{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,6,21]],"date-time":"2026-06-21T03:30:54Z","timestamp":1782012654951,"version":"3.54.5"},"reference-count":68,"publisher":"MDPI AG","issue":"11","license":[{"start":{"date-parts":[[2024,10,23]],"date-time":"2024-10-23T00:00:00Z","timestamp":1729641600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Biology"],"abstract":"<jats:p>Over the past two decades, Drosophila\u00a0melanogaster has proven to be successful in modeling the polyglutamine (polyQ) (caused by CAG repeats) family of neurodegenerative disorders, including the faithful recapitulation of pathological features such as polyQ length-dependent formation of protein aggregates and progressive neuronal degeneration. In this study, pan-neuronal expression of human Ataxin-1 with long polyQ repeat of 82 amino acids was driven using an elav-GAL4 driver line. This would essentially model the polyQ disease spinocerebellar ataxia type 1 (SCA1). Longevity and behavioral analysis of male flies expressing human Ataxin-1 revealed compromised lifespan and accelerated locomotor activity deficits both in diurnal activity and negative geotaxis response compared to control flies. Interestingly, this decline in motor response was coupled to an enhancement of matrix metalloproteinase 1 (dMMP1) expression together with declining expression of extracellular matrix (ECM) fibroblast growth factor (FGF) signaling by hedgehog (Hh) and branchless (bnl) and a significant decrease in expression of survival motor neuron gene (dsmn) in old (30 d) flies. Taken together, our results indicate a role for dysregulation of matrix metalloproteinase in polyQ disease with consequent impact on ECM signaling factors, as well as SMN at the neuromuscular junction causing overt physiological and behavioral deficits.<\/jats:p>","DOI":"10.3390\/biology13110854","type":"journal-article","created":{"date-parts":[[2024,10,23]],"date-time":"2024-10-23T04:28:43Z","timestamp":1729657723000},"page":"854","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["Enhanced Age-Dependent Motor Impairment in Males of Drosophila melanogaster Modeling Spinocerebellar Ataxia Type 1 Is Linked to Dysregulation of a Matrix Metalloproteinase"],"prefix":"10.3390","volume":"13","author":[{"given":"Emma M.","family":"Palmer","sequence":"first","affiliation":[{"name":"Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Caleb A.","family":"Snoddy","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Peyton M.","family":"York","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sydney M.","family":"Davis","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Madelyn F.","family":"Hunter","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-6832-259X","authenticated-orcid":false,"given":"Natraj","family":"Krishnan","sequence":"additional","affiliation":[{"name":"Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology, Mississippi State University, Mississippi State, MS 39762, USA"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,10,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","unstructured":"Dugger, B.N., and Dickson, D.W. (2017). Pathology of neurodegenerative diseases. CSH Perspect. Biol., 9.","DOI":"10.1101\/cshperspect.a028035"},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41572-019-0074-3","article-title":"Spinocerebellar ataxia","volume":"5","author":"Klockgether","year":"2019","journal-title":"Nat. Rev. Dis. Primers"},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"291","DOI":"10.1016\/S1474-4422(04)00737-9","article-title":"Autosomal dominant cerebellar ataxias: Clinical features, genetics, and pathogenesis","volume":"3","author":"Bauer","year":"2004","journal-title":"Lancet Neurol."},{"key":"ref_4","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/B978-0-444-64189-2.00010-X","article-title":"Spinocerebellar ataxias","volume":"Volume 155","author":"Manto","year":"2018","journal-title":"Handbook of Clinical Neurology"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"2307","DOI":"10.1093\/hmg\/10.20.2307","article-title":"SCA1 molecular genetics: A history of a 13 year collaboration against glutamines","volume":"10","author":"Orr","year":"2001","journal-title":"Hum. Mol. Genet."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"221","DOI":"10.1038\/ng0793-221","article-title":"Expansion of an unstable trinucleotide CAG repeat in spinocerebellar ataxia type 1","volume":"4","author":"Orr","year":"1993","journal-title":"Nat. Genet."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"562","DOI":"10.1016\/j.cardiores.2005.12.002","article-title":"Structure and function of matrix metalloproteinases and TIMPs","volume":"69","author":"Nagase","year":"2006","journal-title":"Cardiovasc. Res."},{"key":"ref_8","first-page":"155","article-title":"Nuclear localization of catalytically active MMP-2 in endothelial cells and neurons","volume":"6","author":"Sinha","year":"2014","journal-title":"Am. J. Transl. Res."},{"key":"ref_9","doi-asserted-by":"crossref","first-page":"573","DOI":"10.1111\/j.1750-3639.2008.00195.x","article-title":"Brain extracellular matrix in neurodegeneration","volume":"19","author":"Wiley","year":"2009","journal-title":"Brain Pathol."},{"key":"ref_10","doi-asserted-by":"crossref","first-page":"133","DOI":"10.4062\/biomolther.2012.20.2.133","article-title":"Matrix metalloproteinases, new insights into the understanding of neurodegenerative disorders","volume":"20","author":"Kim","year":"2012","journal-title":"Biomol. Ther."},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"620581","DOI":"10.1155\/2015\/620581","article-title":"Friends or foes: Matrix metalloproteinases and their multifaceted roles in neurodegenerative diseases","volume":"2015","author":"Brkic","year":"2015","journal-title":"Mediat. Inflamm."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"1387","DOI":"10.1007\/s00702-014-1205-3","article-title":"Matrix metalloproteinases (MMPs) and their tissue inhibitors (TIMPs) in amyotrophic lateral sclerosis (ALS)","volume":"121","author":"Mroczko","year":"2014","journal-title":"J. Neural Transm."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"190","DOI":"10.1016\/j.bbi.2016.09.002","article-title":"Traumatic brain injury induced matrix metalloproteinase2 cleaves CXCL12\u03b1 (stromal cell derived factor 1\u03b1) and causes neurodegeneration","volume":"59","author":"Conte","year":"2017","journal-title":"Brain Behav. Immun."},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"703","DOI":"10.1007\/s00429-014-0718-8","article-title":"Metalloproteinase-9 contributes to inflammatory glia activation and nigro-striatal pathway degeneration in both mouse and monkey models of 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP)-induced Parkinsonism","volume":"220","author":"Annese","year":"2015","journal-title":"Brain Struct. Funct."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"499","DOI":"10.1242\/dmm.030205","article-title":"Neurodegenerative disease: Models, mechanisms, and a new hope","volume":"10","author":"Gitler","year":"2017","journal-title":"Dis. Models Mech."},{"key":"ref_16","doi-asserted-by":"crossref","unstructured":"Slanzi, A., Iannoto, G., Rossi, B., Zenaro, E., and Constantin, G. (2020). In vitro Models of Neurodegenerative Diseases. Front. Cell Dev. Biol., 8.","DOI":"10.3389\/fcell.2020.00328"},{"key":"ref_17","doi-asserted-by":"crossref","unstructured":"Pereira, I., Lopez-Martinez, M.J., and Samitier, J. (2023). Advances in current in vitro models on neurodegenerative diseases. Front. Bioeng. Biotechnol., 11.","DOI":"10.3389\/fbioe.2023.1260397"},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/978-981-13-0529-0_1","article-title":"Drosophila as a model organism","volume":"1076","author":"Yamaguchi","year":"2018","journal-title":"Adv. Exp. Med. Biol."},{"key":"ref_19","doi-asserted-by":"crossref","first-page":"421","DOI":"10.1203\/00006450-199710000-00001","article-title":"Homeobox genes in embryogenesis and pathogenesis","volume":"42","author":"Mark","year":"1997","journal-title":"Pediatr. Res."},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"377","DOI":"10.1534\/genetics.115.179457","article-title":"Drosophila as an in vivo model for human neurodegenerative disease","volume":"201","author":"McGurk","year":"2015","journal-title":"Genetics"},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/S1084-9521(02)00162-3","article-title":"Modelling human diseases in Drosophila and Caenorhabditis","volume":"14","year":"2003","journal-title":"Semin. Cell Dev. Biol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"315","DOI":"10.1146\/annurev.pathol.3.121806.151529","article-title":"Drosophila models of neurodegenerative diseases","volume":"4","author":"Lu","year":"2009","journal-title":"Annu. Rev. Pathol."},{"key":"ref_23","doi-asserted-by":"crossref","unstructured":"Bolus, H., Crocker, K., Boekhoff-Falk, G., and Chtarbanova, S. (2020). Modeling neurodegenerative disorders in Drosophila melanogaster. Int. J. Mol. Sci., 21.","DOI":"10.3390\/ijms21093055"},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"275","DOI":"10.1080\/19336934.2022.2087484","article-title":"Studies of neurodegenerative diseases using Drosophila and the development of novel approaches for their analysis","volume":"16","author":"Nitta","year":"2022","journal-title":"Fly"},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"25","DOI":"10.1016\/j.expneurol.2015.08.002","article-title":"Studying polyglutamine diseases in Drosophila","volume":"274","author":"Xu","year":"2015","journal-title":"Exp. Neurol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"9","DOI":"10.1186\/2053-8871-1-9","article-title":"Alleviating neurodegeneration in Drosophila models of PolyQ diseases","volume":"1","author":"Long","year":"2014","journal-title":"Cerebellum Ataxias"},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"95","DOI":"10.1016\/S1534-5807(02)00400-8","article-title":"Drosophila matrix metalloproteinases are required for tissue remodeling, but not embryonic development","volume":"4","author":"Serano","year":"2003","journal-title":"Dev. Cell"},{"key":"ref_28","doi-asserted-by":"crossref","unstructured":"LaFever, K.S., Wang, X., Page-McCaw, P., Bhave, G., and Page-McCaw, A. (2017). Both Drosophila matrix metalloproteinases have released and membrane-tethered forms but have different substrates. Sci. Rep., 7.","DOI":"10.1038\/srep44560"},{"key":"ref_29","doi-asserted-by":"crossref","unstructured":"Bedn\u00e1\u0159ov\u00e1, S.H.A., Draughn, B., Johnson, K., Mills, D., Thomas, C., Scales, J., Keenan, E.T., Welcher, J.V., and Krishnan, N. (2021). Expression of Drosophila matrix metalloproteinases in cultured cell lines alters neural and glial cell morphology. Front. Cell. Dev. Biol., 9.","DOI":"10.3389\/fcell.2021.610887"},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"e12729","DOI":"10.1111\/acel.12729","article-title":"Transcriptomics of aged Drosophila motor neurons reveals a matrix metalloproteinase that impairs motor function","volume":"7","author":"Azpurua","year":"2018","journal-title":"Aging Cell."},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"372","DOI":"10.1016\/j.arr.2005.04.001","article-title":"Functional senescence in Drosophila melanogaster","volume":"4","author":"Grotewiel","year":"2005","journal-title":"Ageing Res. Rev."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"401","DOI":"10.1242\/dev.118.2.401","article-title":"Targeted gene expression as a means of altering cell fates and generating dominant phenotypes","volume":"118","author":"Brand","year":"1993","journal-title":"Development"},{"key":"ref_33","doi-asserted-by":"crossref","unstructured":"Bedn\u00e1\u0159ov\u00e1, A., Tom\u010dala, A., Mochanov\u00e1, M., Kodr\u00edk, D., and Krishnan, N. (2018). Disruption of Adipokinetic hormone mediated energy homeostasis has subtle effects on physiology, behavior and lipid status during aging in Drosophila. Front. Physiol., 9.","DOI":"10.3389\/fphys.2018.00949"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"816","DOI":"10.1111\/ejn.13525","article-title":"Disruption of dopamine homeostasis has sexually dimorphic effects on senescence characteristics of Drosophila melanogaster","volume":"45","author":"Hanna","year":"2017","journal-title":"Eur. J. Neurosci."},{"key":"ref_35","doi-asserted-by":"crossref","first-page":"pdb.prot5518","DOI":"10.1101\/pdb.prot5518","article-title":"Locomotor activity level monitoring using the Drosophila Activity Monitoring (DAM) System","volume":"2010","author":"Pfeiffenberger","year":"2010","journal-title":"Cold Spring Harb. Protoc."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"386","DOI":"10.1016\/j.exger.2005.02.005","article-title":"Rapid iterative negative geotaxis (RING): A new method for assessing age-related locomotor decline in Drosophila","volume":"40","author":"Gargano","year":"2005","journal-title":"Exp. Gerontol."},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"1129","DOI":"10.1016\/j.nbd.2011.12.034","article-title":"Loss of circadian clock accelerates aging in neurodegeneration-prone mutants","volume":"45","author":"Krishnan","year":"2012","journal-title":"Neurobiol. Dis."},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"402","DOI":"10.1006\/meth.2001.1262","article-title":"Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method","volume":"25","author":"Livak","year":"2001","journal-title":"Methods"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"76","DOI":"10.1016\/0003-2697(85)90442-7","article-title":"Measurement of protein using bicinchoninic acid","volume":"150","author":"Smith","year":"1985","journal-title":"Anal. Biochem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"680","DOI":"10.1038\/227680a0","article-title":"Cleavage of structural proteins during the assembly of the head of bacteriophage T4","volume":"227","author":"Laemmli","year":"1970","journal-title":"Nature"},{"key":"ref_41","doi-asserted-by":"crossref","unstructured":"Long, K.R., and Huttner, W.B. (2019). How the extracellular matrix shapes neural development. Open Biol., 9.","DOI":"10.1098\/rsob.180216"},{"key":"ref_42","doi-asserted-by":"crossref","unstructured":"Grice, S.J., and Liu, J.L. (2011). Survival motor neuron protein regulates stem cell division, proliferation, and differentiation in Drosophila. PLoS Genet., 7.","DOI":"10.1371\/journal.pgen.1002030"},{"key":"ref_43","doi-asserted-by":"crossref","unstructured":"Shiraishi, R., Tamura, T., Sone, M., and Okazawa, H. (2014). Systematic analysis of fly models with multiple drivers reveals different effects of ataxin-1 and huntingtin in neuron subtype-specific expression. PLoS ONE, 9.","DOI":"10.1371\/journal.pone.0116567"},{"key":"ref_44","doi-asserted-by":"crossref","unstructured":"Oswal, N., Martin, O.M.F., Stroustrup, S., Bruckner, M.A.M., and Stroustrup, N. (2022). A hierarchical process model links behavioral aging and lifespan in C. elegans. PLoS Comput. Biol., 18.","DOI":"10.1371\/journal.pcbi.1010415"},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"193","DOI":"10.1016\/j.exger.2010.08.029","article-title":"Age-associated alterations of the neuromuscular junction","volume":"46","author":"Jang","year":"2011","journal-title":"Exp. Gerontol."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"721","DOI":"10.1016\/j.neubiorev.2009.10.005","article-title":"Motor control and aging: Links to age-related brain structural, functional, and biochemical effects","volume":"34","author":"Seidler","year":"2010","journal-title":"Neurosci. Biobehav. Rev."},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"26045","DOI":"10.1074\/jbc.M116.758839","article-title":"Extension of health span and life span in Drosophila by S107 requires the calstabin homologue FK506-BP2","volume":"291","author":"Azpurua","year":"2016","journal-title":"J. Biol. Chem."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"6319","DOI":"10.1073\/pnas.1118126109","article-title":"Aging impairs intermediate-term behavioral memory by disrupting the dorsal paired medial neuron memory trace","volume":"109","author":"Tonoki","year":"2012","journal-title":"Proc. Natl. Acad. Sci. USA"},{"key":"ref_49","doi-asserted-by":"crossref","first-page":"753","DOI":"10.1016\/j.neuron.2014.09.039","article-title":"Glial dysfunction causes age-related memory impairment in Drosophila","volume":"84","author":"Yamazaki","year":"2014","journal-title":"Neuron"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Liao, S., Broughton, S., and N\u00e4ssel, D.R. (2017). Behavioral senescence and aging-related changes in motor neurons and brain neuromodulator levels are ameliorated by lifespan-extending reproductive dormancy in Drosophila. Front. Cell. Neurosci., 11.","DOI":"10.3389\/fncel.2017.00111"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"205","DOI":"10.1016\/S1474-4422(09)70016-X","article-title":"Matrix metalloproteinases and their multiple roles in neurodegenerative diseases","volume":"8","author":"Rosenberg","year":"2009","journal-title":"Lancet Neurol."},{"key":"ref_52","first-page":"39","article-title":"Metalloproteinases and neurodegenerative diseases: Pathophysiological and therapeutic perspectives","volume":"2","author":"Rosenberg","year":"2015","journal-title":"Met. Med."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"502","DOI":"10.1038\/35081571","article-title":"Metalloproteinases in biology and pathology of the nervous system","volume":"2","author":"Yong","year":"2001","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"931","DOI":"10.1038\/nrn1807","article-title":"Metalloproteinases: Mediators of pathology and regeneration in the CNS","volume":"6","author":"Yong","year":"2005","journal-title":"Nat. Rev. Neurosci."},{"key":"ref_55","first-page":"75","article-title":"Two classes of matrix metalloproteinases reciprocally regulate synaptogenesis","volume":"143","author":"Dear","year":"2016","journal-title":"Development"},{"key":"ref_56","doi-asserted-by":"crossref","unstructured":"Srahna, M., Leyssen, M., Choi, C.M., Fradkin, L.G., Noordermeer, J.N., and Hassan, B.A. (2006). A signaling network for patterning of neuronal connectivity in the Drosophila brain. PLoS Biol., 4.","DOI":"10.1371\/journal.pbio.0040432"},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"463","DOI":"10.1146\/annurev.cellbio.17.1.463","article-title":"How matrix metalloproteinases regulate cell behavior","volume":"17","author":"Sternlicht","year":"2001","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"ref_58","doi-asserted-by":"crossref","first-page":"2627","DOI":"10.1016\/j.celrep.2020.02.006","article-title":"Hedgehog signaling modulates glial proteostasis and lifespan","volume":"30","author":"Rallis","year":"2020","journal-title":"Cell Rep."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s00401-012-1000-x","article-title":"Brain pathology of spinocerebellar ataxias","volume":"124","author":"Seidel","year":"2012","journal-title":"Acta Neuropathol."},{"key":"ref_60","doi-asserted-by":"crossref","unstructured":"McLoughlin, H.S., Moore, L.R., and Paulson, H.L. (2020). Pathogenesis of SCA3 and implications for other polyglutamine diseases. Neurobiol. Dis., 134.","DOI":"10.1016\/j.nbd.2019.104635"},{"key":"ref_61","doi-asserted-by":"crossref","first-page":"3680","DOI":"10.18632\/aging.202331","article-title":"Polyglutamine-expanded ataxin3 alter specific gene expressions through changing DNA methylation status in SCA3\/MJD","volume":"13","author":"Ding","year":"2020","journal-title":"Aging"},{"key":"ref_62","doi-asserted-by":"crossref","first-page":"1668","DOI":"10.1101\/gad.6.9.1668","article-title":"Breathless, a Drosophila FGF receptor homolog, is essential for migration of tracheal and specific midline glial cells","volume":"6","author":"Glazer","year":"1992","journal-title":"Genes Dev."},{"key":"ref_63","doi-asserted-by":"crossref","first-page":"234","DOI":"10.1016\/j.ydbio.2008.02.025","article-title":"Branchless and Hedgehog operate in a positive feedback loop to regulate the initiation of neuroblast division in the Drosophila larval brain","volume":"317","author":"Barrett","year":"2008","journal-title":"Dev. Biol."},{"key":"ref_64","doi-asserted-by":"crossref","first-page":"319","DOI":"10.1016\/S0092-8674(02)01047-4","article-title":"The Drosophila Wnt, wingless, provides an essential signal for pre- and postsynaptic differentiation","volume":"111","author":"Packard","year":"2002","journal-title":"Cell"},{"key":"ref_65","doi-asserted-by":"crossref","first-page":"241","DOI":"10.1016\/S0896-6273(03)00426-4","article-title":"The BMP homolog Gbb provides a retrograde signal that regulates synaptic growth at the Drosophila neuromuscular junction","volume":"39","author":"McCabe","year":"2003","journal-title":"Neuron"},{"key":"ref_66","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1016\/S0092-8674(00)80367-0","article-title":"The spinal muscular atrophy disease gene product, SMN, and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins","volume":"90","author":"Liu","year":"1997","journal-title":"Cell"},{"key":"ref_67","doi-asserted-by":"crossref","unstructured":"Grice, S.J., and Liu, J.L. (2022). Motor defects in a Drosophila model for spinal muscular atrophy result from SMN depletion during early neurogenesis. PLoS Genet., 18.","DOI":"10.1371\/journal.pgen.1010325"},{"key":"ref_68","doi-asserted-by":"crossref","first-page":"481","DOI":"10.1083\/jcb.201004016","article-title":"Modeling spinal muscular atrophy in Drosophila links Smn to FGF signaling","volume":"192","author":"Sen","year":"2011","journal-title":"J. Cell Biol."}],"container-title":["Biology"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/11\/854\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T16:18:17Z","timestamp":1760113097000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2079-7737\/13\/11\/854"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,10,23]]},"references-count":68,"journal-issue":{"issue":"11","published-online":{"date-parts":[[2024,11]]}},"alternative-id":["biology13110854"],"URL":"https:\/\/doi.org\/10.3390\/biology13110854","relation":{},"ISSN":["2079-7737"],"issn-type":[{"value":"2079-7737","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,10,23]]}}}