Pathogenesis of nephrogenic diabetes insipidus by aquaporin-2 C-terminus mutations

Kidney Int. 2003 Jul;64(1):2-10. doi: 10.1046/j.1523-1755.2003.00049.x.

Abstract

Background: We previously reported three aquaporin-2 (AQP2) gene mutations known to cause autosomal-dominant nephrogenic diabetes insipidus (NDI) (Am J Hum Genet 69:738, 2001). The mutations were found in the C-terminus of AQP2 (721delG, 763 to 772del, and 812 to 818del). The wild-type AQP2 is a 271 amino acid protein, whereas these mutant genes were predicted to encode 330 to 333 amino acid proteins due to the frameshift mutations leading to the creation of a new stop codon 180 nucleotides downstream. The Xenopus oocyte expression study suggested that the trafficking of the mutant AQP2s was impaired.

Methods: To determine the cellular pathogenesis of these NDI-causing mutations in mammalian epithelial cells, Madin-Darby canine kidney (MDCK) cells were stably transfected with the wild-type AQP2, or the 763 to 772del mutant AQP2, or both. Cells were grown on the membrane support to examine the localization of AQP2 proteins by immunofluorescence microscopy.

Results: Confocal immunofluorescence microscopy showed that the wild-type AQP2 was expressed in the apical region, whereas the mutant AQP2 was apparently located at the basolateral region. Furthermore, the wild-type and mutant AQP2s were colocalized at the basolateral region when they were cotransfected, suggesting the formation of mixed oligomers and thereby mistargeting.

Conclusion: Mixed oligomers of the wild-type and the 763 to 772del mutant AQP2s are mistargeted to the basolateral membrane due to the dominant-negative effect of the mutant. This defect is very likely to explain the pathogenesis of autosomal-dominant NDI. The mistargeting of the apical membrane protein to the basolateral membrane is a novel molecular pathogenesis of congenital NDI.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aquaporin 2
  • Aquaporin 6
  • Aquaporins / genetics*
  • Aquaporins / metabolism
  • Cell Line
  • Cell Membrane / metabolism
  • Diabetes Insipidus, Nephrogenic / genetics*
  • Dogs
  • Gene Deletion
  • Humans
  • Intracellular Membranes / metabolism
  • Kidney / cytology
  • Kidney / metabolism
  • Microscopy, Confocal
  • Microscopy, Fluorescence
  • Mutation*
  • Transfection

Substances

  • AQP2 protein, human
  • Aquaporin 2
  • Aquaporin 6
  • Aquaporins