{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,4]],"date-time":"2026-09-04T06:32:01Z","timestamp":1788503521088,"version":"build-2803163510"},"reference-count":99,"publisher":"Frontiers Media SA","license":[{"start":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T00:00:00Z","timestamp":1660521600000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/501100002347","name":"Bundesministerium f\u00fcr Bildung und Forschung","doi-asserted-by":"publisher","id":[{"id":"10.13039\/501100002347","id-type":"DOI","asserted-by":"publisher"}]}],"content-domain":{"domain":["frontiersin.org"],"crossmark-restriction":true},"short-container-title":["Front. Physiol."],"abstract":"<jats:p>Nitric oxide (NO) is a bioactive gas produced by one of the three NO synthases: neuronal NOS (nNOS), inducible (iNOS), and endothelial NOS (eNOS). NO has a relevant modulatory role in muscle contraction; this takes place through two major signaling pathways: (i) activation of soluble guanylate cyclase and, thus, protein kinase G or (ii) nitrosylation of sulfur groups of cysteine. Although it has been suggested that nNOS-derived NO is the responsible isoform in muscle contraction, the roles of eNOS and iNOS and their signaling pathways have not yet been clarified. To elucidate the action of each pathway, we optimized the generation of myooids, an engineered skeletal muscle tissue based on the C2C12 cell line. In comparison with diaphragm strips from wild-type mice, 180 myooids were analyzed, which expressed all relevant excitation\u2013contraction coupling proteins and both nNOS and iNOS isoforms. Along with the biochemical results, myooids treated with NO donor (SNAP) and unspecific NOS blocker (L-NAME) revealed a comparable NO modulatory effect on force production as was observed in the diaphragm strips. Under the effects of pharmacological tools, we analyzed the myooids in response to electrical stimulation of two possible signaling pathways and NO sources. The nNOS-derived NO exerted its negative effect on force production <jats:italic>via<\/jats:italic> the sGG-PKG pathway, while iNOS-derived NO increased the excitability in response to sub-threshold electrical stimulation. These results strengthen the hypotheses of previous reports on the mechanism of action of NO during force production, showed a novel function of iNOS-derived NO, and establish the myooid as a novel and robust alternative model for pathophysiological skeletal muscle research.<\/jats:p>","DOI":"10.3389\/fphys.2022.946682","type":"journal-article","created":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T08:31:12Z","timestamp":1660552272000},"update-policy":"https:\/\/doi.org\/10.3389\/crossmark-policy","source":"Crossref","is-referenced-by-count":5,"title":["nNOS-derived NO modulates force production and iNO-derived NO the excitability in C2C12-derived 3D tissue engineering skeletal muscle via different NO signaling pathways"],"prefix":"10.3389","volume":"13","author":[{"given":"Matias","family":"Mosqueira","sequence":"first","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa-Mareike","family":"Scheid","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dominik","family":"Kiemel","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Talisa","family":"Richardt","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Mona","family":"Rheinberger","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Dirk","family":"Ollech","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Almut","family":"Lutge","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tim","family":"Hei\u00dfenberg","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lena","family":"Pfitzer","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Lisa","family":"Engelskircher","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Umut","family":"Yildiz","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Isabel","family":"Porth","sequence":"additional","affiliation":[],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1965","published-online":{"date-parts":[[2022,8,15]]},"reference":[{"key":"B1","doi-asserted-by":"publisher","first-page":"577","DOI":"10.1111\/j.1469-7793.1998.577bn.x","article-title":"Effect of nitric oxide on single skeletal muscle fibres from the mouse","volume":"509","author":"Andrade","year":"1998","journal-title":"J. Physiol."},{"key":"B2","doi-asserted-by":"publisher","first-page":"35","DOI":"10.1089\/ars.2000.2.1-35","article-title":"Oxidative modification of ion channel activity of ryanodine receptor","volume":"2","author":"Anzai","year":"2000","journal-title":"Antioxid. Redox Signal."},{"key":"B3","doi-asserted-by":"publisher","first-page":"40354","DOI":"10.1074\/jbc.M600876200","article-title":"Identification of cysteines involved in S-nitrosylation, S-glutathionylation, and oxidation to disulfides in ryanodine receptor type 1","volume":"281","author":"Aracena-Parks","year":"2006","journal-title":"J. Biol. Chem."},{"key":"B4","doi-asserted-by":"publisher","first-page":"338","DOI":"10.1002\/micr.20122","article-title":"Addition of nitric oxide donor S-nitroso-N-acetylcysteine to selective iNOS inhibitor 1400W further improves contractile function in reperfused skeletal muscle","volume":"25","author":"Barker","year":"2005","journal-title":"Microsurgery"},{"key":"B5","doi-asserted-by":"publisher","first-page":"325","DOI":"10.1038\/nm.1916","article-title":"Hypernitrosylated ryanodine receptor calcium release channels are leaky in dystrophic muscle","volume":"15","author":"Bellinger","year":"2009","journal-title":"Nat. Med."},{"key":"B6","doi-asserted-by":"publisher","first-page":"293","DOI":"10.1007\/s004410051060","article-title":"Nitric oxide synthase (NOS) in mouse skeletal muscle development and differentiated myoblasts","volume":"292","author":"Blottner","year":"1998","journal-title":"Cell Tissue Res."},{"key":"B7","doi-asserted-by":"publisher","first-page":"1514","DOI":"10.1016\/j.jbiomech.2010.01.039","article-title":"Effects of a combined mechanical stimulation protocol: Value for skeletal muscle tissue engineering","volume":"43","author":"Boonen","year":"2010","journal-title":"J. Biomech."},{"key":"B8","doi-asserted-by":"publisher","first-page":"595","DOI":"10.1097\/01.PRS.0000101064.62289.2F","article-title":"Contractile skeletal muscle tissue-engineered on an acellular scaffold","volume":"113","author":"Borschel","year":"2004","journal-title":"Plast. Reconstr. Surg."},{"key":"B9","doi-asserted-by":"publisher","first-page":"615","DOI":"10.1016\/j.bbrc.2005.02.182","article-title":"Compartmentalization of NO signaling cascade in skeletal muscles","volume":"330","author":"Buchwalow","year":"2005","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"B10","doi-asserted-by":"publisher","first-page":"326","DOI":"10.1034\/j.1600-0854.2000.010406.x","article-title":"Role of cholesterol in developing T-tubules: Analogous mechanisms for T-tubule and caveolae biogenesis","volume":"1","author":"Carozzi","year":"2000","journal-title":"Traffic"},{"key":"B11","doi-asserted-by":"publisher","first-page":"9142","DOI":"10.1073\/pnas.93.17.9142","article-title":"Neuronal nitric oxide synthase and dystrophin-deficient muscular dystrophy","volume":"93","author":"Chang","year":"1996","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B12","doi-asserted-by":"publisher","first-page":"200","DOI":"10.1002\/cm.20010","article-title":"C2C12 co-culture on a fibroblast substratum enables sustained survival of contractile, highly differentiated myotubes with peripheral nuclei and adult fast myosin expression","volume":"58","author":"Cooper","year":"2004","journal-title":"Cell Motil. Cytoskelet."},{"key":"B13","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1111\/j.1549-8719.2011.00111.x","article-title":"Role of neuronal nitric oxide synthase in modulating microvascular and contractile function in rat skeletal muscle","volume":"18","author":"Copp","year":"2011","journal-title":"Microcirculation"},{"key":"B14","doi-asserted-by":"publisher","first-page":"655","DOI":"10.1113\/jphysiol.2008.164947","article-title":"Up-regulation of the peroxiredoxin-6 related metabolism of reactive oxygen species in skeletal muscle of mice lacking neuronal nitric oxide synthase","volume":"587","author":"Da Silva-Azevedo","year":"2009","journal-title":"J. Physiol."},{"key":"B15","doi-asserted-by":"publisher","first-page":"C288","DOI":"10.1152\/ajpcell.2001.280.2.C288","article-title":"Excitability and contractility of skeletal muscle engineered from primary cultures and cell lines","volume":"280","author":"Dennis","year":"2001","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"B16","doi-asserted-by":"publisher","first-page":"327","DOI":"10.1290\/1071-2690(2000)036<0327:EAICPO>2.0.CO;2","article-title":"Excitability and isometric contractile properties of mammalian skeletal muscle constructs engineered in vitro","volume":"36","author":"Dennis","year":"2000","journal-title":"Vitro Cell Dev. Biol. Anim."},{"key":"B17","doi-asserted-by":"publisher","first-page":"C1088","DOI":"10.1152\/ajpcell.00523.2007","article-title":"Nitric oxide facilitates NFAT-dependent transcription in mouse myotubes","volume":"294","author":"Drenning","year":"2008","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"B18","doi-asserted-by":"publisher","first-page":"C316","DOI":"10.1152\/ajpcell.00334.2016","article-title":"S-nitrosylation and S-glutathionylation of Cys134 on troponin I have opposing competitive actions on Ca(2+) sensitivity in rat fast-twitch muscle fibers","volume":"312","author":"Dutka","year":"2017","journal-title":"Am. J. Physiol. Cell Physiol."},{"key":"B19","doi-asserted-by":"publisher","first-page":"2181","DOI":"10.1113\/jphysiol.2010.200451","article-title":"Modulation of contractile apparatus Ca2+ sensitivity and disruption of excitation-contraction coupling by S-nitrosoglutathione in rat muscle fibres","volume":"589","author":"Dutka","year":"2011","journal-title":"J. Physiol."},{"key":"B20","doi-asserted-by":"publisher","first-page":"15229","DOI":"10.1073\/pnas.2433468100","article-title":"Concerted regulation of skeletal muscle contractility by oxygen tension and endogenous nitric oxide","volume":"100","author":"Eu","year":"2003","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B21","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1016\/s0092-8674(00)00054-4","article-title":"The skeletal muscle calcium release channel: Coupled O2 sensor and NO signaling functions","volume":"102","author":"Eu","year":"2000","journal-title":"Cell"},{"key":"B22","doi-asserted-by":"publisher","first-page":"2041731420981339","DOI":"10.1177\/2041731420981339","article-title":"Bioengineered in vitro skeletal muscles as new tools for muscular dystrophies preclinical studies","volume":"12","author":"Fernandez-Costa","year":"2021","journal-title":"J. Tissue Eng."},{"key":"B23","doi-asserted-by":"publisher","first-page":"1338","DOI":"10.1021\/acs.chemrev.7b00568","article-title":"Biochemistry of peroxynitrite and protein tyrosine nitration","volume":"118","author":"Ferrer-Sueta","year":"2018","journal-title":"Chem. Rev."},{"key":"B24","doi-asserted-by":"publisher","first-page":"525","DOI":"10.1124\/pr.110.002907","article-title":"cGMP-dependent protein kinases and cGMP phosphodiesterases in nitric oxide and cGMP action","volume":"62","author":"Francis","year":"2010","journal-title":"Pharmacol. Rev."},{"key":"B25","doi-asserted-by":"publisher","first-page":"1348","DOI":"10.1016\/s0022-3468(03)00394-4","article-title":"Fetal tissue engineering: In vitro analysis of muscle constructs","volume":"38","author":"Fuchs","year":"2003","journal-title":"J. Pediatr. Surg."},{"key":"B26","doi-asserted-by":"publisher","first-page":"720","DOI":"10.1038\/nm.2374","article-title":"Misregulated alternative splicing of BIN1 is associated with T tubule alterations and muscle weakness in myotonic dystrophy","volume":"17","author":"Fugier","year":"2011","journal-title":"Nat. Med."},{"key":"B27","doi-asserted-by":"publisher","first-page":"2330","DOI":"10.1152\/jappl.1998.85.6.2330","article-title":"Regulation of nitric oxide production in response to skeletal muscle activation","volume":"85","author":"Fujii","year":"1998","journal-title":"J. Appl. Physiol."},{"key":"B28","doi-asserted-by":"publisher","first-page":"1034","DOI":"10.1002\/bit.22318","article-title":"Novel method for fabrication of skeletal muscle construct from the C2C12 myoblast cell line using serum-free medium AIM-V","volume":"103","author":"Fujita","year":"2009","journal-title":"Biotechnol. Bioeng."},{"key":"B29","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1002\/term.253","article-title":"Fabrication of scaffold-free contractile skeletal muscle tissue using magnetite-incorporated myogenic C2C12 cells","volume":"4","author":"Fujita","year":"2010","journal-title":"J. Tissue Eng. Regen. Med."},{"key":"B30","doi-asserted-by":"publisher","first-page":"270","DOI":"10.1089\/ten.TEA.2021.0070","article-title":"Extracellular matrix hydrogels promote expression of muscle-tendon junction proteins","volume":"28","author":"Gaffney","year":"2021","journal-title":"Tissue Eng. Part A"},{"key":"B31","doi-asserted-by":"publisher","first-page":"4959","DOI":"10.1074\/jbc.272.8.4959","article-title":"1400W is a slow, tight binding, and highly selective inhibitor of inducible nitric-oxide synthase in vitro and in vivo","volume":"272","author":"Garvey","year":"1997","journal-title":"J. Biol. Chem."},{"key":"B32","doi-asserted-by":"publisher","first-page":"1614","DOI":"10.1096\/fasebj.10.14.9002553","article-title":"Inducible NO synthase II and neuronal NO synthase I are constitutively expressed in different structures of Guinea pig skeletal muscle: Implications for contractile function","volume":"10","author":"Gath","year":"1996","journal-title":"FASEB J."},{"key":"B33","doi-asserted-by":"publisher","first-page":"57","DOI":"10.1007\/s004410050979","article-title":"Co-localization of nitric oxide synthase I (NOS I) and NMDA receptor subunit 1 (NMDAR-1) at the neuromuscular junction in rat and mouse skeletal muscle","volume":"291","author":"Grozdanovic","year":"1998","journal-title":"Cell Tissue Res."},{"key":"B34","doi-asserted-by":"publisher","first-page":"19453","DOI":"10.1038\/s41598-019-55704-8","article-title":"An improved method for studying mouse diaphragm function","volume":"9","author":"Hakim","year":"2019","journal-title":"Sci. Rep."},{"key":"B35","doi-asserted-by":"publisher","first-page":"e0141572","DOI":"10.1371\/journal.pone.0141572","article-title":"L-citrulline protects skeletal muscle cells from cachectic stimuli through an iNOS-dependent mechanism","volume":"10","author":"Ham","year":"2015","journal-title":"PLoS One"},{"key":"B36","doi-asserted-by":"publisher","first-page":"227","DOI":"10.1007\/s002320001022","article-title":"Nitric oxide activates or inhibits skeletal muscle ryanodine receptors depending on its concentration, membrane potential and ligand binding","volume":"173","author":"Hart","year":"2000","journal-title":"J. Membr. Biol."},{"key":"B37","first-page":"637","article-title":"Construction of a recombinant vector based on AAV carrying human endothelial nitric-oxide synthase gene","volume":"24","author":"He","year":"2003","journal-title":"Acta Pharmacol. Sin."},{"key":"B38","doi-asserted-by":"publisher","first-page":"R95","DOI":"10.1152\/ajpregu.2000.278.1.R95","article-title":"Nitric oxide release and contractile properties of skeletal muscles from mice deficient in type III NOS","volume":"278","author":"Hirschfield","year":"2000","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"B39","doi-asserted-by":"publisher","first-page":"1639","DOI":"10.1039\/b004028m","article-title":"Reaction of ascorbic acid with S-nitrosothiols: Clear evidence for two distinct reaction pathways","volume":"2","author":"Holmes","year":"2000","journal-title":"J. Chem. Soc. Perkin Trans. 2"},{"key":"B40","doi-asserted-by":"publisher","first-page":"E838","DOI":"10.1152\/ajpendo.00513.2015","article-title":"Skeletal muscle glucose uptake during treadmill exercise in neuronal nitric oxide synthase-mu knockout mice","volume":"310","author":"Hong","year":"2016","journal-title":"Am. J. Physiol. Endocrinol. Metab."},{"key":"B41","doi-asserted-by":"publisher","first-page":"H429","DOI":"10.1152\/ajpheart.00501.2001","article-title":"Neuronal NOS-dependent dilation to flow in coronary arteries of male eNOS-KO mice","volume":"282","author":"Huang","year":"2002","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"B42","doi-asserted-by":"publisher","first-page":"9265","DOI":"10.1073\/pnas.84.24.9265","article-title":"Endothelium-derived relaxing factor produced and released from artery and vein is nitric oxide","volume":"84","author":"Ignarro","year":"1987","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B43","doi-asserted-by":"publisher","first-page":"47","DOI":"10.1177\/2472555218793374","article-title":"Morphology-based analysis of myoblasts for prediction of myotube formation","volume":"24","author":"Ishikawa","year":"2019","journal-title":"SLAS Discov."},{"key":"B44","doi-asserted-by":"publisher","first-page":"107","DOI":"10.1016\/j.yjmcc.2013.04.017","article-title":"Myofilament Ca2+ desensitization mediates positive lusitropic effect of neuronal nitric oxide synthase in left ventricular myocytes from murine hypertensive heart","volume":"60","author":"Jin","year":"2013","journal-title":"J. Mol. Cell. Cardiol."},{"key":"B45","doi-asserted-by":"publisher","first-page":"17437","DOI":"10.1074\/jbc.274.25.17437","article-title":"Insulin-like growth factor-II, phosphatidylinositol 3-kinase, nuclear factor-kappaB and inducible nitric-oxide synthase define a common myogenic signaling pathway","volume":"274","author":"Kaliman","year":"1999","journal-title":"J. Biol. Chem."},{"key":"B46","doi-asserted-by":"publisher","first-page":"1322","DOI":"10.1161\/01.RES.0000078171.52542.9E","article-title":"Nitric oxide regulation of myocardial contractility and calcium cycling: Independent impact of neuronal and endothelial nitric oxide synthases","volume":"92","author":"Khan","year":"2003","journal-title":"Circ. Res."},{"key":"B47","doi-asserted-by":"publisher","first-page":"501","DOI":"10.1089\/ten.TEC.2008.0286","article-title":"Regulating fibrinolysis to engineer skeletal muscle from the C2C12 cell line","volume":"15","author":"Khodabukus","year":"2009","journal-title":"Tissue Eng. Part C Methods"},{"key":"B48","doi-asserted-by":"publisher","first-page":"2198","DOI":"10.1002\/jcb.24938","article-title":"The effect of serum origin on tissue engineered skeletal muscle function","volume":"115","author":"Khodabukus","year":"2014","journal-title":"J. Cell. Biochem."},{"key":"B49","doi-asserted-by":"publisher","first-page":"2489","DOI":"10.1002\/jcp.24985","article-title":"Role of contraction duration in inducing fast-to-slow contractile and metabolic protein and functional changes in engineered muscle","volume":"230","author":"Khodabukus","year":"2015","journal-title":"J. Cell. Physiol."},{"key":"B50","doi-asserted-by":"publisher","first-page":"619710","DOI":"10.3389\/fphys.2021.619710","article-title":"Tissue-engineered skeletal muscle models to study muscle function, plasticity, and disease","volume":"12","author":"Khodabukus","year":"2021","journal-title":"Front. Physiol."},{"key":"B51","doi-asserted-by":"publisher","first-page":"249","DOI":"10.1042\/bj2980249","article-title":"Nitric oxide synthases in mammals","volume":"298","author":"Knowles","year":"1994","journal-title":"Biochem. J."},{"key":"B52","doi-asserted-by":"publisher","first-page":"546","DOI":"10.1038\/372546a0","article-title":"Nitric oxide in skeletal muscle","volume":"372","author":"Kobzik","year":"1994","journal-title":"Nature"},{"key":"B53","doi-asserted-by":"publisher","first-page":"573","DOI":"10.1089\/107632701753213192","article-title":"Functional development of engineered skeletal muscle from adult and neonatal rats","volume":"7","author":"Kosnik","year":"2001","journal-title":"Tissue Eng."},{"key":"B54","doi-asserted-by":"publisher","first-page":"529","DOI":"10.1002\/term.345","article-title":"Advanced maturation by electrical stimulation: Differences in response between C2C12 and primary muscle progenitor cells","volume":"5","author":"Langelaan","year":"2011","journal-title":"J. Tissue Eng. Regen. Med."},{"key":"B55","doi-asserted-by":"publisher","first-page":"237","DOI":"10.1042\/bj3240237","article-title":"NF-kappaB-dependent expression of nitric oxide synthase is required for membrane fusion of chick embryonic myoblasts","volume":"324","author":"Lee","year":"1997","journal-title":"Biochem. J."},{"key":"B56","doi-asserted-by":"publisher","first-page":"88","DOI":"10.1002\/path.2799","article-title":"Nitrosative stress elicited by nNOS\u00b5 delocalization inhibits muscle force in dystrophin-null mice.","volume":"223","author":"Li","year":"2011","journal-title":"J. Pathol."},{"key":"B57","doi-asserted-by":"publisher","first-page":"321","DOI":"10.1089\/jir.2009.0022","article-title":"Nitric oxide stimulates interleukin-6 production in skeletal myotubes","volume":"30","author":"Makris","year":"2010","journal-title":"J. Interferon Cytokine Res."},{"key":"B58","doi-asserted-by":"publisher","first-page":"2595","DOI":"10.1089\/ten.TEA.2015.0146","article-title":"Neuromuscular junction formation in tissue-engineered skeletal muscle augments contractile function and improves cytoskeletal organization","volume":"21","author":"Martin","year":"2015","journal-title":"Tissue Eng. Part A"},{"key":"B59","doi-asserted-by":"publisher","first-page":"2788","DOI":"10.1002\/jcp.25960","article-title":"Leucine elicits myotube hypertrophy and enhances maximal contractile force in tissue engineered skeletal muscle in vitro","volume":"232","author":"Martin","year":"2017","journal-title":"J. Cell. Physiol."},{"key":"B60","doi-asserted-by":"publisher","first-page":"e50036","DOI":"10.3791\/50036","article-title":"Isometric and eccentric force generation assessment of skeletal muscles isolated from murine models of muscular dystrophies","volume":"71","author":"Moorwood","year":"2013","journal-title":"J. Vis. Exp."},{"key":"B61","doi-asserted-by":"publisher","first-page":"18","DOI":"10.1007\/s00395-021-00860-0","article-title":"Cardiomyocyte depolarization triggers NOS-dependent NO transient after calcium release, reducing the subsequent calcium transient","volume":"116","author":"Mosqueira","year":"2021","journal-title":"Basic Res. Cardiol."},{"key":"B62","doi-asserted-by":"publisher","first-page":"1174","DOI":"10.1002\/med.21279","article-title":"Cardiac and respiratory dysfunction in Duchenne muscular dystrophy and the role of second messengers","volume":"33","author":"Mosqueira","year":"2013","journal-title":"Med. Res. Rev."},{"key":"B63","doi-asserted-by":"publisher","first-page":"1161","DOI":"10.1002\/bit.22636","article-title":"Micropatterning contractile C2C12 myotubes embedded in a fibrin gel","volume":"105","author":"Nagamine","year":"2010","journal-title":"Biotechnol. Bioeng."},{"key":"B64","doi-asserted-by":"publisher","first-page":"13725","DOI":"10.1016\/s0021-9258(17)36703-0","article-title":"Regulation of biosynthesis of nitric oxide","volume":"269","author":"Nathan","year":"1994","journal-title":"J. Biol. Chem."},{"key":"B65","doi-asserted-by":"publisher","first-page":"479","DOI":"10.1186\/s12891-020-03501-0","article-title":"iNOS is not responsible for RyR1 S-nitrosylation in mdx mice with truncated dystrophin","volume":"21","author":"Nogami","year":"2020","journal-title":"BMC Musculoskelet. Disord."},{"key":"B66","doi-asserted-by":"publisher","first-page":"221","DOI":"10.1042\/BJ20091144","article-title":"Myosin is reversibly inhibited by S-nitrosylation","volume":"424","author":"Nogueira","year":"2009","journal-title":"Biochem. J."},{"key":"B67","doi-asserted-by":"publisher","first-page":"19614","DOI":"10.1038\/srep19614","article-title":"Breaking sarcomeres by in vitro exercise","volume":"6","author":"Orfanos","year":"2016","journal-title":"Sci. Rep."},{"key":"B68","doi-asserted-by":"publisher","first-page":"42444","DOI":"10.1021\/acsami.7b03979","article-title":"Gelatin-polyaniline composite nanofibers enhanced excitation-contraction coupling system maturation in myotubes","volume":"9","author":"Ostrovidov","year":"2017","journal-title":"ACS Appl. Mat. Interfaces"},{"key":"B69","doi-asserted-by":"publisher","first-page":"279","DOI":"10.1002\/term.93","article-title":"Effects of electrical stimulation in C2C12 muscle constructs","volume":"2","author":"Park","year":"2008","journal-title":"J. Tissue Eng. Regen. Med."},{"key":"B70","doi-asserted-by":"publisher","first-page":"137","DOI":"10.1083\/jcb.136.1.137","article-title":"Caveolin-3 associates with developing T-tubules during muscle differentiation","volume":"136","author":"Parton","year":"1997","journal-title":"J. Cell Biol."},{"key":"B71","doi-asserted-by":"publisher","first-page":"324","DOI":"10.1002\/micr.20029","article-title":"Inhibition of iNOS with 1400W improves contractile function and alters nos gene and protein expression in reperfused skeletal muscle","volume":"24","author":"Patel","year":"2004","journal-title":"Microsurgery"},{"key":"B72","doi-asserted-by":"publisher","first-page":"36831","DOI":"10.1074\/jbc.274.52.36831","article-title":"A role for cysteine 3635 of RYR1 in redox modulation and calmodulin binding","volume":"274","author":"Porter Moore","year":"1999","journal-title":"J. Biol. Chem."},{"key":"B73","doi-asserted-by":"publisher","first-page":"133","DOI":"10.1042\/BJ20120787","article-title":"Nitric oxide signalling pathway in duchenne muscular dystrophy mice: Up-regulation of L-arginine transporters","volume":"449","author":"Ramachandran","year":"2013","journal-title":"Biochem. J."},{"key":"B74","doi-asserted-by":"publisher","first-page":"401","DOI":"10.1046\/j.1365-201X.1998.0303f.x","article-title":"Role of nitric oxide in skeletal muscle: Synthesis, distribution and functional importance","volume":"162","author":"Reid","year":"1998","journal-title":"Acta Physiol. Scand."},{"key":"B75","doi-asserted-by":"publisher","first-page":"514","DOI":"10.1016\/j.redox.2013.10.006","article-title":"Nitrosative stress in human skeletal muscle attenuated by exercise countermeasure after chronic disuse","volume":"1","author":"Salanova","year":"2013","journal-title":"Redox Biol."},{"key":"B76","doi-asserted-by":"publisher","first-page":"273","DOI":"10.1016\/j.jbiosc.2011.05.007","article-title":"Enhanced contractile force generation by artificial skeletal muscle tissues using IGF-I gene-engineered myoblast cells","volume":"112","author":"Sato","year":"2011","journal-title":"J. Biosci. Bioeng."},{"key":"B77","doi-asserted-by":"publisher","first-page":"H1167","DOI":"10.1152\/ajpheart.1999.277.3.H1167","article-title":"Codistribution of NOS and caveolin throughout peripheral vasculature and skeletal muscle of hamsters","volume":"277","author":"Segal","year":"1999","journal-title":"Am. J. Physiol."},{"key":"B78","doi-asserted-by":"publisher","first-page":"288","DOI":"10.1038\/s41598-019-57213-0","article-title":"Cell fibers promote proliferation of co-cultured cells on a dish","volume":"10","author":"Shima","year":"2020","journal-title":"Sci. Rep."},{"key":"B79","doi-asserted-by":"publisher","first-page":"115","DOI":"10.1016\/j.jbiosc.2012.08.024","article-title":"Evaluation systems of generated forces of skeletal muscle cell-based bio-actuators","volume":"115","author":"Shimizu","year":"2013","journal-title":"J. Biosci. Bioeng."},{"key":"B80","doi-asserted-by":"publisher","first-page":"D504","DOI":"10.2741\/squier","article-title":"Protein oxidation and age-dependent alterations in calcium homeostasis","volume":"5","author":"Squier","year":"2000","journal-title":"Front. Biosci."},{"key":"B81","doi-asserted-by":"publisher","first-page":"209","DOI":"10.1152\/physrev.2001.81.1.209","article-title":"Physiology of nitric oxide in skeletal muscle","volume":"81","author":"Stamler","year":"2001","journal-title":"Physiol. Rev."},{"key":"B82","doi-asserted-by":"publisher","first-page":"68","DOI":"10.1016\/j.freeradbiomed.2012.12.010","article-title":"Quantitative site-specific reactivity profiling of S-nitrosylation in mouse skeletal muscle using cysteinyl peptide enrichment coupled with mass spectrometry","volume":"57","author":"Su","year":"2013","journal-title":"Free Radic. Biol. Med."},{"key":"B83","doi-asserted-by":"publisher","first-page":"11158","DOI":"10.1073\/pnas.201289098","article-title":"Cysteine-3635 is responsible for skeletal muscle ryanodine receptor modulation by NO","volume":"98","author":"Sun","year":"2001","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"B84","doi-asserted-by":"publisher","first-page":"8184","DOI":"10.1074\/jbc.M211940200","article-title":"Nitric oxide, NOC-12, and S-nitrosoglutathione modulate the skeletal muscle calcium release channel\/ryanodine receptor by different mechanisms. An allosteric function for O2 in S-nitrosylation of the channel","volume":"278","author":"Sun","year":"2003","journal-title":"J. Biol. Chem."},{"key":"B85","doi-asserted-by":"publisher","first-page":"4209","DOI":"10.1113\/jphysiol.2008.156083","article-title":"Nitric oxide-cGMP-protein kinase G pathway negatively regulates vascular transient receptor potential channel TRPC6","volume":"586","author":"Takahashi","year":"2008","journal-title":"J. Physiol."},{"key":"B86","doi-asserted-by":"publisher","first-page":"2053","DOI":"10.1084\/jem.20080106","article-title":"Crucial role of nitric oxide synthases system in endothelium-dependent hyperpolarization in mice","volume":"205","author":"Takaki","year":"2008","journal-title":"J. Exp. Med."},{"key":"B87","doi-asserted-by":"publisher","first-page":"437","DOI":"10.1097\/01.fjc.0000139450.64337.cd","article-title":"Up-regulated neuronal nitric oxide synthase compensates coronary flow response to bradykinin in endothelial nitric oxide synthase-deficient mice","volume":"44","author":"Talukder","year":"2004","journal-title":"J. Cardiovasc. Pharmacol."},{"key":"B88","doi-asserted-by":"publisher","first-page":"2415","DOI":"10.1152\/jappl.1996.81.6.2415","article-title":"Expression of the inducible nitric oxide synthase gene in diaphragm and skeletal muscle","volume":"81","author":"Thompson","year":"1996","journal-title":"J. Appl. Physiol."},{"key":"B89","doi-asserted-by":"publisher","first-page":"e0243660","DOI":"10.1371\/journal.pone.0243660","article-title":"Potential roles of neuronal nitric oxide synthase and the PTEN-induced kinase 1 (PINK1)\/Parkin pathway for mitochondrial protein degradation in disuse-induced soleus muscle atrophy in adult rats","volume":"15","author":"Uda","year":"2020","journal-title":"PLoS One"},{"key":"B90","doi-asserted-by":"publisher","first-page":"345","DOI":"10.1007\/978-1-4419-9280-2_45","article-title":"Contribution of neural and endothelial isoforms of the nitric oxide synthase to the inhibitory effects of NO on the cat carotid body","volume":"536","author":"Valdes","year":"2003","journal-title":"Adv. Exp. Med. Biol."},{"key":"B91","doi-asserted-by":"publisher","first-page":"e4267","DOI":"10.3791\/4267","article-title":"Engineering skeletal muscle tissues from murine myoblast progenitor cells and application of electrical stimulation","volume":"73","author":"van der Schaft","year":"2013","journal-title":"J. Vis. Exp."},{"key":"B92","doi-asserted-by":"publisher","first-page":"2195","DOI":"10.1089\/hum.1996.7.17-2195","article-title":"Tissue-engineered skeletal muscle organoids for reversible gene therapy","volume":"7","author":"Vandenburgh","year":"1996","journal-title":"Hum. Gene Ther."},{"key":"B93","doi-asserted-by":"publisher","first-page":"91","DOI":"10.1016\/0021-9290(91)90380-6","article-title":"Mechanically induced alterations in cultured skeletal muscle growth","volume":"24","author":"Vandenburgh","year":"","journal-title":"J. Biomech."},{"key":"B94","doi-asserted-by":"publisher","first-page":"C475","DOI":"10.1152\/ajpcell.1991.260.3.C475","article-title":"Insulin and IGF-I induce pronounced hypertrophy of skeletal myofibers in tissue culture","volume":"260","author":"Vandenburgh","year":"","journal-title":"Am. J. Physiol."},{"key":"B95","doi-asserted-by":"publisher","first-page":"2860","DOI":"10.1096\/fasebj.5.13.1916108","article-title":"Computer-aided mechanogenesis of skeletal muscle organs from single cells in vitro","volume":"5","author":"Vandenburgh","year":"","journal-title":"FASEB J."},{"key":"B96","doi-asserted-by":"publisher","first-page":"657","DOI":"10.1042\/bj3400657","article-title":"Protein modification during biological aging: Selective tyrosine nitration of the SERCA2a isoform of the sarcoplasmic reticulum Ca2+-ATPase in skeletal muscle","volume":"340","author":"Viner","year":"1999","journal-title":"Biochem. J."},{"key":"B97","doi-asserted-by":"publisher","first-page":"455","DOI":"10.1007\/s004010050733","article-title":"Ultrastructural localization of alpha 1-syntrophin and neuronal nitric oxide synthase in normal skeletal myofiber, and their relation to each other and to dystrophin","volume":"94","author":"Wakayama","year":"1997","journal-title":"Acta Neuropathol."},{"key":"B98","doi-asserted-by":"publisher","first-page":"23341","DOI":"10.1074\/jbc.M513341200","article-title":"The sarcolemmal calcium pump, alpha-1 syntrophin, and neuronal nitric-oxide synthase are parts of a macromolecular protein complex","volume":"281","author":"Williams","year":"2006","journal-title":"J. Biol. Chem."},{"key":"B99","doi-asserted-by":"publisher","first-page":"607","DOI":"10.3389\/fphys.2017.00607","article-title":"NO-sGC pathway modulates Ca(2+) release and muscle contraction in zebrafish skeletal muscle","volume":"8","author":"Xiyuan","year":"2017","journal-title":"Front. Physiol."}],"container-title":["Frontiers in Physiology"],"original-title":[],"link":[{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2022.946682\/full","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2022,8,15]],"date-time":"2022-08-15T08:31:16Z","timestamp":1660552276000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.frontiersin.org\/articles\/10.3389\/fphys.2022.946682\/full"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2022,8,15]]},"references-count":99,"alternative-id":["10.3389\/fphys.2022.946682"],"URL":"https:\/\/doi.org\/10.3389\/fphys.2022.946682","relation":{},"ISSN":["1664-042X"],"issn-type":[{"value":"1664-042X","type":"electronic"}],"subject":[],"published":{"date-parts":[[2022,8,15]]},"article-number":"946682"}}