IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v12y2021i1d10.1038_s41467-021-27384-4.html
   My bibliography  Save this article

Non-canonical Wnt signaling promotes directed migration of intestinal stem cells to sites of injury

Author

Listed:
  • Daniel Jun-Kit Hu

    (Genentech Inc.)

  • Jina Yun

    (Genentech Inc.)

  • Justin Elstrott

    (Genentech Inc.)

  • Heinrich Jasper

    (Genentech Inc.)

Abstract

Tissue regeneration after injury requires coordinated regulation of stem cell activation, division, and daughter cell differentiation, processes that are increasingly well understood in many regenerating tissues. How accurate stem cell positioning and localized integration of new cells into the damaged epithelium are achieved, however, remains unclear. Here, we show that enteroendocrine cells coordinate stem cell migration towards a wound in the Drosophila intestinal epithelium. In response to injury, enteroendocrine cells release the N-terminal domain of the PTK7 orthologue, Otk, which activates non-canonical Wnt signaling in intestinal stem cells, promoting actin-based protrusion formation and stem cell migration towards a wound. We find that this migratory behavior is closely linked to proliferation, and that it is required for efficient tissue repair during injury. Our findings highlight the role of non-canonical Wnt signaling in regeneration of the intestinal epithelium, and identify enteroendocrine cell-released ligands as critical coordinators of intestinal stem cell migration.

Suggested Citation

  • Daniel Jun-Kit Hu & Jina Yun & Justin Elstrott & Heinrich Jasper, 2021. "Non-canonical Wnt signaling promotes directed migration of intestinal stem cells to sites of injury," Nature Communications, Nature, vol. 12(1), pages 1-15, December.
  • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27384-4
    DOI: 10.1038/s41467-021-27384-4
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-021-27384-4
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-021-27384-4?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. Xiaowei Lu & Annette G. M. Borchers & Christine Jolicoeur & Helen Rayburn & Julie C. Baker & Marc Tessier-Lavigne, 2004. "PTK7/CCK-4 is a novel regulator of planar cell polarity in vertebrates," Nature, Nature, vol. 430(6995), pages 93-98, July.
    2. Jiae Lee & Alejandra J. H. Cabrera & Cecilia M. T. Nguyen & Young V. Kwon, 2020. "Dissemination of RasV12-transformed cells requires the mechanosensitive channel Piezo," Nature Communications, Nature, vol. 11(1), pages 1-13, December.
    3. 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.
    4. Mariaceleste Aragona & Sophie Dekoninck & Steffen Rulands & Sandrine Lenglez & Guilhem Mascré & Benjamin D. Simons & Cédric Blanpain, 2017. "Defining stem cell dynamics and migration during wound healing in mouse skin epidermis," Nature Communications, Nature, vol. 8(1), pages 1-14, April.
    5. 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.
    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. Jina Yun & Simon Hansen & Otto Morris & David T. Madden & Clare Peters Libeu & Arjun J. Kumar & Cameron Wehrfritz & Aaron H. Nile & Yingnan Zhang & Lijuan Zhou & Yuxin Liang & Zora Modrusan & Michelle, 2023. "Senescent cells perturb intestinal stem cell differentiation through Ptk7 induced noncanonical Wnt and YAP signaling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    2. Ana-Beatriz F. Barletta & Jamie C. Smith & Emily Burkart & Simon Bondarenko & Igor V. Sharakhov & Frank Criscione & David O’Brochta & Carolina Barillas-Mury, 2024. "Mosquito midgut stem cell cellular defense response limits Plasmodium parasite infection," Nature Communications, Nature, vol. 15(1), pages 1-9, 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. Seungjae Lee & Yen-Chung Chen & Austin E. Gillen & J. Matthew Taliaferro & Bart Deplancke & Hongjie Li & Eric C. Lai, 2022. "Diverse cell-specific patterns of alternative polyadenylation in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-16, December.
    2. 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.
    3. Xingting Guo & Yongchao Zhang & Huanwei Huang & Rongwen Xi, 2022. "A hierarchical transcription factor cascade regulates enteroendocrine cell diversity and plasticity in Drosophila," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    4. Christian F. Christensen & Quentin Laurichesse & Rihab Loudhaief & Julien Colombani & Ditte S. Andersen, 2024. "Drosophila activins adapt gut size to food intake and promote regenerative growth," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    5. Xingting Guo & Chenhui Wang & Yongchao Zhang & Ruxue Wei & Rongwen Xi, 2024. "Cell-fate conversion of intestinal cells in adult Drosophila midgut by depleting a single transcription factor," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Zoe Veneti & Virginia Fasoulaki & Nikolaos Kalavros & Ioannis S. Vlachos & Christos Delidakis & Aristides G. Eliopoulos, 2024. "Polycomb-mediated silencing of miR-8 is required for maintenance of intestinal stemness in Drosophila melanogaster," Nature Communications, Nature, vol. 15(1), pages 1-13, December.
    7. Yue Li & Tianfeng Lu & Pengzhen Dong & Jian Chen & Qiang Zhao & Yuying Wang & Tianheng Xiao & Honggang Wu & Quanyi Zhao & Hai Huang, 2024. "A single-cell atlas of Drosophila trachea reveals glycosylation-mediated Notch signaling in cell fate specification," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    8. Agnes Banreti & Shayon Bhattacharya & Frank Wien & Koichi Matsuo & Matthieu Réfrégiers & Cornelia Meinert & Uwe Meierhenrich & Bruno Hudry & Damien Thompson & Stéphane Noselli, 2022. "Biological effects of the loss of homochirality in a multicellular organism," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    9. Sayan Chakraborty & Divyaleka Sampath & Melissa Ong Yu Lin & Matthew Bilton & Cheng-Kuang Huang & Mui Hoon Nai & Kizito Njah & Pierre-Alexis Goy & Cheng-Chun Wang & Ernesto Guccione & Chwee-Teck Lim &, 2021. "Agrin-Matrix Metalloproteinase-12 axis confers a mechanically competent microenvironment in skin wound healing," Nature Communications, Nature, vol. 12(1), pages 1-18, December.
    10. Jina Yun & Simon Hansen & Otto Morris & David T. Madden & Clare Peters Libeu & Arjun J. Kumar & Cameron Wehrfritz & Aaron H. Nile & Yingnan Zhang & Lijuan Zhou & Yuxin Liang & Zora Modrusan & Michelle, 2023. "Senescent cells perturb intestinal stem cell differentiation through Ptk7 induced noncanonical Wnt and YAP signaling," Nature Communications, Nature, vol. 14(1), pages 1-19, December.
    11. Clement Verkest & Irina Schaefer & Timo A. Nees & Na Wang & Juri M. Jegelka & Francisco J. Taberner & Stefan G. Lechner, 2022. "Intrinsically disordered intracellular domains control key features of the mechanically-gated ion channel PIEZO2," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    12. Florian J. Bock & Egor Sedov & Elle Koren & Anna L. Koessinger & Catherine Cloix & Désirée Zerbst & Dimitris Athineos & Jayanthi Anand & Kirsteen J. Campbell & Karen Blyth & Yaron Fuchs & Stephen W. G, 2021. "Apoptotic stress-induced FGF signalling promotes non-cell autonomous resistance to cell death," Nature Communications, Nature, vol. 12(1), pages 1-14, December.
    13. Enas E. Nasr & Zeinab Z. Khater & Martina Zelenakova & Zuzana Vranayova & Mohamed Abu-Hashim, 2020. "Soil Physicochemical Properties, Metal Deposition, and Ultrastructural Midgut Changes in Ground Beetles, Calosoma chlorostictum, under Agricultural Pollution," Sustainability, MDPI, vol. 12(12), pages 1-17, June.
    14. Karen L. Xu & Nikolas Caprio & Hooman Fallahi & Mohammad Dehghany & Matthew D. Davidson & Lorielle Laforest & Brian C. H. Cheung & Yuqi Zhang & Mingming Wu & Vivek Shenoy & Lin Han & Robert L. Mauck &, 2024. "Microinterfaces in biopolymer-based bicontinuous hydrogels guide rapid 3D cell migration," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    15. Zachary T. Spencer & Victoria H. Ng & Hassina Benchabane & Ghalia Saad Siddiqui & Deepesh Duwadi & Ben Maines & Jamal M. Bryant & Anna Schwarzkopf & Kai Yuan & Sara N. Kassel & Anant Mishra & Ashley P, 2023. "The USP46 deubiquitylase complex increases Wingless/Wnt signaling strength by stabilizing Arrow/LRP6," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    16. Ana-Beatriz F. Barletta & Jamie C. Smith & Emily Burkart & Simon Bondarenko & Igor V. Sharakhov & Frank Criscione & David O’Brochta & Carolina Barillas-Mury, 2024. "Mosquito midgut stem cell cellular defense response limits Plasmodium parasite infection," Nature Communications, Nature, vol. 15(1), pages 1-9, 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:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-27384-4. 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.