Influence of dll4 via hif-1α-vegf signaling on the angiogenesis of choroidal neovascularization under hypoxic conditions

PLoS ONE

Volumn 6, Issue 4, 2011, Pages

  Dong, Xiao ^a   Wang, Yu Sheng ^a   Dou, Guo Rui ^a   Hou, Hui Yuan ^a   Shi, Yuan Yuan ^a   Zhang, Rui ^b   Ma, Ke ^a   Wu, Lin ^b   Yao, Li Bo ^b   Cai, Yan ^a   Zhang, Jian ^b  

^a FOURTH MILITARY MEDICAL UNIVERSITY   (China)

^b FOURTH MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

DELTA LIKE LIGAND 4; EPHRIN; EPHRIN B2; EPHRIN B4; GAMMA SECRETASE INHIBITOR; HYPOXIA INDUCIBLE FACTOR 1ALPHA; MESSENGER RNA; NOTCH RECEPTOR; SMALL INTERFERING RNA; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN RECEPTOR 1; VASCULOTROPIN RECEPTOR 2; MEMBRANE PROTEIN; PROTEIN; VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL INVASION; CELL MIGRATION; CELL PROLIFERATION; COCULTURE; CONTROLLED STUDY; HYPOXIA; IMMUNOFLUORESCENCE TEST; MIGRATION INHIBITION; NONHUMAN; PROTEIN EXPRESSION; PROTEIN FUNCTION; QUANTITATIVE ANALYSIS; RAT; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SUBRETINAL NEOVASCULARIZATION; UPREGULATION; WESTERN BLOTTING; ANIMAL; CELL HYPOXIA; CELL LINE; CELL MOTION; GENETIC TRANSFECTION; GENETICS; HUMAN; MACACA MULATTA; METABOLISM; PATHOLOGY; PIGMENT EPITHELIUM;

RATTUS;

ANIMALS; CELL HYPOXIA; CELL LINE; CELL MOVEMENT; CELL PROLIFERATION; CHOROIDAL NEOVASCULARIZATION; COCULTURE TECHNIQUES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MACACA MULATTA; MEMBRANE PROTEINS; RATS; RETINAL PIGMENT EPITHELIUM; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; TRANSFECTION; UP-REGULATION; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 79955434679     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0018481     Document Type: Article

References (52)

1. Grossniklaus HE, Green WR, (2004) Choroidal neovascularization. Am J Ophthalmol 137: 496-503.
2. Saint-Geniez M, Maldonado AE, D'Amore PA, (2006) VEGF expression and receptor activation in the choroid during development and in the adult. Invest Ophthalmol Vis Sci 47: 3135-3142.
3. Penn JS, Madan A, Caldwell RB, Bartoli M, Caldwell RW, et al. (2008) Vascular endothelial growth factor in eye disease. Prog Retin Eye Res 27: 331-371.
4. Hofmann JJ, Iruela-Arispe ML, (2007) Notch signaling in blood vessels: who is talking to whom about what? Circ Res 100: 1556-1568.
5. Phng LK, Gerhardt H, (2009) Angiogenesis: a team effort coordinated by notch. Dev Cell 16: 196-208.
6. Shutter JR, Scully S, Fan W, Richards WG, Kitajewski J, et al. (2000) Dll4, a novel Notch ligand expressed in arterial endothelium. Genes Dev 14: 1313-1318.
7. Gale NW, Dominguez MG, Noguera I, Pan L, Hughes V, et al. (2004) Haploinsufficiency of delta-like 4 ligand results in embryonic lethality due to major defects in arterial and vascular development. Proc Natl Acad Sci U S A 101: 15949-15954.
8. Krebs LT, Shutter JR, Tanigaki K, Honjo T, Stark KL, et al. (2004) Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 18: 2469-2473.
9. Ferrara N, Carver-Moore K, Chen H, Dowd M, Lu L, et al. (1996) Heterozygous embryonic lethality induced by targeted inactivation of the VEGF gene. Nature 380: 439-442.
10. Mailhos C, Modlich U, Lewis J, Harris A, Bicknell R, et al. (2001) Delta4, an endothelial specific notch ligand expressed at sites of physiological and tumor angiogenesis. Differentiation 69: 135-144.
11. Hofmann JJ, Luisa IM, (2007) Notch expression patterns in the retina: An eye on receptor-ligand distribution during angiogenesis. Gene Expr Patterns 7: 461-470.
12. Suchting S, Freitas C, le Noble F, Benedito R, Breant C, et al. (2007) The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci U S A 104: 3225-3230.
13. Li JL, Harris AL, (2009) Crosstalk of VEGF and Notch pathways in tumour angiogenesis: therapeutic implications. Front Biosci 14: 3094-3110.
14. Jakobsson L, Bentley K, Gerhardt H, (2009) VEGFRs and Notch: a dynamic collaboration in vascular patterning. Biochem Soc Trans 37: 1233-1236.
15. Dou GR, Wang YC, Hu XB, Hou LH, Wang CM, et al. (2008) RBP-J, the transcription factor downstream of Notch receptors, is essential for the maintenance of vascular homeostasis in adult mice. FASEB J 22: 1606-1617.
16. Arjamaa O, Nikinmaa M, Salminen A, Kaarniranta K, (2009) Regulatory role of HIF-1alpha in the pathogenesis of age-related macular degeneration (AMD). Ageing Res Rev 8: 349-358.
17. Zhang P, Zhang X, Hao X, Wang Y, Hui Y, et al. (2009) Rac1 activates HIF-1 in retinal pigment epithelium cells under hypoxia. Graefes Arch Clin Exp Ophthalmol 247: 633-639.
18. Zhang P, Wang Y, Hui Y, Hu D, Wang H, et al. (2007) Inhibition of VEGF expression by targeting HIF-1 alpha with small interference RNA in human RPE cells. Ophthalmologica 221: 411-417.
19. Zhao W, Wang YS, Hui YN, Zhu J, Zhang P, et al. (2008) Inhibition of proliferation, migration and tube formation of choroidal microvascular endothelial cells by targeting HIF-1alpha with short hairpin RNA-expressing plasmid DNA in human RPE cells in a coculture system. Graefes Arch Clin Exp Ophthalmol 246: 1413-1422.
20. Diez H, Fischer A, Winkler A, Hu CJ, Hatzopoulos AK, et al. (2007) Hypoxia-mediated activation of Dll4-Notch-Hey2 signaling in endothelial progenitor cells and adoption of arterial cell fate. Exp Cell Res 313: 1-9.
21. Jubb AM, Turley H, Moeller HC, Steers G, Han C, et al. (2009) Expression of delta-like ligand 4 (Dll4) and markers of hypoxia in colon cancer. Br J Cancer 101: 1749-1757.
22. Patel NS, Li JL, Generali D, Poulsom R, Cranston DW, et al. (2005) 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.
23. Taylor KL, Henderson AM, Hughes CC, (2002) Notch activation during endothelial cell network formation in vitro targets the basic HLH transcription factor HESR-1 and downregulates VEGFR-2/KDR expression. Microvasc Res 64: 372-383.
24. Hainaud P, Contreres JO, Villemain A, Liu LX, Plouet J, et al. (2006) The role of the vascular endothelial growth factor-Delta-like 4 ligand/Notch4-ephrin B2 cascade in tumor vessel remodeling and endothelial cell functions. Cancer Res 66: 8501-8510.
25. Yamanda S, Ebihara S, Asada M, Okazaki T, Niu K, et al. (2009) Role of ephrinB2 in nonproductive angiogenesis induced by Delta-like 4 blockade. Blood 113: 3631-3639.
26. Lai EC, (2004) Notch signaling: control of cell communication and cell fate. Development 131: 965-973.
27. Artavanis-Tsakonas S, Rand MD, Lake RJ, (1999) Notch signaling: cell fate control and signal integration in development. Science 284: 770-776.
28. Kopan R, Ilagan MX, (2009) The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-233.
29. Shawber CJ, Kitajewski J, (2004) Notch function in the vasculature: insights from zebrafish, mouse and man. Bioessays 26: 225-234.
30. Benedito R, Duarte A, (2005) Expression of Dll4 during mouse embryogenesis suggests multiple developmental roles. Gene Expr Patterns 5: 750-755.
31. Leslie JD, Ariza-McNaughton L, Bermange AL, McAdow R, Johnson SL, et al. (2007) Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134: 839-844.
32. Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, et al. (2001) Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development 128: 3675-3683.
33. Claxton S, Fruttiger M, (2004) Periodic Delta-like 4 expression in developing retinal arteries. Gene Expr Patterns 5: 123-127.
34. Scehnet JS, Jiang W, Kumar SR, Krasnoperov V, Trindade A, et al. (2007) Inhibition of Dll4-mediated signaling induces proliferation of immature vessels and results in poor tissue perfusion. Blood 109: 4753-4760.
35. Noguera-Troise I, Daly C, Papadopoulos NJ, Coetzee S, Boland P, et al. (2007) Blockade of Dll4 inhibits tumour growth by promoting non-productive angiogenesis. Novartis Found Symp 283: 106-120, 121-125, 238-241.
36. Ottino P, Finley J, Rojo E, Ottlecz A, Lambrou GN, et al. (2004) Hypoxia activates matrix metalloproteinase expression and the VEGF system in monkey choroid-retinal endothelial cells: Involvement of cytosolic phospholipase A2 activity. Mol Vis 10: 341-350.
37. Sakamoto T, Sakamoto H, Murphy TL, Spee C, Soriano D, et al. (1995) Vessel formation by choroidal endothelial cells in vitro is modulated by retinal pigment epithelial cells. Arch Ophthalmol 113: 512-520.
38. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, et al. (2007) Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci U S A 104: 3219-3224.
39. Liu ZJ, Shirakawa T, Li Y, Soma A, Oka M, et al. (2003) 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.
40. Chen L, Lu W, Wei B, Wang N, Li T, (2009) Influence of Delta-like ligand 4/Notch signal transduction pathway upon the biological behavior of human umbilical vein endothelial cells. Zhonghua Yi Xue Za Zhi 89: 3106-3110.
41. Williams CK, Li JL, Murga M, Harris AL, Tosato G, (2006) Up-regulation of the Notch ligand Delta-like 4 inhibits VEGF-induced endothelial cell function. Blood 107: 931-939.
42. Hartnett ME, Lappas A, Darland D, McColm JR, Lovejoy S, et al. (2003) Retinal pigment epithelium and endothelial cell interaction causes retinal pigment epithelial barrier dysfunction via a soluble VEGF-dependent mechanism. Exp Eye Res 77: 593-599.
43. Peterson LJ, Wittchen ES, Geisen P, Burridge K, Hartnett ME, (2007) Heterotypic RPE-choroidal endothelial cell contact increases choroidal endothelial cell transmigration via PI 3-kinase and Rac1. Exp Eye Res 84: 737-744.
44. Benedito R, Roca C, Sorensen I, Adams S, Gossler A, et al. (2009) The notch ligands Dll4 and Jagged1 have opposing effects on angiogenesis. Cell 137: 1124-1135.
45. Henderson AM, Wang SJ, Taylor AC, Aitkenhead M, Hughes CC, (2001) The basic helix-loop-helix transcription factor HESR1 regulates endothelial cell tube formation. J Biol Chem 276: 6169-6176.
46. Wang YS, Hui YN, Wiedemann P, (2002) Role of apoptosis in the cytotoxic effect mediated by daunorubicin in cultured human retinal pigment epithelial cells. J Ocul Pharmacol Ther 18: 377-387.
47. Hou HY, Liang HL, Wang YS, Zhang ZX, Wang BR, et al. (2010) A therapeutic strategy for choroidal neovascularization based on recruitment of mesenchymal stem cells to the sites of lesions. Mol Ther 18: 1837-1845.
48. Yang XM, Wang YS, Zhang J, Li Y, Xu JF, et al. (2009) Role of PI3K/Akt and MEK/ERK in mediating hypoxia-induced expression of HIF-1alpha and VEGF in laser-induced rat choroidal neovascularization. Invest Ophthalmol Vis Sci 50: 1873-1879.
49. Zhu J, Wang YS, Zhang J, Zhao W, Yang XM, et al. (2009) Focal adhesion kinase signaling pathway participates in the formation of choroidal neovascularization and regulates the proliferation and migration of choroidal microvascular endothelial cells by acting through HIF-1 and VEGF expression in RPE cells. Exp Eye Res 88: 910-918.
50. Lu F, Adelman RA, (2009) Are intravitreal bevacizumab and ranibizumab effective in a rat model of choroidal neovascularization? Graefes Arch Clin Exp Ophthalmol 247: 171-177.
51. Sancho-Tello M, Johnsen-Soriano S, Muriach M, Bosch-Morell F, Diaz-Llopis M, et al. (2009) Transient bevacizumab (avastin)-induced alterations in rat eyes. Ophthalmic Res 41: 28-35.
52. Geisen P, McColm JR, Hartnett ME, (2006) Choroidal endothelial cells transmigrate across the retinal pigment epithelium but do not proliferate in response to soluble vascular endothelial growth factor. Exp Eye Res 82: 608-619.