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CaMKII oxidation is a critical performance/disease trade-off acquired at the dawn of vertebrate evolution

Author

Listed:
  • Qinchuan Wang

    (Johns Hopkins School of Medicine)

  • Erick O. Hernández-Ochoa

    (University of Maryland School of Medicine)

  • Meera C. Viswanathan

    (Johns Hopkins School of Medicine)

  • Ian D. Blum

    (Johns Hopkins School of Medicine)

  • Danh C. Do

    (Johns Hopkins School of Medicine)

  • Jonathan M. Granger

    (Johns Hopkins School of Medicine)

  • Kevin R. Murphy

    (Johns Hopkins School of Medicine)

  • An-Chi Wei

    (National Taiwan University)

  • Susan Aja

    (Johns Hopkins School of Medicine
    Johns Hopkins School of Medicine)

  • Naili Liu

    (Kennedy Krieger Institute)

  • Corina M. Antonescu

    (Johns Hopkins Computational Biology Consulting Core)

  • Liliana D. Florea

    (Johns Hopkins Computational Biology Consulting Core)

  • C. Conover Talbot

    (Johns Hopkins School of Medicine)

  • David Mohr

    (Johns Hopkins School of Medicine Genetic Resources Core Facility)

  • Kathryn R. Wagner

    (Johns Hopkins School of Medicine
    Kennedy Krieger Institute)

  • Sergi Regot

    (Johns Hopkins School of Medicine)

  • Richard M. Lovering

    (University of Maryland School of Medicine)

  • Peisong Gao

    (Johns Hopkins School of Medicine)

  • Mario A. Bianchet

    (Johns Hopkins School of Medicine
    Johns Hopkins University)

  • Mark N. Wu

    (Johns Hopkins School of Medicine)

  • Anthony Cammarato

    (Johns Hopkins School of Medicine)

  • Martin F. Schneider

    (University of Maryland School of Medicine)

  • Gabriel S. Bever

    (Johns Hopkins School of Medicine
    Johns Hopkins School of Medicine)

  • Mark E. Anderson

    (Johns Hopkins School of Medicine)

Abstract

Antagonistic pleiotropy is a foundational theory that predicts aging-related diseases are the result of evolved genetic traits conferring advantages early in life. Here we examine CaMKII, a pluripotent signaling molecule that contributes to common aging-related diseases, and find that its activation by reactive oxygen species (ROS) was acquired more than half-a-billion years ago along the vertebrate stem lineage. Functional experiments using genetically engineered mice and flies reveal ancestral vertebrates were poised to benefit from the union of ROS and CaMKII, which conferred physiological advantage by allowing ROS to increase intracellular Ca2+ and activate transcriptional programs important for exercise and immunity. Enhanced sensitivity to the adverse effects of ROS in diseases and aging is thus a trade-off for positive traits that facilitated the early and continued evolutionary success of vertebrates.

Suggested Citation

  • Qinchuan Wang & Erick O. Hernández-Ochoa & Meera C. Viswanathan & Ian D. Blum & Danh C. Do & Jonathan M. Granger & Kevin R. Murphy & An-Chi Wei & Susan Aja & Naili Liu & Corina M. Antonescu & Liliana , 2021. "CaMKII oxidation is a critical performance/disease trade-off acquired at the dawn of vertebrate evolution," Nature Communications, Nature, vol. 12(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-23549-3
    DOI: 10.1038/s41467-021-23549-3
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