Skip to main content
Log in

Three-dimensional morphogenesis of epithelial tubes

管状上皮组织的三维形态发生

  • Research Paper
  • Published:
Acta Mechanica Sinica Aims and scope Submit manuscript

Abstract

Epithelial tubes serve as fundamental structures within diverse organs. Morphogenesis of epithelial tubes involves cell deformations, biochemical signaling, and the cross-talking between cells and the extracellular matrix. However, it remains incompletely understood how the interplay between mechanics and biochemical signaling modulates the morphologies of epithelial tubes. In this work, we develop a three-dimensional (3D) vertex model incorporating biochemical signaling pathways to investigate epithelial tube morphogenesis. We reveal that the mechanical properties of both cells and the apical extracellular matrix can regulate the size of the tube. The chemomechanical deformation of cells can activate supercellular spot and stripe actomyosin patterns, which, consequently, induce the wave- or ring-shaped tube configurations, depending on diffusion of chemical species. Our study highlights the significant role of mechano-chemical interplay in morphodynamics of tissues and also provides a 3D framework to decode complex pattern formation in biological structures.

摘要

管状上皮组织是组成多种器官的基本结构, 其形态发生涉及到细胞变形、生化信号转导, 以及细胞之间和细胞与细胞外基质之 间的相互作用. 目前尚未完全清楚力学和生化信号之间的相互作用如何调节该形态学过程. 本文构建了耦合生化信号通路的三维细胞 顶点模型, 用于探究管状组织的形态发生. 数值计算结果表明管腔尺寸受到细胞和细胞外基质的力学性质的影响, 且细胞的力学-化学 耦合的变形可以激发斑点状和条带状的超细胞肌动球蛋白斑图, 进而介导组织形成波浪形和竹节形的管腔结构, 该过程会受到化学扩 散强度的调节. 本研究突显了力学-化学相互作用在生物组织形态动力学中的重要作用, 并且提供了一个三维计算框架以深入理解生命 系统中复杂的斑图形成过程.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. B. Lubarsky, and M. A. Krasnow, Tube morphogenesis, Cell 112, 19 (2003).

    Article  Google Scholar 

  2. M. L. Iruela-Arispe, and G. J. Beitel, Tubulogenesis, Development 140, 2851 (2013).

    Article  Google Scholar 

  3. S. Hayashi, and B. Dong, Shape and geometry control of the Drosophila tracheal tubule, Dev. Growth Differ. 59, 4 (2017).

    Article  Google Scholar 

  4. K. Skouloudaki, D. K. Papadopoulos, P. Tomancak, and E. Knust, The apical protein Apnoia interacts with Crumbs to regulate tracheal growth and inflation, PLoS Genet. 15, 28 (2019).

    Article  Google Scholar 

  5. B. J. Klußmann-Fricke, M. D. Martín-Bermudo, and M. Llimargas, The basement membrane controls size and integrity of the Drosophila tracheal tubes, Cell Rep. 39, 110734 (2022).

    Article  Google Scholar 

  6. B. Dong, E. Hannezo, and S. Hayashi, Balance between apical membrane growth and luminal matrix resistance determines epithelial tubule shape, Cell Rep. 7, 941 (2014).

    Article  Google Scholar 

  7. E. Hannezo, B. Dong, P. Recho, J. F. Joanny, and S. Hayashi, Cortical instability drives periodic supracellular actin pattern formation in epithelial tubes, Proc. Natl. Acad. Sci. USA 112, 8620 (2015).

    Article  Google Scholar 

  8. D. Förster, K. Armbruster, and S. Luschnig, Sec24-dependent secretion drives cell-autonomous expansion of tracheal tubes in Drosophila, Curr. Biol. 20, 62 (2010).

    Article  Google Scholar 

  9. A. M. Turing, The chemical basis of morphogenesis, Phil. Trans. R. Soc. Lond. B 237, 37 (1952).

    Article  MathSciNet  Google Scholar 

  10. S. Yin, B. Li, and X. Q. Feng, Bio-chemo-mechanical theory of active shells, J. Mech. Phys. Solids 152, 104419 (2021).

    Article  MathSciNet  Google Scholar 

  11. P. Wen, X. Wei, and Y. Lin, A computational model for capturing the distinct in- and out-of-plane response of lipid membranes, Acta Mech. Sin. 37, 138 (2021).

    Article  MathSciNet  Google Scholar 

  12. H. Honda, M. Tanemura, and T. Nagai, A three-dimensional vertex dynamics cell model of space-filling polyhedra simulating cell behavior in a cell aggregate, J. Theor. Biol. 226, 439 (2004).

    Article  MathSciNet  Google Scholar 

  13. A. G. Fletcher, M. Osterfield, R. E. Baker, and S. Y. Shvartsman, Vertex models of epithelial morphogenesis, Biophys. J. 106, 2291 (2014).

    Article  Google Scholar 

  14. S. Alt, P. Ganguly, and G. Salbreux, Vertex models: from cell mechanics to tissue morphogenesis, Phil. Trans. R. Soc. B 372, 20150520 (2017).

    Article  Google Scholar 

  15. D. Bi, J. H. Lopez, J. M. Schwarz, and M. L. Manning, A density-independent rigidity transition in biological tissues, Nat. Phys. 11, 1074 (2015).

    Article  Google Scholar 

  16. S. Z. Lin, B. Li, and X. Q. Feng, A dynamic cellular vertex model of growing epithelial tissues, Acta Mech. Sin. 33, 250 (2017).

    Article  MathSciNet  Google Scholar 

  17. S. Z. Lin, B. Li, G. Lan, and X. Q. Feng, Activation and synchronization of the oscillatory morphodynamics in multicellular monolayer, Proc. Natl. Acad. Sci. USA 114, 8157 (2017).

    Article  Google Scholar 

  18. M. Osterfield, X. X. Du, T. Schupbach, E. Wieschaus, and S. Y. Shvartsman, Three-dimensional epithelial morphogenesis in the developing Drosophila egg, Dev. Cell 24, 400 (2013).

    Article  Google Scholar 

  19. J. Rozman, M. Krajnc, and P. Ziherl, Collective cell mechanics of epithelial shells with organoid-like morphologies, Nat. Commun. 11, 3805 (2020).

    Article  Google Scholar 

  20. S. Okuda, Y. Inoue, M. Eiraku, T. Adachi, and Y. Sasai, Vertex dynamics simulations of viscosity-dependent deformation during tissue morphogenesis, Biomech. Model. Mechanobiol. 14, 413 (2015).

    Article  Google Scholar 

  21. M. Inaki, R. Hatori, N. Nakazawa, T. Okumura, T. Ishibashi, J. Ki-kuta, M. Ishii, K. Matsuno, and H. Honda, Chiral cell sliding drives left-right asymmetric organ twisting, eLife 7, e32506 (2018).

    Article  Google Scholar 

  22. T. Hirashima, and T. Adachi, Polarized cellular mechanoresponse system for maintaining radial size in developing epithelial tubes, Development 146, dev.181206 (2019).

    Article  Google Scholar 

  23. D. Boocock, T. Hirashima, and E. Hannezo, Interplay between mechanochemical patterning and glassy dynamics in cellular mono-layers, PRX Life 1, 013001 (2023).

    Article  Google Scholar 

  24. S. Okuda, T. Miura, Y. Inoue, T. Adachi, and M. Eiraku, Combining Turing and 3D vertex models reproduces autonomous multicellular morphogenesis with undulation, tubulation, and branching, Sci. Rep. 8, 2386 (2018).

    Article  Google Scholar 

  25. J. Schnakenberg, Simple chemical reaction systems with limit cycle behaviour, J. Theor. Biol. 81, 389 (1979).

    Article  MathSciNet  Google Scholar 

  26. A. L. Krause, M. A. Ellis, and R. A. Van Gorder, Influence of curvature, growth, and anisotropy on the evolution of turing patterns on growing manifolds, Bull. Math. Biol. 81, 759 (2019).

    Article  MathSciNet  Google Scholar 

  27. S. Okuda, Y. Inoue, M. Eiraku, Y. Sasai, and T. Adachi, Reversible network reconnection model for simulating large deformation in dynamic tissue morphogenesis, Biomech. Model. Mechanobiol. 12, 627 (2013).

    Article  Google Scholar 

  28. G. Salbreux, G. Charras, and E. Paluch, Actin cortex mechanics and cellular morphogenesis, Trends Cell Biol. 22, 536 (2012).

    Article  Google Scholar 

  29. N. Hino, L. Rossetti, A. Marín-Llauradó, K. Aoki, X. Trepat, M. Matsuda, and T. Hirashima, ERK-mediated mechanochemical waves direct collective cell polarization, Dev. Cell 53, 646 (2020).

    Article  Google Scholar 

  30. P. Ender, P. A. Gagliardi, M. Dobrzyński, A. Frismantiene, C. Dessauges, T. Höhener, M. A. Jacques, A. R. Cohen, and O. Pertz, Spatiotemporal control of ERK pulse frequency coordinates fate decisions during mammary acinar morphogenesis, Dev. Cell 57, 2153 (2022).

    Article  Google Scholar 

  31. R. J. Metzger, and M. A. Krasnow, Genetic control of branching morphogenesis, Science 284, 1635 (1999).

    Article  Google Scholar 

  32. T. Hirashima, Y. Iwasa, and Y. Morishita, Mechanisms for split localization of Fgf10 expression in early lung development, Dev. Dyn 238, 2813 (2009)

    Article  Google Scholar 

  33. V. D. Varner, and C. M. Nelson, Computational models of airway branching morphogenesis, Semin. Cell Dev. Biol. 67, 170 (2017).

    Article  Google Scholar 

  34. X. Zhu, and H. Yang, Turing Instability-driven biofabrication of branching tissue structures: A dynamic simulation and analysis based on the reaction-diffusion mechanism, Micromachines 9, 109 (2018).

    Article  Google Scholar 

  35. A. Nakamasu, and T. Higaki, Theoretical models for branch formation in plants, J. Plant Res. 132, 325 (2019).

    Article  Google Scholar 

Download references

Acknowledgements

This work was supported by the National Natural Science Foundation of China (Grant Nos. 12272202 and 11921002).

Author information

Authors and Affiliations

Authors

Contributions

Author contributions Bo Li conceived the project and designed the research. Pengyu Yu performed theoretical modeling and numerical simulations. Pengyu Yu and Bo Li analyzed the data, discussed the results, and wrote the paper.

Corresponding author

Correspondence to Bo Li  (李博).

Ethics declarations

Conflict of interest On behalf of all authors, the corresponding author states that there is no conflict of interest.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Yu, P., Li, B. Three-dimensional morphogenesis of epithelial tubes. Acta Mech. Sin. 40, 623297 (2024). https://doi.org/10.1007/s10409-023-23297-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • DOI: https://doi.org/10.1007/s10409-023-23297-x

Keywords

Navigation