CoChat
Sign Up
PreprintCited by 21Pluripotent Stem Cells ResearchRNA and protein synthesis mechanismsDevelopmental Biology and Gene Regulation

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

RSL24D1 sustains steady-state ribosome biogenesis and pluripotency translational programs in embryonic stem cells

Open access
Durand, Sébastien, Bruelle, Marion, Bourdelais, Fleur, Bennychen, Bigitha, Blin-Gonthier, Juliana, Isaac, Caroline, Huyghe, Aurélia, Seyve, Antoine, Vanbelle, Christophe, Meyronet, David, Catez, Frédéric, Diaz, Jean-Jacques, Lavial, Fabrice, Ricci, Emiliano P., Ducray, François, Gabut, Mathieu·2021·Nature Communications
DOI 10.1101/2021.05.27.443845PMC PMC9870888

Preprint — published as 10.1038/s41467-023-36037-7 · Paper page

Open this paper in CoChat — free accountOpen PDF

Abstract

Embryonic stem cell (ESC) fate decisions are regulated by a complex molecular circuitry that requires tight and coordinated gene expression regulations at multiple levels from chromatin organization to mRNA processing. Recently, ribosome biogenesis and translation have emerged as key regulatory pathways that efficiently control stem cell homeostasis. However, the molecular mechanisms underlying the regulation of these pathways remain largely unknown to date. Here, we analyzed the expression, in mouse ESCs, of over 300 genes involved in ribosome biogenesis and we identified RSL24D1 as the most differentially expressed between self-renewing and differentiated ESCs. RSL24D1 is highly expressed in multiple mouse pluripotent stem cell models and its expression profile is conserved in human ESCs. RSL24D1 is associated with nuclear pre-ribosomes and is required for the maturation and the synthesis of 60S subunits in mouse ESCs. Interestingly, RSL24D1 depletion significantly impairs global translation, particularly of key pluripotency factors, including POU5F1 and NANOG, as well as components of the polycomb repressive complex 2 (PRC2). Consistently, RSL24D1 is required for mouse ESC self-renewal and proliferation. Taken together, we show that RSL24D1-dependant ribosome biogenesis is required to both sustain the expression of pluripotent transcriptional programs and silence developmental programs, which concertedly dictate ESC homeostasis.

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.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1101/2021.05.27.443845

Cites

1 of 1 references verified0 citation errors · 0 not checkable

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.

A few free checks a day · papers already verified open instantly · results are public

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

Flagged first, then by citations

Research works printed but not linked: 91

  1. Gokbuget D , Blelloch R. Epigenetic control of transcriptional regulation in pluripotency and early differentiation. Development. 2019;146(19). · DOI
  2. 10.1016/j.stem.2015.09.011 · DOI · Paper page
  3. 10.1016/j.cell.2011.01.032 · DOI
  4. 10.1016/j.cell.2011.08.023 · DOI
  5. 2020, The epitranscriptome in stem cell biology and neural development, Neurobiol Dis, 146, 105139, 10.1016/j.nbd.2020.105139 · DOI
  6. 10.1101/gad.316984.118 · DOI
  7. 2017, PRC2 Facilitates the Regulatory Topology Required for Poised Enhancer Function during Pluripotent Stem Cell Differentiation, Cell Stem Cell, 20, 689, 10.1016/j.stem.2017.02.004 · DOI · Paper page
  8. 10.1038/s41467-019-09624-w · DOI
  9. 2016, Roles of H3K27me2 and H3K27me3 Examined during Fate Specification of Embryonic Stem Cells, Cell reports, 17, 1369, 10.1016/j.celrep.2016.09.087 · DOI
  10. 10.1039/B908315D · DOI · Paper page
  11. 10.1038/msb.2013.47 · DOI · Paper page
  12. 10.1038/nature08575 · DOI
  13. 10.1016/j.febslet.2009.10.036 · DOI · Paper page
  14. 10.1038/msb.2011.84 · DOI
  15. Gabut M , Bourdelais F , Durand S. Ribosome and Translational Control in Stem Cells. Cells. 2020;9(2). · DOI
  16. 10.1016/j.stem.2008.03.013 · DOI · Paper page
  17. 10.1038/nature13035 · DOI · Paper page
  18. 10.1073/pnas.1418845112 · DOI
  19. 10.1016/j.stem.2018.02.004 · DOI · Paper page
  20. 10.1016/j.stem.2018.03.002 · DOI
  21. 10.1007/s00294-017-0764-x · DOI
  22. 10.1038/s41580-018-0078-y · DOI
  23. 10.1038/nsmb.3454 · DOI
  24. 2016, The Regulation of rRNA Gene Transcription during Directed Differentiation of Human Embryonic Stem Cells, PLoS One, 11, e0157276, 10.1371/journal.pone.0157276 · DOI
  25. 2018, NoRC Recruitment by H2A.X Deposition at rRNA Gene Promoter Limits Embryonic Stem Cell Proliferation, Cell reports, 23, 1853, 10.1016/j.celrep.2018.04.023 · DOI
  26. 10.1038/nsmb.2638 · DOI
  27. 10.1074/jbc.M111.225185 · DOI
  28. Fong YW , Ho JJ , Inouye C , Tjian R. The dyskerin ribonucleoprotein complex as an OCT4/SOX2 coactivator in embryonic stem cells. Elife. 2014;3. · DOI
  29. 10.1002/stem.1825 · DOI
  30. 10.1101/gad.267112.115 · DOI
  31. Gayraud-Morel B , Le Bouteiller M , Commere PH , Cohen-Tannoudji M , Tajbakhsh S. Notchless defines a stage-specific requirement for ribosome biogenesis during lineage progression in adult skeletal myogenesis. Development. 2018;145(23). · DOI
  32. 10.1084/jem.20122019 · DOI
  33. 10.1038/cdd.2015.57 · DOI
  34. 10.1128/MCB.26.9.3541-3549.2006 · DOI
  35. 10.1038/nature12270 · DOI
  36. 10.1038/ncomms8398 · DOI
  37. 10.1016/j.cell.2012.08.023 · DOI · Paper page
  38. 10.1371/journal.pone.0095304 · DOI
  39. 10.1016/j.molcel.2019.01.042 · DOI
  40. 2015, Reinforcement of STAT3 activity reprogrammes human embryonic stem cells to naive-like pluripotency, Nat Commun, 6, 7095, 10.1038/ncomms8095 · DOI
  41. 10.1128/MCB.23.13.4449-4460.2003 · DOI
  42. 10.1038/nature26156 · DOI
  43. 10.1038/nature17942 · DOI
  44. 10.1038/s41467-019-08880-0 · DOI
  45. 10.1038/s41467-020-17237-x · DOI
  46. 2020, The GAR domain integrates functions that are necessary for the proper localization of fibrillarin (FBL) inside eukaryotic cells, PeerJ, 8, e9029, 10.7717/peerj.9029 · DOI
  47. 10.1007/s00018-019-03231-0 · DOI
  48. 10.1038/nature15515 · DOI
  49. 10.1146/annurev-cellbio-100913-013116 · DOI
  50. 10.1093/nar/gkv529 · DOI
  51. Oki S , Ohta T , Shioi G , Hatanaka H , Ogasawara O , Okuda Y , et al. ChIP-Atlas: a data-mining suite powered by full integration of public ChIP-seq data. EMBO Rep. 2018;19(12). · DOI · Paper page
  52. 10.1155/2015/628368 · DOI
  53. 2002, Embryonic stem cells as a model to study cardiac, skeletal muscle, and vascular smooth muscle cell differentiation, Methods Mol Biol, 185, 127
  54. 10.1016/j.devcel.2013.05.004 · DOI
  55. 10.1016/j.stem.2015.03.008 · DOI
  56. 10.1038/ncb2742 · DOI
  57. 10.1089/scd.2013.0470 · DOI
  58. 2010, The nucleolus: structure/function relationship in RNA metabolism, Wiley interdisciplinary reviews RNA, 1, 415, 10.1002/wrna.39 · DOI
  59. 10.1016/j.cell.2017.11.039 · DOI
  60. 10.1261/rna.069799.118 · DOI
  61. 10.1083/jcb.201205021 · DOI
  62. 10.1016/j.molcel.2010.06.018 · DOI
  63. 10.1128/MCB.00668-07 · DOI
  64. 10.1016/j.molcel.2013.08.011 · DOI
  65. 10.1093/nar/gks609 · DOI
  66. 10.1038/nsmb.3112 · DOI
  67. Gregory B , Rahman N , Bommakanti A , Shamsuzzaman M , Thapa M , Lescure A , et al. The small and large ribosomal subunits depend on each other for stability and accumulation. Life Sci Alliance. 2019;2(2). · DOI
  68. 10.1101/gad.2.2.160 · DOI
  69. 10.1128/MCB.23.2.699-707.2003 · DOI
  70. 2021, A PRC2-independent function for EZH2 in regulating rRNA 2’-O methylation and IRES-dependent translation, Nature cell biology, 23, 341, 10.1038/s41556-021-00653-6 · DOI
  71. Mills EW , Green R. Ribosomopathies: There’s strength in numbers. Science. 2017;358(6363). · DOI
  72. 10.1016/j.cell.2011.10.002 · DOI · Paper page
  73. 2015, Embryonic Stem Cell Growth Factors Regulate eIF2alpha Phosphorylation, PLoS One, 10, e0139076, 10.1371/journal.pone.0139076 · DOI
  74. 10.1038/nmeth.1436 · DOI
  75. 1985, The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium, J Embryol Exp Morphol, 87, 27
  76. 1992, Embryonic stem cells as a model for cardiogenesis, Trends Cardiovasc Med, 2, 44, 10.1016/1050-1738(92)90003-B · DOI
  77. 10.1016/j.cell.2006.01.040 · DOI
  78. 10.1073/pnas.0802655105 · DOI
  79. 10.4161/cc.8.3.7701 · DOI
  80. 10.1186/s12859-017-1934-z · DOI
  81. 2019, The EMBL-EBI search and sequence analysis tools APIs in 2019, Nucleic Acids Res, 47, W636, 10.1093/nar/gkz268 · DOI · Paper page
  82. 10.1093/bioinformatics/btp033 · DOI
  83. 2017, Modeling protein quaternary structure of homo-and hetero-oligomers beyond binary interactions by homology, Scientific reports, 7, 10480, 10.1038/s41598-017-09654-8 · DOI
  84. 10.1093/nar/gkw1132 · DOI
  85. 10.1002/elps.200900140 · DOI
  86. 2018, SWISS-MODEL: homology modelling of protein structures and complexes, Nucleic Acids Res, 46, pW296, 10.1093/nar/gky427 · DOI
  87. 10.1093/bioinformatics/bts356 · DOI
  88. 2015, Differential analyses for RNA-seq: transcript-level estimates improve gene-level inferences, F1000Res, 4, 1521, 10.12688/f1000research.7563.1 · DOI · Paper page
  89. 10.1186/s13059-014-0550-8 · DOI · Paper page
  90. 10.1093/bioinformatics/bti551 · DOI
  91. 10.1101/gr.1239303 · DOI · Paper page

Metadata

Authors
Durand, S., Bruelle, M., Bourdelais, F., Bennychen, B., Blin-Gonthier, J., Isaac, C., Huyghe, A., Seyve, A., Vanbelle, C., Meyronet, D., Catez, F., Diaz, J.-J., Lavial, F., Ricci, E. P., Ducray, F., & Gabut, M.
Affiliations
  • Lyon 1 Université (FR)
  • University of Ottawa (CA)
  • École Normale Supérieure de Lyon (FR)
Corresponding author
Gabut, Mathieu
ORCID
Venue
Nature Communications
Publisher
openRxiv
Published
2021-05-29
Volume
14
Issue
1
Pages
356-356
ISSN
2041-1723 (ISSN-L)
DOI
10.1101/2021.05.27.443845
PMC
PMC9870888
OpenAlex
W4317718280
Cited by
21
References
1
Citations by year
2026: 4 · 2025: 5 · 2024: 7 · 2023: 3 · 2022: 2
FWCI
1.69
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Nature Communications (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
  • Research Square (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, cc-by)
  • NPARC (submittedVersion, cc-by)
  • RePEc: Research Papers in Economics (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • European Commission (631794, ANR-17-EURE-0003)
  • Agence Nationale de la Recherche (ANR-10-INBS-08, ANR-17-EURE-0003, ANR-17-EURE-, Proteomics French Infrastructure,ANR-10-INBS-08, ANR-17, ANR-10, ANR-17-CONV-0002)
  • Institut National de la Santé et de la Recherche Médicale
  • University of Toronto
  • Ligue Contre le Cancer
  • Institut National Du Cancer
  • Samsung Biomedical Research Institute
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA and protein synthesis mechanisms
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
Keywords
ribosome biogenesis, embryonic stem cells, pluripotency, translation (biology), 60S ribosomal subunit, polycomb repressive complex 2, self-renewal, lineage commitment, stem cell fate, pluripotency factors
MeSH terms
Animals, Cell Differentiation, Humans, Pluripotent Stem Cells, Mice, Embryonic Stem Cells, Polycomb Repressive Complex 2

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