Agents that down-regulate or inhibit protein kinase C circumvent resistance to 1-beta-D-arabinofuranosylcytosine-induced apoptosis in human leukemia cells that overexpress Bcl-2

Mol Pharmacol. 1997 Dec;52(6):1000-9. doi: 10.1124/mol.52.6.1000.

Abstract

The effects of the non-tumor-promoting protein kinase C (PKC) activator bryostatin 1 and the PKC inhibitors staurosporine and UCN-01 were examined with respect to modulation of 1-[beta-D-arabinofuranosyl]cytosine (ara-C)-induced apoptosis in human myeloid leukemia cells (HL-60) overexpressing the antiapoptotic protein Bcl-2. HL-60/Bcl-2 cells displayed a 5-fold increase in Bcl-2 protein compared with empty-vector counter-parts (HL-60/pCEP4) but comparable levels of Bax, Mcl-1, and Bcl-xL. After exposure to an equimolar concentration of ara-C (10 microM for 6 hr), HL-60/Bcl-2 cells were significantly less susceptible to apoptosis, DNA fragmentation, and loss of clonogenicity than HL-60/pCEP4 cells. The protective effect of increased Bcl-2 expression was manifested by a failure of ara-C to induce activation/cleavage of the Yama protease (CPP32; caspase-3) and degradation of one of its substrates, poly(ADP-ribose)polymerase to an 85-kDa cleavage product. When HL-60/Bcl-2 cells were preincubated with bryostatin 1 (10 nM; 24 hr) or coincubated with either staurosporine (50 nM; 6 hr) or UCN-01 (300 nM; 6 hr) after a 1-hr preincubation, exposures that exerted minimal effects alone, ara-C-induced apoptosis and DNA fragmentation were restored to levels equivalent to, or greater than, those observed in empty-vector controls. These events were accompanied by restoration of the ability of ara-C to induce CPP32 cleavage and activation, poly(ADP-ribose) polymerase degradation, and inhibition of colony formation. Western analysis of Bcl-2 protein obtained from overexpressing cells treated with bryostatin 1, staurosporine, or UCN-01 revealed the appearance of a slowly migrating species and a general broadening of the protein band, effects that were insensitive to the protein synthesis inhibitor cycloheximide. Alterations in Bcl-2 protein mobility on sodium dodecyl sulfate-polyacrylamide gel electrophoresis were reversed by treatment of lysates with alkaline phosphatase or protein phosphatase 2A; actions of the latter were blocked by the specific phosphatase inhibitor okadaic acid. In vivo labeling studies of Bcl-2 protein demonstrated increased incorporation of [32PO4]orthophosphate in drug-treated cells. Last, phosphorylated Bcl-2 failed to display decreased binding to the proapoptotic protein Bax. Collectively, these findings indicate that bryostatin 1, which down-regulates PKC, and staurosporine and UCN-01, which directly inhibit the enzyme, circumvent resistance of Bcl-2-overexpressing leukemic cells to ara-C-induced apoptosis and activation of the protease cascade. They also raise the possibility that modulation of Bcl-2 phosphorylation status contributes to this effect.

Publication types

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

MeSH terms

  • Alkaloids / pharmacology
  • Antimetabolites, Antineoplastic / pharmacology*
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Blotting, Western
  • Bryostatins
  • Cytarabine / pharmacology*
  • DNA, Neoplasm / drug effects
  • DNA, Neoplasm / metabolism
  • Down-Regulation / drug effects
  • Drug Resistance, Neoplasm
  • Drug Synergism
  • Endopeptidases / metabolism
  • Enzyme Inhibitors / pharmacology
  • HL-60 Cells / drug effects
  • HL-60 Cells / metabolism*
  • Humans
  • Lactones / pharmacology
  • Macrolides
  • Phosphorylation
  • Protein Kinase C / antagonists & inhibitors*
  • Protein Kinase C / drug effects
  • Protein Kinase C / metabolism*
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis*
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • Staurosporine / pharmacology

Substances

  • Alkaloids
  • Antimetabolites, Antineoplastic
  • Antineoplastic Agents
  • Bryostatins
  • DNA, Neoplasm
  • Enzyme Inhibitors
  • Lactones
  • Macrolides
  • Proto-Oncogene Proteins c-bcl-2
  • Cytarabine
  • bryostatin 1
  • 7-hydroxystaurosporine
  • Protein Kinase C
  • Endopeptidases
  • Staurosporine