Atherosclerosis: The interplay between lipids and immune cells

Current Opinion in Lipidology

Volumn 27, Issue 3, 2016, Pages 209-215

  Schaftenaar, Frank ^a   Frodermann, Vanessa ^a   Kuiper, Johan ^a   Lutgens, Esther ^b,c  

^a LEIDEN UNIVERSITY   (Netherlands)

^b ACADEMIC MEDICAL CENTER   (Netherlands)

^c LUDWIG MAXIMILIANS UNIVERSITY   (Germany)

Author keywords

atherosclerosis; immune system; lipids

Indexed keywords

LIPID;

ADAPTIVE IMMUNITY; ATHEROSCLEROSIS; B LYMPHOCYTE; BONE MARROW; CELL FUNCTION; CELL MATURATION; DENDRITIC CELL; EPIGENETICS; HEMATOPOIETIC STEM CELL; HUMAN; HYPERLIPIDEMIA; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; INNATE IMMUNITY; LIPID METABOLISM; MACROPHAGE; MONOCYTE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; STEM CELL; T LYMPHOCYTE; TH1 CELL; TH2 CELL; ANIMAL; GENETIC EPIGENESIS; GENETICS; IMMUNOLOGY; METABOLISM;

ADAPTIVE IMMUNITY; ANIMALS; ATHEROSCLEROSIS; EPIGENESIS, GENETIC; HUMANS; IMMUNITY, INNATE; LIPID METABOLISM;

EID: 84962090706     PISSN: 09579672     EISSN: 14736535     Source Type: Journal    
DOI: 10.1097/MOL.0000000000000302     Document Type: Review

References (76)

1. Libby P, Lichtman AH, Hansson GK. Immune effector mechanisms implicated in atherosclerosis: from mice to humans. Immunity 2013; 38:1092-1104.
2. Hansson GK, Hermansson A. The immune system in atherosclerosis. Nat Immunol 2011; 12:204-212.
3. Legein B, Temmerman L, Biessen EAL, Lutgens E. Inflammation and immune systeminteractions in atherosclerosis. Cell Mol Life Sci 2013; 70:3847-3869.
4. Massberg S, Schaerli P, Knezevic-Maramica I, et al. Immunosurveillance by hematopoietic progenitor cells trafficking through blood, lymph, and peripheral tissues. Cell 2007; 131:994-1008.
5. Baldridge MT, King KY, Goodell MA. Inflammatory signals regulate hematopoietic stem cells. Trends Immunol 2011; 32:57-65.
6. Mendelson A, Frenette PS. Hematopoietic stem cell niche maintenance during homeostasis and regeneration. Nat Med 2014; 20:833-846.
7. Wang LD, Wagers AJ. Dynamic niches in the origination and differentiation of haematopoietic stem cells. Nat Rev Mol Cell Biol 2011; 12:643-655.
8. King KY, Goodell MA. Inflammatory modulation of HSCs: viewing the HSC as a foundation for the immune response. Nat Rev Immunol 2011; 11:685-692.
9. Wilson A, Laurenti E, Oser G, et al. Hematopoietic stem cells reversibly switch from dormancy to self-renewal during homeostasis and repair. Cell 2008; 135:1118-1129.
10. Seijkens T, Hoeksema MA, Beckers L, et al. Hypercholesterolemia-induced priming of hematopoietic stem and progenitor cells aggravates atherosclerosis. FASEB J 2014; 28:2202-2213.
11. Murphy AJ, Akhtari M, Tolani S, et al. ApoE regulates hematopoietic stem cell proliferation, monocytosis, and monocyte accumulation in atherosclerotic lesions in mice. J Clin Invest 2011; 121:4138-4149.
12. Feng Y, Schouteden S, Geenens R, et al. Hematopoietic stem/progenitor cell proliferation and differentiation is differentially regulated by high-density and low-density lipoproteins in mice. PLoS ONE 2012; 7:e47286.
13. Robbins CS, Chudnovskiy A, Rauch PJ, et al. Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation 2012; 125:364-374.
14. Yvan-Charvet L, Pagler T, Gautier EL, et al. ATP-binding cassette transporters and HDL suppress hematopoietic stem cell proliferation. Science 2010; 328:1689-1693.
15. Rogacev KS, Seiler S, Zawada AM, et al. CD14++CD16+ monocytes and cardiovascular outcome in patients with chronic kidney disease. Eur Heart J 2011; 32:84-92.
16. Berg KE, Ljungcrantz I, Andersson L, et al. Elevated CD14++CD16- monocytes predict cardiovascular events. Circ Cardiovasc Genet 2012; 5:122-131.
17. Tacke F, Alvarez D, Kaplan TJ, et al. Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 2007; 117:185-194.
18. Swirski FK, Libby P, Aikawa E, et al. Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 2007; 117:195-205.
19. Geissmann F, Jung S, Littman DR. Blood monocytes consist of two principal subsets with distinct migratory properties. Immunity 2003; 19:71-82.
20. Swirski FK, Nahrendorf M, Etzrodt M, et al. Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 2009; 325:612-616.
21. Westerterp M, Bochem AE, Yvan-Charvet L, et al. ATP-binding cassette transporters, atherosclerosis, and inflammation. CircRes 2014;114:157-170.
22. Tall AR, Yvan-Charvet L. Cholesterol, inflammation and innate immunity. Nat Rev Immunol 2015; 15:104-116.
23. Spann NJ, Garmire LX, McDonald JG, et al. Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 2012; 151:138-152.
24. Duewell P, Kono H, Rayner KJ, et al. NLRP3 inflammasomes are required for atherogenesis and activated by cholesterol crystals. Nature 2010; 464:1357-1361.
25. Moore KJ, Tabas I. Macrophages in the pathogenesis of atherosclerosis. Cell 2011; 145:341-355.
26. Subramanian M, Tabas I. Dendritic cells in atherosclerosis. Semin Immunopathol 2014; 36:93-102.
27. Paulson KE, Zhu S-N, Chen M, et al. Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Circ Res 2010; 106:383-390.
28. Bobryshev YV, Watanabe T. Subset of vascular dendritic cells transforming into foam cells in humanatherosclerotic lesions. Cardiovasc Pathol1997; 6:321-331.
29. Cho HJ, Shashkin P, Gleissner CA, et al. Induction of dendritic cell-like phenotype in macrophages during foam cell formation. Physiol Genomics 2007; 29:149-160.
30. Perrin-Cocon L, Coutant F, Agaugué S, et al. Oxidized low-density lipoprotein promotes mature dendritic cell transition from differentiating monocyte. J Immunol 2001; 167:3785-3791.
31. Alderman CJJ, Bunyard PR, Chain BM, et al. Effects of oxidised low density lipoprotein on dendritic cells: a possible immunoregulatory component of the atherogenic micro-environment? Cardiovasc Res 2002; 55:806-819.
32. Blüml S, Kirchberger S, Bochkov VN, et al. Oxidized phospholipids negatively regulate dendritic cell maturation induced by TLRs and CD40. J Immunol 2005; 175:501-508.
33. Geyeregger R, Zeyda M, Bauer W, et al. Liver X receptors regulate dendritic cell phenotype and function through blocked induction of the actin-bundling protein fascin. Blood 2007; 109:4288-4295.
34. Gautier EL, Huby T, Saint-Charles F, et al. Conventional dendritic cells at the crossroads between immunity and cholesterol homeostasis in atherosclerosis. Circulation 2009; 119:2367-2375.
35. Hjerpe C, Johansson D, Hermansson A, et al. Dendritic cells pulsed with malondialdehyde modified low density lipoprotein aggravate atherosclerosis in Apoe(-/-) mice. Atherosclerosis 2010; 209:436-441.
36. Hermansson A, Johansson DK, Ketelhuth DFJ, et al. Immunotherapy with tolerogenic apolipoprotein B-100-loaded dendritic cells attenuates atherosclerosis in hypercholesterolemic mice. Circulation 2011; 123:1083-1091.
37. Hansson GK, Holm J, Jonasson L. Detection of activated T lymphocytes in the human atherosclerotic plaque. Am J Pathol 1989; 135:169-175.
38. Frostegård J, Ulfgren AK, Nyberg P, et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 1999; 145:33-43.
39. Zhou X, Paulsson G, Stemme S, Hansson GK. Hypercholesterolemia is associated with a T helper (Th) 1/Th2 switch of the autoimmune response in atherosclerotic apo E-knockout mice. J Clin Invest 1998; 101:1717-1725.
40. Laurat E, Poirier B, Tupin E, et al. In vivo downregulation of T helper cell 1 immune responses reduces atherogenesis in apolipoprotein E-knockout mice. Circulation 2001; 104:197-202.
41. Buono C, Binder CJ, Stavrakis G, et al. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci U S A 2005; 102:1596-1601.
42. Gupta S, Pablo AM, Jiang XC, et al. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest 1997; 99:2752-2761.
43. Voloshyna I, Littlefield MJ, Reiss AB. Atherosclerosis and interferon-g: new insights and therapeutic targets. Trends Cardiovasc Med 2014; 24:45-51.
44. Stemme S, Faber B, Holm J, et al. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci U S A 1995; 92:3893-3897.
45. Xu Q, Kleindienst R, Waitz W, et al. Increased expression of heat shock protein 65 coincides with a population of infiltrating T lymphocytes in atherosclerotic lesions of rabbits specifically responding to heat shock protein 65. J Clin Invest 1993; 91:2693-2702.
46. Zhou X, Nicoletti A, Elhage R, Hansson GK. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 2000; 102:2919-2922; 12.
47. Paulsson G, Zhou X, Törnquist E, Hansson GK. Oligoclonal T cell expansions in atherosclerotic lesions of apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2000; 20:10-17.
48. Hermansson A, Ketelhuth DF, Strodthoff D, et al. Inhibition of T cell response to native low-density lipoprotein reduces atherosclerosis. J Exp Med 2010; 207:1081-1093.
49. Walcher D, Kümmel A, Kehrle B, et al. LXR activation reduces proinflammatory cytokine expression in human CD4-positive lymphocytes. Arterioscler Thromb Vasc Biol 2006; 26:1022-1028.
50. Ylä-Herttuala S, Palinski W, Butler SW, et al. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler Thromb 1994; 14:32-40.
51. Foks AC, van Puijvelde GHM, Bot I, et al. Interruption of the OX40-OX40 ligand pathway in LDL receptor-deficient mice causes regression of atherosclerosis. J Immunol 2013; 191:4573-4580.
52. Inouye M, Silander K, Hamalainen E, et al. An immune response network associated with blood lipid levels. PLoS Genet 2010; 6:e1001113.
53. Willems S, Vink A, Bot I, et al. Mast cells in human carotid atherosclerotic plaques are associated with intraplaque microvessel density and the occurrence of future cardiovascular events. Eur Heart J 2013; 34:3699-3706.
54. Tsiantoulas D, Diehl CJ, Witztum JL, Binder CJ. B cells and humoral immunity in atherosclerosis. Circ Res 2014; 114:1743-1756.
55. Ishigami T, Abe K, Aoki I, et al. Anti-interleukin-5 and multiple autoantibodies are associated with human atherosclerotic diseases and serum interleukin-5 levels. FASEB J 2013; 27:3437-3445.
56. Cardilo-Reis L, Gruber S, Schreier SM, et al. Interleukin-13 protects from atherosclerosis and modulates plaque composition by skewing the macrophage phenotype. EMBO Mol Med 2012; 4:1072-1086.
57. Wigren M, Björkbacka H, Andersson L, et al. Low levels of circulating CD4+FoxP3+ T cells are associated with an increased risk for development of myocardial infarction but not for stroke. Arterioscler Thromb Vasc Biol 2012; 32:2000-2004.
58. Mor A, Luboshits G, Planer D, et al. Altered status of CD4(+)CD25(+) regulatory T cells in patients with acute coronary syndromes. Eur Heart J 2006; 27:2530-2537.
59. Mor A, Planer D, Luboshits G, et al. Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscler Thromb Vasc Biol 2007; 27:893-900.
60. Maganto-García E, Tarrio ML, Grabie N, et al. Dynamic changes in regulatory T cells are linked to levels of diet-induced hypercholesterolemia. Circulation 2011; 124:185-195.
61. Von Der Thüsen JH, Kuiper J, Fekkes ML, et al. Attenuation of atherogenesis by systemic and local adenovirus-mediated gene transfer of interleukin-10 in LDLr-/- mice. FASEB J 2001; 15:2730-2732.
62. Foks AC, Frodermann V, ter Borg M, et al. Differential effects of regulatory T cells on the initiation and regression of atherosclerosis. Atherosclerosis 2011; 218:53-60.
63. Binder CJ, Hartvigsen K, Chang M-K, et al. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest 2004; 114:427-437.
64. Ait-Oufella H, Herbin O, Bouaziz J-D, et al. B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 2010; 207:1579-1587.
65. Tsiantoulas D, Sage AP, Mallat Z, Binder CJ. Targeting B cells in atherosclerosis: closing the gap from bench to bedside. Arterioscler Thromb Vasc Biol 2015; 35:296-302.
66. Van den Bossche J, Neele AE, Hoeksema MA, de Winther MPJ. Macrophage polarization: the epigenetic point of view. CurrOpin Lipidol 2014; 25:367-373.
67. Hoeksema MA, Gijbels MJ, Van den Bossche J, et al. Targeting macrophage histone deacetylase 3 stabilizes atherosclerotic lesions. EMBO Mol Med 2014; 6:1124-1132.
68. Bekkering S, Quintin J, Joosten LAB, et al. Oxidized low-density lipoprotein induces long-term proinflammatory cytokine production and foam cell formation via epigenetic reprogramming of monocytes. Arterioscler Thromb Vasc Biol 2014; 34:1731-1738.
69. Feinberg MW, Moore KJ. MicroRNA regulation of atherosclerosis. Circ Res 2016; 118:703-720.
70. Dai Y, Condorelli G, Mehta JL. Scavenger receptors and non-coding RNAs: relevance in atherogenesis. Cardiovasc Res 2016; 109:24-33.
71. Jacobsen MJ, Mentzel CMJ, Olesen AS, et al. Altered methylation profile of lymphocytes is concordant with perturbation of lipids metabolism and inflammatory response in obesity. J Diabetes Res 2016; 2016:8539057.
72. Cholesterol Treatment Trialists' (CTT) Collaborators. Mihaylova B, Emberson J, et al. The effects of lowering LDL cholesterol with statin therapy in people at low risk of vascular disease: meta-analysis of individual data from 27 randomised trials. Lancet 2012; 380:581-590.
73. Sukhova GK, Williams JK, Libby P. Statins reduce inflammation in atheroma of nonhuman primates independent of effects on serum cholesterol. Arterioscler Thromb Vasc Biol 2002; 22:1452-1458.
74. Ridker PM, Lüscher TF. Anti-inflammatory therapies for cardiovascular disease. Eur Heart J 2014; 35:1782-1791.
75. Ridker PM, Thuren T, Zalewski A, Libby P. Interleukin-1b inhibition and the prevention of recurrent cardiovascular events: rationale and design of the Canakinumab Anti-inflammatory Thrombosis Outcomes Study (CANTOS). Am Heart J 2011; 162:597-605.
76. Bhaskar V, Yin J, Mirza AM, et al. Monoclonal antibodies targeting IL-1 beta reduce biomarkers of atherosclerosis in vitro and inhibit atherosclerotic plaque formation in apolipoprotein E-deficient mice. Atherosclerosis 2011; 216:313-320.