The small leucine-rich proteoglycan BGN accumulates in CADASIL and binds to NOTCH3

Transl Stroke Res. 2015 Apr;6(2):148-55. doi: 10.1007/s12975-014-0379-1. Epub 2015 Jan 13.

Abstract

Cerebral autosomal dominant arteriopathy with subcortical infarcts and leukoencephalopathy (CADASIL) is an inherited form of cerebral small vessel disease caused by mutations in conserved residues of NOTCH3. Affected arteries of CADASIL feature fibrosis and accumulation of NOTCH3. A variety of collagen subtypes (types I, III, IV, and VI) have been identified in fibrotic CADASIL vessels. Biglycan (BGN) and decorin (DCN) are class I members of the small leucine-rich proteoglycan (SLRP) family that regulate collagen fibril size. Because DCN has been shown to deposit in arteries in cerebral small vessel disease, we tested whether BGN accumulates in arteries of CADASIL brains. BGN was strongly expressed in both small penetrating and leptomeningeal arteries of CADASIL brain. BGN protein was localized to all three layers of arteries (intima, media, and adventitia). Substantially, more immunoreactivity was observed in CADASIL brains compared to controls. Immunoblotting of brain lysates showed a fourfold increase in CADASIL brains (compared to controls). Messenger RNA encoding BGN was also increased in CADASIL and was localized by in situ hybridization to all three vascular layers in CADASIL. Human cerebrovascular smooth muscle cells exposed to purified NOTCH3 ectodomain upregulated BGN, DCN, and COL4A1 through mechanisms that are sensitive to rapamycin, a potent mTOR inhibitor. In addition, BGN protein interacted directly with NOTCH3 protein in cell culture and in direct protein interaction assays. In conclusion, BGN is a CADASIL-enriched protein that potentially accumulates in vessels by mTOR-mediated transcriptional activation and/or post-translational accumulation via protein interactions with NOTCH3 and collagen.

MeSH terms

  • Aged
  • Aged, 80 and over
  • Biglycan / genetics
  • Biglycan / metabolism*
  • Brain / metabolism*
  • CADASIL / metabolism*
  • CADASIL / pathology*
  • Dose-Response Relationship, Drug
  • Female
  • Gene Expression Regulation / drug effects
  • Gene Expression Regulation / physiology*
  • HEK293 Cells
  • Humans
  • Immunoprecipitation
  • Immunosuppressive Agents / pharmacology
  • Male
  • Middle Aged
  • Myocytes, Smooth Muscle / metabolism
  • Protein Binding / drug effects
  • RNA, Messenger / metabolism
  • Receptor, Notch3
  • Receptors, Notch / metabolism*
  • Sirolimus / pharmacology
  • Transfection

Substances

  • BGN protein, human
  • Biglycan
  • Immunosuppressive Agents
  • NOTCH3 protein, human
  • RNA, Messenger
  • Receptor, Notch3
  • Receptors, Notch
  • Sirolimus