Molecules and Cells

Korean Society for Molecular and Cellular Biology (한국분자세포생물학회)
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Protein Kinase D1, a New Molecular Player in VEGF Signaling and Angiogenesis

  • Ha, Chang Hoon (The Aab Cardiovascular Research Institute and Department of Medicine, University of Rochester School of Medicine and Dentistry) ;
  • Jin, Zheng Gen (The Aab Cardiovascular Research Institute and Department of Medicine, University of Rochester School of Medicine and Dentistry)
  • Received : 2009.06.26
  • Accepted : 2009.06.29
  • Published : 2009.07.31
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Abstract

Vascular endothelial growth factor (VEGF) is essential for many angiogenic processes both in normal and pathological conditions. However, the signaling pathways involved in VEGF-induced angiogenesis are incompletely understood. The protein kinase D1 (PKD1), a newly described calcium/calmodulin-dependent serine/threonine kinase, has been implicated in cell migration, proliferation and membrane trafficking. Increasing evidence suggests critical roles for PKD1-mediated signaling pathways in endothelial cells, particularly in the regulation of VEGF-induced angiogenesis. Recent studies show that class IIa histone deacetylases (HDACs) are PKD1 substrates and VEGF signal-responsive repressors of myocyte enhancer factor-2 (MEF2) transcriptional activation in endothelial cells. This review provides a guide to PKD1 signaling pathways and the direct downstream targets of PKD1 in VEGF signaling, and suggests important functions of PKD1 in angiogenesis.

Keywords

Acknowledgement

Supported by : American Hear Association, National Institute of Health

References

  1. Abedi, H., Rozengurt, E., and Zachary, I. (1998). Rapid activation of the novel serine/threonine protein kinase, protein kinase D by phorbol esters, angiotensin II and PDGF-BB in vascular smooth muscle cells. FEBS Lett. 427, 209-212 https://doi.org/10.1016/S0014-5793(98)00427-X
  2. Auer, A., von Blume, J., Sturany, S., von Wichert, G., Van Lint, J., Vandenheede, J., Adler, G., and Seufferlein, T. (2005). Role of the regulatory domain of protein kinase D2 in phorbol ester binding, catalytic activity, and nucleocytoplasmic shuttling. Mol. Biol. Cell 16, 4375-4385 https://doi.org/10.1091/mbc.E05-03-0251
  3. Avkiran, M., Rowland, A.J., Cuello, F., and Haworth, R.S. (2008). Protein kinase d in the cardiovascular system: emerging roles in health and disease. Circ. Res. 102, 157-163 https://doi.org/10.1161/CIRCRESAHA.107.168211
  4. Backs, J., Song, K., Bezprozvannaya, S., Chang, S., and Olson, E.N. (2006). CaM kinase II selectively signals to histone deacetylase 4 during cardiomyocyte hypertrophy. J. Clin. Invest. 116, 1853-1864 https://doi.org/10.1172/JCI27438
  5. Baron, C.L., and Malhotra, V. (2002). Role of diacylglycerol in PKD recruitment to the TGN and protein transport to the plasma membrane. Science 295, 325-328 https://doi.org/10.1126/science.1066759
  6. Benjamin, L.E., and Keshet, E. (1997). Conditional switching of vascular endothelial growth factor (VEGF) expression in tumors: induction of endothelial cell shedding and regression of heman-gioblastoma-like vessels by VEGF withdrawal. Proc. Natl. Acad. Sci. USA 94, 8761-8766 https://doi.org/10.1073/pnas.94.16.8761
  7. Benjamin, L.E., Golijanin, D., Itin, A., Pode, D., and Keshet, E. (1999). Selective ablation of immature blood vessels in established human tumors follows ascular endothelial growth factor withdrawal. J. Clin. Invest. 103, 159-165 https://doi.org/10.1172/JCI5028
  8. Carmeliet, P. (2000). Mechanisms of angiogenesis and arteriogenesis. Nat. Med. 6, 389-395 https://doi.org/10.1038/74651
  9. Carmeliet, P. (2003). Angiogenesis in health and disease. Nat. Med. 9, 653-660 https://doi.org/10.1038/nm0603-653
  10. Carmeliet, P., Ferreira, V., Breier, G., Pollefeyt, S., Kieckens, L., Gertsenstein, M., Fahrig, M., Vandenhoeck, A., Harpal, K., Eberhardt, C., et al. (1996). Abnormal blood vessel development and lethality in embryos lacking a single VEGF allele. Nature 380, 435-439 https://doi.org/10.1038/380435a0
  11. Carmeliet, P., Lampugnani, M.G., Moons, L., Breviario, F., Compernolle, V., Bono, F., Balconi, G., Spagnuolo, R., Oostuyse, B., Dewerchin, M.I et al. (1999). Targeted deficiency or cytosolic truncation of the VE-cadherin gene in mice impairs VEGF-mediated endothelial survival and angiogenesis. Cell 98, 147-157 https://doi.org/10.1016/S0092-8674(00)81010-7
  12. Chang, S., Young, B.D., Li, S., Qi, X., Richardson, J.A., and Olson, E.N. (2006). Histone deacetylase 7 maintains vascular integrity by repressing matrix metalloproteinase 10. Cell 126, 321-334 https://doi.org/10.1016/j.cell.2006.05.040
  13. Chen, H., Chedotal, A., He, Z., Goodman, C.S., and Tessier-Lavigne, M. (1997). Neuropilin-2, a novel member of the neuropilin family, is a high affinity receptor for the semaphorins Sema E and Sema IV but not Sema III. Neuron 19, 547-559 https://doi.org/10.1016/S0896-6273(00)80371-2
  14. Chiu, T., and Rozengurt, E. (2001a). CCK2 (CCK(B)/gastrin) receptor mediates rapid protein kinase D (PKD) activation through a protein kinase C-dependent pathway. FEBS Lett. 489, 101-106 https://doi.org/10.1016/S0014-5793(01)02076-2
  15. Chiu, T., and Rozengurt, E. (2001b). PKD in intestinal epithelial cells: rapid activation by phorbol esters, LPA, and angiotensin through PKC. Am. J. Physiol. 280, C929-942
  16. Chiu, T., Wu, S.S., Santiskulvong, C., Tangkijvanich, P., Yee, H.F., Jr., and Rozengurt, E. (2002). Vasopressin-mediated mitogenic signaling in intestinal epithelial cells. Am. J. Physiol. 282, C434-450 https://doi.org/10.1152/ajpcell.00240.2001
  17. Claesson-Welsh, L. (2003). Signal transduction by vascular endothelial growth factor receptors. Biochem. Soc. Trans. 31, 20-24 https://doi.org/10.1042/BST0310020
  18. Eliceiri, B.P., Paul, R., Schwartzberg, P.L., Hood, J.D., Leng, J., and Cheresh, D.A. (1999). Selective requirement for Src kinases during VEGF-induced angiogenesis and vascular permeability. Mol. Cell 4, 915-924 https://doi.org/10.1016/S1097-2765(00)80221-X
  19. Ferrara, N. (2002). VEGF and the quest for tumour angiogenesis factors. Nat. Rev. 2, 795-803 https://doi.org/10.1038/nrc909
  20. Ferrara, N., and Alitalo, K. (1999). Clinical applications of angiogenic growth factors and their inhibitors. Nat. Med. 5, 1359-1364 https://doi.org/10.1038/70928
  21. Ferrara, N., and Davis-Smyth, T. (1997). The biology of vascular endothelial growth factor. Endocrine Rev. 18, 4-25 https://doi.org/10.1210/er.18.1.4
  22. Ferrara, N., Gerber, H.P., and LeCouter, J. (2003). The biology of VEGF and its receptors. Nat. Med. 9, 669-676 https://doi.org/10.1038/nm0603-669
  23. Folkman, J. (1995). Angiogenesis in cancer, vascular, rheumatoid and other disease. Nat. Med. 1, 27-31 https://doi.org/10.1038/nm0195-27
  24. Fong, G.H., Rossant, J., Gertsenstein, M., and Breitman, M.L. (1995). Role of the Flt-1 receptor tyrosine kinase in regulating the assembly of vascular endothelium. Nature 376, 66-70 https://doi.org/10.1038/376066a0
  25. Gerber, H.P., Dixit, V., and Ferrara, N. (1998a). Vascular endothelial growth factor induces expression of the antiapoptotic proteins Bcl-2 and A1 in vascular endothelial cells. J. Biol. Chem. 273, 13313-13316 https://doi.org/10.1074/jbc.273.21.13313
  26. Gerber, H.P., McMurtrey, A., Kowalski, J., Yan, M., Keyt, B.A., Dixit, V., and Ferrara, N. (1998b). Vascular endothelial growth factor regulates endothelial cell survival through the phosphatidylinositol 3'-kinase/Akt signal transduction pathway. Requirement for Flk-1/KDR activation. J. Biol. Chem. 273, 30336-30343 https://doi.org/10.1074/jbc.273.46.30336
  27. Gille, H., Kowalski, J., Li, B., LeCouter, J., Moffat, B., Zioncheck, T.F., Pelletier, N., and Ferrara, N. (2001). Analysis of biological effects and signaling properties of Flt-1 (VEGFR-1) and KDR (VEGFR-2). A reassessment using novel receptor-specific vascular endothelial growth factor mutants. J. Biol. Chem. 276, 3222-3230 https://doi.org/10.1074/jbc.M002016200
  28. Guo, D., Jia, Q., Song, H.Y., Warren, R.S., and Donner, D.B. (1995). Vascular endothelial cell growth factor promotes tyrosine phosphorylation of mediators of signal transduction that contain SH2 domains. Association with endothelial cell proliferation. J. Biol. Chem. 270, 6729-6733 https://doi.org/10.1074/jbc.270.12.6729
  29. Ha, C.H., Jhun, B.S., Kao, H.Y., and Jin, Z.G. (2008a). VEGF stimulates HDAC7 phosphorylation and cytoplasmic accumulation modulating matrix metalloproteinase expression and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 28, 1782-1788 https://doi.org/10.1161/ATVBAHA.108.172528
  30. Ha, C.H., Wang, W., Jhun, B.S., Wong, C., Hausser, A., Pfizenmaier, K., McKinsey, T.A., Olson, E.N., and Jin, Z.G. (2008b). Protein kinase D-dependent phosphorylation and nuclear export of histone deacetylase 5 mediates vascular endothelial growth factor-induced gene expression and angiogenesis. J. Biol. Chem. 283, 14590-14599 https://doi.org/10.1074/jbc.M800264200
  31. Hanks, S.K. (2003). Genomic analysis of the eukaryotic protein kinase superfamily: a perspective. Genome Biol. 4, 111 https://doi.org/10.1186/gb-2003-4-5-111
  32. Hao, Q., Wang, L., Zhao, Z.J., and Tang, H. (2009). Identification of protein kinase D2 as a pivotal regulator of endothelial cell proliferation, migration, and angiogenesis. J. Biol. Chem. 284, 799-806 https://doi.org/10.1074/jbc.M807546200
  33. Hausser, A., Link, G., Bamberg, L., Burzlaff, A., Lutz, S., Pfizenmaier,K., and Johannes, F.J. (2002). Structural requirements for localization and activation of protein kinase C mu (PKC mu) at the Golgi compartment. J. Cell Biol. 156, 65-74 https://doi.org/10.1083/jcb.200110047
  34. Haworth, R.S., Goss, M.W., Rozengurt, E., and Avkiran, M. (2000). Expression and activity of protein kinase D/protein kinase C mu in myocardium: evidence for alpha1-adrenergic receptor- and protein kinase C-mediated regulation. J. Mol. Cell. Cardiol. 32, 1013-1023 https://doi.org/10.1006/jmcc.2000.1143
  35. Haworth, R.S., Cuello, F., Herron, T.J., Franzen, G., Kentish, J.C., Gautel, M., and Avkiran, M. (2004). Protein kinase D is a novel mediator of cardiac troponin I phosphorylation and regulates myofilament function. Circ. Res. 95, 1091-1099 https://doi.org/10.1161/01.RES.0000149299.34793.3c
  36. Hayashi, A., Seki, N., Hattori, A., Kozuma, S., and Saito, T. (1999). PKCnu, a new member of the protein kinase C family, composes a fourth subfamily with PKCmu. Biochim. Biophys. Acta 1450, 99-106 https://doi.org/10.1016/S0167-4889(99)00040-3
  37. Houck, K.A., Ferrara, N., Winer, J., Cachianes, G., Li, B., and Leung, D.W. (1991). The vascular endothelial growth factor family: identification of a fourth molecular species and characterization of alternative splicing of RNA. Mol. Endocrinol. (Baltimore, Md 5, 1806-1814 https://doi.org/10.1210/mend-5-12-1806
  38. Iglesias, T., and Rozengurt, E. (1998). Protein kinase D activation by mutations within its pleckstrin homology domain. J. Biol. Chem. 273, 410-416 https://doi.org/10.1074/jbc.273.1.410
  39. Iglesias, T., Matthews, S., and Rozengurt, E. (1998a). Dissimilar phorbol ester binding properties of the individual cysteine-rich motifs of protein kinase D. FEBS Lett. 437, 19-23 https://doi.org/10.1016/S0014-5793(98)01189-2
  40. Iglesias, T., Waldron, R.T., and Rozengurt, E. (1998b). Identification of in vivo phosphorylation sites required for protein kinase D activation. J. Biol. Chem. 273, 27662-27667 https://doi.org/10.1074/jbc.273.42.27662
  41. Jamora, C., Yamanouye, N., Van Lint, J., Laudenslager, J., Vandenheede, J.R., Faulkner, D.J., and Malhotra, V. (1999). Gbetagamma-mediated regulation of Golgi organization is through the direct activation of protein kinase D. Cell 98, 59-68 https://doi.org/10.1016/S0092-8674(00)80606-6
  42. Johannes, F.J., Prestle, J., Eis, S., Oberhagemann, P., and Pfizenmaier, K. (1994). PKCu is a novel, atypical member of the protein kinase C family. J. Biol. Chem. 269, 6140-6148
  43. Kolodkin, A.L., Levengood, D.V., Rowe, E.G., Tai, Y.T., Giger, R.J., and Ginty, D.D. (1997). Neuropilin is a semaphorin III receptor. Cell 90, 753-762 https://doi.org/10.1016/S0092-8674(00)80535-8
  44. Kunkel, M.T., Toker, A., Tsien, R.Y., and Newton, A.C. (2007). Calcium-dependent regulation of protein kinase D revealed by a genetically encoded kinase activity reporter. J. Biol. Chem. 282, 6733-6742 https://doi.org/10.1074/jbc.M608086200
  45. Liljedahl, M., Maeda, Y., Colanzi, A., Ayala, I., Van Lint, J., and Malhotra, V. (2001). Protein kinase D regulates the fission of cell surface destined transport carriers from the trans-Golgi network. Cell 104, 409-420 https://doi.org/10.1016/S0092-8674(01)00228-8
  46. Lin, Q., Lu, J., Yanagisawa, H., Webb, R., Lyons, G.E., Richardson, J.A., and Olson, E.N. (1998). Requirement of the MADS-box transcription factor MEF2C for vascular development. Development 125, 4565-4574
  47. Lint, J.V., Rykx, A., Vantus, T., and Vandenheede, J.R. (2002). Getting to know protein kinase D. Int. J. Biochem. Cell Biol. 34, 577-581
  48. Matthews, S.A., Pettit, G.R., and Rozengurt, E. (1997). Bryostatin 1 induces biphasic activation of protein kinase D in intact cells. J. Biol. Chem. 272, 20245-20250 https://doi.org/10.1074/jbc.272.32.20245
  49. Matthews, S.A., Rozengurt, E., and Cantrell, D. (1999). Characterization of serine 916 as an in vivo autophosphorylation site for protein kinase D/Protein kinase Cmu. J. Biol. Chem. 274, 26543-26549 https://doi.org/10.1074/jbc.274.37.26543
  50. Matthews, S.A., Iglesias, T., Rozengurt, E., and Cantrell, D. (2000a). Spatial and temporal regulation of protein kinase D (PKD). EMBO J. 19, 2935-2945 https://doi.org/10.1093/emboj/19.12.2935
  51. Matthews, S.A., Rozengurt, E., and Cantrell, D. (2000b). Protein kinase D. A selective target for antigen receptors and a downstream target for protein kinase C in lymphocytes. J. Exp. Med. 191, 2075-2082 https://doi.org/10.1084/jem.191.12.2075
  52. McKinsey, T.A., and Olson, E.N. (2005). Toward transcriptional therapies for the failing heart: chemical screens to modulate genes. J. Clin. Invest. 115, 538-546
  53. Mellor, H., and Parker, P.J. (1998). The extended protein kinase C superfamily. Biochem. J. 332, 281-292
  54. Meyer, M., Clauss, M., Lepple-Wienhues, A., Waltenberger, J., Augustin, H.G., Ziche, M., Lanz, C., Buttner, M., Rziha, H.J., and Dehio, C. (1999). A novel vascular endothelial growth factor encoded by Orf virus, VEGF-E, mediates angiogenesis via signalling through VEGFR-2 (KDR) but not VEGFR-1 (Flt-1) receptor tyrosine kinases. EMBO J. 18, 363-374 https://doi.org/10.1093/emboj/18.2.363
  55. Neufeld, G., Cohen, T., Gengrinovitch, S., and Poltorak, Z. (1999). Vascular endothelial growth factor (VEGF) and its receptors. FASEB J. 13, 9-22
  56. Newton, A.C. (1997). Regulation of protein kinase C. Curr. Opin. Cell Biol. 9, 161-167 https://doi.org/10.1016/S0955-0674(97)80058-0
  57. Qin, L., Zeng, H., and Zhao, D. (2006). Requirement of protein kinase D tyrosine phosphorylation for VEGF-A165-induced angiogenesis through its interaction and regulation of phospholipase Cgamma phosphorylation. J. Biol. Chem. 281, 32550-32558 https://doi.org/10.1074/jbc.M604853200
  58. Rey, O., and Rozengurt, E. (2001). Protein kinase D interacts with Golgi via its cysteine-rich domain. Biochem. Biophys. Res. Commun. 287, 21-26 https://doi.org/10.1006/bbrc.2001.5530
  59. Rey, O., Young, S.H., Cantrell, D., and Rozengurt, E. (2001). Rapid protein kinase D translocation in response to G protein-coupled receptor activation. Dependence on protein kinase C. J. Biol. Chem. 276, 32616-32626 https://doi.org/10.1074/jbc.M101649200
  60. Rey, O., Yuan, J., Young, S.H., and Rozengurt, E. (2003). Protein kinase C nu/protein kinase D3 nuclear localization, catalytic activation, and intracellular redistribution in response to G proteincoupled receptor agonists. J. Biol. Chem. 278, 23773-23785 https://doi.org/10.1074/jbc.M300226200
  61. Rey, O., Reeve, J.R., Jr., Zhukova, E., Sinnett-Smith, J., and Rozengurt, E. (2004). G protein-coupled receptor-mediated phosphorylation of the activation loop of protein kinase D: dependence on plasma membrane translocation and protein kinase Cepsilon. J. Biol. Chem. 279, 34361-34372 https://doi.org/10.1074/jbc.M403265200
  62. Robinson, C.J., and Stringer, S.E. (2001). The splice variants of vascular endothelial growth factor (VEGF) and their receptors. J. Cell Sci. 114, 853-865
  63. Rozengurt, E., Rey, O., and Waldron, R.T. (2005). Protein kinase D signaling. J. Biol. Chem. 280, 13205-13208 https://doi.org/10.1074/jbc.R500002200
  64. Sakurai, Y., Ohgimoto, K., Kataoka, Y., Yoshida, N., and Shibuya, M. (2005). Essential role of Flk-1 (VEGF receptor 2) tyrosine residue 1173 in asculogenesis in mice. Proc. Natl. Acad. Sci. USA 102, 1076-1081 https://doi.org/10.1073/pnas.0404984102
  65. Shalaby, F., Rossant, J., Yamaguchi, T.P., Gertsenstein, M., Wu, X.F., Breitman, M.L., and Schuh, A.C. (1995). Failure of bloodisland formation and vasculogenesis in Flk-1-deficient mice. Nature 372, 62-66
  66. Shibuya, M., Yamaguchi, S., Yamane, A., Ikeda, T., Tojo, A., Matsushime, H., and Sato, M. (1990). Nucleotide sequence and expression of a novel human receptor-type tyrosine kinase gene (flt) closely related to the fms family. Oncogene 5, 519-524
  67. Sidorenko, S.P., Law, C.L., Klaus, S.J., Chandran, K.A., Takata, M., Kurosaki, T., and Clark, E.A. (1996). Protein kinase C mu (PKC mu) associates with the B cell antigen receptor complex and regulates lymphocyte signaling. Immunity 5, 353-363 https://doi.org/10.1016/S1074-7613(00)80261-7
  68. Stafford, M.J., Watson, S.P., and Pears, C.J. (2003). PKD: a new protein kinase C-dependent pathway in platelets. Blood 101, 1392-1399 https://doi.org/10.1182/blood-2002-08-2384
  69. Stalmans, I., Ng, Y.S., Rohan, R., Fruttiger, M., Bouche, A., Yuce, A., Fujisawa, H., Hermans, B., Shani, M., Jansen, S., et al. (2002). Arteriolar and venular patterning in retinas of mice selectively expressing VEGF isoforms. J. Clin. Invest. 109, 327-336
  70. Storz, P., and Toker, A. (2003). Protein kinase D mediates a stress-induced NF-kappaB activation and survival pathway. EMBO J. 22, 109-120 https://doi.org/10.1093/emboj/cdg009
  71. Takahashi, T., Ueno, H., and Shibuya, M. (1999). VEGF activates protein kinase C-dependent, but Ras-independent Raf-MEKMAP kinase pathway for DNA synthesis in primary endothelial cells. Oncogene 18, 2221-2230 https://doi.org/10.1038/sj.onc.1202527
  72. Takahashi, T., Yamaguchi, S., Chida, K., and Shibuya, M. (2001). A single autophosphorylation site on KDR/Flk-1 is essential for VEGF-A-dependent activation of PLC-gamma and DNA synthesis in vascular endothelial cells. EMBO J. 20, 2768-2778 https://doi.org/10.1093/emboj/20.11.2768
  73. Terman, B.I., Carrion, M.E., Kovacs, E., Rasmussen, B.A., Eddy, R.L., and Shows, T.B. (1991). Identification of a new endothelial cell growth factor receptor tyrosine kinase. Oncogene 6, 1677-1683
  74. Tischer, E., Mitchell, R., Hartman, T., Silva, M., Gospodarowicz, D., Fiddes, J.C., and Abraham, J.A. (1991). The human gene for vascular endothelial growth factor. Multiple protein forms are encoded through alternative exon splicing. J. Biol. Chem. 266, 11947-11954
  75. Valverde, A.M., Sinnett-Smith, J., Van Lint, J., and Rozengurt, E. (1994). Molecular cloning and characterization of protein kinase D: a target for diacylglycerol and phorbol esters with a distinctive catalytic domain. Proc. Natl. Acad. Sci. USA 91, 8572-8576 https://doi.org/10.1073/pnas.91.18.8572
  76. Van Lint, J.V., Sinnett-Smith, J., and Rozengurt, E. (1995). Expression and characterization of PKD, a phorbol ester and diacylglycerol-stimulated serine protein kinase. J. Biol. Chem. 270, 1455-1461 https://doi.org/10.1074/jbc.270.3.1455
  77. Waldron, R.T., Iglesias, T., and Rozengurt, E. (1999). The pleckstrin homology domain of protein kinase D interacts preferentially with the eta isoform of protein kinase C. J. Biol. Chem. 274, 9224-9230 https://doi.org/10.1074/jbc.274.14.9224
  78. Waldron, R.T., Rey, O., Iglesias, T., Tugal, T., Cantrell, D., and Rozengurt, E. (2001). Activation loop Ser744 and Ser748 in protein kinase D are transphosphorylated in vivo. J. Biol. Chem. 276, 32606-32615 https://doi.org/10.1074/jbc.M101648200
  79. Waldron, R.T., and Rozengurt, E. (2003). Protein kinase C phosphorylates protein kinase D activation loop Ser744 and Ser748 and releases autoinhibition by the pleckstrin homology domain. J. Biol. Chem. 278, 154-163 https://doi.org/10.1074/jbc.M208075200
  80. Wang, S., Li, X., Parra, M., Verdin, E., Bassel-Duby, R., Olson, E.N. (2008). Control of endothelial cell proliferation and migration by VEGF signaling to histone deacetylase 7. Proc. Natl. Acad. Sci. USA 105, 7738-7743 https://doi.org/10.1073/pnas.0802857105
  81. Wise, L.M., Veikkola, T., Mercer, A.A., Savory, L.J., Fleming, S.B., Caesar, C., Vitali, A., Makinen, T., Alitalo, K., and Stacker, S.A. (1999). Vascular endothelial growth factor (VEGF)-like protein from orf virus NZ2 binds to VEGFR2 and neuropilin-1. Proc. Natl. Acad. Sci. USA 96, 3071-3076 https://doi.org/10.1073/pnas.96.6.3071
  82. Wong, C., and Jin, Z.G. (2005). Protein kinase C-dependent protein kinase D activation modulates ERK signal pathway and endothelial cell proliferation by vascular endothelial growth factor. J. Biol. Chem. 280, 33262-33269 https://doi.org/10.1074/jbc.M503198200
  83. Xu, X., Ha, C.H., Wong, C., Wang, W., Hausser, A., Pfizenmaier, K., Olson, E.N., McKinsey, T.A., and Jin, Z.G. (2007). Angiotensin II stimulates protein kinase D-dependent histone deacetylase 5 phosphorylation and nuclear export leading to vascular smooth muscle cell hypertrophy. Arterioscler. Thromb. Vasc. Biol. 27, 2355-2362 https://doi.org/10.1161/ATVBAHA.107.151704
  84. Yancopoulos, G.D., Davis, S., Gale, N.W., Rudge, J.S., Wiegand, S.J., and Holash, J. (2000). Vascular-specific growth factors and blood vessel formation. Nature 407, 242-248 https://doi.org/10.1038/35025215
  85. Yeaman, C., Ayala, M.I., Wright, J.R., Bard, F., Bossard, C., Ang, A., Maeda, Y., Seufferlein, T., Mellman, I., Nelson, W.J.I et al. (2004). Protein kinase D regulates basolateral membrane protein exit from trans-Golgi network. Nat. Cell Biol. 6, 106-112 https://doi.org/10.1038/ncb1090
  86. Youn, H.D., and Liu, J.O. (2000). Cabin1 represses MEF2-dependent Nur77 expression and T cell apoptosis by controlling association of histone eacetylases and acetylases with MEF2. Immunity 13, 85-94 https://doi.org/10.1016/S1074-7613(00)00010-8
  87. Yuan, F., Chen, Y., Dellian, M., Safabakhsh, N., Ferrara, N., and Jain, R.K. (1996). Time-dependent vascular regression and permeability changes in established human tumor xenografts induced by an anti-vascular endothelial growth factor/vascular permeability factor antibody. Proc. Natl. Acad. Sci. USA 93, 14765-14770 https://doi.org/10.1073/pnas.93.25.14765
  88. Zachary, I. (2003). VEGF signalling: integration and multi-tasking in endothelial cell biology. Biochem. Soc. Trans. 31, 1171-1177 https://doi.org/10.1042/BST0311171
  89. Zhang, C.L., McKinsey, T.A., Chang, S., Antos, C.L., Hill, J.A., and Olson, E.N. (2002). Class II histone deacetylases act as signalresponsive repressors of cardiac hypertrophy. Cell 100, 479-488
  90. Zhukova, E., Sinnett-Smith, J., and Rozengurt, E. (2001). Protein kinase D potentiates DNA synthesis and cell proliferation induced by bombesin, vasopressin, or phorbol esters in Swiss 3T3 cells. J. Biol. Chem. 276, 40298-40305
  91. Zugaza, J.L., Sinnett-Smith, J., Van Lint, J., and Rozengurt, E. (1996). Protein kinase D (PKD) activation in intact cells through a protein kinase C-dependent signal transduction pathway. EMBO J. 15, 6220-6230
  92. Zugaza, J.L., Waldron, R.T., Sinnett-Smith, J., and Rozengurt, E. (1997). Bombesin, vasopressin, endothelin, bradykinin, and platelet-derived growth factor rapidly activate protein kinase D through a protein kinase C-dependent signal transduction pathway. J. Biol. Chem. 272, 23952-23960 https://doi.org/10.1074/jbc.272.38.23952

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