Dynamic regulation of ERK2 nuclear translocation and mobility in living cells

Journal of Cell Science

Volumn 119, Issue 23, 2006, Pages 4952-4963

  Costa, Mario ^a   Marchi, Matilde ^b,c   Cardarelli, Francesco ^b,c   Roy, Anusrhee ^b   Beltram, Fabio ^b   Maffel, Lamberto ^a   Ratto, Glan Michele ^a  

^a CNR   (Italy)

^b SCUOLA NORMALE SUPERIORE   (Italy)

^c INDIAN INSTITUTE OF TECHNOLOGY   (India)

Author keywords

Kinase; MAP kinase; Nuclear transport; Phosphatase; Phosphorylation; Signal transduction

Indexed keywords

FLUORESCENT DYE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PHOSPHATASE;

ARTICLE; CELL NUCLEUS; COMPLEX FORMATION; CONTROLLED STUDY; DIFFUSION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FIBROBLAST; HUMAN; HUMAN CELL; IMAGING; NUCLEOCYTOPLASMIC TRANSPORT; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN TRANSPORT; QUANTITATIVE ANALYSIS; REGULATORY MECHANISM;

ACTIVE TRANSPORT, CELL NUCLEUS; ANIMALS; CELL NUCLEUS; ENZYME ACTIVATION; FLUORESCENCE RECOVERY AFTER PHOTOBLEACHING; GREEN FLUORESCENT PROTEINS; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; NIH 3T3 CELLS; NUCLEAR ENVELOPE; PHOSPHORYLATION; RECOMBINANT PROTEINS; SIGNAL TRANSDUCTION;

EID: 33845886924     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: 10.1242/jcs.03272     Document Type: Article

References (51)

1. Adachi, M., Fukuda, M. and Nishida, E. (1999). Two co-existing mechanisms for nuclear import of MAP kinase: passive diffusion of a monomer and active transport of a dimer. EMBO J. 18, 5347-5358.
2. Adachi, M., Fukuda, M. and Nishida, E. (2000). Nuclear export of MAP kinase (ERK) involves a MAP kinase kinase (MEK)-dependent active transport mechanism. J. Cell Biol. 148, 849-856.
3. Ando, R., Mizuno, H. and Miyawaki, A. (2004). Regulated fast nucleocytoplasmic shuttling observed by reversible protein highlighting. Science 306, 1370-1373.
4. Axelrod, D., Koppel, D. E., Schlessinger, J., Elson, E. and Webb, W. W. (1976). Mobility measurement by analysis of fluorescence photobleaching recovery kinetics. Biophys. J. 16, 1055-1069.
5. Bednenko, J., Cingolani, G. and Gerace, L. (2003). Nucleocytoplasmic transport: navigating the channel. Traffic 4, 127-135.
6. Bhalla, U. S. and Iyengar, R. (1999). Emergent properties of networks of biological signaling pathways. Science 283, 381-387.
7. Bhalla, U. S., Ram, P. T. and Iyengar, R. (2002). MAP kinase phosphatase as a locus of flexibility in a mitogen-activated protein kinase signaling network. Science 297, 1018-1023.
8. Brondello, J. M., McKenzie, F. R., Sun, H., Tonks, N. K. and Pouyssegur, J. (1995). Constitutive MAP kinase phosphatase (MKP-1) expression blocks G1 specific gene transcription and S-phase entry in fibroblasts. Oncogene 10, 1895-1904.
9. Brondello, J. M., Brunet, A., Pouyssegur, J. and McKenzie, F. R. (1997). The dual specificity mitogen-activated protein kinase phosphatase-1 and -2 are induced by the p42/p44MAPK cascade. J. Biol. Chem. 272, 1368-1376.
10. Brondello, J. M., Pouyssegur, J. and McKenzie, F. R. (1999). Reduced MAP kinase phosphatase-1 degradation after p42/p44MAPK-dependent phosphorylation. Science 286, 2514-2517.
11. Brunet, A., Roux, D., Lenormand, P., Dowd, S., Keyse, S. and Pouyssegur, J. (1999). Nuclear translocation of p42/p44 mitogen-activated protein kinase is required for growth factor-induced gene expression and cell cycle entry. EMBO J. 18, 664-674.
12. Burack, W. R. and Shaw, A. S. (2005). Live cell imaging of ERK and MEK: simple binding equilibrium explains the regulated nucleocytoplasmic distribution of ERK. J. Biol. Chem. 280, 3832-3837.
13. Camps, M., Nichols, A. and Arkinstall, S. (2000). Dual specificity phosphatases: a gene family for control of MAP kinase function. FASEB J. 14, 6-16.
14. Carrero, G., McDonald, D., Crawford, E., de Vries, G. and Hendzel, M. J. (2003). Using FRAP and mathematical modeling to determine the in vivo kinetics of nuclear proteins. Methods 29, 14-28.
15. Chen, R. H., Sarnecki, C. and Blenis, J. (1992). Nuclear localization and regulation of erk- and rsk-encoded protein kinases. Mol. Cell. Biol. 12, 915-927.
16. Chen, Y., Muller, J. D., Ruan, Q. and Gratton, E. (2002). Molecular brightness characterization of EGFP in vivo by fluorescence fluctuation spectroscopy. Biophys. J. 82, 133-144.
17. Chuderland, D. and Seger, R. (2005). Protein-protein interactions in the regulation of the extracellular signal-regulated kinase. Mal. Biotechnol. 29, 57-74.
18. Cowley, S., Paterson, H., Kemp, P. and Marshall, C. J. (1994). Activation of MAP kinase kinase is necessary and sufficient for PC12 differentiation and for transformation of NIH 3T3 cells. Cell 77, 841-852.
19. English, J. M. and Cobb, M. H. (2002). Pharmacological inhibitors of MAPK pathways. Trends Pharmacol. Sci. 23, 40-45.
20. Feder, T. J., Brust-Mascher, L, Slattery, J. P., Baird, B. and Webb, W. W. (1996). Constrained diffusion or immobile fraction on cell surfaces: a new interpretation. Biophys. J 70, 2767-2773.
21. Ferrell, J. E., Jr (1996). Tripping the switch fantastic: how a protein kinase cascade can convert graded inputs into switch-like outputs. Trends Biochem. Sci. 21, 460-466.
22. Fukuda, M., Gotoh, I., Adachi, M., Gotoh, Y. and Nishida, E. (1997a). A novel regulatory mechanism in the mitogen-activated protein (MAP) kinase cascade. Role of nuclear export signal of MAP kinase kinase. J. Biol. Chem. 272, 32642-32648.
23. Fukuda, M., Gotoh, Y. and Nishida, E. (1997b). Interaction of MAP kinase with MAP kinase kinase: its possible role in the control of nucleocytoplasmic transport of MAP kinase. EMBO J. 16, 1901-1908.
24. Horgan, A. M. and Stork, P. J. (2003). Examining the mechanism of Erk nuclear translocation using green fluorescent protein. Exp. Cell Res. 285, 208-220.
25. Houtsmuller, A. B., Rademakers, S., Nigg, A. L., Hoogstraten, D., Hoeijmakers, J. H. and Vermeulen, W. (1999). Action of DNA repair endonuclease ERCC1/XPF in living cells. Science 284, 958-961.
26. Jacobs, D., Glossip, D., Xing, H., Muslin, A. J. and Kornfeld, K. (1999). Multiple docking sites on substrate proteins form a modular system that mediates recognition by ERK MAP kinase. Genes Dev. 13, 163-175.
27. Khokhlatchev, A. V., Canagarajah, B., Wilsbacher, J., Robinson, M., Atkinson, M., Goldsmith, E. and Cobb, M. H. (1998). Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation. Cell 93, 605-615.
28. Kim, K., Nose, K. and Shibanuma, M. (2000). Significance of nuclear relocalization of ERK1/2 in reactivation of c-fos transcription and DNA synthesis in senescent fibroblasts. J. Biol. Chem. 275, 20685-20692.
29. Koster, M., Frahm, T. and Hauser, H. (2005). Nucleocytoplasmic shuttling revealed by FRAP and FLIP technologies. Curr. Opin. Biotechnol. 16, 28-34.
30. Kudo, N., Taoka, H., Toda, T., Yoshida, M. and Horinouchi, S. (1999). A novel nuclear export signal sensitive to oxidative stress in the fission yeast transcription factor Pap1. J. Biol. Chem. 274, 15151-15158.
31. Lenormand, P., Sardet, C., Pages, G., L'Allemain, G., Brunet, A. and Pouyssegur, J. (1993). Growth factors induce nuclear translocation of MAP kinases (p42mapk and p44mapk) but not of their activator MAP kinase kinase (p45mapkk) in fibroblasts. J. Cell Biol. 122, 1079-1088.
32. Lenormand, P., Brondello, J. M., Brunet, A. and Pouyssegur, J. (1998). Growth factor-induced p42/p44 MAPK nuclear translocation and retention requires both MAPK activation and neosynthesis of nuclear anchoring proteins. J. Cell Biol. 142, 625-633.
33. Lippincott-Schwartz, J., Snapp, E. and Kenworthy, A. (2001). Studying protein dynamics in living cells. Nat. Rev. Mol. Cell Biol. 2, 444-456.
34. Matsubayashi, Y., Fukuda, M. and Nishida, E. (2001). Evidence for existence of a nuclear pore complex-mediated, cytosol-independent pathway of nuclear translocation of ERK MAP kinase in permeabilized cells. J. Biol. Chem. 276, 41755-41760.
35. Murphy, L. O., Smith, S., Chen, R. H., Fingar, D. C. and Blenis, J. (2002). Molecular interpretation of ERK signal duration by immediate early gene products. Nat. Cell Biol. 4, 556-564.
36. Murphy, L. O., MacKeigan, J. P. and Blenis, J. (2004). A network of immediate early gene products propagates subtle differences in mitogen-activated protein kinase signal amplitude and duration. Mol. Cell. Biol. 24, 144-153.
37. Paine, P. L., Moore, L. C. and Horowitz, S. B. (1975). Nuclear envelope permeability. Nature 254, 109-114.
38. Phair, R. D. and Misteli, T. (2000). High mobility of proteins in the mammalian cell nucleus. Nature 404, 604-609.
39. Pouyssegur, J., Volmat, V. and Lenormand, P. (2002). Fidelity and spatio-temporal control in MAP kinase (ERKs) signalling. Biochem. Pharmacol. 64, 755-763.
40. Robinson, M. J. and Cobb, M. H. (1997). Mitogen-activated protein kinase pathways. Curr Opin. Cell Biol. 9, 180-186.
41. Robinson, M. J., Stippec, S. A., Goldsmith, E., White, M. A. and Cobb, M. H. (1998). A constitutively active and nuclear form of the MAP kinase ERK2 is sufficient for neurite outgrowth and cell transformation. Curr Biol. 8, 1141-1150.
42. Roux, P. P. and Bienis, J. (2004). ERK and p38 MAPK-activated protein kinases: a family of protein kinases with diverse biological functions. Microbiol. Mol. Biol. Rev. 68, 320-344.
43. Rubinfeld, H., Hanoch, T. and Seger, R. (1999). Identification of a cytoplasmic-retention ] sequence in ERK2. J. Biol. Chem. 274, 30349-30352.
44. Schramek, H., Schumacher, M. and Pfaller, W. (1996). Sustained ERK-2 activation in rat glomerular mesangial cells: differential regulation by protein phosphatases. Am. J. Physiol. 271, F423-432.
45. Seksek, O., Biwersi, J. and Verkman, A. S. (1997). Translational diffusion of macromolecule-sized solutes in cytoplasm and nucleus. J Cell Biol. 138, 131-142.
46. Traverse, S., Gomez, N., Paterson, H., Marshall, C. and Cohen, P. (1992). Sustained activation of the mitogen-activated protein (MAP) kinase cascade may be required for differentiation of PC12 cells. Comparison of the effects of nerve growth factor and epidermal growth factor. Biochem. J. 288, 351-355.
47. Vantaggiato, C., Formentini, I., Bondanza, A., Bonini, C., Naldini, L. and Brambilla, R. (2006). ERK1 and ERK2 mitogen-activated protein kinases affect Ras-dependent cell signaling differentially. J Biol. 5, 14.
48. Volmat, V., Camps, M., Arkinstall, S., Pouyssegur, J. and Lenormand, P. (2001). The nucleus, a site for signal termination by sequestration and inactivation of p42/p44 MAP kinases. J Cell Sci. 114, 3433-3443.
49. Whitehurst, A. W., Wilsbacher, J. L., You, Y., Luby-Phelps, K., Moore, M. S. and Cobb, M. H. (2002). ERK2 enters the nucleus by a carrier-independent mechanism. Proc. Natl. Acad. Sci. USA 99, 7496-7501.
50. Xu, L. and Massague, J. (2004). Nucleocytoplasmic shuttling of signal transducers. Nat. Rev. Mol. Cell Biol. 5, 209-219.
51. Yokoe, H. and Meyer, T. (1996). Spatial dynamics of GFP-tagged proteins investigated by local fluorescence enhancement. Nat. Biotechnol. 14, 1252-1256.