The role of BMPs in endothelial cell function and dysfunction

Trends in Endocrinology and Metabolism

Volumn 25, Issue 9, 2014, Pages 472-480

  Dyer, Laura A ^a   Pi, Xinchun ^b   Patterson, Cam ^b  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b WEILL CORNELL MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOPOIETIN RECEPTOR; BONE MORPHOGENETIC PROTEIN 2; BONE MORPHOGENETIC PROTEIN 4; BONE MORPHOGENETIC PROTEIN 9; BONE MORPHOGENETIC PROTEIN RECEPTOR; INTERCELLULAR ADHESION MOLECULE 1; MESSENGER RNA; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 2; BONE MORPHOGENETIC PROTEIN; ISOPROTEIN;

ANGIOGENESIS; ATHEROSCLEROSIS; CELL FUNCTION; ENDOTHELIAL DYSFUNCTION; ENDOTHELIUM CELL; HUMAN; HYPERTENSION; INFLAMMATION; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; REVIEW; SHEAR STRESS; VASCULAR ENDOTHELIUM; AGONISTS; ANIMAL; BIOLOGICAL MODEL; CYTOLOGY; GENETICS; HYPERTENSION, PULMONARY; METABOLISM; NEOVASCULARIZATION, PATHOLOGIC; OXIDATIVE STRESS; PHYSIOLOGICAL STRESS; SHEAR STRENGTH; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; VASCULAR DISEASES;

ANIMALS; ATHEROSCLEROSIS; BONE MORPHOGENETIC PROTEIN RECEPTORS; BONE MORPHOGENETIC PROTEINS; ENDOTHELIUM, VASCULAR; HUMANS; HYPERTENSION; HYPERTENSION, PULMONARY; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; OXIDATIVE STRESS; PROTEIN ISOFORMS; SHEAR STRENGTH; SIGNAL TRANSDUCTION; STRESS, PHYSIOLOGICAL; VASCULAR DISEASES;

EID: 84906935590     PISSN: 10432760     EISSN: 18793061     Source Type: Journal    
DOI: 10.1016/j.tem.2014.05.003     Document Type: Review

References (71)

1. Cai J., et al. BMP signaling in vascular diseases. FEBS Lett. 2012, 586:1993-2002.
2. Wiley D.M., Jin S.W. Bone morphogenetic protein functions as a context-dependent angiogenic cue in vertebrates. Semin. Cell Dev. Biol. 2011, 22:1012-1018.
3. Bandyopadhyay A., et al. BMP signaling in development and diseases: a pharmacological perspective. Biochem. Pharmacol. 2013, 85:857-864.
4. Maddaluno L., et al. EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature 2013, 498:492-496.
5. Pi X., et al. Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. J. Cell Biol. 2007, 179:1569-1582.
6. Ciumas M., et al. Bone morphogenetic proteins protect pulmonary microvascular endothelial cells from apoptosis by upregulating alpha-B-crystallin. Arterioscler. Thromb. Vasc. Biol. 2013, 33:2577-2584.
7. David L., et al. Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev. 2009, 20:203-212.
8. Yao Y., et al. Heat shock protein 70 enhances vascular bone morphogenetic protein-4 signaling by binding matrix Gla protein. Circ. Res. 2009, 105:575-584.
9. Yao Y., et al. Matrix Gla protein deficiency causes arteriovenous malformations in mice. J. Clin. Invest. 2011, 121:2993-3004.
10. Suzuki Y., et al. BMP-9 induces proliferation of multiple types of endothelial cells in vitro and in vivo. J. Cell Sci. 2010, 123:1684-1692.
11. Brown M.A., et al. Crystal structure of BMP-9 and functional interactions with pro-region and receptors. J. Biol. Chem. 2005, 280:25111-25118.
12. Orlova V.V., et al. Controlling angiogenesis by two unique TGF-beta type I receptor signaling pathways. Histol. Histopathol. 2011, 26:1219-1230.
13. David L., et al. Identification of BMP9 and BMP10 as functional activators of the orphan activin receptor-like kinase 1 (ALK1) in endothelial cells. Blood 2007, 109:1953-1961.
14. David L., et al. Bone morphogenetic protein-9 is a circulating vascular quiescence factor. Circ. Res. 2008, 102:914-922.
15. Scharpfenecker M., et al. BMP-9 signals via ALK1 and inhibits bFGF-induced endothelial cell proliferation and VEGF-stimulated angiogenesis. J. Cell Sci. 2007, 120:964-972.
16. Townson S.A., et al. Specificity and structure of a high affinity activin receptor-like kinase 1 (ALK1) signaling complex. J. Biol. Chem. 2012, 287:27313-27325.
17. Nolan-Stevaux O., et al. Endoglin requirement for BMP9 signaling in endothelial cells reveals new mechanism of action for selective anti-endoglin antibodies. PLoS ONE 2012, 7:e50920.
18. Park J.E., et al. BMP-9 induced endothelial cell tubule formation and inhibition of migration involves Smad1 driven endothelin-1 production. PLoS ONE 2012, 7:e30075.
19. Upton P.D., et al. Bone morphogenetic protein (BMP) and activin type II receptors balance BMP9 signals mediated by activin receptor-like kinase-1 in human pulmonary artery endothelial cells. J. Biol. Chem. 2009, 284:15794-15804.
20. Finkenzeller G., et al. Effects of bone morphogenetic protein 2 on human umbilical vein endothelial cells. Microvasc. Res. 2012, 84:81-85.
21. Upton P.D., et al. Functional characterization of bone morphogenetic protein binding sites and Smad1/5 activation in human vascular cells. Mol. Pharmacol. 2008, 73:539-552.
22. Pi X., et al. LRP1-dependent endocytic mechanism governs the signaling output of the bmp system in endothelial cells and in angiogenesis. Circ. Res. 2012, 111:564-574.
23. Tian X.Y., et al. Bone morphogenic protein-4 induces endothelial cell apoptosis through oxidative stress-dependent p38MAPK and JNK pathway. J. Mol. Cell Cardiol. 2012, 52:237-244.
24. Wong W.T., et al. Bone morphogenic protein-4 impairs endothelial function through oxidative stress-dependent cyclooxygenase-2 upregulation: implications on hypertension. Circ. Res. 2010, 107:984-991.
25. Yu P.B., et al. Bone morphogenetic protein (BMP) type II receptor deletion reveals BMP ligand-specific gain of signaling in pulmonary artery smooth muscle cells. J. Biol. Chem. 2005, 280:24443-24450.
26. de Jesus Perez V.A., et al. Bone morphogenetic protein 2 induces pulmonary angiogenesis via Wnt-beta-catenin and Wnt-RhoA-Rac1 pathways. J. Cell Biol. 2009, 184:83-99.
27. Tian H., et al. Endoglin mediates fibronectin/alpha5beta1 integrin and TGF-beta pathway crosstalk in endothelial cells. EMBO J. 2012, 31:3885-3900.
28. Kelley R., et al. A concentration-dependent endocytic trap and sink mechanism converts Bmper from an activator to an inhibitor of Bmp signaling. J. Cell Biol. 2009, 184:597-609.
29. Pi X., et al. Bmper inhibits endothelial expression of inflammatory adhesion molecules and protects against atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2012, 32:2214-2222.
30. Moreno-Miralles I., et al. Bone morphogenetic protein endothelial cell precursor-derived regulator regulates retinal angiogenesis in vivo in a mouse model of oxygen-induced retinopathy. Arterioscler. Thromb. Vasc. Biol. 2011, 31:2216-2222.
31. Moser M., et al. BMPER is a conserved regulator of hematopoietic and vascular development in zebrafish. J. Mol. Cell Cardiol. 2007, 43:243-253.
32. Teichert-Kuliszewska K., et al. Bone morphogenetic protein receptor-2 signaling promotes pulmonary arterial endothelial cell survival: implications for loss-of-function mutations in the pathogenesis of pulmonary hypertension. Circ. Res. 2006, 98:209-217.
33. Xu J., et al. Over-expression of BMP4 inhibits experimental choroidal neovascularization by modulating VEGF and MMP-9. Angiogenesis 2012, 15:213-227.
34. Wiley D.M., et al. Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat. Cell Biol. 2011, 13:686-692.
35. Kim J.D., et al. Context-dependent proangiogenic function of bone morphogenetic protein signaling is mediated by disabled homolog 2. Dev. Cell 2012, 23:441-448.
36. Osada M., et al. Platelet activation receptor CLEC-2 regulates blood/lymphatic vessel separation by inhibiting proliferation, migration, and tube formation of lymphatic endothelial cells. J. Biol. Chem. 2012, 287:22241-22252.
37. Ricard N., et al. BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood 2012, 119:6162-6171.
38. Larrivee B., et al. ALK1 signaling inhibits angiogenesis by cooperating with the Notch pathway. Dev. Cell 2012, 22:489-500.
39. Somekawa S., et al. Tmem100, an ALK1 receptor signaling-dependent gene essential for arterial endothelium differentiation and vascular morphogenesis. Proc. Natl. Acad. Sci. U.S.A. 2012, 109:12064-12069.
40. Moya I.M., et al. Stalk cell phenotype depends on integration of Notch and Smad1/5 signaling cascades. Dev. Cell 2012, 22:501-514.
41. Roca C., Adams R.H. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 2007, 21:2511-2524.
42. Yao Y., et al. Crossveinless 2 regulates bone morphogenetic protein 9 in human and mouse vascular endothelium. Blood 2012, 119:5037-5047.
43. Poirier O., et al. Inhibition of apelin expression by BMP signaling in endothelial cells. Am. J. Physiol. Cell Physiol. 2012, 303:C1139-C1145.
44. Tian F., et al. Endothelial cells are activated during hypoxia via endoglin/ALK-1/SMAD1/5 signaling in vivo and in vitro. Biochem. Biophys. Res. Commun. 2010, 392:283-288.
45. -/- mice. PLoS ONE 2013, 8:e58550.
46. Kim Y.W., Byzova T.V. Oxidative stress in angiogenesis and vascular disease. Blood 2014, 123:625-631.
47. Zhang Y., et al. Inhibition of bone morphogenic protein 4 restores endothelial function in db/db diabetic mice. Arterioscler. Thromb. Vasc. Biol. 2014, 34:152-159.
48. Brook R.D., et al. Beyond medications and diet: alternative approaches to lowering blood pressure: a scientific statement from the american heart association. Hypertension 2013, 61:1360-1383.
49. Gangopahyay A., et al. Bone morphogenetic protein receptor II is a novel mediator of endothelial nitric-oxide synthase activation. J. Biol. Chem. 2011, 286:33134-33140.
50. Anderson L., et al. Bmp2 and Bmp4 exert opposing effects in hypoxic pulmonary hypertension. Am. J. Physiol. Regul. Integr. Comp. Physiol. 2010, 298:R833-R842.
51. Star G.P., et al. Bone morphogenic protein-9 stimulates endothelin-1 release from human pulmonary microvascular endothelial cells: a potential mechanism for elevated ET-1 levels in pulmonary arterial hypertension. Microvasc. Res. 2010, 80:349-354.
52. Ma L., Chung W.K. The genetic basis of pulmonary arterial hypertension. Hum. Genet. 2014, 133:471-479.
53. Alastalo T.P., et al. Disruption of PPARgamma/beta-catenin-mediated regulation of apelin impairs BMP-induced mouse and human pulmonary arterial EC survival. J. Clin. Invest. 2011, 121:3735-3746.
54. Spiekerkoetter E., et al. FK506 activates BMPR2, rescues endothelial dysfunction, and reverses pulmonary hypertension. J. Clin. Invest. 2013, 123:3600-3613.
55. Choi E.J., et al. Enhanced responses to angiogenic cues underlie the pathogenesis of hereditary hemorrhagic telangiectasia 2. PLoS ONE 2013, 8:e63138.
56. Yao Y., et al. Reducing Jagged 1 and 2 levels prevents cerebral arteriovenous malformations in matrix Gla protein deficiency. Proc. Natl. Acad. Sci. U.S.A. 2013, 110:19071-19076.
57. Go A.S., et al. Heart disease and stroke statistics - 2014 update: a report from the American Heart Association. Circulation 2014, 129:e28-e292.
58. Yao Y., et al. Inhibition of bone morphogenetic proteins protects against atherosclerosis and vascular calcification. Circ. Res. 2010, 107:485-494.
59. Wentzel J.J., et al. Endothelial shear stress in the evolution of coronary atherosclerotic plaque and vascular remodelling: current understanding and remaining questions. Cardiovasc. Res. 2012, 96:234-243.
60. Csiszar A., et al. Hemodynamic forces, vascular oxidative stress, and regulation of BMP-2/4 expression. Antioxid. Redox. Signal. 2009, 11:1683-1697.
61. Sorescu G.P., et al. Bone morphogenic protein 4 produced in endothelial cells by oscillatory shear stress induces monocyte adhesion by stimulating reactive oxygen species production from a nox1-based NADPH oxidase. Circ. Res. 2004, 95:773-779.
62. Zhou J., et al. BMP receptor-integrin interaction mediates responses of vascular endothelial Smad1/5 and proliferation to disturbed flow. J. Thromb. Haemost. 2013, 11:741-755.
63. Ross T.D., et al. Integrins in mechanotransduction. Curr. Opin. Cell Biol. 2013, 25:613-618.
64. Albrecht E.W., et al. Protective role of endothelial nitric oxide synthase. J. Pathol. 2003, 199:8-17.
65. Helbing T., et al. BMP activity controlled by BMPER regulates the proinflammatory phenotype of endothelium. Blood 2011, 118:5040-5049.
66. Helbing T., et al. BMPER is upregulated by statins and modulates endothelial inflammation by intercellular adhesion molecule-1. Arterioscler. Thromb. Vasc. Biol. 2010, 30:554-560.
67. Kim C.W., et al. Anti-inflammatory and antiatherogenic role of BMP receptor II in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 2013, 33:1350-1359.
68. Derwall M., et al. Inhibition of bone morphogenetic protein signaling reduces vascular calcification and atherosclerosis. Arterioscler. Thromb. Vasc. Biol. 2012, 32:613-622.
69. Su X., et al. Oxidized low density lipoprotein induces bone morphogenetic protein-2 in coronary artery endothelial cells via Toll-like receptors 2 and 4. J. Biol. Chem. 2011, 286:12213-12220.
70. Staton C.A., et al. A critical analysis of current in vitro and in vivo angiogenesis assays. Int. J. Exp. Pathol. 2009, 90:195-221.
71. Stahl A., et al. The mouse retina as an angiogenesis model. Invest. Ophthalmol. Vis. Sci. 2010, 51:2813-2826.