Coordination of cell cycle and morphogenesis during organ formation

Abstract

Organ formation requires precise regulation of cell cycle and morphogenetic events. Using the Drosophila embryonic salivary gland (SG) as a model, we uncover the role of the SP1/KLF transcription factor Huckebein (Hkb) in coordinating cell cycle regulation and morphogenesis. The hkb mutant SG exhibits defects in invagination positioning and organ size due to abnormal death of SG cells. Normal SG development involves distal-to-proximal progression of endoreplication (endocycle), whereas hkb mutant SG cells undergo abnormal cell division, leading to cell death. Hkb represses the expression of key cell cycle and pro-apoptotic genes in the SG. Knockdown of cyclin E or cyclin-dependent kinase 1, or overexpression of fizzy-related rescues most of the morphogenetic defects observed in the hkb mutant SG. These results indicate that Hkb plays a critical role in controlling endoreplication by regulating the transcription of key cell cycle effectors to ensure proper organ formation.

Data availability

All data generated or analyzed during this study are included in the manuscript and supporting file.Supplementary file 3 contains all the full list of Hkb target genes, GO clusters, and the list of genes in each cluster.

The following previously published data sets were used

Article and author information

Author details

  1. Jeffrey Matthew

    Department of Biological Sciences, Louisiana State University, Baton Rouge, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5686-6370
  2. Vishakha Vishwakarma

    Department of Biological Sciences, Louisiana State University, Baton Rouge, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Thao Phuong Le

    Department of Biological Sciences, Louisiana State University, Baton Rouge, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Ryan A Agsunod

    Department of Biological Sciences, Louisiana State University, Baton Rouge, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. SeYeon Chung

    Department of Biological Sciences, Louisiana State University, Baton Rouge, United States
    For correspondence
    seyeonchung@lsu.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5493-6424

Funding

National Science Foundation (MCB 2141387)

  • SeYeon Chung

Louisiana Board of Regents (LEQSF(2019-22)-RD-A-04)

  • SeYeon Chung

Louisiana State University

  • SeYeon Chung

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2024, Matthew et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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https://doi.org/10.7554/eLife.95830

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