Actin(g) on mitochondria – a role for cofilin1 in neuronal cell death pathways

References

Andrianantoandro, E. and Pollard, T.D. (2006). Mechanism of actin filament turnover by severing and nucleation at different concentrations of ADF/cofilin. Mol. Cell 24, 13–23.10.1016/j.molcel.2006.08.006Search in Google Scholar PubMed

Arber, S., Barbayannis, F.A., Hanser, H., Schneider, C., Stanyon, C.A., Bernard, O., and Caroni, P. (1998). Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature 393, 805–809.10.1038/31729Search in Google Scholar PubMed

Bamburg, J.R., Bernstein, B.W., Davis, R.C., Flynn, K.C., Goldsbury, C., Jensen, J.R., Maloney, M.T., Marsden, I.T., Minamide, L.S., Pak, C.W., et al. (2010). ADF/cofilin-actin rods in neurodegenerative diseases. Cur. Alzheimer Res. 7, 241–250.10.2174/156720510791050902Search in Google Scholar PubMed PubMed Central

Bellenchi, G.C., Gurniak, C.B., Perlas, E., Middei, S., Ammassari-Teule, M., and Witke, W. (2007). N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev. 21, 2347–2357.10.1101/gad.434307Search in Google Scholar PubMed PubMed Central

Bernstein, B.W. and Bamburg, J.R. (2010). ADF/cofilin: a functional node in cell biology. Trends Cell Biol. 20, 187–195.10.1016/j.tcb.2010.01.001Search in Google Scholar PubMed PubMed Central

Bernstein, B.W., Chen, H., Boyle, J.A., and Bamburg, J.R. (2006). Formation of actin-ADF/cofilin rods transiently retards decline of mitochondrial potential and ATP in stressed neurons. Am. J. Physiol. Cell Physiol. 291, C828–C839.10.1152/ajpcell.00066.2006Search in Google Scholar PubMed

Boldogh, I.R., Nowakowski, D.W., Yang, H.-C., Chung, H., Karmon, S., Royes, P., and Pon, L.A. (2003). A protein complex containing Mdm10p, Mdm12p, and Mmm1p links mitochondrial membranes and DNA to the cytoskeleton-based segregation machinery. Mol. Biol. Cell 14, 4618–4627.10.1091/mbc.e03-04-0225Search in Google Scholar PubMed PubMed Central

Boldogh, I.R. and Pon, L.A. (2006). Interactions of mitochondria with the actin cytoskeleton. Biochim. Biophys. Acta 1763, 450–462.10.1016/j.bbamcr.2006.02.014Search in Google Scholar PubMed

Boldogh, I.R. and Pon, L.A. (2007). Mitochondria on the move. Trends Cell Biol. 17, 502–510.10.1016/j.tcb.2007.07.008Search in Google Scholar PubMed

Carlier, M.-F., Laurent, V., Santolini, J., Melki, R., Didry, D., Xia, G.-X., Hong, Y., Chua, N.-H., and Pantaloni, D. (1997). Actin depolymerizing factor (ADF/cofilin) enhances the rate of filament turnover: implication in actin-based motility. J. Cell Biol. 136, 1307–1322.10.1083/jcb.136.6.1307Search in Google Scholar PubMed PubMed Central

Cerveny, K.L., McCaffery, J.M., and Jensen, R.E. (2001). Division of mitochondria requires a novel DNM1-interacting protein, Net2p. Mol. Biol. Cell 12, 309–321.10.1091/mbc.12.2.309Search in Google Scholar PubMed PubMed Central

Chakrabarti, R., Ji, W.-K., Stan, R.V., Juan Sanz, J., Ryan, T.A., and Higgs, H.N. (2018). INF2-mediated actin polymerization at the ER stimulates mitochondrial calcium uptake, inner membrane constriction, and division. J. Cell Biol. 217, 251–268.10.1083/jcb.201709111Search in Google Scholar PubMed PubMed Central

Chen, T.-J., Gehler, S., Shaw, A.E., Bamburg, J.R., and Letourneau, P.C. (2006). Cdc42 participates in the regulation of ADF/cofilin and retinal growth cone filopodia by brain derived neurotrophic factor. J. Neurobiol. 66, 103–114.10.1002/neu.20204Search in Google Scholar PubMed

Chen, S.D., Lin, T.K., Yang, D.I., Lee, S.Y., Shaw, F.Z., Liou, C.W., and Chuang, Y.C. (2015). Roles of PTEN-induced putative kinase 1 and dynamin-related protein 1 in transient global ischemia-induced hippocampal neuronal injury. Biochem. Biophys. Res. Commun. 460, 397–403.10.1016/j.bbrc.2015.03.045Search in Google Scholar PubMed

Chua, B.T., Volbracht, C., Tan, K.O., Li, R., Yu, V.C., and Li, P. (2003). Mitochondrial translocation of cofilin is an early step in apoptosis induction. Nat. Cell Biol. 5, 1083–1089.10.1038/ncb1070Search in Google Scholar PubMed

Cichon, J., Sun, C., Chen, B., Jiang, M., Chen, X.A., Sun, Y., Wang, Y., and Chen, G. (2012). Cofilin aggregation blocks intracellular trafficking and induces synaptic loss in hippocampal neurons. J. Biol. Chem. 287, 3919–3929.10.1074/jbc.M111.301911Search in Google Scholar PubMed PubMed Central

Coles, C.H. and Bradke, F. (2015). Coordinating neuronal actin-microtubule dynamics. Curr. Biol. 25, R677–R691.10.1016/j.cub.2015.06.020Search in Google Scholar PubMed

Culmsee, C. and Krieglstein, J. (2007). Ischaemic brain damage after stroke: new insights into efficient therapeutic strategies. International Symposium on Neurodegeneration and Neuroprotection. EMBO Rep. 8, 129–133.10.1038/sj.embor.7400892Search in Google Scholar PubMed PubMed Central

da Silva, J.S. and Dotti, C.G. (2002). Breaking the neuronal sphere: regulation of the actin cytoskeleton in neuritogenesis. Nat. Rev. Neurosci. 3, 694–704.10.1038/nrn918Search in Google Scholar PubMed

Deng, Y., Wei, J., Cheng, J., Zhong, P., Xiong, Z., Liu, A., Lin, L., Chen, S., and Yan, Z. (2016). Partial amelioration of synaptic and cognitive deficits by inhibiting cofilin dephosphorylation in an animal model of Alzheimer’s disease. J. Alzheimer’s Dis. 53, 1419–1432.10.3233/JAD-160167Search in Google Scholar PubMed

Dirnagl, U., Iadecola, C., and Moskowitz, M.A. (1999). Pathobiology of ischaemic stroke: an integrated view. Trends Neurosci. 22, 391–397.10.1016/S0166-2236(99)01401-0Search in Google Scholar

Duffney, L.J., Zhong, P., Wei, J., Matas, E., Cheng, J., Qin, L., Ma, K., Dietz, D.M., Kajiwara, Y., Buxbaum, J.D., et al. (2015). Autism-like deficits in Shank3-deficient mice are rescued by targeting actin regulators. Cell Rep. 11, 1400–1413.10.1016/j.celrep.2015.04.064Search in Google Scholar PubMed PubMed Central

Flynn, K.C., Hellal, F., Neukirchen, D., Jacob, S., Tahirovic, S., Dupraz, S., Stern, S., Garvalov, B.K., Gurniak, C., Shaw, A.E., et al. (2012). ADF/cofilin-mediated actin retrograde flow directs neurite formation in the developing brain. Neuron 76, 1091–1107.10.1016/j.neuron.2012.09.038Search in Google Scholar PubMed

Frederick, R.L. and Shaw, J.M. (2007). Moving mitochondria: establishing distribution of an essential organelle. Traffic 8, 1668–1675.10.1111/j.1600-0854.2007.00644.xSearch in Google Scholar PubMed PubMed Central

Gellert, M., Hanschmann, E.-M., Lepka, K., Berndt, C., and Lillig, C.H. (2015). Redox regulation of cytoskeletal dynamics during differentiation and de-differentiation. Biochim. Biophys. Acta 1850, 1575–1587.10.1016/j.bbagen.2014.10.030Search in Google Scholar PubMed

Gohla, A., Birkenfeld, J., and Bokoch, G.M. (2005). Chronophin, a novel HAD-type serine protein phosphatase, regulates cofilin-dependent actin dynamics. Nat. Cell Biol. 7, 21–29.10.1038/ncb1201Search in Google Scholar PubMed

Goodson, M., Rust, M.B., Witke, W., Bannerman, D., Mott, R., Ponting, C.P., and Flint, J. (2012). Cofilin-1: a modulator of anxiety in mice. PLoS Genet. 8, e1002970.10.1371/journal.pgen.1002970Search in Google Scholar PubMed PubMed Central

Grohm, J., Kim, S.-W., Mamrak, U., Tobaben, S., Cassidy-Stone, A., Nunnari, J., Plesnila, N., and Culmsee, C. (2012). Inhibition of Drp1 provides neuroprotection in vitro and in vivo. Cell Death Differ. 19, 1446–1458.10.1038/cdd.2012.18Search in Google Scholar PubMed PubMed Central

Gu, J., Lee, C.W., Fan, Y., Komlos, D., Tang, X., Sun, C., Yu, K., Hartzell, H.C., Chen, G., Bamburg, J.R., et al. (2010). ADF/cofilin-mediated actin dynamics regulate AMPA receptor trafficking during synaptic plasticity. Nat. Neurosci. 13, 1208–1215.10.1038/nn.2634Search in Google Scholar PubMed PubMed Central

Gurniak, C.B., Chevessier, F., Jokwitz, M., Jönsson, F., Perlas, E., Richter, H., Matern, G., Boyl, P.P., Chaponnier, C., Fürst, D., et al. (2014). Severe protein aggregate myopathy in a knockout mouse model points to an essential role of cofilin2 in sarcomeric actin exchange and muscle maintenance. Eur. J. Cell Biol. 93, 252–266.10.1016/j.ejcb.2014.01.007Search in Google Scholar PubMed

Hatch, A.L., Gurel, P.S., and Higgs, H.N. (2014). Novel roles for actin in mitochondrial fission. J. Cell Sci. 127, 4549–4560.10.1242/jcs.153791Search in Google Scholar PubMed PubMed Central

Hatch, A.L., Ji, W.-K., Merrill, R.A., Strack, S., and Higgs, H.N. (2016). Actin filaments as dynamic reservoirs for Drp1 recruitment. Mol. Biol. Cell 27, 3109–3121.10.1091/mbc.e16-03-0193Search in Google Scholar

Hild, G., Kalmár, L., Kardos, R., Nyitrai, M., and Bugyi, B. (2014). The other side of the coin: functional and structural versatility of ADF/cofilins. Eur. J. Cell Biol. 93, 238–251.10.1016/j.ejcb.2013.12.001Search in Google Scholar PubMed

Hotulainen, P., Llano, O., Smirnov, S., Tanhuanpää, K., Faix, J., Rivera, C., and Lappalainen, P. (2009). Defining mechanisms of actin polymerization and depolymerization during dendritic spine morphogenesis. J. Cell Biol. 185, 323–339.10.1083/jcb.200809046Search in Google Scholar PubMed PubMed Central

Huang, T.Y., Minamide, L.S., Bamburg, J.R., and Bokoch, G.M. (2008). Chronophin mediates an ATP-sensing mechanism for cofilin dephosphorylation and neuronal cofilin-actin rod formation. Dev. Cell 15, 691–703.10.1016/j.devcel.2008.09.017Search in Google Scholar PubMed PubMed Central

Ito, U., Kuroiwa, T., Nagasao, J., Kawakami, E., and Oyanagi, K. (2006). Temporal profiles of axon terminals, synapses and spines in the ischemic penumbra of the cerebral cortex: ultrastructure of neuronal remodeling. Stroke 37, 2134–2139.10.1161/01.STR.0000231875.96714.b1Search in Google Scholar PubMed

Ji, W.-K., Hatch, A.L., Merrill, R.A., Strack, S., and Higgs, H.N. (2015). Actin filaments target the oligomeric maturation of the dynamin GTPase Drp1 to mitochondrial fission sites. eLife 4, e11553.10.7554/eLife.11553.040Search in Google Scholar

Klamt, F., Zdanov, S., Levine, R.L., Pariser, A., Zhang, Y., Zhang, B., Yu, L.-R., Veenstra, T.D., and Shacter, E. (2009). Oxidant-induced apoptosis is mediated by oxidation of the actin-regulatory protein cofilin. Nat. Cell Biol. 11, 1241–1246.10.1038/ncb1968Search in Google Scholar PubMed PubMed Central

Korobova, F., Ramabhadran, V., and Higgs, H.N. (2013). An actin-dependent step in mitochondrial fission mediated by the ER-associated formin INF2. Science 339, 464–467.10.1126/science.1228360Search in Google Scholar PubMed PubMed Central

Kotiadis, V.N., Leadsham, J.E., Bastow, E.L., Gheeraert, A., Whybrew, J.M., Bard, M., Lappalainen, P., and Gourlay, C.W. (2012). Identification of new surfaces of cofilin that link mitochondrial function to the control of multi-drug resistance. J. Cell Sci. 125, 2288–2299.10.1242/jcs.099390Search in Google Scholar PubMed PubMed Central

Li, S., Xu, S., Roelofs, B.A., Boyman, L., Lederer, W.J., Sesaki, H., and Karbowski, M. (2015a). Transient assembly of F-actin on the outer mitochondrial membrane contributes to mitochondrial fission. J. Cell Biol. 208, 109–123.10.1083/jcb.201404050Search in Google Scholar PubMed PubMed Central

Li, G., Zhou, J., Budhraja, A., Hu, X., Chen, Y., Cheng, Q., Liu, L., Zhou, T., Li, P., Liu, E., et al. (2015b). Mitochondrial translocation and interaction of cofilin and Drp1 are required for erucin-induced mitochondrial fission and apoptosis. Oncotarget 6, 1834–1849.10.18632/oncotarget.2795Search in Google Scholar PubMed PubMed Central

Luo, S., Uehara, H., and Shacter, E. (2014). Taurine chloramine-induced inactivation of cofilin protein through methionine oxidation. Free Radic. Biol. Med. 75, 84–94.10.1016/j.freeradbiomed.2014.07.018Search in Google Scholar PubMed

Maciver, S.K. and Weeds, A.G. (1994). Actophorin preferentially binds monomeric ADP-Actin over ATP-bound actin: consequences for cell locomotion. FEBS Lett. 347, 251–256.10.1016/0014-5793(94)00552-4Search in Google Scholar PubMed

Manor, U., Bartholomew, S., Golani, G., Christenson, E., Kozlov, M., Higgs, H., Spudich, J., and Lippincott-Schwartz, J. (2015). A mitochondria-anchored isoform of the actin-nucleating spire protein regulates mitochondrial division. eLife 4.10.7554/eLife.08828Search in Google Scholar PubMed PubMed Central

Minamide, L.S., Striegl, A.M., Boyle, J.A., Meberg, P.J., and Bamburg, J.R. (2000). Neurodegenerative stimuli induce persistent ADF/cofilin-actin rods that disrupt distal neurite function. Nat. Cell Biol. 2, 628–636.10.1038/35023579Search in Google Scholar PubMed

Minamide, L.S., Maiti, S., Boyle, J.A., Davis, R.C., Coppinger, J.A., Bao, Y., Huang, T.Y., Yates, J., Bokoch, G.M., and Bamburg, J.R. (2010). Isolation and characterization of cytoplasmic cofilin-actin rods. J. Biol. Chem. 285, 5450–5460.10.1074/jbc.M109.063768Search in Google Scholar PubMed PubMed Central

Mitchison, T.J. and Cramer, L.P. (1996). Actin-based cell motility and cell locomotion. Cell 84, 371–379.10.1016/S0092-8674(00)81281-7Search in Google Scholar PubMed

Moore, A.S., Wong, Y.C., Simpson, C.L., and Holzbaur, E.L.F. (2016). Dynamic actin cycling through mitochondrial subpopulations locally regulates the fission-fusion balance within mitochondrial networks. Nat. Commun. 7, 12886.10.1038/ncomms12886Search in Google Scholar PubMed PubMed Central

Moriyama, K., Iida, K., and Yahara, I. (1996). Phosphorylation of Ser-3 of cofilin regulates its essential function on actin. Genes Cells 1, 73–86.10.1046/j.1365-2443.1996.05005.xSearch in Google Scholar PubMed

Moskowitz, M.A., Lo, E.H., and Iadecola, C. (2010). The science of stroke: mechanisms in search of treatments. Neuron 67, 181–198.10.1016/j.neuron.2010.07.002Search in Google Scholar PubMed PubMed Central

Munsie, L.N. and Truant, R. (2012). The role of the cofilin-actin rod stress response in neurodegenerative diseases uncovers potential new drug targets. Bioarchitecture 2, 204–208.10.4161/bioa.22549Search in Google Scholar PubMed PubMed Central

Munsie, L., Caron, N., Atwal, R.S., Marsden, I., Wild, E.J., Bamburg, J.R., Tabrizi, S.J., and Truant, R. (2011). Mutant huntingtin causes defective actin remodeling during stress: defining a new role for transglutaminase 2 in neurodegenerative disease. Hum. Mol. Genet. 20, 1937–1951.10.1093/hmg/ddr075Search in Google Scholar PubMed PubMed Central

Munsie, L.N., Desmond, C.R., and Truant, R. (2012). Cofilin nuclear-cytoplasmic shuttling affects cofilin-actin rod formation during stress. J. Cell Sci. 125, 3977–3988.10.1242/jcs.097667Search in Google Scholar PubMed

Niwa, R., Nagata-Ohashi, K., Takeichi, M., Mizuno, K., and Uemura, T. (2002). Control of actin reorganization by Slingshot, a family of phosphatases that dephosphorylate ADF/cofilin. Cell 108, 233–246.10.1016/S0092-8674(01)00638-9Search in Google Scholar PubMed

Olesen, J. and Leonardi, M. (2003). The burden of brain diseases in Europe. Eur. J. Neurol. 10, 471–477.10.1046/j.1468-1331.2003.00682.xSearch in Google Scholar PubMed

Ordonez, D.G., Lee, M.K., and Feany, M.B. (2018). α-Synuclein induces mitochondrial dysfunction through spectrin and the actin cytoskeleton. Neuron 97, 108–124.e106.10.1016/j.neuron.2017.11.036Search in Google Scholar PubMed PubMed Central

Pfannstiel, J., Cyrklaff, M., Habermann, A., Stoeva, S., Griffiths, G., Shoeman, R., and Faulstich, H. (2001). Human cofilin forms oligomers exhibiting actin bundling activity. J. Biol Chem. 276, 49476–49484.10.1074/jbc.M104760200Search in Google Scholar PubMed

Qiu, Y., Chen, W.Y., Wang, Z.Y., Liu, F., Wei, M., Ma, C., and Huang, Y.G. (2016). Simvastatin attenuates neuropathic pain by inhibiting the RhoA/LIMK/cofilin pathway. Neurochem Res. 41, 2457–2469.10.1007/s11064-016-1958-1Search in Google Scholar PubMed

Rehklau, K., Gurniak, C.B., Conrad, M., Friauf, E., Ott, M., and Rust, M.B. (2012). ADF/cofilin proteins translocate to mitochondria during apoptosis but are not generally required for cell death signaling. Cell Death Differ. 19, 958–967.10.1038/cdd.2011.180Search in Google Scholar PubMed PubMed Central

Rehklau, K., Hoffmann, L., Gurniak, C.B., Ott, M., Witke, W., Scorrano, L., Culmsee, C., and Rust, M.B. (2017). Cofilin1-dependent actin dynamics control DRP1-mediated mitochondrial fission. Cell Death Dis. 8, e3063.10.1038/cddis.2017.448Search in Google Scholar PubMed PubMed Central

Revenu, C., Athman, R., Robine, S., and Louvard, D. (2004). The co-workers of actin filaments: from cell structures to signals. Nat. Rev. Mol. Cell Biol. 5, 635–646.10.1038/nrm1437Search in Google Scholar PubMed

Rust, M.B. (2015). ADF/cofilin: a crucial regulator of synapse physiology and behavior. Cell. Mol. Life Sci. 72, 3521–3529.10.1007/s00018-015-1941-zSearch in Google Scholar PubMed

Rust, M.B., Gurniak, C.B., Renner, M., Vara, H., Morando, L., Görlich, A., Sassoè-Pognetto, M., Banchaabouchi, M.A., Giustetto, M., Triller, A., et al. (2010). Learning, AMPA receptor mobility and synaptic plasticity depend on n-cofilin-mediated actin dynamics. EMBO J. 29, 1889–1902.10.1038/emboj.2010.72Search in Google Scholar PubMed PubMed Central

Shu, L., Chen, B., Chen, B., Xu, H., Wang, G., Huang, Y., Zhao, Y., Gong, H., Jiang, M., Chen, L., et al. (2018). Brain ischemic insult induces cofilin rod formation leading to synaptic dysfunction in neurons. J. Cereb. Blood Fow Metabol. 271678X18785567.10.1177/0271678X18785567Search in Google Scholar PubMed PubMed Central

Sungur, A.Ö., Stemmler, L., Wöhr, M., and Rust, M.B. (2018). Impaired object recognition but normal social behavior and ultrasonic communication in cofilin1 mutant mice. Front. Behav. Neurosci. 12, 25.10.3389/fnbeh.2018.00025Search in Google Scholar PubMed PubMed Central

Tilve, S., Difato, F., and Chieregatti, E. (2015). Cofilin 1 activation prevents the defects in axon elongation and guidance induced by extracellular α-synuclein. Sci. Rep. 5, 16524.10.1038/srep16524Search in Google Scholar PubMed PubMed Central

Vartiainen, M.K., Mustonen, T., Mattila, P.K., Ojala, P.J., Thesleff, I., Partanen, J., and Lappalainen, P. (2002). The three mouse actin-depolymerizing factor/cofilins evolved to fulfill cell-type-specific requirements for actin dynamics. Mol. Biol. Cell 13, 183–194.10.1091/mbc.01-07-0331Search in Google Scholar PubMed PubMed Central

Welch, M.D., Mallavarapu, A., Rosenblatt, J., and Mitchison, T.J. (1997). Actin dynamics in vivo. Curr. Opin. Cell Biol. 9, 54–61.10.1016/S0955-0674(97)80152-4Search in Google Scholar

Wioland, H., Guichard, B., Senju, Y., Myram, S., Lappalainen, P., Jégou, A., and Romet-Lemonne, G. (2017). ADF/cofilin accelerates actin dynamics by severing filaments and promoting their depolymerization at both ends. Curr. Biol. 27, 1956–1967.e1957.10.1016/j.cub.2017.05.048Search in Google Scholar PubMed PubMed Central

Wolf, M., Zimmermann, A.-M., Görlich, A., Gurniak, C.B., Sassoè-Pognetto, M., Friauf, E., Witke, W., and Rust, M.B. (2015). ADF/cofilin controls synaptic actin dynamics and regulates synaptic vesicle mobilization and exocytosis. Cereb. Cortex 25, 2863–2875.10.1093/cercor/bhu081Search in Google Scholar PubMed

Won, S.J., Minnella, A.M., Wu, L., Eun, C.H., Rome, E., Herson, P.S., Shaw, A.E., Bamburg, J.R., and Swanson, R.A. (2018). Cofilin-actin rod formation in neuronal processes after brain ischemia. PLoS One 13, e0198709.10.1371/journal.pone.0198709Search in Google Scholar PubMed PubMed Central

Woo, J.A., Zhao, X., Khan, H., Penn, C., Wang, X., Joly-Amado, A., Weeber, E., Morgan, D., and Kang, D.E. (2015). Slingshot-Cofilin activation mediates mitochondrial and synaptic dysfunction via Aβ ligation to β1-integrin conformers. Cell Death Differ. 22, 921–934.10.1038/cdd.2015.5Search in Google Scholar PubMed PubMed Central

Wrogemann, K. and Pena, S.D. (1976). Mitochondrial calcium overload: a general mechanism for cell-necrosis in muscle diseases. Lancet 1, 672–674.10.1016/S0140-6736(76)92781-1Search in Google Scholar PubMed

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, 809–812.10.1038/31735Search in Google Scholar PubMed

Zhao, Y.X., Cui, M., Chen, S.F., Dong, Q., and Liu, X.Y. (2014). Amelioration of ischemic mitochondrial injury and Bax-dependent outer membrane permeabilization by Mdivi-1. CNS Neurosci. Ther. 20, 528–538.10.1111/cns.12266Search in Google Scholar PubMed PubMed Central

Zhou, Q., Homma, K.J., and Poo, M.M. (2004). Shrinkage of dendritic spines associated with long-term depression of hippocampal synapses. Neuron 44, 749–757.10.1016/j.neuron.2004.11.011Search in Google Scholar PubMed

Zimmermann, A.M., Jene, T., Wolf, M., Gorlich, A., Gurniak, C.B., Sassoe-Pognetto, M., Witke, W., Friauf, E., and Rust, M.B. (2015). Attention-deficit/hyperactivity disorder-like phenotype in a mouse model with impaired actin dynamics. Biol. Psychiatry 78, 95–106.10.1016/j.biopsych.2014.03.011Search in Google Scholar PubMed