34
Views
29
CrossRef citations to date
0
Altmetric
Article

Cooperative Signaling between Slit2 and Ephrin-A1 Regulates a Balance between Angiogenesis and Angiostasis

, , , , , , & show all
Pages 404-416 | Received 09 Jun 2010, Accepted 20 Nov 2010, Published online: 21 Mar 2023

REFERENCES

  • Ahmed, Z., and R. Bicknell. 2009. Angiogenic signalling pathways. Methods Mol. Biol. 467:3–24.
  • Arvanitis, D., and A. Davy. 2008. Eph/ephrin signaling: networks. Genes Dev. 22:416–429.
  • Bartley, T. D., et al. 1994. B61 is a ligand for the ECK receptor protein-tyrosine kinase. Nature 368:558–560.
  • Brantley, D. M., et al. 2002. Soluble EphA receptors inhibit tumor angiogenesis and progression in vivo. Oncogene 21:7011–7026.
  • Brantley-Sieders, D., S. Schmidt, M. Parker, and J. Chen. 2004. Eph receptor tyrosine kinases in tumor and tumor microenvironment. Curr. Pharm. Des. 10:3431–3442.
  • Brantley-Sieders, D. M., et al. 2004. EphA2 receptor tyrosine kinase regulates endothelial cell migration and vascular assembly through phosphoinositide 3-kinase-mediated Rac1 GTPase activation. J. Cell Sci. 117:2037–2049.
  • Brantley-Sieders, D. M., and J. Chen. 2004. Eph receptor tyrosine kinases in angiogenesis: from development to disease. Angiogenesis 7:17–28.
  • Brantley-Sieders, D. M., et al. 2005. Impaired tumor microenvironment in EphA2-deficient mice inhibits tumor angiogenesis and metastatic progression. FASEB J. 19:1884–1886.
  • Brantley-Sieders, D. M., W. B. Fang, Y. Hwang, D. Hicks, and J. Chen. 2006. Ephrin-A1 facilitates mammary tumor metastasis through an angiogenesis-dependent mechanism mediated by EphA receptor and vascular endothelial growth factor in mice. Cancer Res. 66:10315–10324.
  • Brantley-Sieders, D. M., et al. 2008. The receptor tyrosine kinase EphA2 promotes mammary adenocarcinoma tumorigenesis and metastatic progression in mice by amplifying ErbB2 signaling. J. Clin. Invest. 118:64–78.
  • Brantley-Sieders, D. M., et al. 2009. Host deficiency in Vav2/3 guanine nucleotide exchange factors impairs tumor growth, survival, and angiogenesis in vivo. Mol. Cancer Res. 7:615–623.
  • Brose, K., et al. 1999. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795–806.
  • Cao, Y. 2009. Tumor angiogenesis and molecular targets for therapy. Front. Biosci. 14:3962–3973.
  • Carmeliet, P., and R. K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature 407:249–257.
  • Chen, J., et al. 2006. Inhibition of retinal neovascularization by soluble EphA2 receptor. Exp. Eye Res. 82:664–673.
  • Chen, J., et al. 2005. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat. Med. 11:1188–1196.
  • Cheng, N., et al. 2003. Inhibition of VEGF-dependent multistage carcinogenesis by soluble EphA receptors. Neoplasia 5:445–456.
  • Cheng, N., et al. 2002. Blockade of EphA receptor tyrosine kinase activation inhibits vascular endothelial cell growth factor-induced angiogenesis. Mol. Cancer Res. 1:2–11.
  • Dada, S., N. Demartines, and O. Dormond. 2008. mTORC2 regulates PGE2-mediated endothelial cell survival and migration. Biochem. Biophys. Res. Commun. 372:875–879.
  • Dickson, B. J., and G. F. Gilestro. 2006. Regulation of commissural axon pathfinding by slit and its Robo receptors. Annu. Rev. Cell Dev. Biol. 22:651–675.
  • Dobrzanski, P., et al. 2004. Antiangiogenic and antitumor efficacy of EphA2 receptor antagonist. Cancer Res. 64:910–919.
  • Endris, V., et al. 2002. The novel Rho-GTPase activating gene MEGAP/srGAP3 has a putative role in severe mental retardation. Proc. Natl. Acad. Sci. U. S. A. 99:11754–11759.
  • Fang, W. B., D. M. Brantley-Sieders, Y. Hwang, A. J. Ham, and J. Chen. 2008. Identification and functional analysis of phosphorylated tyrosine residues within EphA2 receptor tyrosine kinase. J. Biol. Chem. 283:16017–16026.
  • Griffioen, A. W., and G. Molema. 2000. Angiogenesis: potentials for pharmacologic intervention in the treatment of cancer, cardiovascular diseases, and chronic inflammation. Pharmacol. Rev. 52:237–268.
  • Guertin, D. A., et al. 2006. Ablation in mice of the mTORC components raptor, rictor, or mLST8 reveals that mTORC2 is required for signaling to Akt-FOXO and PKCalpha, but not S6K1. Dev. Cell 11:859–871.
  • Han, X., and M. C. Zhang. 2010. Potential anti-angiogenic role of Slit2 in corneal neovascularization. Exp. Eye Res. 90:742–749.
  • Hernandez-Negrete, I., et al. 2007. P-Rex1 links mammalian target of rapamycin signaling to Rac activation and cell migration. J. Biol. Chem. 282:23708–23715.
  • Hohenester, E. 2008. Structural insight into Slit-Robo signalling. Biochem. Soc. Trans. 36:251–256.
  • Holzman, L. B., R. M. Marks, and V. M. Dixit. 1990. A novel immediate-early response gene of endothelium is induced by cytokines and encodes a secreted protein. Mol. Cell. Biol. 10:5830–5838.
  • Hu, H., et al. 2005. Cross GTPase-activating protein (CrossGAP)/Vilse links the Roundabout receptor to Rac to regulate midline repulsion. Proc. Natl. Acad. Sci. U. S. A. 102:4613–4618.
  • Hunter, S. G., et al. 2006. Essential role of Vav family guanine nucleotide exchange factors in EphA receptor-mediated angiogenesis. Mol. Cell. Biol. 26:4830–4842.
  • Jacinto, E., et al. 2006. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127:125–137.
  • Jat, P. S., et al. 1991. Direct derivation of conditionally immortal cell lines from an H-2Kb-tsA58 transgenic mouse. Proc. Natl. Acad. Sci. U. S. A. 88:5096–5100.
  • Jones, C. A., et al. 2008. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 14:448–453.
  • Jones, C. A., et al. 2009. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 11:1325–1331.
  • Jorgensen, C., et al. 2009. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 326:1502–1509.
  • Kaur, S., et al. 2006. Robo4 signaling in endothelial cells implies attraction guidance mechanisms. J. Biol. Chem. 281:11347–11356.
  • Kaur, S., et al. 2008. Silencing of directional migration in roundabout4 knockdown endothelial cells. BMC Cell Biol. 9:61.
  • Kohn, A. D., F. Takeuchi, and R. A. Roth. 1996. Akt, a pleckstrin homology domain containing kinase, is activated primarily by phosphorylation. J. Biol. Chem. 271:21920–21926.
  • Kuijper, S., C. J. Turner, and R. H. Adams. 2007. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc. Med. 17:145–151.
  • Langley, R. R., et al. 2003. Tissue-specific microvascular endothelial cell lines from H-2K(b)-tsA58 mice for studies of angiogenesis and metastasis. Cancer Res. 63:2971–2976.
  • Laplante, M., and D. M. Sabatini. 2009. mTOR signaling at a glance. J. Cell Sci. 122:3589–3594.
  • Legg, J. A., J. M. Herbert, P. Clissold, and R. Bicknell. 2008. Slits and Roundabouts in cancer, tumour angiogenesis and endothelial cell migration. Angiogenesis 11:13–21.
  • Li, H. S., et al. 1999. Vertebrate slit, a secreted ligand for the transmembrane protein roundabout, is a repellent for olfactory bulb axons. Cell 96:807–818.
  • Lindsley, C. W., et al. 2005. Allosteric Akt (PKB) inhibitors: discovery and SAR of isozyme selective inhibitors. Bioorg. Med. Chem. Lett. 15:761–764.
  • Liu, D., et al. 2006. Neuronal chemorepellent Slit2 inhibits vascular smooth muscle cell migration by suppressing small GTPase Rac1 activation. Circ. Res. 98:480–489.
  • Long, H., et al. 2004. Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 42:213–223.
  • Lundstrom, A., et al. 2004. Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev. 18:2161–2171.
  • Miao, H., et al. 2009. EphA2 mediates ligand-dependent inhibition and ligand-independent promotion of cell migration and invasion via a reciprocal regulatory loop with Akt. Cancer Cell 16:9–20.
  • Miao, R. Q., et al. 2008. Dominant-negative Hsp90 reduces VEGF-stimulated nitric oxide release and migration in endothelial cells. Arterioscler. Thromb. Vasc. Biol. 28:105–111.
  • Moon, J. J., S. H. Lee, and J. L. West. 2007. Synthetic biomimetic hydrogels incorporated with ephrin-A1 for therapeutic angiogenesis. Biomacromolecules 8:42–49.
  • Nie, D., et al. 2010. Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat. Neurosci. 13:163–172.
  • Ogawa, K., et al. 2000. The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene 19:6043–6052.
  • Pandey, A., H. Shao, R. M. Marks, P. J. Polverini, and V. M. Dixit. 1995. Role of B61, the ligand for the Eck receptor tyrosine kinase, in TNF-alpha-induced angiogenesis. Science 268:567–569.
  • Park, K. W., et al. 2003. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev. Biol. 261:251–267.
  • Pasquale, E. B. 2008. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133:38–52.
  • Phung, T. L., et al. 2006. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10:159–170.
  • Ribatti, D., B. Nico, and E. Crivellato. 2009. Morphological and molecular aspects of physiological vascular morphogenesis. Angiogenesis 12:101–111.
  • Sander, E. E., et al. 1998. Matrix-dependent Tiam1/Rac signaling in epithelial cells promotes either cell-cell adhesion or cell migration and is regulated by phosphatidylinositol 3-kinase. J. Cell Biol. 143:1385–1398.
  • Sarbassov, D. D., et al. 2006. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22:159–168.
  • Sarbassov, D. D., D. A. Guertin, S. M. Ali, and D. M. Sabatini. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098–1101.
  • Shao, H., A. Pandey, K. S. O'Shea, M. Seldin, and V. M. Dixit. 1995. Characterization of B61, the ligand for the Eck receptor protein-tyrosine kinase. J. Biol. Chem. 270:5636–5641.
  • Sheldon, H., et al. 2009. Active involvement of Robo1 and Robo4 in filopodia formation and endothelial cell motility mediated via WASP and other actin nucleation-promoting factors. FASEB J. 23:513–522.
  • Shiojima, I., and K. Walsh. 2006. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev. 20:3347–3365.
  • Shiojima, I., and K. Walsh. 2002. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90:1243–1250.
  • Shiota, C., J. T. Woo, J. Lindner, K. D. Shelton, and M. A. Magnuson. 2006. Multiallelic disruption of the rictor gene in mice reveals that mTOR complex 2 is essential for fetal growth and viability. Dev. Cell 11:583–589.
  • Stein, E., et al. 1998. Eph receptors discriminate specific ligand oligomers to determine alternative signaling complexes, attachment, and assembly responses. Genes Dev. 12:667–678.
  • Sun, J. F., et al. 2005. Microvascular patterning is controlled by fine-tuning the Akt signal. Proc. Natl. Acad. Sci. U. S. A. 102:128–133.
  • Urbich, C., et al. 2009. HDAC5 is a repressor of angiogenesis and determines the angiogenic gene expression pattern of endothelial cells. Blood 113:5669–5679.
  • Vooijs, M., J. Jonkers, and A. Berns. 2001. A highly efficient ligand-regulated Cre recombinase mouse line shows that LoxP recombination is position dependent. EMBO Rep. 2:292–297.
  • Wu, J. Y., et al. 2001. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 410:948–952.
  • Wykosky, J., et al. 2008. Soluble monomeric EphrinA1 is released from tumor cells and is a functional ligand for the EphA2 receptor. Oncogene 27:7260–7273.
  • Yakes, F. M., et al. 2002. Herceptin-induced inhibition of phosphatidylinositol-3 kinase and Akt is required for antibody-mediated effects on p27, cyclin D1, and antitumor action. Cancer Res. 62:4132–4141.
  • Yang, N. Y., et al. 2010. Crosstalk of the EphA2 receptor with a serine/threonine phosphatase suppresses the Akt-mTORC1 pathway in cancer cells. Cell. Signal. 23:201–212.
  • Yang, X. M., et al. 2010. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Biochem. Biophys. Res. Commun. 396:571–577.
  • Zhang, B., et al. 2009. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood 114:4300–4309.
  • Zhou, B. P., et al. 2000. HER-2/neu blocks tumor necrosis factor-induced apoptosis via the Akt/NF-kappaB pathway. J. Biol. Chem. 275:8027–8031.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.