The translation initiation factor homolog eif4e1c regulates cardiomyocyte metabolism and proliferation during heart regeneration
Open accessPublished version of a preprint
Abstract
The eIF4E family of translation initiation factors bind 5′ methylated caps and act as the limiting step for mRNA translation. The canonical eIF4E1A is required for cell viability, yet other related eIF4E families exist and are utilized in specific contexts or tissues. Here, we describe a family called Eif4e1c, for which we find roles during heart development and regeneration in zebrafish. The Eif4e1c family is present in all aquatic vertebrates but is lost in all terrestrial species. A core group of amino acids shared over 500 million years of evolution forms an interface along the protein surface, suggesting that Eif4e1c functions in a novel pathway. Deletion of eif4e1c in zebrafish caused growth deficits and impaired survival in juveniles. Mutants surviving to adulthood had fewer cardiomyocytes and reduced proliferative responses to cardiac injury. Ribosome profiling of mutant hearts demonstrated changes in translation efficiency of mRNA for genes known to regulate cardiomyocyte proliferation. Although eif4e1c is broadly expressed, its disruption had most notable impact on the heart and at juvenile stages. Our findings reveal context-dependent requirements for translation initiation regulators during heart regeneration.
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
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.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764 · see citing works
Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nature Protocols · doi:10.1038/nprot.2008.211 · Cited by 35,890 · see citing works
IQ-TREE 2: New Models and Efficient Methods for Phylogenetic Inference in the Genomic Era
Minh, B. Q., Schmidt, H. A., Chernomor, O., Schrempf, D., Woodhams, M. D., von Haeseler, A., & Lanfear, R. (2020) · Molecular Biology and Evolution · doi:10.1093/molbev/msaa015 · Cited by 16,873 · see citing works
Comprehensive Integration of Single-Cell Data
Stuart, T., Butler, A., Hoffman, P., Hafemeister, C., Papalexi, E., Mauck, W. M., Hao, Y., Stoeckius, M., Smibert, P., & Satija, R. (2019) · Cell · doi:10.1016/j.cell.2019.05.031 · Cited by 15,453 · see citing works
Sherman, B. T., Hao, M., Qiu, J., Jiao, X., Baseler, M., Lane, H. C., Imamichi, T., & Chang, W. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac194 · Cited by 6,152 · see citing works
Accurate prediction of protein structures and interactions using a 3-track network
Baek, M., DiMaio, F., Anishchenko, I., Dauparas, J., Ovchinnikov, S., Lee, G. R., Wang, J., Cong, Q., Kinch, L. N., Schaeffer, R. D., et al. (2021) · doi:10.1101/2021.06.14.448402 · Cited by 5,542 · see citing works
W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis
Trifinopoulos, J., Nguyen, L.-T., von Haeseler, A., & Minh, B. Q. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw256 · Cited by 5,514 · see citing works
Software for Computing and Annotating Genomic Ranges
Lawrence, M. F., Huber, W. K., Pagès, H., Aboyoun, P., Carlson, M. R. J., Gentleman, R. C., Morgan, M. T., & Carey, V. J. (2013) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1003118 · Cited by 4,438 · see citing works
Heart Regeneration in Zebrafish
Poss, K. D., Wilson, L. G., & Keating, M. T. (2002) · Science · doi:10.1126/science.1077857 · Cited by 1,938 · see citing works
Self-citationSuperoxide activates mitochondrial uncoupling proteins
Echtay, K. S., Roussel, D., St-Pierre, J., Jekabsons, M. B., Cadenas, S., Stuart, J. A., Harper, J. A., Roebuck, S. J., Morrison, A., Pickering, S., et al. (2002) · Nature · doi:10.1038/415096a · Cited by 1,382 · see citing works
mRNAs, proteins and the emerging principles of gene expression control
Buccitelli, C., & Selbach, M. (2020) · Nature Reviews Genetics · doi:10.1038/s41576-020-0258-4 · Cited by 1,243 · see citing works
Ingolia, N. T., Brar, G. A., Rouskin, S., McGeachy, A. M., & Weissman, J. S. (2012) · Nature Protocols · doi:10.1038/nprot.2012.086 · Cited by 1,240 · see citing works
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 1,023 · see citing works
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 833 · see citing works
Self-citationD’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 649 · 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
Comparative genomics provides evidence for an ancient genome duplication event in fish
Taylor, J. S., de Peer, Y. V., Braasch, I., & Meyer, A. (2001) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2001.0975 · Cited by 532 · see citing works
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 · see citing works
Self-citationGraff, J., Konicek, B., Vincent, T. M., Lynch, R. L., Monteith, D., Weir, S., Schwier, P., Capen, A., Goode, R., Dowless, M., et al. (2007) · Journal of Clinical Investigation · doi:10.1172/jci32044 · Cited by 393 · see citing works
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 378 · see citing works
Self-citationDifferential Requirements for eIF4E Dose in Normal Development and Cancer
Truitt, M., Conn, C. S., Shi, Z., Pang, X., Tokuyasu, T. A., Coady, A. M., Seo, Y., Barna, M., & Ruggero, D. (2015) · Cell · doi:10.1016/j.cell.2015.05.049 · Cited by 374 · see citing works
eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans
Syntichaki, P., Troulinaki, K., & Tavernarakis, N. (2007) · Nature · doi:10.1038/nature05603 · Cited by 361 · see citing works
Evidence for hormonal control of heart regenerative capacity during endothermy acquisition
Hirose, K., Payumo, A. Y., Cutie, S., Hoang, A., Zhang, H., Guyot, R., Lunn, D., Bigley, R. B., Yu, H., Wang, J., et al. (2019) · Science · doi:10.1126/science.aar2038 · Cited by 354 · see citing works
A high-resolution mRNA expression time course of embryonic development in zebrafish
White, R. J., Collins, J. E., Sealy, I. M., Wali, N., Dooley, C. M., Digby, Z., Stemple, D. L., Murphy, D. N., Billis, K., Hourlier, T., et al. (2017) · eLife · doi:10.7554/elife.30860 · Cited by 345 · see citing works
Global Circumnavigations: Tracking Year-Round Ranges of Nonbreeding Albatrosses
Croxall, J. P., Silk, J. R. D., Phillips, R. A., Afanasyev, V., & Briggs, D. R. (2005) · Science · doi:10.1126/science.1106042 · Cited by 326 · see citing works
Modulation of tissue repair by regeneration enhancer elements
Kang, J., Hu, J., Karra, R., Dickson, A. L., Tornini, V. A., Nachtrab, G. T., Gemberling, M. P., Goldman, J., Black, B. L., & Poss, K. D. (2016) · Nature · doi:10.1038/nature17644 · Cited by 315 · see citing works
Self-citationGemberling, M. P., Karra, R., Dickson, A. L., & Poss, K. D. (2015) · eLife · doi:10.7554/elife.05871 · Cited by 301 · see citing works
Self-citationMitochondrial complex ii: At the crossroads
Bezawork-Geleta, A., Rohlena, J., Dong, L., Pacak, K., & Neuzil, J. (2017) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2017.01.003 · Cited by 295 · see citing works
Lai, S.-L., Marín‐Juez, R., Moura, P. L., Kuenne, C. T., Lai, J. K. H., Tsedeke, A. T., Günther, S., Looso, M., & Stainier, D. Y. R. (2017) · eLife · doi:10.7554/elife.25605 · Cited by 283 · see citing works
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 283 · see citing works
Self-citationInjury-induced ctgfa directs glial bridging and spinal cord regeneration in zebrafish
Mokalled, M. H., Patra, C., Dickson, A. L., Endo, T., Stainier, D. Y. R., & Poss, K. D. (2016) · Science · doi:10.1126/science.aaf2679 · Cited by 266 · see citing works
Self-citationMitochondrial 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 248 · see citing works
Sosa, J. M., Huber, D. E., Welk, B. A., & Fraser, H. L. (2014) · Integrating materials and manufacturing innovation · doi:10.1186/2193-9772-3-10 · Cited by 234 · see citing works
Retinoic Acid Signaling Restricts the Cardiac Progenitor Pool
Keegan, B. R., Feldman, J. L., Begemann, G., Ingham, P. W., & Yelon, D. L. (2005) · Science · doi:10.1126/science.1101573 · Cited by 232 · see citing works
Heterogeneity and specialized functions of translation machinery: from genes to organisms
Genuth, N. R., & Barna, M. (2018) · Nature Reviews Genetics · doi:10.1038/s41576-018-0008-z · Cited by 221 · see citing works
Azide–Alkyne Coupling: A Powerful Reaction for Bioconjugate Chemistry
Breinbauer, R., & Köhn, M. (2003) · ChemBioChem · doi:10.1002/cbic.200300705 · Cited by 213 · see citing works
Changes in regeneration-responsive enhancers shape regenerative capacities in vertebrates
Wang, W., Hu, C.-K., Zeng, A., Alegre, D., Hu, D., Gotting, K., Ortega Granillo, A., Wang, Y., Robb, S., Schnittker, R., et al. (2020) · Science · doi:10.1126/science.aaz3090 · Cited by 210 · see citing works
Identification of the zebrafish maternal and paternal transcriptomes
Harvey, S. A., Sealy, I. M., Kettleborough, R. N. W., Fényes, F., White, R. J., Stemple, D. L., & Smith, J. C. (2013) · Development · doi:10.1242/dev.095091 · Cited by 202 · see citing works
Fang, Y., Gupta, V., Karra, R., Holdway, J. E., Kikuchi, K., & Poss, K. D. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1309810110 · Cited by 190 · see citing works
Self-citationTranslational control in cellular and developmental processes
Kong, J., & Lasko, P. F. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3184 · Cited by 189 · see citing works
Wu, C. C., Kruse, F., Vasudevarao, M. D., Junker, J. P., Zebrowski, D. C., Fischer, K. J., Noël, E. S., Grün, D., Berezikov, E., Engel, F. B., et al. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.12.010 · Cited by 186 · see citing works
Transcriptome and translatome co-evolution in mammals
Wang, Z., Leushkin, E. V., Liechti, A., Ovchinnikova, S., Mößinger, K., Brüning, T., Rummel, C., Grützner, F., Cardoso-Moreira, M., Janich, P., et al. (2020) · Nature · doi:10.1038/s41586-020-2899-z · Cited by 183 · see citing works
CPEB Interacts with an Ovary-specific eIF4E and 4E-T in Early Xenopus Oocytes*
Minshall, N., Reiter, M., Weil, D., & Standart, N. (2007) · Journal of Biological Chemistry · doi:10.1074/jbc.m704629200 · Cited by 181 · see citing works
Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes
You, X., Bian, C., Zan, Q., Xu, X., Liu, X., Chen, J., Wang, J., Qiu, Y., Li, W., Zhang, X., et al. (2014) · Nature Communications · doi:10.1038/ncomms6594 · Cited by 173 · see citing works
Origin and function of activated fibroblast states during zebrafish heart regeneration
Hu, B., Lelek, S., Spanjaard, B., El‐Sammak, H., Simões, M. G., Mintcheva, J., Aliee, H., Schäfer, R., Meyer, A. M., Theis, F. J., et al. (2022) · Nature Genetics · doi:10.1038/s41588-022-01129-5 · Cited by 137 · see citing works
Grüner, S., Peter, D., Weber, R., Wohlbold, L., Chung, M.-Y., Weichenrieder, O., Valkov, E., Igreja, C., & Izaurralde, E. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.09.020 · Cited by 131 · see citing works
Phylogenetic analysis of eIF4E-family members
Joshi, B., Lee, K., Maeder, D. L., & Jagus, R. (2005) · BMC Evolutionary Biology · doi:10.1186/1471-2148-5-48 · Cited by 129 · see citing works
Heart Regeneration in the Mexican Cavefish
Stockdale, W. T., Lemieux, M. E., Killen, A. C., Zhao, J., Hu, Z., Riepsaame, J., Hamilton, N., Kudoh, T., Riley, P. R., van Aerle, R., et al. (2018) · Cell Reports · doi:10.1016/j.celrep.2018.10.072 · Cited by 119 · see citing works
Stimulation of glycolysis promotes cardiomyocyte proliferation after injury in adult zebrafish
Fukuda, R., Marín‐Juez, R., El‐Sammak, H., Beisaw, A., Ramadass, R., Kuenne, C. T., Günther, S., Konzer, A., Bhagwat, A. M., Graumann, J., et al. (2020) · EMBO Reports · doi:10.15252/embr.201949752 · Cited by 119 · see citing works
Resolving Heart Regeneration by Replacement Histone Profiling
Goldman, J., Kuzu, G., Lee, N., Karasik, J., Gemberling, M. P., Foglia, M. J., Karra, R., Dickson, A. L., Sun, F., Tolstorukov, M. Y., et al. (2017) · Developmental Cell · doi:10.1016/j.devcel.2017.01.013 · Cited by 118 · see citing works
Self-citationLin, J.-J., Wang, F., Li, W., & Wang, T. (2017) · Scientific Reports · doi:10.1038/s41598-017-15868-7 · Cited by 113 · see citing works
Deubiquitinase USP10 regulates Notch signaling in the endothelium
Lim, R., Sugino, T., Nolte, H., Andrade, J., Zimmermann, B., Shi, C., Doddaballapur, A., Ong, Y. T., Wilhelm, K., Fasse, J. W. D., et al. (2019) · Science · doi:10.1126/science.aat0778 · Cited by 112 · see citing works
A Mammalian Translation Initiation Factor Can Substitute for Its Yeast Homologue in Vivo
Altmann, M., Müller, P., Pelletier, J., Sonenberg, N., & Trachsel, H. (1989) · Journal of Biological Chemistry · doi:10.1016/s0021-9258(18)63833-5 · Cited by 112 · see citing works
Bian, C., Hu, Y., Ravi, V., Kuznetsova, I. S., Shen, X., Mu, X., Sun, Y., You, X., Li, J., Li, X., et al. (2016) · Scientific Reports · doi:10.1038/srep24501 · Cited by 107 · see citing works
Ribosome Stoichiometry: From Form to Function
Emmott, E., Jovanović, M., & Slavov, N. (2018) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2018.10.009 · Cited by 95 · see citing works
Poly(A) tail length regulates PABPC1 expression to tune translation in the heart
Chorghade, S., Seimetz, J. W., Emmons, R. S., Yang, J., Bresson, S. M., Lisio, M. D., Parise, G., Conrad, N. K., & Kalsotra, A. (2017) · eLife · doi:10.7554/elife.24139 · Cited by 89 · see citing works
EB1 promotes Aurora-B kinase activity through blocking its inactivation by protein phosphatase 2A
Sun, L., Gao, J., Dong, X., Liu, M., Li, D., Shi, X., Dong, J., Lü, X., Liu, C., & Zhou, J. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0710018105 · Cited by 89 · see citing works
A selective insecticidal protein from Pseudomonas for controlling corn rootworms
Schellenberger, U., Oral, J., Rosen, B. A., Wei, J., Zhu, G., Xie, W., McDonald, M. J., Cerf, D. C., Diehn, S. H., Crane, V. C., et al. (2016) · Science · doi:10.1126/science.aaf6056 · Cited by 87 · see citing works
The Ly6/uPAR protein Bouncer is necessary and sufficient for species-specific fertilization
Herberg, S., Gert, K. R., Schleiffer, A., & Pauli, A. (2018) · Science · doi:10.1126/science.aat7113 · Cited by 83 · see citing works
Lee, H. J., Hou, Y., Chen, Y., Dailey, Z. Z., Riddihough, A., Jang, H. J., Wang, T., & Johnson, S. L. (2020) · Genome biology · doi:10.1186/s13059-020-1948-0 · Cited by 64 · see citing works
RiboProfiling: a Bioconductor package for standard Ribo-seq pipeline processing
Popa, A., Lebrigand, K., Paquet, A. C., Nottet, N., Robbe-Sermesant, K., Waldmann, R., & Barbry, P. (2016) · F1000Research · doi:10.12688/f1000research.8964.1 · Cited by 62 · see citing works
Hu, Y., Xie, S., & Yao, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0149277 · Cited by 61 · see citing works
Regulation of gene expression via translational buffering
Kusnadi, E. P., Timpone, C., Topisirović, I., Larsson, O. S., & Furic, L. (2021) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2021.119140 · Cited by 60 · see citing works
Two Zebrafish eIF4E Family Members Are Differentially Expressed and Functionally Divergent
Robalino, J., Joshi, B., Fahrenkrug, S. C., & Jagus, R. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m313688200 · Cited by 60 · see citing works
High-Phosphate Diet Induces Exercise Intolerance and Impairs Fatty Acid Metabolism in Mice
Peri-Okonny, P., Baskin, K. K., Iwamoto, G. A., Mitchell, J. H., Smith, S. A., Kim, H., Szweda, L. I., Bassel‐Duby, R., Fujikawa, T., Castorena, C. M., et al. (2019) · Circulation · doi:10.1161/circulationaha.118.037550 · Cited by 58 · see citing works
Self-citationThompson, J., Ou, J., Lee, N., Shin, K., Cigliola, V., Song, L., Crawford, G. E., Kang, J., & Poss, K. D. (2020) · Development · doi:10.1242/dev.191262 · Cited by 58 · see citing works
Self-citationBorden, K. L. B., & Volpon, L. (2020) · RNA Biology · doi:10.1080/15476286.2020.1766179 · Cited by 56 · see citing works
A comparative genomics study of carbohydrate/glucose metabolic genes: from fish to mammals
Zhang, Y., Qin, C., Yang, L., Lu, R., Zhao, X., & Nie, G. (2018) · BMC Genomics · doi:10.1186/s12864-018-4647-4 · Cited by 55 · see citing works
Estrogen receptor alpha controls gene expression via translational offsetting
Lorent, J., Rebello, R. J., Hoef, V. V., Lawrence, M. G., Szkop, K. J., Kusnadi, E., Samreen, B., Balanathan, P., Scharmann, K., Takizawa, I., et al. (2018) · doi:10.1101/507574 · Cited by 46 · see citing works
Austin, C. M., Tan, M. H., Croft, L., Hammer, M. P., & Gan, H. M. (2015) · Genome Biology and Evolution · doi:10.1093/gbe/evv186 · Cited by 46 · see citing works
Enhancer selection dictates gene expression responses in remote organs during tissue regeneration
Sun, F., Ou, J., Shoffner, A. R., Luan, Y., Yang, H., Song, L., Safi, A., Cao, J., Yue, F., Crawford, G. E., et al. (2022) · Nature Cell Biology · doi:10.1038/s41556-022-00906-y · Cited by 46 · see citing works
Self-citationTranslational offsetting as a mode of estrogen receptor α‐dependent regulation of gene expression
Lorent, J., Kusnadi, E. P., van Hoef, V., Rebello, R. J., Leibovitch, M., Ristau, J., Chen, S., Lawrence, M. G., Szkop, K. J., Samreen, B., et al. (2019) · The EMBO Journal · doi:10.15252/embj.2018101323 · Cited by 46 · see citing works
Nuclear eIF4E Stimulates 3′-End Cleavage of Target RNAs
Davis, M. R., Delaleau, M., & Borden, K. L. B. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.04.008 · Cited by 45 · see citing works
Amino acid primed mTOR activity is essential for heart regeneration
Miklas, J. W., Levy, S., Hofsteen, P., Ic-Mex, D., Clark, E. C., Muster, J., Robitaille, A. M., Sivaram, G., Abell, L., Goodson, J. M., et al. (2021) · iScience · doi:10.1016/j.isci.2021.103574 · Cited by 41 · see citing works
Perzlmaier, A., Richter, F., & Seufert, W. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.472290 · Cited by 35 · see citing works
Pronobis, M. I., Zheng, S., Singh, S. P., Goldman, J. A., & Poss, K. D. (2021) · eLife · doi:10.7554/elife.66079 · Cited by 29 · see citing works
Self-citationSakurai, T., Tsuchida, M., Lampe, P. D., & Murakami, M. (2013) · Experimental Cell Research · doi:10.1016/j.yexcr.2013.05.022 · Cited by 27 · see citing works
Distinct Features of Cap Binding by eIF4E1b Proteins
Kubacka, D., Miguel, R. N., Minshall, N., Darżynkiewicz, E., Standart, N., & Zuberek, J. (2014) · Journal of Molecular Biology · doi:10.1016/j.jmb.2014.11.009 · Cited by 24 · see citing works
Myostatin is a negative regulator of adult neurogenesis after spinal cord injury in zebrafish
Saraswathy, V. M., Zhou, L., McAdow, A. R., Burris, B., Dogra, D., Reischauer, S., & Mokalled, M. H. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111705 · Cited by 22 · see citing works
The FGF-AKT pathway is necessary for cardiomyocyte survival for heart regeneration in zebrafish
Tahara, N., Akiyama, R., Wang, J., Kawakami, H., Bessho, Y., & Kawakami, Y. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2020.12.019 · Cited by 21 · see citing works
Sénéchal, P., Robert, F., Cencic, R., Yanagiya, A., Chu, J., Sonenberg, N., Paquet, M., & Pelletier, J. (2021) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-021-03940-5 · Cited by 20 · see citing works
Dynamics of Zebrafish Heart Regeneration Using an HPLC–ESI–MS/MS Approach
Ma, D., Tu, C., Sheng, Q., Yang, Y., Kan, Z., Guo, Y. P., Shyr, Y., Scott, I. C., & Lou, X. (2018) · Journal of Proteome Research · doi:10.1021/acs.jproteome.7b00915 · Cited by 20 · see citing works
Okuda, A., & Kimura, G. (1996) · Experimental Cell Research · doi:10.1006/excr.1996.0078 · Cited by 18 · see citing works
MNK2-eIF4E axis promotes cardiac repair in the infarcted mouse heart by activating cyclin D1
Chen, B.-R., Wei, T., Tang, C., Sun, J., Shan, T., Fan, Y., Yang, T., Li, Y., Ma, Y., Wang, S., et al. (2022) · Journal of Molecular and Cellular Cardiology · doi:10.1016/j.yjmcc.2022.02.006 · Cited by 13 · see citing works
Metabolic and Transcriptional Adaptations Improve Physical Performance of Zebrafish
Heinkele, F. J., Lou, B., Erben, V., Bennewitz, K., Poschet, G., Sticht, C., & Krøll, J. (2021) · Antioxidants · doi:10.3390/antiox10101581 · Cited by 11 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
eIF4E1b is a non-canonical eIF4E protecting maternal dormant mRNAs
Lorenzo-Orts, L., Strobl, M., Steinmetz, B., Leesch, F., Pribitzer, C., Roehsner, J., Schutzbier, M., Dürnberger, G., & Pauli, A. (2023) · EMBO Reports · doi:10.1038/s44319-023-00006-4 · Cited by 23 · see citing works
Harnessing the regenerative potential of interleukin11 to enhance heart repair
Shin, K., Rodriguez, A., Kim, C., Silaban, I. M., Xia, Y., Sun, J., Dong, C., Keleş, S., Wang, J., Cao, J., et al. (2024) · Nature Communications · doi:10.1038/s41467-024-54060-0 · Cited by 15 · see citing works
Self-citationCardiac Regeneration in Adult Zebrafish: A Review of Signaling and Metabolic Coordination
Mitra, A., Mandal, S., Banerjee, K., Ganguly, N., Sasmal, P., Banerjee, D., & Gupta, S. (2025) · Current Cardiology Reports · doi:10.1007/s11886-024-02162-y · Cited by 7 · see citing works
Duca, S., Xia, Y., Elmagid, L. M. A., Bakis, I., Qiu, M., Cao, Y., Guo, Y., Eichenbaum, J., McCain, M. L., Kang, J., et al. (2024) · Development · doi:10.1242/dev.202947 · Cited by 6 · see citing works
Self-citationBaliga, U. K., Yang, L., Ivanov, A. V., Schwartz, J. L., Jiang, F., Khor, E.-S., Das, D., Wainwright, L., & Yao, P. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26167863 · Cited by 3 · see citing works
RACK1 contributes to the upregulation of embryonic genes in a model of cardiac hypertrophy
Ceci, M., Bonvissuto, D., Papetti, F., Silvestri, F., Sette, C., Catalani, E., Cervia, D., Gornati, R., & Romano, N. (2024) · Scientific Reports · doi:10.1038/s41598-024-76138-x · Cited by 3 · see citing works
Rao, A., Russell, A., Segura-Bermudez, J. R., Franz, C. M. A. P., Dockery, R., Blatnik, A. J., Panten, J., Zevallos, M., McNulty, C., Pietrzak, M., et al. (2025) · Development · doi:10.1242/dev.204458 · Cited by 3 · see citing works
Self-citationDdx61-enriched condensates refine heart regeneration programs
Pronobis, M. I., DeLuca, S., Lee, S., Garcia, L., Ou, J., Bursac, N., & Poss, K. D. (2025) · Nature Communications · doi:10.1038/s41467-025-64026-5 · Cited by 2 · see citing works
Self-citationReal-time single-molecule imaging in zebrafish embryos uncovers noncanonical translation
Bellec, M., Liang, J., Mattonet, K., Morisaki, T., Lay, M., Maischein, H., Avinens, D., Martinet, V., Muriaux, D. M., Stasevich, T. J., et al. (2026) · Science Advances · doi:10.1126/sciadv.aeb6883 · Cited by 1 · see citing works
Cardiomyocyte Proliferation and Cardiac Cell Therapy
Li, F., & Zhu, W. (2025) · Springer eBooks · doi:10.1007/978-3-031-81743-4_9
Protein synthesis during mouse spermatogenesis
Yang, L., Hou, K., Lee, T., & Qi, H. (2026) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2026.01.001
Dockery, R., Zevallos, M., McNulty, C., Zecchino, T., Ratermann, R., White, R., Kolonay, D., Baskin, K. K., & Goldman, J. A. (2026) · Developmental Biology · doi:10.1016/j.ydbio.2026.02.014
Self-citationImmune-Enhancing Effects of Polygonatum cyrtonema Polysaccharides in Immunodeficient Zebrafish
Li, D., Wang, J., Chen, N., & Chen, N. (2026) · Current Issues in Molecular Biology · doi:10.3390/cimb48050494
Intrinsic oncogene silencing limits RAS-driven leukemogenesis through translational controlPreprint
Mulero, V., Jimenez-Blaya, A., Fernández-Lajarín, M., Martinez-Olmo, I., Cantón-Sandoval, J., García‐Moreno, D., Alcaraz‐Pérez, F., & Cayuela, M. L. (2026) · Research Square · doi:10.21203/rs.3.rs-10542078/v1
- Authors
- Rao, A., Lyu, B., Jahan, I., Lubertozzi, A., Zhou, G., Tedeschi, F., Jankowsky, E., Kang, J., Carstens, B., Poss, K. D., Baskin, K., & Goldman, J. A.
- Affiliations
- The Ohio State University Wexner Medical Center (US)
- The Ohio State University (US)
- Case Western Reserve University (US)
- University of Wisconsin–Madison (US)
- Duke University (US)
- Corresponding author
- Goldman, Joseph Aaron
- ORCID
- Venue
- Development
- Publisher
- The Company of Biologists
- Published
- 2023-06-12
- Volume
- 150
- Issue
- 20
- ISSN
- 0950-1991 (ISSN-L)
- 1477-9129
- PMC
- PMC10281269
- OpenAlex
- W4377940467
- Cited by
- 13
- References
- 85
- Citations by year
- 2026: 4 · 2025: 5 · 2024: 3 · 2023: 1
- FWCI
- 1.15
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Development (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- National Institutes of Health (R35HL150713, R01HL151522, R35GM137878)
- American Heart Association (17SDG33660922)
- Ohio State University
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Congenital heart defects research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Keywords
- translation initiation factors, cardiac regeneration, cardiomyocyte proliferation, cardiomyocyte metabolism, zebrafish, ribosome profiling, mRNA translation efficiency, heart development
- MeSH terms
- Animals, Heart Injuries, Zebrafish, Myocytes, Cardiac, Eukaryotic Initiation Factor-4E, Cell Proliferation
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
