BMP-SMAD signalling output is highly regionalized in cardiovascular and lymphatic endothelial networks

BMC Developmental Biology

Volumn 16, Issue 1, 2016, Pages 1-16

  Beets, Karen ^a,b   Staring, Michael W ^a,b   Criem, Nathan ^a,b   Maas, Elke ^a,b   Schellinx, Niels ^a,b   De Sousa Lopes, Susana M Chuva ^c   Umans, Lieve ^a,b   Zwijsen, An ^a,b  

^a DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^b UNIVERSITY OF LEUVEN   (Belgium)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

BMP SMAD signalling; Endocardium; Heterogeneity; Lymphangiogenesis; Morphogen; Phenotype switching; Retina; Sprouting angiogenesis; Stochastic expression; Valve development

Indexed keywords

BONE MORPHOGENETIC PROTEIN; GREEN FLUORESCENT PROTEIN; SMAD PROTEIN;

ANIMAL; CARDIOVASCULAR SYSTEM; EMBRYOLOGY; ENDOCARDIUM; ENDOTHELIUM CELL; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; GROWTH, DEVELOPMENT AND AGING; MAMMALIAN EMBRYO; METABOLISM; MOUSE; NEWBORN; PHOSPHORYLATION; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION; TRANSGENIC MOUSE;

ANIMALS; ANIMALS, NEWBORN; BONE MORPHOGENETIC PROTEINS; CARDIOVASCULAR SYSTEM; EMBRYO, MAMMALIAN; ENDOCARDIUM; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; GREEN FLUORESCENT PROTEINS; MICE; MICE, TRANSGENIC; PHOSPHORYLATION; SIGNAL TRANSDUCTION; SMAD PROTEINS; TRANSCRIPTIONAL ACTIVATION;

EID: 84991384687     PISSN: None     EISSN: 1471213X     Source Type: Journal    
DOI: 10.1186/s12861-016-0133-x     Document Type: Article

References (77)

1. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nature reviews. Molecular cell biology [Internet]. Nature Publishing Group; 2007 [cited 2014 Jul 17];8:464-78. Available from: http://dx.doi.org/10.1038/nrm2183
2. Tammela T, Alitalo K. Lymphangiogenesis: Molecular mechanisms and future promise. Cell [Internet]. Elsevier; 2010 [cited 2015 Nov 14]; 140:460-76. Available from: http://www.cell.com/article/S0092867410001157/fulltext
3. Kesler CT, Liao S, Munn LL, Padera TP. Lymphatic vessels in health and disease. Wiley Interdiscip Rev Syst Biol Med. 2013;5:111-24.
4. Cueni LN, Detmar M. The lymphatic system in health and disease. Lymphatic research and biology [Internet]. 2008;6:109-22. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3572233&tool=pmcentrez&rendertype=abstract
5. Alitalo K. The lymphatic vasculature in disease. Nature Medicine [Internet]. 2011;17:1371-80. Available from: http://dx.doi.org/10.1038/nm.2545
6. Aranguren XL, Beerens M, Coppiello G, Wiese C, Vandersmissen I, Lo Nigro A, et al. COUP-TFII orchestrates venous and lymphatic endothelial identity by homo-or hetero-dimerisation with PROX1. Journal of cell science [Internet]. 2013 [cited 2015 Nov 20];126:1164-75. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23345397
7. Aird WC. Endothelial cell heterogeneity. Cold Spring Harbor perspectives in medicine [Internet]. 2012 [cited 2015 Jun 18];2:a006429. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3253027&tool=pmcentrez&rendertype=abstract
8. Aird WC. Phenotypic heterogeneity of the endothelium: II. Representative vascular beds. Circulation research [Internet]. 2007 [cited 2015 Sep 14];100:174-90. Available from: http://circres.ahajournals.org/content/100/2/174.long
9. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circulation research [Internet]. 2007 [cited 2014 Jul 11];100:158-73. Available from: http://circres.ahajournals.org/content/100/2/158.abstract
10. Morrell NW, Bloch DB, Ten Dijke P, Goumans M-JTH, Hata A, Smith J, et al. Targeting BMP signalling in cardiovascular disease and anaemia. Nature reviews. Cardiology [Internet]. 2015 [cited 2015 Nov 2]; Available from: http://www.ncbi.nlm.nih.gov/pubmed/26461965
11. Beets K, Huylebroeck D, Moya IM, Umans L, Zwijsen A. Robustness in angiogenesis: Notch and BMP shaping waves. Trends Genet. 2013;29:140-9.
12. Heldin CH, Miyazono K, ten Dijke P. TGF-beta signalling from cell membrane to nucleus through SMAD proteins. Nature [Internet]. 1997 [cited 2016 Feb 4];390:465-71. Available from: http://www.ncbi.nlm.nih.gov/pubmed/9393997
13. de Vinuesa AG, Abdelilah-Seyfried S, Knaus P, Zwijsen A, Bailly S. BMP signaling in vascular biology and dysfunction. Cytokine & Growth Factor Reviews [Internet]. 2015 [cited 2016 Jan 5]; Available from: http://www.sciencedirect.com/science/article/pii/S1359610115000891
14. Guzman A, Zelman-Femiak M, Boergermann JH, Paschkowsky S, Kreuzaler PA, Fratzl P, et al. SMAD versus non-SMAD signaling is determined by lateral mobility of bone morphogenetic protein (BMP) receptors. The Journal of biological chemistry [Internet]. 2012 [cited 2016 Feb 3];287:39492-504. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3501045&tool=pmcentrez&rendertype=abstract
15. Massagué J. TGFß signalling in context. Nature reviews. Molecular cell biology [Internet]. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2012 [cited 2014 Jul 11];13:616-30. Available from: http://dx.doi.org/10.1038/nrm3434
16. Ramel MC, Hill CS. Spatial regulation of BMP activity. FEBS Lett. 2012;586:1929-41.
17. Bier E, De Robertis EM. EMBRYO DEVELOPMENT. BMP gradients: A paradigm for morphogen-mediated developmental patterning. Science (New York, N.Y.) [Internet]. 2015;348:aaa5838. Available from: http://www.sciencemag.org/cgi/doi/10.1126/science.aaa5838\nhttp://www.ncbi.nlm.nih.gov/pubmed/26113727
18. Zhou J, Lee P-L, Tsai C-S, Lee C-I, Yang T-L, Chuang H-S, et al. Force-specific activation of Smad1/5 regulates vascular endothelial cell cycle progression in response to disturbed flow. Proceedings of the National Academy of Sciences of the United States of America [Internet]. 2012 [cited 2016 Jan 20];109:7770-5. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3356658&tool=pmcentrez&rendertype=abstract
19. Vandersmissen I, Craps S, Depypere M, Coppiello G, van Gastel N, Maes F, et al. Endothelial Msx1 transduces hemodynamic changes into an arteriogenic remodeling response. The Journal of cell biology [Internet]. Rockefeller University Press; 2015 [cited 2016 Jan 23];210:1239-56. Available from: http://jcb.rupress.org/content/210/7/1239.full
20. Maddaluno L, Rudini N, Cuttano R, Bravi L, Giampietro C, Corada M, et al. EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature [Internet]. 2013 [cited 2016 Jan 13];498:492-6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23748444
21. Goumans M-J, Valdimarsdottir G, Itoh S, Lebrin F, Larsson J, Mummery C, et al. Activin Receptor-like Kinase (ALK)1 Is an Antagonistic Mediator of Lateral TGFß/ALK5 Signaling. Molecular Cell [Internet]. 2003 [cited 2016 Feb 2];12:817-28. Available from: http://www.sciencedirect.com/science/article/pii/S1097276503003861
22. Lowery JW, de Caestecker MP. BMP signaling in vascular development and disease. Cytokine & growth factor reviews [Internet]. 2010 [cited 2016 Jan 20];21:287-98. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2939258&tool=pmcentrez&rendertype=abstract
23. Govani FS, Shovlin CL. Hereditary haemorrhagic telangiectasia: a clinical and scientific review. European journal of human genetics : EJHG [Internet]. 2009; 17: 860-71. Available from:/pmc/articles/PMC2986493/?report=abstract
24. Tual-Chalot S, Oh SP, Arthur HM. Mouse models of hereditary hemorrhagic telangiectasia: Recent advances and future challenges. Front Genet. 2015.
25. Monteiro RM, De Sousa Lopes SMC, Bialecka M, De Boer S, Zwijsen A, Mummery CL. Real time monitoring of BMP Smads transcriptional activity during mouse development. Genesis. 2008;46:335-46.
26. Monteiro RM, de Sousa Lopes SMC, Korchynskyi O, ten Dijke P, Mummery CL. Spatio-temporal activation of Smad1 and Smad5 in vivo: monitoring transcriptional activity of Smad proteins. Journal of cell science [Internet]. 2004 [cited 2016 Feb 2];117:4653-63. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15331632
27. Collery RF, Link BA. Dynamic smad-mediated BMP signaling revealed through transgenic zebrafish. Developmental dynamics : an official publication of the American Association of Anatomists [Internet]. 2011 [cited 2016 Feb 2];240:712-22. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3072245&tool=pmcentrez&rendertype=abstract
28. Javier AL, Doan LT, Luong M, Reyes de Mochel NS, Sun A, Monuki ES, et al. Bmp indicator mice reveal dynamic regulation of transcriptional response. PloS one [Internet]. Public Library of Science; 2012 [cited 2016 Jan 20];7:e42566. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0042566
29. Laux DW, Febbo JA, Roman BL. Dynamic analysis of BMP-responsive smad activity in live zebrafish embryos. Developmental dynamics : an official publication of the American Association of Anatomists [Internet]. 2011 [cited 2016 Feb 2]; 240:682-94. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4287217&tool=pmcentrez&rendertype=abstract
30. Blank U, Seto ML, Adams DC, Wojchowski DM, Karolak MJ, Oxburgh L. An in vivo reporter of BMP signaling in organogenesis reveals targets in the developing kidney. BMC developmental biology [Internet]. 2008;8:86. Available from: http://www.biomedcentral.com/1471-213X/8/86
31. Leeuwis JW, Nguyen TQ, Chuva de Sousa Lopes SM, van der Giezen DM, van der Ven K, Rouw PJH, et al. Direct visualization of Smad1/5/8-mediated transcriptional activity identifies podocytes and collecting ducts as major targets of BMP signalling in healthy and diseased kidneys. The Journal of pathology [Internet]. 2011;224:121-32. Available from: http://www.ncbi.nlm.nih.gov/pubmed/21381028
32. Daly AC, Randall RA, Hill CS. Transforming growth factor beta-induced Smad1/5 phosphorylation in epithelial cells is mediated by novel receptor complexes and is essential for anchorage-independent growth. Molecular and cellular biology [Internet]. 2008 [cited 2016 Feb 19];28:6889-902. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2573298&tool=pmcentrez&rendertype=abstract
33. Goumans M-J, Valdimarsdottir G, Itoh S, Rosendahl A, Sideras P, ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. The EMBO journal [Internet]. 2002 [cited 2015 Nov 14];21:1743-53. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=125949&tool=pmcentrez&rendertype=abstract
34. Morikawa M, Koinuma D, Tsutsumi S, Vasilaki E, Kanki Y, Heldin C-H, et al. ChIP-seq reveals cell type-specific binding patterns of BMP-specific Smads and a novel binding motif. Nucleic acids research [Internet]. 2011 [cited 2016 Jan 20];39:8712-27. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3203580&tool=pmcentrez&rendertype=abstract
35. Raj A, Peskin CS, Tranchina D, Vargas DY, Tyagi S. Stochastic mRNA synthesis in mammalian cells. PLoS biology [Internet]. Public Library of Science; 2006 [cited 2015 Dec 16];4:e309. Available from: http://journals.plos.org/plosbiology/article?id=10.1371/journal.pbio.0040309
36. Chubb JR, Trcek T, Shenoy SM, Singer RH. Transcriptional pulsing of a developmental gene. Current biology : CB [Internet]. 2006 [cited 2016 Jan 25];16:1018-25. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16713960
37. Moya IM, Umans L, Maas E, Pereira PNG, Beets K, Francis A, et al. Stalk Cell Phenotype Depends on Integration of Notch and Smad1/5 Signaling Cascades. Dev Cell. 2012;22:501-14. Available from: http://linkinghub.elsevier.com/retrieve/pii/S153458071200041X.
38. Fantin A, Vieira JM, Plein A, Maden CH, Ruhrberg C. The embryonic mouse hindbrain as a qualitative and quantitative model for studying the molecular and cellular mechanisms of angiogenesis. Nature Protocols [Internet]. Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved.; 2013 [cited 2015 Dec 9];8:418-29. Available from: http://dx.doi.org/10.1038/nprot.2013.015
39. Kim RY, Robertson EJ, Solloway MJ. Bmp6 and Bmp7 are required for cushion formation and septation in the developing mouse heart. Developmental biology [Internet]. 2001 [cited 2015 Dec 11];235:449-66. Available from: http://www.sciencedirect.com/science/article/pii/S0012160601902842
40. Furuta Y, Piston D, Hogan B. Bone morphogenetic proteins (BMPs) as regulators of dorsal forebrain development. Development [Internet]. 1997 [cited 2016 Jan 31];124:2203-12. Available from: http://dev.biologists.org/content/124/11/2203.long
41. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, et al. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol. 2003;161:1163-77.
42. Milde F, Lauw S, Koumoutsakos P, Iruela-Arispe ML. The mouse retina in 3D: quantification of vascular growth and remodeling. Integr Biol. 2014;5:1426-38.
43. Garside VC, Chang AC, Karsan A, Hoodless PA. Co-ordinating Notch, BMP, and TGF-ß signaling during heart valve development. Cellular and molecular life sciences : CMLS [Internet]. 2013 [cited 2016 Jan 7]; 70:2899-917. Available from: http://www.ncbi.nlm.nih.gov/pubmed/23161060
44. Savolainen SM, Foley JF, Elmore SA. Histology atlas of the developing mouse heart with emphasis on E11.5 to E18.5. Toxicologic pathology [Internet]. 2009 [cited 2016 Jan 7];37:395-414. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2773446&tool=pmcentrez&rendertype=abstract
45. Kruithof BPT, Duim SN, Moerkamp AT, Goumans M-J. TGFß and BMP signaling in cardiac cushion formation: lessons from mice and chicken. Differentiation; research in biological diversity [Internet]. 2012 [cited 2016 Jan 7];84:89-102. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22656450
46. Wu B, Wang Y, Lui W, Langworthy M, Tompkins KL, Hatzopoulos AK, et al. Nfatc1 coordinates valve endocardial cell lineage development required for heart valve formation. Circulation research [Internet]. 2011 [cited 2016 Feb 3];109:183-92. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3132827&tool=pmcentrez&rendertype=abstract
47. Mukouyama YS, Shin D, Britsch S, Taniguchi M, Anderson DJ. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell. 2002;109:693-705.
48. Itoh F, Itoh S, Goumans M-J, Valdimarsdottir G, Iso T, Dotto GP, et al. Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. The EMBO journal [Internet]. European Molecular Biology Organization; 2004 [cited 2016 Feb 24];23:541-51. Available from:/pmc/articles/PMC1271801/?report=abstract
49. Hans F, Dimitrov S. Histone H3 phosphorylation and cell division. Oncogene [Internet]. Nature Publishing Group; 2001 [cited 2015 Nov 22];20:3021-7. Available from: http://www.nature.com/onc/journal/v20/n24/full/1204326a.html
50. Jakobsson L, Franco C, Bentley K, Collins RT, Ponsioen B, Aspalter IM, et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat Cell Biol. 2010;12:943-53.
51. Ricard N, Ciais D, Levet S, Subileau M, Mallet C, Zimmers TA, et al. BMP9 and BMP10 are critical for postnatal retinal vascular remodeling. Blood [Internet]. 2012 [cited 2016 Jan 5];119:6162-71. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3383024&tool=pmcentrez&rendertype=abstract
52. Ueki Y, Wilken MS, Cox KE, Chipman LB, Bermingham-McDonogh O, Reh TA. A transient wave of BMP signaling in the retina is necessary for Müller glial differentiation. Development (Cambridge, England) [Internet]. 2015 [cited 2016 Jan 24];142:533-43. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=4302996&tool=pmcentrez&rendertype=abstract
53. Fruttiger M. Development of the retinal vasculature. Angiogenesis [Internet]. 2007 [cited 2016 Feb 1];10:77-88. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17322966
54. Du Y, Xiao Q, Yip HK. Regulation of retinal progenitor cell differentiation by bone morphogenetic protein 4 is mediated by the smad/id cascade. Investigative ophthalmology & visual science [Internet]. The Association for Research in Vision and Ophthalmology; 2010 [cited 2016 Jan 24];51:3764-73. Available from: http://iovs.arvojournals.org/article.aspx?articleid=2127217
55. Ma L, Lu M-F, Schwartz RJ, Martin JF. Bmp2 is essential for cardiac cushion epithelial-mesenchymal transition and myocardial patterning. Development (Cambridge, England) [Internet]. 2005 [cited 2016 Jan 19];132:5601-11. Available from: http://dev.biologists.org/content/132/24/5601.long
56. McCulley DJ, Kang J-O, Martin JF, Black BL. BMP4 is required in the anterior heart field and its derivatives for endocardial cushion remodeling, outflow tract septation, and semilunar valve development. Developmental dynamics : an official publication of the American Association of Anatomists [Internet]. 2008 [cited 2016 Feb 1]; 237:3200-9. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2728547&tool=pmcentrez&rendertype=abstract
57. Gaussin V, Van de Putte T, Mishina Y, Hanks MC, Zwijsen A, Huylebroeck D, et al. Endocardial cushion and myocardial defects after cardiac myocyte-specific conditional deletion of the bone morphogenetic protein receptor ALK3. Proceedings of the National Academy of Sciences of the United States of America [Internet]. 2002 [cited 2016 Jan 26];99:2878-83. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=122441&tool=pmcentrez&rendertype=abstract
58. Wang J, Sridurongrit S, Dudas M, Thomas P, Nagy A, Schneider MD, et al. Atrioventricular cushion transformation is mediated by ALK2 in the developing mouse heart. Developmental biology [Internet]. 2005 [cited 2016 Feb 17];286:299-310. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=1361261&tool=pmcentrez&rendertype=abstract
59. Park C, Lavine K, Mishina Y, Deng C-X, Ornitz DM, Choi K. Bone morphogenetic protein receptor 1A signaling is dispensable for hematopoietic development but essential for vessel and atrioventricular endocardial cushion formation. Development (Cambridge, England) [Internet]. 2006 [cited 2016 Feb 19];133:3473-84. Available from: http://www.ncbi.nlm.nih.gov/pubmed/16887829
60. Beppu H, Malhotra R, Beppu Y, Lepore JJ, Parmacek MS, Bloch KD. BMP type II receptor regulates positioning of outflow tract and remodeling of atrioventricular cushion during cardiogenesis. Developmental biology [Internet]. 2009 [cited 2016 Feb 19];331:167-75. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2745439&tool=pmcentrez&rendertype=abstract
61. Délot EC, Bahamonde ME, Zhao M, Lyons KM. BMP signaling is required for septation of the outflow tract of the mammalian heart. Development (Cambridge, England) [Internet]. 2003 [cited 2016 Feb 19];130:209-20. Available from: http://www.ncbi.nlm.nih.gov/pubmed/12441304
62. Moskowitz IP, Wang J, Peterson MA, Pu WT, Mackinnon AC, Oxburgh L, et al. Transcription factor genes Smad4 and Gata4 cooperatively regulate cardiac valve development. [corrected]. Proceedings of the National Academy of Sciences of the United States of America [Internet]. 2011 [cited 2016 Feb 19];108:4006-11. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3053967&tool=pmcentrez&rendertype=abstract
63. Song L, Zhao M, Wu B, Zhou B, Wang Q, Jiao K. Cell autonomous requirement of endocardial Smad4 during atrioventricular cushion development in mouse embryos. Developmental dynamics : an official publication of the American Association of Anatomists [Internet]. 2011 [cited 2016 Feb 19];240:211-20. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3020975&tool=pmcentrez&rendertype=abstract
64. Galvin KM, Donovan MJ, Lynch CA, Meyer RI, Paul RJ, Lorenz JN, et al. A role for smad6 in development and homeostasis of the cardiovascular system. Nature genetics [Internet]. 2000 [cited 2016 Feb 19];24:171-4. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10655064
65. Yuan L, Chan GC, Beeler D, Janes L, Spokes KC, Dharaneeswaran H, et al. A role of stochastic phenotype switching in generating mosaic endothelial cell heterogeneity. Nat Commun. 2016;7:10160.
66. Neuhaus H, Rosen V, Thies RS. Heart specific expression of mouse BMP-10 a novel member of the TGF-beta superfamily. Mechanisms of development [Internet]. 1999 [cited 2016 Feb 19];80:181-4. Available from: http://www.ncbi.nlm.nih.gov/pubmed/10072785
67. Chen H, Shi S, Acosta L, Li W, Lu J, Bao S, et al. BMP10 is essential for maintaining cardiac growth during murine cardiogenesis. Development (Cambridge, England) [Internet]. 2004 [cited 2016 Jan 20];131:2219-31. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2628765&tool=pmcentrez&rendertype=abstract
68. Lan Y, Liu B, Yao H, Li F, Weng T, Yang G, et al. Essential role of endothelial Smad4 in vascular remodeling and integrity. Molecular and cellular biology [Internet]. 2007 [cited 2016 Feb 19];27:7683-92. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=2169040&tool=pmcentrez&rendertype=abstract
69. Levet S, Ciais D, Merdzhanova G, Mallet C, Zimmers T, Lee SJ, et al. Bone morphogenetic protein 9 (BMP9) controls lymphatic vessel maturation and valve formation. Blood. 2013;122:598-607.
70. Sun L, Rajamannan NM, Sucosky P. Defining the role of fluid shear stress in the expression of early signaling markers for calcific aortic valve disease. PloS one [Internet]. Public Library of Science; 2013 [cited 2016 Jan 20];8:e84433. Available from: http://journals.plos.org/plosone/article?id=10.1371/journal.pone.0084433
71. Sorescu GP. 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. Circulation Research [Internet]. 2004 [cited 2015 Nov 2];95:773-9. Available from: http://www.ncbi.nlm.nih.gov/pubmed/15388638
72. Bernier-Latmani J, Cisarovsky C, Demir CS, Bruand M, Jaquet M, Davanture S, et al.[Internet]. American Society for Clinical Investigation; 2015 [cited 2016 Jan 20];2015. Available from: https://www.jci.org/articles/view/82045/pdf
73. de Vinuesa AG, Abdelilah-Seyfried S, Knaus P, Zwijsen A, Bailly S. BMP signaling in vascular biology and dysfunction. Cytokine & Growth Factor Reviews [Internet]. Elsevier; 2015 [cited 2016 Jan 5]; Available from: http://www.cgfr.co.uk/article/S1359610115000891/fulltext
74. Wiley DM, Kim J-D, Hao J, Hong CC, Bautch VL, Jin S-W. Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nature cell biology [Internet]. 2011 [cited 2015 Dec 1];13:686-92. Available from: http://www.pubmedcentral.nih.gov/articlerender.fcgi?artid=3107371&tool=pmcentrez&rendertype=abstract
75. Sorensen LK, Brooke BS, Li DY, Urness LD. Loss of distinct arterial and venous boundaries in mice lacking endoglin, a vascular-specific TGF?? coreceptor. Dev Biol. 2003;261:235-50.
76. Oh SP, Seki T, Goss K, Imamura T, Yi Y, Donahoe PK, et al. Activin receptor-like kinase 1 modulates transforming growth factor-beta 1 signaling in the regulation of angiogenesis. Proc Natl Acad Sci U S A. 2000;97:2626-31.
77. Liu D, Wang J, Kinzel B, Müeller M, Mao X, Valdez R, et al. Dosage-dependent requirement of BMP type II receptor for maintenance of vascular integrity. Blood. 2007;110:1502-10.