Arteriosclerosis, Thrombosis, and Vascular Biology. 2000;20:335-342
© 2000 American Heart Association, Inc.
Vascular Biology |
Mouse Model of Femoral Artery Denudation Injury Associated With the Rapid Accumulation of Adhesion Molecules on the Luminal Surface and Recruitment of Neutrophils
From the Zena and Michael A. Wiener Cardiovascular Institute, Department of Medicine (M.R., J.T.F., J.J.B., M.B.T.); the Department of Pathology (J.T.F.); the Department of Physiology and Biophysics (M.B.T.); and the Department of Surgery (W.X.Z., E.D.R.), Mount Sinai School of Medicine, New York, NY.
Correspondence to Ernane D. Reis, MD, Department of Surgery, Box 1259, The Mount Sinai Medical Center, One Gustave L. Levy Pl, New York, NY 10029-6574. E-mail ernane.reis{at}smtplink.mssm.edu
Abstract—Techniques of arterial injury commonly used in animals to mimic endovascular procedures are not suitable for small mouse arteries. This has limited examination of the response to arterial injury in genetically modified mice. We therefore sought to develop a model of transluminal injury to the mouse femoral artery that would be reproducible and result in substantial levels of intimal hyperplasia. Mice of the C57BL/6 strain underwent bilateral femoral artery denudation by passage of an angioplasty guidewire. Intimal hyperplasia was observed in 10% of injured arteries at 1 week, in 88% at 2 weeks, and in 90% at 4 weeks. The mean intimal-to-medial area ratio reached 1.1±0.1 at 4 weeks. No intimal proliferation was found in control sham-operated arteries. One hour after injury, the denuded surface was covered with platelets and leukocytes, predominantly neutrophils. This was associated with the accumulation of P-selectin, intercellular adhesion molecule-1, and vascular cell adhesion molecule-1. Expression of these adhesion molecules was not seen in the underlying medial smooth muscle cells. At 24 hours, few neutrophils remained on the denuded surface. At 1 week, macrophages and platelets were present in the vessel wall, partially covered by regenerated endothelium. Transluminal wire injury to the mouse femoral artery induces abundant intimal hyperplasia formation by 2 and 4 weeks and elicits the rapid accumulation of leukocytes and adhesion molecules on the denuded luminal surface. This model will be a valuable tool to study arterial injury in genetically modified mouse models.
Key Words: arterial injury • cell adhesion molecules • intimal hyperplasia • mice • neutrophils
This article has been cited by other articles:
 |
|
 |
|
  G. Grassia, M. Maddaluno, A. Guglielmotti, G. Mangano, G. Biondi, P. Maffia, and A. Ialenti The anti-inflammatory agent bindarit inhibits neointima formation in both rats and hyperlipidaemic mice Cardiovasc Res, December 1, 2009; 84(3): 485 - 493. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 M. P. Cole, T. K. Rudolph, N. K.H. Khoo, U. N. Motanya, F. Golin-Bisello, J. W. Wertz, F. J. Schopfer, V. Rudolph, S. R. Woodcock, S. Bolisetty, et al. Nitro-Fatty Acid Inhibition of Neointima Formation After Endoluminal Vessel Injury Circ. Res., November 6, 2009; 105(10): 965 - 972. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 Advanced Glycation End Product Receptor-1 Transgenic Mice Are Resistant to Inflammation, Oxidative Stress, and Post-Injury Intimal Hyperplasia Am. J. Pathol., October 1, 2009; 175(4): 1722 - 1732.
|
|
|
|
 |
|
 K. Croce, H. Gao, Y. Wang, T. Mooroka, M. Sakuma, C. Shi, G. K. Sukhova, R. R.S. Packard, N. Hogg, P. Libby, et al. Myeloid-Related Protein-8/14 Is Critical for the Biological Response to Vascular Injury Circulation, August 4, 2009; 120(5): 427 - 436. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 H. Wang, W. Zhang, R. Tang, R. P. Hebbel, M. A. Kowalska, C. Zhang, J. D. Marth, M. Fukuda, C. Zhu, and Y. Huo Core2 1-6-N-Glucosaminyltransferase-I Deficiency Protects Injured Arteries From Neointima Formation in ApoE-Deficient Mice Arterioscler Thromb Vasc Biol, July 1, 2009; 29(7): 1053 - 1059. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S.-L. Liu, Y.-H. Li, G.-Y. Shi, S.-H. Tang, S.-J. Jiang, C.-W. Huang, P.-Y. Liu, J.-S. Hong, and H.-L. Wu Dextromethorphan reduces oxidative stress and inhibits atherosclerosis and neointima formation in mice Cardiovasc Res, April 1, 2009; 82(1): 161 - 169. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 J. Shan, T. B. Nguyen, H. Totary-Jain, H. Dansky, S. O. Marx, and A. R. Marks Leptin-enhanced neointimal hyperplasia is reduced by mTOR and PI3K inhibitors PNAS, December 2, 2008; 105(48): 19006 - 19011. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
A. Schober Chemokines in Vascular Dysfunction and Remodeling Arterioscler Thromb Vasc Biol, November 1, 2008; 28(11): 1950 - 1959. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 E. A. Lasater, W. K. Bessler, L. E. Mead, W. E. Horn, D. W. Clapp, S. J. Conway, D. A. Ingram, and F. Li Nf1+/- mice have increased neointima formation via hyperactivation of a Gleevec sensitive molecular pathway Hum. Mol. Genet., August 1, 2008; 17(15): 2336 - 2344. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
G. Li, J. M. Sanders, M. H. Bevard, Z. Sun, J. W. Chumley, E. V. Galkina, K. Ley, and I. J. Sarembock CD40 Ligand Promotes Mac-1 Expression, Leukocyte Recruitment, and Neointima Formation after Vascular Injury Am. J. Pathol., April 1, 2008; 172(4): 1141 - 1152. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
T. G. Nuhrenberg, N. Langwieser, J. B.K. Schwarz, Y. Hou, P. Frank, F. Sorge, S. Matschurat, S. Seidl, A. Kastrati, A. Schomig, et al. EMAP-II downregulation contributes to the beneficial effects of rapamycin after vascular injury Cardiovasc Res, February 1, 2008; 77(3): 580 - 589. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Yang, M. Koupenova, D. J. McCrann, K. J. Kopeikina, H. M. Kagan, B. M. Schreiber, and K. Ravid The A2b adenosine receptor protects against vascular injury PNAS, January 15, 2008; 105(2): 792 - 796. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. J. Westrick, M. E. Winn, and D. T. Eitzman Murine Models of Vascular Thrombosis Arterioscler Thromb Vasc Biol, October 1, 2007; 27(10): 2079 - 2093. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. M. Sanz-Gonzalez, L. Barquin, I. Garcia-Cao, M. Roque, J. M. Gonzalez, J. J. Fuster, M. T. Castells, J. M. Flores, M. Serrano, and V. Andres Increased p53 gene dosage reduces neointimal thickening induced by mechanical injury but has no effect on native atherosclerosis Cardiovasc Res, September 1, 2007; 75(4): 803 - 812. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 X.-L. Niu, J. Li, Z. S. Hakim, M. Rojas, M. S. Runge, and N. R. Madamanchi Leukocyte Antigen-related Deficiency Enhances Insulin-like Growth Factor-1 Signaling in Vascular Smooth Muscle Cells and Promotes Neointima Formation in Response to Vascular Injury J. Biol. Chem., July 6, 2007; 282(27): 19808 - 19819. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. A. Ali, N. J. Alp, H. Lupton, N. Arnold, T. Bannister, Y. Hu, S. Mussa, M. Wheatcroft, D. R. Greaves, J. Gunn, et al. Increased In-Stent Stenosis in ApoE Knockout Mice: Insights from a Novel Mouse Model of Balloon Angioplasty and Stenting Arterioscler Thromb Vasc Biol, April 1, 2007; 27(4): 833 - 840. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. Kothapalli, L. Zhao, E. A. Hawthorne, Y. Cheng, E. Lee, E. Pure, and R. K. Assoian Hyaluronan and CD44 antagonize mitogen-dependent cyclin D1 expression in mesenchymal cells J. Cell Biol., February 12, 2007; 176(4): 535 - 544. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. R. Anderson, J. M. Tsutsui, F. Xie, S. J. Radio, and T. R. Porter The role of complement in the adherence of microbubbles to dysfunctional arterial endothelium and atherosclerotic plaque Cardiovasc Res, February 1, 2007; 73(3): 597 - 606. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 D. L. Basi, N. Adhikari, A. Mariash, Q. Li, E. Kao, S. V. Mullegama, and J. L. Hall Femoral artery neointimal hyperplasia is reduced after wire injury in Ref-1+/- mice Am J Physiol Heart Circ Physiol, January 1, 2007; 292(1): H516 - H521. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S.-F. Yan, E. Harja, M. Andrassy, T. Fujita, and A. M. Schmidt Protein Kinase C {beta}/Early Growth Response-1 Pathway: A Key Player in Ischemia, Atherosclerosis, and Restenosis J. Am. Coll. Cardiol., October 27, 2006; 48(9_Suppl_A): A47 - A55. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Q. Xiao, L. Zeng, Z. Zhang, A. Margariti, Z. A Ali, K. M. Channon, Q. Xu, and Y. Hu Sca-1+ Progenitors Derived From Embryonic Stem Cells Differentiate Into Endothelial Cells Capable of Vascular Repair After Arterial Injury Arterioscler Thromb Vasc Biol, October 1, 2006; 26(10): 2244 - 2251. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
P. Liu, S. Patil, M. Rojas, A. M. Fong, S. S. Smyth, and D. D. Patel CX3CR1 Deficiency Confers Protection From Intimal Hyperplasia After Arterial Injury Arterioscler Thromb Vasc Biol, September 1, 2006; 26(9): 2056 - 2062. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 B.-A. Khaw, Y. Tekabe, and L. L. Johnson Imaging Experimental Atherosclerotic Lesions in ApoE Knockout Mice: Enhanced Targeting with Z2D3-Anti-DTPA Bispecific Antibody and 99mTc-Labeled Negatively Charged Polymers J. Nucl. Med., May 1, 2006; 47(5): 868 - 876. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. Ogawa, T. Nomiyama, T. Nakamachi, E. B. Heywood, J. F. Stone, J. P. Berger, R. E. Law, and D. Bruemmer Activation of Peroxisome Proliferator-Activated Receptor {gamma} Suppresses Telomerase Activity in Vascular Smooth Muscle Cells Circ. Res., April 14, 2006; 98(7): e50 - e59. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. Wei, T. E. Gorman, X. Liu, B. Ith, A. Tseng, Z. Chen, D. I. Simon, M. D. Layne, and S.-F. Yet Increased Neointima Formation in Cysteine-Rich Protein 2-Deficient Mice in Response to Vascular Injury Circ. Res., December 9, 2005; 97(12): 1323 - 1331. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Wang, M. Sakuma, Z. Chen, V. Ustinov, C. Shi, K. Croce, A. C. Zago, J. Lopez, P. Andre, E. Plow, et al. Leukocyte Engagement of Platelet Glycoprotein Ib{alpha} via the Integrin Mac-1 Is Critical for the Biological Response to Vascular Injury Circulation, November 8, 2005; 112(19): 2993 - 3000. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. Ott, C. Michaelis, M. Schuermann, B. Steppich, I. Seitz, M. Dewerchin, D. Zohlnhofer, R. Wessely, M. Rudelius, A. Schomig, et al. Vascular Remodeling in Mice Lacking the Cytoplasmic Domain of Tissue Factor Circ. Res., August 5, 2005; 97(3): 293 - 298. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Andrassy, D. Belov, E. Harja, Y. S. Zou, M. Leitges, H. A. Katus, P. P. Nawroth, S. D. Yan, A. M. Schmidt, and S.-F. Yan Central Role of PKC{beta} in Neointimal Expansion Triggered by Acute Arterial Injury Circ. Res., March 4, 2005; 96(4): 476 - 483. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Sakata, F. Xiang, Z. Chen, Y. Kiriyama, C. N. Kamei, D. I. Simon, and M. T. Chin Transcription Factor CHF1/Hey2 Regulates Neointimal Formation In Vivo and Vascular Smooth Muscle Proliferation and Migration In Vitro Arterioscler Thromb Vasc Biol, November 1, 2004; 24(11): 2069 - 2074. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
I. F. Charo and M. B. Taubman Chemokines in the Pathogenesis of Vascular Disease Circ. Res., October 29, 2004; 95(9): 858 - 866. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Hutter, F. E. Carrick, C. Valdiviezo, C. Wolinsky, J. S. Rudge, S. J. Wiegand, V. Fuster, J. J. Badimon, and B. V. Sauter Vascular Endothelial Growth Factor Regulates Reendothelialization and Neointima Formation in a Mouse Model of Arterial Injury Circulation, October 19, 2004; 110(16): 2430 - 2435. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Z. Chen, J. F. Keaney Jr., E. Schulz, B. Levison, L. Shan, M. Sakuma, X. Zhang, C. Shi, S. L. Hazen, and D. I. Simon Decreased neointimal formation in Nox2-deficient mice reveals a direct role for NADPH oxidase in the response to arterial injury PNAS, August 31, 2004; 101(35): 13014 - 13019. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
Y. Naka, L. G. Bucciarelli, T. Wendt, L. K. Lee, L. L. Rong, R. Ramasamy, S. F. Yan, and A. M. Schmidt RAGE Axis: Animal Models and Novel Insights Into the Vascular Complications of Diabetes Arterioscler Thromb Vasc Biol, August 1, 2004; 24(8): 1342 - 1349. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Pyo, K. K. Jensen, M. T. Wiekowski, D. Manfra, A. Alcami, M. B. Taubman, and S. A. Lira Inhibition of Intimal Hyperplasia in Transgenic Mice Conditionally Expressing the Chemokine-Binding Protein M3 Am. J. Pathol., June 1, 2004; 164(6): 2289 - 2297. [Abstract] [Full Text] [PDF]
|
|
|
|
 |
|
 S.-F. Yan, R. Ramasamy, L. G Bucciarelli, T. Wendt, L. K Lee, B. I Hudson, D. M Stenr, E. Lalla, S. Du Yan, L. L. Rong, et al. RAGE and its ligands: a lasting memory in diabetic complications? Diabetes and Vascular Disease Research, May 1, 2004; 1(1): 10 - 20. [Abstract] [PDF]
|
|
|
|
 |
|
 N. S. Haque, J. T. Fallon, J. J. Pan, M. B. Taubman, and P. C. Harpel Chemokine receptor-8 (CCR8) mediates human vascular smooth muscle cell chemotaxis and metalloproteinase-2 secretion Blood, February 15, 2004; 103(4): 1296 - 1304. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. H. von der Thusen, M. L. Fekkes, R. Passier, A.J. van Zonneveld, V. Mainfroid, T. J.C. van Berkel, and E. A.L. Biessen Adenoviral Transfer of Endothelial Nitric Oxide Synthase Attenuates Lesion Formation in a Novel Murine Model of Postangioplasty Restenosis Arterioscler Thromb Vasc Biol, February 1, 2004; 24(2): 357 - 362. [Abstract] [Full Text]
|
|
|
|
|
|
K. Stephenson, J. Tunstead, A. Tsai, R. Gordon, S. Henderson, and H. M. Dansky Neointimal Formation After Endovascular Arterial Injury Is Markedly Attenuated in db/db Mice Arterioscler Thromb Vasc Biol, November 1, 2003; 23(11): 2027 - 2033. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. D. Danenberg, A. J. Szalai, R. V. Swaminathan, L. Peng, Z. Chen, P. Seifert, W. P. Fay, D. I. Simon, and E. R. Edelman Increased Thrombosis After Arterial Injury in Human C-Reactive Protein-Transgenic Mice Circulation, August 5, 2003; 108(5): 512 - 515. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. E. Leidenfrost, M. F. Khan, K. P. Boc, B. R. Villa, E. T. Collins, W. C. Parks, D. R. Abendschein, and E. T. Choi A Model of Primary Atherosclerosis and Post-Angioplasty Restenosis in Mice Am. J. Pathol., August 1, 2003; 163(2): 773 - 778. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
H. Takeuchi, K. Ohmori, I. Kondo, A. Oshita, K. Shinomiya, Y. Yu, Y. Takagi, K. Mizushige, K. Kangawa, and M. Kohno Potentiation of C-type natriuretic peptide with ultrasound and microbubbles to prevent neointimal formation after vascular injury in rats Cardiovasc Res, April 1, 2003; 58(1): 231 - 238. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. Hutter, B. V. Sauter, E. D. Reis, M. Roque, D. Vorchheimer, F. E. Carrick, J. T. Fallon, V. Fuster, and J. J. Badimon Decreased Reendothelialization and Increased Neointima Formation With Endostatin Overexpression in a Mouse Model of Arterial Injury Circulation, April 1, 2003; 107(12): 1658 - 1663. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Fontana, C. Giagulli, L. Cominacini, A. F. Pasini, P. Minuz, A. Lechi, A. Sala, and C. Laudanna {beta}2 Integrin-Dependent Neutrophil Adhesion Induced by Minimally Modified Low-Density Lipoproteins Is Mainly Mediated by F2-Isoprostanes Circulation, November 5, 2002; 106(19): 2434 - 2441. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Roque, W. J.H. Kim, M. Gazdoin, A. Malik, E. D. Reis, J. T. Fallon, J. J. Badimon, I. F. Charo, and M. B. Taubman CCR2 Deficiency Decreases Intimal Hyperplasia After Arterial Injury Arterioscler Thromb Vasc Biol, April 1, 2002; 22(4): 554 - 559. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. X. Rong, J. Li, E. D. Reis, R. P. Choudhury, H. M. Dansky, V. I. Elmalem, J. T. Fallon, J. L. Breslow, and E. A. Fisher Elevating High-Density Lipoprotein Cholesterol in Apolipoprotein E-Deficient Mice Remodels Advanced Atherosclerotic Lesions by Decreasing Macrophage and Increasing Smooth Muscle Cell Content Circulation, November 13, 2001; 104(20): 2447 - 2452. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
S. S. Smyth, E. D. Reis, W. Zhang, J. T. Fallon, R. E. Gordon, and B. S. Coller {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, May 22, 2001; 103(20): 2501 - 2507. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. D. Rosen, S. Raymond, A. Zollman, F. Noria, M. Sandoval-Cooper, A. Shulman, J. L. Merz, and F. J. Castellino Laser-Induced Noninvasive Vascular Injury Models in Mice Generate Platelet- and Coagulation-Dependent Thrombi Am. J. Pathol., May 1, 2001; 158(5): 1613 - 1622. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
L. Fontana, C. Giagulli, P. Minuz, A. Lechi, and C. Laudanna 8-Iso-PGF2{{alpha}} Induces {beta}2-Integrin-Mediated Rapid Adhesion of Human Polymorphonuclear Neutrophils : A Link Between Oxidative Stress and Ischemia/Reperfusion Injury Arterioscler Thromb Vasc Biol, January 1, 2001; 21(1): 55 - 60. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
E. D. Reis, M. Roqué, H. Dansky, J. T. Fallon, J. J. Badimon, C. Cordon-Cardo, S. J. Shiff, and E. A. Fisher Sulindac inhibits neointimal formation after arterial injury in wild-type and apolipoprotein E-deficient mice PNAS, October 4, 2000; (2000) 210394497. [Abstract] [Full Text]
|
|
|
|
|
|
E. D. Reis, M. Roque, H. Dansky, J. T. Fallon, J. J. Badimon, C. Cordon-Cardo, S. J. Shiff, and E. A. Fisher Sulindac inhibits neointimal formation after arterial injury in wild-type and apolipoprotein E-deficient mice PNAS, November 7, 2000; 97(23): 12764 - 12769. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
M. Roque, W. J.H. Kim, M. Gazdoin, A. Malik, E. D. Reis, J. T. Fallon, J. J. Badimon, I. F. Charo, and M. B. Taubman CCR2 Deficiency Decreases Intimal Hyperplasia After Arterial Injury Arterioscler Thromb Vasc Biol, April 1, 2002; 22(4): 554 - 559. [Abstract] [Full Text] [PDF]
|
|