Deficiency of FLCN in mouse kidney led to development of polycystic kidneys and renal neoplasia

PLoS One. 2008;3(10):e3581. doi: 10.1371/journal.pone.0003581. Epub 2008 Oct 30.

Abstract

The Birt-Hogg-Dubé (BHD) disease is a genetic cancer syndrome. The responsible gene, BHD, has been identified by positional cloning and thought to be a novel tumor suppressor gene. BHD mutations cause many types of diseases including renal cell carcinomas, fibrofolliculomas, spontaneous pneumothorax, lung cysts, and colonic polyps/cancers. By combining Gateway Technology with the Ksp-Cre gene knockout system, we have developed a kidney-specific BHD knockout mouse model. BHD(flox/flox)/Ksp-Cre mice developed enlarged kidneys characterized by polycystic kidneys, hyperplasia, and cystic renal cell carcinoma. The affected BHD(flox/flox)/Ksp-Cre mice died of renal failure at approximate three weeks of age, having blood urea nitrogen levels over tenfold higher than those of BHD (flox/+)/Ksp-Cre and wild-type littermate controls. We further demonstrated that these phenotypes were caused by inactivation of BHD and subsequent activation of the mTOR pathway. Application of rapamycin, which inhibits mTOR activity, to the affected mice led to extended survival and inhibited further progression of cystogenesis. These results provide a correlation of kidney-targeted gene inactivation with renal carcinoma, and they suggest that the BHD product FLCN, functioning as a cyst and tumor suppressor, like other hamartoma syndrome-related proteins such as PTEN, LKB1, and TSC1/2, is a component of the mTOR pathway, constituting a novel FLCN-mTOR signaling branch that regulates cell growth/proliferation.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Animals, Newborn
  • Carcinoma, Renal Cell / genetics*
  • Carcinoma, Renal Cell / metabolism
  • Carcinoma, Renal Cell / pathology
  • Carrier Proteins / metabolism
  • Cloning, Molecular
  • Embryo, Mammalian
  • Genes, Lethal
  • Genes, Tumor Suppressor / physiology
  • Kidney / metabolism*
  • Kidney / pathology
  • Kidney Neoplasms / genetics*
  • Kidney Neoplasms / metabolism
  • Kidney Neoplasms / pathology
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Models, Biological
  • Organ Specificity / genetics
  • Phosphotransferases (Alcohol Group Acceptor) / metabolism
  • Polycystic Kidney Diseases / genetics*
  • Polycystic Kidney Diseases / metabolism
  • Polycystic Kidney Diseases / pathology
  • Proto-Oncogene Proteins / genetics*
  • Proto-Oncogene Proteins / metabolism
  • TOR Serine-Threonine Kinases
  • Tumor Suppressor Proteins / genetics*
  • Tumor Suppressor Proteins / metabolism

Substances

  • Carrier Proteins
  • FLCN protein, human
  • Proto-Oncogene Proteins
  • Tumor Suppressor Proteins
  • Phosphotransferases (Alcohol Group Acceptor)
  • MTOR protein, human
  • mTOR protein, mouse
  • TOR Serine-Threonine Kinases