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Emerging data demonstrates that nanoscale changes to the regularity of sarcomere structure can affect the overall function of the protein dense ~2\u03bcm sarcomere. Further, sarcomere structure is implicated in many clinical conditions of muscle weakness. However, our understanding of how sarcomere structure changes in disease, especially at the nanoscale, has been limited in part due to the inability to robustly detect and measure at sub-sarcomere resolution. We optimized several methodological steps and developed a robust pipeline to analyze sarcomere structure using structured illumination super-resolution microscopy in conjunction with commercially-available and fluorescently-conjugated Variable Heavy-Chain only fragment secondary antibodies (nanobodies), and achieved a significant increase in resolution of z-disc width (353nm vs. 62nm) compared to confocal microscopy. 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Brynnel","year":"2018","journal-title":"Elife"},{"key":"pone.0300348.ref012","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-017-01144-9","article-title":"The giant protein titin regulates the length of the striated muscle thick filament","volume":"8","author":"P Tonino","year":"2017","journal-title":"Nature Communications"},{"key":"pone.0300348.ref013","doi-asserted-by":"crossref","first-page":"59","DOI":"10.1161\/01.RES.86.1.59","article-title":"Differential Expression of Cardiac Titin Isoforms and Modulation of Cellular Stiffness","volume":"86","author":"O Cazorla","year":"2000","journal-title":"Circ Res"},{"key":"pone.0300348.ref014","doi-asserted-by":"crossref","first-page":"1187","DOI":"10.1007\/s12551-017-0395-y","article-title":"The multiple roles of titin in muscle contraction and force production","volume":"10","author":"W Herzog","year":"2018","journal-title":"Biophys 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Herzog","year":"1992","journal-title":"J Biomech"},{"key":"pone.0300348.ref025","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1111\/j.1365-2818.1977.tb00067.x","article-title":"Cryo-ultramicrotomy and myofibrillar fine structure: a review","volume":"111","author":"M Sj\u00f6str\u00f6m","year":"1977","journal-title":"J Microsc"},{"key":"pone.0300348.ref026","article-title":"Nanometer-scale structure differences in the myofilament lattice spacing of two cockroach leg muscles correspond to their different functions","volume":"223","author":"TC Tune","year":"2020","journal-title":"J Exp Biol"},{"key":"pone.0300348.ref027","doi-asserted-by":"crossref","DOI":"10.3389\/fphys.2014.00375","article-title":"Alterations in thin filament length during postnatal skeletal muscle development and aging in mice","volume":"5","author":"DS Gokhin","year":"2014","journal-title":"Front Physiol"},{"key":"pone.0300348.ref028","doi-asserted-by":"crossref","first-page":"1483","DOI":"10.1083\/jcb.145.7.1483","article-title":"Thin Filament Protein Dynamics in Fully Differentiated Adult Cardiac Myocytes: Toward A Model of Sarcomere Maintenance","volume":"145","author":"DE Michele","year":"1999","journal-title":"Journal of Cell Biology"},{"key":"pone.0300348.ref029","first-page":"261","volume":"62","author":"J. Robbins","year":"2003","journal-title":"Remodeling the Cardiac Sarcomere Using Transgenesis"},{"key":"pone.0300348.ref030","doi-asserted-by":"crossref","first-page":"1614","DOI":"10.1093\/emboj\/17.6.1614","article-title":"Molecular structure of the sarcomeric Z-disk: two types of titin interactions lead to an asymmetrical sorting of \u03b1-actinin","volume":"17","author":"P Young","year":"1998","journal-title":"EMBO J"},{"key":"pone.0300348.ref031","doi-asserted-by":"crossref","first-page":"1663","DOI":"10.1002\/ar.22966","article-title":"Cell biology of sarcomeric protein engineering: disease modeling and therapeutic potential","volume":"297","author":"BR Thompson","year":"2014","journal-title":"Anat Rec (Hoboken)"},{"key":"pone.0300348.ref032","doi-asserted-by":"crossref","first-page":"13118","DOI":"10.1074\/jbc.M212601200","article-title":"Sarcomere Thin Filament Regulatory Isoforms","volume":"278","author":"JM Metzger","year":"2003","journal-title":"Journal of Biological Chemistry"},{"key":"pone.0300348.ref033","doi-asserted-by":"crossref","first-page":"1127","DOI":"10.1152\/jappl.2000.88.3.1127","article-title":"Form follows function: How muscle shape is regulated by work","volume":"88","author":"B Russell","year":"2000","journal-title":"J Appl Physiol"},{"key":"pone.0300348.ref034","unstructured":"Skeletal muscle weakness in old age: underlying mechanisms: Medicine & Science in Sports & Exercise. [cited 26 Jul 2023]. https:\/\/journals.lww.com\/acsm-msse\/Abstract\/1994\/04000\/Skeletal_muscle_weakness_in_old_age__underlying.6.aspx."},{"key":"pone.0300348.ref035","doi-asserted-by":"crossref","first-page":"1482","DOI":"10.2353\/ajpath.2008.070576","article-title":"Myofilament Degradation and Dysfunction of Human Cardiomyocytes in Fabry Disease","volume":"172","author":"C Chimenti","year":"2008","journal-title":"Am J Pathol"},{"key":"pone.0300348.ref036","doi-asserted-by":"crossref","first-page":"19090","DOI":"10.1073\/pnas.1014523107","article-title":"CLOCK and BMAL1 regulate MyoD and are necessary for maintenance of skeletal muscle phenotype and function","volume":"107","author":"JL Andrews","year":"2010","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0300348.ref037","first-page":"1321","volume":"88","author":"WR Frontera","year":"2000","journal-title":"Aging of skeletal muscle: a 12-yr longitudinal study"},{"key":"pone.0300348.ref038","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/2046-2395-3-9","article-title":"It is not just muscle mass: A review of muscle quality, composition and metabolism during ageing as determinants of muscle function and mobility in later life","volume":"3","author":"RA McGregor","year":"2014","journal-title":"Longev Healthspan"},{"key":"pone.0300348.ref039","doi-asserted-by":"crossref","first-page":"458","DOI":"10.1249\/MSS.0000000000001448","article-title":"Associations of Muscle Mass and Strength with All-Cause Mortality among US Older Adults","volume":"50","author":"R Li","year":"2018","journal-title":"Med Sci Sports Exerc"},{"key":"pone.0300348.ref040","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1007\/s10549-005-5991-z","article-title":"Objective and Subjective Upper Body Function Six Months Following Diagnosis of Breast Cancer","volume":"94","author":"S Hayes","year":"2005","journal-title":"Breast Cancer Research and 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Muscle"},{"key":"pone.0300348.ref050","doi-asserted-by":"crossref","first-page":"434","DOI":"10.1161\/CIRCGENETICS.113.000448","article-title":"Sarcomere mutation-specific expression patterns in human hypertrophic cardiomyopathy","volume":"7","author":"AS Helms","year":"2014","journal-title":"Circ Cardiovasc Genet"},{"key":"pone.0300348.ref051","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41467-021-23272-z","article-title":"Cardiomyocyte contractile impairment in heart failure results from reduced BAG3-mediated sarcomeric protein turnover","volume":"12","author":"TG Martin","year":"2021","journal-title":"Nature Communications"},{"key":"pone.0300348.ref052","doi-asserted-by":"crossref","first-page":"1607","DOI":"10.1242\/jcs.080085","article-title":"Super-resolution microscopy at a glance","volume":"124","author":"CG Galbraith","year":"2011","journal-title":"J Cell Sci"},{"key":"pone.0300348.ref053","doi-asserted-by":"crossref","first-page":"15","DOI":"10.4081\/ejtm.2015.4747","article-title":"Revealing T-Tubules in Striated Muscle with New Optical Super-Resolution Microscopy Techniquess","volume":"25","author":"ID Jayasinghe","year":"2015","journal-title":"Eur J Transl Myol"},{"key":"pone.0300348.ref054","doi-asserted-by":"crossref","first-page":"159980","DOI":"10.1371\/journal.pone.0159980","article-title":"Comparison of Confocal and Super-Resolution Reflectance Imaging of Metal Oxide Nanoparticles","volume":"11","author":"EJ Guggenheim","year":"2016","journal-title":"PLoS One"},{"key":"pone.0300348.ref055","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3390\/ijms22041903","article-title":"Comparing Super-Resolution Microscopy Techniques to Analyze Chromosomes","volume":"22","author":"I Kubalov\u00e1","year":"2021","journal-title":"Int J Mol Sci"},{"key":"pone.0300348.ref056","article-title":"Super-resolution microscopy: a brief 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Microscopy"},{"key":"pone.0300348.ref066","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/srep09793","article-title":"Avoiding drying-artifacts in transmission electron microscopy: Characterizing the size and colloidal state of nanoparticles","volume":"5","author":"B Michen","year":"2015","journal-title":"Scientific Reports"},{"key":"pone.0300348.ref067","first-page":"e52793","article-title":"Do\u2019s and Don\u2019ts in the Preparation of Muscle Cryosections for Histological Analysis","volume":"2015","author":"A Kumar","year":"2015","journal-title":"JoVE (Journal of Visualized Experiments)"},{"key":"pone.0300348.ref068","first-page":"241","article-title":"Double staining immunohistochemistry","volume":"2","author":"X Chen","year":"2010","journal-title":"N Am J Med Sci"},{"key":"pone.0300348.ref069","first-page":"327","volume":"45","author":"SR Shi","year":"2016","journal-title":"Antigen Retrieval Immunohistochemistry: Past, Present, and Future"},{"key":"pone.0300348.ref070","doi-asserted-by":"crossref","first-page":"125","DOI":"10.1016\/j.acthis.2018.10.011","article-title":"Comparison of different methodologies and cryostat versus paraffin sections for chromogenic immunohistochemistry","volume":"121","author":"VVV Hira","year":"2019","journal-title":"Acta Histochem"},{"key":"pone.0300348.ref071","first-page":"13","volume":"59","author":"SR Shi","year":"2011","journal-title":"Antigen Retrieval Immunohistochemistry: Review and Future Prospects in Research and Diagnosis over Two Decades"},{"key":"pone.0300348.ref072","doi-asserted-by":"crossref","first-page":"e87","DOI":"10.14440\/jbm.2018.219","article-title":"Isolation, cultivation and immunostaining of single myofibers: An improved approach to study the behavior of satellite cells","volume":"5","author":"CL Lim","year":"2018","journal-title":"J Biol 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regions: biomechanical and metabolic signaling hubs in cross-striated muscles","volume":"13","author":"RJ van der Pijl","year":"2021","journal-title":"Biophys Rev"},{"key":"pone.0300348.ref084","doi-asserted-by":"crossref","first-page":"2100","DOI":"10.1016\/j.apmr.2018.01.008","article-title":"Muscular Strength as a Predictor of All-Cause Mortality in an Apparently Healthy Population: A Systematic Review and Meta-Analysis of Data From Approximately 2 Million Men and Women","volume":"99","author":"A Garc\u00eda-Hermoso","year":"2018","journal-title":"Arch Phys Med Rehabil"},{"key":"pone.0300348.ref085","doi-asserted-by":"crossref","first-page":"697621","DOI":"10.3389\/fnagi.2021.697621","article-title":"Functional Aging in Male C57BL\/6J Mice Across the Life-Span: A Systematic Behavioral Analysis of Motor, Emotional, and Memory Function to Define an Aging Phenotype","volume":"13","author":"S Yanai","year":"2021","journal-title":"Front Aging Neurosci"},{"key":"pone.0300348.ref086","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-70987-y","article-title":"The D2.mdx mouse as a preclinical model of the skeletal muscle pathology associated with Duchenne muscular dystrophy","volume":"10","author":"DW Hammers","year":"2020","journal-title":"Scientific Reports"},{"key":"pone.0300348.ref087","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-020-74192-9","article-title":"Lifetime analysis of mdx skeletal muscle reveals a progressive pathology that leads to myofiber loss","volume":"10","author":"RT Massopust","year":"2020","journal-title":"Sci Rep"},{"key":"pone.0300348.ref088","doi-asserted-by":"crossref","DOI":"10.1016\/j.bbamcr.2019.02.003","article-title":"The M-band: The underestimated part of the sarcomere","volume":"1867","author":"S Lange","year":"2020","journal-title":"Biochim Biophys Acta Mol Cell Res"},{"key":"pone.0300348.ref089","doi-asserted-by":"crossref","DOI":"10.3390\/ijms22147563","article-title":"Titin N2A Domain and Its Interactions at the Sarcomere","volume":"22","author":"AO Adewale","year":"2021","journal-title":"Int J Mol Sci"},{"key":"pone.0300348.ref090","doi-asserted-by":"crossref","first-page":"527","DOI":"10.1007\/BF01753569","article-title":"The Z-band lattice in skeletal muscle before, during and after tetanic contraction","volume":"7","author":"MA Goldstein","year":"1986","journal-title":"J Muscle Res Cell Motil"},{"key":"pone.0300348.ref091","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1038\/s41598-020-73247-1","article-title":"Nanoscopic changes in the lattice structure of striated muscle sarcomeres involved in the mechanism of spontaneous oscillatory contraction (SPOC)","volume":"10","author":"F Kono","year":"2020","journal-title":"Scientific Reports"},{"key":"pone.0300348.ref092","first-page":"20130697","article-title":"The length\u2013tension curve in muscle depends on lattice spacing. Proceedings of the Royal Society B","volume":"280","author":"CD Williams","year":"2013","journal-title":"Biological Sciences"},{"key":"pone.0300348.ref093","doi-asserted-by":"crossref","first-page":"4079","DOI":"10.1016\/j.bpj.2021.08.006","article-title":"A mechanism for sarcomere breathing: volume change and advective flow within the myofilament lattice","volume":"120","author":"JA Cass","year":"2021","journal-title":"Biophys J"},{"key":"pone.0300348.ref094","doi-asserted-by":"crossref","first-page":"784","DOI":"10.1038\/nature07104","article-title":"Minimally invasive high-speed imaging of sarcomere contractile dynamics in mice and humans","volume":"454","author":"ME Llewellyn","year":"2008","journal-title":"Nature"},{"key":"pone.0300348.ref095","first-page":"373","volume":"50","author":"JD Powers","year":"2021","journal-title":"The Sliding Filament Theory Since Andrew Huxley: Multiscale and Multidisciplinary Muscle Research"},{"key":"pone.0300348.ref096","doi-asserted-by":"crossref","first-page":"27","DOI":"10.3389\/fphys.2022.837611","article-title":"What Can We Learn from Single Sarcomere and Myofibril Preparations?","volume":"13","author":"W. Herzog","year":"2022","journal-title":"Front Physiol"},{"key":"pone.0300348.ref097","article-title":"Isolation and Culture of Individual Myofibers and their Satellite Cells from Adult Skeletal Muscle","volume":"50074","author":"A Pasut","year":"2013","journal-title":"J Vis Exp"},{"key":"pone.0300348.ref098","first-page":"e50259","article-title":"Analysis of Embryonic and Larval Zebrafish Skeletal Myofibers from Dissociated Preparations","author":"EJ Horstick","year":"2013","journal-title":"JoVE (Journal of Visualized Experiments)"},{"key":"pone.0300348.ref099","doi-asserted-by":"crossref","first-page":"141","DOI":"10.1007\/978-1-4939-3810-0_11","article-title":"Isolation, culture, functional assays, and immunofluorescence of myofiber-associated satellite cells","volume":"1460","author":"TO Vogler","year":"2016","journal-title":"Methods in Molecular Biology"},{"key":"pone.0300348.ref100","doi-asserted-by":"crossref","DOI":"10.21769\/BioProtoc.1942","article-title":"Isolation, Culture, and Staining of Single Myofibers","volume":"6","author":"YS Gallot","year":"2016","journal-title":"Bio Protoc"},{"key":"pone.0300348.ref101","doi-asserted-by":"crossref","first-page":"15","DOI":"10.1167\/iovs.61.3.15","article-title":"Complex Correlations Between Desmin Content, Myofiber Types, and Innervation Patterns in the Human Extraocular Muscles","volume":"61","author":"JX Liu","year":"2020","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"pone.0300348.ref102","doi-asserted-by":"crossref","first-page":"1216","DOI":"10.1113\/EP090666","article-title":"Changes in vastus lateralis fibre cross-sectional area, pennation angle and fascicle length do not predict changes in muscle cross-sectional area","volume":"107","author":"BA Ruple","year":"2022","journal-title":"Exp Physiol"},{"key":"pone.0300348.ref103","doi-asserted-by":"crossref","first-page":"1172","DOI":"10.1161\/CIRCRESAHA.118.314505","article-title":"SarcTrack","volume":"124","author":"CN Toepfer","year":"2019","journal-title":"Circ Res"},{"key":"pone.0300348.ref104","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.87065","article-title":"Independent regulation of Z-lines and M-lines during sarcomere assembly in cardiac myocytes revealed by the automatic image analysis software sarcApp","volume":"12","author":"AC Neininger-Castro","year":"2023","journal-title":"Elife"},{"key":"pone.0300348.ref105","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1186\/s13395-019-0203-4","article-title":"Culturing C2C12 myotubes on micromolded gelatin hydrogels accelerates myotube maturation","volume":"9","author":"LT Denes","year":"2019","journal-title":"Skelet Muscle"},{"key":"pone.0300348.ref106","doi-asserted-by":"crossref","first-page":"340","DOI":"10.1161\/CIRCRESAHA.108.182469","article-title":"Myofibrillar architecture in engineered cardiac myocytes","volume":"103","author":"KK Parker","year":"2008","journal-title":"Circ Res"},{"key":"pone.0300348.ref107","doi-asserted-by":"crossref","first-page":"2453","DOI":"10.1089\/ten.tea.2012.0181","article-title":"Engineered contractile skeletal muscle tissue on a microgrooved methacrylated gelatin substrate","volume":"18","author":"V Hosseini","year":"2012","journal-title":"Tissue Eng Part A"},{"key":"pone.0300348.ref108","doi-asserted-by":"crossref","first-page":"841","DOI":"10.1074\/mcp.M114.044222","article-title":"Deep Proteomics of Mouse Skeletal Muscle Enables Quantitation of Protein Isoforms, Metabolic Pathways, and Transcription Factors","volume":"14","author":"AS Deshmukh","year":"2015","journal-title":"Molecular & Cellular Proteomics"},{"key":"pone.0300348.ref109","doi-asserted-by":"crossref","first-page":"e2008861118","DOI":"10.1073\/pnas.2008861118","article-title":"Sarcomeres regulate murine cardiomyocyte maturation through MRTF-SRF signaling","volume":"118","author":"Y Guo","year":"2021","journal-title":"Proc Natl Acad Sci U S A"},{"key":"pone.0300348.ref110","article-title":"Nanoscopy reveals the layered organization of the sarcomeric H-zone and I-band complexes","volume":"219","author":"S Szikora","year":"2020","journal-title":"Journal of Cell Biology"},{"key":"pone.0300348.ref111","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.79344","article-title":"Nanobodies combined with DNA-PAINT super-resolution reveal a staggered titin nanoarchitecture in flight muscles","volume":"12","author":"F Schueder","year":"2023","journal-title":"Elife"},{"key":"pone.0300348.ref112","doi-asserted-by":"crossref","DOI":"10.1016\/j.jbc.2021.100791","article-title":"Seeing beyond the limit: A guide to choosing the right super-resolution microscopy technique","volume":"297","author":"J Valli","year":"2021","journal-title":"J Biol Chem"},{"key":"pone.0300348.ref113","doi-asserted-by":"crossref","first-page":"1013","DOI":"10.1083\/jcb.143.4.1013","article-title":"The NH2 terminus of titin spans the Z-disc: its interaction with a novel 19-kD ligand (T-cap) is required for sarcomeric integrity","volume":"143","author":"CC Gregorio","year":"1998","journal-title":"J Cell Biol"},{"key":"pone.0300348.ref114","doi-asserted-by":"crossref","first-page":"695","DOI":"10.1161\/CIRCRESAHA.109.206243","article-title":"A common MLP (Muscle LIM protein) variant is associated with cardiomyopathy","volume":"106","author":"R Knoll","year":"2010","journal-title":"Circ Res"},{"key":"pone.0300348.ref115","doi-asserted-by":"crossref","first-page":"717","DOI":"10.1006\/jmbi.2001.4448","article-title":"Identification of muscle specific ring finger proteins as potential regulators of the titin kinase domain","volume":"306","author":"T Centner","year":"2001","journal-title":"J Mol Biol"},{"key":"pone.0300348.ref116","doi-asserted-by":"crossref","DOI":"10.1038\/s41598-019-40308-z","article-title":"Femtosecond laser-based nanosurgery reveals the endogenous regeneration of single Z-discs including physiological consequences for cardiomyocytes","volume":"9","author":"D M\u00fcller","year":"2019","journal-title":"Sci Rep"},{"key":"pone.0300348.ref117","article-title":"Structure of the thin filament in native skeletal muscles reveals its interaction with nebulin and two distinct conformations of myosin","author":"Z Wang","year":"2021","journal-title":"bioRxiv"},{"key":"pone.0300348.ref118","doi-asserted-by":"crossref","first-page":"317","DOI":"10.1111\/j.1432-1033.1996.00317.x","article-title":"A Molecular Map of the Interactions between Titin and Myosin-Binding Protein C","volume":"235","author":"A Freiburg","year":"1996","journal-title":"Eur J Biochem"},{"key":"pone.0300348.ref119","doi-asserted-by":"crossref","first-page":"1157","DOI":"10.1016\/S0022-2836(02)00372-8","article-title":"Muscle Z-band Ultrastructure: Titin Z-repeats and Z-band Periodicities Do Not Match","volume":"319","author":"PK Luther","year":"2002","journal-title":"J Mol 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