Activated signal transducer and activator of transcription 3 (STAT3) supports the malignant phenotype of human pancreatic cancer

Gastroenterology. 2003 Sep;125(3):891-905. doi: 10.1016/s0016-5085(03)01064-3.

Abstract

Background & aims: Constitutive activation of signal transducer and activator of transcription 3 (STAT3) has been implicated in regulation of growth and malignant transformation. We therefore analyzed the expression and biologic significance of STAT3 in human pancreatic cancer cells.

Methods: Expression and activation of STAT3 were investigated by immunohistochemistry and immunoblotting. Functional inactivation of STAT3 was achieved by stable transfection of dominant-negative STAT3 constructs in 2 pancreatic cancer cell lines and confirmed by electrophoretic mobility shift assay and immunoblotting. Cell proliferation and tumorigenicity were evaluated by cell counting, colony formation in soft agar, and xenotransplantation in nude mice. STAT3-dependent cell cycle distribution was monitored by flow cytometry, immunoprecipitation, immunoblotting, and histone H1 and GST-Rb kinase assays.

Results: Compared with nontransformed human pancreas, activated STAT3 is overexpressed in ductal carcinoma cells but not in ducts from chronic pancreatitis. Constitutive activation was also observed in all human pancreatic cancer cell lines examined. Functional inactivation of STAT3 resulted in significant inhibition of anchorage-dependent and -independent proliferation in vitro and reduced tumor growth in vivo. Cell cycle analysis showed a delay of G(1)/S-phase progression due to inhibition of cyclin-dependent kinase 2 activity based on increased expression of p21(WAF1) in vitro and in vivo. Blocking of the STAT3 upstream activator Janus kinase 2 by tyrphostin also resulted in growth arrest because of delayed G(1)/S-phase progression and increased expression of p21(WAF1).

Conclusions: On malignant transformation, activated STAT3 promotes cellular proliferation by acceleration of G(1)/S-phase progression and thereby contributes to the malignant phenotype of human pancreatic cancer.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins / pharmacology
  • DNA / metabolism
  • DNA-Binding Proteins / antagonists & inhibitors
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / physiology*
  • G1 Phase
  • Humans
  • Janus Kinase 2
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / etiology*
  • Pancreatic Neoplasms / pathology
  • Phenotype
  • Protein-Tyrosine Kinases / antagonists & inhibitors
  • Proto-Oncogene Proteins*
  • S Phase
  • STAT3 Transcription Factor
  • Trans-Activators / antagonists & inhibitors
  • Trans-Activators / genetics
  • Trans-Activators / physiology*
  • Tumor Cells, Cultured

Substances

  • CDKN1A protein, human
  • Cyclin-Dependent Kinase Inhibitor p21
  • Cyclins
  • DNA-Binding Proteins
  • Proto-Oncogene Proteins
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Trans-Activators
  • DNA
  • Protein-Tyrosine Kinases
  • JAK2 protein, human
  • Janus Kinase 2