The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development

Developmental Biology

Volumn 294, Issue 2, 2006, Pages 458-470

  Seo, Seungwoon ^a   Fujita, Hideo ^a   Nakano, Atsushi ^a   Kang, Myengmo ^a   Duarte, Antonio ^b   Kume, Tsutomu ^a  

^a VANDERBILT UNIVERSITY MEDICAL CENTER   (United States)

^b FACULDADE DE MEDICINA VETERINÁRIA   (Portugal)

Author keywords

Arterial venous specification; Forkhead; Lymphatic development; Notch; Vascular development; VEGF

Indexed keywords

BIOLOGICAL MARKER; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR; DELTA LIKE 4 PROTEIN; FORKHEAD TRANSCRIPTION FACTOR FOXC1; FORKHEAD TRANSCRIPTION FACTOR FOXC2; LIGAND; MUTANT PROTEIN; NOTCH1 RECEPTOR; REGULATOR PROTEIN; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; VASCULOTROPIN C;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTERIOVENOUS MALFORMATION; ARTERY; ARTICLE; BINDING SITE; CELL FATE; CELL MUTANT; CELL SPECIFICITY; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; EMBRYO; ENDOTHELIUM CELL; GENE ACTIVATION; GENE INDUCTION; GENE OVEREXPRESSION; LYMPH VESSEL ENDOTHELIUM; LYMPHANGIOGENESIS; MONKEY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPROUTING; VEIN;

VERTEBRATA;

EID: 33745099879     PISSN: 00121606     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.ydbio.2006.03.035     Document Type: Article

References (67)

1. Adams R.H., Wilkinson G.A., Weiss C., Diella F., Gale N.W., Deutsch U., Risau W., and Klein R. Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev. 13 (1999) 295-306
2. Alva J.A., and Iruela-Arispe M.L. Notch signaling in vascular morphogenesis. Curr. Opin. Hematol. 11 (2004) 278-283
3. Banerji S., Ni J., Wang S.X., Clasper S., Su J., Tammi R., Jones M., and Jackson D.G. LYVE-1, a new homologue of the CD44 glycoprotein, is a lymph-specific receptor for hyaluronan. J. Cell Biol. 144 (1999) 789-801
4. Berry F.B., Saleem R.A., and Walter M.A. FOXC1 transcriptional regulation is mediated by N- and C-terminal activation domains and contains a phosphorylated transcriptional inhibitory domain. J. Biol. Chem. 277 (2002) 10292-10297
5. Bi W., Drake C.J., and Schwarz J.J. The transcription factor MEF2C-null mouse exhibits complex vascular malformations and reduced cardiac expression of angiopoietin 1 and VEGF. Dev. Biol. 211 (1999) 255-267
6. Carlsson P., and Mahlapuu M. Forkhead transcription factors: key players in development and metabolism. Dev. Biol. 250 (2002) 1-23
7. Dagenais S.L., Hartsough R.L., Erickson R.P., Witte M.H., Butler M.G., and Glover T.W. Foxc2 is expressed in developing lymphatic vessels and other tissues associated with lymphedema-distichiasis syndrome. Gene Expression Patterns 4 (2004) 611-619
8. Daly C., Wong V., Burova E., Wei Y., Zabski S., Griffiths J., Lai K.M., Lin H.C., Ioffe E., Yancopoulos G.D., and Rudge J.S. Angiopoietin-1 modulates endothelial cell function and gene expression via the transcription factor FKHR (FOXO1). Genes Dev. 18 (2004) 1060-1071
9. Duarte A., Hirashima M., Benedito R., Trindade A., Diniz P., Bekman E., Costa L., Henrique D., and Rossant J. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev. 18 (2004) 2474-2478
10. Dumont D.J., Fong G.H., Puri M.C., Gradwohl G., Alitalo K., and Breitman M.L. Vascularization of the mouse embryo: a study of flk-1, tek, tie, and vascular endothelial growth factor expression during development. Dev. Dyn. 203 (1995) 80-92
11. Fang J., Dagenais S.L., Erickson R.P., Arlt M.F., Glynn M.W., Gorski J.L., Seaver L.H., and Glover T.W. Mutations in FOXC2 (MFH-1), a forkhead family transcription factor, are responsible for the hereditary lymphedema-distichiasis syndrome. Am. J. Hum. Genet. 67 (2000) 1382-1388
12. Fischer A., Schumacher N., Maier M., Sendtner M., and Gessler M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18 (2004) 901-911
13. Fujita H., Kang M., Eren M., Gleaves L.A., Vaughan D.E., and Kume T. Foxc2 is a common mediator of insulin and transforming growth factor beta signaling to regulate plasminogen activator inhibitor type I gene expression. Circ. Res. 98 (2006) 626-634
14. Gale N.W., and Yancopoulos G.D. Growth factors acting via endothelial cell-specific receptor tyrosine kinases: VEGFs, angiopoietins, and ephrins in vascular development. Genes Dev. 13 (1999) 1055-1066
15. Gale N.W., Dominguez M.G., Noguera I., Pan L., Hughes V., Valenzuela D.M., Murphy A.J., Adams N.C., Lin H.C., Holash J., Thurston G., and Yancopoulos G.D. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 15949-15954
16. Gaudet J., and Mango S.E. Regulation of organogenesis by the Caenorhabditis elegans FoxA protein PHA-4. Science 295 (2002) 821-825
17. Goumans M.J., Valdimarsdottir G., Itoh S., Rosendahl A., Sideras P., and ten Dijke P. Balancing the activation state of the endothelium via two distinct TGF-beta type I receptors. EMBO J. 21 (2002) 1743-1753
18. Hiemisch H., Monaghan A.P., Schutz G., and Kaestner K.H. Expression of the mouse Fkh1/Mf1 and Mfh1 genes in late gestation embryos is restricted to mesoderm derivatives. Mech. Dev. 73 (1998) 129-132
19. Hong Y.K., Shin J.W., and Detmar M. Development of the lymphatic vascular system: a mystery unravels. Dev. Dyn. 231 (2004) 462-473
20. Huber T.L., Kouskoff V., Fehling H.J., Palis J., and Keller G. Haemangioblast commitment is initiated in the primitive streak of the mouse embryo. Nature 432 (2004) 625-630
21. Iida K., Koseki H., Kakinuma H., Kato N., Mizutani-Koseki Y., Ohuchi H., Yoshioka H., Noji S., Kawamura K., Kataoka Y., Ueno F., Taniguchi M., Yoshida N., Sugiyama T., and Miura N. Essential roles of the winged helix transcription factor MFH-1 in aortic arch patterning and skeletogenesis. Development 124 (1997) 438-4627
22. Kaestner K.H., Knochel W., and Martinez D.E. Unified nomenclature for the winged helix/forkhead transcription factors. Genes Dev. 14 (2000) 142-146
23. Kappel A., Schlaeger T.M., Flamme I., Orkin S.H., Risau W., and Breier G. Role of SCL/Tal-1, GATA, and ets transcription factor binding sites for the regulation of flk-1 expression during murine vascular development. Blood 96 (2000) 3078-3085
24. Karkkainen M.J., Haiko P., Sainio K., Partanen J., Taipale J., Petrova T.V., Jeltsch M., Jackson D.G., Talikka M., Rauvala H., Betsholtz C., and Alitalo K. Vascular endothelial growth factor C is required for sprouting of the first lymphatic vessels from embryonic veins. Nat. Immunol. 5 (2004) 74-80
25. Kidson S.H., Kume T., Deng K., Winfrey V., and Hogan B.L. The forkhead/winged-helix gene, Mf1, is necessary for the normal development of the cornea and formation of the anterior chamber in the mouse eye. Dev. Biol. 211 (1999) 306-322
26. Kokubo H., Miyagawa-Tomita S., Tomimatsu H., Nakashima Y., Nakazawa M., Saga Y., and Johnson R.L. Targeted disruption of hesr2 results in atrioventricular valve anomalies that lead to heart dysfunction. Circ. Res. 95 (2004) 540-547
27. Kokubo H., Miyagawa-Tomita S., Nakazawa M., Saga Y., and Johnson R.L. Mouse hesr1 and hesr2 genes are redundantly required to mediate Notch signaling in the developing cardiovascular system. Dev. Biol. 278 (2005) 301-309
28. Krebs L.T., Shutter J.R., Tanigaki K., Honjo T., Stark K.L., and Gridley T. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 18 (2004) 2469-2473
29. Kriederman B.M., Myloyde T.L., Witte M.H., Dagenais S.L., Witte C.L., Rennels M., Bernas M.J., Lynch M.T., Erickson R.P., Caulder M.S., Miura N., Jackson D., Brooks B.P., and Glover T.W. FOXC2 haploinsufficient mice are a model for human autosomal dominant lymphedema-distichiasis syndrome. Hum. Mol. Genet. 12 (2003) 1179-1185
30. Kume T., Deng K.Y., Winfrey V., Gould D.B., Walter M.A., and Hogan B.L. The forkhead/winged helix gene Mf1 is disrupted in the pleiotropic mouse mutation congenital hydrocephalus. Cell 93 (1998) 985-996
31. Kume T., Deng K., and Hogan B.L. Minimal phenotype of mice homozygous for a null mutation in the forkhead/winged helix gene, Mf2. Mol. Cell. Biol. 20 (2000) 1419-1425
32. Kume T., Deng K., and Hogan B.L. Murine forkhead/winged helix genes Foxc1 (Mf1) and Foxc2 (Mfh1) are required for the early organogenesis of the kidney and urinary tract. Development 127 (2000) 1387-1395
33. Kume T., Jiang H., Topczewska J.M., and Hogan B.L. The murine winged helix transcription factors, Foxc1 and Foxc2, are both required for cardiovascular development and somitogenesis. Genes Dev. 15 (2001) 2470-2482
34. Lawson N.D., and Weinstein B.M. Arteries and veins: making a difference with zebrafish. Nat. Rev., Genet. 3 (2002) 674-682
35. Lawson N.D., Scheer N., Pham V.N., Kim C.H., Chitnis A.B., Campos-Ortega J.A., and Weinstein B.M. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128 (2001) 3675-3683
36. Lawson N.D., Vogel A.M., and Weinstein B.M. Sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation. Dev. Cell 3 (2002) 127-136
37. Lawson N.D., Mugford J.W., Diamond B.A., and Weinstein B.M. Phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 17 (2003) 1346-1351
38. Le Noble F., Moyon D., Pardanaud L., Yuan L., Djonov V., Matthijsen R., Breant C., Fleury V., and Eichmann A. Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131 (2004) 361-375
39. Liu Z.J., Shirakawa T., Li Y., Soma A., Oka M., Dotto G.P., Fairman R.M., Velazquez O.C., and Herlyn M. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol. Cell. Biol. 23 (2003) 14-25
40. McGrath K.E., Koniski A.D., Malik J., and Palis J. Circulation is established in a stepwise pattern in the mammalian embryo. Blood 101 (2003) 1669-1676
41. Minami T., Kuivenhoven J.A., Evans V., Kodama T., Rosenberg R.D., and Aird W.C. Ets motifs are necessary for endothelial cell-specific expression of a 723-bp Tie-2 promoter/enhancer in Hprt targeted transgenic mice. Arterioscler., Thromb., Vasc. Biol. 23 (2003) 2041-2047
42. Miquerol L., Gertsenstein M., Harpal K., Rossant J., and Nagy A. Multiple developmental roles of VEGF suggested by a LacZ-tagged allele. Dev. Biol. 212 (1999) 307-322
43. Moyon D., Pardanaud L., Yuan L., Breant C., and Eichmann A. Plasticity of endothelial cells during arterial-venous differentiation in the avian embryo. Development 128 (2001) 3359-3370
44. Mukouyama Y., Shin D., Britsch S., Taniguchi M., and Anderson D.J. Sensory nerves determine the pattern of arterial differentiation and blood vessel branching in the skin. Cell 109 (2002) 693-705
45. Oettgen P. Transcriptional regulation of vascular development. Circ. Res. 89 (2001) 380-388
46. Oliver G. Lymphatic vasculature development. Nat. Rev., Immunol. 4 (2004) 35-45
47. Petrova T.V., Karpanen T., Norrmen C., Mellor R., Tamakoshi T., Finegold D., Ferrell R., Kerjaschki D., Mortimer P., Yla-Herttuala S., Miura N., and Alitalo K. Defective valves and abnormal mural cell recruitment underlie lymphatic vascular failure in lymphedema distichiasis. Nat. Med. 10 (2004) 974-981
48. Pierrou S., Hellqvist M., Samuelsson L., Enerback S., and Carlsson P. Cloning and characterization of seven human forkhead proteins: binding site specificity and DNA bending. EMBO J. 13 (1994) 5002-5012
49. Rossant J., and Howard L. Signaling pathways in vascular development. Annu. Rev. Cell Dev. Biol. 18 (2002) 541-573
50. 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
51. Sasaki H., and Hogan B.L. Differential expression of multiple fork head related genes during gastrulation and axial pattern formation in the mouse embryo. Development 118 (1993) 47-59
52. Shawber C.J., Das I., Francisco E., and Kitajewski J. Notch signaling in primary endothelial cells. Ann. N. Y. Acad. Sci. 995 (2003) 162-170
53. Shutter J.R., Scully S., Fan W., Richards W.G., Kitajewski J., Deblandre G.A., Kintner C.R., and Stark K.L. Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev. 14 (2000) 1313-1318
54. Smith R.S., Zabaleta A., Kume T., Savinova O.V., Kidson S.H., Martin J.E., Nishimura D.Y., Alward W.L., Hogan B.L., and John S.W. Haploinsufficiency of the transcription factors FOXC1 and FOXC2 results in aberrant ocular development. Hum. Mol. Genet. 9 (2000) 1021-1032
55. Stalmans I., Ng Y.S., Rohan R., Fruttiger M., Bouche A., Yuce A., Fujisawa H., Hermans B., Shani M., Jansen S., Hicklin D., Anderson D.J., Gardiner T., Hammes H.P., Moons L., Dewerchin M., Collen D., Carmeliet P., and D'Amore P.A. Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109 (2002) 327-336
56. Uyttendaele H., Ho J., Rossant J., and Kitajewski J. Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 5643-5648
57. van Dongen M.J., Cederberg A., Carlsson P., Enerback S., and Wikstrom M. Solution structure and dynamics of the DNA-binding domain of the adipocyte-transcription factor FREAC-11. J. Mol. Biol. 296 (2000) 351-359
58. Villa N., Walker L., Lindsell C.E., Gasson J., Iruela-Arispe M.L., and Weinmaster G. Vascular expression of Notch pathway receptors and ligands is restricted to arterial vessels. Mech. Dev. 108 (2001) 161-164
59. Visconti R.P., Richardson C.D., and Sato T.N. Orchestration of angiogenesis and arteriovenous contribution by angiopoietins and vascular endothelial growth factor (VEGF). Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 8219-8224
60. Wang H.U., Chen Z.F., and Anderson D.J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93 (1998) 741-753
61. Wilm B., James R.G., Schultheiss T.M., and Hogan B.L. The forkhead genes, Foxc1 and Foxc2, regulate paraxial versus intermediate mesoderm cell fate. Dev. Biol. 271 (2004) 176-189
62. Winnier G.E., Hargett L., and Hogan B.L. The winged helix transcription factor MFH1 is required for proliferation and patterning of paraxial mesoderm in the mouse embryo. Genes Dev. 11 (1997) 926-940
63. Winnier G.E., Kume T., Deng K., Rogers R., Bundy J., Raines C., Walter M.A., Hogan B.L., and Conway S.J. Roles for the winged helix transcription factors MF1 and MFH1 in cardiovascular development revealed by nonallelic noncomplementation of null alleles. Dev. Biol. 213 (1999) 418-431
64. Wu J., Iwata F., Grass J.A., Osborne C.S., Elnitski L., Fraser P., Ohneda O., Yamamoto M., and Bresnick E.H. Molecular determinants of NOTCH4 transcription in vascular endothelium. Mol. Cell. Biol. 25 (2005) 1458-1474
65. Yamagishi H., Maeda J., Hu T., McAnally J., Conway S.J., Kume T., Meyers E.N., Yamagishi C., and Srivastava D. Tbx1 is regulated by tissue-specific forkhead proteins through a common Sonic hedgehog-responsive enhancer. Genes Dev. 17 (2003) 269-281
66. You L.R., Lin F.J., Lee C.T., DeMayo F.J., Tsai M.J., and Tsai S.Y. Suppression of Notch signalling by the COUP-TFII transcription factor regulates vein identity. Nature 435 (2005) 98-104
67. Zhong T.P., Childs S., Leu J.P., and Fishman M.C. Gridlock signalling pathway fashions the first embryonic artery. Nature 414 (2001) 216-220