Animals; Base Sequence; Basic Helix-Loop-Helix Transcription Factors/metabolism; Blood Vessels/*embryology; Cloning, Molecular; Cluster Analysis; DNA Primers/genetics; DNA-Binding Proteins/genetics/*metabolism; *Gene Expression Regulation, Developmental; In Situ Hybridization; Mesoderm/metabolism; Molecular Sequence Data; *Phenotype; Sequence Analysis, DNA; Signal Transduction/*physiology; Zebrafish/*embryology; Zebrafish Proteins/genetics/*metabolism
Abstract :
[en] Sox7 and Sox18 are members of the F-subgroup of Sox transcription factors family and are mostly expressed in endothelial compartments. In humans, dominant mutations in Sox18 are the underlying cause of the severe hypotrichosis-lymphedema-telangiectasia disorder characterized by vascular defects. However little is known about which vasculogenic processes Sox7 and Sox18 regulate in vivo. We cloned the orthologs of Sox7 and Sox18 in zebrafish, analysed their expression pattern and performed functional analyses. Both genes are expressed in the lateral plate mesoderm during somitogenesis. At later stages, Sox18 is expressed in all axial vessels whereas Sox7 expression is mainly restricted to the dorsal aorta. Knockdown of Sox7 or Sox18 alone failed to reveal any phenotype. In contrast, blocking the two genes simultaneously led to embryos displaying dysmorphogenesis of the proximal aorta and arteriovenous shunts, all of which can account for the lack of circulation observed in the trunk and tail. Gene expression analyses performed with general endothelial markers on double morphants revealed that Sox7 and Sox18 are dispensable for the initial specification and positioning of the major trunk vessels. However, morphants display ectopic expression of the venous Flt4 marker in the dorsal aorta and a concomitant reduction of the artery-specific markers EphrinB2a and Gridlock. The striking similarities between the phenotype of Sox7/Sox18 morphants and Gridlock mutants strongly suggest that Sox7 and Sox18 control arterial-venous identity by regulating Gridlock expression.
Disciplines :
Biochemistry, biophysics & molecular biology
Author, co-author :
Pendeville-Samain, Hélène ; Université de Liège - ULiège > Département des sciences de la vie > GIGA-R : Biologie et génétique moléculaire
Winandy, Marie ; Université de Liège - ULiège > GIGA-Management : Plate-forme zebrafish
J. Alexander D.Y. Stainier A molecular pathway leading to endoderm formation in zebrafish Curr. Biol. 9 1999 1147 1157
D.R. Bielenberg M. Klagsbrun Targeting endothelial and tumor cells with semaphorins Cancer Metastasis Rev. 26 3–4 2007 421 431
J. Bowles G. Schepers P. Koopman Phylogeny of the SOX family of developmental transcription factors based on sequence and structural indicators Dev. Biol. 227 2000 239 255
L.A. Brown A.R. Rodaway T.F. Schilling T. Jowett P.W. Ingham R.K. Patient A.D. Sharrocks Insights into early vasculogenesis revealed by expression of the ETS-domain transcription factor Fli-1 in wild-type and mutant zebrafish embryos Mech. Dev. 90 2000 237 252
T.W. Chittenden F. Claes A.A. Lanahan M. Autiero R.T. Palac E.V. Tkachenko A. Elfenbein C. Ruiz de Almodovar E. Dedkov R. Tomanek W. Li M. Westmore J.P. Singh A. Horowitz M.J. Mulligan-Kehoe K.L. Moodie Z.W. Zhuang P. Carmeliet M. Simons Selective regulation of arterial branching morphogenesis by synectin Dev. Cell 10 2006 783 795
L.D. Covassin J.A. Villefranc M.C. Kacergis B.M. Weinstein N.D. Lawson Distinct genetic interactions between multiple Vegf receptors are required for development of different blood vessel types in zebrafish Proc. Natl. Acad. Sci. U. S. A. 103 2006 6554 6559
I.A. Darby T. Bisucci S. Raghoenath J. Olsson G.E. Muscat P. Koopman Sox18 is transiently expressed during angiogenesis in granulation tissue of skin wounds with an identical expression pattern to Flk-1 mRNA Lab. Invest. 81 2001 937 943
H.W. Detrich III M.W. Kieran F.Y. Chan L.M. Barone K. Yee J.A. Rundstadler S. Pratt D. Ransom L.I. Zon Intraembryonic hematopoietic cell migration during vertebrate development Proc. Natl. Acad. Sci. U. S. A. 92 1995 10713 10717
M. Downes P. Koopman SOX18 and the transcriptional regulation of blood vessel development Trends Cardiovasc. Med. 11 2001 318 324
I. Flamme T. Frolich W. Risau Molecular mechanisms of vasculogenesis and embryonic angiogenesis J. Cell. Physiol. 173 1997 206 210
B. Fouquet B.M. Weinstein F.C. Serluca M.C. Fishman Vessel patterning in the embryo of the zebrafish: guidance by notochord Dev. Biol. 183 1997 37 48
M. Garcia-Ramirez J. Martinez-Gonzalez J.O. Juan-Babot C. Rodriguez L. Badimon Transcription factor SOX18 is expressed in human coronary atherosclerotic lesions and regulates DNA synthesis and vascular cell growth Arterioscler. Thromb. Vasc. Biol. 25 2005 2398 2403
M. Gering R. Patient Hedgehog signaling is required for adult blood stem cell formation in zebrafish embryos Dev. Cell 8 2005 389 400
M. Gering A.R. Rodaway B. Gottgens R.K. Patient A.R. Green The SCL gene specifies haemangioblast development from early mesoderm EMBO J. 17 1998 4029 4045
K. Goishi M. Klagsbrun Vascular endothelial growth factor and its receptors in embryonic zebrafish blood vessel development Curr. Top. Dev. Biol. 62 2004 127 152
L.F. Hennequin A.P. Thomas C. Johnstone E.S. Stokes P.A. Ple J.J. Lohmann D.J. Ogilvie M. Dukes S.R. Wedge J.O. Curwen J. Kendrew C. Lambert-van der Brempt Design and structure–activity relationship of a new class of potent VEGF receptor tyrosine kinase inhibitors J. Med. Chem. 42 1999 5369 5389
B.M. Hosking S.C. Wang S.L. Chen S. Penning P. Koopman G.E. Muscat SOX18 directly interacts with MEF2C in endothelial cells Biochem. Biophys. Res. Commun. 287 2001 493 500
B.M. Hosking S.C. Wang M. Downes P. Koopman G.E. Muscat The VCAM-1 gene that encodes the vascular cell adhesion molecule is a target of the Sry-related high mobility group box gene, Sox18 J. Biol. Chem. 279 2004 5314 5322
A. Irrthum K. Devriendt D. Chitayat G. Matthijs C. Glade P.M. Steijlen J.P. Fryns M.A. Van Steensel M. Vikkula Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis–lymphedema–telangiectasia Am. J. Hum. Genet. 72 2003 1470 1478
S. Isogai M. Horiguchi B.M. Weinstein The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development Dev. Biol. 230 2001 278 301
Y.J. Jiang M. Brand C.P. Heisenberg D. Beuchle M. Furutani-Seiki R.N. Kelsh R.M. Warga M. Granato P. Haffter M. Hammerschmidt D.A. Kane M.C. Mullins J. Odenthal F.J. van Eeden C. Nusslein-Volhard Mutations affecting neurogenesis and brain morphology in the zebrafish, Danio rerio Development 123 1996 205 216
S.W. Jin D. Beis T. Mitchell J.N. Chen D.Y. Stainier Cellular and molecular analyses of vascular tube and lumen formation in zebrafish Development 132 2005 5199 5209
C.B. Kimmel W.W. Ballard S.R. Kimmel B. Ullmann T.F. Schilling Stages of embryonic development of the zebrafish Dev. Dyn. 203 1995 253 310
R.E. Lamont S. Childs MAPping out arteries and veins Sci. STKE 2006 2006 2006 e39
N.D. Lawson B.M. Weinstein In vivo imaging of embryonic vascular development using transgenic zebrafish Dev. Biol. 248 2002 307 318
N.D. Lawson N. Scheer V.N. Pham C.H. Kim A.B. Chitnis J.A. Campos-Ortega B.M. Weinstein Notch signaling is required for arterial–venous differentiation during embryonic vascular development Development 128 2001 3675 3683
N.D. Lawson A.M. Vogel B.M. Weinstein sonic hedgehog and vascular endothelial growth factor act upstream of the Notch pathway during arterial endothelial differentiation Dev. Cell 3 2002 127 136
D. Liang J.R. Chang A.J. Chin A. Smith C. Kelly E.S. Weinberg R. Ge The role of vascular endothelial growth factor (VEGF) in vasculogenesis, angiogenesis, and hematopoiesis in zebrafish development Mech. Dev. 108 2001 29 43
M.S. Lyons B. Bell D. Stainier K.G. Peters Isolation of the zebrafish homologues for the tie-1 and tie-2 endothelium-specific receptor tyrosine kinases Dev. Dyn. 212 1998 133 140
C. Mailhos U. Modlich J. Lewis A. Harris R. Bicknell D. Ish-Horowicz Delta4, an endothelial specific notch ligand expressed at sites of physiological and tumor angiogenesis Differentiation 69 2001 135 144
A. Majumdar K. Lun M. Brand I.A. Drummond Zebrafish no isthmus reveals a role for pax2.1 in tubule differentiation and patterning events in the pronephric primordia Development 127 2000 2089 2098
T. Matsui M. Kanai-Azuma K. Hara S. Matoba R. Hiramatsu H. Kawakami M. Kurohmaru P. Koopman Y. Kanai Redundant roles of Sox17 and Sox18 in postnatal angiogenesis in mice J. Cell Sci. 119 2006 3513 3526
A. Nasevicius J. Larson S.C. Ekker Distinct requirements for zebrafish angiogenesis revealed by a VEGF-A morphant Yeast 17 2000 294 301
E.A. Ober B. Olofsson T. Makinen S.W. Jin W. Shoji G.Y. Koh K. Alitalo D.Y. Stainier Vegfc is required for vascular development and endoderm morphogenesis in zebrafish EMBO Rep. 5 2004 78 84
L.J. Patterson R. Patient The “Ets” factor: vessel formation in zebrafish—the missing link? PLoS Biol. 4 2006 e24
D. Pennisi J. Bowles A. Nagy G. Muscat P. Koopman Mice null for sox18 are viable and display a mild coat defect Mol. Cell. Biol. 20 2000 9331 9336
D. Pennisi J. Gardner D. Chambers B. Hosking J. Peters G. Muscat C. Abbott P. Koopman Mutations in Sox18 underlie cardiovascular and hair follicle defects in ragged mice Nat. Genet. 24 2000 434 437
V.N. Pham N.D. Lawson J.W. Mugford L. Dye D. Castranova B. Lo B.M. Weinstein Combinatorial function of ETS transcription factors in the developing vasculature Dev. Biol. 303 2007 772 783
W. Risau Mechanisms of angiogenesis Nature 386 1997 671 674
Y. Sakamoto K. Hara M. Kanai-Azuma T. Matsui Y. Miura N. Tsunekawa M. Kurohmaru Y. Saijoh P. Koopman Y. Kanai Redundant roles of Sox17 and Sox18 in early cardiovascular development of mouse embryos Biochem. Biophys. Res. Commun. 360 2007 539 544
D.P. Szeto K.J. Griffin D. Kimelman HrT is required for cardiovascular development in zebrafish Development 129 2002 5093 5101
W. Takash J. Canizares N. Bonneaud F. Poulat M.G. Mattei P. Jay P. Berta SOX7 transcription factor: sequence, chromosomal localisation, expression, transactivation and interference with Wnt signalling Nucleic Acids Res. 29 2001 4274 4283
C. Thisse L.I. Zon Organogenesis—heart and blood formation from the zebrafish point of view Science 295 2002 457 462
C. Thisse B. Thisse T.F. Schilling J.H. Postlethwait Structure of the zebrafish snail1 gene and its expression in wild-type, spadetail and no tail mutant embryos Development 119 1993 1203 1215
J. Torres-Vazquez A.D. Gitler S.D. Fraser J.D. Berk N.P. Van M.C. Fishman S. Childs J.A. Epstein B.M. Weinstein Semaphorin–plexin signaling guides patterning of the developing vasculature Dev. Cell 7 2004 117 123
B. Weinstein Vascular cell biology in vivo: a new piscine paradigm? Trends Cell Biol. 12 2002 439 445
B.M. Weinstein Plumbing the mysteries of vascular development using the zebrafish Semin. Cell Dev. Biol. 13 2002 515 522
N. Young C.N. Hahn A. Poh C. Dong D. Wilhelm J. Olsson G.E. Muscat P. Parsons J.R. Gamble P. Koopman Effect of disrupted SOX18 transcription factor function on tumor growth, vascularization, and endothelial development J. Natl. Cancer Inst. 98 2006 1060 1067
T.P. Zhong M. Rosenberg M.A. Mohideen B. Weinstein M.C. Fishman gridlock, an HLH gene required for assembly of the aorta in zebrafish Science 287 2000 1820 1824
T.P. Zhong S. Childs J.P. Leu M.C. Fishman Gridlock signalling pathway fashions the first embryonic artery Nature 414 2001 216 220