Dendritic cells in atherosclerosis

Seminars in Immunopathology

Volumn 36, Issue 1, 2014, Pages 93-102

  Subramanian, Manikandan ^a   Tabas, Ira ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

Atherosclerosis; Dendritic cells; Efferocytosis; Tregs

Indexed keywords

DENDRITIC CELL VACCINE;

ANTIGEN PRESENTATION; ANTIGEN SPECIFICITY; ARTERY WALL; ATHEROSCLEROSIS; BLOOD VESSEL WALL; CELL FUNCTION; CELL MATURATION; DENDRITIC CELL; HOMEOSTASIS; HUMAN; HUMORAL IMMUNITY; IMMUNOMODULATION; IMMUNOPATHOGENESIS; LIPID METABOLISM; LIPID TRANSPORT; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; TREATMENT PLANNING; VACCINATION;

ANIMALS; ATHEROSCLEROSIS; BLOOD VESSELS; DENDRITIC CELLS; HUMANS;

EID: 84895863576     PISSN: 18632297     EISSN: 18632300     Source Type: Journal    
DOI: 10.1007/s00281-013-0400-x     Document Type: Review

References (73)

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 (Pubitemid 350287108)
2. Moore KJ, Tabas I (2011) Macrophages in the pathogenesis of atherosclerosis. Cell 145:341-355
3. Virmani R, Burke AP, Farb A, Kolodgie FD (2006) Pathology of the vulnerable plaque. J Am Coll Cardiol 47:C13-C18
4. Bobryshev YV, Lord RS (1995) S-100 positive cells in human arterial intima and in atherosclerotic lesions. Cardiovasc Res 29:689-696
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
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
7. Cheong C, Choi JH (2012) Dendritic cells and regulatory T cells in atherosclerosis. Mol Cells 34:341-347
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
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 (Pubitemid 46701996)
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 (Pubitemid 39078651)
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 (Pubitemid 44352229)
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
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 (Pubitemid 46048465)
14. Yona S, Jung S (2010) Monocytes: subsets, origins, fates and functions. Curr Opin Hematol 17:53-59
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 (Pubitemid 351161195)
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
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
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
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
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
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
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
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
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
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 integratesmacrophage lipid metabolism and inflammatory responses. Cell 151:138-152
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
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 (Pubitemid 47256159)
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
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
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 (Pubitemid 39370511)
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 (Pubitemid 43376632)
32. -/- mice during disease regression. J Clin Invest 121:2025-2036
33. Forster R, Davalos-Misslitz AC, Rot A (2008) CCR7 and its ligands: balancing immunity and tolerance. Nat Rev Immunol 8:362-371 (Pubitemid 351595218)
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
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
36. Hansson GK, Hermansson A (2011) The immune system in atherosclerosis. Nat Immunol 12:204-212
37. Buono C, Pang H, Uchida Y, Libby P, Sharpe AH, Lichtman AH (2004) B7-1/B7-2 costimulation regulates plaque antigen-specific Tcell responses and atherogenesis in low-density lipoprotein receptor-deficient mice. Circulation 109:2009-2015 (Pubitemid 38544492)
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
39. + immunoregulatory T cells that control autoimmune diabetes. Immunity 12:431-440
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 (Pubitemid 43214743)
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
42. Subramanian M, Thorp E, Hansson GK, Tabas I (2013) Tregmediated suppression of atherosclerosis requires MYD88 signaling in DCs. J Clin Invest 123:179-188
43. Hansson GK, Nilsson J (2009) Vaccination against atherosclerosis? Induction of atheroprotective immunity. Semin Immunopathol 31:95-101
44. Paulsson G, Zhou X, Tornquist E, Hansson GK (2000) Oligoclonal T cell expansions in atherosclerotic lesions of apolipoprotein Edeficient mice. Arterioscler Thromb Vasc Biol 20:10-17 (Pubitemid 30048341)
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 (Pubitemid 46189953)
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
47. -/- mice. J Exp Med 206:233-248
48. +- inducible regulatory T cells suppress endothelial activation and leukocyte recruitment. J Immunol 187:3521-3529
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 (Pubitemid 38057688)
50. Gotsman I, Gupta R, Lichtman AH (2007) The influence of the regulatory T lymphocytes on atherosclerosis. Arterioscler Thromb Vasc Biol 27:2493-2495 (Pubitemid 350158897)
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
52. + natural regulatory T cells revealed by DNA microarray analysis. Int Immunol 18:1197-1209
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 thymusderived natural regulatory T cells, but not mucosa-generated induced Foxp3+ T reg cells. J Exp Med 209(1723-42):S1
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
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 Tcells via a TGF-beta and retinoic acid-dependent mechanism. J Exp Med 204:1757-1764 (Pubitemid 47236314)
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 (Pubitemid 46154661)
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 (Pubitemid 44901521)
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
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 (Pubitemid 350023750)
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
61. Heath WR, Carbone FR (2001) Cross-presentation in viral immunity and self-tolerance. Nat Rev Immunol 1:126-134 (Pubitemid 33741966)
62. Tabas I (2010) Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 10:36-46
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
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
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
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 (Pubitemid 46659069)
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 (Pubitemid 28478024)
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 (Pubitemid 46674359)
69. Thorp E, Tabas I (2009) Mechanisms and consequences of efferocytosis in advanced atherosclerosis. J Leukoc Biol 86:1089-1095
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 (Pubitemid 26266910)
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
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
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