NF2/merlin is a novel negative regulator of mTOR complex 1, and activation of mTORC1 is associated with meningioma and schwannoma growth

Mol Cell Biol. 2009 Aug;29(15):4250-61. doi: 10.1128/MCB.01581-08. Epub 2009 May 18.

Abstract

Inactivating mutations of the neurofibromatosis 2 (NF2) gene, NF2, result predominantly in benign neurological tumors, schwannomas and meningiomas, in humans; however, mutations in murine Nf2 lead to a broad spectrum of cancerous tumors. The tumor-suppressive function of the NF2 protein, merlin, a membrane-cytoskeleton linker, remains unclear. Here, we identify the mammalian target of rapamycin complex 1 (mTORC1) as a novel mediator of merlin's tumor suppressor activity. Merlin-deficient human meningioma cells and merlin knockdown arachnoidal cells, the nonneoplastic cell counterparts of meningiomas, exhibit rapamycin-sensitive constitutive mTORC1 activation and increased growth. NF2 patient tumors and Nf2-deficient mouse embryonic fibroblasts demonstrate elevated mTORC1 signaling. Conversely, the exogenous expression of wild-type merlin isoforms, but not a patient-derived L64P mutant, suppresses mTORC1 signaling. Merlin does not regulate mTORC1 via the established mechanism of phosphoinositide 3-kinase-Akt or mitogen-activated protein kinase/extracellular signal-regulated kinase-mediated TSC2 inactivation and may instead regulate TSC/mTOR signaling in a novel fashion. In conclusion, the deregulation of mTORC1 activation underlies the aberrant growth and proliferation of NF2-associated tumors and may restrain the growth of these lesions through negative feedback mechanisms, suggesting that rapamycin in combination with phosphoinositide 3-kinase inhibitors may be therapeutic for NF2.

Publication types

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

MeSH terms

  • Animals
  • Antibiotics, Antineoplastic / pharmacology
  • Arachnoid / cytology
  • Arachnoid / drug effects
  • Arachnoid / metabolism
  • Cell Cycle
  • Cell Line
  • Cell Proliferation*
  • Cells, Cultured
  • Fibroblasts / cytology
  • Fibroblasts / drug effects
  • Fibroblasts / metabolism
  • Flow Cytometry
  • Humans
  • Immunoblotting
  • Mechanistic Target of Rapamycin Complex 1
  • Meningioma / genetics
  • Meningioma / metabolism
  • Meningioma / pathology
  • Mice
  • Mice, Knockout
  • Multiprotein Complexes
  • Neurilemmoma / genetics
  • Neurilemmoma / metabolism
  • Neurilemmoma / pathology
  • Neurofibromin 2 / genetics
  • Neurofibromin 2 / metabolism*
  • Phosphatidylinositol 3-Kinases / metabolism
  • Proteins
  • Proto-Oncogene Proteins c-akt / metabolism
  • RNA, Small Interfering / genetics
  • Signal Transduction / drug effects
  • Sirolimus / pharmacology
  • TOR Serine-Threonine Kinases
  • Transcription Factors / genetics
  • Transcription Factors / metabolism*
  • Transfection
  • Tumor Cells, Cultured

Substances

  • Antibiotics, Antineoplastic
  • Multiprotein Complexes
  • Neurofibromin 2
  • Proteins
  • RNA, Small Interfering
  • Transcription Factors
  • Mechanistic Target of Rapamycin Complex 1
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Sirolimus