Regulatory T-cell response to apolipoprotein B100-derived peptides reduces the development and progression of atherosclerosis in mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 32, Issue 3, 2012, Pages 605-612

  Herbin, Olivier ^a   Ait Oufella, Hafid ^a,b   Yu, Wang ^a   Fredrikson, Gunilla Nordin ^b   Aubier, Benjamin ^a   Perez, Nicolas ^a   Barateau, Véronique ^a   Nilsson, Jan ^b   Tedgui, Alain ^a   Mallat, Ziad ^a,c  

^a INSERM   (France)

^b LUND UNIVERSITY HOSPITAL   (Sweden)

^c UNIVERSITY OF CAMBRIDGE   (United Kingdom)

Author keywords

atherosclerosis; cytokines; immune system; leukotrienes

Indexed keywords

APOLIPOPROTEIN B100; COLLAGEN; OVALBUMIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CD4+ CD25+ T LYMPHOCYTE; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE COURSE; IMMUNE RESPONSE; IMMUNOLOGICAL TOLERANCE; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; TH1 CELL; VASCULITIS;

ANIMALS; APOLIPOPROTEIN B-100; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CELLS, CULTURED; CYTOKINES; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; IMMUNE TOLERANCE; IMMUNOTHERAPY; INFUSIONS, SUBCUTANEOUS; LYMPHOCYTE ACTIVATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; OVALBUMIN; PEPTIDES; T-LYMPHOCYTES, REGULATORY; TIME FACTORS;

EID: 84857653448     PISSN: 10795642     EISSN: 15244636     Source Type: Journal    
DOI: 10.1161/ATVBAHA.111.242800     Document Type: Article

References (41)

1. Binder CJ, Chang MK, Shaw PX, Miller YI, Hartvigsen K, Dewan A, Witztum JL. Innate and acquired immunity in atherogenesis. Nat Med. 2002;8:1218-1226. (Pubitemid 35373552)
2. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6:508-519. (Pubitemid 43980523)
3. Tedgui A, Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev. 2006;86:515-581.
4. Hermansson A, Ketelhuth DF, Strodthoff D, Wurm M, Hansson EM, Nicoletti A, Paulsson-Berne G, Hansson GK. Inhibition of T cell response to native low-density lipoprotein reduces atherosclerosis. J Exp Med. 2010;207:1081-1093.
5. Paulsson G, Zhou X, Tornquist E, Hansson GK. Oligoclonal T cell expansions in atherosclerotic lesions of apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2000;20:10-17. (Pubitemid 30048341)
6. Taleb S, Tedgui A, Mallat Z. Adaptive T cell immune responses and atherogenesis. Curr Opin Pharmacol. 2010;10:197-202.
7. Sakaguchi S. Naturally arising Foxp3-expressing CD25CD4αregulatory T cells in immunological tolerance to self and non-self. Nat Immunol. 2005;6:345-352. (Pubitemid 41716771)
8. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol. 2005;6:338-344. (Pubitemid 41716770)
9. Mallat Z, Ait-Oufella H, Tedgui A. Regulatory T cell responses: potential role in the control of atherosclerosis. Curr Opin Lipidol. 2005;16: 518-524. (Pubitemid 41376901)
10. Ait-Oufella H, Horvat B, Kerdiles Y, Herbin O, Gourdy P, Khallou-Laschet J, Merval R, Esposito B, Tedgui A, Mallat Z. Measles virus nucleoprotein induces a regulatory immune response and reduces atherosclerosis in mice. Circulation. 2007;116:1707-1713. (Pubitemid 47537845)
11. Mallat Z, Gojova A, Brun V, Esposito B, Fournier N, Cottrez F, Tedgui A, Groux H. Induction of a regulatory T cell type 1 response reduces the development of atherosclerosis in apolipoprotein E-knockout mice. Circulation. 2003;108:1232-1237. (Pubitemid 37099993)
12. 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. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006;12:178-180. (Pubitemid 43214743)
13. Andersson J, Libby P, Hansson GK. Adaptive immunity and atherosclerosis. Clin Immunol. 2010;134:33-46.
14. George J. Mechanisms of disease: the evolving role of regulatory T cells in atherosclerosis. Nat Clin Pract Cardiovasc Med. 2008;5:531-540.
15. Mallat Z, Taleb S, Ait-Oufella H, Tedgui A. The role of adaptive T cell immunity in atherosclerosis. J Lipid Res 2009;50(suppl):S364-S369.
16. Curotto de Lafaille MA, Lafaille JJ. Natural and adaptive foxp3́regulatory T cells: more of the same or a division of labor? Immunity. 2009;30:626-635.
17. Faria AM, Weiner HL. Oral tolerance. Immunol Rev. 2005;206:232-259. (Pubitemid 41105174)
18. Faria AM, Weiner HL. Oral tolerance: therapeutic implications for autoimmune diseases. Clin Dev Immunol. 2006;13:143-157. (Pubitemid 44950033)
19. Maron R, Sukhova G, Faria AM, Hoffmann E, Mach F, Libby P, Weiner HL. Mucosal administration of heat shock protein-65 decreases atherosclerosis and inflammation in aortic arch of low-density lipoprotein receptor-deficient mice. Circulation. 2002;106:1708-1715.
20. Harats D, Yacov N, Gilburd B, Shoenfeld Y, George J. Oral tolerance with heat shock protein 65 attenuates Mycobacterium tuberculosisinduced and high-fat-diet-driven atherosclerotic lesions. J Am Coll Cardiol. 2002;40:1333-1338.
21. George J, Yacov N, Breitbart E, Bangio L, Shaish A, Gilburd B, Shoenfeld Y, Harats D. Suppression of early atherosclerosis in LDLreceptor deficient mice by oral tolerance withα2-glycoprotein I. Cardiovasc Res. 2004;62:603-609. (Pubitemid 38648975)
22. van Puijvelde GH, Hauer AD, de Vos P, van den Heuvel R, van Herwijnen MJ, van der Zee R, van Eden W, van Berkel TJ, Kuiper J. Induction of oral tolerance to oxidized low-density lipoprotein ameliorates atherosclerosis. Circulation. 2006;114:1968-1976. (Pubitemid 44665392)
23. Klingenberg R, Lebens M, Hermansson A, Fredrikson GN, Strodthoff D, Rudling M, Ketelhuth DF, Gerdes N, Holmgren J, Nilsson J, Hansson GK. Intranasal immunization with an apolipoprotein B-100 fusion protein induces antigen-specific regulatory T cells and reduces atherosclerosis. Arterioscler Thromb Vasc Biol. 2010;30:946-952.
24. Apostolou I, von Boehmer H. In vivo instruction of suppressor commitment in naive T cells. J Exp Med. 2004;199:1401-1408. (Pubitemid 38685731)
25. Larche M, Wraith DC. Peptide-based therapeutic vaccines for allergic and autoimmune diseases. Nat Med. 2005;11:S69-S76. (Pubitemid 40562306)
26. Fredrikson GN, Soderberg I, Lindholm M, Dimayuga P, Chyu KY, Shah PK, Nilsson J. Inhibition of atherosclerosis in apoE-null mice by immunization with apoB-100 peptide sequences. Arterioscler Thromb Vasc Biol. 2003;23:879-884. (Pubitemid 36566181)
27. Fredrikson GN, Hedblad B, Berglund G, Alm R, Ares M, Cercek B, Chyu KY, Shah PK, Nilsson J. Identification of immune responses against aldehyde-modified peptide sequences in apoB associated with cardiovascular disease. Arterioscler Thromb Vasc Biol. 2003;23:872-878. (Pubitemid 36566180)
28. Fredrikson GN, Andersson L, Soderberg I, Dimayuga P, Chyu KY, Shah PK, Nilsson J. Atheroprotective immunization with MDA-modified apo B-100 peptide sequences is associated with activation of Th2 specific antibody expression. Autoimmunity. 2005;38:171-179. (Pubitemid 40872742)
29. Fredrikson GN, Bjorkbacka H, Soderberg I, Ljungcrantz I, Nilsson J. Treatment with apo B peptide vaccines inhibits atherosclerosis in human apo B-100 transgenic mice without inducing an increase in peptidespecific antibodies. J Intern Med. 2008;264:563-570.
30. Taleb S, Herbin O, Ait-Oufella H, Verreth W, Gourdy P, Barateau V, Merval R, Esposito B, Clement K, Holvoet P, Tedgui A, Mallat Z. Defective leptin/leptin receptor signaling improves regulatory T cell immune response and protects mice from atherosclerosis. Arterioscler Thromb Vasc Biol. 2007;27:2691-2698. (Pubitemid 350158924)
31. Binder CJ, Hartvigsen K, Chang MK, Miller M, Broide D, Palinski W, Curtiss LK, Corr M, Witztum JL. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest. 2004;114:427-437. (Pubitemid 39071615)
32. Ameli S, Hultgardh-Nilsson A, Regnstrom J, Calara F, Yano J, Cercek B, Shah PK, Nilsson J. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol. 1996;16:1074-1079. (Pubitemid 26266910)
33. Palinski W, Miller E, Witztum JL. Immunization of low density lipoprotein (LDL) receptor-deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc Natl Acad Sci USA. 1995;92:821-825.
34. Zhou X, Caligiuri G, Hamsten A, Lefvert AK, Hansson GK. LDL immunization induces T-cell-dependent antibody formation and protection against atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21: 108-114. (Pubitemid 32061934)
35. George J, Afek A, Gilburd B, Levkovitz H, Shaish A, Goldberg I, Kopolovic Y, Wick G, Shoenfeld Y, Harats D. Hyperimmunization of apo-E-deficient mice with homologous malondialdehyde low-density lipoprotein suppresses early atherogenesis. Atherosclerosis. 1998;138: 147-152. (Pubitemid 28255163)
36. Xu Q, Dietrich H, Steiner HJ, Gown AM, Schoel B, Mikuz G, Kaufmann SH, Wick G. Induction of arteriosclerosis in normocholesterolemic rabbits by immunization with heat shock protein 65. Arterioscler Thromb. 1992;12:789-799.
37. George J, Shoenfeld Y, Afek A, Gilburd B, Keren P, Shaish A, Kopolovic J, Wick G, Harats D. Enhanced fatty streak formation in C57BL/6J mice by immunization with heat shock protein-65. Arterioscler Thromb Vasc Biol. 1999;19:505-510. (Pubitemid 29135148)
38. George J, Afek A, Gilburd B, Blank M, Levy Y, Aron-Maor A, Levkovitz H, Shaish A, Goldberg I, Kopolovic J, Harats D, Shoenfeld Y. Induction of early atherosclerosis in LDL-receptor-deficient mice immunized withα2- glycoprotein I. Circulation. 1998;98:1108-1115. (Pubitemid 28420703)
39. Metzler B, Mayr M, Dietrich H, Singh M, Wiebe E, Xu Q, Wick G. Inhibition of arteriosclerosis by T-cell depletion in normocholesterolemic rabbits immunized with heat shock protein 65. Arterioscler Thromb Vasc Biol. 1999;19:1905-1911. (Pubitemid 29379920)
40. George J, Harats D, Gilburd B, Afek A, Shaish A, Kopolovic J, Shoenfeld Y. Adoptive transfer ofβ(2)-glycoprotein I-reactive lymphocytes enhances early atherosclerosis in LDL receptor-deficient mice. Circulation. 2000;102:1822-1827.
41. Wigren M, Bengtsson D, Dunér P, Olofsson K, Björkbacka H, Bengtsson E, Fredrikson GN, Nilsson J. Atheroprotective effects of Alum are associated with capture of oxidized LDL antigens and activation of regulatory T cells. Circ Res. 2009;104:e62-e70.