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Neuroprotective gap-junction-mediated bystander transformations in the adult zebrafish spinal cord after injury

Author

Listed:
  • Andrea Pedroni

    (Karolinska Institutet)

  • Yu-Wen E. Dai

    (Karolinska Institutet)

  • Leslie Lafouasse

    (Karolinska Institutet)

  • Weipang Chang

    (Karolinska Institutet)

  • Ipsit Srivastava

    (Karolinska Institutet)

  • Lisa Vecchio

    (Karolinska Institutet)

  • Konstantinos Ampatzis

    (Karolinska Institutet)

Abstract

The adult zebrafish spinal cord displays an impressive innate ability to regenerate after traumatic insults, yet the underlying adaptive cellular mechanisms remain elusive. Here, we show that while the cellular and tissue responses after injury are largely conserved among vertebrates, the large-size fast spinal zebrafish motoneurons are remarkably resilient by remaining viable and functional. We also reveal the dynamic changes in motoneuron glutamatergic input, excitability, and calcium signaling, and we underscore the critical role of calretinin (CR) in binding and buffering the intracellular calcium after injury. Importantly, we demonstrate the presence and the dynamics of a neuron-to-neuron bystander neuroprotective biochemical cooperation mediated through gap junction channels. Our findings support a model in which the intimate and dynamic interplay between glutamate signaling, calcium buffering, gap junction channels, and intercellular cooperation upholds cell survival and promotes the initiation of regeneration.

Suggested Citation

  • Andrea Pedroni & Yu-Wen E. Dai & Leslie Lafouasse & Weipang Chang & Ipsit Srivastava & Lisa Vecchio & Konstantinos Ampatzis, 2024. "Neuroprotective gap-junction-mediated bystander transformations in the adult zebrafish spinal cord after injury," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-48729-9
    DOI: 10.1038/s41467-024-48729-9
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    References listed on IDEAS

    as
    1. Weipang Chang & Andrea Pedroni & Maria Bertuzzi & Caghan Kizil & András Simon & Konstantinos Ampatzis, 2021. "Locomotion dependent neuron-glia interactions control neurogenesis and regeneration in the adult zebrafish spinal cord," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    2. Carmen Diaz Verdugo & Sverre Myren-Svelstad & Ecem Aydin & Evelien Van Hoeymissen & Celine Deneubourg & Silke Vanderhaeghe & Julie Vancraeynest & Robbrecht Pelgrims & Mehmet Ilyas Cosacak & Akira Muto, 2019. "Glia-neuron interactions underlie state transitions to generalized seizures," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    3. Jianren Song & Konstantinos Ampatzis & E. Rebecka Björnfors & Abdeljabbar El Manira, 2016. "Motor neurons control locomotor circuit function retrogradely via gap junctions," Nature, Nature, vol. 529(7586), pages 399-402, January.
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