Impaired regulatory T-cell response and enhanced atherosclerosis in the absence of inducible costimulatory molecule

Circulation

Volumn 114, Issue 19, 2006, Pages 2047-2055

  Gotsman, Israel ^a   Grabie, Nir ^a   Gupta, Rajat ^a   Dacosta, Rosa ^a   MacConmara, Malcolm ^a   Lederer, James ^a   Sukhova, Galina ^a   Witztum, Joseph L ^b   Sharpe, Arlene H ^a   Lichtman, Andrew H ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Atherosclerosis; Cells; Immune systems; Inflammation; Leukocytes; Lymphocytes

Indexed keywords

GAMMA INTERFERON; TRANSCRIPTION FACTOR FOXP3; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ATHEROSCLEROSIS; BONE MARROW; CELL PROLIFERATION; CELL STIMULATION; CELLULAR IMMUNITY; IMMUNE RESPONSE; MACROPHAGE; MOLECULAR DYNAMICS; MOUSE; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; WILD TYPE;

ANIMALS; ANTIGENS, DIFFERENTIATION, T-LYMPHOCYTE; ATHEROSCLEROSIS; CELLS, CULTURED; FEMALE; LYMPHOCYTE DEPLETION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; T-LYMPHOCYTES, REGULATORY;

EID: 33750692702     PISSN: 00097322     EISSN: None     Source Type: Journal    
DOI: 10.1161/CIRCULATIONAHA.106.633263     Document Type: Article

References (40)

1. Hansson GK. Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21:1876-1890.
2. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol. 2006;6:508-519.
3. Zhou X, Robertson AK, Rudling M, Parini P, Hansson GK. Lesion development and response to immunization reveal a complex role for CD4 in atherosclerosis. Circ Res. 2005;96:427-434.
4. Zhou X, Robertson AK, Hjerpe C, Hansson GK. Adoptive transfer of CD4+ T cells reactive to modified low-density lipoprotein aggravates atherosclerosis. Arterioscler Thromb Vasc Biol. 2006;26:864-870.
5. Buono C, Lichtman AH. Co-stimulation and plaque-antigen-specific T-cell responses in atherosclerosis. Trends Cardiovasc Med. 2004;14:166-172.
6. Buono C, Pang H, Uchida Y, Libby P, Sharpe A, Lichtman AH. B7-1/B7-2 co-stimulation regulates plaque antigen-specific T cell responses and atherogenesis in LDLR-deficient mice. Circulation. 2004;109:2009-2015.
7. Dong C, Juedes AE, Temann UA, Shresta S, Allison JP, Ruddle NH, Flavell RA. ICOS co-stimulatory receptor is essential for T-cell activation and function. Nature. 2001;409:97-101.
8. Vieira PL, Wassink L, Smith LM, Nam S, Kingsbury GA, Gutierrez-Ramos JC, Coyle AJ, Kapsenberg ML, Wierenga EA. ICOS-mediated signaling regulates cytokine production by human T cells and provides a unique signal to selectively control the clonal expansion of Th2 helper cells. Eur J Immunol. 2004;34:1282-1290.
9. Nurieva RI, Duong J, Kishikawa H, Dianzani U, Rojo JM, Ho I, Flavell RA, Dong C. Transcriptional regulation of Th2 differentiation by inducible costimulator. Immunity. 2003;18:801-811.
10. Lohning M, Hutloff A, Kallinich T, Mages HW, Bonhagen K, Radbruch A, Hamelmann E, Kroczek RA. Expression of ICOS in vivo defines CD4+ effector T cells with high inflammatory potential and a strong bias for secretion of interleukin 10. J Exp Med. 2003;197:181-193.
11. Herman AE, Freeman GJ, Mathis D, Benoist C. CD4+CD25+ T regulatory cells dependent on ICOS promote regulation of effector cells in the prediabetic lesion. J Exp Med. 2004;199:1479-1489.
12. Kohyama M, Sugahara D, Sugiyama S, Yagita H, Okumura K, Hozumi N. Inducible costimulator-dependent IL-10 production by regulatory T cells specific for self-antigen. Proc Natl Acad Sci U S A. 2004;101:4192-4197.
13. Tafuri A, Shahinian A, Bladt F, Yoshinaga SK, Jordana M, Wakeham A, Boucher LM, Bouchard D, Chan VS, Duncan G, Odermatt B, Ho A, Itie A, Horan T, Whoriskey JS, Pawson T, Penninger JM, Ohashi PS, Mak TW. ICOS is essential for effective T-helper-cell responses. Nature. 2001;409:105-109.
14. McAdam AJ, Greenwald RJ, Levin MA, Chernova T, Malenkovich N, Ling V, Freeman GJ, Sharpe AH. ICOS is critical for CD40-mediated antibody class switching. Nature. 2001;409:102-105.
15. Heller EA, Liu E, Tager AM, Yuan Q, Lin AY, Ahluwalia N, Jones K, Koehn SL, Lok VM, Aikawa E, Moore KJ, Luster AD, Gerszten RE. Chemokine CXCL10 promotes atherogenesis by modulating the local balance of effector and regulatory T cells. Circulation. 2006;113:2301-2312.
16. 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.
17. Buono C, Come CE, Stavrakis G, Maguire GF, Connelly PW, Lichtman AH. Influence of interferon-gamma on the extent and phenotype of diet-induced atherosclerosis in the LDLR-deficient mouse. Arterioscler Thromb Vasc Biol. 2003;23:454-460.
18. Lee TS, Yen HC, Pan CC, Chau LY. The role of interleukin 12 in the development of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 1999;19:734-742.
19. 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;112:1342-1350.
20. Binder CJ, Hartvigsen K, Chang M-K, 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.
21. Horkko S, Bird DA, Miller E, Itabe H, Leitinger N, Subbanagounder G, Berliner JA, Friedman P, Dennis EA, Curtiss LK, Palinski W, Witztum JL. Monoclonal autoantibodies specific for oxidized phospholipids or oxidized phospholipid-protein adducts inhibit macrophage uptake of oxidized low-density lipoproteins. J Clin Invest. 1999;103:117-128.
22. Lichtman AH, Clinton SK, Iiyama K, Connelly PW, Libby P, Cybulsky MI. Hyperlipidemia and atherosclerotic lesion development in LDL receptor-deficient mice fed defined semipurified diets with and without cholate. Arterioscler Thromb Vasc Biol. 1999;19:1938-1944.
23. Paigen B, Morrow A, Holmes PA, Mitchell D, Williams RA. Quantitative assessment of atherosclerotic lesions in mice. Atherosclerosis. 1987;68:231-240.
24. Grabie N, Delfs MW, Westrich JR, Love VA, Stavrakis G, Ahmad F, Seidman CE, Seidman JG, Lichtman AH. IL-12 is required for differentiation of pathogenic CD8+ T cell effectors that cause myocarditis. J Clin Invest. 2003;111:671-680.
25. Usui S, Hara Y, Hosaki S, Okazaki M. A new on-line dual enzymatic method for simultaneous quantification of cholesterol and triglycerides in lipoproteins by HPLC. J Lipid Res. 2002;43:805-814.
26. Binder CJ, Horkko S, Dewan A, Chang MK, Kieu EP, Goodyear CS, Shaw PX, Palinski W, Witztum JL, Silverman GJ. Pneumococcal vaccination decreases atherosclerotic lesion formation: molecular mimicry between Streptococcus pneumoniae and oxidized LDL. Nat Med. 2003;9:736-743.
27. Chen R, Lowe L, Wilson JD, Crowther E, Tzeggai K, Bishop JE, Varro R. Simultaneous quantification of six human cytokines in a single sample using microparticle-based flow cytometric technology. Clin Chem. 1999;45:1693-1694.
28. Giulietti A, Overbergh L, Valckx D, Decallonne B, Bouillon R, Mathieu C. An overview of real-time quantitative PCR: applications to quantify cytokine gene expression. Methods. 2001;25:386-401.
29. Schiller NK, Kubo N, Boisvert WA, Curtiss LK. Effect of gamma-irradiation and bone marrow transplantation on atherosclerosis in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol. 2001;21:1674-1680.
30. McAdam AJ, Chang TT, Lumelsky AE, Greenfield EA, Boussiotis VA, Duke-Cohan JS, Chernova T, Malenkovich N, Jabs C, Kuchroo VK, Ling V, Collins M, Sharpe AH, Freeman GJ. Mouse inducible costimulatory molecule (ICOS) expression is enhanced by CD28 costimulation and regulates differentiation of CD4+ T cells. J Immunol. 2000;165:5035-5040.
31. Bonhagen K, Liesenfeld O, Stadecker MJ, Hutloff A, Erb K, Coyle AJ, Lipp M, Kroczek RA, Kamradt T. ICOS+ Th cells produce distinct cytokines in different mucosal immune responses. Eur J Immunol. 2003;33:392-401.
32. Wassink L, Vieira PL, Smits HH, Kingsbury GA, Coyle AJ, Kapsenberg ML, Wierenga EA. ICOS expression by activated human Th cells is enhanced by IL-12 and IL-23: increased ICOS expression enhances the effector function of both Th1 and Th2 cells. J Immunol. 2004;173:1779-1786.
33. Sakaguchi S. Naturally arising CD4+ regulatory T cells for immunologic self-tolerance and negative control of immune responses. Annu Rev Immunol. 2004;22:531-562.
34. Fontenot JD, Rudensky AY. A well adapted regulatory contrivance: regulatory T cell development and the forkhead family transcription factor Foxp3. Nat Immunol. 2005;6:331-337.
35. Akbari O, Freeman GJ, Meyer EH, Greenfield EA, Chang TT, Sharpe AH, Berry G, DeKruyff RH, Umetsu DT. Antigen-specific regulatory T cells develop via the ICOS-ICOS-ligand pathway and inhibit allergen-induced airway hyperreactivity. Nat Med. 2002;8:1024-1032.
36. Miyamoto K, Kingsley CI, Zhang X, Jabs C, Izikson L, Sobel RA, Weiner HL, Kuchroo VK, Sharpe AH. The ICOS molecule plays a crucial role in the development of mucosal tolerance. J Immunol. 2005;175:7341-7347.
37. Afek A, Harats D, Roth A, Keren G, George J. A functional role for inducible costimulator (ICOS) in atherosclerosis. Atherosclerosis. 2005;183:57-63.
38. Li MO, Wan YY, Sanjabi S, Robertson AK, Flavell RA. Transforming growth factor-beta regulation of immune responses. Annu Rev Immunol. 2006;24:99-146.
39. Chen W, Jin W, Hardegen N, Lei KJ, Li L, Marinos N, McGrady G, Wahl SM. Conversion of peripheral CD4+CD25- naive T cells to CD4+CD25+ regulatory T cells by TGF-beta induction of transcription factor Foxp3. J Exp Med. 2003;198:1875-1886.
40. Wan YY, Flavell RA. Identifying Foxp3-expressing suppressor T cells with a bicistronic reporter. Proc Natl Acad Sci U S A. 2005;102:5126-5131.