Phosphoinositide-dependent kinase 1 and p21-activated protein kinase mediate reactive oxygen species-dependent regulation of platelet-derived growth factor-induced smooth muscle cell migration

Circulation Research

Volumn 94, Issue 9, 2004, Pages 1219-1226

  Weber, David S ^a   Taniyama, Yoshihiro ^a   Rocic, Petra ^a   Seshiah, Puvi N ^a   Dechert, Melissa A ^b   Gerthoffer, William T ^b   Griendling, Kathy K ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF NEVADA SCHOOL OF MEDICINE   (United States)

Author keywords

Growth factors; Migration; Reactive oxygen species; Signaling pathways; Vascular smooth muscle cells

Indexed keywords

ACETYLCYSTEINE; ANTIOXIDANT; CATALASE; DIPHENYLIODONIUM SALT; EBSELEN; GLUTATHIONE PEROXIDASE; PHOSPHOINOSITIDE DEPENDENT KINASE 1; PHOSPHOTRANSFERASE; PLATELET DERIVED GROWTH FACTOR; PROTEIN P21; REACTIVE OXYGEN METABOLITE; THREONINE; UNCLASSIFIED DRUG;

ADENOVIRUS; ANIMAL CELL; ARTICLE; ATHEROSCLEROSIS; CELL MIGRATION; CONTROLLED STUDY; ENZYME INHIBITION; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT; RESTENOSIS; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER;

ACETYLCYSTEINE; ANIMALS; AORTA, THORACIC; AZOLES; CELL MOVEMENT; CELLS, CULTURED; ENZYME ACTIVATION; HUMANS; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; MITOGEN-ACTIVATED PROTEIN KINASES; MUSCLE, SMOOTH, VASCULAR; MYOCYTES, SMOOTH MUSCLE; ORGANOSELENIUM COMPOUNDS; PHOSPHORYLATION; PLATELET-DERIVED GROWTH FACTOR; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES; RAC GTP-BINDING PROTEINS; RATS; REACTIVE OXYGEN SPECIES; RECEPTORS, PLATELET-DERIVED GROWTH FACTOR; RECOMBINANT FUSION PROTEINS; SIGNAL TRANSDUCTION; SRC-FAMILY KINASES;

EID: 2442666453     PISSN: 00097330     EISSN: None     Source Type: Journal    
DOI: 10.1161/01.RES.0000126848.54740.4A     Document Type: Article

References (39)

1. Schwartz SM. Smooth muscle migration in atherosclerosis and restenosis. J Clin Invest. 1997;100:S87-S89.
2. Clowes AW. Regulation of smooth muscle cell proliferation and migration. Transplant Proc. 1999;31:810-811.
3. Rönnstrand L, Heldin CH. Mechanisms of platelet-derived growth factor-induced chemotaxis. Int J Cancer. 2001;91:757-762.
4. Souza HP, Souza LC, Anastacio VM, Pereira AC, Junqueira ML, Krieger JE, da Luz PL, Augusto O, Laurindo FR. Vascular oxidant stress early after balloon injury: evidence for increased NAD(P)H oxidoreductase activity. Free Radic Biol Med. 2000;28:1232-1242.
5. Szöcs K, Lassègue B, Sorescu D, Hilenski LL, Valppu L, Couse TL, Wilcox JN, Quinn MT, Lambeth JD, Griendling KK. Upregulation of Nox-based NAD(P)H oxidases in restenosis after carotid injury. Arterioscler Thromb Vasc Biol. 2002;22:21-27.
6. - production in the pig coronary artery. Circulation. 1997;96:3593-3601.
7. 2 production requires the activation of phosphatidylinositol 3-kinase. J Biol Chem. 2000;275:10527-10531.
8. Sorescu D, Somers MJ, Lassegue B, Grant S, Harrison DG, Griendling KK. Electron spin resonance characterization of the NAD(P)H oxidase in vascular smooth muscle cells. Free Radic Biol Med. 2001;30:603-612.
9. 2 for platelet-derived growth factor signal transduction. Science. 1995;270:296-299.
10. Turner CE. Paxillin and focal adhesion signalling. Nat Cell Biol. 2000;2:E231-E236.
11. Dong LQ, Landa LR, Wick MJ, Zhu L, Mukai H, Ono Y, Liu F. Phosphorylation of protein kinase N by phosphoinositide-dependent protein kinase-1 mediates insulin signals to the actin cytoskeleton. Proc Natl Acad Sci U S A. 2000;97:5089-5094.
12. Park J, Hill MM, Hess D, Brazil DP, Hofsteenge J, Hemmings BA. Identification of tyrosine phosphorylation sites on 3-phosphoinositide-dependent protein kinase-1 and their role in regulating kinase activity. J Biol Chem. 2001;276:37459-37471.
13. Prasad N, Topping RS, Zhou D, Decker SJ. Oxidative stress and vanadate induce tyrosine phosphorylation of phosphoinositide-dependent kinase 1 (PDK1). Biochemistry. 2000;39:6929-6935.
14. Casamayor A, Morrice NA, Alessi DR. 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. 1999;342(pt 2):287-292.
15. Taniyama Y, Weber DS, Rocic P, Hilenski LL, Akers MA, Park J, Hemmings BA, Alexander RW, Griendling KK. Pyk2-and Src-dependent tyrosine phosphorylation of PDK1 regulates focal adhesions. Mol Cell Biol. 2003;40:723-727.
16. King CC, Gardiner EM, Zenke FT, Bohl BP, Newton AC, Hemmings BA, Bokoch GM. p21-activated kinase (PAK1) is phosphorylated and activated by 3-phosphoinositide-dependent kinase-1 (PDK1). J Biol Chem. 2000;275:41201-41209.
17. Kumar R, Vadlamudi RK. Emerging functions of p21-activated kinases in human cancer cells. J Cell Physiol. 2002;193:133-144.
18. Bokoch GM. Biology of the p21-activated kinases. Annu Rev Biochem. 2003;72:743-781.
19. Dharmawardhane S, Sanders LC, Martin SS, Daniels RH, Bokoch GM. Localization of p21-activated kinase 1 (PAK1) to pinocytic vesicles and cortical actin structures in stimulated cells. J Cell Biol. 1997;138:1265-1278.
20. Sells MA, Pfaff A, Chernoff J. Temporal and spatial distribution of activated Pak1 in fibroblasts. J Cell Biol. 2000;151:1449-1458.
21. Dechert MA, Holder JM, Gerthoffer WY. p21-activated kinase 1 participates in tracheal smooth muscle cell migration by signaling to p38 MAPK. Am J Physiol Cell Physiol. 2001;281:C123-C132.
22. Griendling KK, Taubman MB, Akers M, Mendlowitz M, Alexander RW. Characterization of phosphatidylinositol-specific phospholipase C from cultured vascular smooth muscle cells. J Biol Chem. 1991;266:15498-15504.
23. Zafari AM, Ushio-Fukai M, Akers M, Yin Q, Shah A, Harrison DG, Taylor WR, Griendling KK. Novel role of NADH/NADPH oxidase-derived hydrogen peroxide in angiotensin 11-induced hypertrophy of rat vascular smooth muscle cells. Hypertension. 1998;32:488-495.
24. Brown C, Pan X, Hassid A. Nitric oxide and C-type atrial natriuretic peptide stimulate primary aortic smooth muscle cell migration via a cGMP-dependent mechanism: relationship to microfilament dissociation and altered cell morphology. Circ Res. 1999;84:655-667.
25. Boguslawski G, Grogg JR, Harvey KA, English D. Use of DAP1 staining for quantitation of cell chemotaxis. Biotechniques. 2001;30:42-48.
26. Rocic P, Seshiah P, Griendling KK. Reactive oxygen species sensitivity of angiotensin II-dependent translation initiation in vascular smooth muscle cells. J Biol Chem. 2003;278:36973-36979.
27. Seshiah PN, Weber DS, Rocic P, Valppu L, Taniyama Y, Griendling KK. Angiotensin II stimulation of NAD(P)H oxidase activity: upstream mediators. Circ Res. 2002;91:406-413.
28. Griendling KK, Minieri CA, Ollerenshaw JD, Alexander RW. Angiotensin II stimulates NADH and NADPH oxidase activity in cultured vascular smooth muscle cells. Circ Res. 1994;74:1141-1148.
29. Yamboliev IA, Chen J, Gerthoffer WT. PI 3-kinases and Src kinases regulate spreading and migration of cultured VSMCs. Am J Physiol Cell Physiol. 2001;281:C709-C718.
30. Ushio-Fukai M, Alexander RW, Akers M, Yin Q, Fujio Y, Walsh K, Griendling KK. Reactive oxygen species mediate the activation of Akt/protein kinase B by angiotensin II in vascular smooth muscle cells. J Biol Chem. 1999;274:22699-22704.
31. Rao GN, Katki KA, Madamanchi NR, Wu Y, Birrer MJ. JunB forms the majority of the AP-1 complex and is a target for redox regulation by receptor tyrosine kinase and G protein-coupled receptor agonists in smooth muscle cells. J Biol Chem. 1999;274:6003-6010.
32. Tian X, Rusanescu G, Hou W, Schaffhausen B, Feig LA. PDK1 mediates growth factor-induced Ral-GEF activation by a kinase-independent mechanism. EMBO J. 2002;21:1327-1338.
33. Griendling KK, Ushio-Fukai M. Reactive oxygen species as mediators of angiotensin II signaling. Regul Pept. 2000;91:21-27.
34. Higaki M, Sakaue H, Ogawa W, Kasuga M, Shimokado K. Phosphatidylinositol 3-kinase-independent signal transduction pathway for platelet-derived growth factor-induced chemotaxis. J Biol Chem. 1996;271:29342-29346.
35. Ushio-Fukai M, Griendling KK, Becker PL, Hilenski L, Halleran S, Alexander RW. Epidermal growth factor receptor transactivation by angiotensin II requires reactive oxygen species in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol. 2001;21:459-495.
36. Abe J, Takahashi M, Ishida M, Lee JD, Berk BC. c-Src is required for oxidative stress-mediated activation of big mitoge-activated protein kinase 1. J Biol Chem. 1997;272:20389-20394.
37. Aikawa R, Komuro I, Yamazaki T, Zou Y, Kudoh S, Tanaka M, Shiojima I, Hiroi Y, Yazaki Y. Oxidative stress activates extracellular signal-regulated kinases through Src and Ras in cultured cardiac myocytes of neonatal rats. J Clin Invest. 1997;100:1813-1521.
38. Schmitz U, Thommes K, Beier I, Vetter H. Lysophosphatidic acid stimulates p21-activated kinase in vascular smooth muscle cells. Biochem Biophys Res Commun. 2002;291:687-691.
39. Grillo S, Gremeaux T, Casamayor A, Alessi DR, Le Marchand-Brustel Y, Tanti JF. Peroxovanadate induces tyrosine phosphorylation of phosphoinositide-dependent protein kinase-1 potential involvement of src kinase. Eur J Biochem. 2000;267:6642-6649.