Akt-dependent glucose metabolism promotes Mcl-1 synthesis to maintain cell survival and resistance to Bcl-2 inhibition

Cancer Res. 2011 Aug 1;71(15):5204-13. doi: 10.1158/0008-5472.CAN-10-4531. Epub 2011 Jun 13.

Abstract

Most cancer cells utilize aerobic glycolysis, and activation of the phosphoinositide 3-kinase/Akt/mTOR pathway can promote this metabolic program to render cells glucose dependent. Although manipulation of glucose metabolism may provide a means to specifically eliminate cancer cells, mechanistic links between cell metabolism and apoptosis remain poorly understood. Here, we examined the role and metabolic regulation of the antiapoptotic Bcl-2 family protein Mcl-1 in cell death upon inhibition of Akt-induced aerobic glycolysis. In the presence of adequate glucose, activated Akt prevented the loss of Mcl-1 expression and protected cells from growth factor deprivation-induced apoptosis. Mcl-1 associated with and inhibited the proapoptotic Bcl-2 family protein Bim, contributing to cell survival. However, suppression of glucose metabolism led to induction of Bim, decreased expression of Mcl-1, and apoptosis. The proapoptotic Bcl-2/Bcl-xL/Bcl-w inhibitor, ABT-737, shows clinical promise, but Mcl-1 upregulation can promote resistance. Importantly, inhibition of glucose metabolism or mTORC1 overcame Mcl-1-mediated resistance in diffuse large B cell leukemic cells. Together these data show that Mcl-1 protein synthesis is tightly controlled by metabolism and that manipulation of glucose metabolism may provide a mechanism to suppress Mcl-1 expression and sensitize cancer cells to apoptosis.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / physiology
  • Adenosine Triphosphate / metabolism
  • Animals
  • Apoptosis
  • Apoptosis Regulatory Proteins / antagonists & inhibitors*
  • Apoptosis Regulatory Proteins / metabolism
  • Bcl-2-Like Protein 11
  • Biphenyl Compounds / pharmacology
  • Cell Cycle Proteins
  • Cell Line, Tumor / drug effects
  • Cell Survival
  • Gene Expression Regulation, Neoplastic / drug effects
  • Glucose / metabolism*
  • Glycolysis / drug effects
  • Humans
  • Jurkat Cells / drug effects
  • Lymphoma, Large B-Cell, Diffuse / pathology
  • Mechanistic Target of Rapamycin Complex 1
  • Membrane Proteins / antagonists & inhibitors*
  • Membrane Proteins / metabolism
  • Mice
  • Multiprotein Complexes
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Neoplasm Proteins / physiology*
  • Nitrophenols / pharmacology
  • Phosphoproteins / physiology
  • Piperazines / pharmacology
  • Proteins / antagonists & inhibitors
  • Proteins / physiology
  • Proto-Oncogene Proteins / antagonists & inhibitors*
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt / physiology*
  • Proto-Oncogene Proteins c-bcl-2 / antagonists & inhibitors
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis*
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / physiology
  • Ribosomal Protein S6 Kinases / physiology
  • Sulfonamides / pharmacology
  • T-Lymphocytes / drug effects
  • TOR Serine-Threonine Kinases

Substances

  • ABT-737
  • Adaptor Proteins, Signal Transducing
  • Apoptosis Regulatory Proteins
  • BCL2L11 protein, human
  • Bcl-2-Like Protein 11
  • Bcl2l11 protein, mouse
  • Biphenyl Compounds
  • Cell Cycle Proteins
  • EIF4EBP1 protein, human
  • Mcl1 protein, mouse
  • Membrane Proteins
  • Multiprotein Complexes
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Neoplasm Proteins
  • Nitrophenols
  • Phosphoproteins
  • Piperazines
  • Proteins
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • Sulfonamides
  • Adenosine Triphosphate
  • AKT1 protein, human
  • Mechanistic Target of Rapamycin Complex 1
  • Proto-Oncogene Proteins c-akt
  • Ribosomal Protein S6 Kinases
  • TOR Serine-Threonine Kinases
  • Glucose