Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy

Lorenzo A. Cingolani; Yukiko Goda

doi:10.1038/nrn2373

journal article May 01, 2008

Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy

Lorenzo A. Cingolani Yukiko Goda

Nature Reviews Neuroscience Vol. 9 No. 5 pp. 344-356 · Springer Science and Business Media LLC

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References

149

[1]

Landis, D. M., Hall, A. K., Weinstein, L. A. & Reese, T. S. The organization of cytoplasm at the presynaptic active zone of a central nervous system synapse. Neuron 1, 201–209 (1988). 10.1016/0896-6273(88)90140-7

[2]

Hirokawa, N., Sobue, K., Kanda, K., Harada, A. & Yorifuji, H. The cytoskeletal architecture of the presynaptic terminal and molecular structure of synapsin 1. J. Cell Biol. 108, 111–126 (1989). 10.1083/jcb.108.1.111

[3]

Bloom, O. et al. Colocalization of synapsin and actin during synaptic vesicle recycling. J. Cell Biol. 161, 737–747 (2003). 10.1083/jcb.200212140

[4]

Fifkova, E. & Delay, R. J. Cytoplasmic actin in neuronal processes as a possible mediator of synaptic plasticity. J. Cell Biol. 95, 345–350 (1982). 10.1083/jcb.95.1.345

[5]

Matus, A., Ackermann, M., Pehling, G., Byers, H. R. & Fujiwara, K. High actin concentrations in brain dendritic spines and postsynaptic densities. Proc. Natl Acad. Sci. USA 79, 7590–7594 (1982). 10.1073/pnas.79.23.7590

[6]

Matus, A. Actin-based plasticity in dendritic spines. Science 290, 754–758 (2000). 10.1126/science.290.5492.754

[7]

Capani, F., Martone, M. E., Deerinck, T. J. & Ellisman, M. H. Selective localization of high concentrations of F-actin in subpopulations of dendritic spines in rat central nervous system: a three-dimensional electron microscopic study. J. Comp. Neurol. 435, 156–170 (2001). 10.1002/cne.1199

[8]

Yuste, R. & Bonhoeffer, T. Genesis of dendritic spines: insights from ultrastructural and imaging studies. Nature Rev. Neurosci. 5, 24–34 (2004). 10.1038/nrn1300

[9]

Short-Term Synaptic Plasticity

Robert S. Zucker, Wade G. Regehr

Annual Review of Physiology 2002 10.1146/annurev.physiol.64.092501.114547

[10]

Silberberg, G., Grillner, S., LeBeau, F. E., Maex, R. & Markram, H. Synaptic pathways in neural microcircuits. Trends Neurosci. 28, 541–551 (2005). 10.1016/j.tins.2005.08.004

[11]

Kim, S. J. & Linden, D. J. Ubiquitous plasticity and memory storage. Neuron 56, 582–592 (2007). 10.1016/j.neuron.2007.10.030

[12]

Neves, G., Cooke, S. F. & Bliss, T. V. Synaptic plasticity, memory and the hippocampus: a neural network approach to causality. Nature Rev. Neurosci. 9, 65–75 (2008). 10.1038/nrn2303

[13]

Dillon, C. & Goda, Y. The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28, 25–55 (2005). 10.1146/annurev.neuro.28.061604.135757

[14]

Carlisle, H. J. & Kennedy, M. B. Spine architecture and synaptic plasticity. Trends Neurosci. 28, 182–187 (2005). 10.1016/j.tins.2005.01.008

[15]

Actin Binding Proteins: Regulation of Cytoskeletal Microfilaments

C. G. Dos Remedios, D. Chhabra, M. Kekic et al.

Physiological Reviews 2003 10.1152/physrev.00026.2002

[16]

Cellular Motility Driven by Assembly and Disassembly of Actin Filaments

Thomas D Pollard, Gary G Borisy

Cell 2003 10.1016/s0092-8674(03)00120-x

[17]

Revenu, C., Athman, R., Robine, S. & Louvard, D. The co-workers of actin filaments: from cell structures to signals. Nature Rev. Mol. Cell Biol. 5, 635–646 (2004). 10.1038/nrm1437

[18]

Ethell, I. M. & Pasquale, E. B. Molecular mechanisms of dendritic spine development and remodeling. Prog. Neurobiol. 75, 161–205 (2005). 10.1016/j.pneurobio.2005.02.003

[19]

Tada, T. & Sheng, M. Molecular mechanisms of dendritic spine morphogenesis. Curr. Opin. Neurobiol. 16, 95–101 (2006). 10.1016/j.conb.2005.12.001

[20]

Schubert, V. & Dotti, C. G. Transmitting on actin: synaptic control of dendritic architecture. J. Cell Sci. 120, 205–212 (2007). 10.1242/jcs.03337

[21]

Sekino, Y., Kojima, N. & Shirao, T. Role of actin cytoskeleton in dendritic spine morphogenesis. Neurochem. Int. 51, 92–104 (2007). 10.1016/j.neuint.2007.04.029

[22]

Sudhof, T. C. The synaptic vesicle cycle. Annu. Rev. Neurosci. 27, 509–547 (2004). 10.1146/annurev.neuro.26.041002.131412

[23]

Murthy, V. N. & De Camilli, P. Cell biology of the presynaptic terminal. Annu. Rev. Neurosci. 26, 701–728 (2003). 10.1146/annurev.neuro.26.041002.131445

[24]

Fernandez-Alfonso, T. & Ryan, T. A. The efficiency of the synaptic vesicle cycle at central nervous system synapses. Trends Cell Biol. 16, 413–420 (2006). 10.1016/j.tcb.2006.06.007

[25]

Rizzoli, S. O. & Betz, W. J. Synaptic vesicle pools. Nature Rev. Neurosci. 6, 57–69 (2005). 10.1038/nrn1583

[26]

Schikorski, T. & Stevens, C. F. Morphological correlates of functionally defined synaptic vesicle populations. Nature Neurosci. 4, 391–395 (2001). 10.1038/86042

[27]

Rizzoli, S. O. & Betz, W. J. The structural organization of the readily releasable pool of synaptic vesicles. Science 303, 2037–2039 (2004). 10.1126/science.1094682

[28]

Darcy, K. J., Staras, K., Collinson, L. M. & Goda, Y. Constitutive sharing of recycling synaptic vesicles between presynaptic boutons. Nature Neurosci. 9, 315–321 (2006). This study used fluorescence microscopic dye labelling, in combination with FRAP and correlative light and electron microscopy, to demonstrate that synaptic vesicle recycling is not confined to individual synapses, but rather that recycling vesicles are shared between neighbouring boutons in a mechanism that requires actin. 10.1038/nn1640

[29]

Drenckhahn, D. & Kaiser, H. W. Evidence for the concentration of F-actin and myosin in synapses and in the plasmalemmal zone of axons. Eur. J. Cell Biol. 31, 235–240 (1983).

[30]

Drenckhahn, D., Frotscher, M. & Kaiser, H. W. Concentration of F-actin in synaptic formations of the hippocampus as visualized by staining with fluorescent phalloidin. Brain Res. 300, 381–384 (1984). 10.1016/0006-8993(84)90851-5

[31]

Gotow, T., Miyaguchi, K. & Hashimoto, P. H. Cytoplasmic architecture of the axon terminal: filamentous strands specifically associated with synaptic vesicles. Neuroscience 40, 587–598 (1991). 10.1016/0306-4522(91)90143-c

[32]

Greengard, P., Benfenati, F. & Valtorta, F. Synapsin I, an actin-binding protein regulating synaptic vesicle traffic in the nerve terminal. Adv. Second Messenger Phosphoprotein Res. 29, 31–45 (1994). 10.1016/s1040-7952(06)80005-4

[33]

Hilfiker, S. et al. Synapsins as regulators of neurotransmitter release. Philos. Trans. R. Soc. Lond. B Biol. Sci. 354, 269–279 (1999). 10.1098/rstb.1999.0378

[34]

Evergren, E., Benfenati, F. & Shupliakov, O. The synapsin cycle: a view from the synaptic endocytic zone. J. Neurosci. Res. 85, 2648–2656 (2007). 10.1002/jnr.21176

[35]

Chi, P., Greengard, P. & Ryan, T. A. Synapsin dispersion and reclustering during synaptic activity. Nature Neurosci. 4, 1187–1193 (2001). 10.1038/nn756

[36]

Chi, P., Greengard, P. & Ryan, T. A. Synaptic vesicle mobilization is regulated by distinct synapsin I phosphorylation pathways at different frequencies. Neuron 38, 69–78 (2003). 10.1016/s0896-6273(03)00151-x

[37]

Phillips, G. R. et al. The presynaptic particle web: ultrastructure, composition, dissolution, and reconstitution. Neuron 32, 63–77 (2001). 10.1016/s0896-6273(01)00450-0

[38]

Siksou, L. et al. Three-dimensional architecture of presynaptic terminal cytomatrix. J. Neurosci. 27, 6868–6877 (2007). In this study, electron tomography of samples prepared by the high-pressure freezing method revealed a detailed organization of presynaptic terminals with respect to the distribution of synaptic vesicles and their relationship to the active zone and the cytomatrix. 10.1523/jneurosci.1773-07.2007

[39]

Dubochet, J. High-pressure freezing for cryoelectron microscopy. Trends Cell Biol. 5, 366–368 (1995). 10.1016/s0962-8924(00)89071-6

[40]

Zuber, B., Nikonenko, I., Klauser, P., Muller, D. & Dubochet, J. The mammalian central nervous synaptic cleft contains a high density of periodically organized complexes. Proc. Natl Acad. Sci. USA 102, 19192–19197 (2005). 10.1073/pnas.0509527102

[41]

Rostaing, P. et al. Analysis of synaptic ultrastructure without fixative using high-pressure freezing and tomography. Eur. J. Neurosci. 24, 3463–3474 (2006). 10.1111/j.1460-9568.2006.05234.x

[42]

Harata, N., Ryan, T. A., Smith, S. J., Buchanan, J. & Tsien, R. W. Visualizing recycling synaptic vesicles in hippocampal neurons by FM 1–43 photoconversion. Proc. Natl Acad. Sci. USA 98, 12748–12753 (2001). 10.1073/pnas.171442798

[43]

Henkel, A. W., Lubke, J. & Betz, W. J. FM1–43 dye ultrastructural localization in and release from frog motor nerve terminals. Proc. Natl Acad. Sci. USA 93, 1918–1923 (1996). 10.1073/pnas.93.5.1918

[44]

Shtrahman, M., Yeung, C., Nauen, D. W., Bi, G. Q. & Wu, X. L. Probing vesicle dynamics in single hippocampal synapses. Biophys. J. 89, 3615–3627 (2005). 10.1529/biophysj.105.059295

[45]

Jordan, R., Lemke, E. A. & Klingauf, J. Visualization of synaptic vesicle movement in intact synaptic boutons using fluorescence fluctuation spectroscopy. Biophys. J. 89, 2091–2102 (2005). 10.1529/biophysj.105.061663

[46]

Gaffield, M. A. & Betz, W. J. Synaptic vesicle mobility in mouse motor nerve terminals with and without synapsin. J. Neurosci. 27, 13691–13700 (2007). 10.1523/jneurosci.3910-07.2007

[47]

Gaffield, M. A., Rizzoli, S. O. & Betz, W. J. Mobility of synaptic vesicles in different pools in resting and stimulated frog motor nerve terminals. Neuron 51, 317–325 (2006). 10.1016/j.neuron.2006.06.031

[48]

Kuromi, H. & Kidokoro, Y. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20, 917–925 (1998). 10.1016/s0896-6273(00)80473-0

[49]

Delgado, R., Maureira, C., Oliva, C., Kidokoro, Y. & Labarca, P. Size of vesicle pools, rates of mobilization, and recycling at neuromuscular synapses of a Drosophila mutant, shibire. Neuron 28, 941–953 (2000). 10.1016/s0896-6273(00)00165-3

[50]

SNAREs — engines for membrane fusion

Reinhard Jahn, Richard H. Scheller

Nature Reviews Molecular Cell Biology 2006 10.1038/nrm2002

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Details

Published: May 01, 2008
Vol/Issue: 9(5)
Pages: 344-356
License: View

Authors

Laboratory for Synaptic Plasticity and Connectivity, RIKEN Center for Brain Science, Wako, Saitama 351-0198, Japan.

Cite This Article

Lorenzo A. Cingolani, Yukiko Goda (2008). Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nature Reviews Neuroscience, 9(5), 344-356. https://doi.org/10.1038/nrn2373

Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy

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