{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,10,18]],"date-time":"2026-10-18T17:58:14Z","timestamp":1792346294172,"version":"4.4.0"},"reference-count":59,"publisher":"MDPI AG","issue":"3","license":[{"start":{"date-parts":[[2024,2,23]],"date-time":"2024-02-23T00:00:00Z","timestamp":1708646400000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/creativecommons.org\/licenses\/by\/4.0\/"}],"funder":[{"DOI":"10.13039\/100004411","name":"Heart and Stroke Foundation of Canada","doi-asserted-by":"publisher","award":["G-18-0022185"],"award-info":[{"award-number":["G-18-0022185"]}],"id":[{"id":"10.13039\/100004411","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004411","name":"Heart and Stroke Foundation of Canada","doi-asserted-by":"publisher","award":["RGPIN-2016-04879"],"award-info":[{"award-number":["RGPIN-2016-04879"]}],"id":[{"id":"10.13039\/100004411","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004411","name":"Heart and Stroke Foundation of Canada","doi-asserted-by":"publisher","award":["RGPIN-2022-03150"],"award-info":[{"award-number":["RGPIN-2022-03150"]}],"id":[{"id":"10.13039\/100004411","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004411","name":"Heart and Stroke Foundation of Canada","doi-asserted-by":"publisher","award":["NFRFE-1269 2021-00219"],"award-info":[{"award-number":["NFRFE-1269 2021-00219"]}],"id":[{"id":"10.13039\/100004411","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004411","name":"Heart and Stroke Foundation of Canada","doi-asserted-by":"publisher","award":["PG\/14\/46\/30911"],"award-info":[{"award-number":["PG\/14\/46\/30911"]}],"id":[{"id":"10.13039\/100004411","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/100004411","name":"Heart and Stroke Foundation of Canada","doi-asserted-by":"publisher","award":["PG\/19\/13\/34247"],"award-info":[{"award-number":["PG\/19\/13\/34247"]}],"id":[{"id":"10.13039\/100004411","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["G-18-0022185"],"award-info":[{"award-number":["G-18-0022185"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["RGPIN-2016-04879"],"award-info":[{"award-number":["RGPIN-2016-04879"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["RGPIN-2022-03150"],"award-info":[{"award-number":["RGPIN-2022-03150"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["NFRFE-1269 2021-00219"],"award-info":[{"award-number":["NFRFE-1269 2021-00219"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["PG\/14\/46\/30911"],"award-info":[{"award-number":["PG\/14\/46\/30911"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000038","name":"Natural Sciences and Engineering Research Council of Canada","doi-asserted-by":"publisher","award":["PG\/19\/13\/34247"],"award-info":[{"award-number":["PG\/19\/13\/34247"]}],"id":[{"id":"10.13039\/501100000038","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000023","name":"Government of Canada\u2019s New Frontiers in Research Fund","doi-asserted-by":"publisher","award":["G-18-0022185"],"award-info":[{"award-number":["G-18-0022185"]}],"id":[{"id":"10.13039\/501100000023","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000023","name":"Government of Canada\u2019s New Frontiers in Research Fund","doi-asserted-by":"publisher","award":["RGPIN-2016-04879"],"award-info":[{"award-number":["RGPIN-2016-04879"]}],"id":[{"id":"10.13039\/501100000023","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000023","name":"Government of Canada\u2019s New Frontiers in Research Fund","doi-asserted-by":"publisher","award":["RGPIN-2022-03150"],"award-info":[{"award-number":["RGPIN-2022-03150"]}],"id":[{"id":"10.13039\/501100000023","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000023","name":"Government of Canada\u2019s New Frontiers in Research Fund","doi-asserted-by":"publisher","award":["NFRFE-1269 2021-00219"],"award-info":[{"award-number":["NFRFE-1269 2021-00219"]}],"id":[{"id":"10.13039\/501100000023","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000023","name":"Government of Canada\u2019s New Frontiers in Research Fund","doi-asserted-by":"publisher","award":["PG\/14\/46\/30911"],"award-info":[{"award-number":["PG\/14\/46\/30911"]}],"id":[{"id":"10.13039\/501100000023","id-type":"DOI","asserted-by":"publisher"}]},{"DOI":"10.13039\/501100000023","name":"Government of Canada\u2019s New Frontiers in Research Fund","doi-asserted-by":"publisher","award":["PG\/19\/13\/34247"],"award-info":[{"award-number":["PG\/19\/13\/34247"]}],"id":[{"id":"10.13039\/501100000023","id-type":"DOI","asserted-by":"publisher"}]},{"name":"British Heart Foundation","award":["G-18-0022185"],"award-info":[{"award-number":["G-18-0022185"]}]},{"name":"British Heart Foundation","award":["RGPIN-2016-04879"],"award-info":[{"award-number":["RGPIN-2016-04879"]}]},{"name":"British Heart Foundation","award":["RGPIN-2022-03150"],"award-info":[{"award-number":["RGPIN-2022-03150"]}]},{"name":"British Heart Foundation","award":["NFRFE-1269 2021-00219"],"award-info":[{"award-number":["NFRFE-1269 2021-00219"]}]},{"name":"British Heart Foundation","award":["PG\/14\/46\/30911"],"award-info":[{"award-number":["PG\/14\/46\/30911"]}]},{"name":"British Heart Foundation","award":["PG\/19\/13\/34247"],"award-info":[{"award-number":["PG\/19\/13\/34247"]}]}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Genes"],"abstract":"<jats:p>Popeye domain-containing (POPDC) proteins selectively bind cAMP and mediate cellular responses to sympathetic nervous system (SNS) stimulation. The first discovered human genetic variant (POPDC1S201F) is associated with atrioventricular (AV) block, which is exacerbated by increased SNS activity. Zebrafish carrying the homologous mutation (popdc1S191F) display a similar phenotype to humans. To investigate the impact of POPDC1 dysfunction on cardiac electrophysiology and intracellular calcium handling, homozygous popdc1S191F and popdc1 knock-out (popdc1KO) zebrafish larvae and adult isolated popdc1S191F hearts were studied by functional fluorescent analysis. It was found that in popdc1S191F and popdc1KO larvae, heart rate (HR), AV delay, action potential (AP) and calcium transient (CaT) upstroke speed, and AP duration were less than in wild-type larvae, whereas CaT duration was greater. SNS stress by \u03b2-adrenergic receptor stimulation with isoproterenol increased HR, lengthened AV delay, slowed AP and CaT upstroke speed, and shortened AP and CaT duration, yet did not result in arrhythmias. In adult popdc1S191F zebrafish hearts, there was a higher incidence of AV block, slower AP upstroke speed, and longer AP duration compared to wild-type hearts, with no differences in CaT. SNS stress increased AV delay and led to further AV block in popdc1S191F hearts while decreasing AP and CaT duration. Overall, we have revealed that arrhythmogenic effects of POPDC1 dysfunction on cardiac electrophysiology and intracellular calcium handling in zebrafish are varied, but already present in early development, and that AV node dysfunction may underlie SNS-induced arrhythmogenesis associated with popdc1 mutation in adults.<\/jats:p>","DOI":"10.3390\/genes15030280","type":"journal-article","created":{"date-parts":[[2024,2,23]],"date-time":"2024-02-23T06:07:39Z","timestamp":1708668459000},"page":"280","update-policy":"https:\/\/doi.org\/10.3390\/mdpi_crossmark_policy","source":"Crossref","is-referenced-by-count":3,"title":["POPDC1 Variants Cause Atrioventricular Node Dysfunction and Arrhythmogenic Changes in Cardiac Electrophysiology and Intracellular Calcium Handling in Zebrafish"],"prefix":"10.3390","volume":"15","author":[{"given":"Matthew R.","family":"Stoyek","sequence":"first","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sarah E.","family":"Doane","sequence":"additional","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shannon E.","family":"Dallaire","sequence":"additional","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0009-0008-8974-5143","authenticated-orcid":false,"given":"Zachary D.","family":"Long","sequence":"additional","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Jessica M.","family":"Ramia","sequence":"additional","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Donovan L.","family":"Cassidy-Nolan","sequence":"additional","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Kar-Lai","family":"Poon","sequence":"additional","affiliation":[{"name":"National Heart & Lung Institute, Imperial College London, London W12 0NN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0001-7090-5356","authenticated-orcid":false,"given":"Thomas","family":"Brand","sequence":"additional","affiliation":[{"name":"National Heart & Lung Institute, Imperial College London, London W12 0NN, UK"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"ORCID":"https:\/\/orcid.org\/0000-0002-2437-5785","authenticated-orcid":false,"given":"T. Alexander","family":"Quinn","sequence":"additional","affiliation":[{"name":"Department of Physiology & Biophysics, Dalhousie University, Halifax, NS B3H 4R2, Canada"},{"name":"School of Biomedical Engineering, Dalhousie University, Halifax, NS B3H 4R2, Canada"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"1968","published-online":{"date-parts":[[2024,2,23]]},"reference":[{"key":"ref_1","doi-asserted-by":"crossref","first-page":"1423","DOI":"10.1002\/cphy.c140069","article-title":"Ion Channels in the Heart","volume":"5","author":"Bartos","year":"2015","journal-title":"Compr. Physiol."},{"key":"ref_2","doi-asserted-by":"crossref","first-page":"1083","DOI":"10.1152\/physrev.00024.2019","article-title":"Cardiac Transmembrane Ion Channels and Action Potentials: Cellular Physiology and Arrhythmogenic Behavior","volume":"101","author":"Tomek","year":"2021","journal-title":"Physiol. Rev."},{"key":"ref_3","doi-asserted-by":"crossref","first-page":"170","DOI":"10.3389\/fphys.2020.00170","article-title":"Neurohumoral Control of Sinoatrial Node Activity and Heart Rate: Insight from Experimental Models and Findings from Humans","volume":"11","author":"MacDonald","year":"2020","journal-title":"Front. Physiol."},{"key":"ref_4","doi-asserted-by":"crossref","unstructured":"Gruscheski, L., and Brand, T. (2021). The Role of POPDC Proteins in Cardiac Pacemaking and Conduction. J. Cardiovasc. Dev. Dis., 8.","DOI":"10.3390\/jcdd8120160"},{"key":"ref_5","doi-asserted-by":"crossref","first-page":"28","DOI":"10.1016\/j.pbiomolbio.2016.01.001","article-title":"The Popeye Domain Containing Protein Family\u2014A Novel Class of cAMP Effectors with Important Functions in Multiple Tissues","volume":"120","author":"Schindler","year":"2016","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_6","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1007\/s10974-019-09523-z","article-title":"The Popeye Domain Containing Gene Family Encoding a Family of cAMP-Effector Proteins with Important Functions in Striated Muscle and Beyond","volume":"40","author":"Swan","year":"2019","journal-title":"J. Musc. Res. Cell Motil."},{"key":"ref_7","doi-asserted-by":"crossref","first-page":"86","DOI":"10.1016\/j.yjmcc.2022.01.001","article-title":"Phosphodiesterase Type 4 Anchoring Regulates cAMP Signaling to Popeye Domain-Containing Proteins","volume":"165","author":"Tibbo","year":"2022","journal-title":"J. Mol. Cell. Cardiol."},{"key":"ref_8","doi-asserted-by":"crossref","first-page":"1119","DOI":"10.1172\/JCI59410","article-title":"Popeye Domain Containing Proteins Are Essential for Stress-Mediated Modulation of Cardiac Pacemaking in Mice","volume":"122","author":"Froese","year":"2012","journal-title":"J. Clin. Investig."},{"key":"ref_9","doi-asserted-by":"crossref","unstructured":"Holt, I., Fuller, H.R., Schindler, R.F.R., Shirran, S.L., Brand, T., and Morris, G.E. (2020). An Interaction of Heart Disease-Associated Proteins POPDC1\/2 with XIRP1 in Transverse Tubules and Intercalated Discs. BMC Mol. Cell Biol., 21.","DOI":"10.1186\/s12860-020-00329-3"},{"key":"ref_10","doi-asserted-by":"crossref","unstructured":"Soni, S., Raaijmakers, A.J.A., Raaijmakers, L.M., Damen, J.M.A., van Stuijvenberg, L., Vos, M.A., Heck, A.J.R., van Veen, T.A.B., and Scholten, A. (2016). A Proteomics Approach to Identify New Putative Cardiac Intercalated Disk Proteins. PLoS ONE, 11.","DOI":"10.1371\/journal.pone.0152231"},{"key":"ref_11","doi-asserted-by":"crossref","first-page":"362","DOI":"10.1161\/CIRCGENETICS.113.000133","article-title":"Weighted Gene Coexpression Network Analysis of Human Left Atrial Tissue Identifies Gene Modules Associated with Atrial Fibrillation","volume":"6","author":"Tan","year":"2013","journal-title":"Circ. Cardiovasc. Genet."},{"key":"ref_12","doi-asserted-by":"crossref","first-page":"239","DOI":"10.1172\/JCI79562","article-title":"POPDC1S201F Causes Muscular Dystrophy and Arrhythmia by Affecting Protein Trafficking","volume":"126","author":"Schindler","year":"2015","journal-title":"J. Clin. Investig."},{"key":"ref_13","doi-asserted-by":"crossref","first-page":"e10557","DOI":"10.7554\/eLife.10557","article-title":"Discovery and Validation of Sub-Threshold Genome-Wide Association Study Loci Using Epigenomic Signatures","volume":"5","author":"Wang","year":"2016","journal-title":"eLife"},{"key":"ref_14","doi-asserted-by":"crossref","first-page":"4","DOI":"10.1186\/s40478-022-01501-w","article-title":"Differential Effects of Mutations of POPDC Proteins on Heteromeric Interaction and Membrane Trafficking","volume":"11","author":"Swan","year":"2023","journal-title":"Acta Neuropathol. Commun."},{"key":"ref_15","doi-asserted-by":"crossref","first-page":"219","DOI":"10.1111\/cge.14238","article-title":"A Novel Biallelic Variant in the Popeye Domain-containing Protein 1 (POPDC1) Underlies Limb Girdle Muscle Dystrophy Type 25","volume":"103","author":"Mahmood","year":"2023","journal-title":"Clin. Genet."},{"key":"ref_16","doi-asserted-by":"crossref","first-page":"226","DOI":"10.1016\/j.ymgme.2022.05.005","article-title":"Proteomic and Morphological Insights and Clinical Presentation of Two Young Patients with Novel Mutations of BVES (POPDC1)","volume":"136","author":"Hentschel","year":"2022","journal-title":"Mol. Genet. Metab."},{"key":"ref_17","doi-asserted-by":"crossref","first-page":"117259","DOI":"10.1016\/j.jns.2020.117259","article-title":"Severe Adolescent-Onset Limb-Girdle Muscular Dystrophy Due to a Novel Homozygous Nonsense BVES Variant","volume":"420","author":"Beecher","year":"2021","journal-title":"J. Neurol. Sci."},{"key":"ref_18","doi-asserted-by":"crossref","first-page":"674","DOI":"10.1016\/j.nmd.2020.06.004","article-title":"Two Japanese LGMDR25 Patients with a Biallelic Recurrent Nonsense Variant of BVES","volume":"30","author":"Indrawati","year":"2020","journal-title":"Neuromuscul. Disord."},{"key":"ref_19","doi-asserted-by":"crossref","unstructured":"Meinke, P., Kerr, A.R.W., Czapiewski, R., De Las Heras, J.I., Dixon, C.R., Harris, E., K\u00f6lbel, H., Muntoni, F., Schara, U., and Straub, V. (2020). A Multistage Sequencing Strategy Pinpoints Novel Candidate Alleles for Emery-Dreifuss Muscular Dystrophy and Supports Gene Misregulation as Its Pathomechanism. EBioMedicine, 51.","DOI":"10.1016\/j.ebiom.2019.11.048"},{"key":"ref_20","doi-asserted-by":"crossref","first-page":"e321","DOI":"10.1212\/NXG.0000000000000321","article-title":"Muscular Dystrophy with Arrhythmia Caused by Loss-of-Function Mutations in BVES","volume":"5","author":"Nelson","year":"2019","journal-title":"Neurol. Genet."},{"key":"ref_21","doi-asserted-by":"crossref","first-page":"818122","DOI":"10.3389\/fphys.2022.818122","article-title":"Drivers of Sinoatrial Node Automaticity in Zebrafish: Comparison With Mechanisms of Mammalian Pacemaker Function","volume":"13","author":"Stoyek","year":"2022","journal-title":"Front. Physiol."},{"key":"ref_22","doi-asserted-by":"crossref","first-page":"H676","DOI":"10.1152\/ajpheart.00330.2016","article-title":"Zebrafish Heart as a Model to Study the Integrative Autonomic Control of Pacemaker Function","volume":"311","author":"Stoyek","year":"2016","journal-title":"Am. J. Physiol. Heart Circ. Physiol."},{"key":"ref_23","doi-asserted-by":"crossref","first-page":"198","DOI":"10.1016\/j.pbiomolbio.2017.07.012","article-title":"Intrinsic Regulation of Sinoatrial Node Function and the Zebrafish as a Model of Stretch Effects on Pacemaking","volume":"130","author":"MacDonald","year":"2017","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_24","doi-asserted-by":"crossref","first-page":"38","DOI":"10.1016\/j.pbiomolbio.2018.06.008","article-title":"Ionic Basis of Cardiac Electrophysiology in Zebrafish Compared to Human Hearts","volume":"138","author":"Ravens","year":"2018","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_25","doi-asserted-by":"crossref","first-page":"45","DOI":"10.1016\/j.pbiomolbio.2018.05.002","article-title":"Cardiac Ca2+ Signalling in Zebrafish: Translation of Findings to Man","volume":"138","author":"Vos","year":"2018","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_26","doi-asserted-by":"crossref","first-page":"607860","DOI":"10.3389\/fphys.2020.607860","article-title":"Adult and Developing Zebrafish as Suitable Models for Cardiac Electrophysiology and Pathology in Research and Industry","volume":"11","author":"Echeazarra","year":"2021","journal-title":"Front. Physiol."},{"key":"ref_27","doi-asserted-by":"crossref","first-page":"889","DOI":"10.1152\/physrev.00038.2016","article-title":"Little Fish, Big Data: Zebrafish as a Model for Cardiovascular and Metabolic Disease","volume":"97","author":"Gut","year":"2017","journal-title":"Physiol. Rev."},{"key":"ref_28","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1016\/j.pbiomolbio.2018.11.003","article-title":"One Fish, Two Fish, Red Fish, Blue Fish*: Zebrafish as a Model for Cardiac Research","volume":"138","author":"Stoyek","year":"2018","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_29","doi-asserted-by":"crossref","first-page":"3","DOI":"10.1016\/j.pbiomolbio.2018.07.005","article-title":"A Beginner\u2019s Guide to Understanding and Implementing the Genetic Modification of Zebrafish","volume":"138","author":"Rafferty","year":"2018","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_30","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1038\/nature12111","article-title":"The Zebrafish Reference Genome Sequence and Its Relationship to the Human Genome","volume":"496","author":"Howe","year":"2013","journal-title":"Nature"},{"key":"ref_31","doi-asserted-by":"crossref","first-page":"126","DOI":"10.1016\/j.pbiomolbio.2018.07.002","article-title":"Zebrafish Assay Development for Cardiovascular Disease Mechanism and Drug Discovery","volume":"138","author":"Kithcart","year":"2018","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_32","doi-asserted-by":"crossref","first-page":"748570","DOI":"10.3389\/fphys.2021.748570","article-title":"Seeing the Light: The Use of Zebrafish for Optogenetic Studies of the Heart","volume":"12","author":"Baillie","year":"2021","journal-title":"Front. Physiol."},{"key":"ref_33","doi-asserted-by":"crossref","first-page":"4750","DOI":"10.7150\/thno.26108","article-title":"Optogenetic Sensors in the Zebrafish Heart: A Novel In Vivo Electrophysiological Tool to Study Cardiac Arrhythmogenesis","volume":"8","author":"Koopman","year":"2018","journal-title":"Theranostics"},{"key":"ref_34","doi-asserted-by":"crossref","first-page":"91","DOI":"10.1016\/j.pbiomolbio.2018.07.014","article-title":"Age-Associated Changes in Electrical Function of the Zebrafish Heart","volume":"138","author":"Stoyek","year":"2018","journal-title":"Prog. Biophys. Mol. Biol."},{"key":"ref_35","unstructured":"Westerfield, M. (1995). The Zebrafish Book, University of Oregon Press."},{"key":"ref_36","doi-asserted-by":"crossref","first-page":"683","DOI":"10.1038\/nmeth.1235","article-title":"Improving Membrane Voltage Measurements Using FRET with New Fluorescent Proteins","volume":"5","author":"Tsutsui","year":"2008","journal-title":"Nat. Methods"},{"key":"ref_37","doi-asserted-by":"crossref","first-page":"875","DOI":"10.1038\/nmeth.1398","article-title":"Imaging Neural Activity in Worms, Flies and Mice with Improved GCaMP Calcium Indicators","volume":"6","author":"Tian","year":"2009","journal-title":"Nat. Methods"},{"key":"ref_38","doi-asserted-by":"crossref","first-page":"114","DOI":"10.1038\/nature11537","article-title":"In Vivo Genome Editing Using a High-Efficiency TALEN System","volume":"491","author":"Bedell","year":"2012","journal-title":"Nature"},{"key":"ref_39","doi-asserted-by":"crossref","first-page":"2104","DOI":"10.1039\/C7OB00006E","article-title":"Discovery of (S)-3\u2032-Hydroxyblebbistatin and (S)-3\u2032-Aminoblebbistatin: Polar Myosin II Inhibitors with Superior Research Tool Properties","volume":"15","author":"Verhasselt","year":"2017","journal-title":"Org. Biomol. Chem."},{"key":"ref_40","doi-asserted-by":"crossref","first-page":"1086050","DOI":"10.3389\/fphys.2023.1086050","article-title":"The In Vivo Study of Cardiac Mechano-Electric and Mechano-Mechanical Coupling during Heart Development in Zebrafish","volume":"14","author":"Baillie","year":"2023","journal-title":"Front. Physiol."},{"key":"ref_41","doi-asserted-by":"crossref","first-page":"6669","DOI":"10.1007\/s00018-021-03939-y","article-title":"Genomic and Physiological Analyses of the Zebrafish Atrioventricular Canal Reveal Molecular Building Blocks of the Secondary Pacemaker Region","volume":"78","author":"Quinn","year":"2021","journal-title":"Cell. Mol. Life Sci."},{"key":"ref_42","doi-asserted-by":"crossref","first-page":"R823","DOI":"10.1152\/ajpregu.00002.2014","article-title":"Optical Mapping of the Electrical Activity of Isolated Adult Zebrafish Hearts: Acute Effects of Temperature","volume":"306","author":"Lin","year":"2014","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_43","doi-asserted-by":"crossref","first-page":"1","DOI":"10.1002\/ar.1111","article-title":"Cardiac Morphology and Blood Pressure in the Adult Zebrafish","volume":"264","author":"Hu","year":"2001","journal-title":"Anat. Rec."},{"key":"ref_44","doi-asserted-by":"crossref","first-page":"516","DOI":"10.1016\/S0006-3495(01)76034-1","article-title":"Visualizing Excitation Waves inside Cardiac Muscle Using Transillumination","volume":"80","author":"Baxter","year":"2001","journal-title":"Biophys. J."},{"key":"ref_45","doi-asserted-by":"crossref","first-page":"3714","DOI":"10.1529\/biophysj.107.110981","article-title":"The Role of Photon Scattering in Optical Signal Distortion during Arrhythmia and Defibrillation","volume":"93","author":"Bishop","year":"2007","journal-title":"Biophys. J."},{"key":"ref_46","doi-asserted-by":"crossref","first-page":"623","DOI":"10.1002\/jez.2507","article-title":"Hif-1\u03b1 Is Not Required for the Development of Cardiac Adrenergic Control in Zebrafish (Danio rerio)","volume":"335","author":"Joyce","year":"2021","journal-title":"J. Exp. Zool. Part A"},{"key":"ref_47","doi-asserted-by":"crossref","first-page":"1683","DOI":"10.1002\/cne.23764","article-title":"Intrinsic and Extrinsic Innervation of the Heart in Zebrafish (Danio rerio): Zebrafish Cardiac Innervation","volume":"523","author":"Stoyek","year":"2015","journal-title":"J. Comp. Neurol."},{"key":"ref_48","doi-asserted-by":"crossref","first-page":"17075","DOI":"10.1038\/s41598-017-17136-0","article-title":"GWAS of the Electrocardiographic QT Interval in Hispanics\/Latinos Generalizes Previously Identified Loci and Identifies Population-Specific Signals","volume":"7","author":"Gogarten","year":"2017","journal-title":"Sci. Rep."},{"key":"ref_49","doi-asserted-by":"crossref","unstructured":"Alcalay, Y., Hochhauser, E., Kliminski, V., Dick, J., Zahalka, M.A., Parnes, D., Schlesinger, H., Abassi, Z., Shainberg, A., and Schindler, R.F.R. (2013). Popeye Domain Containing 1 (Popdc1\/Bves) Is a Caveolae-Associated Protein Involved in Ischemia Tolerance. PLoS ONE, 8.","DOI":"10.1371\/journal.pone.0071100"},{"key":"ref_50","doi-asserted-by":"crossref","unstructured":"Martin, K.E., and Waxman, J.S. (2021). Atrial and Sinoatrial Node Development in the Zebrafish Heart. J. Cardiovasc. Dev. Dis., 8.","DOI":"10.3390\/jcdd8020015"},{"key":"ref_51","doi-asserted-by":"crossref","first-page":"344","DOI":"10.3389\/fphys.2014.00344","article-title":"Simultaneous Mapping of Membrane Voltage and Calcium in Zebrafish Heart In Vivo Reveals Chamber-Specific Developmental Transitions in Ionic Currents","volume":"5","author":"Hou","year":"2014","journal-title":"Front. Physiol."},{"key":"ref_52","doi-asserted-by":"crossref","first-page":"1445","DOI":"10.1242\/jeb.052803","article-title":"In Vivo and in Vitro Assessment of Cardiac \u03b2-Adrenergic Receptors in Larval Zebrafish (Danio rerio)","volume":"214","author":"Steele","year":"2011","journal-title":"J. Exp. Biol."},{"key":"ref_53","doi-asserted-by":"crossref","first-page":"R412","DOI":"10.1152\/ajpregu.00036.2009","article-title":"Loss of M2 Muscarinic Receptor Function Inhibits Development of Hypoxic Bradycardia and Alters Cardiac \u03b2-Adrenergic Sensitivity in Larval Zebrafish (Danio rerio)","volume":"297","author":"Steele","year":"2009","journal-title":"Am. J. Physiol. Regul. Integr. Comp. Physiol."},{"key":"ref_54","doi-asserted-by":"crossref","first-page":"1093","DOI":"10.1242\/jeb.02117","article-title":"Development of the Sympatho-Vagal Balance in the Cardiovascular System in Zebrafish (Danio rerio) Characterized by Power Spectrum and Classical Signal Analysis","volume":"209","author":"Schwerte","year":"2006","journal-title":"J. Exp. Biol."},{"key":"ref_55","doi-asserted-by":"crossref","unstructured":"Stoyek, M.R., Hortells, L., and Quinn, T.A. (2021). From Mice to Mainframes: Experimental Models for Investigation of the Intracardiac Nervous System. J. Cardiovasc. Dev. Dis., 8.","DOI":"10.3390\/jcdd8110149"},{"key":"ref_56","doi-asserted-by":"crossref","first-page":"143","DOI":"10.1016\/j.bbrc.2008.06.109","article-title":"Characterization of Isolated Ventricular Myocytes from Adult Zebrafish (Danio rerio)","volume":"374","author":"Brette","year":"2008","journal-title":"Biochem. Biophys. Res. Commun."},{"key":"ref_57","doi-asserted-by":"crossref","first-page":"89","DOI":"10.1016\/j.gep.2016.08.003","article-title":"Development of the Cardiac Conduction System in Zebrafish","volume":"21","author":"Poon","year":"2016","journal-title":"Gene Expr. Patterns"},{"key":"ref_58","first-page":"1255","article-title":"A Sexy Approach to Pacemaking: Differences in Function and Molecular Make up of the Sinoatrial Node","volume":"34","author":"Doris","year":"2019","journal-title":"Histol. Histopathol."},{"key":"ref_59","doi-asserted-by":"crossref","first-page":"3457","DOI":"10.1093\/cercor\/bhab426","article-title":"Mice Lacking the cAMP Effector Protein POPDC1 Show Enhanced Hippocampal Synaptic Plasticity","volume":"32","author":"Shetty","year":"2022","journal-title":"Cereb. Cortex"}],"container-title":["Genes"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.mdpi.com\/2073-4425\/15\/3\/280\/pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2025,10,10]],"date-time":"2025-10-10T14:03:44Z","timestamp":1760105024000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.mdpi.com\/2073-4425\/15\/3\/280"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2024,2,23]]},"references-count":59,"journal-issue":{"issue":"3","published-online":{"date-parts":[[2024,3]]}},"alternative-id":["genes15030280"],"URL":"https:\/\/doi.org\/10.3390\/genes15030280","relation":{},"ISSN":["2073-4425"],"issn-type":[{"value":"2073-4425","type":"electronic"}],"subject":[],"published":{"date-parts":[[2024,2,23]]}}}