Reduced decay-accelerating factor expression promotes complement-mediated cystogenesis in murine ADPKD

JCI Insight. 2024 May 23;9(12):e175220. doi: 10.1172/jci.insight.175220.

Abstract

Patients with autosomal dominant polycystic kidney disease (ADPKD), a genetic disease due to mutations of the PKD1 or PKD2 gene, show signs of complement activation in the urine and cystic fluid, but their pathogenic role in cystogenesis is unclear. We tested the causal relationship between complement activation and cyst growth using a Pkd1KO renal tubular cell line and newly generated conditional Pkd1-/- C3-/- mice. Pkd1-deficient tubular cells have increased expression of complement-related genes (C3, C5, CfB, C3ar, and C5ar1), while the gene and protein expression of complement regulators DAF, CD59, and Crry is decreased. Pkd1-/- C3-/- mice are unable to fully activate the complement cascade and are characterized by a significantly slower kidney cystogenesis, preserved renal function, and reduced intrarenal inflammation compared with Pkd1-/- C3+/+ controls. Transgenic expression of the cytoplasmic C-terminal tail of Pkd1 in Pkd1KO cells lowered C5ar1 expression, restored Daf levels, and reduced cell proliferation. Consistently, both DAF overexpression and pharmacological inhibition of C5aR1 (but not C3aR) reduced Pkd1KO cell proliferation. In conclusion, the loss of Pkd1 promotes unleashed activation of locally produced complement by downregulating DAF expression in renal tubular cells. Increased C5a formation and C5aR1 activation in tubular cells promotes cyst growth, offering a new therapeutic target.

Keywords: Complement; Nephrology.

MeSH terms

  • Animals
  • CD55 Antigens* / genetics
  • CD55 Antigens* / metabolism
  • Cell Line
  • Cell Proliferation
  • Complement Activation
  • Complement C3* / genetics
  • Complement C3* / metabolism
  • Disease Models, Animal
  • Humans
  • Male
  • Mice
  • Mice, Knockout*
  • Polycystic Kidney, Autosomal Dominant* / genetics
  • Polycystic Kidney, Autosomal Dominant* / metabolism
  • Polycystic Kidney, Autosomal Dominant* / pathology
  • Receptor, Anaphylatoxin C5a / genetics
  • Receptor, Anaphylatoxin C5a / metabolism
  • Receptors, Complement 3b / genetics
  • Receptors, Complement 3b / metabolism
  • TRPP Cation Channels / genetics
  • TRPP Cation Channels / metabolism

Substances

  • CD55 Antigens
  • Complement C3
  • Receptor, Anaphylatoxin C5a
  • polycystic kidney disease 1 protein
  • C5ar1 protein, mouse
  • TRPP Cation Channels
  • Cr1l protein, mouse
  • C3 protein, mouse
  • Receptors, Complement 3b