Inhibitory Effect of Slit2-N on VEGF165-induced proliferation of vascular endothelia via Slit2-N-Robo4-Akt pathway in choroidal neovascularization

References

• Witmer AN, Vrensen GF, Van Noorden CJ, et al. Vascular endothelial growth factors and angiogenesis in eye disease. Prog Retin Eye Res. 2003;22(1):1–29.
   PubMed Web of Science ®Google Scholar
• Penn JS, Madan A, Caldwell RB, et al. Vascular endothelial growth factor in eye disease. Prog Retin Eye Res. 2008;27(4):331–371.
   PubMed Web of Science ®Google Scholar
• Chen CY, Tsai CH, Chen CY, et al. Human placental multipotent mesenchymal stromal cells modulate placenta angiogenesis through Slit2-Robo signaling. Cell Adh Migr. 2016;10(1–2):66–76.
   PubMed Web of Science ®Google Scholar
• Liu D, Hou J, Hu X, et al. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ Res. 2006;98(4):480–489.
   PubMed Web of Science ®Google Scholar
• Guijarro-Muñoz I, Cuesta AM, Alvarez-Cienfuegos A, et al. The axonal repellent Slit2 inhibits pericyte migration: potential implications in angiogenesis. Exp Cell Res. 2012;318(4):371–378.
   PubMed Web of Science ®Google Scholar
• Ho TH, Serie DJ, Parasramka M, et al. Differential gene expression profiling of matched primary renal cell carcinoma and metastases reveals upregulation of extracellular matrix genes. Ann Oncol. 2017;28(3):604–610.
   PubMed Web of Science ®Google Scholar
• Le LT, Cazares O, Mouw JK, et al. Loss of miR-203 regulates cell shape and matrix adhesion through ROBO1/Rac/FAK in response to stiffness. J Cell Biol. 2016;212(6):707–719.
   PubMed Web of Science ®Google Scholar
• Yang YC, Chen PN, Wang SY, et al. The differential roles of Slit2-exon 15 splicing variants in angiogenesis and HUVEC permeability. Angiogenesis. 2015;18(3):301–312.
   PubMed Web of Science ®Google Scholar
• Sherchan P, Huang L, Akyol O, et al. Recombinant Slit2 reduces surgical brain injury induced blood brain barrier disruption via Robo4 dependent Rac1 activation in a rodent model. Sci Rep. 2017;7(1):746.
   PubMed Web of Science ®Google Scholar
• Li S, Huang L, Sun Y, et al. Slit2 promotes angiogenesis activity via the robo1-VEGFR2-ERK1/2 pathway in both in vivo and in vitro studies. Invest Ophthalmol Vis Sci. 2015;56(9):5210–5217.
   PubMed Web of Science ®Google Scholar
• Rama N, Dubrac A, Mathivet T, et al. Slit2 signaling through Robo1 and Robo2 is required for retinal neovascularization. Nat Med. 2015;21(5):483–491.
   PubMed Web of Science ®Google Scholar
• Jones CA, London NR, Chen H, et al. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat Med. 2008;14(4):448–453.
   PubMed Web of Science ®Google Scholar
• Browning AC, Halligan EP, Stewart EA, et al. Comparative gene expression profiling of human umbilical vein endothelial cells and ocular vascular endothelial cells. Br J Ophthalmol. 2012;96(1):128–132.
   PubMed Web of Science ®Google Scholar
• Jones CA, Nishiya N, London NR, et al. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat Cell Biol. 2009;11(11):1325–1331.
   PubMed Web of Science ®Google Scholar
• Nieminen T, Toivanen PI, Laakkonen JP, et al. Slit2 modifies VEGF-induced angiogenic responses in rabbit skeletal muscle via reduced eNOS activity. Cardiovasc Res. 2015;107(2):267–276.
   PubMed Web of Science ®Google Scholar
• Youngblood V, Wang S, Song W, et al. Elevated Slit2 activity impairs VEGF-induced angiogenesis and tumor neovascularization in EphA2-deficient endothelium. Mol Cancer Res. 2015;13(3):524–537.
   PubMed Web of Science ®Google Scholar
• Yu J, Zhang X, Kuzontkoski PM, et al. Slit2N and Robo4 regulate lymphangiogenesis through the VEGF-C/VEGFR-3 pathway. Cell Commun Signal. 2014;12:25.
   PubMed Web of Science ®Google Scholar
• Fritz RD, Menshykau D, Martin K, et al. SrGAP2-dependent integration of membrane geometry and slit-robo-repulsive cues regulates fibroblast contact inhibition of locomotion. Dev Cell. 2015;35(1):78–92.
   PubMed Web of Science ®Google Scholar
• Anand AR, Zhao H, Nagaraja T, et al. N-terminal Slit2 inhibits HIV-1 replication by regulating the actin cytoskeleton. Retrovirology. 2013;10:2.
   PubMed Web of Science ®Google Scholar
• Sheldon H, Andre M, Legg JA, et al. Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors. Faseb J. 2009;23(2):513–522.
   PubMed Web of Science ®Google Scholar
• Ning Y, Sun Q, Dong Y, et al. Slit2-N inhibits PDGF-induced migration in rat airway smooth muscle cells: WASP and Arp2/3 involved. Toxicology. 2011;283(1):32–40.
   PubMed Web of Science ®Google Scholar
• Cai H, Xue Y, Li Z, et al. Roundabout4 suppresses glioma-induced endothelial cell proliferation, migration and tube formation in vitro by inhibiting VEGR2-mediated PI3K/AKT and FAK signaling pathways. Cell Physiol Biochem. 2015;35(5):1689–1705.
   PubMedGoogle Scholar
• Enomoto S, Mitsui K, Kawamura T, et al. Suppression of Slit2/Robo1 mediated HUVEC migration by Robo4. Biochem Biophys Res Commun. 2016;469(4):797–802.
   PubMed Web of Science ®Google Scholar
• Han HX, Geng JG. Over-expression of Slit2 induces vessel formation and changes blood vessel permeability in mouse brain. Acta Pharmacol Sin. 2011;32(11):1327–1336.
   PubMed Web of Science ®Google Scholar
• Gorbunova EE, Gavrilovskaya IN, Mackow ER. Slit2-Robo4 receptor responses inhibit ANDV directed permeability of human lung microvascular endothelial cells. Antiviral Res. 2013;99(2):108–112.
   PubMed Web of Science ®Google Scholar
• Myers JP, Robles E, Ducharme-Smith A, et al. Focal adhesion kinase modulates Cdc42 activity downstream of positive and negative axon guidance cues. J Cell Sci. 2012;125(Pt 12):2918–2929.
   PubMed Web of Science ®Google Scholar
• Tseng RC, Chang JM, Chen JH, et al. Deregulation of SLIT2-mediated Cdc42 activity is associated with esophageal cancer metastasis and poor prognosis. J Thorac Oncol. 2015;10(1):189–198.
   PubMed Web of Science ®Google Scholar
• Dubrac A, Genet G, Ola R, et al. Targeting NCK-mediated endothelial cell front-rear polarity inhibits neovascularization. Circulation. 2016;133(4):409–421.
   PubMed Web of Science ®Google Scholar
• Zhao H, Ahirwar DK, Oghumu S, et al. Endothelial Robo4 suppresses breast cancer growth and metastasis through regulation of tumor angiogenesis. Mol Oncol. 2016;10(2):272–281.
   PubMed Web of Science ®Google Scholar
• D’Souza-Schorey C, Chavrier P. ARF proteins: roles in membrane traffic and beyond. Nat Rev Mol Cell Biol. 2006;7(5):347–358.
   PubMed Web of Science ®Google Scholar
• Koch AW, Mathivet T, Larrivée B, et al. Robo4 maintains vessel integrity and inhibits angiogenesis by interacting with UNC5B. Dev Cell. 2011;20(1):33–46.
   PubMed Web of Science ®Google Scholar
• Huminiecki L, Gorn M, Suchting S, et al. Magic roundabout is a new member of the roundabout receptor family that is endothelial specific and expressed at sites of active angiogenesis. Genomics. 2002;79(4):547–552.
   PubMed Web of Science ®Google Scholar
• Zhang F, Prahst C, Mathivet T, et al. The Robo4 cytoplasmic domain is dispensable for vascular permeability and neovascularization. Nat Commun. 2016;7:13517.
   PubMed Web of Science ®Google Scholar