Glycogen synthase kinase 3- and extracellular signal-regulated kinase-dependent phosphorylation of paxillin regulates cytoskeletal rearrangement

Molecular and Cellular Biology

Volumn 26, Issue 7, 2006, Pages 2857-2868

  Cai, Xinming ^a   Li, Min ^b   Vrana, Julie ^b   Schaller, Michael D ^a  

^a UNIVERSITY OF NORTH CAROLINA   (United States)

^b Center for Signal Transduction Research   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; COLONY STIMULATING FACTOR; GLYCOGEN SYNTHASE KINASE 3; LIPOPOLYSACCHARIDE; MITOGEN ACTIVATED PROTEIN KINASE; NERVE GROWTH FACTOR; PAXILLIN; RAF PROTEIN; SERINE; TYROSINE;

ANIMAL CELL; ARTICLE; CELL MIGRATION; CELL SPREADING; CONTROLLED STUDY; CYTOSKELETON; FOCAL ADHESION; IMMUNOFLUORESCENCE; IMMUNOPRECIPITATION; IN VITRO STUDY; MACROPHAGE; MOUSE; NERVE FIBER GROWTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN PURIFICATION; RAT;

ANIMALS; CELL MOVEMENT; CYTOSKELETON; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; FIBROBLASTS; GLYCOGEN SYNTHASE KINASE 3; HUMANS; LIPOPOLYSACCHARIDES; MACROPHAGES; MICE; NERVE GROWTH FACTORS; NEURITES; PAXILLIN; PC12 CELLS; PHOSPHORYLATION; PROTEIN TRANSPORT; RATS; SERINE; TYROSINE;

ANIMALIA;

EID: 33645218959     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.26.7.2857-2868.2006     Document Type: Article

References (46)

1. Bellis, S. L., J. A. Perrotta, M. S. Curtis, and C. E. Turner. 1997. Adhesion of fibroblasts to fibronectin stimulates both serine and tyrosine phosphorylation of paxillin. Biochem. J. 325:375-381.
2. Biondi, R. M., and A. R. Nebreda. 2003. Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions. Biochem. J. 372:1-13.
3. Brown, M. C., J. A. Perrotta, and C. E. Turner. 1996. Identification of LIM3 as the principal determinant of paxillin focal adhesion localization and characterization of a novel motif on paxillin directing vinculin and focal adhesion kinase binding. J. Cell Biol. 135:1109-1123.
4. Brown, M. C., J. A. Perrotta, and C. E. Turner. 1998. Serine and threonine phosphorylation of the paxillin LIM domains regulates paxillin focal adhesion localization and cell adhesion to fibronectin. Mol. Biol. Cell 9:1803-1816.
5. Brown, M. C., and C. E. Turner. 1999. Characterization of paxillin LIM domain-associated serine threonine kinases: activation by angiotensin II in vascular smooth muscle cells. J. Cell Biochem. 76:99-108.
6. Brown, M. C., and C. E. Turner. 2004. Paxillin: adapting to change. Physiol. Rev. 84:1315-1339.
7. Burstein, D. E., P. J. Seeley, and L. A. Greene. 1985. Lithium ion inhibits nerve growth factor-induced neurite outgrowth and phosphorylation of nerve growth factor-modulated microtubule-associated proteins. J. Cell Biol. 101:862-870.
8. Chu, B., F. Soncin, B. D. Price, M. A. Stevenson, and S. K. Calderwood. 1996. Sequential phosphorylation by mitogen-activated protein kinase and glycogen synthase kinase 3 represses transcriptional activation by heat shock factor-1. J. Biol. Chem. 271:30847-30857.
9. Cooley, M. A., J. M. Broome, C. Ohngemach, L. H. Romer, and M. D. Schaller. 2000. Paxillin binding is not the sole determinant of focal adhesion localization or dominant-negative activity of focal adhesion kinase/focal adhesion kinase-related nonkinase. Mol. Biol. Cell 11:3247-3263.
10. Del Rio, J. A., C. Gonzalez-Billault, J. M. Urena, E. M. Jimenez, M. J. Barallobre, M. Pascual, L. Pujadas, S. Simo, A. La Torre, F. Wandosell, J. Avila, and E. Soriano. 2004. MAP1B is required for Netrin 1 signaling in neuronal migration and axonal guidance. Curr. Biol. 14:840-850.
11. De Nichilo, M. O., and K. M. Yamada. 1996. Integrin alpha v beta 5-dependent serine phosphorylation of paxillin in cultured human macrophages adherent to vitronectin. J. Biol. Chem. 271:11016-11022.
12. Dikic, I., J. Schlessinger, and I. Lax. 1994. PC12 cells overexpressing the insulin receptor undergo insulin-dependent neuronal differentiation. Curr. Biol. 4:702-708.
13. Doble, B. W., and J. R. Woodgett. 2003. GSK-3: tricks of the trade for a multi-tasking kinase. J. Cell Sci. 116:1175-1186.
14. Embi, N., D. B. Rylatt, and P. Cohen. 1980. Glycogen synthase kinase-3 from rabbit skeletal muscle. Separation from cyclic-AMP-dependent protein kinase and phosphorylase kinase. Eur. J. Biochem. 107:519-527.
15. Fiol, C. J., A. M. Mahrenholz, Y. Wang, R. W. Roeske, and P. J. Roach. 1987. Formation of protein kinase recognition sites by covalent modification of the substrate. Molecular mechanism for the synergistic action of casein kinase II and glycogen synthase kinase 3. J. Biol. Chem. 262:14042-14048.
16. Goold, R. G., and P. R. Gordon-Weeks. 2005. The MAP kinase pathway is upstream of the activation of GSK3beta that enables it to phosphorylate MAP1B and contributes to the stimulation of axon growth. Mol. Cell Neurosci. 28:524-534.
17. Goold, R. G., R. Owen, and P. R. Gordon-Weeks. 1999. Glycogen synthase kinase 3beta phosphorylation of microtubule-associated protein 1B regulates the stability of microtubules in growth cones. J. Cell Sci. 112:3373-3384.
18. Hagel, M., E. L. George, A. Kim, R. Tamimi, S. L. Opitz, C. E. Turner, A. Imamoto, and S. M. Thomas. 2002. The adaptor protein paxillin is essential for normal development in the mouse and is a critical transducer of fibronectin signaling. Mol. Cell. Biol. 22:901-915.
19. Hanger, D. P., K. Hughes, J. R. Woodgett, J. P. Brion, and B. H. Anderton. 1992. Glycogen synthase kinase-3 induces Alzheimer's disease-like phosphorylation of tau: generation of paired helical filament epitopes and neuronal localisation of the kinase. Neurosci. Lett. 147:58-62.
20. He, B., Y. H. Meng, and N. F. Mivechi. 1998. Glycogen synthase kinase 3beta and extracellular signal-regulated kinase inactivate heat shock transcription factor 1 by facilitating the disappearance of transcriptionally active granules after heat shock. Mol. Cell. Biol. 18:6624-6633.
21. Huang, C., C. H. Borchers, M. D. Schaller, and K. Jacobson. 2004. Phosphorylation of paxiliin by p38MAPK is involved in the neurite extension of PC-12 cells. J. Cell Biol. 164:593-602.
22. Huang, C., Z. Rajfur, C. Borchers, M. D. Schaller, and K. Jacobson. 2003. JNK phosphorylates paxillin and regulates cell migration. Nature 424:219-223.
23. Ishibe, S., D. Joly, Z. X. Liu, and L. G. Cantley. 2004. Paxillin serves as an ERK-regulated scaffold for coordinating FAK and Rac activation in epithelial morphogenesis. Mol. Cell 16:257-267.
24. Ishibe, S., D. Joly, X. Zhu, and L. G. Cantley. 2003. Phosphorylation-dependent paxillin-ERK association mediates hepatocyte growth factor-stimulated epithelial morphogenesis. Mol. Cell 12:1275-1285.
25. Ivankovic-Dikic, I., E. Gronroos, A. Blaukat, B. U. Barth, and I. Dikic. 2000. Pyk2 and FAK regulate neurite outgrowth induced by growth factors and integrins. Nat. Cell Biol. 2:574-581.
26. Jope, R. S., and G. V. Johnson. 2004. The glamour and gloom of glycogen synthase kinase-3. Trends Biochem. Sci. 29:95-102.
27. Koivisto, L., K. Alavian, L. Hakkinen, S. Pelech, C. A. McCulloch, and H. Larjava. 2003. Glycogen synthase kinase-3 regulates formation of long lamellipodia in human keratinocytes. J. Cell Sci. 116:3749-3760.
28. Ku, H., and K. E. Meier. 2000. Phosphorylation of paxillin via the ERK mitogen-activated protein kinase cascade in EL4 thymoma cells. J. Biol. Chem. 275:11333-11340.
29. Liu, C., Y. Li, M. Semenov, C. Han, G. H. Baeg, Y. Tan, Z. Zhang, X. Lin, and X. He. 2002. Control of beta-catenin phosphorylation/degradation by a dual-kinase mechanism. Cell 108:837-847.
30. Monick, M. M., A. B. Carter, P. K. Robeff, D. M. Flaherty, M. W. Peterson, and G. W. Hunninghake. 2001. Lipopolysaccharide activates Akt in human alveolar macrophages resulting in nuclear accumulation and transcriptional activity of beta-catenin. J. Immunol. 166:4713-4720.
31. Patel, S., B. Doble, and J. R. Woodgett. 2004. Glycogen synthase kinase-3 in insulin and Wnt signalling: a double-edged sword? Biochem. Soc. Transact. 32:803-808.
32. Petit, V., B. Boyer, D. Lentz, C. E. Turner, J. P. Thiery, and A. M. Valles. 2000. Phosphorylation of tyrosine residues 31 and 118 on paxillin regulates cell migration through an association with CRK in NBT-II cells. J. Cell Biol. 148:957-970.
33. Qui, M. S., and S. H. Green. 1992. PC12 cell neuronal differentiation is associated with prolonged p21ras activity and consequent prolonged ERK activity. Neuron 9:705-717.
34. Schaller, M. D. 2001. Paxillin: a focal adhesion-associated adaptor protein. Oncogene 20:6459-6472.
35. Schaller, M. D., and J. T. Parsons. 1995. pp125FAK-dependent tyrosine phosphorylation of paxillin creates a high-affinity binding site for Crk. Mol. Cell. Biol. 15:2635-2645.
36. Schlaepfer, D. D., S. K. Hanks, T. Hunter, and P. van der Geer. 1994. Integrin-mediated signal transduction linked to Ras pathway by GRB2 binding to focal adhesion kinase. Nature 372:786-791.
37. Shen, Y., G. Schneider, J. F. Cloutier, A. Veillette, and M. D. Schaller. 1998. Direct association of protein-tyrosine phosphatase PTP-PEST with paxillin. J. Biol. Chem. 273:6474-6481.
38. Shi, L., R. Kishore, M. R. McMullen, and L. E. Nagy. 2002. Lipopolysaccharide stimulation of ERK1/2 increases TNF-alpha production via Egr-1. Am. J. Physiol. Cell Physiol. 282:C1205-C1211.
39. Thomas, J. W., M. A. Cooley, J. M. Broome, R. Salgia, J. D. Griffin, C. R. Lombardo, and M. D. Schaller. 1999. The role of focal adhesion kinase binding in the regulation of tyrosine phosphorylation of paxillin. J. Biol. Chem. 274:36684-36692.
40. Turner, C. E., and J. T. Miller. 1994. Primary sequence of paxillin contains putative SH2 and SH3 domain binding motifs and multiple LIM domains: identification of a vinculin and pp125Fak-binding region. J. Cell Sci. 107:1583-1591.
41. Williams, L. M., and A. J. Ridley. 2000. Lipopolysaccharide induces actin reorganization and tyrosine phosphorylation of Pyk2 and paxillin in monocytes and macrophages. J. Immunol. 164:2028-2036.
42. Woodrow, M. A., D. Woods, H. M. Cherwinski, D. Stokoe, and M. McMahon. 2003. Ras-induced serine phosphorylation of the focal adhesion protein paxillin is mediated by the Raf→MEK→ERK pathway. Exp. Cell Res. 287:325-338.
43. Yano, H., H. Uchida, T. Iwasaki, M. Mukai, H. Akedo, K. Nakamura, S. Hashimoto, and H. Sabe. 2000. Paxillin alpha and crk-associated substrate exert opposing effects on cell migration and contact inhibition of growth through tyrosine phosphorylation. Proc. Natl. Acad. Sci. USA 97:9076-9081.
44. Yoshimura, T., Y. Kawano, N. Arimura, S. Kawabata, A. Kikuchi, and K. Kaibuchi. 2005. GSK-3beta regulates phosphorylation of CRMP-2 and neuronal polarity. Cell 120:137-149.
45. Zhou, F. Q., and W. D. Snider. 2005. Cell biology. GSK-3beta and microtubule assembly in axons. Science 308:211-214.
46. Zhou, F. Q., J. Zhou, S. Dedhar, Y. H. Wu, and W. D. Snider. 2004. NGF-induced axon growth is mediated by localized inactivation of GSK-3beta and functions of the microtubule plus end binding protein APC. Neuron 42:897-912.