The epilepsy and intellectual disability-associated protein TBC1D24 regulates the maintenance of excitatory synapses and animal behaviors
Autoři:
Lianfeng Lin aff001; Quanwei Lyu aff001; Pui-Yi Kwan aff001; Junjun Zhao aff001; Ruolin Fan aff001; Anping Chai aff001; Cora Sau Wan Lai aff001; Ying-Shing Chan aff001; Xuting Shen aff001; Kwok-On Lai aff001
Působiště autorů:
School of Biomedical Sciences, The University of Hong Kong, Hong Kong, China
aff001; State Key Laboratory of Brain and Cognitive Sciences, The University of Hong Kong, Hong Kong, China
aff002
Vyšlo v časopise:
The epilepsy and intellectual disability-associated protein TBC1D24 regulates the maintenance of excitatory synapses and animal behaviors. PLoS Genet 16(1): e32767. doi:10.1371/journal.pgen.1008587
Kategorie:
Research Article
doi:
https://doi.org/10.1371/journal.pgen.1008587
Souhrn
Perturbation of synapse development underlies many inherited neurodevelopmental disorders including intellectual disability (ID). Diverse mutations on the human TBC1D24 gene are strongly associated with epilepsy and ID. However, the physiological function of TBC1D24 in the brain is not well understood, and there is a lack of genetic mouse model that mimics TBC1D24 loss-of-function for the study of animal behaviors. Here we report that TBC1D24 is present at the postsynaptic sites of excitatory synapses, where it is required for the maintenance of dendritic spines through inhibition of the small GTPase ARF6. Mice subjected to viral-mediated knockdown of TBC1D24 in the adult hippocampus display dendritic spine loss, deficits in contextual fear memory, as well as abnormal behaviors including hyperactivity and increased anxiety. Interestingly, we show that the protein stability of TBC1D24 is diminished by the disease-associated missense mutation that leads to F251L amino acid substitution. We further generate the F251L knock-in mice, and the homozygous mutants show increased neuronal excitability, spontaneous seizure and pre-mature death. Moreover, the heterozygous F251L knock-in mice survive into adulthood but display dendritic spine defects and impaired memory. Our findings therefore uncover a previously uncharacterized postsynaptic function of TBC1D24, and suggest that impaired dendritic spine maintenance contributes to the pathophysiology of individuals harboring TBC1D24 gene mutations. The F251L knock-in mice represent a useful animal model for investigation of the mechanistic link between TBC1D24 loss-of-function and neurodevelopmental disorders.
Klíčová slova:
Animal behavior – Hippocampus – Mice – Mouse models – Neuronal dendrites – Neurons – Synapses – Transfection
Zdroje
1. Gatto CL, Broadie K. Genetic controls balancing excitatory and inhibitory synaptogenesis in neurodevelopmental disorder models. Front Synaptic Neurosci. 2010;2:4. doi: 10.3389/fnsyn.2010.00004 21423490.
2. Grant SG. Synaptopathies: diseases of the synaptome. Curr Opin Neurobiol. 2012;22(3):522–529. doi: 10.1016/j.conb.2012.02.002 22409856.
3. Volk L, Chiu SL, Sharma K, Huganir RL. Glutamate synapses in human cognitive disorders. Annu Rev Neurosci. 2015;38:127–149. doi: 10.1146/annurev-neuro-071714-033821 25897873.
4. Bourne JN, Harris KM. Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci. 2008;31:47–67. doi: 10.1146/annurev.neuro.31.060407.125646 18284372.
5. Bayes A, van de Lagemaat LN, Collins MO, Croning MD, Whittle IR, Choudhary JS, et al. Characterization of the proteome, diseases and evolution of the human postsynaptic density. Nat Neurosci. 2011;14(1):19–21. doi: 10.1038/nn.2719 21170055.
6. Cingolani LA, Goda Y. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci. 2008;9(5):344–356. doi: 10.1038/nrn2373 18425089.
7. Lai KO, Ip NY. Structural plasticity of dendritic spines: the underlying mechanisms and its dysregulation in brain disorders. Biochim Biophys Acta. 2013;1832(12):2257–2263. doi: 10.1016/j.bbadis.2013.08.012 24012719.
8. Sheng M, Kim E. The postsynaptic organization of synapses. Cold Spring Harb Perspect Biol. 2011;3(12). doi: 10.1101/cshperspect.a005678 22046028.
9. Pavlowsky A, Chelly J, Billuart P. Emerging major synaptic signaling pathways involved in intellectual disability. Mol Psychiatry. 2012;17(7):682–693. doi: 10.1038/mp.2011.139 22024764.
10. Molosh AI, Johnson PL, Spence JP, Arendt D, Federici LM, Bernabe C, et al. Social learning and amygdala disruptions in Nf1 mice are rescued by blocking p21-activated kinase. Nat Neurosci. 2014;17(11):1583–1590. doi: 10.1038/nn.3822 25242307.
11. Balestrini S, Milh M, Castiglioni C, Luthy K, Finelli MJ, Verstreken P, et al. TBC1D24 genotype-phenotype correlation: Epilepsies and other neurologic features. Neurology. 2016;87(1):77–85. doi: 10.1212/WNL.0000000000002807 27281533.
12. Frasa MA, Koessmeier KT, Ahmadian MR, Braga VM. Illuminating the functional and structural repertoire of human TBC/RABGAPs. Nat Rev Mol Cell Biol. 2012;13(2):67–73. doi: 10.1038/nrm3267 22251903.
13. Falace A, Filipello F, La Padula V, Vanni N, Madia F, De Pietri Tonelli D, et al. TBC1D24, an ARF6-interacting protein, is mutated in familial infantile myoclonic epilepsy. Am J Hum Genet. 2010;87(3):365–370. doi: 10.1016/j.ajhg.2010.07.020 20727515.
14. Donaldson JG. Multiple roles for Arf6: sorting, structuring, and signaling at the plasma membrane. J Biol Chem. 2003;278(43):41573–41576. doi: 10.1074/jbc.R300026200 12912991.
15. Fernandes AC, Uytterhoeven V, Kuenen S, Wang YC, Slabbaert JR, Swerts J, et al. Reduced synaptic vesicle protein degradation at lysosomes curbs TBC1D24/sky-induced neurodegeneration. J Cell Biol. 2014;207(4):453–462. doi: 10.1083/jcb.201406026 25422373.
16. Uytterhoeven V, Kuenen S, Kasprowicz J, Miskiewicz K, Verstreken P. Loss of skywalker reveals synaptic endosomes as sorting stations for synaptic vesicle proteins. Cell. 2011;145(1):117–132. doi: 10.1016/j.cell.2011.02.039 21458671.
17. Falace A, Buhler E, Fadda M, Watrin F, Lippiello P, Pallesi-Pocachard E, et al. TBC1D24 regulates neuronal migration and maturation through modulation of the ARF6-dependent pathway. Proc Natl Acad Sci U S A. 2014;111(6):2337–2342. doi: 10.1073/pnas.1316294111 24469796.
18. Tagliatti E, Fadda M, Falace A, Benfenati F, Fassio A. Arf6 regulates the cycling and the readily releasable pool of synaptic vesicles at hippocampal synapse. Elife. 2016;5. doi: 10.7554/eLife.10116 26731518.
19. Choi S, Ko J, Lee JR, Lee HW, Kim K, Chung HS, et al. ARF6 and EFA6A regulate the development and maintenance of dendritic spines. J Neurosci. 2006;26(18):4811–4819. doi: 10.1523/JNEUROSCI.4182-05.2006 16672654.
20. Kim Y, Lee SE, Park J, Kim M, Lee B, Hwang D, et al. ADP-ribosylation factor 6 (ARF6) bidirectionally regulates dendritic spine formation depending on neuronal maturation and activity. J Biol Chem. 2015;290(12):7323–7335. doi: 10.1074/jbc.M114.634527 25605715.
21. Myers KR, Wang G, Sheng Y, Conger KK, Casanova JE, Zhu JJ. Arf6-GEF BRAG1 regulates JNK-mediated synaptic removal of GluA1-containing AMPA receptors: a new mechanism for nonsyndromic X-linked mental disorder. J Neurosci. 2012;32(34):11716–11726. doi: 10.1523/JNEUROSCI.1942-12.2012 22915114.
22. Oku Y, Huganir RL. AGAP3 and Arf6 regulate trafficking of AMPA receptors and synaptic plasticity. J Neurosci. 2013;33(31):12586–12598. doi: 10.1523/JNEUROSCI.0341-13.2013 23904596.
23. Raemaekers T, Peric A, Baatsen P, Sannerud R, Declerck I, Baert V, et al. ARF6-mediated endosomal transport of Telencephalin affects dendritic filopodia-to-spine maturation. Embo j. 2012;31(15):3252–3269. doi: 10.1038/emboj.2012.182 22781129.
24. Scholz R, Berberich S, Rathgeber L, Kolleker A, Kohr G, Kornau HC. AMPA receptor signaling through BRAG2 and Arf6 critical for long-term synaptic depression. Neuron. 2010;66(5):768–780. doi: 10.1016/j.neuron.2010.05.003 20547133.
25. Fernandez E, Collins MO, Frank RAW, Zhu F, Kopanitsa MV, Nithianantharajah J, et al. Arc Requires PSD95 for Assembly into Postsynaptic Complexes Involved with Neural Dysfunction and Intelligence. Cell Rep. 2017;21(3):679–691. doi: 10.1016/j.celrep.2017.09.045 29045836.
26. Peebles CL, Yoo J, Thwin MT, Palop JJ, Noebels JL, Finkbeiner S. Arc regulates spine morphology and maintains network stability in vivo. Proc Natl Acad Sci U S A. 2010;107(42):18173–18178. doi: 10.1073/pnas.1006546107 20921410.
27. Afawi Z, Mandelstam S, Korczyn AD, Kivity S, Walid S, Shalata A, et al. TBC1D24 mutation associated with focal epilepsy, cognitive impairment and a distinctive cerebro-cerebellar malformation. Epilepsy Res. 2013;105(1–2):240–244. doi: 10.1016/j.eplepsyres.2013.02.005 23517570.
28. Corbett MA, Bahlo M, Jolly L, Afawi Z, Gardner AE, Oliver KL, et al. A focal epilepsy and intellectual disability syndrome is due to a mutation in TBC1D24. Am J Hum Genet. 2010;87(3):371–375. doi: 10.1016/j.ajhg.2010.08.001 20797691.
29. Holt CE, Schuman EM. The central dogma decentralized: new perspectives on RNA function and local translation in neurons. Neuron. 2013;80(3):648–657. doi: 10.1016/j.neuron.2013.10.036 24183017.
30. Rao A, Steward O. Evidence that protein constituents of postsynaptic membrane specializations are locally synthesized: analysis of proteins synthesized within synaptosomes. J Neurosci. 1991;11(9):2881–2895. doi: 10.1523/JNEUROSCI.11-09-02881.1991 1880554.
31. Lin L, Lo LH, Lyu Q, Lai KO. Determination of dendritic spine morphology by the striatin scaffold protein STRN4 through interaction with the phosphatase PP2A. J Biol Chem. 2017;292(23):9451–9464. doi: 10.1074/jbc.M116.772442 28442576.
32. Gross GG, Junge JA, Mora RJ, Kwon HB, Olson CA, Takahashi TT, et al. Recombinant probes for visualizing endogenous synaptic proteins in living neurons. Neuron. 2013;78(6):971–985. doi: 10.1016/j.neuron.2013.04.017 23791193.
33. Benson DL, Watkins FH, Steward O, Banker G. Characterization of GABAergic neurons in hippocampal cell cultures. J Neurocytol. 1994;23(5):279–295. doi: 10.1007/bf01188497 8089704.
34. Woodson W, Nitecka L, Ben-Ari Y. Organization of the GABAergic system in the rat hippocampal formation: a quantitative immunocytochemical study. J Comp Neurol. 1989;280(2):254–271. doi: 10.1002/cne.902800207 2925894.
35. Aprile D, Fruscione F, Baldassari S, Fadda M, Ferrante D, Falace A, et al. TBC1D24 regulates axonal outgrowth and membrane trafficking at the growth cone in rodent and human neurons. Cell Death Differ. 2019. doi: 10.1038/s41418-019-0313-x 30858606.
36. Peters PJ, Hsu VW, Ooi CE, Finazzi D, Teal SB, Oorschot V, et al. Overexpression of wild-type and mutant ARF1 and ARF6: distinct perturbations of nonoverlapping membrane compartments. J Cell Biol. 1995;128(6):1003–1017. doi: 10.1083/jcb.128.6.1003 7896867.
37. Santy LC. Characterization of a fast cycling ADP-ribosylation factor 6 mutant. J Biol Chem. 2002;277(43):40185–40188. doi: 10.1074/jbc.C200481200 12218044.
38. Hafner M, Schmitz A, Grune I, Srivatsan SG, Paul B, Kolanus W, et al. Inhibition of cytohesins by SecinH3 leads to hepatic insulin resistance. Nature. 2006;444(7121):941–944. doi: 10.1038/nature05415 17167487.
39. Fazzari P, Snellinx A, Sabanov V, Ahmed T, Serneels L, Gartner A, et al. Cell autonomous regulation of hippocampal circuitry via Aph1b-gamma-secretase/neuregulin 1 signalling. Elife. 2014;3. doi: 10.7554/eLife.02196 24891237.
40. Kim KM, Zamaleeva AI, Lee YW, Ahmed MR, Kim E, Lee HR, et al. Characterization of Brain Dysfunction Induced by Bacterial Lipopeptides That Alter Neuronal Activity and Network in Rodent Brains. J Neurosci. 2018;38(50):10672–10691. doi: 10.1523/JNEUROSCI.0825-17.2018 30381406.
41. Khelfaoui M, Denis C, van Galen E, de Bock F, Schmitt A, Houbron C, et al. Loss of X-linked mental retardation gene oligophrenin1 in mice impairs spatial memory and leads to ventricular enlargement and dendritic spine immaturity. J Neurosci. 2007;27(35):9439–9450. doi: 10.1523/JNEUROSCI.2029-07.2007 17728457.
42. Liang Z, Zhan Y, Shen Y, Wong CC, Yates JR 3rd, Plattner F, et al. The pseudokinase CaMKv is required for the activity-dependent maintenance of dendritic spines. Nat Commun. 2016;7:13282. doi: 10.1038/ncomms13282 27796283.
43. Martinez-Tellez RI, Hernandez-Torres E, Gamboa C, Flores G. Prenatal stress alters spine density and dendritic length of nucleus accumbens and hippocampus neurons in rat offspring. Synapse. 2009;63(9):794–804. doi: 10.1002/syn.20664 19489049.
44. Campeau PM, Kasperaviciute D, Lu JT, Burrage LC, Kim C, Hori M, et al. The genetic basis of DOORS syndrome: an exome-sequencing study. Lancet Neurol. 2014;13(1):44–58. doi: 10.1016/S1474-4422(13)70265-5 24291220.
45. Poulat AL, Ville D, de Bellescize J, Andre-Obadia N, Cacciagli P, Milh M, et al. Homozygous TBC1D24 mutation in two siblings with familial infantile myoclonic epilepsy (FIME) and moderate intellectual disability. Epilepsy Res. 2015;111:72–77. doi: 10.1016/j.eplepsyres.2015.01.008 25769375.
46. Asinof S, Mahaffey C, Beyer B, Frankel WN, Boumil R. Dynamin 1 isoform roles in a mouse model of severe childhood epileptic encephalopathy. Neurobiol Dis. 2016;95:1–11. doi: 10.1016/j.nbd.2016.06.014 27363778.
47. Liu K, Lei R, Li Q, Wang XX, Wu Q, An P, et al. Transferrin Receptor Controls AMPA Receptor Trafficking Efficiency and Synaptic Plasticity. Sci Rep. 2016;6:21019. doi: 10.1038/srep21019 26880306.
48. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H. Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci. 2001;4(11):1086–1092. doi: 10.1038/nn736 11687814.
49. Ultanir SK, Kim JE, Hall BJ, Deerinck T, Ellisman M, Ghosh A. Regulation of spine morphology and spine density by NMDA receptor signaling in vivo. Proc Natl Acad Sci U S A. 2007;104(49):19553–19558. doi: 10.1073/pnas.0704031104 18048342.
50. Wang L, Pang K, Han K, Adamski CJ, Wang W, He L, et al. An autism-linked missense mutation in SHANK3 reveals the modularity of Shank3 function. Mol Psychiatry. 2019. doi: 10.1038/s41380-018-0324-x 30610205.
51. Zhang C, Milunsky JM, Newton S, Ko J, Zhao G, Maher TA, et al. A neuroligin-4 missense mutation associated with autism impairs neuroligin-4 folding and endoplasmic reticulum export. J Neurosci. 2009;29(35):10843–10854. doi: 10.1523/JNEUROSCI.1248-09.2009 19726642.
52. Clement JP, Aceti M, Creson TK, Ozkan ED, Shi Y, Reish NJ, et al. Pathogenic SYNGAP1 mutations impair cognitive development by disrupting maturation of dendritic spine synapses. Cell. 2012;151(4):709–723. doi: 10.1016/j.cell.2012.08.045 23141534.
53. Vazquez LE, Chen HJ, Sokolova I, Knuesel I, Kennedy MB. SynGAP regulates spine formation. J Neurosci. 2004;24(40):8862–8872. doi: 10.1523/JNEUROSCI.3213-04.2004 15470153.
54. Mignot C, von Stulpnagel C, Nava C, Ville D, Sanlaville D, Lesca G, et al. Genetic and neurodevelopmental spectrum of SYNGAP1-associated intellectual disability and epilepsy. J Med Genet. 2016;53(8):511–522. doi: 10.1136/jmedgenet-2015-103451 26989088.
55. Bosch C, Masachs N, Exposito-Alonso D, Martinez A, Teixeira CM, Fernaud I, et al. Reelin Regulates the Maturation of Dendritic Spines, Synaptogenesis and Glial Ensheathment of Newborn Granule Cells. Cereb Cortex. 2016;26(11):4282–4298. doi: 10.1093/cercor/bhw216 27624722.
56. Cerikan B, Shaheen R, Colo GP, Glasser C, Hata S, Knobeloch KP, et al. Cell-Intrinsic Adaptation Arising from Chronic Ablation of a Key Rho GTPase Regulator. Dev Cell. 2016;39(1):28–43. doi: 10.1016/j.devcel.2016.08.020 27693507.
57. El-Brolosy MA, Stainier DYR. Genetic compensation: A phenomenon in search of mechanisms. PLoS Genet. 2017;13(7):e1006780. doi: 10.1371/journal.pgen.1006780 28704371.
58. Rossi A, Kontarakis Z, Gerri C, Nolte H, Holper S, Kruger M, et al. Genetic compensation induced by deleterious mutations but not gene knockdowns. Nature. 2015;524(7564):230–233. doi: 10.1038/nature14580 26168398.
59. Jones KA, Sumiya M, Woolfrey KM, Srivastava DP, Penzes P. Loss of EPAC2 alters dendritic spine morphology and inhibitory synapse density. Mol Cell Neurosci. 2019;98:19–31. doi: 10.1016/j.mcn.2019.05.001 31059774.
60. Srivastava DP, Woolfrey KM, Jones KA, Anderson CT, Smith KR, Russell TA, et al. An autism-associated variant of Epac2 reveals a role for Ras/Epac2 signaling in controlling basal dendrite maintenance in mice. PLoS Biol. 2012;10(6):e1001350. doi: 10.1371/journal.pbio.1001350 22745599.
61. Finelli MJ, Aprile D, Castroflorio E, Jeans A, Moschetta M, Chessum L, et al. The epilepsy-associated protein TBC1D24 is required for normal development, survival and vesicle trafficking in mammalian neurons. Hum Mol Genet. 2019;28(4):584–597. doi: 10.1093/hmg/ddy370 30335140.
62. Li YS, Qin LX, Liu J, Xia WL, Li JP, Shen HL, et al. GIT1 enhances neurite outgrowth by stimulating microtubule assembly. Neural Regen Res. 2016;11(3):427–434. doi: 10.4103/1673-5374.179054 27127481.
63. Moore CD, Thacker EE, Larimore J, Gaston D, Underwood A, Kearns B, et al. The neuronal Arf GAP centaurin alpha1 modulates dendritic differentiation. J Cell Sci. 2007;120(Pt 15):2683–2693. doi: 10.1242/jcs.006346 17635995.
64. Fischer B, Luthy K, Paesmans J, De Koninck C, Maes I, Swerts J, et al. Skywalker-TBC1D24 has a lipid-binding pocket mutated in epilepsy and required for synaptic function. Nat Struct Mol Biol. 2016;23(11):965–973. doi: 10.1038/nsmb.3297 27669036.
65. Frere SG, Chang-Ileto B, Di Paolo G. Role of phosphoinositides at the neuronal synapse. Subcell Biochem. 2012;59:131–175. doi: 10.1007/978-94-007-3015-1_5 22374090.
66. Horne EA, Dell’Acqua ML. Phospholipase C is required for changes in postsynaptic structure and function associated with NMDA receptor-dependent long-term depression. J Neurosci. 2007;27(13):3523–3534. doi: 10.1523/JNEUROSCI.4340-06.2007 17392468.
67. Vicidomini C, Ponzoni L, Lim D, Schmeisser MJ, Reim D, Morello N, et al. Pharmacological enhancement of mGlu5 receptors rescues behavioral deficits in SHANK3 knock-out mice. Mol Psychiatry. 2017;22(5):784. doi: 10.1038/mp.2016.70 27113996.
68. Bhattacharya S, Herrera-Molina R, Sabanov V, Ahmed T, Iscru E, Stober F, et al. Genetically Induced Retrograde Amnesia of Associative Memories After Neuroplastin Ablation. Biol Psychiatry. 2017;81(2):124–135. doi: 10.1016/j.biopsych.2016.03.2107 27215477.
69. Tchantchou F, Puche AA, Leiste U, Fourney W, Blanpied TA, Fiskum G. Rat Model of Brain Injury to Occupants of Vehicles Targeted by Land Mines: Mitigation by Elastomeric Frame Designs. J Neurotrauma. 2018;35(10):1192–1203. doi: 10.1089/neu.2017.5401 29187028.
70. Giralt A, Brito V, Chevy Q, Simonnet C, Otsu Y, Cifuentes-Diaz C, et al. Pyk2 modulates hippocampal excitatory synapses and contributes to cognitive deficits in a Huntington’s disease model. Nat Commun. 2017;8:15592. doi: 10.1038/ncomms15592 28555636.
71. Bellizzi MJ, Hammond JW, Li H, Gantz Marker MA, Marker DF, Freeman RS, et al. The Mixed-Lineage Kinase Inhibitor URMC-099 Protects Hippocampal Synapses in Experimental Autoimmune Encephalomyelitis. eNeuro. 2018;5(6). doi: 10.1523/ENEURO.0245-18.2018 30627663.
72. Simonetti M, Paldy E, Njoo C, Bali KK, Worzfeld T, Pitzer C, et al. The impact of Semaphorin 4C/Plexin-B2 signaling on fear memory via remodeling of neuronal and synaptic morphology. Mol Psychiatry. 2019. doi: 10.1038/s41380-019-0491-4 31444474.
73. Hammond JW, Bellizzi MJ, Ware C, Qiu WQ, Saminathan P, Li H, Luo S, Li Y, Gelbard HA. Complement-dependent synapse loss and microgliosis in a mouse model of multiple sclerosis. bioRxiv 720649. https://doi.org/10.1101/720649.
74. Shiraishi Y, Mizutani A, Mikoshiba K, Furuichi T. Coincidence in dendritic clustering and synaptic targeting of homer proteins and NMDA receptor complex proteins NR2B and PSD95 during development of cultured hippocampal neurons. Mol Cell Neurosci. 2003;22(2):188–201. doi: 10.1016/s1044-7431(03)00037-x 12676529.
75. Niu Y, Dai Z, Liu W, Zhang C, Yang Y, Guo Z, et al. Ablation of SNX6 leads to defects in synaptic function of CA1 pyramidal neurons and spatial memory. Elife. 2017;6. doi: 10.7554/eLife.20991 28134614.
76. Sala C, Piech V, Wilson NR, Passafaro M, Liu G, Sheng M. Regulation of dendritic spine morphology and synaptic function by Shank and Homer. Neuron. 2001;31(1):115–130. doi: 10.1016/s0896-6273(01)00339-7 11498055.
77. Hayashi MK, Tang C, Verpelli C, Narayanan R, Stearns MH, Xu RM, et al. The postsynaptic density proteins Homer and Shank form a polymeric network structure. Cell. 2009;137(1):159–171. doi: 10.1016/j.cell.2009.01.050 19345194.
78. Roselli F, Hutzler P, Wegerich Y, Livrea P, Almeida OF. Disassembly of shank and homer synaptic clusters is driven by soluble beta-amyloid(1–40) through divergent NMDAR-dependent signalling pathways. PLoS One. 2009;4(6):e6011. doi: 10.1371/journal.pone.0006011 19547699.
79. Lu J, Helton TD, Blanpied TA, Racz B, Newpher TM, Weinberg RJ, et al. Postsynaptic positioning of endocytic zones and AMPA receptor cycling by physical coupling of dynamin-3 to Homer. Neuron. 2007;55(6):874–889. doi: 10.1016/j.neuron.2007.06.041 17880892.
80. Elagabani MN, Brisevac D, Kintscher M, Pohle J, Kohr G, Schmitz D, et al. Subunit-selective N-Methyl-d-aspartate (NMDA) Receptor Signaling through Brefeldin A-resistant Arf Guanine Nucleotide Exchange Factors BRAG1 and BRAG2 during Synapse Maturation. J Biol Chem. 2016;291(17):9105–9118. doi: 10.1074/jbc.M115.691717 26884337.
81. Hernandez-Deviez DJ, Casanova JE, Wilson JM. Regulation of dendritic development by the ARF exchange factor ARNO. Nat Neurosci. 2002;5(7):623–624. doi: 10.1038/nn865 12032543.
82. Ito A, Fukaya M, Saegusa S, Kobayashi E, Sugawara T, Hara Y, et al. Pallidin is a novel interacting protein for cytohesin-2 and regulates the early endosomal pathway and dendritic formation in neurons. J Neurochem. 2018;147(2):153–177. doi: 10.1111/jnc.14579 30151872.
83. Frittoli E, Palamidessi A, Pizzigoni A, Lanzetti L, Garre M, Troglio F, et al. The primate-specific protein TBC1D3 is required for optimal macropinocytosis in a novel ARF6-dependent pathway. Mol Biol Cell. 2008;19(4):1304–1316. doi: 10.1091/mbc.E07-06-0594 18199687.
84. Martinu L, Masuda-Robens JM, Robertson SE, Santy LC, Casanova JE, Chou MM. The TBC (Tre-2/Bub2/Cdc16) domain protein TRE17 regulates plasma membrane-endosomal trafficking through activation of Arf6. Mol Cell Biol. 2004;24(22):9752–9762. doi: 10.1128/MCB.24.22.9752-9762.2004 15509780.
85. Itoh T, Satoh M, Kanno E, Fukuda M. Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes Cells. 2006;11(9):1023–1037. doi: 10.1111/j.1365-2443.2006.00997.x 16923123.
86. Haas AK, Fuchs E, Kopajtich R, Barr FA. A GTPase-activating protein controls Rab5 function in endocytic trafficking. Nat Cell Biol. 2005;7(9):887–893. doi: 10.1038/ncb1290 16086013.
87. Guven A, Tolun A. TBC1D24 truncating mutation resulting in severe neurodegeneration. J Med Genet. 2013;50(3):199–202. doi: 10.1136/jmedgenet-2012-101313 23343562.
88. Tona R, Chen W, Nakano Y, Reyes LD, Petralia RS, Wang YX, et al. The phenotypic landscape of a Tbc1d24 mutant mouse includes convulsive seizures resembling human early infantile epileptic encephalopathy. Hum Mol Genet. 2019;28(9):1530–1547. doi: 10.1093/hmg/ddy445 30602030.
89. Mucha BE, Banka S, Ajeawung NF, Molidperee S, Chen GG, Koenig MK, et al. A new microdeletion syndrome involving TBC1D24, ATP6V0C, and PDPK1 causes epilepsy, microcephaly, and developmental delay. Genet Med. 2019;21(5):1058–1064. doi: 10.1038/s41436-018-0290-3 30245510.
90. Lai KO, Wong AS, Cheung MC, Xu P, Liang Z, Lok KC, et al. TrkB phosphorylation by Cdk5 is required for activity-dependent structural plasticity and spatial memory. Nat Neurosci. 2012;15(11):1506–1515. doi: 10.1038/nn.3237 23064382.
91. Bermejo MK, Milenkovic M, Salahpour A, Ramsey AJ. Preparation of synaptic plasma membrane and postsynaptic density proteins using a discontinuous sucrose gradient. J Vis Exp. 2014;(91):e51896. doi: 10.3791/51896 25226023.
92. Lu HC, Mills AA, Tian D. Altered synaptic transmission and maturation of hippocampal CA1 neurons in a mouse model of human chr16p11.2 microdeletion. J Neurophysiol. 2018;119(3):1005–1018. doi: 10.1152/jn.00306.2017 29212915.
93. Manders EMM, Verbeek FJ, Aten JA. Measurement of co-localization of objects in dual-colour confocal images. J Microsc 1993;169(3):375–382. doi: 10.1111/j.1365-2818.1993.tb03313.x
94. Racine RJ. Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol. 1972;32(3):281–294. doi: 10.1016/0013-4694(72)90177-0 4110397.
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