Akten B, Kye MJ, Hao le T, Wertz MH, Singh S, Nie D, Huang J, Merianda TT, Twiss JL, Beattie CE, et al (2011) Interaction of survival of motor neuron (SMN) and HuD proteins with mRNA cpg15 rescues motor neuron axonal deficits. Proc Natl Acad Sci U S A 108: 10337–10342. doi:10.1073/ pnas.1104928108
Ando S, Tanaka M, Chinen N, Nakamura S, Shimazawa M, Hara H (2020) SMN protein contributes to skeletal muscle cell maturation via caspase-3 and akt activation. In Vivo 34: 3247–3254. doi:10.21873/invivo.12161
Boyer JG, Murray LM, Scott K, De Repentigny Y, Renaud JM, Kothary R (2013) Early onset muscle weakness and disruption of muscle proteins in mouse models of spinal muscular atrophy. Skelet Muscle 3: 24. doi:10.1186/2044-5040-3-24
Bricceno KV, Martinez T, Leikina E, Duguez S, Partridge TA, Chernomordik LV, Fischbeck KH, Sumner CJ, Burnett BG (2014) Survival motor neuron protein deficiency impairs myotube formation by altering myogenic gene expression and focal adhesion dynamics. Hum Mol Genet 23: 4745–4757. doi:10.1093/hmg/ddu189
Burghes AHM, Beattie CE (2009) Spinal muscular atrophy: Why do low levels of survival motor neuron protein make motor neurons sick? Nat Rev Neurosci 10: 597–609. doi:10.1038/nrn2670
Cesana M, Cacchiarelli D, Legnini I, Santini T, Sthandier O, Chinappi M, Tramontano A, Bozzoni I (2011) A long noncoding RNA controls muscle differentiation by functioning as a competing endogenous RNA. Cell 147: 358–369. doi:10.1016/j.cell.2011.09.028
Chen JF, Mandel EM, Thomson JM, Wu Q, Callis TE, Hammond SM, Conlon FL, Wang DZ (2006) The role of microRNA-1 and microRNA-133 in skeletal muscle proliferation and differentiation. Nat Genet 38: 228–233. doi:10.1038/ng1725
Chen JF, Tao Y, Li J, Deng Z, Yan Z, Xiao X, Wang DZ (2010) microRNA-1 and microRNA-206 regulate skeletal muscle satellite cell proliferation and differentiation by repressing Pax7. J Cell Biol 190: 867–879. doi:10.1083/ jcb.200911036
De Vivo DC, Bertini E, Swoboda KJ, Hwu WL, Crawford TO, Finkel RS, Kirschner J, Kuntz NL, Parsons JA, Ryan MM, et al (2019) Nusinersen initiated in infants during the presymptomatic stage of spinal muscular atrophy: Interim efficacy and safety results from the Phase 2 NURTURE study. Neuromuscul Disord 29: 842–856. doi:10.1016/j.nmd.2019.09.007
Finkel RS, Chiriboga CA, Vajsar J, Day JW, Montes J, De Vivo DC, Yamashita M, Rigo F, Hung G, Schneider E, et al (2016) Treatment of infantile-onset spinal muscular atrophy with nusinersen: A phase 2, open-label, dose-escalation study. Lancet 388: 3017–3026. doi:10.1016/S0140-6736(16)31408-8
Finkel RS, Mercuri E, Darras BT, Connolly AM, Kuntz NL, Kirschner J, Chiriboga CA, Saito K, Servais L, Tizzano E, et al (2017) Nusinersen versus sham control in infantile-onset spinal muscular atrophy. N Engl J Med 377: 1723–1732. doi:10.1056/NEJMoa1702752
Frangini M, Franzolin E, Chemello F, Laveder P, Romualdi C, Bianchi V, Rampazzo C (2013) Synthesis of mitochondrial DNA precursors during myogenesis, an analysis in purified C2C12 myotubes. J Biol Chem 288: 5624–5635. doi:10.1074/jbc.M112.441147
Grunseich C, Wang IX, Watts JA, Burdick JT, Guber RD, Zhu Z, Bruzel A, Lanman T, Chen K, Schindler AB, et al (2018) Senataxin mutation reveals how R-loops promote transcription by blocking DNA methylation at gene promoters. Mol Cell 69: 426–437.e7. doi:10.1016/j.molcel.2017.12.030
Hao le T, Duy PQ, An M, Talbot J, Iyer CC, Wolman M, Beattie CE (2017) HuD and the survival motor neuron protein interact in motoneurons and are essential for motoneuron development, function, and mRNA regulation. J Neurosci 37: 11559–11571. doi:10.1523/JNEUROSCI.1528-17.2017
Hayhurst M, Wagner AK, Cerletti M, Wagers AJ, Rubin LL (2012) A cell- autonomous defect in skeletal muscle satellite cells expressing low levels of survival of motor neuron protein. Dev Biol 368: 323–334. doi:10.1016/j.ydbio.2012.05.037
Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK (2010) Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38: 576–589. doi:10.1016/ j.molcel.2010.05.004
Hellbach N, Peterson S, Haehnke D, Shankar A, LaBarge S, Pivaroff C, Saenger S, Thomas C, McCarthy K, Ebeling M, et al (2018) Impaired myogenic development, differentiation and function in hESC-derived SMA myoblasts and myotubes. PLoS One 13: e0205589. doi:10.1371/ journal.pone.0205589
Hoang P, Jacquir S, Lemus S, Ma Z (2019) Quantification of contractile dynamic complexities exhibited by human stem cell-derived cardiomyocytes using nonlinear dimensional analysis. Sci Rep 9: 14714. doi:10.1038/ s41598-019-51197-7
Ieronimakis N, Balasundaram G, Rainey S, Srirangam K, Yablonka-Reuveni Z, Reyes M (2010) Absence of CD34 on murine skeletal muscle satellite cells marks a reversible state of activation during acute injury. PLoS One 5: e10920. doi:10.1371/journal.pone.0010920
Jangi M, Fleet C, Cullen P, Gupta SV, Mekhoubad S, Chiao E, Allaire N, Bennett CF, Rigo F, Krainer AR, et al (2017) SMN deficiency in severe models of spinal muscular atrophy causes widespread intron retention and DNA damage. Proc Natl Acad Sci U S A 114: E2347–E2356. doi:10.1073/ pnas.1613181114
Kim JK, Jha NN, Feng Z, Faleiro MR, Chiriboga CA, Wei-Lapierre L, Dirksen RT, Ko CP, Monani UR (2020) Muscle-specific SMN reduction reveals motor neuron-independent disease in spinal muscular atrophy models. J Clin Invest 130: 1271–1287. doi:10.1172/JCI131989
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9: 357–359. doi:10.1038/nmeth.1923
Le TT, Pham LT, Butchbach ME, Zhang HL, Monani UR, Coovert DD, Gavrilina TO, Xing L, Bassell GJ, Burghes AH (2005) 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 14: 845–857. doi:10.1093/hmg/ddi078
Lin CY, Yoshida M, Li LT, Ikenaka A, Oshima S, Nakagawa K, Sakurai H, Matsui E, Nakahata T, Saito MK (2019) iPSC-derived functional human neuromuscular junctions model the pathophysiology of neuromuscular diseases. JCI Insight 4: e124299. doi:10.1172/ jci.insight.124299
Long KK, O’Shea KM, Khairallah RJ, Howell K, Paushkin S, Chen KS, Cote SM, Webster MT, Stains JP, Treece E, et al (2019) Specific inhibition of myostatin activation is beneficial in mouse models of SMA therapy. Hum Mol Genet 28: 1076–1089. doi:10.1093/hmg/ddy382
Lotti F, Imlach WL, Saieva L, Beck ES, Hao L, Li DK, Jiao W, Mentis GZ, Beattie CE, McCabe BD, et al (2012) An SMN-dependent U12 splicing event essential for motor circuit function. Cell 151: 440–454. doi:10.1016/ j.cell.2012.09.012
Luchetti A, Ciafre SA, Murdocca M, Malgieri A, Masotti A, Sanchez M, Farace MG, Novelli G, Sangiuolo F (2015) A perturbed MicroRNA expression pattern characterizes embryonic neural stem cells derived from a severe mouse model of spinal muscular atrophy (SMA). Int J Mol Sci 16: 18312–18327. doi:10.3390/ijms160818312
Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17. doi:10.14806/ej.17.1.200
Martinez TL, Kong L, Wang X, Osborne MA, Crowder ME, Van Meerbeke JP, Xu X, Davis C, Wooley J, Goldhamer DJ, et al (2012) Survival motor neuron protein in motor neurons determines synaptic integrity in spinal muscular atrophy. J Neurosci 32: 8703–8715. doi:10.1523/ JNEUROSCI.0204-12.2012
Mendell JR, Al-Zaidy S, Shell R, Arnold WD, Rodino-Klapac LR, Prior TW, Lowes L, Alfano L, Berry K, Church K, et al (2017) Single-dose gene- replacement therapy for spinal muscular atrophy. N Engl J Med 377: 1713–1722. doi:10.1056/NEJMoa1706198
Miller N, Shi H, Zelikovich AS, Ma YC (2016) Motor neuron mitochondrial dysfunction in spinal muscular atrophy. Hum Mol Genet 25: 3395–3406. doi:10.1093/hmg/ddw262
Nicole S, Desforges B, Millet G, Lesbordes J, Cifuentes-Diaz C, Vertes D, Cao ML, De Backer F, Languille L, Roblot N, et al (2003) Intact satellite cells lead to remarkable protection against Smn gene defect in differentiated skeletal muscle. J Cell Biol 161: 571–582. doi:10.1083/jcb.200210117
Passini MA, Bu J, Roskelley EM, Richards AM, Sardi SP, O’Riordan CR, Klinger KW, Shihabuddin LS, Cheng SH (2010) CNS-targeted gene therapy improves survival and motor function in a mouse model of spinal muscular atrophy. J Clin Invest 120: 1253–1264. doi:10.1172/JCI41615
Piazzon N, Rage F, Schlotter F, Moine H, Branlant C, Massenet S (2008) In vitro and in cellulo evidences for association of the survival of motor neuron complex with the fragile X mental retardation protein. J Biol Chem 283: 5598–5610. doi:10.1074/jbc.M707304200
Przanowska RK, Sobierajska E, Su Z, Jensen K, Przanowski P, Nagdas S, Kashatus JA, Kashatus DF, Bhatnagar S, Lukens JR, et al (2020) miR-206 family is important for mitochondrial and muscle function, but not essential for myogenesis in vitro. FASEB J 34: 7687–7702. doi:10.1096/fj.201902855RR
Liu Q, Fischer U, Wang F, Dreyfuss G (1997) The spinal muscular atrophy disease gene product SMN and its associated protein SIP1 are in a complex with spliceosomal snRNP proteins. Cell 90: 1013–1021. doi:10.1016/s0092-8674(00)80367-0
Rao PK, Kumar RM, Farkhondeh M, Baskerville S, Lodish HF (2006) Myogenic factors that regulate expression of muscle-specific microRNAs. Proc Natl Acad Sci U S A 103: 8721–8726. doi:10.1073/pnas.0602831103
Remels AH, Langen RC, Schrauwen P, Schaart G, Schols AM, Gosker HR (2010) Regulation of mitochondrial biogenesis during myogenesis. Mol Cell Endocrinol 315: 113–120. doi:10.1016/j.mce.2009.09.029
Ripolone M, Ronchi D, Violano R, Vallejo D, Fagiolari G, Barca E, Lucchini V, Colombo I, Villa L, Berardinelli A, et al (2015) Impaired muscle mitochondrial biogenesis and myogenesis in spinal muscular atrophy. JAMA Neurol 72: 666–675. doi:10.1001/jamaneurol.2015.0178
Schiaffino S, Dyar KA, Ciciliot S, Blaauw B, Sandri M (2013) Mechanisms regulating skeletal muscle growth and atrophy. FEBS J 280: 4294–4314. doi:10.1111/febs.12253
Shafey D, Cote PD, Kothary R (2005) Hypomorphic Smn knockdown C2C12 myoblasts reveal intrinsic defects in myoblast fusion and myotube morphology. Exp Cell Res 311: 49–61. doi:10.1016/j.yexcr.2005.08.019
Shao W, Zeitlinger J (2017) Paused RNA polymerase II inhibits new transcriptional initiation. Nat Genet 49: 1045–1051. doi:10.1038/ng.3867
Sharma A, Lambrechts A, Hao Lt, Le TT, Sewry CA, Ampe C, Burghes AH, Morris GE (2005) A role for complexes of survival of motor neurons (SMN) protein with gemins and profilin in neurite-like cytoplasmic extensions of cultured nerve cells. Exp Cell Res 309: 185–197. doi:10.1016/j.yexcr.2005.05.014
Shen L, Shao N, Liu X, Nestler E (2014) ngs.plot: Quick mining and visualization of next-generation sequencing data by integrating genomic databases. BMC Genomics 15: 284. doi:10.1186/1471-2164-15-284
Shintaku J, Peterson JM, Talbert EE, Gu JM, Ladner KJ, Williams DR, Mousavi K, Wang R, Sartorelli V, Guttridge DC (2016) MyoD regulates skeletal muscle oxidative metabolism cooperatively with alternative NF-κB. Cell Rep 17: 514–526. doi:10.1016/j.celrep.2016.09.010
Tadesse H, Deschenes-Furry J, Boisvenue S, Cote J (2007) KH-type splicing regulatory protein interacts with survival motor neuron protein and is misregulated in spinal muscular atrophy. Hum Mol Genet 17: 506–524. doi:10.1093/hmg/ddm327
Tanaka A, Woltjen K, Miyake K, Hotta A, Ikeya M, Yamamoto T, Nishino T, Shoji E, Sehara-Fujisawa A, Manabe Y, et al (2013) Efficient and reproducible myogenic differentiation from human iPS cells: Prospects for modeling miyoshi myopathy in vitro. PLoS One 8: e61540. doi:10.1371/ journal.pone.0061540
Trotta AP, Gelles JD, Serasinghe MN, Loi P, Arbiser JL, Chipuk JE (2017) Disruption of mitochondrial electron transport chain function potentiates the pro-apoptotic effects of MAPK inhibition. J Biol Chem 292: 11727–11739. doi:10.1074/jbc.M117.786442
Wang LT, Chiou SS, Liao YM, Jong YJ, Hsu SH (2014) Survival of motor neuron protein downregulates miR-9 expression in patients with spinal muscular atrophy. Kaohsiung J Med Sci 30: 229–234. doi:10.1016/j.kjms.2013.12.007
Wang C, Liu W, Nie Y, Qaher M, Horton HE, Yue F, Asakura A, Kuang S (2017) Loss of MyoD promotes fate transdifferentiation of myoblasts into brown adipocytes. EBioMedicine 16: 212–223. doi:10.1016/j.ebiom.2017.01.015
Wertz MH, Winden K, Neveu P, Ng SY, Ercan E, Sahin M (2016) Cell-type-specific miR-431 dysregulation in a motor neuron model of spinal muscular atrophy. Hum Mol Genet 25: 2168–2181. doi:10.1093/hmg/ddw084
Wust S, Drose S, Heidler J, Wittig I, Klockner I, Franko A, Bonke E, Gunther S, Gartner U, Boettger T, et al (2018) Metabolic maturation during muscle stem cell differentiation is achieved by miR-1/133a-mediated inhibition of the Dlk1-Dio3 mega gene cluster. Cell Metab 27:1026–1039.e6. doi:10.1016/j.cmet.2018.02.022
Xiao Y, Zhang J, Shu X, Bai L, Xu W, Wang A, Chen A, Tu W-Y, Wang J, Zhang K, et al (2020) Loss of mitochondrial protein CHCHD10 in skeletal muscle causes neuromuscular junction impairment. Hum Mol Genet 29: 1784–1796. doi:10.1093/hmg/ddz154
Yamazaki T, Chen S, Yu Y, Yan B, Haertlein TC, Carrasco MA, Tapia JC, Zhai B, Das R, Lalancette-Hebert M, et al (2012) FUS-SMN protein interactions link the motor neuron diseases ALS and SMA. Cell Rep 2: 799–806. doi:10.1016/j.celrep.2012.08.025
Yan K, An T, Zhai M, Huang Y, Wang Q, Wang Y, Zhang R, Wang T, Liu J, Zhang Y, et al (2019) Mitochondrial miR-762 regulates apoptosis and myocardial infarction by impairing ND2. Cell Death Dis 10: 500. doi:10.1038/s41419-019-1734-7
Yoshida M, Kitaoka S, Egawa N, Yamane M, Ikeda R, Tsukita K, Amano N, Watanabe A, Morimoto M, Takahashi J, et al (2015) Modeling the early phenotype at the neuromuscular junction of spinal muscular atrophy using patient-derived iPSCs. Stem Cell Rep 4: 561–568. doi:10.1016/ j.stemcr.2015.02.010
Zhang Z, Lotti F, Dittmar K, Younis I, Wan L, Kasim M, Dreyfuss G (2008) SMN deficiency causes tissue-specific perturbations in the repertoire of snRNAs and widespread defects in splicing. Cell 133: 585–600. doi:10.1016/j.cell.2008.03.031
Zhang X, Zuo X, Yang B, Li Z, Xue Y, Zhou Y, Huang J, Zhao X, Zhou J, Yan Y, et al (2014) MicroRNA directly enhances mitochondrial translation during muscle differentiation. Cell 158: 607–619. doi:10.1016/ j.cell.2014.05.047
Yanling Zhao D, Gish G, Braunschweig U, Li Y, Ni Z, Schmitges FW, Zhong G, Liu K, Li W, Moffat J, et al (2016) SMN and symmetric arginine dimethylation of RNA polymerase II C-terminal domain control termination. Nature 529: 48–53. doi:10.1038/nature16469