A Snail1/Notch1 signalling axis controls embryonic vascular development

Nature Communications

Volumn 5, Issue , 2014, Pages

  Wu, Zhao Qiu ^a,b   Rowe, R Grant ^a,b,f   Lim, Kim Chew ^c   Lin, Yongshun ^a,b,g   Willis, Amanda ^b   Tang, Yi ^a,b   Li, Xiao Yan ^a,b   Nor, Jacques E ^e   Maillard, Ivan ^b,c,d   Weiss, Stephen J ^a,b  

^a Molecular Medicine and Genetics   (United States)

^b Life Sciences Institute   (United States)

^c Department of Cell and Developmental Biology ^*  (United States)

^d Division of Hematology Oncology 3216 Cancer Center   (United States)

^e UNIVERSITY OF MICHIGAN   (United States)

^f BOSTON CHILDREN S HOSPITAL   (United States)

^g NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DLL4 PROTEIN; GAMMA SECRETASE; MEMBRANE RECEPTOR; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR SNAIL; TRANSCRIPTION FACTOR SNAIL1; UNCLASSIFIED DRUG; VASCULOTROPIN; DLL4 PROTEIN, MOUSE; MEMBRANE PROTEIN; NOTCH1 PROTEIN, MOUSE; SIGNAL PEPTIDE; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR; VASCULAR ENDOTHELIAL GROWTH FACTOR A, MOUSE; VASCULOTROPIN A;

CELL ORGANELLE; DEVELOPMENTAL BIOLOGY; EMBRYONIC DEVELOPMENT; ENZYME ACTIVITY; GENE EXPRESSION; INHIBITION; MOLECULAR ANALYSIS; NUMERICAL MODEL; SIGNALING;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BLOOD VESSEL WALL; CONTROLLED STUDY; EMBRYO; EMBRYO DEVELOPMENT; ENDOTHELIUM CELL; ENZYME ACTIVITY; ENZYME INHIBITION; GENE EXPRESSION; GENE REPRESSION; GENE TARGETING; IN VITRO STUDY; IN VIVO STUDY; LOSS OF FUNCTION MUTATION; MOUSE; NONHUMAN; PERICYTE; RECEPTOR UPREGULATION; SIGNAL TRANSDUCTION; VASCULARIZATION; ANIMAL; BLOOD VESSEL; EMBRYOLOGY; EPITHELIAL MESENCHYMAL TRANSITION; FEEDBACK SYSTEM; GENETICS; KNOCKOUT MOUSE; METABOLISM; VASCULAR REMODELING;

ANIMALS; BLOOD VESSELS; ENDOTHELIAL CELLS; EPITHELIAL-MESENCHYMAL TRANSITION; FEEDBACK, PHYSIOLOGICAL; IN VITRO TECHNIQUES; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; VASCULAR ENDOTHELIAL GROWTH FACTOR A; VASCULAR REMODELING;

EID: 84901916408     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms4998     Document Type: Article

References (70)

1. Phng, L. K. &Gerhardt, H. Angiogenesis: a team effort coordinated by Notch. Dev. Cell 16, 196-208 (2009).
2. de la Pompa, J. L. &Epstein, J. A. Coordinating tissue interactions: Notch signaling in cardiac development and disease. Dev. Cell 22, 244-254 (2012).
3. Limbourg, F. P. et al. Essential role of endothelial Notch1 in angiogenesis. Circulation 111, 1826-1832 (2005). (Pubitemid 40525149)
4. Trindade, A. et al. Overexpression of delta-like 4 induces arterialization and attenuates vessel formation in developing mouse embryos. Blood 112, 1720-1729 (2008).
5. Venkatesh, D. A. et al. Cardiovascular and hematopoietic defects associated with Notch1 activation in embryonic Tie2-expressing populations. Circ. Res. 103, 423-431 (2008).
6. Corada, M. et al. The Wnt/beta-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/Notch signaling. Dev. Cell 18, 938-949 (2010).
7. 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).
8. Wythe, J. D. et al. ETS factors regulate Vegf-dependent arterial specification. Dev. Cell 26, 45-58 (2013).
9. Yamamizu, K. et al. Convergence of Notch and beta-catenin signaling induces arterial fate in vascular progenitors. J. Cell Biol. 189, 325-338 (2010).
10. 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)
11. Krebs, L. T. et al. Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev. 18, 2469-2473 (2004). (Pubitemid 39362888)
12. Duarte, A. et al. Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev. 18, 2474-2478 (2004). (Pubitemid 39362889)
13. Nieto, M. A. The ins and outs of the epithelial to mesenchymal transition in health and disease. Annu. Rev. Cell Dev. Biol. 27, 347-376 (2011).
14. Carver, E. A., Jiang, R., Lan, Y., Oram, K. F. &Gridley, T. The mouse Snail gene encodes a key regulator of the epithelial-mesenchymal transition. Mol. Cell Biol. 21, 8184-8188 (2001). (Pubitemid 33051806)
15. Murray, S. A. &Gridley, T. Snail family genes are required for left-right asymmetry determination, but not neural crest formation, in mice. Proc. Natl Acad. Sci. USA 103, 10300-10304 (2006). (Pubitemid 44051161)
16. Lomeli, H., Starling, C. &Gridley, T. Epiblast-specific Snai1 deletion results in embryonic lethality due to multiple vascular defects. BMC Res. Notes 2, 22 (2009).
17. Rowe, R. G. et al. Mesenchymal cells reactivate Snail1 expression to drive threedimensional invasion programs. J. Cell Biol. 184, 399-408 (2009).
18. 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)
19. de Boer, J. et al. Transgenic mice with hematopoietic and lymphoid specific expression of Cre. Eur. J. Immunol. 33, 314-325 (2003).
20. Ruiz-Herguido, C. et al. Hematopoietic stem cell development requires transient Wnt/beta-catenin activity. J. Exp. Med. 209, 1457-1468 (2012).
21. Walls, J. R., Coultas, L., Rossant, J. &Henkelman, R. M. Three-dimensional analysis of vascular development in the mouse embryo. PLoS One 3, e2853 (2008).
22. Vega, S. et al. Snail blocks the cell cycle and confers resistance to cell death. Genes Dev. 18, 1131-1143 (2004). (Pubitemid 38669034)
23. Lin, Y. et al. Snail1-dependent control of embryonic stem cell pluripotency and lineage commitment. Nat. Commun. 5, 3070 (2014).
24. Tang, Y. et al. MT1-MMP-dependent control of skeletal stem cell commitment via a beta1-integrin/YAP/TAZ signaling axis. Dev. Cell. 25, 402-416 (2013).
25. Lavine, K. J., Long, F., Choi, K., Smith, C. &Ornitz, D. M. Hedgehog signaling to distinct cell types differentially regulates coronary artery and vein development. Development 135, 3161-3171 (2008).
26. Morimoto, M. et al. Canonical Notch signaling in the developing lung is required for determination of arterial smooth muscle cells and selection of Clara versus ciliated cell fate. J. Cell Sci. 123, 213-224 (2010).
27. Fischer, A., Schumacher, N., Maier, M., Sendtner, M. &Gessler, M. The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev. 18, 901-911 (2004). (Pubitemid 38529659)
28. Lucitti, J. L. et al. Vascular remodeling of the mouse yolk sac requires hemodynamic force. Development 134, 3317-3326 (2007). (Pubitemid 350018432)
29. Arora, R. &Papaioannou, V. E. The murine allantois: a model system for the study of blood vessel formation. Blood 120, 2562-2572 (2012).
30. Nor, J. E. et al. Engineering and characterization of functional human microvessels in immunodeficient mice. Lab. Invest. 81, 453-463 (2001). (Pubitemid 32298790)
31. Chang, A. C. et al. Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase. Dev. Cell 21, 288-300 (2011).
32. Red-Horse, K., Ueno, H., Weissman, I. L. &Krasnow, M. A. Coronary arteries form by developmental reprogramming of venous cells. Nature 464, 549-553 (2010).
33. Cristofaro, B. et al. Dll4-Notch signaling determines the formation of native arterial collateral networks and arterial function in mouse ischemia models. Development 140, 1720-1729 (2013).
34. Krebs, L. T., Starling, C., Chervonsky, A. V. &Gridley, T. Notch1 activation in mice causes arteriovenous malformations phenocopied by ephrinB2 and EphB4 mutants. Genesis 48, 146-150 (2010).
35. Copeland, J. N., Feng, Y., Neradugomma, N. K., Fields, P. E. &Vivian, J. L. Notch signaling regulates remodeling and vessel diameter in the extraembryonic yolk sac. BMC Dev. Biol. 11, 12 (2011).
36. Lin, T., Ponn, A., Hu, X., Law, B. K. &Lu, J. Requirement of the histone demethylase LSD1 in Snai1-mediated transcriptional repression during epithelial-mesenchymal transition. Oncogene 29, 4896-4904 (2010).
37. Lin, Y. et al. The SNAG domain of Snail1 functions as a molecular hook for recruiting lysine-specific demethylase 1. EMBO J. 29, 1803-1816 (2010).
38. Wu, Z. Q. et al. Canonical Wnt signaling regulates Slug activity and links epithelial-mesenchymal transition with epigenetic Breast Cancer 1, Early Onset (BRCA1) repression. Proc. Natl Acad. Sci. USA 109, 16654-16659 (2012).
39. Williams, C. K., Li, J. L., Murga, M., Harris, A. L. &Tosato, G. Up-regulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function. Blood 107, 931-939 (2006). (Pubitemid 43156289)
40. Mak, P. et al. ERbeta impedes prostate cancer EMT by destabilizing HIF-1alpha and inhibiting VEGF-mediated snail nuclear localization: implications for Gleason grading. Cancer Cell 17, 319-332 (2010).
41. Wanami, L. S., Chen, H. Y., Peiro, S., Garcia de Herreros, A. &Bachelder, R. E. Vascular endothelial growth factor-A stimulates Snail expression in breast tumor cells: implications for tumor progression. Exp. Cell Res. 314, 2448-2453 (2008).
42. Deng, Y. et al. Endothelial RAF1/ERK activation regulates arterial morphogenesis. Blood 121, S3981-S3989 (2013).
43. DeNiro, M., Al-Mohanna, F. H., Alsmadi, O. &Al-Mohanna, F. A. The nexus between VEGF and NFkappaB orchestrates a hypoxia-independent neovasculogenesis. PLoS One 8, e59021 (2013).
44. Julien, S. et al. Activation of NF-kappaB by Akt upregulates Snail expression and induces epithelium mesenchyme transition. Oncogene 26, 7445-7456 (2007). (Pubitemid 350158710)
45. Yook, J. I. et al. A Wnt-Axin2-GSK3beta cascade regulates Snail1 activity in breast cancer cells. Nat. Cell Biol. 8, 1398-1406 (2006). (Pubitemid 44835115)
46. Wu, Y. et al. Stabilization of Snail by NF-kappaB is required for inflammationinduced cell migration and invasion. Cancer Cell. 15, 416-428 (2009).
47. Patel, N. S. et al. Up-regulation of delta-like 4 ligand in human tumor vasculature and the role of basal expression in endothelial cell function. Cancer Res. 65, 8690-8697 (2005). (Pubitemid 41377356)
48. Wu, Z. Q. et al. Canonical Wnt suppressor, Axin2, promotes colon carcinoma oncogenic activity. Proc. Natl Acad. Sci. USA 109, 11312-11317 (2012).
49. Sahlgren, C., Gustafsson, M. V., Jin, S., Poellinger, L. &Lendahl, U. Notch signaling mediates hypoxia-induced tumor cell migration and invasion. Proc. Natl Acad. Sci. USA 105, 6392-6397 (2008). (Pubitemid 351758356)
50. Timmerman, L. A. et al. Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev. 18, 99-115 (2004). (Pubitemid 38090691)
51. Murphy, P. A. et al. Notch4 normalization reduces blood vessel size in arteriovenous malformations. Sci. Transl. Med. 4, 117ra118 (2012).
52. Suchting, S. et al. The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc. Natl Acad. Sci. USA 104, 3225-3230 (2007). (Pubitemid 46364141)
53. Gomez-del Arco, P. et al. Alternative promoter usage at the Notch1 locus supports ligand-independent signaling in T cell development and leukemogenesis. Immunity 33, 685-698 (2010).
54. Bozkulak, E. C. &Weinmaster, G. Selective use of ADAM10 and ADAM17 in activation of Notch1 signaling. Mol. Cell Biol. 29, 5679-5695 (2009).
55. Sheldon, H. et al. New mechanism for Notch signaling to endothelium at a distance by Delta-like 4 incorporation into exosomes. Blood 116, 2385-2394 (2010).
56. Carmeliet, P. Angiogenesis in health and disease. Nat. Med. 9, 653-660 (2003). (Pubitemid 36749213)
57. Chang, L. et al. Differentiation of vascular smooth muscle cells from local precursors during embryonic and adult arteriogenesis requires Notch signaling. Proc. Natl Acad. Sci. USA 109, 6993-6998 (2012).
58. Luna-Zurita, L. et al. Integration of a Notch-dependent mesenchymal gene program and Bmp2-driven cell invasiveness regulates murine cardiac valve formation. J. Clin. Invest. 120, 3493-3507 (2010).
59. Niessen, K. et al. Slug is a direct Notch target required for initiation of cardiac cushion cellularization. J. Cell Biol. 182, 315-325 (2008).
60. Tao, G., Levay, A. K., Gridley, T. &Lincoln, J. Mmp15 is a direct target of Snai1 during endothelial to mesenchymal transformation and endocardial cushion development. Dev. Biol. 359, 209-221 (2011).
61. Parker, B. S. et al. Alterations in vascular gene expression in invasive breast carcinoma. Cancer Res. 64, 7857-7866 (2004). (Pubitemid 39446919)
62. Schwock, J. et al. SNAI1 expression and the mesenchymal phenotype: an immunohistochemical study performed on 46 cases of oral squamous cell carcinoma. BMC Clin. Pathol. 10, 1 (2010).
63. Zheng, W. et al. Notch restricts lymphatic vessel sprouting induced by vascular endothelial growth factor. Blood 118, 1154-1162 (2011).
64. Zidar, N. et al. Cadherin-catenin complex and transcription factor Snail-1 in spindle cell carcinoma of the head and neck. Virchows Arch. 453, 267-274 (2008).
65. Medici, D., Potenta, S. &Kalluri, R. Transforming growth factor-beta2 promotes Snail-mediated endothelial-mesenchymal transition through convergence of Smad-dependent and Smad-independent signalling. Biochem. J. 437, 515-520 (2011).
66. Alva, J. A. et al. VE-Cadherin-Cre-recombinase transgenic mouse: a tool for lineage analysis and gene deletion in endothelial cells. Dev. Dyn. 235, 759-767 (2006).
67. Zhou, Y. et al. Rescue of the embryonic lethal hematopoietic defect reveals a critical role for GATA-2 in urogenital development. EMBO J. 17, 6689-6700 (1998). (Pubitemid 28521802)
68. Pitulescu, M. E., Schmidt, I., Benedito, R. &Adams, R. H. Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat. Protoc. 5, 1518-1534 (2010).
69. Simonavicius, N. et al. Pericytes promote selective vessel regression to regulate vascular patterning. Blood 120, 1516-1527 (2012).
70. van Beijnum, J. R., Rousch, M., Castermans, K., van der Linden, E. &Griffioen, A. W. Isolation of endothelial cells from fresh tissues. Nat. Protoc. 3, 1085-1091 (2008). (Pubitemid 351818695)