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Implication of thermal signaling in neuronal differentiation revealed by manipulation and measurement of intracellular temperature

Author

Listed:
  • Shunsuke Chuma

    (Osaka University
    Osaka University)

  • Kazuyuki Kiyosue

    (National Institute of Advanced Industrial Science and Technology (AIST))

  • Taishu Akiyama

    (Kyoto University
    Kyoto University)

  • Masaki Kinoshita

    (Kyoto University
    Kyoto University)

  • Yukiho Shimazaki

    (Osaka University
    Osaka University)

  • Seiichi Uchiyama

    (The University of Tokyo)

  • Shingo Sotoma

    (Osaka University)

  • Kohki Okabe

    (The University of Tokyo
    PRESTO)

  • Yoshie Harada

    (Osaka University
    Kyoto University
    Osaka University
    Osaka University)

Abstract

Neuronal differentiation—the development of neurons from neural stem cells—involves neurite outgrowth and is a key process during the development and regeneration of neural functions. In addition to various chemical signaling mechanisms, it has been suggested that thermal stimuli induce neuronal differentiation. However, the function of physiological subcellular thermogenesis during neuronal differentiation remains unknown. Here we create methods to manipulate and observe local intracellular temperature, and investigate the effects of noninvasive temperature changes on neuronal differentiation using neuron-like PC12 cells. Using quantitative heating with an infrared laser, we find an increase in local temperature (especially in the nucleus) facilitates neurite outgrowth. Intracellular thermometry reveals that neuronal differentiation is accompanied by intracellular thermogenesis associated with transcription and translation. Suppression of intracellular temperature increase during neuronal differentiation inhibits neurite outgrowth. Furthermore, spontaneous intracellular temperature elevation is involved in neurite outgrowth of primary mouse cortical neurons. These results offer a model for understanding neuronal differentiation induced by intracellular thermal signaling.

Suggested Citation

  • Shunsuke Chuma & Kazuyuki Kiyosue & Taishu Akiyama & Masaki Kinoshita & Yukiho Shimazaki & Seiichi Uchiyama & Shingo Sotoma & Kohki Okabe & Yoshie Harada, 2024. "Implication of thermal signaling in neuronal differentiation revealed by manipulation and measurement of intracellular temperature," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47542-8
    DOI: 10.1038/s41467-024-47542-8
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    References listed on IDEAS

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    1. Yulia G. Ermakova & Aleksandr A. Lanin & Ilya V. Fedotov & Matvey Roshchin & Ilya V. Kelmanson & Dmitry Kulik & Yulia A. Bogdanova & Arina G. Shokhina & Dmitry S. Bilan & Dmitry B. Staroverov & Pavel , 2017. "Thermogenetic neurostimulation with single-cell resolution," Nature Communications, Nature, vol. 8(1), pages 1-15, August.
    2. Sally Temple, 2001. "The development of neural stem cells," Nature, Nature, vol. 414(6859), pages 112-117, November.
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