Nuclear factor of activated T cells mediates oxidised LDL-induced calcification of vascular smooth muscle cells

Diabetologia

Volumn 54, Issue 10, 2011, Pages 2690-2701

  Goettsch, C ^a   Rauner, M ^a   Hamann, C ^b   Sinningen, K ^a   Hempel, U ^b   Bornstein, S R ^a,c   Hofbauer, L C ^a,c  

^a DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c CENTER FOR REGENERATIVE THERAPIES DRESDEN   (Germany)

Author keywords

Diabetes; Matrix mineralisation; NFAT; Osteogenic transformation; Oxidative stress; oxLDL; RUNX2; Vascular calcification

Indexed keywords

GLUCOSE; MESSENGER RNA; NUCLEAR FACTOR; OXIDIZED LOW DENSITY LIPOPROTEIN; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR NFAT; TRANSCRIPTION FACTOR RUNX2;

ARTICLE; BLOOD VESSEL CALCIFICATION; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; DIABETES MELLITUS; GLUCOSE BLOOD LEVEL; HUMAN; HUMAN CELL; LYMPHOCYTE ACTIVATION; NONHUMAN; OSTEOBLAST; OSTEOLYSIS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RAT; SMOOTH MUSCLE FIBER; T LYMPHOCYTE; VASCULAR SMOOTH MUSCLE;

ANIMALS; CALCINOSIS; CELL DIFFERENTIATION; CELL SURVIVAL; CELLS, CULTURED; CORE BINDING FACTOR ALPHA 1 SUBUNIT; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; LIPOPROTEINS, LDL; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; NFATC TRANSCRIPTION FACTORS; OLIGOPEPTIDES; OSTEOBLASTS; OXIDATIVE STRESS; RATS; RATS, ZUCKER; REAL-TIME POLYMERASE CHAIN REACTION;

EID: 80054097795     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2219-0     Document Type: Article

References (48)

1. LC Hofbauer CC Brueck CM Shanahan M Schoppet H Dobnig 2007 Vascular calcification and osteoporosis-from clinical observation towards molecular understanding Osteoporos Int 18 251 259 17151836 10.1007/s00198-006-0282-z 1:CAS:528:DC%2BD2sXhsV2jsL0%3D (Pubitemid 46233170)
2. LL Demer Y Tintut 2009 Mechanisms linking osteoporosis with cardiovascular calcification Curr Osteoporos Rep 7 42 46 19631027 10.1007/s11914-009-0008-1
3. WJ Jeffcoate LM Rasmussen LC Hofbauer FL Game 2009 Medial arterial calcification in diabetes and its relationship to neuropathy Diabetologia 52 2478 2488 19756483 10.1007/s00125-009-1521-6 1:CAS:528:DC%2BD1MXhsVWls7jI
4. LC Hofbauer U Zeitz M Schoppet, et al. 2009 Prevention of glucocorticoid-induced bone loss in mice by inhibition of RANKL Arthritis Rheum 60 1427 1437 19404943 10.1002/art.24445
5. S Helas C Goettsch M Schoppet, 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 19590040 10.2353/ajpath.2009.080957 1:CAS:528:DC%2BD1MXhtVGqtrvI
6. MJ Duer T Friscic D Proudfoot, 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 18703777 10.1161/ATVBAHA.108.172387 1:CAS:528:DC%2BD1cXht1GgtbzK
7. M Liberman E Bassi MK Martinatti, et al. 2008 Oxidant generation predominates around calcifying foci and enhances progression of aortic valve calcification Arterioscler Thromb Vasc Biol 28 463 470 18162610 10.1161/ATVBAHA.107.156745 1:CAS:528:DC%2BD1cXit1Olsb0%3D
8. S Panizo A Cardus M Encinas, et al. 2009 RANKL increases vascular smooth muscle cell calcification through a RANK-BMP4-dependent pathway Circ Res 104 1041 1048 19325147 10.1161/CIRCRESAHA.108.189001 1:CAS:528:DC%2BD1MXltFelsLc%3D
9. E Aikawa M Nahrendorf JL Figueiredo, et al. 2007 Osteogenesis associates with inflammation in early-stage atherosclerosis evaluated by molecular imaging in vivo Circulation 116 2841 2850 18040026 10.1161/CIRCULATIONAHA.107.732867 1:CAS:528:DC%2BD1cXosVyiug%3D%3D (Pubitemid 350301146)
10. LC Hofbauer M Schoppet 2004 Clinical implications of the osteoprotegerin/RANKL/RANK system for bone and vascular diseases JAMA 292 490 495 15280347 10.1001/jama.292.4.490 1:CAS:528:DC%2BD2cXmtFOmsbw%3D (Pubitemid 38988958)
11. SA Steitz MY Speer G Curinga, et al. 2001 Smooth muscle cell phenotypic transition associated with calcification: upregulation of Cbfa1 and downregulation of smooth muscle lineage markers Circ Res 89 1147 1154 11739279 10.1161/hh2401.101070 1:CAS:528:DC%2BD3MXptFKmtrs%3D (Pubitemid 34627872)
12. Y Tintut J Patel F Parhami LL Demer 2000 Tumor necrosis factor-alpha promotes in vitro calcification of vascular cells via the cAMP pathway Circulation 102 2636 2642 11085968 1:CAS:528:DC%2BD3cXptVSjt7o%3D
13. LC Hofbauer J Schrader U Niebergall, et al. 2006 Interleukin-4 differentially regulates osteoprotegerin expression and induces calcification in vascular smooth muscle cells Thromb Haemost 95 708 714 16601843 1:CAS:528:DC%2BD28XksFWqs7c%3D
14. MY Speer HY Yang T Brabb, et al. 2009 Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries Circ Res 104 733 741 19197075 10.1161/CIRCRESAHA.108.183053 1:CAS:528: DC%2BD1MXjt1Khtbg%3D
15. RK Ambasta P Kumar KK Griendling HH Schmidt R Busse RP Brandes 2004 Direct interaction of the novel Nox proteins with p22phox is required for the formation of a functionally active NADPH oxidase J Biol Chem 279 45935 45941 15322091 10.1074/jbc.M406486200 1:CAS:528:DC%2BD2cXovVCnt78%3D (Pubitemid 39491586)
16. C Goettsch W Goettsch G Muller J Seebach HJ Schnittler H Morawietz 2009 Nox4 overexpression activates reactive oxygen species and p38 MAPK in human endothelial cells Biochem Biophys Res Commun 380 355 360 19280689 10.1016/j.bbrc.2009.01.107 1:CAS:528:DC%2BD1MXitlajsLg%3D
17. S Kopprasch J Pietzsch E Kuhlisch, et al. 2002 In vivo evidence for increased oxidation of circulating LDL in impaired glucose tolerance Diabetes 51 3102 3106 12351454 10.2337/diabetes.51.10.3102 1:CAS:528:DC%2BD38XnslGhsb8%3D
18. S Kopprasch J Pietzsch I Ansurudeen, et al. 2009 Prediabetic and diabetic in vivo modification of circulating low-density lipoprotein attenuates its stimulatory effect on adrenal aldosterone and cortisol secretion J Endocrinol 200 45 52 18835979 10.1677/JOE-08-0293 1:CAS:528:DC%2BD1MXjvVOgtLg%3D
19. F Parhami AD Morrow J Balucan, et al. 1997 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 17 680 687 9108780 10.1161/01.ATV.17.4. 680 1:CAS:528:DyaK2sXjtVajsr8%3D (Pubitemid 27169128)
20. N Mody F Parhami TA Sarafian LL Demer 2001 Oxidative stress modulates osteoblastic differentiation of vascular and bone cells Free Radic Biol Med 31 509 519 11498284 10.1016/S0891-5849(01)00610-4 1:CAS:528:DC%2BD3MXlslGnur4%3D (Pubitemid 32728438)
21. M Bear M Butcher SG Shaughnessy 2008 Oxidized low-density lipoprotein acts synergistically with beta-glycerophosphate to induce osteoblast differentiation in primary cultures of vascular smooth muscle cells J Cell Biochem 105 185 193 18461557 10.1002/jcb.21812 1:CAS:528:DC%2BD1cXhtFGns7zM
22. J Yan SE Stringer A Hamilton, et al. 2011 Decorin GAG synthesis and TGF-beta signaling mediate Ox-LDL-induced mineralization of human vascular smooth muscle cells Arterioscler Thromb Vasc Biol 31 608 615 21205989 10.1161/ATVBAHA.110.220749 1:CAS:528:DC%2BC3MXitVOgurk%3D
23. WM Flanagan B Corthesy RJ Bram GR Crabtree 1991 Nuclear association of a T cell transcription factor blocked by FK-506 and cyclosporin A Nature 352 803 807 1715516 10.1038/352803a0 1:CAS:528:DyaK3MXlvFOqtLw%3D (Pubitemid 21912434)
24. C Maziere P Morliere Z Massy, et al. 2005 Oxidized low-density lipoprotein elicits an intracellular calcium rise and increases the binding activity of the transcription factor NFAT Free Radic Biol Med 38 472 480 15649649 10.1016/j.freeradbiomed.2004.10.028 1:CAS:528:DC%2BD2MXkvFeksg%3D%3D (Pubitemid 40247437)
25. H Yu TJ van Berkel EA Biessen 2007 Therapeutic potential of VIVIT, a selective peptide inhibitor of nuclear factor of activated T cells, in cardiovascular disorders Cardiovasc Drug Rev 25 175 187 17614939 10.1111/j.1527-3466.2007.00011.x 1:CAS:528:DC%2BD2sXht12kurvK (Pubitemid 47035428)
26. A Alexopoulos V Bravou S Peroukides, et al. 2010 Bone regulatory factors NFATc1 and Osterix in human calcific aortic valves Int J Cardiol 139 142 149 19019468 10.1016/j.ijcard.2008.10.014
27. M Rauner W Sipos C Goettsch, et al. 2009 Inhibition of lamin A/C attenuates osteoblast differentiation and enhances RANKL-dependent osteoclastogenesis J Bone Miner Res 24 78 86 18767923 10.1359/jbmr.080902 1:CAS:528:DC%2BD1MXht1yrtb0%3D
28. M Rauner C Goettsch N Stein, et al. 2011 Dissociation of osteogenic and immunological effects by the selective glucocorticoid receptor agonist, compound A, in human bone marrow stromal cells Endocrinology 152 103 112 21084452 10.1210/en.2010-0456 1:CAS:528:DC%2BC3MXitVCisrc%3D
29. J Aramburu MB Yaffe C Lopez-Rodriguez LC Cantley PG Hogan A Rao 1999 Affinity-driven peptide selection of an NFAT inhibitor more selective than cyclosporin A Science 285 2129 2133 10497131 10.1126/science.285.5436.2129 1:CAS:528:DyaK1MXmt12jtLY%3D (Pubitemid 29451431)
30. AP Sanchez K Sharma 2009 Transcription factors in the pathogenesis of diabetic nephropathy Expert Rev Mol Med 11 e13 19397838 10.1017/ S1462399409001057
31. LM Nilsson-Berglund AV Zetterqvist J Nilsson-Ohman, et al. 2010 Nuclear factor of activated T cells regulates osteopontin expression in arterial smooth muscle in response to diabetes-induced hyperglycemia Arterioscler Thromb Vasc Biol 30 218 224 19965778 10.1161/ATVBAHA.109.199299 1:CAS:528: DC%2BC3cXlslansQ%3D%3D
32. J Nilsson LM Nilsson YW Chen JD Molkentin D Erlinge MF Gomez 2006 High glucose activates nuclear factor of activated T cells in native vascular smooth muscle Arterioscler Thromb Vasc Biol 26 794 800 16469950 10.1161/01.ATV. 0000209513.00765.13 1:CAS:528:DC%2BD28XitlKmtbo%3D (Pubitemid 43732153)
33. M Karpurapu D Wang D van Quyen, et al. 2010 Cyclin D1 is a bona fide target gene of NFATc1 and is sufficient in the mediation of injury-induced vascular wall remodeling J Biol Chem 285 3510 3523 19933579 10.1074/jbc.M109. 063727 1:CAS:528:DC%2BC3cXovVeqtg%3D%3D
34. Z Liu C Zhang N Dronadula Q Li GN Rao 2005 Blockade of nuclear factor of activated T cells activation signaling suppresses balloon injury-induced neointima formation in a rat carotid artery model J Biol Chem 280 14700 14708 15681847 10.1074/jbc.M500322200 1:CAS:528:DC%2BD2MXjtFSmu78%3D (Pubitemid 40562817)
35. SC Schafer T Wallerath EI Closs, et al. 2005 Dexamethasone suppresses eNOS and CAT-1 and induces oxidative stress in mouse resistance arterioles Am J Physiol Heart Circ Physiol 288 H436 H444 15598872 10.1152/ajpheart.00587.2004 1:STN:280:DC%2BD2cnitlSltA%3D%3D (Pubitemid 40023876)
36. S Muzaffar N Shukla GD Angelini JY Jeremy 2005 Prednisolone augments superoxide formation in porcine pulmonary artery endothelial cells through differential effects on the expression of nitric oxide synthase and NADPH oxidase Br J Pharmacol 145 688 697 15852033 10.1038/sj.bjp.0706235 1:CAS:528:DC%2BD2MXlslWhsbk%3D (Pubitemid 41032641)
37. T Sutra M Morena AS Bargnoux B Caporiccio B Canaud JP Cristol 2008 Superoxide production: a procalcifying cell signalling event in osteoblastic differentiation of vascular smooth muscle cells exposed to calcification media Free Radic Res 42 789 797 19051077 10.1080/10715760802400766 1:CAS:528:DC%2BD1cXhsVCnurbJ
38. RE Clempus KK Griendling 2006 Reactive oxygen species signaling in vascular smooth muscle cells Cardiovasc Res 71 216 225 16616906 10.1016/j.cardiores.2006.02.033 1:CAS:528:DC%2BD28Xmt1ygsrg%3D
39. C Stielow RA Catar G Muller, et al. 2006 Novel Nox inhibitor of oxLDL-induced reactive oxygen species formation in human endothelial cells Biochem Biophys Res Commun 344 200 205 16603125 10.1016/j.bbrc.2006.03.114 1:CAS:528:DC%2BD28XjvFWnsLs%3D
40. JD Miller Y Chu RM Brooks WE Richenbacher R Pena-Silva DD Heistad 2008 Dysregulation of antioxidant mechanisms contributes to increased oxidative stress in calcific aortic valvular stenosis in humans J Am Coll Cardiol 52 843 850 18755348 10.1016/j.jacc.2008.05.043 1:CAS:528:DC%2BD1cXhtVKju7jK
41. MA Hofmann Bowman J Gawdzik U Bukhari, et al. 2011 S100A12 in vascular smooth muscle accelerates vascular calcification in apolipoprotein E-null mice by activating an osteogenic gene regulatory program Arterioscler Thromb Vasc Biol 31 337 344 20966394 10.1161/ATVBAHA.110.217745 1:CAS:528: DC%2BC3MXnvVWjtg%3D%3D
42. I Takac K Schroder L Zhang, et al. 2011 The E-loop is involved in hydrogen peroxide formation by the NADPH oxidase Nox4 J Biol Chem 286 13304 13313 21343298 10.1074/jbc.M110.192138 1:CAS:528:DC%2BC3MXksVKmtLs%3D
43. K Schroder K Wandzioch I Helmcke RP Brandes 2009 Nox4 acts as a switch between differentiation and proliferation in preadipocytes Arterioscler Thromb Vasc Biol 29 239 245 19057021 10.1161/ATVBAHA.108.174219
44. A Bas I Lopez J Perez M Rodriguez E Aguilera-Tejero 2006 Reversibility of calcitriol-induced medial artery calcification in rats with intact renal function J Bone Miner Res 21 484 490 16491297 10.1359/JBMR.051211 1:CAS:528:DC%2BD28XisFGqu74%3D
45. C Maziere L Louvet C Gomila S Kamel Z Massy JC Maziere 2009 Oxidized low density lipoprotein decreases Rankl-induced differentiation of osteoclasts by inhibition of Rankl signaling J Cell Physiol 221 572 578 19725047 10.1002/jcp.21886 1:CAS:528:DC%2BD1MXhtF2qtb%2FM
46. JB Clark CJ Palmer WN Shaw 1983 The diabetic Zucker fatty rat Proc Soc Exp Biol Med 173 68 75 6344096 1:CAS:528:DyaL3sXitFeksb4%3D (Pubitemid 13088195)
47. P Holvoet NS Jenny PJ Schreiner RP Tracy DR Jacobs 2007 The relationship between oxidized LDL and other cardiovascular risk factors and subclinical CVD in different ethnic groups: the Multi-Ethnic Study of Atherosclerosis (MESA) Atherosclerosis 194 245 252 16982059 10.1016/j.atherosclerosis.2006.08.002 1:CAS:528:DC%2BD2sXhtFWisb3K (Pubitemid 47464304)
48. DA Towler M Bidder T Latifi T Coleman CF Semenkovich 1998 Diet-induced diabetes activates an osteogenic gene regulatory program in the aortas of low density lipoprotein receptor-deficient mice J Biol Chem 273 30427 30434 9804809 10.1074/jbc.273.46.30427 1:CAS:528:DyaK1cXnsVyrurg%3D (Pubitemid 28545516)