Pyk2- and Src-Dependent Tyrosine Phosphorylation of PDK1 Regulates Focal Adhesions

REFERENCES

• Alessi, D. R., M. Deak, A. Casamayor, F. B. Caudwell, N. Morrice, D. G. Norman, P. Gaffney, C. B. Reese, C. N. MacDougall, D. Harbison, A. Ashworth, and M. Bownes. 1997. 3-Phosphoinositide-dependent protein kinase-1 (PDK1): structural and functional homology with the Drosophila DSTPK61 kinase. Curr. Biol. 7: 776–789.
   PubMed Web of Science ®Google Scholar
• Alessi, D. R., S. R. James, C. P. Downes, A. B. Holmes, P. R. Gaffney, C. B. Reese, and P. Cohen. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase B alpha. Curr. Biol. 7: 261–269.
   PubMed Web of Science ®Google Scholar
• Anderson, K. E., J. Coadwell, L. R. Stephens, and P. T. Hawkins. 1998. Translocation of PDK-1 to the plasma membrane is important in allowing PDK-1 to activate protein kinase B. Curr. Biol. 8: 684–691.
   PubMed Web of Science ®Google Scholar
• Avraham, H., S. Y. Park, K. Schinkmann, and S. Avraham. 2000. RAFTK/Pyk2-mediated cellular signalling. Cell Signal. 12: 123–133.
   PubMed Web of Science ®Google Scholar
• Berk, B. C. 1999. Angiotensin II signal transduction in vascular smooth muscle: pathways activated by specific tyrosine kinases. J. Am. Soc. Nephrol. 10(Suppl. 11): S62–S68.
   PubMedGoogle Scholar
• Bokoch, G. M. 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72: 743–781.
   PubMed Web of Science ®Google Scholar
• Brinson, A. E., T. Harding, P. A. Diliberto, Y. He, X. Li, D. Hunter, B. Herman, H. S. Earp, and L. M. Graves. 1998. Regulation of a calcium-dependent tyrosine kinase in vascular smooth muscle cells by angiotensin II and platelet-derived growth factor. Dependence on calcium and the actin cytoskeleton. J. Biol. Chem. 273: 1711–1718.
   PubMedGoogle Scholar
• Casamayor, A., N. A. Morrice, and D. R. Alessi. 1999. Phosphorylation of Ser-241 is essential for the activity of 3-phosphoinositide-dependent protein kinase-1: identification of five sites of phosphorylation in vivo. Biochem. J. 342: 287–292.
   PubMed Web of Science ®Google Scholar
• Chen, H., F. H. Nystrom, L. Q. Dong, Y. Li, S. Song, F. Liu, and M. J. Quon. 2001. Insulin stimulates increased catalytic activity of phosphoinositide-dependent kinase-1 by a phosphorylation-dependent mechanism. Biochemistry 40: 11851–11859.
   PubMedGoogle Scholar
• Daniels, R. H., and G. M. Bokoch. 1999. p21-activated protein kinase: a crucial component of morphological signaling? Trends Biochem. Sci. 24: 350–355.
   PubMed Web of Science ®Google Scholar
• Dikic, I., G. Tokiwa, S. Lev, S. A. Courtneidge, and J. Schlessinger. 1996. A role for Pyk2 and Src in linking G-protein-coupled receptors with MAP kinase activation. Nature 383: 547–550.
   PubMed Web of Science ®Google Scholar
• Dong, L. Q., L. R. Landa, M. J. Wick, L. Zhu, H. Mukai, Y. Ono, and F. Liu. 2000. Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton. Proc. Natl. Acad. Sci. USA 97: 5089–5094.
   PubMedGoogle Scholar
• Eguchi, S., H. Iwasaki, T. Inagami, K. Numaguchi, T. Yamakawa, E. D. Motley, K. M. Owada, F. Marumo, and Y. Hirata. 1999. Involvement of PYK2 in angiotensin II signaling of vascular smooth muscle cells. Hypertension 33: 201–206.
   PubMedGoogle Scholar
• Eguchi, S., H. Iwasaki, H. Ueno, G. D. Frank, E. D. Motley, K. Eguchi, F. Marumo, Y. Hirata, and T. Inagami. 1999. Intracellular signaling of angiotensin II-induced p70 S6 kinase phosphorylation at Ser(411) in vascular smooth muscle cells. Possible requirement of epidermal growth factor receptor, Ras, extracellular signal-regulated kinase, and Akt. J. Biol. Chem. 274: 36843–36851.
   PubMedGoogle Scholar
• Eguchi, S., K. Numaguchi, H. Iwasaki, T. Matsumoto, T. Yamakawa, H. Utsunomiya, E. D. Motley, H. Kawakatsu, K. M. Owada, Y. Hirata, F. Marumo, and T. Inagami. 1998. Calcium-dependent epidermal growth factor receptor transactivation mediates the angiotensin II-induced mitogen-activated protein kinase activation in vascular smooth muscle cells. J. Biol. Chem. 273: 8890–8896.
   PubMed Web of Science ®Google Scholar
• Filippa, N., C. L. Sable, B. A. Hemmings, and E. Van Obberghen. 2000. Effect of phosphoinositide-dependent kinase 1 on protein kinase B translocation and its subsequent activation. Mol. Cell. Biol. 20: 5712–5721.
   PubMed Web of Science ®Google Scholar
• Geiger, B., A. Bershadsky, R. Pankov, and K. M. Yamada. 2001. Transmembrane crosstalk between the extracellular matrix-cytoskeleton crosstalk. Nat. Rev. Mol. Cell. Biol. 2: 793–805.
   PubMed Web of Science ®Google Scholar
• Gismondi, A., L. Bisogno, F. Mainiero, G. Palmieri, M. Piccoli, L. Frati, and A. Santoni. 1997. Proline-rich tyrosine kinase-2 activation by beta 1 integrin fibronectin receptor cross-linking and association with paxillin in human natural killer cells. J. Immunol. 159: 4729–4736.
   PubMedGoogle Scholar
• Griendling, K. K., B. Lassègue, and R. W. Alexander. 1996. Angiotensin receptors and their therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 36: 281–306.
   PubMed Web of Science ®Google Scholar
• Griendling, K. K., C. A. Minieri, J. D. Ollerenshaw, and R. W. Alexander. 1994. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ. Res. 74: 1141–1148.
   PubMed Web of Science ®Google Scholar
• Griendling, K. K., S. E. Rittenhouse, T. A. Brock, L. S. Ekstein, M. A. Gimbrone, Jr., and R. W. Alexander. 1986. Sustained diacylglycerol formation from inositol phospholipids in angiotensin II-stimulated vascular smooth muscle cells. J. Biol. Chem. 261: 5901–5906.
   PubMed Web of Science ®Google Scholar
• Griendling, K. K., M. B. Taubman, M. Akers, M. Mendlowitz, and R. W. Alexander. 1991. Characterization of phosphatidylinositol-specific phospholipase C from cultured vascular smooth muscle cells. J. Biol. Chem. 266: 15498–15504.
   PubMed Web of Science ®Google Scholar
• Griendling, K. K., T. Tsuda, B. C. Berk, and R. W. Alexander. 1989. Angiotensin II stimulation of vascular smooth muscle cells. Secondary signalling mechanisms. Am. J. Hypertens. 2: 659–665.
   PubMed Web of Science ®Google Scholar
• Grillo, S., T. Gremeaux, A. Casamayor, D. R. Alessi, Y. Le Marchand-Brustel, and J. F. Tanti. 2000. Peroxovanadate induces tyrosine phosphorylation of phosphoinositide-dependent protein kinase-1 potential involvement of src kinase. Eur. J. Biochem. 267: 6642–6649.
   PubMedGoogle Scholar
• He, T. C., S. Zhou, L. T. da Costa, J. Yu, K. W. Kinzler, and B. Vogelstein. 1998. A simplified system for generating recombinant adenoviruses. Proc. Natl. Acad. Sci. USA 95: 2509–2514.
   PubMed Web of Science ®Google Scholar
• Ishida, M., M. B. Marrero, B. Schieffer, T. Ishida, K. E. Bernstein, and B. C. Berk. 1995. Angiotensin II activates pp60c-src in vascular smooth muscle cells. Circ. Res. 77: 1053–1059.
   PubMed Web of Science ®Google Scholar
• Ishida, T., M. Ishida, J. Suero, M. Takahashi, and B. C. Berk. 1999. Agonist-stimulated cytoskeletal reorganization and signal transduction at focal adhesions in vascular smooth muscle cells require c-Src. J. Clin. Investig. 103: 789–797.
   PubMed Web of Science ®Google Scholar
• Lassègue, B., R. W. Alexander, G. Nickenig, M. Clark, T. J. Murphy, and K. K. Griendling. 1995. Angiotensin II down-regulates the vascular smooth muscle AT1 receptor by transcriptional and post-transcriptional mechanisms: evidence for homologous and heterologous regulation. Mol. Pharmacol. 48: 601–609.
   PubMedGoogle Scholar
• Lassègue, B., D. Sorescu, K. Szocs, Q. Yin, M. Akers, Y. Zhang, S. L. Grant, J. D. Lambeth, and K. K. Griendling. 2001. Novel gp91(phox) homologues in vascular smooth muscle cells: nox1 mediates angiotensin II-induced superoxide formation and redox-sensitive signaling pathways. Circ. Res. 88: 888–894.
   PubMed Web of Science ®Google Scholar
• Lev, S., H. Moreno, R. Martinez, P. Canoll, E. Peles, J. M. Musacchio, G. D. Plowman, B. Rudy, and J. Schlessinger. 1995. Protein tyrosine kinase PYK2 involved in Ca(2+)-induced regulation of ion channel and MAP kinase functions. Nature 376: 737–745.
   PubMed Web of Science ®Google Scholar
• Li, J., H. Avraham, R. A. Rogers, S. Raja, and S. Avraham. 1996. Characterization of RAFTK, a novel focal adhesion kinase, and its integrin-dependent phosphorylation and activation in megakaryocytes. Blood 88: 417–428.
   PubMed Web of Science ®Google Scholar
• Li, X., and H. S. Earp. 1997. Paxillin is tyrosine-phosphorylated by and preferentially associates with the calcium-dependent tyrosine kinase in rat liver epithelial cells. J. Biol. Chem. 272: 14341–14348.
   PubMedGoogle Scholar
• Liao, D. F., B. Monia, N. Dean, and B. C. Berk. 1997. Protein kinase C-zeta mediates angiotensin II activation of ERK1/2 in vascular smooth muscle cells. J. Biol. Chem. 272: 6146–6150.
   PubMed Web of Science ®Google Scholar
• Litvak, V., D. Tian, Y. D. Shaul, and S. Lev. 2000. Targeting of PYK2 to focal adhesions as a cellular mechanism for convergence between integrins and G protein-coupled receptor signaling cascades. J. Biol. Chem. 275: 32736–32746.
   PubMedGoogle Scholar
• Morales-Ruiz, M., D. Fulton, G. Sowa, L. R. Languino, Y. Fujio, K. Walsh, and W. C. Sessa. 2000. Vascular endothelial growth factor-stimulated actin reorganization and migration of endothelial cells is regulated via the serine/threonine kinase Akt. Circ. Res. 86: 892–896.
   PubMed Web of Science ®Google Scholar
• Murphy, T. J., R. W. Alexander, K. K. Griendling, M. S. Runge, and K. E. Bernstein. 1991. Isolation of a cDNA encoding the vascular type-1 angiotensin II receptor. Nature 351: 233–236.
   PubMed Web of Science ®Google Scholar
• Nakamura, K., H. Yano, H. Uchida, S. Hashimoto, E. Schaefer, and H. Sabe. 2000. Tyrosine phosphorylation of paxillin alpha is involved in temporospatial regulation of paxillin-containing focal adhesion formation and F-actin organization in motile cells. J. Biol. Chem. 275: 27155–27164.
   PubMedGoogle Scholar
• Park, J., M. M. Hill, D. Hess, D. P. Brazil, J. Hofsteenge, and B. A. Hemmings. 2001. Identification of tyrosine phosphorylation sites on 3-phosphoinositide-dependent protein kinase-1 and their role in regulating kinase activity. J. Biol. Chem. 276: 37459–37471.
   PubMedGoogle Scholar
• Prasad, N., R. S. Topping, D. Zhou, and S. J. Decker. 2000. Oxidative stress and vanadate induce tyrosine phosphorylation of phosphoinositide-dependent kinase 1 (PDK1). Biochemistry 39: 6929–6935.
   PubMed Web of Science ®Google Scholar
• Rocic, P., G. Govindarajan, A. Sabri, and P. A. Lucchesi. 2001. A role for PYK2 in regulation of ERK1/2 MAP kinases and PI 3-kinase by ANG II in vascular smooth muscle. Am. J. Physiol. Cell Physiol. 280: C90–C99.
   PubMedGoogle Scholar
• Rocic, P., and P. A. Lucchesi. 2001. Down-regulation by antisense oligonucleotides establishes a role for the proline-rich tyrosine kinase PYK2 in angiotensin II-induced signaling in vascular smooth muscle. J. Biol. Chem. 276: 21902–21906.
   PubMedGoogle Scholar
• Sabri, A., G. Govindarajan, T. M. Griffin, K. L. Byron, A. M. Samarel, and P. A. Lucchesi. 1998. Calcium- and protein kinase C-dependent activation of the tyrosine kinase PYK2 by angiotensin II in vascular smooth muscle. Circ. Res. 83: 841–851.
   PubMedGoogle Scholar
• Salgia, R., S. Avraham, E. Pisick, J. L. Li, S. Raja, E. A. Greenfield, M. Sattler, H. Avraham, and J. D. Griffin. 1996. The related adhesion focal tyrosine kinase forms a complex with paxillin in hematopoietic cells. J. Biol. Chem. 271: 31222–31226.
   PubMed Web of Science ®Google Scholar
• Sastry, S. K., and K. Burridge. 2000. Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell Res. 261: 25–36.
   PubMed Web of Science ®Google Scholar
• Saward, I., and P. Zahradka. 1997. Angiotensin II activates phosphatidylinositol 3-kinase in vascular smooth muscle cells. Circ. Res. 81: 249–257.
   PubMed Web of Science ®Google Scholar
• Schmitz, U., T. Ishida, M. Ishida, J. Surapisitchat, M. I. Hasham, S. Pelech, and B. C. Berk. 1998. Angiotensin II stimulates p21-activated kinase in vascular smooth muscle cells: role in activation of JNK. Circ. Res. 82: 1272–1278.
   PubMed Web of Science ®Google Scholar
• Stephens, L., K. Anderson, D. Stokoe, H. Erdjument-Bromage, G. F. Painter, A. B. Holmes, P. R. Gaffney, C. B. Reese, F. McCormick, P. Tempst, J. Coadwell, and P. T. Hawkins. 1998. Protein kinase B kinases that mediate phosphatidylinositol 3,4,5-trisphosphate-dependent activation of protein kinase B. Science 279: 710–714.
   PubMed Web of Science ®Google Scholar
• Takahashi, E., J. Abe, and B. C. Berk. 1997. Angiotensin II stimulates p90rsk in vascular smooth muscle cells. A potential Na(+)-H+ exchanger kinase. Circ. Res. 81: 268–273.
   PubMed Web of Science ®Google Scholar
• Tang, H., Q. Hao, T. Fitzgerald, T. Sasaki, E. J. Landon, and T. Inagami. 2002. Pyk2/CAKbeta tyrosine kinase activity-mediated angiogenesis of pulmonary vascular endothelial cells. J. Biol. Chem. 277: 5441–5447.
   PubMedGoogle Scholar
• Toker, A., and A. C. Newton. 2000. Cellular signaling: pivoting around PDK-1. Cell 103: 185–188.
   PubMed Web of Science ®Google Scholar
• Ushio-Fukai, M., R. W. Alexander, M. Akers, Q. Yin, Y. Fujio, K. Walsh, and K. K. Griendling. 1999. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J. Biol. Chem. 274: 22699–22704.
   PubMed Web of Science ®Google Scholar
• Ushio-Fukai, M., K. K. Griendling, P. L. Becker, L. Hilenski, S. Halleran, and R. W. Alexander. 2001. Epidermal growth factor receptor transactivation by angiotensin II requires reactive oxygen species in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 21: 489–495.
   PubMed Web of Science ®Google Scholar
• Ushio-Fukai, M., L. Hilenski, N. Santanam, P. L. Becker, Y. Ma, K. K. Griendling, and R. W. Alexander. 2001. Cholesterol depletion inhibits epidermal growth factor receptor transactivation by angiotensin II in vascular smooth muscle cells: role of cholesterol-rich microdomains and focal adhesions in angiotensin II signaling. J. Biol. Chem. 276: 48269–48275.
   PubMed Web of Science ®Google Scholar
• Vanhaesebroeck, B., and D. R. Alessi. 2000. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346: 561–576.
   PubMed Web of Science ®Google Scholar
• Watson, J. M., T. W. Harding, V. Golubovskaya, J. S. Morris, D. Hunter, X. Li, J. S. Haskill, and H. S. Earp. 2001. Inhibition of the calcium-dependent tyrosine kinase (CADTK) blocks monocyte spreading and motility. J. Biol. Chem. 276: 3536–3542.
   PubMedGoogle Scholar
• Xiong, W., and J. T. Parsons. 1997. Induction of apoptosis after expression of PYK2, a tyrosine kinase structurally related to focal adhesion kinase. J. Cell Biol. 139: 529–539.
   PubMed Web of Science ®Google Scholar