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BioMed Research International
Volume 2015, Article ID 314178, 9 pages
http://dx.doi.org/10.1155/2015/314178
Review Article

Actin-Tethered Junctional Complexes in Angiogenesis and Lymphangiogenesis in Association with Vascular Endothelial Growth Factor

Division of Molecular Medical Biochemistry, Department of Biochemistry and Molecular Biology, Shiga University of Medical Science, Seta Tsukinowa-cho, Shiga, Otsu 520-2192, Japan

Received 11 September 2014; Revised 23 October 2014; Accepted 31 October 2014

Academic Editor: Qiang Zhao

Copyright © 2015 Dimitar P. Zankov and Hisakazu Ogita. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. W. C. Aird, “Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms,” Circulation Research, vol. 100, no. 2, pp. 158–173, 2007. View at Publisher · View at Google Scholar · View at Scopus
  2. K. L. Marcelo, L. C. Goldie, and K. K. Hirschi, “Regulation of endothelial cell differentiation and specification,” Circulation Research, vol. 112, no. 9, pp. 1272–1287, 2013. View at Publisher · View at Google Scholar · View at Scopus
  3. L. Coultas, K. Chawengsaksophak, and J. Rossant, “Endothelial cells and VEGF in vascular development,” Nature, vol. 438, no. 7070, pp. 937–945, 2005. View at Publisher · View at Google Scholar · View at Scopus
  4. A. S. Chung and N. Ferrara, “Developmental and pathological angiogenesis,” Annual Review of Cell and Developmental Biology, vol. 27, pp. 563–584, 2011. View at Publisher · View at Google Scholar · View at Scopus
  5. T. Tammela and K. Alitalo, “Lymphangiogenesis: molecular mechanisms and future promise,” Cell, vol. 140, no. 4, pp. 460–476, 2010. View at Publisher · View at Google Scholar · View at Scopus
  6. S. Schulte-Merker, A. Sabine, and T. V. Petrova, “Lymphatic vascular morphogenesis in development, physiology, and disease,” The Journal of Cell Biology, vol. 193, no. 4, pp. 607–618, 2011. View at Publisher · View at Google Scholar · View at Scopus
  7. E. Dejana, “Endothelial cell-cell junctions: happy together,” Nature Reviews Molecular Cell Biology, vol. 5, no. 4, pp. 261–270, 2004. View at Publisher · View at Google Scholar · View at Scopus
  8. C. Rüegg and A. Mariotti, “Vascular integrins: pleiotropic adhesion and signaling molecules in vascular homeostasis and angiogenesis,” Cellular and Molecular Life Sciences, vol. 60, no. 6, pp. 1135–1157, 2003. View at Google Scholar · View at Scopus
  9. G. H. Mahabeleshwar, W. Feng, K. Reddy, E. F. Plow, and T. V. Byzova, “Mechanisms of integrin-vascular endothelial growth factor receptor cross-activation in angiogenesis,” Circulation Research, vol. 101, no. 6, pp. 570–580, 2007. View at Publisher · View at Google Scholar · View at Scopus
  10. A. Cattelino, S. Liebner, R. Gallini et al., “The conditional inactivation of the β-catenin gene in endothelial cells causes a defective vascular pattern and increased vascular fragility,” The Journal of Cell Biology, vol. 162, no. 6, pp. 1111–1122, 2003. View at Publisher · View at Google Scholar · View at Scopus
  11. R. G. Oas, K. Xiao, S. Summers et al., “P120-catenin is required for mouse vascular development,” Circulation Research, vol. 106, no. 5, pp. 941–951, 2010. View at Publisher · View at Google Scholar · View at Scopus
  12. Y. Luo and G. L. Radice, “N-cadherin acts upstream of VE-cadherin in controlling vascular morphogenesis,” The Journal of Cell Biology, vol. 169, no. 1, pp. 29–34, 2005. View at Publisher · View at Google Scholar · View at Scopus
  13. K. J. Bayless and G. A. Johnson, “Role of the cytoskeleton in formation and maintenance of angiogenic sprouts,” Journal of Vascular Research, vol. 48, no. 5, pp. 369–385, 2011. View at Publisher · View at Google Scholar · View at Scopus
  14. H. Schnittler, M. Taha, M. O. Schnittler, A. A. Taha, N. Lindemann, and J. Seebach, “Actin filament dynamics and endothelial cell junctions: the Ying and Yang between stabilization and motion,” Cell and Tissue Research, vol. 355, no. 3, pp. 529–543, 2014. View at Publisher · View at Google Scholar · View at Scopus
  15. H. Ogita, Y. Rikitake, J. Miyoshi, and Y. Takai, “Cell adhesion molecules nectins and associating proteins: Implications for physiology and pathology,” Proceedings of the Japan Academy Series B: Physical and Biological Sciences, vol. 86, no. 6, pp. 621–629, 2010. View at Publisher · View at Google Scholar · View at Scopus
  16. C. Kim, H. Yang, Y. Fukushima et al., “Vascular RhoJ is an effective and selective target for tumor angiogenesis and vascular disruption,” Cancer Cell, vol. 25, no. 1, pp. 102–117, 2014. View at Publisher · View at Google Scholar · View at Scopus
  17. D. Gerald, I. Adini, S. Shechter et al., “RhoB controls coordination of adult angiogenesis and lymphangiogenesis following injury by regulating VEZF1-mediated transcription,” Nature Communications, vol. 4, article 2824, 2013. View at Publisher · View at Google Scholar · View at Scopus
  18. B. A. Bryan, E. Dennstedt, D. C. Mitchell et al., “RhoA/ROCK signaling is essential for multiple aspects of VEGF-mediated angiogenesis,” The FASEB Journal, vol. 24, no. 9, pp. 3186–3195, 2010. View at Publisher · View at Google Scholar · View at Scopus
  19. N. Ferrara, H.-P. Gerber, and J. LeCouter, “The biology of VEGF and its receptors,” Nature Medicine, vol. 9, no. 6, pp. 669–676, 2003. View at Publisher · View at Google Scholar · View at Scopus
  20. K. Mandai, H. Nakanishi, A. Satoh et al., “Afadin: a novel actin filament-binding protein with one PDZ domain localized at cadherin-based cell-to-cell adherens junction,” The Journal of Cell Biology, vol. 139, no. 2, pp. 517–528, 1997. View at Publisher · View at Google Scholar · View at Scopus
  21. Y. Takai and H. Nakanishi, “Nectin and afadin: novel organizers of intracellular junctions,” Journal of Cell Science, vol. 116, no. 1, pp. 17–27, 2003. View at Publisher · View at Google Scholar · View at Scopus
  22. Y. Takai, K. Irie, K. Shimizu, T. Sakisaka, and W. Ikeda, “Nectins and nectin-like molecules: roles in cell adhesion, migration, and polarization,” Cancer Science, vol. 94, no. 8, pp. 655–667, 2003. View at Publisher · View at Google Scholar · View at Scopus
  23. M. Miyata, H. Ogita, H. Komura et al., “Localization of nectin-free afadin at the leading edge and its involvement in directional cell movement induced by platelet-derived growth factor,” Journal of Cell Science, vol. 122, no. 23, pp. 4319–4329, 2009. View at Publisher · View at Google Scholar · View at Scopus
  24. Y. Fukumoto, S. Kurita, Y. Takai, and H. Ogita, “Role of scaffold protein afadin dilute domain-interacting protein (ADIP) in platelet-derived growth factor-induced cell movement by activating Rac protein through Vav2 protein,” The Journal of Biological Chemistry, vol. 286, no. 50, pp. 43537–43548, 2011. View at Publisher · View at Google Scholar · View at Scopus
  25. T. Majima, H. Ogita, T. Yamada et al., “Involvement of afadin in the formation and remodeling of synapses in the hippocampus,” Biochemical and Biophysical Research Communications, vol. 385, no. 4, pp. 539–544, 2009. View at Publisher · View at Google Scholar · View at Scopus
  26. J.-E. van Leeuwen, I. Rafalovich, K. Sellers et al., “Coordinated nuclear and synaptic shuttling of afadin promotes spine plasticity and histone modifications,” The Journal of Biological Chemistry, vol. 289, no. 15, pp. 10831–10842, 2014. View at Publisher · View at Google Scholar · View at Scopus
  27. B. M. Gumbiner, “Cell adhesion: the molecular basis of tissue architecture and morphogenesis,” Cell, vol. 84, no. 3, pp. 345–357, 1996. View at Publisher · View at Google Scholar · View at Scopus
  28. A. B. Zhadanov, D. W. Provance Jr., C. A. Speer et al., “Absence of the tight junctional protein AF-6 disrupts epithelial cell-cell junctions and cell polarity during mouse development,” Current Biology, vol. 9, no. 16, pp. 880–888, 1999. View at Publisher · View at Google Scholar · View at Scopus
  29. G. Fournier, O. Cabaud, E. Josselin et al., “Loss of AF6/afadin, a marker of poor outcome in breast cancer, induces cell migration, invasiveness and tumor growth,” Oncogene, vol. 30, no. 36, pp. 3862–3874, 2011. View at Publisher · View at Google Scholar · View at Scopus
  30. G. M. J. Beaudoin III, C. M. Schofield, T. Nuwal et al., “Afadin, a Ras/Rap effector that controls cadherin function, promotes spine and excitatory synapse density in the hippocampus,” The Journal of Neuroscience, vol. 32, no. 1, pp. 99–110, 2012. View at Publisher · View at Google Scholar · View at Scopus
  31. M. Tanaka-Okamoto, K. Hori, H. Ishizaki et al., “Involvement of afadin in barrier function and homeostasis of mouse intestinal epithelia,” Journal of Cell Science, vol. 124, no. 13, pp. 2231–2240, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. S. Elloul, D. Kedrin, N. W. Knoblauch, A. H. Beck, and A. Toker, “The adherens junction protein Afadin is an AKT substrate that regulates breast cancer cell migration,” Molecular Cancer Research, vol. 12, no. 3, pp. 464–476, 2014. View at Publisher · View at Google Scholar · View at Scopus
  33. M. Potente, H. Gerhardt, and P. Carmeliet, “Basic and therapeutic aspects of angiogenesis,” Cell, vol. 146, no. 6, pp. 873–887, 2011. View at Publisher · View at Google Scholar · View at Scopus
  34. P. Carmeliet, “Mechanisms of angiogenesis and arteriogenesis,” Nature Medicine, vol. 6, no. 4, pp. 389–395, 2000. View at Publisher · View at Google Scholar · View at Scopus
  35. R. H. Adams and K. Alitalo, “Molecular regulation of angiogenesis and lymphangiogenesis,” Nature Reviews Molecular Cell Biology, vol. 8, no. 6, pp. 464–478, 2007. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Jeltsch, V.-M. Leppänen, P. Saharinen, and K. Alitalo, “Receptor tyrosine kinase-mediated angiogenesis,” Cold Spring Harbor Perspectives in Biology, vol. 5, no. 9, Article ID a009183, 2013. View at Publisher · View at Google Scholar · View at Scopus
  37. P. Carmeliet, V. Ferreira, G. Breier et al., “Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele,” Nature, vol. 380, no. 6573, pp. 435–439, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. G.-H. Fong, J. Rossant, M. Gertsenstein, and M. L. Breitman, “Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium,” Nature, vol. 376, no. 6535, pp. 66–70, 1995. View at Publisher · View at Google Scholar · View at Scopus
  39. F. Shalaby, J. Rossant, T. P. Yamaguchi et al., “Failure of blood-island formation and vasculogenesis in Flk-1-deficient mice,” Nature, vol. 376, no. 6535, pp. 62–66, 1995. View at Publisher · View at Google Scholar · View at Scopus
  40. S. Moens, J. Goveia, P. C. Stapor, A. R. Cantelmo, and P. Carmeliet, “The multifaceted activity of VEGF in angiogenesis—implications for therapy responses,” Cytokine & Growth Factor Reviews, vol. 25, no. 4, pp. 473–482, 2014. View at Google Scholar
  41. M. R. H. Kooistra, N. Dubé, and J. L. Bos, “Rap1: a key regulator in cell-cell junction formation,” Journal of Cell Science, vol. 120, no. 1, pp. 17–22, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. T. Sato, N. Fujita, A. Yamada et al., “Regulation of the assembly and adhesion activity of E-cadherin by nectin and afadin for the formation of adherens junctions in Madin-Darby canine kidney cells,” The Journal of Biological Chemistry, vol. 281, no. 8, pp. 5288–5299, 2006. View at Publisher · View at Google Scholar · View at Scopus
  43. H. Tawa, Y. Rikitake, M. Takahashi et al., “Role of afadin in vascular endothelial growth factor-and sphingosine 1-phosphate-induced angiogenesis,” Circulation Research, vol. 106, no. 11, pp. 1731–1742, 2010. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Rikitake, K.-I. Hirata, S. Kawashima et al., “Involvement of endothelial nitric oxide in sphingosine-1-phosphate—induced angiogenesis,” Arteriosclerosis, Thrombosis, and Vascular Biology, vol. 22, no. 1, pp. 108–114, 2002. View at Publisher · View at Google Scholar · View at Scopus
  45. E. Ackah, J. Yu, S. Zoellner et al., “Akt1/protein kinase Bα is critical for ischemic and VEGF-mediated angiogenesis,” The Journal of Clinical Investigation, vol. 115, no. 8, pp. 2119–2127, 2005. View at Publisher · View at Google Scholar · View at Scopus
  46. A. C. Monteiro, R. Sumagin, C. R. Rankin et al., “JAM-A associates with ZO-2, afadin, and PDZ-GEF1 to activate Rap2c and regulate epithelial barrier function,” Molecular Biology of the Cell, vol. 24, no. 18, pp. 2849–2860, 2013. View at Publisher · View at Google Scholar · View at Scopus
  47. A. A. Birukova, X. Tian, Y. Tian, K. Higginbotham, and K. G. Birukov, “Rap-afadin axis in control of Rho signaling and endothelial barrier recovery,” Molecular Biology of the Cell, vol. 24, no. 17, pp. 2678–2688, 2013. View at Publisher · View at Google Scholar · View at Scopus
  48. A. A. Birukova, P. Fu, T. Wu et al., “Afadin controls p120-catenin-ZO-1 interactions leading to endothelial barrier enhancement by oxidized phospholipids,” Journal of Cellular Physiology, vol. 227, no. 5, pp. 1883–1890, 2012. View at Publisher · View at Google Scholar · View at Scopus
  49. Z. Yang, S. Zimmerman, P. R. Brakeman, G. M. Beaudoin, L. F. Reichardt, and D. K. Marciano, “De novo lumen formation and elongation in the developing nephron: a central role for afadin in apical polarity,” Development, vol. 140, no. 8, pp. 1774–1784, 2013. View at Publisher · View at Google Scholar · View at Scopus
  50. E. A. Severson, W. Y. Lee, C. T. Capaldo, A. Nusrat, and C. A. Parkos, “Junctional adhesion molecule a interacts with afadin and PDZ-GEF2 to activate RaplA, regulate β1 integrin levels, and enhance cell migration,” Molecular Biology of the Cell, vol. 20, no. 7, pp. 1916–1925, 2009. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Chrzanowska-Wodnicka, A. E. Kraus, D. Gale, G. C. White II, and J. Vansluys, “Defective angiogenesis, endothelial migration, proliferation, and MAPK signaling in Rap1b-deficient mice,” Blood, vol. 111, no. 5, pp. 2647–2656, 2008. View at Publisher · View at Google Scholar · View at Scopus
  52. J. S. Mudgett, J. Ding, L. Guh-Siesel et al., “Essential role for p38α mitogen-activated protein kinase in placental angiogenesis,” Proceedings of the National Academy of Sciences of the United States of America, vol. 97, no. 19, pp. 10454–10459, 2000. View at Publisher · View at Google Scholar · View at Scopus
  53. N. Hatano, Y. Mori, M. Oh-hora et al., “Essential role for ERK2 mitogen-activated protein kinase in placental development,” Genes to Cells, vol. 8, no. 11, pp. 847–856, 2003. View at Publisher · View at Google Scholar · View at Scopus
  54. M. Chrzanowska-Wodnicka, S. S. Smyth, S. M. Schoenwaelder, T. H. Fischer, and G. C. White II, “Rap1b is required for normal platelet function and hemostasis in mice,” The Journal of Clinical Investigation, vol. 115, no. 3, pp. 680–687, 2005. View at Publisher · View at Google Scholar · View at Scopus
  55. K. Katagiri, A. Maeda, M. Shimonaka, and T. Kinashi, “RAPL, a Rap1-binding molecule that mediates Rap1-induced adhesion through spatial regulation of LFA-1,” Nature Immunology, vol. 4, no. 8, pp. 741–748, 2003. View at Publisher · View at Google Scholar · View at Scopus
  56. G. Carmona, S. Göttig, A. Orlandi et al., “Role of the small GTPase Rap1 for integrin activity regulation in endothelial cells and angiogenesis,” Blood, vol. 113, no. 2, pp. 488–497, 2009. View at Publisher · View at Google Scholar · View at Scopus
  57. T. Majima, K. Takeuchi, K. Sano et al., “An adaptor molecule afadin regulates lymphangiogenesis by modulating RhoA activity in the developing mouse embryo,” PLoS ONE, vol. 8, no. 6, Article ID e68134, 2013. View at Publisher · View at Google Scholar · View at Scopus
  58. J. Waschke, F. E. Curry, R. H. Adamson, and D. Drenckhahn, “Regulation of actin dynamics is critical for endothelial barrier functions,” American Journal of Physiology—Heart and Circulatory Physiology, vol. 288, no. 3, pp. H1296–H1305, 2005. View at Publisher · View at Google Scholar · View at Scopus
  59. K. J. Whitehead, A. C. Chan, S. Navankasattusas et al., “The cerebral cavernous malformation signaling pathway promotes vascular integrity via Rho GTPases,” Nature Medicine, vol. 15, no. 2, pp. 177–184, 2009. View at Publisher · View at Google Scholar · View at Scopus
  60. M. R. H. Kooistra, M. Corada, E. Dejana, and J. L. Bos, “Epac1 regulates integrity of endothelial cell junctions through VE-cadherin,” FEBS Letters, vol. 579, no. 22, pp. 4966–4972, 2005. View at Publisher · View at Google Scholar · View at Scopus
  61. K. Noda, J. Zhang, S. Fukuhara, S. Kunimoto, M. Yoshimura, and N. Mochizuki, “Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through α- and β-catenins in cyclic AMP-Epac-Rap1 signal-activated endothelial cells,” Molecular Biology of the Cell, vol. 21, no. 4, pp. 584–596, 2010. View at Publisher · View at Google Scholar · View at Scopus
  62. P. Baluk, J. Fuxe, H. Hashizume et al., “Functionally specialized junctions between endothelial cells of lymphatic vessels,” The Journal of Experimental Medicine, vol. 204, no. 10, pp. 2349–2362, 2007. View at Publisher · View at Google Scholar · View at Scopus
  63. N. Kanzaki, H. Ogita, H. Komura et al., “Involvement of the nectin-afadin complex in PDGF-induced cell survival,” Journal of Cell Science, vol. 121, no. 12, pp. 2008–2017, 2008. View at Publisher · View at Google Scholar · View at Scopus
  64. N. Rudini and E. Dejana, “Adherens junctions,” Current Biology, vol. 18, no. 23, pp. R1080–R1082, 2008. View at Publisher · View at Google Scholar · View at Scopus
  65. J. E. Nieset, A. R. Redfield, F. Jin, K. A. Knudsen, K. R. Johnson, and M. J. Wheelock, “Characterization of the interactions of α-catenin with α-actinin and β-catenin/plakoglobin,” Journal of Cell Science, vol. 110, no. 8, pp. 1013–1022, 1997. View at Google Scholar · View at Scopus
  66. L. Shapiro and W. I. Weis, “Structure and biochemistry of cadherins and catenins,” Cold Spring Harbor Perspectives in Biology, vol. 1, no. 3, Article ID a003053, 2009. View at Publisher · View at Google Scholar · View at Scopus
  67. A. B. Reynolds and R. H. Carnahan, “Regulation of cadherin stability and turnover by p120ctn: implications in disease and cancer,” Seminars in Cell and Developmental Biology, vol. 15, no. 6, pp. 657–663, 2004. View at Publisher · View at Google Scholar · View at Scopus
  68. P. Carmeliet, M.-G. Lampugnani, L. Moons et al., “Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis,” Cell, vol. 98, no. 2, pp. 147–157, 1999. View at Publisher · View at Google Scholar · View at Scopus
  69. I. Shiojima and K. Walsh, “Role of Akt signaling in vascular homeostasis and angiogenesis,” Circulation Research, vol. 90, no. 12, pp. 1243–1250, 2002. View at Publisher · View at Google Scholar · View at Scopus
  70. M. Corada, M. Mariotti, G. Thurston et al., “Vascular endothelial-cadherin is an important determinant of microvascular integrity in vivo,” Proceedings of the National Academy of Sciences of the United States of America, vol. 96, no. 17, pp. 9815–9820, 1999. View at Publisher · View at Google Scholar · View at Scopus
  71. A. C. Rapraeger, B. J. Ell, M. Roy et al., “Vascular endothelial-cadherin stimulates syndecan-1-coupled insulin-like growth factor-1 receptor and cross-talk between αvβ3 integrin and vascular endothelial growth factor receptor 2 at the onset of endothelial cell dissemination during angiogenesis,” FEBS Journal, vol. 280, no. 10, pp. 2194–2206, 2013. View at Publisher · View at Google Scholar · View at Scopus
  72. M. Hellström, L.-K. Phng, J. J. Hofmann et al., “Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis,” Nature, vol. 445, no. 7129, pp. 776–780, 2007. View at Publisher · View at Google Scholar · View at Scopus
  73. L. Jakobsson, C. A. Franco, K. Bentley et al., “Endothelial cells dynamically compete for the tip cell position during angiogenic sprouting,” Nature Cell Biology, vol. 12, no. 10, pp. 943–953, 2010. View at Publisher · View at Google Scholar · View at Scopus
  74. K. Bentley, C. A. Franco, A. Philippides et al., “The role of differential VE-cadherin dynamics in cell rearrangement during angiogenesis,” Nature Cell Biology, vol. 16, no. 4, pp. 309–321, 2014. View at Publisher · View at Google Scholar · View at Scopus
  75. M. G. Lampugnani, A. Zanetti, M. Corada et al., “Contact inhibition of VEGF-induced proliferation requires vascular endothelial cadherin, β-catenin, and the phosphatase DEP-1/CD148,” The Journal of Cell Biology, vol. 161, no. 4, pp. 793–804, 2003. View at Publisher · View at Google Scholar · View at Scopus
  76. B. Hämmerling, C. Grund, J. Boda-Heggemann, R. Moll, and W. W. Franke, “The Complexus adhaerens of mammalian lymphatic endothelia revisited: a junction even more complex than hitherto thought,” Cell and Tissue Research, vol. 324, no. 1, pp. 55–67, 2006. View at Publisher · View at Google Scholar · View at Scopus
  77. A. M. Goodwin, K. M. Sullivan, and P. A. D'Amore, “Cultured endothelial cells display endogenous activation of the canonical Wnt signaling pathway and express multiple ligands, receptors, and secreted modulators of Wnt signaling,” Developmental Dynamics, vol. 235, no. 11, pp. 3110–3120, 2006. View at Publisher · View at Google Scholar · View at Scopus
  78. H. Clevers, “Wnt/β-Catenin Signaling in Development and Disease,” Cell, vol. 127, no. 3, pp. 469–480, 2006. View at Publisher · View at Google Scholar · View at Scopus
  79. C. A. Franco, S. Liebner, and H. Gerhardt, “Vascular morphogenesis: a Wnt for every vessel?” Current Opinion in Genetics and Development, vol. 19, no. 5, pp. 476–483, 2009. View at Publisher · View at Google Scholar · View at Scopus
  80. M. Corada, D. Nyqvist, F. Orsenigo et al., “The Wnt/β-catenin pathway modulates vascular remodeling and specification by upregulating Dll4/notch signaling,” Developmental Cell, vol. 18, no. 6, pp. 938–949, 2010. View at Publisher · View at Google Scholar · View at Scopus
  81. C. M. Chiasson, K. B. Wittich, P. A. Vincent, V. Faundez, and A. P. Kowalczyk, “P120-catenin inhibits VE-cadherin internalization through a Rho-independent mechanism,” Molecular Biology of the Cell, vol. 20, no. 7, pp. 1970–1980, 2009. View at Publisher · View at Google Scholar · View at Scopus
  82. F. G. Giancotti and E. Ruoslahti, “Integrin signaling,” Science, vol. 285, no. 5430, pp. 1028–1032, 1999. View at Publisher · View at Google Scholar · View at Scopus
  83. Y. Wang, G. Jin, H. Miao, J. Y. S. Li, S. Usami, and S. Chien, “Integrins regulate VE-cadherin and catenins: dependence of this regulation on Src, but not on Ras,” Proceedings of the National Academy of Sciences of the United States of America, vol. 103, no. 6, pp. 1774–1779, 2006. View at Publisher · View at Google Scholar · View at Scopus
  84. N. L. Malinin, E. Pluskota, and T. V. Byzova, “Integrin signaling in vascular function,” Current Opinion in Hematology, vol. 19, no. 3, pp. 206–211, 2012. View at Publisher · View at Google Scholar · View at Scopus
  85. C. J. Avraamides, B. Garmy-Susini, and J. A. Varner, “Integrins in angiogenesis and lymphangiogenesis,” Nature Reviews Cancer, vol. 8, no. 8, pp. 604–617, 2008. View at Publisher · View at Google Scholar · View at Scopus
  86. P. R. Somanath, N. L. Malinin, and T. V. Byzova, “Cooperation between integrin αvβ3 and VEGFR2 in angiogenesis,” Angiogenesis, vol. 12, no. 2, pp. 177–185, 2009. View at Publisher · View at Google Scholar · View at Scopus
  87. A. C. Zovein, A. Luque, K. A. Turlo et al., “β1 integrin establishes endothelial cell polarity and arteriolar lumen formation via a Par3-dependent mechanism,” Developmental Cell, vol. 18, no. 1, pp. 39–51, 2010. View at Publisher · View at Google Scholar · View at Scopus
  88. A. van der Flier, K. Badu-Nkansah, C. A. Whittaker et al., “Endothelial α5 and αv integrins cooperate in remodeling of the vasculature during development,” Development, vol. 137, no. 14, pp. 2439–2449, 2010. View at Publisher · View at Google Scholar · View at Scopus
  89. K. M. Hodivala-Dilke, K. P. McHugh, D. A. Tsakiris et al., “β3-integrin-deficient mice are a model for Glanzmann thrombasthenia showing placental defects and reduced survival,” Journal of Clinical Investigation, vol. 103, no. 2, pp. 229–238, 1999. View at Publisher · View at Google Scholar · View at Scopus
  90. S. J. Monkley, V. Kostourou, L. Spence et al., “Endothelial cell talin1 is essential for embryonic angiogenesis,” Developmental Biology, vol. 349, no. 2, pp. 494–502, 2011. View at Publisher · View at Google Scholar · View at Scopus
  91. M. Moser, K. R. Legate, R. Zent, and R. Fässler, “The tail of integrins, talin, and kindlins,” Science, vol. 324, no. 5929, pp. 895–899, 2009. View at Publisher · View at Google Scholar · View at Scopus
  92. X. Z. Huang, J. F. Wu, R. Ferrando et al., “Fatal bilateral chylothorax in mice lacking the integrin α9β1,” Molecular and Cellular Biology, vol. 20, no. 14, pp. 5208–5215, 2000. View at Publisher · View at Google Scholar · View at Scopus
  93. E. Bazigou, S. Xie, C. Chen et al., “Integrin-α9 is required for fibronectin matrix assembly during lymphatic valve morphogenesis,” Developmental Cell, vol. 17, no. 2, pp. 175–186, 2009. View at Publisher · View at Google Scholar · View at Scopus
  94. N. E. Vlahakis, B. A. Young, A. Atakilit et al., “Integrin α9β1 directly binds to vascular endothelial growth factor (VEGF)-A and contributes to VEGF-A-induced angiogenesis,” The Journal of Biological Chemistry, vol. 282, no. 20, pp. 15187–15196, 2007. View at Publisher · View at Google Scholar · View at Scopus
  95. L.-C. Yao, P. Baluk, R. S. Srinivasan, G. Oliver, and D. M. McDonald, “Plasticity of button-like junctions in the endothelium of airway lymphatics in development and inflammation,” The American Journal of Pathology, vol. 180, no. 6, pp. 2561–2575, 2012. View at Publisher · View at Google Scholar · View at Scopus
  96. M. Dewerchin and P. Carmeliet, “PlGF: a multitasking cytokine with disease-restricted activity,” Cold Spring Harbor Perspectives in Medicine, vol. 2, no. 8, Article ID a011056, 2012. View at Publisher · View at Google Scholar · View at Scopus
  97. E. Boscolo, J. B. Mulliken, and J. Bischoff, “VEGFR-1 mediates endothelial differentiation and formation of blood vessels in a murine model of infantile hemangioma,” The American Journal of Pathology, vol. 179, no. 5, pp. 2266–2277, 2011. View at Publisher · View at Google Scholar · View at Scopus
  98. R. Serpi, A. M. Tolonen, J. Huusko et al., “Vascular endothelial growth factor-B gene transfer prevents angiotensin II-induced diastolic dysfunction via proliferation and capillary dilatation in rats,” Cardiovascular Research, vol. 89, no. 1, pp. 204–213, 2011. View at Publisher · View at Google Scholar · View at Scopus
  99. C. May, J. R. Doody, R. Abdullah et al., “Identification of a transiently exposed VE-cadherin epitope that allows for specific targeting of an antibody to the tumor neovasculature,” Blood, vol. 105, no. 11, pp. 4337–4344, 2005. View at Publisher · View at Google Scholar · View at Scopus
  100. Z. Liu, F. Wang, and X. Chen, “Integrin αvβ3-targeted cancer therapy,” Drug Development Research, vol. 69, no. 6, pp. 329–339, 2008. View at Publisher · View at Google Scholar · View at Scopus