CD4+CD28null T cells in coronary artery disease: When helpers become killers

Cardiovascular Research

Volumn 81, Issue 1, 2009, Pages 11-19

  Dumitriu, Ingrid E ^a   Araguás, Ernesto Trallero ^a   Baboonian, Christina ^a   Kaski, Juan Carlos ^a  

^a ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

CD4+CD28null T cells; Coronary artery disease

Indexed keywords

CD28 ANTIGEN;

ATHEROSCLEROSIS; AUTOIMMUNE DISEASE; AUTOIMMUNITY; CARDIOVASCULAR FUNCTION; CD4+ T LYMPHOCYTE; CORONARY ARTERY DISEASE; HELPER CELL; HUMAN; PHENOTYPE; PRIORITY JOURNAL; REVIEW;

ANIMALS; ANTIGENS, CD28; AUTOIMMUNE DISEASES; CORONARY ARTERY DISEASE; CORONARY VESSELS; DISEASE MODELS, ANIMAL; HUMANS; T-LYMPHOCYTES, HELPER-INDUCER; THROMBOSIS;

EID: 57749208337     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvn248     Document Type: Review

References (95)

1. Lopez AD, Mathers CD, Ezzati M, Jamison DT, Murray CJ. Global and regional burden of disease and risk factors, 2001: systematic analysis of population health data. Lancet 2006;367:1747-1757.
2. Stary HC, Chandler AB, Dinsmore RE, Fuster V, Glagov S, Insull W Jr et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Arteriosclerosis, American Heart Association. Circulation 1995;92:1355-1374.
3. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med 2005;352:1685-1695.
4. Hansson GK, Libby P. The immune response in atherosclerosis: a double-edged sword. Nat Rev Immunol 2006;6:508-519.
5. Libby P. Inflammation in atherosclerosis. Nature 2002;420:868-874.
6. Jonasson L, Holm J, Skalli O, Bondjers G, Hansson GK. Regional accumulations of T cells, macrophages, and smooth muscle cells in the human atherosclerotic plaque. Arteriosclerosis 1986;6:131-138.
7. Hansson GK, Holm J, Jonasson L. Detection of activated T lymphocytes in the human atherosclerotic plaque. Am J Pathol 1989;135:169-175.
8. Khallou-Laschet J, Caligiuri G, Groyer E, Tupin E, Gaston AT, Poirier B et al. The proatherogenic role of T cells requires cell division and is dependent on the stage of the disease. Arterioscler Thromb Vasc Biol 2006;26:353-358.
9. Daugherty A, Rateri DL. T lymphocytes in atherosclerosis: the yin-yang of Th1 and Th2 influence on lesion formation. Circ Res 2002;90:1039- 1040.
10. Liuzzo G, Kopecky SL, Frye RL, O'Fallon WM, Maseri A, Goronzy JJ et al. Perturbation of the T-cell repertoire in patients with unstable angina. Circulation 1999;100:2135-2139.
11. Liuzzo G, Biasucci LM, Trotta G, Brugaletta S, Pinnelli M, Digianuario G et al. Unusual CD4+CD28null T lymphocytes and recurrence of acute coronary events. J Am Coll Cardiol 2007;50:1450-1458.
12. Acuto O, Michel F. CD28-mediated co-stimulation: a quantitative support for TCR signalling. Nat Rev Immunol 2003;3:939-951.
13. Alegre ML, Frauwirth KA, Thompson CB. T-cell regulation by CD28 and CTLA-4. Nat Rev Immunol 2001;1:220-228.
14. Appleman LJ, Boussiotis VA. Tcell anergy and costimulation. Immunol Rev 2003;192:161-180.
15. Weyand CM, Brandes JC, Schmidt D, Fulbright JW, Goronzy JJ. Functional properties of CD4+ CD28- T cells in the aging immune system. Mech Ageing Dev 1998;102:131-147.
16. Nakajima T, Schulte S, Warrington KJ, Kopecky SL, Frye RL, Goronzy JJ et al. T-cell-mediated lysis of endothelial cells in acute coronary syndromes. Circulation 2002;105:570-575.
17. Namekawa T, Wagner UG, Goronzy JJ, Weyand CM. Functional subsets of CD4 T cells in rheumatoid synovitis. Arthritis Rheum 1998;41:2108-2116.
18. Warrington KJ, Takemura S, Goronzy JJ, Weyand CM. CD4+,CD28- T cells in rheumatoid arthritis patients combine features of the innate and adaptive immune systems. Arthritis Rheum 2001;44:13-20.
19. Sawai H, Park YW, Roberson J, Imai T, Goronzy JJ, Weyand CM. T cell costimulation by fractalkine-expressing synoviocytes in rheumatoid arthritis. Arthritis Rheum 2005;52:1392-1401.
20. Snyder MR, Muegge LO, Offord C, O'Fallon WM, Bajzer Z, Weyand CM et al. Formation of the killer Ig-like receptor repertoire on CD4+ CD28null T cells. J Immunol 2002;168:3839-3846.
21. Vallejo AN, Schirmer M, Weyand CM, Goronzy JJ. Clonality and longevity of CD4+CD28null T cells are associated with defects in apoptotic pathways. J Immunol 2000;165:6301-6307.
22. Schirmer M, Vallejo AN, Weyand CM, Goronzy JJ. Resistance to apoptosis and elevated expression of Bcl-2 in clonally expanded CD4+CD28- T cells from rheumatoid arthritis patients. J Immunol 1998;161:1018-1025.
23. Morishita Y, Sao H, Hansen JA, Martin PJ. A distinct subset of human CD4+ cells with a limited alloreactive T cell receptor repertoire. J Immunol 1989;143:2783-2789.
24. Vallejo AN, Weyand CM, Goronzy JJ. T-cell senescence: a culprit of immune abnormalities in chronic inflammation persistent infection. Trends Mol Med 2004;10:119-124.
25. Schmidt D, Martens PB, Weyand CM, Goronzy JJ. The repertoire of CD4+ CD28- T cells in rheumatoid arthritis. Mol Med 1996;2:608-618.
26. Martens PB, Goronzy JJ, Schaid D, Weyand CM. Expansion of unusual CD4+ T cells in severe rheumatoid arthritis. Arthritis Rheum 1997;40:1106-1114.
27. Pawlik A, Ostanek L, Brzosko I, Brzosko M, Masiuk M, Machalinski B et al. The expansion of CD4+CD28- T cells in patients with rheumatoid arthritis. Arthritis Res Ther 2003;5:R210-R213.
28. Schmidt D, Goronzy JJ, Weyand CM. CD4+ CD7- CD28- T cells are expanded in rheumatoid arthritis and are characterized by autoreactivity. J Clin Invest 1996;97:2027-2037.
29. Thewissen M, Somers V, Venken K, Linsen L, van Paassen P, Geusens P et al. Analyses of immunosenescent markers in patients with autoimmune disease. Clin Immunol 2007;123:209-218.
30. Sawai H, Park YW, He X, Goronzy JJ, Weyand CM. Fractalkine mediates T cell-dependent proliferation of synovial fibroblasts in rheumatoid arthritis. Arthritis Rheum 2007;56:3215-3225.
31. Fasth AE, Snir O, Johansson AA, Nordmark B, Rahbar A, Af Klint E et al. Skewed distribution of proinflammatory CD4+CD28null T cells in rheumatoid arthritis. Arthritis Res Ther 2007;9:R87.
32. Moosig F, Csernok E, Wang G, Gross WL. Costimulatory molecules in Wegener's granulomatosis (WG): lack of expression of CD28 and preferential up-regulation of its ligands B7-1 (CD80) and B7-2 (CD86) on T cells. Clin Exp Immunol 1998;114:113-118.
33. Garcia de Tena J, Manzano L, Leal JC, San Antonio E, Sualdea V, Alvarez-Mon M. Active Crohn's disease patients show a distinctive expansion of circulating memory CD4+CD45RO+CD28null T cells. J Clin Immunol 2004;24:185-196.
34. Libby P, Theroux P. Pathophysiology of coronary artery disease. Circulation 2005;111:3481-3488.
35. Liuzzo G, Goronzy JJ, Yang H, Kopecky SL, Holmes DR, Frye RL et al. Monoclonal T-cell proliferation and plaque instability in acute coronary syndromes. Circulation 2000;101:2883-2888.
36. Zal B, Kaski JC, Arno G, Akiyu JP, Xu Q, Cole D et al. Heat-shock protein 60-reactive CD4+CD28null T cells in patients with acute coronary syndromes. Circulation 2004;109:1230-1235.
37. Walsh K, Smith RC, Kim HS. Vascular cell apoptosis in remodeling, restenosis, and plaque rupture. Circ Res 2000;87:184-188.
38. Alber HF, Duftner C, Wanitschek M, Dorler J, Schirmer M, Suessenbacher A et al. Neopterin, CD4+CD28- lymphocytes and the extent and severity of coronary artery disease. Int J Cardiol 2008; Epub ahead of print 28 June 2008, doi:10.1016/j.ijcard.2008.03.010.
39. McMahona M, Hahna BH. Atherosclerosis and systemic lupus erythematosus: mechanistic basis of the association. Curr Opin Immunol 2007;19:633-639.
40. Weyand CM, Goronzy JJ. T-cell responses in rheumatoid arthritis: systemic abnormalities-local disease. Curr Opin Rheumatol 1999;11:210-217.
41. Gerli R, Schillaci G, Giordano A, Bocci EB, Bistoni O, Vaudo G et al. CD4+CD28- T lymphocytes contribute to early atherosclerotic damage in rheumatoid arthritis patients. Circulation 2004;109:2744-2748.
42. Davignon J, Ganz P. Role of endothelial dysfunction in atherosclerosis. Circulation 2004;109:III27-32.
43. Schachinger V, Britten MB, Zeiher AM. Prognostic impact of coronary vasodilator dysfunction on adverse long-term outcome of coronary heart disease. Circulation 2000;101:1899-1906.
44. Kronenberg M, Gapin L. The unconventional lifestyle of NKTcells. Nat Rev Immunol 2002;2:557-568.
45. Nakai Y, Iwabuchi K, Fujii S, Ishimori N, Dashtsoodol N, Watano K et al. Natural killer T cells accelerate atherogenesis in mice. Blood 2004;104:2051-2059.
46. Tupin E, Nicoletti A, Elhage R, Rudling M, Ljunggren HG, Hansson GK et al. CD1d-dependent activation of NKTcells aggravates atherosclerosis. J Exp Med 2004;199:417-422.
47. Andoh Y, Fujii S, Iwabuchi K, Yokota T, Inoue N, Nakai Y et al. Lower prevalence of circulating natural killer T cells in patients with angina: a potential novel marker for coronary artery disease. Coron Artery Dis 2006;17:523-528.
48. Posnett DN, Sinha R, Kabak S, Russo C. Clonal populations of T cells in normal elderly humans: the T cell equivalent to 'benign monoclonal gammapathy'. J Exp Med 1994;179:609-618.
49. Bryl E, Vallejo AN, Weyand CM, Goronzy JJ. Down-regulation of CD28 expression by TNF-alpha. J Immunol 2001;167:3231-3238.
50. Bryl E, Vallejo AN, Matteson EL, Witkowski JM, Weyand CM, Goronzy JJ. Modulation of CD28 expression with anti-tumor necrosis factor alpha therapy in rheumatoid arthritis. Arthritis Rheum 2005;52:2996-3003.
51. Warrington KJ, Vallejo AN, Weyand CM, Goronzy JJ. CD28 loss in senescent CD4+ T cells: reversal by interleukin-12 stimulation. Blood 2003;101:3543-3549.
52. Kuo CC, Shor A, Campbell LA, Fukushi H, Patton DL, Grayston JT. Demonstration of Chlamydia pneumoniae in atherosclerotic lesions of coronary arteries. J Infect Dis 1993;167:841-849.
53. Xu Q, Kleindienst R, Waitz W, Dietrich H, Wick G. Increased expression of heat shock protein 65 coincides with a population of infiltrating T lymphocytes in atherosclerotic lesions of rabbits specifically responding to heat shock protein 65. J Clin Invest 1993;91:2693-2702.
54. Yla-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.
55. 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.
56. Banchereau J, Steinman RM. Dendritic cells and the control of immunity. Nature 1998;392:245-252.
57. Bobryshev YV, Lord RS. Mapping of vascular dendritic cells in atherosclerotic arteries suggests their involvement in local immune-inflammatory reactions. Cardiovasc Res 1998;37:799-810.
58. Bobryshev YV. Dendritic cells in atherosclerosis: current status of the problem and clinical relevance. Eur Heart J 2005;26:1700-1704.
59. Niessner A, Sato K, Chaikof EL, Colmegna I, Goronzy JJ, Weyand CM. Pathogen-sensing plasmacytoid dendritic cells stimulate cytotoxic T-cell function in the atherosclerotic plaque through interferon-alpha. Circulation 2006;114:2482-2489.
60. Jonasson L, Holm J, Skalli O, Gabbiani G, Hansson GK. Expression of class II transplantation antigen on vascular smooth muscle cells in human atherosclerosis. J Clin Invest 1985;76:125-131.
61. Ueno H, Klechevsky E, Morita R, Aspord C, Cao T, Matsui T et al. Dendritic cell subsets in health and disease. Immunol Rev 2007;219:118-142.
62. Llodra J, Angeli V, Liu J, Trogan E, Fisher EA, Randolph GJ. Emigration of monocyte-derived cells from atherosclerotic lesions characterizes regressive, but not progressive, plaques. Proc Natl Acad Sci USA 2004;101:11779-11784.
63. Epstein SE, Zhu J, Burnett MS, Zhou YF, Vercellotti G, Hajjar D. Infection and atherosclerosis: potential roles of pathogen burden and molecular mimicry. Arterioscler Thromb Vasc Biol 2000;20:1417-1420.
64. 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;92:3893-3897.
65. Mosorin M, Surcel HM, Laurila A, Lehtinen M, Karttunen R, Juvonen J et al. Detection of Chlamydia pneumoniae-reactive T lymphocytes in human atherosclerotic plaques of carotid artery. Arterioscler Thromb Vasc Biol 2000;20:1061-1067.
66. Biasucci LM, Liuzzo G, Ciervo A, Petrucca A, Piro M, Angiolillo DJ et al. Antibody response to chlamydial heat shock protein 60 is strongly associated with acute coronary syndromes. Circulation 2003;107:3015-3017.
67. Palinski W, Tangirala RK, Miller E, Young SG, Witztum JL. Increased autoantibody titers against epitopes of oxidized LDL in LDL receptor-deficient mice with increased atherosclerosis. Arterioscler Thromb Vasc Biol 1995;15:1569-1576.
68. Xu Q, Schett G, Perschinka H, Mayr M, Egger G, Oberhollenzer F et al. Serum soluble heat shock protein 60 is elevated in subjects with atherosclerosis in a general population. Circulation 2000;102:14- 20.
69. Monaco C, Crea F, Niccoli G, Summaria F, Cianflone D, Bordone R et al. Autoantibodies against oxidized low density lipoproteins in patients with stable angina, unstable angina or peripheral vascular disease; pathophysiological implications. Eur Heart J 2001;22:1572-1577.
70. Dickson BC, Gotlieb AI. Towards understanding acute destabilization of vulnerable atherosclerotic plaques. Cardiovasc Pathol 2003;12:237-248.
71. Niessner A, Goronzy JJ, Weyand CM. Immune-mediated mechanisms in atherosclerosis: prevention and treatment of clinical manifestations. Curr Pharm Des 2007;13:3701-3710.
72. Newby AC. Metalloproteinases and vulnerable atherosclerotic plaques. Trends Cardiovasc Med 2007;17:253-258.
73. Pingiotti E, Cipriani P, Marrelli A, Liakouli V, Fratini S, Penco M et al. Surface expression of fractalkine receptor (CX3CR1) on CD4+/CD28 T cells in RA patients and correlation with atherosclerotic damage. Ann N Y Acad Sci 2007;1107:32-41.
74. Damas JK, Boullier A, Waehre T, Smith C, Sandberg WJ, Green S et al. Expression of fractalkine (CX3CL1) and its receptor, CX3CR1, is elevated in coronary artery disease and is reduced during statin therapy. Arterioscler Thromb Vasc Biol 2005;25:2567-2572.
75. Leon ML, Zuckerman SH. Gamma interferon: a central mediator in atherosclerosis. Inflamm Res 2005;54:395-411.
76. Johnson JL. Matrix metalloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability. Expert Rev Cardiovasc Ther 2007;5:265-282.
77. Katsuda S, Kaji T. Atherosclerosis and extracellular matrix. J Atheroscler Thromb 2003;10:267-274.
78. Buttice G, Miller J, Wang L, Smith BD. Interferon-gamma induces major histocompatibility class II transactivator (CIITA), which mediates collagen repression and major histocompatibility class II activation by human aortic smooth muscle cells. Circ Res 2006;98:472-479.
79. Rosenson RS, Tangney CC. Antiatherothrombotic properties of statins: implications for cardiovascular event reduction. J Am Med Assoc 1998;279:1643-1650.
80. Kwak BR, Mulhaupt F, Mach F. Atherosclerosis: anti-inflammatory and immunomodulatory activities of statins. Autoimmun Rev 2003;2:332-338.
81. Aikawa M, Libby P. Lipid lowering therapy in atherosclerosis. Semin Vasc Med 2004;4:357-366.
82. Brugaletta S, Biasucci LM, Pinnelli M, Biondi-Zoccai G, Di Giannuario G, Trotta G et al. Novel anti-inflammatory effect of statins: reduction of CD4+CD28null T lymphocyte frequency in patients with unstable angina. Heart 2006;92:249-250.
83. Branen L, Hovgaard L, Nitulescu M, Bengtsson E, Nilsson J, Jovinge S. Inhibition of tumor necrosis factor-alpha reduces atherosclerosis in apolipoprotein E knockout mice. Arterioscler Thromb Vasc Biol 2004;24:2137-2142.
84. Skoog T, Dichtl W, Boquist S, Skoglund-Andersson C, Karpe F, Tang R et al. Plasma tumour necrosis factor-alpha and early carotid atherosclerosis in healthy middle-aged men. Eur Heart J 2002;23:376-383.
85. Criscione LG, St Clair EW. Tumor necrosis factor-alpha antagonists for the treatment of rheumatic diseases. Curr Opin Rheumatol 2002;14:204-211.
86. Hurlimann D, Forster A, Noll G, Enseleit F, Chenevard R, Distler O et al. Anti-tumor necrosis factor-alpha treatment improves endothelial function in patients with rheumatoid arthritis. Circulation 2002;106:2184- 2187.
87. Rizzello V, Liuzzo G, Brugaletta S, Rebuzzi A, Biasucci LM, Crea F. Modulation of CD4(+)CD28null T lymphocytes by tumor necrosis factor-alpha blockade in patients with unstable angina. Circulation 2006;113:2272-2277.
88. Sakaguchi S, Ono M, Setoguchi R, Yagi H, Hori S, Fehervari Z et al. Foxp3+ CD25+ CD4+ natural regulatory T cells in dominant self-tolerance and autoimmune disease. Immunol Rev 2006;212:8-27.
89. Ehrenstein MR, Evans JG, Singh A, Moore S, Warnes G, Isenberg DA et al. Compromised function of regulatory T cells in rheumatoid arthritis and reversal by anti-TNFalpha therapy. J Exp Med 2004;200:277-285.
90. Mor A, Luboshits G, Planer D, Keren G, George J. Altered status of CD4(+)CD25(+) regulatory T cells in patients with acute coronary syndromes. Eur Heart J 2006;27:2530-2537.
91. Thewissen M, Somers V, Hellings N, Fraussen J, Damoiseaux J, Stinissen P. CD4+CD28null T cells in autoimmune disease: pathogenic features and decreased susceptibility to immunoregulation. J Immunol 2007;179:6514-6523.
92. Ait-Oufella H, Salomon BL, Potteaux S, Robertson AK, Gourdy P, Zoll J et al. Natural regulatory T cells control the development of atherosclerosis in mice. Nat Med 2006;12:178-180.
93. Li MO, Flavell RA. Contextual regulation of inflammation: a duet by transforming growth factor-beta and interleukin-10. Immunity 2008;28:468-476.
94. van Puijvelde GH, Hauer AD, de Vos P, van den Heuvel R, van Herwijnen MJ, van der Zee R et al. Induction of oral tolerance to oxidized low-density lipoprotein ameliorates atherosclerosis. Circulation 2006;114:1968-1976.
95. van Puijvelde GH, van Es T, van Wanrooij EJ, Habets KL, de Vos P, van der Zee R et al. Induction of oral tolerance to HSP60 or an HSP60-peptide activates T cell regulation and reduces atherosclerosis. Arterioscler Thromb Vasc Biol 2007;27:2677-2683.