{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,2]],"date-time":"2026-09-02T11:57:46Z","timestamp":1788350266961,"version":"build-2803163510"},"reference-count":45,"publisher":"Springer Science and Business Media LLC","issue":"2","license":[{"start":{"date-parts":[[2022,2,26]],"date-time":"2022-02-26T00:00:00Z","timestamp":1645833600000},"content-version":"tdm","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0"},{"start":{"date-parts":[[2022,2,26]],"date-time":"2022-02-26T00:00:00Z","timestamp":1645833600000},"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":["Cerebellum"],"abstract":"<jats:title>Abstract\n<\/jats:title><jats:p>Cerebellar hypoplasia and dysplasia encompass a group of clinically and genetically heterogeneous disorders frequently associated with neurodevelopmental impairment. The Neuron Navigator 2 (<jats:italic>NAV2<\/jats:italic>) gene (MIM: 607,026) encodes a member of the Neuron Navigator protein family, widely expressed within the central nervous system (CNS), and particularly abundant in the developing cerebellum. Evidence across different species supports a pivotal function of NAV2 in cytoskeletal dynamics and neurite outgrowth. Specifically, deficiency of <jats:italic>Nav2<\/jats:italic> in mice leads to cerebellar hypoplasia with abnormal foliation due to impaired axonal outgrowth. However, little is known about the involvement of the <jats:italic>NAV2<\/jats:italic> gene in human disease phenotypes. In this study, we identified a female affected with neurodevelopmental impairment and a complex brain and cardiac malformations in which clinical exome sequencing led to the identification of <jats:italic>NAV2<\/jats:italic> biallelic truncating variants. Through protein expression analysis and cell migration assay in patient-derived fibroblasts, we provide evidence linking NAV2 deficiency to cellular migration deficits. In model organisms, the overall CNS histopathology of the <jats:italic>Nav2<\/jats:italic> hypomorphic mouse revealed developmental anomalies including cerebellar hypoplasia and dysplasia, corpus callosum hypo-dysgenesis, and agenesis of the olfactory bulbs. Lastly, we show that the <jats:italic>NAV2<\/jats:italic> ortholog in <jats:italic>Drosophila<\/jats:italic>, <jats:italic>sickie<\/jats:italic> (<jats:italic>sick<\/jats:italic>) is widely expressed in the fly brain, and <jats:italic>sick<\/jats:italic> mutants are mostly lethal with surviving escapers showing neurobehavioral phenotypes. In summary, our results unveil a novel human neurodevelopmental disorder due to genetic loss of <jats:italic>NAV2<\/jats:italic>, highlighting a critical conserved role of the <jats:italic>NAV2<\/jats:italic> gene in brain and cerebellar development across species.<\/jats:p>","DOI":"10.1007\/s12311-022-01379-3","type":"journal-article","created":{"date-parts":[[2022,2,26]],"date-time":"2022-02-26T06:02:47Z","timestamp":1645855367000},"page":"206-222","update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":21,"title":["Loss of Neuron Navigator 2 Impairs Brain and Cerebellar Development"],"prefix":"10.1007","volume":"22","author":[{"given":"Andrea","family":"Accogli","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shenzhao","family":"Lu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ilaria","family":"Musante","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paolo","family":"Scudieri","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jill A.","family":"Rosenfeld","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mariasavina","family":"Severino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Simona","family":"Baldassari","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michele","family":"Iacomino","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonella","family":"Riva","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ganna","family":"Balagura","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Gianluca","family":"Piccolo","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Carlo","family":"Minetti","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Denis","family":"Roberto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Fan","family":"Xia","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Razaali","family":"Razak","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emily","family":"Lawrence","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mohamed","family":"Hussein","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emmanuel Yih-Herng","family":"Chang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michelle","family":"Holick","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Elisa","family":"Cal\u00ec","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Emanuela","family":"Aliberto","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Rosalba","family":"De-Sarro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Antonio","family":"Gambardella","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Undiagnosed Diseases","family":"Network","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"SYNaPS Study","family":"Group","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Emrick","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peter J. A.","family":"McCaffery","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Margaret","family":"Clagett-Dame","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Paul C.","family":"Marcogliese","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Hugo J.","family":"Bellen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Seema R.","family":"Lalani","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Federico","family":"Zara","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pasquale","family":"Striano","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Vincenzo","family":"Salpietro","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2022,2,26]]},"reference":[{"issue":"3","key":"1379_CR1","doi-asserted-by":"publisher","first-page":"282","DOI":"10.1002\/dneu.20875","volume":"72","author":"M Hibi","year":"2012","unstructured":"Hibi M, Shimizu T. Development of the cerebellum and cerebellar neural circuits. Dev Neurobiol. 2012;72(3):282\u2013301. https:\/\/doi.org\/10.1002\/dneu.20875.","journal-title":"Dev Neurobiol"},{"issue":"1","key":"1379_CR2","doi-asserted-by":"publisher","first-page":"151","DOI":"10.1007\/s12311-013-0511-x","volume":"13","author":"LF Koziol","year":"2014","unstructured":"Koziol LF, Budding D, Andreasen N, D\u2019Arrigo S, Bulgheroni S, Imamizu H, et al. Consensus paper: the cerebellum\u2019s role in movement and cognition. Cerebellum. 2014;13(1):151\u201377. https:\/\/doi.org\/10.1007\/s12311-013-0511-x.","journal-title":"Cerebellum"},{"issue":"3","key":"1379_CR3","doi-asserted-by":"publisher","first-page":"350","DOI":"10.1111\/dmcn.14059","volume":"61","author":"EF Pinchefsky","year":"2019","unstructured":"Pinchefsky EF, Accogli A, Shevell MI, Saint-Martin C, Srour M. Developmental outcomes in children with congenital cerebellar malformations. Dev Med Child Neurol. 2019;61(3):350\u20138. https:\/\/doi.org\/10.1111\/dmcn.14059.","journal-title":"Dev Med Child Neurol"},{"key":"1379_CR4","doi-asserted-by":"publisher","unstructured":"Accogli A, Addour-Boudrahem N, Srour M. Diagnostic Approach to Cerebellar Hypoplasia. Cerebellum. 2021;20(4):631\u201358. https:\/\/doi.org\/10.1007\/s12311-020-01224-5.","DOI":"10.1007\/s12311-020-01224-5"},{"issue":"3","key":"1379_CR5","doi-asserted-by":"publisher","first-page":"367","DOI":"10.1016\/j.nic.2019.03.008","volume":"29","author":"M Severino","year":"2019","unstructured":"Severino M, Huisman TAGM. Posterior fossa malformations. Neuroimaging Clin N Am. 2019;29(3):367\u201383. https:\/\/doi.org\/10.1016\/j.nic.2019.03.008.","journal-title":"Neuroimaging Clin N Am"},{"issue":"3","key":"1379_CR6","doi-asserted-by":"publisher","first-page":"606","DOI":"10.1016\/j.ajhg.2019.07.019","volume":"105","author":"KA Aldinger","year":"2019","unstructured":"Aldinger KA, Timms AE, Thomson Z, Mirzaa GM, Bennett JT, Rosenberg AB, et al. Redefining the etiologic landscape of cerebellar malformations. Am J Hum Genet. 2019;105(3):606\u201315. https:\/\/doi.org\/10.1016\/j.ajhg.2019.07.019.","journal-title":"Am J Hum Genet"},{"issue":"1","key":"1379_CR7","doi-asserted-by":"publisher","first-page":"21","DOI":"10.1006\/geno.2002.6799","volume":"80","author":"T Maes","year":"2002","unstructured":"Maes T, Barcel\u00f3 A, Buesa C. Neuron navigator: a human gene family with homology to unc-53, a cell guidance gene from Caenorhabditis elegans. Genomics. 2002;80(1):21\u201330. https:\/\/doi.org\/10.1006\/geno.2002.6799.","journal-title":"Genomics"},{"key":"1379_CR8","doi-asserted-by":"publisher","first-page":"119099","DOI":"10.1016\/j.gep.2020.119099","volume":"35","author":"C Pook","year":"2020","unstructured":"Pook C, Ahrens JM, Clagett-Dame M. Expression pattern of Nav2 in the murine CNS with development. Gene Expr Patterns. 2020;35:119099. https:\/\/doi.org\/10.1016\/j.gep.2020.119099.","journal-title":"Gene Expr Patterns"},{"key":"1379_CR9","doi-asserted-by":"publisher","first-page":"1441","DOI":"10.1002\/dneu.20670","volume":"68","author":"PD Muley","year":"2008","unstructured":"Muley PD, McNeill EM, Marzinke MA, Knobel KM, Barr MM, Clagett-Dame M. The atRA-responsive gene neuron navigator 2 functions in neurite outgrowth and axonal elongation. Dev Neurobiol. 2008;68:1441\u201353. https:\/\/doi.org\/10.1002\/dneu.20670.","journal-title":"Dev Neurobiol"},{"issue":"6","key":"1379_CR10","doi-asserted-by":"publisher","first-page":"3422","DOI":"10.1073\/pnas.052017399","volume":"99","author":"RA Merrill","year":"2002","unstructured":"Merrill RA, Plum LA, Kaiser ME, Clagett-Dame M. A mammalian homolog of unc-53 is regulated by all-trans retinoic acid in neuroblastoma cells and embryos. Proc Natl Acad Sci U S A. 2002;99(6):3422\u20137. https:\/\/doi.org\/10.1073\/pnas.052017399.","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"7","key":"1379_CR11","doi-asserted-by":"publisher","first-page":"739","DOI":"10.1002\/neu.20241","volume":"66","author":"M Clagett-Dame","year":"2006","unstructured":"Clagett-Dame M, McNeill EM. Muley PD Role of all-trans retinoic acid in neurite outgrowth and axonal elongation. J Neurobiol. 2006;66(7):739\u201356. https:\/\/doi.org\/10.1002\/neu.20241.","journal-title":"J Neurobiol"},{"issue":"3","key":"1379_CR12","doi-asserted-by":"publisher","first-page":"365","DOI":"10.1242\/dev.100.3.365","volume":"100","author":"EM Hedgecock","year":"1987","unstructured":"Hedgecock EM, Culotti JG, Hall DH, Stern BD. Genetics of cell and axon migrations in Caenorhabditis elegans. Development. 1987;100(3):365\u201382.","journal-title":"Development"},{"issue":"24","key":"1379_CR13","doi-asserted-by":"publisher","first-page":"4716","DOI":"10.1242\/dev.113308","volume":"141","author":"T Abe","year":"2014","unstructured":"Abe T, Yamazaki D, Murakami S, Hiroi M, Nitta Y, Maeyama Y, Tabata T. The NAV2 homolog Sickie regulates F-actin-mediated axonal growth in Drosophila mushroom body neurons via the non-canonical Rac-Cofilin pathway. Development. 2014;141(24):4716\u201328. https:\/\/doi.org\/10.1242\/dev.113308.","journal-title":"Development"},{"issue":"2","key":"1379_CR14","doi-asserted-by":"publisher","first-page":"331","DOI":"10.1016\/j.ydbio.2011.03.008","volume":"353","author":"EM McNeill","year":"2011","unstructured":"McNeill EM, Kl\u00f6ckner-Bormann M, Roesler EC, Talton LE, Moechars D, Clagett-Dame M. Nav2 hypomorphic mutant mice are ataxic and exhibit abnormalities in cerebellar development. Dev Biol. 2011;353(2):331\u201343. https:\/\/doi.org\/10.1016\/j.ydbio.2011.03.008.","journal-title":"Dev Biol"},{"key":"1379_CR15","doi-asserted-by":"publisher","first-page":"305","DOI":"10.1146\/annurev-genom-083118-014915","volume":"21","author":"DR Azzariti","year":"2020","unstructured":"Azzariti DR, Hamosh A. Genomic data sharing for novel Mendelian disease gene discovery: the matchmaker exchange. Annu Rev Genomics Hum Genet. 2020;21:305\u201326. https:\/\/doi.org\/10.1146\/annurev-genom-083118-014915.","journal-title":"Annu Rev Genomics Hum Genet"},{"issue":"18","key":"1379_CR16","doi-asserted-by":"publisher","first-page":"1870","DOI":"10.1001\/jama.2014.14601","volume":"312","author":"Y Yang","year":"2014","unstructured":"Yang Y, Muzny DM, Xia F, Niu Z, Person R, Ding Y, et al. Molecular findings among patients referred for clinical whole-exome sequencing. JAMA. 2014;312(18):1870\u20139. https:\/\/doi.org\/10.1001\/jama.2014.14601.","journal-title":"JAMA"},{"key":"1379_CR17","doi-asserted-by":"publisher","first-page":"644","DOI":"10.3389\/fnins.2020.00644","volume":"14","author":"M Iacomino","year":"2020","unstructured":"Iacomino M, Baldassari S, Tochigi Y, Ko\u015bla K, Buffelli F, Torella A, et al. Loss of Wwox perturbs neuronal migration and impairs early cortical development. Front Neurosci. 2020;14:644. https:\/\/doi.org\/10.3389\/fnins.2020.00644.","journal-title":"Front Neurosci"},{"key":"1379_CR18","doi-asserted-by":"publisher","unstructured":"Goodman LD, Cope H, Nil Z, Ravenscroft TA, Charng WL, Lu S, et al. TNPO2 variants associate with human developmental delays, neurologic deficits, and dysmorphic features and alter TNPO2 activity in Drosophila. Am J Hum Genet. 2021;108(9):1669\u201391. https:\/\/doi.org\/10.1016\/j.ajhg.2021.06.019.","DOI":"10.1016\/j.ajhg.2021.06.019"},{"key":"1379_CR19","doi-asserted-by":"publisher","first-page":"1568","DOI":"10.1093\/hmg\/ddaa081","volume":"29","author":"D Dutta","year":"2020","unstructured":"Dutta D, Briere LC, Kanca O, Marcogliese PC, Walker MA, High FA, et al. De novo mutations in TOMM70, a receptor of the mitochondrial import translocase, cause neurological impairment. Hum Mol Genet. 2020;29:1568\u201379. https:\/\/doi.org\/10.1093\/hmg\/ddaa081.","journal-title":"Hum Mol Genet"},{"key":"1379_CR20","doi-asserted-by":"publisher","first-page":"e52741","DOI":"10.3791\/52741","volume":"100","author":"ST Madabattula","year":"2015","unstructured":"Madabattula ST, Strautman JC, Bysice AM, O\u2019Sullivan JA, Androschuk A, Rosenfelt C, et al. Quantitative analysis of climbing defects in a Drosophila model of neurodegenerative disorders. J Vis Exp. 2015;100:e52741. https:\/\/doi.org\/10.3791\/52741.","journal-title":"J Vis Exp"},{"issue":"41","key":"1379_CR21","doi-asserted-by":"publisher","first-page":"14145","DOI":"10.1523\/JNEUROSCI.2932-12.2012","volume":"32","author":"L Sun","year":"2012","unstructured":"Sun L, Gilligan J, Staber C, Schutte RJ, Nguyen V, O\u2019Dowd DK, Reenan R. A knock-in model of human epilepsy in Drosophila reveals a novel cellular mechanism associated with heat-induced seizure. J Neurosci. 2012;32(41):14145\u201355. https:\/\/doi.org\/10.1523\/JNEUROSCI.2932-12.2012.","journal-title":"J Neurosci"},{"issue":"7616","key":"1379_CR22","doi-asserted-by":"publisher","first-page":"285","DOI":"10.1038\/nature19057","volume":"536","author":"M Lek","year":"2016","unstructured":"Lek M, Karczewski KJ, Minikel EV, Samocha KE, Banks E, Fennell T, et al. Analysis of protein-coding genetic variation in 60,706 humans. Nature. 2016;536(7616):285\u201391. https:\/\/doi.org\/10.1038\/nature19057.","journal-title":"Nature"},{"key":"1379_CR23","doi-asserted-by":"publisher","unstructured":"Quinodoz M, Royer-Bertrand B, Cisarova K, Di Gioia SA, Superti-Furga A, Rivolta C. DOMINO: Using Machine Learning to Predict Genes Associated with Dominant Disorders. Am J Hum Genet. 2017;101(4):623\u20139. https:\/\/doi.org\/10.1016\/j.ajhg.2017.09.001.","DOI":"10.1016\/j.ajhg.2017.09.001"},{"issue":"1","key":"1379_CR24","doi-asserted-by":"publisher","first-page":"33","DOI":"10.1007\/s00234-015-1601-x","volume":"58","author":"M Severino","year":"2016","unstructured":"Severino M, Tortora D, Pistorio A, Ramenghi LA, Napoli F, Mancardi MM, et al. Expanding the spectrum of congenital anomalies of the diencephalic-mesencephalic junction. Neuroradiology. 2016;58(1):33\u201344. https:\/\/doi.org\/10.1007\/s00234-015-1601-x.","journal-title":"Neuroradiology"},{"key":"1379_CR25","doi-asserted-by":"publisher","unstructured":"Diedrichsen, J. A spatially unbiased atlas template of the human cerebellum. 2006. Neuroimage, 33, 1, p. 127\u2013138. doi: https:\/\/doi.org\/10.1016\/j.neuroimage.2009.01.045.","DOI":"10.1016\/j.neuroimage.2009.01.045"},{"key":"1379_CR26","doi-asserted-by":"publisher","first-page":"1","DOI":"10.3389\/fncel.2012.00027","volume":"6","author":"JA Kim","year":"2012","unstructured":"Kim JA, Connors BW. High temperatures alter physiological properties of pyramidal cells and inhibitory interneurons in hippocampus. Front Cell Neurosci. 2012;6:1\u201312. https:\/\/doi.org\/10.3389\/fncel.2012.00027.","journal-title":"Front Cell Neurosci"},{"key":"1379_CR27","doi-asserted-by":"publisher","first-page":"1","DOI":"10.1016\/j.eplepsyres.2017.04.020","volume":"134","author":"TA Warner","year":"2017","unstructured":"Warner TA, Liu Z, Macdonald RL, Kang JQ. Heat induced temperature dysregulation and seizures in Dravet syndrome\/GEFS+ Gabrg2+\/Q390X mice. Epilepsy Res. 2017;134:1\u20138. https:\/\/doi.org\/10.1016\/j.eplepsyres.2017.04.020.","journal-title":"Epilepsy Res"},{"issue":"1","key":"1379_CR28","doi-asserted-by":"publisher","first-page":"28","DOI":"10.1159\/000346368","volume":"35","author":"Z Mangaru","year":"2013","unstructured":"Mangaru Z, Salem E, Sherman M, Van Dine SE, Bhambri A, Brumberg JC, et al. Neuronal migration defect of the developing cerebellar vermis in substrains of C57BL\/6 mice: cytoarchitecture and prevalence of molecular layer heterotopia. Dev Neurosci. 2013;35(1):28\u201339. https:\/\/doi.org\/10.1159\/000346368.","journal-title":"Dev Neurosci"},{"key":"1379_CR29","doi-asserted-by":"publisher","first-page":"242","DOI":"10.1016\/j.neuroscience.2015.09.025","volume":"310","author":"SE Van Dine","year":"2015","unstructured":"Van Dine SE, Siu NY, Toia A, et al. Cuoco JA1, Betz AJ, Bolivar VJ, Spontaneous malformations of the cerebellar vermis prevalence inheritance and relationship to lobule\/fissure organization in the C57BL\/6 lineage. Neuroscience. 2015;310:242\u201351. https:\/\/doi.org\/10.1016\/j.neuroscience.2015.09.025.","journal-title":"Neuroscience"},{"key":"1379_CR30","doi-asserted-by":"publisher","first-page":"6","DOI":"10.1186\/1749-8104-5-6","volume":"5","author":"EM McNeill","year":"2010","unstructured":"McNeill EM, Roos KP, Moechars D, Clagett-Dame M. Nav2 is necessary for cranial nerve development and blood pressure regulation. Neural Dev. 2010;5:6. https:\/\/doi.org\/10.1186\/1749-8104-5-6.","journal-title":"Neural Dev"},{"issue":"2","key":"1379_CR31","doi-asserted-by":"publisher","first-page":"89","DOI":"10.1016\/j.devbrainres.2004.03.004","volume":"150","author":"PJ Peeters","year":"2004","unstructured":"Peeters PJ, Baker A, Goris I, Daneels G, Verhasselt P, Luyten WHML, et al. Sensory deficits in mice hypomorphic for a mammalian homologue of unc-53. Brain Res Dev Brain Res. 2004;150(2):89\u2013101. https:\/\/doi.org\/10.1016\/j.devbrainres.2004.03.004.","journal-title":"Brain Res Dev Brain Res"},{"key":"1379_CR32","doi-asserted-by":"publisher","first-page":"144","DOI":"10.1016\/j.ydbio.2021.07.007","volume":"478","author":"CE Paisley","year":"2021","unstructured":"Paisley CE, Kay JN. Seeing stars: development and function of retinal astrocytes. Dev Biol. 2021;478:144\u201354. https:\/\/doi.org\/10.1016\/j.ydbio.2021.07.007.","journal-title":"Dev Biol"},{"issue":"10","key":"1379_CR33","doi-asserted-by":"publisher","first-page":"1697","DOI":"10.1002\/glia.23189","volume":"65","author":"ML O'Sullivan","year":"2017","unstructured":"O\u2019Sullivan ML, Pu\u00f1al VM, Kerstein PC, Brzezinski JA 4th, Glaser T, Wright KM, Kay JN. Astrocytes follow ganglion cell axons to establish an angiogenic template during retinal development. Glia. 2017;65(10):1697\u2013716. https:\/\/doi.org\/10.1002\/glia.23189.","journal-title":"Glia"},{"issue":"6","key":"1379_CR34","doi-asserted-by":"publisher","first-page":"e1000142","DOI":"10.1371\/journal.pbio.1000142","volume":"7","author":"EA Lundquist","year":"2009","unstructured":"Lundquist EA. The Finer Points of Filopodia. PLoS Biol. 2009;7(6):e1000142. https:\/\/doi.org\/10.1371\/journal.pbio.1000142.","journal-title":"PLoS Biol"},{"key":"1379_CR35","doi-asserted-by":"publisher","unstructured":"Cooper JA. Cell\u00a0biology in neuroscience: mechanisms of\u00a0cell\u00a0migration\u00a0in the nervous system. J Cell Biol. 201; 202(5):725\u201334 https:\/\/doi.org\/10.1083\/jcb.201305021","DOI":"10.1083\/jcb.201305021"},{"key":"1379_CR36","doi-asserted-by":"publisher","first-page":"315","DOI":"10.1186\/s12967-015-0676-9","volume":"13","author":"H Latifi-Pupovci","year":"2015","unstructured":"Latifi-Pupovci H, Ku\u00e7i Z, Wehner S, B\u00f6nig H, Lieberz R, Klingebiel T, Bader P, Ku\u00e7i S. In vitro migration and proliferation (\u201cwound healing\u201d) potential of mesenchymal stromal cells generated from human CD271(+) bone marrow mononuclear cells. J Transl Med. 2015;13:315. https:\/\/doi.org\/10.1186\/s12967-015-0676-9.","journal-title":"J Transl Med"},{"key":"1379_CR37","doi-asserted-by":"publisher","unstructured":"Mutch CA, Poduri A, Sahin M, Barry B, Walsh CA, Barkovich AJ. Disorders of Microtubule Function in Neurons: Imaging Correlates. AJNR Am J Neuroradiol. 2016;37(3):528\u201335. https:\/\/doi.org\/10.3174\/ajnr.A4552.","DOI":"10.3174\/ajnr.A4552"},{"key":"1379_CR38","doi-asserted-by":"publisher","unstructured":"McGuire SE, Le PT, Davis RL. The role of Drosophila mushroom body signaling in olfactory memory Science. 2001; 293(5533):1330\u20133.\u00a0https:\/\/doi.org\/10.1126\/science.1062622","DOI":"10.1126\/science.1062622"},{"key":"1379_CR39","doi-asserted-by":"publisher","first-page":"20259","DOI":"10.1038\/srep20259","volume":"6","author":"CT Hsu","year":"2016","unstructured":"Hsu CT, Bhandawat V. Organization of descending neurons in Drosophila melanogaster. Sci Rep. 2016;6:20259. https:\/\/doi.org\/10.1038\/srep20259.","journal-title":"Sci Rep"},{"key":"1379_CR40","doi-asserted-by":"publisher","unstructured":"Farris SM. Are mushroom bodies cerebellum-like structures? Arthropod Struct Dev. 2011;40(4):368\u201379. https:\/\/doi.org\/10.1016\/j.asd.2011.02.004.","DOI":"10.1016\/j.asd.2011.02.004"},{"key":"1379_CR41","doi-asserted-by":"publisher","first-page":"e62576","DOI":"10.7554\/eLife.62576","volume":"9","author":"F Li","year":"2020","unstructured":"Li F, Lindsey JW, Marin EC, Otto N, Dreher M, Dempsey G, et al. The connectome of the adult Drosophila mushroom body provides insights into function. Elife. 2020;9:e62576. https:\/\/doi.org\/10.7554\/eLife.62576.","journal-title":"Elife"},{"key":"1379_CR42","doi-asserted-by":"publisher","first-page":"16606","DOI":"10.1073\/pnas.1921294117","volume":"117","author":"AA Apostolopoulou","year":"2020","unstructured":"Apostolopoulou AA, Lin AC. Mechanisms underlying homeostatic plasticity in the Drosophila mushroom body in vivo. Proc Natl Acad Sci USA. 2020;117:16606\u201315. https:\/\/doi.org\/10.1073\/pnas.1921294117.","journal-title":"Proc Natl Acad Sci USA"},{"key":"1379_CR43","doi-asserted-by":"publisher","first-page":"e59542","DOI":"10.3791\/59542","volume":"150","author":"J Wang","year":"2019","unstructured":"Wang J, Liu Z, Bellen HJ, Yamamoto S. Navigating MARRVEL, a Web-based tool that integrates human genomics and model organism genetics information. J Vis Exp. 2019;150:e59542. https:\/\/doi.org\/10.3791\/59542.","journal-title":"J Vis Exp"},{"key":"1379_CR44","doi-asserted-by":"publisher","first-page":"e35574","DOI":"10.7554\/eLife.35574","volume":"7","author":"P-T Lee","year":"2018","unstructured":"Lee P-T, Zirin J, Kanca O, Lin W-W, Schulze KL, Li-Kroeger D, et al. A gene-specific T2A-GAL4 library for Drosophila. Elife. 2018;7:e35574. https:\/\/doi.org\/10.7554\/eLife.35574.","journal-title":"Elife"},{"issue":"14","key":"1379_CR45","doi-asserted-by":"publisher","first-page":"3367","DOI":"10.1242\/dev.129.14.3367","volume":"129","author":"E Stringham","year":"2002","unstructured":"Stringham E, Pujol N, Vandekerckhove J, Bogaert T. unc-53 controls longitudinal migration in C elegans. Development. 2002;129(14):3367\u201379.","journal-title":"Development."}],"container-title":["The Cerebellum"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12311-022-01379-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/article\/10.1007\/s12311-022-01379-3\/fulltext.html","content-type":"text\/html","content-version":"vor","intended-application":"text-mining"},{"URL":"https:\/\/link.springer.com\/content\/pdf\/10.1007\/s12311-022-01379-3.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,3,4]],"date-time":"2023-03-04T06:17:40Z","timestamp":1677910660000},"score":1,"resource":{"primary":{"URL":"https:\/\/link.springer.com\/10.1007\/s12311-022-01379-3"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,2,26]]},"references-count":45,"journal-issue":{"issue":"2","published-online":{"date-parts":[[2023,4]]}},"alternative-id":["1379"],"URL":"https:\/\/doi.org\/10.1007\/s12311-022-01379-3","relation":{},"ISSN":["1473-4230"],"issn-type":[{"value":"1473-4230","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,2,26]]},"assertion":[{"value":"27 January 2022","order":1,"name":"accepted","label":"Accepted","group":{"name":"ArticleHistory","label":"Article History"}},{"value":"26 February 2022","order":2,"name":"first_online","label":"First Online","group":{"name":"ArticleHistory","label":"Article History"}},{"order":1,"name":"Ethics","group":{"name":"EthicsHeading","label":"Declarations"}},{"value":"The authors declare no competing interests.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Conflict of Interest"}}]}}