Serum Response Factor Is Required for Sprouting Angiogenesis and Vascular Integrity

Developmental Cell

Volumn 15, Issue 3, 2008, Pages 448-461

  Franco, Claudio Areias ^a,b   Mericskay, Mathias ^a,b   Parlakian, Ara ^a,b   Gary Bobo, Guillaume ^a,b   Gao Li, Jacqueline ^a,b   Paulin, Denise ^b   Gustafsson, Erika ^c   Li, Zhenlin ^a,b  

^a SORBONNE UNIVERSITÉ   (France)

^b CNRS   (France)

^c LUND UNIVERSITY   (Sweden)

Author keywords

CELLBIO; DEVBIO

Indexed keywords

BETA ACTIN; CADHERIN; CYTOSKELETON PROTEIN; FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; SERUM RESPONSE FACTOR; SMALL INTERFERING RNA; TRANSCRIPTION FACTOR; VASCULOTROPIN;

ACTIN FILAMENT; ACTIN POLYMERIZATION; ANEURYSM; ANGIOGENESIS; ANIMAL TISSUE; ARTICLE; BLEEDING; CAPILLARY DENSITY; CELL JUNCTION; CELL MIGRATION; CELL TYPE; CONTROLLED STUDY; EMBRYO; EMBRYO DEATH; ENDOTHELIUM CELL; ENZYME PHOSPHORYLATION; FILOPODIUM; IMMEDIATE EARLY GENE; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION;

ACTINS; ANEURYSM; ANIMALS; ANTIGENS, CD; BLOOD VESSELS; CADHERINS; EMBRYO, MAMMALIAN; ENDOTHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FEMALE; FIBROBLAST GROWTH FACTORS; GENE DELETION; GENE EXPRESSION PROFILING; HEMORRHAGE; INTERCELLULAR JUNCTIONS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEOVASCULARIZATION, PHYSIOLOGIC; RECEPTOR, TIE-1; RNA, SMALL INTERFERING; SERUM RESPONSE FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 51449099892     PISSN: 15345807     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.devcel.2008.07.019     Document Type: Article

References (44)

1. Adams R.H., and Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8 (2007) 464-478
2. Arsenian S., Weinhold B., Oelgeschläger M., Rüther U., and Nordheim A. Serum response factor is essential for mesoderm formation during mouse embryogenesis. EMBO J. 17 (1998) 6289-6299
3. Blum Y., Belting H.G., Ellertsdottir E., Herwig L., Lüders F., and Affolter M. Complex cell rearrangements during intersegmental vessel sprouting and vessel fusion in the zebrafish embryo. Dev. Biol. 316 (2008) 312-322 10.1016/j.ydbio.2008.01.038 Published online February 13, 2008
4. Carmeliet P. Angiogenesis in life, disease and medicine. Nature 438 (2005) 932-936
5. Centanin L., Dekanty A., Romero N., Irisarri M., Gorr T.A., and Wappner P. Cell autonomy of HIF effects in Drosophila: tracheal cells sense hypoxia and induce terminal branch sprouting. Dev. Cell 14 (2008) 547-558
6. Chai J., and Tarnawski A.S. Serum response factor: discovery, biochemistry, biological roles and implications for tissue injury healing. J. Physiol. Pharmacol. 53 (2002) 147-157
7. Chai J., Jones M.K., and Tarnawski A.S. Serum response factor is a critical requirement for VEGF signalling in endothelial cells and VEGF-induced angiogenesis. FASEB J. 18 (2004) 1264-1266
8. Colucci-Guyon E., Portier M.M., Dunia I., Paulin D., Pournin S., and Babinet C. Mice lacking vimentin develop and reproduce without an obvious phenotype. Cell 79 (1994) 679-694
9. Dejana E., Taddei A., and Randi A.M. Foxs and Ets in the transcriptional regulation of endothelial cell differentiation and angiogenesis. Biochim. Biophys. Acta 1775 (2007) 298-312
10. Eichmann A., Makinen T., and Alitalo K. Neural guidance molecules regulate vascular remodeling and vessel navigation. Genes Dev. 19 (2005) 1013-1021
11. Gerhardt H., Golding M., Fruttiger M., Ruhrberg C., Lundkvist A., Abramsson A., Jeltsch M., Mitchell C., Alitalo K., Shima D., and Betsholtz C. VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J. Cell Biol. 161 (2003) 1163-1177 10.1083/jcb.200302047 Published online June 16, 2003
12. Gridley T. Notch signaling in vascular development and physiology. Development 134 (2007) 2709-2718 10.1242/dev.004184 Published online July 4, 2007
13. Guillemin K., Groppe J., Ducker K., Treisman R., Hafen E., Affolter M., and Krasnow M.A. The pruned gene encodes the Drosophila serum response factor and regulates cytoplasmic outgrowth during terminal branching of the tracheal system. Development 122 (1996) 1353-1362
14. Gustafsson E., Brakebusch C., Hietanen K., and Fässler R. Tie-1-directed expression of Cre recombinase in endothelial cells of embryoid bodies and transgenic mice. J. Cell Sci. 114 (2001) 671-676
15. Hanahan D., and Folkman J. Patterns and emerging mechanisms of the angiogenic switch during tumorigenesis. Cell 86 (1996) 353-364
16. Hellström M., Kalén M., Lindahl P., Abramsson A., and Betsholtz C. Role of PDGF-B and PDGFR-β in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126 (1999) 3047-3055
17. 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 445 (2007) 776-780 10.1038/nature05571
18. Johnson D.W., Berg J.N., Baldwin M.A., Gallione C.J., Marondel I., Yoon S.J., Stenzel T.T., Speer M., Pericak-Vance M.A., Diamond A., et al. Mutations in the activin receptor-like kinase 1 gene in hereditary haemorrhagic telangiectasia type 2. Nat. Genet. 13 (1996) 189-195
19. Knöll B., Kretz O., Fiedler C., Alberti S., Schütz G., Frotscher M., and Nordheim A. Serum response factor controls neuronal circuit assembly in the hippocampus. Nat. Neurosci. 9 (2006) 195-204 10.1038/nn1627 Published online January 15, 2006
20. Lamalice L., Houle F., Jourdan G., and Huot J. Phosphorylation of tyrosine 1214 on VEGFR2 is required for VEGF-induced activation of Cdc42 upstream of SAPK2/p38. Oncogene 23 (2004) 434-445
21. Lamalice L., Le Boeuf F., and Huot J. Endothelial cell migration during angiogenesis. Circ. Res. 100 (2007) 782-794
22. Lampugnani M.G., and Dejana E. Adherens junctions in endothelial cells regulate vessel maintenance and angiogenesis. Thromb. Res. 120 Suppl 2 (2007) S1-S6
23. McAllister K.A., Grogg K.M., Johnson D.W., Gallione C.J., Baldwin M.A., Jackson C.E., Helmbold E.A., Markel D.S., McKinnon W.C., Murrell J., et al. Endoglin, a TGF-β binding protein of endothelial cells, is the gene for hereditary haemorrhagic telangiectasia type 1. Nat. Genet. 8 (1994) 345-351
24. Mericskay M., Blanc J., Tritsch E., Moriez R., Aubert P., Neunlist M., Feil R., and Li Z. Inducible mouse model of chronic intestinal pseudo-obstruction by smooth muscle-specific inactivation of the SRF gene. Gastroenterology 133 (2007) 1960-1970 10.1053/j.gastro.2007.09.010 Published online September 16, 2007
25. Miano J.M. Serum response factor: toggling between disparate programs of gene expression. J. Mol. Cell. Cardiol. 35 (2003) 577-593
26. Miano J.M., Ramanan N., Georger M.A., de Mesy Bentley K.L., Emerson R.L., Balza Jr. R.O., Xiao Q., Weiler H., Ginty D.D., and Misra R.P. Restricted inactivation of serum response factor to the cardiovascular system. Proc. Natl. Acad. Sci. USA 101 (2004) 17132-17137 10.1073/pnas.0406041101 Published online November 29, 2004
27. Niu Z., Yu W., Zhang S.X., Barron M., Belaguli N.S., Schneider M.D., Parmacek M., Nordheim A., and Schwartz R.J. Conditional mutagenesis of the murine serum response factor gene blocks cardiogenesis and the transcription of downstream gene targets. J. Biol. Chem. 280 (2005) 32531-32538 10.1074/jbc.M501372200 Published online May 31, 2005
28. Parlakian A., Tuil D., Hamard G., Tavernier G., Hentzen D., Concordet J.P., Paulin D., Li Z., and Daegelen D. Targeted inactivation of serum response factor in the developing heart results in myocardial defects and embryonic lethality. Mol. Cell. Biol. 24 (2004) 5281-5289
29. Parlakian A., Charvet C., Escoubet B., Mericskay M., Molkentin J.D., Gary-Bobo G., De Windt L.J., Ludosky M.A., Paulin D., Daegelen D., et al. Temporally controlled onset of dilated cardiomyopathy through disruption of the SRF gene in adult heart. Circulation 112 (2005) 2930-2939
30. Pollard T.D. The cytoskeleton, cellular motility and the reductionist agenda. Nature 422 (2003) 741-745
31. Ridley A.J. Rho GTPases and actin dynamics in membrane protrusions and vesicle trafficking. Trends Cell Biol. 16 (2006) 522-529 10.1016/j.tcb.2006.08.006 Published online September 1, 2006
32. Risau W. Mechanisms of angiogenesis. Nature 386 (1997) 671-674
33. Roca C., and Adams R.H. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 21 (2007) 2511-2524
34. Ruhrberg C., Gerhardt H., Golding M., Watson R., Ioannidou S., Fujisawa H., Betsholtz C., and Shima D.T. Spatially restricted patterning cues provided by heparin-binding VEGF-A control blood vessel branching morphogenesis. Genes Dev. 16 (2002) 2684-2698
35. Shweiki D., Itin A., Soffer D., and Keshet E. Vascular endothelial growth factor induced by hypoxia may mediate hypoxia-initiated angiogenesis. Nature 359 (1992) 843-845
36. Somogyi K., and Rørth P. Evidence for tension-based regulation of Drosophila MAL and SRF during invasive cell migration. Dev. Cell 7 (2004) 85-93
37. Soriano P. Generalized lacZ expression with the ROSA26 Cre reporter strain. Nat. Genet. 21 (1999) 70-71
38. Sotiropoulos A., Gineitis D., Copeland J., and Treisman R. Signal-regulated activation of serum response factor is mediated by changes in actin dynamics. Cell 98 (1999) 159-169
39. Suchting S., Freitas C., le Noble F., Benedito R., Bréant C., Duarte A., and Eichmann A. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl. Acad. Sci. USA 104 (2007) 3225-3230 10.1073/pnas.0611177104 Published online February 12, 2007
40. Sun Q., Chen G., Streb J.W., Long X., Yang Y., Stoeckert Jr. C.J., and Miano J.M. Defining the mammalian CArGome. Genome Res. 16 (2006) 197-207 Published online December 19, 2005
41. Torres-Vázquez J., Gitler A.D., Fraser S.D., Berk J.D., Pham V.N., Fishman M.C., Childs S., Epstein J.A., and Weinstein B.M. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev. Cell 7 (2004) 117-123
42. Treisman R. Identification and purification of a polypeptide that binds to the c-fos serum response element. EMBO J. 6 (1987) 2711-2717
43. Vestweber D. VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler. Thromb. Vasc. Biol. 28 (2008) 223-232 10.1161/ATVBAHA.107.158014 Published online December 27, 2007
44. Wickramasinghe S.R., Alvania R.S., Ramanan N., Wood J.N., Mandai K., and Ginty D.D. Serum response factor mediates NGF-dependent target innervation by embryonic DRG sensory neurons. Neuron 58 (2008) 532-545