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Published in: Basic Research in Cardiology 4/2015

01-07-2015 | Invited Review

Macrophages and immune cells in atherosclerosis: recent advances and novel concepts

Authors: Clément Cochain, Alma Zernecke

Published in: Basic Research in Cardiology | Issue 4/2015

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Abstract

Atherosclerotic lesion-related thrombosis is the major cause of myocardial infarction and stroke, which together constitute the leading cause of mortality worldwide. The inflammatory response is considered as a predominant driving force in atherosclerotic plaque formation, growth and progression towards instability and rupture. Notably, accumulation of macrophages in the intima and emergence of a pro-inflammatory milieu are a characteristic feature of plaque progression, and these processes can be modulated by adaptive immune responses. Recently, novel evidences of onsite proliferation of macrophages in lesions and transdifferentiation of smooth muscle cells to macrophages have challenged the prevalent paradigm that macrophage accumulation mostly relies on recruitment of circulating monocytes to plaques. Furthermore, previously unrecognized roles of inflammatory cell subsets such as plasmacytoid dendritic cells, innate response activator B cells or CD8+ T cells in atherosclerosis have emerged, as well as novel mechanisms by which regulatory T cells or natural killer T cells contribute to lesion formation. Here, we review and discuss these recent advances in our understanding of inflammatory processes in atherosclerosis.
Literature
1.
go back to reference Ait-Oufella H, Herbin O, Bouaziz JD, Binder CJ, Uyttenhove C, Laurans L, Taleb S, Van Vre E, Esposito B, Vilar J, Sirvent J, Van Snick J, Tedgui A, Tedder TF, Mallat Z (2010) B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 207:1579–1587. doi:10.1084/jem.20100155 PubMedCentralPubMedCrossRef Ait-Oufella H, Herbin O, Bouaziz JD, Binder CJ, Uyttenhove C, Laurans L, Taleb S, Van Vre E, Esposito B, Vilar J, Sirvent J, Van Snick J, Tedgui A, Tedder TF, Mallat Z (2010) B cell depletion reduces the development of atherosclerosis in mice. J Exp Med 207:1579–1587. doi:10.​1084/​jem.​20100155 PubMedCentralPubMedCrossRef
3.
go back to reference Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z (2006) Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 12:178–180. doi:10.1038/nm1343 PubMedCrossRef Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hansson GK, Klatzmann D, Tedgui A, Mallat Z (2006) Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 12:178–180. doi:10.​1038/​nm1343 PubMedCrossRef
5.
go back to reference Andreeva ER, Pugach IM, Orekhov AN (1997) Subendothelial smooth muscle cells of human aorta express macrophage antigen in situ and in vitro. Atherosclerosis 135:19–27PubMedCrossRef Andreeva ER, Pugach IM, Orekhov AN (1997) Subendothelial smooth muscle cells of human aorta express macrophage antigen in situ and in vitro. Atherosclerosis 135:19–27PubMedCrossRef
7.
go back to reference Boring L, Gosling J, Cleary M, Charo IF (1998) Decreased lesion formation in CCR2−/− mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394:894–897. doi:10.1038/29788 PubMedCrossRef Boring L, Gosling J, Cleary M, Charo IF (1998) Decreased lesion formation in CCR2−/− mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 394:894–897. doi:10.​1038/​29788 PubMedCrossRef
8.
go back to reference Brennan PJ, Brigl M, Brenner MB (2013) Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 13:101–117. doi:10.1038/nri3369 PubMedCrossRef Brennan PJ, Brigl M, Brenner MB (2013) Invariant natural killer T cells: an innate activation scheme linked to diverse effector functions. Nat Rev Immunol 13:101–117. doi:10.​1038/​nri3369 PubMedCrossRef
9.
go back to reference Clement M, Guedj K, Andreata F, Morvan M, Bey L, Khallou-Laschet J, Gaston AT, Delbosc S, Alsac JM, Bruneval P, Deschildre C, Le Borgne M, Castier Y, Kim HJ, Cantor H, Michel JB, Caligiuri G, Nicoletti A (2015) Control of the T Follicular Helper-Germinal Center B-cell axis by CD8+ regulatory T cells limits atherosclerosis and tertiary lymphoid organ development. Circulation 131:560–570. doi:10.1161/CIRCULATIONAHA.114.010988 PubMedCrossRef Clement M, Guedj K, Andreata F, Morvan M, Bey L, Khallou-Laschet J, Gaston AT, Delbosc S, Alsac JM, Bruneval P, Deschildre C, Le Borgne M, Castier Y, Kim HJ, Cantor H, Michel JB, Caligiuri G, Nicoletti A (2015) Control of the T Follicular Helper-Germinal Center B-cell axis by CD8+ regulatory T cells limits atherosclerosis and tertiary lymphoid organ development. Circulation 131:560–570. doi:10.​1161/​CIRCULATIONAHA.​114.​010988 PubMedCrossRef
12.
go back to reference Combadiere C, Potteaux S, Rodero M, Simon T, Pezard A, Esposito B, Merval R, Proudfoot A, Tedgui A, Mallat Z (2008) Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 117:1649–1657. doi:10.1161/CIRCULATIONAHA.107.745091 PubMedCrossRef Combadiere C, Potteaux S, Rodero M, Simon T, Pezard A, Esposito B, Merval R, Proudfoot A, Tedgui A, Mallat Z (2008) Combined inhibition of CCL2, CX3CR1, and CCR5 abrogates Ly6C(hi) and Ly6C(lo) monocytosis and almost abolishes atherosclerosis in hypercholesterolemic mice. Circulation 117:1649–1657. doi:10.​1161/​CIRCULATIONAHA.​107.​745091 PubMedCrossRef
13.
go back to reference Courties G, Herisson F, Sager HB, Heidt T, Ye Y, Wei Y, Sun Y, Severe N, Dutta P, Scharff J, Scadden DT, Weissleder R, Swirski FK, Moskowitz MA, Nahrendorf M (2015) Ischemic stroke activates hematopoietic bone marrow stem cells. Circ Res 116:407–417. doi:10.1161/CIRCRESAHA.116.305207 PubMedCrossRef Courties G, Herisson F, Sager HB, Heidt T, Ye Y, Wei Y, Sun Y, Severe N, Dutta P, Scharff J, Scadden DT, Weissleder R, Swirski FK, Moskowitz MA, Nahrendorf M (2015) Ischemic stroke activates hematopoietic bone marrow stem cells. Circ Res 116:407–417. doi:10.​1161/​CIRCRESAHA.​116.​305207 PubMedCrossRef
14.
go back to reference Daissormont IT, Christ A, Temmerman L, Sampedro Millares S, Seijkens T, Manca M, Rousch M, Poggi M, Boon L, van der Loos C, Daemen M, Lutgens E, Halvorsen B, Aukrust P, Janssen E, Biessen EA (2011) Plasmacytoid dendritic cells protect against atherosclerosis by tuning T-cell proliferation and activity. Circ Res 109:1387–1395. doi:10.1161/CIRCRESAHA.111.256529 PubMedCentralPubMedCrossRef Daissormont IT, Christ A, Temmerman L, Sampedro Millares S, Seijkens T, Manca M, Rousch M, Poggi M, Boon L, van der Loos C, Daemen M, Lutgens E, Halvorsen B, Aukrust P, Janssen E, Biessen EA (2011) Plasmacytoid dendritic cells protect against atherosclerosis by tuning T-cell proliferation and activity. Circ Res 109:1387–1395. doi:10.​1161/​CIRCRESAHA.​111.​256529 PubMedCentralPubMedCrossRef
15.
go back to reference Dinh TN, Kyaw TS, Kanellakis P, To K, Tipping P, Toh BH, Bobik A, Agrotis A (2012) Cytokine therapy with interleukin-2/anti-interleukin-2 monoclonal antibody complexes expands CD4+CD25+Foxp3+ regulatory T cells and attenuates development and progression of atherosclerosis. Circulation 126:1256–1266. doi:10.1161/CIRCULATIONAHA.112.099044 PubMedCrossRef Dinh TN, Kyaw TS, Kanellakis P, To K, Tipping P, Toh BH, Bobik A, Agrotis A (2012) Cytokine therapy with interleukin-2/anti-interleukin-2 monoclonal antibody complexes expands CD4+CD25+Foxp3+ regulatory T cells and attenuates development and progression of atherosclerosis. Circulation 126:1256–1266. doi:10.​1161/​CIRCULATIONAHA.​112.​099044 PubMedCrossRef
16.
go back to reference Doring Y, Manthey HD, Drechsler M, Lievens D, Megens RT, Soehnlein O, Busch M, Manca M, Koenen RR, Pelisek J, Daemen MJ, Lutgens E, Zenke M, Binder CJ, Weber C, Zernecke A (2012) Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 125:1673–1683. doi:10.1161/CIRCULATIONAHA.111.046755 PubMedCrossRef Doring Y, Manthey HD, Drechsler M, Lievens D, Megens RT, Soehnlein O, Busch M, Manca M, Koenen RR, Pelisek J, Daemen MJ, Lutgens E, Zenke M, Binder CJ, Weber C, Zernecke A (2012) Auto-antigenic protein-DNA complexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 125:1673–1683. doi:10.​1161/​CIRCULATIONAHA.​111.​046755 PubMedCrossRef
17.
go back to reference Dutta P, Courties G, Wei Y, Leuschner F, Gorbatov R, Robbins CS, Iwamoto Y, Thompson B, Carlson AL, Heidt T, Majmudar MD, Lasitschka F, Etzrodt M, Waterman P, Waring MT, Chicoine AT, van der Laan AM, Niessen HW, Piek JJ, Rubin BB, Butany J, Stone JR, Katus HA, Murphy SA, Morrow DA, Sabatine MS, Vinegoni C, Moskowitz MA, Pittet MJ, Libby P, Lin CP, Swirski FK, Weissleder R, Nahrendorf M (2012) Myocardial infarction accelerates atherosclerosis. Nature 487:325–329. doi:10.1038/nature11260 PubMedCentralPubMedCrossRef Dutta P, Courties G, Wei Y, Leuschner F, Gorbatov R, Robbins CS, Iwamoto Y, Thompson B, Carlson AL, Heidt T, Majmudar MD, Lasitschka F, Etzrodt M, Waterman P, Waring MT, Chicoine AT, van der Laan AM, Niessen HW, Piek JJ, Rubin BB, Butany J, Stone JR, Katus HA, Murphy SA, Morrow DA, Sabatine MS, Vinegoni C, Moskowitz MA, Pittet MJ, Libby P, Lin CP, Swirski FK, Weissleder R, Nahrendorf M (2012) Myocardial infarction accelerates atherosclerosis. Nature 487:325–329. doi:10.​1038/​nature11260 PubMedCentralPubMedCrossRef
18.
go back to reference Elhage R, Gourdy P, Brouchet L, Jawien J, Fouque MJ, Fievet C, Huc X, Barreira Y, Couloumiers JC, Arnal JF, Bayard F (2004) Deleting TCR alpha beta+ or CD4+ T lymphocytes leads to opposite effects on site-specific atherosclerosis in female apolipoprotein E-deficient mice. Am J Pathol 165:2013–2018PubMedCentralPubMedCrossRef Elhage R, Gourdy P, Brouchet L, Jawien J, Fouque MJ, Fievet C, Huc X, Barreira Y, Couloumiers JC, Arnal JF, Bayard F (2004) Deleting TCR alpha beta+ or CD4+ T lymphocytes leads to opposite effects on site-specific atherosclerosis in female apolipoprotein E-deficient mice. Am J Pathol 165:2013–2018PubMedCentralPubMedCrossRef
19.
go back to reference Erbel C, Akhavanpoor M, Okuyucu D, Wangler S, Dietz A, Zhao L, Stellos K, Little KM, Lasitschka F, Doesch A, Hakimi M, Dengler TJ, Giese T, Blessing E, Katus HA, Gleissner CA (2014) IL-17A influences essential functions of the monocyte/macrophage lineage and is involved in advanced murine and human atherosclerosis. J Immunol 193:4344–4355. doi:10.4049/jimmunol.1400181 PubMedCentralPubMedCrossRef Erbel C, Akhavanpoor M, Okuyucu D, Wangler S, Dietz A, Zhao L, Stellos K, Little KM, Lasitschka F, Doesch A, Hakimi M, Dengler TJ, Giese T, Blessing E, Katus HA, Gleissner CA (2014) IL-17A influences essential functions of the monocyte/macrophage lineage and is involved in advanced murine and human atherosclerosis. J Immunol 193:4344–4355. doi:10.​4049/​jimmunol.​1400181 PubMedCentralPubMedCrossRef
20.
go back to reference Erbel C, Tyka M, Helmes CM, Akhavanpoor M, Rupp G, Domschke G, Linden F, Wolf A, Doesch A, Lasitschka F, Katus HA, Gleissner CA (2015) CXCL4-induced plaque macrophages can be specifically identified by co-expression of MMP7+S100A8+ in vitro and in vivo. Innate Immun 21:255–265. doi:10.1177/1753425914526461 PubMedCrossRef Erbel C, Tyka M, Helmes CM, Akhavanpoor M, Rupp G, Domschke G, Linden F, Wolf A, Doesch A, Lasitschka F, Katus HA, Gleissner CA (2015) CXCL4-induced plaque macrophages can be specifically identified by co-expression of MMP7+S100A8+ in vitro and in vivo. Innate Immun 21:255–265. doi:10.​1177/​1753425914526461​ PubMedCrossRef
21.
go back to reference Erbel C, Wolf A, Lasitschka F, Linden F, Domschke G, Akhavanpoor M, Doesch AO, Katus HA, Gleissner CA (2015) Prevalence of M4 macrophages within human coronary atherosclerotic plaques is associated with features of plaque instability. Int J Cardiol 186:219–225. doi:10.1016/j.ijcard.2015.03.151 PubMedCrossRef Erbel C, Wolf A, Lasitschka F, Linden F, Domschke G, Akhavanpoor M, Doesch AO, Katus HA, Gleissner CA (2015) Prevalence of M4 macrophages within human coronary atherosclerotic plaques is associated with features of plaque instability. Int J Cardiol 186:219–225. doi:10.​1016/​j.​ijcard.​2015.​03.​151 PubMedCrossRef
23.
go back to reference Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM (2003) Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med 198:267–279. doi:10.1084/jem.20030324 PubMedCentralPubMedCrossRef Fujii S, Shimizu K, Smith C, Bonifaz L, Steinman RM (2003) Activation of natural killer T cells by alpha-galactosylceramide rapidly induces the full maturation of dendritic cells in vivo and thereby acts as an adjuvant for combined CD4 and CD8 T cell immunity to a coadministered protein. J Exp Med 198:267–279. doi:10.​1084/​jem.​20030324 PubMedCentralPubMedCrossRef
27.
go back to reference Gotsman I, Grabie N, Gupta R, Dacosta R, MacConmara M, Lederer J, Sukhova G, Witztum JL, Sharpe AH, Lichtman AH (2006) Impaired regulatory T-cell response and enhanced atherosclerosis in the absence of inducible costimulatory molecule. Circulation 114:2047–2055. doi:10.1161/CIRCULATIONAHA.106.633263 PubMedCrossRef Gotsman I, Grabie N, Gupta R, Dacosta R, MacConmara M, Lederer J, Sukhova G, Witztum JL, Sharpe AH, Lichtman AH (2006) Impaired regulatory T-cell response and enhanced atherosclerosis in the absence of inducible costimulatory molecule. Circulation 114:2047–2055. doi:10.​1161/​CIRCULATIONAHA.​106.​633263 PubMedCrossRef
29.
go back to reference Heidt T, Sager HB, Courties G, Dutta P, Iwamoto Y, Zaltsman A, von Zur Muhlen C, Bode C, Fricchione GL, Denninger J, Lin CP, Vinegoni C, Libby P, Swirski FK, Weissleder R, Nahrendorf M (2014) Chronic variable stress activates hematopoietic stem cells. Nat Med 20:754–758. doi:10.1038/nm.3589 PubMedCentralPubMedCrossRef Heidt T, Sager HB, Courties G, Dutta P, Iwamoto Y, Zaltsman A, von Zur Muhlen C, Bode C, Fricchione GL, Denninger J, Lin CP, Vinegoni C, Libby P, Swirski FK, Weissleder R, Nahrendorf M (2014) Chronic variable stress activates hematopoietic stem cells. Nat Med 20:754–758. doi:10.​1038/​nm.​3589 PubMedCentralPubMedCrossRef
30.
go back to reference Hilgendorf I, Theurl I, Gerhardt LM, Robbins CS, Weber GF, Gonen A, Iwamoto Y, Degousee N, Holderried TA, Winter C, Zirlik A, Lin HY, Sukhova GK, Butany J, Rubin BB, Witztum JL, Libby P, Nahrendorf M, Weissleder R, Swirski FK (2014) Innate response activator B cells aggravate atherosclerosis by stimulating T helper-1 adaptive immunity. Circulation 129:1677–1687. doi:10.1161/CIRCULATIONAHA.113.006381 PubMedCentralPubMedCrossRef Hilgendorf I, Theurl I, Gerhardt LM, Robbins CS, Weber GF, Gonen A, Iwamoto Y, Degousee N, Holderried TA, Winter C, Zirlik A, Lin HY, Sukhova GK, Butany J, Rubin BB, Witztum JL, Libby P, Nahrendorf M, Weissleder R, Swirski FK (2014) Innate response activator B cells aggravate atherosclerosis by stimulating T helper-1 adaptive immunity. Circulation 129:1677–1687. doi:10.​1161/​CIRCULATIONAHA.​113.​006381 PubMedCentralPubMedCrossRef
31.
go back to reference Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, Lebon P, Heshmati F, Guillet JG, Gannage M, Caillat-Zucman S, Casartelli N, Schwartz O, De la Salle H, Hanau D, Hosmalin A, Maranon C (2007) Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 27:481–492. doi:10.1016/j.immuni.2007.07.021 PubMedCrossRef Hoeffel G, Ripoche AC, Matheoud D, Nascimbeni M, Escriou N, Lebon P, Heshmati F, Guillet JG, Gannage M, Caillat-Zucman S, Casartelli N, Schwartz O, De la Salle H, Hanau D, Hosmalin A, Maranon C (2007) Antigen crosspresentation by human plasmacytoid dendritic cells. Immunity 27:481–492. doi:10.​1016/​j.​immuni.​2007.​07.​021 PubMedCrossRef
32.
go back to reference Kadl A, Meher AK, Sharma PR, Lee MY, Doran AC, Johnstone SR, Elliott MR, Gruber F, Han J, Chen W, Kensler T, Ravichandran KS, Isakson BE, Wamhoff BR, Leitinger N (2010) Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res 107:737–746. doi:10.1161/CIRCRESAHA.109.215715 PubMedCentralPubMedCrossRef Kadl A, Meher AK, Sharma PR, Lee MY, Doran AC, Johnstone SR, Elliott MR, Gruber F, Han J, Chen W, Kensler T, Ravichandran KS, Isakson BE, Wamhoff BR, Leitinger N (2010) Identification of a novel macrophage phenotype that develops in response to atherogenic phospholipids via Nrf2. Circ Res 107:737–746. doi:10.​1161/​CIRCRESAHA.​109.​215715 PubMedCentralPubMedCrossRef
33.
35.
go back to reference Klingenberg R, Gerdes N, Badeau RM, Gistera A, Strodthoff D, Ketelhuth DF, Lundberg AM, Rudling M, Nilsson SK, Olivecrona G, Zoller S, Lohmann C, Luscher TF, Jauhiainen M, Sparwasser T, Hansson GK (2013) Depletion of FOXP3+ regulatory T cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest 123:1323–1334. doi:10.1172/JCI63891 PubMedCentralPubMedCrossRef Klingenberg R, Gerdes N, Badeau RM, Gistera A, Strodthoff D, Ketelhuth DF, Lundberg AM, Rudling M, Nilsson SK, Olivecrona G, Zoller S, Lohmann C, Luscher TF, Jauhiainen M, Sparwasser T, Hansson GK (2013) Depletion of FOXP3+ regulatory T cells promotes hypercholesterolemia and atherosclerosis. J Clin Invest 123:1323–1334. doi:10.​1172/​JCI63891 PubMedCentralPubMedCrossRef
38.
go back to reference Kyaw T, Tay C, Khan A, Dumouchel V, Cao A, To K, Kehry M, Dunn R, Agrotis A, Tipping P, Bobik A, Toh BH (2010) Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immunol 185:4410–4419. doi:10.4049/jimmunol.1000033 PubMedCrossRef Kyaw T, Tay C, Khan A, Dumouchel V, Cao A, To K, Kehry M, Dunn R, Agrotis A, Tipping P, Bobik A, Toh BH (2010) Conventional B2 B cell depletion ameliorates whereas its adoptive transfer aggravates atherosclerosis. J Immunol 185:4410–4419. doi:10.​4049/​jimmunol.​1000033 PubMedCrossRef
39.
go back to reference Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A, Tipping P, Bobik A, Toh BH (2011) B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res 109:830–840. doi:10.1161/CIRCRESAHA.111.248542 PubMedCrossRef Kyaw T, Tay C, Krishnamurthi S, Kanellakis P, Agrotis A, Tipping P, Bobik A, Toh BH (2011) B1a B lymphocytes are atheroprotective by secreting natural IgM that increases IgM deposits and reduces necrotic cores in atherosclerotic lesions. Circ Res 109:830–840. doi:10.​1161/​CIRCRESAHA.​111.​248542 PubMedCrossRef
40.
go back to reference Kyaw T, Winship A, Tay C, Kanellakis P, Hosseini H, Cao A, Li P, Tipping P, Bobik A, Toh BH (2013) Cytotoxic and proinflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoE-deficient mice. Circulation 127:1028–1039. doi:10.1161/CIRCULATIONAHA.112.001347 PubMedCrossRef Kyaw T, Winship A, Tay C, Kanellakis P, Hosseini H, Cao A, Li P, Tipping P, Bobik A, Toh BH (2013) Cytotoxic and proinflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoE-deficient mice. Circulation 127:1028–1039. doi:10.​1161/​CIRCULATIONAHA.​112.​001347 PubMedCrossRef
43.
go back to reference Li Y, To K, Kanellakis P, Hosseini H, Deswaerte V, Tipping P, Smyth MJ, Toh BH, Bobik A, Kyaw T (2015) CD4+ natural killer T cells potently augment aortic root atherosclerosis by perforin- and granzyme B-dependent cytotoxicity. Circ Res 116:245–254. doi:10.1161/CIRCRESAHA.116.304734 PubMedCrossRef Li Y, To K, Kanellakis P, Hosseini H, Deswaerte V, Tipping P, Smyth MJ, Toh BH, Bobik A, Kyaw T (2015) CD4+ natural killer T cells potently augment aortic root atherosclerosis by perforin- and granzyme B-dependent cytotoxicity. Circ Res 116:245–254. doi:10.​1161/​CIRCRESAHA.​116.​304734 PubMedCrossRef
44.
go back to reference Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Barker-Collo S, Bartels DH, Bell ML, Benjamin EJ, Bennett D, Bhalla K, Bikbov B, Bin Abdulhak A, Birbeck G, Blyth F, Bolliger I, Boufous S, Bucello C, Burch M, Burney P, Carapetis J, Chen H, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahodwala N, De Leo D, Degenhardt L, Delossantos A, Denenberg J, Des Jarlais DC, Dharmaratne SD, Dorsey ER, Driscoll T, Duber H, Ebel B, Erwin PJ, Espindola P, Ezzati M, Feigin V, Flaxman AD, Forouzanfar MH, Fowkes FG, Franklin R, Fransen M, Freeman MK, Gabriel SE, Gakidou E, Gaspari F, Gillum RF, Gonzalez-Medina D, Halasa YA, Haring D, Harrison JE, Havmoeller R, Hay RJ, Hoen B, Hotez PJ, Hoy D, Jacobsen KH, James SL, Jasrasaria R, Jayaraman S, Johns N, Karthikeyan G, Kassebaum N, Keren A, Khoo JP, Knowlton LM, Kobusingye O, Koranteng A, Krishnamurthi R, Lipnick M, Lipshultz SE, Ohno SL et al (2012) Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2095–2128. doi:10.1016/S0140-6736(12)61728-0 PubMedCrossRef Lozano R, Naghavi M, Foreman K, Lim S, Shibuya K, Aboyans V, Abraham J, Adair T, Aggarwal R, Ahn SY, Alvarado M, Anderson HR, Anderson LM, Andrews KG, Atkinson C, Baddour LM, Barker-Collo S, Bartels DH, Bell ML, Benjamin EJ, Bennett D, Bhalla K, Bikbov B, Bin Abdulhak A, Birbeck G, Blyth F, Bolliger I, Boufous S, Bucello C, Burch M, Burney P, Carapetis J, Chen H, Chou D, Chugh SS, Coffeng LE, Colan SD, Colquhoun S, Colson KE, Condon J, Connor MD, Cooper LT, Corriere M, Cortinovis M, de Vaccaro KC, Couser W, Cowie BC, Criqui MH, Cross M, Dabhadkar KC, Dahodwala N, De Leo D, Degenhardt L, Delossantos A, Denenberg J, Des Jarlais DC, Dharmaratne SD, Dorsey ER, Driscoll T, Duber H, Ebel B, Erwin PJ, Espindola P, Ezzati M, Feigin V, Flaxman AD, Forouzanfar MH, Fowkes FG, Franklin R, Fransen M, Freeman MK, Gabriel SE, Gakidou E, Gaspari F, Gillum RF, Gonzalez-Medina D, Halasa YA, Haring D, Harrison JE, Havmoeller R, Hay RJ, Hoen B, Hotez PJ, Hoy D, Jacobsen KH, James SL, Jasrasaria R, Jayaraman S, Johns N, Karthikeyan G, Kassebaum N, Keren A, Khoo JP, Knowlton LM, Kobusingye O, Koranteng A, Krishnamurthi R, Lipnick M, Lipshultz SE, Ohno SL et al (2012) Global and regional mortality from 235 causes of death for 20 age groups in 1990 and 2010: a systematic analysis for the Global Burden of Disease Study 2010. Lancet 380:2095–2128. doi:10.​1016/​S0140-6736(12)61728-0 PubMedCrossRef
45.
go back to reference Ludewig B, Freigang S, Jaggi M, Kurrer MO, Pei YC, Vlk L, Odermatt B, Zinkernagel RM, Hengartner H (2000) Linking immune-mediated arterial inflammation and cholesterol-induced atherosclerosis in a transgenic mouse model. Proc Natl Acad Sci USA 97:12752–12757. doi:10.1073/pnas.220427097 PubMedCentralPubMedCrossRef Ludewig B, Freigang S, Jaggi M, Kurrer MO, Pei YC, Vlk L, Odermatt B, Zinkernagel RM, Hengartner H (2000) Linking immune-mediated arterial inflammation and cholesterol-induced atherosclerosis in a transgenic mouse model. Proc Natl Acad Sci USA 97:12752–12757. doi:10.​1073/​pnas.​220427097 PubMedCentralPubMedCrossRef
46.
go back to reference Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ (1999) Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res 41:473–479PubMedCrossRef Lutgens E, de Muinck ED, Kitslaar PJ, Tordoir JH, Wellens HJ, Daemen MJ (1999) Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques. Cardiovasc Res 41:473–479PubMedCrossRef
47.
go back to reference Macritchie N, Grassia G, Sabir SR, Maddaluno M, Welsh P, Sattar N, Ialenti A, Kurowska-Stolarska M, McInnes IB, Brewer JM, Garside P, Maffia P (2012) Plasmacytoid dendritic cells play a key role in promoting atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 32:2569–2579. doi:10.1161/ATVBAHA.112.251314 PubMedCrossRef Macritchie N, Grassia G, Sabir SR, Maddaluno M, Welsh P, Sattar N, Ialenti A, Kurowska-Stolarska M, McInnes IB, Brewer JM, Garside P, Maffia P (2012) Plasmacytoid dendritic cells play a key role in promoting atherosclerosis in apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 32:2569–2579. doi:10.​1161/​ATVBAHA.​112.​251314 PubMedCrossRef
48.
go back to reference Metelitsa LS, Naidenko OV, Kant A, Wu HW, Loza MJ, Perussia B, Kronenberg M, Seeger RC (2001) Human NKT cells mediate antitumor cytotoxicity directly by recognizing target cell CD1d with bound ligand or indirectly by producing IL-2 to activate NK cells. J Immunol 167:3114–3122PubMedCrossRef Metelitsa LS, Naidenko OV, Kant A, Wu HW, Loza MJ, Perussia B, Kronenberg M, Seeger RC (2001) Human NKT cells mediate antitumor cytotoxicity directly by recognizing target cell CD1d with bound ligand or indirectly by producing IL-2 to activate NK cells. J Immunol 167:3114–3122PubMedCrossRef
49.
go back to reference Mohanta SK, Yin C, Peng L, Srikakulapu P, Bontha V, Hu D, Weih F, Weber C, Gerdes N, Habenicht AJ (2014) Artery tertiary lymphoid organs contribute to innate and adaptive immune responses in advanced mouse atherosclerosis. Circ Res 114:1772–1787. doi:10.1161/CIRCRESAHA.114.301137 PubMedCrossRef Mohanta SK, Yin C, Peng L, Srikakulapu P, Bontha V, Hu D, Weih F, Weber C, Gerdes N, Habenicht AJ (2014) Artery tertiary lymphoid organs contribute to innate and adaptive immune responses in advanced mouse atherosclerosis. Circ Res 114:1772–1787. doi:10.​1161/​CIRCRESAHA.​114.​301137 PubMedCrossRef
50.
go back to reference Nakai Y, Iwabuchi K, Fujii S, Ishimori N, Dashtsoodol N, Watano K, Mishima T, Iwabuchi C, Tanaka S, Bezbradica JS, Nakayama T, Taniguchi M, Miyake S, Yamamura T, Kitabatake A, Joyce S, Van Kaer L, Onoe K (2004) Natural killer T cells accelerate atherogenesis in mice. Blood 104:2051–2059. doi:10.1182/blood-2003-10-3485 PubMedCrossRef Nakai Y, Iwabuchi K, Fujii S, Ishimori N, Dashtsoodol N, Watano K, Mishima T, Iwabuchi C, Tanaka S, Bezbradica JS, Nakayama T, Taniguchi M, Miyake S, Yamamura T, Kitabatake A, Joyce S, Van Kaer L, Onoe K (2004) Natural killer T cells accelerate atherogenesis in mice. Blood 104:2051–2059. doi:10.​1182/​blood-2003-10-3485 PubMedCrossRef
51.
52.
go back to reference Olofsson PS, Soderstrom LA, Wagsater D, Sheikine Y, Ocaya P, Lang F, Rabu C, Chen L, Rudling M, Aukrust P, Hedin U, Paulsson-Berne G, Sirsjo A, Hansson GK (2008) CD137 is expressed in human atherosclerosis and promotes development of plaque inflammation in hypercholesterolemic mice. Circulation 117:1292–1301. doi:10.1161/CIRCULATIONAHA.107.699173 PubMedCrossRef Olofsson PS, Soderstrom LA, Wagsater D, Sheikine Y, Ocaya P, Lang F, Rabu C, Chen L, Rudling M, Aukrust P, Hedin U, Paulsson-Berne G, Sirsjo A, Hansson GK (2008) CD137 is expressed in human atherosclerosis and promotes development of plaque inflammation in hypercholesterolemic mice. Circulation 117:1292–1301. doi:10.​1161/​CIRCULATIONAHA.​107.​699173 PubMedCrossRef
53.
go back to reference Potteaux S, Gautier EL, Hutchison SB, van Rooijen N, Rader DJ, Thomas MJ, Sorci-Thomas MG, Randolph GJ (2011) Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe−/− mice during disease regression. J Clin Invest 121:2025–2036. doi:10.1172/JCI43802 PubMedCentralPubMedCrossRef Potteaux S, Gautier EL, Hutchison SB, van Rooijen N, Rader DJ, Thomas MJ, Sorci-Thomas MG, Randolph GJ (2011) Suppressed monocyte recruitment drives macrophage removal from atherosclerotic plaques of Apoe−/− mice during disease regression. J Clin Invest 121:2025–2036. doi:10.​1172/​JCI43802 PubMedCentralPubMedCrossRef
54.
go back to reference Psaltis PJ, Harbuzariu A, Delacroix S, Witt TA, Holroyd EW, Spoon DB, Hoffman SJ, Pan S, Kleppe LS, Mueske CS, Gulati R, Sandhu GS, Simari RD (2012) Identification of a monocyte-predisposed hierarchy of hematopoietic progenitor cells in the adventitia of postnatal murine aorta. Circulation 125:592–603. doi:10.1161/CIRCULATIONAHA.111.059360 PubMedCentralPubMedCrossRef Psaltis PJ, Harbuzariu A, Delacroix S, Witt TA, Holroyd EW, Spoon DB, Hoffman SJ, Pan S, Kleppe LS, Mueske CS, Gulati R, Sandhu GS, Simari RD (2012) Identification of a monocyte-predisposed hierarchy of hematopoietic progenitor cells in the adventitia of postnatal murine aorta. Circulation 125:592–603. doi:10.​1161/​CIRCULATIONAHA.​111.​059360 PubMedCentralPubMedCrossRef
55.
go back to reference Psaltis PJ, Puranik AS, Spoon DB, Chue CD, Hoffman SJ, Witt TA, Delacroix S, Kleppe LS, Mueske CS, Pan S, Gulati R, Simari RD (2014) Characterization of a resident population of adventitial macrophage progenitor cells in postnatal vasculature. Circ Res 115:364–375. doi:10.1161/CIRCRESAHA.115.303299 PubMedCrossRef Psaltis PJ, Puranik AS, Spoon DB, Chue CD, Hoffman SJ, Witt TA, Delacroix S, Kleppe LS, Mueske CS, Pan S, Gulati R, Simari RD (2014) Characterization of a resident population of adventitial macrophage progenitor cells in postnatal vasculature. Circ Res 115:364–375. doi:10.​1161/​CIRCRESAHA.​115.​303299 PubMedCrossRef
57.
go back to reference Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, Tiglao E, Figueiredo JL, Iwamoto Y, Theurl I, Gorbatov R, Waring MT, Chicoine AT, Mouded M, Pittet MJ, Nahrendorf M, Weissleder R, Swirski FK (2012) Innate response activator B cells protect against microbial sepsis. Science 335:597–601. doi:10.1126/science.1215173 PubMedCentralPubMedCrossRef Rauch PJ, Chudnovskiy A, Robbins CS, Weber GF, Etzrodt M, Hilgendorf I, Tiglao E, Figueiredo JL, Iwamoto Y, Theurl I, Gorbatov R, Waring MT, Chicoine AT, Mouded M, Pittet MJ, Nahrendorf M, Weissleder R, Swirski FK (2012) Innate response activator B cells protect against microbial sepsis. Science 335:597–601. doi:10.​1126/​science.​1215173 PubMedCentralPubMedCrossRef
58.
go back to reference Recalde A, Richart A, Guerin C, Cochain C, Zouggari Y, Yin KH, Vilar J, Drouet I, Levy B, Varoquaux O, Silvestre JS (2012) Sympathetic nervous system regulates bone marrow-derived cell egress through endothelial nitric oxide synthase activation: role in postischemic tissue remodeling. Arterioscler Thromb Vasc Biol 32:643–653. doi:10.1161/ATVBAHA.111.244392 PubMedCrossRef Recalde A, Richart A, Guerin C, Cochain C, Zouggari Y, Yin KH, Vilar J, Drouet I, Levy B, Varoquaux O, Silvestre JS (2012) Sympathetic nervous system regulates bone marrow-derived cell egress through endothelial nitric oxide synthase activation: role in postischemic tissue remodeling. Arterioscler Thromb Vasc Biol 32:643–653. doi:10.​1161/​ATVBAHA.​111.​244392 PubMedCrossRef
60.
go back to reference Rekhter MD, Gordon D (1995) Active proliferation of different cell types, including lymphocytes, in human atherosclerotic plaques. Am J Pathol 147:668–677PubMedCentralPubMed Rekhter MD, Gordon D (1995) Active proliferation of different cell types, including lymphocytes, in human atherosclerotic plaques. Am J Pathol 147:668–677PubMedCentralPubMed
61.
go back to reference Robbins CS, Chudnovskiy A, Rauch PJ, Figueiredo JL, Iwamoto Y, Gorbatov R, Etzrodt M, Weber GF, Ueno T, van Rooijen N, Mulligan-Kehoe MJ, Libby P, Nahrendorf M, Pittet MJ, Weissleder R, Swirski FK (2012) Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation 125:364–374. doi:10.1161/CIRCULATIONAHA.111.061986 PubMedCentralPubMedCrossRef Robbins CS, Chudnovskiy A, Rauch PJ, Figueiredo JL, Iwamoto Y, Gorbatov R, Etzrodt M, Weber GF, Ueno T, van Rooijen N, Mulligan-Kehoe MJ, Libby P, Nahrendorf M, Pittet MJ, Weissleder R, Swirski FK (2012) Extramedullary hematopoiesis generates Ly-6C(high) monocytes that infiltrate atherosclerotic lesions. Circulation 125:364–374. doi:10.​1161/​CIRCULATIONAHA.​111.​061986 PubMedCentralPubMedCrossRef
62.
go back to reference Robbins CS, Hilgendorf I, Weber GF, Theurl I, Iwamoto Y, Figueiredo JL, Gorbatov R, Sukhova GK, Gerhardt LM, Smyth D, Zavitz CC, Shikatani EA, Parsons M, van Rooijen N, Lin HY, Husain M, Libby P, Nahrendorf M, Weissleder R, Swirski FK (2013) Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 19:1166–1172. doi:10.1038/nm.3258 PubMedCentralPubMedCrossRef Robbins CS, Hilgendorf I, Weber GF, Theurl I, Iwamoto Y, Figueiredo JL, Gorbatov R, Sukhova GK, Gerhardt LM, Smyth D, Zavitz CC, Shikatani EA, Parsons M, van Rooijen N, Lin HY, Husain M, Libby P, Nahrendorf M, Weissleder R, Swirski FK (2013) Local proliferation dominates lesional macrophage accumulation in atherosclerosis. Nat Med 19:1166–1172. doi:10.​1038/​nm.​3258 PubMedCentralPubMedCrossRef
64.
go back to reference Rosenfeld ME, Ross R (1990) Macrophage and smooth muscle cell proliferation in atherosclerotic lesions of WHHL and comparably hypercholesterolemic fat-fed rabbits. Arterioscler Thromb Vasc Biol 10:680–687. doi:10.1161/01.ATV.10.5.680 CrossRef Rosenfeld ME, Ross R (1990) Macrophage and smooth muscle cell proliferation in atherosclerotic lesions of WHHL and comparably hypercholesterolemic fat-fed rabbits. Arterioscler Thromb Vasc Biol 10:680–687. doi:10.​1161/​01.​ATV.​10.​5.​680 CrossRef
65.
go back to reference Rosengren A, Hawken S, Ounpuu S, Sliwa K, Zubaid M, Almahmeed WA, Blackett KN, Sitthi-amorn C, Sato H, Yusuf S (2004) Association of psychosocial risk factors with risk of acute myocardial infarction in 11119 cases and 13648 controls from 52 countries (the INTERHEART study): case–control study. Lancet 364:953–962. doi:10.1016/S0140-6736(04)17019-0 PubMedCrossRef Rosengren A, Hawken S, Ounpuu S, Sliwa K, Zubaid M, Almahmeed WA, Blackett KN, Sitthi-amorn C, Sato H, Yusuf S (2004) Association of psychosocial risk factors with risk of acute myocardial infarction in 11119 cases and 13648 controls from 52 countries (the INTERHEART study): case–control study. Lancet 364:953–962. doi:10.​1016/​S0140-6736(04)17019-0 PubMedCrossRef
68.
go back to reference Sage A, Murphy DM, Maffia P, Masters LM, Sabir SR, Baker LL, Cambrook H, Finigan AJ, Ait-Oufella H, Grassia G, Harrison JE, Ludewig B, Reith W, Hansson GK, Reizis B, Hugues S, Mallat Z (2014) MHC class II-restricted Antigen presentation by plasmacytoid dendritic cells drives pro-atherogenic T cell immunity. Circulation. doi:10.1161/CIRCULATIONAHA.114.011090 PubMedCentral Sage A, Murphy DM, Maffia P, Masters LM, Sabir SR, Baker LL, Cambrook H, Finigan AJ, Ait-Oufella H, Grassia G, Harrison JE, Ludewig B, Reith W, Hansson GK, Reizis B, Hugues S, Mallat Z (2014) MHC class II-restricted Antigen presentation by plasmacytoid dendritic cells drives pro-atherogenic T cell immunity. Circulation. doi:10.​1161/​CIRCULATIONAHA.​114.​011090 PubMedCentral
69.
go back to reference Sage AP, Tsiantoulas D, Baker L, Harrison J, Masters L, Murphy D, Loinard C, Binder CJ, Mallat Z (2012) BAFF receptor deficiency reduces the development of atherosclerosis in mice–brief report. Arterioscler Thromb Vasc Biol 32:1573–1576. doi:10.1161/ATVBAHA.111.244731 PubMedCrossRef Sage AP, Tsiantoulas D, Baker L, Harrison J, Masters L, Murphy D, Loinard C, Binder CJ, Mallat Z (2012) BAFF receptor deficiency reduces the development of atherosclerosis in mice–brief report. Arterioscler Thromb Vasc Biol 32:1573–1576. doi:10.​1161/​ATVBAHA.​111.​244731 PubMedCrossRef
70.
go back to reference Salio M, Palmowski MJ, Atzberger A, Hermans IF, Cerundolo V (2004) CpG-matured murine plasmacytoid dendritic cells are capable of in vivo priming of functional CD8 T cell responses to endogenous but not exogenous antigens. J Exp Med 199:567–579. doi:10.1084/jem.20031059 PubMedCentralPubMedCrossRef Salio M, Palmowski MJ, Atzberger A, Hermans IF, Cerundolo V (2004) CpG-matured murine plasmacytoid dendritic cells are capable of in vivo priming of functional CD8 T cell responses to endogenous but not exogenous antigens. J Exp Med 199:567–579. doi:10.​1084/​jem.​20031059 PubMedCentralPubMedCrossRef
72.
go back to reference Semmling V, Lukacs-Kornek V, Thaiss CA, Quast T, Hochheiser K, Panzer U, Rossjohn J, Perlmutter P, Cao J, Godfrey DI, Savage PB, Knolle PA, Kolanus W, Forster I, Kurts C (2010) Alternative cross-priming through CCL17–CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 11:313–320. doi:10.1038/ni.1848 PubMedCrossRef Semmling V, Lukacs-Kornek V, Thaiss CA, Quast T, Hochheiser K, Panzer U, Rossjohn J, Perlmutter P, Cao J, Godfrey DI, Savage PB, Knolle PA, Kolanus W, Forster I, Kurts C (2010) Alternative cross-priming through CCL17–CCR4-mediated attraction of CTLs toward NKT cell-licensed DCs. Nat Immunol 11:313–320. doi:10.​1038/​ni.​1848 PubMedCrossRef
73.
go back to reference Soehnlein O, Drechsler M, Doring Y, Lievens D, Hartwig H, Kemmerich K, Ortega-Gomez A, Mandl M, Vijayan S, Projahn D, Garlichs CD, Koenen RR, Hristov M, Lutgens E, Zernecke A, Weber C (2013) Distinct functions of chemokine receptor axes in the atherogenic mobilization and recruitment of classical monocytes. EMBO Mol Med 5:471–481. doi:10.1002/emmm.201201717 PubMedCentralPubMedCrossRef Soehnlein O, Drechsler M, Doring Y, Lievens D, Hartwig H, Kemmerich K, Ortega-Gomez A, Mandl M, Vijayan S, Projahn D, Garlichs CD, Koenen RR, Hristov M, Lutgens E, Zernecke A, Weber C (2013) Distinct functions of chemokine receptor axes in the atherogenic mobilization and recruitment of classical monocytes. EMBO Mol Med 5:471–481. doi:10.​1002/​emmm.​201201717 PubMedCentralPubMedCrossRef
75.
go back to reference Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ (2007) Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 117:195–205. doi:10.1172/JCI29950 PubMedCentralPubMedCrossRef Swirski FK, Libby P, Aikawa E, Alcaide P, Luscinskas FW, Weissleder R, Pittet MJ (2007) Ly-6Chi monocytes dominate hypercholesterolemia-associated monocytosis and give rise to macrophages in atheromata. J Clin Invest 117:195–205. doi:10.​1172/​JCI29950 PubMedCentralPubMedCrossRef
76.
go back to reference Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ (2009) Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325:612–616. doi:10.1126/science.1175202 PubMedCentralPubMedCrossRef Swirski FK, Nahrendorf M, Etzrodt M, Wildgruber M, Cortez-Retamozo V, Panizzi P, Figueiredo JL, Kohler RH, Chudnovskiy A, Waterman P, Aikawa E, Mempel TR, Libby P, Weissleder R, Pittet MJ (2009) Identification of splenic reservoir monocytes and their deployment to inflammatory sites. Science 325:612–616. doi:10.​1126/​science.​1175202 PubMedCentralPubMedCrossRef
77.
go back to reference Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117:185–194. doi:10.1172/JCI28549 PubMedCentralPubMedCrossRef Tacke F, Alvarez D, Kaplan TJ, Jakubzick C, Spanbroek R, Llodra J, Garin A, Liu J, Mack M, van Rooijen N, Lira SA, Habenicht AJ, Randolph GJ (2007) Monocyte subsets differentially employ CCR2, CCR5, and CX3CR1 to accumulate within atherosclerotic plaques. J Clin Invest 117:185–194. doi:10.​1172/​JCI28549 PubMedCentralPubMedCrossRef
80.
go back to reference Weber C, Meiler S, Doring Y, Koch M, Drechsler M, Megens RT, Rowinska Z, Bidzhekov K, Fecher C, Ribechini E, van Zandvoort MA, Binder CJ, Jelinek I, Hristov M, Boon L, Jung S, Korn T, Lutz MB, Forster I, Zenke M, Hieronymus T, Junt T, Zernecke A (2011) CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell homeostasis in mice. J Clin Invest 121:2898–2910. doi:10.1172/JCI44925 PubMedCentralPubMedCrossRef Weber C, Meiler S, Doring Y, Koch M, Drechsler M, Megens RT, Rowinska Z, Bidzhekov K, Fecher C, Ribechini E, van Zandvoort MA, Binder CJ, Jelinek I, Hristov M, Boon L, Jung S, Korn T, Lutz MB, Forster I, Zenke M, Hieronymus T, Junt T, Zernecke A (2011) CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell homeostasis in mice. J Clin Invest 121:2898–2910. doi:10.​1172/​JCI44925 PubMedCentralPubMedCrossRef
82.
go back to reference Weber C, Zernecke A, Libby P (2008) The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Imunol 8:802–815. doi:10.1038/nri2415 CrossRef Weber C, Zernecke A, Libby P (2008) The multifaceted contributions of leukocyte subsets to atherosclerosis: lessons from mouse models. Nat Rev Imunol 8:802–815. doi:10.​1038/​nri2415 CrossRef
Metadata
Title
Macrophages and immune cells in atherosclerosis: recent advances and novel concepts
Authors
Clément Cochain
Alma Zernecke
Publication date
01-07-2015
Publisher
Springer Berlin Heidelberg
Published in
Basic Research in Cardiology / Issue 4/2015
Print ISSN: 0300-8428
Electronic ISSN: 1435-1803
DOI
https://doi.org/10.1007/s00395-015-0491-8

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