Pyoluteorin derivatives induce Mcl-1 degradation and apoptosis in hematological cancer cells

Cancer Biol Ther. 2014;15(12):1688-99. doi: 10.4161/15384047.2014.972799.

Abstract

Mcl-1, a pro-survival member of the Bcl-2 protein family, is an attractive target for cancer therapy. We have recently identified the natural product marinopyrrole A (maritoclax) as a novel small molecule Mcl-1 inhibitor. Here, we describe the structure-activity relationship study of pyoluteorin derivatives based on maritoclax. To date, we synthesized over 30 derivatives of maritoclax and evaluated their inhibitory actions and cytotoxicity toward Mcl-1-dependent cell lines. As a result, several functional groups were identified in the pyoluteorin motif that significantly potentiate biological activity. A number of such derivatives, KS04 and KS18, interacted with Mcl-1 in a conserved fashion according to NMR spectroscopy and molecular modeling. KS04 and KS18 induced apoptosis selectively in Mcl-1-dependent but not Bcl-2-dependent K562 cells through selective Mcl-1 down-regulation, and synergistically enhanced apoptosis in combination with ABT-737. Moreover, the intraperitoneal administration of KS18 (10 mg/kg/d) and ABT-737 (20 mg/kg/d) significantly suppressed the growth of ABT-737-resistant HL-60 xenografts in nude mice without apparent toxicity. Overall, we identified the pharmacophore of pyoluteorin derivatives that act as potent and promising Mcl-1 antagonists against Mcl-1-dependent hematological cancers.

Keywords: ABTR, ABT-737 resistant; AML, Acute Myeloid Leukemia; AUCinf, area under curve extrapolated to time infinity; AUClast, area under curve until last observed timepoint; Apoptosis; BH3, Bcl-2 homology domain 3; Bcl-2 family; Bcl-2, B-cell lymphoma-2; CHX, Cycloheximide; CL, rate of plasma clearance; Cmax, maximal plasma concentration; EC50, Half maximal effective concentration; IRES, Internal ribosome entry site; LD50, median lethal dose; MTD, Maximal tolerated dose; Mcl-1; Mcl-1, Myeloid cell leukemia-1; NMR, Nuclear magnetic resonance; PARP, Poly (ADP-ribose) polymerase; SAR, Structure-activity relationship; T1/2, plasma half-life; Tmax, time to maximal plasma concentration; VD, Volume of distribution; i.p., Intraperitoneal; leukemia; lymphoma; maritoclax; multiple myeloma; pyoluteorin.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / pharmacology
  • Apoptosis / drug effects*
  • Cell Line, Tumor
  • Cell Survival / drug effects
  • Disease Models, Animal
  • Drug Resistance, Neoplasm
  • Drug Synergism
  • Female
  • Hematologic Neoplasms / metabolism*
  • Hematologic Neoplasms / pathology
  • Humans
  • Models, Molecular
  • Molecular Conformation
  • Myeloid Cell Leukemia Sequence 1 Protein / antagonists & inhibitors
  • Myeloid Cell Leukemia Sequence 1 Protein / chemistry
  • Myeloid Cell Leukemia Sequence 1 Protein / metabolism*
  • Phenols / chemistry
  • Phenols / metabolism
  • Phenols / pharmacology*
  • Protein Binding
  • Protein Interaction Domains and Motifs
  • Proteolysis / drug effects
  • Pyrroles / chemistry
  • Pyrroles / metabolism
  • Pyrroles / pharmacology*
  • Stromal Cells / drug effects
  • Stromal Cells / metabolism
  • Time Factors
  • Tumor Burden / drug effects
  • Xenograft Model Antitumor Assays
  • bcl-2 Homologous Antagonist-Killer Protein / metabolism
  • bcl-2-Associated X Protein / metabolism

Substances

  • Antineoplastic Agents
  • Myeloid Cell Leukemia Sequence 1 Protein
  • Phenols
  • Pyrroles
  • bcl-2 Homologous Antagonist-Killer Protein
  • bcl-2-Associated X Protein
  • marinopyrrole A
  • pyoluteorin