RAB27B controls palmitoylation-dependent NRAS trafficking and signaling in myeloid leukemia

J Clin Invest. 2023 Jun 15;133(12):e165510. doi: 10.1172/JCI165510.

Abstract

RAS mutations are among the most prevalent oncogenic drivers in cancers. RAS proteins propagate signals only when associated with cellular membranes as a consequence of lipid modifications that impact their trafficking. Here, we discovered that RAB27B, a RAB family small GTPase, controlled NRAS palmitoylation and trafficking to the plasma membrane, a localization required for activation. Our proteomic studies revealed RAB27B upregulation in CBL- or JAK2-mutated myeloid malignancies, and its expression correlated with poor prognosis in acute myeloid leukemias (AMLs). RAB27B depletion inhibited the growth of CBL-deficient or NRAS-mutant cell lines. Strikingly, Rab27b deficiency in mice abrogated mutant but not WT NRAS-mediated progenitor cell growth, ERK signaling, and NRAS palmitoylation. Further, Rab27b deficiency significantly reduced myelomonocytic leukemia development in vivo. Mechanistically, RAB27B interacted with ZDHHC9, a palmitoyl acyltransferase that modifies NRAS. By regulating palmitoylation, RAB27B controlled c-RAF/MEK/ERK signaling and affected leukemia development. Importantly, RAB27B depletion in primary human AMLs inhibited oncogenic NRAS signaling and leukemic growth. We further revealed a significant correlation between RAB27B expression and sensitivity to MEK inhibitors in AMLs. Thus, our studies presented a link between RAB proteins and fundamental aspects of RAS posttranslational modification and trafficking, highlighting future therapeutic strategies for RAS-driven cancers.

Keywords: Cancer; Cell Biology; Hematology; Signal transduction.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • GTP Phosphohydrolases
  • Humans
  • Leukemia, Myeloid*
  • Lipoylation*
  • Membrane Proteins / genetics
  • Mice
  • Mitogen-Activated Protein Kinase Kinases
  • Proteomics
  • Signal Transduction

Substances

  • Mitogen-Activated Protein Kinase Kinases
  • NRAS protein, human
  • Membrane Proteins
  • GTP Phosphohydrolases