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From the Department of Pathology, A.Z. Middelheim, Antwerp (M.M.K.,
J.M.), and the Division of Pharmacology (UIA) (G.R.Y. De M., H.B., A.G.H.) and
the Centre for Electron Microscopy (W.J.), University of Antwerp, Wilrijk,
Belgium.
Correspondence to Dr M. Kockx, Department of Pathology, A.Z. Middelheim, Lindendreef, 1, B-2020 Antwerp, Belgium. E-mail mark.kockx{at}uia.ua.ac.be
Background—The transition of a fatty
streak into an atherosclerotic plaque is characterized by the
appearance of focal and diffuse regions of cell death. We have
investigated the distribution of apoptotic cell death and
apoptosis-related proteins in early and advanced
atherosclerotic lesions.
Methods and Results—Human atherosclerotic plaques were studied by
whole-mount carotid endarterectomy specimens
(n=18). This approach allowed comparison of adaptive intimal
thickenings, fatty streaks, and advanced atherosclerotic plaques of the
same patient. The fatty streaks differed from adaptive intimal
thickenings by the presence of BAX (P<0.01), a
proapoptotic protein of the BCL-2 family. Both regions were
composed mainly of smooth muscle cells (SMCs), and macrophage
infiltration was low and not different. Apoptosis, as detected
by DNA in situ end labeling (terminal
deoxynucleotidyl transferase end labeling [TUNEL]
and in situ nick translation) was not present in these regions.
Apoptosis of SMCs and macrophages, however, was
present in advanced atherosclerotic plaques that were present
mainly in the carotid sinus. A dense infiltration of
macrophages (5.8±3% surface area) was present in these
advanced atherosclerotic plaques. Cytoplasmic remnants of
apoptotic SMCs, enclosed by a cage of thickened basal lamina,
were TUNEL negative and remained present in the plaques as matrix
vesicles.
Conclusions—We conclude that SMCs within human fatty streaks
express BAX, which increases the susceptibility of these cells to
undergo apoptosis. The localization of these susceptible SMCs
in the deep layer of the fatty streaks could be important in our
understanding of the transition of fatty streaks into atherosclerotic
plaques, which are characterized by regions of cell death. Matrix
vesicles are BAX-immunoreactive cytoplasmic remnants of fragmented SMCs
that can calcify and may be considered the graves of SMCs that have
died in the plaques.
© 1998 American Heart Association, Inc.
Clinical Investigation and Reports
Apoptosis and Related Proteins in Different Stages of Human Atherosclerotic Plaques
Key Words: atherosclerosis • apoptosis • cholesterol • carotid arteries • muscle, smooth • cells
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W.-G. Li, F. J. Miller Jr, M. R. Brown, P. Chatterjee, G. R. Aylsworth, J. Shao, A. A. Spector, L. W. Oberley, and N. L. Weintraub Enhanced H2O2-Induced Cytotoxicity in "Epithelioid" Smooth Muscle Cells : Implications for Neointimal Regression Arterioscler Thromb Vasc Biol, June 1, 2000; 20(6): 1473 - 1479. [Abstract] [Full Text] [PDF]
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 J. Lemay, P. Hamet, and D. deBlois Losartan-induced apoptosis as a novel mechanism for the prevention of vascular lesion formation after injury Journal of Renin-Angiotensin-Aldosterone System, March 1, 2000; 1(1): 46 - 50. [Abstract] [PDF]
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 T. Stefanec Endothelial Apoptosis: Could It Have a Role in the Pathogenesis and Treatment of Disease? Chest, March 1, 2000; 117(3): 841 - 854. [Abstract] [Full Text] [PDF]
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H. Perlman, M. Sata, K. Krasinski, T. Dorai, R. Buttyan, and K. Walsh Adenovirus-encoded hammerhead ribozyme to Bcl-2 inhibits neointimal hyperplasia and induces vascular smooth muscle cell apoptosis Cardiovasc Res, February 1, 2000; 45(3): 570 - 578. [Abstract] [Full Text] [PDF]
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U. Weiland, J. Haendeler, C. Ihling, U. Albus, W. Scholz, H. Ruetten, A. M. Zeiher, and S. Dimmeler Inhibition of endogenous nitric oxide synthase potentiates ischemia-reperfusion-induced myocardial apoptosis via a caspase-3 dependent pathway Cardiovasc Res, February 1, 2000; 45(3): 671 - 678. [Abstract] [Full Text] [PDF]
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M. M Kockx and A. G Herman Apoptosis in atherosclerosis: beneficial or detrimental? Cardiovasc Res, February 1, 2000; 45(3): 736 - 746. [Abstract] [Full Text] [PDF]
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K. Walsh and J. M. Isner Apoptosis in inflammatory-fibroproliferative disorders of the vessel wall Cardiovasc Res, February 1, 2000; 45(3): 756 - 765. [Abstract] [Full Text] [PDF]
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P. Lehtolainen, M. Takeya, and S. Yla-Herttuala Retrovirus-Mediated, Stable Scavenger-Receptor Gene Transfer Leads to Functional Endocytotic Receptor Expression, Foam Cell Formation, and Increased Susceptibility to Apoptosis in Rabbit Aortic Smooth Muscle Cells Arterioscler Thromb Vasc Biol, January 1, 2000; 20(1): 52 - 60. [Abstract] [Full Text] [PDF]
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Y. Hayakawa, G. Takemura, J. Misao, M. Kanoh, M. Ohno, H. Ohashi, H. Takatsu, H. Ito, K. Fukuda, T. Fujiwara, et al. Apoptosis and Overexpression of Bax Protein and bax mRNA in Smooth Muscle Cells Within Intimal Hyperplasia of Human Radial Arteries : Analysis With Arteriovenous Fistulas Used for Hemodialysis Arterioscler Thromb Vasc Biol, September 1, 1999; 19(9): 2066 - 2077. [Abstract] [Full Text] [PDF]
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C Ihling, T Szombathy, K Nampoothiri, J Haendeler, F Beyersdorf, M Uhl, A M Zeiher, and H E Schaefer Cystic medial degeneration of the aorta is associated with p53 accumulation, Bax upregulation, apoptotic cell death, and cell proliferation Heart, September 1, 1999; 82(3): 286 - 293. [Abstract] [Full Text] [PDF]
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K. M Cromheeke, M. M Kockx, G. R.Y De Meyer, J. M Bosmans, H. Bult, W. J.F Beelaerts, C. J Vrints, and A. G Herman Inducible nitric oxide synthase colocalizes with signs of lipid oxidation/peroxidation in human atherosclerotic plaques Cardiovasc Res, August 15, 1999; 43(3): 744 - 754. [Abstract] [Full Text] [PDF]
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K. Kataoka, M. Taneda, T. Asai, A. Kinoshita, M. Ito, and R. Kuroda Structural Fragility and Inflammatory Response of Ruptured Cerebral Aneurysms : A Comparative Study Between Ruptured and Unruptured Cerebral Aneurysms Stroke, July 1, 1999; 30(7): 1396 - 1401. [Abstract] [Full Text] [PDF]
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G. Lizard, S. Monier, C. Cordelet, L. Gesquiere, V. Deckert, S. Gueldry, L. Lagrost, and P. Gambert Characterization and Comparison of the Mode of Cell Death, Apoptosis Versus Necrosis, Induced by 7ß-Hydroxycholesterol and 7-Ketocholesterol in the Cells of the Vascular Wall Arterioscler Thromb Vasc Biol, May 1, 1999; 19(5): 1190 - 1200. [Abstract] [Full Text] [PDF]
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D. E. Gutstein and V. Fuster Pathophysiology and clinical significance of atherosclerotic plaque rupture Cardiovasc Res, February 1, 1999; 41(2): 323 - 333. [Abstract] [Full Text] [PDF]
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E. Lutgens, E. D. de Muinck, P. J.E.H.M. Kitslaar, J. H.M. Tordoir, H. J.J. Wellens, and M. J.A.P. Daemen Biphasic pattern of cell turnover characterizes the progression from fatty streaks to ruptured human atherosclerotic plaques Cardiovasc Res, February 1, 1999; 41(2): 473 - 479. [Abstract] [Full Text] [PDF]
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G. Bauriedel, R. Hutter, U. Welsch, R. Bach, H. Sievert, and B. Luderitz Role of smooth muscle cell death in advanced coronary primary lesions: implications for plaque instability Cardiovasc Res, February 1, 1999; 41(2): 480 - 488. [Abstract] [Full Text] [PDF]
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 S. K. Sharma, D. Chapman, R. Temsah, T. Netticadan, D. P. Brasil, and N. S. Dhalla Prevention of Vascular Apoptosis in Myocardial Infarction by Losartan Journal of Cardiovascular Pharmacology and Therapeutics, January 1, 1999; 4(2): 77 - 84. [Abstract] [PDF]
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M. M. Kockx Apoptosis in the Atherosclerotic Plaque : Quantitative and Qualitative Aspects Arterioscler Thromb Vasc Biol, October 1, 1998; 18(10): 1519 - 1522. [Abstract] [Full Text] [PDF]
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M. M. Kavurma, F. S. Santiago, E. Bonfoco, and L. M. Khachigian Sp1 Phosphorylation Regulates Apoptosis via Extracellular FasL-Fas Engagement J. Biol. Chem., February 9, 2001; 276(7): 4964 - 4971. [Abstract] [Full Text] [PDF]
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