Aberrant glycosylation and localization of polycystin-1 cause polycystic kidney in an AQP11 knockout model

J Am Soc Nephrol. 2014 Dec;25(12):2789-99. doi: 10.1681/ASN.2013060614. Epub 2014 May 22.

Abstract

We previously reported that disruption of the aquaporin-11 (AQP11) gene in mice resulted in cystogenesis in the kidney. In this study, we aimed to clarify the mechanism of cystogenesis in AQP11(-/-) mice. To enable the analyses of AQP11 at the protein level in vivo, AQP11 BAC transgenic mice (Tg(AQP11)) that express 3×HA-tagged AQP11 protein were generated. This AQP11 localized to the endoplasmic reticulum (ER) of proximal tubule cells in Tg(AQP11) mice and rescued renal cystogenesis in AQP11(-/-) mice. Therefore, we hypothesized that the absence of AQP11 in the ER could result in impaired quality control and aberrant trafficking of polycystin-1 (PC-1) and polycystin-2 (PC-2). Compared with kidneys of wild-type mice, AQP11(-/-) kidneys exhibited increased protein expression levels of PC-1 and decreased protein expression levels of PC-2. Moreover, PC-1 isolated from AQP11(-/-) mice displayed an altered electrophoretic mobility caused by impaired N-glycosylation processing, and density gradient centrifugation of kidney homogenate and in vivo protein biotinylation revealed impaired membrane trafficking of PC-1 in these mice. Finally, we showed that the Pkd1(+/-) background increased the severity of cystogenesis in AQP11(-/-) mouse kidneys, indicating that PC-1 is involved in the mechanism of cystogenesis in AQP11(-/-) mice. Additionally, the primary cilia of proximal tubules were elongated in AQP11(-/-) mice. Taken together, these data show that impaired glycosylation processing and aberrant membrane trafficking of PC-1 in AQP11(-/-) mice could be a key mechanism of cystogenesis in AQP11(-/-) mice.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Aquaporins / genetics*
  • Biotinylation
  • Disease Models, Animal
  • Endoplasmic Reticulum / metabolism
  • Genotype
  • Glycosylation
  • Immunoblotting
  • Kidney / metabolism
  • Kidney Tubules, Proximal / metabolism
  • Mice
  • Mice, Knockout
  • Mice, Transgenic
  • Polycystic Kidney Diseases / genetics*
  • Subcellular Fractions / metabolism
  • TRPP Cation Channels / genetics
  • TRPP Cation Channels / metabolism*
  • Transgenes

Substances

  • Aqp11 protein, mouse
  • Aquaporins
  • TRPP Cation Channels
  • polycystic kidney disease 1 protein