The roles of lipid oxidation products and receptor activator of nuclear factor-κb signaling in atherosclerotic calcification

Circulation Research

Volumn 108, Issue 12, 2011, Pages 1482-1493

  Demer, Linda ^a,b,c   Tintut, Yin ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c University of California   (United States)

Author keywords

atherosclerosis; calcification; nuclear factor B ligand; oxidized lipids; receptor activator o

Indexed keywords

OSTEOCLAST DIFFERENTIATION FACTOR;

ATHEROGENESIS; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL CALCIFICATION; HUMAN; LIPID ANALYSIS; LIPID OXIDATION; NONHUMAN; OSTEOBLAST; OSTEOCLAST; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; ATHEROSCLEROSIS; CALCINOSIS; HUMANS; LIPID METABOLISM; LIPIDS; NF-KAPPA B; OSTEOCLASTS; OSTEOGENESIS; OXIDATION-REDUCTION; TUMOR NECROSIS FACTOR DECOY RECEPTORS;

EID: 79958794011     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.110.234245     Document Type: Review

References (156)

1. Bolland MJ, Wang TK, van Pelt NC, Horne AM, Mason BH, Ames RW, Grey AB, Ruygrok PN, Gamble GD, Reid IR. Abdominal aortic calcification on vertebral morphometry images predicts incident myocardial infarction. J Bone Miner Res. 2010;25:505-512.
2. Shao JS, Aly ZA, Lai CF, Cheng SL, Cai J, Huang E, Behrmann A, Towler DA. Vascular Bmp Msx2 Wnt signaling and oxidative stress in arterial calcification. Ann N Y Acad Sci. 2007;117:40-50. (Pubitemid 350191291)
3. Boström K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J Clin Invest. 1993;91:1800-1809. (Pubitemid 23127387)
4. Proudfoot D, Davies JD, Skepper JN, Weissberg PL, Shanahan CM. Acetylated low-density lipoprotein stimulates human vascular smooth muscle cell calcification by promoting osteoblastic differentiation and inhibiting phagocytosis. Circulation. 2002;106:3044-3050. (Pubitemid 35440286)
5. Tanimura A, McGregor DH, Anderson HC. Matrix vesicles in atherosclerotic calcification. Proc Soc Exp Biol Med. 1983;172:173-177. (Pubitemid 13143185)
6. Bobryshev YV, Killingsworth MC, Lord RS, Grabs AJ. Matrix vesicles in the fibrous cap of atherosclerotic plaque: possible contribution to plaque rupture. J Cell Mol Med. 2008;12:2073-2082.
7. Frid MG, Kale VA, Stenmark KR. Mature vascular endothelium can give rise to smooth muscle cells via endothelial-mesenchymal transdifferentiation: in vitro analysis. Circ Res. 2002;90:1189-1196. (Pubitemid 34786904)
8. Cossu G, Bianco P. Mesoangioblasts-vascular progenitors for extravascular mesodermal tissues. Curr Opin Genet Dev. 2003;13:537-542. (Pubitemid 37204932)
9. Traktuev DO, Merfeld-Clauss S, Li J, Kolonin M, Arap W, Pasqualini R, Johnstone BH, March KL. A population of multipotent CD34- positive adipose stromal cells share pericyte and mesenchymal surface markers, reside in a periendothelial location, and stabilize endothelial networks. Circ Res. 2008;102:77-85.
10. Li H, Hong S, Qian J, Zheng Y, Yang J, Yi Q. Crosstalk between the bone and immune systems: osteoclasts function as antigen-presenting cells and activate CD4+ and CD8+ T cells. Blood. 2010;116:210-217.
11. Gallois A, Lachuer J, Yvert G, Wierinckx A, Brunet F, Rabourdin-Combe C, Delprat C, Jurdic P, Mazzorana M. Genome-wide expression analyses establish dendritic cells as a new osteoclast precursor able to generate bone-resorbing cells more efficiently than monocytes. J Bone Miner Res. 2010;25, 661-672.
12. Tintut Y, Alfonso Z, Saini T, Radcliff K, Watson K, Boström K, Demer LL. Multilineage potential of cells from the artery wall. Circulation. 2003;108:2505-2510. (Pubitemid 37444413)
13. Dellavalle A, Sampaolesi M, Tonlorenzi R, Tagliafico E, Sacchetti B, Perani L, Innocenzi A, Galvez BG, Messina G, Morosetti R, Li S, Belicchi M, Peretti G, Chamberlain JS, Wright WE, Torrente Y, Ferrari S, Bianco P, Cossu G. Pericytes of human skeletal muscle are myogenic precursors distinct from satellite cells. Nat Cell Biol. 2007;9:255-267. (Pubitemid 46349927)
14. Farrington-Rock C, Crofts NJ, Doherty MJ, Ashton BA, Griffin-Jones C, Canfield AE. Chondrogenic and adipogenic potential of microvascular pericytes. Circulation. 2004;110:2226-2232. (Pubitemid 39372506)
15. Demer LL, Tintut Y. Vascular calcification: pathobiology of a multifaceted disease. Circulation. 2008;117:2938-2948. (Pubitemid 351787058)
16. Mohler ER III, Gannon F, Reynolds C, Zimmerman R, Keane MG, Kaplan FS. Bone formation and inflammation in cardiac valves. Circulation. 2001;103:1522-1528. (Pubitemid 32226259)
17. Neven E, Persy V, Dauwe S, De Schutter T, De Broe ME, D'Haese PC. Chondrocyte rather than osteoblast conversion of vascular cells underlies medial calcification in uremic rats. Arterioscler Thromb Vasc Biol. 2010;30:1741-1750.
18. Alexander MY. RANKL links arterial calcification with osteolysis. Circ Res. 2009;104:1032-1034.
19. Witztum JL, Steinberg D. Role of oxidized low density lipoprotein in atherogenesis. J Clin Invest. 1991;88:1785-1792.
20. Dzeletovic S, Babiker A, Lund E, Diczfalusy U. Time course of oxysterol formation during in vitro oxidation of low density lipoprotein. Chem Phys Lipids. 1995;78:119-128.
21. Dzeletovic S, Breuer O, Lund E, Diczfalusy U. Determination of cholesterol oxidation products in human plasma by isotope dilution-mass spectrometry. Anal Biochem. 1995;225:73-80.
22. Schor AM, Allen TD, Canfield AE, Sloan P, Schor SL. Pericytes derived from the retinal microvasculature undergo calcification in vitro. J Cell Sci. 1990;97:449-461. (Pubitemid 20374486)
23. Watson KE, Boström K, Ravindranath R, Lam T, Norton B, Demer LL. TGF-beta 1 and 25-hydroxycholesterol stimulate osteoblast-like vascular cells to calcify. J Clin Invest. 1994;93:2106-2113.
24. Parhami F, Morrow AD, Balucan J, Leitinger N, Watson AD, Tintut Y, Berliner JA, Demer LL. Lipid oxidation products have opposite effects on calcifying vascular cell and bone cell differentiation. A possible explanation for the paradox of arterial calcification in osteoporotic patients. Arterioscler Thromb Vasc Biol. 1997;17:680-687. (Pubitemid 27169128)
25. Yan J, Stringer SE, Hamilton A, Charlton-Menys V, Gotting C, Muller B, Aeschlimann D, Alexander MY. Decorin GAG synthesis and TGF-{beta} signaling mediate ox-LDL-induced mineralization of human vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2011;31:608-615.
26. Vyavahare NR, Hirsch D, Lerner E, Baskin JZ, Zand R, Schoen FJ, Levy RJ. Prevention of calcification of glutaraldehyde-crosslinked porcine aortic cusps by ethanol preincubation: mechanistic studies of protein structure and water-biomaterial relationships. J Biomed Mater Res. 1998;40:577-585. (Pubitemid 28225843)
27. Towler DA, Bidder M, Latifi T, Coleman T, Semenkovich CF. Dietinduced diabetes activates an osteogenic gene regulatory program in the aortas of low density lipoprotein receptor-deficient mice. J Biol Chem. 1998;273:30427-30434. (Pubitemid 28545516)
28. Vickers KC, Castro-Chavez F, Morrisett JD. Lyso-phosphatidylcholine induces osteogenic gene expression and phenotype in vascular smooth muscle cells. Atherosclerosis. 2010;211:122-129.
29. Demer LL. Lipid hypothesis of cardiovascular calcification. Circulation. 1997;95:297-298. (Pubitemid 27056186)
30. An WS, Kim SE, Kim KH, Bae HR, Rha SH. Associations between oxidized LDL to LDL ratio, HDL and vascular calcification in the feet of hemodialysis patients. J Korean Med Sci. 2009;24(Suppl):S115-S120.
31. Qasim AN, Martin SS, Mehta NN, Wolfe ML, Park J, Schwartz S, Schutta M, Iqbal N, Reilly MP. Lipoprotein(a) is strongly associated with coronary artery calcification in type-2 diabetic women. Int J Cardiol. 2010 Mar 18 [Epub ahead of print].
32. Shen H, Damcott CM, Rampersaud E, Pollin TI, Horenstein RB, McArdle PF, Peyser PA, Bielak LF, Post WS, Chang YP, Ryan KA, Miller M, Rumberger JA, Sheedy PF II, Shelton J, O'Connell JR, Shuldiner AR, Mitchell BD. Familial defective apolipoprotein B-100 and increased low-density lipoprotein cholesterol and coronary artery calcification in the old order amish. Arch Intern Med. 2010;170: 1850-1855.
33. Orakzai SH, Nasir K, Blaha M, Blumenthal RS, Raggi P. Non-HDL cholesterol is strongly associated with coronary artery calcification in asymptomatic individuals. Atherosclerosis. 2009;202:289-295.
34. Yang X, Fullerton DA, Su X, Ao L, Cleveland JC, Jr., Meng X. Proosteogenic phenotype of human aortic valve interstitial cells is associated with higher levels of Toll-like receptors 2 and 4 and enhanced expression of bone morphogenetic protein 2. J Am Coll Cardiol. 2009;53:491-500.
35. Drolet MC, Couet J, Arsenault M. Development of aortic valve sclerosis or stenosis in rabbits: role of cholesterol and calcium. J Heart Valve Dis. 2008;17:381-387.
36. Miller YI, Choi SH, Wiesner P, Fang L, Harkewicz R, Hartvigsen K, Boullier A, Gonen A, Diehl CJ, Que X, Montano E, Shaw PX, Tsimikas S, Binder CJ, Witztum JL. Oxidation-specific epitopes are dangerassociated molecular patterns recognized by pattern recognition receptors of innate immunity. Circ Res. 2011;108:235-248.
37. Mody N, Parhami F, Sarafian TA, Demer LL. Oxidative stress modulates osteoblastic differentiation of vascular and bone cells. Free Radic Biol Med. 2001;31:509-519. (Pubitemid 32728438)
38. Liberman M, Bassi E, Martinatti MK, Lario FC, Wosniak J Jr, Pomerantzeff PM, Laurindo FR. Oxidant generation predominates around calcifying foci and enhances progression of aortic valve calcification. Arterioscler Thromb Vasc Biol. 2008;28:463-470.
39. Ducy P, Zhang R, Geoffroy V, Ridall AL, Karsenty G. Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell. 1997;89:747-754. (Pubitemid 27516177)
40. Komori T, Yagi H, Nomura S, Yamaguchi A, Sasaki K, Deguchi K, Shimizu Y, Bronson RT, Gao YH, Inada M, Sato M, Okamoto R, Kitamura Y, Yoshiki S, Kishimoto T. Targeted disruption of Cbfa1 results in a complete lack of bone formation owing to maturational arrest of osteoblasts. Cell. 1997;89:755-764. (Pubitemid 27516178)
41. Otto F, Thornell AP, Crompton T, Denzel A, Gilmour KC, Rosewell IR, Stamp GW, Beddington RS, Mundlos S, Olsen BR, Selby PB, Owen MJ. Cbfa1, a candidate gene for cleidocranial dysplasia syndrome, is essential for osteoblast differentiation and bone development. Cell. 1997;89:765-771. (Pubitemid 27516179)
42. Rodan GA, Harada S. The missing bone. Cell. 1997;89:677-680. (Pubitemid 27516169)
43. Byon CH, Javed A, Dai Q, Kappes JC, Clemens TL, Darley-Usmar VM, McDonald JM, Chen Y. Oxidative stress induces vascular calcification through modulation of the osteogenic transcription factor Runx2 by AKT signaling. J Biol Chem. 2008;283:15319-15327.
44. Parhami F, Basseri B, Hwang J, Tintut Y, Demer LL. High-density lipoprotein regulates calcification of vascular cells. Circ Res. 2002;91:570-576.
45. Abedin M, Lim J, Tang TB, Park D, Demer LL, Tintut Y. N-3 fatty acids inhibit vascular calcification via the p38-mitogen-activated protein kinase and peroxisome proliferator-activated receptor-gamma pathways. Circ Res. 2006;98:727-729.
46. Schlemmer CK, Coetzer H, Claassen N, Kruger MC, Rademeyer C, van Jaarsveld L, Smuts CM. Ectopic calcification of rat aortas and kidneys is reduced with n-3 fatty acid supplementation. Prostaglandins Leukot Essent Fatty Acids. 1998;59:221-227. (Pubitemid 28505115)
47. -/- mice with chronic kidney disease. Circ Res. 2010;106:1807-1817.
48. Miller JD, Weiss RM, Serrano KM, Brooks RM II, Berry CJ, Zimmerman K, Young SG, Heistad DD. Lowering plasma cholesterol levels halts progression of aortic valve disease in mice. Circulation. 2009;119:2693-2701.
49. Osman L, Chester AH, Amrani M, Yacoub MH, Smolenski RT. A novel role of extracellular nucleotides in valve calcification: a potential target for atorvastatin. Circulation. 2006;114:I566 -572. (Pubitemid 44297209)
50. Terry JG, Carr JJ, Kouba EO, Davis DH, Menon L, Bender K, Chandler ET, Morgan T, Crouse JR III. Effect of simvastatin (80 mg) on coronary and abdominal aortic arterial calcium (from the coronary artery calcification treatment with zocor [CATZ] study). Am J Cardiol. 2007;99:1714-1717. (Pubitemid 46874323)
51. Tourmousoglou CE, Lalos S, Psarros T. Do statins slow the progression of aortic valve stenosis? Interact Cardiovasc Thorac Surg. 2008;7:684-689.
52. Olsson AG. Lipid lowering and aortic valve disease. Curr Atheroscler Rep. 2009;11:377-383.
53. Rosenhek R, Baumgartner H. Aortic sclerosis, aortic stenosis and lipidlowering therapy. Expert Rev Cardiovasc Ther. 2008;6:385-390.
54. Mundy G, Garrett R, Harris S, Chan J, Chen D, Rossini G, Boyce B, Zhao M, Gutierrez G. Stimulation of bone formation in vitro and in rodents by statins. Science. 1999;286:1946-1949. (Pubitemid 129515901)
55. Tang FT, Chen SR, Wu XQ, Wang TQ, Chen JW, Li J, Bao LP, Huang HQ, Liu PQ. Hypercholesterolemia accelerates vascular calcification induced by excessive vitamin D via oxidative stress. Calcif Tissue Int. 2006;79:326-339. (Pubitemid 44900156)
56. Bear M, Butcher M, Shaughnessy SG. Oxidized low-density lipoprotein acts synergistically with beta-glycerophosphate to induce osteoblast differentiation in primary cultures of vascular smooth muscle cells. J Cell Biochem. 2008;105:185-193.
57. Shao JS, Cheng SL, Charlton-Kachigian N, Loewy AP, Towler DA. Teriparatide (human parathyroid hormone (1-34)) inhibits osteogenic vascular calcification in diabetic low density lipoprotein receptordeficient mice. J Biol Chem. 2003;278:50195-50202. (Pubitemid 37548859)
58. Aikawa E, Nahrendorf M, Figueiredo JL, Swirski FK, Shtatland T, Kohler RH, Jaffer FA, Aikawa M, Weissleder R. Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo. Circulation. 2007;116:2841-2850. (Pubitemid 350301146)
59. Tintut Y, Patel J, Territo M, Saini T, Parhami F, Demer LL. Monocyte/ macrophage regulation of vascular calcification in vitro. Circulation. 2002;105:650-655. (Pubitemid 34123443)
60. Tintut Y, Patel J, Parhami F, Demer LL. Tumor necrosis factor-alpha promotes in vitro calcification of vascular cells via the cAMP pathway. Circulation. 2000;102:2636-2642.
61. -/- mice. Arterioscler Thromb Vasc Biol. 2007;27:2589-2596. (Pubitemid 350158910)
62. Hjortnaes J, Butcher J, Figueiredo JL, Riccio M, Kohler RH, Kozloff KM, Weissleder R, Aikawa E. Arterial and aortic valve calcification inversely correlates with osteoporotic bone remodelling: a role for inflammation. Eur Heart J. 2010;31:1975-1984.
63. Adami S, Braga V, Zamboni M, Gatti D, Rossini M, Bakri J, Battaglia E. Relationship between lipids and bone mass in 2 cohorts of healthy women and men. Calcif Tissue Int. 2004;74:136-142. (Pubitemid 38263855)
64. Allison MA, Wright M, Tiefenbrun J. The predictive power of lowdensity lipoprotein cholesterol for coronary calcification. Int J Cardiol. 2003;90:281-289. (Pubitemid 37087888)
65. Pennisi P, Signorelli SS, Riccobene S, Celotta G, Di Pino L, La Malfa T, Fiore CE. Low bone density and abnormal bone turnover in patients with atherosclerosis of peripheral vessels. Osteoporos Int. 2004;15:389-395. (Pubitemid 38639334)
66. Persy V, D'Haese P. Vascular calcification and bone disease: the calcification paradox. Trends Mol Med. 2009;15:405-416.
67. Szulc P, Kiel DP, Delmas PD. Calcifications in the abdominal aorta predict fractures in men: MINOS study. J Bone Miner Res. 2008;23:95-102.
68. Hak AE, Pols HA, van Hemert AM, Hofman A, Witteman JC. Progression of aortic calcification is associated with metacarpal bone loss during menopause: a population-based longitudinal study. Arterioscler Thromb Vasc Biol. 2000;20:1926-1931. (Pubitemid 30644642)
69. Hmamouchi I, Allali F, Khazzani H, Bennani L, El Mansouri L, Ichchou L, Cherkaoui M, Abouqal R, Hajjaj-Hassouni N. Low bone mineral density is related to atherosclerosis in postmenopausal Moroccan women. BMC Public Health. 2009;9:388.
70. Tomiyama C, Carvalho AB, Higa A, Jorgetti V, Draibe SA, Canziani ME. Coronary calcification is associated with lower bone formation rate in CKD patients not yet in dialysis trreatment. J Bone Miner Res. 2010;25:499-504
71. Reid IR, Bolland MJ, Grey A. Does calcium supplementation increase cardiovascular risk? Clin Endocrinol (Oxf). 2010;73:689-695.
72. Price PA, Faus SA, Williamson MK. Bisphosphonates alendronate and ibandronate inhibit artery calcification at doses comparable to those that inhibit bone resorption. Arterioscler Thromb Vasc Biol. 2001;21:817-824. (Pubitemid 32448773)
73. Qiao JH, Fishbein MC, Demer LL, Lusis AJ. Genetic determination of cartilaginous metaplasia in mouse aorta. Arterioscler Thromb Vasc Biol. 1995;15:2265-2272. (Pubitemid 26001430)
74. Qiao JH, Xie PZ, Fishbein MC, Kreuzer J, Drake TA, Demer LL, Lusis AJ. Pathology of atheromatous lesions in inbred and genetically engineered mice. Genetic determination of arterial calcification. Arterioscler Thromb. 1994;14:1480-1497.
75. Spicer SS, Lewis SE, Tashian RE, Schulte BA. Mice carrying a CAR-2 null allele lack carbonic anhydrase II immunohistochemically and show vascular calcification. Am J Pathol. 1989;134:947-954. (Pubitemid 19111260)
76. Niemeier A, Niedzielska D, Secer R, Schilling A, Merkel M, Enrich C, Rensen PC, Heeren J. Uptake of postprandial lipoproteins into bone in vivo: impact on osteoblast function. Bone. 2008;43:230-237.
77. Tintut Y, Morony S, Demer LL. Hyperlipidemia promotes osteoclastic potential of bone marrow cells ex vivo. Arterioscler Thromb Vasc Biol. 2004;24:e6-e10.
78. Brodeur MR, Brissette L, Falstrault L, Ouellet P, Moreau R. Influence of oxidized low-density lipoproteins (LDL) on the viability of osteoblastic cells. Free Radic Biol Med. 2008;44:506-517. (Pubitemid 351181262)
79. Parhami F, Jackson SM, Tintut Y, Le V, Balucan JP, Territo M, Demer LL. Atherogenic diet and minimally oxidized low density lipoprotein inhibit osteogenic and promote adipogenic differentiation of marrow stromal cells. J Bone Miner Res. 1999;14:2067-2078. (Pubitemid 30026956)
80. Hirasawa H, Tanaka S, Sakai A, Tsutsui M, Shimokawa H, Miyata H, Moriwaki S, Niida S, Ito M, Nakamura T. ApoE gene deficiency enhances the reduction of bone formation induced by a high-fat diet through the stimulation of p53-mediated apoptosis in osteoblastic cells. J Bone Miner Res. 2007;22:1020-1030. (Pubitemid 351339724)
81. Parhami F, Tintut Y, Beamer WG, Gharavi N, Goodman W, Demer LL. Atherogenic high-fat diet reduces bone mineralization in mice. J Bone Miner Res. 2001;16:182-188. (Pubitemid 32046204)
82. Nikolov IG, Joki N, Nguyen-Khoa T, Ivanovski O, Phan O, Lacour B, Drüeke TB, Massy ZA, Dos Reis LM, Jorgetti V, Lafage-Proust MH. Chronic kidney disease bone and mineral disorder (CKD-MBD) in apolipoprotein E-deficient mice with chronic renal failure. Bone. 2010;47:156-163.
83. Almeida M, Ambrogini E, Han L, Manolagas SC, Jilka RL. Increased lipid oxidation causes oxidative stress, increased peroxisome proliferator-activated receptor-gamma expression, and diminished pro-osteogenic Wnt signaling in the skeleton. J Biol Chem. 2009;284:27438-27448.
84. Jilka RL, Almeida M, Ambrogini E, Han L, Roberson PK, Weinstein RS, Manolagas SC. Decreased oxidative stress and greater bone anabolism in the aged, when compared to the young, murine skeleton with parathyroid hormone administration. Aging Cell. 2010;9:851-867.
85. Graham LS, Tintut Y, Parhami F, Kitchen CM, Ivanov Y, Tetradis S, Effros RB. Bone density and hyperlipidemia: the T-lymphocyte connection. J Bone Miner Res. 2010;25:2460-2469.
86. Tintut Y, Parhami F, Tsingotjidou A, Tetradis S, Territo M, Demer LL. 8-Isoprostaglandin E2 enhances receptor-activated NFkappa B ligand (RANKL)-dependent osteoclastic potential of marrow hematopoietic precursors via the cAMP pathway. J Biol Chem. 2002;277:14221-14226. (Pubitemid 34968036)
87. Graham LS, Parhami F, Tintut Y, Kitchen CM, Demer LL, Effros RB. Oxidized lipids enhance RANKL production by T lymphocytes: implications for lipid-induced bone loss. Clin Immunol. 2009;133:265-275.
88. Huang MS, Lu J, Ivanov Y, Sage AP, Tseng W, Demer LL, Tintut Y. Hyperlipidemia impairs osteoanabolic effects of PTH. J Bone Miner Res. 2008;23:1672-1679.
89. Huang MS, Morony S, Lu J, Zhang Z, Bezouglaia O, Tseng W, Tetradis S, Demer LL, Tintut Y. Atherogenic phospholipids attenuate osteogenic signaling by BMP-2 and parathyroid hormone in osteoblasts. J Biol Chem. 2007;282:21237-21243. (Pubitemid 47099940)
90. Navab M, Anantharamaiah GM, Reddy ST, Van Lenten BJ, Fogelman AM. Apo A-1 mimetic peptides as atheroprotective agents in murine models. Curr Drug Targets. 2008;9:204-209. (Pubitemid 351843601)
91. Sage AP, Lu J, Atti E, Tetradis S, Ascenzi MG, Adams DJ, Demer LL, Tintut Y. Hyperlipidemia induces resistance to PTH bone anabolism in mice via oxidized lipids. J Bone Miner Res. 2010 Dec 15 [Epub ahead of print].
92. Hofbauer LC, Khosla S, Dunstan CR, Lacey DL, Boyle WJ, Riggs BL. The roles of osteoprotegerin and osteoprotegerin ligand in the paracrine regulation of bone resorption. J Bone Miner Res. 2000;15:2-12. (Pubitemid 30026926)
93. Lacey DL, Timms E, Tan HL, Kelley MJ, Dunstan CR, Burgess T, Elliott R, Colombero A, Elliott G, Scully S, Hsu H, Sullivan J, Hawkins N, Davy E, Capparelli C, Eli A, Qian YX, Kaufman S, Sarosi I, Shalhoub V, Senaldi G, Guo J, Delaney J, Boyle WJ. Osteoprotegerin ligand is a cytokine that regulates osteoclast differentiation and activation. Cell. 1998;93:165-176. (Pubitemid 28180851)
94. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Mochizuki S, Tomoyasu A, Yano K, Goto M, Murakami A, Tsuda E, Morinaga T, Higashio K, Udagawa N, Takahashi N, Suda T. Osteoclast differentiation factor is a ligand for osteoprotegerin/osteoclastogenesisinhibitory factor and is identical to TRANCE/RANKL. Proc Natl Acad Sci USA. 1998;95:3597-3602.
95. Simonet WS, Lacey DL, Dunstan CR, Kelley M, Chang MS, Lüthy R, Nguyen HQ, Wooden S, Bennett L, Boone T, Shimamoto G, DeRose M, Elliott R, Colombero A, Tan HL, Trail G, Sullivan J, Davy E, Bucay N, Renshaw-Gegg L, Hughes TM, Hill D, Pattison W, Campbell P, Sander S, Van G, Tarpley J, Derby P, Lee R, Boyle WJ. Osteoprotegerin: a novel secreted protein involved in the regulation of bone density. Cell. 1997;89:309-319. (Pubitemid 27199902)
96. Bu R, Borysenko CW, Li Y, Cao L, Sabokbar A, Blair HC. Expression and function of TNF-family proteins and receptors in human osteoblasts. Bone. 2003;33:760-770. (Pubitemid 37393487)
97. Lum L, Wong BR, Josien R, Becherer JD, Erdjument-Bromage H, Schlöndorff J, Tempst P, Choi Y, Blobel CP. Evidence for a role of a tumor necrosis factor-alpha (TNF-alpha)-converting enzyme-like protease in shedding of TRANCE, a TNF family member involved in osteoclastogenesis and dendritic cell survival. J Biol Chem. 1999;274:13613-13618.
98. Hsu H, Lacey DL, Dunstan CR, Solovyev I, Colombero A, Timms E, Tan HL, Elliott G, Kelley MJ, Sarosi I, Wang L, Xia XZ, Elliott R, Chiu L, Black T, Scully S, Capparelli C, Morony S, Shimamoto G, Bass MB, Boyle WJ. Tumor necrosis factor receptor family member RANK mediates osteoclast differentiation and activation induced by osteoprotegerin ligand. Proc Natl Acad Sci USA. 1999;96:3540-3545. (Pubitemid 29168945)
99. Kim HH, Shin HS, Kwak HJ, Ahn KY, Kim JH, Lee HJ, Lee MS, Lee ZH, Koh GY. RANKL regulates endothelial cell survival through the phosphatidylinositol 3 β-kinase/Akt signal transduction pathway. FASEB J. 2003;17:2163-2165.
100. Huang JC, Sakata T, Pfleger LL, Bencsik M, Halloran BP, Bikle DD, Nissenson RA. PTH differentially regulates expression of RANKL and OPG. J Bone Miner Res. 2004;19:235-244. (Pubitemid 38116737)
101. Nakagawa N, Kinosaki M, Yamaguchi K, Shima N, Yasuda H, Yano K, Morinaga T, Higashio K. RANK is the essential signaling receptor for osteoclast differentiation factor in osteoclastogenesis. Biochem Biophys Res Commun. 1998;253:395-400. (Pubitemid 29026714)
102. Yasuda H, Shima N, Nakagawa N, Yamaguchi K, Kinosaki M, Goto M, Mochizuki SI, Tsuda E, Morinaga T, Udagawa N, Takahashi N, Suda T, Higashio K. A novel molecular mechanism modulating osteoclast differentiation and function. Bone. 1999;25:109-113. (Pubitemid 29322072)
103. Matsuzaki K, Udagawa N, Takahashi N, Yamaguchi K, Yasuda H, Shima N, Morinaga T, Toyama Y, Yabe Y, Higashio K, Suda T. Osteoclast differentiation factor (ODF) induces osteoclast-like cell formation in human peripheral blood mononuclear cell cultures. Biochem Biophys Res Commun. 1998;246:199-204. (Pubitemid 28413951)
104. Tsukii K, Shima N, Mochizuki S, Yamaguchi K, Kinosaki M, Yano K, Shibata O, Udagawa N, Yasuda H, Suda T, Higashio K. Osteoclast differentiation factor mediates an essential signal for bone resorption induced by 1 alpha,25-dihydroxyvitamin D3, prostaglandin E2, or parathyroid hormone in the microenvironment of bone. Biochem Biophys Res Commun. 1998;246:337-341. (Pubitemid 28412599)
105. Anderson DM, Maraskovsky E, Billingsley WL, Dougall WC, Tometsko ME, Roux ER, Teepe MC, DuBose RF, Cosman D, Galibert L. A homologue of the TNF receptor and its ligand enhance T-cell growth and dendritic-cell function. Nature. 1997;390:175-179. (Pubitemid 27507987)
106. Kong YY, Feige U, Sarosi I, Bolon B, Tafuri A, Morony S, Capparelli C, Li J, Elliott R, McCabe S, Wong T, Campagnuolo G, Moran E, Bogoch ER, Van G, Nguyen LT, Ohashi PS, Lacey DL, Fish E, Boyle WJ, Penninger JM. Activated T cells regulate bone loss and joint destruction in adjuvant arthritis through osteoprotegerin ligand. Nature. 1999;402:304-309. (Pubitemid 129516268)
107. Dougall WC, Glaccum M, Charrier K, Rohrbach K, Brasel K, De Smedt T, Daro E, Smith J, Tometsko ME, Maliszewski CR, Armstrong A, Shen V, Bain S, Cosman D, Anderson D, Morrissey PJ, Peschon JJ, Schuh J. RANK is essential for osteoclast and lymph node development. Genes Dev. 1999;13:2412-2424. (Pubitemid 29453612)
108. Mizuno A, Kanno T, Hoshi M, Shibata O, Yano K, Fujise N, Kinosaki M, Yamaguchi K, Tsuda E, Murakami A, Yasuda H, Higashio K. Transgenic mice overexpressing soluble osteoclast differentiation factor (sODF) exhibit severe osteoporosis. J Bone Miner Metab. 2002;20:337-344. (Pubitemid 40645655)
109. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, Capparelli C, Scully S, Tan HL, Xu W, Lacey DL, Boyle WJ, Simonet WS. osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev. 1998;12:1260-1268. (Pubitemid 28213402)
110. -/-) mice. Circulation. 2008;117: 411-420.
111. Orita Y, Yamamoto H, Kohno N, Sugihara M, Honda H, Kawamata S, Mito S, Soe NN, Yoshizumi M. Role of osteoprotegerin in arterial calcification: development of new animal model. Arterioscler Thromb Vasc Biol. 2007;27:2058-2064. (Pubitemid 47312318)
112. Lieb W, Gona P, Larson MG, Massaro JM, Lipinska I, Keaney JF Jr, Rong J, Corey D, Hoffmann U, Fox CS, Vasan RS, Benjamin EJ, O'Donnell CJ, Kathiresan S. Biomarkers of the osteoprotegerin pathway: clinical correlates, subclinical disease, incident cardiovascular disease, and mortality. Arterioscler Thromb Vasc Biol. 2010;30:1849-1854.
113. Osako MK, Nakagami H, Koibuchi N, Shimizu H, Nakagami F, Koriyama H, Shimamura M, Miyake T, Rakugi H, Morishita R. Estrogen inhibits vascular calcification via vascular RANKL system: common mechanism of osteoporosis and vascular calcification. Circ Res. 107:466-475.
114. Panizo S, Cardus A, Encinas M, Parisi E, Valcheva P, López-Ongil S, Coll B, Fernandez E, Valdivielso JM. RANKL increases vascular smooth muscle cell calcification through a RANK-BMP4-dependent pathway. Circ Res. 2009;104:1041-1048.
115. Frost ML, Grella R, Millasseau SC, Jiang BY, Hampson G, Fogelman I, Chowienczyk PJ. Relationship of calcification of atherosclerotic plaque and arterial stiffness to bone mineral density and osteoprotegerin in postmenopausal women referred for osteoporosis screening. Calcif Tissue Int. 2008;83:112-120.
116. Browner WS, Lui LY, Cummings SR. Associations of serum osteoprotegerin levels with diabetes, stroke, bone density, fractures, and mortality in elderly women. J Clin Endocrinol Metab. 2001;86:631-637. (Pubitemid 32207471)
117. Jono S, Ikari Y, Shioi A, Mori K, Miki T, Hara K, Nishizawa Y. Serum osteoprotegerin levels are associated with the presence and severity of coronary artery disease. Circulation. 2002;106:1192-1194. (Pubitemid 34988634)
118. Schoppet M, Sattler AM, Schaefer JR, Herzum M, Maisch B, Hofbauer LC. Increased osteoprotegerin serum levels in men with coronary artery disease. J Clin Endocrinol Metab. 2003;88:1024-1028. (Pubitemid 36337751)
119. Brändström H, Stiger F, Lind L, Kahan T, Melhus H, Kindmark A. A single nucleotide polymorphism in the promoter region of the human gene for osteoprotegerin is related to vascular morphology and function. Biochem Biophys Res Commun. 2002;293:13-17. (Pubitemid 34694163)
120. Kiechl S, Schett G, Wenning G, Redlich K, Oberhollenzer M, Mayr A, Santer P, Smolen J, Poewe W, Willeit J. Osteoprotegerin is a risk factor for progressive atherosclerosis and cardiovascular disease. Circulation. 2004;109:2175-2180. (Pubitemid 38625393)
121. Schoppet M, Schaefer JR, Hofbauer LC. Low serum levels of soluble RANK ligand are associated with the presence of coronary artery disease in men. Circulation. 2003;107:e76;author reply e76.
122. Ueland T, Frøland SS, Bollerslev J, Aukrust P. Increased levels of biochemical markers of bone turnover in relation to persistent immune activation in common variable immunodeficiency. Eur J Clin Invest. 2001;31:72-78. (Pubitemid 32151124)
123. Kaden JJ, Bickelhaupt S, Grobholz R, Haase KK, Sarikoç A, Kiliç R, Brueckmann M, Lang S, Zahn I, Vahl C, Hagl S, Dempfle CE, Borggrefe M. Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulate aortic valve calcification. J Mol Cell Cardiol. 2004;36:57-66. (Pubitemid 38084791)
124. Tseng W, Lu J, Bishop GA, Watson AD, Sage AP, Demer L, Tintut Y. Regulation of interleukin-6 expression in osteoblasts by oxidized phospholipids. J Lipid Res. 2010;51:1010-1016.
125. -/- mice. Arterioscler Thromb Vasc Biol. 2006;26:2117-2124. (Pubitemid 44253797)
126. Min H, Morony S, Sarosi I, Dunstan CR, Capparelli C, Scully S, Van G, Kaufman S, Kostenuik PJ, Lacey DL, Boyle WJ, Simonet WS. Osteoprotegerin reverses osteoporosis by inhibiting endosteal osteoclasts and prevents vascular calcification by blocking a process resembling osteoclastogenesis. J Exp Med. 2000;192:463-474. (Pubitemid 30666247)
127. Price PA, June HH, Buckley JR, Williamson MK. Osteoprotegerin inhibits artery calcification induced by warfarin and by vitamin D. Arterioscler Thromb Vasc Biol. 2001;21:1610-1616. (Pubitemid 34215580)
128. Kim YM, Kim YM, Lee YM, Kim HS, Kim JD, Choi Y, Kim KW, Lee SY, Kwon YG. TNF-related activation-induced cytokine (TRANCE) induces angiogenesis through the activation of Src and phospholipase C (PLC) in human endothelial cells. J Biol Chem. 2002;277:6799-6805. (Pubitemid 34953061)
129. Zhang J, Fu M, Myles D, Zhu X, Du J, Cao X, Chen YE. PDGF induces osteoprotegerin expression in vascular smooth muscle cells by multiple signal pathways. FEBS Lett. 2002;521:180-184. (Pubitemid 34628481)
130. Collin-Osdoby P, Rothe L, Anderson F, Nelson M, Maloney W, Osdoby P. Receptor activator of NF-kappa B and osteoprotegerin expression by human microvascular endothelial cells, regulation by inflammatory cytokines, and role in human osteoclastogenesis. J Biol Chem. 2001;276:20659-20672.
131. Ishida A, Fujita N, Kitazawa R, Tsuruo T. Transforming growth factor-beta induces expression of receptor activator of NF-kappa B ligand in vascular endothelial cells derived from bone. J Biol Chem. 2002;277:26217-26224. (Pubitemid 34967109)
132. Dhore CR, Cleutjens JP, Lutgens E, Cleutjens KB, Geusens PP, Kitslaar PJ, Tordoir JH, Spronk HM, Vermeer C, Daemen MJ. Differential expression of bone matrix regulatory proteins in human atherosclerotic plaques. Arterioscler Thromb Vasc Biol. 2001;21:1998-2003. (Pubitemid 34219753)
133. Schoppet M, Al-Fakhri N, Franke FE, Katz N, Barth PJ, Maisch B, Preissner KT, Hofbauer LC. Localization of osteoprotegerin, tumor necrosis factor-related apoptosis-inducing ligand, and receptor activator of nuclear factor-kappaB ligand in Mönckeberg's sclerosis and atherosclerosis. J Clin Endocrinol Metab. 2004;89:4104-4112. (Pubitemid 39071519)
134. Chikatsu N, Takeuchi Y, Fukumoto S, Yano K, Fujita N, Tsuruo T, Fujita T. Clonal endothelial cells produce humoral factors that inhibit osteoclast-like cell formation in vitro. Endocr J. 2002;49:439-447. (Pubitemid 34988235)
135. Hofbauer LC, Schoppet M. Osteoprotegerin: a link between osteoporosis and arterial calcification? Lancet. 2001;358:257-259. (Pubitemid 32738960)
136. Tyson KL, Reynolds JL, McNair R, Zhang Q, Weissberg PL, Shanahan CM. Osteo/chondrocytic transcription factors and their target genes exhibit distinct patterns of expression in human arterial calcification. Arterioscler Thromb Vasc Biol. 2003;23:489-494. (Pubitemid 36337227)
137. Haynes DR, Crotti TN. Regulation of bone lysis in inflammatory diseases. Inflammopharmacology. 2003;11:323-331. (Pubitemid 38175942)
138. Bengtsson AK, Ryan EJ. Immune function of the decoy receptor osteoprotegerin. Crit Rev Immunol. 2002;22:201-215. (Pubitemid 35453704)
139. Seshasayee D, Wang H, Lee WP, Gribling P, Ross J, Van Bruggen N, Carano R, Grewal IS. A novel in vivo role for osteoprotegerin ligand in activation of monocyte effector function and inflammatory response. J Biol Chem. 2004;279:30202-30209. (Pubitemid 38937945)
140. Nakamura M, Udagawa N, Matsuura S, Mogi M, Nakamura H, Horiuchi H, Saito N, Hiraoka BY, Kobayashi Y, Takaoka K, Ozawa H, Miyazawa H, Takahashi N. Osteoprotegerin regulates bone formation through a coupling mechanism with bone resorption. Endocrinology. 2003;144:5441-5449. (Pubitemid 37476073)
141. Jeziorska M, McCollum C, Wooley DE. Observations on bone formation and remodelling in advanced atherosclerotic lesions of human carotid arteries. Virchows Arch. 1998;433:559-565. (Pubitemid 28561189)
142. Steitz SA, Speer MY, McKee MD, Liaw L, Almeida M, Yang H, Giachelli CM. Osteopontin inhibits mineral deposition and promotes regression of ectopic calcification. Am J Pathol. 2002;161:2035-2046. (Pubitemid 35434850)
143. Faust J, Lacey DL, Hunt P, Burgess TL, Scully S, Van G, Eli A, Qian Y, Shalhoub V. Osteoclast markers accumulate on cells developing from human peripheral blood mononuclear precursors. J Cell Biochem. 1999;72:67-80. (Pubitemid 28541482)
144. Scheven BA, Visser JW, Nijweide PJ. In vitro osteoclast generation from different bone marrow fractions, including a highly enriched haematopoietic stem cell population. Nature. 1986;321:79-81. (Pubitemid 16080890)
145. Merkel KD, Erdmann JM, McHugh KP, Abu-Amer Y, Ross FP, Teitelbaum SL. Tumor necrosis factor-alpha mediates orthopedic implant osteolysis. Am J Pathol. 1999;154:203-210. (Pubitemid 29031627)
146. Gerrity RG, Naito HK. Ultrastructural identification of monocytederived foam cells in fatty streak lesions. Artery. 1980;8:208-214. (Pubitemid 11154651)
147. Rosenfeld ME, Ylä-Herttuala S, Lipton BA, Ord VA, Witztum JL, Steinberg D. Macrophage colony-stimulating factor mRNA and protein in atherosclerotic lesions of rabbits and humans. Am J Pathol. 1992;140:291-300.
148. Clinton SK, Underwood R, Hayes L, Sherman ML, Kufe DW, Libby P. Macrophage colony-stimulating factor gene expression in vascular cells and in experimental and human atherosclerosis. Am J Pathol. 1992;140:301-316.
149. Ross FP, Chappel J, Alvarez JI, Sander D, Butler WT, Farach-Carson MC, Mintz KA, Robey PG, Teitelbaum SL, Cheresh DA. Interactions between the bone matrix proteins osteopontin and bone sialoprotein and the osteoclast integrin alpha v beta 3 potentiate bone resorption. J Biol Chem. 1993;268:9901-9907. (Pubitemid 23146055)
150. Matsui Y, Rittling SR, Okamoto H, Inobe M, Jia N, Shimizu T, Akino M, Sugawara T, Morimoto J, Kimura C, Kon S, Denhardt D, Kitabatake A, Uede T. Osteopontin deficiency attenuates atherosclerosis in female apolipoprotein E-deficient mice. Arterioscler Thromb Vasc Biol. 2003;23:1029-1034. (Pubitemid 36713556)
151. Doherty TM, Uzui H, Fitzpatrick LA, Tripathi PV, Dunstan CR, Asotra K, Rajavashisth TB. Rationale for the role of osteoclast-like cells in arterial calcification. FASEB J. 2002;16:577-582. (Pubitemid 34273241)
152. Mazière C, Louvet L, Gomila C, Kamel S, Massy Z, Mazière JC. Oxidized low density lipoprotein decreases Rankl-induced differentiation of osteoclasts by inhibition of Rankl signaling. J Cell Physiol. 2009;221:572-578.
153. Simpson CL, Lindley S, Eisenberg C, Basalyga DM, Starcher BC, Simionescu DT, Vyavahare NR. Toward cell therapy for vascular calcification: osteoclast-mediated demineralization of calcified elastin. Cardiovasc Pathol. 2007;16:29-37. (Pubitemid 46049030)
154. Tintut Y, Abedin M, Cho J, Choe A, Lim J, Demer LL. Regulation of RANKL-induced osteoclastic differentiation by vascular cells. J Mol Cell Cardiol. 2005;39:389-393. (Pubitemid 40995028)
155. Ragnauth CD, Warren DT, Liu Y, McNair R, Tajsic T, Figg N, Shroff R, Skepper J, Shanahan CM. Prelamin A acts to accelerate smooth muscle cell senescence and is a novel biomarker of human vascular aging. Circulation. 2010;121:2200-2210.
156. Towler DA. The osteogenic-angiogenic interface: novel insights into the biology of bone formation and fracture repair. Curr Osteoporos Rep. 2008;6:67-71.