Inhibition of glutathione synthesis overcomes Bcl-2-mediated topoisomerase inhibitor resistance and induces nonapoptotic cell death via mitochondrial-independent pathway

Cancer Res. 2006 Jun 1;66(11):5772-80. doi: 10.1158/0008-5472.CAN-05-3916.

Abstract

Bcl-2 protein plays a critical role in inhibiting anticancer drug-induced apoptosis. We found that Bcl-2 overexpression is associated with a nearly 3-fold increase in cellular glutathione levels and with increased resistance to cell death after treatment with etoposide or SN-38, a derivative of camptothecin, in leukemia 697 cells with wild-type p53. Treatment of Bcl-2-overexpressing 697 cells (697-Bcl-2) with buthionine sulfoximine (BSO), an inhibitor of glutathione synthesis, reduced cellular glutathione levels and completely abolished Bcl-2-mediated drug resistance. Morphologic studies revealed that nonapoptotic cell death was induced in 697-Bcl-2 cells after treatment with BSO plus etoposide or SN-38. Activation of caspase-3/7 and cytochrome c release could not be detected in 697-Bcl-2 cells after these drug treatments. Notably, we showed that proteasome-mediated down-regulation of Puma and Noxa proteins occurs in 697-Bcl-2 cells after treatment with BSO plus topoisomerase inhibitor, although there is an increase in the protein levels of p53 in these 697-Bcl-2 cells. In contrast, parental 697 cells underwent typical apoptosis with up-regulation of Puma and Noxa proteins, followed by cytochrome c release and caspase-3/7 activation after treatment with topoisomerase inhibitor in the presence or absence of BSO. Our data suggest that BSO may possess a unique activity to overcome Bcl-2-mediated drug resistance by stimulating the signals that can bypass mitochondrial process in Bcl-2-overexpressing cells.

Publication types

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

MeSH terms

  • Antineoplastic Combined Chemotherapy Protocols / pharmacology
  • Apoptosis Regulatory Proteins / biosynthesis
  • Apoptosis Regulatory Proteins / genetics
  • Buthionine Sulfoximine / administration & dosage
  • Buthionine Sulfoximine / pharmacology
  • Camptothecin / administration & dosage
  • Camptothecin / analogs & derivatives
  • Camptothecin / pharmacology
  • Caspase 3
  • Caspase 7
  • Caspases / metabolism
  • Cell Death / drug effects
  • Cell Death / physiology
  • Cell Line, Tumor
  • DNA Topoisomerases, Type I / metabolism
  • Drug Resistance, Multiple
  • Drug Resistance, Neoplasm
  • Enzyme Activation
  • Etoposide / administration & dosage
  • Etoposide / pharmacology
  • Gene Expression Regulation, Leukemic / drug effects
  • Glutathione / antagonists & inhibitors*
  • Glutathione / biosynthesis*
  • Humans
  • Irinotecan
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / drug therapy*
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / enzymology
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / metabolism*
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma / pathology
  • Proto-Oncogene Proteins / biosynthesis
  • Proto-Oncogene Proteins / genetics
  • 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 / metabolism*
  • Topoisomerase I Inhibitors*
  • Tumor Suppressor Protein p53 / biosynthesis
  • Tumor Suppressor Protein p53 / genetics

Substances

  • Apoptosis Regulatory Proteins
  • BBC3 protein, human
  • PMAIP1 protein, human
  • Proto-Oncogene Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • TP53 protein, human
  • Topoisomerase I Inhibitors
  • Tumor Suppressor Protein p53
  • Buthionine Sulfoximine
  • Etoposide
  • Irinotecan
  • CASP3 protein, human
  • CASP7 protein, human
  • Caspase 3
  • Caspase 7
  • Caspases
  • DNA Topoisomerases, Type I
  • Glutathione
  • Camptothecin