Structural bases for Na+-Cl- cotransporter inhibition by thiazide diuretic drugs and activation by kinases

Nat Commun. 2024 Aug 14;15(1):7006. doi: 10.1038/s41467-024-51381-y.

Abstract

The Na+-Cl- cotransporter (NCC) drives salt reabsorption in the kidney and plays a decisive role in balancing electrolytes and blood pressure. Thiazide and thiazide-like diuretics inhibit NCC-mediated renal salt retention and have been cornerstones for treating hypertension and edema since the 1950s. Here we determine NCC co-structures individually complexed with the thiazide drug hydrochlorothiazide, and two thiazide-like drugs chlorthalidone and indapamide, revealing that they fit into an orthosteric site and occlude the NCC ion translocation pathway. Aberrant NCC activation by the WNKs-SPAK kinase cascade underlies Familial Hyperkalemic Hypertension, but it remains unknown whether/how phosphorylation transforms the NCC structure to accelerate ion translocation. We show that an intracellular amino-terminal motif of NCC, once phosphorylated, associates with the carboxyl-terminal domain, and together, they interact with the transmembrane domain. These interactions suggest a phosphorylation-dependent allosteric network that directly influences NCC ion translocation.

MeSH terms

  • Animals
  • Chlorthalidone / chemistry
  • Chlorthalidone / metabolism
  • Chlorthalidone / pharmacology
  • Diuretics / chemistry
  • Diuretics / metabolism
  • Diuretics / pharmacology
  • HEK293 Cells
  • Humans
  • Hydrochlorothiazide* / chemistry
  • Hydrochlorothiazide* / pharmacology
  • Models, Molecular
  • Phosphorylation
  • Protein Kinases / chemistry
  • Protein Kinases / metabolism
  • Protein Serine-Threonine Kinases
  • Sodium Chloride Symporter Inhibitors* / pharmacology
  • Solute Carrier Family 12, Member 3* / chemistry
  • Solute Carrier Family 12, Member 3* / metabolism
  • Thiazides / chemistry
  • Thiazides / metabolism
  • Thiazides / pharmacology

Substances

  • Solute Carrier Family 12, Member 3
  • Hydrochlorothiazide
  • Sodium Chloride Symporter Inhibitors
  • Chlorthalidone
  • Protein Kinases
  • Diuretics
  • Thiazides
  • STK39 protein, human
  • Protein Serine-Threonine Kinases