Targeting of active mTOR inhibits primary leukemia T cells and synergizes with cytotoxic drugs and signaling inhibitors

Exp Hematol. 2011 Apr;39(4):457-472.e3. doi: 10.1016/j.exphem.2011.01.005. Epub 2011 Jan 26.

Abstract

Objective: Rationally designed therapies aim at the specific disruption of critical signaling pathways activated by malignant transformation or signals from the tumor microenvironment. Because mammalian target of rapamycin (mTOR) is an important signal integrator and a key translational regulator, we evaluated its potential involvement in T-cell acute lymphoblastic leukemia (T-ALL) and whether mTOR blockade synergizes with chemotherapeutic agents or other signaling antagonists to inhibit primary leukemia T cells.

Materials and methods: mTOR signaling status was assessed using biochemical, immunostaining, and molecular regulation studies and functional assays performed to assess the impact of mTOR blockade on T-ALL proliferation, survival, and cell cycle.

Results: We observed that mTOR signaling is highly activated in all T-ALL patients tested, with phosphorylation of its downstream substrates eIF4G and S6 ribosomal protein. mTOR activation was detected in vivo and was further increased in vitro by stimulation with interleukin-7, a potentially leukemogenic cytokine normally produced by the bone marrow microenvironment. In T-ALL cells, mTOR blockade was associated with accumulation of the cyclin-dependent kinase inhibitor p27(kip1), which preferentially adopted a nuclear localization. Functional studies using rapamycin or CCI-779 showed a dominant inhibitory effect of mTOR blockade on interleukin-7-induced proliferation, survival, and cell-cycle progression of T-ALL cells. Furthermore, mTOR blockade markedly potentiated the antileukemia effects of dexamethasone and doxorubicin, and showed highly synergistic interactions in combination with specific inhibitors of phosphatidylinositol 3-kinase/Akt and Janus kinase 3 signaling.

Conclusions: This study shows activation of mTOR signaling in primary T-ALL cells evolving in the leukemic bone marrow, and supports the inclusion of mTOR antagonists in current therapeutic regimens for this cancer.

Publication types

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

MeSH terms

  • Antibiotics, Antineoplastic / pharmacology
  • Cell Cycle / drug effects
  • Cell Cycle / physiology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Cell Survival / physiology
  • Chromones / pharmacology
  • Dexamethasone / pharmacology
  • Doxorubicin / pharmacology
  • Drug Synergism
  • Enzyme Inhibitors / pharmacology
  • Eukaryotic Initiation Factor-4G / metabolism
  • Humans
  • Immunoblotting
  • Immunohistochemistry
  • Janus Kinase 3 / antagonists & inhibitors
  • Janus Kinase 3 / metabolism
  • Microscopy, Fluorescence
  • Morpholines / pharmacology
  • Phosphatidylinositol 3-Kinase / metabolism
  • Phosphoinositide-3 Kinase Inhibitors
  • Phosphorylation
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma / metabolism*
  • Precursor T-Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Proto-Oncogene Proteins c-akt / metabolism
  • Quinazolines / pharmacology
  • Signal Transduction / drug effects
  • Signal Transduction / physiology*
  • Sirolimus / analogs & derivatives
  • Sirolimus / pharmacology
  • TOR Serine-Threonine Kinases / antagonists & inhibitors
  • TOR Serine-Threonine Kinases / metabolism*

Substances

  • Antibiotics, Antineoplastic
  • Chromones
  • EIF4G1 protein, human
  • Enzyme Inhibitors
  • Eukaryotic Initiation Factor-4G
  • Morpholines
  • Phosphoinositide-3 Kinase Inhibitors
  • Quinazolines
  • WHI P131
  • 2-(4-morpholinyl)-8-phenyl-4H-1-benzopyran-4-one
  • temsirolimus
  • Dexamethasone
  • Doxorubicin
  • MTOR protein, human
  • Phosphatidylinositol 3-Kinase
  • Janus Kinase 3
  • Proto-Oncogene Proteins c-akt
  • TOR Serine-Threonine Kinases
  • Sirolimus