Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast

Abstract

Production of healthy gametes in meiosis relies on the quality control and proper distribution of both nuclear and cytoplasmic contents. Meiotic differentiation naturally eliminates age-induced cellular damage by an unknown mechanism. Using time-lapse fluorescence microscopy in budding yeast, we found that nuclear senescence factors - including protein aggregates, extrachromosomal ribosomal DNA circles, and abnormal nucleolar material - are sequestered away from chromosomes during meiosis II and subsequently eliminated. A similar sequestration and elimination process occurs for the core subunits of the nuclear pore complex in both young and aged cells. Nuclear envelope remodeling drives the formation of a membranous compartment containing the sequestered material. Importantly, de novo generation of plasma membrane is required for the sequestration event, preventing the inheritance of long-lived nucleoporins and senescence factors into the newly formed gametes. Our study uncovers a new mechanism of nuclear quality control and provides insight into its function in meiotic cellular rejuvenation.

Data availability

Data generated or analyzed during this study are included in the manuscript and supporting files. All imaging data used for analysis will be uploaded to the Image Data Resource repository.

Article and author information

Author details

  1. Grant A King

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  2. Jay S Goodman

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  3. Jennifer G Schick

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  4. Keerthana Chetlapalli

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  5. Danielle M Jorgens

    Electron Microscope Lab, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  6. Kent L McDonald

    Electron Microscope Lab, University of California, Berkeley, Berkeley, United States
    Competing interests
    No competing interests declared.
  7. Elçin Ünal

    Department of Molecular and Cell Biology, University of California, Berkeley, Berkeley, United States
    For correspondence
    elcin@berkeley.edu
    Competing interests
    Elçin Ünal, Reviewing editor, eLife.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6768-609X

Funding

National Institutes of Health (DP2 AG055946-01)

  • Elçin Ünal

Pew Charitable Trusts (00027344)

  • Elçin Ünal

Damon Runyon Cancer Research Foundation (35-15)

  • Elçin Ünal

Glenn Foundation for Medical Research

  • Elçin Ünal

National Science Foundation (DGE 1752814)

  • Grant A King

National Institutes of Health (T32 GM007232)

  • Grant A King

National Institutes of Health (F31AG060656)

  • Jay S Goodman

National Institutes of Health (T32 GM007127-41)

  • Jay S Goodman

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Noboru Mizushima, The University of Tokyo, Japan

Publication history

  1. Received: March 26, 2019
  2. Accepted: July 19, 2019
  3. Accepted Manuscript published: August 9, 2019 (version 1)
  4. Version of Record published: August 27, 2019 (version 2)
  5. Version of Record updated: August 28, 2019 (version 3)
  6. Version of Record updated: September 5, 2019 (version 4)

Copyright

© 2019, King et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Grant A King
  2. Jay S Goodman
  3. Jennifer G Schick
  4. Keerthana Chetlapalli
  5. Danielle M Jorgens
  6. Kent L McDonald
  7. Elçin Ünal
(2019)
Meiotic cellular rejuvenation is coupled to nuclear remodeling in budding yeast
eLife 8:e47156.
https://doi.org/10.7554/eLife.47156

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