Actin out: Regulation of the synaptic cytoskeleton

Journal of Biological Chemistry

Volumn 290, Issue 48, 2015, Pages 28613-28622

  Spence, Erin F ^a   Soderling, Scott H ^a  

^a DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BIOCHEMISTRY; BIOLOGY;

ACTIN FILAMENT; CYTOSKELETAL; CYTOSKELETONS; DENDRITIC SPINE; DIFFERENT STRUCTURE; MULTIPLE MUTATIONS; PSYCHIATRIC DISORDERS; SYNAPTIC TRANSMISSION;

PROTEINS;

ACTIN; ALPHA CATENIN; BETA CATENIN; CADHERIN; CARRIER PROTEINS AND BINDING PROTEINS; CATENIN; COFILIN; NERVE CELL ADHESION MOLECULE; OLIGOPHRENIN 1; PROTEIN INTERACTING WITH PROTEIN KINASE C; PROTEIN WASH; RETROMER PROTEIN; UNCLASSIFIED DRUG;

ACTIN FILAMENT; ACTIN POLYMERIZATION; CELL ADHESION; DENDRITIC SPINE; HUMAN; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN TRANSPORT; REVIEW; SYNAPSE; ANIMAL; METABOLISM; PATHOLOGY; SPINE; SPINE DISEASE; STRESS FIBER;

ACTINS; ANIMALS; HUMANS; SPINAL DISEASES; SPINE; STRESS FIBERS; SYNAPSES;

EID: 84948467107     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.R115.655118     Document Type: Review

References (100)

1. Yuste, R. (2013) Electrical compartmentalization in dendritic spines. Annu. Rev. Neurosci. 36, 429-449
2. Frost, N. A., Shroff, H., Kong, H., Betzig, E., and Blanpied, T. A. (2010) Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 67, 86-99
3. Holtmaat, A., and Svoboda, K. (2009) Experience-dependent structural synaptic plasticity in the mammalian brain. Nat. Rev. Neurosci. 10, 647-658
4. van Spronsen, M., and Hoogenraad, C. C. (2010) Synapse pathology in psychiatric and neurologic disease. Curr. Neurol. Neurosci. Rep. 10, 207-214
5. Fromer, M., and Pocklington., A. J., Kavanagh, D. H., Williams, H. J., Dwyer, S., Gormley, P., Georgieva, L., Rees, E., Palta, P., and Ruderfer., D. M., Carrera, N., Humphreys, I., Johnson, J. S., Roussos, P., Barker, D. D., Banks, E., Milanova, V., Grant, S. G., Hannon, E., Rose, S. A., Chambert, K., Mahajan, M., Scolnick, E. M., Moran, J. L., Kirov, G., Palotie, A., McCarroll, S. A., Holmans, P., Sklar, P., Owen, M. J., Purcell, S. M., and O'Donovan, M. C. (2014) De novo mutations in schizophrenia implicate synaptic networks. Nature 506, 179-184
6. Korobova, F., and Svitkina, T. (2010) Molecular architecture of synaptic actin cytoskeleton in hippocampal neurons reveals a mechanism of dendritic spine morphogenesis. Mol. Biol. Cell 21, 165-176
7. Tolias, K. F., and Duman., J. G., and Um, K. (2011) Control of synapse development and plasticity by Rho GTPase regulatory proteins. Prog. Neurobiol. 94, 133-148
8. Russell, T. A., and Blizinsky., K. D., Cobia, D. J., Cahill, M. E., Xie, Z., Sweet, R. A., Duan, J., Gejman, P. V., Wang, L., Csernansky, J. G., and Penzes, P. (2014) A sequence variant in human KALRN impairs protein function and coincides with reduced cortical thickness. Nat. Commun. 5, 4858
9. Carlson, B. R., and Lloyd., K. E., Kruszewski, A., Kim, I. H., Rodriguiz, R. M., Heindel, C., Faytell, M., and Dudek., S. M., Wetsel, W. C., and Soderling, S. H. (2011) WRP/srGAP3 facilitates the initiation of spine development by an inverse F-BAR domain, and its loss impairs long-term memory. J. Neurosci. 31, 2447-2460
10. Endris, V., Wogatzky, B., Leimer, U., Bartsch, D., Zatyka, M., Latif, F., Maher, E. R., Tariverdian, G., Kirsch, S., Karch, D., and Rappold, G. A. (2002) The novel Rho-GTPase activating gene MEGAP /srGAP3 has a putative role in severe mental retardation. Proc. Natl. Acad. Sci. U.S.A. 99, 11754-11759
11. Bugyi, B., and Carlier, M. F. (2010) Control of actin filament treadmilling in cell motility. Annu. Rev. Biophys. 39, 449-470
12. Rotty, J. D., Wu, C., and Bear, J.E. (2013) New insights into the regulation and cellular functions of the ARP2/3 complex. Nat. Rev. Mol. Cell Biol. 14, 7-12
13. Kim, Y., and Sung., J. Y., Ceglia, I., Lee, K. W., Ahn, J. H., Halford, J. M., Kim, A. M., Kwak, S. P., Park, J. B., Ho Ryu, S., Schenck, A., Bardoni, B., Scott, J. D., Nairn, A. C., and Greengard, P. (2006) Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442, 814-817
14. Soderling, S. H., and Guire., E. S., Kaech, S., White, J., Zhang, F., Schutz, K., Langeberg, L. K., Banker, G., Raber, J., and Scott, J. D. (2007) A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J. Neurosci. 27, 355-365
15. Kim, I. H., Racz, B., Wang, H., Burianek, L., Weinberg, R., Yasuda, R., Wetsel, W. C., and Soderling, S.H. (2013) Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J. Neurosci. 33, 6081-6092
16. Kim, I. H., Rossi, M.A., Aryal, D. K., Racz, B., Kim, N., Uezu, A., Wang, F., Wetsel, W. C., Weinberg, R. J., Yin, H., and Soderling, S. H. (2015) Spine pruning drives antipsychotic-sensitive locomotion via circuit control of striatal dopamine. Nat. Neurosci. 18, 883-891
17. Harris, E. S., and Higgs, H. N. (2004) Actin cytoskeleton: formins lead the way. Curr. Biol. 14, R520-R522
18. Chazeau, A., Mehidi, A., Nair, D., Gautier, J. J., Leduc, C., Chamma, I., Kage, F., Kechkar, A., Thoumine, O., Rottner, K., Choquet, D., Gautreau, A., Sibarita, J. B., and Giannone, G. (2014) Nanoscale segregation of actin nucleation and elongation factors determines dendritic spine protrusion. EMBO J. 33, 2745-2764
19. Hotulainen, P., Llano, O., Smirnov, S., Tanhuanpaa, K., Faix, J., Rivera, C., and Lappalainen, P. (2009) Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J. Cell Biol. 185, 323-339
20. Law, R., Dixon-Salazar, T., Jerber, J., Cai, N., Abbasi, A. A., Zaki, M. S., Mittal, K., Gabriel, S. B., Rafiq, M. A., Khan, V., Nguyen, M., Ali, G., Copeland, B., Scott, E., Vasli, N., Mikhailov, A., Khan, M. N., Andrade, D. M., Ayaz, M., Ansar, M., Ayub, M., Vincent, J. B., and Gleeson, J. G. (2014) Biallelic truncating mutations in FMN2, encoding the actin-regulatory protein Formin 2, cause nonsyndromic autosomal-recessive intellectual disability. Am. J. Hum. Genet. 95, 721-728
21. Peleg, S., Sananbenesi, F., Zovoilis, A., Burkhardt, S., Bahari-Javan, S., Agis-Balboa, R. C., Cota, P., Wittnam, J. L., Gogol-Doering, A., Opitz, L., Salinas-Riester, G., Dettenhofer, M., Kang, H., Farinelli, L., Chen, W., and Fischer, A. (2010) Altered histone acetylation is associated with age-dependent memory impairment in mice. Science 328, 753-756
22. Miki, H., Suetsugu, S., and Takenawa, T. (1998) WAVE, a novel WASP-family protein involved in actin reorganization induced by Rac. EMBO J. 17, 6932-6941
23. Romero, S., Le Clainche, C., Didry, D., Egile, C., Pantaloni, D., and Carlier, M. F. (2004) Formin is a processive motor that requires profilin to accelerate actin assembly and associated ATP hydrolysis. Cell 119, 419-429
24. Ackermann, M., and Matus, A. (2003) Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat. Neurosci. 6, 1194-1200
25. Lamprecht, R., and Farb., C. R., Rodrigues, S. M., and LeDoux, J. E. (2006) Fear conditioning drives profilin into amygdala dendritic spines. Nat. Neurosci. 9, 481-483
26. Bernstein, B. W., and Bamburg, J. R. (2010) ADF/cofilin: a functional node in cell biology. Trends Cell Biol. 20, 187-195
27. Racz, B., and Weinberg, R. J. (2006) Spatial organization of cofilin in dendritic spines. Neuroscience 138, 447-456
28. Yang, N., Higuchi, O., Ohashi, K., Nagata, K., Wada, A., Kangawa, K., Nishida, E., and Mizuno, K. (1998) Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature 393, 809-812
29. Gray, V., Karmiloff-Smith, A., Funnell, E., and Tassabehji, M. (2006) In-depth analysis of spatial cognition in Williams syndrome: a critical assessment of the role of the LIMK1 gene. Neuropsychologia 44, 679-685
30. Meng, Y., Zhang, Y., Tregoubov, V., Janus, C., Cruz, L., Jackson, M., Lu, W. Y., MacDonald, J. F., Wang, J. Y., Falls, D. L., and Jia, Z. (2002) Abnormal spine morphology and enhanced LTPin LIMK-1 knockout mice. Neuron 35, 121-133
31. Goodson, M., and Rust., M. B., Witke, W., Bannerman, D., Mott, R., and Ponting., C. P., and Flint, J. (2012) Cofilin-1: a modulator of anxiety in mice. PLoS Genet. 8, e1002970
32. Edwards, M., Zwolak, A., Schafer, D. A., Sept, D., Dominguez, R., and Cooper, J. A. (2014) Capping protein regulators fine-tune actin assembly dynamics. Nat. Rev. Mol. Cell Biol. 15, 677-689
33. Fan, Y., Tang, X., Vitriol, E., Chen, G., and Zheng, J. Q. (2011) Actin capping protein is required for dendritic spine development and synapse formation. J. Neurosci. 31, 10228-10233
34. Menna, E., Zambetti, S., Morini, R., Donzelli, A., Disanza, A., Calvigioni, D., Braida, D., Nicolini, C., Orlando, M., Fossati, G., Cristina Regondi, M., Pattini, L., Frassoni, C., Francolini, M., Scita, G., Sala, M., Fahnestock, M., and Matteoli, M. (2013) Eps8 controls dendritic spine density and synaptic plasticity through its actin-capping activity. EMBO J. 32, 1730-1744
35. Yu, X., and Malenka, R. C. (2004) Multiple functions for the cadherin/catenin complex during neuronal development. Neuropharmacology 47, 779-786
36. Okuda, T., and Yu., L. M., Cingolani, L. A., Kemler, R., and Goda, Y. (2007) β-Catenin regulates excitatory postsynaptic strength at hippocampal synapses. Proc. Natl. Acad. Sci. U.S.A. 104, 13479-13484
37. Yonemura, S., Wada, Y., Watanabe, T., Nagafuchi, A., and Shibata, M. (2010) α-Cateninas a tension transducer that induces adherens junction development. Nat Cell Biol. 12, 533-542
38. Abe, K., Chisaka, O., Van Roy, F., and Takeichi, M. (2004) Stability of dendritic spines and synaptic contacts is controlled by α N-catenin. Nat. Neurosci. 7, 357-363
39. Elia, L. P., Yamamoto, M., Zang, K., and Reichardt, L. F. (2006) p120 catenin regulates dendritic spine and synapse development through Rho-family GTPases and cadherins. Neuron 51, 43-56
40. Martinez, M. C, Ochiishi, T., Majewski, M., and Kosik, K. S. (2003) Dual regulation of neuronal morphogenesis by a S-catenin-cortactin complex and Rho. J. Cell Biol. 162, 99-111
41. Kim, H., and Han., J. R., Park, J., Oh, M., James, S. E., Chang, S., Lu, Q., and Lee., K. Y., Ki, H., Song, W. J., and Kim, K. (2008) S-Catenin-induced dendritic morphogenesis: an essential role of p190RhoGEF interaction through Akt1-mediated phosphorylation. J. Biol. Chem. 283, 977-987
42. Kim, T. J., Zheng, S., Sun, J., Muhamed, I., Wu, J., Lei, L., Kong, X., Leckband, D.E., and Wang, Y. (2015) Dynamic visualization of α-catenin reveals rapid, reversible conformation switching between tension states. Curr. Biol. 25, 218-224
43. Tucci, V., Kleefstra, T., Hardy, A., Heise, I., Maggi, S., Willemsen, M. H., Hilton, H., Esapa, C., Simon, M., Buenavista, M. T., McGuffin, L. J., Vizor, L., Dodero, L., Tsaftaris, S., Romero, R., Nillesen, W. N, Vissers, L. E., Kempers, M.J., Vulto-van Silfhout, A. T., Iqbal, Z., Orlando, M., Maccione, A., Lassi, G., Farisello, P., Contestabile, A., Tinarelli, F., Nieus, T., Raimondi, A., Greco, B., Cantatore, D., Gasparini, L., Berdondini, L., Bifone, A., Gozzi, A., Wells, S., and Nolan, P. M. (2014) Dominant β-catenin mutations cause intellectual disability with recognizable syndromic features. J. Clin. Invest. 124, 1468-1482
44. Medina, M., and Marinescu., R. C., Overhauser, J., and Kosik, K. S. (2000) Hemizygosity of S-catenin (CTNND2) is associated with severe mental retardation in cri-du-chat syndrome. Genomics 63, 157-164
45. Uchida, N, Honjo, Y., Johnson, K. R., Wheelock, M. J., and Takeichi, M. (1996) The catenin/cadherin adhesion system is localized in synaptic junctions bordering transmitter release zones. J. Cell Biol. 135, 767-779
46. Togashi, H., Abe, K., Mizoguchi, A., Takaoka, K., Chisaka, O., and Takeichi, M. (2002) Cadherin regulates dendritic spine morphogenesis. Neuron 35, 77-89
47. Saglietti, L., Dequidt, C, Kamieniarz, K., Rousset, M. C, Valnegri, P., Thoumine, O., Beretta, F., Fagni, L., Choquet, D., Sala, C, Sheng, M., and Passafaro, M. (2007) Extracellular interactions between GluR2 and Ncadherin in spine regulation. Neuron 54, 461-477
48. Chazeau, A., Garcia, M., Czondor, K., Perrais, D., Tessier, B., Giannone, G., and Thoumine, O. (2015) Mechanical coupling between transsynaptic N-cadherin adhesions and actin flow stabilizes dendritic spines. Mol. Biol. Cell 26, 859-873
49. Zhou, Z., Hu, J., Passafaro, M., Xie, W., and Jia, Z. (2011) GluA2 (GluR2) regulates metabotropic glutamate receptor-dependent long-term depression through N-cadherin-dependent and cofilin-mediated actin reorganization. J. Neurosci. 31, 819-833
50. Xie, Z., Photowala, H, and Cahill., M. E., Srivastava, D. P., Woolfrey, K. M., Shum, C Y., Huganir, R. L., and Penzes, P. (2008) Coordination of synaptic adhesion with dendritic spine remodeling by AF-6 and kalirin-7. J. Neurosci. 28, 6079-6091
51. Tachibana, K., Nakanishi, H, Mandai, K., Ozaki, K., Ikeda, W., Yamamoto, Y., Nagafuchi, A., Tsukita, S., and Takai, Y. (2000) Two cell adhesion molecules, nectin and cadherin, interact through their cytoplasmic domain-associated proteins. J. Cell Biol. 150, 1161-1176
52. Srivastava, D.P., Copits, B. A., Xie, Z., Huda, R., Jones, K. A., Mukherji, S., Cahill, M. E., VanLeeuwen, J. E., Woolfrey, K. M., Rafalovich, I., Swanson, G. T., and Penzes, P. (2012) Afadin is required for maintenance of dendritic structure and excitatory tone. J. Biol. Chem. 287, 35964-35974
53. Hirabayashi, T., and Yagi, T. (2014) Protocadherins in neurological diseases. Adv. Neurobiol. 8, 293-314
54. Nakao, S., Platek, A., Hirano, S., and Takeichi, M. (2008) Contact-dependent promotion of cell migration by the OL-protocadherin-Nap1 interaction. J. Cell Biol. 182, 395-410
55. Tai, K., Kubota, M., Shiono, K., Tokutsu, H, and Suzuki, S. T. (2010) Adhesion properties and retinofugal expression of chicken protocadherin-19. Brain Res. 1344, 13-24
56. Chen, B., Brinkmann, K., Chen, Z., Pak, C. W., Liao, Y., Shi, S., Henry, L., Grishin, N V, Bogdan, S., and Rosen, M. K. (2014) The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156, 195-207
57. Huganir, R. L., and Nicoll, R. A. (2013) AMPARs and synaptic plasticity: the last 25 years. Neuron 80, 704-717
58. Allison, D. W., and Gelfand., V. I., Spector, I., and Craig, A. M. (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J. Neurosci. 18, 2423-2436
59. Kim, C. H, and Lisman, J. E. (1999) A role of actin filament in synaptic transmission and long-term potentiation. J. Neurosci. 19, 4314-4324
60. Zhou, Q., Xiao, M., and Nicoll, R. A. (2001) Contribution of cytoskeleton to the internalization of AMPA receptors. Proc. Natl. Acad. Sci. U.S.A. 98, 1261-1266
61. Opazo, P., and Choquet, D. (2011) A three-step model for the synaptic recruitment of AMPA receptors. Mol. Cell. Neurosci. 46, 1-8
62. Gu, J., Lee, C W., Fan, Y., Komlos, D., Tang, X., Sun, C, Yu, K., Hartzell, H. C, Chen, G., Bamburg, J. R., and Zheng, J. Q. (2010) ADF/cofilinmediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci. 13, 1208-1215
63. Rust, M. B., and Gurniak., C. B., Renner, M., Vara, H., Morando, L., Gorlich, A., Sassoe-Pognetto, M., Banchaabouchi, M. A., Giustetto, M., Triller, A., Choquet, D., and Witke, W. (2010) Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBOJ. 29, 1889-1902
64. Kerr, J. M., and Blanpied, T. A. (2012) Subsynaptic AMPA receptor distribution is acutely regulated by actin-driven reorganization of the postsynaptic density. J. Neurosci. 32, 658-673
65. Xia, J., Zhang, X., Staudinger, J., and Huganir, R. L. (1999) Clustering of AMPA receptors by the synaptic PDZ domain-containing protein PICK1. Neuron 22, 179-187
66. Staudinger, J., Zhou, J., Burgess, R., Elledge, S. J., and Olson, E. N. (1995) PICK1: a perinuclear binding protein and substrate for protein kinase C isolated by the yeast two-hybrid system. J. Cell Biol. 128, 263-271
67. Rocca, D. L., Martin, S., Jenkins, E. L., and Hanley, J. G. (2008) Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nat Cell Biol. 10, 259-271
68. Hanley, J. G. (2014) Actin-dependent mechanisms in AMPA receptor trafficking. Front. Cell. Neurosci. 8, 381
69. Staudinger, J., Lu, J., and Olson, E. N. (1997) Specific interaction of the PDZ domain protein PICK1 with the COOH terminus of protein kinase C-α. J. Biol. Chem. 272, 32019-32024
70. Erlendsson, S., Rathje, M., Heidarsson, P. O., Poulsen, F. M., Madsen, K. L., Teilum, K., and Gether, U. (2014) Protein interacting with C-kinase 1 (PICK1) binding promiscuity relies on unconventional PSD-95/discslarge/ZO-1 homology (PDZ) binding modes for nonclass II PDZ ligands. J. Biol. Chem. 289, 25327-25340
71. Madasu, Y., Yang, C, Boczkowska, M., and Bethoney., K. A., Zwolak, A., Rebowski, G., Svitkina, T., and Dominguez, R. (2015) PICK1 is implicated in organelle motility in an Arp2/3 complex-independent manner. Mol. Biol. Cell 26, 1308-1322
72. Derivery, E., Sousa, C, and Gautier., J. J., Lombard, B., Loew, D., and Gautreau, A. (2009) The Arp2/3 activator WASH controls the fission of endosomes through a large multiprotein complex. Dev. Cell 17, 712-723
73. Puthenveedu, M. A., Lauffer, B., Temkin, P., Vistein, R., Carlton, P., Thorn, K., Taunton, J., and Weiner., O. D., Parton, R. G., and von Zastrow, M. (2010) Sequence-dependent sorting of recycling proteins by actin-stabilized endosomal microdomains. Cell 143, 761-773
74. Harbour, M. E., and Breusegem., S. Y., Antrobus, R., Freeman, C., Reid, E., and Seaman, M. N. (2010) The cargo-selective retromer complex is a recruiting hub for protein complexes that regulate endosomal tubule dynamics. J. Cell Sci. 123, 3703-3717
75. Munsie, L. N., and Milnerwood., A. J., Seibler, P., Beccano-Kelly, D. A., Tatarnikov, I., Khinda, J., Volta, M., Kadgien, C., Cao, L. P., Tapia, L., Klein, C., and Farrer, M. J. (2015) Retromer-dependent neurotransmitter receptor trafficking to synapses is altered by the Parkinson's disease VPS35 mutation p. D620N. Hum. Mol. Genet. 24, 1691-1703
76. Choy, R. W., Park, M., Temkin, P., Herring, B. E., Marley, A., Nicoll, R. A., and von Zastrow, M. (2014) Retromer mediates a discrete route of local membrane delivery to dendrites. Neuron 82, 55-62
77. Ropers, F., Derivery, E., Hu, H., Garshasbi, M., Karbasiyan, M., Herold, M., Nurnberg, G., Ullmann, R., Gautreau, A., Sperling, K., Varon, R., and Rajab, A. (2011) Identification of a novel candidate gene for non-syndromic autosomal recessive intellectual disability: the WASH complex member SWIP. Hum. Mol. Genet. 20, 2585-2590
78. Nadif Kasri, N., Nakano-Kobayashi, A., Malinow, R., Li, B., and Van Aelst, L. (2009) The Rho-linked mental retardation protein oligophrenin-1 controls synapse maturation and plasticity by stabilizing AMPA receptors. Genes Dev. 23, 1289-1302
79. Nakano-Kobayashi, A., Tai, Y., Nadif Kasri, N., and Van Aelst, L. (2014) The X-linked mental retardation protein OPHN1 interacts with Homer1b/c to control spine endocytic zone positioning and expression of synaptic potentiation. J. Neurosci. 34, 8665-8671
80. Billuart, P., Bienvenu, T., Ronce, N., des Portes, V., Vinet, M. C., Zemni, R., Roest Crollius, H., Carrie, A., Fauchereau, F., Cherry, M., Briault, S., Hamel, B., Fryns, J. P., Beldjord, C., Kahn, A., Moraine, C., and Chelly, J. (1998) Oligophrenin-1 encodes a rhoGAP protein involved in X-linked mental retardation. Nature 392, 923-926
81. Van Harreveld, A., and Fifkova, E. (1975) Swelling of dendritic spines in the fascia dentata after stimulation of the perforant fibers as a mechanism of post-tetanic potentiation. Exp. Neurol. 49, 736-749
82. Nusser, Z., Lujan, R., Laube, G., Roberts, J. D., Molnar, E., and Somogyi, P. (1998) Cell type and pathway dependence of synaptic AMPA receptor number and variability in the hippocampus. Neuron 21, 545-559
83. Matsuzaki, M., Ellis-Davies, G. C., Nemoto, T., Miyashita, Y., Iino, M., and Kasai, H. (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat. Neurosci. 4, 1086-1092
84. Kasai, H., Matsuzaki, M., Noguchi, J., Yasumatsu, N., and Nakahara, H. (2003) Structure-stability-function relationships of dendritic spines. Trends Neurosci. 26, 360-368
85. Matsuzaki, M., Honkura, N., Ellis-Davies, G. C., and Kasai, H. (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429, 761-766
86. Murakoshi, H., Wang, H., and Yasuda, R. (2011) Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472, 100-104
87. Honkura, N., Matsuzaki, M., Noguchi, J., Ellis-Davies, G. C, and Kasai, H. (2008) The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57, 719-729
88. 2+/calmodulin-dependent protein kinase IIa in dendritic spine enlargement, long-term potentiation, and learning. J. Neurosci. 29, 7607-7618
89. Fukazawa, Y., Saitoh, Y., Ozawa, F., Ohta, Y., Mizuno, K., and Inokuchi, K. (2003) Hippocampal LTP is accompanied by enhanced F-actin content within the dendritic spine that is essential for late LTP maintenance in vivo. Neuron 38, 447-460
90. Burianek, L. E., and Soderling, S. H. (2013) Under lock and key: spatiotemporal regulation of WASP family proteins coordinates separate dynamic cellular processes. Semin. CellDev. Biol. 24, 258-266
91. Kim, I. H., Wang, H, Soderling, S. H, and Yasuda, R. (2014) Loss of Cdc42 leads to defects in synaptic plasticity and remote memory recall. eLife 3, e02839
92. Soderling, S. H., and Langeberg., L. K., Soderling, J. A., Davee, S. M., Simerly, R., Raber, J., and Scott, J. D. (2003) Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc. Natl. Acad. Sci. U.S.A. 100, 1723-1728
93. Hazai, D., Szudoczki, R., Ding, J., Soderling, S. H., Weinberg, R. J., Sótonyi, P., and Rácz, B. (2013) Ultrastructural abnormalities in CA1 hippocampus caused by deletion of the actin regulator WAVE-1. PLoS One 8, e75248
94. Chen, L. Y., and Rex., C. S., Casale, M. S., Gall, C. M., and Lynch, G. (2007) Changes in synaptic morphology accompany actin signaling during LTP. J. Neurosci. 27, 5363-5372
95. Zhou, Q., and Homma., K. J., and Poo, M. M. (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749-757
96. Calabrese, B., and Saffin., J. M., and Halpain, S. (2014) Activity-dependent dendritic spine shrinkage and growth involve downregulation of cofilin via distinct mechanisms. PLoS One 9, e94787
97. Bosch, M., Castro, J., Saneyoshi, T., Matsuno, H., Sur, M., and Hayashi, Y. (2014) Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82, 444-459
98. Tønnesen, J., Katona, G., Rózsa, B., and Nägerl, U. V. (2014) Spine neck plasticity regulates compartmentalization of synapses. Nat. Neurosci. 17, 678-685
99. Xie, Y., and Vessey., J. P., Konecna, A., Dahm, R., Macchi, P., and Kiebler, M. A. (2007) The GTP-binding protein Septin 7 is critical for dendrite branching and dendritic-spine morphology. Curr. Biol. 17, 1746-1751
100. Ewers, H, Tada, T., Petersen, J. D., Racz, B., Sheng, M., and Choquet, D. (2014) A septin-dependent diffusion barrier at dendritic spine necks. PLoS One 9, e113916