Coherent angular motion in the establishment of multicellular architecture of glandular tissues

Kandice Tanner, Hidetoshi Mori, Rana Mroue, Alexandre Bruni-Cardoso, Mina J. Bissell

Research output: Contribution to journalArticle

101 Citations (Scopus)

Abstract

Glandular tissues form ducts (tubes) and acini (spheres) in multicellular organisms. This process is best demonstrated in the organization of the ductal tree of the mammary gland and in 3D models of morphogenesis in culture. Here, we asked a fundamental question: How do single adult epithelial cells generate polarized acini when placed in a surrogate basement membrane 3D gel? Using human breast epithelial cells from either reduction mammoplasty or nonmalignant breast cell lines, we observed a unique cellular movement where single cells undergo multiple rotations and then maintain it cohesively as they divide to assemble into acini. This coherent angular motion (CAMo) was observed in both primary cells and breast cell lines. If CAMo was disrupted, the final geometry was not a sphere. The malignant counterparts of the human breast cell lines in 3D were randomly motile, did not display CAMo, and did not form spheres. Upon "phenotypic reversion" of malignant cells, both CAMo and spherical architecture were restored. We show that cell-cell adhesion and tissue polarity are essential for the formation of acini and link the functional relevance of CAMo to the establishment of spherical architecture rather than to multicellular aggregation or growth. We propose that CAMo is an integral step in the formation of the tissue architecture and that its disruption is involved in malignant transformation.

Original languageEnglish (US)
Pages (from-to)1973-1978
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume109
Issue number6
DOIs
StatePublished - Feb 7 2012
Externally publishedYes

Fingerprint

Breast
Cell Line
Epithelial Cells
Mammaplasty
Human Mammary Glands
Morphogenesis
Basement Membrane
Cell Adhesion
Cell Movement
Gels
Growth

Keywords

  • Actin dynamics
  • Cancer
  • Cell migration
  • Cellular rotation
  • Multicellular assembly

ASJC Scopus subject areas

  • General

Cite this

Coherent angular motion in the establishment of multicellular architecture of glandular tissues. / Tanner, Kandice; Mori, Hidetoshi; Mroue, Rana; Bruni-Cardoso, Alexandre; Bissell, Mina J.

In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 109, No. 6, 07.02.2012, p. 1973-1978.

Research output: Contribution to journalArticle

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