IDO1 involvement in mTOR pathway: a molecular mechanism of resistance to mTOR targeting in medulloblastoma

Oncotarget. 2016 Aug 16;7(33):52900-52911. doi: 10.18632/oncotarget.9284.

Abstract

Medulloblastoma (MB) is the most common malignant brain tumor in children. Despite therapeutic advancements, high-risk groups still present significant mortality. A deeper knowledge of the signaling pathways contributing to MB formation and aggressiveness would help develop new successful therapies. The target of rapamycin, mTOR signaling, is known to be involved in MB and is already targetable in the clinical setting. Furthermore, mTOR is a master metabolic regulator able to control cell growth versus autophagy decisions in conditions of amino-acid deprivation that can be due to IDO1 enzymatic activity. IDO1 has been also implicated in the regulation of inflammation, as well as of T cell-mediated immune responses, in a variety of pathological conditions, including brain tumors. In particular, IDO1 induces expansion of regulatory T-cells (Treg), preventing immune response against tumor cells. Analysis of 27 MB tissue specimens for the expression of both mTOR and IDO1 showed their widespread expression in all samples. Testing their cooperation in vitro, a significant involvement of IDO1 in mTOR immunogenic pathway was found, able to counteract the aim of rapamycin treatment. In MB cell lines, inhibition of mTOR strongly induced IDO1 expression and activity, corroborating its ability to recruit Treg cells in the tumor microenvironment. The mTOR/IDO1 cross talk was found to be strictly specific of MB cells. We demonstrated that mTOR pathway cross talks with IDO1 pathway to promote MB immune escape, possibly contributing to failure of mTOR- targeted therapy.

Keywords: CCL2; IDO1; MB; Treg; mTOR.

MeSH terms

  • Antibiotics, Antineoplastic / therapeutic use
  • Cell Line, Tumor
  • Cerebellar Neoplasms / drug therapy
  • Cerebellar Neoplasms / genetics*
  • Cerebellar Neoplasms / metabolism
  • Child
  • Drug Resistance, Neoplasm / genetics*
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / genetics*
  • Indoleamine-Pyrrole 2,3,-Dioxygenase / metabolism
  • Infant
  • Medulloblastoma / drug therapy
  • Medulloblastoma / genetics*
  • Medulloblastoma / metabolism
  • Molecular Targeted Therapy
  • Signal Transduction / drug effects
  • Signal Transduction / genetics*
  • Sirolimus / therapeutic use
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism
  • TOR Serine-Threonine Kinases / genetics*
  • TOR Serine-Threonine Kinases / metabolism
  • Tumor Microenvironment / drug effects
  • Tumor Microenvironment / genetics
  • Tumor Microenvironment / immunology

Substances

  • Antibiotics, Antineoplastic
  • IDO1 protein, human
  • Indoleamine-Pyrrole 2,3,-Dioxygenase
  • MTOR protein, human
  • TOR Serine-Threonine Kinases
  • Sirolimus