Signaling by members of the TGF-β family in vascular morphogenesis and disease

Trends in Cell Biology

Volumn 20, Issue 9, 2010, Pages 556-567

  Pardali, Evangelia ^a   Goumans, Marie José ^a   ten Dijke, Peter ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; THALIDOMIDE; TRANSFORMING GROWTH FACTOR BETA; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 1; TRANSFORMING GROWTH FACTOR BETA1; TRANSFORMING GROWTH FACTOR BETA2; TRANSFORMING GROWTH FACTOR BETA3;

ANGIOGENESIS; ATAXIA TELANGIECTASIA; ENDOTHELIUM CELL; HUMAN; MICROVASCULARIZATION; MORPHOGENESIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION; TUMOR VASCULARIZATION; VASCULAR SMOOTH MUSCLE;

ANIMALS; BLOOD VESSELS; HUMANS; MORPHOGENESIS; NEOVASCULARIZATION, PATHOLOGIC; NEOVASCULARIZATION, PHYSIOLOGIC; SIGNAL TRANSDUCTION; TRANSFORMING GROWTH FACTOR BETA;

EID: 77956187467     PISSN: 09628924     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.tcb.2010.06.006     Document Type: Review

References (98)

1. Adams R.H., Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 2007, 8:464-478.
2. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 2005, 438:932-936.
3. Folkman J., D'Amore P.A. Blood vessel formation: what is its molecular basis?. Cell 1996, 87:1153-1155.
4. Ribatti D. The discovery of endothelial progenitor cells. An historical review. Leuk. Res. 2007, 31:439-444.
5. Betsholtz C., et al. Role of pericytes in vascular morphogenesis. EXS 2005, 94:115-125.
6. Risau W. Mechanisms of angiogenesis. Nature 1997, 386:671-674.
7. Stehbens W.E. Structural and architectural changes during arterial development and the role of hemodynamics. Acta Anat. (Basel) 1996, 157:261-274.
8. Swift M.R., Weinstein B.M. Arterial-venous specification during development. Circ. Res. 2009, 104:576-588.
9. Carmeliet P., Jain R.K. Angiogenesis in cancer and other diseases. Nature 2000, 407:249-257.
10. Hanahan D., Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 1996, 86:353-364.
11. Gerhardt H., et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 2003, 161:1163-1177.
12. Kamei M., et al. Endothelial tubes assemble from intracellular vacuoles in vivo. Nature 2006, 442:453-456.
13. Stalmans I., et al. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 2002, 109:327-336.
14. Hellstrom M., et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007, 445:776-780.
15. Suchting S., et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:3225-3230.
16. von Tell D., et al. Pericytes and vascular stability. Exp. Cell Res. 2006, 312:623-629.
17. Heldin C.H., et al. TGF-β signalling from cell membrane to nucleus through SMAD proteins. Nature 1997, 390:465-471.
18. Schmierer B., Hill C.S. TGFβ-SMAD signal transduction: molecular specificity and functional flexibility. Nat. Rev. Mol. Cell Biol. 2007, 8:970-982.
19. Guo X., Wang X.F. Signaling cross-talk between TGF-beta/BMP and other pathways. Cell Res. 2009, 19:71-88.
20. ten Dijke P., Arthur H.M. Extracellular control of TGFβ signalling in vascular development and disease. Nat. Rev. Mol. Cell Biol. 2007, 8:857-869.
21. Constam D.B., Robertson E.J. Regulation of bone morphogenetic protein activity by pro domains and proprotein convertases. J. Cell Biol. 1999, 144:139-149.
22. ten Dijke P., et al. Endoglin in angiogenesis and vascular diseases. Angiogenesis 2008, 11:79-89.
23. Oh S.P., et al. Activin receptor-like kinase 1 modulates transforming growth factor-β1 signaling in the regulation of angiogenesis. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:2626-2631.
24. Beppu H., et al. BMPR-II heterozygous mice have mild pulmonary hypertension and an impaired pulmonary vascular remodeling response to prolonged hypoxia. Am. J. Physiol. Lung Cell Mol. Physiol. 2004, 287:L1241-L1247.
25. Venkatesha S., et al. Soluble endoglin contributes to the pathogenesis of preeclampsia. Nat. Med. 2006, 12:642-649.
26. Chen Q., et al. Smad7 is required for the development and function of the heart. J. Biol. Chem. 2009, 284:292-300.
27. Park S.O., et al. ALK5- and TGFBR2-independent role of ALK1 in the pathogenesis of hereditary hemorrhagic telangiectasia type 2. Blood 2008, 111:633-642.
28. Seki T., et al. Nonoverlapping expression patterns of ALK1 and ALK5 reveal distinct roles of each receptor in vascular development. Lab. Invest. 2006, 86:116-129.
29. Carvalho R.L., et al. Defective paracrine signalling by TGFβ in yolk sac vasculature of endoglin mutant mice: a paradigm for hereditary hemorrhagic telangiectasia. Development 2004, 131:6237-6247.
30. Carvalho R.L., et al. Compensatory signalling induced in the yolk sac vasculature by deletion of TGFβ receptors in mice. J. Cell Sci. 2007, 120:4269-4277.
31. Gallione C.J., et al. A combined syndrome of juvenile polyposis and hereditary hemorrhagic telangiectasia associated with mutations in MADH4 (SMAD4). Lancet 2004, 363:852-859.
32. Park S.O., et al. Real-time imaging of de novo arteriovenous malformation in a mouse model of hereditary hemorrhagic telangiectasia. J. Clin. Invest. 2009, 119:3487-3496.
33. Sorensen L.K., et al. Loss of distinct arterial and venous boundaries in mice lacking endoglin, a vascular-specific TGFβ coreceptor. Dev. Biol. 2003, 261:235-250.
34. Roman B.L., et al. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development 2002, 129:3009-3019.
35. Mancini M.L., et al. Endoglin plays distinct roles in vascular smooth muscle cell recruitment and regulation of arteriovenous identity during angiogenesis. Dev. Dyn. 2009, 238:2479-2493.
36. Mahmoud M., et al. Pathogenesis of arteriovenous malformations in the absence of endoglin. Circ. Res. 2010, 106:1425-1433.
37. Blokzijl A., et al. Cross-talk between the Notch and TGF-β signaling pathways mediated by interaction of the Notch intracellular domain with Smad3. J. Cell Biol. 2003, 163:723-728.
38. Niimi H., et al. Notch signaling is necessary for epithelial growth arrest by TGF-β. J. Cell Biol. 2007, 176:695-707.
39. Itoh F., et al. Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J. 2004, 23:541-551.
40. Fu Y., et al. Differential regulation of transforming growth factor β signaling pathways by Notch in human endothelial cells. J. Biol. Chem. 2009, 284:19452-19462.
41. Bauditz J., et al. Thalidomide for treatment of severe intestinal bleeding. Gut 2004, 53:609-612.
42. Bauditz J., Lochs H. Angiogenesis and vascular malformations: antiangiogenic drugs for treatment of gastrointestinal bleeding. World J. Gastroenterol. 2007, 13:5979-5984.
43. Bose P., et al. Bevacizumab in hereditary hemorrhagic telangiectasia. N. Engl. J. Med. 2009, 360:2143-2144.
44. Cunha S.I., et al. Genetic and pharmacological targeting of activin receptor-like kinase 1 impairs tumor growth and angiogenesis. J. Exp. Med. 2010, 207:85.
45. Hawinkels L.J.A.C., et al. MMP-14 (MT1-MMP) mediated endoglin shedding regulates tumor angiogenesis. Canc. Res. 2010, 70:4141-4150.
46. Pardali E., ten Dijke P. Transforming growth factor-β signaling and tumor angiogenesis. Front. Biosci. 2009, 14:4848-4861.
47. Goumans M.J., et al. Balancing the activation state of the endothelium via two distinct TGF-β type I receptors. EMBO J. 2002, 21:1743-1753.
48. Pepper M.S. Transforming growth factor-β: vasculogenesis, angiogenesis, and vessel wall integrity. Cytokine Growth Factor Rev. 1997, 8:21-43.
49. Serrati S., et al. TGFβ1 antagonistic peptides inhibit TGFβ1-dependent angiogenesis. Biochem. Pharmacol. 2009, 77:813-825.
50. Ferrari G., et al. VEGF, a prosurvival factor, acts in concert with TGF-β1 to induce endothelial cell apoptosis. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:17260-17265.
51. Ferrari G., et al. Transforming growth factor-β1 (TGF-β1) induces angiogenesis through vascular endothelial growth factor (VEGF)-mediated apoptosis. J. Cell Physiol. 2009, 219:449-458.
52. James D., et al. Expansion and maintenance of human embryonic stem cell-derived endothelial cells by TGFβ inhibition is Id1 dependent. Nat. Biotechnol. 2010, 28:161-166.
53. Watabe T., et al. TGF-β receptor kinase inhibitor enhances growth and integrity of embryonic stem cell-derived endothelial cells. J. Cell Biol. 2003, 163:1303-1311.
54. Liu Z., et al. VEGF and inhibitors of TGFβ type-I receptor kinase synergistically promote blood-vessel formation by inducing α5-integrin expression. J. Cell Sci. 2009, 122:3294-3302.
55. Goumans M.J., et al. Activin receptor-like kinase (ALK)1 is an antagonistic mediator of lateral TGFβ /ALK5 signaling. Mol. Cell 2003, 12:817-828.
56. Finnson K.W., et al. ALK1 opposes ALK5/Smad3 signaling and expression of extracellular matrix components in human chondrocytes. J. Bone Miner. Res. 2008, 23:896-906.
57. Konig H.G., et al. TGF-β1 activates two distinct type I receptors in neurons: implications for neuronal NF-κB signaling. J. Cell Biol. 2005, 168:1077-1086.
58. Wiercinska E., et al. Id1 is a critical mediator in TGF-βeta-induced transdifferentiation of rat hepatic stellate cells. Hepatology 2006, 43:1032-1041.
59. Daly A.C., et al. Transforming growth factor β-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Mol. Cell Biol. 2008, 28:6889-6902.
60. Liu I.M., et al. TGFβ -stimulated Smad1/5 phosphorylation requires the ALK5 L45 loop and mediates the pro-migratory TGFβ switch. EMBO J. 2009, 28:88-98.
61. Wrighton K.H., et al. Transforming growth factor β can stimulate Smad1 phosphorylation independently of bone morphogenic protein receptors. J. Biol. Chem. 2009, 284:9755-9763.
62. Lamouille S., et al. Activin receptor-like kinase 1 is implicated in the maturation phase of angiogenesis. Blood 2002, 100:4495-4501.
63. 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.
64. 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.
65. 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.
66. Shao E.S., et al. Expression of vascular endothelial growth factor is coordinately regulated by the activin-like kinase receptors 1 and 5 in endothelial cells. Blood 2009, 114:2197-2206.
67. Sadick H., et al. Patients with hereditary hemorrhagic telangiectasia have increased plasma levels of vascular endothelial growth factor and transforming growth factor-β1 as well as high ALK1 tissue expression. Haematologica 2005, 90:818-828.
68. Sadick H., et al. Plasma level and tissue expression of angiogenic factors in patients with hereditary hemorrhagic telangiectasia. Int. J. Mol. Med. 2005, 15:591-596.
69. Mitchell D., et al. ALK1-Fc inhibits multiple mediators of angiogenesis and suppresses tumor growth. Mol. Cancer Ther. 2010, 9:379-388.
70. 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.
71. Velasco S., et al. L- and S-endoglin differentially modulate TGFβ1 signaling mediated by ALK1 and ALK5 in L6E9 myoblasts. J. Cell Sci. 2008, 121:913-919.
72. Ray B.N., et al. ALK5 phosphorylation of the endoglin cytoplasmic domain regulates Smad1/5/8 signaling and endothelial cell migration. Carcinogenesis 2010, 31:435-441.
73. Mahmoud M., et al. Endoglin and activin receptor-like-kinase 1 are co-expressed in the distal vessels of the lung: implications for two familial vascular dysplasias. HHT and PAH. Lab. Invest. 2009, 89:15-25.
74. David L., et al. Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev. 2009, 20:203-212.
75. Suzuki Y., et al. BMPs promote proliferation and migration of endothelial cells via stimulation of VEGF-A/VEGFR2 and angiopoietin-1/Tie2 signalling. J. Biochem. 2008, 143:199-206.
76. Ren R., et al. Gene expression profiles identify a role for cyclooxygenase 2-dependent prostanoid generation in BMP6-induced angiogenic responses. Blood 2007, 109:2847-2853.
77. Valdimarsdottir G., et al. Stimulation of Id1 expression by bone morphogenetic protein is sufficient and necessary for bone morphogenetic protein-induced activation of endothelial cells. Circulation 2002, 106:2263-2270.
78. Pi X., et al. Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. Cell Biol. 2007, 179:1569-1582.
79. Seay U., et al. Transforming growth factor-β-dependent growth inhibition in primary vascular smooth muscle cells is p38-dependent. J. Pharmacol. Exp. Ther. 2005, 315:1005-1012.
80. Hirschi K.K., et al. PDGF, TGF-β, and heterotypic cell-cell interactions mediate endothelial cell-induced recruitment of 10T1/2 cells and their differentiation to a smooth muscle fate. J. Cell Biol. 1998, 141:805-814.
81. Wurdak H., et al. Inactivation of TGFβ signaling in neural crest stem cells leads to multiple defects reminiscent of DiGeorge syndrome. Genes Dev. 2005, 19:530-535.
82. Johnson D.W., et al. Mutations in the activin receptor-like kinase 1 gene in hereditary hemorrhagic telangiectasia type 2. Nat. Genet. 1996, 13:189-195.
83. McAllister K.A., et al. Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary hemorrhagic telangiectasia type 1. Nat. Genet. 1994, 8:345-351.
84. Bot P.T., et al. Increased expression of the transforming growth factor-β signaling pathway, endoglin, and early growth response-1 in stable plaques. Stroke 2009, 40:439-447.
85. Lebrin F., et al. Thalidomide stimulates vessel maturation and reduces epistaxis in individuals with hereditary hemorrhagic telangiectasia. Nat. Med. 2010, 16:420-428.
86. Dorai H., Sampath T.K. Bone morphogenetic protein-7 modulates genes that maintain the vascular smooth muscle cell phenotype in culture. J. Bone Joint Surg. Am. 2001, 83:S70-S78.
87. Nakaoka T., et al. Inhibition of rat vascular smooth muscle proliferation in vitro and in vivo by bone morphogenetic protein-2. J. Clin. Invest 1997, 100:2824-2832.
88. 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.
89. Yu P.B., et al. Bone morphogenetic protein (BMP) type II receptor is required for BMP-mediated growth arrest and differentiation in pulmonary artery smooth muscle cells. J. Biol. Chem. 2008, 283:3877-3888.
90. Harrison R.E., et al. Molecular and functional analysis identifies ALK-1 as the predominant cause of pulmonary hypertension related to hereditary hemorrhagic telangiectasia. J. Med. Genet. 2003, 40:865-871.
91. Trembath R.C. Mutations in the TGF-β type 1 receptor, ALK1, in combined primary pulmonary hypertension and hereditary hemorrhagic telangiectasia, implies pathway specificity. J. Heart Lung Transplant 2001, 20:175.
92. Thomas M., et al. Activin-like kinase 5 (ALK5) mediates abnormal proliferation of vascular smooth muscle cells from patients with familial pulmonary arterial hypertension and is involved in the progression of experimental pulmonary arterial hypertension induced by monocrotaline. Am. J. Pathol. 2009, 174:380-389.
93. Bergers G., Hanahan D. Modes of resistance to anti-angiogenic therapy. Nat. Rev. Cancer 2008, 8:592-603.
94. Petersen M., et al. Smad2 and Smad3 have opposing roles in breast cancer bone metastasis by differentially affecting tumor angiogenesis. Oncogene 2010, 29:1351-1361.
95. Roffe S., et al. Halofuginone inhibits Smad3 phosphorylation via the PI3K/Akt and MAPK/ERK pathways in muscle cells: Effects on myotube fusion. Exp. Cell Res. 2010, 316:1061-1069.
96. North, M.A et al. Amgen Fremont Inc and Pfizer Inc. Human monoclonal antibodies to Activin receptor-like kinase 1, WO/2007/040912.
97. Grinberg, A. et al. Acceleron Pharma, Inc and Ludwig Institute for Cancer Research Ltd. Methods and compositions based on ALK1 antagonists for modulating angiogenesis and pericyte coverage, WO/2009/134428.
98. Seehra, J. et al. (2009) Acceleron Pharma, Inc. Antagonists of BMP9, BMP10, ALK1 and other ALK1 ligands, and uses therof, WO/2009/139891.