CoChat
Sign Up
Cited by 20Developmental Biology and Gene RegulationReproductive Biology and FertilityRNA Research and Splicing

The DOI matches its Crossref record; 5 of the 5 references it cites were found in a registry or an index.

EXOSC10/Rrp6 is essential for the eight-cell embryo/morula transition

Open access
Petit, Fabrice G., Jamin, Soazik P., Kernanec, Pierre-Yves, Becker, Emmanuelle, Halet, Guillaume, Primig, Michael·2022·Developmental Biology
DOI 10.1016/j.ydbio.2021.12.010

Published version of a preprint

Open this paper in CoChat — free accountOpen PDF

Abstract

The conserved 3'-5' exoribonuclease EXOSC10/Rrp6 is required for gametogenesis, brain development, erythropoiesis and blood cell enhancer function. The human ortholog is essential for mitosis in cultured cancer cells. Little is known, however, about the role of Exosc10 during embryo development and organogenesis. We generated an Exosc10 knockout model and find that Exosc10-/- mice show an embryonic lethal phenotype. We demonstrate that Exosc10 maternal wild type mRNA is present in mutant oocytes and that the gene is expressed during all stages of early embryogenesis. Furthermore, we observe that EXOSC10 early on localizes to the periphery of nucleolus precursor bodies in blastomeres, which is in keeping with the protein's role in rRNA processing and may indicate a function in the establishment of chromatin domains during initial stages of embryogenesis. Finally, we infer from genotyping data for embryonic days e7.5, e6.5 and e4.5 and embryos cultured in vitro that Exosc10-/- mutants arrest at the eight-cell embryo/morula transition. Our results demonstrate a novel essential role for Exosc10 during early embryogenesis, and they are consistent with earlier work showing that impaired ribosome biogenesis causes a developmental arrest at the morula stage.

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 · 10.1016/j.ydbio.2021.12.010

Cites

5 of 5 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

Research works printed but not linked: 58

  1. Abou Elela, 1997, Role of the 5.8S rRNA in ribosome translocation, Nucleic Acids Res., 25, 1788, 10.1093/nar/25.9.1788 · DOI
  2. Baran, 2001, Nopp 140 involvement in nucleologenesis of mouse preimplantation embryos, Mol. Reprod. Dev., 59, 277, 10.1002/mrd.1032 · DOI
  3. Bluthner, 1992, Cloning and characterization of the cDNA coding for a polymyositis-scleroderma overlap syndrome-related nucleolar 100-kD protein, J. Exp. Med., 176, 973, 10.1084/jem.176.4.973 · DOI
  4. Briggs, 1998, Rrp6p, the yeast homologue of the human PM-Scl 100-kDa autoantigen, is essential for efficient 5.8 S rRNA 3' end formation, J. Biol. Chem., 273, 13255, 10.1074/jbc.273.21.13255 · DOI
  5. Burger, 2010, Chemotherapeutic drugs inhibit ribosome biogenesis at various levels, J. Biol. Chem., 285, 12416, 10.1074/jbc.M109.074211 · DOI
  6. Chazaud, 2016, Lineage specification in the mouse preimplantation embryo, Development, 143, 1063, 10.1242/dev.128314 · DOI · Paper page
  7. Chen, 2008, Early pre-implantation lethality in mice carrying truncated mutation in the RNA polymerase 1-2 gene, Biochem. Biophys. Res. Commun., 365, 636, 10.1016/j.bbrc.2007.11.019 · DOI
  8. Chen, 2019, Genome organization around nuclear speckles, Curr. Opin. Genet. Dev., 55, 91, 10.1016/j.gde.2019.06.008 · DOI
  9. Clift, 2013, Restarting life: fertilization and the transition from meiosis to mitosis, Nat. Rev. Mol. Cell Biol., 14, 549, 10.1038/nrm3643 · DOI
  10. Davidson, 2019, Rapid depletion of DIS3, EXOSC10, or XRN2 reveals the immediate impact of exoribonucleolysis on nuclear RNA metabolism and transcriptional control, Cell Rep., 26, 2779, 10.1016/j.celrep.2019.02.012 · DOI
  11. Domingo-Prim, 2019, EXOSC10 is required for RPA assembly and controlled DNA end resection at DNA double-strand breaks, Nat. Commun., 10, 2135, 10.1038/s41467-019-10153-9 · DOI
  12. Eberle, 2015, An interaction between RRP6 and SU(VAR)3-9 targets RRP6 to heterochromatin and contributes to heterochromatin maintenance in Drosophila melanogaster, PLoS Genet., 11, 10.1371/journal.pgen.1005523 · DOI
  13. Fang, 2004, 5-fluorouracil enhances exosome-dependent accumulation of polyadenylated rRNAs, Mol. Cell Biol., 24, 10766, 10.1128/MCB.24.24.10766-10776.2004 · DOI
  14. Fei, 2017, Quantitative analysis of multilayer organization of proteins and RNA in nuclear speckles at super resolution, J. Cell Sci., 130, 4180, 10.1242/jcs.206854 · DOI
  15. Fulka, 2016, Nucleolus precursor bodies and ribosome biogenesis in early mammalian embryos: old theories and new discoveries, Biol. Reprod., 94, 143, 10.1095/biolreprod.115.136093 · DOI
  16. Ge, 1992, Cloning of a complementary DNA coding for the 100-kD antigenic protein of the PM-Scl autoantigen, J. Clin. Invest., 90, 559, 10.1172/JCI115895 · DOI
  17. Gudipati, 2012, Extensive degradation of RNA precursors by the exosome in wild-type cells, Mol. Cell., 48, 409, 10.1016/j.molcel.2012.08.018 · DOI · Paper page
  18. Hamdane, 2017, Disruption of the UBF gene induces aberrant somatic nucleolar bodies and disrupts embryo nucleolar precursor bodies, Gene, 612, 5, 10.1016/j.gene.2016.09.013 · DOI
  19. Hoskins, 2007, Evidence for distinct DNA- and RNA-based mechanisms of 5-fluorouracil cytotoxicity in Saccharomyces cerevisiae, Yeast, 24, 861, 10.1002/yea.1516 · DOI
  20. Jamin, 2017, EXOSC10/Rrp6 is post-translationally regulated in male germ cells and controls the onset of spermatogenesis, Sci. Rep., 7, 15065, 10.1038/s41598-017-14643-y · DOI
  21. Jukam, 2017, Zygotic genome activation in vertebrates, Dev. Cell, 42, 316, 10.1016/j.devcel.2017.07.026 · DOI
  22. Kammler, 2008, The RNA exosome component hRrp6 is a target for 5-fluorouracil in human cells, Mol. Cancer Res., 6, 990, 10.1158/1541-7786.MCR-07-2217 · DOI
  23. Kent, 2009, The 5' external transcribed spacer in mouse ribosomal RNA contains two cleavage sites, RNA, 15, 14, 10.1261/rna.1384709 · DOI
  24. Kilchert, 2016, The regulation and functions of the nuclear RNA exosome complex, Nat. Rev. Mol. Cell Biol., 17, 227, 10.1038/nrm.2015.15 · DOI
  25. Knight, 2016, Cooling-induced SUMOylation of EXOSC10 down-regulates ribosome biogenesis, RNA, 22, 623, 10.1261/rna.054411.115 · DOI
  26. Kobylecki, 2018, Elimination of 01/A'-A0 pre-rRNA processing by-product in human cells involves cooperative action of two nuclear exosome-associated nucleases: RRP6 and DIS3, RNA, 24, 1677, 10.1261/rna.066589.118 · DOI
  27. Kone, 2016, Three-dimensional distribution of UBF and Nopp140 in relationship to ribosomal DNA transcription during mouse preimplantation development, Biol. Reprod., 94, 95, 10.1095/biolreprod.115.136366 · DOI
  28. Kresoja-Rakic, 2019, Nucleolus and rRNA gene chromatin in early embryo development, Trends Genet., 35, 868, 10.1016/j.tig.2019.06.005 · DOI
  29. Kuai, 2005, A nuclear degradation pathway controls the abundance of normal mRNAs in Saccharomyces cerevisiae, Proc. Natl. Acad. Sci. U.S.A., 102, 13962, 10.1073/pnas.0506518102 · DOI
  30. Laffleur, 2021, Noncoding RNA processing by DIS3 regulates chromosomal architecture and somatic hypermutation in B cells, Nat. Genet., 53, 230, 10.1038/s41588-020-00772-0 · DOI
  31. Lafontaine, 2021, The nucleolus as a multiphase liquid condensate, Nat. Rev. Mol. Cell Biol., 22, 165, 10.1038/s41580-020-0272-6 · DOI
  32. Lardenois, 2011, Execution of the meiotic noncoding RNA expression program and the onset of gametogenesis in yeast require the conserved exosome subunit Rrp6, Proc. Natl. Acad. Sci. U.S.A., 108, 1058, 10.1073/pnas.1016459108 · DOI
  33. Lerch-Gaggl, 2002, Pescadillo is essential for nucleolar assembly, ribosome biogenesis, and mammalian cell proliferation, J. Biol. Chem., 277, 45347, 10.1074/jbc.M208338200 · DOI
  34. Li, 2010, Maternal control of early mouse development, Development, 137, 859, 10.1242/dev.039487 · DOI
  35. Mahler, 2007, Novel aspects of autoantibodies to the PM/Scl complex: clinical, genetic and diagnostic insights, Autoimmun. Rev., 6, 432, 10.1016/j.autrev.2007.01.013 · DOI
  36. Makino, 2013, Crystal structure of an RNA-bound 11-subunit eukaryotic exosome complex, Nature, 495, 70, 10.1038/nature11870 · DOI
  37. Marin-Vicente, 2015, RRP6/EXOSC10 is required for the repair of DNA double-strand breaks by homologous recombination, J. Cell Sci., 128, 1097
  38. Mehta, 2021, RNA-regulatory exosome complex confers cellular survival to promote erythropoiesis, Nucleic Acids Res., 49, 9007, 10.1093/nar/gkab367 · DOI
  39. Meldal, 2015, The complex portal--an encyclopaedia of macromolecular complexes, Nucleic Acids Res., 43, D479, 10.1093/nar/gku975 · DOI
  40. Midtgaard, 2006, Structure of the nuclear exosome component Rrp6p reveals an interplay between the active site and the HRDC domain, Proc. Natl. Acad. Sci. U.S.A., 103, 11898, 10.1073/pnas.0604731103 · DOI
  41. Neil, 2009, Widespread bidirectional promoters are the major source of cryptic transcripts in yeast, Nature, 457, 1038, 10.1038/nature07747 · DOI
  42. Pefanis, 2015, RNA exosome-regulated long non-coding RNA transcription controls super-enhancer activity, Cell, 161, 774, 10.1016/j.cell.2015.04.034 · DOI · Paper page
  43. Pisani, 2019, Nuclear paraspeckles function in mediating gene regulatory and apoptotic pathways, Noncoding RNA Res, 4, 128, 10.1016/j.ncrna.2019.11.002 · DOI
  44. Scavizzi, 2015, Blastocyst genotyping for quality control of mouse mutant archives: an ethical and economical approach, Transgenic Res., 24, 921, 10.1007/s11248-015-9897-1 · DOI
  45. Schneider, 2012, Transcriptome-wide analysis of exosome targets, Mol. Cell., 48, 422, 10.1016/j.molcel.2012.08.013 · DOI · Paper page
  46. Schulz, 2019, Mechanisms regulating zygotic genome activation, Nat. Rev. Genet., 20, 221, 10.1038/s41576-018-0087-x · DOI
  47. Silverstein, 2011, The incorporation of 5-fluorouracil into RNA affects the ribonucleolytic activity of the exosome subunit Rrp6, Mol. Cancer Res., 9, 332, 10.1158/1541-7786.MCR-10-0084 · DOI
  48. Stuparevic, 2021, Regulation of the conserved 3’-5’ exoribonuclease EXOSC10/Rrp6 during cell division, development and cancer, Biol. Rev. Camb. Phil. Soc., 96, 1092, 10.1111/brv.12693 · DOI
  49. Testa, 2004, A reliable lacZ expression reporter cassette for multipurpose, knockout-first alleles, Genesis, 38, 151, 10.1002/gene.20012 · DOI
  50. Ulmke, 2021, Post-transcriptional regulation by the exosome complex is required for cell survival and forebrain development via repression of P53 signaling, Development, 148, dev188276, 10.1242/dev.188276 · DOI
  51. Wagschal, 2012, Microprocessor, Setx, Xrn2, and Rrp6 co-operate to induce premature termination of transcription by RNAPII, Cell, 150, 1147, 10.1016/j.cell.2012.08.004 · DOI
  52. Wasmuth, 2014, Structure of an Rrp6-RNA exosome complex bound to poly(A) RNA, Nature, 511, 435, 10.1038/nature13406 · DOI
  53. Wasmuth, 2017, The Rrp6 C-terminal domain binds RNA and activates the nuclear RNA exosome, Nucleic Acids Res., 45, 846, 10.1093/nar/gkw1152 · DOI
  54. Wu, 2020, EXOSC10 sculpts the transcriptome during the growth-to-maturation transition in mouse oocytes, Nucleic Acids Res., 48, 5349, 10.1093/nar/gkaa249 · DOI
  55. Xu, 2009, Bidirectional promoters generate pervasive transcription in yeast, Nature, 457, 1033, 10.1038/nature07728 · DOI
  56. Zatsepina, 2003, The step-wise assembly of a functional nucleolus in preimplantation mouse embryos involves the cajal (coiled) body, Dev. Biol., 253, 66, 10.1006/dbio.2002.0865 · DOI
  57. Zernicka-Goetz, 2009, Making a firm decision: multifaceted regulation of cell fate in the early mouse embryo, Nat. Rev. Genet., 10, 467, 10.1038/nrg2564 · DOI
  58. Zhang, 2015, Maternal control of early embryogenesis in mammals, Reprod. Fertil. Dev., 27, 880, 10.1071/RD14441 · DOI

Metadata

Authors
Petit, F. G., Jamin, S. P., Kernanec, P.-Y., Becker, E., Halet, G., & Primig, M.
Affiliations
  • Inserm (FR)
  • Centre National de la Recherche Scientifique (FR)
Corresponding author
  • Petit, Fabrice G.
  • Primig, Michael
ORCID
Venue
Developmental Biology
Publisher
Elsevier BV
Published
2022-03
Volume
483
Pages
58-65
ISSN
0012-1606 (ISSN-L)
DOI
10.1016/j.ydbio.2021.12.010
OpenAlex
W4220880976
Cited by
20
References
5
Citations by year
2026: 6 · 2025: 6 · 2024: 2 · 2023: 5 · 2022: 1
FWCI
0.63
Type
journal article
Language
en
Open access
Licence
Locations
  • Developmental Biology (publishedVersion)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • HAL (submittedVersion, other-oa)
Funders
  • National Institutes of Health
  • Institut National de la Santé et de la Recherche Médicale
  • Ligue Nationale Contre Le Cancer
  • École des Hautes Études en Santé Publique
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Health Sciences › Medicine › Reproductive Medicine › Reproductive Biology and Fertility
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › RNA Research and Splicing
Keywords
Rrp6, 3'-5' exoribonuclease, early embryonic development, embryonic lethality, knockout mice, ribosome biogenesis, rRNA processing, maternal mRNA, chromatin domains, blastomeres
MeSH terms
Animals, Blastocyst, Blastomeres, Cell Nucleolus, Exoribonucleases, Female, Male, Morula, Oocytes, Phenotype, Ribosomes, RNA Processing, Post-Transcriptional, RNA, Ribosomal, Signal Transduction, Mice, Knockout, Gene Expression Regulation, Developmental, Embryonic Development, Mice, Exosome Multienzyme Ribonuclease Complex

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