Evidence that atypical protein kinase C-λ and atypical protein kinase C-ζ participate in Ras-mediated reorganization of the F-actin cytoskeleton

Journal of Cell Biology

Volumn 144, Issue 3, 1999, Pages 413-425

  Überall, Florian ^a   Hellbert, Karina ^a   Kampfer, Sonja ^a   Maly, Karl ^a   Villunger, Andreas ^a   Spitaler, Martin ^a   Mwanjewe, James ^a   Baier Bitterlich, Gabriele ^a   Baier, Gottfried ^a   Grunicke, Hans H ^a  

^a UNIVERSITY OF INNSBRUCK   (Austria)

Author keywords

Atypical PKC; F actin; Ha Ras L61; PI3K; Rac 1

Indexed keywords

2 [1 (3 DIMETHYLAMINOPROPYL) 3 INDOLYL] 3 (3 INDOLYL)MALEIMIDE; 2 MORPHOLINO 8 PHENYLCHROMONE; F ACTIN; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE C; PROTEIN KINASE C INHIBITOR; WORTMANNIN;

ACTIN FILAMENT; ARTICLE; CELL ULTRASTRUCTURE; CONCENTRATION RESPONSE; CYTOSKELETON; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; ONCOGENE H RAS; PRIORITY JOURNAL; RNA SEQUENCE;

3T3 CELLS; ACTINS; ANIMALS; CYTOSKELETON; ENZYME INHIBITORS; INDOLES; ISOENZYMES; MALEIMIDES; MICE; MICROSCOPY, FLUORESCENCE; MUTATION; PROTEIN KINASE C; RAS PROTEINS; SIGNAL TRANSDUCTION; TRANSFECTION;

EID: 17744417743     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.144.3.413     Document Type: Article

References (69)

1. Aktories, K., S. Braun, S. Roesener, I. Just, and A. Hall. 1989. The rho gene product expressed in E. coli is a substrate for botulinum ADP-ribosyltransferase C3. Biochem. Biophys. Res. Commun. 158:209-213.
2. Arber, S., F.A. Barbayannis, H. Hanser, C. Schneider, C.A. Stanyon, O. Bernard, and P. Caroni. 1998. Regulation of actin dynamics through phosphorylation of cofilin by LIM-kinase. Nature. 393:805-809.
3. Baier-Bitterlich, G., F. Überall, B. Bauer, F. Fresser, H. Wachter, H. Grunicke, G. Utermann, A. Altman, and G. Baier. 1996. PKC-θ isoenzyme selective stimulation of the transcription factor complex AP-I in T-lymphocytes Mol. Cell. Biol. 16:1842-1850.
4. Bar-Sagi, D., and J.R. Feramisco. 1986. Induction of membrane ruffling and fluid-phase pinocytosis in quiescent fibroblasts by Ras proteins. Science. 233: 1061-1068.
5. Bjorkoy, G., M. Perander, A. Overvatn, and T. Johansen. 1997. Reversion of Ras- and phosphatidylcholine-hydrolyzing phospholipase C-mediated transformation of NIH 3T3 cells by a dominant interfering mutant of protein kinase C lambda is accompanied by the loss of constitutive nuclear mitogen-activated protein kinase/extracellular signal-regulated kinase activity. J. Biol. Chem. 272:11557-11565.
6. Boguski, M.S., R.C. Hardison, S. Schwartz, and W. Miller. 1992. Analysis of conserved domains and sequences motifs in cellular regulatory proteins and locus control regions using new software tools for multiple alignment and visualization. New Biol. 4:247-260.
7. Burridge, K., K. Fath, T. Kelly, G. Nuckolls, and C. Turner. 1988. Focal adhesions: transmembrane junctions between the extracellular matrix and the cytoskeleton. Annu. Rev. Cell Biol. 4:487-525.
8. Burridge, K., C.E. Turner, and L.H. Romer. 1992. Tyrosine phosphorylation of paxillin and pp125FAK accompanies cell adhesion to extracelluar matrix: role in cytoskeletal assembly. J. Cell Biol. 119:893-903.
9. Chang, J.H., S. Gill, J. Settleman, and S.J. Parsons. 1995. c-Src regulates the simultaneous rearrangement of actin cytoskeleton, p190RhoGAP, and p120RasGAP following epidermal growth factor stimulation. J. Cell Biol. 130:355-368.
10. Chant, J., and L. Stowers. 1995. GTPase cascades choreographing cellular behavior: movement, morphogenesis, and more. Cell. 81:1-4.
11. Chardin, P., P. Boquet, P. Maduale, M.R. Popoff, E.J. Rubin, and D.M. Gill. 1989. The mammalian G protein rhoC is ADP-ribosylated by Clostridium botulinum exoenzyme C3 and affects actin microfilaments in Vero cells. EMBO (Eur. Mol. Biol. Organ.) J. 8:1087-1092.
12. Chun, J.S., and B.S. Jacobson. 1992. Requirement for diacylglycerol and protein kinase C in HELA cell-substratum adhesion and their feedback amplification of arachidonic acid production for optimum cell spreading. Mol. Biol. Cell. 4:271-281.
13. Clark, E.A., and J.S. Brugge. 1995. Integrins and signal transduction pathways: the road taken. Science. 268:233-239.
14. Cubitt, A.B., R. Heim, S.R. Adams, A.E. Boyd, L.A. Gross, and R.Y. Tsien. 1995. Understanding, improving and using green fluorescent proteins. Trends Biochem. Sci. 20:448-455.
15. Dartsch, P.C., M. Ritter, D. Haussinger, and F. Lang. 1994. Cytoskeletal reorganization in NIH3T3 fibroblasts expressing the Ras oncogene. Eur. J. Cell Biol. 63:316-325.
16. Diaz-Meco, M.T., M.M. Municio, E. Berra, S. Frutos, L. Sanzo, and J. Moscat. 1994. Evidence for the in vitro and in vivo interaction of Ras with protein kinase zeta. J. Biol. Chem. 269:31706-31710.
17. Feig, L., and B. Schaffhausen. 1994. The hunt for Ras targets. Nature. 370:508-509.
18. Felice, G.R., P. Eason, M.V. Nermut, and S. Kellie. 1990. pp60src association with the cytoskeleton induces actin reorganization without affecting polymerization status. Eur. J. Cell Biol. 52:47-59.
19. Fincham, V.J., J.A. Wyke, and M.C. Frame. 1995. v-Src-induced degradation of focal adhesion kinase during morphological transformation of chicken embryo fibroblasts. Oncogene. 10:2247-2252.
20. Foster, R., K.Q. Hu, D.A. Shaywitz, and J. Settleman. 1994. p190 rhoGAP, the major rasGAP-associated protein, binds GTP directly. Mol. Cell. Biol. 14: 7173-7181.
21. Gomez, J., L. Rodriguez-Borlado, C. Martinez, A. Silva, M. Fresno, A.C. Carrera, C. Eicher-Streiber, and A. Rebello. 1997. IL-2 signaling controls actin reorganization through Rho-like protein family, phosphatidylinositol 3-kinase, and protein kinase C-zeta. J. Immunol. 158:1516-1522.
22. Guan, J.T., J.E. Trevithick, and R.O. Hynes. 1991. Fibronectin/integrin interaction induces tyrosine phosphorylation of a 120-kDa protein. Cell Regul. 2:951-964.
23. Guasch, R.M., P. Scambler, G.E. Jones, and A.J. Ridley. 1998. RhoE regulates actin cytoskeleton organization and cell migration. Mol. Cell. Biol. 18:4761-4771.
24. Hall, A. 1990. The cellular function of small GTP-binding proteins. Science. 249:635-640.
25. Hildebrand, J.D., M.D. Schaller, and J.T. Parsons. 1993. Identification of sequences required for the efficient localization of the focal adhesion kinase, pp125FAK, to cellular focal adhesions. J. Cell Biol. 23:993-1005.
26. Hiraoka, K., K. Kaibuchi, S. Ando, T. Musha, K. Takaishio, T. Mizuno, L. Menard, E. Tomhave, and J. Didsbury. 1992. Both stimulatory and inhibitory GDT/GTP exchange proteins, smg GDS and rho GDI, are active on multiple small GTP-binding proteins. Biochem. Biophys. Res. Commun. 182:921-930.
27. Horii, Y., J.F. Beeler, K. Sakaguchi, M. Tachibana, and T. Miki. 1994. A novel oncogene, ost, encodes a guanine nucleotide exchange factor that potentially links rho and rac signaling pathways. EMBO (Eur. Mol. Biol. Organ.) J. 13: 4776-4786.
28. Hynes, R.O. 1992. Integrins: versatility, modulation, and signaling in cell adhesion. Cell. 69:11-25.
29. Joneson, T., and D. Bar-Sagi. 1997. Ras effectors and their role in mitogenesis and oncogenesis. J. Mol. Med. 75:587-593.
30. Kampfer, S., K. Hellbert, A. Villunger, W. Doppler, G. Baier, H.H. Grunicke, and F. Überall. 1998. Transcriptional activation of c-fos by oncogenic Ha-Ras in mouse mammary epithelial cells requires the combined activities of PKC-λ, ε, and ζ. EMBO (Eur. Mol. Biol. Organ.) J. 17:4046-4055.
31. Kang, J.S., and R.S. Krauss. 1996. Ras induces anchorage-independent growth by subverting multiple adhesion regulated cell cycle events. Mol Cell. Biol. 16:3370-3380.
32. Keenan, C., and D. Kelleher. 1998. Protein kinase C and the cytoskeleton. Cell Signal. 10:225-232.
33. Khosravi-Far, R., P.A. Solski, G.J. Clark, M.S. Kinch, and C.J. Der. 1995. Activation of racl, rhoA. and mitogen-activated protein kinases is required for ras transformation. Mol. Cell. Biol. 15:6443-6453.
34. Kornberg, L., H.S. Earp, J.T. Parsons, M. Schaller, and R.L. Juliano. 1992. Cell adhesion or integrin clustering increases phosphorylation of a focal adhesion-associated tyrosine kinase. J. Biol. Chem. 267:23439-23442.
35. Kumar, C.C., C. Rogers-Prorock, J. Kelly, Z. Dong, J.-J. Lin, L. Armstrong, H.-F. Kung, M.J. Weber, and A. Afonso. 1995. SCH51344 inhibits Ras transformation by a novel mechanism. Cancer Res. 55:5106-5117.
36. Martiny-Baron, G., M.G. Kazanietz, H. Mischak, P.M. Blumberg, G. Kochs, H. Hug, D. Marme, and C. Schaechtele. 1993. Selective inhibition of protein kinase C isoenzymes by the indolocarbazole Goe 6976. J. Biol. Chem. 268: 9194-9197.
37. Mellström, K., C.H. Heldin, and B. Westermark. 1988. Induction of circular membrane ruffling on human fibroblasts by platelet-derived growth factor. Exp. Cell Res. 177:347-359.
38. Miki, T., C.L. Smith, J.E. Long, A. Eva, and T.P. Fleming. 1993. Oncogene ect-2 is related to regulators of small GTP-binding proteins. Nature. 362:462-465.
39. Mogi, A., M. Hatai, H. Soga, S. Takenoshita, Y. Nagamachi, J. Fujimoto, T. Yamamoto, J. Yokota, and Y. Yaoi. 1995. Possible role of protein kinase C in the regulation of intracellular stability of focal adhesion kinase in mouse 3T3 cells. FEBS (Fed. Eur. Biochem. Soc.) Lett. 373:135-140.
40. Morris, J.D.H., B. Price, A.C. Lloyd, A.J. Self, C.H. Marshall, and A. Hall. 1989. Scrape-loading of Swiss 3T3 cells with Ras protein rapidly activates protein kinase C in the absence of phosphoinositide hydrolysis. Oncogene. 4:27-31.
41. Nobes, C.D., and A. Hall. 1994. Regulation and function of the rho subfamily of small GTPases. Curr. Opin. Genet. Dev. 4:71-81.
42. Nobes, C.D., and A. Hall. 1995. Rho, rac. and cdc42 GTPase regulates the assembly of multimolecular focal complexes associated with actin stress fibres, lamellipodia, and filopodia. Cell. 81:53-62.
43. Nobes, C.D., I. Lauritzen, M.G. Mattei, A. Hall, and P. Chardin. 1998. A new member of the Rho family. Rndl. promotes disassembly of actin filament structures and loss of cell adhesion. J. Cell. Biol. 141:187-197.
44. Olson, M.F., H.F. Paterson, and C.J. Marshall. 1998. Signals from Ras and Rho GTPases interact to regulate expression of p21Waf1/Cip1. Nature. 394:295-299.
45. Paterson, H.F., A.J. Self, M.D. Garrett, I. Just, K. Aktories, and A. Hall. 1990. Microinjection of recombinant p21rho induces rapid changes in cell morphology. J. Cell Biol. 111:1001-1007.
46. Prendergast, G.C., and J.B. Gibbs. 1993. Pathways of Ras function: connections to the actin cytoskeleton. Adv. Cancer Res. 62:19-64.
47. Prendergast, G.C., R. Khosravi-Far, P.A. Solski, H. Kurzawa, P.F. Lebowitz, and C.J. Der. 1995. Critical role of Rho in cell transformation by oncogenic Ras. Oncogene. 10:2289-2296.
48. Qui, R.G., J. Chen, D. Kim, F. McCormick, and M. Symons. 1995a. An essential role for rac in Ras transformation. Nature. 374:457-459.
49. Qui, R.G., J. Chen, D. Kim, F. McCormick, and M. Symons. 1995b. A role of rho in Ras transformation. Proc. Natl. Acad. Sci. USA. 92:11781-11785.
50. Rankin, S., and E. Rozengurt. 1994. Platelet-derived growth factor modulation of focal adhesion kinase p125FAK and paxillin tyrosine phosphorylation in Swiss 3T3 cells. Bell-shaped dose response and cross-talk with bombesin. J. Biol. Chem. 269:704-710.
51. Ridley, A.J. 1995. Rho-related proteins: actin cytoskeleton and cell cycle. Curr. Opin. Genet. Dev. 5:24-30.
52. Ridley, A.J., H.F. Paterson, C.L. Johnston, D. Dickmann, and A. Hall. 1992. The small GTP-binding protein rac regulates growth factor-induced membrane ruffling. Cell. 70:401-410.
53. Ridley, A.J., and A. Hall. 1992. The small GTP-binding protein rho regulates the assembly of local adhesions and actin stress fibres in response to growth factors. Cell. 70:389-399.
54. Rodriguez-Viciana, P., P.H. Warne, R. Dhand, B. Vanhaesebroeck, I. Gout, M.J. Fry, M.D. Waterfield, and J. Downward. 1994. Phosphatidylinositol-3-OH kinase as a direct target of Ras. Nature. 370:527-532.
55. Rosales, C., V. O'Brien, L. Kornberg, and R. Juliano. 1995. Signal transduction by cell adhesion receptors. Biochem. Biophys. Acta. 1242:77-98.
56. Rosen, A., K.F. Keenan, M. Thelen, A.C. Nairn, and A. Aderem. 1990. Activation of protein kinase C results in the displacement of its myristoylaled, alanine-rich substrate from punctate structures in macrophage filopodia. J. Exp. Med. 92:1211-1215.
57. Rubin, E.J., D.M. Gill, P. Boquet, and M.R. Popoff. 1988. Functional modification of a 21 kDa G protein when ADP-ribosylated by exoenzyme C3 of Clostridium botulinum. Mol. Cell. Biol. 8:418-426.
58. Sahai, E., A.S. Alberts, and R. Treisman. 1998. RhoA effector mutants reveal distinct effector pathways for cytoskeletal reorganization, SRF activation and transformation. EMBO (Eur. Mol. Biol. Organ.) J. 17:1350-1361.
59. Schlaepler, D.D., K.C. Jones, and T. Hunter. 1998. Multiple Grb2-mediated integrin-stimulated signaling pathways to ERK2/mitogen-activated protein kinase: summation of both c-Src- and focal adhesion kinase-initiated tyrosine phosphorylation events. Mol. Cell. Biol. 18:2571-2585.
60. Schwartz, M.A., M.D. Schaller, and M.H. Ginsberg. 1995. Integrins: emerging paradigms of signal transduction. Annu. Rev. Cell. Dev. Biol. 11:549-599.
61. Settleman, J., C.F. Albright, L.C. Foster, and R.A. Weinberg. 1992. Association between GTPase activators for Rho and Ras families. Nature. 359:153-154.
62. Shinjo, K., J.G. Koland, M.J. Hart, V. Narasimhan, D.I. Johnson, T. Evans, and R.A. Cerione. 1990. Molecular cloning of the gene for the human placental GTP-binding protein Gp (G25K): identification of this GTP-binding protein as the human homolog of the yeast cell-division-cycle protein CDC42. Proc. Natl. Acad. Sci. USA. 87:9853-9857.
63. Smith-Sinnett, J., I. Zachary, A.M. Valverde, and E. Rozengurt. 1993. Bombesin stimulation of p125 focal adhesion kinase tyrosine phosphorylation. J. Biol. Chem. 268:14261-14268.
64. Toullee, D., P. Pianetti, H. Coste, P. Bellevergue, T. Grand-Perret, M. Ajakane, V. Baudet, P. Boissin, E. Brousier, F. Loriolle, L. Duhamel, D. Charon, and J. Kirilovsky. 1991. The bisindolylmaleimide GFX 109203 X is a potent and selective inhibitor of protein kinase C. J. Biol. Chem. 266:15771-15781.
65. Überall, F., S. Giselbrecht, K. Hellbert, F. Fresser, B. Bauer, M. Gschwendt, H.H. Grunicke, and G. Baier. 1997. Conventional PKC-α. novel PKC-ε and PKC-θ, but not atypical PKC-λ are MARCKS kinases in intact NIH3T3 fibroblasts. J. Biol. Chem. 272:4072-4078.
66. Vuori, K., and E. Ruoslathi. 1993. Activation of protein kinase C precedes α5β1 integrin-mediated cell spreading on fibronectin. J. Biol. Chem. 268:21459-21462.
67. Wu, C., V.M. Keivens, T.E. O'Toole, J.A. McDonald, and M.H. Ginsberg. 1995. Integrin activation and cytoskelelal interaction are essential for the assembly of fibronectin matrix. Cell. 83:715-724.
68. Yang, N., O. Higuchi, K. Ohasi, K. Nagata, A. Wada, K. Kangawa, E. Nishida, and K. Mizuno. 1998. Cofilin phosphorylation by LIM-kinase 1 and its role in Rac-mediated actin reorganization. Nature. 393:809-812.
69. Zachary, I., and E. Rozengurt. 1992. Focal adhesion kinase (p125FAK): a point of convergence in the action of neuropeptides, integrins and oncogenes. Cell. 71:891-894.