Cited by 331Inflammasome and immune disordersAtherosclerosis and Cardiovascular DiseasesCholesterol and Lipid Metabolism

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Cholesterol Efflux Pathways Suppress Inflammasome Activation, NETosis, and Atherogenesis

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Westerterp, Marit, Fotakis, Panagiotis, Ouimet, Mireille, Bochem, Andrea E., Zhang, Hanrui, Molusky, Matthew M., Wang, Wei, Abramowicz, Sandra, la Bastide-van Gemert, Sacha, Wang, Nan, Welch, Carrie L., Reilly, Muredach P., Stroes, Erik S., Moore, Kathryn J., Tall, Alan R.·2018·Circulation

DOI 10.1161/circulationaha.117.032636PMC PMC6160368

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Abstract

Background: The CANTOS trial (Canakinumab Antiinflammatory Thrombosis Outcome Study) showed that antagonism of interleukin (IL)–1β reduces coronary heart disease in patients with a previous myocardial infarction and evidence of systemic inflammation, indicating that pathways required for IL-1β secretion increase cardiovascular risk. IL-1β and IL-18 are produced via the NLRP3 inflammasome in myeloid cells in response to cholesterol accumulation, but mechanisms linking NLRP3 inflammasome activation to atherogenesis are unclear. The cholesterol transporters ATP binding cassette A1 and G1 (ABCA1/G1) mediate cholesterol efflux to high-density lipoprotein, and Abca1/g1 deficiency in myeloid cells leads to cholesterol accumulation. Methods: To interrogate mechanisms connecting inflammasome activation with atherogenesis, we used mice with myeloid Abca1/g1 deficiency and concomitant deficiency of the inflammasome components Nlrp3 or Caspase-1/11 . Bone marrow from these mice was transplanted into Ldlr −/− recipients, which were fed a Western-type diet. Results: Myeloid Abca1/g1 deficiency increased plasma IL-18 levels in Ldlr −/− mice and induced IL-1β and IL-18 secretion in splenocytes, which was reversed by Nlrp3 or Caspase-1/11 deficiency, indicating activation of the NLRP3 inflammasome. Nlrp3 or Caspase-1/11 deficiency decreased atherosclerotic lesion size in myeloid Abca1/g1 -deficient Ldlr −/− mice. Myeloid Abca1/g1 deficiency enhanced caspase-1 cleavage not only in splenic monocytes and macrophages, but also in neutrophils, and dramatically enhanced neutrophil accumulation and neutrophil extracellular trap formation in atherosclerotic plaques, with reversal by Nlrp3 or Caspase-1/11 deficiency, suggesting that inflammasome activation promotes neutrophil recruitment and neutrophil extracellular trap formation in atherosclerotic plaques. These effects appeared to be indirectly mediated by systemic inflammation leading to activation and accumulation of neutrophils in plaques. Myeloid Abca1/g1 deficiency also activated the noncanonical inflammasome, causing increased susceptibility to lipopolysaccharide-induced mortality. Patients with Tangier disease, who carry loss-of-function mutations in ABCA1 and have increased myeloid cholesterol content, showed a marked increase in plasma IL-1β and IL-18 levels. Conclusions: Cholesterol accumulation in myeloid cells activates the NLRP3 inflammasome, which enhances neutrophil accumulation and neutrophil extracellular trap formation in atherosclerotic plaques. Patients with Tangier disease, who have increased myeloid cholesterol content, showed markers of inflammasome activation, suggesting human relevance.

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Authors: Westerterp, M., Fotakis, P., Ouimet, M., Bochem, A. E., Zhang, H., Molusky, M. M., Wang, W., Abramowicz, S., la Bastide-van Gemert, S., Wang, N., Welch, C. L., Reilly, M. P., Stroes, E. S., Moore, K. J., & Tall, A. R.
Affiliations: Division of Molecular Medicine (M.W., P.F., A.E.B., M.M.M., W.W., S.A., N.W., C.L.W., A.R.T.)
University of Ottawa (CA)
Amsterdam UMC Location University of Amsterdam (NL)
Columbia University Irving Medical Center (US)
Department of Epidemiology (S.l.B-v.G.), University of Groningen, University Medical Center Groningen, The Netherlands
NYU Langone Health (US)
Corresponding author: Westerterp, Marit
Fotakis, Panagiotis
ORCID: Westerterp, Marit
Fotakis, Panagiotis
Ouimet, Mireille
Zhang, Hanrui
Molusky, Matthew M.
Wang, Wei
Wang, Nan
Welch, Carrie L.
Reilly, Muredach P.
Stroes, Erik S.
Moore, Kathryn J.
Tall, Alan R.
Venue: Circulation
Publisher: Ovid Technologies (Wolters Kluwer Health)
Published: 2018-08-28
Volume: 138
Issue: 9
Pages: 898-912
ISSN: 0009-7322 (ISSN-L)
1524-4539
DOI: 10.1161/circulationaha.117.032636
PMC: PMC6160368
OpenAlex: W2795137969
Cited by: 331
References: 49
Citations by year: 2026: 37 · 2025: 40 · 2024: 41 · 2023: 47 · 2022: 45 · 2021: 45 · 2020: 36 · 2019: 28 · 2018: 11
FWCI: 10.67
Type: journal article
Language: en
Open access: bronze
doi.org
Locations: Circulation (publishedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, other-oa)
PubMed (publishedVersion)
Pure Amsterdam UMC (publishedVersion, other-oa)
Europe PMC (PubMed Central) (acceptedVersion)
PubMed Central (acceptedVersion)
Data Archiving and Networked Services (DANS) (submittedVersion)
University of Groningen research database (University of Groningen / Centre for Information Technology) (submittedVersion, other-oa)
Funders: University of Ottawa
York University
Rijksuniversiteit Groningen
Universiteit van Amsterdam
Universitair Medisch Centrum Groningen
National Institutes of Health
National Heart, Lung, and Blood Institute (K24HL107643, R01HL113147, R01HL117334, R35HL135799, K99HL130574, R01HL107653, T32HL007343)
National Center for Research Resources (S10RR027050)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Inflammasome and immune disorders
Life Sciences › Immunology and Microbiology › Immunology › Atherosclerosis and Cardiovascular Diseases
Life Sciences › Biochemistry, Genetics and Molecular Biology › Biochemistry › Cholesterol and Lipid Metabolism
Keywords: cholesterol efflux, ABCA1, ABCG1, NLRP3 inflammasome, caspase-1, caspase-11, IL-1β, IL-18, NETosis, atherogenesis, myeloid cells, non-canonical inflammasome, Tangier disease
MeSH terms: ATP Binding Cassette Transporter, Subfamily G, Member 1, NLR Family, Pyrin Domain-Containing 3 Protein, Animals, Cholesterol, Disease Models, Animal, Humans, Inflammation, Receptors, LDL, Spleen, Tangier Disease, Case-Control Studies, Cytokines, Mice, Knockout, Caspases, Caspase 1, Myeloid Cells, Atherosclerosis, Caspases, Initiator, Plaque, Atherosclerotic, Inflammasomes, ATP Binding Cassette Transporter 1, Extracellular Traps

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Cholesterol Efflux Pathways Suppress Inflammasome Activation, NETosis, and Atherogenesis

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