Lifespan extension in female mice by early, transient exposure to adult female olfactory cues

  1. Michael Garratt  Is a corresponding author
  2. Ilkim Erturk
  3. Roxann Alonso
  4. Frank Zufall
  5. Trese Leinders-Zufall
  6. Scott D Pletcher
  7. Richard A Miller
  1. University of Otago, New Zealand
  2. University of Michigan-Ann Arbor, United States
  3. Saarland University, Germany

Abstract

Several previous lines of research have suggested, indirectly, that mouse lifespan is particularly susceptible to endocrine or nutritional signals in the first few weeks of life, as tested by manipulations of litter size, growth hormone levels, or mutations with effects specifically on early-life growth rate. The pace of early development in mice can also be influenced by exposure of nursing and weanling mice to olfactory cues. In particular, odors of same-sex adult mice can in some circumstances delay maturation. We hypothesized that olfactory information might also have a sex-specific effect on lifespan, and we show here that lifespan of female mice can be increased significantly by odors from adult females administered transiently, i.e. from 3 days until 60 days of age. Female lifespan was not modified by male odors, nor was male lifespan susceptible to odors from adults of either sex. Conditional deletion of the G protein Gαo in the olfactory system, which leads to impaired accessory olfactory system function and blunted reproductive priming responses to male odors in females, did not modify the effect of female odors on female lifespan. Our data provide support for the idea that very young mice are susceptible to influences that can have long-lasting effects on health maintenance in later life, and provide a potential example of lifespan extension by olfactory cues in mice.

Data availability

All data presented in the manuscript is contained within the Supplementary source data file.

Article and author information

Author details

  1. Michael Garratt

    Department of Anatomy, University of Otago, Dunedin, New Zealand
    For correspondence
    mike.garratt@otago.ac.nz
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9383-3313
  2. Ilkim Erturk

    Department of Pathology and Geriatrics Center, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Roxann Alonso

    Department of Pathology and Geriatrics Center, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Frank Zufall

    Center for Integrative Physiology and Molecular Medicine, Saarland University, Homburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4383-8618
  5. Trese Leinders-Zufall

    Center for Integrative Physiology and Molecular Medicine, Saarland University, Homburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-0678-362X
  6. Scott D Pletcher

    Department of Molecular and Integrative Physiology, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-4812-3785
  7. Richard A Miller

    Department of Pathology and Geriatrics Center, University of Michigan-Ann Arbor, Ann Arbor, United States
    Competing interests
    The authors declare that no competing interests exist.

Funding

National Institute for Aging (AG024824)

  • Richard A Miller

Glenn Foundation for Medical Research

  • Scott D Pletcher
  • Richard A Miller

Deutsche Forschungsgemeinschaft (SFB 894)

  • Frank Zufall
  • Trese Leinders-Zufall

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

Ethics

Animal experimentation: The proposed lifespan experiment was approved by the University of Michigan Animal Care and Use Program, Protocol PRO00007884. All experiments strictly adhered to this approved protocol.

Reviewing Editor

  1. Bérénice A Benayoun, University of Southern California, United States

Publication history

  1. Received: October 12, 2022
  2. Accepted: December 14, 2022
  3. Accepted Manuscript published: December 16, 2022 (version 1)

Copyright

© 2022, Garratt 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. Michael Garratt
  2. Ilkim Erturk
  3. Roxann Alonso
  4. Frank Zufall
  5. Trese Leinders-Zufall
  6. Scott D Pletcher
  7. Richard A Miller
(2022)
Lifespan extension in female mice by early, transient exposure to adult female olfactory cues
eLife 11:e84060.
https://doi.org/10.7554/eLife.84060
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