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


Journal

Physiological reports
ISSN: 2051-817X
Titre abrégé: Physiol Rep
Pays: United States
ID NLM: 101607800

Informations de publication

Date de publication:
02 2021
Historique:
received: 19 09 2020
revised: 16 12 2020
accepted: 17 12 2020
entrez: 2 2 2021
pubmed: 3 2 2021
medline: 15 12 2021
Statut: ppublish

Résumé

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. 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 ( 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. 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.

Sections du résumé

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 (
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.

Identifiants

pubmed: 33527668
doi: 10.14814/phy2.14721
pmc: PMC7851436
doi:

Substances chimiques

Biomarkers 0
CD36 Antigens 0
CD36 protein, human 0
IL1B protein, human 0
Inflammasomes 0
Interleukin-1beta 0
LDLR protein, human 0
NLR Family, Pyrin Domain-Containing 3 Protein 0
NLRP3 protein, human 0
Receptors, LDL 0
Cholesterol 97C5T2UQ7J
PCSK9 protein, human EC 3.4.21.-
Proprotein Convertase 9 EC 3.4.21.-

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e14721

Subventions

Organisme : CIHR
ID : 93581
Pays : Canada
Organisme : CIHR
ID : 123409
Pays : Canada
Organisme : CIHR
ID : SVB#145591
Pays : Canada
Organisme : CIHR
ID : MOP#133598
Pays : Canada

Informations de copyright

© 2021 The Authors. Physiological Reports published by Wiley Periodicals LLC on behalf of The Physiological Society and the American Physiological Society.

Références

N Engl J Med. 2016 Dec;375(22):2144-2153
pubmed: 27959767
Arterioscler Thromb Vasc Biol. 2004 Aug;24(8):1454-9
pubmed: 15178557
JAMA. 2015 Mar 10;313(10):1016-7
pubmed: 25756436
Genes Dev. 2008 Nov 1;22(21):2941-52
pubmed: 18981473
Lancet. 2010 Feb 27;375(9716):735-42
pubmed: 20167359
Arterioscler Thromb Vasc Biol. 2012 Nov;32(11):2785-93
pubmed: 22995522
J Lipid Res. 2013 May;54(5):1466-76
pubmed: 23417739
J Lipid Res. 2018 Jul;59(7):1084-1093
pubmed: 29627764
Can J Cardiol. 1999 Apr;15(4):409-18
pubmed: 10322250
J Physiol. 2013 Dec 1;591(23):5823-31
pubmed: 24127618
Immunol Cell Biol. 2014 Apr;92(4):304-13
pubmed: 24518981
J Nutr. 2019 Jan 1;149(1):57-67
pubmed: 30535058
Lancet Diabetes Endocrinol. 2017 Dec;5(12):941-950
pubmed: 28927706
J Lipid Res. 2016 Jun;57(6):1074-85
pubmed: 27040450
Diabetes Care. 2010 Sep;33(9):2098-103
pubmed: 20805282
JAMA. 2016 Oct 4;316(13):1383-1391
pubmed: 27701660
Biochem Biophys Res Commun. 2008 Jun 13;370(4):634-40
pubmed: 18406350
J Lipid Res. 2004 Apr;45(4):657-66
pubmed: 14703506
Obes Facts. 2008;1(4):184-9
pubmed: 20054179
Nat Immunol. 2011 May;12(5):408-15
pubmed: 21478880
Diabetes Care. 2013 Aug;36(8):2239-46
pubmed: 23514733
Lancet. 2015 Jan 24;385(9965):351-61
pubmed: 25262344
Am J Clin Nutr. 2018 Jul 1;108(1):62-76
pubmed: 29917037
J Biomed Res. 2020 Mar 12;34(4):251-259
pubmed: 32701068
J Clin Lipidol. 2017 Jan - Feb;11(1):34-45.e2
pubmed: 28391908
Nat Med. 2011 Feb;17(2):179-88
pubmed: 21217695
Nutr Diabetes. 2015 Sep 28;5:e180
pubmed: 26417659
Diabetes. 2010 Jan;59(1):105-9
pubmed: 19846802
J Lipid Res. 1998 Apr;39(4):777-88
pubmed: 9555943
Lancet Diabetes Endocrinol. 2019 Aug;7(8):618-628
pubmed: 31272931
Diabetes Care. 2012 Aug;35(8):1654-62
pubmed: 22699287
N Engl J Med. 2007 Apr 12;356(15):1517-26
pubmed: 17429083
Sci Rep. 2017 Jun 6;7(1):2861
pubmed: 28588189
Lancet Diabetes Endocrinol. 2018 Jan;6(1):11
pubmed: 29273162
J Biol Chem. 2001 May 25;276(21):18464-71
pubmed: 11279134
Nat Rev Immunol. 2019 Aug;19(8):477-489
pubmed: 31036962
Endocrinology. 2011 Oct;152(10):3769-78
pubmed: 21862623
Lancet. 2012 Aug 11;380(9841):565-71
pubmed: 22883507
Cell Metab. 2010 Dec 1;12(6):593-605
pubmed: 21109192
Nat Immunol. 2013 Aug;14(8):812-20
pubmed: 23812099
Diabetes Care. 2014 Aug;37(8):2225-32
pubmed: 24969582
J Clin Lipidol. 2015 Sep-Oct;9(5):664-75
pubmed: 26350813
Arterioscler Thromb Vasc Biol. 2015 Dec;35(12):2517-25
pubmed: 26494228
Obesity (Silver Spring). 2020 Dec;28(12):2357-2367
pubmed: 33043593
Diabetes. 2017 Apr;66(4):815-822
pubmed: 28052966
Trends Pharmacol Sci. 2015 Oct;36(10):688-704
pubmed: 26435213
Lancet Diabetes Endocrinol. 2017 Feb;5(2):97-105
pubmed: 27908689
Public Health Nutr. 2007 Oct;10(10A):1132-7
pubmed: 17903321

Auteurs

Yannick Cyr (Y)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Valérie Lamantia (V)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Simon Bissonnette (S)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Melanie Burnette (M)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Aurèle Besse-Patin (A)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Annie Demers (A)

Institut de cardiologie de Montréal (ICM), Montréal, QC, Canada.

Martin Wabitsch (M)

Department of Pediatrics and Adolescent Medicine, Ulm University Hospital, Ulm, Germany.

Michel Chrétien (M)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Ottawa Health Research Institute (OHRI), Ottawa, ON, Canada.

Gaétan Mayer (G)

Department of Pediatrics and Adolescent Medicine, Ulm University Hospital, Ulm, Germany.
Faculty of Pharmacy, Université de Montréal, Montréal, QC, Canada.

Jennifer L Estall (JL)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Maya Saleh (M)

Department of Medicine, McGill University, Montréal, QC, Canada.
Department of Life Sciences and Health, The University of Bordeaux, Bordeaux, France.

May Faraj (M)

Institut de recherches cliniques de Montréal (IRCM), Montréal, QC, Canada.
Faculty of Medicine, Université de Montréal, Montréal, QC, Canada.
Montreal Diabetes Research Center (MDRC), Montréal, QC, Canada.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH