{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,7,20]],"date-time":"2026-07-20T10:32:14Z","timestamp":1784543534905,"version":"3.55.0"},"reference-count":77,"publisher":"Springer Science and Business Media LLC","issue":"1","license":[{"start":{"date-parts":[[2023,10,18]],"date-time":"2023-10-18T00:00:00Z","timestamp":1697587200000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2023,10,18]],"date-time":"2023-10-18T00:00:00Z","timestamp":1697587200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"}],"content-domain":{"domain":["link.springer.com"],"crossmark-restriction":false},"short-container-title":["Commun Biol"],"abstract":"<jats:title>Abstract<\/jats:title><jats:p>Neuroligins are transmembrane cell adhesion proteins well-known for their genetic links to autism spectrum disorders. Neuroligins can function by regulating the actin cytoskeleton, however the factors and mechanisms involved are still largely unknown. Here, using the <jats:italic>Drosophila<\/jats:italic> neuromuscular junction as a model, we reveal that F-Actin assembly at the <jats:italic>Drosophila<\/jats:italic> NMJ is controlled through Cofilin signaling mediated by an interaction between DNlg2 and RACK1, factors not previously known to work together. The deletion of DNlg2 displays disrupted RACK1-Cofilin signaling pathway with diminished actin cytoskeleton proteo-stasis at the terminal of the NMJ, aberrant NMJ structure, reduced synaptic transmission, and abnormal locomotion at the third-instar larval stage. Overexpression of wildtype and activated Cofilin in muscles are sufficient to rescue the morphological and physiological defects in <jats:italic>dnlg2<\/jats:italic> mutants, while inactivated Cofilin is not. Since the DNlg2 paralog DNlg1 is known to regulate F-actin assembly mainly via a specific interaction with WAVE complex, our present work suggests that the orchestration of F-actin by Neuroligins is a diverse and complex process critical for neural connectivity.<\/jats:p>","DOI":"10.1038\/s42003-023-05428-3","type":"journal-article","created":{"date-parts":[[2023,10,18]],"date-time":"2023-10-18T12:03:30Z","timestamp":1697630610000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":4,"title":["Neuroligin 2 governs synaptic morphology and function through RACK1-cofilin signaling in Drosophila"],"prefix":"10.1038","volume":"6","author":[{"ORCID":"https:\/\/orcid.org\/0000-0003-1732-5955","authenticated-orcid":false,"given":"Yichen","family":"Sun","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0003-3566-3931","authenticated-orcid":false,"given":"Moyi","family":"Li","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Junhua","family":"Geng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sibie","family":"Meng","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Renjun","family":"Tu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yan","family":"Zhuang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mingkuan","family":"Sun","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Menglong","family":"Rui","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mengzhu","family":"Ou","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Guangling","family":"Xing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Travis K.","family":"Johnson","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Wei","family":"Xie","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2023,10,18]]},"reference":[{"key":"5428_CR1","doi-asserted-by":"crossref","first-page":"7629","DOI":"10.1074\/jbc.R100052200","volume":"277","author":"TC S\u00fcdhof","year":"2002","unstructured":"S\u00fcdhof, T. C. Synaptotagmins: why so many? J. Biol. Chem. 277, 7629\u20137632 (2002).","journal-title":"J. Biol. Chem."},{"key":"5428_CR2","doi-asserted-by":"crossref","first-page":"389","DOI":"10.1146\/annurev.neuro.22.1.389","volume":"22","author":"JR Sanes","year":"1999","unstructured":"Sanes, J. R. & Lichtman, J. W. Development of the vertebrate neuromuscular junction. Annu. Rev. Neurosci. 22, 389\u2013442 (1999).","journal-title":"Annu. Rev. Neurosci."},{"key":"5428_CR3","doi-asserted-by":"crossref","first-page":"255","DOI":"10.1002\/syn.890030312","volume":"3","author":"JE Vaughn","year":"1989","unstructured":"Vaughn, J. E. Fine structure of synaptogenesis in the vertebrate central nervous system. Synapse 3, 255\u2013285 (1989).","journal-title":"Synapse"},{"key":"5428_CR4","doi-asserted-by":"crossref","first-page":"549","DOI":"10.14348\/molcells.2021.0129","volume":"44","author":"S Jeong","year":"2021","unstructured":"Jeong, S. Molecular mechanisms underlying motor axon guidance in drosophila. Mol. Cells 44, 549\u2013556 (2021).","journal-title":"Mol. Cells"},{"key":"5428_CR5","doi-asserted-by":"crossref","unstructured":"Ali, H., Marth, L. & Krueger-Burg, D. Neuroligin-2 as a central organizer of inhibitory synapses in health and disease. Sci Signal 13, eabd8379 (2020).","DOI":"10.1126\/scisignal.abd8379"},{"key":"5428_CR6","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1016\/j.mcn.2016.11.004","volume":"78","author":"S Banerjee","year":"2017","unstructured":"Banerjee, S., Venkatesan, A. & Bhat, M. A. Neurexin, neuroligin and wishful thinking coordinate synaptic cytoarchitecture and growth at neuromuscular junctions. Mol. Cell Neurosci. 78, 9\u201324 (2017).","journal-title":"Mol. Cell Neurosci."},{"key":"5428_CR7","doi-asserted-by":"crossref","first-page":"724","DOI":"10.1016\/j.neuron.2010.05.020","volume":"66","author":"D Banovic","year":"2010","unstructured":"Banovic, D. et al. Drosophila neuroligin 1 promotes growth and postsynaptic differentiation at glutamatergic neuromuscular junctions. Neuron 66, 724\u2013738 (2010).","journal-title":"Neuron"},{"key":"5428_CR8","doi-asserted-by":"crossref","first-page":"56","DOI":"10.1038\/nn.3601","volume":"17","author":"MA Bemben","year":"2014","unstructured":"Bemben, M. A. et al. CaMKII phosphorylation of neuroligin-1 regulates excitatory synapses. Nat. Neurosci. 17, 56\u201364 (2014).","journal-title":"Nat. Neurosci."},{"key":"5428_CR9","doi-asserted-by":"crossref","first-page":"357","DOI":"10.1093\/cercor\/bhq100","volume":"21","author":"P Jedlicka","year":"2011","unstructured":"Jedlicka, P. et al. Increased dentate gyrus excitability in neuroligin-2-deficient mice in vivo. Cereb. Cortex 21, 357\u2013367 (2011).","journal-title":"Cereb. Cortex"},{"key":"5428_CR10","doi-asserted-by":"crossref","first-page":"47","DOI":"10.1007\/s00429-013-0636-1","volume":"220","author":"P Jedlicka","year":"2015","unstructured":"Jedlicka, P. et al. Neuroligin-1 regulates excitatory synaptic transmission, LTP and EPSP-spike coupling in the dentate gyrus in vivo. Brain Struct. Funct. 220, 47\u201358 (2015).","journal-title":"Brain Struct. Funct."},{"key":"5428_CR11","doi-asserted-by":"crossref","first-page":"1314","DOI":"10.1097\/j.pain.0000000000000513","volume":"157","author":"JV Kim","year":"2016","unstructured":"Kim, J. V. et al. Neuroligin 2 regulates spinal GABAergic plasticity in hyperalgesic priming, a model of the transition from acute to chronic pain. Pain 157, 1314\u20131324 (2016).","journal-title":"Pain"},{"key":"5428_CR12","doi-asserted-by":"crossref","DOI":"10.1038\/s41398-018-0093-y","volume":"8","author":"MA Medina","year":"2018","unstructured":"Medina, M. A. et al. Wnt\/\u03b2-catenin signaling stimulates the expression and synaptic clustering of the autism-associated Neuroligin 3 gene. Transl. Psychiatry 8, 45 (2018).","journal-title":"Transl. Psychiatry"},{"key":"5428_CR13","doi-asserted-by":"crossref","first-page":"1100","DOI":"10.1073\/pnas.96.3.1100","volume":"96","author":"JY Song","year":"1999","unstructured":"Song, J. Y., Ichtchenko, K., S\u00fcdhof, T. C. & Brose, N. Neuroligin 1 is a postsynaptic cell-adhesion molecule of excitatory synapses. Proc. Natl Acad. Sci. USA 96, 1100\u20131105 (1999).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5428_CR14","doi-asserted-by":"crossref","first-page":"687","DOI":"10.1523\/JNEUROSCI.3854-10.2011","volume":"31","author":"M Sun","year":"2011","unstructured":"Sun, M. et al. Neuroligin 2 is required for synapse development and function at the Drosophila neuromuscular junction. J. Neurosci. 31, 687\u2013699 (2011).","journal-title":"J. Neurosci."},{"key":"5428_CR15","doi-asserted-by":"crossref","first-page":"71","DOI":"10.1126\/science.1146221","volume":"318","author":"K Tabuchi","year":"2007","unstructured":"Tabuchi, K. et al. A neuroligin-3 mutation implicated in autism increases inhibitory synaptic transmission in mice. Science 318, 71\u201376 (2007).","journal-title":"Science"},{"key":"5428_CR16","doi-asserted-by":"crossref","unstructured":"Uchigashima, M. et al. Specific Neuroligin3-\u03b1Neurexin1 signaling regulates GABAergic synaptic function in mouse hippocampus. Elife 9, e59545 (2020).","DOI":"10.7554\/eLife.59545"},{"key":"5428_CR17","doi-asserted-by":"crossref","first-page":"4206","DOI":"10.1073\/pnas.1514074113","volume":"113","author":"M Uchigashima","year":"2016","unstructured":"Uchigashima, M., Ohtsuka, T., Kobayashi, K. & Watanabe, M. Dopamine synapse is a neuroligin-2-mediated contact between dopaminergic presynaptic and GABAergic postsynaptic structures. Proc. Natl Acad. Sci. USA 113, 4206\u20134211 (2016).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5428_CR18","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1078\/0171-9335-00410","volume":"83","author":"F Varoqueaux","year":"2004","unstructured":"Varoqueaux, F., Jamain, S. & Brose, N. Neuroligin 2 is exclusively localized to inhibitory synapses. Eur. J. Cell Biol. 83, 449\u2013456 (2004).","journal-title":"Eur. J. Cell Biol."},{"key":"5428_CR19","doi-asserted-by":"crossref","unstructured":"Xing, G. et al. Neurexin-Neuroligin 1 regulates synaptic morphology and functions via the WAVE regulatory complex in Drosophila neuromuscular junction. Elife 7, e30457 (2018).","DOI":"10.7554\/eLife.30457"},{"key":"5428_CR20","doi-asserted-by":"crossref","first-page":"621","DOI":"10.1016\/S0955-0674(03)00107-8","volume":"15","author":"M Yamagata","year":"2003","unstructured":"Yamagata, M., Sanes, J. R. & Weiner, J. A. Synaptic adhesion molecules. Curr. Opin. Cell Biol. 15, 621\u2013632 (2003).","journal-title":"Curr. Opin. Cell Biol."},{"key":"5428_CR21","volume":"12","author":"T Yoshida","year":"2021","unstructured":"Yoshida, T. et al. Canonical versus non-canonical transsynaptic signaling of neuroligin 3 tunes development of sociality in mice. Nat. Commun. 12, 1848 (2021).","journal-title":"Nat. Commun."},{"key":"5428_CR22","doi-asserted-by":"crossref","first-page":"17991","DOI":"10.1074\/jbc.M117.810242","volume":"292","author":"X Zhang","year":"2017","unstructured":"Zhang, X. et al. Neuroligin 4 regulates synaptic growth via the bone morphogenetic protein (BMP) signaling pathway at the Drosophila neuromuscular junction. J. Biol. Chem. 292, 17991\u201318005 (2017).","journal-title":"J. Biol. Chem."},{"key":"5428_CR23","doi-asserted-by":"crossref","first-page":"737","DOI":"10.1007\/s12264-017-0166-6","volume":"33","author":"Y Tian","year":"2017","unstructured":"Tian, Y., Zhang, Z. C. & Han, J. Drosophila studies on autism spectrum disorders. Neurosci. Bull. 33, 737\u2013746 (2017).","journal-title":"Neurosci. Bull."},{"key":"5428_CR24","doi-asserted-by":"crossref","first-page":"919","DOI":"10.1016\/j.neuron.2007.05.029","volume":"54","author":"AA Chubykin","year":"2007","unstructured":"Chubykin, A. A. et al. Activity-dependent validation of excitatory versus inhibitory synapses by neuroligin-1 versus neuroligin-2. Neuron 54, 919\u2013931 (2007).","journal-title":"Neuron"},{"key":"5428_CR25","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1016\/j.neuron.2009.08.023","volume":"63","author":"A Poulopoulos","year":"2009","unstructured":"Poulopoulos, A. et al. Neuroligin 2 drives postsynaptic assembly at perisomatic inhibitory synapses through gephyrin and collybistin. Neuron 63, 628\u2013642 (2009).","journal-title":"Neuron"},{"key":"5428_CR26","doi-asserted-by":"crossref","first-page":"741","DOI":"10.1016\/j.neuron.2006.09.003","volume":"51","author":"F Varoqueaux","year":"2006","unstructured":"Varoqueaux, F. et al. Neuroligins determine synapse maturation and function. Neuron 51, 741\u2013754 (2006).","journal-title":"Neuron"},{"key":"5428_CR27","doi-asserted-by":"crossref","first-page":"31867","DOI":"10.1074\/jbc.M114.574897","volume":"289","author":"G Xing","year":"2014","unstructured":"Xing, G. et al. Drosophila neuroligin3 regulates neuromuscular junction development and synaptic differentiation. J. Biol. Chem. 289, 31867\u201331877 (2014).","journal-title":"J. Biol. Chem."},{"key":"5428_CR28","doi-asserted-by":"crossref","first-page":"16018","DOI":"10.1523\/JNEUROSCI.1685-12.2012","volume":"32","author":"YC Chen","year":"2012","unstructured":"Chen, Y. C. et al. Drosophila neuroligin 2 is required presynaptically and postsynaptically for proper synaptic differentiation and synaptic transmission. J. Neurosci. 32, 16018\u201316030 (2012).","journal-title":"J. Neurosci."},{"key":"5428_CR29","doi-asserted-by":"crossref","first-page":"19","DOI":"10.3389\/fnana.2020.00019","volume":"14","author":"G Guangming","year":"2020","unstructured":"Guangming, G., Junhua, G., Chenchen, Z., Yang, M. & Wei, X. Neurexin and neuroligins maintain the balance of ghost and satellite boutons at the drosophila neuromuscular junction. Front Neuroanat. 14, 19 (2020).","journal-title":"Front Neuroanat."},{"key":"5428_CR30","doi-asserted-by":"crossref","unstructured":"Harris, K. P., Zhang, Y. V., Piccioli, Z. D., Perrimon, N. & Littleton, J. T. The postsynaptic t-SNARE Syntaxin 4 controls traffic of Neuroligin 1 and Synaptotagmin 4 to regulate retrograde signaling. Elife 5, e13881 (2016).","DOI":"10.7554\/eLife.13881"},{"key":"5428_CR31","doi-asserted-by":"crossref","first-page":"15545","DOI":"10.1523\/JNEUROSCI.0819-13.2013","volume":"33","author":"Y Li","year":"2013","unstructured":"Li, Y. et al. Drosophila neuroligin 4 regulates sleep through modulating GABA transmission. J. Neurosci. 33, 15545\u201315554 (2013).","journal-title":"J. Neurosci."},{"key":"5428_CR32","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.mcn.2012.08.010","volume":"51","author":"BA Mozer","year":"2012","unstructured":"Mozer, B. A. & Sandstrom, D. J. Drosophila neuroligin 1 regulates synaptic growth and function in response to activity and phosphoinositide-3-kinase. Mol. Cell Neurosci. 51, 89\u2013100 (2012).","journal-title":"Mol. Cell Neurosci."},{"key":"5428_CR33","doi-asserted-by":"crossref","first-page":"113","DOI":"10.3389\/fpsyt.2017.00113","volume":"8","author":"K Corthals","year":"2017","unstructured":"Corthals, K. et al. Neuroligins Nlg2 and Nlg4 affect social behavior in Drosophila melanogaster. Front. Psychiatry 8, 113 (2017).","journal-title":"Front. Psychiatry"},{"key":"5428_CR34","doi-asserted-by":"crossref","first-page":"344","DOI":"10.1038\/nrn2373","volume":"9","author":"LA Cingolani","year":"2008","unstructured":"Cingolani, L. A. & Goda, Y. Actin in action: the interplay between the actin cytoskeleton and synaptic efficacy. Nat. Rev. Neurosci. 9, 344\u2013356 (2008).","journal-title":"Nat. Rev. Neurosci."},{"key":"5428_CR35","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1016\/j.tcb.2021.10.006","volume":"32","author":"AM Gautreau","year":"2022","unstructured":"Gautreau, A. M., Fregoso, F. E., Simanov, G. & Dominguez, R. Nucleation, stabilization, and disassembly of branched actin networks. Trends Cell Biol. 32, 421\u2013432 (2022).","journal-title":"Trends Cell Biol."},{"key":"5428_CR36","doi-asserted-by":"crossref","unstructured":"Gentile, J. E., Carrizales, M. G. & Koleske, A. J. Control of synapse structure and function by actin and its regulators. Cells 11, 603 (2022).","DOI":"10.3390\/cells11040603"},{"key":"5428_CR37","doi-asserted-by":"crossref","first-page":"147","DOI":"10.3389\/fncel.2017.00147","volume":"11","author":"A Konietzny","year":"2017","unstructured":"Konietzny, A., B\u00e4r, J. & Mikhaylova, M. Dendritic actin cytoskeleton: structure, functions, and regulations. Front. Cell Neurosci. 11, 147 (2017).","journal-title":"Front. Cell Neurosci."},{"key":"5428_CR38","doi-asserted-by":"crossref","first-page":"187","DOI":"10.1016\/j.tcb.2010.01.001","volume":"20","author":"BW Bernstein","year":"2010","unstructured":"Bernstein, B. W. & Bamburg, J. R. ADF\/cofilin: a functional node in cell biology. Trends Cell Biol. 20, 187\u2013195 (2010).","journal-title":"Trends Cell Biol."},{"key":"5428_CR39","doi-asserted-by":"crossref","first-page":"364","DOI":"10.1016\/S0962-8924(99)01619-0","volume":"9","author":"JR Bamburg","year":"1999","unstructured":"Bamburg, J. R., McGough, A. & Ono, S. Putting a new twist on actin: ADF\/cofilins modulate actin dynamics. Trends Cell Biol. 9, 364\u2013370 (1999).","journal-title":"Trends Cell Biol."},{"key":"5428_CR40","doi-asserted-by":"crossref","first-page":"429","DOI":"10.1038\/nrc2148","volume":"7","author":"W Wang","year":"2007","unstructured":"Wang, W., Eddy, R. & Condeelis, J. The cofilin pathway in breast cancer invasion and metastasis. Nat. Rev. Cancer 7, 429\u2013440 (2007).","journal-title":"Nat. Rev. Cancer"},{"key":"5428_CR41","doi-asserted-by":"crossref","first-page":"3521","DOI":"10.1007\/s00018-015-1941-z","volume":"72","author":"MB Rust","year":"2015","unstructured":"Rust, M. B. ADF\/cofilin: a crucial regulator of synapse physiology and behavior. Cell Mol. Life Sci. 72, 3521\u20133529 (2015).","journal-title":"Cell Mol. Life Sci."},{"key":"5428_CR42","doi-asserted-by":"crossref","first-page":"R273","DOI":"10.1016\/j.cub.2008.02.002","volume":"18","author":"JR Bamburg","year":"2008","unstructured":"Bamburg, J. R. & Bernstein, B. W. ADF\/cofilin. Curr. Biol. 18, R273\u2013R275 (2008).","journal-title":"Curr. Biol."},{"key":"5428_CR43","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1111\/dgd.12213","volume":"57","author":"K Ohashi","year":"2015","unstructured":"Ohashi, K. Roles of cofilin in development and its mechanisms of regulation. Dev., growth Differ. 57, 275\u2013290 (2015).","journal-title":"Dev., growth Differ."},{"key":"5428_CR44","doi-asserted-by":"crossref","first-page":"2347","DOI":"10.1101\/gad.434307","volume":"21","author":"GC Bellenchi","year":"2007","unstructured":"Bellenchi, G. C. et al. N-cofilin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev. 21, 2347\u20132357 (2007).","journal-title":"Genes Dev."},{"key":"5428_CR45","doi-asserted-by":"crossref","first-page":"628","DOI":"10.1038\/35023579","volume":"2","author":"LS Minamide","year":"2000","unstructured":"Minamide, L. S., Striegl, A. M., Boyle, J. A., Meberg, P. J. & Bamburg, J. R. Neurodegenerative stimuli induce persistent ADF\/cofilin-actin rods that disrupt distal neurite function. Nat. cell Biol. 2, 628\u2013636 (2000).","journal-title":"Nat. cell Biol."},{"key":"5428_CR46","doi-asserted-by":"crossref","first-page":"635","DOI":"10.1002\/cm.20388","volume":"66","author":"JR Bamburg","year":"2009","unstructured":"Bamburg, J. R. & Bloom, G. S. Cytoskeletal pathologies of Alzheimer disease. Cell Motil. Cytoskelet. 66, 635\u2013649 (2009).","journal-title":"Cell Motil. Cytoskelet."},{"key":"5428_CR47","doi-asserted-by":"crossref","DOI":"10.1186\/1478-811X-9-22","volume":"9","author":"DR Adams","year":"2011","unstructured":"Adams, D. R., Ron, D. & Kiely, P. A. RACK1, a multifaceted scaffolding protein: structure and function. Cell Commun. Signal 9, 22 (2011).","journal-title":"Cell Commun. Signal"},{"key":"5428_CR48","doi-asserted-by":"crossref","first-page":"2207","DOI":"10.1002\/dvdy.21217","volume":"236","author":"JL Kadrmas","year":"2007","unstructured":"Kadrmas, J. L., Smith, M. A., Pronovost, S. M. & Beckerle, M. C. Characterization of RACK1 function in Drosophila development. Dev. Dyn. 236, 2207\u20132215 (2007).","journal-title":"Dev. Dyn."},{"key":"5428_CR49","doi-asserted-by":"crossref","first-page":"1439","DOI":"10.1007\/s00018-012-1215-y","volume":"70","author":"V Volta","year":"2013","unstructured":"Volta, V. et al. RACK1 depletion in a mouse model causes lethality, pigmentation deficits and reduction in protein synthesis efficiency. Cell Mol. Life Sci. 70, 1439\u20131450 (2013).","journal-title":"Cell Mol. Life Sci."},{"key":"5428_CR50","doi-asserted-by":"crossref","first-page":"2388","DOI":"10.1242\/jcs.169441","volume":"128","author":"J Dopie","year":"2015","unstructured":"Dopie, J. et al. Genome-wide RNAi screen for nuclear actin reveals a network of cofilin regulators. J. Cell Sci. 128, 2388\u20132400 (2015).","journal-title":"J. Cell Sci."},{"key":"5428_CR51","doi-asserted-by":"crossref","first-page":"2265","DOI":"10.1105\/tpc.107.054395","volume":"20","author":"A Nakashima","year":"2008","unstructured":"Nakashima, A. et al. RACK1 functions in rice innate immunity by interacting with the Rac1 immune complex. Plant Cell 20, 2265\u20132279 (2008).","journal-title":"Plant Cell"},{"key":"5428_CR52","doi-asserted-by":"crossref","first-page":"e1001215","DOI":"10.1371\/journal.pgen.1001215","volume":"6","author":"RS Demarco","year":"2010","unstructured":"Demarco, R. S. & Lundquist, E. A. RACK-1 acts with Rac GTPase signaling and UNC-115\/abLIM in Caenorhabditis elegans axon pathfinding and cell migration. PLoS Genet. 6, e1001215 (2010).","journal-title":"PLoS Genet."},{"key":"5428_CR53","doi-asserted-by":"crossref","first-page":"555","DOI":"10.1007\/s10549-010-0955-3","volume":"126","author":"XX Cao","year":"2011","unstructured":"Cao, X. X. et al. RACK1 promotes breast carcinoma migration\/metastasis via activation of the RhoA\/Rho kinase pathway. Breast Cancer Res. Treat. 126, 555\u2013563 (2011).","journal-title":"Breast Cancer Res. Treat."},{"key":"5428_CR54","doi-asserted-by":"crossref","first-page":"20","DOI":"10.1016\/j.semcdb.2005.11.010","volume":"17","author":"A Prokop","year":"2006","unstructured":"Prokop, A. & Meinertzhagen, I. A. Development and structure of synaptic contacts in Drosophila. Semin Cell Dev. Biol. 17, 20\u201330 (2006).","journal-title":"Semin Cell Dev. Biol."},{"key":"5428_CR55","doi-asserted-by":"crossref","first-page":"204","DOI":"10.1038\/35055120","volume":"3","author":"J Chen","year":"2001","unstructured":"Chen, J. et al. Cofilin\/ADF is required for cell motility during Drosophila ovary development and oogenesis. Nat. Cell Biol. 3, 204\u2013209 (2001).","journal-title":"Nat. Cell Biol."},{"key":"5428_CR56","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1016\/j.tcb.2004.05.002","volume":"14","author":"VO Paavilainen","year":"2004","unstructured":"Paavilainen, V. O., Bertling, E., Falck, S. & Lappalainen, P. Regulation of cytoskeletal dynamics by actin-monomer-binding proteins. Trends Cell Biol. 14, 386\u2013394 (2004).","journal-title":"Trends Cell Biol."},{"key":"5428_CR57","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/j.mcn.2014.07.005","volume":"61","author":"AD Blunk","year":"2014","unstructured":"Blunk, A. D. et al. Postsynaptic actin regulates active zone spacing and glutamate receptor apposition at the Drosophila neuromuscular junction. Mol. Cell Neurosci. 61, 241\u2013254 (2014).","journal-title":"Mol. Cell Neurosci."},{"key":"5428_CR58","doi-asserted-by":"crossref","first-page":"779","DOI":"10.1016\/j.neuron.2004.11.014","volume":"44","author":"J Ng","year":"2004","unstructured":"Ng, J. & Luo, L. Rho GTPases regulate axon growth through convergent and divergent signaling pathways. Neuron 44, 779\u2013793 (2004).","journal-title":"Neuron"},{"key":"5428_CR59","doi-asserted-by":"crossref","first-page":"231","DOI":"10.1093\/jmcb\/mjx015","volume":"9","author":"R Tu","year":"2017","unstructured":"Tu, R. et al. Proteolytic cleavage is required for functional neuroligin 2 maturation and trafficking in Drosophila. J. Mol. Cell Biol. 9, 231\u2013242 (2017).","journal-title":"J. Mol. Cell Biol."},{"key":"5428_CR60","doi-asserted-by":"crossref","first-page":"833","DOI":"10.1016\/j.neuron.2006.02.008","volume":"49","author":"DA Wagh","year":"2006","unstructured":"Wagh, D. A. et al. Bruchpilot, a protein with homology to ELKS\/CAST, is required for structural integrity and function of synaptic active zones in drosophila. Neuron 49, 833\u2013844 (2006).","journal-title":"Neuron"},{"key":"5428_CR61","doi-asserted-by":"crossref","first-page":"313","DOI":"10.1016\/j.biopha.2013.01.011","volume":"67","author":"J Wu","year":"2013","unstructured":"Wu, J. et al. RACK1 promotes the proliferation, migration and invasion capacity of mouse hepatocellular carcinoma cell line in vitro probably by PI3K\/Rac1 signaling pathway. Biomed. Pharmacother. 67, 313\u2013319 (2013).","journal-title":"Biomed. Pharmacother."},{"key":"5428_CR62","doi-asserted-by":"crossref","first-page":"1036","DOI":"10.4103\/1673-5374.211175","volume":"12","author":"L Kershner","year":"2017","unstructured":"Kershner, L. & Welshhans, K. RACK1 regulates neural development. Neural Regen. Res. 12, 1036\u20131039 (2017).","journal-title":"Neural Regen. Res."},{"key":"5428_CR63","doi-asserted-by":"crossref","first-page":"47","DOI":"10.4161\/sgtp.2.1.15062","volume":"2","author":"RS Demarco","year":"2011","unstructured":"Demarco, R. S. & Lundquist, E. A. \u201cRACK\u201d-ing up the effectors: Receptor for activated C kinase acts downstream of Rac GTPase signaling in growth cone outgrowth. Small GTPases 2, 47\u201350 (2011).","journal-title":"Small GTPases"},{"key":"5428_CR64","doi-asserted-by":"crossref","unstructured":"Filho, E. G. F. et al. RACK1 plays a critical role in mast cell secretion and Ca2+ mobilization by modulating F-actin dynamics. J Cell Sci 134, jcs252585 (2021).","DOI":"10.1242\/jcs.252585"},{"key":"5428_CR65","doi-asserted-by":"crossref","first-page":"4661","DOI":"10.1073\/pnas.1813244116","volume":"116","author":"H Yang","year":"2019","unstructured":"Yang, H. et al. Opposite regulation of Wnt\/beta-catenin and Shh signaling pathways by Rack1 controls mammalian cerebellar development. Proc. Natl Acad. Sci. USA 116, 4661\u20134670 (2019).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5428_CR66","doi-asserted-by":"crossref","first-page":"109639","DOI":"10.1016\/j.celrep.2021.109639","volume":"36","author":"Q Zhu","year":"2021","unstructured":"Zhu, Q. et al. Rack1 is essential for corticogenesis by preventing p21-dependent senescence in neural stem cells. Cell Rep. 36, 109639 (2021).","journal-title":"Cell Rep."},{"key":"5428_CR67","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1038\/nature08242","volume":"461","author":"M Machacek","year":"2009","unstructured":"Machacek, M. et al. Coordination of Rho GTPase activities during cell protrusion. Nature 461, 99\u2013103 (2009).","journal-title":"Nature"},{"key":"5428_CR68","doi-asserted-by":"crossref","first-page":"496","DOI":"10.1016\/0166-2236(95)92773-J","volume":"18","author":"DJ Mackay","year":"1995","unstructured":"Mackay, D. J., Nobes, C. D. & Hall, A. The Rho\u2019s progress: a potential role during neuritogenesis for the Rho family of GTPases. Trends Neurosci. 18, 496\u2013501 (1995).","journal-title":"Trends Neurosci."},{"key":"5428_CR69","doi-asserted-by":"crossref","first-page":"53","DOI":"10.1016\/0092-8674(95)90370-4","volume":"81","author":"CD Nobes","year":"1995","unstructured":"Nobes, C. D. & Hall, A. Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53\u201362 (1995).","journal-title":"Cell"},{"key":"5428_CR70","doi-asserted-by":"crossref","first-page":"679","DOI":"10.1242\/jcs.064964","volume":"124","author":"ST Sit","year":"2011","unstructured":"Sit, S. T. & Manser, E. Rho GTPases and their role in organizing the actin cytoskeleton. J. Cell Sci. 124, 679\u2013683 (2011).","journal-title":"J. Cell Sci."},{"key":"5428_CR71","doi-asserted-by":"crossref","first-page":"17582","DOI":"10.1074\/jbc.270.29.17582","volume":"270","author":"BJ Agnew","year":"1995","unstructured":"Agnew, B. J., Minamide, L. S. & Bamburg, J. R. Reactivation of phosphorylated actin depolymerizing factor and identification of the regulatory site. J. Biol. Chem. 270, 17582\u201317587 (1995).","journal-title":"J. Biol. Chem."},{"key":"5428_CR72","doi-asserted-by":"crossref","first-page":"3082","DOI":"10.1038\/s41418-020-0563-7","volume":"27","author":"Y Li","year":"2020","unstructured":"Li, Y. et al. Dual functions of Rack1 in regulating Hedgehog pathway. Cell Death Differ. 27, 3082\u20133096 (2020).","journal-title":"Cell Death Differ."},{"key":"5428_CR73","doi-asserted-by":"crossref","first-page":"3312","DOI":"10.1073\/pnas.0611511104","volume":"104","author":"J Bischof","year":"2007","unstructured":"Bischof, J., Maeda, R. K., Hediger, M., Karch, F. & Basler, K. An optimized transgenesis system for Drosophila using germ-line-specific phiC31 integrases. Proc. Natl Acad. Sci. USA 104, 3312\u20133317 (2007).","journal-title":"Proc. Natl Acad. Sci. USA"},{"key":"5428_CR74","doi-asserted-by":"crossref","first-page":"449","DOI":"10.1083\/jcb.201509023","volume":"212","author":"A Liu","year":"2016","unstructured":"Liu, A. et al. Neuroligin 1 regulates spines and synaptic plasticity via LIMK1\/cofilin-mediated actin reorganization. J. Cell Biol. 212, 449\u2013463 (2016).","journal-title":"J. Cell Biol."},{"key":"5428_CR75","doi-asserted-by":"crossref","first-page":"583","DOI":"10.1002\/dneu.20728","volume":"69","author":"P Ramachandran","year":"2009","unstructured":"Ramachandran, P., Barria, R., Ashley, J. & Budnik, V. A critical step for postsynaptic F-actin organization: regulation of Baz\/Par-3 localization by aPKC and PTEN. Dev. Neurobiol. 69, 583\u2013602 (2009).","journal-title":"Dev. Neurobiol."},{"key":"5428_CR76","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1016\/j.cell.2015.11.034","volume":"164","author":"SK Singh","year":"2016","unstructured":"Singh, S. K. et al. Astrocytes Assemble Thalamocortical Synapses by Bridging NRX1\u03b1 and NL1 via Hevin. Cell 164, 183\u2013196 (2016).","journal-title":"Cell"},{"key":"5428_CR77","doi-asserted-by":"crossref","first-page":"D543","DOI":"10.1093\/nar\/gkab1038","volume":"50","author":"Y Perez-Riverol","year":"2022","unstructured":"Perez-Riverol, Y. et al. The PRIDE database resources in 2022: a hub for mass spectrometry-based proteomics evidences. Nucleic Acids Res. 50, D543\u2013d552 (2022).","journal-title":"Nucleic Acids Res."}],"container-title":["Communications Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.nature.com\/articles\/s42003-023-05428-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-023-05428-3","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/www.nature.com\/articles\/s42003-023-05428-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,11,17]],"date-time":"2023-11-17T07:32:21Z","timestamp":1700206341000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.nature.com\/articles\/s42003-023-05428-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,10,18]]},"references-count":77,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,12]]}},"alternative-id":["5428"],"URL":"https:\/\/doi.org\/10.1038\/s42003-023-05428-3","relation":{},"ISSN":["2399-3642"],"issn-type":[{"value":"2399-3642","type":"electronic"}],"subject":[],"published":{"date-parts":[[2023,10,18]]},"assertion":[{"value":"8 February 2023","order":1,"name":"received","label":"Received","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"6 October 2023","order":2,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"18 October 2023","order":3,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"The authors declare no competing interests.","order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"1056"}}