Organization and dynamics of the actin cytoskeleton during dendritic spine morphological remodeling

Cellular and Molecular Life Sciences

Volumn 73, Issue 16, 2016, Pages 3053-3073

  Chazeau, Anaël ^a,b,c   Giannone, Grégory ^a,b  

^a UNIVERSITÉ DE BORDEAUX   (France)

^b CNRS   (France)

^c UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Actin binding proteins; Actin cytoskeleton; CAMKII; Dendritic spines; PSD; Super resolution microscopy; Synaptic plasticity

Indexed keywords

ACTIN BINDING PROTEIN; F ACTIN; ACTIN;

ACTIN FILAMENT; CELL MATURATION; CELL MOTILITY; CELL STRUCTURE; DENDRITIC SPINE; FILOPODIUM; HUMAN; LONG TERM DEPRESSION; LONG TERM POTENTIATION; MOLECULAR DYNAMICS; NERVE CELL PLASTICITY; NONHUMAN; POSTSYNAPTIC DENSITY; PROTEIN CROSS LINKING; PROTEIN STRUCTURE; REVIEW; SIGNAL TRANSDUCTION; SYNAPTIC TRANSMISSION; ANIMAL; METABOLISM; PHYSIOLOGY; SYNAPSE;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; DENDRITIC SPINES; HUMANS; MICROFILAMENT PROTEINS; NEURONAL PLASTICITY; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 84964290577     PISSN: 1420682X     EISSN: 14209071     Source Type: Journal    
DOI: 10.1007/s00018-016-2214-1     Document Type: Review

References (304)

1. Ramón y Cajal S S (1888) Estructura de los centros nerviosos de las aves. Rev Trim Histol Norm Pat 1:1–10
2. Yuste R (2015) The discovery of dendritic spines by Cajal. Front Neuroanat 9:1–6. doi:10.3389/fnana.2015.00018
3. Ramón y Cajal S (1891) Significación fisiológica de las expansiones protoplásmicas y nerviosas de la sustancia gris. Rev Cienc Med Barcelona 22:23
4. Ramón y Cajal S (1893) Neue darstellung vom histologischen bau des centralnervensystem. Arch Anat Entwick 319–428
5. Ramón y Cajal S (1894) La fine structure des centres nerveux. The croonian lecture. Proc R Soc Lond B 55:443–468
6. Gray EG (1959) Electron microscopy of synaptic contacts on dendrite spines of the cerebral cortex. Nature 183:1592–1593. doi:10.1038/1831592a0
7. Gray EG (1959) Axo-somatic and axo-dendritic synapses of the cerebral cortex. J Anat 93:420–433. doi:10.1038/1831592a0
8. Guillery RW (2000) Early electron microscopic observations of synaptic structures in the cerebral cortex: a view of the contributions made by George Gray (1924–1999). Trends Neurosci 23:594–598. doi:10.1016/S0166-2236(00)01635-0
9. Hebb DO (1949) The organization of behaviour: a neuropsychological theory. Wiley, New York
10. Kandel ER (2009) The biology of memory: a forty-year perspective. J Neurosci 29:12748–12756. doi:10.1523/JNEUROSCI.3958-09.2009
11. Squire LR (2009) Memory and brain systems: 1969–2009. J Neurosci 29:12711–12716. doi:10.1523/JNEUROSCI.3575-09.2009
12. Nabavi S, Fox R, Proulx CD, Lin JY, Tsien RY, Malinow R (2014) Engineering a memory with LTD and LTP. Nature 511:348–352. doi:10.1038/nature13294
13. Hayashi-Takagi A, Yagishita S, Nakamura M, Shirai F, Wu YI, Loshbaugh AL, Kuhlman B, Hahn KM, Kasai H (2015) Labelling and optical erasure of synaptic memory traces in the motor cortex. Nature 525:333–338. doi:10.1038/nature15257
14. Harris KM, Jensen FE, Tsao B (1992) Three-dimensional structure of dendritic spines and synapses in rat hippocampus (CA1) at postnatal day 15 and adult ages: implications for the maturation of synaptic physiology and long-term potentiation. J Neurosci 12:2685–2705
15. Bourne JN, Harris KM (2008) Balancing structure and function at hippocampal dendritic spines. Annu Rev Neurosci 31:47–67. doi:10.1146/annurev.neuro.31.060407.125646
16. Nägerl UV, Willig KI, Hein B, Hell SW, Bonhoeffer T (2008) Live-cell imaging of dendritic spines by STED microscopy. Proc Natl Acad Sci USA 105:18982–18987. doi:10.1073/pnas.0810028105
17. Izeddin I, Specht CG, Lelek M, Darzacq X, Triller A, Zimmer C, Dahan M (2011) Super-resolution dynamic imaging of dendritic spines using a low-affinity photoconvertible actin probe. PLoS ONE 6:e15611. doi:10.1371/journal.pone.0015611
18. Dailey E, Smith S (1996) The dynamics of dendritic structure in developing hippocampal slices. J Neurosci 16:2983–2994
19. Fischer M, Kaech S, Knutti D, Matus A (1998) Rapid actin-based plasticity in dendritic spines. Neuron 20:847–854
20. Lendvai B, Stern EA, Chen B, Svoboda K (2000) Experience-dependent plasticity of dendritic spines in the developing rat barrel cortex in vivo. Nature 404:876–881. doi:10.1038/35009107
21. Grutzendler J, Kasthuri N, Gan W-B (2002) Long-term dendritic spine stability in the adult cortex. Nature 420:812–816. doi:10.1038/nature01276
22. Berning S, Willig KI, Steffens H, Dibaj P, Hell SW (2012) Nanoscopy in a living mouse brain. Science 335:551. doi:10.1126/science.1215369
23. Buchs PA, Muller D (1996) Induction of long-term potentiation is associated with major ultrastructural changes of activated synapses. Proc Natl Acad Sci USA 93:8040–8045
24. Engert F, Bonhoeffer T (1999) Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399:66–70. doi:10.1038/19978
25. Toni N, Buchs P, Nikonenko I, Bron C, Muller D (1999) LTP promotes formation of multiple spine synapses between a single axon terminal and a dendrite. Nature 402:421–425. doi:10.1038/46574
26. Nägerl UV, Eberhorn N, Cambridge SB, Bonhoeffer T (2004) Bidirectional activity-dependent morphological plasticity in hippocampal neurons. Neuron 44:759–767. doi:10.1016/j.neuron.2004.11.016
27. Nishiyama J, Yasuda R (2015) Biochemical computation for spine structural plasticity. Neuron 87:63–75. doi:10.1016/j.neuron.2015.05.043
28. Matsuzaki M, Honkura N, Ellis-Davies GCR, Kasai H (2004) Structural basis of long-term potentiation in single dendritic spines. Nature 429:761–766. doi:10.1038/nature02617
29. Zhou Q, Homma KJ, Poo MM (2004) Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44:749–757. doi:10.1016/j.neuron.2004.11.011
30. Oh WC, Hill TC, Zito K (2013) Synapse-specific and size-dependent mechanisms of spine structural plasticity accompanying synaptic weakening. Proc Natl Acad Sci USA 110:E305–E312. doi:10.1073/pnas.1214705110
31. Tønnesen J, Katona G, Rózsa B, Nägerl UV (2014) Spine neck plasticity regulates compartmentalization of synapses. Nat Neurosci 17:678–685. doi:10.1038/nn.3682
32. Noguchi J, Nagaoka A, Watanabe S, Ellis-Davies GCR, Kitamura K, Kano M, Matsuzaki M, Kasai H (2011) In vivo two-photon uncaging of glutamate revealing the structure-function relationships of dendritic spines in the neocortex of adult mice. J Physiol 589:2447–2457. doi:10.1113/jphysiol.2011.207100
33. Loewenstein Y, Kuras A, Rumpel S (2011) Multiplicative dynamics underlie the emergence of the log-normal distribution of spine sizes in the neocortex in vivo. J Neurosci 31:9481–9488. doi:10.1523/JNEUROSCI.6130-10.2011
34. Zhang Y, Cudmore RH, Lin D-T, Linden DJ, Huganir RL (2015) Visualization of NMDA receptor-dependent AMPA receptor synaptic plasticity in vivo. Nat Neurosci 18:402–407. doi:10.1038/nn.3936
35. Sheng M, Hoogenraad CC (2007) The postsynaptic architecture of excitatory synapses: a more quantitative view. Annu Rev Biochem 76:823–847. doi:10.1146/annurev.biochem.76.060805.160029
36. Fifkova E, Delay RJ (1982) Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J Cell Biol 95:345–350
37. Kaech S, Fischer M, Doll T, Matus A (1997) Isoform specificity in the relationship of actin to dendritic spines. J Neurosci 17:9565–9572
38. Cheng D, Hoogenraad C, Rush J, Schlager M, Duong D, Xu P, Wijayawardana S, Hanfelt J, Nakagawa T, Sheng M, Peng J (2006) Relative and absolute quantification of postsynaptic density proteome isolated from rat forebrain and cerebellum. Mol Cell Proteomics 5:1158–1170. doi:10.1074/mcp.D500009-MCP200
39. Korobova F, 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. doi:10.1091/mbc.E09-07-0596
40. Dunaevsky A, Tashiro A, Majewska A, Mason C, Yuste R (1999) Developmental regulation of spine motility in the mammalian central nervous system. Proc Natl Acad Sci USA 96:13438–13443
41. Korkotian E, Segal M (2001) Regulation of dendritic spine motility in cultured hippocampal neurons. J Neurosci 21:6115–6124
42. Portera-Cailliau C, Pan DT, Yuste R (2003) Activity-regulated dynamic behavior of early dendritic protrusions: evidence for different types of dendritic filopodia. J Neurosci 23:7129–7142
43. Cingolani LA, Goda Y (2008) Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat Rev Neurosci 9:344–356. doi:10.1038/nrn2373
44. Hotulainen P, Hoogenraad CC (2010) Actin in dendritic spines: connecting dynamics to function. J Cell Biol 189:619–629. doi:10.1083/jcb.201003008
45. Pollard TD, Cooper JA (2009) Actin, a central player in cell shape and movement. Science 326:1208–1212. doi:10.1126/science.1175862
46. Carlier M-F, Pernier J, Montaville P, Shekhar S, Kühn S (2015) Control of polarized assembly of actin filaments in cell motility. Cell Mol Life Sci 72:3051–3067. doi:10.1007/s00018-015-1914-2
47. Pilo Boyl P, Witke W (2014) Small, smaller. dendritic spine. EMBO J 33:2737–2739. doi:10.15252/embj.201490137
48. Lin W-H, Webb DJ (2009) Actin and actin-binding proteins: masters of dendritic spine formation, morphology, and function. Open Neurosci J 3:54–66. doi:10.2174/1874082000903020054
49. Bosch M, Castro J, Saneyoshi T, Matsuno H, Sur M, Hayashi Y (2014) Structural and molecular remodeling of dendritic spine substructures during long-term potentiation. Neuron 82:444–459. doi:10.1016/j.neuron.2014.03.021
50. Chen X, Winters C, Azzam R, Li X, Galbraith JA, Leapman RD, Reese TS (2008) Organization of the core structure of the postsynaptic density. Proc Natl Acad Sci USA 105:4453–4458. doi:10.1073/pnas.0800897105
51. Rácz B, Weinberg RJ (2013) Microdomains in forebrain spines: an ultrastructural perspective. Mol Neurobiol 47:77–89. doi:10.1007/s12035-012-8345-y
52. Huang B, Bates M, Zhuang X (2009) Super-resolution fluorescence microscopy. Annu Rev Biochem 78:993–1016. doi:10.1146/annurev.biochem.77.061906.092014
53. Maglione M, Sigrist SJ (2013) Seeing the forest tree by tree: super-resolution light microscopy meets the neurosciences. Nat Neurosci 16:790–797. doi:10.1038/nn.3403
54. Choquet D, Triller A (2013) The dynamic synapse. Neuron 80:691–703. doi:10.1016/j.neuron.2013.10.013
55. Adrian M, Kusters R, Wierenga CJ, Storm C, Hoogenraad CC, Kapitein LC (2014) Barriers in the brain: resolving dendritic spine morphology and compartmentalization. Front Neuroanat 8:1–12. doi:10.3389/fnana.2014.00142
56. MacGillavry HD, Hoogenraad CC (2015) The internal architecture of dendritic spines revealed by super-resolution imaging: what did we learn so far? Exp Cell Res 335:180–186. doi:10.1016/j.yexcr.2015.02.024
57. Ziv NE, Smith SJ (1996) Evidence for a role of dendritic filopodia in synaptogenesis and spine formation. Neuron 17:91–102
58. Yuste R, Bonhoeffer T (2004) Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nat Rev Neurosci 5:24–34. doi:10.1038/nrn1300
59. Zuo Y, Lin A, Chang P, Gan W-B (2005) Development of long-term dendritic spine stability in diverse regions of cerebral cortex. Neuron 46:181–189. doi:10.1016/j.neuron.2005.04.001
60. Chazeau A, Garcia M, Czondor K, Perrais D, Tessier B, Giannone G, Thoumine O (2015) Mechanical coupling between transsynaptic N-cadherin adhesions and actin flow stabilizes dendritic spines. Mol Biol Cell 26:859–873. doi:10.1091/mbc.E14-06-1086
61. Hotulainen P, Llano O, Smirnov S, Tanhuanpää K, Faix J, Rivera C, Lappalainen P (2009) Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J Cell Biol 185:323–339. doi:10.1083/jcb.200809046
62. Mallavarapu A, Mitchison T (1999) Regulated actin cytoskeleton assembly at filopodium tips controls their extension and retraction. J Cell Biol 146:1097–1106. doi:10.1083/jcb.146.5.1097
63. Ponti A, Machacek M, Gupton SL, Waterman-Storer CM, Danuser G (2004) Two distinct actin networks drive the protrusion of migrating cells. Science 305:1782–1786. doi:10.1126/science.1100533
64. Medeiros NA, Burnette DT, Forscher P (2006) Myosin II functions in actin-bundle turnover in neuronal growth cones. Nat Cell Biol 8:215–226. doi:10.1038/ncb1367
65. Giannone G, Dubin-Thaler BJ, Rossier O, Cai Y, Chaga O, Jiang G, Beaver W, Döbereiner H-G, Freund Y, Borisy G, Sheetz MP (2007) Lamellipodial actin mechanically links myosin activity with adhesion-site formation. Cell 128:561–575. doi:10.1016/j.cell.2006.12.039
66. Tatavarty V, Das S, Yu J (2012) Polarization of actin cytoskeleton is reduced in dendritic protrusions during early spine development in hippocampal neuron. Mol Biol Cell 23:3167–3177. doi:10.1091/mbc.E12-02-0165
67. Chazeau A, Mehidi A, Nair D, Gautier JJ, Leduc C, Chamma I, Kage F, Kechkar A, Thoumine O, Rottner K, Choquet D, Gautreau A, Sibarita J-B, Giannone G (2014) Nanoscale segregation of actin nucleation and elongation factors determines dendritic spine protrusion. EMBO J 33:2745–2764. doi:10.15252/embj.201488837
68. Mitchison T, Kirschner M (1988) Cytoskeletal dynamics and nerve growth. Neuron 1:761–772
69. Suter DM, Forscher P (2000) Substrate-cytoskeletal coupling as a mechanism for the regulation of growth cone motility and guidance. J Neurobiol 44:97–113. doi:10.1002/1097-4695(200008)44:2<97:AID-NEU2>3.3.CO;2-L
70. Giannone G, Mège R-M, Thoumine O (2009) Multi-level molecular clutches in motile cell processes. Trends Cell Biol 19:475–486. doi:10.1016/j.tcb.2009.07.001
71. Bard L, Boscher C, Lambert M, Mège R-M, Choquet D, Thoumine O (2008) A molecular clutch between the actin flow and N-cadherin adhesions drives growth cone migration. J Neurosci 28:5879–5890. doi:10.1523/JNEUROSCI.5331-07.2008
72. Garcia M, Leduc C, Lagardère M, Argento A, Sibarita J-B, Thoumine O (2015) Two-tiered coupling between flowing actin and immobilized N-cadherin/catenin complexes in neuronal growth cones. Proc Natl Acad Sci USA 112:201423455. doi:10.1073/pnas.1423455112
73. Spacek J, Harris KM (2004) Trans-endocytosis via spinules in adult rat hippocampus. J Neurosci 24:4233–4241. doi:10.1523/JNEUROSCI.0287-04.2004
74. Tao-Cheng J-H, Dosemeci A, Gallant PE, Miller S, Galbraith JA, Winters CA, Azzam R, Reese TS (2009) Rapid turnover of spinules at synaptic terminals. Neuroscience 160:42–50. doi:10.1016/j.neuroscience.2009.02.031
75. Okamoto K-I, Nagai T, Miyawaki A, Hayashi Y (2004) Rapid and persistent modulation of actin dynamics regulates postsynaptic reorganization underlying bidirectional plasticity. Nat Neurosci 7:1104–1112. doi:10.1038/nn1311nn1311
76. Star EN, Kwiatkowski DJ, Murthy VN (2002) Rapid turnover of actin in dendritic spines and its regulation by activity. Nat Neurosci 5:239–246. doi:10.1038/nn811
77. Honkura N, Matsuzaki M, Noguchi J, Ellis-Davies GCR, Kasai H (2008) The subspine organization of actin fibers regulates the structure and plasticity of dendritic spines. Neuron 57:719–729. doi:10.1016/j.neuron.2008.01.013
78. Frost NA, Shroff H, Kong H, Betzig E, Blanpied TA (2010) Single-molecule discrimination of discrete perisynaptic and distributed sites of actin filament assembly within dendritic spines. Neuron 67:86–99. doi:10.1016/j.neuron.2010.05.026
79. Betzig E, Patterson GH, Sougrat R, Lindwasser OW, Olenych S, Bonifacino JS, Davidson MW, Lippincott-Schwartz J, Hess HF (2006) Imaging intracellular fluorescent proteins at nanometer resolution. Science 313:1642–1645. doi:10.1126/science.1127344
80. Manley S, Gillette JM, Patterson GH, Shroff H, Hess HF, Betzig E, Lippincott-Schwartz J (2008) High-density mapping of single-molecule trajectories with photoactivated localization microscopy. Nat Methods 5:155–157. doi:10.1038/nmeth.1176
81. Tatavarty V, Kim E-J, Rodionov V, Yu J (2009) Investigating sub-spine actin dynamics in rat hippocampal neurons with super-resolution optical imaging. PLoS ONE 4:e7724. doi:10.1371/journal.pone.0007724
82. Pollard TD (2003) The cytoskeleton, cellular motility and the reductionist agenda. Nature 422:741–745. doi:10.1038/nature01598
83. Lai FPL, Szczodrak M, Block J, Faix J, Breitsprecher D, Mannherz HG, Stradal TEB, Dunn GA, Small JV, Rottner K (2008) Arp2/3 complex interactions and actin network turnover in lamellipodia. EMBO J 27:982–992. doi:10.1038/emboj.2008.34
84. Achard V, Martiel J-L, Michelot A, Guérin C, Reymann A-C, Blanchoin L, Boujemaa-Paterski R (2010) A “primer”-based mechanism underlies branched actin filament network formation and motility. Curr Biol 20:423–428. doi:10.1016/j.cub.2009.12.056
85. Sykes C, Plastino J (2010) Cell biology: actin filaments up against a wall. Nature 464:365–366. doi:10.1038/464365a
86. Frost NA, Kerr JM, Lu HE, Blanpied TA (2010) A network of networks: cytoskeletal control of compartmentalized function within dendritic spines. Curr Opin Neurobiol 20:578–587. doi:10.1016/j.conb.2010.06.009
87. Rácz B, Weinberg RJ (2008) Organization of the Arp2/3 complex in hippocampal spines. J Neurosci 28:5654–5659. doi:10.1523/JNEUROSCI.0756-08.2008
88. Burette AC, Lesperance T, Crum J, Martone M, Volkmann N, Ellisman MH, Weinberg RJ (2012) Electron tomographic analysis of synaptic ultrastructure. J Comp Neurol 520:2697–2711. doi:10.1002/cne.23067
89. Blanchoin L, Amann KJ, Higgs HN, Marchand J, Kaiser DA, Pollard TD (2000) Direct observation of dendritic actin filament networks nucleated by Arp2/3 complex and WASP/Scar proteins. Nature 171:1007–1011
90. Amann KJ, Pollard TD (2001) Direct real-time observation of actin filament branching mediated by Arp2/3 complex using total internal reflection fluorescence microscopy. Proc Natl Acad Sci USA 98:15009–15013. doi:10.1073/pnas.211556398
91. Goley ED, Welch MD (2006) The ARP2/3 complex: an actin nucleator comes of age. Nat Rev Mol Cell Biol 7:713–726. doi:10.1038/nrm2026
92. Campellone KG, Welch MD (2010) A nucleator arms race: cellular control of actin assembly. Nat Rev Mol Cell Biol 11:237–251. doi:10.1038/nrm2867
93. Kim IH, Racz B, Wang H, Burianek L, Weinberg R, Yasuda R, Wetsel WC, Soderling SH (2013) Disruption of Arp2/3 results in asymmetric structural plasticity of dendritic spines and progressive synaptic and behavioral abnormalities. J Neurosci 33:6081–6092. doi:10.1523/JNEUROSCI.0035-13.2013
94. Helgeson LA, Nolen BJ (2013) Mechanism of synergistic activation of Arp2/3 complex by cortactin and N-WASP. Elife 2:e00884. doi:10.7554/eLife.00884
95. Helgeson LA, Prendergast JG, Wagner AR, Rodnick-Smith M, Nolen BJ (2014) Interactions with actin monomers, actin filaments, and Arp2/3 complex define the roles of WASP family proteins and cortactin in coordinately regulating branched actin networks. J Biol Chem 289:28856–28869. doi:10.1074/jbc.M114.587527
96. Rocca DL, Martin S, Jenkins EL, Hanley JG (2008) Inhibition of Arp2/3-mediated actin polymerization by PICK1 regulates neuronal morphology and AMPA receptor endocytosis. Nat Cell Biol 10:259–271. doi:10.1038/ncb1688
97. Kim Y, Sung JY, Ceglia I, Lee K-W, Ahn J-H, Halford JM, Kim AM, Kwak SP, Park JB, Ho Ryu S, Schenck A, Bardoni B, Scott JD, Nairn AC, Greengard P (2006) Phosphorylation of WAVE1 regulates actin polymerization and dendritic spine morphology. Nature 442:814–817. doi:10.1038/nature04976
98. Grove M, Demyanenko G, Echarri A, Zipfel PA, Quiroz ME, Rodriguiz RM, Playford M, Martensen SA, Robinson MR, Wetsel WC, Maness PF, Pendergast AM (2004) ABI2-deficient mice exhibit defective cell migration, aberrant dendritic spine morphogenesis, and deficits in learning and memory. Mol Cell Biol 24:10905–10922. doi:10.1128/MCB.24.24.10905
99. Pilpel Y, Segal M (2005) Rapid WAVE dynamics in dendritic spines of cultured hippocampal neurons is mediated by actin polymerization. J Neurochem 95:1401–1410. doi:10.1111/j.1471-4159.2005.03467.x
100. Soderling SH, Guire ES, Kaech S, White J, Zhang F, Schutz K, Langeberg LK, Banker G, Raber J, Scott JD (2007) A WAVE-1 and WRP signaling complex regulates spine density, synaptic plasticity, and memory. J Neurosci 27:355–365. doi:10.1523/JNEUROSCI.3209-06.2006
101. Proepper C, Johannsen S, Liebau S, Dahl J, Vaida B, Bockmann J, Kreutz MR, Gundelfinger ED, Boeckers TM (2007) Abelson interacting protein 1 (Abi-1) is essential for dendrite morphogenesis and synapse formation. EMBO J 26:1397–1409. doi:10.1038/sj.emboj.7601569
102. Hering H, Sheng M (2003) Activity-dependent redistribution and essential role of cortactin in dendritic spine morphogenesis. J Neurosci 23:11759–11769 (pii:23/37/11759)
103. Racz B, Weinberg RJ (2004) The subcellular organization of cortactin in hippocampus. J Neurosci 24:10310–10317. doi:10.1523/JNEUROSCI.2080-04.2004
104. Lee S, Lee K, Hwang S, Kim SH, Song WK, Park ZY, Chang S (2006) SPIN90/WISH interacts with PSD-95 and regulates dendritic spinogenesis via an N-WASP-independent mechanism. EMBO J 25:4983–4995. doi:10.1038/sj.emboj.7601349
105. Wegner AM, Nebhan CA, Hu L, Majumdar D, Meier KM, Weaver AM, Webb DJ (2008) N-wasp and the arp2/3 complex are critical regulators of actin in the development of dendritic spines and synapses. J Biol Chem 283:15912–15920. doi:10.1074/jbc.M801555200
106. Nakamura Y, Wood CL, Patton AP, Jaafari N, Henley JM, Mellor JR, Hanley JG (2011) PICK1 inhibition of the Arp2/3 complex controls dendritic spine size and synaptic plasticity. EMBO J 30:719–730. doi:10.1038/emboj.2010.357
107. Mejillano MR, Kojima S, Applewhite DA, Gertler FB, Svitkina TM, Borisy GG (2004) Lamellipodial versus filopodial mode of the actin nanomachinery. Cell 118:363–373. doi:10.1016/j.cell.2004.07.019
108. Goldschmidt-Clermont PJ, Machesky LM, Doberstein SK, Pollard TD (1991) Mechanism of the interaction of human platelet profilin with actin. J Cell Biol 113:1081–1089
109. Lodish H, Berk A, Zipursky SL, Matsudaira P, Baltimore D, Darnell J (2000) Molecular cell biology, 4th edn. Section 18.2: the dynamics of actin assembly. W. H. Freeman, New York
110. Ackermann M, Matus A (2003) Activity-induced targeting of profilin and stabilization of dendritic spine morphology. Nat Neurosci 6:1194–1200. doi:10.1038/nn1135nn1135
111. Chesarone MA, DuPage AG, Goode BL (2010) Unleashing formins to remodel the actin and microtubule cytoskeletons. Nat Rev Mol Cell Biol 11:62–74. doi:10.1038/nrm2816
112. Breitsprecher D, Kiesewetter AK, Linkner J, Vinzenz M, Stradal TEB, Small JV, Curth U, Dickinson RB, Faix J (2011) Molecular mechanism of Ena/VASP-mediated actin-filament elongation. EMBO J 30:456–467. doi:10.1038/emboj.2010.348
113. Breitsprecher D, Jaiswal R, Bombardier JP, Gould CJ, Gelles J, Goode BL (2012) Rocket launcher mechanism of collaborative actin assembly defined by single-molecule imaging. Science 336:1164–1168. doi:10.1126/science.1218062
114. Edwards M, Zwolak A, Schafer DA, Sept D, Dominguez R, Cooper JA (2014) Capping protein regulators fine-tune actin assembly dynamics. Nat Rev Mol Cell Biol 15:677–689. doi:10.1038/nrm3869
115. Disanza A, Carlier M-F, Stradal TEB, Didry D, Frittoli E, Confalonieri S, Croce A, Wehland J, Di Fiore PP, Scita G (2004) Eps8 controls actin-based motility by capping the barbed ends of actin filaments. Nat Cell Biol 6:1180–1188. doi:10.1038/ncb1199
116. Fan Y, Tang X, Vitriol E, Chen G, Zheng JQ (2011) Actin capping protein is required for dendritic spine development and synapse formation. J Neurosci 31:10228–10233. doi:10.1523/JNEUROSCI.0115-11.2011
117. 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, Matteoli M (2013) Eps8 controls dendritic spine density and synaptic plasticity through its actin-capping activity. EMBO J 32:1730–1744. doi:10.1038/emboj.2013.107
118. Suarez C, Roland J, Boujemaa-Paterski R, Kang H, McCullough BR, Reymann A-C, Guérin C, Martiel J-L, De la Cruz EM, Blanchoin L (2011) Cofilin tunes the nucleotide state of actin filaments and severs at bare and decorated segment boundaries. Curr Biol 21:862–868. doi:10.1016/j.cub.2011.03.064
119. McCullough BR, Grintsevich EE, Chen CK, Kang H, Hutchison AL, Henn A, Cao W, Suarez C, Martiel J-L, Blanchoin L, Reisler E, De La Cruz EM (2011) Cofilin-linked changes in actin filament flexibility promote severing. Biophys J 101:151–159. doi:10.1016/j.bpj.2011.05.049
120. Jansen S, Collins A, Chin SM, Ydenberg CA, Gelles J, Goode BL (2015) Single-molecule imaging of a three-component ordered actin disassembly mechanism. Nat Commun 6:7202. doi:10.1038/ncomms8202
121. Gressin L, Guillotin A, Guérin C, Blanchoin L, Michelot A (2015) Architecture dependence of actin filament network disassembly. Curr Biol 25:1437–1447. doi:10.1016/j.cub.2015.04.011
122. Meng Y, Zhang Y, Tregoubov V, Janus C, Cruz L, Jackson M, Lu WY, MacDonald JF, Wang JY, Falls DL, Jia Z (2002) Abnormal spine morphology and enhanced LTP in LIMK-1 knockout mice. Neuron 35:121–133. doi:10.1016/S0896-6273(02)00758-4
123. Zhou L, Jones EV, Murai KK (2012) EphA signaling promotes actin-based dendritic spine remodeling through slingshot phosphatase. J Biol Chem 287:9346–9359. doi:10.1074/jbc.M111.302802
124. Scita G, Confalonieri S, Lappalainen P, Suetsugu S (2008) IRSp53: crossing the road of membrane and actin dynamics in the formation of membrane protrusions. Trends Cell Biol 18:52–60. doi:10.1016/j.tcb.2007.12.002
125. Suetsugu S, Gautreau A (2012) Synergistic BAR-NPF interactions in actin-driven membrane remodeling. Trends Cell Biol 22:141–150. doi:10.1016/j.tcb.2012.01.001
126. Bockmann J, Kreutz MR, Gundelfinger ED, Böckers TM (2002) ProSAP/Shank postsynaptic density proteins interact with insulin receptor tyrosine kinase substrate IRSp53. J Neurochem 83:1013–1017
127. Choi J, Ko J, Racz B, Burette A, Lee J-R, Kim S, Na M, Lee HW, Kim K, Weinberg RJ, Kim E (2005) Regulation of dendritic spine morphogenesis by insulin receptor substrate 53, a downstream effector of Rac1 and Cdc42 small GTPases. J Neurosci 25:869–879. doi:10.1523/JNEUROSCI.3212-04.2005
128. Park E, Chi S, Park D (2012) Activity-dependent modulation of the interaction between CaMKIIα and Abi1 and its involvement in spine maturation. J Neurosci 32:13177–13188. doi:10.1523/JNEUROSCI.2257-12.2012
129. Han K, Holder JL, Schaaf CP, Lu H, Chen H, Kang H, Tang J, Wu Z, Hao S, Cheung SW, Yu P, Sun H, Breman AM, Patel A, Lu H-C, Zoghbi HY (2013) SHANK3 overexpression causes manic-like behaviour with unique pharmacogenetic properties. Nature 503:72–77. doi:10.1038/nature12630
130. Chen B, Brinkmann K, Chen Z, Pak CW, Liao Y, Shi S, Henry L, Grishin NV, Bogdan S, Rosen MK (2014) The WAVE regulatory complex links diverse receptors to the actin cytoskeleton. Cell 156:195–207. doi:10.1016/j.cell.2013.11.048
131. Chen XJ, Squarr AJ, Stephan R, Chen B, Higgins TE, Barry DJ, Martin MC, Rosen MK, Bogdan S, Way M (2014) Ena/VASP proteins cooperate with the WAVE complex to regulate the actin cytoskeleton. Dev Cell 30:569–584. doi:10.1016/j.devcel.2014.08.001
132. Yang C, Svitkina T (2011) Filopodia initiation: focus on the Arp2/3 complex and formins. Cell Adh Migr 5(5):402–408. doi: 10.4161/cam.5.5.16971
133. Giannone G, Dubin-Thaler BJ, Döbereiner H-G, Kieffer N, Bresnick AR, Sheetz MP (2004) Periodic lamellipodial contractions correlate with rearward actin waves. Cell 116:431–443
134. Ylänne J, Scheffzek K, Young P, Saraste M (2001) Crystal structure of the alpha-actinin rod reveals an extensive torsional twist. Structure 9:597–604. doi:10.1016/S0969-2126(01)00619-0
135. Nakagawa T, Engler JA, Sheng M (2004) The dynamic turnover and functional roles of α-actinin in dendritic spines. Neuropharmacology 47:734–745. doi:10.1016/j.neuropharm.2004.07.022
136. Hodges JL, Vilchez SM, Asmussen H, Whitmore LA, Horwitz AR (2014) α-actinin-2 mediates spine morphology and assembly of the post-synaptic density in hippocampal neurons. PLoS ONE 9:e101770. doi:10.1371/journal.pone.0101770
137. Allen PB, Ouimet CC, Greengard P (1997) Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc Natl Acad Sci USA 94:9956–9961. doi:10.1073/pnas.94.18.9956
138. Nakanishi H, Obaishi H, Satoh A, Wada M, Mandai K, Satoh K, Nishioka H, Matsuura Y, Mizoguchi A, Takai Y (1997) Neurabin: a novel neural tissue-specific actin filament-binding protein involved in neurite formation. J Cell Biol 139:951–961
139. Satoh A, Nakanishi H, Obaishi H, Wada M, Takahashi K, Satoh K, Hirao K, Nishioka H, Hata Y, Al E (1998) Neurabin-II/spinophilin: an actin filament-binding protein with one PDZ domain localized at cadherin-based cell-cell adhesion sites. J Biol Chem 273:3470–3475. doi:10.1074/jbc.273.6.3470
140. Zito K, Knott G, Shepherd GMG, Shenolikar S, Svoboda K (2004) Induction of spine growth and synapse formation by regulation of the spine actin cytoskeleton. Neuron 44:321–334. doi:10.1016/j.neuron.2004.09.022
141. Sarrouilhe D, di Tommaso A, Métayé T, Ladeveze V (2006) Spinophilin: from partners to functions. Biochimie 88:1099–1113. doi:10.1016/j.biochi.2006.04.010
142. Aoki C, Sekino Y, Hanamura K, Fujisawa S, Mahadomrongkul V, Ren Y, Shirao T (2005) Drebrin A is a postsynaptic protein that localizes in vivo to the submembranous surface of dendritic sites forming excitatory synapses. J Comp Neurol 483:383–402. doi:10.1002/cne.20449
143. Mikati MA, Grintsevich EE, Reisler E (2013) Drebrin-induced stabilization of actin filaments. J Biol Chem 288:19926–19938. doi:10.1074/jbc.M113.472647
144. Worth DC, Daly CN, Geraldo S, Oozeer F, Gordon-Weeks PR (2013) Drebrin contains a cryptic F-actin-bundling activity regulated by Cdk5 phosphorylation. J Cell Biol 202:793–806. doi:10.1083/jcb.201303005
145. Kreis P, Hendricusdottir R, Kay L, Papageorgiou IE, van Diepen M, Mack T, Ryves J, Harwood A, Leslie NR, Kann O, Parsons M, Eickholt BJ (2013) Phosphorylation of the actin binding protein drebrin at S647 is regulated by neuronal activity and PTEN. PLoS ONE 8:1–12. doi:10.1371/journal.pone.0071957
146. Jayo A, Parsons M (2010) Fascin: a key regulator of cytoskeletal dynamics. Int J Biochem Cell Biol 42:1614–1617. doi:10.1016/j.biocel.2010.06.019
147. Breitsprecher D, Koestler SA, Chizhov I, Nemethova M, Mueller J, Goode BL, Small JV, Rottner K, Faix J (2011) Cofilin cooperates with fascin to disassemble filopodial actin filaments. J Cell Sci 124:3305–3318. doi:10.1242/jcs.086934
148. Terry-Lorenzo R, Roadcap D, Otsuka T, Blanpied T, Zamorano P, Garner C, Shenolikar S, Ehlers M (2005) Neurabin/protein phosphatase-1 complex regulates dendritic spine morphogenesis and maturation. Mol Biol Cell 16:2349–2362. doi:10.1091/mbc.E04-12-1054
149. Biou V, Brinkhaus H, Malenka RC, Matus A (2008) Interactions between drebrin and Ras regulate dendritic spine plasticity. Eur J Neurosci 27:2847–2859. doi:10.1111/j.1460-9568.2008.06269.x
150. Wyszynski M, Lin J, Rao A, Nigh E, Beggs AH, Craig AM, Sheng M (1997) Competitive binding of alpha-actinin and calmodulin to the NMDA receptor. Nature 385:439–442. doi:10.1038/385439a0
151. Shirao T, González-Billault C (2013) Actin filaments and microtubules in dendritic spines. J Neurochem 126:155–164. doi:10.1111/jnc.12313
152. Mizui T, Sekino Y, Yamazaki H, Ishizuka Y, Takahashi H, Kojima N, Kojima M, Shirao T (2014) Myosin II ATPase activity mediates the long-term potentiation-induced exodus of stable F-actin bound by drebrin A from dendritic spines. PLoS ONE 9:e85367. doi:10.1371/journal.pone.0085367
153. Okamoto K, Bosch M, Hayashi Y (2009) The roles of CaMKII and F-actin in the structural plasticity of dendritic spines: a potential molecular identity of a synaptic tag? Physiology (Bethesda) 24:357–366. doi:10.1152/physiol.00029.2009
154. Lisman J, Yasuda R, Raghavachari S (2012) Mechanisms of CaMKII action in long-term potentiation. Nat Rev Neurosci 13:169–182. doi:10.1038/nrn3192
155. Hell JW (2014) CaMKII: claiming center stage in postsynaptic function and organization. Neuron 81:249–265. doi:10.1016/j.neuron.2013.12.024
156. Okamoto K-I, Narayanan R, Lee SH, Murata K, Hayashi Y (2007) The role of CaMKII as an F-actin-bundling protein crucial for maintenance of dendritic spine structure. Proc Natl Acad Sci USA 104:6418–6423. doi:10.1073/pnas.0701656104
157. Lin Y-C, Redmond L (2008) CaMKIIbeta binding to stable F-actin in vivo regulates F-actin filament stability. Proc Natl Acad Sci USA 105:15791–15796. doi:10.1073/pnas.0804399105
158. Kim K, Lakhanpal G, Lu HE, Khan M, Suzuki A, Kato Hayashi M, Narayanan R, Luyben TT, Matsuda T, Nagai T, Blanpied TA, Hayashi Y, Okamoto K (2015) A temporary gating of actin remodeling during synaptic plasticity consists of the interplay between the kinase and structural functions of CaMKII. Neuron 87:813–826. doi:10.1016/j.neuron.2015.07.023
159. Lu HE, MacGillavry HD, Frost NA, Blanpied TA (2014) Multiple spatial and kinetic subpopulations of CaMKII in spines and dendrites as resolved by single-molecule tracking PALM. J Neurosci 34:7600–7610. doi:10.1523/JNEUROSCI.4364-13.2014
160. Wilson CA, Tsuchida MA, Allen GM, Barnhart EL, Applegate KT, Yam PT, Ji L, Keren K, Danuser G, Theriot JA (2010) Myosin II contributes to cell-scale actin network treadmilling through network disassembly. Nature 465:373–377. doi:10.1038/nature08994
161. Burnette DT, Manley S, Sengupta P, Sougrat R, Davidson MW, Kachar B, Lippincott-Schwartz J (2011) A role for actin arcs in the leading-edge advance of migrating cells. Nat Cell Biol 13:371–381. doi:10.1038/ncb2205
162. Yang Q, Zhang X-F, Pollard TD, Forscher P (2012) Arp2/3 complex-dependent actin networks constrain myosin II function in driving retrograde actin flow. J Cell Biol 197:939–956. doi:10.1083/jcb.201111052
163. Reymann A-C, Boujemaa-Paterski R, Martiel J-L, Guérin C, Cao W, Chin HF, De La Cruz EM, Théry M, Blanchoin L (2012) Actin network architecture can determine myosin motor activity. Science 336:1310–1314. doi:10.1126/science.1221708
164. Burnette DT, Shao L, Ott C, Pasapera AM, Fischer RS, Baird MA, Der Loughian C, Delanoe-Ayari H, Paszek MJ, Davidson MW, Betzig E, Lippincott-Schwartz J (2014) A contractile and counterbalancing adhesion system controls the 3D shape of crawling cells. J Cell Biol 205:83–96. doi:10.1083/jcb.201311104
165. Zhang H, Webb DJ, Asmussen H, Niu S, Horwitz AF (2005) A GIT1/PIX/Rac/PAK signaling module regulates spine morphogenesis and synapse formation through MLC. J Neurosci 25:3379–3388. doi:10.1523/JNEUROSCI.3553-04.2005
166. Ryu J, Liu L, Wong TP, Wu DC, Burette A, Weinberg R, Wang YT, Sheng M (2006) A critical role for myosin IIb in dendritic spine morphology and synaptic function. Neuron 49:175–182. doi:10.1016/j.neuron.2005.12.017
167. Hodges JL, Newell-Litwa K, Asmussen H, Vicente-Manzanares M, Horwitz AR (2011) Myosin IIb activity and phosphorylation status determines dendritic spine and post-synaptic density morphology. PLoS ONE 6:e24149. doi:10.1371/journal.pone.0024149
168. Rubio MDM, Johnson R, Miller CA, Huganir RL, Rumbaugh G (2011) Regulation of synapse structure and function by distinct myosin II motors. J Neurosci 31:1448–1460. doi:10.1523/JNEUROSCI.3294-10.2011.Regulation
169. Rex CS, Gavin CF, Rubio MD, Kramar EA, Chen LY, Jia Y, Huganir RL, Muzyczka N, Gall CM, Miller CA, Lynch G, Rumbaugh G (2010) Myosin IIb regulates actin dynamics during synaptic plasticity and memory formation. Neuron 67:603–617. doi:10.1016/j.neuron.2010.07.016
170. Koskinen M, Bertling E, Hotulainen R, Tanhuanpää K, Hotulainen P (2014) Myosin IIb controls actin dynamics underlying the dendritic spine maturation. Mol Cell Neurosci 61:56–64. doi:10.1016/j.mcn.2014.05.008
171. Qualmann B, Boeckers TM, Jeromin M, Gundelfinger ED, Kessels MM (2004) Linkage of the actin cytoskeleton to the postsynaptic density via direct interactions of Abp1 with the ProSAP/Shank family. J Neurosci 24:2481–2495. doi:10.1523/JNEUROSCI.5479-03.2004
172. Haeckel A, Ahuja R, Gundelfinger ED, Qualmann B, Kessels MM (2008) The actin-binding protein Abp1 controls dendritic spine morphology and is important for spine head and synapse formation. J Neurosci 28:10031–10044. doi:10.1523/JNEUROSCI.0336-08.2008
173. Vlachos A, Korkotian E, Schonfeld E, Copanaki E, Deller T, Segal M (2009) Synaptopodin regulates plasticity of dendritic spines in hippocampal neurons. J Neurosci 29:1017–1033. doi:10.1523/JNEUROSCI.5528-08.2009
174. Korkotian E, Frotscher M, Segal M (2014) Synaptopodin regulates spine plasticity: mediation by calcium stores. J Neurosci 34:11641–11651. doi:10.1523/JNEUROSCI.0381-14.2014
175. Cueille N, Blanc CT, Popa-Nita S, Kasas S, Catsicas S, Dietler G, Riederer BM (2007) Characterization of MAP1B heavy chain interaction with actin. Brain Res Bull 71:610–618. doi:10.1016/j.brainresbull.2006.12.003
176. Tortosa E, Montenegro-Venegas C, Benoist M, Hartel S, Gonzalez-Billault C, Esteban JA, Avila J (2011) Microtubule-associated protein 1B (MAP1B) is required for dendritic spine development and synaptic maturation. J Biol Chem 286:40638–40648. doi:10.1074/jbc.M111.271320
177. Saneyoshi T, Hayashi Y (2012) The Ca(2+) and Rho GTPase signaling pathways underlying activity-dependent actin remodeling at dendritic spines. Cytoskeleton (Hoboken) 69:545–554. doi:10.1002/cm.21037
178. Lisman JE, Raghavachari S, Tsien RW (2007) The sequence of events that underlie quantal transmission at central glutamatergic synapses. Nat Rev Neurosci 8:597–609. doi:10.1038/nrn2191
179. Hall A (1998) Rho GTPases and the actin cytoskeleton. Science 279(5350):509–514. doi:10.1126/science.279.5350.509
180. Heasman SJ, Ridley AJ (2008) Mammalian Rho GTPases: new insights into their functions from in vivo studies. Nat Rev Mol Cell Biol 9:690–701. doi:10.1038/nrm2476
181. Guilluy C, Garcia-Mata R, Burridge K (2011) Rho protein crosstalk: another social network? Trends Cell Biol 21:718–726. doi:10.1016/j.tcb.2011.08.002
182. Stankiewicz TR, Linseman DA (2014) Rho family GTPases: key players in neuronal development, neuronal survival, and neurodegeneration. Front Cell Neurosci 8:314. doi:10.3389/fncel.2014.00314
183. Fleming IN, Elliott CM, Buchanan FG, Downes CP, Exton JH (1999) Ca2+/calmodulin-dependent protein kinase II regulates Tiam1 by reversible protein phosphorylation. J Biol Chem 274:12753–12758. doi:10.1074/jbc.274.18.12753
184. Okabe T, Nakamura T, Nishimura YN, Kohu K, Ohwada S, Morishita Y, Akiyama T (2003) RICS, a novel GTPase-activating protein for Cdc42 and Rac1, is involved in the beta-catenin-N-cadherin and N-methyl-d-aspartate receptor signaling. J Biol Chem 278:9920–9927. doi:10.1074/jbc.M208872200
185. Tolias KF, Bikoff JB, Burette A, Paradis S, Harrar D, Tavazoie S, Weinberg RJ, Greenberg ME (2005) The Rac1-GEF Tiam1 couples the NMDA receptor to the activity-dependent development of dendritic arbors and spines. Neuron 45:525–538. doi:10.1016/j.neuron.2005.01.024
186. Xie Z, Srivastava DP, Photowala H, Kai L, Cahill ME, Woolfrey KM, Shum CY, Surmeier DJ, Penzes P (2007) Kalirin-7 controls activity-dependent structural and functional plasticity of dendritic spines. Neuron 56:640–656. doi:10.1016/j.neuron.2007.10.005
187. Grossman SD, Futter M, Snyder GL, Allen PB, Nairn AC, Greengard P, Hsieh-Wilson LC (2004) Spinophilin is phosphorylated by Ca2+/calmodulin-dependent protein kinase II resulting in regulation of its binding to F-actin. J Neurochem 90:317–324. doi:10.1111/j.1471-4159.2004.02491.x
188. Ryan XP, Alldritt J, Svenningsson P, Allen PB, Wu G-Y, Nairn AC, Greengard P (2005) The Rho-specific GEF Lfc interacts with neurabin and spinophilin to regulate dendritic spine morphology. Neuron 47:85–100. doi:10.1016/j.neuron.2005.05.013
189. Murakoshi H, Wang H, Yasuda R (2011) Local, persistent activation of Rho GTPases during plasticity of single dendritic spines. Nature 472:100–104. doi:10.1038/nature09823
190. Saneyoshi T, Wayman G, Fortin D, Davare M, Hoshi N, Nozaki N, Natsume T, Soderling TR (2008) Activity-dependent synaptogenesis: regulation by a CaM-kinase kinase/CaM-kinase I/betaPIX signaling complex. Neuron 57:94–107. doi:10.1016/j.neuron.2007.11.016
191. Wayman GA, Lee Y-S, Tokumitsu H, Silva AJ, Silva A, Soderling TR (2008) Calmodulin-kinases: modulators of neuronal development and plasticity. Neuron 59:914–931. doi:10.1016/j.neuron.2008.08.021
192. Takenawa T, Suetsugu S (2007) The WASP-WAVE protein network: connecting the membrane to the cytoskeleton. Nat Rev Mol Cell Biol 8:37–48. doi:10.1038/nrm2069
193. Derivery E, Gautreau A (2010) Generation of branched actin networks: assembly and regulation of the N-WASP and WAVE molecular machines. BioEssays 32:119–131. doi:10.1002/bies.200900123
194. Chen Z, Borek D, Padrick SB, Gomez TS, Metlagel Z, Ismail AM, Umetani J, Billadeau DD, Otwinowski Z, Rosen MK (2010) Structure and control of the actin regulatory WAVE complex. Nature 468:533–538. doi:10.1038/nature09623
195. Riento K, Ridley AJ (2003) Rocks: multifunctional kinases in cell behaviour. Nat Rev Mol Cell Biol 4:446–456. doi:10.1038/nrm1128
196. Rane CK, Minden A (2014) P21 activated kinases: structure, regulation, and functions. Small GTPases 5:37–41. doi:10.4161/sgtp.28003
197. Julian L, Olson MF (2014) Rho-associated coiled-coil containing kinases (ROCK): structure, regulation, and functions. Small GTPases 5:e29846. doi:10.4161/sgtp.29846
198. Niwa R, Nagata-Ohashi K, Takeichi M, Mizuno K, Uemura T (2002) Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108:233–246
199. Collingridge GL, Peineau S, Howland JG, Wang YT (2010) Long-term depression in the CNS. Nat Rev Neurosci 11:459–473. doi:10.1038/nrn2867
200. Hanley JG, Henley JM (2005) PICK1 is a calcium-sensor for NMDA-induced AMPA receptor trafficking. EMBO J 24:3266–3278. doi:10.1038/sj.emboj.7600801
201. Rocca DL, Amici M, Antoniou A, Blanco Suarez E, Halemani N, Murk K, McGarvey J, Jaafari N, Mellor JR, Collingridge GL, Hanley JG (2013) The small GTPase Arf1 modulates Arp2/3-mediated actin polymerization via PICK1 to regulate synaptic plasticity. Neuron 79:293–307. doi:10.1016/j.neuron.2013.05.003
202. Rocca DL, Hanley JG (2015) PICK1 links AMPA receptor stimulation to Cdc42. Neurosci Lett 585:155–159. doi:10.1016/j.neulet.2014.11.046
203. Machacek M, Hodgson L, Welch C, Elliott H, Pertz O, Nalbant P, Abell A, Johnson GL, Hahn KM, Danuser G (2009) Coordination of Rho GTPase activities during cell protrusion. Nature 461:99–103. doi:10.1038/nature08242
204. Wu YI, Frey D, Lungu OI, Jaehrig A, Schlichting I, Kuhlman B, Hahn KM (2009) A genetically encoded photoactivatable Rac controls the motility of living cells. Nature 461:104–108. doi:10.1038/nature08241
205. Lee SR, Escobedo-Lozoya Y, Szatmari EM, Yasuda R (2009) Activation of CaMKII in single dendritic spines during long-term potentiation. Nature 458:299–304. doi:10.1038/nature07842
206. Van Harreveld A, 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. doi:10.1016/0014-4886(75)90055-2
207. Fifková E, Anderson CL (1981) Stimulation-induced changes in dimensions of stalks of dendritic spines in the dentate molecular layer. Exp Neurol 74:621–627. doi:10.1016/0014-4886(81)90197-7
208. Desmond N, Levy W (1986) Changes in the postsynaptic density with long-term potentiation in the dentate gyrus. J Comp Neurol 253:476–482. doi:10.1002/cne.902530405
209. Matsuzaki M, Ellis-Davies GC, Nemoto T, Miyashita Y, Iino M, Kasai H (2001) Dendritic spine geometry is critical for AMPA receptor expression in hippocampal CA1 pyramidal neurons. Nat Neurosci 4:1086–1092. doi:10.1038/nn736
210. Patterson MA, Szatmari EM, Yasuda R (2010) AMPA receptors are exocytosed in stimulated spines and adjacent dendrites in a Ras-ERK-dependent manner during long-term potentiation. Proc Natl Acad Sci USA 107:15951–15956. doi:10.1073/pnas.0913875107
211. Fukazawa Y, Saitoh Y, Ozawa F, Ohta Y, Mizuno K, 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
212. Rochefort NL, Konnerth A (2012) Dendritic spines: from structure to in vivo function. EMBO Rep 13:699–708. doi:10.1038/embor.2012.102
213. Yamagata Y, Kobayashi S, Umeda T, Inoue A, Sakagami H, Fukaya M, Watanabe M, Hatanaka N, Totsuka M, Yagi T, Obata K, Imoto K, Yanagawa Y, Manabe T, Okabe S (2009) Kinase-dead knock-in mouse reveals an essential role of kinase activity of Ca2+/calmodulin-dependent protein kinase IIalpha in dendritic spine enlargement, long-term potentiation, and learning. J Neurosci 29:7607–7618. doi:10.1523/JNEUROSCI.0707-09.2009
214. Chen LY, Rex CS, Casale MS, Gall CM, Lynch G (2007) Changes in synaptic morphology accompany actin signaling during LTP. J Neurosci 27:5363–5372. doi:10.1523/JNEUROSCI.0164-07.2007
215. Ghosh M, Song X, Mouneimne G, Sidani M, Lawrence DS, Condeelis JS (2004) Cofilin promotes actin polymerization and defines the direction of cell motility. Science 304:743–746. doi:10.1126/science.1094561
216. Durand CM, Perroy J, Loll F, Perrais D, Fagni L, Bourgeron T, Montcouquiol M, Sans N (2012) SHANK3 mutations identified in autism lead to modification of dendritic spine morphology via an actin-dependent mechanism. Mol Psychiatry 17:71–84. doi:10.1038/mp.2011.57
217. Andrianantoandro E, Pollard TD (2006) Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol Cell 24:13–23. doi:10.1016/j.molcel.2006.08.006
218. Merriam EB, Millette M, Lumbard DC, Saengsawang W, Fothergill T, Hu X, Ferhat L, Dent EW (2013) Synaptic regulation of microtubule dynamics in dendritic spines by calcium, F-actin, and drebrin. J Neurosci 33:16471–16482. doi:10.1523/JNEUROSCI.0661-13.2013
219. Yang Y, Wang X-B, Frerking M, Zhou Q (2008) Spine expansion and stabilization associated with long-term potentiation. J Neurosci 28:5740–5751. doi:10.1523/JNEUROSCI.3998-07.2008
220. Fortin DA, Davare MA, Srivastava T, Brady JD, Nygaard S, Derkach VA, Soderling TR (2010) Long-term potentiation-dependent spine enlargement requires synaptic Ca2+-permeable AMPA receptors recruited by CaM-kinase I. J Neurosci 30:11565–11575. doi:10.1523/JNEUROSCI.1746-10.2010
221. Tai C-Y, Mysore SP, Chiu C, Schuman EM (2007) Activity-regulated N-cadherin endocytosis. Neuron 54:771–785. doi:10.1016/j.neuron.2007.05.013
222. Kobielak A, Pasolli HA, Fuchs E (2004) Mammalian formin-1 participates in adherens junctions and polymerization of linear actin cables. Nat Cell Biol 6:21–30. doi:10.1038/ncb1075
223. Okamura K, Tanaka H, Yagita Y, Saeki Y, Taguchi A, Hiraoka Y, Zeng L-H, Colman DR, Miki N (2004) Cadherin activity is required for activity-induced spine remodeling. J Cell Biol 167:961–972. doi:10.1083/jcb.200406030
224. Wang X, Yang Y, Zhou Q (2007) Independent expression of synaptic and morphological plasticity associated with long-term depression. J Neurosci 27:12419–12429. doi:10.1523/JNEUROSCI.2015-07.2007
225. He K, Lee A, Song L, Kanold PO, Lee H-K (2011) AMPA receptor subunit GluR1 (GluA1) serine-845 site is involved in synaptic depression but not in spine shrinkage associated with chemical long-term depression. J Neurophysiol 105:1897–1907. doi:10.1152/jn.00913.2010
226. Hayama T, Noguchi J, Watanabe S, Takahashi N, Hayashi-Takagi A, Ellis-Davies GCR, Matsuzaki M, Kasai H (2013) GABA promotes the competitive selection of dendritic spines by controlling local Ca2+ signaling. Nat Neurosci 16:1409–1416. doi:10.1038/nn.3496
227. Kopec CD, Li B, Wei W, Boehm J, Malinow R (2006) Glutamate receptor exocytosis and spine enlargement during chemically induced long-term potentiation. J Neurosci 26:2000–2009. doi:10.1523/JNEUROSCI.3918-05.2006
228. Kopec CD, Real E, Kessels HW, Malinow R (2007) GluR1 links structural and functional plasticity at excitatory synapses. J Neurosci 27:13706–13718. doi:10.1523/JNEUROSCI.3503-07.2007
229. Sdrulla AD, Linden DJ (2007) Double dissociation between long-term depression and dendritic spine morphology in cerebellar Purkinje cells. Nat Neurosci 10:546–548. doi:10.1038/nn1889
230. Gu J, Lee CW, Fan Y, Komlos D, Tang X, Sun C, Yu K, Hartzell HC, Chen G, Bamburg JR, Zheng JQ (2010) ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat Neurosci 13:1208–1215. doi:10.1038/nn.2634
231. Kim CH, Lisman JE (1999) A role of actin filament in synaptic transmission and long-term potentiation. J Neurosci 19:4314–4324
232. Krucker T, Siggins GR, Halpain S (2000) Dynamic actin filaments are required for stable long-term potentiation (LTP) in area CA1 of the hippocampus. Proc Natl Acad Sci USA 97:6856–6861. doi:10.1073/pnas.100139797
233. Ramachandran B, Frey JU (2009) Interfering with the actin network and its effect on long-term potentiation and synaptic tagging in hippocampal CA1 neurons in slices in vitro. J Neurosci 29:12167–12173. doi:10.1523/JNEUROSCI.2045-09.2009
234. Soderling SH, Langeberg LK, Soderling JA, Davee SM, Simerly R, Raber J, Scott JD (2003) Loss of WAVE-1 causes sensorimotor retardation and reduced learning and memory in mice. Proc Natl Acad Sci USA 100:1723–1728. doi:10.1073/pnas.0438033100
235. Meng J, Meng Y, Hanna A, Janus C, Jia Z (2005) Abnormal long-lasting synaptic plasticity and cognition in mice lacking the mental retardation gene Pak3. J Neurosci 25:6641–6650. doi:10.1523/JNEUROSCI.0028-05.2005
236. Asrar S, Meng Y, Zhou Z, Todorovski Z, Huang WW, Jia Z (2009) Regulation of hippocampal long-term potentiation by p21-activated protein kinase 1 (PAK1). Neuropharmacology 56:73–80. doi:10.1016/j.neuropharm.2008.06.055
237. Haditsch U, Leone DP, Farinelli M, Chrostek-Grashoff A, Brakebusch C, Mansuy IM, McConnell SK, Palmer TD (2009) A central role for the small GTPase Rac1 in hippocampal plasticity and spatial learning and memory. Mol Cell Neurosci 41:409–419. doi:10.1016/j.mcn.2009.04.005
238. Rust MB, Gurniak CB, Renner M, Vara H, Morando L, Görlich A, Sassoè-Pognetto M, Al Banchaabouchi M, Giustetto M, Triller A, Choquet D, Witke W (2010) Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBO J 29:1889–1902. doi:10.1038/emboj.2010.72
239. Kang J, Park H, Kim E (2016) IRSp53/BAIAP2 in dendritic spine development, NMDA receptor regulation, and psychiatric disorders. Neuropharmacology 100:27–39. doi:10.1016/j.neuropharm.2015.06.019
240. Schenck A, Bardoni B, Langmann C, Harden N, Mandel JL, Giangrande A (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38:887–898
241. Penzes P, Cahill ME, Jones KA, VanLeeuwen J-E, Woolfrey KM (2011) Dendritic spine pathology in neuropsychiatric disorders. Nat Neurosci 14:285–293. doi:10.1038/nn.2741
242. De Rubeis S, Pasciuto E, Li KW, Fernández E, Di Marino D, Buzzi A, Ostroff LE, Klann E, Zwartkruis FJT, Komiyama NH, Grant SGN, Poujol C, Choquet D, Achsel T, Posthuma D, Smit AB, Bagni C (2013) CYFIP1 coordinates mRNA translation and cytoskeleton remodeling to ensure proper dendritic spine formation. Neuron 79:1169–1182. doi:10.1016/j.neuron.2013.06.039
243. Derkach VA, Oh MC, Guire ES, Soderling TR (2007) Regulatory mechanisms of AMPA receptors in synaptic plasticity. Nat Rev Neurosci 8:101–113. doi:10.1038/nrn2055
244. Lau CG, Takeuchi K, Rodenas-Ruano A, Takayasu Y, Murphy J, Bennett MVL, Zukin RS (2009) Regulation of NMDA receptor Ca2+ signalling and synaptic plasticity. Biochem Soc Trans 37:1369–1374. doi:10.1042/BST0371369
245. Lau CG, Zukin RS (2007) NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 8:413–426. doi:10.1038/nrn2153
246. Anggono V, Huganir RL (2012) Regulation of AMPA receptor trafficking and synaptic plasticity. Curr Opin Neurobiol 22:461–469. doi:10.1016/j.conb.2011.12.006
247. Opazo P, Sainlos M, Choquet D (2012) Regulation of AMPA receptor surface diffusion by PSD-95 slots. Curr Opin Neurobiol 22:453–460. doi:10.1016/j.conb.2011.10.010
248. Ladépêche L, Dupuis JP, Groc L (2014) Surface trafficking of NMDA receptors: gathering from a partner to another. Semin Cell Dev Biol 27:3–13. doi:10.1016/j.semcdb.2013.10.005
249. Hanley JG (2014) Actin-dependent mechanisms in AMPA receptor trafficking. Front Cell Neurosci 8:1–8. doi:10.3389/fncel.2014.00381
250. Soltau M, Richter D, Kreienkamp H (2002) The insulin receptor substrate IRSp53 links postsynaptic shank1 to the small G-protein cdc42. Mol Cell Neurosci 21:575–583. doi:10.1006/mcne.2002.1201
251. Park E, Na M, Choi J, Kim S, Lee J-R, Yoon J, Park D, Sheng M, Kim E (2003) The Shank family of postsynaptic density proteins interacts with and promotes synaptic accumulation of the beta PIX guanine nucleotide exchange factor for Rac1 and Cdc42. J Biol Chem 278:19220–19229. doi:10.1074/jbc.M301052200
252. Soltau M, Berhörster K, Kindler S, Buck F, Richter D, Kreienkamp H-J (2004) Insulin receptor substrate of 53 kDa links postsynaptic shank to PSD-95. J Neurochem 90:659–665. doi:10.1111/j.1471-4159.2004.02523.x
253. Kuriu T, Inoue A, Bito H, Sobue K, Okabe S (2006) Differential control of postsynaptic density scaffolds via actin-dependent and -independent mechanisms. J Neurosci 26:7693–7706. doi:10.1523/JNEUROSCI.0522-06.2006
254. Kerr JM, Blanpied TA (2012) Subsynaptic AMPA receptor distribution is acutely regulated by actin-driven reorganization of the postsynaptic density. J Neurosci 32:658–673. doi:10.1523/JNEUROSCI.2927-11.2012
255. MacGillavry HD, Song Y, Raghavachari S, Blanpied TA (2013) Nanoscale scaffolding domains within the postsynaptic density concentrate synaptic AMPA receptors. Neuron 78:615–622. doi:10.1016/j.neuron.2013.03.009
256. Zhang W, Benson DL (2001) Stages of synapse development defined by dependence on F-actin. J Neurosci 21:5169–5181
257. Allison DW, Gelfand VI, Spector I, Craig AM (1998) Role of actin in anchoring postsynaptic receptors in cultured hippocampal neurons: differential attachment of NMDA versus AMPA receptors. J Neurosci 18:2423–2436
258. Renner M, Choquet D, Triller A (2009) Control of the postsynaptic membrane viscosity. J Neurosci 29:2926–2937. doi:10.1523/JNEUROSCI.4445-08.2009
259. Czondor K, Mondin M, Garcia M, Heine M, Frischknecht R, Choquet D, Sibarita J-B, Thoumine OR (2012) Unified quantitative model of AMPA receptor trafficking at synapses. Proc Natl Acad Sci USA 109:3522–3527. doi:10.1073/pnas.1109818109
260. Kusters R, Kapitein LC, Hoogenraad CC, Storm C (2013) Shape-induced asymmetric diffusion in dendritic spines allows efficient synaptic AMPA receptor trapping. Biophys J 105:2743–2750. doi:10.1016/j.bpj.2013.11.016
261. Jewell JL, Luo W, Oh E, Wang Z, Thurmond DC (2008) Filamentous actin regulates insulin exocytosis through direct interaction with Syntaxin 4. J Biol Chem 283:10716–10726. doi:10.1074/jbc.M709876200
262. Jaiswal JK, Rivera VM, Simon SM (2009) Exocytosis of post-golgi vesicles is regulated by components of the endocytic machinery. Cell 137:1308–1319. doi:10.1016/j.cell.2009.04.064
263. Yang Y, Wang X-B, Frerking M, Zhou Q (2008) Delivery of AMPA receptors to perisynaptic sites precedes the full expression of long-term potentiation. Proc Natl Acad Sci USA 105:11388–11393. doi:10.1073/pnas.0802978105
264. Porat-Shliom N, Milberg O, Masedunskas A, Weigert R (2013) Multiple roles for the actin cytoskeleton during regulated exocytosis. Cell Mol Life Sci 70:2099–2121. doi:10.1007/s00018-012-1156-5
265. Mooren OL, Galletta BJ, Cooper JA (2012) Roles for actin assembly in endocytosis. Annu Rev Biochem 81:661–686. doi:10.1146/annurev-biochem-060910-094416
266. Kennedy MJ, Davison IG, Robinson CG, Ehlers MD (2010) Syntaxin-4 defines a domain for activity-dependent exocytosis in dendritic spines. Cell 141:524–535. doi:10.1016/j.cell.2010.02.042
267. Jullie D, Choquet D, Perrais D (2014) Recycling endosomes undergo rapid closure of a fusion pore on exocytosis in neuronal dendrites. J Neurosci 34:11106–11118. doi:10.1523/JNEUROSCI.0799-14.2014
268. Terashima A, Pelkey KA, Rah JC, Suh YH, Roche KW, Collingridge GL, McBain CJ, Isaac JTR (2008) An essential role for PICK1 in NMDA receptor-dependent bidirectional synaptic plasticity. Neuron 57:872–882. doi:10.1016/j.neuron.2008.01.028
269. Kelly EE, Horgan CP, McCaffrey MW, Young P (2011) The role of endosomal-recycling in long-term potentiation. Cell Mol Life Sci 68:185–194. doi:10.1007/s00018-010-0516-2
270. Osterweil E, Wells DG, Mooseker MS (2005) A role for myosin VI in postsynaptic structure and glutamate receptor endocytosis. J Cell Biol 168:329–338. doi:10.1083/jcb.200410091
271. Wang Z, Edwards JG, Riley N, Provance DW, Karcher R, Li X-D, Davison IG, Ikebe M, Mercer JA, Kauer JA, Ehlers MD (2008) Myosin Vb mobilizes recycling endosomes and AMPA receptors for postsynaptic plasticity. Cell 135:535–548. doi:10.1016/j.cell.2008.09.057
272. Huber K, Kayser M, Bear M (2000) Role for rapid dendritic protein synthesis in hippocampal mGluR-dependent long-term depression. Science 288(5469):1254–1257. doi:10.1126/science.288.5469.1254
273. Nosyreva E, Huber K (2005) Developmental Switch in synaptic mechanisms of hippocampal metabotropic glutamate receptor-dependent long-term depression. J Neurosci 25:2992–3001. doi:10.1523/JNEUROSCI.3652-04.2005
274. Tanaka J-I, Horiike Y, Matsuzaki M, Miyazaki T, Ellis-Davies GCR, Kasai H (2008) Protein synthesis and neurotrophin-dependent structural plasticity of single dendritic spines. Science 319:1683–1687. doi:10.1126/science.1152864
275. Holbro N, Grunditz Å, Oertner TG (2009) Differential distribution of endoplasmic reticulum controls metabotropic signaling and plasticity at hippocampal synapses. Proc Natl Acad Sci USA 106:15055–15060. doi:10.1073/pnas.0905110106
276. Govindarajan A, Israely I, Huang S-Y, Tonegawa S (2011) The dendritic branch is the preferred integrative unit for protein synthesis-dependent LTP. Neuron 69:132–146. doi:10.1016/j.neuron.2010.12.008
277. Ramiro-Cortés Y, Israely I (2013) Long lasting protein synthesis- and activity-dependent spine shrinkage and elimination after synaptic depression. PLoS ONE 8:e71155. doi:10.1371/journal.pone.0071155
278. Lynch G, Kramár EA, Babayan AH, Rumbaugh G, Gall CM (2013) Differences between synaptic plasticity thresholds result in new timing rules for maximizing long-term potentiation. Neuropharmacology 64:27–36. doi:10.1016/j.neuropharm.2012.07.006
279. Redondo RL, Okuno H, Spooner PA, Frenguelli BG, Bito H, Morris RGM (2010) Synaptic tagging and capture: differential role of distinct calcium/calmodulin kinases in protein synthesis-dependent long-term potentiation. J Neurosci 30:4981–4989. doi:10.1523/JNEUROSCI.3140-09.2010
280. Redondo RL, Morris RGM (2011) Making memories last: the synaptic tagging and capture hypothesis. Nat Rev Neurosci 12:17–30. doi:10.1038/nrn2963
281. Tam J, Cordier GA, Bálint Š, Sandoval Álvarez Á, Borbely JS, Lakadamyali M (2014) A microfluidic platform for correlative live-cell and super-resolution microscopy. PLoS ONE 9:e115512. doi:10.1371/journal.pone.0115512
282. Jungmann R, Steinhauer C, Scheible M, Kuzyk A, Tinnefeld P, Simmel FC (2010) Single-molecule kinetics and super-resolution microscopy by fluorescence imaging of transient binding on DNA origami. Nano Lett 10:4756–4761. doi:10.1021/nl103427w
283. Jungmann R, Avendaño MS, Woehrstein JB, Dai M, Shih WM, Yin P (2014) Multiplexed 3D cellular super-resolution imaging with DNA-PAINT and Exchange-PAINT. Nat Methods 11:313–318. doi:10.1038/nmeth.2835
284. Tam J, Cordier GA, Borbely JS, Sandoval Álvarez Á, Lakadamyali M (2014) Cross-talk-free multi-color STORM imaging using a single fluorophore. PLoS ONE 9:e101772. doi:10.1371/journal.pone.0101772
285. Zhang Z, Kenny SJ, Hauser M, Li W, Xu K (2015) Ultrahigh-throughput resolved super-resolution microscopy. Nat Methods. doi:10.1038/nmeth.3528
286. Meyer D, Bonhoeffer T, Scheuss V (2014) Balance and stability of synaptic structures during synaptic plasticity. Neuron 82:430–443. doi:10.1016/j.neuron.2014.02.031
287. Xu K, Babcock HP, Zhuang X (2012) Dual-objective STORM reveals three-dimensional filament organization in the actin cytoskeleton. Nat Methods 9:185–188. doi:10.1038/nmeth.1841
288. Galland R, Grenci G, Aravind A, Viasnoff V, Studer V, Sibarita J-B (2015) 3D high- and super-resolution imaging using single-objective SPIM. Nat Methods 12:641–644. doi:10.1038/nmeth.3402
289. Dani A, Huang B, Bergan J, Dulac C, Zhuang X (2010) Superresolution imaging of chemical synapses in the brain. Neuron 68:843–856. doi:10.1016/j.neuron.2010.11.021
290. Vangindertael J, Beets I, Rocha S, Dedecker P, Schoofs L, Vanhoorelbeeke K, Hofkens J, Mizuno H (2015) Super-resolution mapping of glutamate receptors in C. elegans by confocal correlated PALM. Sci Rep 5:13532. doi:10.1038/srep13532
291. Urban NT, Willig KI, Hell SW, Nägerl UV (2011) STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys J 101:1277–1284. doi:10.1016/j.bpj.2011.07.027
292. Hofmann M, Eggeling C, Jakobs S, Hell SW (2005) Breaking the diffraction barrier in fluorescence microscopy at low light intensities by using reversibly photoswitchable proteins. Proc Natl Acad Sci USA 102:17565–17569. doi:10.1073/pnas.0506010102
293. Testa I, Urban NT, Jakobs S, Eggeling C, Willig KI, Hell SW (2012) Nanoscopy of living brain slices with low light levels. Neuron 75:992–1000. doi:10.1016/j.neuron.2012.07.028
294. Kner P, Chhun BB, Griffis ER, Winoto L, Gustafsson MGL (2009) Super-resolution video microscopy of live cells by structured illumination. Nat Methods 6:339–342. doi:10.1038/nmeth.1324
295. Shao L, Kner P, Rego EH, Gustafsson MGL (2011) Super-resolution 3D microscopy of live whole cells using structured illumination. Nat Methods 8:1044–1046. doi:10.1038/nmeth.1734
296. Ahrens MB, Orger MB, Robson DN, Li JM, Keller PJ (2013) Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat Methods 10:413–420. doi:10.1038/nmeth.2434
297. Chen B-C, Legant WR, Wang K, Shao L, Milkie DE, Davidson MW, Janetopoulos C, Wu XS, Hammer JA 3rd, Liu Z, English BP, Mimori-Kiyosue Y, Romero DP, Ritter AT, Lippincott-Schwartz J, Fritz-Laylin L, Mullins RD, Mitchell DM, Reymann A-C, Bembenek JN, Bohme R, Grill SW, Wang JT, Seydoux G, Tulu US, Kiehart DP, Betzig E, Reymann A-C, Bohme R, Grill SW, Wang JT, Seydoux G, Tulu US, Kiehart DP, Betzig E (2014) Lattice light-sheet microscopy: Imaging molecules to embryos at high spatiotemporal resolution. Science 346(6208):1257998. doi:10.1126/science.1257998
298. Li D, Shao L, Chen B, Zhang X, Zhang M, Moses B, Milkie DE, Beach JR, Hammer J 3rd, Pasham M, Kirchhausen T, Baird MA, Davidson MW, Xu P, Betzig E (2015) ADVANCED IMAGING. Extended-resolution structured illumination imaging of endocytic and cytoskeletal dynamics. Science 349(6251):aab3500. doi:10.1126/science.aab3500
299. Keller PJ, Ahrens MB (2015) Visualizing whole-brain activity and development at the single-cell level using light-sheet microscopy. Neuron 85:462–483. doi:10.1016/j.neuron.2014.12.039
300. Benson DL, Huntley GW (2012) Synapse adhesion: a dynamic equilibrium conferring stability and flexibility. Curr Opin Neurobiol 22:397–404. doi:10.1016/j.conb.2011.09.011
301. van Bergeijk P, Adrian M, Hoogenraad CC, Kapitein LC (2015) Optogenetic control of organelle transport and positioning. Nature 518:111–114. doi:10.1038/nature14128
302. Taslimi A, Vrana JD, Chen D, Borinskaya S, Mayer BJ, Kennedy MJ, Tucker CL (2014) An optimized optogenetic clustering tool for probing protein interaction and function. Nat Commun 5:4925. doi:10.1038/ncomms5925
303. Yuste R (2015) From the neuron doctrine to neural networks. Nat Rev Neurosci 16:487–497. doi:10.1038/nrn3962
304. Markram H, Muller E, Ramaswamy S, Reimann MW, Abdellah M, Sanchez CA, Ailamaki A, Alonso-Nanclares L, Antille N, Arsever S, Kahou GAA, Berger TK, Bilgili A, Buncic N, Chalimourda A, Chindemi G, Courcol J-D, Delalondre F, Delattre V, Druckmann S, Dumusc R, Dynes J, Eilemann S, Gal E, Gevaert ME, Ghobril J-P, Gidon A, Graham JW, Gupta A, Haenel V, Hay E, Heinis T, Hernando JB, Hines M, Kanari L, Keller D, Kenyon J, Khazen G, Kim Y, King JG, Kisvarday Z, Kumbhar P, Lasserre S, Le Bé J-V, Magalhães BRC, Merchán-Pérez A, Meystre J, Morrice BR, Muller J, Muñoz-Céspedes A, Muralidhar S, Muthurasa K, Nachbaur D, Newton TH, Nolte M, Ovcharenko A, Palacios J, Pastor L, Perin R, Ranjan R, Riachi I, Rodríguez J-R, Riquelme JL, Rössert C, Sfyrakis K, Shi Y, Shillcock JC, Silberberg G, Silva R, Tauheed F, Telefont M, Toledo-Rodriguez M, Tränkler T, Van Geit W, Díaz JV, Walker R, Wang Y, Zaninetta SM, DeFelipe J, Hill SL, Segev I, Schürmann F (2015) Reconstruction and simulation of neocortical microcircuitry. Cell 163:456–492. doi:10.1016/j.cell.2015.09.029