Regardless of etiology, progressive renal disease causes ultrastructural and functional alterations of peritubular capillaries

Kidney Int. 2017 Jan;91(1):70-85. doi: 10.1016/j.kint.2016.07.038. Epub 2016 Sep 24.

Abstract

Progressive renal diseases are associated with rarefaction of peritubular capillaries, but the ultrastructural and functional alterations of the microvasculature are not well described. To study this, we analyzed different time points during progressive kidney damage and fibrosis in 3 murine models of different disease etiologies. These models were unilateral ureteral obstruction, unilateral ischemia-reperfusion injury, and Col4a3-deficient mice, we analyzed ultrastructural alterations in patient biopsy specimens. Compared with kidneys of healthy mice, we found a significant and progressive reduction of peritubular capillaries in all models analyzed. Ultrastructurally, compared with the kidneys of control mice, focal widening of the subendothelial space and higher numbers of endothelial vacuoles and caveolae were found in fibrotic kidneys. Quantitative analysis showed that peritubular capillary endothelial cells in fibrotic kidneys had significantly and progressively reduced numbers of fenestrations and increased thickness of the cell soma and lamina densa of the capillary basement membrane. Similar ultrastructural changes were also observed in patient's kidney biopsy specimens. Compared with healthy murine kidneys, fibrotic kidneys had significantly increased extravasation of Evans blue dye in all 3 models. The extravasation could be visualized using 2-photon microscopy in real time in living animals and was mainly localized to capillary branching points. Finally, fibrotic kidneys in all models exhibited a significantly greater degree of interstitial deposition of fibrinogen. Thus, peritubular capillaries undergo significant ultrastructural and functional alterations during experimental progressive renal diseases, independent of the underlying injury. Analyses of these alterations could provide read-outs for the evaluation of therapeutic approaches targeting the renal microvasculature.

Keywords: chronic kidney disease; endothelial cells; endothelial dysfunction; leakage; microvasculature; ultrastructure.

MeSH terms

  • Animals
  • Basement Membrane / blood supply
  • Basement Membrane / pathology
  • Biopsy
  • Capillaries / pathology*
  • Capillaries / ultrastructure
  • Disease Models, Animal
  • Disease Progression
  • Endothelial Cells / pathology*
  • Endothelial Cells / ultrastructure
  • Fibrosis
  • Humans
  • Immunohistochemistry
  • Kidney Diseases / etiology
  • Kidney Diseases / genetics
  • Kidney Diseases / pathology*
  • Kidney Tubules / blood supply*
  • Kidney Tubules / cytology
  • Kidney Tubules / pathology*
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microcirculation
  • Microscopy, Electron, Scanning
  • Microscopy, Fluorescence, Multiphoton
  • Protein Serine-Threonine Kinases / genetics
  • Reperfusion Injury / complications
  • Time Factors
  • Ureteral Obstruction / complications

Substances

  • Col4a3bp protein, mouse
  • Protein Serine-Threonine Kinases