Acid sphingomyelinase is required for cell surface presentation of Met receptor tyrosine kinase in cancer cells

J Cell Sci. 2016 Nov 15;129(22):4238-4251. doi: 10.1242/jcs.191684. Epub 2016 Oct 6.

Abstract

Receptor tyrosine kinases (RTKs) are embedded in the lipid bilayer of the plasma membrane, but the specific roles of various lipids in cell signaling remain largely uncharacterized. We have previously found that acid sphingomyelinase (ASM; also known as SMPD1) regulates the conserved DAF-2 (the ortholog IGF-1R in mammals) RTK signaling pathway in Caenorhabditis elegans How ASM and its catalytic products, ceramides, control RTK signaling pathways remain unclear. Here, we report that ASM regulates the homeostasis of Met, an RTK that is frequently overexpressed in various cancers. Inactivation of ASM led to a rapid loss of Met from the plasma membrane, reduced Met phosphorylation and activation, and induced Met accumulation in the trans-Golgi network (TGN). However, trafficking of integrin β3 and vesicular stomatitis virus glycoprotein (VSVG) was largely unaffected. Knockdown of syntaxin 6 (STX6) also blocked the Golgi exit of Met. Depletion of either ASM or STX6 led to aberrant trafficking of Met to lysosomes, promoting its degradation. Our studies reveal that ASM and ceramides, together with STX6 and cholesterol, constitute a new regulatory mechanism for the exit of Met from the Golgi during its biosynthetic route, which is used to rapidly replenish and regulate the plasma membrane levels of Met in various cancer cells.

Keywords: ASM; Acid Sphingomyelinase; Ceramide; Golgi; Met; RTK; Receptor tyrosine kinase; SMPD1; STX6; Syntaxin 6.

Publication types

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

MeSH terms

  • Breast Neoplasms / metabolism
  • Breast Neoplasms / pathology
  • Cell Line, Tumor
  • Cell Membrane / metabolism*
  • Cholesterol / metabolism
  • Enzyme Activation
  • Female
  • Humans
  • Integrin beta3 / metabolism
  • Ligands
  • Melanoma / metabolism
  • Melanoma / pathology
  • Membrane Glycoproteins / metabolism
  • Neoplasms / metabolism*
  • Neoplasms / pathology
  • Phosphotyrosine / metabolism
  • Proto-Oncogene Proteins c-met / metabolism*
  • Qa-SNARE Proteins / metabolism
  • Receptor, IGF Type 1 / metabolism
  • Signal Transduction
  • Sphingomyelin Phosphodiesterase / metabolism*
  • Viral Envelope Proteins / metabolism
  • trans-Golgi Network / metabolism

Substances

  • G protein, vesicular stomatitis virus
  • Integrin beta3
  • Ligands
  • Membrane Glycoproteins
  • Qa-SNARE Proteins
  • STX6 protein, human
  • Viral Envelope Proteins
  • Phosphotyrosine
  • Cholesterol
  • Proto-Oncogene Proteins c-met
  • Receptor, IGF Type 1
  • Sphingomyelin Phosphodiesterase