A hypusine-eIF5A-PEAK1 switch regulates the pathogenesis of pancreatic cancer

Cancer Res. 2014 Nov 15;74(22):6671-81. doi: 10.1158/0008-5472.CAN-14-1031. Epub 2014 Sep 26.

Abstract

Deregulation of protein synthesis is a hallmark of cancer cell proliferation, survival, and metastatic progression. eIF5A1 and its highly related isoform eIF5A2 are translation initiation factors that have been implicated in a range of human malignancies, but how they control cancer development and disease progression is still poorly understood. Here, we investigated how eIF5A proteins regulate pancreatic ductal adenocarcinoma (PDAC) pathogenesis. eIF5A proteins are the only known proteins regulated by a distinct posttranslational modification termed hypusination, which is catalyzed by two enzymes, deoxyhypusine synthase (DHPS) and deoxyhypusine hydroxylase (DOHH). The highly selective nature of the hypusine modification and its amenability to pharmacologic inhibition make eIF5A proteins attractive therapeutic targets. We found that the expression and hypusination of eIF5A proteins are upregulated in human PDAC tissues and in premalignant pancreatic intraepithelial neoplasia tissues isolated from Pdx-1-Cre: LSL-KRAS(G12D) mice. Knockdown of eIF5A proteins in PDAC cells inhibited their growth in vitro and orthotopic tumor growth in vivo, whereas amplification of eIF5A proteins increased PDAC cell growth and tumor formation in mice. Small-molecule inhibitors of DHPS and DOHH both suppressed eIF5A hypusination, preventing PDAC cell growth. Interestingly, we found that eIF5A proteins regulate PDAC cell growth by modulating the expression of PEAK1, a nonreceptor tyrosine kinase essential for PDAC cell growth and therapy resistance. Our findings suggest that eIF5A proteins utilize PEAK1 as a downstream effector to drive PDAC pathogenesis and that pharmacologic inhibition of the eIF5A-hypusine-PEAK1 axis may provide a novel therapeutic strategy to combat this deadly disease.

Publication types

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

MeSH terms

  • Animals
  • Carcinoma, Pancreatic Ductal / drug therapy
  • Carcinoma, Pancreatic Ductal / etiology*
  • Cell Line, Tumor
  • Cell Proliferation
  • Ciclopirox
  • Deoxycytidine / analogs & derivatives
  • Deoxycytidine / pharmacology
  • Eukaryotic Translation Initiation Factor 5A
  • Female
  • Gemcitabine
  • Humans
  • Lysine / analogs & derivatives*
  • Lysine / physiology
  • Mice
  • Pancreatic Neoplasms / drug therapy
  • Pancreatic Neoplasms / etiology*
  • Peptide Initiation Factors / physiology*
  • Protein-Tyrosine Kinases / physiology*
  • Proto-Oncogene Proteins / physiology
  • Proto-Oncogene Proteins p21(ras)
  • Pyridones / pharmacology
  • RNA-Binding Proteins / physiology*
  • ras Proteins / physiology

Substances

  • KRAS protein, human
  • Peptide Initiation Factors
  • Proto-Oncogene Proteins
  • Pyridones
  • RNA-Binding Proteins
  • Deoxycytidine
  • Ciclopirox
  • hypusine
  • PEAK1 protein, human
  • Protein-Tyrosine Kinases
  • Proto-Oncogene Proteins p21(ras)
  • ras Proteins
  • Lysine
  • Gemcitabine