The DOI matches its Crossref record; 25 of the 25 references it cites were found in a registry or an index.
Zebrafish heart regeneration occurs by cardiomyocyte dedifferentiation and proliferation
Open accessAbstract
Although mammalian hearts show almost no ability to regenerate, there is a growing initiative to determine whether existing cardiomyocytes or progenitor cells can be coaxed into eliciting a regenerative response. In contrast to mammals, several non-mammalian vertebrate species are able to regenerate their hearts, including the zebrafish, which can fully regenerate its heart after amputation of up to 20% of the ventricle. To address directly the source of newly formed cardiomyocytes during zebrafish heart regeneration, we first established a genetic strategy to trace the lineage of cardiomyocytes in the adult fish, on the basis of the Cre/lox system widely used in the mouse. Here we use this system to show that regenerated heart muscle cells are derived from the proliferation of differentiated cardiomyocytes. Furthermore, we show that proliferating cardiomyocytes undergo limited dedifferentiation characterized by the disassembly of their sarcomeric structure, detachment from one another and the expression of regulators of cell-cycle progression. Specifically, we show that the gene product of polo-like kinase 1 (plk1) is an essential component of cardiomyocyte proliferation during heart regeneration. Our data provide the first direct evidence for the source of proliferating cardiomyocytes during zebrafish heart regeneration and indicate that stem or progenitor cells are not significantly involved in this process.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“Injury is a well-established trigger of cellular de-differentiation, and the changes we observed are likely a consequence of human neurons adhering to this principle (Gu et al., 2020; Jopling et al., 2010; Poplawski et al., 2020; Renthal et al., 2020; Tzahor and Poss, 2017; Wagner et al., 2017).”
From Age-dependent instability of mature neuronal fate in induced neurons from Alzheimer’s patients (2021) · cites this paper as Jopling et al., 2010
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Adult pancreatic β-cells are formed by self-duplication rather than stem-cell differentiation
Dor, Y., Brown, J., Martinez, O. I., & Melton, D. A. (2004) · Nature · doi:10.1038/nature02520 · Cited by 2,219
Heart Regeneration in Zebrafish
Poss, K. D., Wilson, L. G., & Keating, M. T. (2002) · Science · doi:10.1126/science.1077857 · Cited by 1,938
The Tol2kit: A multisite gateway‐based construction kit for Tol2 transposon transgenesis constructs
Kwan, K. M., Fujimoto, E., Grabher, C., Mangum, B. D., Hardy, M., Campbell, D. S., Parant, J. M., Yost, H. J., Kanki, J. P., & Chien, C.-B. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21343 · Cited by 1,768
Neuregulin1/ErbB4 Signaling Induces Cardiomyocyte Proliferation and Repair of Heart Injury
Bersell, K. R., Arab, S., Haring, B., & Kühn, B. (2009) · Cell · doi:10.1016/j.cell.2009.04.060 · Cited by 1,053
Practical Methods in Electron Microscopy
Corliss, J. O., & Glauert, A. M. (1973) · Transactions of the American Microscopical Society · doi:10.2307/3224938 · Cited by 1,012
Lepilina, A., Coon, A. N., Kikuchi, K., Holdway, J. E., Roberts, R. W., Burns, C. G., & Poss, K. D. (2006) · Cell · doi:10.1016/j.cell.2006.08.052 · Cited by 848
Controlled expression of transgenes introduced by in vivo electroporation
Matsuda, T., & Cepko, C. L. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0610155104 · Cited by 666
p38 MAP kinase inhibition enables proliferation of adult mammalian cardiomyocytesPreprint
Engel, F. B., Schebesta, M., Duong, M. T., Lü, G., Ren, S. V., Madwed, J. B., Jiang, H., Wang, Y., & Keating, M. T. (2005) · Genes & Development · doi:10.1101/gad.1306705 · Cited by 595
Conditional targeted cell ablation in zebrafish: A new tool for regeneration studies
Curado, S., Anderson, R. M., Jungblut, B., Mumm, J. S., Schroeter, E. H., & Stainier, D. Y. R. (2007) · Developmental Dynamics · doi:10.1002/dvdy.21100 · Cited by 509
Huang, C., Tu, C., Hsiao, C., Hsieh, F., & Tsai, H. (2003) · Developmental Dynamics · doi:10.1002/dvdy.10356 · Cited by 506
Flagged first, then by citations
Cited by
Sorted by citations
Transient Regenerative Potential of the Neonatal Mouse Heart
Porrello, E. R., Mahmoud, A. I., Simpson, E., Hill, J. A., Richardson, J. A., Olson, E. N., & Sadek, H. A. (2011) · Science · doi:10.1126/science.1200708 · Cited by 2,545
Mammalian heart renewal by pre-existing cardiomyocytes
Senyo, S. E., Steinhauser, M. L., Pizzimenti, C. L., Yang, V. K., Cai, L., Wang, M., Wu, T.-D., Guerquin-Kern, J.-L., Lechene, C. P., & Lee, R. T. (2013) · Nature · doi:10.1038/nature11682 · Cited by 1,343
Laflamme, M. A., & Murry, C. E. (2011) · Nature · doi:10.1038/nature10147 · Cited by 1,272
Functional screening identifies miRNAs inducing cardiac regeneration
Eulalio, A., Mano, M., Ferro, M. D., Zentilin, L., Sinagra, G., Zacchigna, S., & Giacca, M. (2012) · Nature · doi:10.1038/nature11739 · Cited by 1,029
Cardiac fibrosis in myocardial infarction—from repair and remodeling to regeneration
Talman, V., & Ruskoaho, H. J. (2016) · Cell and Tissue Research · doi:10.1007/s00441-016-2431-9 · Cited by 959
Hippo pathway effector Yap promotes cardiac regeneration
Xin, M., Kim, Y., Sutherland, L. B., Murakami, M., Qi, X., McAnally, J., Porrello, E. R., Mahmoud, A. I., Tan, W., Shelton, J. M., et al. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1313192110 · Cited by 895
Regulation of neonatal and adult mammalian heart regeneration by the miR-15 family
Porrello, E. R., Mahmoud, A. I., Simpson, E., Johnson, B. A., Grinsfelder, D. B., Canseco, D. C., Mammen, P. P. A., Rothermel, B. A., Olson, E. N., & Sadek, H. A. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1208863110 · Cited by 754
Dedifferentiation, transdifferentiation and reprogramming: three routes to regeneration
Jopling, C., Boué, S., & Belmonte, J. C. I. (2011) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3043 · Cited by 750
Self-citationBone Marrow Mesenchymal Stem Cells Stimulate Cardiac Stem Cell Proliferation and Differentiation
Hatzistergos, K. E., Quevedo, H. C., Oskouei, B. N., Hu, Q., Feigenbaum, G. S., Margitich, I. S., Mazhari, R., Boyle, A., Zambrano, J. P., Rodríguez, J. E., et al. (2010) · Circulation Research · doi:10.1161/circresaha.110.222703 · Cited by 719
Hypoxia induces heart regeneration in adult mice
Nakada, Y., Canseco, D. C., Thet, S., Abdisalaam, S., Asaithamby, A., Santos, C. X. C., Shah, A. M., Zhang, H., Faber, J. E., Kinter, M. T., et al. (2016) · Nature · doi:10.1038/nature20173 · Cited by 714
Burridge, P. W., Keller, G., Gold, J. D., & Wu, J. C. (2012) · Cell Stem Cell · doi:10.1016/j.stem.2011.12.013 · Cited by 670
Dedifferentiation of committed epithelial cells into stem cells in vivo
Tata, P. R., Mou, H., Pardo–Saganta, A., Zhao, R., Prabhu, M., Law, B. M., Vinarsky, V., Cho, J. L., Breton, S., Sahay, A., et al. (2013) · Nature · doi:10.1038/nature12777 · Cited by 679
Cardiomyocyte Maturation: New Phase in Development
Guo, Y., & Pu, W. T. (2020) · Circulation Research · doi:10.1161/circresaha.119.315862 · Cited by 653
D’Uva, G., Aharonov, A., Lauriola, M., Kain, D., Yahalom-Ronen, Y., Carvalho, S., Weisinger, K., Bassat, E., Rajchman, D., Yifa, O., et al. (2015) · Nature Cell Biology · doi:10.1038/ncb3149 · Cited by 667
Regulation of Cell Cycle to Stimulate Adult Cardiomyocyte Proliferation and Cardiac Regeneration
Mohamed, T., Ang, Y.-S., Radzinsky, E., Zhou, P., Huang, Y., Elfenbein, A., Foley, A., Magnitsky, S. G., & Srivastava, D. (2018) · Cell · doi:10.1016/j.cell.2018.02.014 · Cited by 582
The Cellular Basis for Animal Regeneration
Tanaka, E. M., & Reddien, P. W. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.06.016 · Cited by 573
The zebrafish as a model for complex tissue regeneration
Gemberling, M. P., Bailey, T. J., Hyde, D. R., & Poss, K. D. (2013) · Trends in Genetics · doi:10.1016/j.tig.2013.07.003 · Cited by 596
Meis1 regulates postnatal cardiomyocyte cell cycle arrest
Mahmoud, A. I., Kocabaş, F., Muralidhar, S. A., Kimura, W., Koura, A. S., Thet, S., Porrello, E. R., & Sadek, H. A. (2013) · Nature · doi:10.1038/nature12054 · Cited by 565
Mending broken hearts: cardiac development as a basis for adult heart regeneration and repair
Xin, M., Olson, E. N., & Bassel-Duby, R. (2013) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3619 · Cited by 514
Hooked! Modeling human disease in zebrafish
Santoriello, C., & Zon, L. I. (2012) · Journal of Clinical Investigation · doi:10.1172/jci60434 · Cited by 534
Adult mouse epicardium modulates myocardial injury by secreting paracrine factors
Zhou, B., Honor, L. B., He, H., Ma, Q., Oh, J., Butterfield, C., Lin, R., Melero‐Martin, J. M., Dolmatova, E. V., Duffy, H. S., et al. (2011) · Journal of Clinical Investigation · doi:10.1172/jci45529 · Cited by 522
The AP2/ERF Transcription Factor WIND1 Controls Cell Dedifferentiation in Arabidopsis
Iwase, A., Mitsuda, N., Koyama, T., Hiratsu, K., Kojima, M., Arai, T., Inoue, Y., Seki, M., Sakakibara, H., Sugimoto, K., et al. (2011) · Current Biology · doi:10.1016/j.cub.2011.02.020 · Cited by 506
Epicardial FSTL1 reconstitution regenerates the adult mammalian heart
Wei, K., Serpooshan, V., Hurtado, C., Diez-Cuñado, M., Zhao, M., Maruyama, S., Zhu, W., Fajardo, G., Noseda, M., Nakamura, K., et al. (2015) · Nature · doi:10.1038/nature15372 · Cited by 498
MicroRNA therapy stimulates uncontrolled cardiac repair after myocardial infarction in pigs
Gabisonia, K., Prosdocimo, G., Aquaro, G. D., Carlucci, L., Zentilin, L., Secco, I., Ali, H., Braga, L., Gorgodze, N., Bernini, F., et al. (2019) · Nature · doi:10.1038/s41586-019-1191-6 · Cited by 478
Extensive scar formation and regression during heart regeneration after cryoinjury in zebrafish
González‐Rosa, J. M., Martín, V., Peralta, M., Torres, M., & Mercader, N. (2011) · Development · doi:10.1242/dev.060897 · Cited by 463
Kikuchi, K., Holdway, J. E., Major, R. J., Blum, N., Dahn, R. D., Begemann, G., & Poss, K. D. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.01.010 · Cited by 458
Regeneration of the adult zebrafish brain from neurogenic radial glia-type progenitors
Kroehne, V., Freudenreich, D., Hans, S., Kaslin, J., & Brand, M. (2011) · Development · doi:10.1242/dev.072587 · Cited by 470
miR-15 Family Regulates Postnatal Mitotic Arrest of Cardiomyocytes
Porrello, E. R., Johnson, B. A., Aurora, A. B., Simpson, E., Nam, Y., Matkovich, S. J., Dorn, G. W., van Rooij, E., & Olson, E. N. (2011) · Circulation Research · doi:10.1161/circresaha.111.248880 · Cited by 449
Advances in understanding tissue regenerative capacity and mechanisms in animals
Poss, K. D. (2010) · Nature Reviews Genetics · doi:10.1038/nrg2879 · Cited by 442
The zebrafish heart regenerates after cryoinjury-induced myocardial infarction
Chablais, F., Veit, J., Rainer, G., & Jaźwińska, A. (2011) · BMC Developmental Biology · doi:10.1186/1471-213x-11-21 · Cited by 415
Chen, J., Huang, Z., Seok, H., Ding, J., Kataoka, M., Zhang, Z., Hu, X., Wang, G., Lin, Z., Wang, S., et al. (2013) · Circulation Research · doi:10.1161/circresaha.112.300658 · Cited by 403
Vincent, S. D., & BUCKINGHAM, M. E. (2010) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/s0070-2153(10)90001-x · Cited by 390
The Hippo pathway in the heart: pivotal roles in development, disease, and regeneration
Wang, J., Liu, S., Heallen, T. R., & Martin, J. F. (2018) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0063-3 · Cited by 389
Wang, J., Panáková, D., Kikuchi, K., Holdway, J. E., Gemberling, M. P., Burris, J. S., Singh, S. P., Dickson, A. L., Lin, Y., Sabeh, M. K., et al. (2011) · Development · doi:10.1242/dev.068601 · Cited by 388
Bone Regenerates via Dedifferentiation of Osteoblasts in the Zebrafish Fin
Knopf, F., Hammond, C., Chekuru, A., Kurth, T., Hans, S., Weber, C., Mahatma, G., Fisher, S., Brand, M., Schulte‐Merker, S., et al. (2011) · Developmental Cell · doi:10.1016/j.devcel.2011.04.014 · Cited by 374
Adult cell plasticity in vivo: de-differentiation and transdifferentiation are back in style
Merrell, A. J., & Stanger, B. Z. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2016.24 · Cited by 369
Force, T. L., & Kolaja, K. L. (2011) · Nature Reviews Drug Discovery · doi:10.1038/nrd3252 · Cited by 370
Cardiac Stem Cell Therapy and the Promise of Heart Regeneration
Garbern, J. C., & Lee, R. T. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.05.008 · Cited by 376
Oncostatin M Is a Major Mediator of Cardiomyocyte Dedifferentiation and Remodeling
Kubin, T., Pöling, J., Sawa Kostin, D., Gajawada, P., Hein, S., Rees, W., Wietelmann, A., Tanaka, M., Lörchner, H., Schimanski, S., et al. (2011) · Cell stem cell · doi:10.1016/j.stem.2011.08.013 · Cited by 355
Sugimoto, K., Gordon, S., & Meyerowitz, E. M. (2011) · Trends in Cell Biology · doi:10.1016/j.tcb.2010.12.004 · Cited by 356
Cardiac regeneration strategies: Staying young at heart
Tzahor, E., & Poss, K. D. (2017) · Science · doi:10.1126/science.aam5894 · Cited by 357
Adult neurogenesis and brain regeneration in zebrafish
Kızıl, Ç., Kaslin, J., Kroehne, V., & Brand, M. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20918 · Cited by 370
Functional Recovery of a Human Neonatal Heart After Severe Myocardial Infarction
Haubner, B. J., Schneider, J., Schweigmann, U., Schuetz, T., Dichtl, W., Velik‐Salchner, C., Stein, J.-I., & Penninger, J. M. (2015) · Circulation Research · doi:10.1161/circresaha.115.307017 · Cited by 355
The Role of Oxidative Stress in Myocardial Ischemia and Reperfusion Injury and Remodeling: Revisited
Kurian, G. A., Rajagopal, R., Vedantham, S., & Rajesh, M. (2016) · Oxidative Medicine and Cellular Longevity · doi:10.1155/2016/1656450 · Cited by 343
Little Fish, Big Data: Zebrafish as a Model for Cardiovascular and Metabolic Disease
Gut, P., Reischauer, S., Stainier, D. Y. R., & Arnaout, R. (2017) · Physiological Reviews · doi:10.1152/physrev.00038.2016 · Cited by 339
Sandoval‐Guzmán, T., Wang, H., Khattak, S., Schuez, M., Roensch, K., Nacu, E., Tazaki, A., Joven, A., Tanaka, E. M., & Simon, A. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.11.007 · Cited by 321
Frequency of mononuclear diploid cardiomyocytes underlies natural variation in heart regeneration
Patterson, M., Barske, L. A., Handel, B. V., Rau, C. D., Gan, P., Sharma, A., Parikh, S. S., Denholtz, M., Huang, Y., Yamaguchi, Y., et al. (2017) · Nature Genetics · doi:10.1038/ng.3929 · Cited by 322
Acquistapace, A., Bru, T., Lesault, P., Figeac, F., Coudert, A. E., Coz, O. L., Christov, C., Baudin, X., Auber, F., Yiou, R., et al. (2011) · Stem Cells · doi:10.1002/stem.632 · Cited by 312
Cahill, T. J., Choudhury, R. P., & Riley, P. R. (2017) · Nature Reviews Drug Discovery · doi:10.1038/nrd.2017.106 · Cited by 315
Immune Modulation of Stem Cells and Regeneration
Aurora, A. B., & Olson, E. N. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.06.009 · Cited by 322
MicroRNAs in cardiovascular disease: from pathogenesis to prevention and treatment
Quiat, D., & Olson, E. N. (2013) · Journal of Clinical Investigation · doi:10.1172/jci62876 · Cited by 307
Gemberling, M. P., Karra, R., Dickson, A. L., & Poss, K. D. (2015) · eLife · doi:10.7554/elife.05871 · Cited by 311
Myocardial Metabolomics of Human Heart Failure With Preserved Ejection Fraction
Hahn, V. S., Petucci, C. J., Kim, M., Bedi, K. C., Wang, H., Mishra, S., Koleini, N., Yoo, E., Margulies, K. B., Arany, Z. P., et al. (2023) · Circulation · doi:10.1161/circulationaha.122.061846 · Cited by 305
Kikuchi, K., Gupta, V., Wang, J., Holdway, J. E., Wills, A. A., Fang, Y., & Poss, K. D. (2011) · Development · doi:10.1242/dev.067041 · Cited by 293
Mechanisms of Cardiac Regeneration
Uygur, A., & Lee, R. T. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.01.018 · Cited by 304
YAP Partially Reprograms Chromatin Accessibility to Directly Induce Adult Cardiogenesis In Vivo
Monroe, T. O., Hill, M. C., Morikawa, Y., Leach, J. P., Heallen, T., Cao, S., Krijger, P. H. L., de Laat, W., Wehrens, X. H. T., Rodney, G. G., et al. (2019) · Developmental Cell · doi:10.1016/j.devcel.2019.01.017 · Cited by 289
Cardiac Regenerative Capacity and Mechanisms
Kikuchi, K., & Poss, K. D. (2012) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev-cellbio-101011-155739 · Cited by 305
Multicellular Transcriptional Analysis of Mammalian Heart Regeneration
Quaife-Ryan, G. A., Sim, C. B., Ziemann, M., Kaspi, A., Rafehi, H., Ramialison, M., El‐Osta, A., Hudson, J. E., & Porrello, E. R. (2017) · Circulation · doi:10.1161/circulationaha.117.028252 · Cited by 293
Notch and interacting signalling pathways in cardiac development, disease, and regeneration
MacGrogan, D., Münch, J., & de la Pompa, J. L. (2018) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0100-2 · Cited by 295
Honkoop, H., de Bakker, D. E. M., Aharonov, A., Kruse, F., Shakked, A., Nguyen, P. D., de Heus, C., Garric, L., Muraro, M. J., Shoffner, A. R., et al. (2019) · eLife · doi:10.7554/elife.50163 · Cited by 293
Signaling and Transcriptional Networks in Heart Development and RegenerationPreprint
Bruneau, B. (2013) · Cold Spring Harbor Perspectives in Biology · doi:10.1101/cshperspect.a008292 · Cited by 295
Ruvinov, E., Leor, J., & Cohen, S. (2010) · Biomaterials · doi:10.1016/j.biomaterials.2010.08.097 · Cited by 278
Uncovering the Molecular and Cellular Mechanisms of Heart Development Using the Zebrafish
Staudt, D., & Stainier, D. Y. R. (2012) · Annual Review of Genetics · doi:10.1146/annurev-genet-110711-155646 · Cited by 278
Schnabel, K., Wu, C. C., Kurth, T., & Weidinger, G. (2011) · PLoS ONE · doi:10.1371/journal.pone.0018503 · Cited by 274
Resident and Monocyte-Derived Macrophages in Cardiovascular Disease
Honold, L., & Nahrendorf, M. (2018) · Circulation Research · doi:10.1161/circresaha.117.311071 · Cited by 283
Zebrafish Regulatory T Cells Mediate Organ-Specific Regenerative Programs
Hui, S. P., Sheng, D. Z., Sugimoto, K., González-Rajal, Á., Nakagawa, S., Hesselson, D., & Kikuchi, K. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.11.010 · Cited by 272
Tissue repair and regeneration with endogenous stem cells
Xia, H., Li, X., Gao, W., Fu, X., Fang, R. H., Zhang, L., & Zhang, K. (2018) · Nature Reviews Materials · doi:10.1038/s41578-018-0027-6 · Cited by 275
Nerves Regulate Cardiomyocyte Proliferation and Heart Regeneration
Mahmoud, A. I., O'Meara, C. C., Gemberling, M. P., Zhao, L., Bryant, D. M., Zheng, R., Gannon, J., Cai, L., Choi, W.-Y., Egnaczyk, G. F., et al. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.06.017 · Cited by 273
Complete cardiac regeneration in a mouse model of myocardial infarction
Haubner, B. J., Adamowicz-Brice, M., Khadayate, S., Tiefenthaler, V., Metzler, B., Aitman, T., & Penninger, J. M. (2012) · Aging · doi:10.18632/aging.100526 · Cited by 261
In vivo cardiac reprogramming contributes to zebrafish heart regeneration
Zhang, R., Han, P., Yang, H., Ouyang, K., Lee, D. P. H., Lin, Y.-F., Ocorr, K. A., Kang, G., Chen, J., Stainier, D. Y. R., et al. (2013) · Nature · doi:10.1038/nature12322 · Cited by 265
Existing cardiomyocytes generate cardiomyocytes at a low rate after birth in mice
Ali, S. R., Hippenmeyer, S., Saadat, L. V., Luo, L., Weissman, I. L., & Ardehali, R. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1408233111 · Cited by 260
Clonally dominant cardiomyocytes direct heart morphogenesis
Gupta, V., & Poss, K. D. (2012) · Nature · doi:10.1038/nature11045 · Cited by 255
Notch signaling regulates cardiomyocyte proliferation during zebrafish heart regeneration
Zhao, L., Borikova, A. L., Ben-Yair, R., Guner‐Ataman, B., MacRae, C. A., Lee, R. T., Burns, C. G., & Burns, C. E. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1311705111 · Cited by 264
Comparative regenerative mechanisms across different mammalian tissues
Iismaa, S. E., Kaidonis, X., Nicks, A. M., Bogush, N., Kikuchi, K., Naqvi, N., Harvey, R. P., Husain, A., & Graham, R. M. (2018) · npj Regenerative Medicine · doi:10.1038/s41536-018-0044-5 · Cited by 270
Embryonic Heart Progenitors and Cardiogenesis
Brade, T., Pane, L. S., Moretti, A., Chien, K. R., & Laugwitz, K.-L. (2013) · Cold Spring Harbor Perspectives in Medicine · doi:10.1101/cshperspect.a013847 · Cited by 254
Endocardial Notch Signaling in Cardiac Development and Disease
Luxán, G., D’Amato, G., MacGrogan, D., & de la Pompa, J. L. (2015) · Circulation Research · doi:10.1161/circresaha.115.305350 · Cited by 254
Mitochondrial substrate utilization regulates cardiomyocyte cell-cycle progression
Cardoso, A. C., Lam, N. T., Savla, J. J., Nakada, Y., Pereira, A. H. M., Elnwasany, A., Menendez-Montes, I., Ensley, E. L., Petric, U. B., Sharma, G., et al. (2020) · Nature Metabolism · doi:10.1038/s42255-020-0169-x · Cited by 259
Building and re-building the heart by cardiomyocyte proliferation
Foglia, M. J., & Poss, K. D. (2016) · Development · doi:10.1242/dev.132910 · Cited by 247
Age-dependent instability of mature neuronal fate in induced neurons from Alzheimer’s patients
Mertens, J., Herdy, J. R., Traxler, L., Schafer, S. T., Schlachetzki, J. C. M., Böhnke, L., Reid, D. A., Lee, H., Zangwill, D., Fernandes, D. P., et al. (2021) · Cell Stem Cell · doi:10.1016/j.stem.2021.04.004 · Cited by 240
He, J., Lu, H., Zou, Q., & Luo, L. (2013) · Gastroenterology · doi:10.1053/j.gastro.2013.11.045 · Cited by 247
Model systems for regeneration: zebrafish
Marques, I. J., Lupi, E., & Mercader, N. (2019) · Development · doi:10.1242/dev.167692 · Cited by 254
The regenerative capacity of the zebrafish heart is dependent on TGFβ signaling
Chablais, F., & Jaźwińska, A. (2012) · Development · doi:10.1242/dev.078543 · Cited by 237
The epicardium as a hub for heart regeneration
Cao, J., & Poss, K. D. (2018) · Nature Reviews Cardiology · doi:10.1038/s41569-018-0046-4 · Cited by 241
Skeletogenic Fate of Zebrafish Cranial and Trunk Neural Crest
Kague, É., Gallagher, M. D., Burke, S., Parsons, M. J., Franz‐Odendaal, T. A., & Fisher, S. (2012) · PLoS ONE · doi:10.1371/journal.pone.0047394 · Cited by 234
Wang, J., Karra, R., Dickson, A. L., & Poss, K. D. (2013) · Developmental Biology · doi:10.1016/j.ydbio.2013.08.012 · Cited by 234
MicroRNA-34a Plays a Key Role in Cardiac Repair and Regeneration Following Myocardial Infarction
Yang, Y., Cheng, H.-W., Qiu, Y., Dupee, D., Noonan, M., Lin, Y., Fisch, S., Unno, K., Sereti, K., & Liao, R. (2015) · Circulation Research · doi:10.1161/circresaha.117.305962 · Cited by 234
Morikawa, Y., Zhang, M., Heallen, T. R., Leach, J. P., Tao, G., Xiao, Y., Bai, Y., Li, W., Willerson, J. T., & Martin, J. F. (2015) · Science Signaling · doi:10.1126/scisignal.2005781 · Cited by 227
Wang, W. E., Li, L., Xia, X., Fu, W., Liao, Q., Lan, C., Yang, D., Chen, H., Yue, R., Zeng, C., et al. (2017) · Circulation · doi:10.1161/circulationaha.116.024307 · Cited by 220
The Hippo Pathway in Heart Development, Regeneration, and Diseases
Zhou, Q., Li, L., Zhao, B., & Guan, K. (2015) · Circulation Research · doi:10.1161/circresaha.116.303311 · Cited by 229
Silva, A. C., Pereira, C., Fonseca, A. C. R. G., Pinto‐do‐Ó, P., & Nascimento, D. S. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.621644 · Cited by 231
Physiological Relevance of Cell Cycle Kinases
Malumbres, M. (2011) · Physiological Reviews · doi:10.1152/physrev.00025.2010 · Cited by 225
ERBB2 drives YAP activation and EMT-like processes during cardiac regeneration
Aharonov, A., Shakked, A., Umansky, K. B., Savidor, A., Genzelinakh, A., Kain, D., Lendengolts, D., Revach, O., Morikawa, Y., Dong, J., et al. (2020) · Nature Cell Biology · doi:10.1038/s41556-020-00588-4 · Cited by 217
Bizuayehu, T. T., & Babiak, I. (2014) · Genome Biology and Evolution · doi:10.1093/gbe/evu151 · Cited by 219
Lesizza, P., Prosdocimo, G., Martinelli, V. C., Sinagra, G., Zacchigna, S., & Giacca, M. (2017) · Circulation Research · doi:10.1161/circresaha.116.309589 · Cited by 211
Genetic Lineage Tracing of Nonmyocyte Population by Dual Recombinases
Li, Y., He, L., Huang, X., Bhaloo, S. I., Zhao, H., Zhang, S., Pu, W., Tian, X., Liu, Q., Liu, Q., et al. (2018) · Circulation · doi:10.1161/circulationaha.118.034250 · Cited by 207
Fast revascularization of the injured area is essential to support zebrafish heart regeneration
Marín‐Juez, R., Marass, M., Gauvrit, S., Rossi, A., Lai, S.-L., Materna, S. C., Black, B. L., & Stainier, D. Y. R. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1605431113 · Cited by 201
Dedifferentiation and Proliferation of Mammalian Cardiomyocytes
Zhang, Y., Li, T., Lee, S.-T., Wawrowsky, K., Cheng, K., Galang, G., Malliaras, K. G., Abraham, M. R., Wang, C., & Marbán, E. (2010) · PLoS ONE · doi:10.1371/journal.pone.0012559 · Cited by 203
Gene regulatory programmes of tissue regeneration
Goldman, J. A., & Poss, K. D. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0239-7 · Cited by 200
Cardiac Regeneration from Activated Epicardium
van Wijk, B., Gunst, Q. D., Moorman, A. F. M., & van den Hoff, M. J. B. (2012) · PLoS ONE · doi:10.1371/journal.pone.0044692 · Cited by 207
In Vivo Activation of a Conserved MicroRNA Program Induces Mammalian Heart Regeneration
Aguirre, A., Montserrat, N., Zacchigna, S., Nivet, E., Hishida, T., Krause, M. N., Kurian, L., Ocampo, A., Vazquez-Ferrer, E., Rodrı́guez-Esteban, C., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.10.003 · Cited by 198
Self-citation
Metadata
- Authors
- Jopling, C., Sleep, E., Raya, M., Martí, M., Raya, A., & Belmonte, J. C. I.
- Affiliations
- Center of Regenerative Medicine in Barcelona (ES)
- Biomedical Research Networking Center in Bioengineering, Biomaterials and Nanomedicine (ES)
- Salk Institute for Biological Studies (US)
- Corresponding author
- Belmonte, Juan Carlos Izpisúa
- Venue
- Nature
- Published
- 2010-03-25
- Volume
- 464
- Issue
- 7288
- Pages
- 606-609
- ISSN
- 0028-0836 (ISSN-L)
- 1476-4687
- PMC
- PMC2846535
- OpenAlex
- W1998457769
- Cited by
- 1,333
- References
- 25
- Citations by year
- 2026: 54 · 2025: 73 · 2024: 53 · 2023: 59 · 2022: 85 · 2021: 104 · 2020: 98 · 2019: 83 · 2018: 99 · 2017: 74 · 2016: 82 · 2015: 88 · 2014: 82 · 2013: 93 · 2012: 101
- FWCI
- 38.85
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Nature (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- RePEc: Research Papers in Economics (submittedVersion)
- Funders
- G. Harold and Leila Y. Mathers Foundation
- Ministerio de Ciencia e Innovación
- National Heart, Lung, and Blood Institute (R33HL088293)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Life Sciences › Neuroscience › Developmental Neuroscience › Neurogenesis and neuroplasticity mechanisms
- Keywords
- zebrafish heart regeneration, cardiomyocyte dedifferentiation, cardiomyocyte proliferation, myocardial infarction, PLK1, sarcomere disassembly, cell cycle regulators, cardiac progenitor cells
- MeSH terms
- Polo-Like Kinase 1, Animals, Gene Expression Regulation, Heart, Proto-Oncogene Proteins, Regeneration, Sarcomeres, Zebrafish, Protein Serine-Threonine Kinases, Cell Cycle Proteins, Cell Lineage, Myocytes, Cardiac, Cell Proliferation, Cell Dedifferentiation
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.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
