Bone morphogenetic protein 6 and oxidized low-density lipoprotein synergistically recruit osteogenic differentiation in endothelial cells

Cardiovascular Research

Volumn 108, Issue 2, 2015, Pages 278-287

  Yung, Lai Ming ^a   Sánchez Duffhues, Gonzalo ^b   Ten Dijke, Peter ^b   Yu, Paul B ^a  

^a BRIGHAM AND WOMEN S HOSPITAL   (United States)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Atherosclerosis; Bone morphogenetic protein; Endothelial cells; Oxidative stress; Oxidized low density lipoprotein

Indexed keywords

ALKALINE PHOSPHATASE; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 6; BONE MORPHOGENETIC PROTEIN 9; BONE MORPHOGENETIC PROTEIN RECEPTOR 1; HYDROGEN PEROXIDE; MESSENGER RNA; OSTEOPONTIN; OXIDIZED LOW DENSITY LIPOPROTEIN; REACTIVE OXYGEN METABOLITE; SMAD1 PROTEIN; SMAD5 PROTEIN; SMAD8 PROTEIN; TRANSCRIPTION FACTOR MSX2; TRANSCRIPTION FACTOR OSTERIX; TRANSCRIPTION FACTOR RUNX2; LOW DENSITY LIPOPROTEIN;

ANIMAL CELL; ARTICLE; BONE DEVELOPMENT; CELL DIFFERENTIATION; CONTROLLED STUDY; ENZYME ACTIVITY; EPITHELIAL MESENCHYMAL TRANSITION; IMMUNOFLUORESCENCE; MINERALIZATION; NONHUMAN; OXIDATIVE STRESS; PHENOTYPIC PLASTICITY; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UPREGULATION; VASCULAR ENDOTHELIUM; ANIMAL; BOVINE; CELL LINE; ENDOTHELIUM CELL; HUMAN; METABOLISM; PHYSIOLOGY; VASCULAR CALCIFICATION;

ANIMALS; BONE MORPHOGENETIC PROTEIN 6; CATTLE; CELL DIFFERENTIATION; CELL LINE; ENDOTHELIAL CELLS; HUMANS; LIPOPROTEINS, LDL; OSTEOGENESIS; VASCULAR CALCIFICATION;

EID: 84947587287     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvv221     Document Type: Article

References (53)

1. Elkeles RS. Coronary artery calcium and cardiovascular risk in diabetes. Atherosclerosis 2010;210:331-336.
2. Mizobuchi M, Towler D, Slatopolsky E. Vascular calcification: the killer of patients with chronic kidney disease. J Am Soc Nephrol 2009;20:1453-1464.
3. Ketteler M, Gross ML, Ritz E. Calcification and cardiovascular problems in renal failure. Kidney Int Suppl 2005;67:S120-S127.
4. Dalfino G, Simone S, Porreca S, Cosola C, Balestra C, Manno C, Schena FP, Grandaliano G, Pertosa G. Bone morphogenetic protein-2 may represent the molecular link between oxidative stress and vascular stiffness in chronic kidney disease. Atherosclerosis 2010;211:418-423.
5. Parhami F, Basseri B, Hwang J, Tintut Y, Demer LL. High-density lipoprotein regulates calcification of vascular cells. Circ Res 2002;91:570-576.
6. Hruska KA, Mathew S, Saab G. Bone morphogenetic proteins in vascular calcification. Circ Res 2005;97:105-114.
7. Bobik A. Transforming growth factor-betas and vascular disorders. Arterioscler Thromb Vasc Biol 2006;26:1712-1720.
8. Cai J, Pardali E, Sanchez-Duffhues G, ten Dijke P. BMP signaling in vascular diseases. FEBS Lett 2012;586:1993-2002.
9. Waite KA, Eng C. From developmental disorder to heritable cancer: it's all in the BMP/TGF-beta family. Nat Rev Genet 2003;4:763-773.
10. Bostrom K, Watson KE, Horn S, Wortham C, Herman IM, Demer LL. Bone morphogenetic protein expression in human atherosclerotic lesions. J ClinInvest1993;91:1800-1809.
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. Bostrom 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.
13. Zebboudj AF, Imura M, Bostrom K. Matrix GLA protein, a regulatory protein for bone morphogenetic protein-2. J Biol Chem 2002;277:4388-4394.
14. Yao Y, Bennett BJ, Wang X, Rosenfeld ME, Giachelli C, Lusis AJ, Bostrom KI. Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ Res 2010;107:485-494.
15. 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.
16. Liberman M, Johnson RC, Handy DE, Loscalzo J, Leopold JA. Bone morphogenetic protein-2 activates NADPH oxidase to increase endoplasmic reticulum stress and human coronary artery smooth muscle cell calcification. Biochem Biophys Res Commun 2011;413:436-441.
17. Yao Y, Jumabay M, Ly A, Radparvar M, Cubberly MR, Bostrom KI. A role for the endothelium in vascular calcification. Circ Res 2013;113:495-504.
18. 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.
19. 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.
20. 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.
21. 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.
22. Byon CH, Sun Y, Chen J, Yuan K, Mao X, Heath JM, Anderson PG, Tintut Y, Demer LL, Wang D, Chen Y. Runx2-upregulated receptor activator of nuclear factor kappaB ligand in calcifying smooth muscle cells promotes migration and osteoclastic differentiation of macrophages. Arterioscler Thromb Vasc Biol 2011;31:1387-1396.
23. Kocher O, Madri JA. Modulation of actin mRNAs in cultured vascular cells by matrix components and TGF-beta 1. In Vitro Cell Dev Biol 1989;25:424-434.
24. Yu PB, Deng DY, Lai CS, Hong CC, Cuny GD, Bouxsein ML, Hong DW, McManus PM, Katagiri T, Sachidanandan C, Kamiya N, Fukuda T, Mishina Y, Peterson RT, Bloch KD. BMP type I receptor inhibition reduces heterotopic ossification. Nat Med 2008;14:1363-1369.
25. Cuny GD, Yu PB, Laha JK, Xing X, Liu JF, Lai CS, Deng DY, Sachidanandan C, Bloch KD, Peterson RT. Structure-activity relationship study of bone morphogenetic protein (BMP) signaling inhibitors. Bioorg Med Chem Lett 2008;18:4388-4392.
26. 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.
27. 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.
28. Parhami F, Bostrom K, Watson K, Demer LL. Role of molecular regulation in vascular calcification. J Atheroscler Thromb 1996;3:90-94.
29. 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.
30. Camenisch TD, Molin DG, Person A, Runyan RB, Gittenberger-de Groot AC, McDonald JA, Klewer SE. Temporal and distinct TGFbeta ligand requirements during mouse and avian endocardial cushion morphogenesis. Dev Biol 2002;248:170-181.
31. Liebner S, Cattelino A, Gallini R, Rudini N, Iurlaro M, Piccolo S, Dejana E. Beta-catenin is required for endothelial-mesenchymal transformation during heart cushion development in the mouse. J Cell Biol 2004;166:359-367.
32. Nakajima Y, Yamagishi T, Hokari S, Nakamura H. Mechanisms involved in valvuloseptal endocardial cushion formation in early cardiogenesis: roles of transforming growth factor (TGF)-beta and bone morphogenetic protein (BMP). Anat Rec 2000;258:119-127.
33. Zeisberg EM, Potenta S, Xie L, Zeisberg M, Kalluri R. Discovery of endothelial to mesenchymal transition as a source for carcinoma-associated fibroblasts. Cancer Res 2007;67:10123-10128.
34. Goumans MJ, van Zonneveld AJ, ten Dijke P. Transforming growth factor beta-induced endothelial-to-mesenchymal transition: a switch to cardiac fibrosis? Trends Cardiovasc Med 2008;18:293-298.
35. Kitao A, Sato Y, Sawada-Kitamura S, Harada K, Sasaki M, Morikawa H, Shiomi S, Honda M, Matsui O, Nakanuma Y. Endothelial to mesenchymal transition via transforming growth factor-beta1/Smad activation is associated with portal venous stenosis in idiopathic portal hypertension. Am J Pathol 2009;175:616-626.
36. Egorova AD, Khedoe PP, Goumans MJ, Yoder BK, Nauli SM, ten Dijke P, Poelmann RE, Hierck BP. Lack of primary cilia primes shear-induced endothelial-to-mesenchymal transition. Circ Res 2011;108:1093-1101.
37. Diez M, Musri MM, Ferrer E, Barbera JA, Peinado VI. Endothelial progenitor cells undergo an endothelial-to-mesenchymal transition-like process mediated by TGFbetaRI. Cardiovasc Res 2010;88:502-511.
38. Rieder F, Kessler SP, West GA, Bhilocha S, de la Motte C, Sadler TM, Gopalan B, Stylianou E, Fiocchi C. Inflammation-induced endothelial-to-mesenchymal transition: a novel mechanism of intestinal fibrosis. Am J Pathol 2011;179:2660-2673.
39. Lounev VY, Ramachandran R, Wosczyna MN, Yamamoto M, Maidment AD, Shore EM, Glaser DL, Goldhamer DJ, Kaplan FS. Identification of progenitor cells that contribute to heterotopic skeletogenesis. J Bone Joint Surg Am 2009;91:652-663.
40. Wosczyna MN, Biswas AA, Cogswell CA, Goldhamer DJ. Multipotent progenitors resident in the skeletal muscle interstitium exhibit robust BMP-dependent osteogenic activity and mediate heterotopic ossification. J Bone Miner Res 2012;27:1004-1017.
41. Pandey D, Bhunia A, Oh YJ, Chang F, Bergman Y, Kim JH, Serbo J, Boronina TN, Cole RN, Van Eyk J, Remaley AT, Berkowitz DE, Romer LH. OxLDL triggers retrograde translocation of arginase2 in aortic endothelial cells via ROCK and mitochondrial processing peptidase. Circ Res 2014;115:450-459.
42. Huang CY, Lin FY, Shih CM, Au HK, Chang YJ, Nakagami H, Morishita R, Chang NC, Shyu KG, Chen JW. Moderate to high concentrations of high-density lipoprotein from healthy subjects paradoxically impair human endothelial progenitor cells and related angiogenesis by activating Rho-associated kinase pathways. Arterioscler Thromb Vasc Biol 2012;32:2405-2417.
43. Michel T, Vanhoutte PM. Cellular signaling and NO production. Pflugers Arch 2010;459:807-816.
44. Ricard N, Ciais D, Levet S, Subileau M, Mallet C, Zimmers TA, Lee SJ, Bidart M, Feige JJ, Bailly S. BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood 2012;119:6162-6171.
45. Choi EJ, Kim YH, Choe SW, Tak YG, Garrido-Martin EM, Chang M, Lee YJ, Oh SP. Enhanced responses to angiogenic cues underlie the pathogenesis of hereditary hemorrhagic telangiectasia 2. PLoS ONE 2013;8:e63138.
46. Kajimoto H, Kai H, Aoki H, Uchiwa H, Aoki Y, Yasuoka S, Anegawa T, Mishina Y, Suzuki A, Fukumoto Y, Imaizumi T. BMP type I receptor inhibition attenuates endothelial dysfunction in mice with chronic kidney disease. Kidney Int 2015;87:128-136.
47. Koga M, Engberding N, Dikalova AE, Chang KH, Seidel-Rogol B, Long JS, Lassegue B, Jo H, Griendling KK. The bone morphogenic protein inhibitor, noggin, reduces glycemia and vascular inflammation in db/db mice. Am J Physiol Heart Circ Physiol 2013;305:H747-H755.
48. Saeed O, Otsuka F, Polavarapu R, Karmali V, Weiss D, Davis T, Rostad B, Pachura K, Adams L, Elliott J, Taylor WR, Narula J, Kolodgie F, Virmani R, Hong CC, Finn AV. Pharmacological suppression of hepcidin increases macrophage cholesterol efflux and reduces foam cell formation and atherosclerosis. Arterioscler Thromb Vasc Biol 2012;32:299-307.
49. Margaritis M, Channon KM, Antoniades C. Statins as regulators of redox state in the vascular endothelium: beyond lipid lowering. Antioxid Redox Signal 2014;20:1198-1215.
50. Lahera V, Goicoechea M, de Vinuesa SG, Miana M, de las Heras N, Cachofeiro V, Luno J. Endothelial dysfunction, oxidative stress and inflammation in atherosclerosis: beneficial effects of statins. Curr Med Chem 2007;14:243-248.
51. Liao JK. Clinical implications for statin pleiotropy. Curr Opin Lipidol 2005;16:624-629.
52. Hamilton CA, Miller WH, Al-Benna S, Brosnan MJ, Drummond RD, McBride MW, Dominiczak AF. Strategies to reduce oxidative stress in cardiovascular disease. Clin Sci (Lond) 2004;106:219-234.
53. Rosenson RS. Statins in atherosclerosis: lipid-lowering agents with antioxidant capabilities. Atherosclerosis 2004;173:1-12.