Murine glomerular transcriptome links endothelial cell-specific molecule-1 deficiency with susceptibility to diabetic nephropathy

PLoS One. 2017 Sep 21;12(9):e0185250. doi: 10.1371/journal.pone.0185250. eCollection 2017.

Abstract

Diabetic nephropathy (DN) is the leading cause of kidney disease; however, there are no early biomarkers and no cure. Thus, there is a large unmet need to predict which individuals will develop nephropathy and to understand the molecular mechanisms that govern this susceptibility. We compared the glomerular transcriptome from mice with distinct susceptibilities to DN at four weeks after induction of diabetes, but before histologic injury, and identified differential regulation of genes that modulate inflammation. From these genes, we identified endothelial cell specific molecule-1 (Esm-1), as a glomerular-enriched determinant of resistance to DN. Glomerular Esm-1 mRNA and protein were lower in DN-susceptible, DBA/2, compared to DN-resistant, C57BL/6, mice. We demonstrated higher Esm-1 secretion from primary glomerular cultures of diabetic mice, and high glucose was sufficient to increase Esm-1 mRNA and protein secretion in both strains of mice. However, induction was significantly attenuated in DN-susceptible mice. Urine Esm-1 was also significantly higher only in DN-resistant mice. Moreover, using intravital microscopy and a biomimetic microfluidic assay, we showed that Esm-1 inhibited rolling and transmigration in a dose-dependent manner. For the first time we have uncovered glomerular-derived Esm-1 as a potential non-invasive biomarker of DN. Esm-1 inversely correlates with disease susceptibility and inhibits leukocyte infiltration, a critical factor in protecting the kidney from DN.

MeSH terms

  • Animals
  • Cell Movement / drug effects
  • Diabetic Nephropathies / genetics*
  • Diabetic Nephropathies / metabolism
  • Dose-Response Relationship, Drug
  • Gene Expression Profiling*
  • Genetic Predisposition to Disease*
  • Glucose / pharmacology
  • Humans
  • Kidney Glomerulus / drug effects
  • Kidney Glomerulus / metabolism*
  • Leukocytes / cytology
  • Leukocytes / drug effects
  • Male
  • Mice
  • Neoplasm Proteins / pharmacology
  • Proteoglycans / deficiency*
  • Proteoglycans / genetics*
  • Proteoglycans / pharmacology
  • RNA, Messenger / genetics
  • RNA, Messenger / metabolism
  • Species Specificity

Substances

  • ESM1 protein, human
  • Neoplasm Proteins
  • Proteoglycans
  • RNA, Messenger
  • endothelial cell-specific molecule-1, mouse
  • Glucose