A novel small-molecule disrupts Stat3 SH2 domain-phosphotyrosine interactions and Stat3-dependent tumor processes

Biochem Pharmacol. 2010 May 15;79(10):1398-409. doi: 10.1016/j.bcp.2010.01.001. Epub 2010 Jan 11.

Abstract

The molecular modeling of the phosphotyrosine (pTyr)-SH2 domain interaction in the Stat3:Stat3 dimerization, combined with in silico structural analysis of the Stat3 dimerization disruptor, S3I-201, has furnished a diverse set of analogs. We present evidence from in vitro biochemical and biophysical studies that the structural analog, S3I-201.1066 directly interacts with Stat3 or the SH2 domain, with an affinity (K(D)) of 2.74microM, and disrupts the binding of Stat3 to the cognate pTyr-peptide, GpYLPQTV-NH(2), with an IC(50) of 23microM. Moreover, S3I-201.1066 selectively blocks the association of Stat3 with the epidermal growth factor receptor (EGFR), and inhibits Stat3 tyrosine phosphorylation and nuclear translocation in EGF-stimulated mouse fibroblasts. In cancer cells that harbor aberrant Stat3 activity, S3I-201.1066 inhibits constitutive Stat3 DNA-binding and transcriptional activities. By contrast, S3I-201.1066 has no effect on Src activation or the EGFR-mediated activation of the Erk1/2(MAPK) pathway. S3I-201.1066 selectively suppresses the viability, survival, and malignant transformation of the human breast and pancreatic cancer lines and the v-Src-transformed mouse fibroblasts harboring persistently active Stat3. Treatment with S3I-201.1066 of malignant cells harboring aberrantly active Stat3 down-regulated the expression of c-Myc, Bcl-xL, Survivin, the matrix metalloproteinase 9, and VEGF. The in vivo administration of S3I-201.1066-induced significant antitumor response in mouse models of human breast cancer, which correlates with the inhibition of constitutively active Stat3 and the suppression of known Stat3-regulated genes. Our studies identify a novel small-molecule that binds with a high affinity to Stat3, blocks Stat3 activation and function, and thereby induces antitumor response in human breast tumor xenografts harboring persistently active Stat3.

Publication types

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

MeSH terms

  • Aminosalicylic Acids / pharmacology
  • Animals
  • Benzenesulfonates / pharmacology*
  • Breast Neoplasms / physiopathology
  • Cell Line
  • Cell Line, Tumor
  • Cell Transformation, Neoplastic / drug effects
  • Cell Transformation, Neoplastic / metabolism
  • DNA, Neoplasm / drug effects
  • DNA, Neoplasm / metabolism
  • ErbB Receptors / drug effects
  • ErbB Receptors / physiology
  • Female
  • Fluorescence Polarization Immunoassay
  • Gene Expression Regulation, Neoplastic / drug effects*
  • Gene Expression Regulation, Neoplastic / physiology
  • Humans
  • Mice
  • Mice, Nude
  • Pancreatic Neoplasms / physiopathology
  • STAT3 Transcription Factor / antagonists & inhibitors
  • STAT3 Transcription Factor / drug effects*
  • STAT3 Transcription Factor / genetics
  • STAT3 Transcription Factor / metabolism
  • STAT3 Transcription Factor / physiology
  • Surface Plasmon Resonance
  • Transcriptional Activation / drug effects
  • Transcriptional Activation / physiology
  • src Homology Domains / drug effects*
  • src Homology Domains / physiology

Substances

  • Aminosalicylic Acids
  • Benzenesulfonates
  • DNA, Neoplasm
  • NSC 74859
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Stat3 protein, mouse
  • ErbB Receptors