A nuclear jamming transition in vertebrate organogenesis
Source abstract
Abstract
Jamming of cell collectives and associated rigidity transitions have been shown to play a key role in tissue dynamics, structure and morphogenesis. Cellular jamming is controlled by cellular density and the mechanics of cell-cell contacts. However, the contribution of subcellular organelles to the physical state of the emergent tissue is unclear. Here we report a nuclear jamming transition in zebrafish retina and brain tissues, where physical interactions between highly packed nuclei restrict cellular movements and control tissue mechanics and architecture. Computational modelling suggests that the nuclear volume fraction and anisotropy of cells control the emerging tissue physical state. Analysis of tissue architecture, mechanics and nuclear movements during eye development show that retina tissues undergo a nuclear jamming transition as they form, with increasing nuclear packing leading to more ordered cellular arrangements, reminiscent of the crystalline cellular packings in the functional adult eye. Our results reveal an important role of the cell nucleus in tissue mechanics and architecture.
Source: europepmc · Quality: candidate unverified · Source record ↗
Research context
OpenAlex topics: Cellular Mechanics and Interactions · Microtubule and mitosis dynamics · Hippo pathway signaling and YAP/TAZ
SciVX discovery tags are terminology-based. OpenAlex topics are source-provided classifications.
References (58)
Show source-provided references
1. Heisenberg, C. P. & Bellaïche, Y. Forces in tissue morphogenesis and patterning. Cell 153, 948–962 (2013).10.1016/j.cell.2013.05.008 ↗
2. Guillot, C. & Lecuit, T. Mechanics of epithelial tissue homeostasis and morphogenesis. Science 340, 1185–1189 (2013).10.1126/science.1235249 ↗
3. Cohen, R. et al. Mechanical forces drive ordered patterning of hair cells in the mammalian inner ear. Nat. Commun. 11, 5137 (2020).10.1038/s41467-020-18894-8 ↗
4. Salbreux, G., Barthel, L. K., Raymond, P. A. & Lubensky, D. K. Coupling mechanical deformations and planar cell polarity to create regular patterns in the zebrafish retina. PLoS Comput. Biol. 8, e1002618 (2012).10.1371/journal.pcbi.1002618 ↗
5. Kim, S., Cassidy, J. J., Yang, B., Carthew, R. W. & Hilgenfeldt, S. Hexagonal patterning of the insect compound eye: facet area variation, defects, and disorder. Biophys. J. 111, 2735–2746 (2016).10.1016/j.bpj.2016.11.004 ↗
6. Mongera, A. et al. A fluid-to-solid jamming transition underlies vertebrate body axis elongation. Nature 561, 401–405 (2018).10.1038/s41586-018-0479-2 ↗
7. Kim, S., Pochitaloff, M., Stooke-Vaughan, G. A. & Campàs, O. Embryonic tissues as active foams. Nat. Phys. 17, 859–866 (2021).10.1038/s41567-021-01215-1 ↗
8. Petridou, N. I., Grigolon, S., Salbreux, G., Hannezo, E. & Heisenberg, C.-P. Fluidization-mediated tissue spreading by mitotic cell rounding and non-canonical Wnt signalling. Nat. Cell Biol. 21, 169–178 (2019).10.1038/s41556-018-0247-4 ↗
9. Lenne, P. F. & Trivedi, V. Sculpting tissues by phase transitions. Nat. Commun. 13, 664 (2022).10.1038/s41467-022-28151-9 ↗
10. Atia, L. et al. Geometric constraints during epithelial jamming. Nat. Phys. 14, 613–620 (2018).10.1038/s41567-018-0089-9 ↗
11. Parada, C. et al. Mechanical feedback defines organizing centers to drive digit emergence. Dev. Cell 57, 854–866.e6 (2022).10.1016/j.devcel.2022.03.004 ↗
12. Shelton, E. R. et al. Stress-driven tissue fluidization physically segments vertebrate somites. Preprint at BioRxiv https://doi.org/10.1101/2021.03.27.437325 (2021).10.1101/2021.03.27.437325 ↗
13. Lawton, A. K. et al. Regulated tissue fluidity steers zebrafish body elongation. Development 140, 573–582 (2013).10.1242/dev.090381 ↗
14. Bénaźeraf, B. et al. A random cell motility gradient downstream of FGF controls elongation of an amniote embryo. Nature 466, 248–252 (2010).10.1038/nature09151 ↗
15. Schotz, E. M., Lanio, M., Talbot, J. A. & Manning, M. L. Glassy dynamics in three-dimensional embryonic tissues. J. R. Soc. Interface 10, 20130726–20130726 (2013).10.1098/rsif.2013.0726 ↗
16. Yanagida, A. et al. Cell surface fluctuations regulate early embryonic lineage sorting. Cell 185, 777–793.e20 (2022).10.1016/j.cell.2022.01.022 ↗
17. Oswald, L., Grosser, S., Smith, D. M. & Käs, J. A. Jamming transitions in cancer. J. Phys. D: Appl. Phys. 50, 483001–483018 (2017).10.1088/1361-6463/aa8e83 ↗
18. Palamidessi, A. et al. Unjamming overcomes kinetic and proliferation arrest in terminally differentiated cells and promotes collective motility of carcinoma. Nat. Mater. 80, 1252–1263 (2019).10.1038/s41563-019-0425-1 ↗
19. Kang, W. et al. A novel jamming phase diagram links tumor invasion to non-equilibrium phase separation. iScience 24, 103252 (2021).10.1016/j.isci.2021.103252 ↗
20. Campàs, O., Noordstra, I. & Yap, A. S. Adherens junctions as molecular regulators of emergent tissue mechanics. Nat. Rev. Mol. Cell Biol. 252–269 (2023).10.1038/s41580-023-00688-7 ↗
21. Bonn, D., Denn, M. M., Berthier, L., Divoux, T. & Manneville, S. Yield stress materials in soft condensed matter. Rev. Mod. Phys. 89, 15 (2017).10.1103/RevModPhys.89.035005 ↗
22. Angelini, T. E. et al. Glass-like dynamics of collective cell migration. Proc. Natl Acad. Sci. USA 108, 4714–4719 (2011).10.1073/pnas.1010059108 ↗
23. Park, J.-A. et al. Unjamming and cell shape in the asthmatic airway epithelium. Nat. Mater. 14, 1040–1048 (2015).10.1038/nmat4357 ↗
24. Krajnc, M. Solid–fluid transition and cell sorting in epithelia with junctional tension fluctuations. Soft Matter 16, 3209–3215 (2020).10.1039/C9SM02310K ↗
25. Krajnc, M., Dasgupta, S., Ziherl, P. & Prost, J. Fluidization of epithelial sheets by active cell rearrangements. Phys. Rev. E 98, 022409 (2018).10.1103/PhysRevE.98.022409 ↗
26. Boromand, A., Signoriello, A., Ye, F., O’Hern, C. S. & Shattuck, M. D. Jamming of deformable polygons. Phys. Rev. Lett. 121, 248003 (2018).10.1103/PhysRevLett.121.248003 ↗
27. Bi, D., Lopez, J. H., Schwarz, J. M. & Manning, M. L. A density-independent rigidity transition in biological tissues. Nat. Phys. 11, 1074–1079 (2015).10.1038/nphys3471 ↗
28. Bi, D., Yang, X., Marchetti, M. C. & Manning, M. L. Motility-driven glass and jamming transitions in biological tissues. Phys. Rev. X 6, 021011 (2016).
29. Farhadifar, R., Röper, J.-C., Aigouy, B., Eaton, S. & Jülicher, F. The influence of cell mechanics, cell-cell interactions, and proliferation on epithelial packing. Curr. Biol. 17, 2095–2104 (2007).10.1016/j.cub.2007.11.049 ↗
30. Lammerding, J. Mechanics of the nucleus. Compr. Physiol. 1, 783–807 (2011).10.1002/cphy.c100038 ↗
31. Jevtić, P., Edens, L. J., Vuković, L. D. & Levy, D. L. Sizing and shaping the nucleus: mechanisms and significance. Curr. Opin. Cell Biol. 28, 16–27 (2014).10.1016/j.ceb.2014.01.003 ↗
32. Chow, K.-H., Factor, R. E. & Ullman, K. S. The nuclear envelope environment and its cancer connections. Nat. Rev. Cancer 12, 196–209 (2012).10.1038/nrc3219 ↗
33. Dutta, S., Djabrayan, N. J.-V., Torquato, S., Shvartsman, S. Y. & Krajnc, M. Self-similar dynamics of nuclear packing in the early Drosophila embryo. Biophys. J. 117, 743–750 (2019).10.1016/j.bpj.2019.07.009 ↗
34. Donoughe, S., Hoffmann, J., Nakamura, T., Rycroft, C. H. & Extavour, C. G. Nuclear speed and cycle length co-vary with local density during syncytial blastoderm formation in a cricket. Nat. Commun. 13, 3889 (2022).10.1038/s41467-022-31212-8 ↗
35. Kaiser, F. et al. Mechanical model of nuclei ordering in Drosophila embryos reveals dilution of stochastic forces. Biophys. J. 114, 1730–1740 (2018).10.1016/j.bpj.2018.02.018 ↗
36. Azizi, A. et al. Nuclear crowding and nonlinear diffusion during interkinetic nuclear migration in the zebrafish retina. eLife 9, e58635 (2020).10.7554/eLife.58635 ↗
37. Hecht, S. et al. Mechanical constraints to cell-cycle progression in a pseudostratified epithelium. Curr. Biol. 32, 2076–2083.e2 (2022).10.1016/j.cub.2022.03.004 ↗
38. Fuhrmann, S. Chapter three—eye morphogenesis and patterning of the optic vesicle. Curr. Top. Dev. Biol. 93, 61–84 (2010).10.1016/B978-0-12-385044-7.00003-5 ↗
39. Agathocleous, M. & Harris, W. A. From progenitors to differentiated cells in the vertebrate retina. Annu Rev. Cell Dev. Biol. 25, 45–69 (2009).10.1146/annurev.cellbio.042308.113259 ↗
40. Dowling, J. E. The Retina: An Approachable Part of the Brain, Revised Edition (Harvard Univ. Press, 2012).10.2307/j.ctv31zqj2d ↗
41. Galli-Resta, L. et al. The genesis of retinal architecture: an emerging role for mechanical interactions? Prog. Retin. Eye Res. 27, 260–283 (2008).10.1016/j.preteyeres.2008.02.001 ↗
42. Amini, R. et al. Amoeboid-like migration ensures correct horizontal cell layer formation in the developing vertebrate retina. eLife 11, e76408 (2022).10.7554/eLife.76408 ↗
43. Lammerding, J. et al. Lamins A and C but not lamin B1 regulate nuclear mechanics. J. Biol. Chem. 281, 25768–25780 (2006).10.1074/jbc.M513511200 ↗
44. Serwane, F. et al. In vivo quantification of spatially varying mechanical properties in developing tissues. Nat. Methods 14, 181–186 (2017).10.1038/nmeth.4101 ↗
45. Mongera, A. et al. Mechanics of the cellular microenvironment as probed by cells in vivo during zebrafish presomitic mesoderm differentiation. Nat. Mater. 22, 135–143 (2023).10.1038/s41563-022-01433-9 ↗
46. Maia-Gil, M. et al. Nuclear deformability facilitates apical nuclear migration in the developing zebrafish retina. Preprint at bioRxiv https://doi.org/10.1101/2024.04.04.588091 (2024).10.1101/2024.04.04.588091 ↗
47. Mueller, T. & Wullimann, M. Atlas of Early Zebrafish Brain Development: A Tool for Molecular Neurogenetics (Academic Press, 2016).
48. Suzuki, D. G., Pérez-Fernández, J., Wibble, T., Kardamakis, A. A. & Grillner, S. The role of the optic tectum for visually evoked orienting and evasive movements. Proc. Natl Acad. Sci. USA 116, 15272–15281 (2019).10.1073/pnas.1907962116 ↗
49. Lomakin, A. J. et al. The nucleus acts as a ruler tailoring cell responses to spatial constraints. Science 370, eaba2894 (2020).10.1126/science.aba2894 ↗
50. Venturini, V. et al. The nucleus measures shape changes for cellular proprioception to control dynamic cell behavior. Science 370, eaba2644 (2020).10.1126/science.aba2644 ↗
51. Nüsslein-Volhard, C. & Dahm, R. Zebrafish (Oxford Univ. Press, 2002).10.1093/oso/9780199638086.001.0001 ↗
52. Cooper, M. S. et al. Visualizing morphogenesis in transgenic zebrafish embryos using BODIPY TR methyl ester dye as a vital counterstain for GFP. Dev. Dyn. 232, 359–368 (2005).10.1002/dvdy.20252 ↗
53. Xiong, F. et al. Specified neural progenitors sort to form sharp domains after noisy Shh signaling. Cell 153, 550–561 (2013).10.1016/j.cell.2013.03.023 ↗
54. Knopf, F. et al. Bone regenerates via dedifferentiation of osteoblasts in the zebrafish fin. Dev. Cell 20, 713–724 (2011).10.1016/j.devcel.2011.04.014 ↗
55. Pauls, S., Geldmacher-Voss, B. & Campos-Ortega, J. A. A zebrafish histone variant H2A.F/Z and a transgenic H2A.F/Z:GFP fusion protein for in vivo studies of embryonic development. Dev. Genes Evol. 211, 603–610 (2001).10.1007/s00427-001-0196-x ↗
56. Icha, J. et al. Using light sheet fluorescence microscopy to image zebrafish eye development. J. Vis. Exp. 110, e53966 (2016).
57. Tinevez, J.-Y. et al. TrackMate: an open and extensible platform for single-particle tracking. Methods 115, 80–90 (2017).10.1016/j.ymeth.2016.09.016 ↗
58. Lim, I. et al. Fluorous soluble cyanine dyes for visualizing perfluorocarbons in living systems. J. Am. Chem. Soc. 142, 16072–16081 (2020).10.1021/jacs.0c07761 ↗