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The composition of skeletal muscle fiber type affects systemic energy expenditures, and perturbations in metabolic homeostasis contribute to the onset of obesity and other metabolic dysfunctions. Long noncoding RNAs (lncRNAs) have been demonstrated to play critical roles in diverse cellular processes and diseases, including human cancers; however, the functional importance of lncRNAs in muscle performance, energy balance, and obesity remains elusive. We previously reported that the lncRNA <jats:italic>H19<\/jats:italic> regulates the poly-ubiquitination and protein stability of dystrophin (DMD) in muscular dystrophy.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Methods<\/jats:title>\n                <jats:p>Here, we identified mouse\/human <jats:italic>H19-<\/jats:italic>interacting proteins using mouse\/human skeletal muscle tissues and liquid chromatography\u2013mass spectrometry (LC-MS). Human induced pluripotent stem-derived skeletal muscle cells (iPSC-SkMC) from a healthy donor and Becker Muscular Dystrophy (BMD) patients were utilized to study DMD post-translational modifications and associated proteins. We identified a gain-of-function (GOF) mutant of <jats:italic>H19<\/jats:italic> and characterized the effects on myoblast differentiation and fusion to myotubes using iPSCs. We then conjugated <jats:italic>H19<\/jats:italic> RNA gain-of-function oligonucleotides (Rgof) with the skeletal muscle enrichment peptide agrin (referred to as AGR-<jats:italic>H19<\/jats:italic>-Rgof) and evaluated AGR-<jats:italic>H19<\/jats:italic>-Rgof\u2019s effects on skeletal muscle performance using wild-type (WT) C57BL\/6\u2009J mice and its anti-obesity effects using high-fat diet (HFD)- and <jats:italic>leptin<\/jats:italic> deficiency-induced obese mouse models.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Results<\/jats:title>\n                <jats:p>We demonstrated that both human and mouse <jats:italic>H19<\/jats:italic> associated with DMD and that the <jats:italic>H19<\/jats:italic> GOF exhibited enhanced interaction with DMD compared to WT <jats:italic>H19<\/jats:italic>. DMD was found to associate with serine\/threonine-protein kinase MRCK alpha (MRCK\u03b1) and \u03b1-synuclein (SNCA) in iPSC-SkMC derived from BMD patients. Inhibition of MRCK\u03b1 and SNCA-mediated phosphorylation of DMD antagonized the interaction between <jats:italic>H19<\/jats:italic> and DMD. These signaling events led to improved skeletal muscle cell differentiation and myotube fusion. The administration of AGR-<jats:italic>H19<\/jats:italic>-Rgof improved the muscle mass, muscle performance, and base metabolic rate of WT mice. Furthermore, mice treated with AGR-<jats:italic>H19<\/jats:italic>-Rgof exhibited resistance to HFD- or <jats:italic>leptin<\/jats:italic> deficiency-induced obesity.<\/jats:p>\n              <\/jats:sec><jats:sec>\n                <jats:title>Conclusions<\/jats:title>\n                <jats:p>Our study suggested the functional importance of the <jats:italic>H19<\/jats:italic> GOF mutant in enhancing muscle performance and anti-obesity effects.<\/jats:p>\n              <\/jats:sec>","DOI":"10.1186\/s13073-021-00937-4","type":"journal-article","created":{"date-parts":[[2021,8,28]],"date-time":"2021-08-28T13:02:44Z","timestamp":1630155764000},"update-policy":"https:\/\/doi.org\/10.1007\/springer_crossmark_policy","source":"Crossref","is-referenced-by-count":25,"title":["Functional significance of gain-of-function H19 lncRNA in skeletal muscle differentiation and anti-obesity effects"],"prefix":"10.1186","volume":"13","author":[{"given":"Yajuan","family":"Li","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yaohua","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Qingsong","family":"Hu","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sergey D.","family":"Egranov","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhen","family":"Xing","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Zhao","family":"Zhang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Ke","family":"Liang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Youqiong","family":"Ye","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yinghong","family":"Pan","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sujash S.","family":"Chatterjee","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Brandon","family":"Mistretta","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tina K.","family":"Nguyen","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"David H.","family":"Hawke","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Preethi H.","family":"Gunaratne","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mien-Chie","family":"Hung","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Leng","family":"Han","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Liuqing","family":"Yang","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-6473-8229","authenticated-orcid":false,"given":"Chunru","family":"Lin","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"297","published-online":{"date-parts":[[2021,8,28]]},"reference":[{"key":"937_CR1","doi-asserted-by":"publisher","unstructured":"Hughes DC, Ellefsen S, Baar K. 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All of the human specimen-related studies have been approved by the Institutional Review Board of The University of Texas, MD Anderson Cancer Center. De-identified fresh-frozen human skeletal muscle tissues were commercially obtained from ProteoGenex Inc. All hiPSC-related studies were approved by the Human Embryonic & Induced Pluripotent Stem Cell Research Oversight committee of The University of Texas, MD Anderson Cancer Center.","order":2,"name":"Ethics","group":{"name":"EthicsHeading","label":"Ethics approval and consent to participate"}},{"value":"Not applicable.","order":3,"name":"Ethics","group":{"name":"EthicsHeading","label":"Consent for publication"}},{"value":"Zhen Xing is now an employee of Sanofi U.S. The remaining authors declare that they have no competing interests.","order":4,"name":"Ethics","group":{"name":"EthicsHeading","label":"Competing interests"}}],"article-number":"137"}}