Cooperative signaling between Slit2 and ephrin-A1 regulates a balance between angiogenesis and angiostasis

Molecular and Cellular Biology

Volumn 31, Issue 3, 2011, Pages 404-416

  Dunaway, Charlene M ^b   Hwang, Yoonha ^b   Lindsley, Craig W ^b   Cook, Rebecca S ^b,c   Wu, Jane Y ^d   Boothby, Mark ^b   Chen, Jin ^a,b,c   Brantley Sieders, Dana M ^b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c VANDERBILT INGRAM CANCER CENTER   (United States)

^d NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EPHRIN A1; SLIT2 PROTEIN;

ANGIOGENESIS; ANIMAL CELL; ARTICLE; CELL CULTURE; CELL MIGRATION; CELL MOTILITY; CELL STIMULATION; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE OVEREXPRESSION; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; SIGNAL TRANSDUCTION;

ANIMALS; CARRIER PROTEINS; CATTLE; CELL MOVEMENT; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EPHRIN-A1; GENES, DOMINANT; HEK293 CELLS; HUMANS; INTERCELLULAR SIGNALING PEPTIDES AND PROTEINS; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; NERVE TISSUE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; RAC GTP-BINDING PROTEINS; SIGNAL TRANSDUCTION; SUBCUTANEOUS TISSUE; TRANS-ACTIVATORS;

EID: 78751487441     PISSN: 02707306     EISSN: 10985549     Source Type: Journal    
DOI: 10.1128/MCB.00667-10     Document Type: Article

References (77)

1. Ahmed, Z., and R. Bicknell. 2009. Angiogenic signalling pathways. Methods Mol. Biol. 467:3-24.
2. Arvanitis, D., and A. Davy. 2008. Eph/ephrin signaling: networks. Genes Dev. 22:416-429.
3. Bartley, T. D., et al. 1994. B61 is a ligand for the ECK receptor proteintyrosine kinase. Nature 368:558-560.
4. Brantley, D. M., et al. 2002. Soluble EphA receptors inhibit tumor angiogenesis and progression in vivo. Oncogene 21:7011-7026.
5. 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.
6. 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.
7. Brantley-Sieders, D. M., and J. Chen. 2004. Eph receptor tyrosine kinases in angiogenesis: from development to disease. Angiogenesis 7:17-28. (Pubitemid 39127767)
8. 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.
9. 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.
10. 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.
11. 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.
12. Brose, K., et al. 1999. Slit proteins bind Robo receptors and have an evolutionarily conserved role in repulsive axon guidance. Cell 96:795-806. (Pubitemid 29165083)
13. Cao, Y. 2009. Tumor angiogenesis and molecular targets for therapy. Front. Biosci. 14:3962-3973.
14. Carmeliet, P., and R. K. Jain. 2000. Angiogenesis in cancer and other diseases. Nature 407:249-257.
15. Chen, J., et al. 2006. Inhibition of retinal neovascularization by soluble EphA2 receptor. Exp. Eye Res. 82:664-673.
16. Chen, J., et al. 2005. Akt1 regulates pathological angiogenesis, vascular maturation and permeability in vivo. Nat. Med. 11:1188-1196.
17. Cheng, N., et al. 2003. Inhibition of VEGF-dependent multistage carcinogenesis by soluble EphA receptors. Neoplasia 5:445-456.
18. 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.
19. Dada, S., N. Demartines, and O. Dormond. 2008. mTORC2 regulates PGE2-mediated endothelial cell survival and migration. Biochem. Biophys. Res. Commun. 372:875-879.
20. 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.
21. Dobrzanski, P., et al. 2004. Antiangiogenic and antitumor efficacy of EphA2 receptor antagonist. Cancer Res. 64:910-919.
22. 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.
23. 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.
24. 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.
25. 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.
26. Han, X., and M. C. Zhang. 2010. Potential anti-angiogenic role of Slit2 in corneal neovascularization. Exp. Eye Res. 90:742-749.
27. 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.
28. Hohenester, E. 2008. Structural insight into Slit-Robo signalling. Biochem. Soc. Trans. 36:251-256.
29. Holzman, L. B., R. M. Marks, and V. M. Dixit. 1990. A novel immediateearly response gene of endothelium is induced by cytokines and encodes a secreted protein. Mol. Cell. Biol. 10:5830-5838.
30. 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.
31. 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.
32. Jacinto, E., et al. 2006. SIN1/MIP1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127:125-137. (Pubitemid 44466632)
33. 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.
34. Jones, C. A., et al. 2008. Robo4 stabilizes the vascular network by inhibiting pathologic angiogenesis and endothelial hyperpermeability. Nat. Med. 14: 448-453.
35. Jones, C. A., et al. 2009. Slit2-Robo4 signalling promotes vascular stability by blocking Arf6 activity. Nat. Cell Biol. 11:1325-1331.
36. Jorgensen, C., et al. 2009. Cell-specific information processing in segregating populations of Eph receptor ephrin-expressing cells. Science 326:1502-1509.
37. Kaur, S., et al. 2006. Robo4 signaling in endothelial cells implies attraction guidance mechanisms. J. Biol. Chem. 281:11347-11356.
38. Kaur, S., et al. 2008. Silencing of directional migration in roundabout4 knockdown endothelial cells. BMC Cell Biol. 9:61.
39. 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.
40. Kuijper, S., C. J. Turner, and R. H. Adams. 2007. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc. Med. 17:145-151.
41. 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.
42. Laplante, M., and D. M. Sabatini. 2009. mTOR signaling at a glance. J. Cell Sci. 122:3589-3594.
43. 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.
44. 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.
45. Lindsley, C. W., et al. 2005. Allosteric Akt (PKB) inhibitors: discovery and SAR of isozyme selective inhibitors. Bioorg. Med. Chem. Lett. 15:761-764.
46. 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.
47. Long, H., et al. 2004. Conserved roles for Slit and Robo proteins in midline commissural axon guidance. Neuron 42:213-223.
48. Lundstrom, A., et al. 2004. Vilse, a conserved Rac/Cdc42 GAP mediating Robo repulsion in tracheal cells and axons. Genes Dev. 18:2161-2171.
49. 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.
50. 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.
51. 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.
52. Nie, D., et al. 2010. Tsc2-Rheb signaling regulates EphA-mediated axon guidance. Nat. Neurosci. 13:163-172.
53. Ogawa, K., et al. 2000. The ephrin-A1 ligand and its receptor, EphA2, are expressed during tumor neovascularization. Oncogene 19:6043-6052. (Pubitemid 32039378)
54. 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-alphainduced angiogenesis. Science 268:567-569.
55. Park, K. W., et al. 2003. Robo4 is a vascular-specific receptor that inhibits endothelial migration. Dev. Biol. 261:251-267.
56. Pasquale, E. B. 2008. Eph-ephrin bidirectional signaling in physiology and disease. Cell 133:38-52.
57. Phung, T. L., et al. 2006. Pathological angiogenesis is induced by sustained Akt signaling and inhibited by rapamycin. Cancer Cell 10:159-170.
58. Ribatti, D., B. Nico, and E. Crivellato. 2009. Morphological and molecular aspects of physiological vascular morphogenesis. Angiogenesis 12:101-111.
59. 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.
60. Sarbassov, D. D., et al. 2006. Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol. Cell 22:159-168.
61. 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.
62. 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.
63. 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.
64. Shiojima, I., and K. Walsh. 2006. Regulation of cardiac growth and coronary angiogenesis by the Akt/PKB signaling pathway. Genes Dev. 20:3347-3365.
65. Shiojima, I., and K. Walsh. 2002. Role of Akt signaling in vascular homeostasis and angiogenesis. Circ. Res. 90:1243-1250.
66. 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.
67. 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.
68. 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.
69. 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.
70. 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. (Pubitemid 32401523)
71. Wu, J. Y., et al. 2001. The neuronal repellent Slit inhibits leukocyte chemotaxis induced by chemotactic factors. Nature 410:948-952.
72. 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.
73. 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.
74. 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.
75. Yang, X. M., et al. 2010. Slit-Robo signaling mediates lymphangiogenesis and promotes tumor lymphatic metastasis. Biochem. Biophys. Res. Commun. 396:571-577.
76. Zhang, B., et al. 2009. Repulsive axon guidance molecule Slit3 is a novel angiogenic factor. Blood 114:4300-4309.
77. 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.