Vitamin K-Antagonists Accelerate Atherosclerotic Calcification and Induce a Vulnerable Plaque Phenotype

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Schurgers, Leon J ^a   Joosen, Ivo A ^a   Laufer, Eduard M ^a   Chatrou, Martijn L L ^a   Herfs, Marjolein ^b   Winkens, Mark H M ^a   Westenfeld, Ralf ^c   Veulemans, Verena ^c   Krueger, Thilo ^d   Shanahan, Catherine M ^e   Jahnen Dechent, Willi ^d   Biessen, Erik ^f   Narula, Jagat ^g   Vermeer, Cees ^b   Hofstra, Leonard ^a,h   Reutelingsperger, Chris P ^a  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c UNIVERSITY HOSPITAL DÜSSELDORF   (Germany)

^d RWTH AACHEN UNIVERSITY   (Germany)

^e KING'S COLLEGE LONDON   (United Kingdom)

^f MAASTRICHT UNIVERSITY MEDICAL CENTER   (Netherlands)

^g MOUNT SINAI SCHOOL OF MEDICINE   (United States)

^h Cardiology Center Netherlands   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACETYLSALICYLIC ACID; ANTIVITAMIN K; APOLIPOPROTEIN E; BETA ADRENERGIC RECEPTOR BLOCKING AGENT; HIGH DENSITY LIPOPROTEIN CHOLESTEROL; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; LOW DENSITY LIPOPROTEIN CHOLESTEROL; OSTEOCALCIN; REGULATOR PROTEIN; TRIACYLGLYCEROL; VERAPAMIL; VITAMIN K GROUP; WARFARIN;

ADULT; APOPTOSIS; ARTICLE; ATHEROSCLEROSIS; BLOOD VESSEL CALCIFICATION; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CORONARY ARTERY CALCIFICATION; CORONARY ARTERY DISEASE; FEMALE; HEART MUSCLE REVASCULARIZATION; HEART VENTRICLE REMODELING; HUMAN; MAJOR CLINICAL STUDY; MALE; MORPHOLOGY; MOUSE; MULTIDETECTOR COMPUTED TOMOGRAPHY; NONHUMAN; PHENOTYPE; PLAGUE; RISK FACTOR; THROMBOEMBOLISM; TRIACYLGLYCEROL BLOOD LEVEL; VEIN THROMBOSIS;

AGED; ANIMALS; APOLIPOPROTEINS E; ATHEROSCLEROSIS; CALCINOSIS; CORONARY ARTERY DISEASE; FEMALE; HUMANS; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; PHENOTYPE; PLAQUE, ATHEROSCLEROTIC; RISK; THROMBOEMBOLISM; VITAMIN K; WARFARIN;

ANIMALIA; MUS; WHITE TIP DIE-BACK PHYTOPLASMA;

EID: 84865598969     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043229     Document Type: Article

References (55)

1. D'Andrea G, D'Ambrosio R, Margaglione M, (2008) Oral anticoagulants: Pharmacogenetics Relationship between genetic and non-genetic factors. Blood Rev 22: 127-140.
2. Chatrou MLL, Reutelingsperger CP, Schurgers LJ (2011) Role of vitamin K-dependent proteins in the arterial vessel wall. Hamostaseologie 31.
3. Price P, Williamson M, (1985) Primary structure of bovine matrix Gla protein, a new vitamin K-dependent bone protein. J Biol Chem 260: 14971-14975.
4. Luo G, Ducy P, McKee M, Pinero G, Loyer E, et al. (1997) Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 385: 78-81.
5. Murshed M, Schinke T, McKee M, Karsenty G, (2004) Extracellular matrix mineralization is regulated locally; different roles of two gla-containing proteins. J Cell Biol 165: 625-630.
6. Schurgers LJ, Spronk HMH, Soute BAM, Schiffers PM, DeMey JGR, et al. (2007) Regression of warfarin-induced medial elastocalcinosis by high intake of vitamin K in rats. Blood 109: 2823-2831.
7. Zebboudj A, Imura M, Bostrom K, (2002) Matrix GLA protein, a regulatory protein for bone morphogenetic protein-2. J Biol Chem 277: 4388-4394.
8. Yao Y, Zebboudj A, Shao E, Perez M, Bostrom K, (2006) Regulation of bone morphogenetic protein-4 by matrix GLA protein in vascular endothelial cells involves activin-like kinase receptor 1. J Biol Chem 281: 33921-33930.
9. Speer MY, Yang H-Y, Brabb T, Leaf E, Look A, et al. (2009) Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res 104: 733-741.
10. Schurgers LJ, Spronk HMH, Skepper JN, Hackeng TM, Shanahan CM, et al. (2007) Post-translational modifications regulate matrix Gla protein function: importance for inhibition of vascular smooth muscle cell calcification. J Thromb Haemost 5: 2503-2511.
11. O'Young J, Liao Y, Xiao Y, Jalkanen J, Lajoie G, et al. (2011) Matrix gla protein inhibits ectopic calcification by a direct interaction with hydroxyapatite crystals. J Am Chem Soc 133: 18406-18412.
12. Schurgers LJ, Aebert H, Vermeer C, Bültmann B, Janzen J, (2004) Oral anticoagulant treatment: friend or foe in cardiovascular disease? Blood 104: 3231-3232.
13. Weijs B, Blaauw Y, Rennenberg RJMW, Schurgers LJ, Timmermans CCMM, et al. (2011) Patients using vitamin K antagonists show increased levels of coronary calcification: an observational study in low-risk atrial fibrillation patients. European heart journal 32: 2555-2562.
14. Rennenberg RJMW, van Varik BJ, Schurgers LJ, Hamulyak K, Ten Cate H, et al. (2010) Chronic coumarin treatment is associated with increased extracoronary arterial calcification in humans. Blood 115: 5121-5123.
15. Koos R, Mahnken A, Muhlenbruch G, Brandenburg V, Pflueger B, et al. (2005) Relation of oral anticoagulation to cardiac valvular and coronary calcium assessed by multislice spiral computed tomography. Am J Cardiol 96: 747-749.
16. Shanahan CM, Cary NR, Metcalfe JC, Weissberg PL, (1994) High expression of genes for calcification-regulating proteins in human atherosclerotic plaques. J Clin Invest 93: 2393-2402.
17. Naik V, Leaf EM, Hu JH, Yang H-Y, Nguyen NB, et al. (2012) Sources of cells that contribute to atherosclerotic intimal calcification: an in vivo genetic fate mapping study. Cardiovascular research 94: 545-554.
18. Yao Y, Bennett BJ, Wang X, Rosenfeld ME, Giachelli C, et al. (2010) Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circulation Research 107: 485-494.
19. Nakagawa Y, Ikeda K, Akakabe Y, Koide M, Uraoka M, 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.
20. Ehara S, Kobayashi Y, Yoshiyama M, Shimada K, Shimada Y, et al. (2004) Spotty calcification typifies the culprit plaque in patients with acute myocardial infarction: an intravascular ultrasound study. Circulation 110: 3424-3429.
21. Vengrenyuk Y, Carlier S, Xanthos S, Cardoso L, Ganatos P, et al. (2006) A hypothesis for vulnerable plaque rupture due to stress-induced debonding around cellular microcalcifications in thin fibrous caps. Proc Natl Acad Sci U S A 103: 14678-14683.
22. Chen N, Kircelli F, O'Neill K, Chen X, Moe S, (2010) Verapamil inhibits calcification and matrix vesicle activity of bovine vascular smooth muscle cells. Kidney Int 77: 436-442.
23. Price P, Faus S, Williamson M, (1998) Warfarin causes rapid calcification of the elastic lamellae in rat arteries and heart valves. Arterioscler Thromb Vasc Biol 18: 1400-1407.
24. Clarke M, Figg N, Maguire J, Davenport A, Goddard M, et al. (2006) Apoptosis of vascular smooth muscle cells induces features of plaque vulnerability in atherosclerosis. Nat Med 12: 1075-1080.
25. Clarke M, Littlewood T, Figg N, Maguire J, Davenport A, et al. (2008) Chronic apoptosis of vascular smooth muscle cells accelerates atherosclerosis and promotes calcification and medial degeneration. Circ Res 102: 1529-1538.
26. Ewence AE, Bootman M, Roderick HL, Skepper JN, McCarthy G, et al. (2008) Calcium phosphate crystals induce cell death in human vascular smooth muscle cells: a potential mechanism in atherosclerotic plaque destabilization. Circulation research 103: e28-34.
27. Nadra I, Mason J, Philippidis P, Florey O, Smythe C, et al. (2005) Proinflammatory Activation of Macrophages by Basic Calcium Phosphate Crystals via Protein Kinase C and MAP Kinase Pathways: A Vicious Cycle of Inflammation and Arterial Calcification? Circ Res 96: 1248-1256.
28. Amann K, (2008) Media Calcification and Intima Calcification Are Distinct Entities in Chronic Kidney Disease. Clin J Am Soc Nephrol 6: 1599-1605.
29. Doherty T, Fitzpatrick L, Inoue D, Qiao J, Fishbein M, et al. (2004) Molecular, endocrine, and genetic mechanisms of arterial calcification. Endocr Rev 25: 629-672.
30. Spronk HMH, Soute BAM, Schurgers LJ, Thijssen HHW, De Mey JGR, et al. (2003) Tissue-specific utilization of menaquinone-4 results in the prevention of arterial calcification in warfarin-treated rats. J Vasc Res 40: 531-537.
31. Essalihi R, Dao H, Yamaguchi N, Moreau P, (2003) A new model of isolated systolic hypertension induced by chronic warfarin and vitamin K1 treatment. Am J Hypertens 16: 103-110.
32. Motoyama S, Kondo T, Sarai M, Sugiura A, Harigaya H, et al. (2007) Multislice computed tomographic characteristics of coronary lesions in acute coronary syndromes. Journal of the American College of Cardiology 50: 319-326.
33. Raggi P, Shaw L, Berman D, Callister T, (2004) Prognostic value of coronary artery calcium screening in subjects with and without diabetes. J Am Coll Cardiol 43: 1663-1669.
34. Rennenberg RJMW, Kessels AGH, Schurgers LJ, van Engelshoven JMA, de Leeuw PW, et al. (2009) Vascular calcifications as a marker of increased cardiovascular risk: a meta-analysis. Vascular health and risk management 5: 185-197.
35. Huang H, Virmani R, Younis H, Burke A, Kamm R, et al. (2001) The impact of calcification on the biomechanical stability of atherosclerotic plaques. Circulation 103: 1051-1056.
36. Detrano R, Hsiai T, Wang S, Puentes G, Fallavollita J, et al. (1996) Prognostic value of coronary calcification and angiographic stenoses in patients undergoing coronary angiography. Journal of the American College of Cardiology 27: 285-290.
37. Detrano R, Guerci AD, Carr JJ, Bild DE, Burke G, et al. (2008) Coronary calcium as a predictor of coronary events in four racial or ethnic groups. The New England journal of medicine 358: 1336-1345.
38. Fujii K, Carlier SG, Mintz GS, Takebayashi H, Yasuda T, et al. (2005) Intravascular ultrasound study of patterns of calcium in ruptured coronary plaques. The American journal of cardiology 96: 352-357.
39. Schurgers LJ, Cranenburg ECM, Vermeer C, (2008) Matrix Gla-protein: the calcification inhibitor in need of vitamin K. Thromb Haemost. 100: 593-603.
40. Roijers RB, Debernardi N, Cleutjens JP, Schurgers LJ, Mutsaers PH, et al. (2011) Microcalcifications in Early Intimal Lesions of Atherosclerotic Human Coronary Arteries. The American journal of pathology 178: 2879-2887.
41. Csiszar A, Smith KE, Koller A, Kaley G, Edwards JG, et al. (2005) Regulation of bone morphogenetic protein-2 expression in endothelial cells: role of nuclear factor-kappaB activation by tumor necrosis factor-alpha, H2O2, and high intravascular pressure. Circulation 111: 2364-2372.
42. Hruska KA, Mathew S, Saab G, (2005) Bone morphogenetic proteins in vascular calcification. Circulation research 97: 105-114.
43. El-Maadawy S, Kaartinen M, Schinke T, Murshed M, Karsenty G, et al. (2003) Cartilage formation and calcification in arteries of mice lacking matrix Gla protein. Connect Tissue Res 44 (Suppl 1): 272-278.
44. Proudfoot D, Skepper JN, Hegyi L, Bennett MR, Shanahan CM, et al. (2000) Apoptosis regulates human vascular calcification in vitro: evidence for initiation of vascular calcification by apoptotic bodies. Circ Res 87: 1055-1062.
45. Kolodgie FD, Narula J, Haider N, Virmani R (2001) Apoptosis in atherosclerosis. Does it contribute to plaque instability? Cardiol Clin 19: 127-139, ix.
46. Tabas I, (2010) Macrophage death and defective inflammation resolution in atherosclerosis. Nat Rev Immunol 10: 36-46.
47. Bouvet C, Moreau S, Blanchette J, de Blois D, Moreau P, (2008) Sequential activation of matrix metalloproteinase 9 and transforming growth factor beta in arterial elastocalcinosis. Arteriosclerosis, thrombosis, and vascular biology 28: 856-862.
48. Motoyama S, Sarai M, Harigaya H, Anno H, Inoue K, et al. (2009) Computed tomographic angiography characteristics of atherosclerotic plaques subsequently resulting in acute coronary syndrome. Journal of the American College of Cardiology 54: 49-57.
49. Borissoff JI, Spronk HM, Ten Cate H, (2011) The Hemostatic System as a Modulator of Atherosclerosis. N Engl J Med 364: 1746-1760.
50. Chatrou MLL, Winckers K, Hackeng TM, Reutelingsperger CP, Schurgers LJ, (2012) Vascular calcification: The price to pay for anticoagulation therapy with vitamin K-antagonists. Blood Rev 26: 155-166.
51. Agatston AS, Janowitz WR, Hildner FJ, Zusmer NR, Viamonte M, et al. (1990) Quantification of coronary artery calcium using ultrafast computed tomography. Journal of the American College of Cardiology 15: 827-832.
52. McCollough CH, Ulzheimer S, Halliburton SS, Shanneik K, White RD, et al. (2007) Coronary artery calcium: a multi-institutional, multimanufacturer international standard for quantification at cardiac CT. Radiology 243: 527-538.
53. Braunwald E, Antman EM, Beasley JW, Califf RM, Cheitlin MD, et al. (2002) ACC/AHA 2002 guideline update for the management of patients with unstable angina and non-ST-segment elevation myocardial infarction-summary article: a report of the American College of Cardiology/American Heart Association task force on practice guidelines (Committee on the Management of Patients With Unstable Angina). Journal of the American College of Cardiology. 1366-1374.
54. Dumont EA, Hofstra L, van Heerde WL, van den Eijnde S, Doevendans PA, et al. (2000) Cardiomyocyte death induced by myocardial ischemia and reperfusion: measurement with recombinant human annexin-V in a mouse model. Circulation 102: 1564-1568.
55. Lutgens E, Daemen M, Kockx M, Doevendans P, Hofker M, et al. (1999) Atherosclerosis in APOE*3-Leiden transgenic mice: from proliferative to atheromatous stage. Circulation 99: 276-283.