Nuclear deformability facilitates apical nuclear migration in the developing zebrafish retina

Research output: Contribution to journalResearch articleContributedpeer-review

Contributors

  • Mariana Maia-Gil - , Instituto Gulbenkian de Ciência (Author)
  • Maria Gorjão - , Instituto Gulbenkian de Ciência (Author)
  • Roman Belousov - , European Molecular Biology Laboratory (EMBL) Heidelberg (Author)
  • Jaime A. Espina - , Instituto Gulbenkian de Ciência, Clusters of Excellence PoL: Physics of Life (Author)
  • João Coelho - , Instituto Gulbenkian de Ciência (Author)
  • Juliette Gouhier - , Instituto Gulbenkian de Ciência (Author)
  • Ana P. Ramos - , Instituto Gulbenkian de Ciência (Author)
  • Elias H. Barriga - , Clusters of Excellence PoL: Physics of Life, Physical Measurements and Manipulations of Living Systems, Instituto Gulbenkian de Ciência (Author)
  • Anna Erzberger - , European Molecular Biology Laboratory (EMBL) Heidelberg (Author)
  • Caren Norden - , Instituto Gulbenkian de Ciência (Author)

Abstract

Nuclear positioning is a crucial aspect of cell and developmental biology. One example is the apical movement of nuclei in neuroepithelia before mitosis, which is essential for proper tissue formation. While the cytoskeletal mechanisms that drive nuclei to the apical side have been explored, the influence of nuclear properties on apical nuclear migration is less understood. Nuclear properties, such as deformability, can be linked to lamin A/C expression levels, as shown in various in vitro studies. Interestingly, many nuclei in early development, including neuroepithelial nuclei, express only low levels of lamin A/C. Therefore, we investigated whether increased lamin A expression in the densely packed zebrafish retinal neuroepithelium affects nuclear deformability and, consequently, migration phenomena. We found that overexpressing lamin A in retinal nuclei increases nuclear stiffness, which in turn indeed impairs apical nuclear migration. Interestingly, nuclei that do not overexpress lamin A but are embedded in a stiffer lamin A-overexpressing environment also exhibit impaired apical nuclear migration, indicating that these effects can be cell non-autonomous. Additionally, in the less crowded hindbrain neuroepithelium, only minor effects on apical nuclear migration are observed. Together, this suggests that the material properties of the nucleus influence nuclear movements in a tissue-dependent manner.

Details

Original languageEnglish
Pages (from-to)5429-5443.e8
JournalCurrent biology
Volume34
Issue number23
Publication statusPublished - 2 Dec 2024
Peer-reviewedYes