Zebrafish models of sarcopenia
Open accessAbstract
Sarcopenia - the accelerated age-related loss of muscle mass and function - is an under-diagnosed condition, and is central to deteriorating mobility, disability and frailty in older age. There is a lack of treatment options for older adults at risk of sarcopenia. Although sarcopenia's pathogenesis is multifactorial, its major phenotypes - muscle mass and muscle strength - are highly heritable. Several genome-wide association studies of muscle-related traits were published recently, providing dozens of candidate genes, many with unknown function. Therefore, animal models are required not only to identify causal mechanisms, but also to clarify the underlying biology and translate this knowledge into new interventions. Over the past several decades, small teleost fishes had emerged as powerful systems for modeling the genetics of human diseases. Owing to their amenability to rapid genetic intervention and the large number of conserved genetic and physiological features, small teleosts - such as zebrafish, medaka and killifish - have become indispensable for skeletal muscle genomic studies. The goal of this Review is to summarize evidence supporting the utility of small fish models for accelerating our understanding of human skeletal muscle in health and disease. We do this by providing a basic foundation of the (zebra)fish skeletal muscle morphology and physiology, and evidence of muscle-related gene homology. We also outline challenges in interpreting zebrafish mutant phenotypes and in translating them to human disease. Finally, we conclude with recommendations on future directions to leverage the large body of tools developed in small fish for the needs of genomic exploration in sarcopenia.
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Many researchers have developed reliable zebrafish models to understand muscle degeneration and its pathophysiology.
“Many researchers have developed reliable zebrafish models to understand muscle degeneration and its pathophysiology [13,14].”
From A High-Fat Diet Induces Muscle Mitochondrial Dysfunction and Impairs Swimming Capacity in Zebrafish: A New Model of Sarcopenic Obesity (2022) · cites this paper as [13]
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Sarcopenia: revised European consensus on definition and diagnosis
Cruz-Jentoft, A. J., Bahat, G., Bauer, J., Boirie, Y., Bruyère, O., Cederholm, T., Cooper, C., Landi, F., Rolland, Y., Sayer, A. A., et al. (2019) · Age and Ageing · doi:10.1093/ageing/afy169 · Cited by 13,818 · see citing works
Stages of embryonic development of the zebrafish
Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B., & Schilling, T. F. (1995) · Developmental Dynamics · doi:10.1002/aja.1002030302 · Cited by 12,037 · see citing works
Long non-coding RNAs: insights into functions
Mercer, T. R., Dinger, M. E., & Mattick, J. S. (2009) · Nature Reviews Genetics · doi:10.1038/nrg2521 · Cited by 5,654 · see citing works
The zebrafish reference genome sequence and its relationship to the human genome.
Howe, K., Clark, M. D., Torroja, C. F., Torrance, J., Berthelot, C., Muffato, M., Collins, J. E., Humphray, S., McLaren, K., Matthews, L., et al. (2013) · Nature · doi:10.1038/nature12111 · Cited by 5,100 · see citing works
Buniello, A., MacArthur, J. A. L., Cerezo, M., Harris, L. W., Hayhurst, J., Malangone, C., McMahon, A., Morales, J., Mountjoy, E., Sollis, E., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gky1120 · Cited by 4,000 · see citing works
Systematic Localization of Common Disease-Associated Variation in Regulatory DNA
Maurano, M. T., Humbert, R., Rynes, E., Thurman, R. E., Haugen, E., Wang, H., Reynolds, A. P., Sandstrom, R., Qu, H., Brody, J., et al. (2012) · Science · doi:10.1126/science.1222794 · Cited by 3,716 · see citing works
Fielding, R. A., Vellas, B., Evans, W. J., Bhasin, S., Morley, J. E., Newman, A. B., Abellan van Kan, G., Andrieu, S., Bauer, J., Breuille, D., et al. (2011) · Journal of the American Medical Directors Association · doi:10.1016/j.jamda.2011.01.003 · Cited by 3,256 · cited 1× · see citing works
“Furthermore, the diagnostic algorithms used to define the sarcopenic individual attempted to consider the measured components of physical function and muscle strength differently (Cruz-Jentoft et al., 2014; Fielding et al., 2011).”
Satellite Cells and the Muscle Stem Cell Niche
Yin, H., Price, F., & Rudnicki, M. A. (2013) · Physiological Reviews · doi:10.1152/physrev.00043.2011 · Cited by 2,166 · see citing works
Cruz-Jentoft, A. J., Landi, F., Schneider, S. M., Zuniga, C., Arai, H., Boirie, Y., Chen, L.-K., Fielding, R. A., Martin, F. C., Michel, J.-P., et al. (2014) · Age and Ageing · doi:10.1093/ageing/afu115 · Cited by 1,963 · see citing works
Use of NeuroEyeCoach™ to Improve Eye Movement Efficacy in Patients with Homonymous Visual Field Loss
Sahraie, A., Smania, N., & Zihl, J. (2016) · BioMed Research International · doi:10.1155/2016/5186461 · Cited by 1,775 · see citing works
The support of human genetic evidence for approved drug indications
Nelson, M. R., Tipney, H., Painter, J. L., Shen, J., Nicoletti, P., Shen, Y., Floratos, A., Sham, P. C., Li, M. J., Wang, J., et al. (2015) · Nature Genetics · doi:10.1038/ng.3314 · Cited by 1,666 · see citing works
The Landscape of long noncoding RNA classification
Laurent, G. S., Wahlestedt, C., & Kapranov, P. (2015) · Trends in Genetics · doi:10.1016/j.tig.2015.03.007 · Cited by 1,192 · see citing works
In vivo enhancer analysis of human conserved non-coding sequences
Pennacchio, L. A., Ahituv, N., Moses, A. M., Prabhakar, S., Nobrega, M. A., Shoukry, M., Minovitsky, S., Dubchak, I., Holt, A., Lewis, K. D., et al. (2006) · Nature · doi:10.1038/nature05295 · Cited by 1,165 · see citing works
Conserved Function of lincRNAs in Vertebrate Embryonic Development despite Rapid Sequence Evolution
Ulitsky, I., Shkumatava, A., Jan, C. H., Sive, H. L., & Bartel, D. P. (2011) · Cell · doi:10.1016/j.cell.2011.11.055 · Cited by 1,162 · see citing works
Dent, E., Morley, J. E., Cruz-Jentoft, A. J., Arai, H., Kritchevsky, S. B., Guralnik, J., Bauer, J. M., Pahor, M., Clark, B. C., Cesari, M., et al. (2018) · The Journal of nutrition, health and aging · doi:10.1007/s12603-018-1139-9 · Cited by 1,130 · see citing works
The evolution of lncRNA repertoires and expression patterns in tetrapods
Necsulea, A., Soumillon, M., Warnefors, M., Liechti, A., Daish, T., Zeller, U., Baker, J. C., Grützner, F., & Kaessmann, H. (2014) · Nature · doi:10.1038/nature12943 · Cited by 984 · see citing works
How Muscle Structure and Composition Influence Meat and Flesh Quality
Listrat, A., Lebret, B., Louveau, I., Astruc, T., Bonnet, M., Lefaucheur, L., Picard, B. B., & Bugeon, J. (2016) · The Scientific World JOURNAL · doi:10.1155/2016/3182746 · Cited by 878 · see citing works
Zebrafish Comparative Genomics and the Origins of Vertebrate Chromosomes
Postlethwait, J. H., Woods, I. G., Ngo-Hazelett, P., Yan, Y.-L., Kelly, P. D., Chu, F., Huang, H., Hill-Force, A., & Talbot, W. S. (2000) · Genome Research · doi:10.1101/gr.164800 · Cited by 688 · see citing works
The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons
Braasch, I., Gehrke, A. R., Smith, J. J., Kawasaki, K., Manousaki, T., Pasquier, J., Amores, A., Desvignes, T., Batzel, P., Catchen, J., et al. (2016) · Nature Genetics · doi:10.1038/ng.3526 · Cited by 604 · see citing works
Dynamics of muscle fibre growth during postnatal mouse development
White, R. B., Biérinx, A.-S., Gnocchi, V. F., & Zammit, P. S. (2010) · BMC Developmental Biology · doi:10.1186/1471-213x-10-21 · Cited by 512 · see citing works
Hooked! Modeling human disease in zebrafish
Santoriello, C., & Zon, L. I. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60434 · Cited by 511 · see citing works
Dhawan, J., & Rando, T. A. (2005) · Trends in Cell Biology · doi:10.1016/j.tcb.2005.10.007 · Cited by 466 · see citing works
Talbot, J. C., & Maves, L. (2016) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.230 · Cited by 439 · see citing works
Mommsen, T. P. (2001) · Comparative Biochemistry and Physiology Part B Biochemistry and Molecular Biology · doi:10.1016/s1096-4959(01)00312-8 · Cited by 408 · see citing works
Subfunction partitioning, the teleost radiation and the annotation of the human genome
Postlethwait, J. H., Amores, A., Cresko, W. A., Singer, A., & Yan, Y. (2004) · Trends in Genetics · doi:10.1016/j.tig.2004.08.001 · Cited by 395 · see citing works
Frailty syndrome and skeletal muscle: results from the Invecchiare in Chianti study
Cesari, M., Leeuwenburgh, C., Lauretani, F., Onder, G., Bandinelli, S., Maraldi, C., Guralnik, J. M., Pahor, M., & Ferrucci, L. (2006) · The American Journal of Clinical Nutrition · doi:10.1093/ajcn/83.5.1142 · Cited by 365 · see citing works
Amores, A., Catchen, J., Ferrara, A. M., Fontenot, Q. C., & Postlethwait, J. H. (2011) · Genetics · doi:10.1534/genetics.111.127324 · Cited by 364 · see citing works
Smith, J. J., Timoshevskaya, N., Ye, C., Holt, C., Keinath, M. C., Parker, H. J., Cook, M. E., Hess, J. E., Narum, S. R., Lamanna, F., et al. (2018) · Nature Genetics · doi:10.1038/s41588-017-0036-1 · Cited by 305 · see citing works
Cellular heterogeneity during vertebrate skeletal muscle development
Biressi, S., Molinaro, M., & Cossu, G. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.06.006 · Cited by 294 · see citing works
The genetics of vertebrate myogenesis
Bryson‐Richardson, R. J., & Currie, P. D. (2008) · Nature Reviews Genetics · doi:10.1038/nrg2369 · Cited by 285 · see citing works
Dystrophin is required for the formation of stable muscle attachments in the zebrafish embryo
Bassett, D. I., Bryson‐Richardson, R. J., Daggett, D. F., Gautier, P. E., Keenan, D. G., & Currie, P. D. (2003) · Development · doi:10.1242/dev.00799 · Cited by 270 · see citing works
Horstick, E. J., Linsley, J. W., Dowling, J. J., Hauser, M. A., Gibson, K. M., Ashley‐Koch, A. E., Saint‐Amant, L., Satish, A., Cui, W. W., Zhou, W., et al. (2013) · Nature Communications · doi:10.1038/ncomms2952 · Cited by 260 · see citing works
Brocklehurst's Textbook of Geriatric Medicine and Gerontology
Fillit, H., & Rockwood, K. (2010) · Elsevier eBooks · doi:10.1016/b978-1-4160-6231-8.x0001-3 · Cited by 258 · see citing works
Quantitative analysis of skeletal muscle by computed tomography imaging—State of the art
Engelke, K., Museyko, O., Wang, L., & Larédo, J.-D. (2018) · Journal of Orthopaedic Translation · doi:10.1016/j.jot.2018.10.004 · Cited by 255 · see citing works
Rands, C. M., Meader, S., Ponting, C. P., & Lunter, G. A. (2014) · PLoS Genetics · doi:10.1371/journal.pgen.1004525 · Cited by 247 · see citing works
Kyle, U. G., Genton, L., Hans, D., & Pichard, C. (2003) · Clinical Nutrition · doi:10.1016/s0261-5614(03)00048-7 · Cited by 246 · cited 2× · see citing works
“, 2018), and bioelectrical impedance (Kyle et al., 2003).”
Annual fishes of the genus Nothobranchius as a model system for aging research
Genade, T., Benedetti, M., Tozzini, E. T., Roncaglia, P., Valenzano, D. R., Cattaneo, A., & Cellerino, A. (2005) · Aging Cell · doi:10.1111/j.1474-9726.2005.00165.x · Cited by 238 · see citing works
Willems, S. M., Wright, D. J., Day, F. R., Trajanoska, K., Joshi, P. K., Morris, J. A., Matteini, A. M., Garton, F. C., Grarup, N., Oskolkov, N., et al. (2017) · Nature Communications · doi:10.1038/ncomms16015 · Cited by 220 · see citing works
Beyond the zebrafish: diverse fish species for modeling human disease
Schartl, M. (2013) · Disease Models & Mechanisms · doi:10.1242/dmm.012245 · Cited by 214 · see citing works
The zebrafish as a vertebrate model of functional aging and very gradual senescence
Kishi, S., Uchiyama, J., Baughman, A. M., Goto, T., Lin, M. C., & Tsai, S. B. (2003) · Experimental Gerontology · doi:10.1016/s0531-5565(03)00108-6 · Cited by 208 · see citing works
The functions of long noncoding RNAs in development and stem cells
Perry, R. B., & Ulitsky, I. (2016) · Development · doi:10.1242/dev.140962 · Cited by 208 · see citing works
Chromosome evolution at the origin of the ancestral vertebrate genome
Sacerdot, C., Louis, A., Bon, C., Berthelot, C., & Roest Crollius, H. (2018) · Genome Biology · doi:10.1186/s13059-018-1559-1 · Cited by 206 · see citing works
Drug screening in a zebrafish model of Duchenne muscular dystrophy
Kawahara, G., Karpf, J. A., Myers, J. A., Alexander, M. S., Guyon, J. R., & Kunkel, L. M. (2011) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1102116108 · Cited by 191 · see citing works
Large meta-analysis of genome-wide association studies identifies five loci for lean body mass
Zillikens, M. C., Demissie, S., Hsu, Y., Yerges-Armstrong, L. M., Chou, W., Stolk, L., Livshits, G., Broer, L., Johnson, T., Koller, D. L., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-00031-7 · Cited by 186 · see citing works
Gilbert, M. J. H., Zerulla, T. C., & Tierney, K. B. (2013) · Experimental Gerontology · doi:10.1016/j.exger.2013.11.013 · Cited by 184 · see citing works
The Divergent Genomes of Teleosts
Ravi, V., & Venkatesh, B. (2018) · Annual Review of Animal Biosciences · doi:10.1146/annurev-animal-030117-014821 · Cited by 183 · see citing works
Hollway, G. E., Bryson‐Richardson, R. J., Berger, S., et al. (2007) · Developmental Cell · doi:10.1016/j.devcel.2007.01.001 · Cited by 180 · see citing works
D3‐Creatine dilution and the importance of accuracy in the assessment of skeletal muscle mass
Evans, W. J., Hellerstein, M. K., ORWOLL, E. S., Cummings, S., & Cawthon, P. M. (2019) · Journal of Cachexia Sarcopenia and Muscle · doi:10.1002/jcsm.12390 · Cited by 179 · see citing works
Hall, T. E., Bryson-Richardson, R. J., Berger, S., Jacoby, A. S., Cole, N. J., Hollway, G. E., Berger, J., & Currie, P. D. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0700942104 · Cited by 178 · see citing works
The African turquoise killifish: A research organism to study vertebrate aging and diapause
Hu, C., & Brunet, A. (2018) · Aging Cell · doi:10.1111/acel.12757 · Cited by 165 · see citing works
Mintzer, K. A., Lee, M. A., Runke, G., et al. (2001) · Development · doi:10.1242/dev.128.6.859 · Cited by 160 · see citing works
First mutation in cardiac troponin C, L29Q, in a patient with hypertrophic cardiomyopathy
Hoffmann, B., Schmidt-Traub, H., Perrot, A., et al. (2001) · Human Mutation · doi:10.1002/humu.1143 · Cited by 153 · see citing works
Bauer, H., Lele, Z., Rauch, G.-J., et al. (2001) · Development · doi:10.1242/dev.128.6.849 · Cited by 153 · see citing works
Irimia, M., Tena, J. J., Alexis, M. S., Fernandez-Miñan, A., Maeso, I., Bogdanović, O., de la Calle-Mustienes, E., Roy, S. W., Gómez-Skarmeta, J. L., & Fraser, H. B. (2012) · Genome Research · doi:10.1101/gr.139725.112 · Cited by 146 · see citing works
Asymmetric division of clonal muscle stem cells coordinates muscle regeneration in vivo
Gurevich, D., Nguyen, P. D., Siegel, A. L., Ehrlich, O., Sonntag, C., Phan, J. M. N., Berger, S., Ratnayake, D., Hersey, L., Berger, J., et al. (2016) · Science · doi:10.1126/science.aad9969 · Cited by 146 · see citing works
The short-lived African turquoise killifish: an emerging experimental model for ageing
Kim, Y., Nam, H. G., & Valenzano, D. R. (2016) · Disease Models & Mechanisms · doi:10.1242/dmm.023226 · Cited by 139 · see citing works
Cawthon, P. M., Travison, T. G., Manini, T. M., Patel, S., Pencina, K. M., Fielding, R. A., Magaziner, J. M., Newman, A. B., Brown, T., Kiel, D. P., et al. (2020) · The Journals of Gerontology Series A · doi:10.1093/gerona/glz081 · Cited by 127 · see citing works
Hirata, H., Watanabe, T., Hatakeyama, J., Sprague, S. M., Saint‐Amant, L., Nagashima, A., Cui, W. W., Zhou, W., & Kuwada, J. Y. (2007) · Development · doi:10.1242/dev.004531 · Cited by 125 · see citing works
The zebrafish dag1 mutant: a novel genetic model for dystroglycanopathies
Gupta, V., Kawahara, G., Gundry, S. R., Chen, A. T., Lencer, W. I., Zhou, Y., Zon, L. I., Kunkel, L. M., & Beggs, A. H. (2011) · Human Molecular Genetics · doi:10.1093/hmg/ddr047 · Cited by 111 · see citing works
Gupta, V., Kawahara, G., Myers, J. A., Chen, A. T., Hall, T. E., Manzini, M. C., Currie, P. D., Zhou, Y., Zon, L. I., Kunkel, L. M., et al. (2012) · PLoS ONE · doi:10.1371/journal.pone.0043794 · Cited by 111 · see citing works
Into the Wild: GWAS Exploration of Non-coding RNAs
Giral, H., Landmesser, U., & Kratzer, A. (2018) · Frontiers in Cardiovascular Medicine · doi:10.3389/fcvm.2018.00181 · Cited by 111 · see citing works
Evidence for pleiotropic factors in genetics of the musculoskeletal system
Karasik, D., & Kiel, D. P. (2010) · Bone · doi:10.1016/j.bone.2010.01.382 · Cited by 109 · see citing works
Self-citationSkeletal Muscle Mitochondrial Function and Fatigability in Older Adults
Santanasto, A. J., Glynn, N. W., Jubrias, S. A., Conley, K. E., Boudreau, R. M., Amati, F., Mackey, D. C., Simonsick, E. M., Strotmeyer, E. S., Coen, P. M., et al. (2014) · The Journals of Gerontology Series A · doi:10.1093/gerona/glu134 · Cited by 108 · see citing works
Biological Insights Into Muscular Strength: Genetic Findings in the UK Biobank
Tikkanen, E., Gustafsson, S., Amar, D., Shcherbina, A., Waggott, D. M., Ashley, E. A., & Ingelsson, E. (2018) · Scientific Reports · doi:10.1038/s41598-018-24735-y · Cited by 106 · see citing works
POPDC1S201F causes muscular dystrophy and arrhythmia by affecting protein trafficking
Schindler, R. F. R., Scotton, C., Zhang, J., Passarelli, C., Ortiz‐Bonnin, B., Simrick, S., Schwerte, T., Poon, K., Fang, M., Rinné, S., et al. (2015) · Journal of Clinical Investigation · doi:10.1172/jci79562 · Cited by 105 · see citing works
Functional Aging and Gradual Senescence in Zebrafish
Kishi, S. (2004) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1297.097 · Cited by 103 · see citing works
Jamb and Jamc Are Essential for Vertebrate Myocyte Fusion
Powell, G. T., & Wright, G. J. (2011) · PLoS Biology · doi:10.1371/journal.pbio.1001216 · Cited by 97 · see citing works
Small teleost fish provide new insights into human skeletal diseases
Witten, P. E., Harris, M. P., Huysseune, A., & Winkler, C. (2016) · Methods in cell biology · doi:10.1016/bs.mcb.2016.09.001 · Cited by 97 · see citing works
IDENTIFICATION OF A ZEBRAFISH MODEL OF MUSCULAR DYSTROPHY
Bassett, D. I., & Currie, P. D. (2004) · Clinical and Experimental Pharmacology and Physiology · doi:10.1111/j.1440-1681.2004.04030.x · Cited by 90 · see citing works
Ancient Vertebrate Conserved Noncoding Elements Have Been Evolving Rapidly in Teleost Fishes
Lee, A., Kerk, S. Y., Tan, Y., Brenner, S., & Venkatesh, B. (2010) · Molecular Biology and Evolution · doi:10.1093/molbev/msq304 · Cited by 85 · see citing works
Satellite-like cells contribute to pax7-dependent skeletal muscle repair in adult zebrafish
Berberoglu, M. A., Gallagher, T. L., Morrow, Z. T., Talbot, J. C., Hromowyk, K. J., Tenente, I. M., Langenau, D. M., & Amacher, S. L. (2017) · Developmental Biology · doi:10.1016/j.ydbio.2017.03.004 · Cited by 85 · see citing works
Hoegg, S., Boore, J. L., Kuehl, J. V., & Meyer, A. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-317 · Cited by 84 · see citing works
Audira, G., Sarasamma, S., Chen, J., Juniardi, S., Sampurna, B. P., Liang, S., Lai, Y., Lin, G.-M., Hsieh, M., & Hsiao, C. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19124038 · Cited by 82 · see citing works
Hirata, H., Saint‐Amant, L., Waterbury, J. A., et al. (2004) · Development · doi:10.1242/dev.01410 · Cited by 81 · see citing works
Akazawa, N., Harada, K., Okawa, N., Tamura, K., & Moriyama, H. (2018) · PLoS ONE · doi:10.1371/journal.pone.0201789 · Cited by 80 · see citing works
Genetic isolation and characterization of a splicing mutant of zebrafish dystrophin
Guyon, J. R., Goswami, J., Jun, S. J., Thorne, M., Howell, M. H., Pusack, T. J., Kawahara, G., Steffen, L. S., Galdzicki, M., & Kunkel, L. M. (2008) · Human Molecular Genetics · doi:10.1093/hmg/ddn337 · Cited by 79 · see citing works
Robb, L. G., Hartley, L., Begley, C. G., Brodnicki, T. C., Copeland, N. G., Gilbert, D. J., Jenkins, N. A., & Elefanty, A. G. (2000) · Developmental Dynamics · doi:10.1002/1097-0177(2000)9999:9999 · Cited by 78 · see citing works
Clemen, C. S., Tangavelou, K., Strucksberg, K.-H., Just, S., Gaertner, L., Regus‐Leidig, H., Stumpf, M., Reimann, J., Coras, R., Morgan, R. O., et al. (2010) · Brain · doi:10.1093/brain/awq222 · Cited by 75 · see citing works
Sarcopenia: Pharmacology of Today and Tomorrow
Brotto, M., & de Abreu, E. L. (2012) · Journal of Pharmacology and Experimental Therapeutics · doi:10.1124/jpet.112.191759 · Cited by 75 · see citing works
The Developmental Phases of Zebrafish Myogenesis
Keenan, S. R., & Currie, P. D. (2019) · Journal of Developmental Biology · doi:10.3390/jdb7020012 · Cited by 73 · see citing works
Small laboratory fish as models for aging research
Gerhard, G. S. (2007) · Ageing Research Reviews · doi:10.1016/j.arr.2007.02.007 · Cited by 72 · see citing works
Hiller, M., Agarwal, S., Notwell, J. H., Parikh, R., Guturu, H., Wenger, A. M., & Bejerano, G. (2013) · Nucleic Acids Research · doi:10.1093/nar/gkt557 · Cited by 72 · see citing works
Markworth, J. F., Maddipati, K. R., & Cameron‐Smith, D. (2018) · PubMed · Cited by 72 · see citing works
Evolution of MicroRNAs and the Diversification of Species
Loh, Y. E., Yi, S. V., & Streelman, J. T. (2010) · Genome Biology and Evolution · doi:10.1093/gbe/evq085 · Cited by 71 · see citing works
Zebrafish orthologs of human muscular dystrophy genes
Steffen, L. S., Guyon, J. R., Vogel, E. D., Beltre, R., Pusack, T. J., Zhou, Y., Zon, L. I., & Kunkel, L. M. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-79 · Cited by 71 · see citing works
Stellabotte, F., & Devoto, S. H. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21253 · Cited by 69 · see citing works
Fluoxetine prevents dystrophic changes in a zebrafish model of Duchenne muscular dystrophy
Waugh, T. A., Horstick, E. J., Hur, J., Jackson, S. W., Davidson, A. E., Li, X., & Dowling, J. J. (2014) · Human Molecular Genetics · doi:10.1093/hmg/ddu185 · Cited by 67 · see citing works
GWAS analysis of handgrip and lower body strength in older adults in the CHARGE consortium
Matteini, A. M., Tanaka, T., Karasik, D., Atzmon, G., Chou, W., Eicher, J. D., Johnson, A. D., Arnold, A. M., Callisaya, M. L., Davies, G., et al. (2016) · Aging Cell · doi:10.1111/acel.12468 · Cited by 64 · see citing works
Self-citationLiang, W., Zhu, W., Mitsuhashi, S., et al. (2015) · Skeletal Muscle · doi:10.1186/s13395-015-0056-4 · Cited by 63 · see citing works
Henke, K., Daane, J. M., Hawkins, M. B., Dooley, C. M., Busch‐Nentwich, E. M., Stemple, D. L., & Harris, M. P. (2017) · Genetics · doi:10.1534/genetics.117.300187 · Cited by 62 · see citing works
MYBPC1 mutations impair skeletal muscle function in zebrafish models of arthrogryposis
Ha, K., Buchan, J. G., Alvarado, D. M., et al. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt344 · Cited by 60 · see citing works
Growth in the larval zebrafish pectoral fin and trunk musculature
Patterson, S. E., Mook, L. B., & Devoto, S. H. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21400 · Cited by 59 · see citing works
Myostatin inhibitors as pharmacological treatment for muscle wasting and muscular dystrophy
Saitoh, M., Ishida, J., Ebner, N., Anker, S. D., Springer, J., & von Haehling, S. (2017) · JCSM Clinical Reports · doi:10.17987/jcsm-cr.v2i1.37 · Cited by 57 · see citing works
The timing of emergence of muscle progenitors is controlled by an FGF/ERK/SNAIL1 pathway
Delfini, M.-C., Celle, M. D. L., Gros, J., Serralbo, O., Marics, I., Seux, M., Scaal, M., & Marcelle, C. (2009) · Developmental Biology · doi:10.1016/j.ydbio.2009.05.544 · Cited by 55 · see citing works
Li, M., Andersson‐Lendahl, M., Sejersen, T., & Arner, A. (2013) · The Journal of General Physiology · doi:10.1085/jgp.201210915 · Cited by 55 · see citing works
Genge, C. E., Davidson, W. S., & Tibbits, G. F. (2013) · Physiological Genomics · doi:10.1152/physiolgenomics.00074.2013 · Cited by 51 · see citing works
neb: a zebrafish model of nemaline myopathy due to nebulin mutation
Telfer, W. R., Nelson, D. D., Waugh, T. A., et al. (2011) · Disease Models & Mechanisms · doi:10.1242/dmm.008631 · Cited by 48 · see citing works
Shi, J., Cai, M., Si, Y., Zhang, J., & Du, S. (2018) · Human Molecular Genetics · doi:10.1093/hmg/ddy268 · Cited by 48 · see citing works
Disentangling the genetics of lean mass
Karasik, D., Zillikens, M. C., Hsu, Y., Aghdassi, A. A., Åkesson, K., Amin, N., Barroso, I., Bennett, D. A. A., Bertram, L., Bochud, M., et al. (2018) · American Journal of Clinical Nutrition · doi:10.1093/ajcn/nqy272 · Cited by 48 · see citing works
Self-citationCongenital myopathy results from misregulation of a muscle Ca 2+ channel by mutant Stac3
Linsley, J. W., Hsu, I.-U. Y., Groom, L. A., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1619238114 · Cited by 47 · see citing works
Bennett, A. H., O’Donohue, M.-F., Gundry, S. R., Chan, A. T., Widrick, J. J., Draper, I., Chakraborty, A., Zhou, Y., Zon, L. I., Gleizes, P., et al. (2018) · PLoS Genetics · doi:10.1371/journal.pgen.1007226 · Cited by 47 · see citing works
Ramspacher, C., Steed, E., Boselli, F., et al. (2015) · Cell Reports · doi:10.1016/j.celrep.2015.05.010 · Cited by 45 · see citing works
Zebrafish based small molecule screens for novel DMD drugs
Kawahara, G., & Kunkel, L. M. (2012) · Drug Discovery Today Technologies · doi:10.1016/j.ddtec.2012.03.001 · Cited by 45 · see citing works
Characterization and investigation of zebrafish models of filamin-related myofibrillar myopathy
Ruparelia, A. A., Zhao, M., Currie, P. D., et al. (2012) · Human Molecular Genetics · doi:10.1093/hmg/dds231 · Cited by 44 · see citing works
Giacomotto, J., Brouilly, N., Walter, L., Mariol, M., Berger, J., Ségalat, L., Becker, T. S., Currie, P. D., & Gieseler, K. (2013) · Human Molecular Genetics · doi:10.1093/hmg/ddt302 · Cited by 43 · see citing works
Berger, J., Berger, S., Jacoby, A. S., Wilton, S. D., & Currie, P. D. (2011) · Journal of Cellular and Molecular Medicine · doi:10.1111/j.1582-4934.2011.01260.x · Cited by 42 · see citing works
Muscle diseases in the zebrafish
Lin, Y. (2012) · Neuromuscular Disorders · doi:10.1016/j.nmd.2012.04.007 · Cited by 41 · see citing works
Morphological and Functional Aspects of Human Skeletal Muscle
Trovato, F., Imbesi, R., Conway, N., & Castrogiovanni, P. (2016) · Journal of Functional Morphology and Kinesiology · doi:10.3390/jfmk1030289 · Cited by 41 · see citing works
Enhancer–gene maps in the human and zebrafish genomes using evolutionary linkage conservation
Clément, Y., Torbey, P., Gilardi‐Hebenstreit, P., & Crollius, H. R. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1199 · Cited by 41 · see citing works
Recent advances using zebrafish animal models for muscle disease drug discovery
Maves, L. (2014) · Expert Opinion on Drug Discovery · doi:10.1517/17460441.2014.927435 · Cited by 40 · see citing works
The titin A-band rod domain is dispensable for initial thick filament assembly in zebrafish
Myhre, J. L., Hills, J. A., Prill, K., et al. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.12.020 · Cited by 38 · see citing works
Gupta, V., Hnia, K., Smith, L. L., et al. (2013) · PLoS Genetics · doi:10.1371/journal.pgen.1003583 · Cited by 38 · see citing works
Presenting the Epigenome Roadmap
Skipper, M., Eccleston, A., Gray, N. W., Heemels, M.-T., Bot, N. L., Marte, B. M., & Weiss, U. K. (2015) · Nature · doi:10.1038/518313a · Cited by 37 · see citing works
Berger, J., Tarakci, H., Berger, S., Li, M., Hall, T. E., Arner, A., & Currie, P. D. (2014) · Disease Models & Mechanisms · doi:10.1242/dmm.017376 · Cited by 37 · see citing works
Bivariate Genome-Wide Linkage Analysis of Femoral Bone Traits and Leg Lean Mass: Framingham Study
Karasik, D., Zhou, Y., Cupples, L. A., Hannan, M. T., Kiel, D. P., & Demissie, S. (2008) · Journal of Bone and Mineral Research · doi:10.1359/jbmr.081222 · Cited by 36 · see citing works
Self-citationA Zebrafish Model for a Human Myopathy Associated with Mutation of the Unconventional Myosin MYO18B
Gurung, R., Ono, Y., Baxendale, S., et al. (2016) · Genetics · doi:10.1534/genetics.116.192864 · Cited by 35 · see citing works
Distinct troponin C isoform requirements in cardiac and skeletal muscle
Sogah, V. M., Serluca, F. C., Fishman, M. C., et al. (2010) · Developmental Dynamics · doi:10.1002/dvdy.22445 · Cited by 34 · see citing works
The HDAC Inhibitor TSA Ameliorates a Zebrafish Model of Duchenne Muscular Dystrophy
Johnson, N. M., Farr, G. H., & Maves, L. (2013) · PLoS Currents · doi:10.1371/currents.md.8273cf41db10e2d15dd3ab827cb4b027 · Cited by 34 · see citing works
Hypermuscular mice with mutation in the myostatin gene display altered calcium signalling
Bodnár, D., Geyer, N., Ruzsnavszky, O., Oláh, T., Hegyi, B., Sztretye, M. T., Fodor, J., Dienes, B., Balogh, Á., Papp, Z., et al. (2014) · The Journal of Physiology · doi:10.1113/jphysiol.2013.261958 · Cited by 33 · see citing works
Chen, W., Zhang, X., Li, J., Huang, S., Xiang, S., Hu, X., & Liu, C. (2018) · BMC Genomics · doi:10.1186/s12864-018-4458-7 · Cited by 33 · see citing works
Myo18b is essential for sarcomere assembly in fast skeletal muscle
Berger, J., Berger, S., Li, M., et al. (2017) · Human Molecular Genetics · doi:10.1093/hmg/ddx025 · Cited by 32 · see citing works
Madelaine, R., Notwell, J. H., Skariah, G. M., Halluin, C., Chen, C. C., Bejerano, G., & Mourrain, P. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky166 · Cited by 32 · see citing works
Froehlich, J. M., Fowler, Z. G., Galt, N. J., Smith, D. L., & Biga, P. R. (2013) · Frontiers in Genetics · doi:10.3389/fgene.2013.00159 · Cited by 31 · see citing works
A TALEN-Exon Skipping Design for a Bethlem Myopathy Model in Zebrafish
Radev, Z., Hermel, J., Elipot, Y., Bretaud, S., Arnould, S., Duchateau, P. N., Ruggiero, F., Joly, J., & Sohm, F. (2015) · PLoS ONE · doi:10.1371/journal.pone.0133986 · Cited by 30 · see citing works
The proteasomal inhibitor MG132 prevents muscular dystrophy in zebrafish.
Winder, S. J., Lipscomb, L., Angela Parkin, C., & Juusola, M. (2011) · PLoS Currents · doi:10.1371/currents.rrn1286 · Cited by 30 · see citing works
The complex genetics of gait speed: genome-wide meta-analysis approach
Ben-Avraham, D., Karasik, D., Verghese, J., et al. (2016) · Aging · doi:10.18632/aging.101151 · Cited by 29 · see citing works
Self-citationTensile properties of craniofacial tendons in the mature and aged zebrafish
Shah, R. R., Nerurkar, N. L., Wang, C. C., et al. (2015) · Journal of Orthopaedic Research® · doi:10.1002/jor.22847 · Cited by 27 · see citing works
Genetic Insights Into Frailty: Association of 9p21-23 Locus With Frailty
Sathyan, S., Barzilai, N., Atzmon, G., Milman, S., Ayers, E. I., & Verghese, J. (2018) · Frontiers in Medicine · doi:10.3389/fmed.2018.00105 · Cited by 27 · see citing works
Muscle growth in teleost fish is regulated by factors utilizing the activin II B receptor
Phelps, M., Jaffe, I. M., & Bradley, T. M. (2013) · Journal of Experimental Biology · doi:10.1242/jeb.086660 · Cited by 26 · see citing works
Early Fish Myoseptal Cells: Insights from the Trout and Relationships with Amniote Axial Tenocytes
Bricard, Y., Rallière, C., Lebret, V., et al. (2014) · PLoS ONE · doi:10.1371/journal.pone.0091876 · Cited by 24 · see citing works
van der Meulen, T., Schipper, H., LEEUWEN, J. L. V., et al. (2005) · Journal of Experimental Biology · doi:10.1242/jeb.01826 · Cited by 24 · see citing works
Exercise quantity-dependent muscle hypertrophy in adult zebrafish (Danio rerio)
Hasumura, T., & Meguro, S. (2016) · Journal of Comparative Physiology B · doi:10.1007/s00360-016-0977-1 · Cited by 23 · see citing works
Defective sarcomere assembly in smyd1a and smyd1b zebrafish mutants
Cai, M., Han, L., Liu, L., He, F., Chu, W., Zhang, J., Tian, Z., & Du, S. (2019) · The FASEB Journal · doi:10.1096/fj.201801578r · Cited by 23 · see citing works
A zebrafish model for FHL1-opathy reveals loss-of-function effects of human FHL1 mutations
Keßler, M., Kieltsch, A., Kayvanpour, E., et al. (2018) · Neuromuscular Disorders · doi:10.1016/j.nmd.2018.03.001 · Cited by 19 · see citing works
Byrne, C. A., McNeil, A. T., Koh, T. J., Brunskill, A. F., & Fantuzzi, G. (2019) · PLOS ONE · doi:10.1371/journal.pone.0222345 · Cited by 15 · see citing works
celsr1a is essential for tissue homeostasis and onset of aging phenotypes in the zebrafish
Li, C., Barton, C. L., Henke, K., Daane, J., Treaster, S. B., Caetano‐Lopes, J., Tanguay, R. L., & Harris, M. P. (2020) · eLife · doi:10.7554/elife.50523 · Cited by 14 · see citing works
Accumulation of intramuscular toxic lipids, a link between fat mass accumulation and sarcopenia
Capel, F., Pinel, A., & Walrand, S. (2019) · OCL · doi:10.1051/ocl/2019023 · Cited by 11 · see citing works
Using the zebrafish to understand tendon development and repair
Chen, J. W., & Galloway, J. L. (2016) · Methods in cell biology · doi:10.1016/bs.mcb.2016.10.003 · Cited by 10 · see citing works
Mazelet, L., Parker, M. O., Li, M., et al. (2016) · Frontiers in Physiology · doi:10.3389/fphys.2016.00091 · Cited by 9 · see citing works
Cavin4b/Murcb Is Required for Skeletal Muscle Development and Function in Zebrafish
Housley, M. P., Njaine, B., Ricciardi, F., Stone, O. A., Hölper, S., Krüger, M., Sawa Kostin, D., & Stainier, D. Y. R. (2016) · PLoS Genetics · doi:10.1371/journal.pgen.1006099 · Cited by 9 · see citing works
Rasal, K. D., Chakrapani, V., Patra, S. K., Mohapatra, S. D., Nayak, S., Jena, S., Sundaray, J. K., Jayasankar, P., & Barman, H. K. (2016) · BioMed Research International · doi:10.1155/2016/7562368 · Cited by 8 · see citing works
Advances in the Understanding of Skeletal Myopathies from Zebrafish Models
Baxter, E. C., & Bryson‐Richardson, R. J. (2018) · Springer eBooks · doi:10.1007/978-981-13-1879-5_9 · Cited by 2 · see citing works
Interactions Between Muscle and Bone
Brotto, M. A. P. (2018) · Primer on the metabolic bone diseases and disorders of mineral metabolism · doi:10.1002/9781119266594.ch135 · Cited by 1 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Christian, C. J., & Benian, G. M. (2020) · Aging Cell · doi:10.1111/acel.13223 · Cited by 113 · see citing works
Zou, Y.-Y., Chen, Z.-L., Sun, C.-C., Yang, D., Zhou, Z.-Q., Xiao, Q., Peng, X.-Y., & Tang, C.-F. (2022) · Nutrients · doi:10.3390/nu14091975 · Cited by 24 · see citing works
- Authors
- Daya, A., Donaka, R., & Karasik, D.
- Affiliations
- Ruppin Academic Center (IL)
- The Musculoskeletal Genetics Laboratory, The Azrieli Faculty of Medicine, Bar-Ilan University, Safed 130010, Israel
- Bar-Ilan University (IL)
- Corresponding author
- Karasik, David
- Venue
- Disease Models & Mechanisms
- Publisher
- The Company of Biologists
- Published
- 2020-03-01
- Volume
- 13
- Issue
- 3
- Pages
- dmm042689
- ISSN
- 1754-8403 (ISSN-L)
- 1754-8411
- PMC
- PMC7132805
- OpenAlex
- W3015072723
- Cited by
- 55
- References
- 143
- Citations by year
- 2026: 4 · 2025: 9 · 2024: 15 · 2023: 14 · 2022: 5 · 2021: 5 · 2020: 3
- FWCI
- 0.65
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Disease Models & Mechanisms (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- HighWire Press Open Archive (submittedVersion)
- Funders
- Israel Science Foundation (1121/19)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Muscle Physiology and Disorders
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Health Sciences › Medicine › Physiology › Nutrition and Health in Aging
- Keywords
- sarcopenia, zebrafish model, skeletal muscle, muscle mass, muscle strength, aging, frailty, teleosts, medaka, killifish, gene homology, genome-wide association study, animal models of human disease
- MeSH terms
- Animals, Disease Models, Animal, Zebrafish, Muscle, Skeletal, Biomedical Research, Genome-Wide Association Study, Sarcopenia
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
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