Mechanism of mutant calreticulin-mediated activation of the thrombopoietin receptor in cancers

J Cell Biol. 2021 Jul 5;220(7):e202009179. doi: 10.1083/jcb.202009179.

Abstract

Myeloproliferative neoplasms (MPNs) are frequently driven by mutations within the C-terminal domain (C-domain) of calreticulin (CRT). CRTDel52 and CRTIns5 are recurrent mutations. Oncogenic transformation requires both mutated CRT and the thrombopoietin receptor (Mpl), but the molecular mechanism of CRT-mediated constitutive activation of Mpl is unknown. We show that the acquired C-domain of CRTDel52 mediates both Mpl binding and disulfide-linked CRTDel52 dimerization. Cysteine mutations within the novel C-domain (C400A and C404A) and the conserved N-terminal domain (N-domain; C163A) of CRTDel52 are required to reduce disulfide-mediated dimers and multimers of CRTDel52. Based on these data and published structures of CRT oligomers, we identify an N-domain dimerization interface relevant to both WT CRT and CRTDel52. Elimination of disulfide bonds and ionic interactions at both N-domain and C-domain dimerization interfaces is required to abrogate the ability of CRTDel52 to mediate cell proliferation via Mpl. Thus, MPNs exploit a natural dimerization interface of CRT combined with C-domain gain of function to achieve cell transformation.

Publication types

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

MeSH terms

  • Calreticulin / genetics*
  • Carcinogenesis / genetics
  • Humans
  • Mutation / genetics
  • Myeloproliferative Disorders / genetics*
  • Myeloproliferative Disorders / pathology
  • Neoplasms / genetics
  • Neoplasms / pathology
  • Receptors, Thrombopoietin / genetics*
  • Signal Transduction / genetics
  • Thrombopoietin / genetics

Substances

  • Calreticulin
  • Receptors, Thrombopoietin
  • MPL protein, human
  • Thrombopoietin