Humoral and cellular immunity against atherosclerosis: possibility to develop a vaccine

Abstract


Development of atherosclerosis is influenced by innate and adaptive immune responses. Innate immunity based on detection of pathogen-associated molecular patterns by pattern recognition receptors on macrophages and dendritic cells. Pattern recognition receptors binding a wide range of protein, carbohydrates, lipids and nucleic acids, but those considered most important in atherosclerosis are scavenger receptors and the Toll-like receptors. Recent observation has suggested the possibility that selective suppression of proatherogenic immune responses or selective activation of antiatherogenic immune response may provide new approaches for atherosclerosis prevention and treatment.

V A Nagornev

Institute of Experimental Medicine RAMS, St. Petersburg; SSC «State Research Institute of Highly Pure BioSubstances», St. Petersburg

S A Ketlinsky

Institute of Experimental Medicine RAMS, St. Petersburg; SSC «State Research Institute of Highly Pure BioSubstances», St. Petersburg

  1. Аничков Н. Н. Главные результаты исследований, проведенных в отделе патологической анатомии Института экспериментальной медицины АМН СССР//Вестн. АМН СССР. 1961. № 11. С. 33-40.
  2. Денисенко А. Д., Виноградов А. Г., Нагорнев В. А. и др. Взаимодействие макрофагов с
  3. Климов А. Н. Аутоиммунная теория атерогенеза и концепция модифицированных липопротеидов // Вести. АМН СССР. 1990. № 11. С. 30-36.
  4. Климов А. Н., Нагорнев В А., Денисенко А. Д. Изучение иммунологических механизмов развития атеросклероза и новые методы его диагностики и лечения // Мед. акад. журн. 2005. Т. 5. № 2. С. 18-32.
  5. Нагорнев В. А. Патогенез атеросклероза. 2007.
  6. Ait-Oufella Н., Salomon B.L., Potteaux S. et al. Natural regulatory T cells control the development of atherosclerosis in mice // Nat. Med. 2006. Vol. 12. P. 178-180.
  7. Ameli S., Hultgardh-Nilsson S., Regnstrom J. et al. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits // Arterioscler. Thromb. Vase. Biol. 1996. Vol. 16. P. 1074-1079.
  8. Alipour A., van Oostrom J.H.H.M., Israeljan A. et al. Leukocyte activation by triglyceride-rich lipoproteins //Ateroscler. Thromb. Vase. Biol. 2008. Vol. 28. P. 792-797.
  9. Anitshkov N. Uber die Veranderungen der Kaninchen aorta bei experimenteller Cholesterin-steatose // Beitrag. pathol. Anat. und allgem. Pathol. 1913. Bd. 56. S. 379-405.
  10. Baum PR., Gayle B.B., Ramsdell. Molecular characterization of murine aqnd human OX40/OX40 ligand systems: identification of a human OX40 ligand as the HTLV-1 regulated protein gp34 // Embo J. 1994. Vol. 13. P. 3992-4001.
  11. Benko S., Magyarics Z., Szabo A. et al. Dendritic cell subtypes as primary targets of vaccines: the emerging role and cross-talk of pattern recognition receptors // Biol. Chem. 2008. Vol. 389. P. 469-485.
  12. Bettelli E., Oukka, Kuchroo. T(H)-17 cells in the circle of immunity and autoimmunity // Nat. Immunol. 2007. Vol. 8. P. 345-350.
  13. Blankenberg S., Tirel L., Bickel C. Interleukin-18 is a strong predictor of cardiovascular death in stable and unstable angina // Circulation. 2002. Vol. 106. P. 24-30.
  14. Bochkov V. N., Mechtcheriakova D., Lucerna M. et al. Oxidized phospholipids stimulate tissue factor expression in human endothelial cells via activation of ERK/ EGR-1 and Ca(++0 NFAT // Blood. 2002. Vol. 99. P. 199-206.
  15. Buono C. et al. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses // Proc. Natl. Acad. Sci. USA. 2005. Vol. 102. P. 15961601.
  16. Caligiuri G., Nicoletti A., Poirier В., Hansson G. K. Protective immunity carried by В cells of hypercholesterolemic mice // J. Clin. Invast. 2002. Vol. 109. P. 745-753.
  17. Chen Z., Tato L., Muul A. et al. Distinct regulation of interleukin-17 in human T-helper lymphocytes // Arthritis Rheum. 2007. Vol. 56. P. 2936-2946.
  18. Cheng X., Liao H., Ge B. Thl/Th2 functional imbalance after acute myocardial infarction: coronary arterial inflammation of myocardial inflammation or myocardial inflammation // J. Clin. Immunol. 2005. Vol. 25. P. 246-253.
  19. Cheng X, Yu X., Ying-jan Ding et al. The Thl7/Treg imbalance in patients with acute coronary syndrome // Clin. Immunol. 2008. Vol. 127. P. 89-97.
  20. Choi J., Enis D. R., Koh K. P. et al. T lymphocyte-endothelial cell interactions // Annu. Rev. Immunol. 2004. Vol. 22. P. 683-709.
  21. Csiszar A., Ungravi Z. Sinergistic effects of vascular IL-17 and TNF-a may promote coronary artery disease // Med. Hypotheses. 2004. Vol. 63. P. 696-698.
  22. Cui M. Z., Perm M. S., Chisolm G. M. Native and oxidized low density lipoprotein induction of tissue factor gene expression in smooth muscle cells is mediated by both Egr-1 and Spt // J. Biol. Chem. 1999. Vol. 274. P. 32795-32802.
  23. Edfeldt K., Swedeborg J., Hansson G.K., Yan Z-Q. Expression of toll-like receptors in human atherosclerotic lesions: a possible pathway for plaque activation // Circulation. 2002. Vol. 105. P. 1158-1161.
  24. Elhage R., Courdy P., Brouchet L. et al. Deleting TCRccP or CD4+ T cells leads to opposite effects on site-specific atherosclerosis in famalt ApoE '' deficient mice //Am. J. Pathol. 2004. Vol. 165. P. 2013-2018.
  25. Faure E., Thomas L., Xu H. et al. Bacterial lipopoly-saccharide and IFN-y induce Toll-like receptor 2 and Toll-like Receptor 4 expression in human endothelial cells: role NF-кВ activation // J. Immunol. 2001. Vol. 166. P. 2018-2024.
  26. Fong L.G., Albert T.S., Horn S.E. Inhibition of the mac-rophages-induced oxidation of LDL by interferon-gam-ma // J. Lipid. Res. 1994. Vol. 35. P. 893-904.
  27. Fredrikson G.K., Hedblad В., Berglund G. et al. Identification of immune responses against aldehydemodified peptide sequences in apo B-100 associated with cardiovascular disease // Arterioscler. Thromb. Vase. Biol. 2003. Vol. 23. P. 872-878.
  28. Fredrikson G.K., Andersson L., Soderberg I. et al. Atheroprotective immunization with MDA-modified apoB-100 peptide sequences is associated with activation of Th2 specific antibody expression //Autoimmunity. 2005. Vol. 38. P. 171-179.
  29. Fredrikson G.K., Hedblad В., Berglund G. et al. Association between IgM against an aldehyde-modified peptide in Apolipoprotein B-100 and progression of carotid disease // Stroke. 2007. Vol. 38. P. 1495-1500.
  30. Fredrikson G. K., Bjorkhacka H., Soderberg I. Treatment with apoB peptide vaccines inhibits atherosclerosis in human apoB-100 transgenic mice without inducing an increase in peptide-specific antibodies // J. Intern. Med. 2008. Vol. 10. P. 1-8.
  31. Frostegard J., Ulfgren A. K., Nyberg P. et al. Cytokine expression in advanced human atherosclerotic plaques: dominance of proinflammatory (Thl) and macrophage-stimulating cytokines // Atherosclerosis. 1999. Vol. 145. P. 33-43.
  32. Gejrge J., Afek A., Gilburd B. Hyperimmunization of ApoE deficient mice with homologous malondialdegid low-density lipoprotein suppresses early atherogenesis //Atherosclerosis. 1998. Vol. 138. P. 147-152.
  33. George J. et al. Supression of early atherosclerosis in LDL-receptor deficient mice by oral tolerance with P2-glycoprotein 1 // Cardiovasc. Res. 2004. Vol. 62. P. 603-609.
  34. Gong J., Koido S., Calderwood S.K. Cell fusion: from hybridoma to dendritic cell-based vaccine // Expert. Rev. Vaccines. 2008. Vol. 7. P. 1055-1068.
  35. Hansson G. K. Vaccination against atherosclerosis. Science of fiction? // Circulation. 2002. Vol. 106. P. 337356.
  36. Hansson G. K. Inflammation, atherosclerosis, and coronary disease //N. Engl. J. Med. 2005. Vol. 352. P. 1685-1695.
  37. Hansson G. K. Atherosclerosis - an immune disease. The Anitschkov lecture 2007 //Atherosclerosis. 2009. Vol. 202. P. 2-10.
  38. Hansson G. K., Libby P. The immune response in atherosclerosis: a double-edged sword // Nature Rev. Immunol. 2006. Vol. 6. P. 508-519.
  39. Harats D., Yacov N., Gilburn B. Oral tolerance with heat shock protein-65 attenuates Mycobacterium tuberculosis-induced and high-fat-diet-driven atherosclerotic lesions // J. Am. Coll. Cardiol. 2002. Vol. 40. P. 1333-1338.
  40. Hashmi S., Zeng Q. T. Role of interleukin-17 and interleukin-17 - induced cytokines interleukin-6, interleukin-8 in unstable coronary artery disease // Artery Dis. 2006. Vol. 17. P. 699-706.
  41. Hauer A. D., Uyttenhove C, de Vos P. et al. Blocade of interleukin-12 function by protein vaccination attenuates atherosclerosis // Circulation. 2005. Vol. 112. P. 1054-1062.
  42. Hendersen E. L. et al. Death of smooth muscle cells and expression of mediators of apoptosis by T cells in aorta aneurysms // Circulation. 1999. Vol. 99. P. 96-104.
  43. Horkko S., Miller E. et al. Immunization of LDL receptor-deficient mice with homologous malandialde-hyde-modified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes // Arterioscler. Thromb. Vase. Biol. 1998. Vol. 18. P. 19721982.
  44. Horkko S., Binder C. J., Shaw P. X. et al. Immunological responses to oxidized LDL // Free Radic. Biol. Med. 2000. Vol. 28. P. 1771-1779.
  45. Huber S.A., Sakkinen P, David C, Chen C, Tracy R.P. T helper cells phenotype regulates atherosclerosis in mice under conditions of mild hypercholesterjlemia // Circulation. 2001. Vol. 103. P. 2610-2616.
  46. Imura A., Hori Т., Ishikawa T. et al. The human ОХ40/ gp34 system directly mediates adhesion of activated T cells to vascular endothelial cells // J. Exp. Med. 1996. Vol. 183. P. 2185-2195.
  47. Ito Т., Wang Y. H., Duramad O. et al. OX40 ligand shuts down IL-10-producing regulatory T cells // Proc. Natl. Acad. Sci. USA. 2006. Vol. 103. P. 1313813143.
  48. Kolls J.K., Linden A. Interleukin-17 family members and inflammation // Immunity. 2004. Vol. 21. P. 467-176.
  49. Li H., Sun B. Toll-like receptor 4 in atherosclerosis // J. Cell. Mol. Med. 2007. Vol. 11. P. 88-95.
  50. Libby P. Inflammation in atherosclerosis // Nature. 2002. Vol. 420. P. 868-874.
  51. Liu-Wu Y, Hurt-Camejo E., Wiklund O. Lysophos-phatidylcholine induces the production of IL-1 beta by human monocytes //Atherosclerosis. 1998. Vol. 137. P. 351-357.
  52. Lotze M.T., Thomson A.W. Dendritic cells: Biology and Clinical Applications. 2nd edition. San Diego, CA: Academic Press, 2001.
  53. Lutgens E., Cleutjens К. В., Heeneman S. et al. Both early and delayed anti-CD40L antibody treatment induces a stable plaque phenotype // Proc. Natl. Acad. Sci. USA. 2000. Vol. 97. P. 7464-7469.
  54. Madan M. and Amar S. Toll-like receptor-2 mediates diet and/or pathogen assocated atherosclerosis: proteomic findings // Plos. One. 2008. Vol. 3. P. 1-12.
  55. Mallat Z. et al. Protective role of IL-10 in atherosclerosis // Circ. Res. 1999. Vol. 85. P. 17-24.
  56. Mallat Z., Gojova A., Brun V. et al. Induction of a regulatory T-cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice //2003. Vol. 108. P. 1232-1237.
  57. Malmstrom V, Shiplon D., Singh B. CD134L expression on dendritic cells in the mesenteric lypmph nodes drives colitis in T cell-restored SCID mice // J. Immunol. 2001. Vol. 166. P. 6972-6981.
  58. Mangan M.E., Flierman L.M., van Duivenvoord H.J. et al. Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells // Arthritis. Rheum. 2005. Vol. 52. P. 2212-2221.
  59. Maron R., Sukhova G., Faria A.M. et al. Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aorta arch of low-density lipoprotein receptor-deficient mice // Circulation. 2002. Vol. 106. P. 1708-1715.
  60. McLaren J.E., Ramji D. Interferon gamma : a master regulator of atherosclerosis // Cytokine & Growth factor reviews. 2009. Vol. 20. P. 125-135.
  61. Medhitov R. Toll-like receptors and innate immunity //Nat. Rev. Immunol. 2006. Vol. 1. P. 135-145.
  62. Melief C. J. Cancer immunotherapy by dendritic cells // Immunity. 2008. Vol. 29. P. 372-383.
  63. Methe H., Brunner S., Wiegand D. Enhanced T-helper-1 lymphocyte activation patterns in acute coco-nary syndromes // J. Am. Coll. Cardiol. 2005. Vol. 45. P. 1939-1945.
  64. Moore K.J., Freeman M.W. Scavanger receptors in atherosclerosis: beyond lipid uptake // Arterioscler. Tromb. Vase. Biol. 2006. Vol. 26. P. 208-222.
  65. Nilsson J., Hansson J. K., Shah P. K. Immunomodulation of atherosclerosis. Implications for vaccine development // Arterioscler. Thromb. Vase. Biol. 2005. Vol. 25. P. 18-28.
  66. Okabe Т., Kishimoto C, Shimada K. et al. Effects of late administration of immunoglobulin on experimental atherosclerosis in apolipoprotein E-deficient mice // Exp. Invest. 2005. Vol. 69. P. 1543-1546.
  67. Palinski W., Miller E., Witztum J.L. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis // Proc. Natl. Acad. Sci. USA. 1995. Vol. 92. P. 821-825.
  68. Podrez E.A., Shmitt D., Hoff H.F. et al. Myeloperoxidase-generated nitrogen species convert LDL into an atherogenic form in vitro // J. Clin. Invest. 1999. Vol. 103. P. 1547-1560.
  69. Reyes O. S., Chyu K. Y., Yano J. et al. Immunization with a novel human Apo B-100 related peptide reduces atherosclerosis and inflammation in apo E null mice // 2002. Vol. 39 (Suppl. A). S. 240A.
  70. Robertson A.K.L., Rudling M., Zhou X. et al. Disruption of TGF-P signaling in T cells accelerates atherosclerosis // J. Clin. Invest. 2003. Vol. 112. P. 13421350.
  71. Roselaar S.E., Kakkanathu P.X., Daugherry A. Lymphocyte population in aterosclerosis lesions of ApoE"'" and LDLR '" mice. Decreasing density with disease progression // Arterioscler. Tromb. Vase. Biol. 1996. Vol. 16. P. 1013-1018.
  72. Roselaar S.E., Daugherry A. ApoE deficient mice have impaired innate response to Listeria monocytogenes in vivo // J. Lipid. Res. 1999. Vol. 40. P. 680-685.
  73. Sainz J., Sata M. Open Seasame! CXCR4 blockade recruits neutrophils into the plaque // Circ. Res. 2008. Vol. 102. P. 154-156.
  74. Sakaguchi S., Ono R., Setoguchi H. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tol-eranc and autoimmu disease // Immunol. Rev. 2006. Vol. 212. P. 8-27.
  75. Sasu S., LaVerda D., Qureshi N. Clamidia pneumonia and Clamidial heat shock protein 60 stimulate proliferation of human vascular smooth muscle cells via toll-like receptor 4 b p44/42 mitogen-activated protein kinase activation // Circ. Res. 2001. Vol. 89. P. 244-250.
  76. Al-Shamkhani A., Birkeland M.L., Puklavec M. et al. CD40 is differentially expressed on activated rat and mouse T cells and is the sole receptor for the OX40 ligand // Eur. J. Immunol. 1996. Vol. 26. P. 1695-1699.
  77. Schiopu A., Bengtsson J., Soderberg I. et al. Recombinant human antibodies against aldehydemodified apolipoprotein B-100 peptide sequences inhibit atherosclerosis // Circulation. 2004. Vol. 102. P. 2919-2922.
  78. Schiopu A., Frendeus В., Jansson B. et al. Recombinant antibodies to an oxidized lowOdensity lipoprotein epitope ind rapid regression of atherosclerosis in apobec-1"'" low density lipoprotein idyreceptor'- mice // J. Am. College Cardiol. 2008. Vol. 50. P. 23132318.
  79. Schonbeck U., Libby P. The CD40/CD154 receptor/ligand dyad // Cell. Mol. Life. Sci. 2001. Vol. 58. P. 4-43.
  80. Schoneveld O.N., van M. Laman de K. et al. Tolllike receptor 2 stimulation induces intimal hyperplasia and atherosclerrotic lesion development // Cardiovasc. Res. 2005. Vol. 66. P. 162-169.
  81. Sjogren P., Fredrikson G.N., Samnegard A. et al. High plasma concentration of autoantibodies against native peptide 210 of apo B-100 are related to less coronary atherosclerosis and lower risk of myocardial infarction // Eur. Heart J. 2008. Vol. 29. № 18. P. 2218-2226.
  82. Swirski F.K., Pittet M.J., Kircher M.F. et al. Monocyte accumulation in mouse atherogenesis is progressive and propotional to extent of disease // Proc. Natl. Acad. Sci. USA. 2006. Vol.103. P. 1340-1345.
  83. Taleb S., Tegui A., Mallat Z. Regulatory T cell immunity and its relevance to atherosclerosis // J. Intern. Med. 2008. Vol. 263. P. 489-499.
  84. Takahara N., Kashiwag A., Maegawa H. et al. Lisophosphatidylcholine stimulated the expression and production of MCP-1 by human vascular endothelial cells // Metabolism. 1996. Vol. 45. P. 59-64.
  85. Takeda К., Akira S. Microbial recognition by Tolllike receptors // J. Dermatol. Sci. 2004. Vol. 34. P. 73-82.
  86. Tellides G. Interferon-y elicits atherosclerosis in the ad-sence of leucocytes // Nature. 2000. Vol. 403. P. 207211.
  87. Tornvall P., Waeg G., Nilsson J. et al. Autoantibodies against modified low-density lipoproteins in coronary artery disease // Atherosclerosis. 2003. Vol. 167. P. 347-353.
  88. Tupin E., Nicoletti A., Eihage R. et al. CDl-dependent activation of NKT cell aggravates atherosclerosis // J. Exp. Med. 2004. Vol. 199. P. 417-422.
  89. Eva J.A. van Wanrooij, Gijs H.M., van Puijvelde et al. Interruption of the Tnfrsf4/Tnfsf4 (OX40/OX40L0) pathway attenuates atherogenesis in low-density lipoprotein receptor-deficient mice //Arterioscler. Thromb. Vase. Biol. 2007. Vol. 27. P. 204-210.
  90. Weber C, Zeraecke A. and Libby P. The multifaceted contridutionjf leukocyte subset to aterosclerosis: lessons from mouse models // Nature Rev. Immunol. 2006. Vol. 8. P. 802-815.
  91. Wilson N. J., Boniface K., Chan B.S. et al. Development, cytokine profile and function of human interleukin 17-producing helper T cells // Nat. Immunol. 2007. Vol. 8. P. 950-957.
  92. Xu X.H., Shah P.K., Faure E. et al. TLR-4 is expressed by macrophages in murine and human lipid-rich atherosclerotic plaques and upregulated by oxidized LDL // Circulation. 2001. Vol. 104. P. 3103-3108.
  93. Zernecke A., Bot I., Djalali-Talab Y. et al. Protective role of CXCR4/CXCL12 unveils the importance of neutrophils in atherosclerosis // Circ. Res. 2008. Vol. 102. P. 154-156.
  94. Zhou X., Stemme S., Hansson G.K. Evidence for a local immune response in atherosclerosis. CD4+ T cells infiltrate lesions of apoprotein - E-defi-cient mice //Am. J. Pathol. 1996. Vol. 149. P. 359366.
  95. Zhou X., Nicoletti A., Eihage R., Hansson G.K. Transfer of CD4+ T cells aggravates atherosclerosis in im-munodeficient apolipoprotein E knockout mice // Circulation. 2000. Vol. 102. P. 2919-2922.

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