Regulatory T cell responses: Potential role in the control of atherosclerosis

Current Opinion in Lipidology

Volumn 16, Issue 5, 2005, Pages 518-524

  Mallat, Ziad ^a   Ait Oufella, Hafid ^a   Tedgui, Alain ^a  

^a INSERM   (France)

Author keywords

Atherosclerosis; Immunity; Inflammation; Lymphocyte

Indexed keywords

INTERLEUKIN 10; TRANSFORMING GROWTH FACTOR BETA;

ADOPTIVE IMMUNOTHERAPY; ATHEROSCLEROSIS; CELL DIFFERENTIATION; DISEASE COURSE; DRUG INHIBITION; DRUG MECHANISM; HUMAN; HUMORAL IMMUNITY; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; IMMUNOREGULATION; IMMUNOSUPPRESSIVE TREATMENT; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; T LYMPHOCYTE; TH1 CELL; TH2 CELL;

EID: 25444463325     PISSN: 09579672     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.mol.0000182532.11512.90     Document Type: Review

References (81)

1. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005; 352:1685-1695. An excellent, updated review of our current understanding of the pathogenesis of atherosclerosis.
2. Binder CJ, Chang MK, Shaw PX, et al. Innate and acquired immunity in atherogenesis. Nat Med 2002; 8:1218-1226.
3. Dansky HM, Charlton SA, Harper MM, Smith JD. T and B lymphocytes play a minor sole in atherosclerotic plaque formation in the apolipoprotein E-deficient mouse. Proc Natl Acad Sci USA 1997; 94:4642-4646.
4. Daugherty A, Pure E, Delfel-Butteiger D, et al. The effects of total lymphocyte deficiency on the extent of atherosclerosis in apolipoprotein E-/- mice. J Clin Invest 1997; 100:1575-1580.
5. Song L, Leung C, Schindler C. Lymphocytes are important in early atherosclerosis. J Clin Invest 2001; 108:251-259.
6. Reardon CA, Blachowicz L, White T, et al. Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol 2001; 21:1011-1016.
7. Zhou X, Nicoletti A, Elhage R, Hansson GK. Transfer of CD4(+) T cells aggravates atherosclerosis in immunodeficient apolipoprotein E knockout mice. Circulation 2000; 102:2919-2922.
8. Banchereau J, Pulendran B, Steinman R, Palucka K. Will the making of plasmacytoid dendritic cells in vitro help unravel their mysteries? J Exp Med 2000; 192:F39-F44.
9. Maldonado-Lopez R, De Smedt T, Michel P, et al. CD8alpha+ and CD8alpha- subclasses of dendritic cells direct the development of distinct T helper cells in vivo. J Exp Med 1999; 189:587-592.
10. Mach F, Schonbeck U, Sukhova GK, et al. Reduction of atherosclerosis in mice by inhibition of CD40 signalling. Nature 1998; 394:200-203.
11. Lutgens E, Gorelik L, Daemen MJ, et al. Requirement for CD154 in the progression of atherosclerosis. Nat Med 1999; 5:1313-1316.
12. Mallat Z, Corbaz A, Scoazec A, et al. Interleukin-18/interleukin-18 binding protein signaling modulates atherosclerotic lesion development and stability. Circ Res 2001; 89:E41-E45.
13. Whitman SC, Ravisankar P, Daugherty A. Interleukin-18 enhances atherosclerosis in apolipoprotein E(-/-) mice through release of interferon-gamma. Circ Res 2002; 90:E34-E38.
14. Elhage R, Jawien J, Rudling M, et al. Reduced atherosclerosis in interleukin-18 deficient apolipoprotein E-knockout mice. Cardiovasc Res 2003; 59:234-240.
15. de Nooijer R, von der Thusen JH, Verkleij CJ, et al. Overexpression of IL-18 decreases intimal collagen content and promotes a vulnerable plaque phenotype in apolipoprotein-E-deficient mice. Arterioscler Thromb Vasc Biol 2004; 24:2313-2319.
16. Buono C, Binder CJ, Stavrakis G, et al. T-bet deficiency reduces atherosclerosis and alters plaque antigen-specific immune responses. Proc Natl Acad Sci USA 2005; 102:1596-1601. This work identified an important role for the Th1 transcription factor in experimental atherosclerosis.
17. Schonbeck U, Sukhova GK, Shimizu K, et al. Inhibition of CD40 signalings limits evolution of established atherosclerosis in mice. Proc Natl Acad Sci USA 2000; 97:7458-7463.
18. Lutgens E, Cleutjens KB, Heeneman S, et al. Both early and delayed anti-CD40L antibody treatment induces a stable plaque phenotype. Proc Natl Acad Sci USA 2000; 97:7464-7469.
19. Szabo SJ, Kim ST, Costa GL, et al. A novel transcription factor, T-bet, directs Th1 lineage commitment. Cell 2000; 100:655-669.
20. Zhou X, Paulsson G, Stemme S, Hansson GK. Hypercholesterolemia is associated with a T helper (Th) 1/Th2 switch of the autoimmune response in atherosclerotic apo E-knockout mice. J Clin Invest 1998; 101:1717-1725.
21. Caligiuri G, Nicoletti A, Poirier B, Hansson GK. Protective immunity against atherosclerosis carried by B cells of hypercholesterolemic mice. J Clin Invest 2002; 109:745-753.
22. 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.
23. Ameli S, Hultgardhnilsson A, Regnstrom J, et al. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol 1996; 16:1074-1079.
24. Freigang S, Horkko S, Miller E, et al. Immunization of LDL receptor-deficient mice with homologous malondialdehyde-modified and native LDL reduces progression of atherosclerosis by mechanisms other than induction of high titers of antibodies to oxidative neoepitopes. Arterioscler Thromb Vasc Biol 1998; 18:1972-1982.
25. George J, Afek A, Gilburd B, et al. Hyperimmunization of apo-E-deficient mice with homologous malondialdehyde low-density lipoprotein suppresses early atherogenesis. Atherosclerosis 1998; 138:147-152.
26. Hansen PR, Chew M, Zhou J, et al. Freunds adjuvant alone is antiatherogenic in apoE-deficient mice and specific immunization against TNFalpha confers no additional benefit. Atherosclerosis 2001; 158:87-94.
27. Binder CJ, Hartvigsen K, Chang MK, et al. IL-5 links adaptive and natural immunity specific for epitopes of oxidized LDL and protects from atherosclerosis. J Clin Invest 2004; 114:427-437. An important work showing a critical role for the Th2 cytokine interleukin-5 in the activation of B1 cells to produce anti-oxLDL autoantibodies.
28. Binder CJ, Shaw PX, Chang MK, et al. Thematic review series: The Immune System and Atherogenesis. The role of natural antibodies in atherogenesis. J Lipid Res 2005; 46:1353-1363. An excellent review on the role of natural antibodies specific for oxidized phospholipid epitopes common to bacteria, apoptotic cells and oxidized lipids in atherogenesis.
29. Pinderski LJ, Fischbein MP, Subbanagounder G, et al. Overexpression of interleukin-10 by activated T lymphocytes inhibits atherosclerosis in LDL receptor-deficient mice by altering lymphocyte and macrophage phenotypes. Circ Res 2002; 90:1064-1071.
30. Huber SA, Sakkinen P, David C, et al. T helper-cell phenotype regulates atherosclerosis in mice under conditions of mild hypercholesterolemia. Circulation 2001; 103:2610-2616.
31. King VL, Szilvassy SJ, Daugherty A. Interleukin-4 deficiency decreases atherosclerotic lesion formation in a site-specific manner in female LDL receptor-/- mice. Arterioscler Thromb Vasc Biol 2002; 22:456-461.
32. Davenport P, Tipping PG. The role of interleukin-4 and interleukin-12 in the progression of atherosclerosis in apolipoprotein E-deficient mice. Am J Pathol 2003; 163:1117-1125.
33. Mallat Z, Tedgui A. Immunomodulation to combat atherosclerosis: the potential role of immune regulatory cells. Expert Opin Biol Ther 2004; 4: 1387-1393. This works proposes a novel view of atherosclerosis where regulatory immunity plays a critical role.
34. Sakaguchi S. Naturally arising Foxp3-expressing CD25+CD4+ regulatory T cells in immunological tolerance to self and non-self. Nat Immunol 2005; 6:345-352. Excellent review of our understanding of the development of natural regulatory T cells.
35. Fontenot JD, Rasmussen JP, Williams LM, et al. Regulatory T cell lineage specification by the forkhead transcription factor foxp3. Immunity 2005; 22:329-341. Excellent review on the critical role of Foxp3 in the commitment of T cells to the regulatory T cell lineage.
36. von Boehmer H. Mechanisms of suppression by suppressor T cells. Nat Immunol 2005; 6:338-344. Excellent review on the various modes of suppression used by reguatory T cells.
37. Bennett CL, Christie J, Ramsdell F, et al. The immune dysregulation, polyendocrinopathy, enteropathy, X-linked syndrome (IPEX) is caused by mutations of FOXP3. Nat Genet 2001; 27:20-21.
38. Wildin RS, Ramsdell F, Peake J, et al. X-linked neonatal diabetes mellitus, enteropathy and endocrinopathy syndrome is the human equivalent of mouse scurfy. Nat Genet 2001; 27:18-20.
39. Salomon B, Lenschow DJ, Rhee L, et al. B7/CD28 costimulation is essential for the homeostasis of the CD4+CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity 2000; 12:431-440.
40. Tang Q, Henriksen KJ, Boden EK, et al. Cutting edge: CD28 controls peripheral homeostasis of CD4+CD25+ regulatory T cells. J Immunol 2003; 171:3348-3352.
41. O'Garra A, Vieira PL, Vieira P, Goldfeld AE. IL-10-producing and naturally occurring CD4+ Tregs: limiting collateral damage. J Clin Invest 2004; 114: 1372-1378. Excellent review discussing the role of antigen-induced and natural regulatory T cells in the control of effector immune responses.
42. Vieira PL, Christensen JR, Minaee S, et al. IL-10-secreting regulatory T cells do not express Foxp3 but have comparable regulatory function to naturally occurring CD4+CD25+ regulatory T cells. J Immunol 2004; 172:5986-5993.
43. Sundstedt A, O'Neill EJ, Nicolson KS, Wraith DC. Role for IL-10 in suppression mediated by peptide-induced regulatory T cells in vivo. J Immunol 2003; 170:1240-1248.
44. Akbari O, DeKruyff RH, Umetsu DT. Pulmonary dendritic cells producing IL-10 mediate tolerance induced by respiratory exposure to antigen. Nat Immunol 2001; 2:725-731.
45. Cottrez F, Groux H. Specialization in tolerance: innate CD(4+)CD(25+) versus acquired TR1 and TH3 regulatory T cells. Transplantation 2004; 77:S12-S15. An interesting review discussing the coexistence of innate and acquired regulatory T cell subtypes.
46. Wakkach A, Fournier N, Brun V, et al. Characterization of dendritic cells that induce tolerance and T regulatory 1 cell differentiation in vivo. Immunity 2003; 18:605-617.
47. Albert ML, Pearce SF, Francisco LM, et al. Immature dendritic cells phagocytose apoptotic cells via alphavbeta5 and CD36, and cross-present antigens to cytotoxic T lymphocytes. J Exp Med 1998; 188:1359-1368.
48. Albert ML, Kim JI, Birge RB. alphavbeta5 integrin recruits the CrkII-Dock 180-rac1 complex for phagocytosis of apoptotic cells. Nat Cell Biol 2000; 2: 899-905.
49. Sauter B, Albert ML, Francisco L, et al. Consequences of cell death: exposure to necrotic tumor cells, but not primary tissue cells or apoptotic cells, induces the maturation of immunostimulatory dendritic cells. J Exp Med 2000; 191: 423-434.
50. Savill J, Dransfield I, Gregory C, Haslett C. A blast from the past: clearance of apoptotic cells regulates immune responses. Nat Rev Immunol 2002; 2: 965-975.
51. Albert ML. Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat Rev Immunol 2004; 4:223-231.
52. Verbovetski I, Bychkov H, Trahtemberg U, et al. Opsonization of apoptotic cells by autologous iC3b facilitates clearance by immature dendritic cells, down-regulates DR and CD86, and up-regulates CC chemokine receptor 7. J Exp Med 2002; 196:1553-1561.
53. Sohn JH, Bora PS, Suk HJ, et al. Tolerance is dependent on complement C3 fragment iC3b binding to antigen-presenting cells. Nat Med 2003; 9: 206-212.
54. Apostolou I, Sarukhan A, Klein L, von Boehmer H. Origin of regulatory T cells with known specificity for antigen. Nat Immunol 2002; 3:756-763.
55. Chen Y, Kuchroo VK, Inobe J, et al. Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 1994; 265:1237-1240.
56. Groux H, O'Garra A, Bigler M, et al. A CD4+ T-cell subset inhibits antigen-specific T-cell responses and prevents colitis. Nature 1997; 389: 737-742.
57. Weiner HL. Oral tolerance: immune mechanisms and the generation of Th3-type TGF-beta-secreting regulatory cells. Microbes Infect 2001; 3: 947-954.
58. Green EA, Gorelik L, McGregor CM, et al. CD4+CD25+ T regulatory cells control anti-islet CD8+ T cells through TGF-beta-TGF-beta receptor interactions in type 1 diabetes. Proc Natl Acad Sci USA 2003; 100:10878-10883.
59. Chen ML, Pittet MJ, Gorelik L, et al. Regulatory T cells suppress tumor-specific CD8 T cell cytotoxicity through TGF-beta signals in vivo. Proc Natl Acad Sci USA 2005; 102:419-424.
60. Belghith M, Bluestone JA, Barriot S, et al. TGF-beta-dependent mechanisms mediate restoration of self-tolerance induced by antibodies to CD3 in overt autoimmune diabetes. Nat Med 2003; 9:1202-1208.
61. Bogdan C, Vodovotz Y, Nathan C. Macrophage deactivation by interleukin-10. J Exp Med 1991; 174:1549-1555.
62. Tedgui A, Mallat Z. Anti-inflammatory mechanisms in the vascular wall. Circ Res 2001; 88:877-887.
63. Grunig G, Corry DB, Leach MW, et al. Interleukin-10 is a natural suppressor of cytokine production and inflammation in a murine model of allergic bronchopulmonary aspergillosis. J Exp Med 1997; 185:1089-1099.
64. Cottrez F, Hurst SD, Coffman RL, Groux H. T regulatory cells 1 inhibit a Th2-specific response in vivo. J Immunol 2000; 165:4848-4853.
65. Uyemura K, Demer LL, Castle SC, et al. Cross-regulatory roles of interleukin (IL)-12 and IL-10 in atherosclerosis. J Clin Invest 1996; 97:2130-2138.
66. Mallat Z, Besnard S, Duriez M, et al. Protective role of interleukin-10 in atherosclerosis. Circ Res 1999; 85:e17-e24.
67. Pinderski Oslund LJ, Hedrick CC, et al. Interleukin-10 blocks atherosclerotic events In vitro and In vivo. Arterioscler Thromb Vasc Biol 1999; 19:2847-2853.
68. Von Der Thusen JH, Kuiper J, et al. Attenuation of atherogenesis by systemic and local adenovirus-mediated gene transfer of interleukin-10 in LDLr-/-mice. FASEB J 2001; 15:2730-2732.
69. Potteaux S, Esposito B, Van Oostrom O, et al. Leukocyte-derived interleukin 10 is required for protection against atherosclerosis in low-density lipoprotein receptor knockout mice. Arterioscler Thromb Vasc Biol 2004; 24:1474-1478.
70. Geissmann F, Revy P, Regnault A, et al. TGF-beta 1 prevents the noncognate maturation of human dendritic Langerhans cells. J Immunol 1999; 162:4567-4575.
71. Nandan D, Reiner NE. TGF-beta attenuates the class II transactivator and reveals an accessory pathway of IFN-gamma action. J Immunol 1997; 158: 1095-1101.
72. Gorelik L, Flavell RA. Abrogation of TGFbeta signaling in T cells leads to spontaneous T cell differentiation and autoimmune disease. Immunity 2000; 12:171-181.
73. Gojova A, Brun V, Esposito B, et al. Specific abrogation of transforming growth factor-(beta) signaling in T cells alters atherosclerotic lesion size and composition in mice. Blood 2003; 102:4052-4058.
74. Robertson AK, Rudling M, Zhou X, et al. Disruption of TGF-beta signaling in T cells accelerates atherosclerosis. J Clin Invest 2003; 112:1342-1350.
75. Mallat Z, Gojova A, Marchiol-Fournigault C, et al. Inhibition of transforming growth factor-beta signaling accelerates atherosclerosis and induces an unstable plaque phenotype in mice. Circ Res 2001; 89:930-934.
76. Lutgens E, Gijbels M, Smook M, et al. Transforming growth factor-beta mediates balance between inflammation and fibrosis during plaque progression. Arterioscler Thromb Vasc Biol 2002; 22:975-982.
77. Mallat Z, Tedgui A. The role of transforming growth factor beta in atherosclerosis: novel insights and future perspectives. Curr Opin Lipidol 2002; 13: 523-529.
78. Grainger DJ. Transforming growth factor beta and atherosclerosis: so far, so good for the protective cytokine hypothesis. Arterioscler Thromb Vasc Biol 2004; 24:399-404. An interesting review on the role of TGF-β as a protective cytokine in atherosclerosis.
79. Harats D, Yacov N, Gilburd B, et al. Oral tolerance with heat shock protein 65 attenuates Mycobacterium tuberculosis-induced and high-fat-diet-driven atherosclerotic lesions. J Am Coll Cardiol 2002; 40:1333-1338.
80. Maron R, Sukhova G, Faria AM, et al. 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.
81. 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. Circulation 2003; 108:1232-1237.