Vaccination to modulate atherosclerosis

Autoimmunity

Volumn 48, Issue 3, 2015, Pages 152-160

  Kimura, Takayuki ^a   Tse, Kevin ^a   Sette, Alessandro ^a   Ley, Klaus ^a  

^a LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

Author keywords

Apolipoprotein B 100; Atherosclerosis; Heat shock protein 65; Immunization; Low density lipoprotein

Indexed keywords

APOLIPOPROTEIN B100; CHAPERONIN 60; HEAT SHOCK PROTEIN 65; MAJOR HISTOCOMPATIBILITY ANTIGEN CLASS 2; OXIDIZED LOW DENSITY LIPOPROTEIN; ANTIBODY; AUTOANTIGEN; HEAT SHOCK PROTEIN; HEAT-SHOCK PROTEIN 65, HUMAN; LOW DENSITY LIPOPROTEIN; PEPTIDE; VACCINE;

ADAPTIVE IMMUNITY; ANTIGEN RECOGNITION; ARTICLE; ATHEROSCLEROSIS; HUMAN; HUMORAL IMMUNITY; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; MUCOSAL IMMUNITY; T LYMPHOCYTE; VACCINATION; ANIMAL; ANTAGONISTS AND INHIBITORS; ARTERY; DRUG EFFECTS; GENE EXPRESSION; GENETICS; IMMUNOLOGY; MOUSE; PATHOLOGY; PLAQUE, ATHEROSCLEROTIC;

ADAPTIVE IMMUNITY; ANIMALS; ANTIBODIES; APOLIPOPROTEIN B-100; ARTERIES; ATHEROSCLEROSIS; AUTOANTIGENS; GENE EXPRESSION; HEAT-SHOCK PROTEINS; HUMANS; IMMUNITY, HUMORAL; LIPOPROTEINS, LDL; MICE; PEPTIDES; PLAQUE, ATHEROSCLEROTIC; VACCINATION; VACCINES;

EID: 84928598816     PISSN: 08916934     EISSN: 1607842X     Source Type: Journal    
DOI: 10.3109/08916934.2014.1003641     Document Type: Article

References (119)

1. Witztum, J. L., and A. H. Lichtman. 2014. The influence of innate and adaptive immune responses on atherosclerosis. Annu. Rev. Pathol. 9: 73-102.
2. Ait-Oufella, H., A. P. Sage, Z. Mallat, and A. Tedgui. 2014. Adaptive (T and B cells) immunity and control by dendritic cells in atherosclerosis. Circ. Res. 114: 1640-1660.
3. Lichtman, A. H., C. J. Binder, S. Tsimikas, and J. L. Witztum. 2013. Adaptive immunity in atherogenesis: new insights and therapeutic approaches. J. Clin. Invest. 123: 27-36.
4. Hansson, G. K., and A. Hermansson. 2011. The immune system in atherosclerosis. Nat. Immunol. 12: 204-212.
5. Libby, P., P. M. Ridker, and G. K. Hansson. 2011. Progress and challenges in translating the biology of atherosclerosis. Nature. 473: 317-325.
6. Tse, K., H. Tse, J. Sidney, et al. 2013. T cells in atherosclerosis. Int. Immunol. 25: 615-622.
7. Koltsova, E. K., and K. Ley. 2011. How dendritic cells shape atherosclerosis. Trends Immunol. 32: 540-547.
8. Ley, K., Y. I. Miller, and C. C. Hedrick. 2011. Monocyte and macrophage dynamics during atherogenesis. Arterioscler. Thromb. Vasc. Biol. 31: 1506-1516.
9. Koltsova, E. K., C. C. Hedrick, and K. Ley. 2013. Myeloid cells in atherosclerosis: a delicate balance of anti-inflammatory and proinflammatory mechanisms. Curr. Opin. Lipidol. 24: 371-380.
10. Andersson, J., P. Libby, and G. K. Hansson. 2010. Adaptive immunity and atherosclerosis. Clin. Immunol. 134: 33-46.
11. Ketelhuth, D. F., and G. K. Hansson. 2011. Cellular immunity, lowdensity lipoprotein and atherosclerosis: break of tolerance in the artery wall. Thromb. Haemost. 106: 779-786.
12. Shimada, K. 2009. Immune system and atherosclerotic disease: heterogeneity of leukocyte subsets participating in the pathogenesis of atherosclerosis. Circ. J. 73: 994-1001.
13. Steinberg, D., and J. L. Witztum. 2010. Oxidized low-density lipoprotein and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 30: 2311-2316.
14. Fredrikson, G. N., B. Hedblad, G. Berglund, et al. 2003. Identification of immune responses against aldehyde-modified peptide sequences in apoB associated with cardiovascular disease. Arterioscler. Thromb. Vasc. Biol. 23: 872-878.
15. Nilsson, J., G. N. Fredrikson, H. Bjorkbacka, et al. 2009. Vaccines modulating lipoprotein autoimmunity as a possible future therapy for cardiovascular disease. J. Intern. Med. 266: 221-231.
16. Wick, G., B. Jakic, M. Buszko, et al. 2014. The role of heat shock proteins in atherosclerosis. Nat. Rev. Cardiol. 11: 516-529.
17. Fifth Joint Task Force of the European Society of, C., E. European Association of, I. European Association of Percutaneous Cardiovascular, A. European Heart Rhythm, A. Heart Failure, P. European Association for Cardiovascular, Rehabilitation, S. European Atherosclerosis, M. International Society of Behavioural, O. European Stroke, H. European Society of, D. European Association for the Study of, M. European Society of General Practice/Family, E. International Diabetes Federation, and N. European Heart. 2012. European Guidelines on cardiovascular disease prevention in clinical practice (version 2012): the Fifth Joint Task Force of the European Society of Cardiology and Other Societies on Cardiovascular Disease Prevention in Clinical Practice (constituted by representatives of nine societies and by invited experts). Eur. J. Prev. Cardiol. 19: 585-667.
18. Grundtman, C., S. B. Kreutmayer, G. Almanzar, et al. 2011. Heat shock protein 60 and immune inflammatory responses in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 31: 960-968.
19. Gounopoulos, P., E. Merki, L. F. Hansen, et al. 2007. Antibodies to oxidized low density lipoprotein: epidemiological studies and potential clinical applications in cardiovascular disease. Minerva Cardioangiol. 55: 821-837.
20. Ravandi, A., S. M. Boekholdt, Z. Mallat, et al. 2011. Relationship of IgG and IgM autoantibodies and immune complexes to oxidized LDL with markers of oxidation and inflammation and cardiovascular events: results from the EPIC-Norfolk Study. J. Lipid Res. 52: 1829-1836.
21. Song, L., C. Leung, and C. Schindler. 2001. Lymphocytes are important in early atherosclerosis. J. Clin. Invest. 108: 251-259.
22. Zhou, X., A. Nicoletti, R. Elhage, and G. K. Hansson. 2000. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 102: 2919-2922.
23. Kahlenberg, J. M., and M. J. Kaplan. 2013. Mechanisms of premature atherosclerosis in rheumatoid arthritis and lupus. Annu. Rev. Med. 64: 249-263.
24. Karvonen, J., M. Paivansalo, Y. A. Kesaniemi, and S. Horkko. 2003. Immunoglobulin M type of autoantibodies to oxidized lowdensity lipoprotein has an inverse relation to carotid artery atherosclerosis. Circulation 108: 2107-2112.
25. Tsimikas, S., E. S. Brilakis, R. J. Lennon, et al. 2007. Relationship of IgG and IgM autoantibodies to oxidized low density lipoprotein with coronary artery disease and cardiovascular events. J. Lipid Res. 48: 425-433.
26. Hulthe, J., L. Bokemark, and B. Fagerberg. 2001. Antibodies to oxidized LDL in relation to intima-media thickness in carotid and femoral arteries in 58-year-old subjectively clinically healthy men. Arterioscler. Thromb. Vasc. Biol. 21: 101-107.
27. Tsiantoulas, D., C. J. Diehl, J. L. Witztum, and C. J. Binder. 2014. B cells and humoral immunity in atherosclerosis. Circ. Res. 114: 1743-1756.
28. Crotty, S. 2011. Follicular helper CD4 T cells (TFH). Annu. Rev. Immunol. 29: 621-663.
29. Lewis, M. J., T. H. Malik, M. R. Ehrenstein, et al. 2009. Immunoglobulin M is required for protection against atherosclerosis in low-density lipoprotein receptor-deficient mice. Circulation 120: 417-426.
30. Stevens, T. L., A. Bossie, V. M. Sanders, et al. 1988. Regulation of antibody isotype secretion by subsets of antigen-specific helper T cells. Nature 334: 255-258.
31. Dotevall, A., J. Hulthe, A. Rosengren, et al. 2001. Autoantibodies against oxidized low-density lipoprotein and C-reactive protein are associated with diabetes and myocardial infarction in women. Clin. Sci. (Lond.) 101: 523-531.
32. Sjogren, P., G. N. Fredrikson, A. Samnegard, et al. 2008. High plasma concentrations of autoantibodies against native peptide 210 of apoB-100 are related to less coronary atherosclerosis and lower risk of myocardial infarction. Eur. Heart J. 29: 2218-2226.
33. Uyemura, K., L. L. Demer, S. C. Castle, et al. 1996. Crossregulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. J. Clin. Invest. 97: 2130-2138.
34. Frostegard, J., A. K. Ulfgren, P. Nyberg, et al. 1999. Cytokine expression in advanced human atherosclerotic plaques: dominance of pro-inflammatory (Th1) and macrophage-stimulating cytokines. Atherosclerosis 145: 33-43.
35. Laurat, E., B. Poirier, E. Tupin, et al. 2001. In vivo downregulation of T helper cell 1 immune responses reduces atherogenesis in apolipoprotein E-knockout mice. Circulation 104: 197-202.
36. Whitman, S. C., P. Ravisankar, H. Elam, and A. Daugherty. 2000. Exogenous interferon-gamma enhances atherosclerosis in apolipoprotein E-/- mice. Am. J. Pathol. 157: 1819-1824.
37. Whitman, S. C., P. Ravisankar, and A. Daugherty. 2002. IFNgamma deficiency exerts gender-specific effects on atherogenesis in apolipoprotein E-/- mice. J. Interferon. Cytokine Res. 22: 661-670.
38. Buono, C., C. E. Come, G. Stavrakis, et al. 2003. Influence of interferon-gamma on the extent and phenotype of diet-induced atherosclerosis in the LDLR-deficient mouse. Arterioscler. Thromb. Vasc. Biol. 23: 454-460.
39. Gupta, S., A. M. Pablo, X. Jiang, et al. 1997. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J. Clin. Invest. 99: 2752-2761.
40. Buono, C., C. J. Binder, G. Stavrakis, et al. 2005. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc. Natl. Acad. Sci. USA 102: 1596-1601.
41. Ohkura, N., Y. Kitagawa, and S. Sakaguchi. 2013. Development and maintenance of regulatory T cells. Immunity 38: 414-423.
42. Josefowicz, S. Z., L. F. Lu, and A. Y. Rudensky. 2012. Regulatory T cells: mechanisms of differentiation and function. Annu. Rev. Immunol. 30: 531-564.
43. Sakaguchi, S., T. Yamaguchi, T. Nomura, and M. Ono. 2008. Regulatory T cells and immune tolerance. Cell 133: 775-787.
44. Chen, Y., V. K. Kuchroo, J. Inobe, et al. 1994. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265: 1237-1240.
45. Groux, H., A. O'Garra, M. Bigler, et al. 1997. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 389: 737-742.
46. Weiner, H. L., A. P. da Cunha, F. Quintana, and H. Wu. 2011. Oral tolerance. Immunol. Rev. 241: 241-259.
47. Mallat, Z., A. Gojova, V. Brun, et al. 2003. Induction of a regulatory T cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice. Circulation 108: 1232-1237.
48. Ait-Oufella, H., B. L. Salomon, S. Potteaux, et al. 2006. Natural regulatory T cells control the development of atherosclerosis in mice. Nat. Med. 12: 178-180.
49. King, V. L., L. A. Cassis, and A. Daugherty. 2007. Interleukin-4 does not influence development of hypercholesterolemia or angiotensin II-induced atherosclerotic lesions in mice. Am. J. Pathol. 171: 2040-2047.
50. Binder, C. J., K. Hartvigsen, M. K. Chang, et al. 2004. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J. Clin. Invest. 114: 427-437.
51. Cheng, X., S. Taleb, J. Wang, et al. 2011. Inhibition of IL-17A in atherosclerosis. Atherosclerosis 215: 471-474.
52. Madhur, M. S., S. A. Funt, L. Li, et al. 2011. Role of interleukin 17 in inflammation, atherosclerosis, and vascular function in apolipoprotein e-deficient mice. Arterioscler. Thromb. Vasc. Biol. 31: 1565-1572.
53. Danzaki, K., Y. Matsui, M. Ikesue, et al. 2012. Interleukin-17A deficiency accelerates unstable atherosclerotic plaque formation in apolipoprotein E-deficient mice. Arterioscler. Thromb. Vasc. Biol. 32: 273-280.
54. Smith, E., K. M. Prasad, M. Butcher, et al. 2010. Blockade of interleukin-17A results in reduced atherosclerosis in apolipoprotein E-deficient mice. Circulation 121: 1746-1755.
55. Butcher, M. J., B. N. Gjurich, T. Phillips, and E. V. Galkina. 2012. The IL-17A/IL-17RA axis plays a proatherogenic role via the regulation of aortic myeloid cell recruitment. Circ. Res. 110: 675-687.
56. Boyle, J. J. 1997. Association of coronary plaque rupture and atherosclerotic inflammation. J. Pathol. 181: 93-99.
57. Kyaw, T., A. Winship, C. Tay, et al. 2013. Cytotoxic and proinflammatory CD8+ T lymphocytes promote development of vulnerable atherosclerotic plaques in apoE-deficient mice. Circulation 127: 1028-1039.
58. Palinski, W., M. E. Rosenfeld, S. Yla-Herttuala, et al. 1989. Low density lipoprotein undergoes oxidative modification in vivo. Proc. Natl. Acad. Sci. USA 86: 1372-1376.
59. Yla-Herttuala, S., W. Palinski, S. W. Butler, et al. 1994. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler. Thromb. Vasc. Biol. 14: 32-40.
60. Stemme, S., B. Faber, J. Holm, et al. 1995. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc. Natl. Acad. Sci. USA 92: 3893-3897.
61. Palinski, W., E. Miller, and J. L. Witztum. 1995. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc. Natl. Acad. Sci. USA 92: 821-825.
62. Ameli, S., A. Hultgardh-Nilsson, J. Regnstrom, et al. 1996. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler. Thromb. Vasc. Biol. 16: 1074-1079.
63. Freigang, S., S. Horkko, E. Miller, et al. 1998. Immunization of LDL receptor-deficient mice with homologous malondialdehydemodified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes. Arterioscler. Thromb. Vasc. Biol. 18: 1972-1982.
64. George, J.,B. Afek, H. Gilburd, et al. 1998. Hyperimmunization of apo-E-deficient mice with homologous malondialdehyde lowdensity lipoprotein suppresses early atherogenesis. Atherosclerosis 138: 147-152.
65. Zhou, X., G. Caligiuri, A. Hamsten, et al. 2001. LDL immunization induces T-cell-dependent antibody formation and protection against atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 21: 108-114.
66. van Leeuwen, M., M. J. Kemna, M. P. de Winther, et al. 2013. Passive immunization with hypochlorite-oxLDL specific antibodies reduces plaque volume in LDL receptor-deficient mice. PLoS One 8: e68039.
67. Zhou, X., A. K. Robertson, M. Rudling, et al. 2005. Lesion development and response to immunization reveal a complex role for CD4 in atherosclerosis. Circ. Res. 96: 427-434.
68. Habets, K. L., G. H. van Puijvelde, L. M. van Duivenvoorde, et al. 2010. Vaccination using oxidized low-density lipoprotein-pulsed dendritic cells reduces atherosclerosis in LDL receptor-deficient mice. Cardiovasc. Res. 85: 622-630.
69. Hjerpe, C., D. Johansson, A. Hermansson, et al. 2010. Dendritic cells pulsed with malondialdehyde modified low density lipoprotein aggravate atherosclerosis in Apoe(-/-) mice. Atherosclerosis 209: 436-441.
70. Zhou, X., A. K. Robertson, C. Hjerpe, and G. K. Hansson. 2006. Adoptive transfer of CD4+ T cells reactive to modified low-density lipoprotein aggravates atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 26: 864-870.
71. Schiopu, A., J. Bengtsson, I. Soderberg, et al. 2004. Recombinant human antibodies against aldehyde-modified apolipoprotein B-100 peptide sequences inhibit atherosclerosis. Circulation 110: 2047-2052.
72. Fredrikson, G. N., A. Schiopu, G. Berglund, et al. 2007. Autoantibody against the amino acid sequence 661-680 in apo B-100 is associated with decreased carotid stenosis and cardiovascular events. Atherosclerosis 194: e188-e192.
73. Fredrikson, G. N., L. Andersson, I. Soderberg, et al. 2005. Atheroprotective immunization with MDA-modified apo B-100 peptide sequences is associated with activation of Th2 specific antibody expression. Autoimmunity 38: 171-179.
74. Fredrikson, G. N., I. Soderberg, M. Lindholm, et al. 2003. Inhibition of atherosclerosis in apoE-null mice by immunization with apoB-100 peptide sequences. Arterioscler. Thromb. Vasc. Biol. 23: 879-884.
75. Fredrikson, G. N., H. Bjorkbacka, I. Soderberg, et al. 2008. Treatment with apo B peptide vaccines inhibits atherosclerosis in human apo B-100 transgenic mice without inducing an increase in peptide-specific antibodies. J. Intern. Med. 264: 563-570.
76. Hermansson, A., D. F. Ketelhuth, D. Strodthoff, et al. 2010. Inhibition of T cell response to native low-density lipoprotein reduces atherosclerosis. J. Exp. Med. 207: 1081-1093.
77. Wigren, M., D. Kolbus, P. Duner, et al. 2011. Evidence for a role of regulatory T cells in mediating the atheroprotective effect of apolipoprotein B peptide vaccine. J. Intern. Med. 269: 546-556.
78. Khallou-Laschet, J., E. Tupin, G. Caligiuri, et al. 2006. Atheroprotective effect of adjuvants in apolipoprotein E knockout mice. Atherosclerosis 184: 330-341.
79. Herbin, O., H. Ait-Oufella, W. Yu, et al. 2012. Regulatory T-cell response to apolipoprotein B100-derived peptides reduces the development and progression of atherosclerosis in mice. Arterioscler. Thromb. Vasc. Biol. 32: 605-612.
80. Pierides, C., A. Bermudez-Fajardo, G. N. Fredrikson, et al. 2013. Immune responses elicited by apoB-100-derived peptides in mice. Immunol. Res. 56: 96-108.
81. Hermansson, A., D. K. Johansson, D. F. Ketelhuth, et al. 2011. Immunotherapy with tolerogenic apolipoprotein B-100-loaded dendritic cells attenuates atherosclerosis in hypercholesterolemic mice. Circulation 123: 1083-1091.
82. Nilsson, J., M. Wigren, and P. K. Shah. 2013. Vaccines against atherosclerosis. Expert Rev. Vaccines 12: 311-321.
83. Engelbertsen, D., S. Rattik, A. Knutsson, et al. 2014. Induction of T helper 2 responses against human apolipoprotein B100 does not affect atherosclerosis in ApoE-/- mice. Cardiovasc. Res. 103: 304-312.
84. Chyu, K. Y., X. Zhao, P. C. Dimayuga, et al. 2012. CD8+ T cells mediate the athero-protective effect of immunization with an ApoB-100 peptide. PLoS One 7: e30780.
85. Alexander, J., J. Sidney, S. Southwood, et al. 1994. Development of high potency universal DR-restricted helper epitopes by modification of high affinity DR-blocking peptides. Immunity 1: 751-761.
86. Petersen, T. R., E. Bettelli, J. Sidney, et al. 2004. Characterization of MHC-and TCR-binding residues of the myelin oligodendrocyte glycoprotein 38-51 peptide. Eur. J. Immunol. 34: 165-173.
87. Hansson, G. K., and P. Libby. 2006. The immune response in atherosclerosis: a double-edged sword. Nat. Rev. Immunol. 6: 508-519.
88. Chicz, R. M., R. G. Urban, J. C. Gorga, et al. 1993. Specificity and promiscuity among naturally processed peptides bound to HLADR alleles. J. Exp. Med. 178: 27-47.
89. Sidney, J., S. Southwood, C. Moore, et al. 2013. Measurement of MHC/peptide interactions by gel filtration or monoclonal antibody capture. Curr. Protoc. Immunol. 18: 3 Unit doi: 10.1002/ 0471142735.im1803s100.
90. Tse, K., A. Gonen, J. Sidney, et al. 2013. Atheroprotective vaccination with MHC-II restricted peptides from ApoB-100. Front. Immunol. 4: 493. doi: 10.3389/fimmu.2013.00493.
91. Wick, G., G. Schett, A. Amberger, et al. 1995. Is atherosclerosis an immunologically mediated disease? Immunol. Today 16: 27-33.
92. Wick, G., and Q. Xu. 1999. Atherosclerosis-an autoimmune disease. Exp. Gerontol. 34: 559-566.
93. Perschinka, H., M. Mayr, G. Millonig, et al. 2003. Cross-reactive B-cell epitopes of microbial and human heat shock protein 60/65 in atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 23: 1060-1065.
94. Zhu, J., A. A. Quyyumi, D. Rott, et al. 2001. Antibodies to human heat-shock protein 60 are associated with the presence and severity of coronary artery disease: evidence for an autoimmune component of atherogenesis. Circulation 103: 1071-1075.
95. Kervinen, H., T. Huittinen, O. Vaarala, et al. 2003. Antibodies to human heat shock protein 60, hypertension and dyslipidemia. A study of joint effects on coronary risk. Atherosclerosis 169: 339-344.
96. Xu, Q., H. Dietrich, H. J. Steiner, et al. 1992. Induction of arteriosclerosis in normocholesterolemic rabbits by immunization with heat shock protein 65. Arterioscler. Thromb. 12: 789-799.
97. George, J., Y. Shoenfeld, A. Afek, et al. 1999. Enhanced fatty streak formation in C57BL/6J mice by immunization with heat shock protein-65. Arterioscler. Thromb. Vasc. Biol. 19: 505-510.
98. Metzler, B., M. Mayr, H. Dietrich, et al. 1999. Inhibition of arteriosclerosis by T-cell depletion in normocholesterolemic rabbits immunized with heat shock protein 65. Arterioscler. Thromb. Vasc. Biol. 19: 1905-1911.
99. Afek, A., J. George, B. Gilburd, et al. 2000. Immunization of lowdensity lipoprotein receptor deficient (LDL-RD) mice with heat shock protein 65 (HSP-65) promotes early atherosclerosis. J. Autoimmun. 14: 115-121.
100. George, J., A. Afek, B. Gilburd, et al. 2001. Cellular and humoral immune responses to heat shock protein 65 are both involved in promoting fatty-streak formation in LDL-receptor deficient mice. J. Am. Coll. Cardiol. 38: 900-905.
101. Foteinos, G., A. R. Afzal, K. Mandal, et al. 2005. Anti-heat shock protein 60 autoantibodies induce atherosclerosis in apolipoprotein E-deficient mice via endothelial damage. Circulation. 112: 1206-1213.
102. Klingenberg, R., D. F. Ketelhuth, D. Strodthoff, et al. 2012. Subcutaneous immunization with heat shock protein-65 reduces atherosclerosis in Apoe(-)/(-) mice. Immunobiology 217: 540-547.
103. van Puijvelde, G. H., T. van Es, E. J. van Wanrooij, et al. 2007. Induction of oral tolerance to HSP60 or an HSP60-peptide activates T cell regulation and reduces atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 27: 2677-2683.
104. Lu, X., D. Chen, V. Endresz, et al. 2010. Immunization with a combination of ApoB and HSP60 epitopes significantly reduces early atherosclerotic lesion in Apobtm2SgyLdlrtm1Her/J mice. Atherosclerosis 212: 472-480.
105. Tsutsumi, A., E. Matsuura, K. Ichikawa, et al. 1996. Antibodies to beta 2-glycoprotein I and clinical manifestations in patients with systemic lupus erythematosus. Arthritis. Rheum. 39: 1466-1474.
106. George, J., B. Afek, M. Gilburd, et al. 1998. Induction of early atherosclerosis in LDL-receptor deficient mice immunized with 2-glycoprotein I. Circulation 98: 1108-1115.
107. De Haro, J., L. Esparza, S. Bleda, et al. 2014. Attenuation of early atherosclerotic lesions by immunotolerance with beta2 glycoprotein I and the immunomodulatory effectors interleukin 2 and 10 in a murine model. J. Vasc. Surg. [Epub ahead of print]. doi: 10.1016/j.jvs.2014.05.096.
108. Binder, C. J., S. Horkko, A. Dewan, et al. 2003. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat. Med. 9: 736-743.
109. Lu, X., M. Xia, V. Endresz, et al. 2012. Immunization with a combination of 2 peptides derived from the C5a receptor significantly reduces early atherosclerotic lesion in Ldlr(tm1Her) Apob(tm2Sgy) J mice. Arterioscler. Thromb. Vasc. Biol. 32: 2358-2371.
110. Duner, P., F. To, K. Beckmann, et al. 2011. Immunization of apoE-/- mice with aldehyde-modified fibronectin inhibits the development of atherosclerosis. Cardiovasc. Res. 91: 528-536.
111. Wigren, M., D. Bengtsson, P. Duner, et al. 2009. Atheroprotective effects of Alum are associated with capture of oxidized LDL antigens and activation of regulatory T cells. Circ. Res. 104: e62-e70.
112. Faria, A. M., and H. L. Weiner. 1999. Oral tolerance: mechanisms and therapeutic applications. Adv. Immunol. 73: 153-264.
113. van Puijvelde, G. H., A. D. Hauer, P. de Vos, et al. 2006. Induction of oral tolerance to oxidized low-density lipoprotein ameliorates atherosclerosis. Circulation 114: 1968-1976.
114. Klingenberg, R., M. Lebens, A. Hermansson, et al. 2010. Intranasal immunization with an apolipoprotein B-100 fusion protein induces antigen-specific regulatory T cells and reduces atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 30: 946-952.
115. Maron, R., G. Sukhova, A. M. Faria, et al. 2002. Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aortic arch of low-density lipoprotein receptor-deficient mice. Circulation 106: 1708-1715.
116. Xiong, Q., J. Li, L. Jin, et al. 2009. Nasal immunization with heat shock protein 65 attenuates atherosclerosis and reduces serum lipids in cholesterol-fed wild-type rabbits probably through different mechanisms. Immunol. Lett. 125: 40-45.
117. Harats, D., N. Yacov, B. Gilburd, et al. 2002. Oral tolerance with heat shock protein 65 attenuates Mycobacterium tuberculosisinduced and high-fat-diet-driven atherosclerotic lesions. J. Am. Coll. Cardiol. 40: 1333-1338.
118. Jing, H., L. Yong, L. Haiyan, et al. 2011. Oral administration of Lactococcus lactis delivered heat shock protein 65 attenuates atherosclerosis in low-density lipoprotein receptor-deficient mice. Vaccine 29: 4102-4109.
119. Mundkur, L., R. Mukhopadhyay, S. Samson, et al. 2013. Mucosal tolerance to a combination of ApoB and HSP60 peptides controls plaque progression and stabilizes vulnerable plaque in Apob(tm2Sgy)Ldlr(tm1Her)/J mice. PLoS One 8: e58364.