Human epicardial fat has a beige profile and contains higher type 2 innate lymphoid cells than subcutaneous fat.


Journal

Obesity (Silver Spring, Md.)
ISSN: 1930-739X
Titre abrégé: Obesity (Silver Spring)
Pays: United States
ID NLM: 101264860

Informations de publication

Date de publication:
15 May 2024
Historique:
revised: 12 02 2024
received: 19 10 2023
accepted: 20 02 2024
medline: 15 5 2024
pubmed: 15 5 2024
entrez: 15 5 2024
Statut: aheadofprint

Résumé

Epicardial adipose tissue (EAT) is a visceral fat that has been associated with coronary artery disease and atrial fibrillation. Previous work has revealed that EAT exhibits beige features. First, a new pan-genomic microarray analysis was performed on previously collected paired human EAT and thoracic subcutaneous AT (thSAT) from the EPICAR study (n = 31) to decipher a specific immune signature and its link with browning genes. Then, adaptive (T and B cells) and innate lymphoid cell (ILC1, ILC2, and ILC3) immunophenotyping assay panels, including CD127, CD117, and prostaglandin D2 receptor 2, were performed on prospectively collected paired human multiorgan donors (n = 18; INTERFACE study). In the EPICAR study, a positive correlation between the T helper cell subtype Th2 immune pathway and browning genes was found in EAT versus thSAT (r = 0.82; p < 0.0001). In the INTERFACE study, this correlation was also observed (r = 0.31; p = 0.017), and a preponderance of CD4 This is the first study, to our knowledge, to provide a comparison between innate and adaptive lymphoid cells in human EAT. Further studies are ongoing to decipher whether these cells could be involved in EAT beiging.

Identifiants

pubmed: 38747118
doi: 10.1002/oby.24023
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Aix-Marseille University Excellence Initiative-A*MIDEX
ID : AMX-21-PEP-026
Organisme : Fondation de l'Avenir
ID : AP-RM-22-017

Informations de copyright

© 2024 The Authors. Obesity published by Wiley Periodicals LLC on behalf of The Obesity Society.

Références

Baker AR, da Silva NF, Quinn DW, et al. Human epicardial adipose tissue expresses a pathogenic profile of adipocytokines in patients with cardiovascular disease. Cardiovasc Diabetol. 2006;5:1.
Gruzdeva O, Uchasova E, Dyleva Y, et al. Adipocytes directly affect coronary artery disease pathogenesis via induction of adipokine and cytokine imbalances. Front Immunol. 2019;10:2163.
Gaborit B, Sengenes C, Ancel P, Jacquier A, Dutour A. Role of epicardial adipose tissue in health and disease: a matter of fat? Compr Physiol. 2017;7:1051‐1082.
Gaborit B, Abdesselam I, Dutour A. Epicardial fat: more than just an “epi” phenomenon? Horm Metab Res. 2013;45:991‐1001.
Iacobellis G. Epicardial adipose tissue in contemporary cardiology. Nat Rev Cardiol. 2022;19:593‐606.
Venteclef N, Guglielmi V, Balse E, et al. Human epicardial adipose tissue induces fibrosis of the atrial myocardium through the secretion of adipo‐fibrokines. Eur Heart J. 2015;36:795‐805a.
Camarena V, Sant D, Mohseni M, et al. Novel atherogenic pathways from the differential transcriptome analysis of diabetic epicardial adipose tissue. Nutr Metab Cardiovasc Dis. 2017;27:739‐750.
Sacks HS, Fain JN, Bahouth SW, et al. Adult epicardial fat exhibits beige features. J Clin Endocrinol Metab. 2013;98:E1448‐E1455.
Gaborit B, Venteclef N, Ancel P, et al. Human epicardial adipose tissue has a specific transcriptomic signature depending on its anatomical peri‐atrial, peri‐ventricular, or peri‐coronary location. Cardiovasc Res. 2015;108:62‐73.
Barchuk M, Dutour A, Ancel P, et al. Untargeted lipidomics reveals a specific enrichment in plasmalogens in epicardial adipose tissue and a specific signature in coronary artery disease. Arterioscler Thromb Vasc Biol. 2020;40:986‐1000.
Brestoff JR, Kim BS, Saenz SA, et al. Group 2 innate lymphoid cells promote beiging of white adipose tissue and limit obesity. Nature. 2015;519:242‐246.
Doukbi E, Soghomonian A, Sengenès C, et al. Browning epicardial adipose tissue: friend or foe? Cells. 2022;11:991.
Lee M‐W, Odegaard JI, Mukundan L, et al. Activated type 2 innate lymphoid cells regulate beige fat biogenesis. Cell. 2015;160:74‐87.
O'Sullivan TE, Rapp M, Fan X, et al. Adipose‐resident group 1 innate lymphoid cells promote obesity‐associated insulin resistance. Immunity. 2016;45:428‐441.
Carpentier AC, Blondin DP, Haman F, Richard D. Brown adipose tissue—a translational perspective. Endocr Rev. 2023;44:143‐192.
Deslex S, Negrel R, Vannier C, Etienne J, Ailhaud G. Differentiation of human adipocyte precursors in a chemically defined serum‐free medium. Int J Obes (Lond). 1987;11:19‐27.
Hauner H, Entenmann G, Wabitsch M, et al. Promoting effect of glucocorticoids on the differentiation of human adipocyte precursor cells cultured in a chemically defined medium. J Clin Invest. 1989;84:1663‐1670.
Carvelli J, Piperoglou C, Bourenne J, et al. Imbalance of circulating innate lymphoid cell subpopulations in patients with septic shock. Front Immunol. 2019;10:2179.
Vély F, Barlogis V, Vallentin B, et al. Evidence of innate lymphoid cell redundancy in humans. Nat Immunol. 2016;17:1291‐1299.
Chechi K, Gelinas Y, Mathieu P, Deshaies Y, Richard D. Validation of reference genes for the relative quantification of gene expression in human epicardial adipose tissue. PloS One. 2012;7:e32265.
Mazurek T, Zhang L, Zalewski A, et al. Human epicardial adipose tissue is a source of inflammatory mediators. Circulation. 2003;108:2460‐2466.
Hirata Y, Tabata M, Kurobe H, et al. Coronary atherosclerosis is associated with macrophage polarization in epicardial adipose tissue. J Am Coll Cardiol. 2011;58:248‐255.
Klein M, Varga I. Microenvironment of immune cells within the visceral adipose tissue sensu lato vs. epicardial adipose tissue: what do we know? Inflammation. 2018;41:1142‐1156.
Beiroa D, Imbernon M, Gallego R, et al. GLP‐1 agonism stimulates brown adipose tissue thermogenesis and browning through hypothalamic AMPK. Diabetes. 2014;63:3346‐3358.
Malavazos AE, Iacobellis G, Dozio E, et al. Human epicardial adipose tissue expresses glucose‐dependent insulinotropic polypeptide, glucagon, and glucagon‐like peptide‐1 receptors as potential targets of pleiotropic therapies. Eur J Prev Cardiol. 2023;30:680‐693.
Chechi K, Vijay J, Voisine P, et al. UCP1 expression–associated gene signatures of human epicardial adipose tissue. JCI Insight. 2019;4:e123618.
Nakajima T, Yokota T, Shingu Y, et al. Impaired mitochondrial oxidative phosphorylation capacity in epicardial adipose tissue is associated with decreased concentration of adiponectin and severity of coronary atherosclerosis. Sci Rep. 2019;9:3535.
Wang H, Shen L, Sun X, et al. Adipose group 1 innate lymphoid cells promote adipose tissue fibrosis and diabetes in obesity. Nat Commun. 2019;10:3254.
Horckmans M, Bianchini M, Santovito D, et al. Pericardial adipose tissue regulates granulopoiesis, fibrosis, and cardiac function after myocardial infarction. Circulation. 2018;137:948‐960.
Li J, Wu J, Zhang M, Zheng Y. Dynamic changes of innate lymphoid cells in acute ST‐segment elevation myocardial infarction and its association with clinical outcomes. Sci Rep. 2020;10:5099.
Li Q, Liu M, Fu R, et al. Alteration of circulating innate lymphoid cells in patients with atherosclerotic cerebral infarction. Am J Transl Res. 2018;10:4322‐4330.
Newland SA, Mohanta S, Clément M, et al. Type‐2 innate lymphoid cells control the development of atherosclerosis in mice. Nat Commun. 2017;8:15781.
Engelbertsen D, Foks AC, Alberts‐Grill N, et al. Expansion of CD25+ innate lymphoid cells reduces atherosclerosis. Arterioscler Thromb Vasc Biol. 2015;35:2526‐2535.
Mantani PT, Dunér P, Bengtsson E, et al. IL‐25 inhibits atherosclerosis development in apolipoprotein E deficient mice. PloS One. 2015;10:e0117255.
Molofsky AB, Nussbaum JC, Liang H‐E, et al. Innate lymphoid type 2 cells sustain visceral adipose tissue eosinophils and alternatively activated macrophages. J Exp Med. 2013;210:535‐549.
Yang H, Youm Y‐H, Vandanmagsar B, et al. Obesity increases the production of proinflammatory mediators from adipose tissue T cells and compromises TCR repertoire diversity: implications for systemic inflammation and insulin resistance. J Immunol. 2010;185:1836‐1845.
Schwartz C, Schmidt V, Deinzer A, et al. Innate PD‐L1 limits T cell–mediated adipose tissue inflammation and ameliorates diet‐induced obesity. Sci Transl Med. 2022;14:eabj6879.
Sonnenberg GF, Artis D. Innate lymphoid cells in the initiation, regulation and resolution of inflammation. Nat Med. 2015;21:698‐708.
Eken A, Yetkin MF, Vural A, et al. Fingolimod alters tissue distribution and cytokine production of human and murine innate lymphoid cells. Front Immunol. 2019;10:217.
Filgotinib in the Induction and Maintenance of Remission in Subjects With Moderately to Severely Active Crohn's Disease (DIVERSITY1). ClinicalTrials.gov identifier NCT02914561. Published December 18, 2023. https://classic.clinicaltrials.gov/ct2/show/NCT02914561
Enterome. https://www.enterome.com/
Walford HH, Lund SJ, Baum RE, et al. Increased ILC2s in the eosinophilic nasal polyp endotype are associated with corticosteroid responsiveness. Clin Immunol. 2014;155:126‐135.
Moriyama S, Brestoff JR, Flamar A‐L, et al. β2‐adrenergic receptor‐mediated negative regulation of group 2 innate lymphoid cell responses. Science. 2018;359:1056‐1061.
Galle‐Treger L, Sankaranarayanan I, Hurrell BP, et al. Costimulation of type‐2 innate lymphoid cells by GITR promotes effector function and ameliorates type 2 diabetes. Nat Commun. 2019;10:713.
Vyas V, Blythe H, Wood EG, et al. Obesity and diabetes are major risk factors for epicardial adipose tissue inflammation. JCI Insight. 2021;6:e145495.

Auteurs

Elisa Doukbi (E)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.

Patricia Ancel (P)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.

Anne Dutour (A)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.
Department of Endocrinology, Metabolic Diseases and Nutrition, Pole Endocrinology-Nutrition-Diabetes-Obesity, Public Assistance Marseille Hospitals, Marseille, France.

Astrid Soghomonian (A)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.
Department of Endocrinology, Metabolic Diseases and Nutrition, Pole Endocrinology-Nutrition-Diabetes-Obesity, Public Assistance Marseille Hospitals, Marseille, France.

Shaista Ahmed (S)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.
Heart Repair and Regeneration Laboratory, Department of Endocrinology, Metabolism, and Cardiovascular System, Faculty of Sciences and Medicine, University of Fribourg, Fribourg, Switzerland.

Victoria Castejon (V)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.

Christelle Piperoglou (C)

Aix-Marseille University, CNRS, National Institute for Health and Medical Research (INSERM), Marseille-Luminy Immunology Center (CIML), Marseille University Hospital Timone, Public Assistance Marseille Hospitals, Marseille Immunopole, Marseille, France.

Vlad Gariboldi (V)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.
Department of Cardiac Surgery, Marseille University Hospital Timone, Public Assistance Marseille Hospitals, Marseille, France.

Marien Lenoir (M)

Division of Paediatric Cardiac Surgery, Marseille University Hospital Timone, Public Assistance Marseille Hospitals, Marseille, France.

Eric Lechevallier (E)

Department of Urology Surgery, Conception Hospital, Public Assistance Marseille Hospitals, Marseille, France.

Bastien Gondran-Tellier (B)

Department of Urology Surgery, Conception Hospital, Public Assistance Marseille Hospitals, Marseille, France.

Romain Boissier (R)

Department of Urology Surgery, Conception Hospital, Public Assistance Marseille Hospitals, Marseille, France.

Mikael Ebbo (M)

Aix-Marseille University, CNRS, National Institute for Health and Medical Research (INSERM), Marseille-Luminy Immunology Center (CIML), Marseille University Hospital Timone, Public Assistance Marseille Hospitals, Marseille Immunopole, Marseille, France.
Internal Medicine Department, Marseille University Hospital Timone, Public Assistance Marseille Hospitals, Marseille, France.

Frédéric Vély (F)

Aix-Marseille University, CNRS, National Institute for Health and Medical Research (INSERM), Marseille-Luminy Immunology Center (CIML), Marseille University Hospital Timone, Public Assistance Marseille Hospitals, Marseille Immunopole, Marseille, France.

Bénédicte Gaborit (B)

Aix-Marseille University, National Institute for Health and Medical Research (INSERM), National Research Institute for Agriculture, Food and the Environment (INRAE), Cardiovascular and Nutrition Research Center (C2VN), Marseille, France.
Department of Endocrinology, Metabolic Diseases and Nutrition, Pole Endocrinology-Nutrition-Diabetes-Obesity, Public Assistance Marseille Hospitals, Marseille, France.

Classifications MeSH