HANAC Syndrome Col4a1 Mutation Causes Neonate Glomerular Hyperpermeability and Adult Glomerulocystic Kidney Disease

J Am Soc Nephrol. 2016 Apr;27(4):1042-54. doi: 10.1681/ASN.2014121217. Epub 2015 Aug 10.

Abstract

Hereditary angiopathy, nephropathy, aneurysms, and muscle cramps (HANAC) syndrome is an autosomal dominant syndrome caused by mutations in COL4A1 that encodes the α1 chain of collagen IV, a major component of basement membranes. Patients present with cerebral small vessel disease, retinal tortuosity, muscle cramps, and kidney disease consisting of multiple renal cysts, chronic kidney failure, and sometimes hematuria. Mutations producing HANAC syndrome localize within the integrin binding site containing CB3[IV] fragment of the COL4A1 protein. To investigate the pathophysiology of HANAC syndrome, we generated mice harboring the Col4a1 p.Gly498Val mutation identified in a family with the syndrome. Col4a1 G498V mutation resulted in delayed glomerulogenesis and podocyte differentiation without reduction of nephron number, causing albuminuria and hematuria in newborns. The glomerular defects resolved within the first month, but glomerular cysts developed in 3-month-old mutant mice. Abnormal structure of Bowman's capsule was associated with metalloproteinase induction and activation of the glomerular parietal epithelial cells that abnormally expressed CD44,α-SMA, ILK, and DDR1. Inflammatory infiltrates were observed around glomeruli and arterioles. Homozygous Col4a1 G498V mutant mice additionally showed dysmorphic papillae and urinary concentration defects. These results reveal a developmental role for the α1α1α2 collagen IV molecule in the embryonic glomerular basement membrane, affecting podocyte differentiation. The observed association between molecular alteration of the collagenous network in Bowman's capsule of the mature kidney and activation of parietal epithelial cells, matrix remodeling, and inflammation may account for glomerular cyst development and CKD in patients with COL4A1-related disorders.

Keywords: genetic renal disease; glomerular epithelial cells; kidney development; molecular biology.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Age Factors
  • Animals
  • Animals, Newborn
  • Collagen Type IV / genetics*
  • Kidney Diseases, Cystic / etiology*
  • Kidney Diseases, Cystic / metabolism
  • Kidney Glomerulus / metabolism
  • Mice
  • Muscle Cramp / complications*
  • Muscle Cramp / genetics*
  • Muscle Cramp / metabolism
  • Muscle Cramp / physiopathology
  • Mutation*
  • Permeability
  • Raynaud Disease / complications*
  • Raynaud Disease / genetics*
  • Raynaud Disease / metabolism
  • Raynaud Disease / physiopathology

Substances

  • Collagen Type IV

Supplementary concepts

  • Angiopathy, Hereditary, With Nephropathy, Aneurysms, And Muscle Cramps