Experimental models investigating the inflammatory basis of atherosclerosis

Current Atherosclerosis Reports

Volumn 10, Issue 3, 2008, Pages 260-271

  Soliman, Ahmed ^b   Kee, Patrick ^a  

^a UNIVERSITY OF TEXAS MEDICAL SCHOOL   (United States)

^b NONE

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; CD40 ANTIGEN; CD40 LIGAND; CHEMOKINE; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR2; COLONY STIMULATING FACTOR 1; CXCL1 CHEMOKINE; ENDOTHELIAL LEUKOCYTE ADHESION MOLECULE 1; FRACTALKINE; GAMMA INTERFERON; INTERCELLULAR ADHESION MOLECULE 1; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 18; INTERLEUKIN 4; INTERLEUKIN 6; INTERLEUKIN 8; L SELECTIN; LOW DENSITY LIPOPROTEIN CHOLESTEROL; LOW DENSITY LIPOPROTEIN RECEPTOR; MONOCYTE CHEMOTACTIC PROTEIN 1; PADGEM PROTEIN; VASCULAR CELL ADHESION MOLECULE 1; CELL ADHESION MOLECULE; CYTOKINE;

ARTERY WALL; ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; CARDIOVASCULAR INFLAMMATION; CELL INFILTRATION; CHOLESTEROL BLOOD LEVEL; CHOLESTEROL DIET; CYTOKINE RELEASE; DISEASE COURSE; DISEASE PREDISPOSITION; EXPERIMENTAL MODEL; FAMILIAL HYPERCHOLESTEROLEMIA; FAMILIAL HYPERLIPEMIA; GENE MUTATION; GENETIC RISK; INFLAMMATORY CELL; NONHUMAN; PROTEIN DEFICIENCY; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN TARGETING; PROTEIN TRANSPORT; REVIEW; ANIMAL; BLOOD VESSEL; DISEASE MODEL; GENETICS; INFLAMMATION; INJURY; MOUSE; MOUSE MUTANT; PATHOPHYSIOLOGY; PHYSIOLOGY; RABBIT; RAT;

ANIMALS; ATHEROSCLEROSIS; BLOOD VESSELS; CELL ADHESION MOLECULES; CYTOKINES; DISEASE MODELS, ANIMAL; INFLAMMATION; MICE; MICE, KNOCKOUT; RABBITS; RATS;

EID: 49949114514     PISSN: 15233804     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11883-008-0040-0     Document Type: Review

References (85)

1. Lawn R, Wade D, Hammer R, et al.: Atherogenesis in transgenic mice expressing human apolipoprotein(a). Nature 1992, 360:670-672.
2. Tenger C, Zhou X: Apolipoprotein E modulates immune activation by acting on the antigen-presenting cell. Immunology 2003, 109:392-397.
3. Calara F, Silvestre M, Casanada F, et al.: Spontaneous plaque rupture and secondary thrombosis in apolipoprotein E-deficient and LDL receptor-deficient mice. J Pathol 2001, 195:257-263.
4. Masucci-Magoulas L, Goldberg I, Bisgaier C, et al.: A mouse model with features of familial Combined hyperlipidemia. Science 1997, 275:391-394.
5. Bannykh S, Witztum J, Bergmark C: Mechanical aortic injury in apoE-deficient mice as a model for development of atherosclerosis: demonstration of leukocyte rolling early after injury. Ultrastructural Pathol 2002, 26:251-260.
6. vonder Thüsen J, van Berkel T, Biessen E: Induction of rapid atherogenesis by perivascular carotid collar placement in apolipoprotein E-deficient and low-density lipoprotein receptor-deficient mice. Circulation 2001, 103:1164-1170.
7. Grimsditch DC, Penfold S, Latcham J, et al.: C3H apoE(-/-) mice have less atherosclerosis than C57BL apoE(-/-) mice despite having a more atherogenic serum lipid profile. Atherosclerosis 2000, 151:389-397.
8. Shi W, Wang NJ, Shih DM, et al.: Determinants of atherosclerosis susceptibility in the C3H and C57BL/6 mouse model: evidence for involvement of endothelial cells but not blood cells or cholesterol metabolism. Circ Res 2000, 86:1078-1084.
9. Tabibiazar R, Wagner RA, Spin JM, et al.: Mouse strain-specific differences in vascular wall gene expression and their relationship to vascular disease. Arterioscler Thromb 2005, 25:302-308.
10. Johnson R, Chapman S, Dong Z, et al.: Absence of P-selectin delays fatty streak formation in mice. J Clin Invest 1997, 99:1037-1043.
11. Dong Z, Brown A, Wagner D: Prominent role of P-selectin in the development of advanced atherosclerosis in ApoE-deficient mice. Circulation 2000, 101:2290-2295.
12. Nageh M, Sandberg E, Marotti K, et al.: Deficiency of inflammatory cell adhesion molecules protects against atherosclerosis in mice. Arterioscler Thromb Vasc Biol 1997, 17:1517-1520.
13. Molenaar T, Twisk J, de Haas S, et al.: P-selectin as a candidate target in atherosclerosis. Biochem Pharmacol 2003, 66:859-866.
14. Kumar A, Hoover J, Simmons C, et al.: Remodeling and neointimal formation in the carotid artery of normal and P-selectin-deficient mice. Circulation 1997, 96:4333-4342.
15. Manka D, Collins R, Ley K, et al.: Absence of P-selectin, but not intercellular adhesion molecule-1, attenuates neointimal growth after arterial injury in apolipoprotein e-deficient mice. Circulation 2001, 103:1000-1005.
16. Hayashi S, Watanabe N, Nakazawa K, et al.: Roles of P-selectin in inflammation, neointimal formation, and vascular remodeling in balloon-injured rat carotid arteries. Circulation 2000, 102:1710-1717.
17. Molenaar T, Appeldoorn C, de Haas S, et al.: Specific inhibition of P-selectin-mediated cell adhesion by phage display-derived peptide antagonists. Blood 2002, 100:3570-3577.
18. Iiyama K, Hajra L, Iiyama M, et al.: Patterns of vascular cell adhesion molecule-1 and intercellular adhesion molecule-1 expression in rabbit and mouse atherosclerotic lesions and at sites predisposed to lesion formation. Circ Res 1999, 85:199-207.
19. Collins R, Velji R, Guevara N, et al.: P-Selectin or intercellular adhesion molecule (ICAM)-1 deficiency substantially protects against atherosclerosis in apolipoprotein E-deficient mice. J Exp Med 2000, 191:189-194.
20. Patel S, Thiagarajan R, Willerson J, Yeh E: Inhibition of alpha4 integrin and ICAM-1 markedly attenuate macrophage homing to atherosclerotic plaques in ApoE-deficient mice. Circulation 1998, 97:75-81.
21. Bourdillon M, Poston R, Covacho C, et al.: ICAM-1 deficiency reduces atherosclerotic lesions in double-knockout mice (ApoE(-/-)/ICAM-I(-/-)) fed a fat or a chow diet. Arterioscler Thromb 2000, 20:2630-2635.
22. Cybulsky M, Iiyama K, Li H, et al.: A major role for VCAM-1, but not ICAM-1, in early atherosclerosis. J Clin Invest 2001, 107:1255-1262.
23. Elices M, Osborn L, Takada Y, et al.: VCAM-1 on activated endothelium interacts with the leukocyte integrin VLA-4 at a site distinct from the VLA-4/fibronectin binding site. Cell 1990, 60:577-584.
24. Li H, Cybulsky M, Gimbrone M, Libby P: An atherogenic diet rapidly induces VCAM-1, a cytokine-regulatable mononuclear leukocyte adhesion molecule, in rabbit aortic endothelium. Arterioscler Thromb 1993, 13:197-204.
25. Sakai A, Kume N, Nishi E, et al.: P-selectin and vascular cell adhesion molecule-1 are focally expressed in aortas of hypercholesterolemic rabbits before intimal accumulation of macrophages and T lymphocytes. Arterioscler Thromb Vasc Biol 1997, 17:310-316.
26. Nakashima Y, Raines E, Plump A, et al.: Upregulation of VCAM-1 and ICAM-1 at atherosclerosis-prone sites on the endothelium in the ApoE-deficient mouse. Arterioscler Thromb Vasc Biol 1998, 18:842-851.
27. Gurtner G, Davis V, Li H, et al.: Targeted disruption of the murine VCAM1 gene: essential role of VCAM-1 in chorioallantoic fusion and placentation. Genes Dev 1995, 9:1-14.
28. Koni P, Joshi S, Temann U, et al.: Conditional vascular cell adhesion molecule 1 deletion in mice: impaired lymphocyte migration to bone marrow. J Exp Med 2001, 193:741-754.
29. Dansky H, Barlow C, Lominska C, et al.: Adhesion of monocytes to arterial endothelium and initiation of atherosclerosis are critically dependent on vascular cell adhesion molecule-1 gene dosage. Arterioscler Thromb 2001, 21:1662-1667.
30. Shih P, Brennan M, Vora D, et al.: Blocking very late antigen-4 integrin decreases leukocyte entry and fatty streak formation in mice fed an atherogenic diet. Circ Res 1999, 84:345-351.
31. Bavendiek U, Zirlik A, LaClair S, et al.: Atherogenesis in mice does not require CD40 ligand from bone marrow-derived cells. Arterioscler Thromb 2005, 25:1244-1249.
32. Mach F, Schönbeck U, Sukhova G, et al.: Reduction of atherosclerosis in mice by inhibition of CD40 signalling. Nature 1998, 394:200-203.
33. Schönbeck U, Sukhova G, Shimizu K, et al.: Inhibition of CD40 signaling limits evolution of established atherosclerosis in mice. Proc Natl Acad Sci U S A 2000, 97:7458-7463.
34. Lutgens E, Gorelik L, Daemen M, et al.: Requirement for CD154 in the progression of atherosclerosis. Nat Med 1999, 5:1313-1316.
35. Qiao J, Tripathi J, Mishra N, et al.: Role of macrophage colony-stimulating factor in atherosclerosis: studies of osteopetrotic mice. Am J Pathol 1997, 150:1687-1699.
36. Smith J, Trogan E, Ginsberg M, et al.: 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.
37. Boring L, Gosling J, Chensue S, et al.: Impaired monocyte migration and reduced type 1 (Th1) cytokine responses in C-C chemokine receptor 2 knockout mice. J Clin Invest 1997, 100:2552-2561.
38. Lu B, Rutledge B, Gu L, et al.: Abnormalities in monocyte recruitment and cytokine expression in monocyte chemoattractant protein 1-deficient mice. J Exp Med 1998, 187:601-608.
39. Takeya M, Yoshimura T, Leonard E, Takahashi K: Detection of monocyte chemoattractant protein-1 in human atherosclerotic lesions by an anti-monocyte chemoattractant protein-1 monoclonal antibody. Hum Pathol 1993, 24:534-539.
40. Clinton S, Libby P: Cytokines and growth factors in atherogenesis. Arch Pathol Lab Med 1992, 116:1292-1300.
41. Yu X, Dluz S, Graves D, et al.: Elevated expression of monocyte chemoattractant protein 1 by vascular smooth muscle cells in hypercholesterolemic primates. Proc Natl Acad Sci U S A 1992, 89:6953-6957.
42. Kuziel WA, Morgan SJ, Dawson TC, et al.: Severe reduction in leukocyte adhesion and monocyte extravasation in mice deficient in CC chemokine receptor 2. Proc Natl Acad Sci U S A 1997, 94:12053-12058.
43. Reckless J, Rubin E, Verstuyft J, et al.: Monocyte chemoattractant protein-1 but not tumor necrosis factor-alpha is correlated with monocyte infiltration in mouse lipid lesions. Circulation 1999, 99:2310-2316.
44. Gu L, Okada Y, Clinton S, et al.: Absence of monocyte chemoattractant protein-1 reduces atherosclerosis in low density lipoprotein receptor-deficient mice. Mol Cell 1998, 2:275-281.
45. Gosling J, Slaymaker S, Gu L, et al.: MCP-1 deficiency reduces susceptibility to atherosclerosis in mice that overexpress human apolipoprotein B. J Clin Invest 1999, 103:773-778.
46. Dawson T, Kuziel W, Osahar T, Maeda N: Absence of CC chemokine receptor-2 reduces atherosclerosis in apolipoprotein E-deficient mice. Atherosclerosis 1999, 143:205-211.
47. Boring L, Gosling J, Cleary M, Charo I: Decreased lesion formation in CCR2-/- mice reveals a role for chemokines in the initiation of atherosclerosis. Nature 1998, 394:894-897.
48. Namiki M, Kawashima S, Yamashita T, et al.: Local over-expression of monocyte chemoattractant protein-1 at vessel wall induces infiltration of macrophages and formation of atherosclerotic lesion: synergism with hypercholesterolemia. Arterioscler Thromb 2002, 22:115-120.
49. Ni W, Egashira K, Kitamoto S, et al.: New anti-monocyte chemoattractant protein-1 gene therapy attenuates atherosclerosis in apolipoprotein E-knockout mice. Circulation 2001, 103:2096-2101.
50. Inoue S, Egashira K, Ni W, et al.: Anti-monocyte chemo-attractant protein-1 gene therapy limits progression and destabilization of established atherosclerosis in apolipoprotein E-knockout mice. Circulation 2002, 106:2700-2706.
51. Usui M, Egashira K, Ohtani K, et al.: Anti-monocyte chemoattractant protein-1 gene therapy inhibits restenotic changes (neointimal hyperplasia) after balloon injury in rats and monkeys. FASEB J 2002, 16:1838-1840.
52. Kuziel W, Dawson T, Quinones M, et al.: CCR5 deficiency is not protective in the early stages of atherogenesis in apoE knockout mice. Atherosclerosis 2003, 167:25-32.
53. Braunersreuther V, Zernecke A, Arnaud C, et al.: CCR5 but not CCR1 deficiency reduces development of diet-induced atherosclerosis in mice. Arterioscler Thromb Vasc Biol 2007, 27:373-379.
54. Zernecke A, Liehn E, Gao J, et al.: Deficiency in CCR5 but not CCR1 protects against neointima formation in atherosclerosis-prone mice: involvement of IL-10. Blood 2006, 107:4240-4243.
55. van Wanrooij EJ, Happe H, Hauer AD, et al.: HIV entry inhibitor TAK-779 attenuates atherogenesis in low-density lipoprotein receptor-deficient mice. Arterioscler Thromb Vasc Biol 2005, 25:2642-2647.
56. Wilcox JN, Nelken NA, Coughlin SR, et al.: Local expression of inflammatory cytokines in human atherosclerotic plaques. J Atheroscler Thromb 1994, 1(Suppl 1):S10-S13.
57. Haley KJ, Lilly CM, Yang JH, et al.: Overexpression of eotaxin and the CCR3 receptor in human atherosclerosis: using genomic technology to identify a potential novel pathway of vascular inflammation. Circulation 2000, 102:2185-2189.
58. Inoue T, Komoda H, Nonaka M, et al.: Interleukin-8 as an independent predictor of long-term clinical outcome in patients with coronary artery disease. Int J Cardiol 2007 [Epub ahead of print].
59. Boisvert W, Santiago R, Curtiss L, Terkeltaub R: A leukocyte homologue of the IL-8 receptor CXCR-2 mediates the accumulation of macrophages in atherosclerotic lesions of LDL receptor-deficient mice. J Clin Invest 1998, 101:353-363.
60. Boisvert W, Rose D, Johnson K, et al.: Up-regulated expression of the CXCR2 ligand KC/GRO-alpha in atherosclerotic lesions plays a central role in macrophage accumulation and lesion progression. Am J Pathol 2006, 168:1385-1395.
61. vonder Thüsen J, Kuiper J, van Berkel T, Biessen E: Interleukins in atherosclerosis: molecular pathways and therapeutic potential. Pharmacol Rev 2003, 55:133-166.
62. Caligiuri G, Rudling M, Ollivier V, et al.: Interleukin-10 deficiency increases atherosclerosis, thrombosis, and low-density lipoproteins in apolipoprotein E knockout mice. Mol Med 2003, 9:10-17.
63. Pinderski Oslund L, Hedrick C, Olvera T, et al.: Interleukin-10 blocks atherosclerotic events in vitro and in vivo. Arterioscler Thromb Vasc Biol 1999, 19:2847-2853.
64. Pinderski L, Fischbein M, Subbanagounder G, et al.: Over-expression 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.
65. Von Der Thüsen J, Kuiper J, Fekkes M, 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.
66. Whitman S, Ravisankar P, Elam H, Daugherty A: Exogenous interferon-gamma enhances atherosclerosis in apolipoprotein E-/- mice. Am J Pathol 2000, 157:1819-1824.
67. Tellides G, Tereb D, Kirkiles-Smith N, et al.: Interferon-gamma elicits arteriosclerosis in the absence of leukocytes. Nature 2000, 403:207-211.
68. Gupta S, Pablo A, Jiang X, et al.: IFN-gamma potentiates atherosclerosis in ApoE knock-out mice. J Clin Invest 1997, 99:2752-2761.
69. Whitman S, 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.
70. Koga M, Kai H, Yasukawa H, et al.: Inhibition of progression and stabilization of plaques by postnatal interferon-gamma function blocking in ApoE-knockout mice. Circ Res 2007, 101:348-356.
71. 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.
72. Lee T, Yen H, Pan C, Chau L: The role of interleukin 12 in the development of atherosclerosis in ApoE-deficient mice. Arterioscler Thromb Vasc Biol 1999, 19:734-742.
73. Hauer A, Uyttenhove C, de Vos P, et al.: Blockade of interleukin-12 function by protein vaccination attenuates atherosclerosis. Circulation 2005, 112:1054-1062.
74. Whitman S, Ravisankar P, Daugherty A: Interleukin-18 enhances atherosclerosis in apolipoprotein E(-/-) mice through release of interferon-gamma. Circ Res 2002, 90: E34-E38.
75. 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.
76. George J, Mulkins M, Shaish A, et al.: Interleukin (IL)-4 deficiency does not influence fatty streak formation in C57BL/6 mice. Atherosclerosis 2000, 153:403-411.
77. Huber S, Sakkinen P, Conze D, et al.: Interleukin-6 exacerbates early atherosclerosis in mice. Arterioscler Thromb Vasc Biol 1999, 19:2364-2367.
78. Bazan J, Bacon K, Hardiman G, et al.: A new class of membrane-bound chemokine with a CX3C motif. Nature 1997, 385:640-644.
79. Lucas A, Bursill C, Guzik T, et al.: Smooth muscle cells in human atherosclerotic plaques express the fractalkine receptor CX3CR1 and undergo chemotaxis to the CX3C chemokine fractalkine (CX3CL1). Circulation 2003, 108:2498-2504.
80. Wong B, Wong D, McManus B: Characterization of fractalkine (CX3CL1) and CX3CR1 in human coronary arteries with native atherosclerosis, diabetes mellitus, and transplant vascular disease. Cardiovasc Pathol 2002, 11:332-338.
81. Teupser D, Pavlides S, Tan M, et al.: Major reduction of atherosclerosis in fractalkine (CX3CL1)-deficient mice is at the brachiocephalic artery, not the aortic root. Proc Natl Acad Sci U S A 2004, 101:17795-17800.
82. Combadière C, Potteaux S, Gao J, et al.: Decreased atherosclerotic lesion formation in CX3CR1/apolipoprotein E double knockout mice. Circulation 2003, 107:1009-1016.
83. Lesnik P, Haskell C, Charo I: Decreased atherosclerosis in CX3CR1-/- mice reveals a role for fractalkine in atherogenesis. J Clin Invest 2003, 111:333-340.
84. Berliner J, Navab M, Fogelman A, et al.: Atherosclerosis: basic mechanisms. Oxidation, inflammation, and genetics. Circulation 1995, 91:2488-2496.
85. Schober A, Zernecke A, Liehn E, et al.: Crucial role of the CCL2/CCR2 axis in neointimal hyperplasia after arterial injury in hyperlipidemic mice involves early monocyte recruitment and CCL2 presentation on platelets. Circ Res 2004, 95:1125-1133.