Stalk Cell Phenotype Depends on Integration of Notch and Smad1/5 Signaling Cascades

Developmental Cell

Volumn 22, Issue 3, 2012, Pages 501-514

  Moya, Iván M ^a   Umans, Lieve ^a   Maas, Elke ^a   Pereira, Paulo N G ^a   Beets, Karen ^a   Francis, Annick ^a   Sents, Ward ^a   Robertson, Elizabeth J ^b   Mummery, Christine L ^c   Huylebroeck, Danny ^a   Zwijsen, An ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

BONE MORPHOGENETIC PROTEIN; INHIBITOR OF DIFFERENTIATION 1; INHIBITOR OF DIFFERENTIATION 2; INHIBITOR OF DIFFERENTIATION 3; JAGGED1; NOTCH RECEPTOR; SMAD1 PROTEIN; SMAD5 PROTEIN; TRANSCRIPTION FACTOR HES 1; TRANSFORMING GROWTH FACTOR BETA; VASCULOTROPIN RECEPTOR 1;

ANGIOGENESIS; ARTICLE; CELL POLARITY; CELL SELECTION; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENDOTHELIUM CELL; GENE TARGETING; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; VASCULARIZATION;

ANIMALS; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CALCIUM-BINDING PROTEINS; CELL CYCLE PROTEINS; CELLS, CULTURED; DOWN-REGULATION; HOMEODOMAIN PROTEINS; HUMANS; INHIBITOR OF DIFFERENTIATION PROTEIN 1; INHIBITOR OF DIFFERENTIATION PROTEIN 2; INHIBITOR OF DIFFERENTIATION PROTEINS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; PHENOTYPE; SIGNAL TRANSDUCTION; SMAD1 PROTEIN; SMAD5 PROTEIN; VASCULAR ENDOTHELIAL GROWTH FACTOR RECEPTOR-1;

MOYA;

EID: 84858286273     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.01.007     Document Type: Article

References (41)

1. Bai G., Sheng N., Xie Z., Bian W., Yokota Y., Benezra R., Kageyama R., Guillemot F., Jing N. Id sustains Hes1 expression to inhibit precocious neurogenesis by releasing negative autoregulation of Hes1. Dev. Cell 2007, 13:283-297.
2. Bentley K., Mariggi G., Gerhardt H., Bates P.A. Tipping the balance: robustness of tip cell selection, migration and fusion in angiogenesis. PLoS Comput. Biol. 2009, 5:e1000549.
3. Chang H., Huylebroeck D., Verschueren K., Guo Q., Matzuk M.M., Zwijsen A. Smad5 knockout mice die at mid-gestation due to multiple embryonic and extraembryonic defects. Development 1999, 126:1631-1642.
4. Dahlqvist C., Blokzijl A., Chapman G., Falk A., Dannaeus K., Ibâñez C.F., Lendahl U. Functional Notch signaling is required for BMP4-induced inhibition of myogenic differentiation. Development 2003, 130:6089-6099.
5. David L., Feige J.J., Bailly S. Emerging role of bone morphogenetic proteins in angiogenesis. Cytokine Growth Factor Rev. 2009, 20:203-212.
6. De Smet F., Segura I., De Bock K., Hohensinner P.J., Carmeliet P. Mechanisms of vessel branching: filopodia on endothelial tip cells lead the way. Arterioscler. Thromb. Vasc. Biol. 2009, 29:639-649.
7. Eilken H.M., Adams R.H. Dynamics of endothelial cell behavior in sprouting angiogenesis. Curr. Opin. Cell Biol. 2010, 22:617-625.
8. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 2003, 161:1163-1177.
9. Hao J., Ho J.N., Lewis J.A., Karim K.A., Daniels R.N., Gentry P.R., Hopkins C.R., Lindsley C.W., Hong C.C. In vivo structure-activity relationship study of dorsomorphin analogues identifies selective VEGF and BMP inhibitors. ACS Chem. Biol. 2010, 5:245-253.
10. Harrington L.S., Sainson R.C., Williams C.K., Taylor J.M., Shi W., Li J.L., Harris A.L. Regulation of multiple angiogenic pathways by Dll4 and Notch in human umbilical vein endothelial cells. Microvasc. Res. 2008, 75:144-154.
11. Hellström M., Phng L.-K., Hofmann J.J., Wallgard E., Coultas L., Lindblom P., Alva J., Nilsson A.-K., Karlsson L., Gaiano N., et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 2007, 445:776-780.
12. Henderson A.M., Wang S.J., Taylor A.C., Aitkenhead M., Hughes C.C. The basic helix-loop-helix transcription factor HESR1 regulates endothelial cell tube formation. J. Biol. Chem. 2001, 276:6169-6176.
13. Holderfield M.T., Henderson Anderson A.M., Kokubo H., Chin M.T., Johnson R.L., Hughes C.C. HESR1/CHF2 suppresses VEGFR2 transcription independent of binding to E-boxes. Biochem. Biophys. Res. Commun. 2006, 346:637-648.
14. Hu-Lowe D.D., Chen E., Zhang L., Watson K.D., Mancuso P., Lappin P., Wickman G., Chen J.H., Wang J., Jiang X., et al. Targeting activin receptor-like kinase 1 inhibits angiogenesis and tumorigenesis through a mechanism of action complementary to anti-VEGF therapies. Cancer Res. 2011, 71:1362-1373.
15. Itoh F., Itoh S., Goumans M.J., Valdimarsdottir G., Iso T., Dotto G.P., Hamamori Y., Kedes L., Kato M., ten Dijke Pt P. Synergy and antagonism between Notch and BMP receptor signaling pathways in endothelial cells. EMBO J. 2004, 23:541-551.
16. Jakobsson L., Franco C.A., Bentley K., Collins R.T., Ponsioen B., Aspalter I.M., Rosewell I., Busse M., Thurston G., Medvinsky A., et al. Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting. Nat. Cell Biol. 2010, 12:943-953.
17. Kobayashi T., Kageyama R. Hes1 regulates embryonic stem cell differentiation by suppressing Notch signaling. Genes Cells 2010, 15:689-698.
18. Kobayashi T., Mizuno H., Imayoshi I., Furusawa C., Shirahige K., Kageyama R. The cyclic gene Hes1 contributes to diverse differentiation responses of embryonic stem cells. Genes Dev. 2009, 23:1870-1875.
19. Lechleider R.J., Ryan J.L., Garrett L., Eng C., Deng C., Wynshaw-Boris A., Roberts A.B. Targeted mutagenesis of Smad1 reveals an essential role in chorioallantoic fusion. Dev. Biol. 2001, 240:157-167.
20. Leslie J.D., Ariza-McNaughton L., Bermange A.L., McAdow R., Johnson S.L., Lewis J. Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 2007, 134:839-844.
21. Lobov I.B., Renard R.A., Papadopoulos N., Gale N.W., Thurston G., Yancopoulos G.D., Wiegand S.J. Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc. Natl. Acad. Sci. USA 2007, 104:3219-3224.
22. Lyden D., Young A.Z., Zagzag D., Yan W., Gerald W., O'Reilly R., Bader B.L., Hynes R.O., Zhuang Y., Manova K., Benezra R. Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 1999, 401:670-677.
23. Monteiro R.M., de Sousa Lopes S.M., Bialecka M., de Boer S., Zwijsen A., Mummery C.L. Real time monitoring of BMP Smads transcriptional activity during mouse development. Genesis 2008, 46:335-346.
24. Morikawa M., Koinuma D., Tsutsumi S., Vasilaki E., Kanki Y., Heldin C.H., Aburatani H., Miyazono K. ChIP-seq reveals cell type-specific binding patterns of BMP-specific Smads and a novel binding motif. Nucleic Acids Res. 2011, 39:8712-8727.
25. Noguera-Troise I., Daly C., Papadopoulos N.J., Coetzee S., Boland P., Gale N.W., Lin H.C., Yancopoulos G.D., Thurston G. Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Nature 2006, 444:1032-1037.
26. Norton J.D., Atherton G.T. Coupling of cell growth control and apoptosis functions of Id proteins. Mol. Cell. Biol. 1998, 18:2371-2381.
27. Pardali E., Goumans M.J., ten Dijke P. Signaling by members of the TGF-beta family in vascular morphogenesis and disease. Trends Cell Biol. 2010, 20:556-567.
28. Pi X., Ren R., Kelley R., Zhang C., Moser M., Bohil A.B., Divito M., Cheney R.E., Patterson C. Sequential roles for myosin-X in BMP6-dependent filopodial extension, migration, and activation of BMP receptors. J. Cell Biol. 2007, 179:1569-1582.
29. Quillien A., Blanco-Sanchez B., Halluin C., Moore J.C., Lawson N.D., Blader P., Cau E. BMP signaling orchestrates photoreceptor specification in the zebrafish pineal gland in collaboration with Notch. Development 2011, 138:2293-2302.
30. Ridgway J., Zhang G., Wu Y., Stawicki S., Liang W.C., Chanthery Y., Kowalski J., Watts R.J., Callahan C., Kasman I., et al. Inhibition of Dll4 signalling inhibits tumour growth by deregulating angiogenesis. Nature 2006, 444:1083-1087.
31. Ruhrberg C., Gerhardt H., Golding M., Watson R., Ioannidou S., Fujisawa H., Betsholtz C., Shima D.T. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 2002, 16:2684-2698.
32. Shimojo H., Ohtsuka T., Kageyama R. Oscillations in notch signaling regulate maintenance of neural progenitors. Neuron 2008, 58:52-64.
33. Siekmann A.F., Lawson N.D. Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 2007, 445:781-784.
34. Tremblay K.D., Dunn N.R., Robertson E.J. Mouse embryos lacking Smad1 signals display defects in extra-embryonic tissues and germ cell formation. Development 2001, 128:3609-3621.
35. Umans L., Vermeire L., Francis A., Chang H., Huylebroeck D., Zwijsen A. Generation of a floxed allele of Smad5 for cre-mediated conditional knockout in the mouse. Genesis 2003, 37:5-11.
36. Umans L., Cox L., Tjwa M., Bito V., Vermeire L., Laperre K., Sipido K., Moons L., Huylebroeck D., Zwijsen A. Inactivation of Smad5 in endothelial cells and smooth muscle cells demonstrates that Smad5 is required for cardiac homeostasis. Am. J. Pathol. 2007, 170:1460-1472.
37. Valdimarsdottir G., Goumans M.J., Rosendahl A., Brugman M., Itoh S., Lebrin F., Sideras P., ten Dijke P. 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.
38. Wiley D.M., Kim J.D., Hao J., Hong C.C., Bautch V.L., Jin S.W. Distinct signalling pathways regulate sprouting angiogenesis from the dorsal aorta and the axial vein. Nat. Cell Biol. 2011, 13:686-692.
39. Yang X., Castilla L.H., Xu X., Li C., Gotay J., Weinstein M., Liu P.P., Deng C.X. Angiogenesis defects and mesenchymal apoptosis in mice lacking SMAD5. Development 1999, 126:1571-1580.
40. Yoshiura S., Ohtsuka T., Takenaka Y., Nagahara H., Yoshikawa K., Kageyama R. Ultradian oscillations of Stat, Smad, and Hes1 expression in response to serum. Proc. Natl. Acad. Sci. USA 2007, 104:11292-11297.
41. Zebedee Z., Hara E. Id proteins in cell cycle control and cellular senescence. Oncogene 2001, 20:8317-8325.