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Early-adulthood spike in protein translation drives aging via juvenile hormone/germline signaling

Author

Listed:
  • Harper S. Kim

    (University of Alabama at Birmingham
    University of Alabama at Birmingham
    University of Texas Health San Antonio
    University of Texas Health San Antonio)

  • Danitra J. Parker

    (University of Alabama at Birmingham
    McGovern Medical School at UTHealth)

  • Madison M. Hardiman

    (University of Alabama at Birmingham)

  • Erin Munkácsy

    (University of Texas Health San Antonio)

  • Nisi Jiang

    (University of Texas Health San Antonio)

  • Aric N. Rogers

    (MDI Biological Laboratory)

  • Yidong Bai

    (University of Texas Health San Antonio
    University of Texas Health San Antonio)

  • Colin Brent

    (USDA-ARS Arid Land Agricultural Research Center)

  • James A. Mobley

    (University of Alabama at Birmingham)

  • Steven N. Austad

    (University of Alabama at Birmingham
    University of Alabama at Birmingham)

  • Andrew M. Pickering

    (University of Alabama at Birmingham
    University of Texas Health San Antonio
    McGovern Medical School at UTHealth
    University of Texas Health San Antonio)

Abstract

Protein translation (PT) declines with age in invertebrates, rodents, and humans. It has been assumed that elevated PT at young ages is beneficial to health and PT ends up dropping as a passive byproduct of aging. In Drosophila, we show that a transient elevation in PT during early-adulthood exerts long-lasting negative impacts on aging trajectories and proteostasis in later-life. Blocking the early-life PT elevation robustly improves life-/health-span and prevents age-related protein aggregation, whereas transiently inducing an early-life PT surge in long-lived fly strains abolishes their longevity/proteostasis benefits. The early-life PT elevation triggers proteostatic dysfunction, silences stress responses, and drives age-related functional decline via juvenile hormone-lipid transfer protein axis and germline signaling. Our findings suggest that PT is adaptively suppressed after early-adulthood, alleviating later-life proteostatic burden, slowing down age-related functional decline, and improving lifespan. Our work provides a theoretical framework for understanding how lifetime PT dynamics shape future aging trajectories.

Suggested Citation

  • Harper S. Kim & Danitra J. Parker & Madison M. Hardiman & Erin Munkácsy & Nisi Jiang & Aric N. Rogers & Yidong Bai & Colin Brent & James A. Mobley & Steven N. Austad & Andrew M. Pickering, 2023. "Early-adulthood spike in protein translation drives aging via juvenile hormone/germline signaling," Nature Communications, Nature, vol. 14(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-40618-x
    DOI: 10.1038/s41467-023-40618-x
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    References listed on IDEAS

    as
    1. Cynthia J. Kenyon, 2010. "The genetics of ageing," Nature, Nature, vol. 464(7288), pages 504-512, March.
    2. Cynthia J. Kenyon, 2010. "Erratum: The genetics of ageing," Nature, Nature, vol. 467(7315), pages 622-622, September.
    3. Popi Syntichaki & Kostoula Troulinaki & Nektarios Tavernarakis, 2007. "eIF4E function in somatic cells modulates ageing in Caenorhabditis elegans," Nature, Nature, vol. 445(7130), pages 922-926, February.
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