Depletion of natural killer cell function decreases atherosclerosis in low-density lipoprotein receptor null mice

Arteriosclerosis, Thrombosis, and Vascular Biology

Volumn 24, Issue 6, 2004, Pages 1049-1054

  Whitman, Stewart C ^a   Rateri, Debra L ^b   Szilvassy, Stephen J ^c   Yokoyama, Wayne ^d   Daugherty, Alan ^b  

^a UNIVERSITY OF OTTAWA HEART INSTITUTE   (Canada)

^b UNIVERSITY OF KENTUCKY   (United States)

^c AMGEN INC   (United States)

^d WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Atherosclerosis; Bone marrow transplantation; LDL receptor null mice; NK cells

Indexed keywords

CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; SATURATED FATTY ACID;

ANIMAL CELL; ANIMAL MODEL; ANIMAL TISSUE; AORTA ATHEROSCLEROSIS; ARTICLE; ATHEROSCLEROSIS; BONE MARROW CELL; BONE MARROW TRANSPLANTATION; CELL FUNCTION; CELL INFILTRATION; CHOLESTEROL BLOOD LEVEL; DIET; FEMALE; GENE EXPRESSION; HEMATOPOIETIC SYSTEM; HUMAN; IMMUNITY; IMMUNOHISTOCHEMISTRY; MOUSE; NATURAL KILLER CELL; NONHUMAN; PRIORITY JOURNAL; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; ANTIGENS, LY; AORTIC DISEASES; ARTERIOSCLEROSIS; BONE MARROW TRANSPLANTATION; DIET, ATHEROGENIC; FEMALE; HYPERLIPIDEMIAS; IMMUNOLOGIC DEFICIENCY SYNDROMES; INFLAMMATION; KILLER CELLS, NATURAL; LECTINS, C-TYPE; LIPIDS; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; RADIATION CHIMERA; RECEPTORS, LDL;

EID: 2942516034     PISSN: 10795642     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.ATV.0000124923.95545.2c     Document Type: Article

References (53)

1. Ross R. Atherosclerosis-an inflammatory disease. N Engl J Med. 1999;340:115-126.
2. Hansson GK. Immune mechanisms in atherosclerosis. Arterioscler Thromb Vasc Biol. 2001;21:1876-1890.
3. 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.
4. Roselaar SE, Kakkanathu PX, Daugherty A. Lymphocyte populations in atherosclerotic lesions of apoE -/- and LDL receptor -/- mice. Decreasing density with disease progression. Arterioscler Thromb Vasc Biol. 1996;16:1013-1018.
5. Dansky HM, Charlton SA, Harper MM, Smith JD. T and B lymphocytes play a minor role in atherosclerotic plaque formation in the apolipoprotein E-deficient mouse. Proc Natl Acad Sci U S A. 1997;94:4642-4646.
6. Smith JD, Trogan E, Ginsberg M, Grigaux C, Tian J, Miyata M. Decreased atherosclerosis in mice deficient in both macrophage colony-stimulating factor (op) and apolipoprotein E. Proc Natl Acad Sci U S A. 1995;92:8264-8268.
7. -/- mice. J Clin Invest. 1997;100:1575-1580.
8. Song L, Leung C, Schindler C. Lymphocytes are important in early atherosclerosis. J Clin Invest. 2001;108:251-259.
9. Reardon CA, Blachowicz L, White T, Cabana V, Wang Y, Lukens J, Bluestone J, Getz GS. Effect of immune deficiency on lipoproteins and atherosclerosis in male apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2001;21:1011-1016.
10. Sohma Y, Sasano H, Shiga R, Saeki S, Suzuki T, Nagura H, Nose M, Yamamoto T. Accumulation of plasma cells in atherosclerotic lesions of Watanabe heritable hyperlipidemic rabbits. Proc Natl Acad Sci USA. 1995;92:4937-4941.
11. Zhou X, Hansson GK. Detection of B cells and proinflammatory cytokines in atherosclerotic plaques of hypercholesterolaemic apolipoprotein E knockout mice. Scand J Immunol. 1999;50:25-30.
12. Kaartinen M, Penttila A, Kovanen PT. Accumulation of activated mast cells in the shoulder region of human coronary atheroma, the predilection site of atheromatous rupture. Circulation. 1994;90:1669-1678.
13. Bobryshev YV, Taksir T, Lord RS, Freeman MW. Evidence that dendritic cells infiltrate atherosclerotic lesions in apolipoprotein E-deficient mice. Histol Histopathol. 2001;16:801-808.
14. 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.
15. Curtiss LK, Kubo N, Schiller NK, Boisvert WA. Participation of innate and acquired immunity in atherosclerosis. Immunol Res. 2000;21:167-176.
16. Hansson GK, Libby P, Schonbeck U, Yan ZQ. Innate and adaptive immunity in the pathogenesis of atherosclerosis. Circ Res. 2002;91:281-291.
17. Lanier LL. NK cell receptors. Annu Rev Immunol. 1998;16:359-393.
18. Trinchieri G. Biology of natural killer cells. Adv Immunol. 1989;47:187-376.
19. Yokoyama WM. Natural killer cell receptors. Curr Opin Immunol. 1998;10:298-305.
20. Roder J, Duwe A. The beige mutation in the mouse selectively impairs natural killer cell function. Nature. 1979;278:451-453.
21. Roder JC. The beige mutation in the mouse. I. A stem cell predetermined impairment in natural killer cell function. J Immunol. 1979;123:2168-2173.
22. Roder JC, Lohmann-Matthes ML, Domzig W, Wigzell H. The beige mutation in the mouse. II. Selectivity of the natural killer (NK) cell defect. J Immunol. 1979;123:2174-2181.
23. Paigen B, Holmes PA, Novak EK, Swank RT. Analysis of atherosclerosis susceptibility in mice with genetic defects in platelet function. Arteriosclerosis. 1990;10:648-652.
24. Schiller NK, Boisvert WA, Curtiss LK. Inflammation in atherosclerosis: lesion formation in LDL receptor-deficient mice with perforin and Lyst (beige) mutations. Arterioscler Thromb Vasc Biol. 2002;22:1341-1346.
25. Kim S, Iizuka K, Aguila HL, Weissman IL, Yokoyama WM. In vivo natural killer cell activities revealed by natural killer cell-deficient mice. Proc Natl Acad Sci USA. 2000;97:2731-2736.
26. Boisvert WA, Spangenberg J, Curtiss LK. Treatment of severe hypercholesterolemia in apolipoprotein E-deficient mice by bone marrow transplantation. J Clin Invest. 1995;96:1118-1124.
27. Linton MF, Atkinson JB, Fazio S. Prevention of atherosclerosis in apolipoprotein E-deficient mice by bone marrow transplantation. Science. 1995;267:1034-1037.
28. Daugherty A, Rateri DL. Presence of LDL receptor-related protein/alpha 2-macroglobulin receptors in macrophages of atherosclerotic lesions from cholesterol-fed New Zealand and heterozygous Watanabe heritable hyperlipidemic rabbits. Arterioscler Thromb. 1994;14:2017-2024.
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. Daugherty A, Manning MW, Cassis LA. Angiotensin II promotes atherosclerotic lesions and aneurysms in apolipoprotein E-deficient mice. J Clin Invest. 2000;105:1605-1612.
31. Whitman SC, Ravisankar P, Daugherty A. IFN-gamma deficiency exerts gender-specific effects on atherogenesis in apolipoprotein E-/- mice. J Interferon Cytokine Res. 2002;22:661-670.
32. Whitman SC, Ravisankar P, Elam H, Daugherty A. Exogenous interferon-gamma enhances atherosclerosis in apolipoprotein E-/- mice. Am J Pathol. 2000;157:1819-1824.
33. 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.
34. Whitman SC, Rateri DL, Szilvassy SJ, Cornicelli JA, Daugherty A. Macrophage-specific expression of class A scavenger receptors in LDL receptor(-/-) mice decreases atherosclerosis and changes spleen morphology. J Lipid Res. 2002;43:1201-1208.
35. de Villiers WJ, Smith JD, Miyata M, Dansky HM, Darley E, Gordon S. Macrophage phenotype in mice deficient in both macrophage-colony-stimulating factor (op) and apolipoprotein E. Arterioscler Thromb Vasc Biol. 1998;18:631-640.
36. Rajavashisth T, Qiao JH, Tripathi S, Tripathi J, Mishra N, Hua M, Wang XP, Loussararian A, Clinton S, Libby P, Lusis A. Heterozygous osteopetrotic (op) mutation reduces atherosclerosis in LDL receptor- deficient mice. J Clin Invest. 1998;101:2702-2710.
37. Kowala MC, Recce R, Beyer S, Gu C, Valentine M. Characterization of atherosclerosis in LDL receptor knockout mice: macrophage accumulation correlates with rapid and sustained expression of aortic MCP-1/JE. Atherosclerosis. 2000;149:323-330.
38. Gu L, Rutledge B, Fiorillo J, Ernst C, Grewal I, Flavell R, Gladue R, Rollins B. In vivo properties of monocyte chemoattractant protein-1. J Leukoc Biol. 1997;62:577-580.
39. Gu L, Okada Y, Clinton SK, Gerard C, Sukhova GK, Libby P, Rollins BJ. Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell. 1998;2:275-281.
40. Gosling J, Slaymaker S, Gu L, Tseng S, Zlot CH, Young SG, Rollins BJ, Charo IF. MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J Clin Invest. 1999;103:773-778.
41. -/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature. 1998;394:894-897.
42. Dawson TC, Kuziel WA, Osahar TA, Maeda N. Absence of CC chemokine receptor-2 reduces atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis. 1999;143:205-211.
43. Wuttge DM, Eriksson P, Sirsjo A, Hansson GK, Stemme S. Expression of interleukin-15 in mouse and human atherosclerotic lesions. Am J Pathol. 2001;159:417-423.
44. Houtkamp MA, Der Wal AC, de Boer OJ, Der Loos CM, de Boer PA, Moorman AF, Becker AE. Interleukin-15 expression in atherosclerotic plaques: an alternative pathway for T-cell activation in atherosclerosis? Arterioscler Thromb Vasc Biol. 2001;21:1208-1213.
45. 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.
46. 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.
47. Elhage R, Jawien J, Rudling M, Ljunggren HG, Takeda K, Akira S, Bayard F, Hansson GK. Reduced atherosclerosis in interleukin-18 deficient apolipoprotein E-knockout mice. Cardiovasc Res. 2003;59:234-240.
48. 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.
49. Wherry JC, Schreiber RD, Unanue ER. Regulation of gamma interferon production by natural killer cells in scid mice: roles of tumor necrosis factor and bacterial stimuli. Infect Immun. 1991;59:1709-1715.
50. Shindo J, Ishibashi T, Yokoyama K, Nakazato K, Ohwada T, Shiomi M, Maruyama Y. Granulocyte-macrophage colony-stimulating factor prevents the progression of atherosclerosis via changes in the cellular and extracellular composition of atherosclerotic lesions in watanabe heritable hyperlipidemic rabbits. Circulation. 1999;99:2150-2156.
51. Schreyer SA, Vick CM, LeBoeuf RC. Loss of lymphotoxin-alpha but not tumor necrosis factor-alpha reduces atherosclerosis in mice. J Biol Chem. 2002;277:12364-12368.
52. 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-e24.
53. Pinderski Oslund LJ, Hedrick CC, Olvera T, Hagenbaugh A, Territo M, Berliner JA, Fyfe AI. Interleukin-10 blocks atherosclerotic events in vitro and in vivo. Arterioscler Thromb Vasc Biol. 1999;19:2847-2853.