A role for the endothelium in vascular calcification

Circulation Research

Volumn 113, Issue 5, 2013, Pages 495-504

  Yao, Yucheng ^a   Jumabay, Medet ^a   Ly, Albert ^a   Radparvar, Melina ^a   Cubberly, Mark R ^a   Boström, Kristina I ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

bone morphogenetic protein; endothelium; matrix Gla protein; progenitor cells; vascular calcification

Indexed keywords

ALKALINE PHOSPHATASE; ALPHA SMOOTH MUSCLE ACTIN; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; CADHERIN; CD31 ANTIGEN; GLUCOSE; MYOSIN HEAVY CHAIN; OSTEOCALCIN; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; TRANSGELIN; VASCULOTROPIN RECEPTOR 2; VON WILLEBRAND FACTOR; ACTIN BINDING PROTEIN; ANGIOPOIETIN RECEPTOR; CALCIUM BINDING PROTEIN; HYBRID PROTEIN; INS2 PROTEIN, MOUSE; INSULIN; MATRIX GLA PROTEIN; MUSCLE PROTEIN; SCLEROPROTEIN; SMALL INTERFERING RNA; TAGLN PROTEIN, MOUSE; TEK PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIGEN EXPRESSION; ARTERY CALCIFICATION; ARTERY ENDOTHELIUM; ARTICLE; BONE DEVELOPMENT; CELL TRANSFORMATION; CONTROLLED STUDY; DISEASE MODEL; ENDOTHELIAL MESENCHYMAL TRANSITION; ENDOTHELIUM CELL; FLUORESCENCE ACTIVATED CELL SORTING; GENE DELETION; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; MALE; MOUSE; MULTIPOTENT STEM CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; SIGNAL TRANSDUCTION; STEM CELL; ANIMAL; AORTA; C57BL MOUSE; CALCINOSIS; CELL CULTURE; CELL LINEAGE; CELL TRANSDIFFERENTIATION; CYTOLOGY; DEFICIENCY; DIABETIC ANGIOPATHY; DRUG EFFECTS; GENETICS; HETEROZYGOTE; KNOCKOUT MOUSE; NON INSULIN DEPENDENT DIABETES MELLITUS; PATHOLOGY; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE; VASCULAR DISEASE; VASCULAR ENDOTHELIUM;

ANIMALS; AORTA; CALCINOSIS; CALCIUM-BINDING PROTEINS; CELL LINEAGE; CELL TRANSDIFFERENTIATION; CELLS, CULTURED; DIABETES MELLITUS, TYPE 2; DIABETIC ANGIOPATHIES; DISEASE MODELS, ANIMAL; ENDOTHELIAL CELLS; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX PROTEINS; GLUCOSE; HETEROZYGOTE; HUMANS; INSULIN; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; MICROFILAMENT PROTEINS; MULTIPOTENT STEM CELLS; MUSCLE PROTEINS; RECEPTOR, TIE-2; RECOMBINANT FUSION PROTEINS; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; VASCULAR DISEASES;

EID: 84883458350     PISSN: 00097330     EISSN: 15244571     Source Type: Journal    
DOI: 10.1161/CIRCRESAHA.113.301792     Document Type: Article

References (43)

1. Sage AP, Tintut Y, Demer LL. Regulatory mechanisms in vascular calcification. Nat Rev Cardiol. 2010;7:528-536
2. Speer MY, Yang HY, Brabb T, Leaf E, Look A, Lin WL, Frutkin A, Dichek D, Giachelli CM. Smooth muscle cells give rise to osteochondrogenic precursors and chondrocytes in calcifying arteries. Circ Res. 2009;104:733-741
3. Medici D, Shore EM, Lounev VY, Kaplan FS, Kalluri R, Olsen BR. Conversion of vascular endothelial cells into multipotent stem-like cells. Nat Med. 2010;16:1400-1406
4. Kaplan FS, Xu M, Seemann P, et al. Classic and atypical fibrodysplasia ossificans progressiva (FOP) phenotypes are caused by mutations in the bone morphogenetic protein (BMP) type I receptor ACVR1. Hum Mutat. 2009;30:379-390
5. Dudley AC, Khan ZA, Shih SC, Kang SY, Zwaans BM, Bischoff J, Klagsbrun M. Calcification of multipotent prostate tumor endothelium. Cancer Cell. 2008;14:201-211
6. Wylie-Sears J, Aikawa E, Levine RA, Yang JH, Bischoff J. Mitral valve endothelial cells with osteogenic differentiation potential. Arterioscler Thromb Vasc Biol. 2011;31:598-607
7. Tang R, Gao M, Wu M, Liu H, Zhang X, Liu B. High glucose mediates endothelial-to-chondrocyte transition in human aortic endothelial cells. Cardiovasc Diabetol. 2012;11:113
8. Yao Y, Bennett BJ, Wang X, Rosenfeld ME, Giachelli C, Lusis AJ, Boström KI. Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ Res. 2010;107:485-494
9. Boström KI, Jumabay M, Matveyenko A, Nicholas SB, Yao Y. Activation of vascular bone morphogenetic protein signaling in diabetes mellitus. Circ Res. 2011;108:446-457
10. Derwall M, Malhotra R, Lai CS, Beppu Y, Aikawa E, Seehra JS, Zapol WM, Bloch KD, Yu PB. Inhibition of bone morphogenetic protein signaling reduces vascular calcification and atherosclerosis. Arterioscler Thromb Vasc Biol. 2012;32:613-622
11. Nakagawa Y, Ikeda K, Akakabe Y, Koide M, Uraoka M, Yutaka KT, Kurimoto-Nakano R, Takahashi T, Matoba S, Yamada H, Okigaki M, Matsubara H. Paracrine osteogenic signals via bone morphogenetic protein-2 accelerate the atherosclerotic intimal calcification in vivo. Arterioscler Thromb Vasc Biol. 2010;30:1908-1915
12. Csiszar A, Lehoux S, Ungvari Z. Hemodynamic forces, vascular oxidative stress, and regulation of BMP-2/4 expression. Antioxid Redox Signal. 2009;11:1683-1697
13. Boström KI, Rajamannan NM, Towler DA. The regulation of valvular and vascular sclerosis by osteogenic morphogens. Circ Res. 2011;109:564-577
14. Chang K, Weiss D, Suo J, Vega JD, Giddens D, Taylor WR, Jo H. Bone morphogenic protein antagonists are coexpressed with bone morphogenic protein 4 in endothelial cells exposed to unstable flow in vitro in mouse aortas and in human coronary arteries: Role of bone morphogenic protein antagonists in inflammation and atherosclerosis. Circulation. 2007;116:1258-1266
15. Yao Y, Zebboudj AF, Shao E, Perez M, Boström K. Regulation of bone morphogenetic protein-4 by matrix GLA protein in vascular endothelial cells involves activin-like kinase receptor 1. J Biol Chem. 2006;281:33921-33930
16. Yao Y, Shahbazian A, Boström KI. Proline and gamma-carboxylated glutamate residues in matrix Gla protein are critical for binding of bone morphogenetic protein-4. Circ Res. 2008;102:1065-1074
17. Yao Y, Jumabay M, Wang A, Boström KI. Matrix Gla protein deficiency causes arteriovenous malformations in mice. J Clin Invest. 2011;121:2993-3004
18. Wallin R, Cain D, Hutson SM, Sane DC, Loeser R. Modulation of the binding of matrix Gla protein (MGP) to bone morphogenetic protein-2 (BMP-2). Thromb Haemost. 2000;84:1039-1044
19. Luo G, Ducy P, McKee MD, Pinero GJ, Loyer E, Behringer RR, Karsenty G. Spontaneous calcification of arteries and cartilage in mice lacking matrix GLA protein. Nature. 1997;386:78-81
20. Yoshioka M, Kayo T, Ikeda T, Koizumi A. A novel locus, Mody4, distal to D7Mit189 on chromosome 7 determines early-onset NIDDM in nonobese C57BL/6 (Akita) mutant mice. Diabetes. 1997;46:887-894
21. Breyer MD, Böttinger E, Brosius FC 3rd, Coffman TM, Harris RC, Heilig CW, Sharma K; AMDCC. Mouse models of diabetic nephropathy. J Am Soc Nephrol. 2005;16:27-45
22. Yao Y, Nowak S, Yochelis A, Garfinkel A, Boström KI. Matrix GLA protein, an inhibitory morphogen in pulmonary vascular development. J Biol Chem. 2007;282:30131-30142
23. Motoike T, Loughna S, Perens E, Roman BL, Liao W, Chau TC, Richardson CD, Kawate T, Kuno J, Weinstein BM, Stainier DY, Sato TN. Universal GFP reporter for the study of vascular development. Genesis. 2000;28:75-81
24. Lee H, Shi W, Tontonoz P, Wang S, Subbanagounder G, Hedrick CC, Hama S, Borromeo C, Evans RM, Berliner JA, Nagy L. Role for peroxisome proliferator-activated receptor alpha in oxidized phospholipid-induced synthesis of monocyte chemotactic protein-1 and interleukin-8 by endothelial cells. Circ Res. 2000;87:516-521
25. Boström K, Tsao D, Shen S, Wang Y, Demer LL. Matrix GLA protein modulates differentiation induced by bone morphogenetic protein-2 in C3H10T1/2 cells. J Biol Chem. 2001;276:14044-14052
26. Yao Y, Bennett BJ, Wang X, Rosenfeld ME, Giachelli C, Lusis AJ, Boström KI. Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ Res. 2010;107:485-494
27. Hartley CJ, Taffet GE, Reddy AK, Entman ML, Michael LH. Noninvasive cardiovascular phenotyping in mice. ILAR J. 2002;43:147-158
28. Basu R, Oudit GY, Wang X, Zhang L, Ussher JR, Lopaschuk GD, Kassiri Z. Type 1 diabetic cardiomyopathy in the Akita (Ins2WT/C96Y) mouse model is characterized by lipotoxicity and diastolic dysfunction with preserved systolic function. Am J Physiol Heart Circ Physiol. 2009;297:H2096-H2108
29. Nasrallah R, Xiong H, Hébert RL. Renal prostaglandin E2 receptor (EP) expression profile is altered in streptozotocin and B6-Ins2Akita type I diabetic mice. Am J Physiol Renal Physiol. 2007;292:F278-F284
30. Sun Y, Byon CH, Yuan K, Chen J, Mao X, Heath JM, Javed A, Zhang K, Anderson PG, Chen Y. Smooth muscle cell-specific runx2 deficiency inhibits vascular calcification. Circ Res. 2012;111:543-552
31. Kokudo T, Suzuki Y, Yoshimatsu Y, Yamazaki T, Watabe T, Miyazono K. Snail is required for TGFbeta-induced endothelial-mesenchymal transition of embryonic stem cell-derived endothelial cells. J Cell Sci. 2008;121:3317-3324
32. Wirz W, Antoine M, Tag CG, Gressner AM, Korff T, Hellerbrand C, Kiefer P. Hepatic stellate cells display a functional vascular smooth muscle cell phenotype in a three-dimensional co-culture model with endothelial cells. Differentiation. 2008;76:784-794
33. Ding R, Darland DC, Parmacek MS, D'Amore PA. Endothelialmesenchymal interactions in vitro reveal molecular mechanisms of smooth muscle/pericyte differentiation. Stem Cells Dev. 2004;13:509-520
34. el-Labban NG, Hopper C, Barber P. Ultrastructural finding of vascular degeneration in fibrodysplasia ossificans progressiva (FOP). J Oral Pathol Med. 1995;24:125-129
35. Vicente López MA, Vázquez García MN, Entrena A, Olmedillas Lopez S, García-Arranz M, García-Olmo D, Zapata A. Low doses of bone morphogenetic protein 4 increase the survival of human adipose-derived stem cells maintaining their stemness and multipotency. Stem Cells Dev. 2011;20:1011-1019
36. Yang L, Soonpaa MH, Adler ED, Roepke TK, Kattman SJ, Kennedy M, Henckaerts E, Bonham K, Abbott GW, Linden RM, Field LJ, Keller GM. Human cardiovascular progenitor cells develop from a KDR+ embryonicstem- cell-derived population. Nature. 2008;453:524-528
37. Boyd NL, Dhara SK, Rekaya R, Godbey EA, Hasneen K, Rao RR, West FD 3rd, Gerwe BA, Stice SL. BMP4 promotes formation of primitive vascular networks in human embryonic stem cell-derived embryoid bodies. Exp Biol Med (Maywood). 2007;232:833-843
38. Alva JA, Zovein AC, Monvoisin A, Murphy T, Salazar A, Harvey NL, Carmeliet P, Iruela-Arispe ML. VE-Cadherin-Cre-recombinase transgenic mouse: A tool for lineage analysis and gene deletion in endothelial cells. Dev Dyn. 2006;235:759-767
39. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. Tie2-Cre transgenic mice: A new model for endothelial cell-lineage analysis in vivo. Dev Biol. 2001;230:230-242
40. Cho HJ, Cho HJ, Lee HJ, Song MK, Seo JY, Bae YH, Kim JY, Lee HY, Lee W, Koo BK, Oh BH, Park YB, Kim HS. Vascular calcifying progenitor cells possess bidirectional differentiation potentials. PLoS Biol. 2013;11:e1001534
41. Naik V, Leaf EM, Hu JH, Yang HY, Nguyen NB, Giachelli CM, Speer MY. Sources of cells that contribute to atherosclerotic intimal calcification: An in vivo genetic fate mapping study. Cardiovasc Res. 2012;94:545-554
42. Tang Z, Wang A, Yuan F, Yan Z, Liu B, Chu JS, Helms JA, Li S. Differentiation of multipotent vascular stem cells contributes to vascular diseases. Nat Commun. 2012;3:875
43. Boström KI, Garfinkel A, Yao Y, Jumabay M. Concise review: Applying stem cell biology to vascular structures. Stem Cells. 2012;30:386-391