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Endothelial Snail Regulates Capillary Branching Morphogenesis via Vascular Endothelial Growth Factor Receptor 3 Expression
Endothelial cells have the intrinsic capacity to shuffle between tip, stalk, and phalanx cells in angiogenic processes. These transitions require the induction or repression of transcripts that are specific for their phenotypes, along with morphological changes. To gain insight into spatiotemporal induction during vascular branching morphogenesis, we used Affymetrix oligonucleotide arrays to screen for Snail. Then, we used stable, small-interfering RNA or the lentivirus-short hairpin RNA system to examine the angiogenic roles of endothelial Snail during retinal capillary morphogenesis. Knockdown of Snail in the developing retinal vasculature impaired deep capillary formation and attenuated vascular endothelial growth factor receptor 3 expression, indicating a functional link between Snail and vascular endothelial growth factor receptor 3. Moreover, we showed vascular endothelial growth factor receptor 3 as a transcriptional target of Snail in vitro. In the retinal vasculature, the deep capillary plexus is a unique vessel with only capillary. The deep capillary plays a critical role in retinal development, neuronal survival, and pathological conditions, including ischemic diseases. Our findings provide molecular insights into the role of the Snail-vascular endothelial growth factor receptor 3 axis in capillary formation under pathophysiological conditions.
Vyšlo v časopise: Endothelial Snail Regulates Capillary Branching Morphogenesis via Vascular Endothelial Growth Factor Receptor 3 Expression. PLoS Genet 11(7): e32767. doi:10.1371/journal.pgen.1005324
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pgen.1005324Souhrn
Endothelial cells have the intrinsic capacity to shuffle between tip, stalk, and phalanx cells in angiogenic processes. These transitions require the induction or repression of transcripts that are specific for their phenotypes, along with morphological changes. To gain insight into spatiotemporal induction during vascular branching morphogenesis, we used Affymetrix oligonucleotide arrays to screen for Snail. Then, we used stable, small-interfering RNA or the lentivirus-short hairpin RNA system to examine the angiogenic roles of endothelial Snail during retinal capillary morphogenesis. Knockdown of Snail in the developing retinal vasculature impaired deep capillary formation and attenuated vascular endothelial growth factor receptor 3 expression, indicating a functional link between Snail and vascular endothelial growth factor receptor 3. Moreover, we showed vascular endothelial growth factor receptor 3 as a transcriptional target of Snail in vitro. In the retinal vasculature, the deep capillary plexus is a unique vessel with only capillary. The deep capillary plays a critical role in retinal development, neuronal survival, and pathological conditions, including ischemic diseases. Our findings provide molecular insights into the role of the Snail-vascular endothelial growth factor receptor 3 axis in capillary formation under pathophysiological conditions.
Zdroje
1. Herbert SP, Stainier DY (2011) Molecular control of endothelial cell behaviour during blood vessel morphogenesis. Nat Rev Mol Cell Biol 12 : 551–564. doi: 10.1038/nrm3176 21860391
2. Gariano RF, Gardner TW (2005) Retinal angiogenesis in development and disease. Nature 438 : 960–966. 16355161
3. Fruttiger M (2007) Development of the retinal vasculature. Angiogenesis 10 : 77–88. 17322966
4. 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. 17296940
5. Shibuya M, Claesson-Welsh L (2006) Signal transduction by VEGF receptors in regulation of angiogenesis and lymphangiogenesis. Exp Cell Res 312 : 549–560. 16336962
6. Tammela T, Zarkada G, Wallgard E, Murtomaki A, Suchting S, et al. (2008) Blocking VEGFR-3 suppresses angiogenic sprouting and vascular network formation. Nature 454 : 656–660. doi: 10.1038/nature07083 18594512
7. Tammela T, Zarkada G, Nurmi H, Jakobsson L, Heinolainen K, et al. (2011) VEGFR-3 controls tip to stalk conversion at vessel fusion sites by reinforcing Notch signalling. Nat Cell Biol 13 : 1202–1213. doi: 10.1038/ncb2331 21909098
8. Hogan BM, Herpers R, Witte M, Helotera H, Alitalo K, et al. (2009) Vegfc/Flt4 signalling is suppressed by Dll4 in developing zebrafish intersegmental arteries. Development 136 : 4001–4009. doi: 10.1242/dev.039990 19906867
9. Galvagni F, Pennacchini S, Salameh A, Rocchigiani M, Neri F, et al. (2010) Endothelial cell adhesion to the extracellular matrix induces c-Src-dependent VEGFR-3 phosphorylation without the activation of the receptor intrinsic kinase activity. Circ Res 106 : 1839–1848. doi: 10.1161/CIRCRESAHA.109.206326 20431062
10. Nieto MA (2002) The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3 : 155–166. 11994736
11. Cano A, Perez-Moreno MA, Rodrigo I, Locascio A, Blanco MJ, et al. (2000) The transcription factor snail controls epithelial-mesenchymal transitions by repressing E-cadherin expression. Nat Cell Biol 2 : 76–83. 10655586
12. Thiery JP, Acloque H, Huang RY, Nieto MA (2009) Epithelial-mesenchymal transitions in development and disease. Cell 139 : 871–890. doi: 10.1016/j.cell.2009.11.007 19945376
13. Lee K, Gjorevski N, Boghaert E, Radisky DC, Nelson CM (2011) Snail1, Snail2, and E47 promote mammary epithelial branching morphogenesis. EMBO J 30 : 2662–2674. doi: 10.1038/emboj.2011.159 21610693
14. Affolter M, Zeller R, Caussinus E (2009) Tissue remodelling through branching morphogenesis. Nat Rev Mol Cell Biol 10 : 831–842. doi: 10.1038/nrm2797 19888266
15. Lomeli H, Starling C, Gridley T (2009) Epiblast-specific Snai1 deletion results in embryonic lethality due to multiple vascular defects. BMC Res Notes 2 : 22. doi: 10.1186/1756-0500-2-22 19284699
16. Rodrigues CO, Nerlick ST, White EL, Cleveland JL, King ML (2008) A Myc-Slug (Snail2)/Twist regulatory circuit directs vascular development. Development 135 : 1903–1911. doi: 10.1242/dev.011296 18469221
17. del Toro R, Prahst C, Mathivet T, Siegfried G, Kaminker JS, et al. (2010) Identification and functional analysis of endothelial tip cell-enriched genes. Blood 116 : 4025–4033. doi: 10.1182/blood-2010-02-270819 20705756
18. Welch-Reardon KM, Ehsan SM, Wang K, Wu N, Newman AC, et al. (2014) Angiogenic sprouting is regulated by endothelial cell expression of Slug. J Cell Sci 127 : 2017–2028. doi: 10.1242/jcs.143420 24554431
19. Parker BS, Argani P, Cook BP, Liangfeng H, Chartrand SD, et al. (2004) Alterations in vascular gene expression in invasive breast carcinoma. Cancer Res 64 : 7857–7866. 15520192
20. Stahl A, Connor KM, Sapieha P, Chen J, Dennison RJ, et al. (2010) The mouse retina as an angiogenesis model. Invest Ophthalmol Vis Sci 51 : 2813–2826. doi: 10.1167/iovs.10-5176 20484600
21. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, et al. (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15 : 4738–4747. 7623107
22. Daley WP, Yamada KM (2013) ECM-modulated cellular dynamics as a driving force for tissue morphogenesis. Curr Opin Genet Dev 23 : 408–414. doi: 10.1016/j.gde.2013.05.005 23849799
23. Zhou BP, Deng J, Xia W, Xu J, Li YM, et al. (2004) Dual regulation of Snail by GSK-3beta-mediated phosphorylation in control of epithelial-mesenchymal transition. Nat Cell Biol 6 : 931–940. 15448698
24. Zhang X, Groopman JE, Wang JF (2005) Extracellular matrix regulates endothelial functions through interaction of VEGFR-3 and integrin alpha5beta1. J Cell Physiol 202 : 205–214. 15389531
25. Flister MJ, Wilber A, Hall KL, Iwata C, Miyazono K, et al. (2010) Inflammation induces lymphangiogenesis through up-regulation of VEGFR-3 mediated by NF-kappaB and Prox1. Blood 115 : 418–429. doi: 10.1182/blood-2008-12-196840 19901262
26. Yoshimatsu Y, Yamazaki T, Mihira H, Itoh T, Suehiro J, et al. (2011) Ets family members induce lymphangiogenesis through physical and functional interaction with Prox1. J Cell Sci 124 : 2753–2762. doi: 10.1242/jcs.083998 21807940
27. Shawber CJ, Funahashi Y, Francisco E, Vorontchikhina M, Kitamura Y, et al. (2007) Notch alters VEGF responsiveness in human and murine endothelial cells by direct regulation of VEGFR-3 expression. J Clin Invest 117 : 3369–3382. 17948123
28. Yan SF, Fujita T, Lu J, Okada K, Shan Zou Y, et al. (2000) Egr-1, a master switch coordinating upregulation of divergent gene families underlying ischemic stress. Nat Med 6 : 1355–1361. 11100120
29. Fahmy RG, Dass CR, Sun LQ, Chesterman CN, Khachigian LM (2003) Transcription factor Egr-1 supports FGF-dependent angiogenesis during neovascularization and tumor growth. Nat Med 9 : 1026–1032. 12872165
30. Hu CT, Chang TY, Cheng CC, Liu CS, Wu JR, et al. (2010) Snail associates with EGR-1 and SP-1 to upregulate transcriptional activation of p15INK4b. FEBS J 277 : 1202–1218. doi: 10.1111/j.1742-4658.2009.07553.x 20121949
31. Benedito R, Rocha SF, Woeste M, Zamykal M, Radtke F, et al. (2012) Notch-dependent VEGFR3 upregulation allows angiogenesis without VEGF-VEGFR2 signalling. Nature 484 : 110–114. doi: 10.1038/nature10908 22426001
32. Beets K, Huylebroeck D, Moya IM, Umans L, Zwijsen A (2013) Robustness in angiogenesis: notch and BMP shaping waves. Trends Genet 29 : 140–149. doi: 10.1016/j.tig.2012.11.008 23279848
33. Carmeliet P, De Smet F, Loges S, Mazzone M (2009) Branching morphogenesis and antiangiogenesis candidates: tip cells lead the way. Nat Rev Clin Oncol 6 : 315–326. doi: 10.1038/nrclinonc.2009.64 19483738
34. Valtola R, Salven P, Heikkila P, Taipale J, Joensuu H, et al. (1999) VEGFR-3 and its ligand VEGF-C are associated with angiogenesis in breast cancer. Am J Pathol 154 : 1381–1390. 10329591
35. Okada K, Kobayashi S, Yamada T, Kurihara T, Tai-Nagara I, et al. (2014) Neurons limit angiogenesis by titrating VEGF in retina. Cell 159 : 584–596. doi: 10.1016/j.cell.2014.09.025 25417109
36. Stefater JA 3rd, Lewkowich I, Rao S, Mariggi G, Carpenter AC, et al. (2011) Regulation of angiogenesis by a non-canonical Wnt-Flt1 pathway in myeloid cells. Nature 474 : 511–515. doi: 10.1038/nature10085 21623369
37. Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, et al. (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood 116 : 829–840. doi: 10.1182/blood-2009-12-257832 20404134
38. Lobov IB, Rao S, Carroll TJ, Vallance JE, Ito M, et al. (2005) WNT7b mediates macrophage-induced programmed cell death in patterning of the vasculature. Nature 437 : 417–421. 16163358
39. Napp LC, Augustynik M, Paesler F, Krishnasamy K, Woiterski J, et al. (2012) Extrinsic Notch ligand Delta-like 1 regulates tip cell selection and vascular branching morphogenesis. Circ Res 110 : 530–535. doi: 10.1161/CIRCRESAHA.111.263319 22282195
40. Dorrell MI, Aguilar E, Friedlander M (2002) Retinal vascular development is mediated by endothelial filopodia, a preexisting astrocytic template and specific R-cadherin adhesion. Invest Ophthalmol Vis Sci 43 : 3500–3510. 12407162
41. Luhmann UF, Lin J, Acar N, Lammel S, Feil S, et al. (2005) Role of the Norrie disease pseudoglioma gene in sprouting angiogenesis during development of the retinal vasculature. Invest Ophthalmol Vis Sci 46 : 3372–3382. 16123442
42. Liu Y, Senger DR (2004) Matrix-specific activation of Src and Rho initiates capillary morphogenesis of endothelial cells. FASEB J 18 : 457–468. 15003991
43. Zhou Y, Zhang Y, Gao F, Guo F, Wang J, et al. (2010) N-n-butyl haloperidol iodide protects cardiac microvascular endothelial cells from hypoxia/reoxygenation injury by down-regulating Egr-1 expression. Cell Physiol Biochem 26 : 839–848. doi: 10.1159/000323993 21220915
44. Zhang K, Corsa CA, Ponik SM, Prior JL, Piwnica-Worms D, et al. (2013) The collagen receptor discoidin domain receptor 2 stabilizes SNAIL1 to facilitate breast cancer metastasis. Nat Cell Biol 15 : 677–687. doi: 10.1038/ncb2743 23644467
45. Potenta S, Zeisberg E, Kalluri R (2008) The role of endothelial-to-mesenchymal transition in cancer progression. Br J Cancer 99 : 1375–1379. doi: 10.1038/sj.bjc.6604662 18797460
46. Maddaluno L, Rudini N, Cuttano R, Bravi L, Giampietro C, et al. (2013) EndMT contributes to the onset and progression of cerebral cavernous malformations. Nature 498 : 492–496. doi: 10.1038/nature12207 23748444
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