Peak inflammation in atherosclerosis, primary biliary cirrhosis and autoimmune arthritis is counter-intuitively associated with regulatory T cell enrichment

Immunobiology

Volumn 220, Issue 8, 2015, Pages 1025-1029

  Garetto, Stefano ^a   Trovato, Anna Elisa ^a   Lleo, Ana ^a,b   Sala, Federica ^b   Martini, Elisa ^a   Betz, Alexander G ^c   Norata, Giuseppe D ^b,d,e   Invernizzi, Pietro ^a,f   Kallikourdis, Marinos ^a,b  

^a HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^b UNIVERSITY OF MILAN   (Italy)

^c MRC LABORATORY OF MOLECULAR BIOLOGY   (United Kingdom)

^d Ospedale Bassini   (Italy)

^e QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^f UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Atherosclerosis; Autoimmunity; Inflammation; Primary biliary cirrhosis; Regulatory T cells; Rheumatoid arthritis

Indexed keywords

CYTOKINE; LOW DENSITY LIPOPROTEIN RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; AUTOIMMUNITY; BIOACCUMULATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DISEASE ASSOCIATION; DISEASE MODEL; FEMALE; LYMPHATIC DRAINAGE; LYMPHOCYTE COUNT; LYMPHOCYTE FUNCTION; MOUSE; NONHUMAN; PRIMARY BILIARY CIRRHOSIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; RHEUMATOID ARTHRITIS; ADVERSE EFFECTS; ANIMAL; ARTHRITIS; ATHEROGENIC DIET; BILIARY CIRRHOSIS; C57BL MOUSE; CELL PROLIFERATION; DISEASE COURSE; GENETICS; HUMAN; IMMUNOLOGY; INFLAMMATION; KNOCKOUT MOUSE;

ANIMALS; ARTHRITIS; ATHEROSCLEROSIS; AUTOIMMUNE DISEASES; CELL PROLIFERATION; DIET, ATHEROGENIC; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FEMALE; HUMANS; INFLAMMATION; LIVER CIRRHOSIS, BILIARY; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; RECEPTORS, LDL; T-LYMPHOCYTES, REGULATORY;

EID: 84929955232     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2015.02.006     Document Type: Article

References (38)

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., Flavell R.A., Hansson G.K., Klatzmann D., Tedgui A., Mallat Z. Natural regulatory T cells control the development of atherosclerosis in mice. Nat. Med. 2006, 12:178-180.
2. Allan S.E., Broady R., Gregori S., Himmel M.E., Locke N., Roncarolo M.G., Bacchetta R., Levings M.K. CD4+ T-regulatory cells: toward therapy for human diseases. Immunol. Rev. 2008, 223:391-421.
3. Ammirati E., Cianflone D., Vecchio V., Banfi M., Vermi A.C., De Metrio M., Grigore L., Pellegatta F., Pirillo A., Garlaschelli K., Manfredi A.A., Catapano A.L., Maseri A., Palini A.G., Norata G.D. Effector memory T cells are associated with atherosclerosis in humans and animal models. J. Am. Heart Assoc. 2012, 1:27-41.
4. Benito-Miguel M., Garcia-Carmona Y., Balsa A., Perez de Ayala C., Cobo-Ibanez T., Martin-Mola E., Miranda-Carus M.E. A dual action of rheumatoid arthritis synovial fibroblast IL-15 expression on the equilibrium between CD4+CD25+ regulatory T cells and CD4+CD25- responder T cells. J. Immunol. 2009, 183:8268-8279.
5. Chen G.Y., Chen C., Wang L., Chang X., Zheng P., Liu Y. Cutting edge: broad expression of the FoxP3 locus in epithelial cells: a caution against early interpretation of fatal inflammatory diseases following in vivo depletion of FoxP3-expressing cells. J. Immunol. 2008, 180:5163-5166.
6. Germain R.N. Maintaining system homeostasis: the third law of Newtonian immunology. Nat. Immunol. 2012, 13:902-906.
7. Hori S. Regulatory T cell plasticity: beyond the controversies. Trends Immunol. 2011, 32:295-300.
8. Humby F., Bombardieri M., Manzo A., Kelly S., Blades M.C., Kirkham B., Spencer J., Pitzalis C. Ectopic lymphoid structures support ongoing production of class-switched autoantibodies in rheumatoid synovium. PLoS Med. 2009, 6. e1.
9. Ji H.B., Liao G., Faubion W.A., Abadia-Molina A.C., Cozzo C., Laroux F.S., Caton A., Terhorst C. Cutting edge: the natural ligand for glucocorticoid-induced TNF receptor-related protein abrogates regulatory T cell suppression. J. Immunol. 2004, 172:5823-5827.
10. Kallikourdis M., Betz A.G. Periodic accumulation of regulatory T cells in the uterus: preparation for the implantation of a semi-allogeneic fetus?. PLoS ONE 2007, 2:e382.
11. Klingenberg R., Lebens M., Hermansson A., Fredrikson G.N., Strodthoff D., Rudling M., Ketelhuth D.F., Gerdes N., Holmgren J., Nilsson J., Hansson G.K. 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.
12. Ko H.J., Cho M.L., Lee S.Y., Oh H.J., Heo Y.J., Moon Y.M., Kang C.M., Kwok S.K., Ju J.H., Park S.H., Park K.S., Kim H.Y. CTLA4-Ig modifies dendritic cells from mice with collagen-induced arthritis to increase the CD4+CD25+Foxp3+ regulatory T cell population. J. Autoimmun. 2010, 34:111-120.
13. Kofler S., Sisic Z., Shvets N., Lohse P., Weis M. Expression of circulatory dendritic cells and regulatory T-cells in patients with different subsets of coronary artery disease. J. Cardiovasc. Pharmacol. 2011, 57:542-549.
14. Korn T., Reddy J., Gao W., Bettelli E., Awasthi A., Petersen T.R., Backstrom B.T., Sobel R.A., Wucherpfennig K.W., Strom T.B., Oukka M., Kuchroo V.K. Myelin-specific regulatory T cells accumulate in the CNS but fail to control autoimmune inflammation. Nat. Med. 2007, 13:423-431.
15. Lan R.Y., Cheng C., Lian Z.X., Tsuneyama K., Yang G.X., Moritoki Y., Chuang Y.H., Nakamura T., Saito S., Shimoda S., Tanaka A., Bowlus C.L., Takano Y., Ansari A.A., Coppel R.L., Gershwin M.E. Liver-targeted and peripheral blood alterations of regulatory T cells in primary biliary cirrhosis. Hepatology 2006, 43:729-737.
16. Liston A., Gray D.H. Homeostatic control of regulatory T cell diversity. Nat. Rev. Immunol. 2014, 14:154-165.
17. Maganto-Garcia E., Tarrio M.L., Grabie N., Bu D.X., Lichtman A.H. Dynamic changes in regulatory T cells are linked to levels of diet-induced hypercholesterolemia. Circulation 2011, 124:185-195.
18. Miyao T., Floess S., Setoguchi R., Luche H., Fehling H.J., Waldmann H., Huehn J., Hori S. Plasticity of Foxp3(+) T cells reflects promiscuous Foxp3 expression in conventional T cells but not reprogramming of regulatory T cells. Immunity 2012, 36:262-275.
19. Morgan M.E., Flierman R., van Duivenvoorde L.M., Witteveen H.J., van Ewijk W., van Laar J.M., de Vries R.R., Toes R.E. Effective treatment of collagen-induced arthritis by adoptive transfer of CD25+ regulatory T cells. Arthritis Rheum. 2005, 52:2212-2221.
20. Mottonen M., Heikkinen J., Mustonen L., Isomaki P., Luukkainen R., Lassila O. CD4+ CD25+ T cells with the phenotypic and functional characteristics of regulatory T cells are enriched in the synovial fluid of patients with rheumatoid arthritis. Clin. Exp. Immunol. 2005, 140:360-367.
21. Munoz-Suano A., Kallikourdis M., Sarris M., Betz A.G. Regulatory T cells protect from autoimmune arthritis during pregnancy. J. Autoimmun. 2012, 38:J103-J108.
22. Nguyen L.T., Jacobs J., Mathis D., Benoist C. Where FoxP3-dependent regulatory T cells impinge on the development of inflammatory arthritis. Arthritis Rheum. 2007, 56:509-520.
23. Nie H., Zheng Y., Li R., Guo T.B., He D., Fang L., Liu X., Xiao L., Chen X., Wan B., Chin Y.E., Zhang J.Z. Phosphorylation of FOXP3 controls regulatory T cell function and is inhibited by TNF-alpha in rheumatoid arthritis. Nat. Med. 2013, 19:322-328.
24. Norata G.D., Venu V.K., Callegari E., Paloschi V., Catapano A.L. Effect of Tie-2 conditional deletion of BDNF on atherosclerosis in the ApoE null mutant mouse. Biochim. Biophys. Acta 2012, 1822:927-935.
25. Notley C.A., Ehrenstein M.R. The yin and yang of regulatory T cells and inflammation in RA. Nat. Rev. Rheumatol. 2010, 6:572-577.
26. Patel S., Chung S.H., White G., Bao S., Celermajer D.S. The atheroprotective mediators apolipoprotein A-I and Foxp3 are over-abundant in unstable carotid plaques. Int. J. Cardiol. 2010, 145:183-187.
27. Rubtsov Y.P., Niec R.E., Josefowicz S., Li L., Darce J., Mathis D., Benoist C., Rudensky A.Y. Stability of the regulatory T cell lineage in vivo. Science 2010, 329:1667-1671.
28. Ruprecht C.R., Gattorno M., Ferlito F., Gregorio A., Martini A., Lanzavecchia A., Sallusto F. Coexpression of CD25 and CD27 identifies FoxP3+ regulatory T cells in inflamed synovia. J. Exp. Med. 2005, 201:1793-1803.
29. Sakaki M., Hiroishi K., Baba T., Ito T., Hirayama Y., Saito K., Tonoike T., Kushima M., Imawari M. Intrahepatic status of regulatory T cells in autoimmune liver diseases and chronic viral hepatitis. Hepatol. Res. 2008, 38:354-361.
30. Sasaki M., Ikeda H., Sawada S., Sato Y., Nakanuma Y. Naturally-occurring regulatory T cells are increased in inflamed portal tracts with cholangiopathy in primary biliary cirrhosis. J. Clin. Pathol. 2007, 60:1102-1107.
31. Sharma M.D., Hou D.Y., Baban B., Koni P.A., He Y., Chandler P.R., Blazar B.R., Mellor A.L., Munn D.H. Reprogrammed foxp3(+) regulatory T cells provide essential help to support cross-presentation and CD8(+) T cell priming in naive mice. Immunity 2010, 33:942-954.
32. Torgerson T.R. Regulatory T cells in human autoimmune diseases. Springer Semin. Immunopathol. 2006, 28:63-76.
33. van Amelsfort J.M., Jacobs K.M., Bijlsma J.W., Lafeber F.P., Taams L.S. CD4(+)CD25(+) regulatory T cells in rheumatoid arthritis: differences in the presence, phenotype, and function between peripheral blood and synovial fluid. Arthritis Rheum. 2004, 50:2775-2785.
34. Wakabayashi K., Lian Z.X., Leung P.S., Moritoki Y., Tsuneyama K., Kurth M.J., Lam K.S., Yoshida K., Yang G.X., Hibi T., Ansari A.A., Ridgway W.M., Coppel R.L., Mackay I.R., Gershwin M.E. Loss of tolerance in C57BL/6 mice to the autoantigen E2 subunit of pyruvate dehydrogenase by a xenobiotic with ensuing biliary ductular disease. Hepatology 2008, 48:531-540.
35. Wang D., Zhang H., Liang J., Gu Z., Zhou Q., Fan X., Hou Y., Sun L. CD4+ CD25+ but not CD4+ Foxp3+ T cells as a regulatory subset in primary biliary cirrhosis. Cell Mol. Immunol. 2010, 7:485-490.
36. Weih F., Grabner R., Hu D., Beer M., Habenicht A.J. Control of dichotomic innate and adaptive immune responses by artery tertiary lymphoid organs in atherosclerosis. Front. Physiol. 2012, 3:226.
37. Wing K., Sakaguchi S. Regulatory T cells exert checks and balances on self tolerance and autoimmunity. Nat. Immunol. 2010, 11:7-13.
38. Zhang W., Sharma R., Ju S.T., He X.S., Tao Y., Tsuneyama K., Tian Z., Lian Z.X., Fu S.M., Gershwin M.E. Deficiency in regulatory T cells results in development of antimitochondrial antibodies and autoimmune cholangitis. Hepatology 2009, 49:545-552.