C3a receptor blockade protects podocytes from injury in diabetic nephropathy

JCI Insight. 2020 Mar 12;5(5):e131849. doi: 10.1172/jci.insight.131849.

Abstract

Renal activation of the complement system has been described in patients with diabetic nephropathy (DN), although its pathological relevance is still ill-defined. Here, we studied whether glomerular C3a, generated by uncontrolled complement activation, promotes podocyte damage, leading to proteinuria and renal injury in mice with type 2 diabetes. BTBR ob/ob mice exhibited podocyte loss, albuminuria, and glomerular injury accompanied by C3 deposits and increased C3a and C3a receptor (C3aR) levels. Decreased glomerular nephrin and α-actinin4 expression, coupled with integrin-linked kinase induction, were also observed. Treatment of DN mice with a C3aR antagonist enhanced podocyte density and preserved their phenotype, limiting proteinuria and glomerular injury. Mechanistically, ultrastructural and functional mitochondrial alterations, accompanied by downregulation of antioxidant superoxide dismutase 2 (SOD2) and increased protein oxidation, occurred in podocytes and were normalized by C3aR blockade. In cultured podocytes, C3a induced cAMP-dependent mitochondrial fragmentation. Alterations of mitochondrial membrane potential, SOD2 expression, and energetic metabolism were also found in response to C3a. Notably, C3a-induced podocyte motility was inhibited by SS-31, a peptide with mitochondrial protective effects. These data indicate that C3a blockade represents a potentially novel therapeutic strategy in DN for preserving podocyte integrity through the maintenance of mitochondrial functions.

Keywords: Complement; Diabetes; Mitochondria; Nephrology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Complement Activation
  • Complement C3a / metabolism*
  • Cyclic AMP / metabolism
  • Diabetes Mellitus, Type 2 / complications
  • Diabetes Mellitus, Type 2 / metabolism
  • Diabetic Nephropathies / metabolism
  • Diabetic Nephropathies / pathology*
  • Disease Models, Animal
  • Kidney Glomerulus / pathology
  • Mice
  • Mitochondria / metabolism
  • Oxidative Stress
  • Podocytes / metabolism
  • Podocytes / pathology*
  • Receptors, Complement / antagonists & inhibitors*
  • Receptors, Complement / metabolism
  • Superoxide Dismutase / metabolism

Substances

  • Receptors, Complement
  • Complement C3a
  • Cyclic AMP
  • Superoxide Dismutase
  • superoxide dismutase 2