Angiogenic gene signature in human pancreatic cancer correlates with TGF-beta and inflammatory transcriptomes

Oncotarget. 2016 Jan 5;7(1):323-41. doi: 10.18632/oncotarget.6345.

Abstract

Pancreatic ductal adenocarcinomas (PDACs) are hypovascular, but overexpress pro-angiogenic factors and exhibit regions of microvasculature. Using RNA-seq data from The Cancer Genome Atlas (TCGA), we previously reported that ~12% of PDACs have an angiogenesis gene signature with increased expression of multiple pro-angiogenic genes. By analyzing the recently expanded TCGA dataset, we now report that this signature is present in ~35% of PDACs but that it is mostly distinct from an angiogenesis signature present in pancreatic neuroendocrine tumors (PNETs). These PDACs exhibit a transcriptome that reflects active TGF-β signaling, and up-regulation of several pro-inflammatory genes, and many members of JAK signaling pathways. Moreover, expression of SMAD4 and HDAC9 correlates with endothelial cell abundance in PDAC tissues. Concomitantly targeting the TGF-β type I receptor (TβRI) kinase with SB505124 and JAK1-2 with ruxolitinib suppresses JAK1 phosphorylation and blocks proliferative cross-talk between human pancreatic cancer cells (PCCs) and human endothelial cells (ECs), and these anti-proliferative effects were mimicked by JAK1 silencing in ECs. By contrast, either inhibitor alone does not suppress their enhanced proliferation in 3D co-cultures. These findings suggest that targeting both TGF-β and JAK1 signaling could be explored therapeutically in the 35% of PDAC patients whose cancers exhibit an angiogenesis gene signature.

Keywords: TCGA; TGF-β; angiogenesis; inflammation; pancreatic cancer.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Carcinoma, Pancreatic Ductal / blood supply
  • Carcinoma, Pancreatic Ductal / genetics*
  • Carcinoma, Pancreatic Ductal / metabolism
  • Cell Line, Tumor
  • Cells, Cultured
  • Cluster Analysis
  • Coculture Techniques
  • Endothelial Cells / metabolism
  • Gene Expression Profiling / methods*
  • Gene Expression Regulation, Neoplastic*
  • Histone Deacetylases / genetics
  • Histone Deacetylases / metabolism
  • Humans
  • Immunoblotting
  • Inflammation Mediators / metabolism
  • Janus Kinase 1 / genetics
  • Janus Kinase 1 / metabolism
  • Neovascularization, Pathologic / genetics*
  • Neovascularization, Pathologic / metabolism
  • Pancreatic Neoplasms / blood supply
  • Pancreatic Neoplasms / genetics*
  • Pancreatic Neoplasms / metabolism
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Receptor, Transforming Growth Factor-beta Type I
  • Receptors, Transforming Growth Factor beta / genetics
  • Receptors, Transforming Growth Factor beta / metabolism
  • Repressor Proteins / genetics
  • Repressor Proteins / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Signal Transduction / genetics
  • Smad4 Protein / genetics
  • Smad4 Protein / metabolism
  • Survival Analysis
  • Transforming Growth Factor beta / genetics*
  • Transforming Growth Factor beta / metabolism

Substances

  • Inflammation Mediators
  • Receptors, Transforming Growth Factor beta
  • Repressor Proteins
  • Smad4 Protein
  • Transforming Growth Factor beta
  • JAK1 protein, human
  • Janus Kinase 1
  • Protein Serine-Threonine Kinases
  • Receptor, Transforming Growth Factor-beta Type I
  • HDAC9 protein, human
  • Histone Deacetylases