TRAIL-Deficiency Accelerates Vascular Calcification in Atherosclerosis via Modulation of RANKL

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Di Bartolo, Belinda A ^a   Cartland, Siân P ^a   Harith, Hanis H ^a,b   Bobryshev, Yuri V ^a   Schoppet, Michael ^c   Kavurma, Mary M ^a  

^a UNIVERSITY OF NEW SOUTH WALES   (Australia)

^b UNIVERSITY PUTRA MALAYSIA   (Malaysia)

^c PHILIPPS UNIVERSITY MARBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN E; BONE MORPHOGENETIC PROTEIN 2; COLLAGEN TYPE 2; COMPLEMENTARY DNA; INTERLEUKIN 1BETA; MESSENGER RNA; OSTEOCLAST DIFFERENTIATION FACTOR; OSTEOPROTEGERIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; TRANSCRIPTION FACTOR RUNX2; TUMOR NECROSIS FACTOR ALPHA; TUMOR NECROSIS FACTOR RELATED APOPTOSIS INDUCING LIGAND;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; ATHEROSCLEROSIS; ATHEROSCLEROTIC PLAQUE; BLOOD VESSEL CALCIFICATION; BONE TURNOVER; BRACHIOCEPHALIC TRUNK; CARTILAGE CELL; CELL ISOLATION; CONTROLLED STUDY; DNA SYNTHESIS; HISTOPATHOLOGY; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; LIPID DIET; MOUSE; NONHUMAN; POLYMERASE CHAIN REACTION; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RNA EXTRACTION; SMOOTH MUSCLE FIBER;

ANIMALS; AORTA; APOLIPOPROTEINS E; ATHEROSCLEROSIS; BRACHIOCEPHALIC TRUNK; CALCIUM; CELLS, CULTURED; CHONDROCYTES; COLLAGEN TYPE II; DIET, HIGH-FAT; GENE EXPRESSION REGULATION; HUMANS; MICE; MICE, KNOCKOUT; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; OSTEOPROTEGERIN; PLAQUE, ATHEROSCLEROTIC; RANK LIGAND; RNA, MESSENGER; SIGNAL TRANSDUCTION; TNF-RELATED APOPTOSIS-INDUCING LIGAND; VASCULAR CALCIFICATION;

EID: 84883507476     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0074211     Document Type: Article

References (66)

1. LeGeros RZ, (2001) Formation and transformation of calcium phosphates: relevance to vascular calcification. Z Kardiol 90: 116-124.
2. Doherty TM, Asotra K, Fitzpatrick LA, Qiao JH, Wilkin DJ, et al. (2003) Calcification in atherosclerosis: bone biology and chronic inflammation at the arterial crossroads. Proceedings of the National Academy of Sciences of the United States of America 100: 11201-11206.
3. Bobryshev YV, (2005) Transdifferentiation of smooth muscle cells into chondrocytes in atherosclerotic arteries in situ: implications for diffuse intimal calcification. J Pathol 205: 641-650.
4. Doehring LC, Heeger C, Aherrahrou Z, Kaczmarek PM, Erdmann J, et al. (2010) Myeloid CD34+CD13+ precursor cells transdifferentiate into chondrocyte-like cells in atherosclerotic intimal calcification. The American journal of pathology 177: 473-480.
5. Duer MJ, Friscic T, Proudfoot D, Reid DG, Schoppet M, et al. (2008) Mineral surface in calcified plaque is like that of bone: further evidence for regulated mineralization. Arterioscler Thromb Vasc Biol 28: 2030-2034.
6. Panizo S, Cardus A, Encinas M, Parisi E, Valcheva P, et al. (2009) RANKL increases vascular smooth muscle cell calcification through a RANK-BMP4-dependent pathway. Circulation research 104: 1041-1048.
7. Speer MY, Yang HY, Brabb T, Leaf E, Look A, et al. (2009) Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circulation research 104: 733-741.
8. Sattler AM, Schoppet M, Schaefer JR, Hofbauer LC, (2004) Novel aspects on RANK ligand and osteoprotegerin in osteoporosis and vascular disease. Calcified tissue international 74: 103-106.
9. Schoppet M, Preissner KT, Hofbauer LC, (2002) RANK ligand and osteoprotegerin: paracrine regulators of bone metabolism and vascular function. Arteriosclerosis, thrombosis, and vascular biology 22: 549-553.
10. Hofbauer LC, Schoppet M, (2004) Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases. JAMA: the journal of the American Medical Association 292: 490-495.
11. Helas S, Goettsch C, Schoppet M, Zeitz U, Hempel U, et al. (2009) Inhibition of receptor activator of NF-kappaB ligand by denosumab attenuates vascular calcium deposition in mice. Am J Pathol 175: 473-478.
12. Kaden JJ, Bickelhaupt S, Grobholz R, Haase KK, Sarikoc A, et al. (2004) Receptor activator of nuclear factor kappaB ligand and osteoprotegerin regulate aortic valve calcification. Journal of molecular and cellular cardiology 36: 57-66.
13. Ndip A, Williams A, Jude EB, Serracino-Inglott F, Richardson S, et al. (2011) The RANKL/RANK/OPG signaling pathway mediates medial arterial calcification in diabetic Charcot neuroarthropathy. Diabetes 60: 2187-2196.
14. Olesen M, Skov V, Mechta M, Mumm BH, Rasmussen LM, (2012) No influence of OPG and its ligands, RANKL and TRAIL, on proliferation and regulation of the calcification process in primary human vascular smooth muscle cells. Molecular and cellular endocrinology 362: 149-156.
15. Tseng W, Graham LS, Geng Y, Reddy A, Lu J, et al. (2010) PKA-induced receptor activator of NF-kappaB ligand (RANKL) expression in vascular cells mediates osteoclastogenesis but not matrix calcification. The Journal of biological chemistry 285: 29925-29931.
16. Di Bartolo BA, Schoppet M, Mattar MZ, Rachner TD, Shanahan CM, et al. (2011) Calcium and osteoprotegerin regulate IGF1R expression to inhibit vascular calcification. Cardiovascular Research 91: 537-545.
17. Kong YY, Yoshida H, Sarosi I, Tan HL, Timms E, et al. (1999) OPGL is a key regulator of osteoclastogenesis, lymphocyte development and lymph-node organogenesis. Nature 397: 315-323.
18. Morony S, Sage AP, Corbin T, Lu J, Tintut Y, et al. (2012) Enhanced mineralization potential of vascular cells from SM22alpha-Rankl (tg) mice. Calcified tissue international 91: 379-386.
19. Volpato S, Ferrucci L, Secchiero P, Corallini F, Zuliani G, et al. (2011) Association of tumor necrosis factor-related apoptosis-inducing ligand with total and cardiovascular mortality in older adults. Atherosclerosis 215: 452-458.
20. Browner WS, Lui LY, Cummings SR, (2001) Associations of serum osteoprotegerin levels with diabetes, stroke, bone density, fractures, and mortality in elderly women. J Clin Endocrinol Metab 86: 631-637.
21. Jono S, Ikari Y, Shioi A, Mori K, Miki T, et al. (2002) Serum osteoprotegerin levels are associated with the presence and severity of coronary artery disease. Circulation 106: 1192-1194.
22. Schoppet M, Sattler AM, Schaefer JR, Herzum M, Maisch B, et al. (2003) Increased osteoprotegerin serum levels in men with coronary artery disease. J Clin Endocrinol Metab 88: 1024-1028.
23. Schoppet M, Schaefer JR, Hofbauer LC (2003) Low serum levels of soluble RANK ligand are associated with the presence of coronary artery disease in men. Circulation 107: e76; author reply e76.
24. Kavurma MM, Bennett MR, (2008) Expression, regulation and function of trail in atherosclerosis. Biochem Pharmacol 75: 1441-1450.
25. Wiley SR, (1995) Schooley K, Smolak PJ, Din WS, Huang CP, et al (1995) Identification and characterization of a new member of the TNF family that induces apoptosis. Immunity 2: 673-682.
26. Azahri NS, Kavurma MM (2013) Transcriptional regulation of tumour necrosis factor-related apoptosis-inducing ligand. Cellular and molecular life sciences. doi: 10.1007/s00018-013-1264-x.
27. Kavurma MM, Tan NY, Bennett MR, (2008) Death receptors and their ligands in atherosclerosis. Arterioscler Thromb Vasc Biol 28: 1694-1702.
28. Azijli K, Weyhenmeyer B, Peters GJ, de Jong S, Kruyt FAE, (2013) Non-canonical kinase signaling by the death ligand TRAIL in cancer cells: discord in the death receptor family. Cell Death and Differentiation 20: 858-868.
29. Di Bartolo BA, Chan J, Bennett MR, Cartland S, Bao S, et al. (2011) TNF-related apoptosis-inducing ligand (TRAIL) protects against diabetes and atherosclerosis in Apoe (-/-) mice. Diabetologia 54: 3157-3167.
30. Schoppet M, Al-Fakhri N, Franke FE, Katz N, Barth PJ, et al. (2004) Localization of osteoprotegerin, tumor necrosis factor-related apoptosis-inducing ligand, and receptor activator of nuclear factor-kappaB ligand in Monckeberg's sclerosis and atherosclerosis. J Clin Endocrinol Metab 89: 4104-4112.
31. Liu X, Winrow VR, Horrocks M, Stevens CR, (2007) Differential expression of TRAIL and its receptors relative to calcification in AAA. Biochemical and biophysical research communications 358: 18-23.
32. Chasseraud M, Liabeuf S, Mozar A, Mentaverri R, Brazier M, et al. (2011) Tumor necrosis factor-related apoptosis-inducing ligand and vascular calcification. Therapeutic apheresis and dialysis: official peer-reviewed journal of the International Society for Apheresis, the Japanese Society for Apheresis, the Japanese Society for Dialysis Therapy 15: 140-146.
33. Azahri NS, Di Bartolo BA, Khachigian LM, Kavurma MM, (2012) Sp1, acetylated histone-3 and p300 regulate TRAIL transcription: Mechanisms for PDGF-BB-mediated VSMC proliferation and migration. Journal of cellular biochemistry 113(8): 2597-2606.
34. Gregory CA, Gunn WG, Peister A, Prockop DJ, (2004) An Alizarin red-based assay of mineralization by adherent cells in culture: comparison with cetylpyridinium chloride extraction. Anal Biochem 329: 77-84.
35. Al-Fakhri N, Hofbauer LC, Preissner KT, Franke FE, Schoppet M, (2005) Expression of bone-regulating factors osteoprotegerin (OPG) and receptor activator of NF-kappaB ligand (RANKL) in heterotopic vascular ossification. Thrombosis and haemostasis 94: 1335-1337.
36. Rattazzi M, Bennett BJ, Bea F, Kirk EA, Ricks JL, et al. (2005) Calcification of advanced atherosclerotic lesions in the innominate arteries of ApoE-deficient mice: potential role of chondrocyte-like cells. Arteriosclerosis, thrombosis, and vascular biology 25: 1420-1425.
37. DeLise AM, Fischer L, Tuan RS, (2000) Cellular interactions and signaling in cartilage development. Osteoarthritis and cartilage/OARS, Osteoarthritis Research Society 8: 309-334.
38. Allison MA, Criqui MH, Wright CM, (2004) Patterns and risk factors for systemic calcified atherosclerosis. Arteriosclerosis, thrombosis, and vascular biology 24: 331-336.
39. Hruska KA, Mathew S, Saab G, (2005) Bone morphogenetic proteins in vascular calcification. Circulation research 97: 105-114.
40. Johnson RC, Leopold JA, Loscalzo J, (2006) Vascular calcification: pathobiological mechanisms and clinical implications. Circulation research 99: 1044-1059.
41. Lee MH, Kim YJ, Kim HJ, Park HD, Kang AR, et al. (2003) BMP-2-induced Runx2 expression is mediated by Dlx5, and TGF-beta 1 opposes the BMP-2-induced osteoblast differentiation by suppression of Dlx5 expression. The Journal of biological chemistry 278: 34387-34394.
42. Byon CH, Sun Y, Chen J, Yuan K, Mao X, et al. (2011) Runx2-upregulated receptor activator of nuclear factor kappaB ligand in calcifying smooth muscle cells promotes migration and osteoclastic differentiation of macrophages. Arteriosclerosis, thrombosis, and vascular biology 31: 1387-1396.
43. Susperregui AR, Vinals F, Ho PW, Gillespie MT, Martin TJ, et al. (2008) BMP-2 regulation of PTHrP and osteoclastogenic factors during osteoblast differentiation of C2C12 cells. Journal of cellular physiology 216: 144-152.
44. Lencel P, Delplace S, Pilet P, Leterme D, Miellot F, et al. (2011) Cell-specific effects of TNF-alpha and IL-1beta on alkaline phosphatase: implication for syndesmophyte formation and vascular calcification. Lab Invest 91: 1434-1442.
45. Wan Y, Chong LW, Evans RM, (2007) PPAR-gamma regulates osteoclastogenesis in mice. Nature medicine 13: 1496-1503.
46. Bucay N, Sarosi I, Dunstan CR, Morony S, Tarpley J, et al. (1998) osteoprotegerin-deficient mice develop early onset osteoporosis and arterial calcification. Genes Dev 12: 1260-1268.
47. Morony S, Tintut Y, Zhang Z, Cattley RC, Van G, et al. (2008) Osteoprotegerin inhibits vascular calcification without affecting atherosclerosis in ldlr(-/-) mice. Circulation 117: 411-420.
48. Price PA, June HH, Buckley JR, Williamson MK, (2001) Osteoprotegerin inhibits artery calcification induced by warfarin and by vitamin D. Arteriosclerosis, thrombosis, and vascular biology 21: 1610-1616.
49. Osako MK, Nakagami H, Koibuchi N, Shimizu H, Nakagami F, et al. (2010) Estrogen inhibits vascular calcification via vascular RANKL system: common mechanism of osteoporosis and vascular calcification. Circulation research 107: 466-475.
50. Wittrant Y, Lamoureux F, Mori K, Riet A, Kamijo A, et al. (2006) RANKL directly induces bone morphogenetic protein-2 expression in RANK-expressing POS-1 osteosarcoma cells. International journal of oncology 28: 261-269.
51. Goldring SR, Goldring MB (2004) The role of cytokines in cartilage matrix degeneration in osteoarthritis. Clinical orthopaedics and related research: S27-36.
52. Breuil V, Schmid-Antomarchi H, Schmid-Alliana A, Rezzonico R, Euller-Ziegler L, et al. (2003) The receptor activator of nuclear factor (NF)-kappaB ligand (RANKL) is a new chemotactic factor for human monocytes. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 17: 1751-1753.
53. Collin-Osdoby P, Rothe L, Anderson F, Nelson M, Maloney W, et al. (2001) Receptor activator of NF-kappa B and osteoprotegerin expression by human microvascular endothelial cells, regulation by inflammatory cytokines, and role in human osteoclastogenesis. The Journal of biological chemistry 276: 20659-20672.
54. Braam LA, Dissel P, Gijsbers BL, Spronk HM, Hamulyak K, et al. (2000) Assay for human matrix gla protein in serum: potential applications in the cardiovascular field. Arteriosclerosis, thrombosis, and vascular biology 20: 1257-1261.
55. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, et al. (1997) Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature 386: 78-81.
56. Mody N, Tintut Y, Radcliff K, Demer LL, (2003) Vascular calcification and its relation to bone calcification: possible underlying mechanisms. Journal of nuclear cardiology: official publication of the American Society of Nuclear Cardiology 10: 177-183.
57. Collin-Osdoby P, (2004) Regulation of vascular calcification by osteoclast regulatory factors RANKL and osteoprotegerin. Circ Res 95: 1046-1057.
58. Fu M, Zhang J, Lin Yg Y, Zhu X, Willson TM, et al. (2002) Activation of peroxisome proliferator-activated receptor gamma inhibits osteoprotegerin gene expression in human aortic smooth muscle cells. Biochemical and biophysical research communications 294: 597-601.
59. Yuan LQ, Zhu JH, Wang HW, Liang QH, Xie H, et al. (2011) RANKL is a downstream mediator for insulin-induced osteoblastic differentiation of vascular smooth muscle cells. PLoS One 6: e29037.
60. Zauli G, Rimondi E, Nicolin V, Melloni E, Celeghini C, et al. (2004) TNF-related apoptosis-inducing ligand (TRAIL) blocks osteoclastic differentiation induced by RANKL plus M-CSF. Blood 104: 2044-2050.
61. Lee SW, Lee HJ, Chung WT, Choi SM, Rhyu SH, et al. (2004) TRAIL induces apoptosis of chondrocytes and influences the pathogenesis of experimentally induced rat osteoarthritis. Arthritis Rheum 50: 534-542.
62. Chan J, Prado-Lourenco L, Khachigian LM, Bennett MR, Di Bartolo BA, et al. (2010) TRAIL promotes VSMC proliferation and neointima formation in a FGF-2-, Sp1 phosphorylation-, and NFkappaB-dependent manner. Circ Res 106: 1061-1071.
63. Kavurma MM, Schoppet M, Bobryshev YV, Khachigian LM, Bennett MR, (2008) Trail stimulates proliferation of vascular smooth muscle cells via activation of NF-kappa B and induction of insulin-like growth factor-1 receptor. J Biol Chem 283: 7754-7762.
64. Hameed AG, Arnold ND, Chamberlain J, Pickworth JA, Paiva C, et al. (2012) Inhibition of tumor necrosis factor-related apoptosis-inducing ligand (TRAIL) reverses experimental pulmonary hypertension. The Journal of experimental medicine 209: 1919-1935.
65. Secchiero P, Candido R, Corallini F, Zacchigna S, Toffoli B, et al. (2006) Systemic tumor necrosis factor-related apoptosis-inducing ligand delivery shows antiatherosclerotic activity in apolipoprotein E-null diabetic mice. Circulation 114: 1522-1530.
66. Sato K, Niessner A, Kopecky SL, Frye RL, Goronzy JJ, et al. (2006) TRAIL-expressing T cells induce apoptosis of vascular smooth muscle cells in the atherosclerotic plaque. J Exp Med 203: 239-250.