Serum amyloid A-containing HDL binds adipocyte-derived versican and macrophage-derived biglycan, reducing its antiinflammatory properties.
Adipocytes
/ immunology
Adult
Animals
Apolipoprotein A-I
/ genetics
Biglycan
/ antagonists & inhibitors
Diet, High-Fat
/ adverse effects
Female
Gene Expression Regulation
Humans
Insulin Resistance
/ immunology
Lipoproteins, HDL
/ genetics
Macrophages, Peritoneal
/ immunology
Male
Mice
Mice, Inbred C57BL
Mice, Knockout
Middle Aged
Obesity
/ etiology
Protein Binding
Protein Transport
RNA, Small Interfering
/ genetics
Reactive Oxygen Species
/ immunology
Serum Amyloid A Protein
/ genetics
Silver Nitrate
/ administration & dosage
Toll-Like Receptor 4
/ genetics
Versicans
/ antagonists & inhibitors
Adipose tissue
Cell Biology
Inflammation
Lipoproteins
Macrophages
Journal
JCI insight
ISSN: 2379-3708
Titre abrégé: JCI Insight
Pays: United States
ID NLM: 101676073
Informations de publication
Date de publication:
24 09 2020
24 09 2020
Historique:
received:
24
07
2020
accepted:
16
09
2020
pubmed:
25
9
2020
medline:
20
5
2021
entrez:
24
9
2020
Statut:
epublish
Résumé
The ability of HDL to inhibit inflammation in adipocytes and adipose tissue is reduced when HDL contains serum amyloid A (SAA) that is trapped by proteoglycans at the adipocyte surface. Because we recently found that the major extracellular matrix proteoglycan produced by hypertrophic adipocytes is versican, whereas activated adipose tissue macrophages produce mainly biglycan, we further investigated the role of proteoglycans in determining the antiinflammatory properties of HDL. The distributions of versican, biglycan, apolipoprotein A1 (the major apolipoprotein of HDL), and SAA were similar in adipose tissue from obese mice and obese human subjects. Colocalization of SAA-enriched HDL with versican and biglycan at the cell surface of adipocyte and peritoneal macrophages, respectively, was blocked by silencing these proteoglycans, which also restored the antiinflammatory property of SAA-enriched HDL despite the presence of SAA. Similar to adipocytes, normal HDL exerted its antiinflammatory function in macrophages by reducing lipid rafts, reactive oxygen species generation, and translocation of Toll-like receptor 4 and NADPH oxidase 2 into lipid rafts, effects that were not observed with SAA-enriched HDL. These findings imply that SAA present in HDL can be trapped by adipocyte-derived versican and macrophage-derived biglycan, thereby blunting HDL's antiinflammatory properties.
Identifiants
pubmed: 32970631
pii: 142635
doi: 10.1172/jci.insight.142635
pmc: PMC7605543
doi:
pii:
Substances chimiques
APOA1 protein, human
0
Apolipoprotein A-I
0
BGN protein, human
0
Biglycan
0
Lipoproteins, HDL
0
RNA, Small Interfering
0
Reactive Oxygen Species
0
Serum Amyloid A Protein
0
TLR4 protein, human
0
Toll-Like Receptor 4
0
VCAN protein, human
0
Versicans
126968-45-4
Silver Nitrate
95IT3W8JZE
Types de publication
Journal Article
Research Support, N.I.H., Extramural
Langues
eng
Sous-ensembles de citation
IM
Subventions
Organisme : NIAID NIH HHS
ID : R01 AI130280
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK035816
Pays : United States
Organisme : NIAID NIH HHS
ID : U19 AI125378
Pays : United States
Organisme : NHLBI NIH HHS
ID : P01 HL092969
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK017047
Pays : United States
Références
BJOG. 2006 Oct;113(10):1141-7
pubmed: 16903845
Eur J Immunol. 2015 Jan;45(1):101-12
pubmed: 25345597
Arterioscler Thromb Vasc Biol. 2010 Feb;30(2):139-43
pubmed: 19797709
Cell Metab. 2017 Jan 10;25(1):197-207
pubmed: 27866837
J Lipid Res. 2009 Jul;50(7):1353-62
pubmed: 19286646
Arterioscler Thromb Vasc Biol. 2015 May;35(5):1156-65
pubmed: 25745063
J Clin Invest. 2003 Dec;112(12):1821-30
pubmed: 14679177
Arterioscler Thromb Vasc Biol. 2014 Feb;34(2):255-61
pubmed: 24265416
J Lipid Res. 2010 Nov;51(11):3117-25
pubmed: 20667817
J Exp Med. 1994 Jul 1;180(1):203-9
pubmed: 7516407
Obesity (Silver Spring). 2013 May;21(5):993-6
pubmed: 23784902
J Lipid Res. 2012 Jul;53(7):1254-67
pubmed: 22504909
Am Heart J. 2005 Nov;150(5):900-6
pubmed: 16290958
Circulation. 2004 Feb 17;109(6):726-32
pubmed: 14970107
Diabetes. 2010 Feb;59(2):386-96
pubmed: 19934003
Int J Obes Relat Metab Disord. 2004 Aug;28(8):993-7
pubmed: 15211360
Arterioscler Thromb Vasc Biol. 2010 Feb;30(2):156-63
pubmed: 19778948
Amyloid. 2002 Dec;9(4):237-41
pubmed: 12557751
Cell Rep. 2020 Jun 30;31(13):107818
pubmed: 32610121
J Clin Invest. 2003 Dec;112(12):1785-8
pubmed: 14679172
J Biol Chem. 2005 Feb 11;280(6):4617-26
pubmed: 15536073
J Lipid Res. 1997 Aug;38(8):1583-90
pubmed: 9300780
J Lipid Res. 2018 Feb;59(2):339-347
pubmed: 29247043
Cell Metab. 2006 Jul;4(1):13-24
pubmed: 16814729
Sci Rep. 2020 Jun 25;10(1):10397
pubmed: 32587356
Eur J Biochem. 1999 Oct;265(2):501-23
pubmed: 10504381
Arterioscler Thromb Vasc Biol. 2019 Dec;39(12):e253-e272
pubmed: 31578081
Arterioscler Thromb Vasc Biol. 2017 Mar;37(3):466-475
pubmed: 28062496
Arterioscler Thromb Vasc Biol. 2011 Jun;31(6):1326-32
pubmed: 21474830
Atherosclerosis. 2004 Jun;174(2):349-56
pubmed: 15136066
Circulation. 2018 Aug 28;138(9):898-912
pubmed: 29588315
Arterioscler Thromb Vasc Biol. 2006 Aug;26(8):1806-13
pubmed: 16709944
Obesity (Silver Spring). 2006 Feb;14(2):309-18
pubmed: 16571858
Arterioscler Thromb Vasc Biol. 2008 Apr;28(4):685-91
pubmed: 18239153
Arterioscler Thromb Vasc Biol. 2005 Apr;25(4):785-90
pubmed: 15692094
J Clin Invest. 2016 Feb;126(2):796
pubmed: 26829628
Arterioscler Thromb Vasc Biol. 2010 Jul;30(7):1430-8
pubmed: 20448206
Circ Res. 2013 May 10;112(10):1345-54
pubmed: 23501697
Circulation. 2004 Aug 3;110(5):540-5
pubmed: 15277327
N Engl J Med. 2000 Mar 23;342(12):836-43
pubmed: 10733371
Scand J Immunol. 1987 Apr;25(4):375-81
pubmed: 3107118
PLoS Med. 2006 Jun;3(6):e287
pubmed: 16737350
J Clin Invest. 2003 Dec;112(12):1796-808
pubmed: 14679176
Cell. 2009 Oct 30;139(3):485-98
pubmed: 19836068
Obes Res. 2003 Apr;11(4):525-31
pubmed: 12690081
J Biol Chem. 2012 Mar 23;287(13):10379-93
pubmed: 22287546