Oscillatory nucleocytoplasmic shuttling of the general stress response transcriptional activators Msn2 and Msn4 in Saccharomyces cerevisiae

Journal of Cell Biology

Volumn 161, Issue 3, 2003, Pages 497-505

  Jacquet, Michel ^a,d   Renault, Georges ^a   Lallet, Sylvie ^a   De Mey, Jan ^b,e   Goldbeter, Albert ^c  

^a UNIVERSITÉ PARIS SACLAY   (France)

^b CNRS   (France)

^c UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

^d INSTITUTE FOR INTEGRATIVE BIOLOGY OF THE CELL I2BC   (France)

^e CNRS UMR 7100   (France)

Author keywords

Computational model; Imaging; Nuclear localization; Signaling; Stress response

Indexed keywords

CYCLIC AMP; CYCLIC AMP DEPENDENT PROTEIN KINASE; GREEN FLUORESCENT PROTEIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR MSN2; TRANSCRIPTION FACTOR MSN4; UNCLASSIFIED DRUG;

ARTICLE; AUTOREGULATION; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; GENE EXPRESSION; MATHEMATICAL MODEL; NONHUMAN; NUCLEOCYTOPLASMIC TRANSPORT; OSCILLATION; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN SYNTHESIS; SACCHAROMYCES CEREVISIAE; STRESS;

BINDING SITES; BIOLOGICAL CLOCKS; CELL COMPARTMENTATION; CELL NUCLEUS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP-DEPENDENT PROTEIN KINASES; CYTOPLASM; DNA-BINDING PROTEINS; FEEDBACK, BIOCHEMICAL; GREEN FLUORESCENT PROTEINS; LUMINESCENT PROTEINS; MODELS, BIOLOGICAL; PHOTIC STIMULATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN TRANSPORT; RECOMBINANT FUSION PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; TRANS-ACTIVATION (GENETICS); TRANSCRIPTION FACTORS;

SACCHAROMYCES; SACCHAROMYCES CEREVISIAE;

EID: 0038612842     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200303030     Document Type: Article

References (38)

1. Alepuz, P.M., D. Matheos, K.W. Cunningham, and F. Estruch. 1999. The Saccharomyces cerevisiae RanGTP-binding protein msn5p is involved in different signal transduction pathways. Genetics. 153:1219-1231.
2. Attfield, P.V., H.Y. Choi, D.A. Veal, and P.J. Bell. 2001. Heterogeneity of stress gene expression and stress resistance among individual cells of Saccharomyces cerevisiae. Mol. Microbiol. 40:1000-1008.
3. Belli, G., E. Gari, M. Aldea, and E. Herrero. 2001. Osmotic stress causes a G1 cell cycle delay and downregulation of Cln3/Cdc28 activity in Saccharomyces cerevisiae. Mol. Microbiol. 39:1022-1035.
4. Berridge, M.J. 1997. Elementary and global aspects of calcium signalling. J. Physiol. 499:291-306.
5. Boy-Marcotte, E., M. Perrot, F. Bussereau, H. Boucherie, and M. Jacquet. 1998. Msn2p and Msn4p control a large number of genes induced at the diauxic transition, which are repressed by cyclic AMP in Saccharomyces cerevisiae. J. Bacteriol. 180:1044-1052.
6. Causton, H.C., B. Ren, S.S. Koh, C.T. Harbison, E. Kanin, E.G. Jennings, T.I. Lee, H.L. True, E.S. Lander, and R.A. Young. 2001. Remodeling of yeast genome expression in response to environmental changes. Mol. Biol. Cell. 12:323-337.
7. Chi, Y., M.J. Huddleston, X. Zhang, R.A. Young, R.S. Annan, S.A. Carr, and R.J. Deshaies. 2001. Negative regulation of Gcn4 and Msn2 transcription factors by Srb10 cyclin-dependent kinase. Genes Dev. 15:1078-1092.
8. Dale, J.K., M. Maroto, M.L. Dequeant, P. Malapert, M. McGrew, and O. Pourquie. 2003. Periodic Notch inhibition by Lunatic Fringe underlies the chick segmentation clock. Nature. 421:275-278.
9. Darlington, T.K., K. Wager-Smith, M.F. Ceriani, D. Staknis, N. Gekakis, T.D. Steeves, C.J. Weitz, J.S. Takahashi, and S.A. Kay. 1998. Closing the circadian loop: CLOCK-induced transcription of its own inhibitors per and tim. Science. 280:1599-1603.
10. Garreau, H., R.N. Hasan, G. Renault, F. Estruch, E. Boy-Marcotte, and M. Jacquet. 2000. Hyperphosphorylation of Msn2p and Msn4p in response to heat shock and the diauxic shift is inhibited by cAMP in Saccharomyces cerevisiae. Microbiology. 146:2113-2120.
11. Garrett, S., M.M. Menold, and J.R. Broach. 1991. The Saccharomyces cerevisiae YAK1 gene encodes a protein kinase that is induced by arrest early in the cell cycle. Mol. Cell. Biol. 11:4045-4052.
12. Gasch, A.P., P.T. Spellman, C.M. Kao, O. Carmel-Harel, M.B. Eisen, G. Storz, D. Botstein, and P.O. Brown. 2000. Genomic expression programs in the response of yeast cells to environmental changes. Mol. Biol. Cell. 11:4241-4257.
13. Goldbeter, A. 1991. A minimal cascade model for the mitotic oscillator involving cyclin and cdc2 kinase. Proc. Natl. Acad. Sci. USA. 88:9107-9111.
14. Goldbeter, A. 1996. Biochemical Oscillations and Cellular Rhythms. Cambridge University Press, Cambridge, UK. 605 pp.
15. Goldbeter, A. 2002. Computational approaches to cellular rhythms. Nature. 420: 238-245.
16. Gonze, D., J. Halloy, and A. Goldbeter. 2002. Robustness of circadian rhythms with respect to molecular noise. Proc. Natl. Acad. Sci. USA. 99:673-678.
17. Gorner, W., E. Durchschlag, M.T. Martinez-Pastor, F. Estruch, G. Ammerer, B. Hamilton, H. Ruis, and C. Schuller. 1998. Nuclear localization of the C2H2 zinc finger protein Msn2p is regulated by stress and protein kinase A activity. Genes Dev. 12:586-597.
18. Gorner, W., E. Durchschlag, J. Wolf, E.L. Brown, G. Ammerer, H. Ruis, and C. Schuller. 2002. Acute glucose starvation activates the nuclear localization signal of a stress-specific yeast transcription factor. EMBO J. 21:135-144.
19. Griffioen, G., P. Branduardi, A. Ballarini, P. Anghileri, J. Norbeck, M.D. Baroni, and H. Ruis. 2001. Nucleocytoplasmic distribution of budding yeast protein kinase A regulatory subunit Bcy1 requires Zds1 and is regulated by Yak1-dependent phosphorylation of its targeting domain. Mol. Cell. Biol. 21:511-523.
20. Hess, B., and A. Boiteux. 1971. Oscillatory phenomena in biochemistry. Annu. Rev. Biochem. 40:237-258.
21. Hirata, H., S. Yoshiura, T. Ohtsuka, Y. Bessho, T. Harada, K. Yoshikawa, and R. Kageyama. 2002. Oscillatory expression of the bHLH factor Hes1 regulated by a negative feedback loop. Science. 298:840-843.
22. Hoffmann, A., A. Levchenko, M.L. Scott, and D. Baltimore. 2002. The IκB-NF-κB signaling module: temporal control and selective gene activation. Science. 298:1241-1245.
23. Lenssen, E., U. Oberholzer, J. Labarre, C. De Virgilio, and M.A. Collart. 2002. Saccharomyces cerevisiae Ccr4-Not complex contributes to the control of Msn2p-dependent transcription by the Ras/cAMP pathway. Mol. Microbiol. 43:1023-1037.
24. Lev Bar-Or, R., R. Maya, L.A. Segel, U. Alon, A.J. Levine, and M. Oren. 2000. Generation of oscillations by the p53-Mdm2 feedback loop: a theoretical and experimental study. Proc. Natl. Acad. Sci. USA. 97:11250-11255.
25. Mallet, L., G. Renault, and M. Jacquet. 2000. Functional cloning of the adenylate cyclase gene of Candida albicans in Saccharomyces cerevisiae within a genomic fragment containing five other genes, including homologues of CHS6 and SAP185. Yeast. 16:959-966.
26. Maroto, M., and O. Pourquie. 2001. A molecular clock involved in somite segmentation. Curr. Top. Dev. Biol. 51:221-248.
27. Martinez-Pastor, M.T., G. Marchler, C. Schuller, A. Marchler-Bauer, H. Ruis, and F. Estruch. 1996. The Saccharomyces cerevisiae zinc finger proteins Msn2p and Msn4p are required for transcriptional induction through the stress response element (STRE). EMBO J. 15:2227-2235.
28. Moskvina, E., C. Schuller, C.T. Maurer, W.H. Mager, and H. Ruis. 1998. A search in the genome of Saccharomyces cerevisiae for genes regulated via stress response elements. Yeast. 14:1041-1050.
29. Niedenthal, R.K., L. Riles, M. Johnston, and J.H. Hegemann. 1996. Green fluorescent protein as a marker for gene expression and subcellular localization in budding yeast. Yeast. 12:773-786.
30. Nikawa, J.-I., S. Cameron, T. Toda, K.M. Ferguson, and M. Wigler. 1987. Rigorous feedback control of cAMP levels in Saccharomyces cerevisiae. Genes Dev. 1:931-937.
31. Olsen, L.F., A. Lunding, F.R. Lauritsen, and M. Allegra. 2001. Melatonin activates the peroxidase-oxidase reaction and promotes oscillations. Biochem. Biophys. Res. Commun. 284:1071-1076.
32. Ribbeck, K., and D. Gorlich. 2001. Kinetic analysis of translocation through nuclear pore complexes. EMBO J. 20:1320-1330.
33. Sehgal, A., A. Rothenfluh-Hilfiker, M. Hunter-Ensor, Y. Chen, M.P. Myers, and M.W. Young. 1995. Rhythmic expression of timeless: a basis for promoting circadian cycles in period gene autoregulation. Science. 270:808-810.
34. Sibarita, J.B., H. Magnin, and J.R. De Mey. 2002. Ultra-fast 4D microscopy and high throuput distributed deconvolution. In IEEE International Symposium on Biomedical Imaging, Washington, DC. 669-772.
35. Thierry, A., L. Gaillon, F. Galibert, and B. Dujon. 1995. Construction of a complete genomic library of Saccharomyces cerevisiae and physical mapping of chromosome XI at 3.7 kb resolution. Yeast. 11:121-135.
36. Wilson, R.B., G. Renault, M. Jacquet, and K. Tatchell. 1993. The PDE2 gene of Saccharomyces cerevisiae is allelic to rca1 and encodes a phosphodiesterase which protects the cell from extracellular cAMP. FEBS Lett. 325:191-195.
37. Young, M.W. 1998. The molecular control of circadian behavioral rhythms and their entrainment in Drosophila. Annu. Rev. Biochem. 67:135-152.
38. Zhu, X., N. Demolis, M. Jacquet, and T. Michaeli. 2000. MSI1 suppresses hyperactive RAS via the cAMP-dependent protein kinase and independently of chromatin assembly factor-1. Curr. Genet. 38:60-70.