Proteomic identification of the oncoprotein STAT3 as a target of a novel Skp1 inhibitor

Oncotarget. 2017 Jan 10;8(2):2681-2693. doi: 10.18632/oncotarget.13153.

Abstract

The S phase kinase-associated protein 1 (Skp1), an adaptor protein of the Skp1-Cul1-F-box protein complex, binds the ubiquitin E3 ligase Skp2 and is critical to its biological functions. Targeting of Skp1 by a small compound 6-O-angeloylplenolin (6-OAP) results in dissociation and degradation of Skp2 and mitotic arrest of lung cancer cells. Here, by using a proteome microarray containing 16,368 proteins and a biotinylated 6-OAP, we identified 99 proteins that could bind 6-OAP, with Skp1 and STAT3 sitting at the central position of the 6-OAP interactome. 6-OAP formed hydrogen bonds with Ser611/Ser613/Arg609 at the SH2 domain of STAT3 and inhibited the constitutive and interleukin-6-induced phosphorylated STAT3 (pSTAT3), leading to inhibitory effects on lung cancer cells and suppression of Skp2 transcription. STAT3 was overexpressed in tumor samples compared to counterpart normal lung tissues and was inversely associated with prognosis of the patients. 6-OAP inhibited tumor growth in SCID mice intravenously injected with lung cancer cells, and downregulated both STAT3 and Skp2 in tumor samples. Given that 6-OAP is a Skp1 inhibitor, our data suggest that this compound may target Skp1 and STAT3 to suppress Skp2, augmenting its anti-lung cancer activity.

Keywords: 6-O-angeloylplenolin; STAT3 inhibitor; Skp2; lung cancer; proteome microarray.

MeSH terms

  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Apoptosis / drug effects
  • Cell Cycle / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Disease Models, Animal
  • Gene Expression Regulation
  • Humans
  • Lactones / chemistry
  • Lactones / pharmacology
  • Mice
  • Models, Molecular
  • Molecular Conformation
  • Oncogene Proteins / antagonists & inhibitors
  • Oncogene Proteins / chemistry
  • Oncogene Proteins / metabolism*
  • Protein Binding
  • Protein Kinase Inhibitors / chemistry
  • Protein Kinase Inhibitors / pharmacology*
  • Proteomics* / methods
  • S-Phase Kinase-Associated Proteins / antagonists & inhibitors*
  • S-Phase Kinase-Associated Proteins / chemistry
  • S-Phase Kinase-Associated Proteins / genetics
  • S-Phase Kinase-Associated Proteins / metabolism
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / chemistry
  • STAT3 Transcription Factor / metabolism*
  • Sesquiterpenes / chemistry
  • Sesquiterpenes / pharmacology
  • Structure-Activity Relationship
  • Transcription, Genetic
  • Xenograft Model Antitumor Assays

Substances

  • 6-O-angeloylprenolin
  • Antineoplastic Agents
  • Lactones
  • Oncogene Proteins
  • Protein Kinase Inhibitors
  • S-Phase Kinase-Associated Proteins
  • SKP1 protein, human
  • STAT3 Transcription Factor
  • Sesquiterpenes