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Arteriosclerosis, Thrombosis, and Vascular Biology. 2001;21:1998-2003
doi: 10.1161/hq1201.100229
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(Arteriosclerosis, Thrombosis, and Vascular Biology. 2001;21:1998.)
© 2001 American Heart Association, Inc.


Atherosclerosis and Lipoproteins

Differential Expression of Bone Matrix Regulatory Proteins in Human Atherosclerotic Plaques

Cherida R. Dhore; Jack P.M. Cleutjens; Esther Lutgens; Kitty B.J.M. Cleutjens; Piet P.M. Geusens; Peter J.E.H.M. Kitslaar; Jan H.M. Tordoir; Henri M.H. Spronk; Cees Vermeer; Mat J.A.P. Daemen

From the Departments of Pathology (C.R.D., J.P.M.C., E.L., K.B.J.M.C., M.J.A.P.D.), Vascular Surgery (P.J.E.H.M.K., J.H.M.T.), and Biochemistry (H.M.H.S., C.V.), Cardiovascular Research Institute Maastricht, University of Maastricht, and Department of Rheumatology (P.P.M.G.), University Hospital Maastricht, Maastricht, Netherlands.

Correspondence to M.J.A.P. Daemen, MD, PhD, Department of Pathology, CARIM, University of Maastricht, PO Box 616, 6200 MD Maastricht, Netherlands. E-mail MDA{at}lpat.azm.nl

In the present study, we examined the expression of regulators of bone formation and osteoclastogenesis in human atherosclerosis because accumulating evidence suggests that atherosclerotic calcification shares features with bone calcification. The most striking finding of this study was the constitutive immunoreactivity of matrix Gla protein, osteocalcin, and bone sialoprotein in nondiseased aortas and the absence of bone morphogenetic protein (BMP)-2, BMP-4, osteopontin, and osteonectin in nondiseased aortas and early atherosclerotic lesions. When atherosclerotic plaques demonstrated calcification or bone formation, BMP-2, BMP-4, osteopontin, and osteonectin were upregulated. Interestingly, this upregulation was associated with a sustained immunoreactivity of matrix Gla protein, osteocalcin, and bone sialoprotein. The 2 modulators of osteoclastogenesis (osteoprotegerin [OPG] and its ligand, OPGL) were present in the nondiseased vessel wall and in early atherosclerotic lesions. In advanced calcified lesions, OPG was present in bone structures, whereas OPGL was only present in the extracellular matrix surrounding calcium deposits. The observed expression patterns suggest a tight regulation of the expression of bone matrix regulatory proteins during human atherogenesis. The expression pattern of both OPG and OPGL during atherogenesis might suggest a regulatory role of these proteins not only in osteoclastogenesis but also in atherosclerotic calcification.


Key Words: bone matrix proteins • atherosclerosis • vascular calcification • osteogenesis • osteoclastogenesis




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TNF-Related Activation-Induced Cytokine Enhances Leukocyte Adhesiveness: Induction of ICAM-1 and VCAM-1 via TNF Receptor-Associated Factor and Protein Kinase C-Dependent NF-{kappa}B Activation in Endothelial Cells
J. Immunol., July 1, 2005; 175(1): 531 - 540.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
M. Rattazzi, B. J. Bennett, F. Bea, E. A. Kirk, J. L. Ricks, M. Speer, S. M. Schwartz, C. M. Giachelli, and M. E. Rosenfeld
Calcification of Advanced Atherosclerotic Lesions in the Innominate Arteries of ApoE-Deficient Mice: Potential Role of Chondrocyte-Like Cells
Arterioscler Thromb Vasc Biol, July 1, 2005; 25(7): 1420 - 1425.
[Abstract] [Full Text] [PDF]


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CirculationHome page
A. Csiszar, K. E. Smith, A. Koller, G. Kaley, J. G. Edwards, and Z. Ungvari
Regulation of Bone Morphogenetic Protein-2 Expression in Endothelial Cells: Role of Nuclear Factor-{kappa}B Activation by Tumor Necrosis Factor-{alpha}, H2O2, and High Intravascular Pressure
Circulation, May 10, 2005; 111(18): 2364 - 2372.
[Abstract] [Full Text] [PDF]


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Cardiovasc ResHome page
M. Y. Speer, Y.-C. Chien, M. Quan, H.-Y. Yang, H. Vali, M. D. McKee, and C. M. Giachelli
Smooth muscle cells deficient in osteopontin have enhanced susceptibility to calcification in vitro
Cardiovasc Res, May 1, 2005; 66(2): 324 - 333.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
C. A. Simmons, G. R. Grant, E. Manduchi, and P. F. Davies
Spatial Heterogeneity of Endothelial Phenotypes Correlates With Side-Specific Vulnerability to Calcification in Normal Porcine Aortic Valves
Circ. Res., April 15, 2005; 96(7): 792 - 799.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
J. W. Fischer, S. A. Steitz, P. Y. Johnson, A. Burke, F. Kolodgie, R. Virmani, C. Giachelli, and T. N. Wight
Decorin Promotes Aortic Smooth Muscle Cell Calcification and Colocalizes to Calcified Regions in Human Atherosclerotic Lesions
Arterioscler Thromb Vasc Biol, December 1, 2004; 24(12): 2391 - 2396.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
P. Collin-Osdoby
Regulation of Vascular Calcification by Osteoclast Regulatory Factors RANKL and Osteoprotegerin
Circ. Res., November 26, 2004; 95(11): 1046 - 1057.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
T. Ueland, R. Jemtland, K. Godang, J. Kjekshus, A. Hognestad, T. Omland, I. B. Squire, L. Gullestad, J. Bollerslev, K. Dickstein, et al.
Prognostic value of osteoprotegerin in heart failure after acute myocardial infarction
J. Am. Coll. Cardiol., November 16, 2004; 44(10): 1970 - 1976.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
L. L. Demer and M. Abedin
Skeleton key to vascular disease
J. Am. Coll. Cardiol., November 16, 2004; 44(10): 1977 - 1979.
[Full Text] [PDF]


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BloodHome page
L. J. Schurgers, H. Aebert, C. Vermeer, B. Bultmann, and J. Janzen
Oral anticoagulant treatment: friend or foe in cardiovascular disease?
Blood, November 15, 2004; 104(10): 3231 - 3232.
[Abstract] [Full Text] [PDF]


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Circ. Res.Home page
S. M. Moe and N. X. Chen
Pathophysiology of Vascular Calcification in Chronic Kidney Disease
Circ. Res., September 17, 2004; 95(6): 560 - 567.
[Abstract] [Full Text] [PDF]


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Endocr. Rev.Home page
T. M. Doherty, L. A. Fitzpatrick, D. Inoue, J.-H. Qiao, M. C. Fishbein, R. C. Detrano, P. K. Shah, and T. B. Rajavashisth
Molecular, Endocrine, and Genetic Mechanisms of Arterial Calcification
Endocr. Rev., August 1, 2004; 25(4): 629 - 672.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
M. Soufi, M. Schoppet, A. M. Sattler, M. Herzum, B. Maisch, L. C. Hofbauer, and J. R. Schaefer
Osteoprotegerin Gene Polymorphisms in Men with Coronary Artery Disease
J. Clin. Endocrinol. Metab., August 1, 2004; 89(8): 3764 - 3768.
[Abstract] [Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
M. Schoppet, N. Al-Fakhri, F. E. Franke, N. Katz, P. J. Barth, B. Maisch, K. T. Preissner, and L. C. Hofbauer
Localization of Osteoprotegerin, Tumor Necrosis Factor-Related Apoptosis-Inducing Ligand, and Receptor Activator of Nuclear Factor-{kappa}B Ligand in Monckeberg's Sclerosis and Atherosclerosis
J. Clin. Endocrinol. Metab., August 1, 2004; 89(8): 4104 - 4112.
[Abstract] [Full Text] [PDF]


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Nephrol Dial TransplantHome page
K. Nitta, T. Akiba, K. Uchida, S. Otsubo, T. Takei, W. Yumura, T. Kabaya, and H. Nihei
Serum osteoprotegerin levels and the extent of vascular calcification in haemodialysis patients
Nephrol. Dial. Transplant., July 1, 2004; 19(7): 1886 - 1889.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
M. Abedin, Y. Tintut, and L. L. Demer
Vascular Calcification: Mechanisms and Clinical Ramifications
Arterioscler Thromb Vasc Biol, July 1, 2004; 24(7): 1161 - 1170.
[Abstract] [Full Text] [PDF]


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CirculationHome page
S. Kiechl, G. Schett, G. Wenning, K. Redlich, M. Oberhollenzer, A. Mayr, P. Santer, J. Smolen, W. Poewe, and J. Willeit
Osteoprotegerin Is a Risk Factor for Progressive Atherosclerosis and Cardiovascular Disease
Circulation, May 11, 2004; 109(18): 2175 - 2180.
[Abstract] [Full Text] [PDF]


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J Am Coll CardiolHome page
A. Mazzone, M. C. Epistolato, R. De Caterina, S. Storti, S. Vittorini, S. Sbrana, J. Gianetti, S. Bevilacqua, M. Glauber, A. Biagini, et al.
Neoangiogenesis, T-lymphocyte infiltration, and heat shock protein-60 are biological hallmarks of an immunomediated inflammatory process in end-stage calcified aortic valve stenosis
J. Am. Coll. Cardiol., May 5, 2004; 43(9): 1670 - 1676.
[Abstract] [Full Text] [PDF]


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Am. J. Physiol. Endocrinol. Metab.Home page
R. Vattikuti and D. A. Towler
Osteogenic regulation of vascular calcification: an early perspective
Am J Physiol Endocrinol Metab, May 1, 2004; 286(5): E686 - E696.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
D. J. Grainger
Transforming Growth Factor {beta} and Atherosclerosis: So Far, So Good for the Protective Cytokine Hypothesis
Arterioscler Thromb Vasc Biol, March 1, 2004; 24(3): 399 - 404.
[Abstract] [Full Text]


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Mayo Clin Proc.Home page
T. M. Doherty, L. A. Fitzpatrick, A. Shaheen, T. B. Rajavashisth, and R. C. Detrano
Genetic Determinants of Arterial Calcification Associated With Atherosclerosis
Mayo Clin. Proc., February 1, 2004; 79(2): 197 - 210.
[Abstract] [PDF]


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Proc. Natl. Acad. Sci. USAHome page
T. M. Doherty, K. Asotra, L. A. Fitzpatrick, J.-H. Qiao, D. J. Wilkin, R. C. Detrano, C. R. Dunstan, P. K. Shah, and T. B. Rajavashisth
Calcification in atherosclerosis: Bone biology and chronic inflammation at the arterial crossroads
PNAS, September 30, 2003; 100(20): 11201 - 11206.
[Abstract] [Full Text] [PDF]


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J. Biol. Chem.Home page
G. P. Sorescu, M. Sykes, D. Weiss, M. O. Platt, A. Saha, J. Hwang, N. Boyd, Y. C. Boo, J. D. Vega, W. R. Taylor, et al.
Bone Morphogenic Protein 4 Produced in Endothelial Cells by Oscillatory Shear Stress Stimulates an Inflammatory Response
J. Biol. Chem., August 15, 2003; 278(33): 31128 - 31135.
[Abstract] [Full Text] [PDF]


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CirculationHome page
M. Schoppet, J. R. Schaefer, L. C. Hofbauer, S. Jono, K. Mori, Y. Nishizawa, A. Shioi, T. Miki, Y. Ikari, and K. Hara
Low Serum Levels of Soluble RANK Ligand Are Associated With the Presence of Coronary Artery Disease in Men * Response
Circulation, March 25, 2003; 107 (11): e76 - e76.
[Full Text] [PDF]


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J. Clin. Endocrinol. Metab.Home page
M. Schoppet, A. M. Sattler, J. R. Schaefer, M. Herzum, B. Maisch, and L. C. Hofbauer
Increased Osteoprotegerin Serum Levels in Men with Coronary Artery Disease
J. Clin. Endocrinol. Metab., March 1, 2003; 88(3): 1024 - 1028.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
K. L. Tyson, J. L. Reynolds, R. McNair, Q. Zhang, P. L. Weissberg, and C. M. Shanahan
Osteo/Chondrocytic Transcription Factors and Their Target Genes Exhibit Distinct Patterns of Expression in Human Arterial Calcification
Arterioscler Thromb Vasc Biol, March 1, 2003; 23(3): 489 - 494.
[Abstract] [Full Text] [PDF]


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StrokeHome page
G. J. Adams, D. M. Simoni, C. B. Bordelon Jr, G. W. Vick III, K. T. Kimball, W. Insull Jr, and J. D. Morrisett
Bilateral Symmetry of Human Carotid Artery Atherosclerosis
Stroke, November 1, 2002; 33(11): 2575 - 2580.
[Abstract] [Full Text] [PDF]


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JEMHome page
M. Y. Speer, M. D. McKee, R. E. Guldberg, L. Liaw, H.-Y. Yang, E. Tung, G. Karsenty, and C. M. Giachelli
Inactivation of the Osteopontin Gene Enhances Vascular Calcification of Matrix Gla Protein-deficient Mice: Evidence for Osteopontin as an Inducible Inhibitor of Vascular Calcification In Vivo
J. Exp. Med., October 21, 2002; 196(8): 1047 - 1055.
[Abstract] [Full Text] [PDF]


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CirculationHome page
S. Jono, Y. Ikari, A. Shioi, K. Mori, T. Miki, K. Hara, and Y. Nishizawa
Serum Osteoprotegerin Levels Are Associated With the Presence and Severity of Coronary Artery Disease
Circulation, September 3, 2002; 106(10): 1192 - 1194.
[Abstract] [Full Text] [PDF]


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Arterioscler. Thromb. Vasc. Bio.Home page
M. Schoppet, K. T. Preissner, and L. C. Hofbauer
RANK Ligand and Osteoprotegerin: Paracrine Regulators of Bone Metabolism and Vascular Function
Arterioscler Thromb Vasc Biol, April 1, 2002; 22(4): 549 - 553.
[Abstract] [Full Text] [PDF]