Lower plasma PCSK9 in normocholesterolemic subjects is associated with upregulated adipose tissue surface-expression of LDLR and CD36 and NLRP3 inflammasome

Physiol Rep. 2021 Feb;9(3):e14721. doi: 10.14814/phy2.14721.

Abstract

Background: LDL-cholesterol lowering variants that upregulate receptor uptake of LDL, such as in PCSK9 and HMGCR, are associated with diabetes via unclear mechanisms. Activation of the NLRP3 inflammasome/interleukin-1 beta (IL-1β) pathway promotes white adipose tissue (WAT) dysfunction and type 2 diabetes (T2D) and is regulated by LDL receptors (LDLR and CD36). We hypothesized that: (a) normocholesterolemic subjects with lower plasma PCSK9, identifying those with higher WAT surface-expression of LDLR and CD36, have higher activation of WAT NLRP3 inflammasome and T2D risk factors, and; (b) LDL upregulate adipocyte NLRP3 inflammasome and inhibit adipocyte function.

Methodology: Post hoc analysis was conducted in 27 overweight/ obese subjects with normal plasma LDL-C and measures of disposition index (DI during Botnia clamps) and postprandial fat metabolism. WAT was assessed for surface-expression of LDLR and CD36 (immunohistochemistry), protein expression (immunoblot), IL-1β secretion (AlphaLISA), and function (3 H-triolein storage).

Results: Compared to subjects with higher than median plasma PCSK9, subjects with lower PCSK9 had higher WAT surface-expression of LDLR (+81%) and CD36 (+36%), WAT IL-1β secretion (+284%), plasma IL-1 receptor-antagonist (+85%), and postprandial hypertriglyceridemia, and lower WAT pro-IL-1β protein (-66%), WAT function (-62%), and DI (-28%), without group-differences in body composition, energy intake or expenditure. Adjusting for WAT LDLR or CD36 eliminated group-differences in WAT function, DI, and postprandial hypertriglyceridemia. Native LDL inhibited Simpson-Golabi Behmel-syndrome (SGBS) adipocyte differentiation and function and increased inflammation.

Conclusion: Normocholesterolemic subjects with lower plasma PCSK9 and higher WAT surface-expression of LDLR and CD36 have higher WAT NLRP3 inflammasome activation and T2D risk factors. This may be due to LDL-induced inhibition of adipocyte function.

Keywords: adipose tissue and systemic inflammation; apoB-lipoproteins; cardiometabolic risk; plasma apoB-to-PCSK9.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adipocytes, White / immunology
  • Adipocytes, White / metabolism
  • Adipogenesis
  • Adipose Tissue, White / immunology
  • Adipose Tissue, White / metabolism*
  • Aged
  • Biomarkers / blood
  • CD36 Antigens / metabolism*
  • Cells, Cultured
  • Cholesterol / blood*
  • Diabetes Mellitus, Type 2 / etiology
  • Down-Regulation
  • Female
  • Humans
  • Inflammasomes / metabolism*
  • Interleukin-1beta / metabolism
  • Male
  • Middle Aged
  • NLR Family, Pyrin Domain-Containing 3 Protein / metabolism*
  • Obesity / blood*
  • Obesity / complications
  • Obesity / enzymology
  • Obesity / immunology
  • Proprotein Convertase 9 / blood*
  • Receptors, LDL / metabolism*
  • Risk Assessment
  • Risk Factors

Substances

  • Biomarkers
  • CD36 Antigens
  • CD36 protein, human
  • IL1B protein, human
  • Inflammasomes
  • Interleukin-1beta
  • LDLR protein, human
  • NLR Family, Pyrin Domain-Containing 3 Protein
  • NLRP3 protein, human
  • Receptors, LDL
  • Cholesterol
  • PCSK9 protein, human
  • Proprotein Convertase 9