Sox17 is indispensable for acquisition and maintenance of arterial identity

Nature Communications

Volumn 4, Issue , 2013, Pages

  Corada, Monica ^a   Orsenigo, Fabrizio ^a   Morini, Marco Francesco ^a   Pitulescu, Mara Elena ^b   Bhat, Ganesh ^a   Nyqvist, Daniel ^c   Breviario, Ferruccio ^a   Conti, Valentina ^d   Briot, Anais ^e   Iruela Arispe, M Luisa ^e   Adams, Ralf H ^b   Dejana, Elisabetta ^a,f  

^a FIRC INSTITUTE OF MOLECULAR ONCOLOGY   (Italy)

^b UNIVERSITY OF MÜNSTER   (Germany)

^c KAROLINSKA INSTITUTE   (Sweden)

^d Section of Nutrition Metabolism   (Italy)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f UNIVERSITY OF MILAN   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; BETA CATENIN; CD31 ANTIGEN; CD45 ANTIGEN; CHEMOKINE RECEPTOR CXCR4; CHICKEN OVALBUMIN UPSTREAM PROMOTER TRANSCRIPTION FACTOR 2; DESMIN; EPHRIN; EPHRIN B2; EPHRIN B4; HEY 1 PROTEIN; ISOLECTIN B4; NOTCH LIGAND DELTA LIKE 1; NOTCH LIGAND DELTA LIKE 4; NOTCH RECEPTOR; NOTCH1 RECEPTOR; NOTCH4 RECEPTOR; TRANSCRIPTION FACTOR SOX17; UNCLASSIFIED DRUG; WNT PROTEIN;

ADULT; CARDIOVASCULAR SYSTEM; EMBRYO; EYE; GENE EXPRESSION; RODENT;

ANIMAL CELL; ARTERIAL IDENTITY; ARTERIOVENOUS MALFORMATION; ARTERY DIAMETER; ARTERY ENDOTHELIUM; ARTICLE; BLOOD VESSEL PARAMETERS; BRAIN BLOOD VESSEL; CELL DIFFERENTIATION; CELL ISOLATION; CHROMATIN IMMUNOPRECIPITATION; CONSENSUS SEQUENCE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; EMBRYO DEATH; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IMMUNOHISTOCHEMISTRY; MESENTERIC ARTERY; MESENTERIC VEIN; MOUSE; NEWBORN; NONHUMAN; POSTNATAL DEVELOPMENT; PROMOTER REGION; PROTEIN EXPRESSION; RETINA; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; UMBILICAL VEIN ENDOTHELIAL CELL; UPREGULATION; WNT SIGNALING PATHWAY; YOLK SAC;

ANIMALS; ARTERIES; CELL DIFFERENTIATION; CELL PROLIFERATION; EMBRYO, MAMMALIAN; ENDODERM; ENDOTHELIAL CELLS; GENE EXPRESSION REGULATION, DEVELOPMENTAL; HMGB PROTEINS; MICE; MORPHOGENESIS; NEOVASCULARIZATION, PATHOLOGIC; RECEPTORS, NOTCH; RETINA; SIGNAL TRANSDUCTION; SOXF TRANSCRIPTION FACTORS; VEINS; WNT PROTEINS;

EID: 84886678124     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms3609     Document Type: Article

References (55)

1. Adams, R. H. & Alitalo, K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat. Rev. Mol. Cell Biol. 8, 464-478 (2007). (Pubitemid 46823443)
2. Potente, M., Gerhardt, H. & Carmeliet, P. Basic and therapeutic aspects of angiogenesis. Cell 146, 873-887 (2011).
3. Swift, M. R. & Weinstein, B. M. Arterial-venous specification during development. Circ. Res. 104, 576-588 (2009).
4. Wang, H. U., Chen, Z. F. & Anderson, D. J. Molecular distinction and angiogenic interaction between embryonic arteries and veins revealed by ephrin-B2 and its receptor Eph-B4. Cell 93, 741-753 (1998). (Pubitemid 28257581)
5. De Val, S. & Black, B. L. Transcriptional control of endothelial cell development. Dev. Cell 16, 180-195 (2009).
6. Dejana, E. The role of wnt signalling in physiological and pathological angiogenesis. Circ. Res. 107, 943-952 (2010).
7. Lin, F. J., Tsai, M. J. & Tsai, S. Y. Artery and vein formation: a tug of war between different forces. EMBO Rep. 8, 920-924 (2007). (Pubitemid 47500474)
8. Liu, Z. J. et al. Regulation of Notch1 and Dll4 by vascular endothelial growth factor in arterial endothelial cells: implications for modulating arteriogenesis and angiogenesis. Mol. Cell Biol. 23, 14-25 (2003).
9. Phng, L. K. & Gerhardt, H. Angiogenesis: a team effort coordinated by notch. Dev. Cell 16, 196-208 (2009).
10. Seo, S. et al. The forkhead transcription factors, Foxc1 and Foxc2, are required for arterial specification and lymphatic sprouting during vascular development. Dev. Biol. 294, 458-470 (2006). (Pubitemid 43884821)
11. Benedito, R. & Hellstrom, M. Notch as a hub for signalling in angiogenesis. Exp. Cell Res. 319, 1281-1288 (2013).
12. Kume, T. Novel insights into the differential functions of Notch ligands in vascular formation. J. Angiogenes. Res. 1, 8 (2009).
13. Lawson, N. D. et al. Notch signalling is required for arterial-venous differentiation during embryonic vascular development. Development 128, 3675-3683 (2001). (Pubitemid 32998917)
14. Trindade, A. et al. Overexpression of delta-like 4 induces arterialization and attenuates vessel formation in developing mouse embryos. Blood 112, 1720-1729 (2008).
15. Gale, N. W. et al. Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc. Natl Acad. Sci. USA 101, 15949-15954 (2004). (Pubitemid 39507907)
16. Krebs, L. T. et al. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 18, 2469-2473 (2004). (Pubitemid 39362888)
17. Limbourg, A. et al. Notch ligand Delta-like 1 is essential for postnatal arteriogenesis. Circ. Res. 100, 363-371 (2007).
18. Corada, M. et al. The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signalling. Dev. Cell 18, 938-949 (2010).
19. Francois, M., Koopman, P. & Beltrame, M. SoxF genes: Key players in the development of the cardio-vascular system. Int. J. Biochem. Cell Biol. 42, 445-448 (2010).
20. Wegner, M. All purpose Sox: The many roles of Sox proteins in gene expression. Int. J. Biochem. Cell Biol. 42, 381-390 (2010).
21. Kormish, J. D., Sinner, D. & Zorn, A. M. Interactions between SOX factors and Wnt/beta-catenin signalling in development and disease. Dev. Dyn. 239, 56-68 (2010).
22. Kim, I., Saunders, T. L. & Morrison, S. J. Sox17 dependence distinguishes the transcriptional regulation of fetal from adult hematopoietic stem cells. Cell 130, 470-483 (2007). (Pubitemid 47208520)
23. Francois, M. et al. Sox18 induces development of the lymphatic vasculature in mice. Nature 456, 643-647 (2008).
24. Sakamoto, Y. et al. Redundant roles of Sox17 and Sox18 in early cardiovascular development of mouse embryos. Biochem. Biophys. Res. Commun. 360, 539-544 (2007). (Pubitemid 47048133)
25. Cermenati, S. et al. Sox18 and Sox7 play redundant roles in vascular development. Blood 111, 2657-2666 (2008).
26. Herpers, R., van de Kamp, E., Duckers, H. J. & Schulte-Merker, S. Redundant roles for sox7 and sox18 in arteriovenous specification in zebrafish. Circ. Res. 102, 12-15 (2008).
27. Pendeville, H. et al. Zebrafish Sox7 and Sox18 function together to control arterial-venous identity. Dev. Biol. 317, 405-416 (2008).
28. Irrthum, A. et al. Mutations in the transcription factor gene SOX18 underlie recessive and dominant forms of hypotrichosis-lymphedema- telangiectasia. Am. J. Hum. Genet. 72, 1470-1478 (2003). (Pubitemid 36628386)
29. James, K., Hosking, B., Gardner, J., Muscat, G. E. & Koopman, P. Sox18 mutations in the ragged mouse alleles ragged-like and opossum. Genesis 36, 1-6 (2003). (Pubitemid 36666232)
30. Wang, Y. et al. Ephrin-B2 controls VEGF-induced angiogenesis and lymphangiogenesis. Nature 465, 483-486 (2010).
31. Izumi, N. et al. Fbxw7 controls angiogenesis by regulating endothelial Notch activity. PLoS One 7, e41116 (2012).
32. Yamamizu, K. et al. Convergence of Notch and beta-catenin signalling induces arterial fate in vascular progenitors. J. Cell Biol. 189, 325-338 (2010).
33. Ye, X. et al. Norrin, frizzled-4, and Lrp5 signalling in endothelial cells controls a genetic program for retinal vascularization. Cell 139, 285-298 (2009).
34. Liao, W. P., Uetzmann, L., Burtscher, I. & Lickert, H. Generation of a mouse line expressing Sox17-driven Cre recombinase with specific activity in arteries. Genesis 47, 476-483 (2009).
35. Yang, H. et al. Sox17 promotes tumor angiogenesis and destabilizes tumor vessels in mice. J. Clin. Invest. 123, 418-431 (2013).
36. Sacilotto, N. et al. Analysis of Dll4 regulation reveals a combinatorial role for Sox and Notch in arterial development. Proc. Natl Acad. Sci. USA 110, 11893-11898 (2013).
37. Hosking, B. et al. Sox7 and Sox17 are strain-specific modifiers of the lymphangiogenic defects caused by Sox18 dysfunction in mice. Development 136, 2385-2391 (2009).
38. Matsui, T. et al. Redundant roles of Sox17 and Sox18 in postnatal angiogenesis in mice. J. Cell Sci. 119, 3513-3526 (2006). (Pubitemid 44501857)
39. Clarke, R. L. et al. The expression of Sox17 identifies and regulates haemogenic endothelium. Nat. Cell Biol. 15, 502-510 (2013).
40. Benedito, R. et al. Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484, 110-114 (2012).
41. Ye, X., Wang, Y. & Nathans, J. The Norrin/Frizzled4 signalling pathway in retinal vascular development and disease. Trends Mol. Med. 16, 417-425 (2010).
42. Bilguvar, K. et al. Susceptibility loci for intracranial aneurysm in European and Japanese populations. Nat. Genet. 40, 1472-1477 (2008).
43. Foroud, T. et al. Genome-wide association study of intracranial aneurysms confirms role of Anril and SOX17 in disease risk. Stroke 43, 2846-2852 (2012).
44. Fernandez, P. C. et al. Genomic targets of the human c-Myc protein. Genes Dev. 17, 1115-1129 (2003). (Pubitemid 36534986)
45. Brault, V. et al. Inactivation of the beta-catenin gene by Wnt1-Cre-mediated deletion results in dramatic brain malformation and failure of craniofacial development. Development 128, 1253-1264 (2001). (Pubitemid 32409648)
46. Harada, N. et al. Intestinal polyposis in mice with a dominant stable mutation of the beta-catenin gene. EMBO J. 18, 5931-5942 (1999). (Pubitemid 29515670)
47. Murtaugh, L. C., Stanger, B. Z., Kwan, K. M. & Melton, D. A. Notch signalling controls multiple steps of pancreatic differentiation. Proc. Natl Acad. Sci. USA 100, 14920-14925 (2003). (Pubitemid 37517992)
48. Claxton, S. et al. Efficient, inducible Cre-recombinase activation in vascular endothelium. Genesis 46, 74-80 (2008). (Pubitemid 351498176)
49. Koch, U. et al. Delta-like 4 is the essential, nonredundant ligand for Notch1 during thymic T cell lineage commitment. J. Exp. Med. 205, 2515-2523 (2008).
50. Han, H. et al. Inducible gene knockout of transcription factor recombination signal binding protein-J reveals its essential role in T versus B lineage decision. Int. Immunol. 14, 637-645 (2002). (Pubitemid 34649719)
51. Kisanuki, Y. Y. et al. Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev. Biol. 230, 230-242 (2001). (Pubitemid 32171420)
52. Cattelino, A. et al. The conditional inactivation of the beta-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility. J. Cell Biol. 162, 1111-1122 (2003). (Pubitemid 37174193)
53. Lampugnani, M. G., Orsenigo, F., Gagliani, M. C., Tacchetti, C. & Dejana, E. Vascular endothelial cadherin controls VEGFR-2 internalization and signalling from intracellular compartments. J. Cell Biol. 174, 593-604 (2006). (Pubitemid 44231870)
54. Taddei, A. et al. Endothelial adherens junctions control tight junctions by VE-cadherin-mediated upregulation of claudin-5. Nat. Cell Biol. 10, 923-934 (2008).
55. Baluk, P. et al. Functionally specialized junctions between endothelial cells of lymphatic vessels. J. Exp. Med. 204, 2349-2362 (2007). (Pubitemid 47529321)