TNFα induces sequential activation of Cdc42- and p38/p53-dependent pathways that antagonistically regulate filopodia formation

Journal of Cell Science

Volumn 117, Issue 26, 2004, Pages 6355-6364

  Gadea, Gilles ^a   Roger, Lauréline ^a   Anguille, Christelle ^a   de Toledo, Marion ^a   Gire, Véronique ^a   Roux, Pierre ^a  

^a Centre National de la Recherche Scientifique   (France)

Author keywords

Cdc42; Filopodia; p38 kinase; p53; Phosphorylation; TNF

Indexed keywords

ACTIN; CYCLIN DEPENDENT KINASE INHIBITOR 1; DACTINOMYCIN; GUANOSINE TRIPHOSPHATASE; MITOGEN ACTIVATED PROTEIN KINASE P38; MUTANT PROTEIN; PROTEIN CDC42; PROTEIN P53; SERINE DERIVATIVE; TUMOR NECROSIS FACTOR; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL KINETICS; CELL MIGRATION; CELL STRUCTURE; CONTROLLED STUDY; DATA ANALYSIS; EMBRYO CELL; ENZYME ACTIVATION; ENZYME INDUCTION; ENZYME INHIBITION; FIBROBLAST; FILOPODIUM; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; PROTEIN TARGETING; REGULATORY MECHANISM; SIGNAL TRANSDUCTION; ANIMAL; CELL CULTURE; DRUG EFFECT; EMBRYO; KINETICS; METABOLISM; PHOSPHORYLATION; PHYSIOLOGY; PSEUDOPODIUM;

ANIMALIA;

ANIMALS; CDC42 GTP-BINDING PROTEIN; CELLS, CULTURED; EMBRYO; ENZYME ACTIVATION; FIBROBLASTS; KINETICS; MICE; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PSEUDOPODIA; TUMOR NECROSIS FACTOR-ALPHA; TUMOR SUPPRESSOR PROTEIN P53;

EID: 13444261035     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.01566     Document Type: Article

References (45)

1. Allen, W. E., Jones, G. E., Pollard, J. W. and Ridley, A. J. (1997). Rho, Rac and Cdc42 regulate actin organization and cell adhesion in macrophages. J. Cell Sci. 110, 707-720.
2. Ashcroft M., Kubbutat, M. H. and Vousden, K. H. (1999). Regulation of p53 function and stability by phosphorylation. Mol. Cell. Biol. 19, 1751-1758.
3. Aspenstrom, P., Lindberg, U. and Hall, A. (1996). Two GTPases, Cdc42 and Rac, bind directly to a protein implicated in the immunodeficiency disorder Wiskott-Aldrich syndrome. Curr. Biol. 6, 70-75.
4. Barak, Y., Lupo, A., Zauberman, A., Juven, T., Aloni-Grinstein, R., Gottlieb, E., Rutter, V. and Oren, M. (1994). Targets for transcriptional activation by wild-type p53: endogenous retroviral LTR, immunoglobulin-like promoter, and an internal promoter of the mdm2 gene. Cold Spring Harb. Symp. Quant. Biol. 59, 225-235.
5. Bulavin, D. V., Saito, S., Hollander, M. C., Sakaguchi, K., Anderson, C. W., Appella, E. and Fornace, A. J., Jr (1999). Phosphorylation of human p53 by p38 kinase coordinates N-terminal phosphorylation and apoptosis in response to UV radiation. EMBO J. 18, 6845-6854.
6. Coso, O. A., Chiariello, M., Yu, J. C., Teramoto, H., Crespo, P., Xu, N., Miki, T. and Gutkind, J. S. (1995). The small GTP-binding proteins Rac1 and Cdc42 regulate the activity of the JNK/SAPK signaling pathway. Cell 81, 1137-1146.
7. Dutartre, H., Davoust, J., Gorvel, J. P. and Chavrier, P. (1996). Cytokinesis arrest and redistribution of actin-cytoskeleton regulatory components in cells expressing the Rho GTPase CDC42Hs. J. Cell Sci. 109, 367-377.
8. Etienne-Manneville, S. and Hall, A. (2001). Integrin-mediated activation of Cdc42 controls cell polarity in migrating astrocytes through PKCzeta. Cell 106, 489-498.
9. Gadea, G., Lapasset, L., Gauthier-Rouviere, C. and Roux, P. (2002). Regulation of Cdc42-mediated morphological effects: a novel function for p53. EMBO J 21, 2373-2382.
10. Gauthier-Rouviere, C., Vignal, E., Meriane, M., Roux, P., Montcourier, P. and Fort, P. (1998). RhoG GTPase controls a pathway that independently activates Rac1 and Cdc42Hs. Mol. Biol. Cell 9 1379-1394.
11. Huang, C., Ma, W. Y., Maxiner, A., Sun, Y. and Dong, Z. (1999). p38 kinase mediates UV-induced phosphorylation of p53 protein at serine 389. J. Biol. Chem. 274, 12229-12235.
12. Kater, S. B. and Rehder, V. (1995). The sensory-motor role of growth cone filopodia. Curr. Opin. Neurobiol. 5, 68-74.
13. Keller, D., Zeng, X., Li, X., Kapoor, M., Iordanov, M. S., Taya, Y., Lozano, G., Magun, B. and Lu, H. (1999). The p38MAPK inhibitor SB203580 alleviates ultraviolet-induced phosphorylation at serine 389 but not serine 15 and activation of p53. Biochem. Biophys. Res. Commun. 261, 464-471.
14. Kim, S. J., Hwang, S. G., Shin, D. Y., Kang, S. S. and Chun, J. S. (2002). p38 kinase regulates nitric oxide-induced apoptosis of articular chondrocytes by accumulating p53 via NFkappa B-dependent transcription and stabilization by serine 15 phosphorylation. J. Biol. Chem. 277, 33501-33508.
15. Kishi, H., Nakagawa, K., Matsumoto, M., Suga, M., Ando, M., Taya, Y. and Yamaizumi, M. (2001). Osmotic shock induces G1 arrest through p53 phosphorylation at Ser33 by activated p38MAPK without phosphorylation at Ser15 and Ser20. J. Biol. Chem. 276, 39115-39122.
16. Kozma, R., Ahmed, S., Best, A. and Lim, L. (1995). The Ras-related protein Cdc42Hs and bradykinin promote formation of peripheral actin microspikes and filopodia in Swiss 3T3 fibroblasts. Mol. Cell. Biol. 15, 1942-1952.
17. Lakin, N. D. and Jackson, S. P. (1999). Regulation of p53 in response to DNA damage. Oncogene 18, 7644-7655.
18. Lambert, P. F., Kashanchi, F., Radonovich, M. E, Shiekhattar, R. and Brady, J. N. (1998). Phosphorylation of p53 serine 15 increases interaction with CBP. J. Biol. Chem. 273, 33048-33053.
19. Levine, A. J. (1997). p53, the cellular gatekeeper for growth and division. Cell 88, 323-331.
20. McClay, D. R. (1999). The role of thin filopodia in motility and morphogenesis. Exp. Cell Res. 253, 296-301.
21. McDermott, E. P. and O'Neill, L. A. (2002). Ras participates in the activation of p38 MAPK by interleukin-1 by associating with IRAK, IRAK2, TRAF6, and TAK-1. J. Biol. Chem. 277, 7808-7815.
22. Minden, A., Lin, A., Claret, F. X., Abo, A. and Karin, M. (1995). Selective activation of the JNK signaling cascade and c-Jun transcriptional activity by the small GTPases Rac and Cdc42Hs. Cell 81, 1147-1157.
23. Nobes, C. D. and Hall, A. (1995). Rho, rac, and cdc42 GTPases regulate the assembly of multimolecular focal complexes associated with actin stress fibers, lamellipodia, and filopodia. Cell 81, 53-62.
24. Nobes, C. D. and Hall, A. (1999). Rho GTPases control polarity, protrusion, and adhesion during cell movement. J. Cell Biol. 144, 1235-1244.
25. Oren, M. (1999). Regulation of the p53 tumor suppressor protein. J. Biol. Chem. 274, 36031-36034.
26. Ory, S., Munari-Silem, Y., Fort, P. and Jurdic, P. (2000). Rho and Rac exert antagonistic functions on spreading of macrophage-derived multinucleated cells and are not required for actin fiber formation. J. Cell Sci. 113, 1177-1188.
27. Peppelenbosch, M., Boone, E., Jones, G. E., van Deventer, S. J., Haegeman, G., Fiers, W., Grooten, J. and Ridley, A. J. (1999). Multiple signal transduction pathways regulate TNF-induced actin reorganization in macrophages: inhibition of Cdc42-mediated filopodium formation by TNF. J. Immunol. 162, 837-845.
28. Philips, A., Roux, P., Coulon, V., Bellanger, J. M., Vie, A., Vignais, M. L. and Blanchard, J. M. (2000). Differential effect of rac and cdc42 on p38 kinase activity and cell cycle progression of nonadherent primary mouse fibroblasts. J. Biol. Chem. 275, 5911-5917.
29. Postlethwaite, A. E. and Seyer, J. M. (1990). Stimulation of fibroblast chemotaxis by human recombinant tumor necrosis factor alpha (TNF-alpha) and a synthetic TNF-alpha 31-68 peptide. J. Exp. Med. 172, 1749-1756.
30. Prives, C. and Hall, P. A. (1999). The p53 pathway. J. Pathol. 187, 112-126.
31. Puls, A., Eliopoulos, A. G., Nobes, C. D., Bridges, T., Young, L. S. and Hall, A. (1999). Activation of the small GTPase Cdc42 by the inflammatory cytokines TNF(alpha) and IL-1, and by the Epstein-Barr virus transforming protein LMP1. J. Cell Sci. 112 2983-2992.
32. Ridley, A. J., Allen, W. E., Peppelenbosch, M. and Jones, G. E. (1999). Rho family proteins and cell migration. Biochem. Soc. Symp. 65, 111-123.
33. Rosen, E. M., Goldberg, I. D., Liu, D., Setter, E., Donovan, M. A., Bhargava, M., Reiss, M. and Kacinski, B. M. (1991). Tumor necrosis factor stimulates epithelial tumor cell motility. Cancer Res. 51, 5315-5321.
34. Roux, P., Gauthier-Rouviere, C., Doucet-Brutin, S. and Fort, P. (1997). The small GTPases Cdc42Hs, Rac1 and RhoG delineate Raf-independent pathways that cooperate to transform NIH3T3 cells. Curr. Biol. 7, 629-637.
35. Sanchez-Prieto, R., Rojas, J. M., Taya, Y. and Gutkind, J. S. (2000). A role for the p38 mitogen-acitvated protein kinase pathway in the transcriptional activation of p53 on genotoxic stress by chemotherapeutic agents. Cancer Res. 60, 2464-2472.
36. Sayed, M., Kim, S. O., Salh, B. S., Issinger, O. G. and Pelech, S. L. (2000). Stress-induced activation of protein kinase CK2 by direct interaction with p38 mitogen-activated protein kinase. J. Biol. Chem. 275, 16569-16573.
37. She, Q. B., Chen, N. and Dong, Z. (2000). ERKs and p38 kinase phosphorylate p53 protein at serine 15 in response to UV radiation. J. Biol. Chem. 275, 20444-20449.
38. Shieh, S. Y., Ikeda, M., Taya, Y. and Prives, C. (1997). DNA damage-induced phosphorylation of p53 alleviates inhibition by MDM2. Cell 91, 325-334.
39. Siliciano, J. D., Canman, C. E., Taya, Y., Sakaguchi, K., Appella, E. and Kastan, M. B. (1997). DNA damage induces phosphorylation of the amino terminus of p53. Genes Dev. 11, 3471-3481.
40. Sugihara, K., Asano, S., Tanaka, K., Iwamatsu, A., Okawa, K. and Ohta, Y. (2002). The exocyst complex binds the small GTPase Ra1A to mediate filopodia formation. Nat. Cell Biol. 4, 73-78.
41. Takekawa, M., Adachi, M., Nakahata, A., Nakayama, I., Rob, F., Tsukuda, H., Taya, Y. and Imai, K. (2000). p53-inducible wip1 phosphatase mediates a negative feedback regulation of p38 MAPK-p53 signaling in response to UV radiation. EMBO J. 19, 6517-6526.
42. Tibbetts, R. S., Brumbaugh, K. M., Williams, J. M., Sarkaria, J. N., Cliby, W. A., Shieh, S. Y., Taya, Y., Prives, C. and Abraham, R. T. (1999). A role for ATR in the DNA damage-induced phosphorylation of p53. Genes Dev. 13, 152-157.
43. Winston, B. W., Chan, E. D., Johnson, G. L. and Riches, D. W. (1997). Activation of p38mapk, MKK3, and MKK4 by TNF-alpha in mouse bone marrow-derived macrophages. J. Immunol. 159, 4491-4497.
44. Wojciak-Stothard, B., Entwistle, A., Garg, R. and Ridley, A. J. (1998). Regulation of TNF-alpha-induced reorganization of the actin cytoskeleton and cell-cell junctions by Rho, Rac, and Cdc42 in human endothelial cells. J. Cell Physiol. 176, 150-165.
45. Zugasti, O., Rul, W., Roux, P., Peyssonnaux, C., Eychene, A., Franke, T. F., Fort, P. and Hibner, U. (2001). Raf-MEK-Erk cascade in anoikis is controlled by Rac1 and Cdc42 via Akt. Mol. Cell. Biol. 21, 6706-6717.