The atherogenic role of immune cells in familial hypercholesterolemia.
atherosclerosis
familial hypercholesterolemia
inflammation
lipid metabolism
oxidized-LDL
Journal
IUBMB life
ISSN: 1521-6551
Titre abrégé: IUBMB Life
Pays: England
ID NLM: 100888706
Informations de publication
Date de publication:
04 2020
04 2020
Historique:
received:
05
08
2019
accepted:
16
09
2019
pubmed:
22
10
2019
medline:
22
6
2021
entrez:
22
10
2019
Statut:
ppublish
Résumé
Familial hypercholesterolemia (FH) is an autosomal dominant disorder of lipoprotein metabolism that mainly occurs due to mutations in the low-density lipoprotein receptor gene and is characterized by increased levels of low-density lipoprotein cholesterol, leading to accelerated atherogenesis and premature coronary heart disease. Both innate and adaptive immune responses, which mainly include monocytes, macrophages, neutrophils, T lymphocytes, and B lymphocytes, have been shown to play a key role for the initiation and progression of atherogenesis in the general population. In FH patients, these immune cells have been suggested to play specific pro-atherosclerotic activities, from the initial leukocyte recruitment to plaque rupture. In fact, the accumulation of cholesterol crystals and oxLDL in the vessels in FH patients is particularly high, with consequent abnormal mobilization of immune cells and secretion of various pro-inflammatory and chemokines. In addition, cholesterol accumulation in immune cells is exaggerated with chronic exposure to relevant pro-atherosclerotic triggers. The topics considered in this review may provide a more specific focus on the immune system alterations in FH and open new insights toward immune cells as potential therapeutic targets in FH.
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
782-789Informations de copyright
© 2019 International Union of Biochemistry and Molecular Biology.
Références
Prajapati R, Agrawal V. Familial hypercholesterolemia supravalvular aortic stenosis and extensive atherosclerosis. Indian Heart J. 2018;70(4):575-577.
Couture P, Morissette J, Gaudet D, et al. Fine mapping of low-density lipoprotein receptor gene by genetic linkage on chromosome 19p13. 1-p13. 3 and study of the founder effect of four French Canadian low-density lipoprotein receptor gene mutations. Atherosclerosis. 1999;143(1):145-151.
Henderson R, O'Kane M, McGilligan V, Watterson S. The genetics and screening of familial hypercholesterolaemia. J Biomed Sci. 2016;23(1):39.
Miserez AR, Muller PY, Barella L, et al. Sterol-regulatory element-binding protein (SREBP)-2 contributes to polygenic hypercholesterolaemia. Atherosclerosis. 2002;164(1):15-26.
Fouchier SW, Dallinga-Thie GM, Meijers JC, et al. Mutations in STAP1 are associated with autosomal dominant hypercholesterolemia. Circ Res. 2014;115(6):552-555.
Hajighasemi S, Mahdavi Gorabi A, Bianconi V, et al. A review of gene- and cell-based therapies for familial hypercholesterolemia. Pharmacol Res. 2019;143:119-132.
Berberich AJ, Hegele RA. The complex molecular genetics of familial hypercholesterolaemia. Nat Rev Cardiol. 2019;16(1):9-20.
Nordestgaard BG, Chapman MJ, Humphries SE, et al. Familial hypercholesterolaemia is underdiagnosed and undertreated in the general population: Guidance for clinicians to prevent coronary heart disease: Consensus statement of the European atherosclerosis society. Eur Heart J. 2013;34(45):3478-3490.
Reiner Ž. Management of patients with familial hypercholesterolaemia. Nat Rev Cardiol. 2015;12(10):565.
Kolansky DM, Cuchel M, Clark BJ, et al. Longitudinal evaluation and assessment of cardiovascular disease in patients with homozygous familial hypercholesterolemia. Am J Cardiol. 2008;102(11):1438-1443.
Wang HY, Quan C, Hu C, et al. A lipidomics study reveals hepatic lipid signatures associating with deficiency of the LDL receptor in a rat model. Biology open. 2016;5(7):979-986.
Migliara G, Baccolini V, Rosso A, et al. Familial hypercholesterolemia: A systematic review of guidelines on genetic testing and patient management. Front Public Health. 2017;5:252.
Hopkins PN, Toth PP, Ballantyne CM, Rader DJ. Familial hypercholesterolemias: Prevalence, genetics, diagnosis and screening recommendations from the National Lipid Association Expert Panel on familial hypercholesterolemia. J Clin Lipidol. 2011;5(3):S9-S17.
Hoseini Z, Sepahvand F, Rashidi B, Sahebkar A, Masoudifar A, Mirzaei H. NLRP3 inflammasome: Its regulation and involvement in atherosclerosis. J Cell Physiol. 2018;233(3):2116-2132.
Parsamanesh N, Moossavi M, Bahrami A, Fereidouni M, Barreto G, Sahebkar A. NLRP3 inflammasome as a treatment target in atherosclerosis: A focus on statin therapy. Int Immunopharmacol. 2019;73:146-155.
Abdolmaleki F, Gheibi Hayat SM, Bianconi V, Johnston TP, Sahebkar A. Atherosclerosis and immunity: A perspective. Trends Cardiovasc Med. 2019;29(6):363-371.
Ertunc ME, Hotamisligil GS. Lipid signaling and lipotoxicity in metaflammation: Indications for metabolic disease pathogenesis and treatment. J Lipid Res. 2016;57(12):2099-2114.
Seijkens T, Hoeksema MA, Beckers L, et al. Hypercholesterolemia-induced priming of hematopoietic stem and progenitor cells aggravates atherosclerosis. FASEB J. 2014;28(5):2202-2213.
Koltsova EK, Garcia Z, Chodaczek G, et al. Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis. J Clin Invest. 2012;122(9):3114-3126.
Malle E, Marsche G, Arnhold J, Davies MJ. Modification of low-density lipoprotein by myeloperoxidase-derived oxidants and reagent hypochlorous acid. Biochimica et Biophysica Acta (BBA)-molecular and cell biology of. Lipids. 2006;1761(4):392-415.
Ait-Oufella H, Salomon BL, Potteaux S. Robertson A-KL, Gourdy P, Zoll J, et al. natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006;12(2):178.
Butcher MJ, Gjurich BN, Phillips T, Galkina EV. The IL-17A/IL-17RA axis plays a proatherogenic role via the regulation of aortic myeloid cell recruitment. Circ Res. 2012;110(5):675-687.
Lacy M, Atzler D, Liu R, de Winther M, Weber C, Lutgens E. Interactions between dyslipidemia and the immune system and their relevance as putative therapeutic targets in atherosclerosis. Pharmacol Ther. 2019;193:50-62.
Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest. 2002;109(6):745-753.
Tsiantoulas D, Diehl C, Witztum J, Binder C. B cells and humoral immunity in atherosclerosis. Circ Res. 2014;114(11):1743-1756.
Hotamisligil GS. Foundations of immunometabolism and implications for metabolic health and disease. Immunity. 2017;47(3):406-420.
Berk BC, Weintraub WS, Alexander RW. Elevation of C-reactive protein in “active” coronary artery disease. Am J Cardiol. 1990;65(3):168-172.
van Wijk DF, Sjouke B, Figueroa A, et al. Nonpharmacological lipoprotein apheresis reduces arterial inflammation in familial hypercholesterolemia. J Am Coll Cardiol. 2014;64(14):1418-1426.
Jin C, Henao-Mejia J, Flavell RA. Innate immune receptors: Key regulators of metabolic disease progression. Cell Metab. 2013;17(6):873-882.
Greaves DR, Gordon S. The macrophage scavenger receptor at 30 years of age: Current knowledge and future challenges. J Lipid Res. 2009;50(Supplement):S282-S286.
Rothe G, Gabriel H, Kovacs E, et al. Peripheral blood mononuclear phagocyte subpopulations as cellular markers in hypercholesterolemia. Arterioscler Thromb Vasc Biol. 1996;16(12):1437-1447.
Soehnlein O, Swirski FK. Hypercholesterolemia links hematopoiesis with atherosclerosis. Trends in Endocrinology & Metabolism. 2013;24(3):129-136.
Shapiro H, Lutaty A, Ariel A. Macrophages, meta-inflammation, and immuno-metabolism. Scientific World Journal. 2011;11:2509-2529.
Gordon S, Taylor PR. Monocyte and macrophage heterogeneity. Nat Rev Immunol. 2005;5(12):953.
Fingerle G, Pforte A, Passlick B, Blumenstein M, Strobel M, Ziegler-Heitbrock H. The novel subset of CD14+/CD16+ blood monocytes is expanded in sepsis patients. Blood. 1993;82(10):3170-3176.
Merino A, Buendia P, Martin-Malo A, Aljama P, Ramirez R, Carracedo J. Senescent CD14+ CD16+ monocytes exhibit proinflammatory and proatherosclerotic activity. The Journal of Immunology. 2011;186(3):1809-1815.
Medzhitov R, Horng T. Transcriptional control of the inflammatory response. Nat Rev Immunol. 2009;9(10):692.
Libby P, Ridker PM, Hansson GK. Inflammation in atherosclerosis: From pathophysiology to practice. J Am Coll Cardiol. 2009;54(23):2129-2138.
Ross R. Atherosclerosis-An inflammatory disease. N Engl J Med. 1999;340(2):115-126.
Vallejo-Vaz AJ, Seshasai SRK, Cole D, et al. Familial hypercholesterolaemia: A global call to arms. Atherosclerosis. 2015;243(1):257-259.
Baardman J, Verberk SG, Prange KH, et al. A defective pentose phosphate pathway reduces inflammatory macrophage responses during hypercholesterolemia. Cell reports. 2018;25(8):2044-2052.
Libby P. Inflammation in atherosclerosis. Nature. 2002;420(6917):868-874.
Artieda M, Cenarro A, Junquera C, et al. Tendon xanthomas in familial hypercholesterolemia are associated with a differential inflammatory response of macrophages to oxidized LDL. FEBS Lett. 2005;579(20):4503-4512.
Murr C, Widner B, Wirleitner B, Fuchs D. Neopterin as a marker for immune system activation. Curr Drug Metab. 2002;3(2):175-187.
Aljenedil S, Ruel I, Watters K, Genest J. Severe xanthomatosis in heterozygous familial hypercholesterolemia. J Clin Lipidol. 2018;12(4):872-877.
Charakida M, Tousoulis D, Skoumas I, et al. Inflammatory and thrombotic processes are associated with vascular dysfunction in children with familial hypercholesterolemia. Atherosclerosis. 2009;204(2):532-537.
Tall AR, Yvan-Charvet L. Cholesterol. inflammation and innate immunity Nature Reviews Immunology. 2015;15(2):104.
Stewart CR, Stuart LM, Wilkinson K, et al. CD36 ligands promote sterile inflammation through assembly of a toll-like receptor 4 and 6 heterodimer. Nat Immunol. 2010;11(2):155.
Yang C, McDonald JG, Patel A, et al. Sterol intermediates from cholesterol biosynthetic pathway as liver X receptor ligands. J Biol Chem. 2006;281(38):27816-27826.
Pagler TA, Wang M, Mondal M, et al. Deletion of ABCA1 and ABCG1 impairs macrophage migration because of increased Rac1 signaling. Circ Res. 2011;108(2):194-200.
Tontonoz P, Mangelsdorf DJ. Liver X receptor signaling pathways in cardiovascular disease. Mol Endocrinol. 2003;17(6):985-993.
Venkateswaran A, Laffitte BA, Joseph SB, et al. Control of cellular cholesterol efflux by the nuclear oxysterol receptor LXRα. Proc Natl Acad Sci. 2000;97(22):12097-12102.
Feingold KR, Grunfeld C. Introduction to lipids and lipoproteins. Endotext [Internet]: MDText.com, Inc. 2018.
Castrillo A, Joseph SB, Vaidya SA, et al. Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol Cell. 2003;12(4):805-816.
Li HB, Jin C, Chen Y, Flavell RA. Inflammasome activation and metabolic disease progression. Cytokine Growth Factor Rev. 2014;25(6):699-706.
Yvan-Charvet L, Wang N, Tall AR. Role of HDL, ABCA1, and ABCG1 transporters in cholesterol efflux and immune responses. Arterioscler Thromb Vasc Biol. 2010;30(2):139-143.
Witko-Sarsat V, Rieu P, Descamps-Latscha B, Lesavre P, Halbwachs-Mecarelli L. Neutrophils: Molecules. Func Pathophysiol Aspects Lab Investig. 2000;80(5):617.
Soehnlein O, Zernecke A, Eriksson EE, et al. Neutrophil secretion products pave the way for inflammatory monocytes. Blood. 2008;112(4):1461-1471.
Migeotte I, Communi D, Parmentier M. Formyl peptide receptors: A promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev. 2006;17(6):501-519.
Farah R, Shurtz-Swirski R, Dorlechter F. Primed polymorphonuclear leukocytes constitute a possible link between inflammation and oxidative stress in hyperlipidemic patients: Effect of statins. Minerva Cardioangiol. 2010;58(2):175-181.
Drechsler M, Megens RT, van Zandvoort M, Weber C, Soehnlein O. Hyperlipidemia-triggered neutrophilia promotes early atherosclerosis. Circulation. 2010;122(18):1837-1845.
Eash KJ, Greenbaum AM, Gopalan PK, Link DC. CXCR2 and CXCR4 antagonistically regulate neutrophil trafficking from murine bone marrow. J Clin Invest. 2010;120(7):2423-2431.
Jerke U, Rolle S, Purfürst B, Luft FC, Nauseef WM, Kettritz R. β2 integrin-mediated cell-cell contact transfers active myeloperoxidase from neutrophils to endothelial cells. J Biol Chem. 2013;288(18):12910-12919.
Gil-Pulido J, Zernecke A. Antigen-presenting dendritic cells in atherosclerosis. Eur J Pharmacol. 2017;816:25-31.
Haddad Y, Lahoute C, Clément M, et al. The dendritic cell receptor DNGR-1 promotes the development of atherosclerosis in mice. Circ Res. 2017;121(3):234-243.
Hansson GK, Jonasson L. The discovery of cellular immunity in the atherosclerotic plaque. Arterioscler Thromb Vasc Biol. 2009;29(11):1714-1717.
Moriya J. Critical roles of inflammation in atherosclerosis. J Cardiol. 2019;73(1):22-27.
Walch L, Massade L, Dufilho M, Brunet A, Rendu F. Pro-atherogenic effect of interleukin-4 in endothelial cells: Modulation of oxidative stress, nitric oxide and monocyte chemoattractant protein-1 expression. Atherosclerosis. 2006;187(2):285-291.
O'garra A, Vieira P. Regulatory T cells and mechanisms of immune system control. Nat Med. 2004;10(8):801.
Gu P, Gao JF, D'souza CA, Kowalczyk A, Chou K-Y, Zhang L. Trogocytosis of CD80 and CD86 by induced regulatory T cells. Cell Mol Immunol. 2012;9(2):136.
Maganto-García E, Tarrio ML, Grabie N. Bu D-x, Lichtman AH. Dynamic changes in regulatory T cells are linked to levels of diet-induced hypercholesterolemia. Circulation. 2011;124(2):185-195.
Harris DP, Haynes L, Sayles PC, et al. Reciprocal regulation of polarized cytokine production by effector B and T cells. Nat Immunol. 2000;1(6):475.
Galkina E, Ley K. Immune and inflammatory mechanisms of atherosclerosis. Annu Rev Immunol. 2009;27:165-197.
Oliveira H, Popi A, Bachi A, Nonogaki S, Lopes J, Mariano M. B-1 cells modulate the kinetics of wound-healing process in mice. Immunobiology. 2010;215(3):215-222.
LeBien TW. Tedder TF. B lymphocytes: How they develop and function. Blood. 2008;112(5):1570-1580.
Lichtman AH, Binder CJ, Tsimikas S, Witztum JL. Adaptive immunity in atherogenesis: New insights and therapeutic approaches. J Clin Invest. 2013;123(1):27-36.
Freigang S, Hörkkö S, Miller E, Witztum JL, Palinski W. Immunization of LDL receptor-deficient mice with homologous malondialdehyde-modified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes. Arterioscler Thromb Vasc Biol. 1998;18(12):1972-1982.
Ait-Oufella H, Herbin O, Bouaziz JD, et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med. 2010;207(8):1579-1587.
Kyaw T, Tay C, Hosseini H, et al. Depletion of B2 but not B1a B cells in BAFF receptor-deficient ApoE mice attenuates atherosclerosis by potently ameliorating arterial inflammation. PLoS One. 2012;7(1):e29371-e.