CD4+LAP+ and CD4+CD25 +Foxp3+ regulatory T cells induced by nasal oxidized low-density lipoprotein suppress effector T cells response and attenuate atherosclerosis in ApoE-/- Mice

Journal of Clinical Immunology

Volumn 32, Issue 5, 2012, Pages 1104-1117

  Zhong, Yucheng ^a   Wang, Xiang ^a   Ji, Qingwei ^b   Mao, Xiaobo ^a   Tang, Hongxia ^c   Yi, Guiwen ^a   Meng, Kai ^a   Yang, Xiaofang ^a   Zeng, Qiutang ^a  

^a Union Hospital   (China)

^b PEOPLE'S HOSPITAL OF GUANGXI ZHUANG AUTONOMOUS REGION   (China)

^c HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Atherosclerosis; Immune system; Oxidized LDL; Regulatory T cells; Tolerance induction

Indexed keywords

APOLIPOPROTEIN E; OXIDIZED LOW DENSITY LIPOPROTEIN; TRANSCRIPTION FACTOR FOXP3; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROTIC PLAQUE; CD4+ CD25+ FOXP3+ REGULATORY T LYMPHOCYTE; CD4+ LAP+ REGULATORY T LYMPHOCYTE; CERVICAL LYMPH NODE; CONTROLLED STUDY; CYTOKINE PRODUCTION; CYTOKINE RELEASE; CYTOKINE RESPONSE; DISEASE COURSE; HEART PROTECTION; IMMUNE RESPONSE; IMMUNIZATION; IMMUNOLOGICAL TOLERANCE; IN VIVO STUDY; LYMPHOCYTE FUNCTION; MALE; MOLECULAR MECHANICS; MOUSE; NONHUMAN; PRIORITY JOURNAL; REGULATORY MECHANISM; REGULATORY T LYMPHOCYTE; SPLEEN; SUPPRESSOR CELL; T LYMPHOCYTE SUBPOPULATION; TH1 CELL; TH17 CELL; TH2 CELL;

ADMINISTRATION, INTRANASAL; ANIMALS; ANTIGENS, CD4; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CHOLESTEROL; CYTOKINES; DIET, HIGH-FAT; FORKHEAD TRANSCRIPTION FACTORS; INTERLEUKIN-2 RECEPTOR ALPHA SUBUNIT; LIPOPROTEINS, LDL; LYMPH NODES; MALE; MICE; MICE, KNOCKOUT; SPLEEN; T-LYMPHOCYTES, HELPER-INDUCER; T-LYMPHOCYTES, REGULATORY; TRANSFORMING GROWTH FACTOR BETA;

EID: 84866734766     PISSN: 02719142     EISSN: 15732592     Source Type: Journal    
DOI: 10.1007/s10875-012-9699-7     Document Type: Article

References (40)

1. + T Cells: A Novel Regulatory T Cell Subset. J Immunol. 2010; 184:4620-4.
2. high-induced colitis by a TGF-beta-dependent mechanism. J Immunol. 2003; 170:2516-22.
3. Sasaki N, Yamashita T, Takeda M, Shinohara M, Nakajima K, Tawa H, Usui T, Hirata K. Oral anti-CD3 antibody treatment induces regulatory T cells and inhibits the development of atherosclerosis in mice. Circulation. 2009; 120:1996-2005.
4. + T cells. Nat Med. 2006; 12:627-35.
5. Ishikawa H, Ochi H, Chen ML, Frenkel D, Maron R, Weiner HL. Inhibition of autoimmune diabetes by oral administration of anti-CD3 monoclonal antibody. Diabetes. 2007; 56:2103-9.
6. + follicular helper T cells. Lupus. 2009; 18:586-96.
7. Ross R. Atherosclerosis - an inflammatory disease. N Engl J Med. 1999; 340:115-26.
8. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006; 6:508-19.
9. Tabas I, Williams KJ, Boren J. Subendothelial lipoprotein retention as the initiating process in atherosclerosis: update and therapeutic implications. Circulation. 2007; 116:1832-44.
10. Binder CJ, Chang MK, Shaw PX, Miller YI, Hartvigsen K, Dewan A, Witztum JL. Innate and acquired immunity in atherogenesis. Na Med. 2002; 8:1218-26.
11. 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; 106:1708-15.
12. George J, Yacov N, Breitbart E, Bangio L, Shaish A, Gilburd B, Shoenfeld Y, Harats D. Suppression of early atherosclerosis in LDL-receptor deficient mice by oral tolerance with beta 2-glycoprotein I. Cardiovas Res. 2004; 62:603-9.
13. 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; 114:1968-76.
14. van Puijvelde GH, van Es T, van Wanrooij EJ, Habets KL, de Vos P, van der Zee R, van Eden W, van Berkel TJ, Kuiper J. Induction of oral tolerance to HSP60 or an HSP60-peptide activates T cell regulation and reduces atherosclerosis. Arterioscler Thromb Vasc Biol. 2007; 27:2677-83.
15. Xiong Q, Li J, Jin L, Liu J, Li T. 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. 2009; 125:40-5.
16. Tian J, Atkinson MA, Clare-Salzler M, Herschenifeld A, Forsthuber T, Lehmann PV, Kaufman DL. Nasal administration of glutamate decarboxylase (GAD65) peptides induces Th2 responses and prevents murine insulin-dependent diabetes. J Exp Med. 1996; 183:1561-7.
17. Garcia G, Komagata Y, Slavin AJ, Maron R, Weiner HL. Suppression of collagen-induced arthritis by oral or nasal administration of type-II collagen. J Autoimmun. 1999; 13:315-24.
18. Nussenblatt R. Orally and nasally induced tolerance studies in ocular inflammatory disease: guidance for future interventions. Ann N Y Acad Sci. 2004; 1029:278-85.
19. Broere F, Wieten L, Klein Koerkamp EI, van Roon JA, Guichelaar T, Lafeber FP, van Eden W. Oral or nasal antigen induces regulatory T cells that suppress arthritis and proliferation of arthritogenic Tcells in joint draining lymph nodes. J Immunol. 2008; 181:899-906.
20. + regulatory T cells and is enhanced by administration of an emulsome-based Th2-skewing adjuvant. J Immunol. 2010; 185:3401-7.
21. Redgrave TG, Roberts DC, West CE. Separation of plasma lip-oproteins by density-gradient ultracentrifugation. Anal Biochem. 1975; 65:42-9.
22. Holven KB, Aukrust P, Holm T, Ose L, Nenseter MS. Folic acid treatment reduces chemokine release from peripheral blood mono-nuclear cells in hyperhomocysteinemic subjects. Arterioscler Thromb Vasc Biol. 2002; 22:699-703.
23. Wolvers DA, Coenen-de Roo CJ, Mebius RE, van der Cammen MJ, Tirion F, Miltenburg AM, Kraal G. Intranasal induced immu-nological tolerance is determined by characteristics of the draining lymph nodes: studies with OVA and human cartilage gp-39. J Immunol. 1999; 162:1994-8.
24. Cheng X, Chen Y, Xie JJ, Yao R, Yu X, Liao MY, Ding YJ, Tang TT, Liao YH, Cheng Y. Suppressive oligodeoxynucleotides inhibit atherosclerosis in ApoE(-/-) mice through modulation of Th1/Th2 balance. J Mol Cell Cardiol. 2008; 45:168-75.
25. Chang MK, Binder CJ, Miller YI, Subbanagounder G, Silverman GJ, Berliner JA, Witztum JL. Apoptotic cells with oxidation-specific epitopes are immunogenic and proinflammatory. J Exp Med. 2004; 200:1359-70.
26. Tang H, Zhong Y, Zhu Y, Zhao F, Cui X, Wang Z. Low responder T cell susceptibility to the suppressive function of regulatory T cells in patients with dilated cardiomyopathy. Heart. 2010; 96:765-71.
27. Salonen JT, Ylä-Herttuala S, Yamamoto R, Butler S, Korpela H, Salonen R, Nyyssänen K, Palinski W, Witztum JL. Autoantibody against oxidised LDL and progression of carotid atherosclerosis. Lancet. 1992; 339:883-7.
28. Ylä-Herttuala S, Palinski W, Butler SW, Picard S, Steinberg D, Witztum JL. Rabbit and human atherosclerotic lesions contain IgG that recognizes epitopes of oxidized LDL. Arterioscler Thromb. 1994; 14:32-40.
29. Stemme S, Faber B, Holm J, Wiklund O, Witztum JL, Hansson GK. T lymphocytes from human atherosclerotic plaques recognize oxidized low density lipoprotein. Proc Natl Acad Sci USA. 1995; 92:3893-7.
30. Mallat Z, Taleb S, Ait-Oufella H, Tedgui A. The role of adaptive T cell immunity in atherosclerosis. J Lipi Res. 2009; 50:S364-9.
31. Ma CG, Zhang GX, Xiao BG, Link J, Olsson T, Link H. Suppression of experimental autoimmune myasthenia gravis by nasal administration of acetylcholine receptor. J Neuroim-munol. 1995; 58:51-60.
32. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J, Merval R, Esposito B, Cohen JL, Fisson S, Flavell RA, Hasson GK, Klatzmann D, Tedgui A, Mallat Z. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med. 2006; 12:178-80.
33. Ji QW, Guo M, Zheng JS, Mao XB, Peng YD, Li SN, Liang ZS, Dai ZY, Mao Y, Zeng QT. Downregulation of T helper cell type 3 in patients with acute coronary syndrome. Arch Med Res. 2009; 40:285-93.
34. -/mice. Circulation. 2003; 108:1232-7.
35. Klingenberg R, Lebens M, Hermansson A, Fredrikson GN, Strodth-off D, Rudling M, Ketelhuth DF, Gerdes N, Holmgren J, Nilsson J, Hansson GK. Intranasal immunization with an ApoB-100 fusion protein induces antigen-specific regulatory T cells and reduces atherosclerosis. Arterioscler Thromb Vasc Biol. 2010; 30:946-52.
36. Chen ML, Yan BS, Bando Y, Kuchroo VK, Weiner HL. Latency-Associated Peptide Identifies a Novel CD4+CD25+Regulatory T Cell Subset with TGFβ-Mediated Function and Enhanced Suppression of Experimental Autoimmune Encephalomyelitis. J Immunol. 2008; 180:7327-37.
37. Park H, Li Z, Yang XO, Chang SH, Nurieva R, Wang YH, Wang Y, Hood L, Zhu Z, Tian Q, Dong C. A distinct lineage of CD4 T cells regulates tissue inflammation by producing interleukin 17. Nat Immunol. 2005; 6:1133-41.
38. Robertson AK, Rudling M, Zhou X, Gorelik L, Flavell RA, Hansson GK. Disruption of TGF-beta signaling in T cells accelerates atherosclerosis. J Clin Invest. 2003; 112:1342-50.
39. Bettelli E, Carrier Y, Gao W, Korn T, Strom TB, Oukka M, Weiner HL, Kuchroo VK. Reciprocal developmental pathways for the generation of pathogenic effector TH17 and regulatory T cells. Nature. 2006; 441:235-8.
40. Powrie F, Carlino J, Leach MW, Mauze S, Coffman RL. A critical role for transforming growth factor-beta but not inter-leukin 4 in the suppression of T helper type 1-mediated colitis by CD45RB(low) CD4+ T cells. J Exp Med. 1996; 183:2669-74.