Bone morphogenetic proteins and vascular differentiation

Martin Moser; Cam Patterson

doi:10.1160/TH05-05-0312

Thrombosis and Haemostasis, Table of Contents

Thromb Haemost 2005; 94(04): 713-718
DOI: 10.1160/TH05-05-0312

Theme Issue Article

Schattauer GmbH

Bone morphogenetic proteins and vascular differentiation

BMPing up vasculogenesis

Martin Moser

¹Department of Cardiology, University of Freiburg, Germany

,

Cam Patterson

²2Carolina Cardiovascular Biology Center, University of North Carolina at Chapel Hill, USA

› Author Affiliations

Abstract

Summary

Vasculogenesis is an important mechanism of blood vessel formation not only in embryos but also in adults. It may contribute to reparative effects of progenitor cell therapy in ischemic diseases such as myocardial infarction. Signaling pathways involved in embryonic development, including the BMP pathway, are reactivated in adult vasculogenesis. As a consequence knowledge about embryonic signaling events will help to understand blood vessel formation in the adult. The role of BMPs in embryonic development has been studied extensively in the past decades but only recently their role in vasculogenesis has been recognized. Gain and loss of function models indicate that BMPs stimulate vasculogenesis in the embryo as well as in the adult. Additionally, BMPs interact with other pathways involved in blood vessel formation, such as VEGF signaling. Studying novel molecules such as BMPER that modulate BMP activity and that are expressed in vascular cells will help to understand vasculogenetic signaling and may open up new therapeutic avenues in vascular disease.

Keywords

Bone morphogenetic proteins - vasculogenesis - novel proteins

Full Text

References

References
1 Choi K. Hemangioblast development and regulation. Biochem Cell Biol 1998; 76: 947-56.
2 Choi K, Kennedy M, Kazarov A. et al. A common precursor for hematopoietic and endothelial cells. Development Supplement. 1998; 125: 725-32.
3 Masuda H, Asahara T. Post-natal endothelial progenitor cells for neovascularization in tissue regeneration. Cardiovasc Res. 2003; 58: 390-8.
4 Jain RK. Molecular regulation of vessel maturation. Nat Med. 2003; 9: 685-93.
5 Pardanaud L, Yassine F, Dieterlen-Lievre F. Relationship between vasculogenesis, angiogenesis and haemopoiesis during avian ontogeny. Development. 1989; 105: 473-85.
6 Risau W, Flamme I. Vasculogenesis. Annu Rev Cell Dev Biol. 1995; 11: 73-91.
7 Medvinsky AL, Dzierzak E. Definitive hematopoiesis is autonomously initiated by the AGM region. Cell 1996; 86: 897-906.
8 Asahara T, Murohara T, Sullivan A. et al. Isolation of putative progenitor endothelial cells for angiogenesis. Science 1997; 275: 964-7.
9 Massa M, Rosti V, Ferrario M. et al. Increased circulating hematopoietic and endothelial progenitor cells in the early phase of acute myocardial infarction. Blood 2005; 105: 199-206.
10 Orlic D, Kajstura J, Chimenti S. et al. Bone marrow cells regenerate infarcted myocardium. Nature 2001; 410: 701-5.
11 Kocher AA, Schuster MD, Szabolcs M J. et al. Neovascularization of ischemic myocardium by human bone-marrow-derived angioblasts prevents cardiomyocyte apoptosis, reduces remodeling and improves cardiac function. Nat Med 2001; 7: 430-6.
12 Schuster MD, Kocher AA, Seki T. et al. Myocardial neovascularization by bone marrow angioblasts results in cardiomyocyte regeneration. Am J Physiol Heart Circ Physiol 2004; 287: H525-32.
13 Anderson KV, Ingham PW. The transformation of the model organism: a decade of developmental genetics. Nat Genet. 2003 33 285-93.
14 Urist M. Bone: Formation by autoinduction. Science 1965; 150: 893-9.
15 Kawabata M, Imamura T, Miyazono K. Signal transduction by bone morphogenetic proteins. Cytokine Growth Factor Rev 1998; 9: 49-61.
16 De Robertis EM, Kuroda H. Dorsal-ventral patterning and neural induction in Xenopus embryos. Annu Rev Cell Dev Biol 2004; 20: 285-308.
17 Marshall CJ, Kinnon C, Thrasher AJ. Polarized expression of bone morphogenetic protein-4 in the human aorta-gonad-mesonephros region. Blood 2000; 96: 1591-3.
18 Park C, Afrikanova I, Chung YS. et al. A hierarchical order of factors in the generation of FLK1– and SCLexpressing hematopoietic and endothelial progenitors from embryonic stem cells. Development 2004; 131: 2749-62.
19 Reese DE, Hall CE, Mikawa T. Negative regulation of midline vascular development by the notochord. Dev Cell 2004; 6: 699-708.
20 Nimmagadda S, Geetha Loganathan P, Huang R. et al. BMP4 and noggin control embryonic blood vessel formation by antagonistic regulation of VEGFR-2 (Quek1) expression. Dev Biol 2005; 280: 100-10.
21 Valdimarsdottir G, Goumans MJ, Rosendahl A. 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: 2263-70.
22 Deckers MM, van Bezooijen RL, van der Horst G. et al. Bone morphogenetic proteins stimulate angiogenesis through osteoblast-derived vascular endothelial growth factor A. Endocrinology 2002; 143: 1545-53.
23 Folkman J. Tumor angiogenesis: therapeutic implications. N Engl J Med 1971; 285: 1182-6.
24 Langenfeld EM, Langenfeld J. Bone morphogenetic protein-2 stimulates angiogenesis in developing tumors. Mol Cancer Res 2004; 2: 141-9.
25 Winnier G, Blessing M, Labosky P A. et al. Bone morphogenetic protein-4 is required for mesoderm formation and patterning in the mouse. Genes Dev 1995; 9: 2105-16.
26 Gu Z, Reynolds EM, Song J. et al. The type I serine/ threonine kinase receptor ActRIA (ALK2) is required for gastrulation of the mouse embryo. Development 1999; 126: 2551-61.
27 Mishina Y, Suzuki A, Ueno N. et al. Bmpr encodes a type I bone morphogenetic protein receptor that is essential for gastrulation during mouse embryogenesis. Genes Dev 1995; 9: 3027-37.
28 Beppu H, Kawabata M, Hamamoto T. et al. BMP type II receptor is required for gastrulation and early development of mouse embryos. Dev Biol 2000; 221: 249-58.
29 Beppu H, Ichinose F, Kawai N. 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: L1241-7.
30 Morse JH. Bone morphogenetic protein receptor 2 mutations in pulmonary hypertension. Chest 2002; 121: 50S-53S.
31 Urness LD, Sorensen LK, Li DY. Arteriovenous malformations in mice lacking activin receptor-like kinase-. Nat Genet 2000; 26: 328-31.
32 Srinivasan S, Hanes MA, Dickens T. et al. A mouse model for hereditary hemorrhagic telangiectasia (HHT) type 2. Hum Mol Genet 2003; 12: 473-82.
33 Arthur HM, Ure J, Smith A J. et al. Endoglin, an ancillary TGFbeta receptor, is required for extraembryonic angiogenesis and plays a key role in heart development. Dev Biol 2000; 217: 42-53.
34 Li DY, Sorensen LK, Brooke B S. et al. Defective angiogenesis in mice lacking endoglin. Science 1999; 284: 1534-7.
35 Chang H, Huylebroeck D, Verschueren K. et al. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 1999; 126: 1631-42.
36 Yang X, Castilla LH, Xu X. et al. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 1999; 126: 1571-80.
37 Lechleider RJ, Ryan JL, Garrett L. et al. Targeted mutagenesis of Smad1 reveals an essential role in chorioallantoic fusion. Dev Biol 2001; 240: 157-67.
38 Tremblay KD, Dunn NR, Robertson EJ. Mouse embryos lacking Smad1 signals display defects in extraembryonic tissues and germ cell formation. Development 2001; 128: 3609-21.
39 Liu B, Sun Y, Jiang F. et al. Disruption of Smad5 gene leads to enhanced proliferation of high-proliferative potential precursors during embryonic hematopoiesis. Blood 2003; 101: 124-33.
40 Nohe A, Keating E, Knaus P. et al. Signal transduction of bone morphogenetic protein receptors. Cell Signal 2004; 16: 291-9.
41 Ferrara N, Carver-Moore K, Chen H. et al. Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 1996; 380: 439-42.
42 Carmeliet P, Ferreira V, Breier G. et al. Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 1996; 380: 435-9.
43 Miquerol L, Langille BL, Nagy A. Embryonic development is disrupted by modest increases in vascular endothelial growth factor gene expression. Development 2000; 127: 3941-6.
44 Tokuda H, Hatakeyama D, Shibata T. et al. p38 MAP kinase regulates BMP-4-stimulated VEGF synthesis via p70 S6 kinase in osteoblasts. Am J Physiol Endocrinol Metab 2003; 284: E1202-9.
45 Kozawa O, Matsuno H, Uematsu T. Involvement of p70 S6 kinase in bone morphogenetic protein signaling: vascular endothelial growth factor synthesis by bone morphogenetic protein-4 in osteoblasts. J Cell Biochem 2001; 81: 430-6.
46 Carano RA, Filvaroff EH. Angiogenesis and bone repair. Drug Discov Today 2003; 8: 980-9.
47 He C, Chen X. Transcription regulation of the vegf gene by the BMP/Smad pathway in the angioblast of zebrafish embryos. Biochem Biophys Res Commun 2005; 329: 324-30.