Coibamide A induces mTOR-independent autophagy and cell death in human glioblastoma cells

PLoS One. 2013 Jun 6;8(6):e65250. doi: 10.1371/journal.pone.0065250. Print 2013.

Abstract

Coibamide A is an N-methyl-stabilized depsipeptide that was isolated from a marine cyanobacterium as part of an International Cooperative Biodiversity Groups (ICBG) program based in Panama. Previous testing of coibamide A in the NCI in vitro 60 cancer cell line panel revealed a potent anti-proliferative response and "COMPARE-negative" profile indicative of a unique mechanism of action. We report that coibamide A is a more potent and efficacious cytotoxin than was previously appreciated, inducing concentration- and time-dependent cytotoxicity (EC50<100 nM) in human U87-MG and SF-295 glioblastoma cells and mouse embryonic fibroblasts (MEFs). This activity was lost upon linearization of the molecule, highlighting the importance of the cyclized structure for both anti-proliferative and cytotoxic responses. We show that coibamide A induces autophagosome accumulation in human glioblastoma cell types and MEFs via an mTOR-independent mechanism; no change was observed in the phosphorylation state of ULK1 (Ser-757), p70 S6K1 (Thr-389), S6 ribosomal protein (Ser-235/236) and 4EBP-1 (Thr-37/46). Coibamide A also induces morphologically and biochemically distinct forms of cell death according to cell type. SF-295 glioblastoma cells showed caspase-3 activation and evidence of apoptotic cell death in a pattern that was also seen in wild-type and autophagy-deficient (ATG5-null) MEFs. In contrast, cell death in U87-MG glioblastoma cells was characterized by extensive cytoplasmic vacuolization and lacked clear apoptotic features. Cell death was attenuated, but still triggered, in Apaf-1-null MEFs lacking a functional mitochondria-mediated apoptotic pathway. From the study of ATG5-null MEFs we conclude that a conventional autophagy response is not required for coibamide A-induced cell death, but likely occurs in dying cells in response to treatment. Coibamide A represents a natural product scaffold with potential for the study of mTOR-independent signaling and cell death mechanisms in apoptotic-resistant cancer cells.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adaptor Proteins, Signal Transducing / metabolism
  • Animals
  • Apoptosis / drug effects
  • Apoptotic Protease-Activating Factor 1 / deficiency
  • Apoptotic Protease-Activating Factor 1 / genetics
  • Autophagy / drug effects*
  • Autophagy-Related Protein 5
  • Autophagy-Related Protein-1 Homolog
  • Caspase 3 / genetics
  • Caspase 3 / metabolism
  • Cell Cycle Proteins
  • Cell Line, Tumor
  • Cytotoxins / pharmacology*
  • Depsipeptides / pharmacology*
  • Fibroblasts / cytology
  • Fibroblasts / drug effects*
  • Fibroblasts / metabolism
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Mice
  • Microtubule-Associated Proteins / deficiency
  • Microtubule-Associated Proteins / genetics
  • Organ Specificity
  • Phosphoproteins / genetics
  • Phosphoproteins / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Ribosomal Protein S6 Kinases / genetics
  • Ribosomal Protein S6 Kinases / metabolism
  • Signal Transduction / drug effects*
  • TOR Serine-Threonine Kinases / genetics
  • TOR Serine-Threonine Kinases / metabolism

Substances

  • APAF1 protein, human
  • ATG5 protein, human
  • Adaptor Proteins, Signal Transducing
  • Apoptotic Protease-Activating Factor 1
  • Autophagy-Related Protein 5
  • Cell Cycle Proteins
  • Cytotoxins
  • Depsipeptides
  • EIF4EBP1 protein, human
  • Intracellular Signaling Peptides and Proteins
  • Microtubule-Associated Proteins
  • Phosphoproteins
  • coibamide A
  • Autophagy-Related Protein-1 Homolog
  • Protein Serine-Threonine Kinases
  • Ribosomal Protein S6 Kinases
  • TOR Serine-Threonine Kinases
  • ULK1 protein, human
  • Caspase 3