The VEGF-regulated transcription factor HLX controls the expression of guidance cues and negatively regulates sprouting of endothelial cells

Blood

Volumn 117, Issue 9, 2011, Pages 2735-2744

  Testori, Julia ^a   Schweighofer, Bernhard ^a,d   Helfrich, Iris ^b,e   Sturtzel, Caterina ^a   Lipnik, Karoline ^a   Gesierich, Sabine ^b   Nasarre, Patrick ^b,f   Hofer Warbinek, Renate ^a   Bilban, Martin ^a,c   Augustin, Hellmut G ^b   Hofer, Erhard ^a  

^a MEDICAL UNIVERSITY OF VIENNA   (Austria)

^b UNIVERSITY OF HEIDELBERG   (Germany)

^c LUDWIG BOLTZMANN INSTITUTE FOR LUNG VASCULAR RESEARCH   (Austria)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

^e UNIVERSITY HOSPITAL ESSEN   (Germany)

^f MEDICAL UNIVERSITY OF SOUTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN A1; INTERLEUKIN 27; MESSENGER RNA; PLEXIN A1; PROTEIN; SEMAPHORIN 3G; SHORT HAIRPIN RNA; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR HES 1; TRANSCRIPTION FACTOR HLX; TRANSCRIPTION FACTOR SLUG; UNCLASSIFIED DRUG; UNCOORDINATED 5B RECEPTOR; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CELL PROLIFERATION; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; HYPOXIA; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPRESSOR GENE; UPREGULATION;

EID: 79953104037     PISSN: 00064971     EISSN: 15280020     Source Type: Journal    
DOI: 10.1182/blood-2010-07-293209     Document Type: Article

References (42)

1. Lohela M, Bry M, Tammela T, Alitalo K. VEGFs and receptors involved in angiogenesis versus lymphangiogenesis. Curr Opin Cell Biol. 2009;21(2):154-165.
2. Adams RH, Alitalo K. Molecular regulation of angiogenesis and lymphangiogenesis. Nat Rev Mol Cell Biol. 2007;8(6):464-478. (Pubitemid 46823443)
3. Loges S, Roncal C, Carmeliet P. Development of targeted angiogenic medicine. J Thromb Haemost. 2009;7(1):21-33.
4. Ferrara N. Vascular endothelial growth factor: basic science and clinical progress. Endocr Rev. 2004;25(4):581-611. (Pubitemid 39099316)
5. Schweighofer B, Testori J, Sturtzel C, et al. The VEGF-induced transcriptional response comprises gene clusters at the crossroad of angiogenesis and inflammation. Thromb Haemost. 2009;102(3):544-554.
6. Minami T, Horiuchi K, Miura M, et al. Vascular endothelial growth factor- and thrombin-induced termination factor, Down syndrome critical region- 1, attenuates endothelial cell proliferation and angiogenesis. J Biol Chem. 2004;279(48):50537-50554. (Pubitemid 39577872)
7. Liu D, Jia H, Holmes DI, Stannard A, Zachary I. Vascular endothelial growth factor-regulated gene expression in endothelial cells: KDR-mediated induction of Egr3 and the related nuclear receptors Nur77, Nurr1, and Nor1. Arterioscler Thromb Vasc Biol. 2003;23(11):2002-2007.
8. Hofer E, Schweighofer B. Signal transduction induced in endothelial cells by growth factor receptors involved in angiogenesis. Thromb Haemost. 2007;97(3):355-363. (Pubitemid 46437796)
9. Barad M, Erlebacher A, McGinnis W. Despite expression in embryonic visceral mesoderm, H2.0 is not essential for Drosophila visceral muscle morphogenesis. Dev Genet. 1991;12(3):206-211.
10. Deguchi Y, Kehrl JH. Selective expression of two homeobox genes in CD34-positive cells from human bone marrow. Blood. 1991;78(2):323-328.
11. Mikhalkevich N, Becknell B, Caligiuri MA, Bates MD, Harvey R, Zheng WP. Responsiveness of naive CD4 T cells to polarizing cytokine determines the ratio of Th1 and Th2 cell differentiation. J Immunol. 2006;176(3):1553-1560. (Pubitemid 43134299)
12. Mullen AC, Hutchins AS, High FA, et al. Hlx is induced by and genetically interacts with T-bet to promote heritable T(H)1 gene induction. Nat Immunol. 2002;3(7):652-658. (Pubitemid 34752474)
13. Becknell B, Hughes TL, Freud AG, et al. Hlx homeobox transcription factor negatively regulates interferon-gamma production in monokine-activated natural killer cells. Blood. 2007;109(6):2481-2487. (Pubitemid 46425892)
14. Murthi P, So M, Gude NM, Doherty VL, Brennecke SP, Kalionis B. Homeobox genes are differentially expressed in macrovascular human umbilical vein endothelial cells and microvascular placental endothelial cells. Placenta. 2007;28(2-3):219-223. (Pubitemid 44914527)
15. Hentsch B, Lyons I, Li R, et al. Hlx homeo box gene is essential for an inductive tissue interaction that drives expansion of embryonic liver and gut. Genes Dev. 1996;10(1):70-79. (Pubitemid 26025300)
16. Bates MD, Dunagan DT, Welch LC, Kaul A, Harvey RP. The Hlx homeobox transcription factor is required early in enteric nervous system development. BMC Dev Biol. 2006;6:33.
17. Larrivee B, Freitas C, Suchting S, Brunet I, Eichmann A. Guidance of vascular development: lessons from the nervous system. Circ Res. 2009;104(4):428-441.
18. Wojta J, Hoover RL, Daniel TO. Vascular origin determines plasminogen activator expression in human endothelial cells. Renal endothelial cells produce large amounts of single chain urokinase type plasminogen activator. J Biol Chem. 1989; 264(5):2846-2852. (Pubitemid 19057779)
19. Gomez-Foix AM, Coats WS, Baque S, Alam T, Gerard RD, Newgard CB. Adenovirus-mediated transfer of the muscle glycogen phosphorylase gene into hepatocytes confers altered regulation of glycogen metabolism. J Biol Chem. 1992;267(35):25129-25134.
20. Lucerna M, Mechtcheriakova D, Kadl A, et al. NAB2, a corepressor of EGR-1, inhibits vascular endothelial growth factor-mediated gene induction and angiogenic responses of endothelial cells. J Biol Chem. 2003;278(13):11433- 11440. (Pubitemid 36792702)
21. Bilban M, Ghaffari-Tabrizi N, Hintermann E, et al. Kisspeptin-10, a KiSS-1/metastin-derived decapeptide, is a physiological invasion inhibitor of primary human trophoblasts. J Cell Sci. 2004; 117(Pt 8):1319-1328. (Pubitemid 38559810)
22. Bilban M, Heintel D, Scharl T, et al. Deregulated expression of fat and muscle genes in B-cell chronic lymphocytic leukemia with high lipoprotein lipase expression. Leukemia. 2006;20(6):1080-1088. (Pubitemid 43797301)
23. Vichai V, Kirtikara K. Sulforhodamine B colorimetric assay for cytotoxicity screening. Nat Protoc. 2006;1(3):1112-1116.
24. Korff T, Krauss T, Augustin HG. Three-dimensional spheroidal culture of cytotrophoblast cells mimics the phenotype and differentiation of cytotrophoblasts from normal and preeclamptic pregnancies. Exp Cell Res. 2004;297(2):415-423. (Pubitemid 38798403)
25. Korff T, Augustin HG. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci. 1999;112(Pt 19):3249-3258. (Pubitemid 29507205)
26. Manalo DJ, Rowan A, Lavoie T, et al. Transcriptional regulation of vascular endothelial cell responses to hypoxia by HIF-1. Blood. 2005;105(2):659-669. (Pubitemid 40070750)
27. Alajati A, Laib AM, Weber H, et al. Spheroid-based engineering of a human vasculature in mice. Nat Methods. 2008;5(5):439-445. (Pubitemid 351619103)
28. Cantile M, Schiavo G, Terracciano L, Cillo C. Homeobox genes in normal and abnormal vasculogenesis. Nutr Metab Cardiovasc Dis. 2008; 18(10):651-658.
29. Douville JM, Wigle JT. Regulation and function of homeodomain proteins in the embryonic and adult vascular systems. Can J Physiol Pharmacol. 2007;85(1):55-65. (Pubitemid 46996104)
30. Gorski DH, Walsh K. Control of vascular cell differentiation by homeobox transcription factors. Trends Cardiovasc Med. 2003;13(6):213-220. (Pubitemid 36960167)
31. Presta M, Dell'Era P, Mitola S, Moroni E, Ronca R, Rusnati M. Fibroblast growth factor/fibroblast growth factor receptor system in angiogenesis. Cytokine Growth Factor Rev. 2005;16(2):159-178. (Pubitemid 40616114)
32. Rajaraman G, Murthi P, Leo B, Brennecke SP, Kalionis B. Homeobox gene HLX1 is a regulator of colony stimulating factor-1 dependent trophoblast cell proliferation. Placenta. 2007;28(10): 991-998. (Pubitemid 47355229)
33. Rajaraman G, Murthi P, Pathirage N, Brennecke SP, Kalionis B. Downstream targets of homeobox gene HLX show altered expression in human idiopathic fetal growth restriction. Am J Pathol. 2010;176(1):278-287.
34. Lu X, Le Noble F, Yuan L, et al. The netrin receptor UNC5B mediates guidance events controlling morphogenesis of the vascular system. Nature. 2004;432(7014):179-186. (Pubitemid 39545842)
35. Larrivee B, Freitas C, Trombe M, et al. Activation of the UNC5B receptor by Netrin-1 inhibits sprouting angiogenesis. Genes Dev. 2007;21(19):2433-2447. (Pubitemid 47533561)
36. Gaur P, Bielenberg DR, Samuel S, et al. Role of class 3 semaphorins and their receptors in tumor growth and angiogenesis. Clin Cancer Res. 2009; 15(22):6763-6770.
37. Neufeld G, Kessler O. The semaphorins: versatile regulators of tumour progression and tumour angiogenesis. Nat Rev Cancer. 2008;8(8):632-645.
38. Kutschera S, Weber H, Weick A, et al. Differential endothelial transcriptomics identifies semaphorin 3G as a vascular class 3 semaphorin. Arterioscler Thromb Vasc Biol. 2011; 31(1):151-159.
39. Serini G, Valdembri D, Zanivan S, et al. Class 3 semaphorins control vascular morphogenesis by inhibiting integrin function. Nature. 2003;4246947):391-397. (Pubitemid 36917481)
40. Fischer A, Gessler M. Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res. 2007;35(14):4583-4596. (Pubitemid 47250333)
41. Roca C, Adams RH. Regulation of vascular morphogenesis by Notch signaling. Genes Dev. 2007;21(20):2511-2524. (Pubitemid 47607663)
42. Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell. 2009;16(2):196-208.