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(Arteriosclerosis, Thrombosis, and Vascular Biology. 1995;15:551-561.)
© 1995 American Heart Association, Inc.

Articles

The Response-to-Retention Hypothesis of Early Atherogenesis

Kevin Jon Williams; Ira Tabas

From the Division of Endocrinology and Metabolic Diseases, Thomas Jefferson University, Philadelphia, Pa (K.J.W.), and the Departments of Medicine and Anatomy and Cell Biology, Columbia University, New York, NY (I.T.).

Correspondence to Kevin Jon Williams, MD, Division of Endocrinology and Metabolic Diseases, Thomas Jefferson University, Jefferson Alumni Hall, Suite 349, 1020 Locust St, Philadelphia, PA 19107-6799. E-mail k_williams@lac.jci.tju.edu.

	Introduction

 
Many processes have been implicated in early atherogenesis. These include endothelial denudation, injury, or activation, including shear stress–related events; local adherence of platelets; lipoprotein oxidation; lipoprotein aggregation; macrophage chemotaxis and foam cell formation; and smooth muscle cell alterations. Which process, if any, could be regarded as the key event in early atherogenesis, ie, absolutely required, yet also sufficient as the sole pathological stimulus in an otherwise normal artery to provoke a cascade of events leading to lesion formation? The work of many investigators, which we summarize here, strongly supports subendothelial retention of atherogenic lipoproteins as the central pathogenic process in atherogenesis (for prior reviews, see References 1 through 6^{1 2 3 4 5 6} ). Our thesis is that other contributory processes are either not individually necessary or are not sufficient. Most often, they are merely normal, expected responses of otherwise-healthy tissue to the presence of retained lipoproteins.

	Competing Hypotheses

 
It is instructive to catalog other processes that have been argued to be central to the initiation of atherogenesis. The first is endothelial denudation,^{7 8 9} injury,¹⁰ or activation,^{11 12} as outlined in the "response-to-injury" hypothesis of Ross, Glomset, and coworkers. Although this important hypothesis has stimulated much of the work that we cite here, there is no definitive evidence in vivo that endothelial injury is either necessary or sufficient for lesion formation.

The response-to-injury hypothesis originally presupposed endothelial desquamation as the key event in atherogenesis.^{7 8 9} It is now clear, however, that developing atheromata are covered by an intact endothelial layer throughout most stages of lesion progression: lipoprotein retention, fatty . . . [Full Text of this Article]

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				K. E. Lewis, E. A. Kirk, T. O. McDonald, S. Wang, T. N. Wight, K. D. O'Brien, and A. Chait Increase in Serum Amyloid A Evoked by Dietary Cholesterol Is Associated With Increased Atherosclerosis in Mice Circulation, August 3, 2004; 110(5): 540 - 545. [Abstract] [Full Text] [PDF]

				T. N. Wight and M. J. Merrilees Proteoglycans in Atherosclerosis and Restenosis: Key Roles for Versican Circ. Res., May 14, 2004; 94(9): 1158 - 1167. [Abstract] [Full Text] [PDF]

				A. E. Cozen, H. Moriwaki, M. Kremen, M. B. DeYoung, H. L. Dichek, K. I. Slezicki, S. G. Young, M. Veniant, and D. A. Dichek Macrophage-Targeted Overexpression of Urokinase Causes Accelerated Atherosclerosis, Coronary Artery Occlusions, and Premature Death Circulation, May 4, 2004; 109(17): 2129 - 2135. [Abstract] [Full Text] [PDF]

				C. Flood, M. Gustafsson, R. E. Pitas, L. Arnaboldi, R. L. Walzem, and J. Boren Molecular Mechanism for Changes in Proteoglycan Binding on Compositional Changes of the Core and the Surface of Low-Density Lipoprotein-Containing Human Apolipoprotein B100 Arterioscler Thromb Vasc Biol, March 1, 2004; 24(3): 564 - 570. [Abstract] [Full Text]

				E. F LaBelle and T. N Tulenko LDL, IGF-1, and VSMC apoptosis: linking atherogenesis to plaque rupture in vulnerable lesions Cardiovasc Res, February 1, 2004; 61(2): 204 - 205. [Full Text] [PDF]

				M. Formato, M. Farina, R. Spirito, M. Maggioni, A. Guarino, G. M. Cherchi, P. Biglioli, C. Edelstein, and A. M. Scanu Evidence for a Proinflammatory and Proteolytic Environment in Plaques From Endarterectomy Segments of Human Carotid Arteries Arterioscler Thromb Vasc Biol, January 1, 2004; 24(1): 129 - 135. [Abstract] [Full Text] [PDF]

				X.-C. Jiang, T. P. Beyer, Z. Li, J. Liu, W. Quan, R. J. Schmidt, Y. Zhang, W. R. Bensch, P. I. Eacho, and G. Cao Enlargement of High Density Lipoprotein in Mice via Liver X Receptor Activation Requires Apolipoprotein E and Is Abolished by Cholesteryl Ester Transfer Protein Expression J. Biol. Chem., December 5, 2003; 278(49): 49072 - 49078. [Abstract] [Full Text] [PDF]

				F. E. Thorngate, P. G. Yancey, G. Kellner-Weibel, L. L. Rudel, G. H. Rothblat, and D. L. Williams Testing the role of apoA-I, HDL, and cholesterol efflux in the atheroprotective action of low-level apoE expression J. Lipid Res., December 1, 2003; 44(12): 2331 - 2338. [Abstract] [Full Text] [PDF]

				M. Patel, J. Morrow, F. R. Maxfield, D. K. Strickland, S. Greenberg, and I. Tabas The Cytoplasmic Domain of the Low Density Lipoprotein (LDL) Receptor-related Protein, but Not That of the LDL Receptor, Triggers Phagocytosis J. Biol. Chem., November 7, 2003; 278(45): 44799 - 44807. [Abstract] [Full Text] [PDF]

				C. D. Meyers, L. R. Tannock, T. N. Wight, and A. Chait Statin-exposed vascular smooth muscle cells secrete proteoglycans with decreased binding affinity for LDL J. Lipid Res., November 1, 2003; 44(11): 2152 - 2160. [Abstract] [Full Text] [PDF]

				W. Cao, Y. V Bobryshev, R. S.A Lord, R. E.I Oakley, S. H Lee, and J. Lu Dendritic cells in the arterial wall express C1q: potential significance in atherogenesis Cardiovasc Res, October 15, 2003; 60(1): 175 - 186. [Abstract] [Full Text] [PDF]

				B. OSTERUD and E. BJORKLID Role of Monocytes in Atherogenesis Physiol Rev, October 1, 2003; 83(4): 1069 - 1112. [Abstract] [Full Text] [PDF]

				G McGwin Jr, C Owsley, C A Curcio, and R J Crain The association between statin use and age related maculopathy Br J Ophthalmol, September 1, 2003; 87(9): 1121 - 1125. [Abstract] [Full Text] [PDF]

				G. Camejo Hydrolytic Enzymes Released From Resident Macrophages and Located in the Intima Extracellular Matrix as Agents That Modify Retained Apolipoprotein B Lipoproteins Arterioscler Thromb Vasc Biol, August 1, 2003; 23(8): 1312 - 1313. [Full Text] [PDF]

				T. B. Twickler, M. J. M. Cramer, G. M. Dallinga-Thie, M. J. Chapman, D. W. Erkelens, and H. P. F. Koppeschaar Adult-Onset Growth Hormone Deficiency: Relation of Postprandial Dyslipidemia to Premature Atherosclerosis J. Clin. Endocrinol. Metab., June 1, 2003; 88(6): 2479 - 2488. [Full Text] [PDF]

				M. Y. Chang, C. Tsoi, T. N. Wight, and A. Chait Lysophosphatidylcholine Regulates Synthesis of Biglycan and the Proteoglycan Form of Macrophage Colony Stimulating Factor Arterioscler Thromb Vasc Biol, May 1, 2003; 23(5): 809 - 815. [Abstract] [Full Text] [PDF]

				Z. Chen, R. L. Fitzgerald, J. E. Saffitz, C. F. Semenkovich, and G. Schonfeld Amino Terminal 38.9% of Apolipoprotein B-100 Is Sufficient to Support Cholesterol-Rich Lipoprotein Production and Atherosclerosis Arterioscler Thromb Vasc Biol, April 1, 2003; 23(4): 668 - 674. [Abstract] [Full Text] [PDF]

				T. Nassar, B. S. Sachais, S.'e. Akkawi, M. A. Kowalska, K. Bdeir, E. Leitersdorf, E. Hiss, L. Ziporen, M. Aviram, D. Cines, et al. Platelet Factor 4 Enhances the Binding of Oxidized Low-density Lipoprotein to Vascular Wall Cells J. Biol. Chem., February 14, 2003; 278(8): 6187 - 6193. [Abstract] [Full Text] [PDF]

				G. Malek, C.-M. Li, C. Guidry, N. E. Medeiros, and C. A. Curcio Apolipoprotein B in Cholesterol-Containing Drusen and Basal Deposits of Human Eyes with Age-Related Maculopathy Am. J. Pathol., February 1, 2003; 162(2): 413 - 425. [Abstract] [Full Text] [PDF]

				K. Olin-Lewis, R. M. Krauss, M. La Belle, P. J. Blanche, P. H. R. Barrett, T. N. Wight, and A. Chait ApoC-III content of apoB-containing lipoproteins is associated with binding to the vascular proteoglycan biglycan J. Lipid Res., November 1, 2002; 43(11): 1969 - 1977. [Abstract] [Full Text] [PDF]

				A. Zalewski, Y. Shi, and A. G. Johnson Diverse Origin of Intimal Cells: Smooth Muscle Cells, Myofibroblasts, Fibroblasts, and Beyond? Circ. Res., October 18, 2002; 91(8): 652 - 655. [Full Text] [PDF]