Phosphorylation of the MAP kinase ERK2 promotes its homodimerization and nuclear translocation

Cell

Volumn 93, Issue 4, 1998, Pages 605-615

  Khokhlatchev, Andrei V ^a   Canagarajah, Bertram ^a   Wilsbacher, Julie ^a   Robinson, Megan ^a   Atkinson, Mark ^b   Goldsmith, Elizabeth ^a   Cobb, Melanie H ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b UNIVERSITY OF TEXAS HEALTH CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; DIMERIZATION; DISSOCIATION CONSTANT; ENZYME ACTIVATION; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME MECHANISM; ENZYME PHOSPHORYLATION; ENZYME SUBSTRATE COMPLEX; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROTEIN INTERACTION; RAT; SIGNAL TRANSDUCTION;

ANIMALIA; EUKARYOTA;

EID: 0032524356     PISSN: 00928674     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0092-8674(00)81189-7     Document Type: Article

References (66)

1. Bacon, D.J., and Anderson, W.E. (1988). A fast algorithm for rendering space filling molecular pictures. J. Mol. Graphics 6, 219-220.
2. Brunner, D., Dücker, K., Oellers, N., Hafen, E., Scholz, H., and Klämbt, C. (1994). The ETS domain protein Pointed-P2 is a target of MAP kinase in the Sevenless signal transduction pathway. Nature 370, 386-389.
3. Canagarajah, B., Khokhlatchev, A., Cobb, M.H., and Goldsmith, E.J. (1997). Activation mechanism of the MAP kinase ERK2 by dual phosphorylation. Cell 90, 859-869.
4. Cassel, D., and Glaser, L. (1982). Resistance to phosphatase of thiophosphorylated epidermal growth factor receptor in A431 membranes. Proc. Natl. Acad. Sci. USA 79, 2231-2235.
5. Cavigelli, M., Dolfi, F., Claret, F.-X., and Karin, M. (1995). Induction of c-fos expression through JNK-mediated TCF/Elk-1 phosphorylation. EMBO J. 14, 5957-5964.
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. Cheng, J.-T., Cobb, M.H., and Baer, R. (1993). Phosphorylation of the TAL1 oncoprotein by the extracellular signal-regulated protein kinase ERK1. Mol. Cell. Biol. 13, 801-808.
8. Cheng, M., Boulton, T.G., and Cobb, M.H. (1996). ERK3 is a constitutively nuclear protein kinase. J. Biol. Chem. 271, 8951-8958.
9. Chi-Ying, F.H., and Ferrell, J.E., Jr. (1996). Ultrasensitivity in the mitogen-activated protein kinase cascade. Proc. Natl. Acad. Sci. USA 93, 10078-10083.
10. Chou, S.-y., Baichwal, V., and Ferrell, J.E., Jr. (1992). Inhibition of c-Jun DNA binding by mitogen-activated protein kinase. Mol. Biol. Cell 3, 1117-1130.
11. Dérijard, B., Hibi, M., Wu, I.-H., Barrett, T., Su, B., Deng, T., Karin, M., and Davis, R.J. (1994). JNK1: aprotein kinase stimulated by UV light and Ha-Ras that binds and phosphorylates the c-Jun activation domain. Cell 76, 1025-1037.
12. Durschlag, H. (1986). Specific volumes of biological macromolecules and some other molecules of biological interest. In Thermodynamic Data for Biochemistry and Biotechnology, H.-J. Hinz, ed. (Berlin: Springer-Verlag), pp. 45-128.
13. Ferrell, J.E., Jr. (1996). Tripping the switch fantastic: how a protein kinase cascade can convert graded in puts into switch-like outputs. TIBS 21, 460-466.
14. Frost, J., Xu, S., Hutchison, M., Marcus, S., and Cobb, M.H. (1996). Actions of Rho family small G proteins and p21-activated protein kinases on mitogen-activated protein kinase family members. Mol. Cell. Biol. 16, 3707-3713.
15. Fukuda, M., Gotoh, Y., and Nishida, E. (1997). 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. Gille, H., Sharrocks, A.D., and Shaw, P.E. (1992). Phosphorylation of transcription factor p62TCF by MAP kinase stimulates ternary complex formation at c-fos promoter. Nature 358, 414-416.
17. Glover, J.N.M., and Harrison, S.C. (1995). Crystal structure of the heterodimeric Bzip transcription factor c-Fos-c-Jun. Nature 373, 257-261.
18. 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.
19. Görlich, D., and Mattaj, I.W. (1996). Nucleocytoplasmic transport. Science 271, 1513-1518.
20. Guan, K.L., and Dixon, J.E. (1991). Eukaryotic proteins expressed in Escherichia coli: an improved thrombin cleavage and purification procedure of fusion proteins with glutathione S-transferase. Anal. Biochem. 192, 262-267.
21. Gupta, S., Barrett, T., Whitmarsh, A.J., Cavanagh, J., Sluss, H.K., Dérijard, B., and Davis, R.J. (1996). Selective interaction of JNK protein kinase isoforms with transcription factors. EMBO J. 15, 2760-2770.
22. Hibi, M., Lin, A., Smeal, T., Minden, A., and Karin, M. (1993). Identification of an oncoprotein-and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev. 7, 2135-2148.
23. Hsiao, K.-M., Chou, S.-y., Shih, S.-J., and Ferrell, J.E., Jr. (1994). Evidence that inactive p42 mitogen-activated protein kinase and inactive Rsk exist as a heterodimer in vivo. Proc. Natl. Acad. Sci. USA 91, 5480-5484.
24. Hu, E., Kim, J.B., Sarraf, P., and Spiegelman, B.M. (1996). Inhibition of adipogenesis through MAP kinase-mediated phosphorylation of PPARγ. Science 274, 2100-2103.
25. Hunter, T. (1995). Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell 80, 225-236.
26. Hunter, T., and Karin, M. (1992). The regulation of transcription by phosphorylation. Cell 70, 375-387.
27. Jans, D.A. (1995). The regulation of protein transport to the nucleus by phosphorylation. Biochem. J. 311, 705-716.
28. Kallunki, T., Su, B., Tsigelny, I., Sluss, H.K., Dérijard, B., Moore, G., Davis, R., and Karin, M. (1994). JNK2 contains a specificity-determining region responsible for efficient c-Jun binding and phosphorylation. Genes Dev. 8, 2996-3007.
29. Kallunki, T., Deng, T., Hibi, M., and Karin, M. (1996). c-Jun can recruit JNK to phosphorylate dimerization partners via specific docking interactions. Cell 87, 929-939.
30. Karin, M. (1995). The regulation of AP-1 activity by mitogen-activated protein kinases. J. Biol. Chem. 270, 16483-16486.
31. Kato, S., Endoh, H., Masuhiro, Y., Kitamoto, T., Uchiyama, S., Sasaki, H., Masushige, S., Gotoh, Y., Nishida, E., Kawashima, H., et al. (1995). Activation of the estrogen receptor through phosphorylation by mitogen-activated protein kinase. Science 270, 1491-1494.
32. Khokhlatchev, A., Xu, S., English, J., Wu, P., Schaefer, E., and Cobb, M.H. (1997). Reconstitution of mitogen-activated protein kinase phosphorylation cascades in bacteria. J. Biol. Chem. 272, 11057-11062.
33. Knighton, D.R., Zheng, J., Ten Eyck, L.F., Xuong, N.-H., Taylor, S.S., and Sowadski, J.M. (1991). Structure of a peptide inhibitor bound to the catalytic subunit of cyclic adenosine monophosphate-dependent protein kinase. Science 253, 414-429.
34. Kortenjann, M., Thomae, O., and Shaw, P.E. (1994). Inhibition of v-Raf dependent c-fos expression and transformation by a kinase-defective mutant of the mitogen-activated protein kinase Erk2. Mol. Cell. Biol. 14, 4185-4824.
35. Kraulis, P.J. (1991). MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
36. Kyriakis, J.M., and Avruch, J. (1996). Sounding the alarm: protein kinase cascades activated by stress and inflammation. J. Biol. Chem. 271, 24313-24316.
37. mapkk) in fibroblasts. J. Cell Biol. 122, 1079-1088.
38. Lewis, T.S., Shapiro, P.S., and Ahn, N.G. (1998). Signal transduction through MAP kinase cascades. Adv. Cancer Res. 74, 49-139.
39. Mangelsdorf, D.J., Thummel, C., Beato, M., Herrlich, P., Schütz, G., Umesono, K., Blumberg, B., Kastner, P., Mark, M., Chambon, P., and Evans, R.M. (1995). The nuclear receptor superfamily: the second decade. Cell 83, 835-839.
40. Mansour, S.J., Matten, W.T., Hermann, A.S., Candia, J.M., Rong, S., Fukasawa, K., Vande Woude, G.F., and Ahn, N.G. (1994). Transformation of mammalian cells by constitutively active MAP kinase kinase. Science 265, 966-970.
41. Marshall, C.J. (1995). Specificity of receptor tyrosine kinase signaling: transient versus sustained extracellular signal-regulated kinase activation. Cell 80, 179-185.
42. Minden, A., Lin, A., Smeal, T., Dérijard, B., Cobb, M., Davis, R., and Karin, M. (1994). c-Jun N-terminal phosphorylation correlates with activation of the JNK subgroup but not the ERK subgroup of mitogen-activated protein kinases. Mol. Cell. Biol. 14, 6683-6688.
43. 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.
44. Moriguchi, T., Gotoh, Y., and Nishida, E. (1996). Roles of the MAP kinase cascade in vertebrates. Adv. Pharmacol. 36, 121-137.
45. Ngai, P.K., and Chang, J.-Y. (1991). A novel one-step purification of human-thrombin after direct activation of crude prothrombin enriched from plasma. Biochem. J. 280, 805-808.
46. Nguyen, T.T., Scimeca, J.-C., Filloux, C., Peraldi, P., Carpentier, J.-L., and Van Obberghen, E. (1993). Co-regulation of the mitogen-activated protein kinase, extracellular signal-regulated kinase 1, and the 90-kDa ribosomal S6 kinase in PC12 cells. Distinct effects of the neurotrophic factor, nerve growth factor, and the mitogenic factor, epidermal growth factor. J. Biol. Chem. 268, 9803-9810.
47. Nicholls, A., Sharp, K.A., and Honig, B. (1991). Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbons. Proteins 11, 281-296.
48. Pollard, V.W., Michael, W.M., Nakielny, S., Siomi, M.C., Wang, F., and Dreyfuss, G. (1996). A novel receptor-mediated nuclear protein import pathway. Cell 86, 985-994.
49. Reszka, A.A., Seger, R., Diltz, C.D., Krebs, E.G., and Fischer, E.H. (1995). Association of mitogen-activated protein kinase with the microtubule cytoskeleton. Proc. Natl. Acad. Sci. USA 92, 8881-8885.
50. Robbins, D.J., Zhen, E., Owaki, H., Vanderbilt, C., Ebert, D., Geppert, T.D., and Cobb, M.H. (1993). Regulation and properties of extracellular signal-regulated protein kinases 1 and 2 in vitro. J. Biol. Chem. 268, 5097-5106.
51. Robinson, M.J., and Cobb, M.H. (1997). Mitogen-activated protein kinase pathways. Curr. Opin. Cell Biol. 9, 180-186.
52. Robinson, M.J., Cheng, M., Khokhlatchev, A., Ebert, D., Ahn, N., Guan, K., Stein, B., Goldsmith, E., and Cobb, M.H. (1996). Contribution of the MAP kinase backbone and phosphorylation lip to MEK specificity. J. Biol. Chem. 277, 29734-29739.
53. Seth, A., Gonzalez, F.A., Gupta, S., Raden, D.L., and Davis, R.J. (1992). Signal transduction within the nucleus by mitogen-activated protein kinase. J. Biol. Chem. 267, 24796-24804.
54. Sontag, E., Federov, S., Robbins, D., Cobb, M., and Mumby, M. (1993). The interaction of SV40 small tumor antigen with protein phosphatase 2A stimulates the MAP kinase pathway and induces cell proliferation. Cell 75, 887-897.
55. 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.
56. Treisman, R. (1996). Regulation of transcription by MAP kinase cascades. Curr. Opin. Cell Biol. 8, 205-215.
57. Wang, Z., Harkins, P.C., Ulevitch, R.J., Man, J., Cobb, M.H., and Goldsmith, E.J. (1997). The structure of mitogen-activated protein kinase p38at 2.1-Å resolution. Proc. Natl. Acad. Sci. USA 94, 2327-2332.
58. Waskiewicz, A.J., and Cooper, J.A. (1995). Mitogen and stress response pathways: MAP kinase cascades and phosphatase regulation in mammals and yeast. Curr. Opin. Cell Biol. 7, 798-805.
59. 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.
60. Wilson, K.P., Fitzgibbon, M.J., Caron, P.R., Griffith, J.P., Chen, W., McCaffrey, P.G., Chambers, S.P., and Su, M.S.-S. (1996). Crystal structure of p38 mitogen-activated protein kinase. J. Biol. Chem. 277, 27696-27700.
61. Winston, L.A., and Hunter, T. (1996). Intracellular signaling: putting JAKs on the kinase MAP. Curr. Biol. 6, 668-671.
62. Zamyatnin, A.A. (1972). Protein volume in solution. Prog. Biophys. Mol. Biol. 24, 107-123.
63. Zervos, A.S., Faccio, L., Gatto, J.P., Kyriakis, J.M., and Brent, R. (1995). Mxi2, a mitogen-activated protein kinase that recognizes and phosphorylates Max protein. Proc. Natl. Acad. Sci. USA 92, 10531-10534.
64. Zhang, F., Strand, A., Robbins, D., Cobb, M.H., and Goldsmith, E.J. (1994). Atomic structure of the MAP kinase ERK2 at 2.3 Å resolution. Nature 367, 704-710.
65. Zhang, J., Zhang, F., Ebert, D., Cobb, M.H., and Goldsmith, E.J. (1995). Activity of the MAP kinase ERK2 is controlled by a flexible surface loop. Structure 3, 299-307.
66. Zhao, Y., Bjorbæk, C., and Moller, D.E. (1996). Regulation and interaction of pp90rsk isoforms with mitogen-activated protein kinases. J. Biol. Chem. 277, 29773-29779.