Recapitulation of pancreatic neuroendocrine tumors in human multiple endocrine neoplasia type I syndrome via Pdx1-directed inactivation of Men1

Cancer Res. 2009 Mar 1;69(5):1858-66. doi: 10.1158/0008-5472.CAN-08-3662. Epub 2009 Feb 10.

Abstract

Multiple endocrine neoplasia type 1 (MEN1) is an autosomal syndrome caused by mutations in the MEN1 tumor suppressor gene. Whereas the protein product of MEN1, menin, is ubiquitously expressed, somatic loss of the remaining wild-type MEN1 allele results in tumors primarily in parathyroid, pituitary, and endocrine pancreas. To understand the endocrine specificity of the MEN1 syndrome, we evaluated biallelic loss of Men1 by inactivating Men1 in pancreatic progenitor cells using the Cre-lox system. Men1 deletion in progenitor cells that differentiate into exocrine and endocrine pancreas did not affect normal pancreas morphogenesis and development. However, mice having homozygous inactivation of the Men1 in pancreas developed endocrine tumors with no exocrine tumor manifestation, recapitulating phenotypes seen in the MEN1 patients. In the absence of menin, the endocrine pancreas showed increase in cell proliferation, vascularity, and abnormal vascular structures; such changes were lacking in exocrine pancreas. Further analysis revealed that these endocrine manifestations were associated with up-regulation in vascular endothelial growth factor expression in both human and mouse MEN1 pancreatic endocrine tumors. Together, these data suggest the presence of cell-specific factors for menin and a permissive endocrine environment for MEN1 tumorigenesis in endocrine pancreas. Based on our analysis, we propose that menin's ability to maintain cellular and microenvironment integrity might explain the endocrine- restrictive nature of the MEN1 syndrome.

Publication types

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

MeSH terms

  • Animals
  • Cell Proliferation
  • Homeodomain Proteins / physiology*
  • Humans
  • Islets of Langerhans / blood supply
  • Mice
  • Multiple Endocrine Neoplasia Type 1 / etiology*
  • Neuroendocrine Tumors / etiology*
  • Pancreatic Neoplasms / etiology*
  • Proto-Oncogene Proteins / physiology*
  • Trans-Activators / physiology*
  • Vascular Endothelial Growth Factor A / physiology

Substances

  • Homeodomain Proteins
  • MEN1 protein, human
  • Men1 protein, mouse
  • Proto-Oncogene Proteins
  • Trans-Activators
  • Vascular Endothelial Growth Factor A
  • pancreatic and duodenal homeobox 1 protein