Two co-existing mechanisms for nuclear import of MAP kinase: Passive diffusion of a monomer and active transport of a dimer

EMBO Journal

Volumn 18, Issue 19, 1999, Pages 5347-5358

  Adachi, Makoto ^a   Fukuda, Makoto ^a   Nishida, Eisuke ^a  

^a KYOTO UNIVERSITY   (Japan)

Author keywords

Nuclear translocation; Signal transduction; Tyrosine phosphorylation

Indexed keywords

BETA GALACTOSIDASE; HYBRID PROTEIN; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE KINASE; PROTEIN KINASE; TYROSINE; UNCLASSIFIED DRUG; WHEAT GERM AGGLUTININ;

ACTIVE TRANSPORT; ARTICLE; CELL NUCLEUS; CELL NUCLEUS MEMBRANE; CONTROLLED STUDY; CYTOPLASM; DIFFUSION; DIMERIZATION; ENZYME ACTIVATION; MOLECULAR WEIGHT; NONHUMAN; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN TRANSPORT; XENOPUS;

ANIMALS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; CELL LINE; CELL NUCLEUS; DIFFUSION; DIMERIZATION; DNA PRIMERS; FATTY ACIDS, UNSATURATED; MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; RECOMBINANT PROTEINS; TYROSINE; XENOPUS;

NES; TRITICUM AESTIVUM;

EID: 0033215340     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/18.19.5347     Document Type: Article

References (45)

1. Alessi, D.R., Smythe, C. and Keyse, S.M. (1993) The human CL100 gene encodes a Tyr/Thr-protein phosphatase which potently and specifically inactivates MAP kinase and suppresses its activation by oncogenic ras in Xenopus oocyte extracts. Oncogene, 8, 2015-2020.
2. Bardwell, L., Cook, J.G., Chang, E.C., Cairns, B.R. and Thorner, J. (1996) Signaling in the yeast pheromone response pathway: specific and high-affinity interaction of the mitogen-activated protein (MAP) kinases Kss1 and Fus3 with the upstream MAP kinase kinase Ste7. Mol. Cell. Biol., 16, 3637-3650.
3. Bischoff, F.R., Klebe C., Kretschmer, J., Wittinghofer, A. and Ponstingl, H. (1994) RanGAP1 induces GTPase activity of nuclear Ras-related Ran. Proc. Natl Acad. Sci. USA, 91, 2587-2591.
4. Blenis, J. (1993) Signal transduction via the MAP kinase: proceed at your own RSK. Proc. Natl Acad. Sci. USA, 90, 5889-5892.
5. 1-specific gene transcription and S-phase entry in fibloblasts. Oncogene, 10, 1895-1904.
6. 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.
7. Canagarajah, B.J., Khokhlatchev, A., Cobb, M.H. and Goldsmith, E.J. (1997) Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell, 90, 859-869.
8. 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.
9. Davis, R.J. (1993) The mitogen-activated protein kinase signal transduction pathway. J. Biol. Chem., 268, 14553-14556.
10. Dickmanns, A., Bischoff, F.R., Marshallsay, C., Lührmann, R., Ponstingl, H. and Fanning, E. (1996) The thermolability of nuclear protein import in tsBN2 cells is suppressed by microinjected Ran-GTP or Ran-GDP, but not by RanQ69L or RanT24N. J. Cell Sci., 109, 1449-1457.
11. Finlay, D.R., Newmeyer, D.D., Price, J.M. and Forbes, D.J. (1987) Inhibition of in vitro nuclear transport by a lectin that binds to nuclear pores. J. Cell Biol. 104, 189-200.
12. Fischer, U., Huber, J. Boelens, W.C., Mattaj, I.W. and Lührmann, R. (1995) The HIV-1 Rev activation domain is a nuclear export signal that accesses an export pathway used by specific cellular RNAs. Cell, 82, 475-483.
13. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell, 90, 1051-1060.
14. Fukuda, M., Gotoh, I., Gotoh, Y. and Nishida, E. (1996) Cytoplasmic localization of MAP kinase kinase directed by its N-terminal, leucinerich short amino acid sequence, which acts as a nuclear export signal. J. Biol. Chem., 271, 20024-20028.
15. Fukuda, M., Gotoh, Y. and Nishida, E. (1997a) 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.
16. Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M. and Nishida, E. (1997b) CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature, 390, 308-311.
17. Fukuda, M., Gotoh, I., Adachi, M., Gotoh, Y. and Nishida, E. (1997c) A novel regulatory mechanism in the mitogen-activated protein (MAP) kinase cascade. J. Biol. Chem., 272, 32642-32648.
18. Gaits, F., Degols, G., Shiozaki, K. and Russel, P. (1998) Phosphorylation and association with the transcription factor Atf1 regulate localization of Spc1/Sty1 stress-activated kinase in fission yeast. Genes Dev., 12, 1464-1473.
19. Gonzalez, F.A., Seth, A., Raden, D.L., Bowman, D.S., Fay, F.S. and Davis, R.J. (1993) Serum-induced translocation of mitogen-activated protein kinase to the cell surface ruffling membrane and the nucleus. J. Cell Biol., 122, 1089-1101.
20. Gotoh, Y., Matsuda, S., Takenaka, K., Hattori, S., Iwamatsu, A., Ishikawa, M. Kosako, H. and Nishida, E. (1994) Characterization of recombinant Xenopus MAP kinase kinases mutated at potential phosphorylation sites. Oncogene, 9, 1891-1898.
21. mapk by MAP kinase kinase. FEBS Lett., 306, 17-22.
22. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I.W. and Gorlich, D. (1997) The asymmetric distribution of the constituents of the Ran system is essential for transport into and out of the nucleus. EMBO J., 16, 6535-6547.
23. 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.
24. Klebe, C., Bischoff, F.R., Ponstingl, H. and Wittinghofer, A. (1995) Interaction of the nuclear GTP-binding protein Ran with its regulatory proteins RCC1 and RanGAP1. Biochemistry, 34, 639-647.
25. Kunkel, T.A., Roberts, J.D. and Zakour, R.A. (1987) Rapid and efficient site-specific mutagenesis without phenotypic selection. Methods Enzymol., 154, 367-382.
26. mapkk) in fibroblasts. J. Cell Biol., 122, 1079-1088.
27. 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.
28. Lewis, T.S., Shapiro, P.S. and Ahn, N.G. (1998) Signal transduction through MAP kinase cascades. Adv. Cancer Res., 74, 49-139.
29. Marshall, C.J. (1994) MAP kinase kinase kinase, MAP kinase kinase and MAP kinase. Curr. Opin. Genet. Dev., 4, 82-89.
30. Moriguchi, T., Gotoh, Y. and Nishida, E. (1995) Activation of two isoforms of mitogen-activated protein kinase kinase in response to epidermal growth factor and nerve growth factor. Eur. J. Biochem., 234, 32-38.
31. Muda, M., Boschert, U., Dickinson, R., Martinou, J.-C., Martinou, I., Camps, M., Schlegel, W. and Arkinstall, S. (1996) MKP-3, a novel cytosolic protein-tyrosine phosphatase that exemplifies a new class of mitogen-activated protein kinase phosphatase. J. Biol. Chem., 271, 4319-4326.
32. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
33. Nishida, E. and Gotoh, Y. (1993) The MAP kinase cascade is essential for diverse signal transduction pathways. Trends Biochem. Sci., 18, 128-131.
34. Ossareh-Nazari, B., Bachelerie, F. and Dargemont, C. (1997) Evidence for a role of CRM1 in signal-mediated nuclear protein export. Science, 278, 141-144.
35. Palacios, I., Weis, K., Klebe, C. and Dingwall, C. (1996) Ran/TC4 mutants identify a common requirement for snRNP and protein import into the nucleus. J. Cell Biol., 133, 485-494.
36. Payne, D.M., Rossomando, A.J., Martino, P., Erickson, A.K., Her, J.-H., Shabanowitz, J., Hunt, D.F., Weber, M.J. and Sturgill, T.W. (1991) Identification of the regulatory phosphorylation sites in p42/mitogen-activated protein kinase (MAP kinase). EMBO J., 10, 885-892.
37. Pritchard, C.A., Samuels, M.L., Bosch, E. and McMahon, M. (1995) Conditionally oncogenic forms of the A-Raf and B-Raf protein kinases display different biological and biochemical properties in NIH 3T3 cells. Mol. Cell. Biol., 15, 6430-6442.
38. Ren, M., Drivas, G., D'Eustachio, P. and Rush, M.G. (1993) Ran/TC4: a small nuclear GTP-binding protein that regulates DNA synthesis. J. Cell Biol., 120, 313-323.
39. Robinson, M.J. and Cobb, M.H. (1997) Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol., 9, 180-186.
40. Schaeffer, H.J., Catling, A.D., Eblen, S.T., Collier, L.S., Krauss, A. and Weber, M.J. (1998) MPI: A MEK binding partner that enhances enzymatic activation of the MAP kinase cascade. Science, 281, 1668-1671.
41. Sturgill, T.W. and Wu, J. (1991) Recent progress in characterization of protein kinase cascade for phosphorylation of ribosomal protein S6. Biochim. Biophys. Acta, 1092, 350-357.
42. Thomas, G. (1992) MAP kinase by any other name smells just as sweet. Cell, 68, 1-4.
43. Wolff, B., Sanglier, J.J. and Wang, Y. (1997) Leptomycin B is an inhibitor of nucler export: inhibition of nucleo-cytoplasmic translocation of the human immunodeficiency virus type 1 (HIV-1) Rev protein and Rev-dependent mRNA. Chem. Biol., 4, 139-147.
44. Yoneda, Y., Imamoto-Sonobe, N., Yamaizumi, M. and Uchida, T. (1987) Reversible inhibition of protein import into the nucleus by wheat germ agglutinin injected into cultured cells. Exp. Cell Res., 173, 586-595.
45. Zheng, C.-F. and Guan, K.L. (1994) Cytoplasmic localization of the mitogen-activated protein kinase activator MEK. J. Biol. Chem., 269, 19947-19952.