Skip to main content
Log in

Dendritic cells in atherosclerosis

  • Review
  • Published:
Seminars in Immunopathology Aims and scope Submit manuscript

Abstract

Atherosclerosis is a chronic inflammatory disease with activation of both the innate and adaptive arms of the immune system. Dendritic cells (DCs) are potent activators of adaptive immunity and have been identified in the normal arterial wall and within atherosclerotic lesions. Recent evidence points to a functional role for DCs in all stages of atherosclerosis because of their myriad functions including lipid uptake, antigen presentation, efferocytosis, and inflammation resolution. Moreover, DC-based vaccination strategies are currently being developed for the treatment of atherosclerosis. This review will focus on the current evidence as well as the proposed roles for DCs in the pathogenesis of atherosclerosis and discuss future therapeutic strategies.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

References

  1. Tabas I, Williams KJ, Boren J (2007) Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation 116:1832–1844

    Article  CAS  PubMed  Google Scholar 

  2. Moore KJ, Tabas I (2011) Macrophages in the pathogenesis of atherosclerosis. Cell 145:341–355

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  3. Virmani R, Burke AP, Farb A, Kolodgie FD (2006) Pathology of the vulnerable plaque. J Am Coll Cardiol 47:C13–C18

    Article  CAS  PubMed  Google Scholar 

  4. Bobryshev YV, Lord RS (1995) S-100 positive cells in human arterial intima and in atherosclerotic lesions. Cardiovasc Res 29:689–696

    CAS  PubMed  Google Scholar 

  5. Choi JH, Do Y, Cheong C, Koh H, Boscardin SB, Oh YS, Bozzacco L, Trumpfheller C, Park CG, Steinman RM (2009) Identification of antigen-presenting dendritic cells in mouse aorta and cardiac valves. J Exp Med 206:497–505

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  6. Miller JC, Brown BD, Shay T, Gautier EL, Jojic V, Cohain A, Pandey G, Leboeuf M, Elpek KG, Helft J, Hashimoto D, Chow A, Price J, Greter M, Bogunovic M, Bellemare-Pelletier A, Frenette PS, Randolph GJ, Turley SJ, Merad M (2012) Deciphering the transcriptional network of the dendritic cell lineage. Nat Immunol 13:888–899

    Article  CAS  PubMed  Google Scholar 

  7. Cheong C, Choi JH (2012) Dendritic cells and regulatory T cells in atherosclerosis. Mol Cells 34:341–347

    Article  CAS  PubMed  Google Scholar 

  8. Gerner MY, Kastenmuller W, Ifrim I, Kabat J, Germain RN (2012) Histo-cytometry: a method for highly multiplex quantitative tissue imaging analysis applied to dendritic cell subset microanatomy in lymph nodes. Immunity 37:364–376

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  9. Cho HJ, Shashkin P, Gleissner CA, Dunson D, Jain N, Lee JK, Miller Y, Ley K (2007) Induction of dendritic cell-like phenotype in macrophages during foam cell formation. Physiol Genomics 29:149–160

    Article  CAS  PubMed  Google Scholar 

  10. Yilmaz A, Lochno M, Traeg F, Cicha I, Reiss C, Stumpf C, Raaz D, Anger T, Amann K, Probst T, Ludwig J, Daniel WG, Garlichs CD (2004) Emergence of dendritic cells in rupture-prone regions of vulnerable carotid plaques. Atherosclerosis 176:101–110

    Article  CAS  PubMed  Google Scholar 

  11. Jongstra-Bilen J, Haidari M, Zhu SN, Chen M, Guha D, Cybulsky MI (2006) Low-grade chronic inflammation in regions of the normal mouse arterial intima predisposed to atherosclerosis. J Exp Med 203:2073–2083

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  12. Choi JH, Cheong C, Dandamudi DB, Park CG, Rodriguez A, Mehandru S, Velinzon K, Jung IH, Yoo JY, Oh GT, Steinman RM (2011) Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 35:819–831

    Article  CAS  PubMed  Google Scholar 

  13. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  14. Yona S, Jung S (2010) Monocytes: subsets, origins, fates and functions. Curr Opin Hematol 17:53–59

    Article  PubMed  Google Scholar 

  15. Liu P, Yu YR, Spencer JA, Johnson AE, Vallanat CT, Fong AM, Patterson C, Patel DD (2008) CX3CR1 deficiency impairs dendritic cell accumulation in arterial intima and reduces atherosclerotic burden. Arterioscler Thromb Vasc Biol 28:243–250

    Article  CAS  PubMed  Google Scholar 

  16. 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

    Article  PubMed  Google Scholar 

  17. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  18. Zhu SN, Chen M, Jongstra-Bilen J, Cybulsky MI (2009) GM-CSF regulates intimal cell proliferation in nascent atherosclerotic lesions. J Exp Med 206:2141–2149

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  19. Greter M, Helft J, Chow A, Hashimoto D, Mortha A, Agudo-Cantero J, Bogunovic M, Gautier EL, Miller J, Leboeuf M, Lu G, Aloman C, Brown BD, Pollard JW, Xiong H, Randolph GJ, Chipuk JE, Frenette PS, Merad M (2012) GM-CSF controls nonlymphoid tissue dendritic cell homeostasis but is dispensable for the differentiation of inflammatory dendritic cells. Immunity 36:1031–1046

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  20. Satpathy AT, Kc W, Albring JC, Edelson BT, Kretzer NM, Bhattacharya D, Murphy TL, Murphy KM (2012) Zbtb46 expression distinguishes classical dendritic cells and their committed progenitors from other immune lineages. J Exp Med 209:1135–1152

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  21. Meredith MM, Liu K, Darrasse-Jeze G, Kamphorst AO, Schreiber HA, Guermonprez P, Idoyaga J, Cheong C, Yao KH, Niec RE, Nussenzweig MC (2012) Expression of the zinc finger transcription factor zDC (Zbtb46, Btbd4) defines the classical dendritic cell lineage. J Exp Med 209:1153–1165

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  22. Paulson KE, Zhu SN, Chen M, Nurmohamed S, Jongstra-Bilen J, Cybulsky MI (2010) Resident intimal dendritic cells accumulate lipid and contribute to the initiation of atherosclerosis. Circ Res 106:383–390

    Article  CAS  PubMed  Google Scholar 

  23. Gautier EL, Huby T, Saint-Charles F, Ouzilleau B, Pirault J, Deswaerte V, Ginhoux F, Miller ER, Witztum JL, Chapman MJ, Lesnik P (2009) Conventional dendritic cells at the crossroads between immunity and cholesterol homeostasis in atherosclerosis. Circulation 119:2367–2375

    Article  CAS  PubMed  Google Scholar 

  24. Virginie Deswaerte TH, Flora Saint-Charles, Nicolas Proschogo, Sophie Beliard, John Pirault, Philippe Lesnik, Wendy Jessup (2012) Influence of dendritic cells on cholesterol absorption and excretion: implication in atherogenesis. Arterioscler Thromb Vasc Biol 32:A307

    Google Scholar 

  25. Spann NJ, Garmire LX, McDonald JG, Myers DS, Milne SB, Shibata N, Reichart D, Fox JN, Shaked I, Heudobler D, Raetz CR, Wang EW, Kelly SL, Sullards MC, Murphy RC, Merrill AH Jr, Brown HA, Dennis EA, Li AC, Ley K, Tsimikas S, Fahy E, Subramaniam S, Quehenberger O, Russell DW, Glass CK (2012) Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 151:138–152

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  26. Alderman CJJ, Bunyard PR, Chain BM, Foreman JC, Leake DS, Katz DR (2002) Effects of oxidised low density lipoprotein on dendritic cells: a possible immunoregulatory component of the atherogenic micro-environment? Cardiovasc Res 55:806–819

    Article  CAS  PubMed  Google Scholar 

  27. Zaguri R, Verbovetski I, Atallah M, Trahtemberg U, Krispin A, Nahari E, Leitersdorf E, Mevorach D (2007) ‘Danger’ effect of low-density lipoprotein (LDL) and oxidized LDL on human immature dendritic cells. Clin Exp Immunol 149:543–552

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  28. Nickel T, Schmauss D, Hanssen H, Sicic Z, Krebs B, Jankl S, Summo C, Fraunberger P, Walli AK, Pfeiler S, Weis M (2009) oxLDL uptake by dendritic cells induces upregulation of scavenger-receptors, maturation and differentiation. Atherosclerosis 205:442–450

    Article  CAS  PubMed  Google Scholar 

  29. Packard RR, Maganto-Garcia E, Gotsman I, Tabas I, Libby P, Lichtman AH (2008) CD11c(+) dendritic cells maintain antigen processing, presentation capabilities, and CD4(+) T-cell priming efficacy under hypercholesterolemic conditions associated with atherosclerosis. Circ Res 103:965–973

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  30. Angeli V, Llodra J, Rong JX, Satoh K, Ishii S, Shimizu T, Fisher EA, Randolph GJ (2004) Dyslipidemia associated with atherosclerotic disease systemically alters dendritic cell mobilization. Immunity 21:561–574

    Article  CAS  PubMed  Google Scholar 

  31. Trogan E, Feig JE, Dogan S, Rothblat GH, Angeli V, Tacke F, Randolph GJ, Fisher EA (2006) Gene expression changes in foam cells and the role of chemokine receptor CCR7 during atherosclerosis regression in ApoE-deficient mice. Proc Natl Acad Sci U S A 103:3781–3786

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  32. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  33. Forster R, Davalos-Misslitz AC, Rot A (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8:362–371

    Article  PubMed  Google Scholar 

  34. Feig JE, Shang Y, Rotllan N, Vengrenyuk Y, Wu C, Shamir R, Torra IP, Fernandez-Hernando C, Fisher EA, Garabedian MJ (2011) Statins promote the regression of atherosclerosis via activation of the CCR7-dependent emigration pathway in macrophages. PLoS One 6:e28534

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  35. van Gils JM, Derby MC, Fernandes LR, Ramkhelawon B, Ray TD, Rayner KJ, Parathath S, Distel E, Feig JL, Alvarez-Leite JI, Rayner AJ, McDonald TO, O’Brien KD, Stuart LM, Fisher EA, Lacy-Hulbert A, Moore KJ (2012) The neuroimmune guidance cue netrin-1 promotes atherosclerosis by inhibiting the emigration of macrophages from plaques. Nat Immunol 13:136–143

    Article  PubMed Central  PubMed  Google Scholar 

  36. Hansson GK, Hermansson A (2011) The immune system in atherosclerosis. Nat Immunol 12:204–212

    Article  CAS  PubMed  Google Scholar 

  37. Buono C, Pang H, Uchida Y, Libby P, Sharpe AH, Lichtman AH (2004) B7-1/B7-2 costimulation regulates plaque antigen-specific T-cell responses and atherogenesis in low-density lipoprotein receptor-deficient mice. Circulation 109:2009–2015

    Article  CAS  PubMed  Google Scholar 

  38. Sun J, Hartvigsen K, Chou MY, Zhang Y, Sukhova GK, Zhang J, Lopez-Ilasaca M, Diehl CJ, Yakov N, Harats D, George J, Witztum JL, Libby P, Ploegh H, Shi GP (2010) Deficiency of antigen-presenting cell invariant chain reduces atherosclerosis in mice. Circulation 122:808–820

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  39. Salomon B, Lenschow DJ, Rhee L, Ashourian N, Singh B, Sharpe A, Bluestone JA (2000) B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431–440

    Article  CAS  PubMed  Google Scholar 

  40. 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

    Article  CAS  PubMed  Google Scholar 

  41. Hou B, Reizis B, DeFranco AL (2008) Toll-like receptors activate innate and adaptive immunity by using dendritic cell-intrinsic and -extrinsic mechanisms. Immunity 29:272–282

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  42. Subramanian M, Thorp E, Hansson GK, Tabas I (2013) Treg-mediated suppression of atherosclerosis requires MYD88 signaling in DCs. J Clin Invest 123:179–188

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  43. Hansson GK, Nilsson J (2009) Vaccination against atherosclerosis? Induction of atheroprotective immunity. Semin Immunopathol 31:95–101

    Article  CAS  PubMed  Google Scholar 

  44. Paulsson G, Zhou X, Tornquist E, Hansson GK (2000) Oligoclonal T cell expansions in atherosclerotic lesions of apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 20:10–17

    Article  CAS  PubMed  Google Scholar 

  45. Erbel C, Sato K, Meyer FB, Kopecky SL, Frye RL, Goronzy JJ, Weyand CM (2007) Functional profile of activated dendritic cells in unstable atherosclerotic plaque. Basic Res Cardiol 102:123–132

    Article  CAS  PubMed  Google Scholar 

  46. Koltsova EK, Garcia Z, Chodaczek G, Landau M, McArdle S, Scott SR, von Vietinghoff S, Galkina E, Miller YI, Acton ST, Ley K (2012) Dynamic T cell-APC interactions sustain chronic inflammation in atherosclerosis. J Clin Invest 122:3114–3126

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  47. Grabner R, Lotzer K, Dopping S, Hildner M, Radke D, Beer M, Spanbroek R, Lippert B, Reardon CA, Getz GS, Fu YX, Hehlgans T, Mebius RE, van der Wall M, Kruspe D, Englert C, Lovas A, Hu D, Randolph GJ, Weih F, Habenicht AJ (2009) Lymphotoxin beta receptor signaling promotes tertiary lymphoid organogenesis in the aorta adventitia of aged ApoE−/− mice. J Exp Med 206:233–248

    Article  PubMed Central  PubMed  Google Scholar 

  48. Maganto-Garcia E, Bu DX, Tarrio ML, Alcaide P, Newton G, Griffin GK, Croce KJ, Luscinskas FW, Lichtman AH, Grabie N (2011) Foxp3+-inducible regulatory T cells suppress endothelial activation and leukocyte recruitment. J Immunol 187:3521–3529

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  49. Robertson AK, Rudling M, Zhou X, Gorelik L, Flavell RA, Hansson GK (2003) Disruption of TGF-beta signaling in T cells accelerates atherosclerosis. J Clin Invest 112:1342–1350

    CAS  PubMed Central  PubMed  Google Scholar 

  50. Gotsman I, Gupta R, Lichtman AH (2007) The influence of the regulatory T lymphocytes on atherosclerosis. Arterioscler Thromb Vasc Biol 27:2493–2495

    Article  CAS  PubMed  Google Scholar 

  51. Lin X, Chen M, Liu Y, Guo Z, He X, Brand D, Zheng SG (2013) Advances in distinguishing natural from induced Foxp3(+) regulatory T cells. Int J Clin Exp Pathol 6:116–123

    PubMed Central  PubMed  Google Scholar 

  52. Sugimoto N, Oida T, Hirota K, Nakamura K, Nomura T, Uchiyama T, Sakaguchi S (2006) Foxp3-dependent and -independent molecules specific for CD25+CD4+ natural regulatory T cells revealed by DNA microarray analysis. Int Immunol 18:1197–1209

    Article  CAS  PubMed  Google Scholar 

  53. Weiss JM, Bilate AM, Gobert M, Ding Y, Curotto de Lafaille MA, Parkhurst CN, Xiong H, Dolpady J, Frey AB, Ruocco MG, Yang Y, Floess S, Huehn J, Oh S, Li MO, Niec RE, Rudensky AY, Dustin ML, Littman DR, Lafaille JJ (2012) Neuropilin 1 is expressed on thymus-derived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J Exp Med 209(1723–42):S1

    Google Scholar 

  54. Bour-Jordan H, Bluestone JA (2009) Regulating the regulators: costimulatory signals control the homeostasis and function of regulatory T cells. Immunol Rev 229:41–66

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  55. Coombes JL, Siddiqui KR, Arancibia-Carcamo CV, Hall J, Sun CM, Belkaid Y, Powrie F (2007) A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204:1757–1764

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  56. Beaty SR, Rose CE Jr, Sung SS (2007) Diverse and potent chemokine production by lung CD11bhigh dendritic cells in homeostasis and in allergic lung inflammation. J Immunol 178:1882–1895

    CAS  PubMed  Google Scholar 

  57. Niessner A, Sato K, Chaikof EL, Colmegna I, Goronzy JJ, Weyand CM (2006) Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-alpha. Circulation 114:2482–2489

    Article  CAS  PubMed  Google Scholar 

  58. Goossens P, Gijbels MJ, Zernecke A, Eijgelaar W, Vergouwe MN, van der Made I, Vanderlocht J, Beckers L, Buurman WA, Daemen MJ, Kalinke U, Weber C, Lutgens E, de Winther MP (2010) Myeloid type I interferon signaling promotes atherosclerosis by stimulating macrophage recruitment to lesions. Cell Metab 12:142–153

    Article  CAS  PubMed  Google Scholar 

  59. Niessner A, Shin MS, Pryshchep O, Goronzy JJ, Chaikof EL, Weyand CM (2007) Synergistic proinflammatory effects of the antiviral cytokine interferon-alpha and Toll-like receptor 4 ligands in the atherosclerotic plaque. Circulation 116:2043–2052

    Article  CAS  PubMed  Google Scholar 

  60. 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

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  61. Heath WR, Carbone FR (2001) Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 1:126–134

    Article  CAS  PubMed  Google Scholar 

  62. Tabas I (2010) Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 10:36–46

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  63. Thorp E, Cui D, Schrijvers DM, Kuriakose G, Tabas I (2008) Mertk receptor mutation reduces efferocytosis efficiency and promotes apoptotic cell accumulation and plaque necrosis in atherosclerotic lesions of apoe−/− mice. Arterioscler Thromb Vasc Biol 28:1421–1428

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  64. Ait-Oufella H, Pouresmail V, Simon T, Blanc-Brude O, Kinugawa K, Merval R, Offenstadt G, Leseche G, Cohen PL, Tedgui A, Mallat Z (2008) Defective mer receptor tyrosine kinase signaling in bone marrow cells promotes apoptotic cell accumulation and accelerates atherosclerosis. Arterioscler Thromb Vasc Biol 28:1429–1431

    Article  CAS  PubMed  Google Scholar 

  65. Yancey PG, Blakemore J, Ding L, Fan D, Overton CD, Zhang Y, Linton MF, Fazio S (2010) Macrophage LRP-1 controls plaque cellularity by regulating efferocytosis and Akt activation. Arterioscler Thromb Vasc Biol 30:787–795

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  66. Ait-Oufella H, Kinugawa K, Zoll J, Simon T, Boddaert J, Heeneman S, Blanc-Brude O, Barateau V, Potteaux S, Merval R, Esposito B, Teissier E, Daemen MJ, Leseche G, Boulanger C, Tedgui A, Mallat Z (2007) Lactadherin deficiency leads to apoptotic cell accumulation and accelerated atherosclerosis in mice. Circulation 115:2168–2177

    Article  CAS  PubMed  Google Scholar 

  67. Albert ML, Pearce SF, Francisco LM, Sauter B, Roy P, Silverstein RL, Bhardwaj N (1998) Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 188:1359–1368

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  68. Seitz HM, Camenisch TD, Lemke G, Earp HS, Matsushima GK (2007) Macrophages and dendritic cells use different Axl/Mertk/Tyro3 receptors in clearance of apoptotic cells. J Immunol 178:5635–5642

    CAS  PubMed  Google Scholar 

  69. Thorp E, Tabas I (2009) Mechanisms and consequences of efferocytosis in advanced atherosclerosis. J Leukoc Biol 86:1089–1095

    Article  CAS  PubMed  Google Scholar 

  70. Ameli S, Hultgardh-Nilsson A, Regnstrom J, Calara F, Yano J, Cercek B, Shah PK, Nilsson J (1996) Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol 16:1074–1079

    Article  CAS  PubMed  Google Scholar 

  71. Habets KL, van Puijvelde GH, van Duivenvoorde LM, van Wanrooij EJ, de Vos P, Tervaert JW, van Berkel TJ, Toes RE, Kuiper J (2010) Vaccination using oxidized low-density lipoprotein-pulsed dendritic cells reduces atherosclerosis in LDL receptor-deficient mice. Cardiovasc Res 85:622–630

    Article  CAS  PubMed  Google Scholar 

  72. Palinski W, Miller E, Witztum JL (1995) Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc Natl Acad Sci U S A 92:821–825

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  73. Hermansson A, Johansson DK, Ketelhuth DF, Andersson J, Zhou X, Hansson GK (2011) Immunotherapy with tolerogenic apolipoprotein B-100-loaded dendritic cells attenuates atherosclerosis in hypercholesterolemic mice. Circulation 123:1083–1091

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

I.T. is supported by National Institutes of Health grants HL106019, HL075662, and HL054591.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Manikandan Subramanian.

Additional information

This article is a contribution to the special issue on Metabolic Syndrome - Guest Editor: T. Miyazaki

Rights and permissions

Reprints and permissions

About this article

Cite this article

Subramanian, M., Tabas, I. Dendritic cells in atherosclerosis. Semin Immunopathol 36, 93–102 (2014). https://doi.org/10.1007/s00281-013-0400-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00281-013-0400-x

Keywords

Navigation