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

Molecular and Cellular Biology

Volumn 23, Issue 22, 2003, Pages 8019-8029

  Taniyama, Yoshihiro ^a   Weber, David S ^a   Rocic, Petra ^a   Hilenski, Lula ^a   Akers, Marjorie L ^a   Park, Jongsun ^b   Hemmings, Brian A ^b   Alexander, R Wayne ^a   Griendling, Kathy K ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b FRIEDRICH MIESCHER INSTITUTE FOR BIOMEDICAL RESEARCH   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

3 PHOSPHOINOSITIDE DEPENDENT PROTEIN KINASE 1; ANGIOTENSIN; FOCAL ADHESION KINASE 2; G PROTEIN COUPLED RECEPTOR; PROTEIN KINASE; PROTEIN TYROSINE KINASE; TYROSINE; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL GROWTH; CELL MIGRATION; CONTROLLED STUDY; ENZYME ACTIVATION; FOCAL ADHESION; MALE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FAMILY; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; RAT; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ANGIOTENSIN II; ANIMALS; BASE SEQUENCE; BINDING SITES; CELLS, CULTURED; DNA, COMPLEMENTARY; FOCAL ADHESION KINASE 2; FOCAL ADHESIONS; MUSCLE, SMOOTH, VASCULAR; MUTAGENESIS, SITE-DIRECTED; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; RATS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES; TYROSINE;

ANIMALIA;

EID: 0242580122     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.23.22.8019-8029.2003     Document Type: Article

References (56)

1. 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.
2. 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.
3. 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.
4. Avraham, H., S. Y. Park, K. Schinkmann, and S. Avraham. 2000. RAFTK/Pyk2-mediated cellular signalling. Cell Signal. 12:123-133.
5. 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.
6. Bokoch, G. M. 2003. Biology of the p21-activated kinases. Annu. Rev. Biochem. 72:743-781.
7. 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.
8. 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.
9. 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.
10. Daniels, R. H., and G. M. Bokoch. 1999. p21-activated protein kinase: a crucial component of morphological signaling? Trends Biochem. Sci. 24:350-355.
11. 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.
12. 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.
13. 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.
14. 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.
15. 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.
16. 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.
17. 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.
18. 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.
19. Griendling, K. K., B. Lassègue, and R. W. Alexander. 1996. Angiotensin receptors and their therapeutic implications. Annu. Rev. Pharmacol. Toxicol. 36:281-306.
20. 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.
21. 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.
22. 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.
23. 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.
24. 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.
25. 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.
26. 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.
27. 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.
28. Lassègne, 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.
29. 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.
30. 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.
31. 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.
32. 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.
33. 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.
34. 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.
35. 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.
36. 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.
37. 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.
38. 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.
39. 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.
40. 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.
41. 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.
42. 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.
43. 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.
44. Sastry, S. K., and K. Burridge. 2000. Focal adhesions: a nexus for intracellular signaling and cytoskeletal dynamics. Exp. Cell Res. 261:25-36.
45. Saward, I., and P. Zahradka. 1997. Angiotensin II activates phosphatidylinositol 3-kinase in vascular smooth muscle cells. Circ. Res. 81:249-257.
46. 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.
47. 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.
48. 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.
49. 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.
50. Toker, A., and A. C. Newton. 2000. Cellular signaling: pivoting around PDK-1. Cell 103:185-188.
51. 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.
52. 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. Vase. Biol. 21:489-495.
53. 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.
54. Vanhaesebroeck, B., and D. R. Alessi. 2000. The PI3K-PDK1 connection: more than just a road to PKB. Biochem. J. 346:561-576.
55. 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.
56. 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.