Organelle Specific O-Glycosylation Drives MMP14 Activation, Tumor Growth, and Metastasis

Cancer Cell. 2017 Nov 13;32(5):639-653.e6. doi: 10.1016/j.ccell.2017.10.001.

Abstract

Cancers grow within tissues through molecular mechanisms still unclear. Invasiveness correlates with perturbed O-glycosylation, a covalent modification of cell-surface proteins. Here, we show that, in human and mouse liver cancers, initiation of O-glycosylation by the GALNT glycosyl-transferases increases and shifts from the Golgi to the endoplasmic reticulum (ER). In a mouse liver cancer model, expressing an ER-targeted GALNT1 (ER-G1) massively increased tumor expansion, with median survival reduced from 23 to 10 weeks. In vitro cell growth was unaffected, but ER-G1 strongly enabled matrix degradation and tissue invasion. Unlike its Golgi-localized counterpart, ER-G1 glycosylates the matrix metalloproteinase MMP14, a process required for tumor expansion. Together, our results indicate that GALNTs strongly promote liver tumor growth after relocating to the ER.

Keywords: GALA; GALNTs; MMP14; MT1-MMP; O-glycosylation; Tn antigen; invasion; membrane trafficking; metastasis; tumor growth.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Blotting, Western
  • Cell Proliferation / genetics
  • Endoplasmic Reticulum / metabolism*
  • Gene Expression Regulation, Neoplastic
  • Glycosylation
  • Golgi Apparatus / metabolism*
  • Hep G2 Cells
  • Humans
  • Liver Neoplasms / genetics
  • Liver Neoplasms / metabolism*
  • Liver Neoplasms / pathology
  • Male
  • Matrix Metalloproteinase 14 / genetics
  • Matrix Metalloproteinase 14 / metabolism*
  • Mice, Inbred C57BL
  • N-Acetylgalactosaminyltransferases / genetics
  • N-Acetylgalactosaminyltransferases / metabolism
  • Neoplasm Metastasis
  • Polypeptide N-acetylgalactosaminyltransferase
  • Reverse Transcriptase Polymerase Chain Reaction

Substances

  • N-Acetylgalactosaminyltransferases
  • Matrix Metalloproteinase 14