Antitumor activity of a novel oncrasin analogue is mediated by JNK activation and STAT3 inhibition

PLoS One. 2011;6(12):e28487. doi: 10.1371/journal.pone.0028487. Epub 2011 Dec 12.

Abstract

Background: To optimize the antitumor activity of oncrasin-1, a small molecule identified through synthetic lethality screening on isogenic K-Ras mutant tumor cells, we developed several analogues and determined their antitumor activities. Here we investigated in vitro and in vivo antitumor activity of NSC-743380 (1-[(3-chlorophenyl) methyl]-1H-indole-3-methanol, oncrasin-72), one of most potent analogues of oncrasin-1.

Methodology and principal findings: In vitro antitumor activity was determined in NCI-60 cancer cell line panel using cell viability assay. In vivo antitumor activity was determined in parallel with NSC-741909 (oncrasin-60) in xenograft tumors established in nude mice from A498, a human renal cancer cell line. Changes in gene expression levels and signaling pathway activities upon treatment with NSC-743380 were analyzed in breast and renal cancer cells by Western blot analysis. Apoptosis was demonstrated by Western blot analysis and flow cytometric analysis. NSC-743380 is highly active against a subset of cancer cell lines derived from human lung, colon, ovary, kidney, and breast cancers. The 50% growth-inhibitory concentration (GI(50)) for eight of the most sensitive cell lines was ≤ 10 nM. In vivo study showed that NSC-743380 has a better safety profile and greater antitumor activity than NSC-741909. Treatment with NSC-743380 caused complete regression of A498 xenograft tumors in nude mice at the tested doses ranging from 67 mg/kg to 150 mg/kg. Mechanistic characterization revealed that NSC-743380 suppressed the phosphorylation of C-terminal domain of RNA polymerase II, induced JNK activation, inhibited JAK2/STAT3 phosphorylation and suppressed cyclin D1 expression in sensitive human cancer cells. Blocking JNK activation or overexpression of constitutively active STAT3 partially blocked NSC-743380-induced antitumor activity.

Conclusions: NSC-743380 induces antitumor activity through modulation of functions in multiple cancer related pathways and could be a potential anticancer agent for some solid tumors.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Cell Line, Tumor
  • Enzyme Activation / drug effects
  • Female
  • Humans
  • Indoles / chemistry
  • Indoles / pharmacology*
  • JNK Mitogen-Activated Protein Kinases / metabolism*
  • Mice
  • Mice, Nude
  • Protein Kinase Inhibitors / pharmacology
  • RNA Polymerase II / metabolism
  • STAT3 Transcription Factor / antagonists & inhibitors*
  • STAT3 Transcription Factor / metabolism
  • Signal Transduction / drug effects
  • Subcutaneous Tissue / drug effects
  • Subcutaneous Tissue / pathology
  • Xenograft Model Antitumor Assays

Substances

  • 1-((3-chlorophenyl)methyl)-1H-indole-3-carbinol
  • Antineoplastic Agents
  • Indoles
  • Protein Kinase Inhibitors
  • STAT3 Transcription Factor
  • oncrasin-1
  • JNK Mitogen-Activated Protein Kinases
  • RNA Polymerase II