Mouse models of neointimal hyperplasia: Techniques and applications

Medical Science Monitor

Volumn 12, Issue 9, 2006, Pages

  Wang, Xinwen ^a   Chai, Hong ^a   Lin, Peter H ^a   Lumsden, Alan B ^a   Yao, Qizhi ^a   Chen, Changyi ^a  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

Flow cessation; Mechanical injury; Mouse; Neointimal hyperplasia; Restenosis; Vein graft

Indexed keywords

FASUDIL; INTERLEUKIN 10; RAPAMYCIN; ROSIGLITAZONE; SIMVASTATIN; TANSHINONE; TRANILAST;

ALLOGRAFT; ARTERY INTIMA PROLIFERATION; BLOOD FLOW; BYPASS SURGERY; CAROTID ARTERY LIGATION; ELECTRIC INJURY; GENE TRANSFER; NONHUMAN; REVIEW; VASCULAR DISEASE;

ANIMALS; DISEASE MODELS, ANIMAL; HYPERPLASIA; MICE; TUNICA INTIMA;

EID: 33748549007     PISSN: 12341010     EISSN: 16433750     Source Type: Journal    
DOI: None     Document Type: Review

References (91)

1. Muller DW, Ellis SG, Topol EJ: Experimental models of coronary artery restenosis. J Am Coll Cardiol, 1992; 19(2): 418-32
2. Schwartz RS: Neointima and arterial injury: dogs, rats, pigs, and more. Lab Invest, 1994; 71(6): 789-91
3. Ferns GA, Avades TY: The mechanisms of coronary restenosis: insights from experimental models. Int J Exp Pathol, 2000; 81(2): 63-88
4. Clowes AW, Reidy MA, Clowes MM: Kinetics of cellular proliferation after arterial injury. I. Smooth muscle growth in the absence of endothelium. Lab Invest, 1983; 49(3): 327-33
5. Reidy MA, Clowes AW, Schwartz SM: Endothelial regeneration. V. Inhibition of endothelial regrowth in arteries of rat and rabbit. Lab Invest, 1983; 49(5): 569-75
6. Richardson M, Kinlough-Rathbone RL, Groves HM et al: Ultrastructural changes in re-endothelialized and non-endothelialized rabbit aortic neo-intima following re-injury with a balloon catheter. Br J Exp Pathol, 1984; 65(5): 597-611
7. Alavi M, Dunnett CW, Moore S: Lipid composition of rabbit aortic wall following removal of endothelium by balloon catheter. Arteriosclerosis, 1983; 3(5): 413-19
8. Schwartz RS, Murphy JG, Edwards WD et al: Restenosis after balloon angioplasty. A practical proliferative model in porcine coronary arteries. Circulation, 1990; 82(6): 2190-200
9. Geary RL, Williams JK, Golden D et al: Time course of cellular proliferation, intimal hyperplasia, and remodeling following angioplasty in monkeys with established atherosclerosis. A nonhuman primate model of restenosis. Arterioscler Thromb Vasc Biol, 1996; 16(1): 34-43
10. Allayee H, Ghazalpour A, Lusis AJ: Using mice to dissect genetic factors in atherosclerosis. Arterioscler Thromb Vasc Biol, 2003; 23(9): 1501-9
11. Knowles JW, Maeda N: Genetic modifiers of atherosclerosis in mice. Arterioscler Thromb Vasc Biol, 2000; 20(11): 2336-45
12. Xu Q: Mouse models of arteriosclerosis: from arterial injuries to vascular grafts. Am J Pathol, 2004; 165(1): 1-10
13. Geary RL, Kohler TR, Vergel S et al: Time course of flow-induced smooth muscle cell proliferation and intimal thickening in endothelialized baboon vascular grafts. Circ Res, 1994; 74(1): 14-23
14. Kohler TR, Kirkman TR, Kraiss LW et al: Increased blood flow inhibits neointimal hyperplasia in endothelialized vascular grafts. Circ Res, 1991; 69(6): 1557-65
15. Kumar A, Lindner V: Remodeling with neointima formation in the mouse carotid artery after cessation of blood flow. Arterioscler Thromb Vasc Biol, 1997; 17(10): 2238-44
16. Korshunov VA, Berk BC: Flow-induced vascular remodeling in the mouse: a model for carotid intima-media thickening. Arterioscler Thromb Vasc Biol, 2003; 23(12): 2185-91
17. Rudic RD, Shesely EG, Maeda N et al: Direct evidence for the importance of endothelium-derived nitric oxide in vascular remodeling. J Clin Invest, 1998; 101(4): 731-36
18. Ku DN, Giddens DP, Zarins CK, Glagov S: Pulsatile flow and atherosclerosis in the human carotid bifurcation. Positive correlation between plaque location and low oscillating shear stress. Arteriosclerosis, 1985; 5(3): 293-302
19. Harmon KJ, Couper LL, Lindner V: Strain-dependent vascular remodeling phenotypes in inbred mice. Am J Pathol, 2000; 156(5): 1741-48
20. Korshunov VA, Berk BC: Strain-dependent vascular remodeling: the "Glagov phenomenon" is genetically determined. Circulation, 2004; 110(2): 220-26
21. Li Y, Minamino T, Tsukamoto O et al: Ablation of MEK kinase 1 suppresses intimal hyperplasia by impairing smooth muscle cell migration and urokinase plasminogen activator expression in a mouse blood-flow cessation model. Circulation, 2005; 111(13): 1672-78
22. Myers DL, Harmon KJ, Lindner V, Liaw L: Alterations of arterial physiology in osteopontin-null mice. Arterioscler Thromb Vasc Biol, 2003; 23(6): 1021-28
23. Kuzuya M, Kanda S, Sasaki T et al: Deficiency of gelatinase a suppresses smooth muscle cell invasion and development of experimental intimal hyperplasia. Circulation, 2003; 108(11): 1375-81
24. Galis ZS, Johnson C, Godin D et al: Targeted disruption of the matrix metalloproteinase-9 gene impairs smooth muscle cell migration and geometrical arterial remodeling. Circ Res, 2002; 91(9): 852-59
25. Kawasaki T, Dewerchin M, Lijnen HR et al: Mouse carotid artery ligation induces platelet-leukocyte-dependent luminal fibrin, required for neointima development. Circ Res, 2001; 88(2): 159-66
26. Horiba M, Kadomatsu K, Nakamura E et al: Neointima formation in a restenosis model is suppressed in midkine-deficient mice. J Clin Invest, 2000; 105(4): 489-95
27. Emanueli C, Bonaria Salis M, Figueroa C et al: Participation of kinins in the captopril-induced inhibition of intimal hyperplasia caused by interruption of carotid blood flow in the mouse. Br J Pharmacol, 2000; 130(5): 1076-82
28. Spencer JA, Hacker SL, Davis EC et al: Altered vascular remodeling in fibulin-5-deficient mice reveals a role of fibulin-5 in smooth muscle cell proliferation and migration. Proc Natl Acad Sci USA, 2005; 102(8): 2946-51
29. de Waard V, Arkenbout EK, Carmeliet P et al: Plasminogen activator inhibitor 1 and vitronectin protect against stenosis in a murine carotid artery ligation model. Arterioscler Thromb Vasc Biol, 2002; 22(12): 1978-83
30. Murakoshi N, Miyauchi T, Kakinuma Y et al: Vascular endothelin-B receptor system in vivo plays a favorable inhibitory role in vascular remodeling after injury revealed by endothelin-B receptor-knockout mice. Circulation, 2002; 106(15): 1991-98
31. Kraemer R: Reduced apoptosis and increased lesion development in the flow-restricted carotid artery of p75(NTR)-null mutant mice. Circ Res, 2002; 91(6): 494-500
32. Ivan E, Khatri JJ, Johnson C et al: Expansive arterial remodeling is associated with increased neointimal macrophage foam cell content: the murine model of macrophage-rich carotid artery lesions. Circulation, 2002; 105(22): 2686-91
33. Yuan Y, Liao L, Tulis DA, Xu J: Steroid receptor coactivator-3 is required for inhibition of neointima formation by estrogen. Circulation, 2002; 105(22): 2653-59
34. Sindermann JR, Smith J, Kobbert C et al: Direct evidence for the importance of p130 in injury response and arterial remodeling following carotid artery ligation. Cardiovasc Res, 2002; 54(3): 676-83
35. Sata M, Walsh K: Fas ligand-deficient mice display enhanced leukocyte infiltration and intima hyperplasia in flow-restricted vessels. J Mol Cell Cardiol, 2000; 32(8): 1395-400
36. Arkenbout EK, de Waard V, van Bragt M et al: Protective function of transcription factor TR3 orphan receptor in atherogenesis: decreased lesion formation in carotid artery ligation model in TR3 transgenic mice. Circulation, 2002; 106(12): 1530-35
37. Kawashima S, Yamashita T, Ozaki M et al: Endothelial NO synthase overexpression inhibits lesion formation in mouse model of vascular remodeling. Arterioscler Thromb Vasc Biol, 2001; 21(2): 201-7
38. Emanueli C, Salis MB, Chao J et al: Adenovirus-mediated human tissue kallikrein gene delivery inhibits neointima formation induced by interruption of blood flow in mice. Arterioscler Thromb Vasc Biol, 2000; 20(6): 1459-66
39. Lombardi JV, Naji M, Larson RA et al: Adenoviral mediated uteroglobin gene transfer to the adventitia reduces arterial intimal hyperplasia. J Surg Res, 2001; 99(2): 377-80
40. Singh R, Pan S, Mueske CS et al: Role for tissue factor pathway in murine model of vascular remodeling. Circ Res, 2001; 89(1): 71-76
41. Jonsson-Rylander AC, Nilsson T, Fritsche-Danielson R et al: Role of ADAMTS-1 in atherosclerosis: remodeling of carotid artery, immunohistochemistry, and proteolysis of versican. Arterioscler Thromb Vasc Biol, 2005; 25(1): 180-85
42. Chen YL, Yang SP, Shiao MS et al: Salvia miltiorrhiza inhibits intimal hyperplasia and monocyte chemotactic protein-1 expression after balloon injury in cholesterol-fed rabbits. J Cell Biochem, 2001; 83(3): 484-93
43. Du JR, Li X, Zhang R, Qian ZM: Tanshinone inhibits intimal hyperplasia in the ligated carotid artery in mice. J Ethnopharmacol, 2005; 98(3): 319-22
44. Pearce JD, Li J, Edwards MS, English WP, Geary RL: Differential effects of Rho-kinase inhibition on artery wall mass and remodeling. J Vasc Surg, 2004; 39(1): 223-28
45. Qin F, Impeduglia T, Schaffer P, Dardik H: Overexpression of von Willebrand factor is an independent risk factor for pathogenesis of intimal hyperplasia: preliminary studies. J Vasc Surg, 2003; 37(2): 433-39
46. Godin D, Ivan E, Johnson C, Magid R, Galis ZS: Remodeling of carotid artery is associated with increased expression of matrix metalloproteinases in mouse blood flow cessation model. Circulation, 2000; 102(23): 2861-66
47. Lindner V, Fingerle J, Reidy MA: Mouse model of arterial injury. Circ Res, 1993; 73(5): 792-96
48. Carmeliet P, Moons L, Collen D: Mouse models of angiogenesis, arterial stenosis, atherosclerosis and hemostasis. Cardiovasc Res, 1998; 39(1): 8-33
49. Cheung WM, D'Andrea MR, Andrade-Gordon P, Damiano BP: Altered vascular injury responses in mice deficient in protease-activated receptor-1. Arterioscler Thromb Vasc Biol, 1999; 19(12): 3014-24
50. Konishi H, Katoh Y, Takaya N et al: Platelets activated by collagen through immunoreceptor tyrosine-based activation motif play pivotal role in initiation and generation of neointimal hyperplasia after vascular injury. Circulation, 2002; 105(8): 912-16
51. Smyth SS, Reis ED, Zhang W et al: Beta(3)-integrin-deficient mice but not P-selectin-deficient mice develop intimal hyperplasia after vascular injury: correlation with leukocyte recruitment to adherent platelets 1 hour after injury. Circulation, 2001; 103(20): 2501-7
52. Sata M, Sugiura S, Yoshizumi M et al: Acute and chronic smooth muscle cell apoptosis after mechanical vascular injury can occur independently of the Fas-death pathway. Arterioscler Thromb Vasc Biol, 2001; 21(11): 1733-37
53. Sullivan TR Jr, Karas RH, Aronovitz M et al: Estrogen inhibits the response-to-injury in a mouse carotid artery model. J Clin Invest, 1995; 96(5): 2482-88
54. Iafrati MD, Karas RH, Aronovitz M et al: Estrogen inhibits the vascular injury response in estrogen receptor alpha-deficient mice. Nat Med, 1997; 3(5): 545-48
55. De Geest B, Zhao Z, Collen D, Holvoet P: Effects of adenovirus-mediated human apo A-I gene transfer on neointima formation after endothelial denudation in apo E-deficient mice. Circulation, 1997; 96(12): 4349-56
56. Hutter R, Carrick FE, Valdiviezo C et al: Vascular endothelial growth factor regulates reendothelialization and neointima formation in a mouse model of arterial injury. Circulation, 2004; 110(16): 2430-35
57. Pyo R, Jensen KK, Wiekowski MT et al: Inhibition of intimal hyperplasia in transgenic mice conditionally expressing the chemokine-binding protein M3. Am J Pathol, 2004; 164(6): 2289-97
58. Zimmerman MA, Reznikov LL, Raeburn CD, Selzman CH: Interleukin-10 attenuates the response to vascular injury. J Surg Res, 2004; 121(2): 206-13
59. Wang CH, Ciliberti N, Li SH et al: Rosiglitazone facilitates angiogenic progenitor cell differentiation toward endothelial lineage: a new paradigm in glitazone pleiotropy. Circulation, 2004; 109(11): 1392-400
60. Werner N, Junk S, Laufs U et al: Intravenous transfusion of endothelial progenitor cells reduces neointima formation after vascular injury. Circ Res, 2003; 93(2): e17-24
61. Zou Y, Dietrich H, Hu Y et al: Mouse model of venous bypass graft arteriosclerosis. Am J Pathol, 1998; 153(4): 1301-10
62. Zhang L, Hagen PO, Kisslo J et al: Neointimal hyperplasia rapidly reaches steady state in a novel murine vein graft model. J Vasc Surg, 2002; 36(4): 824-32
63. Kwei S, Stavrakis G, Takahas M et al: Early adaptive responses of the vascular wall during venous arterialization in mice. Am J Pathol, 2004; 164(1): 81-89
64. Diao Y, Xue J, Segal MS: A novel mouse model of autologous venous graft intimal hyperplasia(1,2). J Surg Res, 2005; 126(1): 106-13
65. Shi C, Patel A, Zhang D et al: Plasminogen is not required for neointima formation in a mouse model of vein graft stenosis. Circ Res, 1999; 84(8): 883-90
66. Cooley BC: Model of murine interpositional vein grafting. Microsurgery, 2005; 25(3): 209-12
67. Dietrich H, Hu Y, Zou Y et al: Rapid development of vein graft atheroma in ApoE-deficient mice. Am J Pathol, 2000; 157(2): 659-69
68. Mayr U, Mayr M, Li C et al: Loss of p53 accelerates neointimal lesions of vein bypass grafts in mice. Circ Res, 2002; 90(2): 197-204
69. Zou Y, Hu Y, Mayr M et al: Reduced neointima hyperplasia of vein bypass grafts in intercellular adhesion molecule-1-deficient mice. Circ Res, 2000; 86(4): 434-40
70. Lardenoye JH, de Vries MR, Lowik CW et al: Accelerated atherosclerosis and calcification in vein grafts: a study in APOE*3 Leiden transgenic mice. Circ Res, 2002; 91(7): 577-84
71. Hu Y, Baker AH, Zou Y et al: Local gene transfer of tissue inhibitor of metalloproteinase-2 influences vein graft remodeling in a mouse model. Arterioscler Thromb Vasc Biol, 2001; 21(8): 1275-80
72. Schachner T, Zou Y, Oberhuber A et al: Local application of rapamycin inhibits neointimal hyperplasia in experimental vein grafts. Ann Thorac Surg, 2004; 77(5): 1580-85
73. Schachner T, Zou Y, Oberhuber A et al: Perivascular application of C-type natriuretic peptide attenuates neointimal hyperplasia in experimental vein grafts. Eur J Cardiothorac Surg, 2004; 25(4): 585-90
74. Hu Y, Zou Y, Dietrich H et al: Inhibition of neointima hyperplasia of mouse vein grafts by locally applied suramin. Circulation, 1999; 100(8): 861-68
75. Carmeliet P, Moons L, Stassen JM et al: Vascular wound healing and neointima formation induced by perivascular electric injury in mice. Am J Pathol, 1997; 150(2): 761-76
76. Carmeliet P, Moons L, Herbert JM et al: Urokinase but not tissue plasminogen activator mediates arterial neointima formation in mice. Circ Res, 1997; 81(5): 829-39
77. Carmeliet P, Moons L, Lijnen R et al: Inhibitory role of plasminogen activator inhibitor-1 in arterial wound healing and neointima formation: a gene targeting and gene transfer study in mice. Circulation, 1997; 96(9): 3180-91
78. Carmeliet P, Moons L, Ploplis V et al: Impaired arterial neointima formation in mice with disruption of the plasminogen gene. J Clin Invest, 1997; 99(2): 200-8
79. Booth RF, Martin JF, Honey AC et al: Rapid development of atherosclerotic lesions in the rabbit carotid artery induced by perivascular manipulation. Atherosclerosis, 1989; 76(2-3): 257-68
80. Moroi M, Zhang L, Yasuda T et al: Interaction of genetic deficiency of endothelial nitric oxide, gender, and pregnancy in vascular response to injury in mice. J Clin Invest, 1998; 101(6): 1225-32
81. Isoda K, Shiigai M, Ishigami N et al: Deficiency of interleukin-1 receptor antagonist promotes neointimal formation after injury. Circulation, 2003; 108(5): 516-18
82. Tacken PJ, Delsing DJ, Gijbels MJ et al: VLDL receptor deficiency enhances intimal thickening after vascular injury but does not affect atherosclerotic lesion area. Atherosclerosis, 2002; 162(1): 103-10
83. Fishman JA, Ryan GB, Karnovsky MJ: Endothelial regeneration in the rat carotid artery and the significance of endothelial denudation in the pathogenesis of myointimal thickening. Lab Invest, 1975; 32(3): 339-51
84. Simon DI, Dhen Z, Seifert P et al: Decreased neointimal formation in Mac-1(-/-) mice reveals a role for inflammation in vascular repair after angioplasty. J Clin Invest, 2000; 105(3): 293-300
85. Kikuchi S, Umemura K, Kondo K et al: Photochemically induced endothelial injury in the mouse as a screening model for inhibitors of vascular intimal thickening. Arterioscler Thromb Vasc Biol, 1998; 18(7): 1069-78
86. Kondo K, Umemura K, Miyaji M, Nakashima M: Milrinone, a phosphodiesterase inhibitor, suppresses intimal thickening after photochemically induced endothelial injury in the mouse femoral artery. Atherosclerosis, 1999; 142(1): 133-38
87. Shi C, Russell ME, Bianchi C et al: Murine model of accelerated transplant arteriosclerosis. Circ Res, 1994; 75(2): 199-207
88. Shi C, Feinberg MW, Zhang D et al: Donor MHC and adhesion molecules in transplant arteriosclerosis. J Clin Invest, 1999; 103(4): 469-74
89. Russell PS, Chase CM, Winn HJ, Colvin RB: Coronary atherosclerosis in transplanted mouse hearts. I. Time course and immunogenetic and immunopathological considerations. Am J Pathol, 1994; 144(2): 260-74
90. Hirozane T, Matsumori A, Furukawa Y, Sasayama S: Experimental graft coronary artery disease in a murine heterotopic cardiac transplant model. Circulation, 1995; 91(2): 386-92
91. Russell PS, Chase CM, Colvin RB: Accelerated atheromatous lesions in mouse hearts transplanted to apolipoprotein-E-deficient recipients. Am J Pathol, 1996; 149(1): 91-99