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The emergence of circadian timekeeping in the intestine

Author

Listed:
  • Kathyani Parasram

    (University of Windsor)

  • Amy Zuccato

    (University of Windsor)

  • Minjeong Shin

    (University of Alberta)

  • Reegan Willms

    (University of Alberta)

  • Brian DeVeale

    (University of Windsor)

  • Edan Foley

    (University of Alberta)

  • Phillip Karpowicz

    (University of Windsor)

Abstract

The circadian clock is a molecular timekeeper, present from cyanobacteria to mammals, that coordinates internal physiology with the external environment. The clock has a 24-h period however development proceeds with its own timing, raising the question of how these interact. Using the intestine of Drosophila melanogaster as a model for organ development, we track how and when the circadian clock emerges in specific cell types. We find that the circadian clock begins abruptly in the adult intestine and gradually synchronizes to the environment after intestinal development is complete. This delayed start occurs because individual cells at earlier stages lack the complete circadian clock gene network. As the intestine develops, the circadian clock is first consolidated in intestinal stem cells with changes in Ecdysone and Hnf4 signalling influencing the transcriptional activity of Clk/cyc to drive the expression of tim, Pdp1, and vri. In the mature intestine, stem cell lineage commitment transiently disrupts clock activity in differentiating progeny, mirroring early developmental clock-less transitions. Our data show that clock function and differentiation are incompatible and provide a paradigm for studying circadian clocks in development and stem cell lineages.

Suggested Citation

  • Kathyani Parasram & Amy Zuccato & Minjeong Shin & Reegan Willms & Brian DeVeale & Edan Foley & Phillip Karpowicz, 2024. "The emergence of circadian timekeeping in the intestine," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-45942-4
    DOI: 10.1038/s41467-024-45942-4
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    References listed on IDEAS

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    1. Craig A. Micchelli & Norbert Perrimon, 2006. "Evidence that stem cells reside in the adult Drosophila midgut epithelium," Nature, Nature, vol. 439(7075), pages 475-479, January.
    2. Benjamin Ohlstein & Allan Spradling, 2006. "The adult Drosophila posterior midgut is maintained by pluripotent stem cells," Nature, Nature, vol. 439(7075), pages 470-474, January.
    3. Li He & Guangwei Si & Jiuhong Huang & Aravinthan D. T. Samuel & Norbert Perrimon, 2018. "Mechanical regulation of stem-cell differentiation by the stretch-activated Piezo channel," Nature, Nature, vol. 555(7694), pages 103-106, March.
    4. Zongzhao Zhai & Shu Kondo & Nati Ha & Jean-Philippe Boquete & Michael Brunner & Ryu Ueda & Bruno Lemaitre, 2015. "Accumulation of differentiating intestinal stem cell progenies drives tumorigenesis," Nature Communications, Nature, vol. 6(1), pages 1-13, December.
    5. Jerome Korzelius & Sina Azami & Tal Ronnen-Oron & Philipp Koch & Maik Baldauf & Elke Meier & Imilce A. Rodriguez-Fernandez & Marco Groth & Pedro Sousa-Victor & Heinrich Jasper, 2019. "The WT1-like transcription factor Klumpfuss maintains lineage commitment of enterocyte progenitors in the Drosophila intestine," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    6. Steven M. Reppert & David R. Weaver, 2002. "Coordination of circadian timing in mammals," Nature, Nature, vol. 418(6901), pages 935-941, August.
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