Lefebvre S, Bürglen L, Reboullet S, Clermont O, Burlet P, Viollet L, et al. Identification and characterization of a spinal muscular atrophy-determining gene. Cell. 1995;80:155–65.
Article
CAS
PubMed
Google Scholar
Rodrigues NR, Owen N, Talbot K, Ignatius J, Dubowitz V, Davies KE. Deletions in the survival motor neuron gene on 5q13 in autosomal recessive spinal muscular atrophy. Hum Mol Genet. 1995;4:631–4.
Article
CAS
PubMed
Google Scholar
Monani UR. Spinal muscular atrophy: a deficiency in a ubiquitous protein; a motor neuron-specific disease. Neuron. 2005;48:885–95.
Article
CAS
PubMed
Google Scholar
Velasco E, Valero C, Valero A, Moreno F, Hernández-Chico C. Molecular analysis of the SMN and NAIP genes in Spanish spinal muscular atrophy (SMA) families and correlation between number of copies of cBCD541 and SMA phenotype. Hum Mol Genet. 1996;5:257–63.
Article
CAS
PubMed
Google Scholar
McAndrew PE, Parsons DW, Simard LR, Rochette C, Ray PN, Mendell JR, et al. Identification of proximal spinal muscular atrophy carriers and patients by analysis of SMNT and SMNC gene copy number. Am J Hum Genet. 1997;60:1411–22.
Article
CAS
PubMed
PubMed Central
Google Scholar
Hoy SM. Nusinersen: a review in 5q spinal muscular atrophy. CNS Drugs. 2018;32:689–96.
Article
PubMed
Google Scholar
Pattali R, Mou Y, Li X-J. AAV9 vector: a novel modality in gene therapy for spinal muscular atrophy. Gene Ther. 2019;26:287–95.
Article
CAS
PubMed
Google Scholar
Dhillon S. Risdiplam: first approval. Drugs. 2020;80:1853–8.
Article
CAS
PubMed
Google Scholar
Ratni H, Ebeling M, Baird J, Bendels S, Bylund J, Chen KS, et al. Discovery of Risdiplam, a selective survival of motor neuron-2 (SMN2) gene splicing modifier for the treatment of spinal muscular atrophy (SMA). J Med Chem. 2018;61:6501–17.
Article
CAS
PubMed
Google Scholar
Finkel RS, Chiriboga CA, Vajsar J, Day JW, Montes J, Vivo DCD, et al. Treatment of infantile-onset spinal muscular atrophy with nusinersen: a phase 2, open-label, dose-escalation study. Lancet. 2016;388:3017–26.
Article
CAS
PubMed
Google Scholar
Pechmann A, Langer T, Schorling D, Stein S, Vogt S, Schara U, et al. Evaluation of children with SMA type 1 under treatment with nusinersen within the expanded access program in germany. J Neuromuscul Dis. 2018;5:135–43.
Article
PubMed
PubMed Central
Google Scholar
Strauss KA, Farrar MA, Muntoni F, Saito K, Mendell JR, Servais L, et al. Onasemnogene abeparvovec for presymptomatic infants with two copies of SMN2 at risk for spinal muscular atrophy type 1: the Phase III SPR1NT trial. Nat Med. 2022;28:1–9.
CAS
Google Scholar
Edinoff AN, Nguyen LH, Odisho AS, Maxey BS, Pruitt JW, Girma B, et al. The antisense oligonucleotide nusinersen for treatment of spinal muscular atrophy. Orthop Rev. 2021;13:24934.
Article
Google Scholar
Murray LM, Comley LH, Thomson D, Parkinson N, Talbot K, Gillingwater TH. Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum Mol Genet. 2008;17:949–62.
Article
CAS
PubMed
Google Scholar
Courtney NL, Mole AJ, Thomson AK, Murray LM. Reduced P53 levels ameliorate neuromuscular junction loss without affecting motor neuron pathology in a mouse model of spinal muscular atrophy. Cell Death Dis. 2019;10:515.
Article
PubMed
PubMed Central
Google Scholar
Buettner JM, Sime Longang JK, Gerstner F, Apel KS, Blanco-Redondo B, Sowoidnich L, et al. Central synaptopathy is the most conserved feature of motor circuit pathology across spinal muscular atrophy mouse models. iScience. 2021;24:103376.
Article
CAS
PubMed
PubMed Central
Google Scholar
Kariya S, Park G-H, Maeno-Hikichi Y, Leykekhman O, Lutz C, Arkovitz MS, et al. Reduced SMN protein impairs maturation of the neuromuscular junctions in mouse models of spinal muscular atrophy. Hum Mol Genet. 2008;17:2552–69.
Article
CAS
PubMed
PubMed Central
Google Scholar
Kong L, Wang X, Choe DW, Polley M, Burnett BG, Bosch-Marcé M, et al. Impaired synaptic vesicle release and immaturity of neuromuscular junctions in spinal muscular atrophy mice. J Neurosci. 2009;29:842–51.
Article
CAS
PubMed
PubMed Central
Google Scholar
Dachs E, Hereu M, Piedrafita L, Casanovas A, Calderó J, Esquerda JE. Defective neuromuscular junction organization and postnatal myogenesis in mice with severe spinal muscular atrophy. J Neuropathol Exp Neurol. 2011;70:444–61.
Article
PubMed
Google Scholar
Ling KKY, Gibbs RM, Feng Z, Ko C-P. Severe neuromuscular denervation of clinically relevant muscles in a mouse model of spinal muscular atrophy. Hum Mol Genet. 2012;21:185–95.
Article
PubMed
CAS
Google Scholar
Dubowitz V. Very severe spinal muscular atrophy (SMA type 0): an expanding clinical phenotype. Eur J Paediatr Neurol. 1999;3:49–51.
Article
CAS
PubMed
Google Scholar
Wadman RI, Wijngaarde CA, Stam M, Bartels B, Otto LA, Lemmink HH, et al. Muscle strength and motor function throughout life in a cross-sectional cohort of 180 patients with spinal muscular atrophy types 1c–4. Eur J Neurol. 2018;25:512–8.
Article
CAS
PubMed
Google Scholar
Deymeer F, Serdaroglu P, Parman Y, Poda M. Natural history of SMA IIIb: muscle strength decreases in a predictable sequence and magnitude. Neurology. 2008;71:644–9.
Article
PubMed
Google Scholar
Murray LM, Lee S, Bäumer D, Parson SH, Talbot K, Gillingwater TH. Pre-symptomatic development of lower motor neuron connectivity in a mouse model of severe spinal muscular atrophy. Hum Mol Genet. 2010;19:420–33.
Article
CAS
PubMed
Google Scholar
Thomson SR, Nahon JE, Mutsaers CA, Thomson D, Hamilton G, Parson SH, et al. Morphological characteristics of motor neurons do not determine their relative susceptibility to degeneration in a mouse model of severe spinal muscular atrophy. PLoS ONE. 2012;7:e52605.
Article
CAS
PubMed
PubMed Central
Google Scholar
Murray LM, Beauvais A, Bhanot K, Kothary R. Defects in neuromuscular junction remodelling in the Smn(2B/-) mouse model of spinal muscular atrophy. Neurobiol Dis. 2013;49:57–67.
Article
CAS
PubMed
Google Scholar
Murray LM, Beauvais A, Gibeault S, Courtney NL, Kothary R. Transcriptional profiling of differentially vulnerable motor neurons at pre-symptomatic stage in the Smn (2b/-) mouse model of spinal muscular atrophy. Acta Neuropathol Commun. 2015;3:55.
Article
PubMed
PubMed Central
CAS
Google Scholar
Comley LH, Nijssen J, Frost-Nylen J, Hedlund E. Cross-disease comparison of amyotrophic lateral sclerosis and spinal muscular atrophy reveals conservation of selective vulnerability but differential neuromuscular junction pathology. J Comp Neurol. 2016;524:1424–42.
Article
PubMed
Google Scholar
Lin T-L, Chen T-H, Hsu Y-Y, Cheng Y-H, Juang B-T, Jong Y-J. Selective neuromuscular denervation in Taiwanese severe SMA mouse can be reversed by morpholino antisense oligonucleotides. PLoS ONE [Internet]. 2016; [cited 2019 Nov 27];11. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4849667/.
Hammond SM, Gogliotti RG, Rao V, Beauvais A, Kothary R, DiDonato CJ. Mouse survival motor neuron alleles that mimic SMN2 splicing and are inducible rescue embryonic lethality early in development but not late. PLOS ONE. Public Library of. Science. 2010;5:e15887.
CAS
Google Scholar
Bowerman M, Murray LM, Beauvais A, Pinheiro B, Kothary R. A critical smn threshold in mice dictates onset of an intermediate spinal muscular atrophy phenotype associated with a distinct neuromuscular junction pathology. Neuromuscul Disord NMD. 2012;22:263–76.
Article
PubMed
Google Scholar
Eshraghi M, McFall E, Gibeault S, Kothary R. Effect of genetic background on the phenotype of the Smn2B/- mouse model of spinal muscular atrophy. Hum Mol Genet. 2016;25:4494–506.
CAS
PubMed
PubMed Central
Google Scholar
Govoni A, Gagliardi D, Comi GP, Corti S. Time is motor neuron: therapeutic window and its correlation with pathogenetic mechanisms in spinal muscular atrophy. Mol Neurobiol. 2018;55:6307–18.
Article
CAS
PubMed
Google Scholar
Comley LH, Kline RA, Thomson AK, Woschitz V, Landeros EV, Osman EY, et al. Motor unit recovery following Smn restoration in mouse models of spinal muscular atrophy. Hum Mol Genet. 2022;12:ddac097.
Google Scholar
Kariyawasam D, D’Silva A, Howells J, Herbert K, Geelan-Small P, Lin CS-Y, et al. Motor unit changes in children with symptomatic spinal muscular atrophy treated with nusinersen. J Neurol Neurosurg Psychiatry. 2020;jnnp-2020:324254.
Google Scholar
Hedlund E, Karlsson M, Osborn T, Ludwig W, Isacson O. Global gene expression profiling of somatic motor neuron populations with different vulnerability identify molecules and pathways of degeneration and protection. Brain. 2010;133:2313–30.
Article
PubMed
PubMed Central
Google Scholar
Brockington A, Ning K, Heath PR, Wood E, Kirby J, Fusi N, et al. Unravelling the enigma of selective vulnerability in neurodegeneration: motor neurons resistant to degeneration in ALS show distinct gene expression characteristics and decreased susceptibility to excitotoxicity. Acta Neuropathol (Berl). 2013;125:95–109.
Article
CAS
Google Scholar
Kaplan A, Spiller KJ, Towne C, Kanning KC, Choe GT, Geber A, et al. Neuronal matrix metalloproteinase-9 is a determinant of selective neurodegeneration. Neuron. 2014;81:333–48.
Article
CAS
PubMed
PubMed Central
Google Scholar
Nizzardo M, Taiana M, Rizzo F, Aguila Benitez J, Nijssen J, Allodi I, et al. Synaptotagmin 13 is neuroprotective across motor neuron diseases. Acta Neuropathol (Berl). 2020;139:837–53.
Article
CAS
Google Scholar
Boyd PJ, Tu W-Y, Shorrock HK, Groen EJN, Carter RN, Powis RA, et al. Bioenergetic status modulates motor neuron vulnerability and pathogenesis in a zebrafish model of spinal muscular atrophy. PLOS Genet. 2017;13:e1006744.
Article
PubMed
PubMed Central
CAS
Google Scholar
Nichterwitz S, Nijssen J, Storvall H, Schweingruber C, Comley LH, Allodi I, et al. LCM-seq reveals unique transcriptional adaptation mechanisms of resistant neurons and identifies protective pathways in spinal muscular atrophy. Genome Res. 2020; [cited 2021 May 17]; Available from: https://genome.cshlp.org/content/early/2020/08/12/gr.265017.120.
Kline RA, Kaifer KA, Osman EY, Carella F, Tiberi A, Ross J, et al. Comparison of independent screens on differentially vulnerable motor neurons reveals alpha-synuclein as a common modifier in motor neuron diseases. PLoS Genet. 2017;13:e1006680.
Article
PubMed
PubMed Central
CAS
Google Scholar
Villalón E, Kline RA, Smith CE, Lorson ZC, Osman EY, O’Day S, et al. AAV9-Stathmin1 gene delivery improves disease phenotype in an intermediate mouse model of spinal muscular atrophy. Hum Mol Genet. 2019;28:3742–54.
Article
PubMed
PubMed Central
CAS
Google Scholar
Murray LM, Comley LH, Gillingwater TH, Parson SH. The response of neuromuscular junctions to injury is developmentally regulated. FASEB J. 2011;25:1306–13.
Article
CAS
PubMed
Google Scholar
Mole AJ, Bell S, Thomson AK, Dissanayake KN, Ribchester RR, Murray LM. Synaptic withdrawal following nerve injury is influenced by postnatal maturity, muscle-specific properties, and the presence of underlying pathology in mice. J Anat. 2020; [cited 2020 Jun 15];n/a. Available from: https://onlinelibrary.wiley.com/doi/abs/10.1111/joa.13187.
Van BS, Groothuis-Oudshoorn K. mice: multivariate imputation by chained equations in R. J Stat Softw. 2011;45:1–67.
Google Scholar
Love MI, Huber W, Anders S. Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2. Genome Biol. 2014;15:550.
Article
PubMed
PubMed Central
CAS
Google Scholar
Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, et al. The STRING database in 2017: quality-controlled protein–protein association networks, made broadly accessible. Nucleic Acids Res. 2017;45:D362–8.
Article
CAS
PubMed
Google Scholar
Pun S, Santos AF, Saxena S, Xu L, Caroni P. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci. 2006;9:408–19.
Article
CAS
PubMed
Google Scholar
Nijssen J, Comley LH, Hedlund E. Motor neuron vulnerability and resistance in amyotrophic lateral sclerosis. Acta Neuropathol (Berl). 2017;133:863–85.
Article
Google Scholar
Pun S, Sigrist M, Santos AF, Ruegg MA, Sanes JR, Jessell TM, et al. An intrinsic distinction in neuromuscular junction assembly and maintenance in different skeletal muscles. Neuron. Elsevier. 2002;34:357–70.
Article
CAS
Google Scholar
Mentis GZ, Blivis D, Liu W, Drobac E, Crowder ME, Kong L, et al. Early functional impairment of sensory-motor connectivity in a mouse model of spinal muscular atrophy. Neuron. 2011;69:453–67.
Article
CAS
PubMed
PubMed Central
Google Scholar
d’Errico P, Boido M, Piras A, Valsecchi V, De Amicis E, Locatelli D, et al. Selective vulnerability of spinal and cortical motor neuron subpopulations in delta7 SMA mice. PLoS ONE. 2013; [cited 2019 Sep 9];8. Available from: https://www.ncbi.nlm.nih.gov/pmc/articles/PMC3855775/.
Hsieh-Li HM, Chang J-G, Jong Y-J, Wu M-H, Wang NM, Tsai CH, et al. A mouse model for spinal muscular atrophy. Nat Genet. 2000;24:66–70.
Article
CAS
PubMed
Google Scholar
Monani UR, Sendtner M, Coovert DD, Parsons DW, Andreassi C, Le TT, et al. The human centromeric survival motor neuron gene (SMN2) rescues embryonic lethality in Smn–/– mice and results in a mouse with spinal muscular atrophy. Hum Mol Genet. 2000;9:333–9.
Article
CAS
PubMed
Google Scholar
Le TT, Pham LT, Butchbach MER, Zhang HL, Monani UR, Coovert DD, et al. SMNΔ7, the major product of the centromeric survival motor neuron (SMN2) gene, extends survival in mice with spinal muscular atrophy and associates with full-length SMN. Hum Mol Genet. 2005;14:845–57.
Article
CAS
PubMed
Google Scholar
Kline RA, Dissanayake KN, Hurtado ML, Martínez NW, Ahl A, Mole AJ, et al. Altered mitochondrial bioenergetics are responsible for the delay in Wallerian degeneration observed in neonatal mice. Neurobiol Dis. 2019;130:104496.
Article
CAS
PubMed
PubMed Central
Google Scholar
Kim Y, Yang DS, Katti P, Glancy B. Protein composition of the muscle mitochondrial reticulum during postnatal development. J Physiol. 2019;597:2707–27.
Article
CAS
PubMed
PubMed Central
Google Scholar
Lauria F, Bernabò P, Tebaldi T, Groen EJN, Perenthaler E, Maniscalco F, et al. SMN-primed ribosomes modulate the translation of transcripts related to spinal muscular atrophy. Nat Cell Biol. 2020;22:1239–51.
Article
CAS
PubMed
PubMed Central
Google Scholar
Sanchez G, Dury AY, Murray LM, Biondi O, Tadesse H, El Fatimy R, et al. A novel function for the survival motoneuron protein as a translational regulator. Hum Mol Genet. 2013;22:668–84.
Article
CAS
PubMed
Google Scholar
Martinez-Salas E, Embarc-Buh A, Francisco-Velilla R. Emerging roles of Gemin5: from snRNPs assembly to translation control. Int J Mol Sci. 2020;21:E3868.
Article
PubMed
CAS
Google Scholar
Singh RN, Howell MD, Ottesen EW, Singh NN. Diverse role of survival motor neuron protein. Biochim Biophys Acta Gene Regul Mech. 2017;1860:299–315.
Article
CAS
PubMed
Google Scholar
Nicolas A, Kenna KP, Renton AE, Ticozzi N, Faghri F, Chia R, et al. Genome-wide analyses identify KIF5A as a novel ALS gene. Neuron. 2018;97:1268–1283.e6.
Article
CAS
PubMed
PubMed Central
Google Scholar
Shi P, Ström A-L, Gal J, Zhu H. Effects of ALS-related SOD1 mutants on dynein- and KIF5-mediated retrograde and anterograde axonal transport. Biochim Biophys Acta. 2010;1802:707–16.
Article
CAS
PubMed
PubMed Central
Google Scholar
Fallini C, Bassell GJ, Rossoll W. Spinal muscular atrophy: the role of SMN in axonal mRNA regulation. Brain Res. 2012;1462:81–92.
Article
CAS
PubMed
PubMed Central
Google Scholar
Fallini C, Zhang H, Su Y, Silani V, Singer RH, Rossoll W, et al. The survival of motor neuron (SMN) protein interacts with the mRNA-binding protein HuD and regulates localization of poly(A) mRNA in primary motor neuron axons. J Neurosci. 2011;31:3914–25.
Article
CAS
PubMed
PubMed Central
Google Scholar
Dombert B, Sivadasan R, Simon CM, Jablonka S, Sendtner M. Presynaptic Localization of Smn and hnRNP R in axon terminals of embryonic and postnatal mouse motoneurons. PLOS ONE. Public Library of. Science. 2014;9:e110846.
Google Scholar
Pletto D, Capra S, Finardi A, Colciaghi F, Nobili P, Battaglia GS, et al. Axon outgrowth and neuronal differentiation defects after a-SMN and FL-SMN silencing in primary hippocampal cultures. PLOS ONE. Public Library of. Science. 2018;13:e0199105.
Google Scholar
Pagliardini S, Giavazzi A, Setola V, Lizier C, Di Luca M, DeBiasi S, et al. Subcellular localization and axonal transport of the survival motor neuron (SMN) protein in the developing rat spinal cord. Hum Mol Genet. 2000;9:47–56.
Article
CAS
PubMed
Google Scholar
Bartolome F, Esteras N, Martin-Requero A, Boutoleau-Bretonniere C, Vercelletto M, Gabelle A, et al. Pathogenic p62/SQSTM1 mutations impair energy metabolism through limitation of mitochondrial substrates. Sci Rep. 2017;7:1666.
Article
PubMed
PubMed Central
CAS
Google Scholar
Lee M, Shin J. Triage of oxidation-prone proteins by Sqstm1/p62 within the mitochondria. Biochem Biophys Res Commun. 2011;413:122–7.
Article
CAS
PubMed
Google Scholar
Seibenhener ML, Du Y, Diaz-Meco M-T, Moscat J, Wooten MC, Wooten MW. A role for sequestosome 1/p62 in mitochondrial dynamics, import and genome integrity. Biochim Biophys Acta. 2013;1833:452–9.
Article
CAS
PubMed
Google Scholar
de Castro IP, Costa AC, Celardo I, Tufi R, Dinsdale D, Loh SHY, et al. Drosophila ref(2) P is required for the parkin-mediated suppression of mitochondrial dysfunction in pink1 mutants. Cell Death Dis. 2013;4:e873.
Article
PubMed
PubMed Central
CAS
Google Scholar