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Molecular Mechanisms of Angiogenesis pp 149–167Cite as

Emerging Role of the Two Related Basic Helix-Loop-Helix Proteins TAL1 and LYL1 in Angiogenesis

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Abstract

Throughout the multistep process of angiogenesis, endothelial cells have to integrate key signaling pathways that are tightly regulated by the coordinated activity of several transcriptional networks. The two related basic helix-loop-helix proteins LYL1 and TAL1 and their cofactor LMO2 (a LIM-only protein) have recently emerged as new important regulators of endothelial morphogenesis, in addition to their well-known hematopoietic functions. This chapter reviews the essential role of TAL1 and LMO2 in early hematopoietic and vascular development and highlights their important contribution in controlling the early steps of angiogenesis. It also discusses recent data showing that LYL1 is dispensable during embryonic development but has a dual function in the hematopoietic and endothelial lineages during adult life. Indeed, besides its role in maintaining the pool of functional hematopoietic stem cells, LYL1 promotes the maturation and stabilization of new vessels.

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References

  • Antas VI, Al-Drees MA, Prudence AJ, Sugiyama D, Fraser ST (2013) Hemogenic endothelium: a vessel for blood production. Int J Biochem Cell Biol 45(3):692–695. doi:10.1016/j.biocel.2012.12.013, S1357-2725(12)00409-8 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Aplan PD, Begley CG, Bertness V, Nussmeier M, Ezquerra A, Coligan J, Kirsch IR (1990) The SCL gene is formed from a transcriptionally complex locus. Mol Cell Biol 10(12):6426–6435

    CAS  PubMed Central  PubMed  Google Scholar 

  • Augustin HG, Koh GY, Thurston G, Alitalo K (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 10(3):165–177

    Article  CAS  PubMed  Google Scholar 

  • Avraamides CJ, Garmy-Susini B, Varner JA (2008) Integrins in angiogenesis and lymphangiogenesis. Nat Rev Cancer 8(8):604–617

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Baer R (1993) TAL1, TAL2 and LYL1: a family of basic helix-loop-helix proteins implicated in T cell acute leukaemia. Semin Cancer Biol 4(6):341–347

    CAS  PubMed  Google Scholar 

  • Bernard O, Lecointe N, Jonveaux P, Souyri M, Mauchauffe M, Berger R, Larsen CJ, Mathieu-Mahul D (1991) Two site-specific deletions and t(1;14) translocation restricted to human T-cell acute leukemias disrupt the 5ʹ part of the tal-1 gene. Oncogene 6(8):1477–1488

    CAS  PubMed  Google Scholar 

  • Bernard O, Azogui O, Lecointe N, Mugneret F, Berger R, Larsen CJ, Mathieu-Mahul D (1992) A third tal-1 promoter is specifically used in human T cell leukemias. J Exp Med 176(4):919–925

    Article  CAS  PubMed  Google Scholar 

  • Bertrand JY, Chi NC, Santoso B, Teng S, Stainier DY, Traver D (2010) Haematopoietic stem cells derive directly from aortic endothelium during development. Nature 464(7285):108–111. doi:10.1038/nature08738, nature08738 [pii]

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Boisset JC, van Cappellen W, Andrieu-Soler C, Galjart N, Dzierzak E, Robin C (2010) In vivo imaging of haematopoietic cells emerging from the mouse aortic endothelium. Nature 464(7285):116–120. doi:10.1038/nature08764, nature08764 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Bussmann J, Bakkers J, Schulte-Merker S (2007) Early endocardial morphogenesis requires Scl/Tal1. PLoS Genet 3(8):e140

    Article  PubMed Central  PubMed  Google Scholar 

  • Calkhoven CF, Muller C, Martin R, Krosl G, Pietsch H, Hoang T, Leutz A (2003) Translational control of SCL-isoform expression in hematopoietic lineage choice. Genes Dev 17(8):959–964

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Capron C, Lecluse Y, Kaushik AL, Foudi A, Lacout C, Sekkai D, Godin I, Albagli O, Poullion I, Svinartchouk F, Schanze E, Vainchenker W, Sablitzky F, Bennaceur-Griscelli A, Dumenil D (2006) The SCL relative LYL-1 is required for fetal and adult hematopoietic stem cell function and B-cell differentiation. Blood 107(12):4678–4686

    Article  CAS  PubMed  Google Scholar 

  • Carmeliet P, Lampugnani MG, Moons L, Breviario F, Compernolle V, Bono F, Balconi G, Spagnuolo R, Oostuyse B, Dewerchin M, Zanetti A, Angellilo A, Mattot V, Nuyens D, Lutgens E, Clotman F, de Ruiter MC, Gittenberger-de Groot A, Poelmann R, Lupu F, Herbert JM, Collen D, Dejana E (1999) Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98(2):147–157

    Article  CAS  PubMed  Google Scholar 

  • Chan WY, Follows GA, Lacaud G, Pimanda JE, Landry JR, Kinston S, Knezevic K, Piltz S, Donaldson IJ, Gambardella L, Sablitzky F, Green AR, Kouskoff V, Gottgens B (2007) The paralogous hematopoietic regulators Lyl1 and Scl are coregulated by Ets and GATA factors, but Lyl1 cannot rescue the early Scl−/− phenotype. Blood 109(5):1908–1916

    Article  CAS  PubMed  Google Scholar 

  • Choi K, Kennedy M, Kazarov A, Papadimitriou JC, Keller G (1998) A common precursor for hematopoietic and endothelial cells. Development 125(4):725–732

    CAS  PubMed  Google Scholar 

  • Curtis DJ, Salmon JM, Pimanda JE (2012) Concise review: blood relatives: formation and regulation of hematopoietic stem cells by the basic helix-loop-helix transcription factors stem cell leukemia and lymphoblastic leukemia-derived sequence 1. Stem Cells 30(6):1053–1058. doi:10.1002/stem.1093

    Article  CAS  PubMed  Google Scholar 

  • Dejana E, Vestweber D (2013) The role of VE-cadherin in vascular morphogenesis and permeability control. Prog Mol Biol Transl Sci 116:119–144. doi:10.1016/B978-0-12-394311-8.00006-6, B978-0-12-394311-8.00006-6 [pii]

    Article  CAS  PubMed  Google Scholar 

  • Dekel B, Hochman E, Sanchez MJ, Maharshak N, Amariglio N, Green AR, Izraeli S (2004) Kidney, blood, and endothelium: developmental expression of stem cell leukemia during nephrogenesis. Kidney Int 65(4):1162–1169

    Article  PubMed  Google Scholar 

  • Deleuze V, Chalhoub E, El-Hajj R, Dohet C, Le Clech M, Couraud PO, Huber P, Mathieu D (2007) TAL-1/SCL and its partners E47 and LMO2 up-regulate VE-cadherin expression in endothelial cells. Mol Cell Biol 27(7):2687–2697

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Deleuze V, El-Hajj R, Chalhoub E, Dohet C, Pinet V, Couttet P, Mathieu D (2012) Angiopoietin-2 is a direct transcriptional target of TAL1, LYL1 and LMO2 in endothelial cells. PLoS ONE 7(7):e40484. doi:10.1371/journal.pone.0040484, PONE-D-12-07293 [pii]

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Dooley KA, Davidson AJ, Zon LI (2005) Zebrafish scl functions independently in hematopoietic and endothelial development. Dev Biol 277(2):522–536

    Article  CAS  PubMed  Google Scholar 

  • Drake CJ, Fleming PA (2000) Vasculogenesis in the day 6.5 to 9.5 mouse embryo. Blood 95(5):1671–1679

    CAS  PubMed  Google Scholar 

  • Drake CJ, Brandt SJ, Trusk TC, Little CD (1997) TAL1/SCL is expressed in endothelial progenitor cells/angioblasts and defines a dorsal-to-ventral gradient of vasculogenesis. Dev Biol 192(1):17–30

    Article  CAS  PubMed  Google Scholar 

  • Eklund L, Saharinen P (2013) Angiopoietin signaling in the vasculature. Exp Cell Res 319(9):1271–1280

    Article  CAS  PubMed  Google Scholar 

  • El Omari K, Hoosdally SJ, Tuladhar K, Karia D, Vyas P, Patient R, Porcher C, Mancini EJ (2011) Structure of the leukemia oncogene LMO2: implications for the assembly of a hematopoietic transcription factor complex. Blood 117(7):2146–2156

    Article  PubMed  Google Scholar 

  • Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, Prykhozhij S, Peri F, Wilson SW, Ruhrberg C (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116(5):829–840

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Fehling HJ, Lacaud G, Kubo A, Kennedy M, Robertson S, Keller G, Kouskoff V (2003) Tracking mesoderm induction and its specification to the hemangioblast during embryonic stem cell differentiation. Development 130(17):4217–4227

    Article  CAS  PubMed  Google Scholar 

  • Ferrier R, Nougarede R, Doucet S, Kahn-Perles B, Imbert J, Mathieu-Mahul D (1999) Physical interaction of the bHLH LYL1 protein and NF-kappaB1 p105. Oncogene 18(4):995–1005

    Article  CAS  PubMed  Google Scholar 

  • Fiedler U, Scharpfenecker M, Koidl S, Hegen A, Grunow V, Schmidt JM, Kriz W, Thurston G, Augustin HG (2004) The Tie-2 ligand angiopoietin-2 is stored in and rapidly released upon stimulation from endothelial cell Weibel-Palade bodies. Blood 103(11):4150–4156

    Article  CAS  PubMed  Google Scholar 

  • Gering M, Rodaway AR, Gottgens B, Patient RK, Green AR (1998) The SCL gene specifies haemangioblast development from early mesoderm. EMBO J 17(14):4029–4045

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gering M, Yamada Y, Rabbitts TH, Patient RK (2003) Lmo2 and Scl/Tal1 convert non-axial mesoderm into haemangioblasts which differentiate into endothelial cells in the absence of Gata1. Development 130(25):6187–6199

    Article  CAS  PubMed  Google Scholar 

  • Giroux S, Kaushik AL, Capron C, Jalil A, Kelaidi C, Sablitzky F, Dumenil D, Albagli O, Godin I (2007) lyl-1 and tal-1/scl, two genes encoding closely related bHLH transcription factors, display highly overlapping expression patterns during cardiovascular and hematopoietic ontogeny. Gene Expr Patterns 7(3):215–226

    Article  CAS  PubMed  Google Scholar 

  • Goardon N, Lambert JA, Rodriguez P, Nissaire P, Herblot S, Thibault P, Dumenil D, Strouboulis J, Romeo PH, Hoang T (2006) ETO2 coordinates cellular proliferation and differentiation during erythropoiesis. EMBO J 25:357–366

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Gory-Faure S, Prandini MH, Pointu H, Roullot V, Pignot-Paintrand I, Vernet M, Huber P (1999) Role of vascular endothelial-cadherin in vascular morphogenesis. Development 126(10):2093–2102

    CAS  PubMed  Google Scholar 

  • Harris IS, Black BL (2010) Development of the endocardium. Pediatr Cardiol 31(3):391–399

    Article  PubMed Central  PubMed  Google Scholar 

  • Herberth B, Minko K, Csillag A, Jaffredo T, Madarasz E (2005) SCL, GATA-2 and Lmo2 expression in neurogenesis. Int J Dev Neurosci 23(5):449–463

    Article  CAS  PubMed  Google Scholar 

  • Hsu HL, Wadman I, Baer R (1994) Formation of in vivo complexes between the TAL1 and E2A polypeptides of leukemic T cells. Proc Natl Acad Sci U S A 91(8):3181–3185

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang S, Brandt SJ (2000) mSin3A regulates murine erythroleukemia cell differentiation through association with the TAL1 (or SCL) transcription factor. Mol Cell Biol 20(6):2248–2259

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Huang S, Qiu Y, Stein RW, Brandt SJ (1999) p300 functions as a transcriptional coactivator for the TAL1/SCL oncoprotein. Oncogene 18(35):4958–4967

    Article  CAS  PubMed  Google Scholar 

  • Hwang LY, Siegelman M, Davis L, Oppenheimer MN, Baer R (1993) Expression of the TAL1 proto-oncogene in cultured endothelial cells and blood vessels of the spleen. Oncogene 8(11):3043–3046

    CAS  PubMed  Google Scholar 

  • Jaffredo T, Lempereur A, Richard C, Bollerot K, Gautier R, Canto PY, Drevon C, Souyri M, Durand C (2013) Dorso-ventral contributions in the formation of the embryonic aorta and the control of aortic hematopoiesis. Blood Cells Mol Dis 51(4):232–238

    Article  PubMed  Google Scholar 

  • Kallianpur AR, Jordan JE, Brandt SJ (1994) The SCL/TAL-1 gene is expressed in progenitors of both the hematopoietic and vascular systems during embryogenesis. Blood 83(5):1200–1208

    CAS  PubMed  Google Scholar 

  • Kassouf MT, Chagraoui H, Vyas P, Porcher C (2008) Differential use of SCL/TAL-1 DNA-binding domain in developmental hematopoiesis. Blood 112(4):1056–1067

    Article  CAS  PubMed  Google Scholar 

  • Kissa K, Herbomel P (2010) Blood stem cells emerge from aortic endothelium by a novel type of cell transition. Nature 464(7285):112–115

    Article  CAS  PubMed  Google Scholar 

  • Lahlil R, Lecuyer E, Herblot S, Hoang T (2004) SCL assembles a multifactorial complex that determines glycophorin A expression. Mol Cell Biol 24(4):1439–1452

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Landry JR, Bonadies N, Kinston S, Knezevic K, Wilson NK, Oram SH, Janes M, Piltz S, Hammett M, Carter J, Hamilton T, Donaldson IJ, Lacaud G, Frampton J, Follows G, Kouskoff V, Gottgens B (2009) Expression of the leukemia oncogene Lmo2 is controlled by an array of tissue-specific elements dispersed over 100 kb and bound by Tal1/Lmo2, Ets, and Gata factors. Blood 113(23):5783–5792

    Article  CAS  PubMed  Google Scholar 

  • Lazrak M, Lecointe N, Dohet C, Mathieu D (2001) Upregulation of the basic helix-loop-helix tal-1 transcription factor in endothelial: a switch from quiescent to angiogenic phenotype? Blood (ASH Meeting) 98:30

    Google Scholar 

  • Lazrak M, Deleuze V, Noel D, Haouzi D, Chalhoub E, Dohet C, Robbins I, Mathieu D (2004) The bHLH TAL-1/SCL regulates endothelial cell migration and morphogenesis. J Cell Sci 117(Pt 7):1161–1171

    Article  CAS  PubMed  Google Scholar 

  • Lecuyer E, Lariviere S, Sincennes MC, Haman A, Lahlil R, Todorova M, Tremblay M, Wilkes BC, Hoang T (2007) Protein stability and transcription factor complex assembly determined by the SCL-LMO2 interaction. J Biol Chem 282(46):33649–33658

    Article  CAS  PubMed  Google Scholar 

  • Lukov GL, Goodell MA (2010) LYL1 degradation by the proteasome is directed by a N-terminal PEST rich site in a phosphorylation-independent manner. PLoS One 5(9):1–7

    Article  Google Scholar 

  • Lyden D, Young AZ, Zagzag D, Yan W, Gerald W, O’Reilly R, Bader BL, Hynes RO, Zhuang Y, Manova K, Benezra R (1999) Id1 and Id3 are required for neurogenesis, angiogenesis and vascularization of tumour xenografts. Nature 401(6754):670–677

    Article  CAS  PubMed  Google Scholar 

  • Lyden D, Hattori K, Dias S, Costa C, Blaikie P, Butros L, Chadburn A, Heissig B, Marks W, Witte L, Wu Y, Hicklin D, Zhu Z, Hackett NR, Crystal RG, Moore MA, Hajjar KA, Manova K, Benezra R, Rafii S (2001) Impaired recruitment of bone-marrow-derived endothelial and hematopoietic precursor cells blocks tumor angiogenesis and growth. Nat Med 7(11):1194–1201

    Article  CAS  PubMed  Google Scholar 

  • Massari ME, Murre C (2000) Helix-loop-helix proteins: regulators of transcription in eucaryotic organisms. Mol Cell Biol 20(2):429–440

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Miyamoto A, Cui X, Naumovski L, Cleary ML (1996) Helix-loop-helix proteins LYL1 and E2a form heterodimeric complexes with distinctive DNA-binding properties in hematolymphoid cells. Mol Cell Biol 16(5):2394–2401

    CAS  PubMed Central  PubMed  Google Scholar 

  • Nishiyama K, Takaji K, Uchijima Y, Kurihara Y, Asano T, Yoshimura M, Ogawa H, Kurihara H (2007) Protein kinase A-regulated nucleocytoplasmic shuttling of Id1 during angiogenesis. J Biol Chem 282(23):17200–17209

    Article  CAS  PubMed  Google Scholar 

  • Patterson LJ, Gering M, Patient R (2005) Scl is required for dorsal aorta as well as blood formation in zebrafish embryos. Blood 105(9):3502–3511

    Article  CAS  PubMed  Google Scholar 

  • Pirot N, Deleuze V, El-Hajj R, Dohet C, Sablitzky F, Couttet P, Mathieu D, Pinet V (2010) LYL1 activity is required for the maturation of newly formed blood vessels in adulthood. Blood 115(25):5270–5279

    Article  CAS  PubMed  Google Scholar 

  • Porcher C, Swat W, Rockwell K, Fujiwara Y, Alt FW, Orkin SH (1996) The T cell leukemia oncoprotein SCL/tal-1 is essential for development of all hematopoietic lineages. Cell 86(1):47–57

    Article  CAS  PubMed  Google Scholar 

  • Porcher C, Liao EC, Fujiwara Y, Zon LI, Orkin SH (1999) Specification of hematopoietic and vascular development by the bHLH transcription factor SCL without direct DNA binding. Development 126(20):4603–4615

    CAS  PubMed  Google Scholar 

  • Potente M, Gerhardt H, Carmeliet P (2011) Basic and therapeutic aspects of angiogenesis. Cell 146(6):873–887

    Article  CAS  PubMed  Google Scholar 

  • Pulford K, Lecointe N, Leroy VK, Jones M, Mathieu MD, Mason DY (1995) Expression of TAL-1 proteins in human tissues. Blood 85(3):675–684

    CAS  PubMed  Google Scholar 

  • Rabbitts TH (1998) LMO T-cell translocation oncogenes typify genes activated by chromosomal translocations that alter transcription and developmental processes. Genes Dev 12(17):2651–2657

    Article  CAS  PubMed  Google Scholar 

  • Ravet E, Reynaud D, Titeux M, Izac B, Fichelson S, Romeo PH, Dubart-Kupperschmitt A, Pflumio F (2004) Characterization of DNA-binding-dependent and -independent functions of SCL/TAL1 during human erythropoiesis. Blood 103(9):3326–3335

    Article  CAS  PubMed  Google Scholar 

  • Ren X, Gomez GA, Zhang B, Lin S (2010) Scl isoforms act downstream of etsrp to specify angioblasts and definitive hematopoietic stem cells. Blood 115(26):5338–5346

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Robb L, Lyons I, Li R, Hartley L, Kontgen F, Harvey RP, Metcalf D, Begley CG (1995) Absence of yolk sac hematopoiesis from mice with a targeted disruption of the scl gene. Proc Natl Acad Sci U S A 92(15):7075–7079

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Robb L, Elwood NJ, Elefanty AG, Kontgen F, Li R, Barnett LD, Begley CG (1996) The scl gene product is required for the generation of all hematopoietic lineages in the adult mouse. EMBO J 15(16):4123–4129

    CAS  PubMed Central  PubMed  Google Scholar 

  • Ryan DP, Duncan JL, Lee C, Kuchel PW, Matthews JM (2008) Assembly of the oncogenic DNA-binding complex LMO2-Ldb1-TAL1-E12. Proteins 70(4):1461–1474

    Article  CAS  PubMed  Google Scholar 

  • San-Marina S, Han Y, Suarez Saiz F, Trus MR, Minden MD (2008) Lyl1 interacts with CREB1 and alters expression of CREB1 target genes. Biochim Biophys Acta 1783(3):503–517

    Article  CAS  PubMed  Google Scholar 

  • San-Marina S, Han Y, Liu J, Minden MD (2012) Suspected leukemia oncoproteins CREB1 and LYL1 regulate Op18/STMN1 expression. Biochim Biophys Acta 1819(11–12):1164–1172

    Article  CAS  PubMed  Google Scholar 

  • Schlaeger TM, Schuh A, Flitter S, Fisher A, Mikkola H, Orkin SH, Vyas P, Porcher C (2004) Decoding hematopoietic specificity in the helix-loop-helix domain of the transcription factor SCL/Tal-1. Mol Cell Biol 24(17):7491–7502

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schuh AH, Tipping AJ, Clark AJ, Hamlett I, Guyot B, Iborra FJ, Rodriguez P, Strouboulis J, Enver T, Vyas P, Porcher C (2005) ETO-2 associates with SCL in erythroid cells and megakaryocytes and provides repressor functions in erythropoiesis. Mol Cell Biol 25(23):10235–10250

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Schumacher JA, Bloomekatz J, Garavito-Aguilar ZV, Yelon D (2013) tal1 regulates the formation of intercellular junctions and the maintenance of identity in the endocardium. Dev Biol 383(2):214–226

    Article  CAS  PubMed  Google Scholar 

  • Shivdasani RA, Mayer EL, Orkin SH (1995) Absence of blood formation in mice lacking the T-cell leukaemia oncoprotein tal-1/SCL. Nature 373(6513):432–434

    Article  CAS  PubMed  Google Scholar 

  • Souroullas GP, Goodell MA (2011) A new allele of Lyl1 confirms its important role in hematopoietic stem cell function. Genesis 49(6):441–448

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Souroullas GP, Salmon JM, Sablitzky F, Curtis DJ, Goodell MA (2009) Adult hematopoietic stem and progenitor cells require either Lyl1 or Scl for survival. Cell Stem Cell 4(2):180–186

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Strilic B, Kucera T, Eglinger J, Hughes MR, McNagny KM, Tsukita S, Dejana E, Ferrara N, Lammert E (2009) The molecular basis of vascular lumen formation in the developing mouse aorta. Dev Cell 17(4):505–515

    Article  CAS  PubMed  Google Scholar 

  • Tang T, Shi Y, Opalenik SR, Brantley-Sieders DM, Chen J, Davidson JM, Brandt SJ (2006) Expression of the TAL1/SCL transcription factor in physiological and pathological vascular processes. J Pathol 210(1):121–129

    Article  CAS  PubMed  Google Scholar 

  • Van Handel B, Montel-Hagen A, Sasidharan R, Nakano H, Ferrari R, Boogerd CJ, Schredelseker J, Wang Y, Hunter S, Org T, Zhou J, Li X, Pellegrini M, Chen JN, Orkin SH, Kurdistani SK, Evans SM, Nakano A, Mikkola HK (2012) Scl represses cardiomyogenesis in prospective hemogenic endothelium and endocardium. Cell 150(3):590–605

    Article  PubMed Central  PubMed  Google Scholar 

  • Vandenbroucke E, Mehta D, Minshall R, Malik AB (2008) Regulation of endothelial junctional permeability. Ann N Y Acad Sci 1123:134–145

    Article  CAS  PubMed  Google Scholar 

  • Visvader JE, Fujiwara Y, Orkin SH (1998) Unsuspected role for the T-cell leukemia protein SCL/tal-1 in vascular development. Genes Dev 12(4):473–479

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Wadman I, Li J, Bash RO, Forster A, Osada H, Rabbitts TH, Baer R (1994) Specific in vivo association between the bHLH and LIM proteins implicated in human T cell leukemia. EMBO J 13(20):4831–4839

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wadman IA, Osada H, Grutz GG, Agulnick AD, Westphal H, Forster A, Rabbitts TH (1997) The LIM-only protein Lmo2 is a bridging molecule assembling an erythroid, DNA-binding complex which includes the TAL1, E47, GATA-1 and Ldb1/NLI proteins. EMBO J 16(11):3145–3157

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Warren AJ, Colledge WH, Carlton MB, Evans MJ, Smith AJ, Rabbitts TH (1994) The oncogenic cysteine-rich LIM domain protein rbtn2 is essential for erythroid development. Cell 78(1):45–57

    Article  CAS  PubMed  Google Scholar 

  • Weiss O, Kaufman R, Michaeli N, Inbal A (2012) Abnormal vasculature interferes with optic fissure closure in lmo2 mutant zebrafish embryos. Dev Biol 369(2):191–198

    Article  CAS  PubMed  Google Scholar 

  • Wilson NK, Foster SD, Wang X, Knezevic K, Schutte J, Kaimakis P, Chilarska PM, Kinston S, Ouwehand WH, Dzierzak E, Pimanda JE, de Bruijn MF, Gottgens B (2010) Combinatorial transcriptional control in blood stem/progenitor cells: genome-wide analysis of ten major transcriptional regulators. Cell Stem Cell 7(4):532–544

    Article  CAS  PubMed  Google Scholar 

  • Yamada Y, Warren AJ, Dobson C, Forster A, Pannell R, Rabbitts TH (1998) The T cell leukemia LIM protein Lmo2 is necessary for adult mouse hematopoiesis. Proc Natl Acad Sci U S A 95(7):3890–3895

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Yamada Y, Pannell R, Forster A, Rabbitts TH (2000) The oncogenic LIM-only transcription factor Lmo2 regulates angiogenesis but not vasculogenesis in mice. Proc Natl Acad Sci U S A 97(1):320–324

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Zhen F, Lan Y, Yan B, Zhang W, Wen Z (2013) Hemogenic endothelium specification and hematopoietic stem cell maintenance employ distinct Scl isoforms. Development 140(19):3977–3985

    Article  CAS  PubMed  Google Scholar 

  • Zohren F, Souroullas GP, Luo M, Gerdemann U, Imperato MR, Wilson NK, Gottgens B, Lukov GL, Goodell MA (2012) The transcription factor Lyl-1 regulates lymphoid specification and the maintenance of early T lineage progenitors. Nat Immunol 13(8):761–769

    Article  CAS  PubMed Central  PubMed  Google Scholar 

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Authors and Affiliations

  1. Institute of Molecular Genetics (IGMM), CNRS UMR 5535, University of Montpellier, 1919 route de Mende, 34293, Montpellier, France

    Valérie Pinet, Virginie Deleuze & Danièle Mathieu

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  1. Valérie Pinet
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  2. Virginie Deleuze
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  3. Danièle Mathieu
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Correspondence to Danièle Mathieu .

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  1. UMR 1036, Biologie du Cancer et de l’Infection, Institut de Recherches en Technologies et Sciences pour le Vivant, Université Grenoble-Alpes, Grenoble, France

    Jean-Jacques Feige

  2. Institute for Research on Cancer and aging of Nice (IRCAN), University of Nice Sophia Antipolis, Nice, France

    Gilles Pagès

  3. CNRS UMR8161, Institut Pasteur de Lille, Institut de Biologie de Lille, Lille, France

    Fabrice Soncin

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Pinet, V., Deleuze, V., Mathieu, D. (2014). Emerging Role of the Two Related Basic Helix-Loop-Helix Proteins TAL1 and LYL1 in Angiogenesis. In: Feige, JJ., Pagès, G., Soncin, F. (eds) Molecular Mechanisms of Angiogenesis. Springer, Paris. https://doi.org/10.1007/978-2-8178-0466-8_7

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