A proteomic approach to identify endosomal cargoes controlling cancer invasiveness

J Cell Sci. 2017 Feb 15;130(4):697-711. doi: 10.1242/jcs.190835. Epub 2017 Jan 6.

Abstract

We have previously shown that Rab17, a small GTPase associated with epithelial polarity, is specifically suppressed by ERK2 (also known as MAPK1) signalling to promote an invasive phenotype. However, the mechanisms through which Rab17 loss permits invasiveness, and the endosomal cargoes that are responsible for mediating this, are unknown. Using quantitative mass spectrometry-based proteomics, we have found that knockdown of Rab17 leads to a highly selective reduction in the cellular levels of a v-SNARE (Vamp8). Moreover, proteomics and immunofluorescence indicate that Vamp8 is associated with Rab17 at late endosomes. Reduced levels of Vamp8 promote transition between ductal carcinoma in situ (DCIS) and a more invasive phenotype. We developed an unbiased proteomic approach to elucidate the complement of receptors that redistributes between endosomes and the plasma membrane, and have pin-pointed neuropilin-2 (NRP2) as a key pro-invasive cargo of Rab17- and Vamp8-regulated trafficking. Indeed, reduced Rab17 or Vamp8 levels lead to increased mobilisation of NRP2-containing late endosomes and upregulated cell surface expression of NRP2. Finally, we show that NRP2 is required for the basement membrane disruption that accompanies the transition between DCIS and a more invasive phenotype.

Keywords: Breast cancer; Cell migration; Ductal carcinoma in situ; Invasion; Invasive ductal carcinoma; Late endosome; Neuropilin-2; Rab17; SILAC; Vamp8.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / metabolism
  • Breast Neoplasms / genetics
  • Breast Neoplasms / metabolism*
  • Breast Neoplasms / pathology*
  • Cell Line, Tumor
  • Endosomes / metabolism*
  • Female
  • Gene Knockdown Techniques
  • Humans
  • Intracellular Membranes / metabolism
  • Isotope Labeling
  • Models, Biological
  • Neoplasm Grading
  • Neoplasm Invasiveness
  • Neuropilin-2 / metabolism
  • Protein Binding
  • Protein Transport
  • Proteomics / methods*
  • R-SNARE Proteins / metabolism
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Receptors, Estrogen / metabolism
  • SNARE Proteins / metabolism
  • Survival Analysis
  • rab GTP-Binding Proteins / genetics
  • rab GTP-Binding Proteins / metabolism

Substances

  • Amino Acids
  • Neuropilin-2
  • R-SNARE Proteins
  • RNA, Messenger
  • Receptors, Estrogen
  • SNARE Proteins
  • VAMP8 protein, human
  • neuropilin-2, human
  • rab GTP-Binding Proteins