An aging-independent replicative lifespan in a symmetrically dividing eukaryote

  1. Eric C Spivey
  2. Stephen K Jones
  3. James R Rybarski
  4. Fatema A Saifuddin
  5. Ilya J Finkelstein  Is a corresponding author
  1. The University of Texas at Austin, United States

Abstract

The replicative lifespan (RLS) of a cell-defined as the number of cell divisions before death-has informed our understanding of the mechanisms of cellular aging. However, little is known about aging and longevity in symmetrically dividing eukaryotic cells because most prior studies have used budding yeast for RLS studies. Here, we describe a multiplexed fission yeast lifespan micro-dissector (multFYLM) and an associated image processing pipeline for performing high-throughput and automated single-cell micro-dissection. Using the multFYLM, we observe continuous replication of hundreds of individual fission yeast cells for over seventy-five generations. Surprisingly, cells die without the classic hallmarks of cellular aging, such as progressive changes in size, doubling time, or sibling health. Genetic perturbations and drugs can extend the RLS via an aging-independent mechanism. Using a quantitative model to analyze these results, we conclude that fission yeast does not age and that cellular aging and replicative lifespan can be uncoupled in a eukaryotic cell.

Data availability

The following previously published data sets were used
    1. Wood et al.
    (2002) The genome sequence of Schizosaccharomyces pombe
    Publicly available at the NCBI Nucleotide (sccession no: CU329670.1).
    1. Wood et al.
    (2002) The genome sequence of Schizosaccharomyces pombe
    Publicly available at the NCBI Nucleotide (sccession no: CU329671.1).
    1. Wood et al.
    (2002) The genome sequence of Schizosaccharomyces pombe
    Publicly available at the NCBI Nucleotide (sccession no: CU329672.1).

Article and author information

Author details

  1. Eric C Spivey

    Department of Molecular Biosciences, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4080-8616
  2. Stephen K Jones

    Department of Molecular Biosciences, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. James R Rybarski

    Department of Molecular Biosciences, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Fatema A Saifuddin

    Department of Molecular Biosciences, The University of Texas at Austin, Austin, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Ilya J Finkelstein

    Department of Molecular Biosciences, The University of Texas at Austin, Austin, United States
    For correspondence
    ifinkelstein@cm.utexas.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9371-2431

Funding

American Federation for Aging Research (AFAR-020)

  • Eric C Spivey
  • Stephen K Jones
  • James R Rybarski
  • Fatema A Saifuddin
  • Ilya J Finkelstein

National Institute on Aging (F32 AG053051)

  • Stephen K Jones

Cancer Prevention and Research Institute of Texas (R1214)

  • James R Rybarski
  • Fatema A Saifuddin
  • Ilya J Finkelstein

Welch Foundation (F-l808)

  • Eric C Spivey
  • Stephen K Jones
  • James R Rybarski
  • Fatema A Saifuddin
  • Ilya J Finkelstein

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

Reviewing Editor

  1. Jeff Smith, University of Virginia, United States

Version history

  1. Received: August 9, 2016
  2. Accepted: January 27, 2017
  3. Accepted Manuscript published: January 31, 2017 (version 1)
  4. Version of Record published: March 1, 2017 (version 2)
  5. Version of Record updated: April 12, 2018 (version 3)

Copyright

© 2017, Spivey 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. Eric C Spivey
  2. Stephen K Jones
  3. James R Rybarski
  4. Fatema A Saifuddin
  5. Ilya J Finkelstein
(2017)
An aging-independent replicative lifespan in a symmetrically dividing eukaryote
eLife 6:e20340.
https://doi.org/10.7554/eLife.20340

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https://doi.org/10.7554/eLife.20340