Wnt/β-catenin regulates blood pressure and kidney injury in rats

Biochim Biophys Acta Mol Basis Dis. 2019 Jun 1;1865(6):1313-1322. doi: 10.1016/j.bbadis.2019.01.027. Epub 2019 Jan 30.

Abstract

Activation of the renin-angiotensin system (RAS) plays a pivotal role in mediating hypertension, chronic kidney and cardiovascular diseases. As Wnt/β-catenin regulates multiple RAS genes, we speculated that this developmental signaling pathway might also participate in blood pressure (BP) regulation. To test this, we utilized two rat models of experimental hypertension: chronic angiotensin II infusion and remnant kidney after 5/6 nephrectomy. Inhibition of Wnt/β-catenin by ICG-001 blunted angiotensin II-induced hypertension. Interestingly, angiotensin II was able to induce the expression of multiple Wnt genes in vivo and in vitro, thereby creating a vicious cycle between Wnt/β-catenin and RAS activation. In the remnant kidney model, renal β-catenin was upregulated, and delayed administration of ICG-001 also blunted BP elevation and abolished the induction of angiotensinogen, renin, angiotensin-converting enzyme and angiotensin II type 1 receptor. ICG-001 also reduced albuminuria, serum creatinine and blood urea nitrogen, and inhibited renal expression of fibronectin, collagen I and plasminogen activator inhibitor-1, and suppressed the infiltration of CD3+ T cells and CD68+ monocytes/macrophages. In vitro, incubation with losartan prevented Wnt/β-catenin-mediated fibronectin, α-smooth muscle actin and Snail1 expression, suggesting that the fibrogenic action of Wnt/β-catenin is dependent on RAS activation. Taken together, these results suggest an intrinsic linkage of Wnt/β-catenin signaling with BP regulation. Our studies also demonstrate that hyperactive Wnt/β-catenin can drive hypertension and kidney damage via RAS activation.

Keywords: Blood pressure; Renal fibrosis; Renin-angiotensin system; Wnt; β-Catenin.

Publication types

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

MeSH terms

  • Albuminuria / drug therapy
  • Albuminuria / etiology
  • Albuminuria / genetics*
  • Albuminuria / physiopathology
  • Angiotensin II / administration & dosage
  • Angiotensinogen / genetics
  • Angiotensinogen / metabolism
  • Animals
  • Blood Pressure / drug effects
  • Blood Urea Nitrogen
  • Bridged Bicyclo Compounds, Heterocyclic / pharmacology
  • Collagen Type I / genetics
  • Collagen Type I / metabolism
  • Creatinine / blood
  • Cyclic AMP Response Element-Binding Protein / antagonists & inhibitors
  • Cyclic AMP Response Element-Binding Protein / genetics
  • Cyclic AMP Response Element-Binding Protein / metabolism
  • Disease Models, Animal
  • Fibronectins / genetics
  • Fibronectins / metabolism
  • Gene Expression Regulation
  • Hypertension / drug therapy
  • Hypertension / etiology
  • Hypertension / genetics*
  • Hypertension / physiopathology
  • Kidney / metabolism*
  • Kidney / physiopathology
  • Male
  • Nephrectomy / methods
  • Peptidyl-Dipeptidase A / genetics
  • Peptidyl-Dipeptidase A / metabolism
  • Plasminogen Activator Inhibitor 1 / genetics
  • Plasminogen Activator Inhibitor 1 / metabolism
  • Pyrimidinones / pharmacology
  • Rats
  • Rats, Sprague-Dawley
  • Receptor, Angiotensin, Type 1 / genetics
  • Receptor, Angiotensin, Type 1 / metabolism
  • Renin / genetics
  • Renin / metabolism
  • Renin-Angiotensin System / drug effects
  • Wnt Proteins / genetics*
  • Wnt Proteins / metabolism
  • Wnt Signaling Pathway
  • beta Catenin / genetics*
  • beta Catenin / metabolism

Substances

  • Bridged Bicyclo Compounds, Heterocyclic
  • Collagen Type I
  • Ctnnb1 protein, rat
  • Cyclic AMP Response Element-Binding Protein
  • Fibronectins
  • ICG 001
  • Plasminogen Activator Inhibitor 1
  • Pyrimidinones
  • Receptor, Angiotensin, Type 1
  • Wnt Proteins
  • beta Catenin
  • Angiotensinogen
  • Angiotensin II
  • Creatinine
  • Peptidyl-Dipeptidase A
  • Renin