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Synchronization between peripheral circadian clock and feeding-fasting cycles in microfluidic device sustains oscillatory pattern of transcriptome

Author

Listed:
  • Onelia Gagliano

    (University of Padova
    Venetian Institute of Molecular Medicine (VIMM)
    University of Texas Southwestern Medical Center)

  • Camilla Luni

    (ShanghaiTech University
    University of Bologna)

  • Yan Li

    (University of Texas Southwestern Medical Center)

  • Silvia Angiolillo

    (University of Padova
    Venetian Institute of Molecular Medicine (VIMM))

  • Wei Qin

    (University of Padova
    Venetian Institute of Molecular Medicine (VIMM))

  • Francesco Panariello

    (Telethon Institute of Genetics and Medicine (TIGEM)
    University of Naples “Federico II”)

  • Davide Cacchiarelli

    (Telethon Institute of Genetics and Medicine (TIGEM)
    University of Naples “Federico II”)

  • Joseph S. Takahashi

    (University of Texas Southwestern Medical Center
    University of Texas Southwestern Medical Center)

  • Nicola Elvassore

    (University of Padova
    Venetian Institute of Molecular Medicine (VIMM)
    University College London GOS Institute of Child Health)

Abstract

The circadian system cyclically regulates many physiological and behavioral processes within the day. Desynchronization between physiological and behavioral rhythms increases the risk of developing some, including metabolic, disorders. Here we investigate how the oscillatory nature of metabolic signals, resembling feeding-fasting cycles, sustains the cell-autonomous clock in peripheral tissues. By controlling the timing, period and frequency of glucose and insulin signals via microfluidics, we find a strong effect on Per2::Luc fibroblasts entrainment. We show that the circadian Per2 expression is better sustained via a 24 h period and 12 h:12 h frequency-encoded metabolic stimulation applied for 3 daily cycles, aligned to the cell-autonomous clock, entraining the expression of hundreds of genes mostly belonging to circadian rhythms and cell cycle pathways. On the contrary misaligned feeding-fasting cycles synchronize and amplify the expression of extracellular matrix-associated genes, aligned during the light phase. This study underlines the role of the synchronicity between life-style-associated metabolic signals and peripheral clocks on the circadian entrainment.

Suggested Citation

  • Onelia Gagliano & Camilla Luni & Yan Li & Silvia Angiolillo & Wei Qin & Francesco Panariello & Davide Cacchiarelli & Joseph S. Takahashi & Nicola Elvassore, 2021. "Synchronization between peripheral circadian clock and feeding-fasting cycles in microfluidic device sustains oscillatory pattern of transcriptome," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26294-9
    DOI: 10.1038/s41467-021-26294-9
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    References listed on IDEAS

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    1. Fabin Dang & Xiujie Sun & Xiang Ma & Rong Wu & Deyi Zhang & Yaqiong Chen & Qian Xu & Yuting Wu & Yi Liu, 2016. "Insulin post-transcriptionally modulates Bmal1 protein to affect the hepatic circadian clock," Nature Communications, Nature, vol. 7(1), pages 1-12, November.
    2. Tal Danino & Octavio Mondragón-Palomino & Lev Tsimring & Jeff Hasty, 2010. "A synchronized quorum of genetic clocks," Nature, Nature, vol. 463(7279), pages 326-330, January.
    3. Michael J. Haydon & Olga Mielczarek & Fiona C. Robertson & Katharine E. Hubbard & Alex A. R. Webb, 2013. "Photosynthetic entrainment of the Arabidopsis thaliana circadian clock," Nature, Nature, vol. 502(7473), pages 689-692, October.
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    Cited by:

    1. Meredith E. Fay & Oluwamayokun Oshinowo & Elizabeth Iffrig & Kirby S. Fibben & Christina Caruso & Scott Hansen & Jamie O. Musick & José M. Valdez & Sally S. Azer & Robert G. Mannino & Hyoann Choi & Da, 2023. "iCLOTS: open-source, artificial intelligence-enabled software for analyses of blood cells in microfluidic and microscopy-based assays," Nature Communications, Nature, vol. 14(1), pages 1-16, December.
    2. Francesco Panariello & Onelia Gagliano & Camilla Luni & Antonio Grimaldi & Silvia Angiolillo & Wei Qin & Anna Manfredi & Patrizia Annunziata & Shaked Slovin & Lorenzo Vaccaro & Sara Riccardo & Valenti, 2023. "Cellular population dynamics shape the route to human pluripotency," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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