ReviewCirculation research2018
MUSCLEMOTION: A Versatile Open Software Tool to Quantify Cardiomyocyte and Cardiac Muscle Contraction In Vitro and In Vivo.
Open access · greenAbstract readReview
In one paragraph
Review in Circulation research, 2018. The graph could read no effect estimate from its abstract, so it casts no vote on the map. Cited by 251 papers.
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251citing papers in PubMed
10.5field-weighted citation impact, top 1% of its field
What it found
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Who cites it
251 citing papers in PubMed, 386 citations in OpenAlex.
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- A Generative AI Framework to Predict Cardiomyocyte Contraction Function from Single Static Images.Advanced intelligent discovery · 2026Article
- Ambient Temperature Preservation Supports Recovery of Beating Capacity in Human Cardiac Organoids After Exposure to Simulated Space Stressors.International journal of molecular sciences · 2026Article
- Mitophagy Facilitates Cytosolic Proteostasis to Preserve Cardiac Function.Circulation research · 2026Article
- New approach methodologies: drug screening platform to identify antifibrotic compounds.Nature protocols · 2026Review
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- Digital Light Processing 3D Printing Enables Versatile Fabrication of Human Engineered Heart Tissues.Cell biomaterials · 2026Article
- An Integrated Cardiac Microtissue Proteome Map Extends Therapeutic Remodeling by Nanovesicles.Molecular & cellular proteomics : MCP · 2026Article
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- Nucleoside-Modified mRNA Encoding Alpha-Galactosidase A Ameliorates Fabry Disease Phenotypes in Human IPSC-Derived Cardiomyocytes.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026Article
- High and intermittent hydrostatic pressure promotes maturation of engineered cardiac tissues derived from human pluripotent stem cells.Stem cell reports · 2026Article
- Metabolic fatty acid substrates enhance the structural and mechanical performance of human-induced pluripotent stem cell-derived cardiomyocytes.Cellular and molecular life sciences : CMLS · 2026Article
- Real-time GPU-accelerated coupled cardiac system: Integrating bidirectional interactions between living optogenetic monolayers and computational simulations.PLoS computational biology · 2026Article
- Brown Adipocyte Sheets Alleviate Myocardial Ischemia-Reperfusion Injury Through NRG4-ErbB4-Dependent Ferroptosis Inhibition.Advanced science (Weinheim, Baden-Wurttemberg, Germany) · 2026Article
191 more citing papers are in PubMed but not listed here.
Corrections and comments
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Authors and funding
27 authors at 1 institution in 1 country.
Luca SalaFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Berend J van MeerFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Leon G J TertoolenFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Jeroen BakkersFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Milena BellinFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Richard P DavisFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Chris DenningFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Michel A E DiebenFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Thomas EschenhagenFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Elisa GiacomelliFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Catarina GrandelaFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Arne HansenFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Eduard R HolmanFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Monique R M JongbloedFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Sarah M KamelFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Charlotte D KoopmanFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Quentin LachaudFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Ingra MannhardtFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Mervyn P H MolFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Diogo MosqueiraFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Valeria V OrlovaFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Robert PassierFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Marcelo C RibeiroFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Umber SaleemFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Godfrey L SmithFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Francis L BurtonFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.).
Christine L MummeryFrom the Department of Anatomy and Embryology, Leiden University Medical Center, The Netherlands (L.S., B.J.v.M., L.G.J.T., M.B., R.P.D., M.A.E.D., E.G., C.G., M.R.M.J., M.P.H.M., V.V.O., R.P., C.L.M.); Institute of Cardiovascular and Medical Sciences, College of Medical, Veterinary, and Life Science, University of Glasgow, United Kingdom (Q.L., G.L.S., F.L.B.); Hubrecht Institute - Royal Netherlands Academy of Arts and Sciences, Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); Department of Stem Cell Biology, University of Nottingham, University Park, Nottingham, United Kingdom (C.D., D.M.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Germany (T.E., A.H., I.M., U.S.); DZHK (German Centre for Cardiovascular Research), Partner Site Hamburg/Kiel/Lübeck (T.E., A.H., I.M., U.S.); Department of Experimental Pharmacology and Toxicology, University Medical Center Hamburg Eppendorf, Hamburg, Germany (U.S.); Hart Long Centrum, Leiden University Medical Center, The Netherlands (E.R.H., M.R.M.J.); Department of Applied Stem Cell Technologies, University of Twente, Enschede, The Netherlands (R.P., M.C.R., C.L.M.).; Division of Heart and Lungs, Department of Medical Physiology, University Medical Center Utrecht, The Netherlands (J.B., S.M.K., C.D.K.); and Clyde Biosciences, Ltd, BioCity Scotland, United Kingdom (G.L.S., F.L.B.). c.l.mummery@lumc.nl.
Amsterdam UMC Location Vrije Universiteit Amsterdam · NL
Funding
British Heart Foundation PG/09/027/27141British Heart Foundation PG/14/59/31000British Heart Foundation SP/15/9/31605National Centre for the Replacement, Refinement and Reduction of Animals in Research NC/C013202/1
Abstract
rationaleThere are several methods to measure cardiomyocyte and muscle contraction, but these require customized hardware, expensive apparatus, and advanced informatics or can only be used in single experimental models. Consequently, data and techniques have been difficult to reproduce across models and laboratories, analysis is time consuming, and only specialist researchers can quantify data.
objectiveHere, we describe and validate an automated, open-source software tool (MUSCLEMOTION) adaptable for use with standard laboratory and clinical imaging equipment that enables quantitative analysis of normal cardiac contraction, disease phenotypes, and pharmacological responses. METHODS AND
resultsMUSCLEMOTION allowed rapid and easy measurement of movement from high-speed movies in (1) 1-dimensional in vitro models, such as isolated adult and human pluripotent stem cell-derived cardiomyocytes; (2) 2-dimensional in vitro models, such as beating cardiomyocyte monolayers or small clusters of human pluripotent stem cell-derived cardiomyocytes; (3) 3-dimensional multicellular in vitro or in vivo contractile tissues, such as cardiac "organoids," engineered heart tissues, and zebrafish and human hearts. MUSCLEMOTION was effective under different recording conditions (bright-field microscopy with simultaneous patch-clamp recording, phase contrast microscopy, and traction force microscopy). Outcomes were virtually identical to the current gold standards for contraction measurement, such as optical flow, post deflection, edge-detection systems, or manual analyses. Finally, we used the algorithm to quantify contraction in in vitro and in vivo arrhythmia models and to measure pharmacological responses.
conclusionsUsing a single open-source method for processing video recordings, we obtained reliable pharmacological data and measures of cardiac disease phenotype in experimental cell, animal, and human models.
Indexed as
Myocardial ContractionSoftwareAlgorithmsAnimalsCardiomyopathy, HypertrophicCardiovascular AgentsCell DifferentiationCells, CulturedGTP-Binding Protein beta SubunitsHumansLong QT SyndromeMaleMicroscopyModels, CardiovascularMyocytes, CardiacPatch-Clamp TechniquesCardiovascular Agentsgnb5b protein, zebrafishGTP-Binding Protein beta SubunitsZebrafish Proteinsarrhythmias, cardiachumanspluripotent stem cellssoftwarezebrafish
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