IDEAS home Printed from https://ideas.repec.org/a/plo/pone00/0039992.html
   My bibliography  Save this article

Mechanical Stretch and PI3K Signaling Link Cell Migration and Proliferation to Coordinate Epithelial Tubule Morphogenesis in the Zebrafish Pronephros

Author

Listed:
  • Aleksandr Vasilyev
  • Yan Liu
  • Nathan Hellman
  • Narendra Pathak
  • Iain A Drummond

Abstract

Organ development leads to the emergence of organ function, which in turn can impact developmental processes. Here we show that fluid flow-induced collective epithelial migration during kidney nephron morphogenesis induces cell stretch that in turn signals epithelial proliferation. Increased cell proliferation was dependent on PI3K signaling. Inhibiting epithelial proliferation by blocking PI3K or CDK4/Cyclin D1 activity arrested cell migration prematurely and caused a marked overstretching of the distal nephron tubule. Computational modeling of the involved cell processes predicted major morphological and kinetic outcomes observed experimentally under a variety of conditions. Overall, our findings suggest that kidney development is a recursive process where emerging organ function “feeds back” to the developmental program to influence fundamental cellular events such as cell migration and proliferation, thus defining final organ morphology.

Suggested Citation

  • Aleksandr Vasilyev & Yan Liu & Nathan Hellman & Narendra Pathak & Iain A Drummond, 2012. "Mechanical Stretch and PI3K Signaling Link Cell Migration and Proliferation to Coordinate Epithelial Tubule Morphogenesis in the Zebrafish Pronephros," PLOS ONE, Public Library of Science, vol. 7(7), pages 1-11, July.
  • Handle: RePEc:plo:pone00:0039992
    DOI: 10.1371/journal.pone.0039992
    as

    Download full text from publisher

    File URL: https://journals.plos.org/plosone/article?id=10.1371/journal.pone.0039992
    Download Restriction: no

    File URL: https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0039992&type=printable
    Download Restriction: no

    File URL: https://libkey.io/10.1371/journal.pone.0039992?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. Jay R. Hove & Reinhard W. Köster & Arian S. Forouhar & Gabriel Acevedo-Bolton & Scott E. Fraser & Morteza Gharib, 2003. "Intracardiac fluid forces are an essential epigenetic factor for embryonic cardiogenesis," Nature, Nature, vol. 421(6919), pages 172-177, January.
    2. Luigi Adamo & Olaia Naveiras & Pamela L. Wenzel & Shannon McKinney-Freeman & Peter J. Mack & Jorge Gracia-Sancho & Astrid Suchy-Dicey & Momoko Yoshimoto & M. William Lensch & Mervin C. Yoder & Guiller, 2009. "Biomechanical forces promote embryonic haematopoiesis," Nature, Nature, vol. 459(7250), pages 1131-1135, June.
    3. Carlos Carmona-Fontaine & Helen K. Matthews & Sei Kuriyama & Mauricio Moreno & Graham A. Dunn & Maddy Parsons & Claudio D. Stern & Roberto Mayor, 2008. "Contact inhibition of locomotion in vivo controls neural crest directional migration," Nature, Nature, vol. 456(7224), pages 957-961, December.
    4. Aleksandr Vasilyev & Yan Liu & Sudha Mudumana & Steve Mangos & Pui-Ying Lam & Arindam Majumdar & Jinhua Zhao & Kar-Lai Poon & Igor Kondrychyn & Vladimir Korzh & Iain A Drummond, 2009. "Collective Cell Migration Drives Morphogenesis of the Kidney Nephron," PLOS Biology, Public Library of Science, vol. 7(1), pages 1-14, 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. Margherita Perillo & S. Zachary Swartz & Cosmo Pieplow & Gary M. Wessel, 2023. "Molecular mechanisms of tubulogenesis revealed in the sea star hydro-vascular organ," Nature Communications, Nature, vol. 14(1), pages 1-17, 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. András Szabó & Eric Theveneau & Melissa Turan & Roberto Mayor, 2019. "Neural crest streaming as an emergent property of tissue interactions during morphogenesis," PLOS Computational Biology, Public Library of Science, vol. 15(4), pages 1-21, April.
    2. Yassine El Bakkouri & Rony Chidiac & Chantal Delisle & Jeanne Corriveau & Gael Cagnone & Vanda Gaonac’h-Lovejoy & Ashley Chin & Éric Lécuyer & Stephane Angers & Jean-Sébastien Joyal & Ivan Topisirovic, 2024. "ZO-1 interacts with YB-1 in endothelial cells to regulate stress granule formation during angiogenesis," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    3. Masataka Yamao & Honda Naoki & Shin Ishii, 2011. "Multi-Cellular Logistics of Collective Cell Migration," PLOS ONE, Public Library of Science, vol. 6(12), pages 1-11, December.
    4. Dorothee Bornhorst & Amulya V. Hejjaji & Lena Steuter & Nicole M. Woodhead & Paul Maier & Alessandra Gentile & Alice Alhajkadour & Octavia Santis Larrain & Michael Weber & Khrievono Kikhi & Stefan Gue, 2024. "The heart is a resident tissue for hematopoietic stem and progenitor cells in zebrafish," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    5. Agustin D. Pizarro & Claudio L. A. Berli & Galo J. A. A. Soler-Illia & Martín G. Bellino, 2022. "Droplets in underlying chemical communication recreate cell interaction behaviors," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    6. Wen Hao Neo & Yiran Meng & Alba Rodriguez-Meira & Muhammad Z. H. Fadlullah & Christopher A. G. Booth & Emanuele Azzoni & Supat Thongjuea & Marella F. T. R. Bruijn & Sten Eirik W. Jacobsen & Adam J. Me, 2021. "Ezh2 is essential for the generation of functional yolk sac derived erythro-myeloid progenitors," Nature Communications, Nature, vol. 12(1), pages 1-12, December.
    7. Ariadna Marín-Llauradó & Sohan Kale & Adam Ouzeri & Tom Golde & Raimon Sunyer & Alejandro Torres-Sánchez & Ernest Latorre & Manuel Gómez-González & Pere Roca-Cusachs & Marino Arroyo & Xavier Trepat, 2023. "Mapping mechanical stress in curved epithelia of designed size and shape," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
    8. Matthew A. Heinrich & Ricard Alert & Abraham E. Wolf & Andrej Košmrlj & Daniel J. Cohen, 2022. "Self-assembly of tessellated tissue sheets by expansion and collision," Nature Communications, Nature, vol. 13(1), pages 1-10, December.
    9. Christine Chiasson-MacKenzie & Jeremie Vitte & Ching-Hui Liu & Emily A. Wright & Elizabeth A. Flynn & Shannon L. Stott & Marco Giovannini & Andrea I. McClatchey, 2023. "Cellular mechanisms of heterogeneity in NF2-mutant schwannoma," Nature Communications, Nature, vol. 14(1), pages 1-17, December.

    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:plo:pone00:0039992. 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: plosone (email available below). General contact details of provider: https://journals.plos.org/plosone/ .

    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.