Salt-inducible kinase-1 represses cAMP response element-binding protein activity both in the nucleus and in the cytoplasm

European Journal of Biochemistry

Volumn 271, Issue 21, 2004, Pages 4307-4319

  Katoh, Yoshiko ^a   Takemori, Hiroshi ^a   Min, Li ^a   Muraoka, Hasaaki ^a,b   Doi, Junko ^c   Horike, Nanao ^a   Okamoto, Mitsuhiro ^a,d  

^a OSAKA UNIVERSITY   (Japan)

^b Protein Express Co Ltd   (Japan)

^c SENRI KINRAN UNIVERSITY   (Japan)

^d OSAKA UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

Author keywords

cAMP; CRE; Nuclear localization signal; SIK; Transcription repression

Indexed keywords

ARGININE; CORTICOTROPIN; CYCLIC AMP DEPENDENT PROTEIN KINASE; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; GREEN FLUORESCENT PROTEIN; LYSINE; PHOSPHOTRANSFERASE; SALT INDUCIBLE KINASE 1; SERINE; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CELL NUCLEUS; CHIMERA; CYTOPLASM; GENETIC TRANSCRIPTION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TRANSCRIPTION REGULATION; WILD TYPE;

3T3-L1 CELLS; ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; ANIMALS; ARGININE; CELL NUCLEUS; CLONING, MOLECULAR; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; DNA, COMPLEMENTARY; GENES, REPORTER; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; LYSINE; MICE; MICROSCOPY, FLUORESCENCE; MODELS, GENETIC; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; NUCLEAR LOCALIZATION SIGNALS; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; PROTEIN-SERINE-THREONINE KINASES; RATS; RECOMBINANT FUSION PROTEINS; TRANSCRIPTION, GENETIC;

ANIMALIA;

EID: 8644226763     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.2004.04372.x     Document Type: Article

References (56)

1. Brindle, P., Linke, S. & Montminy, M. (1993) Protein-kinase-A- dependent activator in transcription factor CREB reveals new role for CREM repressors. Nature 364, 821-824.
2. Quinn, P.G. (1993) Distinct activation domains within cAMP response element-binding protein (CREB) mediate basal and cAMP-stimulated transcription. J. Biol. Chem. 268, 16999-17009.
3. Mayr, B. & Montminy, M. (2001) Transcriptional regulation by the phosphorylation-dependent factor CREB. Nat. Rev. Mol. Cell Biol. 2, 599-609.
4. Gonzalez, G.A. & Montminy, M.R. (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59, 675-680.
5. Boshart, M., Weih, F., Nichols, M. & Schutz, G. (1991) The tissue-specific extinguisher locus TSE1 encodes a regulatory subunit of cAMP-dependent protein kinase. Cell 66, 849-859.
6. Xing, J., Kornhauser, J.M., Xia, Z., Thiele, E.A. & Greenberg, M.E. (1998) Nerve growth factor activates extracellular signal-regulated kinase and p38 mitogen-activated protein kinase pathways to stimulate CREB serine 133 phosphorylation. Mol. Cell. Biol. 18, 1946-1955.
7. Arthur, J.S. & Cohen, P. (2000) MSK1 is required for CREB phosphorylation in response to mitogens in mouse embryonic stem cells. FEBS Lett. 482, 44-48.
8. Xing, J., Ginty, D.D. & Greenberg, M.E. (1996) Coupling of the RAS-MAPK pathway to gene activation by RSK2, a growth factor-regulated CREB kinase. Science 273, 959-963.
9. Du, K. & Montminy, M. (1998) CREB is a regulatory target for the protein kinase Akt/PKB. J. Biol. Chem. 273, 32377-323779.
10. 2+/calmodulin-dependent protein kinases type II and type IV involves phosphorylation of a site that negatively regulates activity. Genes Dev. 8, 2527-2539.
11. Matthews, R.P., Guthrie, C.R., Wailes, L.M., Zhao, X., Means, A.R. & McKnight, G.S. (1994) Calcium/calmodulin-dependent protein kinase types II and IV differentially regulate CREB-dependent gene expression. Mol. Cell. Biol. 14, 6107-6116.
12. Shimomura, A., Ogawa, Y., Kitani, T., Fujisawa, H. & Hagiwara, M. (1996) Calmodulin-dependent protein kinase II potentiates transcriptional activation through activating transcription factor 1 but not cAMP response element-binding protein. J. Biol. Chem. 271, 17957-17960.
13. Wu, X. & McMurray, C.T. (2001) Calmodulin kinase II attenuation of gene transcription by preventing cAMP response element-binding protein (CREB) dimerization and binding of the CREB-binding protein. J. Biol. Chem. 276, 1735-1741.
14. Chrivia, J.C., Kwok, R.P., Lamb, N., Hagiwara, M., Montminy, M.R. & Goodman, R.H. (1993) Phosphorylated CREB binds specifically to the nuclear protein CBP. Nature 365, 855-885.
15. Kwok, R.P., Lundblad, J.R., Chrivia, J.C., Richards, J.P., Bachinger, H.P., Brennan, R.G., Roberts, S.G., Green, M.R. & Goodman, R.H. (1994) Nuclear protein CBP is a coactivator for the transcription factor CREB. Nature 370, 223-226.
16. Arias, J., Alberts, A.S., Brindle, P., Claret, F.X., Smeal, T., Karin, M., Feramisco, J. & Montminy, M. (1994) Activation of cAMP and mitogen responsive genes relies on a common nuclear factor. Nature 370, 226-229.
17. Lundblad, J.R., Kwok, R.P., Laurance, M.E., Harter, M.L. & Goodman, R.H. (1995) Adenoviral E1A-associated protein p300 as a functional homologue of the transcriptional co-activator CBP. Nature 374, 85-88.
18. Silverman, M.A., Benard, O., Jaaro, H., Rattner, A., Citri, Y. & Seger, R. (1999) CPG16, a novel protein serine/threonine kinase downstream of cAMP-dependent protein kinase. J. Biol. Chem. 274, 2631-2636.
19. Reddy, U.R., Basu, A., Bannerman, P., Ikegaki, N., Reddy, C.D. & Pleasure, D. (1999) ZPK inhibits PKA induced transcriptional activation by CREB and blocks retinoic acid induced neuronal differentiation. Oncogene 18, 4474-4484.
20. Wang, Z., Takemori, H., Halder, S.K., Nonaka, Y. & Okamoto, M. (1999) Cloning of a novel kinase (SIK) of the SNF1/AMPK family from high salt diet-treated rat adrenal. FEBS Lett. 453, 135-139.
21. Feldman, J.D., Vician, L., Crispino, M., Hoe, W., Baudry, M. & Herschman, H.R. (2000) The salt-inducible kinase, SIK, is induced by depolarization in brain. J. Neurochem. 74, 2227-2238.
22. Hardie, D.G. & Carling, D. (1997) The AMP-activated protein kinase - fuel gauge of the mammalian cell? Eur. J. Biochem. 246, 259-273.
23. Drewes, G., Ebneth, A., Preuss, U., Mandelkow, E.M. & Mandelkow, E. (1997) MARK, a novel family of protein kinases that phosphorylate microtubule-associated proteins and triggers microtubule disruption. Cell 89, 297-308.
24. Lanjuin, A. & Sengupta, P. (2002) Regulation of chemosensory receptor expression and sensory signaling by the KIN-29 Ser/Thr kinase. Neuron 33, 369-381.
25. da Silva Xavier, G., Leclerc, I., Varadi, A., Tsuboi, T., Moule, S.K. & Rutter, G.A. (2003) Role for AMP-activated protein kinase in glucose-stimulated insulin secretion and preproinsulin gene expression. Biochem. J. 371, 761-774.
26. Shaw, R.J., Kosmatka, M., Bardeesy, N., Hurley, R.L., Witters, L.A., DePinho, R.A. & Cantley, L.C. (2004) LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J. 23, 833-843.
27. Lin, X., Takemori, H., Katoh, Y., Doi, J., Horike, N., Makino, A., Nonaka, Y. & Okamoto, M. (2001) Salt-inducible kinase is involved in the ACTH/cAMP-dependent protein kinase signaling in Y1 mouse adrenocortical tumor cells. Mol. Endocrinol. 15, 1264-1276.
28. Takemori, H., Katoh, Y., Horike, N., Doi, J. & Okamoto, M. (2002) ACTH-induced nucleocytoplasmic translocation of salt-inducible kinase. Implication in the protein kinase A-activated gene transcription in mouse adrenocortical tumor cells. J. Biol. Chem. 277, 42334-42343.
29. Doi, J., Takemori, H., Lin, X.-Z., Horike, N., Katoh, Y. & Okamoto, M. (2002) Salt-inducible kinase represses PKA-mediated activation of human cholesterol side chain cleavage cytochrome promoter through the CREB basic leucine zipper domain. J. Biol. Chem. 277, 15629-15637.
30. Takemori, H., Doi, J., Horike, N., Katoh, Y., Min, L., Lin, X.Z., Wang, Z.N., Muraoka, M. & Okamoto, M. (2003) Salt-inducible kinase-mediated regulation of steroidogenesis at the early stage of ACTH-stimulation. J. Steroid Biochem. Mol. Biol. 85, 397-400.
31. Horike, N., Takemori, H., Katoh, Y., Doi, J., Min, L., Asano, T., Sun, X.J., Yamamoto, H., Kasayama, S., Muraoka, M., Nonaka, Y. & Okamoto, M. (2003) Adipose-specific expression, phosphorylation of Ser794 in insulin receptor substrate-1, and activation in diabetic animals of salt-inducible kinase-2. J. Biol. Chem. 278, 18440-18447.
32. Gorlich, D. (1998) Transport into and out of the cell nucleus. EMBO J. 17, 2721-2727.
33. Nigg, E.A. (1997) Nucleocytoplasmic transport: signals, mechanisms and regulation. Nature 386, 779-787.
34. Kalderon, D., Roberts, B.L., Richardson, W.D. & Smith, A.E. (1984) A short amino acid sequence able to specify nuclear location. Cell 39, 499-509.
35. Tiganis, T., Flint, A.J., Adam, S.A. & Tonks, N.K. (1997) Association of the T-cell protein tyrosine phosphatase with nuclear import factor p97. J. Biol Chem. 272, 21548-21557.
36. Fischer, U., Huber, J., Boelens, W.C., Mattaj, I.W. & Luhrmann, 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.
37. Okamoto, M., Takemori, H. & Katoh, Y. (2004) Salt-inducible kinase in steroidogenesis and adipogenesis. Trends Endocrinol. Metab. 15, 21-26.
38. Conkright, M.D., Canettieri, G., Screaton, R., Guzman, E., Miraglia, L., Hogenesch, J.B. & Montminy, M. (2003) TORCs: transducers of regulated CREB activity. Mol. Cell 12, 413-423.
39. Iourgenko, V., Zhang, W., Mickanin, C., Daly, I., Jiang, C., Hexham, J.M., Orth, A.P., Miraglia, L., Meltzer, J., Garza, D., Chirn, G.W., McWhinnie, E., Cohen, D., Skelton, J., Terry, R., Yu, Y., Bodian, D., Buxton, P.P., Zhu, J., Song, C. & Labow, M.A. (2003) Identification of a family of cAMP response element-binding protein coactivators by genome-scale functional analysis in mammalian cells. Proc. Natl Acad. Sci. USA 100, 12147-12152.
40. Screaton, R.A., Conkright, M.D., Katoh, Y., Best, J., Canettieri, G., Jeffries, S., Guzman, E., Messen, S., Yates, J.R. III, Takemori, H., Okamoto, M. & Montminy, M.R. (2004) The CREB Coactivator TORC2 Functions as a Calcium- and cAMP-Sensitive Coincidence Detector. Cell 119, 61-74.
41. Robbins, J., Dilworth, S.M., Laskey, R.A. & Dingwall, C. (1991) Two interdependent basic domains in nucleoplasmin nuclear targeting sequence: identification of a class of bipartite nuclear targeting sequence. Cell 64, 615-623.
42. Siomi, H. & Dreyfuss, G. (1995) A nuclear localization domain in the hnRNP A1 protein. J. Cell Biol. 129, 551-560.
43. Jakel, S. & Gorlich, D. (1998) Importin beta, transportin, RanBP5 and RanBP7 mediate nuclear import of ribosomal proteins in mammalian cells. EMBO J. 17, 4491-4502.
44. Mo, Y.Y., Wang, C. & Beck, W.T. (2000) A novel nuclear localization signal in human DNA topoisomerase I. J. Biol. Chem. 275, 41107-41113.
45. Jans, D.A., Xiao, C.Y. & Lam, M.H. (2000) Nuclear targeting signal recognition: a key control point in nuclear transport? Bioessays 22, 532-544.
46. Fukuda, M., Asano, S., Nakamura, T., Adachi, M., Yoshida, M., Yanagida, M. & Nishida, E. (1997) CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390, 308-311.
47. Ducret, C., Maira, S.M., Dierich, A. & Wasylyk, B. (1999) The net repressor is regulated by nuclear export in response to anisomycin, UV, and heat shock. Mol. Cell Biol. 19, 7076-7087.
48. Graves, P.R., Lovly, C.M., Uy, G.L. & Piwnica Worms, H. (2001) Localization of human Cdc25C is regulated both by nuclear export and 14-3-3 protein binding. Oncogene 20, 1839-1851.
49. Kuersten, S., Ohno, M. & Mattaj, I.W. (2001) Nucleocytoplasmic transport: Ran, beta and beyond. Trends Cell Biol. 11, 497-503.
50. Webster, M.K., Goya, L. & Firestone, G.L. (1993) Immediate-early transcriptional regulation and rapid mRNA turnover of a putative serine/threonine protein kinase. J. Biol. Chem. 268, 11482-11485.
51. Buse, P., Tran, S.H., Luther, E., Phu, P.T., Aponte, G.W. & Firestone, G.L. (1999) Cell cycle and hormonal control of nuclear-cytoplasmic localization of the serum- and glucocorticoid-inducible protein kinase, Sgk, in mammary tumor cells. A novel convergence point of anti-proliferative and proliferative cell signaling pathways. J. Biol. Chem. 274, 7253-7263.
52. Kim, J.E. & Chen, J. (2000) Cytoplasmic-nuclear shuttling of FKBP12-rapamycin-associated protein is involved in rapamycin-sensitive signaling and translation initiation. Proc. Natl. Acad. Sci. USA 97, 14340-14345.
53. Xiao, Z., Watson, N., Rodriguez, C. & Lodish, H.F. (2001) Nucleocytoplasmic shuttling of Smad1 conferred by its nuclear localization and nuclear export signals. J. Biol. Chem. 276, 39404-39410.
54. Xiao, Z., Latek, R. & Lodish, H.F. (2003) An extended bipartite nuclear localization signal in Smad4 is required for its nuclear import and transcriptional activity. Oncogene 22, 1057-1069.
55. Xiao, Z., Brownawell, A.M., Macara, I.G. & Lodish, H.F. (2003) A novel export signal in Smad1 is essential for its signaling activity. J. Biol. Chem. 278, 34245-34252.
56. Seternes, O.M., Johansen, B., Hegge, B., Johannessen, M., Keyse, S.M. & Moens, U. (2002) Both binding and activation of p38 mitogen-activated protein kinase (MAPK) play essential roles in regulation of the nucleocytoplasmic distribution of MAPK-activated protein kinase 5 by cellular stress. Mol. Cell Biol. 22, 6931-6945.