Leptomycin B-sensitive nuclear export of MAPKAP kinase 2 is regulated by phosphorylation

EMBO Journal

Volumn 17, Issue 12, 1998, Pages 3363-3371

  Engel, Katrin ^a   Kotlyarov, Alexey ^a   Gaestel, Matthias ^b  

^a MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^b MARTIN LUTHER UNIVERSITY HALLE WITTENBERG   (Germany)

Author keywords

Nuclear export; Nuclear import; Protein phosphorylation; Signal transduction; Stress response

Indexed keywords

4 (4 FLUOROPHENYL) 2 (4 METHYLSULFINYLPHENYL) 5 (4 PYRIDYL)IMIDAZOLE; CARRIER PROTEIN; GREEN FLUORESCENT PROTEIN; LEPTOMYCIN B; MITOGEN ACTIVATED PROTEIN KINASE;

AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; GENETIC TRANSFECTION; MOLECULAR MIMICRY; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION;

3T3 CELLS; ADENOSINE TRIPHOSPHATE; ANIMALS; ANTIBIOTICS, ANTINEOPLASTIC; BIOLOGICAL TRANSPORT; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CELL NUCLEUS; CYTOPLASM; ENZYME ACTIVATION; FATTY ACIDS, UNSATURATED; MICE; MITOGEN-ACTIVATED PROTEIN KINASES; MOLECULAR MIMICRY; PHOSPHORYLATION; PROTEIN-SERINE-THREONINE KINASES; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; STRESS; TRANSFECTION;

ANIMALIA; NES;

EID: 0032526988     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1093/emboj/17.12.3363     Document Type: Article

References (47)

1. Ben-Levy, R., Leighton, I.A., Doza, Y.N., Attwood, P., Morrice, N., Marshall, C.J. and Cohen, P. (1995) Identification of novel phosphorylation sites required for activation of MAPKAP kinase-2. EMBO J., 14, 5920-5930.
2. Bogerd, H.P., Fridell, R.A., Benson, R.E., Hua, J. and Cullen, B.R. (1996) Protein sequence requirements for function of the human T-cell leukemia virus type 1 Rex nuclear export signal delineated by a novel in vivo randomization-selection assay. Mol. Cell. Biol., 16, 4207-4214.
3. Brewster, J.L., de Valoir, T., Dwyer, N.D., Winter, E. and Gustin, M.C. (1993) An osmosensing signal transduction pathway in yeast. Science, 259, 1760-1763.
4. Brunet, A. and Pouyssegur, J. (1996) Identification of MAP kinase domains by redirecting stress signals into growth factor responses. Science, 272, 1652-1655.
5. Cano, E., Doza, Y.N., Ben-Levy, R., Cohen P. and Mahadevan, L.C. (1996) Identification of anisomycin-activated kinases p45 and p55 in murine cells as MAPKAP kinase-2. Oncogene, 12, 805-812.
6. 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.
7. Clifton, A.D., Young, P.R. and Cohen, P. (1996) A comparison of the substrate specificity of MAPKAP kinase-2 and MAPKAP kinase-3 and their activation by cytokines and cellular stress. FEBS Lett., 392, 209-214.
8. Cuenda, A., Rouse, J., Doza, Y.N., Meier, R., Cohen, P., Gallagher, T.F., Young, P.R. and Lee, J.C. (1995) SB 203580 is a specific inhibitor of a MAP kinase homologue which is stimulated by cellular stresses and interleukin-1. FEBS Lett., 364, 229-233.
9. Dickens, M., Rogers, J.S., Cavanagh, J., Raitano, A., Xia, Z., Halpern, J.R., Greenberg, M.E., Sawyers, C.L. and Davis, R.J. (1997) A cytoplasmic inhibitor of the JNK signal transduction pathway. Science, 277, 693-696.
10. Engel, K., Plath, K. and Gaestel, M. (1993) The MAP kinase-activated protein kinase 2 contains a proline-rich SH3-binding domain. FEBS Lett., 336, 143-147.
11. Engel, K., Schultz, H., Martin, F., Kotlyarov, A., Plath, K. Hahn, M., Heinemann, U. and Gaestel, M. (1995) Constitutive activation of mitogen-activated protein kinase-activated protein kinase 2 by mutation of phosphorylation sites and an A-helix motif. J. Biol. Chem., 270, 7213-7221.
12. Faux, M.C. and Scott, J.D. (1996) Molecular glue: kinase anchoring and scaffold proteins. Cell, 85, 9-12.
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. Freshney, N.W., Rawlinson, L., Guesdon, F., Jones, E., Cowley, S., Hsuan, J. and Saklatvala, J. (1994) Interleukin-1 activates a novel protein kinase cascade that results in the phosphorylation of Hsp27. Cell, 78, 1039-1049.
15. Fridell, RA., Partin, K.M., Carpenter, S. and Cullen, B.R. (1993) Identification of the activation domain of equine infectious anemia virus rev. J. Virol., 67, 7317-7323.
16. 2-terminal, leucine-rich short amino acid sequence, which acts as a nuclear export signal. J. Biol. Chem., 271, 20024-20028.
17. 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.
18. 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.
19. Fukuda, M., Gotoh, I., Adachi, M., Gotoh, Y. and Nishida, E. (1997c) A novel regulatory mechanism in the mitogen-activated protein kinase cascade. Role of the nuclear export signal of MAP kinase kinase. J. Biol. Chem., 272, 32642-32648.
20. Hubbard, M.J. and Cohen, P. (1993) On target with a new mechanism for the regulation of protein phosphorylation. Trends Biochem. Sci., 18, 172-177.
21. Hunter, T. and Plowman, G.D. (1997) The protein kinases of budding yeast: six score and more. Trends Biochem. Sci., 22, 18-22.
22. Izaurralde, E., Kutay, U., von Kobbe, C., Mattaj, I. and Görlich, 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. Jaaro, H., Rubinfeld, H., Hanoch, T. and Seger, R. (1997) Nuclear translocation of mitogen-activated protein kinase kinase (MEK1) in response to mitogenic stimulation. Proc. Natl Acad. Sci. USA, 94, 3742-3747.
24. Karin, M. and Hunter, T. (1995) Transcriptional control by protein phosphorylation: signal transmission from the cell surface to the nucleus. Curr. Biol., 5, 747-757.
25. Laskey, R.A. and Dingwall, C. (1993) Nuclear shuttling: the default pathway for nuclear proteins? Cell, 74, 385-386.
26. Lee, J.C. et al. (1994) A protein kinase involved in the regulation of inflammatory cytokine biosynthesis. Nature, 372, 739-746.
27. 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.
28. Ludwig, S., Engel, K., Hoffmeyer, A., Sithanandam, G., Neufeld, B., Palm, D., Gaestel, M. and Rapp, U.R. (1996) 3pK, a novel mitogen-activated protein (MAP) kinase-activated protein kinase, is targeted by three MAP kinase pathways. Mol. Cell. Biol., 16, 6687-6697.
29. Mancuso, V.A., Hope, T.J., Zhu, L., Derse, D., Phillips, T. and Parslow, T.G. (1994) Posttranscriptional effector domains in the Rev proteins of feline immunodeficiency virus and equine infectious anemia virus. J. Virol., 68, 1998-2001.
30. McLaughlin, M.M., Kumar, S., McDonnell, P.C., Van-Horn, S., Lee, J.C., Livi, G.P. and Young, P.R. (1996) Identification of mitogen-activated protein (MAP) kinase-activated protein kinase-3, a novel substrate of CSBP p38 MAP kinase. J. Biol. Chem., 271, 8488-8492.
31. Murphy, R, and Wente, S.R, (1996) An RNA-export mediator with an essential nuclear export signal. Nature, 383, 357-360.
32. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature, 386, 779-787.
33. 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.
34. Raingeaud, J., Gupta, S., Rogers, J.S., Dickens, M., Han, J., Ulevitch, R.J. and Davis, R.J. (1995) Pro-inflammatory cytokines and environmental stress cause p38 mitogen-activated protein kinase activation by dual phosphorylation on tyrosine and threonine. J. Biol. Chem., 270, 7420-7426.
35. Read, M.A., Whitley, M.Z., Gupta, S., Pierce, J.W., Best, J., Davis, R.J. and Collins, T. (1997) Tumor necrosis factor alpha-induced E-selectin expression is activated by the nuclear factor-kappaB and c-JUN N-terminal kinase/p38 mitogen-activated protein kinase pathways. J. Biol. Chem., 272, 2753-2761.
36. Rouse, J., Cohen, P., Trigon, S., Morange, M., Alonso-Llamazares, A., Zamanillo, D., Hunt, T. and Nebreda, A.R. (1994) A novel kinase cascade triggered by stress and heat shock that stimulates MAPKAP kinase-2 and phosphorylation of the small heat shock proteins. Cell, 78, 1027-1037.
37. Schultz, H., Engel, K. and Gaestel, M. (1997) PMA-induced activation of the p42/44ERK- and p38RK-MAP kinase cascades in HL-60 cells is PKC dependent but not essential for differentiation to the macrophage-like phenotype. J. Cell. Physiol., 173, 310-318.
38. Sithanandam, G. et al. (1996) 3pK, a new mitogen-activated protein kinase-activated protein kinase located in the small cell lung cancer tumor suppressor gene region. Mol. Cell. Biol., 16, 868-876.
39. Stade, K., Ford, C.S., Guthrie, C. and Weis, K. (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell, 90, 1041-1050.
40. Stokoe, D., Engel, K., Campbell, D.G., Cohen, P. and Gaestel, M. (1992a) Identification of MAPKAP kinase 2 as a major enzyme responsible for the phosphorylation of the small mammalian heat shock proteins. FEBS Lett., 313, 307-313.
41. Stokoe, D., Campbell, D.G., Nakielny, S., Hidaka, H., Leevers, S.J., Marshall, C. and Cohen, P. (1992b) MAPKAP kinase-2; a novel protein kinase activated by mitogen-activated protein kinase. EMBO J., 11, 3985-3994.
42. Stokoe, D., Caudwell, B., Cohen, P.T. and Cohen, P. (1993) The substrate specificity and structure of mitogen-activated protein (MAP) kinase-activated protein kinase-2. Biochem. J., 296, 843-849.
43. Sutherland, C., Alterio, J., Campbell, D.G., Le Bourdelles, B., Mallet, J., Haavik, J. and Cohen, P. (1993) Phosphorylation and activation of human tyrosine hydroxylase in vitro by mitogen-activated protein (MAP) kinase and MAP-kinase-activated kinases 1 and 2. Eur. J. Biochem., 217, 715-722.
44. Tan, Y., Rouse, J., Zhang, A., Cariati, S., Cohen, P. and Comb, M.J. (1996) FGF and stress regulate CREB and ATF-1 via a pathway involving p38 MAP kinase and MAPKAP kinase-2. EMBO J., 15, 4629-4642.
45. Ullman, K.S., Powers, M.A. and Forbes, D.J. (1997) Nuclear export receptors: from importin to exportin. Cell, 90, 967-970.
46. Wen, W., Meinkoth, J.L., Tsien, R.Y. and Taylor, S.S. (1995) Identification of a signal for rapid export of proteins from the nucleus. Cell, 82, 463-473.
47. Wolff, B., Sanglier, J.J. and Wang, Y. (1997) Leptomycin B is an inhibitor of nuclear 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.