Deep nuclear invaginations are linked to cytoskeletal filaments - integrated bioimaging of epithelial cells in 3D culture

Danielle Jorgens, Jamie L. Inman, Michal Wojcik, Claire Robertson, Hildur Palsdottir, Wen Ting Tsai, Haina Huang, Alexandre Bruni-Cardoso, Claudia Lopez, Mina J. Bissell, Ke Xu, Manfred Auer

Research output: Contribution to journalArticle

17 Citations (Scopus)

Abstract

The importance of context in regulation of gene expression is now an accepted principle; yet the mechanism by which the microenvironment communicates with the nucleus and chromatin in healthy tissues is poorly understood. A functional role for nuclear and cytoskeletal architecture is suggested by the phenotypic differences observed between epithelial and mesenchymal cells. Capitalizing on recent advances in cryogenic techniques, volume electron microscopy and super-resolution light microscopy, we studied human mammary epithelial cells in three-dimensional (3D) cultures forming growtharrested acini. Intriguingly, we found deep nuclear invaginations and tunnels traversing the nucleus, encasing cytoskeletal actin and/or intermediate filaments, which connect to the outer nuclear envelope. The cytoskeleton is also connected both to other cells through desmosome adhesion complexes and to the extracellular matrix through hemidesmosomes. This finding supports a physical and/or mechanical link from the desmosomes and hemidesmosomes to the nucleus, which had previously been hypothesized but now is visualized for the first time. These unique structures, including the nuclear invaginations and the cytoskeletal connectivity to the cell nucleus, are consistent with a dynamic reciprocity between the nucleus and the outside of epithelial cells and tissues.

Original languageEnglish (US)
Pages (from-to)177-189
Number of pages13
JournalJournal of Cell Science
Volume130
Issue number1
DOIs
StatePublished - 2017

Fingerprint

Cytoskeleton
Hemidesmosomes
Desmosomes
Epithelial Cells
Intermediate Filaments
Nuclear Envelope
Gene Expression Regulation
Cell Nucleus
Actin Cytoskeleton
Chromatin
Extracellular Matrix
Microscopy
Electron Microscopy
Breast
Epithelium
Light

Keywords

  • Cytoskeleton
  • Extracellular matrix
  • Human mammary epithelial cells
  • Integrated bioimaging
  • Mechanotransduction
  • Nucleoplasmic reticulum

ASJC Scopus subject areas

  • Cell Biology

Cite this

Jorgens, D., Inman, J. L., Wojcik, M., Robertson, C., Palsdottir, H., Tsai, W. T., ... Auer, M. (2017). Deep nuclear invaginations are linked to cytoskeletal filaments - integrated bioimaging of epithelial cells in 3D culture. Journal of Cell Science, 130(1), 177-189. https://doi.org/10.1242/jcs.190967

Deep nuclear invaginations are linked to cytoskeletal filaments - integrated bioimaging of epithelial cells in 3D culture. / Jorgens, Danielle; Inman, Jamie L.; Wojcik, Michal; Robertson, Claire; Palsdottir, Hildur; Tsai, Wen Ting; Huang, Haina; Bruni-Cardoso, Alexandre; Lopez, Claudia; Bissell, Mina J.; Xu, Ke; Auer, Manfred.

In: Journal of Cell Science, Vol. 130, No. 1, 2017, p. 177-189.

Research output: Contribution to journalArticle

Jorgens, D, Inman, JL, Wojcik, M, Robertson, C, Palsdottir, H, Tsai, WT, Huang, H, Bruni-Cardoso, A, Lopez, C, Bissell, MJ, Xu, K & Auer, M 2017, 'Deep nuclear invaginations are linked to cytoskeletal filaments - integrated bioimaging of epithelial cells in 3D culture', Journal of Cell Science, vol. 130, no. 1, pp. 177-189. https://doi.org/10.1242/jcs.190967
Jorgens, Danielle ; Inman, Jamie L. ; Wojcik, Michal ; Robertson, Claire ; Palsdottir, Hildur ; Tsai, Wen Ting ; Huang, Haina ; Bruni-Cardoso, Alexandre ; Lopez, Claudia ; Bissell, Mina J. ; Xu, Ke ; Auer, Manfred. / Deep nuclear invaginations are linked to cytoskeletal filaments - integrated bioimaging of epithelial cells in 3D culture. In: Journal of Cell Science. 2017 ; Vol. 130, No. 1. pp. 177-189.
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