020 May;65(5):481-485
pubmed: 32005903
Springerplus. 2015 Jun 12;4(Suppl 1):L37
pubmed: 27386198
J Biol Chem. 1995 Jul 21;270(29):17582-7
pubmed: 7615564
Neuropsychopharmacology. 2014 Dec;39(13):2938-48
pubmed: 24964813
Nature. 1997 Jul 3;388(6637):78-82
pubmed: 9214506
Nat Neurosci. 2010 Oct;13(10):1208-15
pubmed: 20835250
Mol Cell Biol. 1997 Mar;17(3):1201-11
pubmed: 9032247
Neurogenesis (Austin). 2016 Dec 27;3(1):e1261653
pubmed: 28405589
Sci Rep. 2018 May 8;8(1):7254
pubmed: 29740022
Cell. 2015 Aug 13;162(4):795-807
pubmed: 26255772
Neuron. 2013 Oct 30;80(3):704-17
pubmed: 24183021
Elife. 2014 Jul 08;3:
pubmed: 25006034
Proc Natl Acad Sci U S A. 2005 Jan 4;102(1):227-31
pubmed: 15615853
Sci Rep. 2018 Jun 11;8(1):8811
pubmed: 29891904
Mol Cell Neurosci. 2003 Aug;23(4):661-8
pubmed: 12932445
Int J Biochem Cell Biol. 2008;40(4):619-37
pubmed: 18023603
J Neurochem. 2015 Jun;133(6):767-79
pubmed: 25818528
J Neurosci. 2004 Jun 23;24(25):5778-88
pubmed: 15215300
J Mol Neurosci. 2020 Jun;70(6):908-915
pubmed: 31942680
Neurogenetics. 2018 Jan;19(1):9-16
pubmed: 29130122
J Cell Biol. 1998 Jun 29;141(7):1625-36
pubmed: 9647654
J Cell Sci. 2008 Aug 1;121(Pt 15):2601-11
pubmed: 18628310
J Appl Genet. 2010;51(1):111-3
pubmed: 20145308
J Comp Neurol. 2000 Jan 17;416(3):319-34
pubmed: 10602091
Am J Med Genet A. 2014 May;164A(5):1277-83
pubmed: 24664804
EMBO J. 1996 Apr 15;15(8):1885-93
pubmed: 8617235
Eur J Neurosci. 2004 Jun;19(12):3151-64
pubmed: 15217371
Cell Rep. 2019 Mar 5;26(10):2805-2817.e9
pubmed: 30840899
Mol Cell Biol. 2011 Feb;31(3):388-403
pubmed: 21115725
Mol Cell Biol. 2015 Apr;35(8):1316-28
pubmed: 25645926
J Cell Biol. 2008 Jun 2;181(5):817-29
pubmed: 18519736
J Cell Sci. 2005 Feb 15;118(Pt 4):651-4
pubmed: 15701920
Nat Genet. 2012 Mar 18;44(4):379-80
pubmed: 22426309
J Neurosci. 2003 Nov 19;23(33):10593-603
pubmed: 14627644
Nucleic Acids Res. 2021 Jan 8;49(D1):D1207-D1217
pubmed: 33264411
Cell Motil Cytoskeleton. 1998;39(2):172-90
pubmed: 9484959
Mol Cell Neurosci. 1997 Jan;9(1):1-12
pubmed: 9204476
Cell Calcium. 2013 May-Jun;53(5-6):338-48
pubmed: 23578580
Cereb Cortex. 2000 Oct;10(10):927-38
pubmed: 11007543
J Hum Genet. 2018 Mar;63(3):387-390
pubmed: 29335451
Am J Hum Genet. 2011 Mar 11;88(3):306-16
pubmed: 21376300
Sci Rep. 2018 Jul 24;8(1):11138
pubmed: 30042445
J Neurosci. 2020 Mar 25;40(13):2776-2788
pubmed: 32098904
Cytoskeleton (Hoboken). 2016 Oct;73(10):596-611
pubmed: 27112918
Proc Natl Acad Sci U S A. 1996 May 28;93(11):5466-71
pubmed: 8643598
Sci Rep. 2019 Jul 5;9(1):9731
pubmed: 31278311
J Neurosci. 2012 Jul 4;32(27):9217-27
pubmed: 22764230
Nat Neurosci. 2007 Apr;10(4):411-3
pubmed: 17322876
Proc Natl Acad Sci U S A. 2000 Oct 24;97(22):12074-8
pubmed: 11050238
Neuromolecular Med. 2002;2(1):61-9
pubmed: 12230305
J Biol Chem. 1995 Nov 10;270(45):26897-903
pubmed: 7592934
Protein Cell. 2020 Dec 11;:
pubmed: 33306168
Neuron. 2005 Jul 7;47(1):85-100
pubmed: 15996550
J Biol Chem. 2013 Jul 19;288(29):21117-21125
pubmed: 23760270
Nat Rev Mol Cell Biol. 2008 Apr;9(4):309-22
pubmed: 18322465
Int J Mol Sci. 2017 Mar 18;18(3):
pubmed: 28335463
J Hum Genet. 2016 Apr;61(4):283-93
pubmed: 26657932
Front Cell Neurosci. 2018 Jun 14;12:165
pubmed: 29962938
Brain Struct Funct. 2018 Dec;223(9):4227-4241
pubmed: 30196430
Bioessays. 2004 Feb;26(2):141-50
pubmed: 14745832
Ann Clin Transl Neurol. 2015 Jun;2(6):623-35
pubmed: 26125038
Hum Mol Genet. 2016 Jun 1;25(11):2314-2323
pubmed: 27146843
Mol Biol Cell. 2017 Jan 1;28(1):1-8
pubmed: 28035040
J Neurosci. 2007 Nov 28;27(48):13117-29
pubmed: 18045906
Front Genet. 2018 Sep 18;9:349
pubmed: 30279698
Biol Chem. 2019 Aug 27;400(9):1129-1139
pubmed: 31280237
Genes Dev. 2005 Jan 1;19(1):1-49
pubmed: 15630019
Curr Biol. 2019 Nov 18;29(22):3874-3886.e9
pubmed: 31679934
Nature. 1994 Jan 6;367(6458):40-6
pubmed: 8107774
Mol Psychiatry. 2017 Nov;22(11):1576-1584
pubmed: 27400854
Trends Neurosci. 2013 Jan;36(1):3-13
pubmed: 23041052
Hum Mol Genet. 2009 Jan 1;18(1):105-17
pubmed: 18829665
Dev Neurobiol. 2009 Sep 1;69(10):633-46
pubmed: 19513995
FEBS Lett. 1996 Aug 26;392(2):189-93
pubmed: 8772201
J Biol Chem. 2002 Aug 23;277(34):30495-501
pubmed: 12063253
Eur J Hum Genet. 2018 Jan;26(1):64-74
pubmed: 29180823
Am J Hum Genet. 2016 Jan 7;98(1):149-64
pubmed: 26748517
J Cell Biol. 1997 Sep 22;138(6):1279-87
pubmed: 9298983
Biol Psychiatry. 2006 Dec 1;60(11):1224-30
pubmed: 16806091
Int J Dev Neurosci. 2012 Apr;30(2):147-58
pubmed: 22155002
Science. 2007 Feb 23;315(5815):1143-7
pubmed: 17289941
Nat Cell Biol. 1999 Sep;1(5):253-9
pubmed: 10559936
Singapore Med J. 2001 Jun;42(6):243-6
pubmed: 11547959
J Clin Invest. 2020 Apr 1;130(4):2024-2040
pubmed: 31945017
Neuron. 2016 Mar 16;89(6):1208-1222
pubmed: 26924435
Proc Natl Acad Sci U S A. 2000 Aug 1;97(16):9287-92
pubmed: 10922077
Neuron. 2001 Jul 19;31(1):115-30
pubmed: 11498055
Am J Physiol Cell Physiol. 2001 Jun;280(6):C1669-79
pubmed: 11350763
Brain. 2019 Nov 1;142(11):3351-3359
pubmed: 31504246
Eur J Hum Genet. 2015 Mar;23(3):416
pubmed: 25672248
J Biol Chem. 1995 Dec 29;270(52):31321-30
pubmed: 8537403
Int J Mol Sci. 2018 Jan 27;19(2):
pubmed: 29382077
J Neurosci. 2011 Jan 26;31(4):1528-38
pubmed: 21273437
Cold Spring Harb Mol Case Stud. 2016 Jan;2(1):a000661
pubmed: 27148580
PLoS One. 2013 Sep 11;8(9):e74924
pubmed: 24040362
Am J Med Genet A. 2013 Aug;161A(8):1897-903
pubmed: 23824974
J Neurosci. 2007 Apr 4;27(14):3884-93
pubmed: 17409253
Science. 2012 Dec 21;338(6114):1619-22
pubmed: 23160955
J Med Genet. 2006 Oct;43(10):822-8
pubmed: 16284256
Mol Psychiatry. 2017 Sep;22(9):1335-1344
pubmed: 28115743
J Cell Sci. 2006 Apr 15;119(Pt 8):1570-8
pubmed: 16569658
Mol Cytogenet. 2012 Jun 11;5(1):30
pubmed: 22686481
Neuron. 2020 Dec 9;108(5):887-904.e12
pubmed: 33027640
Nature. 2002 Jan 31;415(6871):526-30
pubmed: 11793011
Dev Neurobiol. 2009 Apr;69(5):279-98
pubmed: 19224562
Bioinformatics. 2010 May 15;26(10):1378-80
pubmed: 20378558
J Biol Chem. 2008 Nov 21;283(47):32542-52
pubmed: 18809681
J Biol Chem. 2012 Apr 13;287(16):13228-38
pubmed: 22383527
Glia. 2020 Sep;68(9):1729-1742
pubmed: 32073702
Biochemistry. 2007 Mar 20;46(11):3494-502
pubmed: 17302440
J Neurosci. 1994 Jan;14(1):384-98
pubmed: 8283245
Biochem Biophys Res Commun. 2012 Apr 6;420(2):247-52
pubmed: 22405825
Am J Med Genet A. 2015 Nov;167A(11):2822-5
pubmed: 26386261
J Neurosci. 2013 Apr 3;33(14):6081-92
pubmed: 23554489
J Biol Chem. 2001 Nov 2;276(44):40606-13
pubmed: 11514549
EMBO J. 1996 May 1;15(9):2208-16
pubmed: 8641286
Neuron. 2015 Feb 18;85(4):742-54
pubmed: 25695269
Genes Dev. 2007 Sep 15;21(18):2347-57
pubmed: 17875668
Front Mol Neurosci. 2018 Jul 06;11:223
pubmed: 30042656
Nat Neurosci. 2016 Sep;19(9):1194-6
pubmed: 27479843
J Neurosci. 2012 Mar 14;32(11):3601-11
pubmed: 22423084
J Neurosci. 2011 Mar 23;31(12):4555-68
pubmed: 21430156
J Neurochem. 2008 Apr;105(1):113-26
pubmed: 18005226
Neurobiol Dis. 2020 Mar;136:104709
pubmed: 31843706
J Neurosci. 1997 Nov 1;17(21):8178-86
pubmed: 9334393
Mol Cell Neurosci. 2018 Sep;91:122-130
pubmed: 30004015
J Neurosci. 2021 Feb 10;41(6):1191-1206
pubmed: 33328293
Am J Med Genet A. 2016 Apr;170A(4):852-5
pubmed: 26708094
PLoS One. 2012;7(8):e42422
pubmed: 22900020
J Neurosci. 2014 Jan 22;34(4):1542-53
pubmed: 24453341
Eur J Hum Genet. 2013 Mar;21(3):266-73
pubmed: 22872100
Cell. 2007 Mar 23;128(6):1077-88
pubmed: 17320160
J Biol Chem. 2000 Feb 4;275(5):3577-82
pubmed: 10652353
J Comp Neurol. 2001 Jan 15;429(3):388-402
pubmed: 11116227
Mol Biol Cell. 2008 Apr;19(4):1561-74
pubmed: 18256280
J Neurosci. 2006 Oct 25;26(43):10967-83
pubmed: 17065439
PLoS Genet. 2017 Jul 24;13(7):e1006905
pubmed: 28742085
J Neurosci. 2008 Nov 12;28(46):12120-4
pubmed: 19005076
J Neurosci. 2004 May 5;24(18):4421-31
pubmed: 15128856
Nat Cell Biol. 2006 Mar;8(3):215-26
pubmed: 16501565
Nat Med. 2015 Apr;21(4):318-26
pubmed: 25774849
Neural Regen Res. 2014 Jul 1;9(13):1261-4
pubmed: 25221576
Small GTPases. 2021 Mar;12(2):122-132
pubmed: 31451035
Nature. 2013 Nov 7;503(7474):72-7
pubmed: 24153177
J Neurosci. 2015 Jul 15;35(28):10154-67
pubmed: 26180192
J Physiol. 2012 Feb 15;590(4):763-76
pubmed: 22124149
Biochemistry. 1984 Dec 18;23(26):6631-41
pubmed: 6543322
Neurobiol Dis. 2017 Feb;98:137-148
pubmed: 27940202
J Neurosci. 2005 Jul 13;25(28):6641-50
pubmed: 16014725
Mol Cell Biol. 2001 Aug;21(15):5179-89
pubmed: 11438672
J Neurosci. 2016 Sep 14;36(37):9696-709
pubmed: 27629719
Nature. 2000 Mar 9;404(6774):151-8
pubmed: 10724160
J Biol Chem. 1999 Nov 19;274(47):33587-93
pubmed: 10559246
Neuron. 2012 May 24;74(4):691-705
pubmed: 22632727
Neurosci Lett. 2008 Mar 5;433(1):22-7
pubmed: 18226451
Mol Autism. 2013 Jun 11;4(1):18
pubmed: 23758760
Proc Natl Acad Sci U S A. 2017 Aug 15;114(33):E6952-E6961
pubmed: 28760966
J Cell Sci. 2011 Aug 15;124(Pt 16):2786-96
pubmed: 21807943
Cells. 2020 May 29;9(6):
pubmed: 32486060
Int J Mol Sci. 2017 Jul 26;18(8):
pubmed: 28933765
Genes Brain Behav. 2012 Apr;11(3):325-31
pubmed: 22257369
Cereb Cortex. 2009 Apr;19(4):861-75
pubmed: 18701438
J Cell Sci. 2017 Aug 1;130(15):2506-2519
pubmed: 28606990
Neuron. 2018 Oct 24;100(2):276-293
pubmed: 30359597
Neurosci Biobehav Rev. 2014 Oct;46 Pt 2:161-74
pubmed: 24709068
Am J Hum Genet. 2004 Jul;75(1):97-105
pubmed: 15154114
Cell. 2018 Jun 28;174(1):59-71.e14
pubmed: 29804835
J Biol Chem. 2010 Aug 6;285(32):24834-44
pubmed: 20516067