Renal COP9 Signalosome Deficiency Alters CUL3-KLHL3-WNK Signaling Pathway

J Am Soc Nephrol. 2018 Nov;29(11):2627-2640. doi: 10.1681/ASN.2018030333. Epub 2018 Oct 9.

Abstract

Background: The familial hyperkalemic hypertension (FHHt) cullin 3 (CUL3) mutant does not degrade WNK kinases normally, thereby leading to thiazide-sensitive Na-Cl cotransporter (NCC) activation. CUL3 mutant (CUL3Δ9) does not bind normally to the COP9 signalosome (CSN), a deneddylase involved in regulating cullin-RING ligases. CUL3Δ9 also caused increased degradation of the CUL3-WNK substrate adaptor kelch-like 3 (KLHL3). Here, we sought to determine how defective CSN action contributes to the CUL3Δ9 phenotype.

Methods: The Pax8/LC1 mouse system was used to generate mice in which the catalytically active CSN subunit, Jab1, was deleted only along the nephron, after full development (KS-Jab1-/-).

Results: Western blot analysis demonstrated that Jab1 deletion increased the abundance of neddylated CUL3. Moreover, total CUL3 expression was reduced, suggesting decreased CUL3 stability. KLHL3 was almost completely absent in KS-Jab1-/- mice. Conversely, the protein abundances of WNK1, WNK4, and SPAK kinases were substantially higher. Activation of WNK4, SPAK, and OSR1 was indicated by higher phosphorylated protein levels and translocation of the proteins into puncta, as observed by immunofluorescence. The ratio of phosphorylated NCC to total NCC was also higher. Surprisingly, NCC protein abundance was low, likely contributing to hypokalemia and Na+ and K+ wasting. Additionally, long-term Jab1 deletion resulted in kidney damage.

Conclusions: Together, the results indicate that deficient CSN binding contributes importantly to the FHHt phenotype. Although defective CUL3Δ9-faciliated WNK4 degradation likely contributes, dominant effects on KLHL3 may be a second factor that is necessary for the phenotype.

Keywords: Cell & Transport Physiology; Na transport; distal tubule; renal hypertension.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adaptor Proteins, Signal Transducing
  • Animals
  • COP9 Signalosome Complex / deficiency*
  • COP9 Signalosome Complex / genetics*
  • COP9 Signalosome Complex / metabolism
  • Cullin Proteins / metabolism
  • Disease Models, Animal
  • Female
  • HEK293 Cells
  • Humans
  • Intracellular Signaling Peptides and Proteins / genetics
  • Intracellular Signaling Peptides and Proteins / metabolism
  • Kidney / metabolism*
  • Kidney / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Mice, Knockout
  • Microfilament Proteins / metabolism
  • Microscopy, Fluorescence
  • Mutation
  • Nephrons / metabolism
  • Nephrons / pathology
  • Peptide Hydrolases / deficiency
  • Peptide Hydrolases / genetics
  • Peptide Hydrolases / metabolism
  • Phenotype
  • Protein Serine-Threonine Kinases / metabolism
  • Proteolysis
  • Pseudohypoaldosteronism / genetics*
  • Pseudohypoaldosteronism / metabolism*
  • Pseudohypoaldosteronism / pathology
  • Signal Transduction

Substances

  • Adaptor Proteins, Signal Transducing
  • Cul3 protein, mouse
  • Cullin Proteins
  • Intracellular Signaling Peptides and Proteins
  • KLHL3 protein, mouse
  • Microfilament Proteins
  • Prkwnk4 protein, mouse
  • Stk39 protein, mouse
  • OXSR1 protein, mouse
  • Protein Serine-Threonine Kinases
  • Peptide Hydrolases
  • COPS5 protein, human
  • Cops5 protein, mouse
  • COP9 Signalosome Complex