Induction of tumor necrosis factor by bryostatin 1 is involved in synergistic interactions with paclitaxel in human myeloid leukemia cells

Blood. 2003 May 1;101(9):3648-57. doi: 10.1182/blood-2002-09-2739. Epub 2003 Jan 9.

Abstract

Interactions between the protein kinase C (PKC) activator/down-regulator bryostatin 1 and paclitaxel have been examined in human myeloid leukemia cells (U937) and in highly paclitaxel-resistant cells ectopically expressing a Bcl-2 phosphorylation loop-deleted protein (Delta Bcl-2). Treatment (24 hours) of wild-type cells with paclitaxel (eg, 5 to 20 nM) in combination with 10 nM bryostatin 1 induced a marked increase in mitochondrial damage (eg, cytochrome c and Smac/DIABLO [second mitochondria-derived activator of caspases/direct IAP binding protein with low pI] release), caspase activation, Bid cleavage, and apoptosis; moreover, bryostatin 1 circumvented the block to paclitaxel-induced mitochondrial injury and apoptosis conferred by ectopic expression of the loop-deleted protein. Coadministration of tumor necrosis factor (TNF) soluble receptors, or ectopic expression of CrmA or dominant-negative caspase-8, abrogated potentiation of paclitaxel-induced mitochondrial injury and apoptosis by bryostatin 1, implicating the extrinsic apoptotic pathway in this process. Similar events occurred in HL-60 leukemia cells. Potentiation of paclitaxel-induced apoptosis in wild-type and mutant cells by bryostatin 1 was associated with increases in TNF-alpha mRNA and protein and was mimicked by exogenous TNF-alpha. Coadministration of the selective PKC inhibitor GFX (1 microM) blocked the increase in TNF-alpha mRNA levels and apoptosis in bryostatin 1/paclitaxel-treated cells. Lastly, synchronization of cells in G(2)M increased their sensitivity to TNF-alpha-associated lethality. Collectively, these findings indicate that in U937 cells, bryostatin 1 promotes paclitaxel-mediated mitochondrial injury and apoptosis, and circumvents resistance to cell death conferred by loss of the Bcl-2 phosphorylation domain, through the PKC-dependent induction of TNF-alpha. They further suggest that this process is amplified by paclitaxel-mediated arrest of cells in G(2)M, where they are more susceptible to TNF-alpha-induced lethality.

Publication types

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

MeSH terms

  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Agents, Phytogenic / pharmacology
  • Apoptosis / drug effects*
  • BH3 Interacting Domain Death Agonist Protein
  • Bryostatins
  • Carrier Proteins / metabolism
  • Caspase 8
  • Caspase 9
  • Caspases / metabolism
  • Drug Synergism
  • Enzyme Activation / drug effects
  • G2 Phase / drug effects
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Genes, bcl-2
  • HL-60 Cells / drug effects
  • Humans
  • Lactones / pharmacology*
  • Macrolides
  • Mitochondria / drug effects
  • Models, Biological
  • Monocytes / drug effects
  • Neoplasm Proteins / biosynthesis*
  • Neoplasm Proteins / genetics
  • Paclitaxel / pharmacology*
  • Phosphorylation / drug effects
  • Protein Kinase C / metabolism
  • Protein Processing, Post-Translational / drug effects
  • Proto-Oncogene Proteins c-bcl-2 / biosynthesis
  • Proto-Oncogene Proteins c-bcl-2 / chemistry
  • Proto-Oncogene Proteins c-bcl-2 / genetics
  • Proto-Oncogene Proteins c-bcl-2 / metabolism
  • RNA, Messenger / biosynthesis
  • RNA, Neoplasm / biosynthesis
  • Recombinant Fusion Proteins / antagonists & inhibitors
  • Recombinant Fusion Proteins / metabolism
  • Recombinant Fusion Proteins / pharmacology
  • Sequence Deletion
  • Tumor Cells, Cultured / drug effects
  • Tumor Necrosis Factor-alpha / biosynthesis*
  • Tumor Necrosis Factor-alpha / genetics
  • Tumor Necrosis Factor-alpha / pharmacology
  • U937 Cells / drug effects
  • bcl-X Protein

Substances

  • Antineoplastic Agents
  • Antineoplastic Agents, Phytogenic
  • BCL2L1 protein, human
  • BH3 Interacting Domain Death Agonist Protein
  • BID protein, human
  • Bryostatins
  • Carrier Proteins
  • Lactones
  • Macrolides
  • Neoplasm Proteins
  • Proto-Oncogene Proteins c-bcl-2
  • RNA, Messenger
  • RNA, Neoplasm
  • Recombinant Fusion Proteins
  • Tumor Necrosis Factor-alpha
  • bcl-X Protein
  • bryostatin 1
  • Protein Kinase C
  • CASP8 protein, human
  • CASP9 protein, human
  • Caspase 8
  • Caspase 9
  • Caspases
  • Paclitaxel