Hypercholesterolemia in Progressive Renal Failure Is Associated with Changes in Hepatic Heparan Sulfate - PCSK9 Interaction

J Am Soc Nephrol. 2021 Jun 1;32(6):1371-1388. doi: 10.1681/ASN.2020091376. Epub 2021 Mar 23.

Abstract

Background: Dyslipidemia is an important risk factor in CKD. The liver clears triglyceride-rich lipoproteins (TRL) via LDL receptor (LDLR), LDLR-related protein-1 (LRP-1), and heparan sulfate proteoglycans (HSPGs), mostly syndecan-1. HSPGs also facilitate LDLR degradation by proprotein convertase subtilisin/kexin type 9 (PCSK9). Progressive renal failure affects the structure and activity of hepatic lipoprotein receptors, PCSK9, and plasma cholesterol.

Methods: Uninephrectomy- and aging-induced CKD in normotensive Wistar rats and hypertensive Munich-Wistar-Frömter (MWF) rats.

Results: Compared with 22-week-old sex- and strain-matched rats, 48-week-old uninephrectomized Wistar-CKD and MWF-CKD rats showed proteinuria, increased plasma creatinine, and hypercholesterolemia (all P<0.05), which were most apparent in hypertensive MWF-CKD rats. Hepatic PCSK9 expression increased in both CKD groups (P<0.05), with unusual sinusoidal localization, which was not seen in 22-week-old rats. Heparan sulfate (HS) disaccharide analysis, staining with anti-HS mAbs, and mRNA expression of HS polymerase exostosin-1 (Ext-1), revealed elongated HS chains in both CKD groups. Solid-phase competition assays showed that the PCSK9 interaction with heparin-albumin (HS-proteoglycan analogue) was critically dependent on polysaccharide chain length. VLDL binding to HS from CKD livers was reduced (P<0.05). Proteinuria and plasma creatinine strongly associated with plasma cholesterol, PCSK9, and HS changes.

Conclusions: Progressive CKD induces hepatic HS elongation, leading to increased interaction with PCSK9. This might reduce hepatic lipoprotein uptake and thereby induce dyslipidemia in CKD. Therefore, PCSK9/HS may be a novel target to control dyslipidemia.

Keywords: PCSK9; chronic kidney disease; dyslipidemia; heparan sulfate; syndecan-1.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Aging*
  • Animals
  • Cholesterol / blood
  • Creatinine / blood
  • Disaccharides / metabolism
  • Disease Models, Animal
  • Disease Progression
  • Heparan Sulfate Proteoglycans / analogs & derivatives
  • Heparan Sulfate Proteoglycans / metabolism*
  • Hypercholesterolemia / complications
  • Hypercholesterolemia / metabolism*
  • Hypertension / complications
  • Hypertension / metabolism
  • Lipoproteins, VLDL / metabolism
  • Liver / metabolism*
  • Male
  • N-Acetylglucosaminyltransferases / genetics
  • Nephrectomy
  • Proprotein Convertase 9 / genetics
  • Proprotein Convertase 9 / metabolism*
  • Rats
  • Rats, Wistar
  • Renal Insufficiency, Chronic / complications
  • Renal Insufficiency, Chronic / metabolism*
  • Renal Insufficiency, Chronic / physiopathology
  • Syndecan-1 / genetics
  • Syndecan-1 / metabolism

Substances

  • Disaccharides
  • Heparan Sulfate Proteoglycans
  • Lipoproteins, VLDL
  • Sdc1 protein, rat
  • Syndecan-1
  • Cholesterol
  • Creatinine
  • N-Acetylglucosaminyltransferases
  • exostosin-1
  • PCSK9 protein, rat
  • Proprotein Convertase 9