Bone marrow transplantation improves proximal tubule dysfunction in a mouse model of Dent disease

Kidney Int. 2017 Apr;91(4):842-855. doi: 10.1016/j.kint.2016.11.016. Epub 2017 Jan 28.

Abstract

Dent disease is a rare X-linked tubulopathy caused by mutations in the endosomal chloride-proton exchanger (ClC-5) resulting in defective receptor-mediated endocytosis and severe proximal tubule dysfunction. Bone marrow transplantation has recently been shown to preserve kidney function in cystinosis, a lysosomal storage disease causing proximal tubule dysfunction. Here we test the effects of bone marrow transplantation in Clcn5Y/- mice, a faithful model for Dent disease. Transplantation of wild-type bone marrow in Clcn5Y/- mice significantly improved proximal tubule dysfunction, with decreased low-molecular-weight proteinuria, glycosuria, calciuria, and polyuria four months after transplantation, compared to Clcn5Y/- mice transplanted with ClC-5 knockout bone marrow. Bone marrow-derived cells engrafted in the interstitium, surrounding proximal tubule cells, which showed a rescue of the apical expression of ClC-5 and megalin receptors. The improvement of proximal tubule dysfunction correlated with Clcn5 gene expression in kidneys of mice transplanted with wild-type bone marrow cells. Coculture of Clcn5Y/- proximal tubule cells with bone marrow-derived cells confirmed rescue of ClC-5 and megalin, resulting in improved endocytosis. Nanotubular extensions between the engrafted bone marrow-derived cells and proximal tubule cells were observed in vivo and in vitro. No rescue was found when the formation of the tunneling nanotubes was prevented by actin depolymerization or when cells were physically separated by transwell inserts. Thus, bone marrow transplantation may rescue the epithelial phenotype due to an inherited endosomal defect. Direct contacts between bone marrow-derived cells and diseased tubular cells play a key role in the rescue mechanism.

Keywords: ClC-5; bone marrow cell; low-molecular weight proteinuria; proximal tubule; renal Fanconi syndrome.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Bone Marrow Transplantation*
  • Cell Communication
  • Cells, Cultured
  • Chloride Channels / deficiency*
  • Chloride Channels / genetics
  • Coculture Techniques
  • Dent Disease / genetics
  • Dent Disease / metabolism
  • Dent Disease / physiopathology
  • Dent Disease / surgery*
  • Disease Models, Animal
  • Endocytosis
  • Genetic Predisposition to Disease
  • Glycosuria / genetics
  • Glycosuria / metabolism
  • Glycosuria / physiopathology
  • Glycosuria / prevention & control
  • Hypercalciuria / genetics
  • Hypercalciuria / metabolism
  • Hypercalciuria / physiopathology
  • Hypercalciuria / prevention & control
  • Kidney Tubules, Proximal / metabolism
  • Kidney Tubules, Proximal / pathology
  • Kidney Tubules, Proximal / physiopathology*
  • Low Density Lipoprotein Receptor-Related Protein-2 / metabolism
  • Male
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Phenotype
  • Polyuria / genetics
  • Polyuria / metabolism
  • Polyuria / physiopathology
  • Polyuria / prevention & control
  • Proteinuria / genetics
  • Proteinuria / metabolism
  • Proteinuria / physiopathology
  • Proteinuria / prevention & control
  • Recovery of Function
  • Transplantation Chimera

Substances

  • CLC-5 chloride channel
  • Chloride Channels
  • Low Density Lipoprotein Receptor-Related Protein-2
  • Lrp2 protein, mouse