Enhanced immune system activation and arterial inflammation accelerates atherosclerosis in lupus-prone mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 27, Issue 7, 2007, Pages 1625-1631

  Gautier, Emmanuel L ^a   Huby, Thierry ^a   Ouzilleau, Betty ^a   Doucet, Chantal ^a   Saint Charles, Flora ^a   Gremy, Guilaine ^a   Chapman, M John ^a   Lesnik, Philippe ^a,b  

^a PITIÉ SALPÊTRIÈRE HOSPITAL   (France)

^b INSERM   (France)

Author keywords

Apoptotic cells; Arterial inflammation; Atherosclerosis; Immune system; Lupus

Indexed keywords

HIGH DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN CHOLESTEROL; TRIACYLGLYCEROL; VERY LOW DENSITY LIPOPROTEIN CHOLESTEROL;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTERY ENDOTHELIUM; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; AUTOIMMUNE DISEASE; B LYMPHOCYTE ACTIVATION; BONE MARROW TRANSPLANTATION; CD4+ T LYMPHOCYTE; CELL ACTIVATION; CHOLESTEROL METABOLISM; CONTROLLED STUDY; DISEASE COURSE; ENDOTHELIUM CELL; EXPERIMENTAL MODEL; IMMUNE RESPONSE; IMMUNOPATHOLOGY; INFLAMMATION; KIDNEY DYSFUNCTION; KIDNEY FUNCTION; LIPID BLOOD LEVEL; LIPID DIET; MACROPHAGE; MONOCYTE; MOUSE; NEUTROPHIL CHEMOTAXIS; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; SYSTEMIC LUPUS ERYTHEMATOSUS; T LYMPHOCYTE ACTIVATION; WILD TYPE;

ANIMALS; ANTIBODIES, ANTIPHOSPHOLIPID; APOPTOSIS; ATHEROSCLEROSIS; BONE MARROW TRANSPLANTATION; CD4-POSITIVE T-LYMPHOCYTES; CYTOKINES; DISEASE MODELS, ANIMAL; IMMUNE SYSTEM; LIPID METABOLISM; LIPOPROTEINS; LUPUS ERYTHEMATOSUS, SYSTEMIC; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; PROBABILITY; RADIATION CHIMERA; REFERENCE VALUES; SENSITIVITY AND SPECIFICITY;

EID: 34250898642     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/ATVBAHA.107.142430     Document Type: Article

References (43)

1. Urowitz MB, Bookman AA, Koehler BE, Gordon DA, Smythe HA, Ogryzlo MA. The bimodal mortality pattern of systemic lupus erythematosus. Am J Med. 1976;60:221-225.
2. Frostegard J. Atherosclerosis in patients with autoimmune disorders. Arterioscler Thromb Vasc Biol. 2005;25:1776-1785.
3. Roman MJ, Shanker BA, Davis A, Lockshin MD, Sammaritano L, Simantov R, Crow MK, Schwartz JE, Paget SA, Devereux RB, Salmon JE. Prevalence and correlates of accelerated atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2399-2406.
4. Asanuma Y, Oeser A, Shintani AK, Turner E, Olsen N, Fazio S, Linton MF, Raggi P, Stein CM. Premature coronary-artery atherosclerosis in systemic lupus erythematosus. N Engl J Med. 2003;349:2407-2415.
5. del Rincon I, O'Leary DH, Haas RW, Escalante A. Effect of glucocorticoids on the arteries in rheumatoid arthritis. Arthritis Rheum. 2004;50:3813-3822.
6. Liu K, Mohan C. What do mouse models teach us about human SLE? Clin Immunol. 2006;119:123-130.
7. Cohen PL, Eisenberg RA. Lpr and gld: single gene models of systemic autoimmunity and lymphoproliferative disease. Annu Rev Immunol. 1991;9:243-269.
8. Aprahamian T, Rifkin I, Bonegio R, Hugel B, Freyssinet JM, Sato K, Castellot JJ, Jr., Walsh K. Impaired clearance of apoptotic cells promotes synergy between atherogenesis and autoimmune disease. J Exp Med. 2004;199:1121-1131.
9. Grainger DJ, Reckless J, McKilligin E. Apolipoprotein E modulates clearance of apoptotic bodies in vitro and in vivo, resulting in a systemic proinflammatory state in apolipoprotein E-deficient mice. J Immunol. 2004;173:6366-6375.
10. Bro S, Bentzon JF, Falk E, Andersen CB, Olgaard K, Nielsen LB. Chronic renal failure accelerates atherogenesis in apolipoprotein E-deficient mice. J Am Soc Nephrol. 2003;14:2466-2474.
11. Ivanovski O, Szumilak D, Nguyen-Khoa T, Ruellan N, Phan O, Lacour B, Descamps-Latscha B, Drueke TB, Massy ZA. The antioxidant N-acetylcysteine prevents accelerated atherosclerosis in uremic apolipoprotein E knockout mice. Kidney Int. 2005;67:2288-2294.
12. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med. 2004;351:1296-1305.
13. Huby T, Doucet C, Dachet C, Ouzilleau B, Ueda Y, Afzal V, Rubin E, Chapman MJ, Lesnik P Knockdown expression and hepatic deficiency reveal an atheroprotective role for SR-BI in liver and peripheral tissues. J Clin Invest. 2006.
14. Lesnik P, Haskell CA, Charo IF. Decreased atherosclerosis in CX3CR1-/- mice reveals a role for fractalkine in atherogenesis. J Clin Invest. 2003;111:333-340.
15. 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.
16. Munoz LE, Gaipl US, Franz S, Sheriff A, Voll RE, Kalden JR, Herrmann M. SLE - a disease of clearance deficiency? Rheumatology (Oxford). 2005;44:1101-1107.
17. Stanic AK, Stein CM, Morgan AC, Fazio S, Linton MF, Wakeland EK, Olsen NJ, Major AS. Immune dysregulation accelerates atherosclerosis and modulates plaque composition in systemic lupus erythematosus. Proc Natl Acad Sci U S A. 2006;103:7018-7023.
18. Theofilopoulos AN, Lawson BR Tumour necrosis factor and other cytokines in murine lupus. Ann Rheum Dis. 1999;58 Suppl 1:I49-55.
19. Jones BM, Liu T, Wong RW. Reduced in vitro production of interferon-gamma, interleukin-4 and interleukin-12 and increased production of interleukin-6, interleukin-10 and tumour necrosis factor-alpha in systemic lupus erythematosus. Weak correlations of cytokine production with disease activity. Autoimmunity 1999;31:117-124.
20. Hagiwara E, Gourley MF, Lee S, Klinman DK. Disease severity in patients with systemic lupus erythematosus correlates with an increased ratio of interleukin-10:interferon-gamma-secreting cells in the peripheral blood. Arthritis Rheum. 1996;39:379-385.
21. Horwitz DA, Gray JD, Behrendsen SC, Kubin M, Rengaraju M, Ohtsuka K, Trinchieri G. Decreased production of interleukin-12 and other Th1-type cytokines in patients with recent-onset systemic lupus erythematosus. Arthritis Rheum. 1998;41:838-844.
22. Richaud-Patin Y, Alcocer-Varela J, Llorente L. High levels of TH2 cytokine gene expression in systemic lupus erythematosus. Rev Invest Clin. 1995;47:267-272.
23. Lin LC, Chen YC, Chou CC, Hsieh KH, Chiang BL. Dysregulation of T helper cell cytokines in autoimmune prone NZB x NZW F1 mice. Scand J Immunol. 1995;42:466-472.
24. Alleva DG, Kaser SB, Beller DI. Aberrant cytokine expression and autocrine regulation characterize macrophages from young MRL+/+ and NZB/W F1 lupus-prone mice. J Immunol. 1997;159:5610-5619.
25. Gupta S, Pablo AM, Jiang X, Wang N, Tall AR, Schindler C. IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest. 1997;99:2752-2761.
26. 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.
27. 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.
28. Hauer AD, Uyttenhove C, de Vos P, Stroobant V, Renauld JC, van Berkel TJ, van Snick J, Kuiper J. Blockade of interleukin-12 function by protein vaccination attenuates atherosclerosis. Circulation. 2005;112:1054-1062.
29. 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.
30. Kirii H, Niwa T, Yamada Y, Wada H, Saito K, Iwakura Y, Asano M, Moriwaki H, Seishima M. Lack of interleukin-1beta decreases the severity of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:656-660.
31. Mallat Z, Besnard S, Duriez M, Deleuze V, Emmanuel F, Bureau MF, Soubrier F, Esposito B, Duez H, Fievet C, Staels B, Duverger N, Scherman D, Tedgui A. Protective role of interleukin-10 in atherosclerosis. Circ Res. 1999;85:e17-24.
32. Manderson AP, Botto M, Walport MJ. The role of complement in the development of systemic lupus erythematosus. Annu Rev Immunol. 2004;22:431-456.
33. Laderach D, Bach JF, Koutouzov S. Nucleosomes inhibit phagocytosis of apoptotic thymocytes by peritoneal macrophages from MRL+/+ lupus-prone mice. J Leukoc Biol. 1998;64:774-780.
34. Tabas I. Consequences and therapeutic implications of macrophage apoptosis in atherosclerosis: the importance of lesion stage and phagocytic efficiency. Arterioscler Thromb Vasc Biol. 2005;25:2255-2264.
35. Albert ML. Death-defying immunity: do apoptotic cells influence antigen processing and presentation? Nat Rev Immunol. 2004;4:223-231.
36. Boisvert WA, Rose DM, Boullier A, Quehenberger O, Sydlaske A, Johnson KA, Curtiss LK, Terkeltaub R. Leukocyte transglutaminase 2 expression limits atherosclerotic lesion size. Arterioscler Thromb Vasc Biol. 2006;26:563-569.
37. Binstadt BA, Patel PR, Alencar H, Nigrovic PA, Lee DM, Mahmood U, Weissleder R, Mathis D, Benoist C. Particularities of the vasculature can promote the organ specificity of autoimmune attack. Nat Immunol. 2006;7:284-292.
38. Cho CS, Cho ML, Chen PP, Min SY, Hwang SY, Park KS, Kim WU, Min DJ, Min JK, Park SH, Kim HY. Antiphospholipid antibodies induce monocyte chemoattractant protein-1 in endothelial cells. J Immunol. 2002;168:4209-4215.
39. Papa ND, Raschi E, Moroni G, Panzeri P, Borghi MO, Ponticelli C, Tincani A, Balestrieri G, Meroni PL. Anti-endothelial cell IgG fractions from systemic lupus erythematosus patients bind to human endothelial cells and induce a pro-adhesive and a pro-inflammatory phenotype in vitro. Lupus. 1999;8:423-429.
40. Carvalho D, Savage CO, Isenberg D, Pearson JD. IgG anti-endothelial cell autoantibodies from patients with systemic lupus erythematosus or systemic vasculitis stimulate the release of two endothelial cell-derived mediators, which enhance adhesion molecule expression and leukocyte adhesion in an autocrine manner. Arthritis Rheum. 1999;42:631-640.
41. Libby P. Inflammation in atherosclerosis. Nature. 2002;420:868-874.
42. Hansson GK. Inflammation, atherosclerosis, and coronary artery disease. N Engl J Med. 2005;352:1685-1695.
43. Zhu J, Liu X, Xie C, Yan M, Yu Y, Sobel ES, Wakeland EK, Mohan C. T cell hyperactivity in lupus as a consequence of hyperstimulatory antigen-presenting cells. J Clin Invest. 2005;115:1869-1878.