Cucurbitacin Q: a selective STAT3 activation inhibitor with potent antitumor activity

Oncogene. 2005 May 5;24(20):3236-45. doi: 10.1038/sj.onc.1208470.

Abstract

Constitutive activation of the JAK/STAT3 pathway is a major contributor to oncogenesis. In the present study, structure-activity relationship (SAR) studies with five cucurbitacin (Cuc) analogs, A, B, E, I, and Q, led to the discovery of Cuc Q, which inhibits the activation of STAT3 but not JAK2; Cuc A which inhibits JAK2 but not STAT3 activation; and Cuc B, E, and I, which inhibit the activation of both. Furthermore, these SAR studies demonstrated that conversion of the C3 carbonyl of the cucurbitacins to a hydroxyl results in loss of anti-JAK2 activity, whereas addition of a hydroxyl group to C11 of the cucurbitacins results in loss of anti-STAT3 activity. Cuc Q inhibits selectively the activation of STAT3 and induces apoptosis without inhibition of JAK2, Src, Akt, Erk, or JNK activation. Furthermore, Cuc Q induces apoptosis more potently in human and murine tumors that contain constitutively activated STAT3 (i.e., A549, MDA-MB-435, and v-Src/NIH 3T3) as compared to those that do not (i.e., H-Ras/NIH 3T3, MDA-MB-453, and NIH 3T3 cells). Finally, in a nude mouse tumor xenograft model, Cuc Q, but not Cuc A, suppresses tumor growth indicating that JAK2 inhibition is not sufficient to inhibit tumor growth and suggesting that the ability of Cuc Q to inhibit tumor growth is related to its anti-STAT3 activity. These studies further validate STAT3 as a drug discovery target and provide evidence that pharmacological agents that can selectively reduce the P-STAT3 levels in human cancer cells result in tumor apoptosis and growth inhibition.

Publication types

  • Research Support, U.S. Gov't, P.H.S.

MeSH terms

  • 3T3 Cells
  • Animals
  • Antineoplastic Agents / pharmacology*
  • Apoptosis
  • Blotting, Western
  • Cell Line, Tumor
  • Cell Proliferation
  • Cucurbitacins
  • DNA-Binding Proteins / antagonists & inhibitors*
  • DNA-Binding Proteins / metabolism*
  • Humans
  • Immunohistochemistry
  • Immunoprecipitation
  • In Situ Nick-End Labeling
  • Inhibitory Concentration 50
  • Janus Kinase 2
  • Mice
  • Mice, Nude
  • Models, Chemical
  • NIH 3T3 Cells
  • Neoplasm Transplantation
  • Phosphotyrosine / chemistry
  • Protein Serine-Threonine Kinases / metabolism
  • Protein-Tyrosine Kinases / metabolism
  • Proto-Oncogene Proteins / metabolism
  • Proto-Oncogene Proteins c-akt
  • STAT3 Transcription Factor
  • Signal Transduction
  • Structure-Activity Relationship
  • Time Factors
  • Trans-Activators / antagonists & inhibitors*
  • Trans-Activators / metabolism*
  • Triterpenes / chemistry
  • Triterpenes / pharmacology*
  • src-Family Kinases / metabolism

Substances

  • Antineoplastic Agents
  • DNA-Binding Proteins
  • Proto-Oncogene Proteins
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Stat3 protein, mouse
  • Trans-Activators
  • Triterpenes
  • cucurbitacin Q
  • Phosphotyrosine
  • Cucurbitacins
  • Protein-Tyrosine Kinases
  • JAK2 protein, human
  • Jak2 protein, mouse
  • Janus Kinase 2
  • src-Family Kinases
  • AKT1 protein, human
  • Protein Serine-Threonine Kinases
  • Proto-Oncogene Proteins c-akt