{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,6]],"date-time":"2026-10-06T09:45:51Z","timestamp":1791279951170,"version":"4.1.0"},"reference-count":71,"publisher":"Oxford University Press (OUP)","issue":"7","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2014,4,1]]},"abstract":"<jats:title>Abstract<\/jats:title>\n                  <jats:p>Spinal muscular atrophy (SMA) is a progressive neurodegenerative disease affecting lower motor neurons. SMA is caused by mutations in the Survival Motor Neuron 1 (SMN1) gene, which result in reduced levels of functional SMN protein. Biochemical studies have linked the ubiquitously expressed SMN protein to the assembly of pre-mRNA processing U snRNPs, raising the possibility that aberrant splicing is a major defect in SMA. Accordingly, several transcripts affected upon SMN deficiency have been reported. A second function for SMN in axonal mRNA transport has also been proposed that may likewise contribute to the SMA phenotype. The underlying etiology of SMA, however, is still not fully understood. Here, we have used a combination of genomics and live Ca2+ imaging to investigate the consequences of SMN deficiency in a zebrafish model of SMA. In a transcriptome analyses of SMN-deficient zebrafish, we identified neurexin2a (nrxn2a) as strongly down-regulated and displaying changes in alternative splicing patterns. Importantly, the knock-down of two distinct nrxn2a isoforms phenocopies SMN-deficient fish and results in a significant reduction of motor axon excitability. Interestingly, we observed altered expression and splicing of Nrxn2 also in motor neurons from the Smn\u2212\/\u2212;SMN2+\/+ mouse model of SMA, suggesting conservation of nrxn2 regulation by SMN in mammals. We propose that SMN deficiency affects splicing and abundance of nrxn2a. This may explain the pre-synaptic defects at neuromuscular endplates in SMA pathophysiology.<\/jats:p>","DOI":"10.1093\/hmg\/ddt567","type":"journal-article","created":{"date-parts":[[2013,11,11]],"date-time":"2013-11-11T21:23:29Z","timestamp":1384205009000},"page":"1754-1770","source":"Crossref","is-referenced-by-count":78,"title":["<i>SMN<\/i>\n                    deficiency alters\n                    <i>Nrxn2<\/i>\n                    expression and splicing in zebrafish and mouse models of spinal muscular atrophy"],"prefix":"10.1093","volume":"23","author":[{"given":"Kelvin","family":"See","sequence":"first","affiliation":[{"name":"1 \u00a0Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"},{"name":"2 \u00a0NUS Centre for BioImaging Sciences (CBIS), Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Preeti","family":"Yadav","sequence":"additional","affiliation":[{"name":"3 \u00a0Institute for Clinical Neurobiology, University of Wuerzburg, Wuerzburg 97078, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Marieke","family":"Giegerich","sequence":"additional","affiliation":[{"name":"4 \u00a0Department of Biochemistry, University of Wuerzburg, Wuerzburg 97074, Germany and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Pearl S.","family":"Cheong","sequence":"additional","affiliation":[{"name":"1 \u00a0Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"},{"name":"2 \u00a0NUS Centre for BioImaging Sciences (CBIS), Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martin","family":"Graf","sequence":"additional","affiliation":[{"name":"1 \u00a0Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"},{"name":"2 \u00a0NUS Centre for BioImaging Sciences (CBIS), Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Himanshu","family":"Vyas","sequence":"additional","affiliation":[{"name":"1 \u00a0Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"},{"name":"2 \u00a0NUS Centre for BioImaging Sciences (CBIS), Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Serene G. P.","family":"Lee","sequence":"additional","affiliation":[{"name":"5 \u00a0Genome Institute of Singapore, Singapore 138672, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sinnakaruppan","family":"Mathavan","sequence":"additional","affiliation":[{"name":"5 \u00a0Genome Institute of Singapore, Singapore 138672, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Utz","family":"Fischer","sequence":"additional","affiliation":[{"name":"4 \u00a0Department of Biochemistry, University of Wuerzburg, Wuerzburg 97074, Germany and"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Michael","family":"Sendtner","sequence":"additional","affiliation":[{"name":"3 \u00a0Institute for Clinical Neurobiology, University of Wuerzburg, Wuerzburg 97078, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Christoph","family":"Winkler","sequence":"additional","affiliation":[{"name":"1 \u00a0Department of Biological Sciences, National University of Singapore, Singapore 117543, Singapore"},{"name":"2 \u00a0NUS Centre for BioImaging Sciences (CBIS), Singapore, Singapore"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2013,11,11]]},"reference":[{"key":"2022050522053760600_DDT567C1","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1016\/0092-8674(95)90460-3","article-title":"Identification and characterization of a spinal muscular atrophy-determining gene","volume":"80","author":"Lefebvre","year":"1995","journal-title":"Cell"},{"key":"2022050522053760600_DDT567C2","doi-asserted-by":"publisher","first-page":"276","DOI":"10.1001\/archneur.1971.00490030102014","article-title":"Two early infantile hereditary cases of progressive muscular atrophy simulating dystrophy, but on a neural basis. 1891","volume":"25","author":"Werdnig","year":"1971","journal-title":"Arch. Neurol."},{"key":"2022050522053760600_DDT567C3","doi-asserted-by":"publisher","first-page":"1177","DOI":"10.1093\/hmg\/8.7.1177","article-title":"A single nucleotide difference that alters splicing patterns distinguishes the SMA gene SMN1 from the copy gene SMN2","volume":"8","author":"Monani","year":"1999","journal-title":"Hum. Mol. Genet."},{"key":"2022050522053760600_DDT567C4","doi-asserted-by":"publisher","first-page":"460","DOI":"10.1038\/ng1207","article-title":"A negative element in SMN2 exon 7 inhibits splicing in spinal muscular atrophy","volume":"34","author":"Kashima","year":"2003","journal-title":"Nat. Genet."},{"key":"2022050522053760600_DDT567C5","doi-asserted-by":"publisher","first-page":"3149","DOI":"10.1093\/hmg\/ddm276","article-title":"hnRNP A1 functions with specificity in repression of SMN2 exon 7 splicing","volume":"16","author":"Kashima","year":"2007","journal-title":"Hum. Mol. Genet."},{"key":"2022050522053760600_DDT567C6","doi-asserted-by":"publisher","first-page":"307","DOI":"10.1002\/ajmg.a.30251","article-title":"Homozygous SMN1 deletions in unaffected family members and modification of the phenotype by SMN2","volume":"130A","author":"Prior","year":"2004","journal-title":"Am. J. Med. Genet. A"},{"key":"2022050522053760600_DDT567C7","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1093\/hmg\/9.3.333","article-title":"The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn(\u2212\/\u2212) mice and results in a mouse with spinal muscular atrophy","volume":"9","author":"Monani","year":"2000","journal-title":"Hum. Mol. Genet."},{"key":"2022050522053760600_DDT567C8","doi-asserted-by":"publisher","first-page":"265","DOI":"10.1038\/ng0797-265","article-title":"Correlation between severity and SMN protein level in spinal muscular atrophy","volume":"16","author":"Lefebvre","year":"1997","journal-title":"Nat Genet."},{"key":"2022050522053760600_DDT567C9","doi-asserted-by":"publisher","first-page":"1411","DOI":"10.1086\/515465","article-title":"Identification of proximal spinal muscular atrophy carriers and patients by analysis of SMNT and SMNC gene copy number","volume":"60","author":"McAndrew","year":"1997","journal-title":"Am. J. Hum. Genet."},{"key":"2022050522053760600_DDT567C10","doi-asserted-by":"publisher","first-page":"1205","DOI":"10.1093\/hmg\/6.8.1205","article-title":"The survival motor neuron protein in spinal muscular atrophy","volume":"6","author":"Coovert","year":"1997","journal-title":"Hum. Mol. 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Cell Biol."},{"key":"2022050522053760600_DDT567C14","doi-asserted-by":"publisher","first-page":"1023","DOI":"10.1016\/S0092-8674(00)80368-2","article-title":"The SMN-SIP1 complex has an essential role in spliceosomal snRNP biogenesis","volume":"90","author":"Fischer","year":"1997","journal-title":"Cell"},{"key":"2022050522053760600_DDT567C15","doi-asserted-by":"publisher","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":"2022050522053760600_DDT567C16","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1016\/S0092-8674(00)81632-3","article-title":"A novel function for SMN, the spinal muscular atrophy disease gene product, in pre-mRNA splicing","volume":"95","author":"Pellizzoni","year":"1998","journal-title":"Cell"},{"key":"2022050522053760600_DDT567C17","doi-asserted-by":"publisher","first-page":"333","DOI":"10.1146\/annurev.genet.36.043002.091635","article-title":"Allosteric cascade of spliceosome activation","volume":"36","author":"Brow","year":"2002","journal-title":"Annu. Rev. Genet."},{"key":"2022050522053760600_DDT567C18","doi-asserted-by":"publisher","first-page":"585","DOI":"10.1016\/j.cell.2008.03.031","article-title":"SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing","volume":"133","author":"Zhang","year":"2008","journal-title":"Cell"},{"key":"2022050522053760600_DDT567C19","doi-asserted-by":"publisher","first-page":"2320","DOI":"10.1101\/gad.342005","article-title":"Reduced U snRNP assembly causes motor axon degeneration in an animal model for spinal muscular atrophy","volume":"19","author":"Winkler","year":"2005","journal-title":"Genes Dev."},{"key":"2022050522053760600_DDT567C20","doi-asserted-by":"publisher","first-page":"e921","DOI":"10.1371\/journal.pone.0000921","article-title":"Ribonucleoprotein assembly defects correlate with spinal muscular atrophy severity and preferentially affect a subset of spliceosomal snRNPs","volume":"2","author":"Gabanella","year":"2007","journal-title":"PLoS One"},{"key":"2022050522053760600_DDT567C21","doi-asserted-by":"publisher","first-page":"440","DOI":"10.1016\/j.cell.2012.09.012","article-title":"An SMN-dependent U12 splicing event essential for motor circuit function","volume":"151","author":"Lotti","year":"2012","journal-title":"Cell"},{"key":"2022050522053760600_DDT567C22","doi-asserted-by":"publisher","first-page":"641","DOI":"10.1093\/hmg\/ddq508","article-title":"Impaired minor tri-snRNP assembly generates differential splicing defects of U12-type introns in lymphoblasts derived from a type I SMA patient","volume":"20","author":"Boulisfane","year":"2011","journal-title":"Hum. Mol. Genet."},{"key":"2022050522053760600_DDT567C23","doi-asserted-by":"publisher","first-page":"427","DOI":"10.1016\/j.cell.2012.09.011","article-title":"SMN Is Required for Sensory-Motor Circuit Function in Drosophila","volume":"151","author":"Imlach","year":"2012","journal-title":"Cell"},{"key":"2022050522053760600_DDT567C24","doi-asserted-by":"publisher","first-page":"1605","DOI":"10.1093\/hmg\/11.14.1605","article-title":"Survival motor neuron (SMN) protein: role in neurite outgrowth and neuromuscular maturation during neuronal differentiation and development","volume":"11","author":"Fan","year":"2002","journal-title":"Hum. Mol. 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Neurosci."},{"key":"2022050522053760600_DDT567C29","doi-asserted-by":"publisher","first-page":"2552","DOI":"10.1093\/hmg\/ddn156","article-title":"Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy","volume":"17","author":"Kariya","year":"2008","journal-title":"Hum. Mol. Genet."},{"key":"2022050522053760600_DDT567C30","doi-asserted-by":"publisher","first-page":"2900","DOI":"10.1093\/hmg\/ddn189","article-title":"Embryonic motor axon development in the severe SMA mouse","volume":"17","author":"McGovern","year":"2008","journal-title":"Hum. Mol. Genet."},{"key":"2022050522053760600_DDT567C31","doi-asserted-by":"publisher","first-page":"849","DOI":"10.1523\/JNEUROSCI.4496-09.2010","article-title":"Altered intracellular Ca2+ homeostasis in nerve terminals of severe spinal muscular atrophy mice","volume":"30","author":"Ruiz","year":"2010","journal-title":"J. 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