Kinase-mediated RAS signaling via membraneless cytoplasmic protein granules

Cell. 2021 May 13;184(10):2649-2664.e18. doi: 10.1016/j.cell.2021.03.031. Epub 2021 Apr 12.

Abstract

Receptor tyrosine kinase (RTK)-mediated activation of downstream effector pathways such as the RAS GTPase/MAP kinase (MAPK) signaling cascade is thought to occur exclusively from lipid membrane compartments in mammalian cells. Here, we uncover a membraneless, protein granule-based subcellular structure that can organize RTK/RAS/MAPK signaling in cancer. Chimeric (fusion) oncoproteins involving certain RTKs including ALK and RET undergo de novo higher-order assembly into membraneless cytoplasmic protein granules that actively signal. These pathogenic biomolecular condensates locally concentrate the RAS activating complex GRB2/SOS1 and activate RAS in a lipid membrane-independent manner. RTK protein granule formation is critical for oncogenic RAS/MAPK signaling output in these cells. We identify a set of protein granule components and establish structural rules that define the formation of membraneless protein granules by RTK oncoproteins. Our findings reveal membraneless, higher-order cytoplasmic protein assembly as a distinct subcellular platform for organizing oncogenic RTK and RAS signaling.

Keywords: ALK; MAPK; RAS; RET; anaplastic lymphoma kinase; biomolecular condensate; gene fusion; kinase; protein granule; receptor tyrosine kinase.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / metabolism
  • Biomolecular Condensates / metabolism*
  • Cytoplasmic Granules / metabolism*
  • Enzyme Activation
  • GRB2 Adaptor Protein / genetics
  • GRB2 Adaptor Protein / metabolism
  • HEK293 Cells
  • Humans
  • Neoplasms / metabolism*
  • Oncogene Proteins, Fusion / metabolism*
  • SOS1 Protein / metabolism
  • Signal Transduction
  • ras Proteins / metabolism*

Substances

  • Adaptor Proteins, Signal Transducing
  • EML4-ALK fusion protein, human
  • GAB1 protein, human
  • GRB2 Adaptor Protein
  • GRB2 protein, human
  • Oncogene Proteins, Fusion
  • SOS1 Protein
  • SOS1 protein, human
  • ras Proteins