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ETS transcription factors in embryonic vascular development

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Abstract

At least thirteen ETS-domain transcription factors are expressed during embryonic hematopoietic or vascular development and potentially function in the formation and maintenance of the embryonic vasculature or blood lineages. This review summarizes our current understanding of the specific roles played by ETS factors in vasculogenesis and angiogenesis and the implications of functional redundancies between them.

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References

  1. Nunn MF, Seeburg PH, Moscovici C et al (1983) Tripartite structure of the avian erythroblastosis virus E26 transforming gene. Nature 306:391–395

    Article  CAS  PubMed  Google Scholar 

  2. Lelievre E, Lionneton F, Soncin F (2001) Role of the ETS transcription factors in the control of endothelial-specific gene expression and in angiogenesis. Bull Cancer 88:137–142

    CAS  PubMed  Google Scholar 

  3. Verger A, Buisine E, Carrere S et al (2001) Identification of amino acid residues in the ETS transcription factor Erg that mediate Erg-Jun/Fos-DNA ternary complex formation. J Biol Chem 276:17181–17189

    Article  CAS  PubMed  Google Scholar 

  4. De Val S, Chi NC, Meadows SM et al (2008) Combinatorial regulation of endothelial gene expression by ets and forkhead transcription factors. Cell 135:1053–1064

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  5. Hollenhorst PC, Jones DA, Graves BJ (2004) Expression profiles frame the promoter specificity dilemma of the ETS family of transcription factors. Nucl Acids Res 32:5693–5702

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  6. Wei G, Srinivasan R, Cantemir-Stone CZ et al (2009) Ets1 and Ets2 are required for endothelial cell survival during embryonic angiogenesis. Blood 114:1123–1130

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  7. Liu F, Patient R (2008) Genome-wide analysis of the zebrafish ETS family identifies three genes required for hemangioblast differentiation or angiogenesis. Circ Res 103:1147–1154

    Article  CAS  PubMed  Google Scholar 

  8. Garrett-Sinha LA, Dahl R, Rao S et al (2001) PU.1 exhibits partial functional redundancy with Spi-B, but not with Ets-1 or Elf-1. Blood 97:2908–2912

    Article  CAS  PubMed  Google Scholar 

  9. Abedin MJ, Nguyen A, Jiang N et al (2014) Fli1 acts downstream of Etv2 to govern cell survival and vascular homeostasis via positive autoregulation. Circ Res 114:1690–1699

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  10. Craig MP, Grajevskaja V, Liao HK et al (2015) Etv2 and fli1b function together as key regulators of vasculogenesis and angiogenesis. Arterioscler Thromb Vasc Biol 35:865–876

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Liu F, Li D, Yu YY et al (2015) Induction of hematopoietic and endothelial cell program orchestrated by ETS transcription factor ER71/ETV2. EMBO Rep 16:654–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Brown TA, McKnight SL (1992) Specificities of protein-protein and protein-DNA interaction of GABP alpha and two newly defined ets-related proteins. Genes Dev 6:2502–2512

    Article  CAS  PubMed  Google Scholar 

  13. Sumanas S, Jorniak T, Lin S (2005) Identification of novel vascular endothelial-specific genes by the microarray analysis of the zebrafish cloche mutants. Blood 106:534–541

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hayashi M, Pluchinotta M, Momiyama A et al (2012) Endothelialization and altered hematopoiesis by persistent Etv2 expression in mice. Exp Hematol 40(738–750):e11

    PubMed  Google Scholar 

  15. Koyano-Nakagawa N, Kweon J, Iacovino M et al (2012) Etv2 is expressed in the yolk sac hematopoietic and endothelial progenitors and regulates Lmo2 gene expression. Stem Cells 30:1611–1623

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Lee D, Park C, Lee H et al (2008) ER71 acts downstream of BMP, Notch, and Wnt signaling in blood and vessel progenitor specification. Cell Stem Cell 2:497–507

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Ferdous A, Caprioli A, Iacovino M et al (2009) Nk2–5 transactivates the Ets-related protein 71 gene and specifies an endothelial/endocardial fate in the developing embryo. Proc Natl Acad Sci USA 106:814–819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Sumanas S, Lin S (2006) Ets1-related protein is a key regulator of vasculogenesis in zebrafish. PLoS Biol 4:e10

    Article  PubMed  CAS  Google Scholar 

  19. Glenn NO, Schumacher JA, Kim HJ et al (2014) Distinct regulation of the anterior and posterior myeloperoxidase expression by Etv2 and Gata1 during primitive Granulopoiesis in zebrafish. Dev Biol 393:149–159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Sumanas S, Gomez G, Zhao Y et al (2008) Interplay among Etsrp/ER71, Scl, and Alk8 signaling controls endothelial and myeloid cell formation. Blood 111:4500–4510

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  21. Salanga MC, Meadows SM, Myers CT et al (2010) ETS family protein ETV2 is required for initiation of the endothelial lineage but not the hematopoietic lineage in the Xenopus embryo. Dev Dyn 239:1178–1187

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Moore JC, Sheppard-Tindell S, Shestopalov IA et al (2013) Post-transcriptional mechanisms contribute to Etv2 repression during vascular development. Dev Biol 384:128–140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Park C, Lee TJ, Bhang SH et al (2016) Injury-mediated vascular regeneration requires endothelial ER71/ETV2. Arterioscler Thromb Vasc Biol 36:86–96

    Article  CAS  PubMed  Google Scholar 

  24. Pham VN, Lawson ND, Mugford JW et al (2007) Combinatorial function of ETS transcription factors in the developing vasculature. Dev Biol 303:772–783

    Article  CAS  PubMed  Google Scholar 

  25. Robinson AS, Materna SC, Barnes RM et al (2014) An arterial-specific enhancer of the human endothelin converting enzyme 1 (ECE1) gene is synergistically activated by Sox17, FoxC2, and Etv2. Dev Biol 395:379–389

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Palencia-Desai S, Kohli V, Kang J et al (2011) Vascular endothelial and endocardial progenitors differentiate as cardiomyocytes in the absence of Etsrp/Etv2 function. Development 138:4721–4732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Rasmussen TL, Kweon J, Diekmann MA et al (2011) ER71 directs mesodermal fate decisions during embryogenesis. Development 138:4801–4812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  28. Lee D, Kim T, Lim DS (2011) The Er71 is an important regulator of hematopoietic stem cells in adult mice. Stem Cells 29:539–548

    Article  PubMed  CAS  Google Scholar 

  29. Veldman MB, Zhao C, Gomez GA et al (2013) Transdifferentiation of fast skeletal muscle into functional endothelium in vivo by transcription factor Etv2. PLoS Biol 11:e1001590

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Ishitobi H, Wakamatsu A, Liu F et al (2011) Molecular basis for Flk1 expression in hemato-cardiovascular progenitors in the mouse. Development 138:5357–5368

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  31. Veldman MB, Lin S (2012) Etsrp/Etv2 is directly regulated by Foxc1a/b in the zebrafish angioblast. Circ Res 110:220–229

    Article  CAS  PubMed  Google Scholar 

  32. Schupp MO, Waas M, Chun CZ et al (2014) Transcriptional inhibition of etv2 expression is essential for embryonic cardiac development. Dev Biol 393:71–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Rasmussen TL, Shi X, Wallis A et al (2012) VEGF/Flk1 signaling cascade transactivates Etv2 gene expression. PLoS ONE 7:e50103

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  34. Peterkin T, Gibson A, Patient R (2009) Common genetic control of haemangioblast and cardiac development in zebrafish. Development 136:1465–1474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wareing S, Mazan A, Pearson S et al (2012) The Flk1-Cre-mediated deletion of ETV2 defines its narrow temporal requirement during embryonic hematopoietic development. Stem Cells 30:1521–1531

    Article  CAS  PubMed  Google Scholar 

  36. Kohli V, Schumacher JA, Desai SP et al (2013) Arterial and venous progenitors of the major axial vessels originate at distinct locations. Dev Cell 25:196–206

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Thompson MA, Ransom DG, Pratt SJ et al (1998) The cloche and spadetail genes differentially affect hematopoiesis and vasculogenesis. Dev Biol 197:248–269

    Article  CAS  PubMed  Google Scholar 

  38. Shi X, Zirbes KM, Rasmussen TL et al (2015) The transcription factor Mesp1 interacts with cAMP-responsive element binding protein 1 (Creb1) and coactivates Ets variant 2 (Etv2) gene expression. J Biol Chem 290:9614–9625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  39. Zhang L, Lemarchandel V, Romeo PH et al (1993) The Fli-1 proto-oncogene, involved in erythroleukemia and Ewing’s sarcoma, encodes a transcriptional activator with DNA-binding specificities distinct from other Ets family members. Oncogene 8:1621–1630

    CAS  PubMed  Google Scholar 

  40. Stoll G, Surdez D, Tirode F et al (2013) Systems biology of Ewing sarcoma: a network model of EWS-FLI1 effect on proliferation and apoptosis. Nucleic Acids Res 41:8853–8871

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Spyropoulos DD, Pharr PN, Lavenburg KR et al (2000) Hemorrhage, impaired hematopoiesis, and lethality in mouse embryos carrying a targeted disruption of the Fli1 transcription factor. Mol Cell Biol 20:5643–5652

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Liu F, Walmsley M, Rodaway A et al (2008) Fli1 acts at the top of the transcriptional network driving blood and endothelial development. Curr Biol 18:1234–1240

    Article  CAS  PubMed  Google Scholar 

  43. Ren X, Gomez GA, Zhang B et al (2010) Scl isoforms act downstream of etsrp to specify angioblasts and definitive hematopoietic stem cells. Blood 115:5338–5346

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Wong KS, Proulx K, Rost MS et al (2009) Identification of vasculature-specific genes by microarray analysis of etsrp/etv2 overexpressing zebrafish embryos. Dev Dyn 238:1836–1850

    Article  CAS  PubMed  Google Scholar 

  45. Law SH, Sargent TD (2013) Maternal pak4 expression is required for primitive myelopoiesis in zebrafish. Mech Dev 130:181–194

    Article  CAS  PubMed  Google Scholar 

  46. Kruse EA, Loughran SJ, Baldwin TM et al (2009) Dual requirement for the ETS transcription factors Fli-1 and Erg in hematopoietic stem cells and the megakaryocyte lineage. Proc Natl Acad Sci USA 106:13814–13819

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Loughran SJ, Kruse EA, Hacking DF et al (2008) The transcription factor Erg is essential for definitive hematopoiesis and the function of adult hematopoietic stem cells. Nat Immunol 9:810–819

    Article  CAS  PubMed  Google Scholar 

  48. Giovannini M, Biegel JA, Serra M et al (1994) EWS-erg and EWS-Fli1 fusion transcripts in Ewing’s sarcoma and primitive neuroectodermal tumors with variant translocations. J Clin Invest 94:489–496

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Tomlins SA, Palanisamy N, Brenner JC et al (2013) Usefulness of a monoclonal ERG/FLI1 antibody for immunohistochemical discrimination of Ewing family tumors. Am J Clin Pathol 139:771–779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  50. Martens JH (2011) Acute myeloid leukemia: a central role for the ETS factor ERG. Int J Biochem Cell Biol 43:1413–1416

    Article  CAS  PubMed  Google Scholar 

  51. Baltzinger M, Mager-Heckel AM, Remy P (1999) Xl erg: expression pattern and overexpression during development plead for a role in endothelial cell differentiation. Dev Dyn 216:420–433

    Article  CAS  PubMed  Google Scholar 

  52. Petzold AM, Balciunas D, Sivasubbu S et al (2009) Nicotine response genetics in the zebrafish. Proc Natl Acad Sci USA 106:18662–18667

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Abzug MJ, Nachman SA, Muresan P et al (2013) Safety and immunogenicity of 2009 pH1N1 vaccination in HIV-infected pregnant women. Clin Infect Dis 56:1488–1497

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Carrere S, Verger A, Flourens A et al (1998) Erg proteins, transcription factors of the Ets family, form homo, heterodimers and ternary complexes via two distinct domains. Oncogene 16:3261–3268

    Article  CAS  PubMed  Google Scholar 

  55. Han R, Pacifici M, Iwamoto M et al (2015) Endothelial Erg expression is required for embryogenesis and vascular integrity. Organogenesis 11:75–86

    Article  PubMed  PubMed Central  Google Scholar 

  56. Birdsey GM, Shah AV, Dufton N et al (2015) The endothelial transcription factor ERG promotes vascular stability and growth through Wnt/beta-catenin signaling. Dev Cell 32:82–96

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Garrett-Sinha LA (2013) Review of Ets1 structure, function, and roles in immunity. Cell Mol Life Sci 70:3375–3390

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Verschoor ML, Singh G (2013) Ets-1 regulates intracellular glutathione levels: key target for resistant ovarian cancer. Mol Cancer 12:138

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  59. Asano Y, Stawski L, Hant F et al (2010) Endothelial Fli1 deficiency impairs vascular homeostasis: a role in scleroderma vasculopathy. Am J Pathol 176:1983–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Goll MG, Anderson R, Stainier DY et al (2009) Transcriptional silencing and reactivation in transgenic zebrafish. Genetics 182:747–755

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  61. Ellett F, Kile BT, Lieschke GJ (2009) The role of the ETS factor erg in zebrafish vasculogenesis. Mech Dev 126:220–229

    Article  CAS  PubMed  Google Scholar 

  62. Wythe JD, Dang LT, Devine WP et al (2013) ETS factors regulate Vegf-dependent arterial specification. Dev Cell 26:45–58

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  63. Muthusamy N, Barton K, Leiden JM (1995) Defective activation and survival of T cells lacking the Ets-1 transcription factor. Nature 377:639–642

    Article  CAS  PubMed  Google Scholar 

  64. Bories JC, Willerford DM, Grevin D et al (1995) Increased T-cell apoptosis and terminal B-cell differentiation induced by inactivation of the Ets-1 proto-oncogene. Nature 377:635–638

    Article  CAS  PubMed  Google Scholar 

  65. Tanaka K, Oda N, Iwasaka C et al (1998) Induction of Ets-1 in endothelial cells during reendothelialization after denuding injury. J Cell Physiol 176:235–244

    Article  CAS  PubMed  Google Scholar 

  66. Iwasaka C, Tanaka K, Abe M et al (1996) Ets-1 regulates angiogenesis by inducing the expression of urokinase-type plasminogen activator and matrix metalloproteinase-1 and the migration of vascular endothelial cells. J Cell Physiol 169:522–531

    Article  CAS  PubMed  Google Scholar 

  67. Sato Y, Abe M, Tanaka K et al (2000) Signal transduction and transcriptional regulation of angiogenesis. Adv Exp Med Biol 476:109–115

    Article  CAS  PubMed  Google Scholar 

  68. Chen Z, Fisher RJ, Riggs CW et al (1997) Inhibition of vascular endothelial growth factor-induced endothelial cell migration by ETS1 antisense oligonucleotides. Cancer Res 57:2013–2019

    CAS  PubMed  Google Scholar 

  69. Watanabe D, Takagi H, Suzuma K et al (2004) Transcription factor Ets-1 mediates ischemia- and vascular endothelial growth factor-dependent retinal neovascularization. Am J Pathol 164:1827–1835

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  70. Elvert G, Kappel A, Heidenreich R et al (2003) Cooperative interaction of hypoxia-inducible factor-2alpha (HIF-2alpha) and Ets-1 in the transcriptional activation of vascular endothelial growth factor receptor-2 (Flk-1). J Biol Chem 278:7520–7530

    Article  CAS  PubMed  Google Scholar 

  71. Dutta D, Ray S, Vivian JL et al (2008) Activation of the VEGFR1 chromatin domain: an angiogenic signal-ETS1/HIF-2alpha regulatory axis. J Biol Chem 283:25404–25413

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Nor JE, Christensen J, Mooney DJ et al (1999) Vascular endothelial growth factor (VEGF)-mediated angiogenesis is associated with enhanced endothelial cell survival and induction of Bcl-2 expression. Am J Pathol 154:375–384

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Distel M, Wullimann MF, Koster RW (2009) Optimized Gal4 genetics for permanent gene expression mapping in zebrafish. Proc Natl Acad Sci U S A 106:13365–13370

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Rahim S, Uren A (2013) Emergence of ETS transcription factors as diagnostic tools and therapeutic targets in prostate cancer. Am J Transl Res 5:254–268

    CAS  PubMed  PubMed Central  Google Scholar 

  75. Paulo P, Ribeiro FR, Santos J et al (2012) Molecular subtyping of primary prostate cancer reveals specific and shared target genes of different ETS rearrangements. Neoplasia 14:600–611

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  76. Nakano T, Abe M, Tanaka K et al (2000) Angiogenesis inhibition by transdominant mutant Ets-1. J Cell Physiol 184:255–262

    Article  CAS  PubMed  Google Scholar 

  77. Oda N, Abe M, Sato Y (1999) ETS-1 converts endothelial cells to the angiogenic phenotype by inducing the expression of matrix metalloproteinases and integrin beta3. J Cell Physiol 178:121–132

    Article  CAS  PubMed  Google Scholar 

  78. Lelievre E, Mattot V, Huber P et al (2000) ETS1 lowers capillary endothelial cell density at confluence and induces the expression of VE-cadherin. Oncogene 19:2438–2446

    Article  CAS  PubMed  Google Scholar 

  79. Lincoln DW 2nd, Phillips PG, Bove K (2003) Estrogen-induced Ets-1 promotes capillary formation in an in vitro tumor angiogenesis model. Breast Cancer Res Treat 78:167–178

    Article  CAS  PubMed  Google Scholar 

  80. Pourtier-Manzanedo A, Vercamer C, Van Belle E et al (2003) Expression of an Ets-1 dominant-negative mutant perturbs normal and tumor angiogenesis in a mouse ear model. Oncogene 22:1795–1806

    Article  CAS  PubMed  Google Scholar 

  81. Aperlo C, Pognonec P, Stanley ER et al (1996) Constitutive c-ets2 expression in M1D + myeloblast leukemic cells induces their differentiation to macrophages. Mol Cell Biol 16:6851–6858

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Polydorou C, Georgiades P (2013) Ets2-dependent trophoblast signalling is required for gastrulation progression after primitive streak initiation. Nat Commun 4:1658

    Article  PubMed  CAS  Google Scholar 

  83. Wallace JA, Li F, Balakrishnan S et al (2013) Ets2 in tumor fibroblasts promotes angiogenesis in breast cancer. PLoS ONE 8:e71533

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Kappel A, Schlaeger TM, Flamme I et al (2000) Role of SCL/Tal-1, GATA, and ets transcription factor binding sites for the regulation of flk-1 expression during murine vascular development. Blood 96:3078–3085

    CAS  PubMed  Google Scholar 

  85. Trimboli AJ, Cantemir-Stone CZ, Li F et al (2009) Pten in stromal fibroblasts suppresses mammary epithelial tumours. Nature 461:1084–1091

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Wang X, Huang W, Liu G et al (2014) Cardiomyocytes mediate anti-angiogenesis in type 2 diabetic rats through the exosomal transfer of miR-320 into endothelial cells. J Mol Cell Cardiol 74:139–150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Yoshimatsu Y, Yamazaki T, Mihira H et al (2011) Ets family members induce lymphangiogenesis through physical and functional interaction with Prox1. J Cell Sci 124:2753–2762

    Article  CAS  PubMed  Google Scholar 

  88. Wernert N, Okuducu AF, Pepper MS (2003) Ets 1 is expressed in capillary blood vessels but not in lymphatics. J Pathol 200:561–567

    Article  CAS  PubMed  Google Scholar 

  89. Thompson CB, Wang CY, Ho IC et al (1992) cis-acting sequences required for inducible interleukin-2 enhancer function bind a novel Ets-related protein, Elf-1. Mol Cell Biol 12:1043–1053

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  90. Wang CY, Bassuk AG, Boise LH et al (1994) Activation of the granulocyte-macrophage colony-stimulating factor promoter in T cells requires cooperative binding of Elf-1 and AP-1 transcription factors. Mol Cell Biol 14:1153–1159

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Serdobova I, Pla M, Reichenbach P et al (1997) Elf-1 contributes to the function of the complex interleukin (IL)-2-responsive enhancer in the mouse IL-2 receptor alpha gene. J Exp Med 185:1211–1221

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Dube A, Thai S, Gaspar J et al (2001) Elf-1 is a transcriptional regulator of the Tie2 gene during vascular development. Circ Res 88:237–244

    Article  CAS  PubMed  Google Scholar 

  93. Sato TN, Tozawa Y, Deutsch U et al (1995) Distinct roles of the receptor tyrosine kinases Tie-1 and Tie-2 in blood vessel formation. Nature 376:70–74

    Article  CAS  PubMed  Google Scholar 

  94. Karantzoulis-Fegaras F, Antoniou H, Lai SL et al (1999) Characterization of the human endothelial nitric-oxide synthase promoter. J Biol Chem 274:3076–3093

    Article  CAS  PubMed  Google Scholar 

  95. Hegen A, Koidl S, Weindel K et al (2004) Expression of angiopoietin-2 in endothelial cells is controlled by positive and negative regulatory promoter elements. Arterioscler Thromb Vasc Biol 24:1803–1809

    Article  CAS  PubMed  Google Scholar 

  96. Oettgen P, Akbarali Y, Boltax J et al (1996) Characterization of NERF, a novel transcription factor related to the Ets factor ELF-1. Mol Cell Biol 16:5091–5106

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Wang LC, Kuo F, Fujiwara Y et al (1997) Yolk sac angiogenic defect and intra-embryonic apoptosis in mice lacking the Ets-related factor TEL. EMBO J 16:4374–4383

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Gaspar J, Thai S, Voland C et al (2002) Opposing functions of the Ets factors NERF and ELF-1 during chicken blood vessel development. Arterioscler Thromb Vasc Biol 22:1106–1112

    Article  CAS  PubMed  Google Scholar 

  99. Lopez RG, Carron C, Oury C et al (1999) TEL is a sequence-specific transcriptional repressor. J Biol Chem 274:30132–30138

    Article  CAS  PubMed  Google Scholar 

  100. De Braekeleer E, Douet-Guilbert N, Morel F et al (2012) ETV6 fusion genes in hematological malignancies: a review. Leuk Res 36:945–961

    Article  PubMed  CAS  Google Scholar 

  101. Hock H, Meade E, Medeiros S et al (2004) Tel/Etv6 is an essential and selective regulator of adult hematopoietic stem cell survival. Genes Dev 18:2336–2341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Roukens MG, Alloul-Ramdhani M, Baan B et al (2010) Control of endothelial sprouting by a Tel-CtBP complex. Nat Cell Biol 12:933–942

    Article  CAS  PubMed  Google Scholar 

  103. Rasighaemi P, Onnebo SM, Liongue C et al (2015) ETV6 (TEL1) regulates embryonic hematopoiesis in zebrafish. Haematologica 100:23–31

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  104. Ciau-Uitz A, Pinheiro P, Gupta R et al (2010) Tel1/ETV6 specifies blood stem cells through the agency of VEGF signaling. Dev Cell 18:569–578

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This study was supported in part by the National Institutes of Health R01 award HL107369 to S.S., an award from Ohio Cancer Research Associates to S.S. and the Cincinnati Children’s Research Foundation.

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  1. Department of Biochemistry and Molecular Biology, Wright State University, 3640 Colonel Glenn Hwy., Dayton, OH, 45435, USA

    Michael P. Craig

  2. Division of Developmental Biology, Cincinnati Children’s Hospital Medical Center, 3333 Burnet Avenue, Cincinnati, OH, 45229, USA

    Michael P. Craig & Saulius Sumanas

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Correspondence to Saulius Sumanas.

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Craig, M.P., Sumanas, S. ETS transcription factors in embryonic vascular development. Angiogenesis 19, 275–285 (2016). https://doi.org/10.1007/s10456-016-9511-z

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