Dendritic cells and regulatory T cells in atherosclerosis

Molecules and Cells

Volumn 34, Issue 4, 2012, Pages 341-347

  Cheong, Cheolho ^a   Choi, Jae Hoon ^b  

^a CLIN RESEARCH INSTITUTE OF MONTREAL   (Canada)

^b Hanyang University   (South Korea)

Author keywords

Atherosclerosis; Dendritic cell; Regulatory T cell

Indexed keywords

AORTA; AORTA ATHEROSCLEROSIS; ATHEROSCLEROSIS; CELL STIMULATION; CELL TYPE; DENDRITIC CELL; HUMAN; IMMUNOSTIMULATION; MACROPHAGE; NONHUMAN; REGULATORY T LYMPHOCYTE; REVIEW;

ANIMALS; AORTA; ATHEROSCLEROSIS; DENDRITIC CELLS; DISEASE MODELS, ANIMAL; HUMANS; MODELS, CARDIOVASCULAR; T-LYMPHOCYTES, REGULATORY;

MUS;

EID: 84870377818     PISSN: 10168478     EISSN: 02191032     Source Type: Journal    
DOI: 10.1007/s10059-012-0128-9     Document Type: Review

References (62)

1. Ait-Oufella, H., Salomon, B.L., Potteaux, S., Robertson, A.K., Gourdy, P., Zoll, J., Merval, R., Esposito, B., Cohen, J.L., Fisson, S., et al. (2006). Natural regulatory T cells control the development of atherosclerosis in mice. Nat. Med. 12, 178-180.
2. Angeli, V., Llodra, J., Rong, J.X., Satoh, K., Ishii, S., Shimizu, T., Fisher, E.A., and Randolph, G.J. (2004). Dyslipidemia associated with atherosclerotic disease systemically alters den-dritic cell mobilization. Immunity 21, 561-574.
3. Blasius, A.L., Cella, M., Maldonado, J., Takai, T., and Colonna, M. (2006). Siglec-H is an IPC-specific receptor that modu-lates type I IFN secretion through DAP12. Blood 107, 2474-2476.
4. Bobryshev, Y.V., and Lord R.S. (1995). S-100 positive cells in human arterial intima and in atherosclerotic lesions. Car-diovasc. Res. 29, 689-696.
5. Bobryshev, Y.V., and Lord, R.S. (1998). Mapping of vascular dendritic cells in atherosclerotic arteries suggests their involvement in local immune-inflammatory reactions. Car-diovasc. Res. 37, 799-810.
6. Bobryshev, Y.V., and Lord, R.S. (2002). Expression of heat shock protein-70 by dendritic cells in the arterial intima and its potential significance in atherogenesis. J. Vasc. Surg. 35, 368-375.
7. Bobryshev, Y.V., Babaev, V.R., Lord, R.S., and Watanabe, T. (1999). Ultrastructural identification of cells with dendritic cell appearance in atherosclerotic aorta of apolipoprotein E deficient mice. J. Submicrosc. Cytol. Pathol. 31, 527-531.
8. Bobryshev, Y.V., Ikezawa, T., and Watanabe, T. (1997). Forma-tion of Birbeck granule-like structures in vascular dendritic cells in human atherosclerotic aorta. Lag-antibody to epi-dermal Langerhans cells recognizes cells in the aortic wall. Atherosclerosis 133, 193-202.
9. Bobryshev, Y.V., Taksir, T., Lord, R.S., and Freeman, M.W. (2001). Evidence that dendritic cells infiltrate atherosclerotic lesions in apolipoprotein E-deficient mice. Histol. Histopathol. 16, 801-808.
10. Cao, W., Bobryshev, Y.V., Lord, R.S., Oakley, R.E., Lee, S.H., and Lu, J. (2003). Dendritic cells in the arterial wall express C1q: Potential significance in atherogenesis. Cardiovasc. Res. 60, 175-186.
11. Choi, J.H., Do, Y., Cheong, C., Koh, H., Boscardin, S.B., Oh, Y.S., Bozzacco, L., Trumpfheller, C., Park, C.G., and Stein-man, R.M. (2009). Identification of antigen-presenting den-dritic cells in mouse aorta and cardiac valves. J. Exp. Med. 206, 497-505.
12. Choi, J.H., Cheong, C., Dandamudi, D.B., Park, C.G., Rodri-guez, A., Mehandru, S., Velinzon, K., Jung, I.H., Yoo, J.Y., Oh, G.T., et al. (2011). Flt3 signaling-dependent dendritic cells protect against atherosclerosis. Immunity 35, 819-831.
13. Daissormont, I.T., Christ, A., Temmerman, L., Sampedro, Mil-lares, S., Seijkens, T., Manca, M., Rousch, M., Poggi, M., Boon, L., van der Loos, C., et al. (2011). Plasmacytoid den-dritic cells protect against atherosclerosis by tuning T-cell proliferation and activity. Circ. Res. 109, 1387-1395.
14. Doring, Y., Manthey, H.D., Drechsler, M., Lievens, D., Megens, R.T., Soehnlein, O., Busch, M., Manca, M., Koenen, R.R., Pelisek, J., et al. (2012). Auto-antigenic protein-DNA com-plexes stimulate plasmacytoid dendritic cells to promote atherosclerosis. Circulation 125, 1673-1683.
15. Galkina, E., Kadl, A., Sanders, J., Varughese, D., Sarembock, I.J., and Ley, K. (2006). Lymphocyte recruitment into the aortic wall before and during development of atherosclerosis is partially Lselectin dependent. J. Exp. Med. 203, 1273-1282.
16. Gautier, E.L., Huby, T., Saint-Charles, F., Ouzilleau, B., Pirault, J., Deswaerte, V., Ginhoux, F., Miller, E.R., Witztum, J.L., Chapman, M.J., et al. (2009). Conventional dendritic cells at the crossroads between immunity and cholesterol home-ostasis in atherosclerosis. Circulation 119, 2367-2375.
17. Geissmann, F., Gordon, S., Hume, D.A., Mowat, A.M., and Randolph, G.J. (2010). Unravelling mononuclear phagocyte heterogeneity. Nat. Rev. Immunol. 10, 453-460.
18. Ginhoux, F., Tacke, F., Angeli, V., Bogunovic, M., Loubeau, M., Dai, X.M., Stanley, E.R., Randolph, G.J., and Merad, M. (2006). Langerhans cells arise from monocytes in vivo. Nat. Immunol. 7, 265-273.
19. Gotsman, I., Grabie, N., Gupta, R., Dacosta, R., MacConmara, M., Lederer, J., Sukhova, G., Witztum, J.L., Sharpe, A.H., and Lichtman, A.H. (2006). Impaired regulatory T-cell res-ponse and enhanced atherosclerosis in the absence of inducible costimulatory molecule. Circulation 114, 2047-2055.
20. Habets, K.L., van Puijvelde, G.H., van Duivenvoorde, L.M., van Wanrooij, E.J., de Vos, P., Tervaert, J.W., van Berkel, T.J., Toes, R.E., and Kuiper, J. (2010). Vaccination using oxidized lowdensity lipoprotein-pulsed dendritic cells reduces athe-rosclerosis in LDL receptor-deficient mice. Cardiovasc. Res. 85, 622-630.
21. Hansson, G.K., and Hermansson, A. (2011). The immune system in atherosclerosis. Nat. Immunol. 12, 204-212.
22. Hawiger, D., Inaba, K., Dorsett, Y., Guo, M., Mahnke, K., Ri-vera, M., Ravetch, J.V., Steinman, R.M., and Nussenzweig, M.C. (2001). Dendritic cells induce peripheral T cell unres-ponsiveness under steady state conditions in vivo. J. Exp. Med. 194, 769-780.
23. Hermansson, A., Johansson, D.K., Ketelhuth, D.F., Andersson, J., Zhou, X., and Hansson, G.K. (2011). Immunotherapy with tolerogenic apolipoprotein B-100-loaded dendritic cells atte-nuates atherosclerosis in hypercholesterolemic mice. Circu-lation 123, 1083-1091.
24. Houtkamp, M.A., de Boer, O.J., van der Loos, C.M., van der Wal, A.C., and Becker, A.E. (2001). Adventitial infiltrates associated with advanced atherosclerotic plaques: Structural organization suggests generation of local humoral immune responses. J. Pathol. 193, 263-269.
25. Inder, S.J., Bobryshev, Y.V., Cherian, S.M., Lord, R.S., Masuda, K., and Yutani, C. (2000). Accumulation of lymphocytes, dendritic cells, and granulocytes in the aortic wall affected by Takayasu's disease. Angiology 51, 565-579.
26. Jongstra-Bilen, J., Haidari, M., Zhu, S.N., Chen, M., Guha, D., and Cybulsky, M.I. (2006). Low-grade chronic inflammation in regions of the normal mouse arterial intima predisposed to atherosclerosis. J. Exp. Med. 203, 2073-2084.
27. Josefowicz, S.Z., Lu, L.F., and Rudensky, A.Y. (2012). Regula-tory T cells: Mechanisms of differentiation and function. Annu. Rev. Immunol. 30, 531-564.
28. Kretschmer, K., Apostolou, I., Hawiger, D., Khazaie, K., Nussenzweig, M.C., and von Boehmer, H. (2005). Inducing and expanding regulatory T cell populations by foreign antigen. Nat. Immunol. 6, 1219-1227.
29. Liu, P., Yu, Y.R., Spencer, J.A., Johnson, A.E., Vallanat, C.T., Fong, A.M., Patterson, C., and Patel, D.D. (2008). CX3CR1 deficiency impairs dendritic cell accumulation in arterial intima and reduces atherosclerotic burden. Arterioscler. Thromb. Vasc. Biol. 28, 243-250.
30. Ludewig, B., Freigang, S., Jaggi, M., Kurrer, M.O., Pei, Y.C., Vlk, L., Odermatt, B., Zinkernagel, R.M., and Hengartner, H. (2000). Linking immune-mediated arterial inflammation and cholesterolinduced atherosclerosis in a transgenic mouse model. Proc. Natl. Acad. Sci. USA 97, 12752-12757.
31. Maganto-Garcia, E., Tarrio, M.L., Grabie, N., Bu, D.X., and Lichtman, A.H. (2011). Dynamic changes in regulatory T cells are linked to levels of diet-induced hypercholestero-lemia. Circulation 124, 185-195.
32. McKenna, H.J., Stocking, K.L., Miller, R.E., Brasel, K., De Smedt, T., Maraskovsky, E., Maliszewski, C.R., Lynch, D.H., Smith, J., Pulendran, B., et al. (2000). Mice lacking flt3 ligand have deficient hematopoiesis affecting hematopoietic pro-genitor cells, dendritic cells, and natural killer cells. Blood 95, 3489-3497.
33. Millonig, G., Niederegger, H., Rabl, W., Hochleitner, B.W., Hoefer, D., Romani, N., and Wick, G. (2001). Network of vascular-associated dendritic cells in intima of healthy young individuals. Arterioscler. Thromb. Vasc. Biol. 21, 503-508.
34. Millonig, G., Malcom, G.T., and Wick, G. (2002). Early inflam-matoryimmunological lesions in juvenile atherosclerosis from the pathobiological determinants of atherosclerosis in Youth (PDAY)-study. Atherosclerosis 160, 441-448.
35. Moos, M.P., John, N., Grabner, R., Nossmann, S., Gunther, B., Vollandt, R., Funk, C.D., Kaiser, B., and Habenicht, A.J. (2005). The lamina adventitia is the major site of immune cell accumulation in standard chow-fed apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 25, 2386-23891.
36. Mor, A., Planer, D., Luboshits, G., Afek, A., Metzger, S., Chajek-Shaul, T., Keren, G., and George, J. (2007). Role of naturally occurring CD4+ CD25+ regulatory T cells in experimental atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 27, 893-900.
37. Niessner, A., Sato, K., Chaikof, E.L., Colmegna, I., Goronzy, J.J., and Weyand, C.M. (2006). Pathogen-sensing plasma-cytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-alpha. Circulation 114, 2482-2489.
38. Ozmen, J., Bobryshev, Y.V., Lord, R.S., and Ashwell, K.W. (2002). Identification of dendritic cells in aortic atheroscle-rotic lesions in rats with diet-induced hypercholesterolaemia. Histol. Histopathol. 17, 223-237.
39. Packard, R.R., Maganto-Garcia, E., Gotsman, I., Tabas, I., Libby, P., and Lichtman, A.H. (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.
40. Pryshchep, O., Ma-Krupa, W., Younge, B.R., Goronzy, J.J., and Weyand, C.M. (2008). Vessel-specific Toll-like receptor profiles in human medium and large arteries. Circulation 118, 1276-1284.
41. Sasaki, N., Yamashita, T., Takeda, M., Shinohara, M., Naka-jima, K., Tawa, H., Usui, T., and Hirata, K. (2009). Oral anti-CD3 antibody treatment induces regulatory T cells and inhibits the development of atherosclerosis in mice. Circu-lation 120, 1996-2005.
42. Shamshiev, A.T., Ampenberger, F., Ernst, B., Rohrer, L., Marsland, B.J., and Kopf, M. (2007). Dyslipidemia inhibits Toll-like receptorinduced activation of CD8a-negative den-dritic cells and protective Th1 type immunity. J. Exp. Med. 204, 441-452.
43. Shaposhnik, Z., Wang, X., Weinstein, M., Bennett, B.J., and Lusis, A.J. (2007). Granulocyte macrophage colony-stimula-ting factor regulates dendritic cell content of atherosclerotic lesions. Arterioscler. Thromb. Vasc. Biol. 27, 621-627.
44. Soilleux, E.J., Morris, L.S., Trowsdale, J., Coleman, N., and Boyle, J.J. (2002). Human atherosclerotic plaques express DC-SIGN, a novel protein found on dendritic cells and macrophages. J. Pathol. 198, 511-516.
45. Spanbroek, R., Grabner, R., Lotzer, K., Hildner, M., Urbach, A., Ruhling, K., Moos, M.P., Kaiser, B., Cohnert, T.U., Wahlers, T., et al. (2003). Expanding expression of the 5-lipoxyge-nase pathway within the arterial wall during human athero-genesis. Proc. Natl. Acad. Sci. USA 100, 1238-1243.
46. Steinman, R.M. (2012). Decisions about dendritic cells: Past, present, and future. Annu. Rev. Immunol. 30, 1-22.
47. Steinman, R.M., and Cohn, Z.A. (1973). Identification of a novel cell type in peripheral lymphoid organs of mice. I. Morpho-logy, quantitation, tissue distribution. J. Exp. Med. 137, 1142-1162.
48. Steinman, R.M., and Cohn, Z.A. (1974). Identification of a novel cell type in peripheral lymphoid organs of mice. II. Functional properties in vitro. J. Exp. Med. 139, 380-397.
49. Steinman, R.M., and Nussenzweig, M.C. (2002). Avoiding horror autotoxicus: The importance of dendritic cells in peri-pheral T cell tolerance. Proc. Natl. Acad. Sci. USA 99, 351-358.
50. Steinman, R.M., and Witmer, M.D. (1978). Lymphoid dendritic cells are potent stimulators of the primary mixed leukocyte reaction in mice. Proc. Natl. Acad. Sci. USA 75, 5132-5136.
51. Swiecki, M., Gilfillan, S., Vermi, W., Wang, Y., and Colonna, M. (2010). Plasmacytoid dendritic cell ablation impacts early interferon responses and antiviral NK and CD8+ T cell accrual. Immunity 33, 955-966.
52. Takagi, H., Fukaya, T., Eizumi, K., Sato, Y., Sato, K., Shibazaki, A., Otsuka, H., Hijikata, A., Watanabe, T., Ohara, O., et al. (2011). Plasmacytoid dendritic cells are crucial for the initia-tion of inflammation and T cell immunity in vivo. Immunity 35, 958-971.
53. Takeda, M., Yamashita, T., Sasaki, N., Nakajima, K., Kita, T., Shinohara, M., Ishida, T., and Hirata, K. (2010). Oral admi-nistration of an active form of vitamin D3 (calcitriol) decrea-ses atherosclerosis in mice by inducing regulatory T cells and immature dendritic cells with tolerogenic functions. Arterioscler. Thromb. Vasc. Biol. 30, 2495-2503.
54. Van Vre, E.A., Bosmans, J.M., Van Brussel, I., Maris, M., De Meyer, G.R., Van Schil, P.E., Vrints, C.J., and Bult, H. (2011). Immunohistochemical characterisation of dendritic cells in human atherosclerotic lesions: Possible pitfalls. Pathology 43, 239-247.
55. Waskow, C., Liu, K., Darrasse-Jeze, G., Guermonprez, P., Ginhoux, F., Merad, M., Shengelia, T., Yao, K., and Nussen-zweig, M. (2008). The receptor tyrosine kinase Flt3 is required for dendritic cell development in peripheral lymphoid tissues. Nat. Immunol. 9, 676-683.
56. Weber, C., Zernecke, A., and Libby, P. (2008). The multifa-ceted contributions of leukocyte subsets to atherosclerosis: Lessons from mouse models. Nat. Rev. Immunol. 8, 802-815.
57. Weber, C., Meiler, S., Doring, Y., Koch, M., Drechsler, M., Megens, R.T., Rowinska, Z., Bidzhekov, K., Fecher, C., Ribechini, E., et al. (2011). CCL17-expressing dendritic cells drive atherosclerosis by restraining regulatory T cell home-ostasis in mice. J. Clin. Invest. 121, 2898-2910.
58. Weyand, C.M., Ma-Krupa, W., Pryshchep, O., Groschel, S., Bernardino, R., and Goronzy, J.J. (2005). Vascular dendritic cells in giant cell arteritis. Ann. N.Y. Acad. Sci. 1062, 195-208.
59. Witmer-Pack, M.D., Crowley, M.T., Inaba, K., and Steinman, R.M. (1993). Macrophages, but not dendritic cells, accumu-late colloidal carbon following administration in situ. J. Cell Sci. 105, 965-973.
60. Yilmaz, A., Lochno, M., Traeg, F., Cicha, I., Reiss, C., Stumpf, C., Raaz, D., Anger, T., Amann, K., Probst, T., et al. (2004). Emergence of dendritic cells in rupture-prone regions of vulnerable carotid plaques. Atherosclerosis 176, 101-110.
61. Zhang, J., Raper, A., Sugita, N., Hingorani, R., Salio, M., Palmowski, M.J., Cerundolo, V., and Crocker, P.R. (2006). Characterization of Siglec-H as a novel endocytic receptor expressed on murine plasmacytoid dendritic cell precursors. Blood 107, 3600-3608.
62. Zhu, S.N., Chen, M., Jongstra-Bilen, J., and Cybulsky, M.I. (2009). GM-CSF regulates intimal cell proliferation in na-scent atherosclerotic lesions. J. Exp. Med. 206, 2141-2149.