Increased longevity due to sexual activity in mole-rats is associated with transcriptional changes in HPA stress axis

  1. Arne Sahm  Is a corresponding author
  2. Matthias Platzer
  3. Philipp Koch
  4. Yoshiyuki Henning
  5. Martin Bens
  6. Marco Groth
  7. Hynek Burda
  8. Sabine Begall
  9. Saskia Ting
  10. Moritz Goetz
  11. Paul Van Daele
  12. Magdalena Staniszewska
  13. Jasmin Klose
  14. Pedro Fragoso Costa
  15. Steve Hoffmann
  16. Karol Szafranski
  17. Philip Dammann
  1. Leibniz Institute on Aging - Fritz Lipmann Institute, Germany
  2. University of Duisburg-Essen, University Hospital Essen, Germany
  3. University of Duisburg-Essen, Germany
  4. University of South Bohemia, Czech Republic
  5. University Hospital, University of Duisburg-Essen, Germany

Abstract

Sexual activity and/or reproduction are associated with a doubling of life expectancy in the long-lived rodent genus Fukomys. To investigate the molecular mechanisms underlying this phenomenon, we analyzed 636 RNA-seq samples across 15 tissues. This analysis suggests that changes in the regulation of the hypothalamic-pituitary-adrenal stress axis play a key role regarding the extended life expectancy of reproductive vs. non-reproductive mole-rats. This is substantiated by a corpus of independent evidence. In accordance with previous studies, the up-regulation of the proteasome and so-called "anti-aging molecules", e.g. DHEA, is linked with enhanced lifespan. On the other hand, several of our results are not consistent with knowledge about aging of short-lived model organisms. For example, we found the up-regulation of the IGF1/GH axis and several other anabolic processes to be compatible with a considerable lifespan prolongation. These contradictions question the extent to which findings from short-lived species can be transferred to longer-lived ones.

Data availability

Read datasets generated during the current study are available in the European Nucleotide Archive, study ID: PRJEB29798.

The following data sets were generated

Article and author information

Author details

  1. Arne Sahm

    Computational Biology Group, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    For correspondence
    arne.sahm@leibniz-fli.de
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7330-1790
  2. Matthias Platzer

    Genome Analysis, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0596-8582
  3. Philipp Koch

    Core Facility Life Science Computing, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2825-7943
  4. Yoshiyuki Henning

    Institute of Physiology, University of Duisburg-Essen, University Hospital Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Martin Bens

    Platzer Research Group, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7940-6668
  6. Marco Groth

    CF DNA sequencing, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9199-8990
  7. Hynek Burda

    Department of General Zoology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Sabine Begall

    Department of General Zoology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9907-6387
  9. Saskia Ting

    Institute of Pathology and Neuropathology, University of Duisburg-Essen, University Hospital Essen, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Moritz Goetz

    Institute of Pathology and Neuropathology, University of Duisburg-Essen, University Hospital Essen, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  11. Paul Van Daele

    Department of Zoology, University of South Bohemia, České Budějovice, Czech Republic
    Competing interests
    The authors declare that no competing interests exist.
  12. Magdalena Staniszewska

    Department of Nuclear Medicine, University Hospital, University of Duisburg-Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  13. Jasmin Klose

    Department of Nuclear Medicine, University Hospital, University of Duisburg-Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  14. Pedro Fragoso Costa

    Department of Nuclear Medicine, University Hospital, University of Duisburg-Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
  15. Steve Hoffmann

    Computational Biology Group, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
  16. Karol Szafranski

    CF DNA sequencing, Leibniz Institute on Aging - Fritz Lipmann Institute, Jena, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-6391-1766
  17. Philip Dammann

    Department of General Zoology, Faculty of Biology, University of Duisburg-Essen, Essen, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0624-3965

Funding

Deutsche Forschungsgemeinschaft (PL 173/8-1)

  • Matthias Platzer

Deutsche Forschungsgemeinschaft (DA 992/3-1)

  • Philip Dammann

Deutsche Forschungsgemeinschaft (Research Training Group 1739)

  • Magdalena Staniszewska

Wiedenfeld-Stiftung/Stiftung Krebsforschung Duisburg

  • Magdalena Staniszewska

Joachim Herz Stiftung

  • Arne Sahm

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

Ethics

Animal experimentation: Animal housing and tissue collection were compliant with national and state legislation (breeding allowances 32-2-1180-71/328 and 32-2-11-80-71/345; ethics/animal experimentation approval 84-02.04.2013/A164, Landesamt für Natur-, Umwelt- und Verbraucherschutz Nordrhein-Westfalen). Before sampling, animals were anaesthetized with ketamine combined with xylazine (Garcia Montero et al. 2015). Every effort was made to minimize suffering.

Reviewing Editor

  1. Jing-Dong Jackie Han, Chinese Academy of Sciences, China

Publication history

  1. Received: April 15, 2020
  2. Accepted: March 15, 2021
  3. Accepted Manuscript published: March 16, 2021 (version 1)
  4. Version of Record published: March 31, 2021 (version 2)
  5. Version of Record updated: July 21, 2021 (version 3)

Copyright

© 2021, Sahm 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. Arne Sahm
  2. Matthias Platzer
  3. Philipp Koch
  4. Yoshiyuki Henning
  5. Martin Bens
  6. Marco Groth
  7. Hynek Burda
  8. Sabine Begall
  9. Saskia Ting
  10. Moritz Goetz
  11. Paul Van Daele
  12. Magdalena Staniszewska
  13. Jasmin Klose
  14. Pedro Fragoso Costa
  15. Steve Hoffmann
  16. Karol Szafranski
  17. Philip Dammann
(2021)
Increased longevity due to sexual activity in mole-rats is associated with transcriptional changes in HPA stress axis
eLife 10:e57843.
https://doi.org/10.7554/eLife.57843

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