Mechanisms of arterial remodeling: Lessons from genetic diseases

Frontiers in Genetics

Volumn 3, Issue DEC, 2012, Pages

  Van Varik, Bernard J ^a   Rennenberg, Roger J M W ^a   Reutelingsperger, Chris P ^b   Kroon, Abraham A ^a   De Leeuw, Peter W ^a   Schurgers, Leon J ^a,b  

^a MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

Arterial remodeling; Calcification; Genetic disease; Vitamin K; Vitamin K antagonists

Indexed keywords

EID: 84876076876     PISSN: None     EISSN: 16648021     Source Type: Journal    
DOI: 10.3389/fgene.2012.00290     Document Type: Review

References (111)

1. Alexander, M. R., and Owens, G. K. (2012). Epigenetic control of smooth muscle cell differentiation and phenotypic switching in vascular development and disease. Annu. Rev. Physiol. 74, 13-40.
2. Avolio, A., Jones, D., and Tafazzoli-Shadpour, M. (1998). Quantification of alterations in structure and function of elastin in the arterial media. Hypertension 32, 170-175.
3. Bendeck, M. P., Irvin, C., and Reidy, M. A. (1996). Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. Circ. Res. 78, 38-43.
4. Bennett, M. R., Evan, G. I., and Schwartz, S. M. (1995). Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J. Clin. Invest. 95, 2266-2274.
5. Bidani, A. K., and Griffin, K. A. (2004). Pathophysiology of hypertensive renal damage: implications for therapy. Hypertension 44, 595-601.
6. Bidani, A. K., Griffin, K. A., Williamson, G., Wang, X., and Loutzenhiser, R. (2009). Protective importance of the myogenic response in the renal circulation. Hypertension 54, 393-398.
7. Blackman, B. R., García-Cardeña, G., and Gimbrone, M. A. (2002). A new in vitro model to evaluate differential responses of endothelial cells to simulated arterial shear stress waveforms. J. Biomech. Eng. 124, 397-407.
8. Blaha, M. J., Budoff, M. J., Rivera, J. J., Katz, R., O'Leary, D. H., Polak, J. F., et al. (2009). Relationship of carotid distensibility and thoracic aorta calcification: multi-ethnic study of atherosclerosis. Hypertension 54, 1408-1415.
9. Boraldi, F., Annovi, G., Guerra, D., Paolinelli Devincenzi, C., Garcia-Fernandez, M. I., Panico, F., et al. (2009). Fibroblast protein profile analysis highlights the role of oxida-tive stress and vitamin K recycling in the pathogenesis of pseudoxan-thoma elasticum. Proteomics Clin. Appl. 3, 1084-1098.
10. Boström, K. I., Jumabay, M., Matveyenko, A., Nicholas, S. B., and Yao, Y. (2011). Activation of vascular bone morphogenetic protein signaling in diabetes mellitus. Circ. Res. 108, 446-457.
11. Boström, K., Watson, K. E., Horn, S., Wortham, C., Herman, I. M., and Demer, L. L. (1993). Bone morphogenetic protein expression in human atherosclerotic lesions. J. Clin. Invest. 91, 1800-1809.
12. Boutouyrie, P., Lacolley, P., Briet, M., Regnault, V., Stanton, A., Laurent, S., et al. (2011). Pharmacological modulation of arterial stiffness. Drugs 71, 1689-1701.
13. Braam, L. A., Knapen, M. H., Geusens, P., Brouns, F., Hamulyak, K., Gerichhausen, M. J., et al. (2003). Vitamin K1 supplementation retards bone loss in postmenopausal women between 50 and 60 years of age. Calcif. Tissue Int. 73, 21-26.
14. Briet, M., Collin, C., Karras, A., Laurent, S., Bozec, E., Jacquot, C., et al. (2011). Arterial remodeling associates with CKD progression. J. Am. Soc. Nephrol. 22, 967-974.
15. Budoff, M. J., Achenbach, S., Blumenthal, R. S., Carr, J. J., Goldin, J. G., Greenland, P., et al. (2006). Assessment of coronary artery disease by cardiac computed tomography: a scientific statement from the American Heart Association Committee on Cardiovascular Imaging and Intervention, Council on Cardiovascular Radiology and Intervention, and Committee on Cardiac Imaging, Council on Clinical Cardiology. Circulation 114, 1761-1791.
16. Bunton, T. E., Biery, N. J., Myers, L., Gayraud, B., Ramirez, F., and Dietz, H. C. (2001). Phenotypic alteration of vascular smooth muscle cells precedes elastolysis in a mouse model of Marfan syndrome. Circ. Res. 88, 37-43.
17. Cecelja, M., Jiang, B., Bevan, L., Frost, M. L., Spector, T. D., and Chowienczyk, P. J. (2011). Arterial stiffening relates to arterial calcification but not to noncalcified atheroma in women. A twin study. J. Am. Coll. Cardiol. 57, 1480-1486.
18. Ceravolo, R., Maio, R., Pujia, A., Sciacqua, A., Ventura, G., Costa, M. C., et al. (2003). Pulse pressure and endothelial dysfunction in never-treated hypertensive patients. J. Am. Coll. Cardiol. 41, 1753-1758.
19. Chatrou, M. L., Winckers, K., Hackeng, T. M., Reutelingsperger, C. P., and Schurgers, L. J. (2012). Vascular calcification: the price to pay for anticoagulation therapy with vitamin K-antagonists. Blood Rev. 26, 155-166.
20. Chen, S., Chang, J., Liu, W., Tsai, Y., Tsai, J., Hsu, P., et al. (2011). Brachial-ankle pulse wave velocity and rate of renal function decline and mortality in chronic kidney disease. Clin. J. Am. Soc. Nephrol. 6, 724-732.
21. Csiszar, A., Lehoux, S., and Ungvari, Z. (2009). Hemodynamic forces, vascular oxidative stress, and regulation of BMP-2/4 expression. Antioxid. Redox Signal. 11, 1683-1697.
22. Dingemans, K. P., Teeling, P., Lagendijk, J. H., and Becker, A. E. (2000). Extracellular matrix of the human aortic media: an ultrastructural his-tochemical and immunohistochem-ical study of the adult aortic media. Anat. Rec. 258, 1-14.
23. Domanski, M. J., Davis, B. R., Pfeffer, M. A., Kastantin, M., and Mitchell, G. F. (1999). Isolated systolic hypertension: prognostic information provided by pulse pressure. Hypertension 34, 375-380.
24. Eys, G. J., Niessen, P. M., and Rensen, S. S. (2007). Smoothelin in vascular smooth muscle cells. Tr e n d s Cardiovasc. Med. 17, 26-30.
25. Farand, P., Garon, A., and Plante, G. E. (2007). Structure of large arteries: orientation of elastin in rabbit aortic internal elastic lamina and in the elastic lamellae of aortic media. Microvasc. Res. 73, 95-99.
26. Fleckenstein-Grün, G., Frey, M., Thimm, F., Hofgärtner, W., and Fleckenstein, A. (1992). Calcium overload-an important cellular mechanism in hypertension and arteriosclerosis. Drugs 44(Suppl. 1), 23-30.
27. Ford, M. L., Tomlinson, L. A., Chapman, T. P., Rajkumar, C., and Holt, S. G. (2010). Aortic stiffness is independently associated with rate of renal function decline in chronic kidney disease stages 3 and 4. Hypertension 55, 1110-1115.
28. Galis, Z. S., and Khatri, J. J. (2002). Matrix metalloproteinases in vascular remodeling and atherogenesis: the good, the bad, and the ugly. Circ. Res. 90, 251-262.
29. Galis, Z. S., Sukhova, G. K., Lark, M. W., and Libby, P. (1994). Increased expression of matrix metallopro-teinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J. Clin. Invest. 94, 2493-2503.
30. Garcia-Fernandez, M. I., Gheduzzi, D., Boraldi, F., Paolinelli, C. D., Sanchez, P., Valdivielso, P., et al. (2008). Parameters of oxidative stress are present in the circulation of PXE patients. Biochim. Biophys. Acta 1782, 474-481.
31. Gast, G. C., Roos, N. M., Sluijs, I., Bots, M. L., Beulens, J. W., Geleijnse, J. M., et al. (2009). A high menaquinone intake reduces the incidence of coronary heart disease. Nutr. Metab. Cardiovasc. Dis. 19, 504-510.
32. Geleijnse, J. M., Vermeer, C., Grobbee, D E., Schurgers, L. J., Knapen, M. H., Meer, I. M., et al. (2004). Dietary intake of menaquinone is associ ated with a reduced risk of coronary heart disease: the Rotterdam Study. J. Nutr. 134, 3100-3105.
33. Gerthoffer, W. T. (2007). Mechanisms of vascular smooth muscle cell migration. Circ. Res. 100, 607-621.
34. Gheduzzi, D., Boraldi, F., Annovi, G., Devincenzi, C. P., Schurgers, L. J., Vermeer, C., et al. (2007). Matrix Gla protein is involved in elastic fiber calcification in the der-mis of pseudoxanthoma elasticum patients. Lab. Invest. 87, 998-1008.
35. Gimbrone, M. A., and García-Cardeña, G. (2012). Vascular endothelium, hemodynamics, and the pathobiol-ogy of atherosclerosis. Cardiovasc. Pathol. pii: S1054-8807(12)00076-2. doi: 10.1016/j.carpath.2012.06.006
36. Goodall, S., Porter, K. E., Bell, P. R., and Thompson, M. M. (2002). Enhanced invasive properties exhibited by smooth muscle cells are associated with elevated production of MMP-2 in patients with aortic aneurysms. Eur. J. Vasc. Endovasc. Surg. 24, 72-80.
37. Greenwald, S. E. (2007). Ageing of the conduit arteries. J. Pathol. 211, 157-172.
38. Hsu, H. H., and Camacho, N. P. (1999). Isolation of calcifiable vesicles from human atherosclerotic aortas. Atherosclerosis 143, 353-362.
39. Hultström, M. (2012). Development of structural kidney damage in spontaneously hypertensive rats. J. Hypertens. 30, 1087-1091.
40. Iyemere, V. P., Proudfoot, D., Weissberg, P. L., and Shanahan, C. M. (2006). Vascular smooth muscle cell phenotypic plasticity and the regulation of vascular calcification. J. Intern. Med. 260, 192-210.
41. Jang, S., Yong, H. S., Doo, K. W., Kang, E., Woo, O. H., and Choi, E. J. (2012). Relation of aortic cal cification, wall thickness, and dis-tensibility with severity of coronary artery disease: evaluation with coro nary CT angiography. Acta Radiol. 53, 839-844.
42. Johnson, J. L. (2007). Matrix met-alloproteinases: influence on smooth muscle cells and atherosclerotic plaque stability. Expert Rev. Cardiovasc. Ther. 5, 265-282.
43. Kass, D. A., Shapiro, E. P., Kawaguchi, M., Capriotti, A. R., Scuteri, A., Degroof, R. C., et al. (2001). Improved arterial compliance by a novel advanced glycation end-product crosslink breaker. Circulation 104, 1464-1470.
44. Keulenaer, G. W., Chappell, D. C., Ishizaka, N., Nerem, R. M., Alexander, R. W., and Griendling, K. K. (1998). Oscillatory and steady laminar shear stress differentially affect human endothelial redox state: role of a superoxide-producing NADH oxidase. Circ. Res. 82, 1094-1101.
45. Kielty, C. M. (2006). Elastic fibres in health and disease. Expert Rev. Mol. Med. 8, 1-23.
46. Kim, K. M. (1976). Calcification of matrix vesicles in human aortic valve and aortic media. Fed. Proc. 35, 156-162.
47. Kockx, M. M., De Meyer, G. R., Muhring, J., Jacob, W., Bult, H., and Herman, A. G. (1998). Apoptosis and related proteins in different stages of human atherosclerotic plaques. Circulation 97, 2307-2315.
48. Laurent, S., Alivon, M., Beaussier, H., and Boutouyrie, P. (2012). Aortic stiffness as a tissue biomarker for predicting future cardiovascular events in asymptomatic hypertensive subjects. Ann. Med. 44(Suppl. 1), S93-S97.
49. Laurent, S., and Boutouyrie, P. (2005). Arterial stiffness and stroke in hypertension: therapeutic implications for stroke prevention. CNS Drugs 19, 1-11.
50. Laurent, S., Boutouyrie, P., Asmar, R., Gautier, I., Laloux, B., Guize, L., et al. (2001). Aortic stiffness is an independent predictor of all-cause and cardiovascular mortality in hypertensive patients. Hypertension 37, 1236-1241.
51. Li, Q., Grange, D. K., Armstrong, N. L., Whelan, A. J., Hurley, M. Y., Rishavy, M. A., et al. (2009a). Mutations in the GGCX and ABCC6 genes in a family with pseudoxan-thoma elasticum-like phenotypes. J. Invest. Dermatol. 129, 553-563.
52. Li, Q., Jiang, Q., Pfendner, E., Váradi, A., and Uitto, J. (2009b). Pseudoxanthoma elasticum: clinical phenotypes, molecular genetics and putative pathomechanisms. Exp. Dermatol. 18, 1-11.
53. Libby, P. (2002). Inflammation in atherosclerosis. Nature 420, 868-874.
54. Luo, G., Ducy, P., McKee, M. D., Pinero, G. J., Loyer, E., Behringer, R. R., et al. (1997). Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386, 78-81.
55. Mitchell, G. F. (2004). Increased aortic stiffness: an unfavorable cardiorenal connection. Hypertension 43, 151-153.
56. Mitchell, G. F. (2009). Arterial stiffness and wave reflection: biomarkers of cardiovascular risk. Artery Res. 3, 56-64.
57. Mitchell, G. F., Hwang, S., Vasan, R. S., Larson, M. G., Pencina, M. J., Hamburg, N. M., et al. (2010). Arterial stiffness and cardiovascular events: the Framingham Heart Study. Circulation 121, 505-511.
58. Mulvany, M. J. (2008). Small artery remodelling in hypertension: causes, consequences and therapeutic implications. Med. Biol. Eng. Comput. 46, 461-467.
59. Mulvany, M. J., Baumbach, G. L., Aalkjaer, C., Heagerty, A. M., Korsgaard, N., Schiffrin, E. L., et al. (1996). Vascular remodeling. Hypertension 28, 505-506.
60. Munroe, P. B., Olgunturk, R. O., Fryns, J. P., Maldergem, L., Ziereisen, F., Yuksel, B., et al. (1999). Mutations in the gene encoding the human matrix Gla protein cause Keutel syndrome. Nat. Genet. 21, 142-144.
61. Nakagawa, Y., Ikeda, K., Akakabe, Y., Koide, M., Uraoka, M., Yutaka, K., et al. (2010). Paracrine osteogenic signals via bone morphogenetic protein-2 accelerate the atherosclerotic intimal calcification in vivo. Arterioscler. Thromb. Vasc. Biol. 30, 1908-1915.
62. Nichols, W., and O'Rourke, M. (2005). Mc Donald's Blood Flow in Arteries. London: Hodder Arnold.
63. Nurnberger, J., Keflioglu-Scheiber, A., Opazo Saez, A. M., Wenzel, R. R., Philipp, T., and Schafers, R. F. (2002). Augmentation index is associated with cardiovascular risk. J. Hypertens. 20, 2407-2414.
64. O'Rourke, M. F. (1976). Pulsatile arterial haemodynamics in hypertension. Aust. N. Z. J. Med. 6(Suppl. 2), 40-48.
65. O'Rourke, M. F., and Hashimoto, J. (2007). Mechanical factors in arterial aging: a clinical perspective. J. Am. Coll. Cardiol. 50, 1-13.
66. Odink, A. E., Mattace-Raso, F. U., Lugt, A., Hofman, A., Hunink, M. G., Breteler, M. M., et al. (2008). The association of arterial stiffness and arterial calcification: the Rotterdam study. J. Hum. Hypertens. 22, 205-207.
67. Orr, A. W., Hastings, N. E., Blackman, B. R., and Wamhoff, B. R. (2010). Complex regulation and function of the inflammatory smooth muscle cell phenotype in atherosclerosis. J. Vasc. Res. 47, 168-180.
68. Pasquali-Ronchetti, I., Garcia-Fernandez, M. I., Boraldi, F., Quaglino, D., Gheduzzi, D., De Vincenzi Paolinelli, C., et al. (2006). Oxidative stress in fibro-blasts from patients with pseudoxanthoma elasticum: possible role in the pathogenesis of clinical manifestations. J. Pathol. 208, 54-61.
69. Pratt, B., and Curci, J. (2010). Arterial elastic fiber structure. Function and potential roles in acute aortic dissection. J. Cardiovasc. Surg. 51, 647-656.
70. Price, P. A., Faus, S. A., and Williamson, M. K. (1998). Warfarin causes rapid calcification of the elastic lamellae in rat arteries and heart valves. Arterioscler. Thromb. Vasc. Biol. 18, 1400-1407.
71. Qiu, Y., and Tarbell, J. M. (2000). Interaction between wall shear stress and circumferential strain affects endothelial cell biochemical production. J. Vasc. Res. 37, 147-157.
72. Rachev, A., and Hayashi, K. (1999). Theoretical study of the effects of vascular smooth muscle contraction on strain and stress distributions in arteries. Ann. Biomed. Eng. 27, 459-468.
73. Raggi, P., Callister, T. Q., and Shaw, L. J. (2004). Progression of coronary artery calcium and risk of first myocardial infarction in patients receiving cholesterol-lowering therapy. Arterioscler. Thromb. Vasc. Biol. 24, 1272-1277.
74. Rennenberg, R. J., Varik, B. J., Schurgers, L. J., Hamulyak, K., Cate, H., Leiner, T., et al. (2010). Chronic coumarin treatment is associated with increased extra-coronary arterial calcification in humans. Blood 115, 5121-5123.
75. Rutsch, F., Nitschke, Y., and Terkeltaub, R. (2011). Genetics in arterial calcification: pieces of a puzzle and cogs in a wheel. Circ. Res. 109, 578-592.
76. Safar, M. E., London, G. M., Asmar, R., and Frohlich, E. D. (1998). Recent advances on large arteries in hypertension. Hypertension 32, 156-161.
77. Safar, M. E., London, G. M., and Plante, G. E. (2004). Arterial stiffness and kidney function. Hypertension 43, 163-168.
78. Safar, M. E., Nilsson, P. M., Blacher, J., and Mimran, A. (2012). Pulse pressure, arterial stiffness, and end-organ damage. Curr. Hypertens. Rep. 14, 339-344.
79. Schurgers, L. J., Cranenburg, E. C., and Vermeer, C. (2008). Matrix Gla-protein: the calcification inhibitor in need of vitamin K. Thromb. Haemost. 100, 593-603.
80. Schurgers, L. J., Joosen, I. A., Laufer, E. M., Chatrou, M. L., Herfs, M., Winkens, M. H., et al. (2012). Vitamin k-antagonists accelerate atherosclerotic calcification and induce a vulnerable plaque phenotype. PLoS ONE 7:e43229. doi: 10.1371/journal.pone.0043229
81. Schurgers, L. J., Spronk, H. M., Soute, B. A., Schiffers, P. M., Demey, J. G., and Vermeer, C. (2007). Regression of warfarin-induced medial elas-tocalcinosis by high intake of vitamin K in rats. Blood 109, 2823-2831.
82. Schwartz, S. M., Virmani, R., and Rosenfeld, M. E. (2000). The good smooth muscle cells in atherosclerosis. Curr. Atheroscler. Rep. 2, 422-429.
83. Sekikawa, A., Shin, C., Curb, J. D., Barinas-Mitchell, E., Masaki, K., El-Saed, A., et al. (2012). Aortic stiffness and calcification in men in a population-based international study. Atherosclerosis 222, 473-477.
84. Shanahan, C. M., Cary, N. R., Metcalfe, J. C., and Weissberg, P. L. (1994). High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J. Clin. Invest. 93, 2393-2402.
85. Shanahan, C. M., Cary, N. R., Salisbury, J. R., Proudfoot, D., Weissberg, P. L., and Edmonds, M. E. (1999). Medial localization of mineralization-regulating proteins in association with Monckeberg's sclerosis: evidence for smooth muscle cell-mediated vascular calcification. Circulation 100, 2168-2176.
86. Shanahan, C. M., Crouthamel, M. H., Kapustin, A., and Giachelli, C. M. (2011). Arterial calcification in chronic kidney disease: key roles for calcium and phosphate. Circ. Res. 109, 697-711.
87. Shea, M. K., O'Donnell, C. J., Hoffmann, U., Dallal, G. E., Dawson-Hughes, B., Ordovas, J. M., et al. (2009). Vitamin K supplementation and progression of coronary artery calcium in older men and women. Am. J. Clin. Nutr. 89, 1799-1807.
88. Simionescu, A., Philips, K., and Vyavahare, N. (2005). Elastin-derived peptides and TGF-beta1 induce osteogenic responses in smooth muscle cells. Biochem. Biophys. Res. Commun. 334, 524-532.
89. Smith, E. R., Tomlinson, L. A., Ford, M. L., McMahon, L. P., Rajkumar, C., and Holt, S. G. (2012). Elastin degradation is associated with progressive aortic stiffening and all-cause mortality in predialysis chronic kidney disease. Hypertension 59, 973-978.
90. Sorescu, G. P., Sykes, M., Weiss, D., Platt, M. O., Saha, A., Hwang, J., et al. (2003). Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress stimulates an inflammatory response. J. Biol. Chem. 278, 31128-31135.
91. Speer, M. Y., McKee, M. D., Guldberg, R. E., Liaw, L., Yang, H., Tung, E., et al. (2002). Inactivation of the osteopontin gene enhances vascular calcification of matrix Gla protein-deficient mice: evidence for osteo-pontin as an inducible inhibitor of vascular calcification in vivo. J. Exp. Med. 196, 1047-1055.
92. Tanimura, A., McGregor, D. H., and Anderson, H. C. (1983). Matrix vesicles in atherosclerotic calcification. Proc. Soc. Exp. Biol. Med. 172, 173-177.
93. Tropeano, A., Boutouyrie, P., Pannier, B., Joannides, R., Balkestein, E., Katsahian, S., et al. (2006). Brachial pressure-independent reduction in carotid stiffness after long-term angiotensin-converting enzyme inhibition in diabetic hypertensives. Hypertension 48, 80-86.
94. Uitto, J., Li, Q., and Jiang, Q. (2010). Pseudoxanthoma elasticum: molecular genetics and putative pathome-chanisms. J. Invest. Dermatol. 130, 661-670.
95. Urschel, K., Cicha, I., Daniel, W. G., and Garlichs, C. D. (2012). Shear stress patterns affect the secreted chemokine profile in endothelial cells. Clin. Hemorheol. Microcirc. 50, 143-152.
96. Vanakker, O. M., Martin, L., Gheduzzi, D., Leroy, B. P., Loeys, B. L., Guerci, V. I., et al. (2007). Pseudoxanthoma elasticum-like phenotype with cutis laxa and multiple coagulation factor deficiency represents a separate genetic entity. J. Invest. Dermatol. 127, 581-587.
97. Vanakker, O. M., Martin, L., Schurgers, L. J., Quaglino, D., Costrop, L., Vermeer, C., et al. (2010). Low serum vitamin K in PXE results in defective carboxylation of mineralization inhibitors similar to the GGCX mutations in the PXE-like syndrome. Lab. Invest. 90, 895-905.
98. Verhave, J. C., Fesler, P., Cailar, G., Ribstein, J., Safar, M. E., and Mimran, A. (2005). Elevated pulse pressure is associated with low renal function in elderly patients with isolated systolic hypertension. Hypertension 45, 586-591.
99. Virmani, R., Avolio, A. P., Mergner, W. J., Robinowitz, M., Herderick, E. E., Cornhill, J. F., et al. (1991). Effect of aging on aortic morphology in populations with high and low prevalence of hypertension and atherosclerosis. Comparison between occidental and Chinese communities. Am. J. Pathol. 139, 1119-1129.
100. Vita, J. A., and Mitchell, G. F. (2003). Effects of shear stress and flow pulsatility on endothelial function: insights gleaned from external counterpulsation therapy. J. Am. Coll. Cardiol. 42, 2096-2098.
101. Vlachopoulos, C., Aznaouridis, K., and Stefanadis, C. (2010). Prediction of cardiovascular events and all-cause mortality with arterial stiffness: a systematic review and meta-analysis. J. Am. Coll. Cardiol. 55, 1318-1327.
102. Wallin, R., Cain, D., Hutson, S. M., Sane, D. C., and Loeser, R. (2000). Modulation of the binding of matrix Gla protein (MGP) to bone morphogenetic protein-2 (BMP-2). Thromb. Haemost. 84, 1039-1044.
103. Weijs, B., Blaauw, Y., Rennenberg, R. J., Schurgers, L. J., Timmermans, C. C., Pison, L., et al. (2011). Patients using vitamin K antagonists show increased levels of coronary calcification: an observational study in low-risk atrial fibrillation patients. Eur. Heart J. 32, 2555-2562.
104. Westenfeld, R., Krueger, T., Schlieper, G., Cranenburg, E. C., Magdeleyns, E. J., Heidenreich, S., et al. (2012). Effect of vitamin K2 supplementation on functional vitamin K deficiency in hemodialysis patients: a randomized trial. Am. J. Kidney Dis. 59, 186-195.
105. White, W. B., Duprez, D., Hillaire, R. S., Krause, S., Roniker, B., Kuse-Hamilton, J., et al. (2003). Effects of the selective aldosterone blocker eplerenone versus the calcium antagonist amlodipine in systolic hypertension. Hypertension 41, 1021-1026.
106. Williams, B. (1998). Mechanical influences on vascular smooth muscle cell function. J. Hypertens. 16, 1921-1929.
107. Willis, A. I., Pierre-Paul, D., Sumpio, B. E., and Gahtan, V. (2004). Vascular smooth muscle cell migration: current research and clinical implications. Vasc. Endovascular Surg. 38, 11-23.
108. Yao, Y., Bennett, B. J., Wang, X., Rosenfeld, M. E., Giachelli, C., Lusis, A. J., et al. (2010). Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ. Res. 107, 485-494.
109. Zebboudj, A. F., Shin, V., and Boström, K. (2003). Matrix GLA protein and BMP-2 regulate osteoinduction in calcifying vascular cells. J. Cell. Biochem. 90, 756-765.
110. Zieman, S. J., Melenovsky, V., Clattenburg, L., Corretti, M. C., Capriotti, A., Gerstenblith, G., et al. (2007). Advanced glyca-tion endproduct crosslink breaker (alagebrium) improves endothelial function in patients with isolated systolic hypertension. J. Hypertens. 25, 577-583.
111. Ziereisen, F., De Munter, C., and Perlmutter, N. (1993). The Keutel syndrome. Report of a case and review of the literature. Pediatr. Radiol. 23, 314-315.