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The branching programme of mouse lung development

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  • Ross J. Metzger

    (Stanford University School of Medicine, Stanford, California 94305-5307, USA
    Present addresses: Department of Anatomy, School of Medicine, University of California at San Francisco, California 94158-2517, USA (R.J.M.); Departments of Orofacial Sciences and Pediatrics, and Institute of Human Genetics, Schools of Dentistry and Medicine, University of California at San Francisco, San Francisco, California 94143-0442, USA (O.D.K.).)

  • Ophir D. Klein

    (School of Medicine, University of California at San Francisco, San Francisco, California 94158-2324, USA
    Present addresses: Department of Anatomy, School of Medicine, University of California at San Francisco, California 94158-2517, USA (R.J.M.); Departments of Orofacial Sciences and Pediatrics, and Institute of Human Genetics, Schools of Dentistry and Medicine, University of California at San Francisco, San Francisco, California 94143-0442, USA (O.D.K.).)

  • Gail R. Martin

    (School of Medicine, University of California at San Francisco, San Francisco, California 94158-2324, USA)

  • Mark A. Krasnow

    (Stanford University School of Medicine, Stanford, California 94305-5307, USA)

Abstract

Mammalian lungs are branched networks containing thousands to millions of airways arrayed in intricate patterns that are crucial for respiration. How such trees are generated during development, and how the developmental patterning information is encoded, have long fascinated biologists and mathematicians. However, models have been limited by a lack of information on the normal sequence and pattern of branching events. Here we present the complete three-dimensional branching pattern and lineage of the mouse bronchial tree, reconstructed from an analysis of hundreds of developmental intermediates. The branching process is remarkably stereotyped and elegant: the tree is generated by three geometrically simple local modes of branching used in three different orders throughout the lung. We propose that each mode of branching is controlled by a genetically encoded subroutine, a series of local patterning and morphogenesis operations, which are themselves controlled by a more global master routine. We show that this hierarchical and modular programme is genetically tractable, and it is ideally suited to encoding and evolving the complex networks of the lung and other branched organs.

Suggested Citation

  • Ross J. Metzger & Ophir D. Klein & Gail R. Martin & Mark A. Krasnow, 2008. "The branching programme of mouse lung development," Nature, Nature, vol. 453(7196), pages 745-750, June.
    • Handle: RePEc:nat:nature:v:453:y:2008:i:7196:d:10.1038_nature07005
    DOI: 10.1038/nature07005
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    Cited by:

    1. Mehmet Can Uçar & Dmitrii Kamenev & Kazunori Sunadome & Dominik Fachet & Francois Lallemend & Igor Adameyko & Saida Hadjab & Edouard Hannezo, 2021. "Theory of branching morphogenesis by local interactions and global guidance," Nature Communications, Nature, vol. 12(1), pages 1-10, December.
    2. Kuan Zhang & Erica Yao & Ethan Chuang & Biao Chen & Evelyn Y. Chuang & Pao-Tien Chuang, 2022. "mTORC1 signaling facilitates differential stem cell differentiation to shape the developing murine lung and is associated with mitochondrial capacity," Nature Communications, Nature, vol. 13(1), pages 1-19, December.
    3. Mingzhu Sun & Hui Xu & Xingjuan Zeng & Xin Zhao, 2017. "Automated numerical simulation of biological pattern formation based on visual feedback simulation framework," PLOS ONE, Public Library of Science, vol. 12(2), pages 1-16, February.
    4. Anna Urciuolo & Giovanni Giuseppe Giobbe & Yixiao Dong & Federica Michielin & Luca Brandolino & Michael Magnussen & Onelia Gagliano & Giulia Selmin & Valentina Scattolini & Paolo Raffa & Paola Caccin , 2023. "Hydrogel-in-hydrogel live bioprinting for guidance and control of organoids and organotypic cultures," Nature Communications, Nature, vol. 14(1), pages 1-14, December.
    5. Douglas G. Brownfield & Alex Diaz Arce & Elisa Ghelfi & Astrid Gillich & Tushar J. Desai & Mark A. Krasnow, 2022. "Alveolar cell fate selection and lifelong maintenance of AT2 cells by FGF signaling," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    6. Yina Guo & Mingzhu Sun & Alan Garfinkel & Xin Zhao, 2014. "Mechanisms of Side Branching and Tip Splitting in a Model of Branching Morphogenesis," PLOS ONE, Public Library of Science, vol. 9(7), pages 1-14, July.
    7. Mehmet Can Uçar & Edouard Hannezo & Emmi Tiilikainen & Inam Liaqat & Emma Jakobsson & Harri Nurmi & Kari Vaahtomeri, 2023. "Self-organized and directed branching results in optimal coverage in developing dermal lymphatic networks," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    8. Cemal Cagatay Bilgin & Shayoni Ray & Banu Baydil & William P Daley & Melinda Larsen & Bülent Yener, 2012. "Multiscale Feature Analysis of Salivary Gland Branching Morphogenesis," PLOS ONE, Public Library of Science, vol. 7(3), pages 1-19, March.
    9. Yihwa Kim & Robert Sinclair & Nol Chindapol & Jaap A Kaandorp & Erik De Schutter, 2012. "Geometric Theory Predicts Bifurcations in Minimal Wiring Cost Trees in Biology Are Flat," PLOS Computational Biology, Public Library of Science, vol. 8(4), pages 1-7, April.
    10. Elif Tekin & David Hunt & Mitchell G Newberry & Van M Savage, 2016. "Do Vascular Networks Branch Optimally or Randomly across Spatial Scales?," PLOS Computational Biology, Public Library of Science, vol. 12(11), pages 1-28, November.

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