The EMT activator ZEB1 accelerates endosomal trafficking to establish a polarity axis in lung adenocarcinoma cells

Nat Commun. 2021 Nov 3;12(1):6354. doi: 10.1038/s41467-021-26677-y.

Abstract

Epithelial-to-mesenchymal transition (EMT) is a transcriptionally governed process by which cancer cells establish a front-rear polarity axis that facilitates motility and invasion. Dynamic assembly of focal adhesions and other actin-based cytoskeletal structures on the leading edge of motile cells requires precise spatial and temporal control of protein trafficking. Yet, the way in which EMT-activating transcriptional programs interface with vesicular trafficking networks that effect cell polarity change remains unclear. Here, by utilizing multiple approaches to assess vesicular transport dynamics through endocytic recycling and retrograde trafficking pathways in lung adenocarcinoma cells at distinct positions on the EMT spectrum, we find that the EMT-activating transcription factor ZEB1 accelerates endocytosis and intracellular trafficking of plasma membrane-bound proteins. ZEB1 drives turnover of the MET receptor tyrosine kinase by hastening receptor endocytosis and transport to the lysosomal compartment for degradation. ZEB1 relieves a plus-end-directed microtubule-dependent kinesin motor protein (KIF13A) and a clathrin-associated adaptor protein complex subunit (AP1S2) from microRNA-dependent silencing, thereby accelerating cargo transport through the endocytic recycling and retrograde vesicular pathways, respectively. Depletion of KIF13A or AP1S2 mitigates ZEB1-dependent focal adhesion dynamics, front-rear axis polarization, and cancer cell motility. Thus, ZEB1-dependent transcriptional networks govern vesicular trafficking dynamics to effect cell polarity change.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Actins / metabolism
  • Adaptor Protein Complex sigma Subunits
  • Adenocarcinoma of Lung / metabolism
  • Cell Line, Tumor
  • Cell Polarity
  • Cytoskeleton / metabolism
  • Endocytosis
  • Endosomes / metabolism*
  • Epithelial-Mesenchymal Transition / genetics*
  • Epithelial-Mesenchymal Transition / physiology*
  • Focal Adhesions / metabolism
  • Gene Expression Regulation, Neoplastic
  • Humans
  • Kinesins
  • Lung Neoplasms / genetics
  • Lung Neoplasms / metabolism*
  • Membrane Proteins / metabolism
  • MicroRNAs / metabolism
  • Neoplasm Metastasis
  • Zinc Finger E-box-Binding Homeobox 1 / genetics*
  • Zinc Finger E-box-Binding Homeobox 1 / metabolism*

Substances

  • AP1S2 protein, human
  • Actins
  • Adaptor Protein Complex sigma Subunits
  • KIF13A protein, human
  • Membrane Proteins
  • MicroRNAs
  • ZEB1 protein, human
  • Zinc Finger E-box-Binding Homeobox 1
  • Kinesins