IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-26294-9.html
   My bibliography  Save this article

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
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-26294-9
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-26294-9?utm_source=ideas
    LibKey link: if access is restricted and if your library uses this service, LibKey will redirect you to where you can use your library subscription to access this item
    ---><---

    References listed on IDEAS

    as
    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. 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.
    3. 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.
    Full references (including those not matched with items on IDEAS)

    Citations

    Citations are extracted by the CitEc Project, subscribe to its RSS feed for this item.
    as


    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.

    Most related items

    These are the items that most often cite the same works as this one and are cited by the same works as this one.
    1. Masa Tsuchiya & Vincent Piras & Alessandro Giuliani & Masaru Tomita & Kumar Selvarajoo, 2010. "Collective Dynamics of Specific Gene Ensembles Crucial for Neutrophil Differentiation: The Existence of Genome Vehicles Revealed," PLOS ONE, Public Library of Science, vol. 5(8), pages 1-10, August.
    2. Lukas Aufinger & Johann Brenner & Friedrich C. Simmel, 2022. "Complex dynamics in a synchronized cell-free genetic clock," Nature Communications, Nature, vol. 13(1), pages 1-9, December.
    3. Singh, Vijai & Chaudhary, Dharmendra Kumar & Mani, Indra & Dhar, Pawan Kumar, 2016. "Recent advances and challenges of the use of cyanobacteria towards the production of biofuels," Renewable and Sustainable Energy Reviews, Elsevier, vol. 60(C), pages 1-10.
    4. Lucas Henrion & Juan Andres Martinez & Vincent Vandenbroucke & Mathéo Delvenne & Samuel Telek & Andrew Zicler & Alexander Grünberger & Frank Delvigne, 2023. "Fitness cost associated with cell phenotypic switching drives population diversification dynamics and controllability," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    5. Volkov, Evgeny & Hellen, Edward H., 2021. "The effect of characteristic times on collective modes of two quorum sensing coupled identical ring oscillators," Chaos, Solitons & Fractals, Elsevier, vol. 151(C).
    6. Jung Hun Park & Gábor Holló & Yolanda Schaerli, 2024. "From resonance to chaos by modulating spatiotemporal patterns through a synthetic optogenetic oscillator," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Yu-Yu Cheng & Zhengyi Chen & Xinyun Cao & Tyler D. Ross & Tanya G. Falbel & Briana M. Burton & Ophelia S. Venturelli, 2023. "Programming bacteria for multiplexed DNA detection," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Christin Köbler & Nicolas M. Schmelling & Anika Wiegard & Alice Pawlowski & Gopal K. Pattanayak & Philipp Spät & Nina M. Scheurer & Kim N. Sebastian & Florian P. Stirba & Lutz C. Berwanger & Petra Kol, 2024. "Two KaiABC systems control circadian oscillations in one cyanobacterium," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    9. Navneet Rai & Rajat Anand & Krishna Ramkumar & Varun Sreenivasan & Sugat Dabholkar & K V Venkatesh & Mukund Thattai, 2012. "Prediction by Promoter Logic in Bacterial Quorum Sensing," PLOS Computational Biology, Public Library of Science, vol. 8(1), pages 1-14, January.
    10. Grzegorczyk Marco & Aderhold Andrej & Husmeier Dirk, 2015. "Inferring bi-directional interactions between circadian clock genes and metabolism with model ensembles," Statistical Applications in Genetics and Molecular Biology, De Gruyter, vol. 14(2), pages 143-167, April.
    11. Alice Boo & Tyler Toth & Qiguo Yu & Alexander Pfotenhauer & Brandon D. Fields & Scott C. Lenaghan & C. Neal Stewart & Christopher A. Voigt, 2024. "Synthetic microbe-to-plant communication channels," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    12. Beregov, R.Y. & Melkikh, A.V., 2015. "De-synchronization and chaos in two inductively coupled Van der Pol auto-generators," Chaos, Solitons & Fractals, Elsevier, vol. 73(C), pages 17-28.
    13. Mark Greenwood & Mirela Domijan & Peter D Gould & Anthony J W Hall & James C W Locke, 2019. "Coordinated circadian timing through the integration of local inputs in Arabidopsis thaliana," PLOS Biology, Public Library of Science, vol. 17(8), pages 1-31, August.

    More about this item

    Statistics

    Access and download statistics

    Corrections

    All material on this site has been provided by the respective publishers and authors. You can help correct errors and omissions. When requesting a correction, please mention this item's handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26294-9. See general information about how to correct material in RePEc.

    If you have authored this item and are not yet registered with RePEc, we encourage you to do it here. This allows to link your profile to this item. It also allows you to accept potential citations to this item that we are uncertain about.

    If CitEc recognized a bibliographic reference but did not link an item in RePEc to it, you can help with this form .

    If you know of missing items citing this one, you can help us creating those links by adding the relevant references in the same way as above, for each refering item. If you are a registered author of this item, you may also want to check the "citations" tab in your RePEc Author Service profile, as there may be some citations waiting for confirmation.

    For technical questions regarding this item, or to correct its authors, title, abstract, bibliographic or download information, contact: Sonal Shukla or Springer Nature Abstracting and Indexing (email available below). General contact details of provider: http://www.nature.com .

    Please note that corrections may take a couple of weeks to filter through the various RePEc services.

    IDEAS is a RePEc service. RePEc uses bibliographic data supplied by the respective publishers.