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PreprintCited by 13Congenital heart defects researchRNA and protein synthesis mechanismsZebrafish Biomedical Research Applications

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The Translation Initiation Factor Homolog, eif4e1c , Regulates Cardiomyocyte Metabolism and Proliferation During Heart Regeneration

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Rao, Anupama, Lyu, Baken, Jahan, Ishrat, Lubertozzi, Anna, Zhou, Gao, Tedeschi, Frank, Jankowsky, Eckhard, Kang, Junsu, Carstens, Bryan, Poss, Ken, Baskin, Kedryn, Goldman, Joseph Aaron·2022·Development
DOI 10.1101/2022.08.15.502524PMC PMC10281269

Preprint — published as 10.1242/dev.201376 · Paper page

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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 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.

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Research works printed but not linked: 77

  1. 1989, A Mammalian Translation Initiation Factor Can Substitute for Its Yeast Homologue in Vivo, J Biol Chem, 264, 12145, 10.1016/S0021-9258(18)63833-5 · DOI
  2. 10.1093/gbe/evv186 · DOI
  3. 2021, Accurate prediction of protein structures and interactions using a 3-track neural network, Sci New York N Y, 373, 871, 10.1126/science.abj8754 · DOI · Paper page
  4. 10.1016/j.tibs.2017.01.003 · DOI · Paper page
  5. 2016, The Asian arowana (Scleropages formosus) genome provides new insights into the evolution of an early lineage of teleosts, Sci Rep-uk, 6, 24501, 10.1038/srep24501 · DOI · Paper page
  6. 2020, The diversity, plasticity, and adaptability of cap-dependent translation initiation and the associated machinery, Rna Biol, 17, 1
  7. 2016, The spotted gar genome illuminates vertebrate evolution and facilitates human-teleost comparisons, Nat Genet, 48, 437
  8. 2020, mRNAs, proteins and the emerging principles of gene expression control, Nat Rev Genet, 21, 630, 10.1038/s41576-020-0258-4 · DOI · Paper page
  9. 2020, Mitochondrial Substrate Utilization Regulates Cardiomyocyte Cell Cycle Progression, Nat Metabolism, 2, 167, 10.1038/s42255-020-0169-x · DOI
  10. 2022, MNK2-eIF4E axis promotes cardiac repair in the infarcted mouse heart by activating cyclin D1, J Mol Cell Cardiol, 166, 91, 10.1016/j.yjmcc.2022.02.006 · DOI
  11. 2017, Poly(A) tail length regulates PABPC1 expression to tune translation in the heart, Elife, 6, 568
  12. 2019, Nuclear eIF4E Stimulates 3’-End Cleavage of Target RNAs, Cell Reports, 27, 1408
  13. 10.1038/415096a · DOI · Paper page
  14. 2018, Ribosome Stoichiometry: From Form to Function, Trends Biochem Sci, 44, 95
  15. Fang, Y. , Gupta, V. , Karra, R. , Holdway, J. E. , Kikuchi, K. and Poss, K. D . (2013). Translational profiling of cardiomyocytes identifies an early Jak1/Stat3 injury response required for zebrafish heart regeneration. Proc National Acad Sci 110, 13416 13421. · DOI
  16. 2020, Stimulation of glycolysis promotes cardiomyocyte proliferation after injury in adult zebrafish, Embo Rep, 21, e49752, 10.15252/embr.201949752 · DOI
  17. 2018, Heterogeneity and specialized functions of translation machinery: from genes to organisms, Nat Rev Genet, 19, 452
  18. 2017, Resolving Heart Regeneration by Replacement Histone Profiling, Dev Cell, 40, 404
  19. 10.1172/JCI32044 · DOI
  20. 10.1016/j.molcel.2016.09.020 · DOI
  21. 2013, Identification of the zebrafish maternal and paternal transcriptomes, Dev Camb Engl, 140, 2703
  22. Heinkele, F. J. , Lou, B. , Erben, V. , Bennewitz, K. , Poschet, G. , Sticht, C. and Kroll, J. (2021). Metabolic and Transcriptional Adaptations Improve Physical Performance of Zebrafish. Antioxidants Basel Switz 10, 1581. · DOI
  23. 10.1126/science.aat7113 · DOI
  24. 10.1126/science.aat0778 · DOI
  25. 2018, Single-cell analysis uncovers that metabolic reprogramming by ErbB2 signaling is essential for cardiomyocyte proliferation in the regenerating heart, Elife, 8, e50163
  26. 10.1371/journal.pone.0149277 · DOI
  27. 2022, Origin and function of activated fibroblast states during zebrafish heart regeneration, Nat Genet, 54, 1227, 10.1038/s41588-022-01129-5 · DOI
  28. 10.1038/nprot.2008.211 · DOI · Paper page
  29. 10.1038/nprot.2012.086 · DOI
  30. 10.1186/1471-2148-5-48 · DOI
  31. 2016, Modulation of tissue repair by regeneration enhancer elements, Nature, 532, 206
  32. 10.1126/science.1106042 · DOI
  33. 2011, Retinoic acid production by endocardium and epicardium is an injury response essential for zebrafish heart regeneration, Dev Cell, 20, 404
  34. 10.1038/nrg3184 · DOI
  35. 2015, Distinct Features of Cap Binding by eIF4E1b Proteins, J Mol Biol, 427, 387, 10.1016/j.jmb.2014.11.009 · DOI
  36. 2021, Regulation of gene expression via translational buffering, Biochimica Et Biophysica Acta Bba - Mol Cell Res, 1869, 119140
  37. 10.7554/eLife.25605 · DOI
  38. 10.1371/journal.pcbi.1003118 · DOI
  39. 10.1186/s13059-020-1948-0 · DOI
  40. 2006, A dynamic epicardial injury response supports progenitor cell activity during zebrafish heart regeneration, Cell, 127, 619
  41. 2017, The rises and falls of opsin genes in 59 ray-finned fish genomes and their implications for environmental adaptation, Sci Rep-uk, 7, 15568, 10.1038/s41598-017-15868-7 · DOI
  42. 2019, Translational offsetting as a mode of estrogen receptor α-dependent regulation of gene expression, Embo J, 38, e101323, 10.15252/embj.2018101323 · DOI · Paper page
  43. 10.1186/s13059-014-0550-8 · DOI · Paper page
  44. 2018, Dynamics of Zebrafish Heart Regeneration Using an HPLC–ESI–MS/MS Approach, J Proteome Res, 17, 1308
  45. 2021, Amino acid primed mTOR activity is essential for heart regeneration, Iscience, 25, 103574
  46. 10.1093/molbev/msaa015 · DOI · Paper page
  47. 10.1074/jbc.M704629200 · DOI
  48. 10.1126/science.aaf6056 · DOI
  49. 10.1006/excr.1996.0078 · DOI
  50. 2019, High-Phosphate Diet Induces Exercise Intolerance and Impairs Fatty Acid Metabolism in Mice, Circulation, 139, 1422, 10.1161/CIRCULATIONAHA.118.037550 · DOI
  51. 10.1074/jbc.M113.472290 · DOI
  52. Popa, A. , Lebrigand, K. , Paquet, A. , Nottet, N. , Robbe-Sermesant, K. , Waldmann, R. and Barbry, P. (2016). RiboProfiling: a Bioconductor package for standard Ribo-seq pipeline processing. F1000research 5, 1309. · DOI
  53. 2002, Heart regeneration in zebrafish, Science, 298, 2190
  54. 2021, In vivo proximity labeling identifies cardiomyocyte protein networks during zebrafish heart regeneration, Elife, 10, e66079, 10.7554/eLife.66079 · DOI
  55. 10.1074/jbc.M313688200 · DOI
  56. 2013, Cardiomyocyte FGF signaling is required for Cx43 phosphorylation and cardiac gap junction maintenance, Exp Cell Res, 319, 2152, 10.1016/j.yexcr.2013.05.022 · DOI
  57. 2022, Myostatin is a negative regulator of adult neurogenesis after spinal cord injury in zebrafish, Cell Reports, 41, 111705, 10.1016/j.celrep.2022.111705 · DOI
  58. 2021, Assessing eukaryotic initiation factor 4F subunit essentiality by CRISPR-induced gene ablation in the mouse, Cell Mol Life Sci, 78, 6709, 10.1007/s00018-021-03940-5 · DOI · Paper page
  59. 10.1093/NAR/GKAC194 · DOI
  60. 2014, Development and application of MIPARTM: a novel software package for two-and three-dimensional microstructural characterization, Integrating Mater Manuf Innovation, 3, 123, 10.1186/2193-9772-3-10 · DOI
  61. 2018, Heart Regeneration in the Mexican Cavefish, Cell Reports, 25, 2007
  62. 10.1016/j.cell.2019.05.031 · DOI · Paper page
  63. 10.1073/pnas.0710018105 · DOI
  64. 2022, Enhancer selection dictates gene expression responses in remote organs during tissue regeneration, Nat Cell Biol, 24, 685, 10.1038/s41556-022-00906-y · DOI
  65. 10.1038/nature05603 · DOI · Paper page
  66. 2021, The FGF- AKT pathway is necessary for cardiomyocyte survival for heart regeneration in zebrafish, Dev Biol, 472, 30, 10.1016/j.ydbio.2020.12.019 · DOI
  67. 2001, Comparative genomics provides evidence for an ancient genome duplication event in fish, Philosophical Transactions Royal Soc Lond Ser B Biological Sci, 356, 1661, 10.1098/rstb.2001.0975 · DOI
  68. Thompson, J. D. , Ou, J. , Lee, N. , Shin, K. , Cigliola, V. , Song, L. , Crawford, G. E. , Kang, J. and Poss, K. D . (2020). Identification and requirements of enhancers that direct gene expression during zebrafish fin regeneration. Development 147, dev191262. · DOI
  69. 10.1093/nar/gkw256 · DOI
  70. 2015, Differential Requirements for eIF4E Dose in Normal Development and Cancer, Cell, 162, 71
  71. 2011, The regenerative capacity of zebrafish reverses cardiac failure caused by genetic cardiomyocyte depletion, Development, 138, 3430
  72. 10.1038/s41586-020-2899-z · DOI
  73. 10.1126/science.aaz3090 · DOI · Paper page
  74. 10.7554/eLife.30860 · DOI
  75. 10.1016/j.devcel.2015.12.010 · DOI
  76. You, X. , Bian, C. , Zan, Q. , Xu, X. , Liu, X. , Chen, J. , Wang, J. , Qiu, Y. , Li, W. , Zhang, X. , et al. (2014). Mudskipper genomes provide insights into the terrestrial adaptation of amphibious fishes. Nat Commun 5, 5594. · DOI
  77. 2018, A comparative genomics study of carbohydrate/glucose metabolic genes: from fish to mammals, Bmc Genomics, 19, 246, 10.1186/s12864-018-4647-4 · DOI

Metadata

Authors
Rao, A., Lyu, B., Jahan, I., Lubertozzi, A., Zhou, G., Tedeschi, F., Jankowsky, E., Kang, J., Carstens, B., Poss, K., 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)
Corresponding author
Goldman, Joseph Aaron
ORCID
Venue
Development
Publisher
openRxiv
Published
2022-08-15
Volume
150
Issue
20
ISSN
0950-1991 (ISSN-L)
DOI
10.1101/2022.08.15.502524
PMC
PMC10281269
OpenAlex
W4377940467
Cited by
13
References
1
Citations by year
2026: 4 · 2025: 5 · 2024: 3 · 2023: 1
FWCI
1.15
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Development (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
Funders
  • American Heart Association (17SDG33660922)
  • Ohio State University
  • National Institutes of Health (1s10od026842-01)
  • National Heart, Lung, and Blood Institute (R35HL150713, R01HL151522)
  • National Institute of General Medical Sciences (R35GM118088, R35GM137878)
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

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