Upregulation of VCAM-1 and ICAM-1 at Atherosclerosis-Prone Sites on the Endothelium in the ApoE-Deficient Mouse

From the Department of Pathology, University of Washington, Seattle (Y.N., E.W.R., R.R.); and the Laboratory of Biochemical Genetics and Metabolism, The Rockefeller University, New York, NY (A.S.P., J.L.B.).

Correspondence to Russell Ross, PhD, Department of Pathology, University of Washington School of Medicine, 1959 NE Pacific St, Box 357470, Seattle WA 98195-7470. E-mail rross{at}u.washington.edu

Abstract—Focal recruitment of monocytes and lymphocytes is one of the earliest detectable cellular responses in the formation of lesions of atherosclerosis. This localized accumulation of leukocytes is a multistep process in which the endothelium remains intact and may regulate leukocyte recruitment by expressing specific adhesion molecules. To examine the relationship of adhesion molecule expression to initiation factors and the sites of lesion formation, we analyzed the expression of vascular cell adhesion molecule-1 (VCAM-1), intercellular adhesion molecule-1 (ICAM-1), and platelet–endothelial cell adhesion molecule-1 (PECAM-1) en face on the aortic endothelium of control mice and homozygous apolipoprotein E–deficient (ApoE -/-) mice that develop complex lesions of atherosclerosis similar to those in humans. In control mice, VCAM-1 staining was weak and limited to sites of altered blood flow. In contrast, in the ApoE -/- mice, VCAM-1 appeared to be localized over the surface of groups of endothelial cells in lesion-prone sites. Expression of VCAM-1 preceded lesion formation, and increased expression above control levels appeared to be correlated with the extent of exposure to plasma cholesterol. Although ICAM-1 was the most prominent adhesion molecule in lesion-prone sites, its expression appeared to be independent of plasma cholesterol levels and was upregulated in both ApoE -/- and control mice. At lesion-prone sites associated with altered blood flow, ICAM-1 was located over the surface of each endothelial cell and on microvilli, whereas VCAM-1 was confined to the cell periphery in non–lesion-prone sites. PECAM-1 was localized at the cell periphery throughout the aorta, and its expression did not appear to be regulated. Thus, the levels, localization, and characteristics of expression of VCAM-1, ICAM-1, and PECAM-1 appear to be differentially regulated. Upregulation of VCAM-1 and ICAM-1 is associated with sites of lesion formation.

Key Words: transgenic mouse • monocytes • PECAM-1 • adhesion • microvilli

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				M. E. Rosenfeld Leukocyte Recruitment Into Developing Atherosclerotic Lesions: The Complex Interaction Between Multiple Molecules Keeps Getting More Complex Arterioscler Thromb Vasc Biol, March 1, 2002; 22(3): 361 - 363. [Full Text] [PDF]

				R. J. Aiello, P.-A. Bourassa, S. Lindsey, W. Weng, A. Freeman, and H. J. Showell Leukotriene B4 Receptor Antagonism Reduces Monocytic Foam Cells in Mice Arterioscler Thromb Vasc Biol, March 1, 2002; 22(3): 443 - 449. [Abstract] [Full Text] [PDF]

				T. Minami and W. C. Aird Thrombin Stimulation of the Vascular Cell Adhesion Molecule-1 Promoter in Endothelial Cells Is Mediated by Tandem Nuclear Factor-kappa B and GATA Motifs J. Biol. Chem., December 7, 2001; 276(50): 47632 - 47641. [Abstract] [Full Text] [PDF]

				G. K. Hansson Immune Mechanisms in Atherosclerosis Arterioscler Thromb Vasc Biol, December 1, 2001; 21(12): 1876 - 1890. [Abstract] [Full Text] [PDF]

				A. K. Stannard, D. R. Riddell, S. M. Sacre, A. D. Tagalakis, C. Langer, A. von Eckardstein, P. Cullen, T. Athanasopoulos, G. Dickson, and J. S. Owen Cell-derived Apolipoprotein E (ApoE) Particles Inhibit Vascular Cell Adhesion Molecule-1 (VCAM-1) Expression in Human Endothelial Cells J. Biol. Chem., November 30, 2001; 276(49): 46011 - 46016. [Abstract] [Full Text] [PDF]

				W.-J. ZHANG and B. FREI {alpha}-Lipoic acid inhibits TNF-{alpha}-induced NF-{kappa}B activation and adhesion molecule expression in human aortic endothelial cells FASEB J, November 1, 2001; 15(13): 2423 - 2432. [Abstract] [Full Text] [PDF]

				C. G. Kevil, R. P. Patel, and D. C. Bullard Essential role of ICAM-1 in mediating monocyte adhesion to aortic endothelial cells Am J Physiol Cell Physiol, November 1, 2001; 281(5): C1442 - C1447. [Abstract] [Full Text] [PDF]

				H. M. Dansky, C. B. Barlow, C. Lominska, J. L. Sikes, C. Kao, J. Weinsaft, M. I. Cybulsky, and J. D. Smith Adhesion of Monocytes to Arterial Endothelium and Initiation of Atherosclerosis Are Critically Dependent on Vascular Cell Adhesion Molecule-1 Gene Dosage Arterioscler Thromb Vasc Biol, October 1, 2001; 21(10): 1662 - 1667. [Abstract] [Full Text] [PDF]

				D. M. Wuttge, P. Eriksson, A. Sirsjo, G. K. Hansson, and S. Stemme Expression of Interleukin-15 in Mouse and Human Atherosclerotic Lesions Am. J. Pathol., August 1, 2001; 159(2): 417 - 423. [Abstract] [Full Text]

				M. Yoshida, T. Sawada, H. Ishii, R. E. Gerszten, A. Rosenzweig, M. A. Gimbrone Jr, Y. Yasukochi, and F. Numano HMG-CoA Reductase Inhibitor Modulates Monocyte-Endothelial Cell Interaction Under Physiological Flow Conditions In Vitro : Involvement of Rho GTPase-Dependent Mechanism Arterioscler Thromb Vasc Biol, July 1, 2001; 21(7): 1165 - 1171. [Abstract] [Full Text] [PDF]

				M. Umetani, C. Mataki, N. Minegishi, M. Yamamoto, T. Hamakubo, and T. Kodama Function of GATA Transcription Factors in Induction of Endothelial Vascular Cell Adhesion Molecule-1 by Tumor Necrosis Factor-{{alpha}} Arterioscler Thromb Vasc Biol, June 1, 2001; 21(6): 917 - 922. [Abstract] [Full Text] [PDF]

				J. A. McPherson, K. G. Barringhaus, G. G. Bishop, J. M. Sanders, J. M. Rieger, S. E. Hesselbacher, L. W. Gimple, E. R. Powers, T. Macdonald, G. Sullivan, et al. Adenosine A2A Receptor Stimulation Reduces Inflammation and Neointimal Growth in a Murine Carotid Ligation Model Arterioscler Thromb Vasc Biol, May 1, 2001; 21(5): 791 - 796. [Abstract] [Full Text] [PDF]

				E. E. ERIKSSON, X. XIE, J. WERR, P. THOREN, and L. LINDBOM Direct viewing of atherosclerosis in vivo: plaque invasion by leukocytes is initiated by the endothelial selectins FASEB J, May 1, 2001; 15(7): 1149 - 1157. [Abstract] [Full Text] [PDF]

				N. Rifai and P. M. Ridker High-Sensitivity C-Reactive Protein: A Novel and Promising Marker of Coronary Heart Disease Clin. Chem., March 1, 2001; 47(3): 403 - 411. [Abstract] [Full Text] [PDF]

				D. Manka, R. G. Collins, K. Ley, A. L. Beaudet, and I. J. Sarembock Absence of P-Selectin, but Not Intercellular Adhesion Molecule-1, Attenuates Neointimal Growth After Arterial Injury in Apolipoprotein E-Deficient Mice Circulation, February 20, 2001; 103(7): 1000 - 1005. [Abstract] [Full Text] [PDF]

				G. W. Cockerill, T. Y. Huehns, A. Weerasinghe, C. Stocker, P. G. Lerch, N. E. Miller, and D. O. Haskard Elevation of Plasma High-Density Lipoprotein Concentration Reduces Interleukin-1-Induced Expression of E-Selectin in an In Vivo Model of Acute Inflammation Circulation, January 2, 2001; 103(1): 108 - 112. [Abstract] [Full Text] [PDF]

				M.-C. Bourdillon, R. N. Poston, C. Covacho, E. Chignier, G. Bricca, and J. L. McGregor ICAM-1 Deficiency Reduces Atherosclerotic Lesions in Double-Knockout Mice (ApoE-/-/ICAM-1-/-) Fed a Fat or a Chow Diet Arterioscler Thromb Vasc Biol, December 1, 2000; 20(12): 2630 - 2635. [Abstract] [Full Text] [PDF]

				K. Zibara, E. Chignier, C. Covacho, R. Poston, G. Canard, P. Hardy, and J. McGregor Modulation of Expression of Endothelial Intercellular Adhesion Molecule-1, Platelet-Endothelial Cell Adhesion Molecule-1, and Vascular Cell Adhesion Molecule-1 in Aortic Arch Lesions of Apolipoprotein E-Deficient Compared With Wild-Type Mice Arterioscler Thromb Vasc Biol, October 1, 2000; 20(10): 2288 - 2296. [Abstract] [Full Text] [PDF]

				J. A. de Lemos, C. H. Hennekens, and P. M. Ridker Plasma concentration of soluble vascular cell adhesion molecule-1 and subsequent cardiovascular risk J. Am. Coll. Cardiol., August 1, 2000; 36(2): 423 - 426. [Abstract] [Full Text] [PDF]

				F. E. Thorngate, L. L. Rudel, R. L. Walzem, and D. L. Williams Low Levels of Extrahepatic Nonmacrophage ApoE Inhibit Atherosclerosis Without Correcting Hypercholesterolemia in ApoE-Deficient Mice Arterioscler Thromb Vasc Biol, August 1, 2000; 20(8): 1939 - 1945. [Abstract] [Full Text] [PDF]