Scattered Deletion of PKD1 in Kidneys Causes a Cystic Snowball Effect and Recapitulates Polycystic Kidney Disease

J Am Soc Nephrol. 2015 Jun;26(6):1322-33. doi: 10.1681/ASN.2013080864. Epub 2014 Oct 31.

Abstract

In total, 1 in 1000 individuals carries a germline mutation in the PKD1 or PKD2 gene, which leads to autosomal dominant polycystic kidney disease (ADPKD). Cysts can form early in life and progressively increase in number and size during adulthood. Extensive research has led to the presumption that somatic inactivation of the remaining allele initiates the formation of cysts, and the progression is further accelerated by renal injury. However, this hypothesis is primarily on the basis of animal studies, in which the gene is inactivated simultaneously in large percentages of kidney cells. To mimic human ADPKD in mice more precisely, we reduced the percentage of Pkd1-deficient kidney cells to 8%. Notably, no pathologic changes occurred for 6 months after Pkd1 deletion, and additional renal injury increased the likelihood of cyst formation but never triggered rapid PKD. In mildly affected mice, cysts were not randomly distributed throughout the kidney but formed in clusters, which could be explained by increased PKD-related signaling in not only cystic epithelial cells but also, healthy-appearing tubules near cysts. In the majority of mice, these changes preceded a rapid and massive onset of severe PKD that was remarkably similar to human ADPKD. Our data suggest that initial cysts are the principal trigger for a snowball effect driving the formation of new cysts, leading to the progression of severe PKD. In addition, this approach is a suitable model for mimicking human ADPKD and can be used for preclinical testing.

Keywords: autosomal dominant polycystic kidney disease; genetic renal disease; polycystic kidney disease; renal injury; signaling.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Proliferation
  • Disease Models, Animal
  • Disease Progression
  • Dose-Response Relationship, Drug
  • Gene Deletion*
  • Gene Expression Regulation
  • Germ-Line Mutation*
  • Humans
  • Immunohistochemistry
  • Magnetic Resonance Imaging
  • Mice
  • Phenotype
  • Polycystic Kidney Diseases / genetics
  • Polycystic Kidney Diseases / pathology
  • Polycystic Kidney, Autosomal Dominant / genetics*
  • Polycystic Kidney, Autosomal Dominant / pathology
  • Polycystic Kidney, Autosomal Dominant / physiopathology
  • Random Allocation
  • Recombination, Genetic
  • Signal Transduction
  • Statistics, Nonparametric
  • TRPP Cation Channels / genetics*
  • Tamoxifen / adverse effects*
  • Tamoxifen / pharmacology

Substances

  • TRPP Cation Channels
  • polycystic kidney disease 1 protein
  • Tamoxifen