IDEAS home Printed from https://ideas.repec.org/a/nat/natcom/v14y2023i1d10.1038_s41467-023-39124-x.html
   My bibliography  Save this article

Inflationary theory of branching morphogenesis in the mouse salivary gland

Author

Listed:
  • Ignacio Bordeu

    (University of Cambridge
    University of Cambridge
    Universidad de Chile)

  • Lemonia Chatzeli

    (University of Cambridge
    University of Cambridge)

  • Benjamin D. Simons

    (University of Cambridge
    University of Cambridge
    University of Cambridge)

Abstract

The mechanisms that regulate the patterning of branched epithelia remain a subject of long-standing debate. Recently, it has been proposed that the statistical organization of multiple ductal tissues can be explained through a local self-organizing principle based on the branching-annihilating random walk (BARW) in which proliferating tips drive a process of ductal elongation and stochastic bifurcation that terminates when tips encounter maturing ducts. Here, applied to mouse salivary gland, we show the BARW model struggles to explain the large-scale organization of tissue. Instead, we propose that the gland develops as a tip-driven branching-delayed random walk (BDRW). In this framework, a generalization of the BARW, tips inhibited through steric interaction with proximate ducts may continue their branching program as constraints become alleviated through the persistent expansion of the surrounding tissue. This inflationary BDRW model presents a general paradigm for branching morphogenesis when the ductal epithelium grows cooperatively with the domain into which it expands.

Suggested Citation

  • Ignacio Bordeu & Lemonia Chatzeli & Benjamin D. Simons, 2023. "Inflationary theory of branching morphogenesis in the mouse salivary gland," Nature Communications, Nature, vol. 14(1), pages 1-11, December.
  • Handle: RePEc:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39124-x
    DOI: 10.1038/s41467-023-39124-x
    as

    Download full text from publisher

    File URL: https://www.nature.com/articles/s41467-023-39124-x
    File Function: Abstract
    Download Restriction: no

    File URL: https://libkey.io/10.1038/s41467-023-39124-x?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. Andrea Ventura & David G. Kirsch & Margaret E. McLaughlin & David A. Tuveson & Jan Grimm & Laura Lintault & Jamie Newman & Elizabeth E. Reczek & Ralph Weissleder & Tyler Jacks, 2007. "Restoration of p53 function leads to tumour regression in vivo," Nature, Nature, vol. 445(7128), pages 661-665, February.
    2. Min Kyu Yum & Seungmin Han & Juergen Fink & Szu-Hsien Sam Wu & Catherine Dabrowska & Teodora Trendafilova & Roxana Mustata & Lemonia Chatzeli & Roberta Azzarelli & Irina Pshenichnaya & Eunmin Lee & Fr, 2021. "Tracing oncogene-driven remodelling of the intestinal stem cell niche," Nature, Nature, vol. 594(7863), pages 442-447, June.
    3. S. Randriamanantsoa & A. Papargyriou & H. C. Maurer & K. Peschke & M. Schuster & G. Zecchin & K. Steiger & R. Öllinger & D. Saur & C. Scheel & R. Rad & E. Hannezo & M. Reichert & A. R. Bausch, 2022. "Spatiotemporal dynamics of self-organized branching in pancreas-derived organoids," Nature Communications, Nature, vol. 13(1), pages 1-15, December.
    Full references (including those not matched with items on IDEAS)

    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. Kristoffer Sølvsten Burgdorf & Niels Grarup & Johanne Marie Justesen & Marie Neergaard Harder & Daniel Rinse Witte & Torben Jørgensen & Annelli Sandbæk & Torsten Lauritzen & Sten Madsbad & Torben Hans, 2011. "Studies of the Association of Arg72Pro of Tumor Suppressor Protein p53 with Type 2 Diabetes in a Combined Analysis of 55,521 Europeans," PLOS ONE, Public Library of Science, vol. 6(1), pages 1-6, January.
    2. Wassim Abou-Jaoudé & Madalena Chaves & Jean-Luc Gouzé, 2011. "A Theoretical Exploration of Birhythmicity in the p53-Mdm2 Network," PLOS ONE, Public Library of Science, vol. 6(2), pages 1-12, February.
    3. Mei Zhao & Tianxiao Wang & Frederico O. Gleber-Netto & Zhen Chen & Daniel J. McGrail & Javier A. Gomez & Wutong Ju & Mayur A. Gadhikar & Wencai Ma & Li Shen & Qi Wang & Ximing Tang & Sen Pathak & Mari, 2024. "Mutant p53 gains oncogenic functions through a chromosomal instability-induced cytosolic DNA response," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    4. Samuel A Danziger & Roberta Baronio & Lydia Ho & Linda Hall & Kirsty Salmon & G Wesley Hatfield & Peter Kaiser & Richard H Lathrop, 2009. "Predicting Positive p53 Cancer Rescue Regions Using Most Informative Positive (MIP) Active Learning," PLOS Computational Biology, Public Library of Science, vol. 5(9), pages 1-12, September.
    5. Dadi Jiang & Youming Guo & Tianyu Wang & Liang Wang & Yuelong Yan & Ling Xia & Rakesh Bam & Zhifen Yang & Hyemin Lee & Takao Iwawaki & Boyi Gan & Albert C. Koong, 2024. "IRE1α determines ferroptosis sensitivity through regulation of glutathione synthesis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    6. Jonuelle Acosta & Qinglan Li & Nelson F. Freeburg & Nivitha Murali & Alexandra Indeglia & Grant P. Grothusen & Michelle Cicchini & Hung Mai & Amy C. Gladstein & Keren M. Adler & Katherine R. Doerig & , 2023. "p53 restoration in small cell lung cancer identifies a latent cyclophilin-dependent necrosis mechanism," Nature Communications, Nature, vol. 14(1), pages 1-18, December.
    7. Christopher W. Murray & Jennifer J. Brady & Mingqi Han & Hongchen Cai & Min K. Tsai & Sarah E. Pierce & Ran Cheng & Janos Demeter & David M. Feldser & Peter K. Jackson & David B. Shackelford & Monte M, 2022. "LKB1 drives stasis and C/EBP-mediated reprogramming to an alveolar type II fate in lung cancer," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    8. Szu-Hsien Sam Wu & Somi Kim & Heetak Lee & Ji-Hyun Lee & So-Yeon Park & Réka Bakonyi & Isaree Teriyapirom & Natalia Hallay & Sandra Pilat-Carotta & Hans-Christian Theussl & Jihoon Kim & Joo-Hyeon Lee , 2024. "Red2Flpe-SCON: a versatile, multicolor strategy for generating mosaic conditional knockout mice," Nature Communications, Nature, vol. 15(1), pages 1-12, December.
    9. Jean-Philippe Coppé & Christopher K Patil & Francis Rodier & Yu Sun & Denise P Muñoz & Joshua Goldstein & Peter S Nelson & Pierre-Yves Desprez & Judith Campisi, 2008. "Senescence-Associated Secretory Phenotypes Reveal Cell-Nonautonomous Functions of Oncogenic RAS and the p53 Tumor Suppressor," PLOS Biology, Public Library of Science, vol. 6(12), pages 1-1, December.
    10. Mariana Shumliakivska & Guillermo Luxán & Inga Hemmerling & Marina Scheller & Xue Li & Carsten Müller-Tidow & Bianca Schuhmacher & Zhengwu Sun & Andreas Dendorfer & Alisa Debes & Simone-Franziska Glas, 2024. "DNMT3A clonal hematopoiesis-driver mutations induce cardiac fibrosis by paracrine activation of fibroblasts," Nature Communications, Nature, vol. 15(1), pages 1-20, December.
    11. C. Biben & T. S. Weber & K. S. Potts & J. Choi & D. C. Miles & A. Carmagnac & T. Sargeant & C. A. Graaf & K. A. Fennell & A. Farley & O. J. Stonehouse & M. A. Dawson & D. J. Hilton & S. H. Naik & S. T, 2023. "In vivo clonal tracking reveals evidence of haemangioblast and haematomesoblast contribution to yolk sac haematopoiesis," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    12. Luye An & Dahihm Kim & Leanne R. Donahue & Menansili Abraham Mejooli & Chi-Yong Eom & Nozomi Nishimura & Andrew C. White, 2024. "Sexual dimorphism in melanocyte stem cell behavior reveals combinational therapeutic strategies for cutaneous repigmentation," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    13. Li Weng & Wen-Shuai Tang & Xu Wang & Yingyun Gong & Changqin Liu & Ni-Na Hong & Ying Tao & Kuang-Zheng Li & Shu-Ning Liu & Wanzi Jiang & Ying Li & Ke Yao & Li Chen & He Huang & Yu-Zheng Zhao & Ze-Ping, 2024. "Surplus fatty acid synthesis increases oxidative stress in adipocytes and induces lipodystrophy," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    14. Ritsuko Nakai & Takafumi Yokota & Masahiro Tokunaga & Mikiro Takaishi & Tomomasa Yokomizo & Takao Sudo & Henyun Shi & Yoshiaki Yasumizu & Daisuke Okuzaki & Chikara Kokubu & Sachiyo Tanaka & Katsuyoshi, 2024. "A newly identified gene Ahed plays essential roles in murine haematopoiesis," Nature Communications, Nature, vol. 15(1), pages 1-16, December.
    15. Natthakan Thongon & Feiyang Ma & Andrea Santoni & Matteo Marchesini & Elena Fiorini & Ashley Rose & Vera Adema & Irene Ganan-Gomez & Emma M. Groarke & Fernanda Gutierrez-Rodrigues & Shuaitong Chen & P, 2021. "Hematopoiesis under telomere attrition at the single-cell resolution," Nature Communications, Nature, vol. 12(1), pages 1-13, December.
    16. Kazuki Nakai & Hancheng Lin & Shotaro Yamano & Shinya Tanaka & Sho Kitamoto & Hitoshi Saitoh & Kenta Sakuma & Junpei Kurauchi & Eilma Akter & Masamitsu Konno & Kojiro Ishibashi & Ryo Kamata & Akihiro , 2023. "Wnt activation disturbs cell competition and causes diffuse invasion of transformed cells through NF-κB-MMP21 pathway," Nature Communications, Nature, vol. 14(1), pages 1-17, December.
    17. Gloria Asantewaa & Emily T. Tuttle & Nathan P. Ward & Yun Pyo Kang & Yumi Kim & Madeline E. Kavanagh & Nomeda Girnius & Ying Chen & Katherine Rodriguez & Fabio Hecht & Marco Zocchi & Leonid Smorodints, 2024. "Glutathione synthesis in the mouse liver supports lipid abundance through NRF2 repression," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    18. Claire Soudais & Romane Schaus & Camille Bachelet & Norbert Minet & Sara Mouasni & Cécile Garcin & Caique Lopes Souza & Pierre David & Clara Cousu & Hélène Asnagli & Andrew Parker & Paul Palmquist-Gom, 2024. "Inactivation of cytidine triphosphate synthase 1 prevents fatal auto-immunity in mice," Nature Communications, Nature, vol. 15(1), pages 1-19, December.
    19. L. Paige Ferguson & Jovylyn Gatchalian & Matthew L. McDermott & Mari Nakamura & Kendall Chambers & Nirakar Rajbhandari & Nikki K. Lytle & Sara Brin Rosenthal & Michael Hamilton & Sonia Albini & Martin, 2023. "Smarcd3 is an epigenetic modulator of the metabolic landscape in pancreatic ductal adenocarcinoma," 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:nat:natcom:v:14:y:2023:i:1:d:10.1038_s41467-023-39124-x. 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.