Dominant role for signal transduction in the transcriptional memory of yeast GAL genes

Molecular and Cellular Biology

Volumn 30, Issue 10, 2010, Pages 2330-2340

  Kundu, Sharmistha ^a,b   Peterson, Craig L ^a  

^a UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARTICLE; CHROMATIN STRUCTURE; FUNGAL GENE; FUNGAL GENETICS; GAL GENE; GENETIC TRANSCRIPTION; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; YEAST;

CHROMATIN; GENE EXPRESSION REGULATION, FUNGAL; HISTONES; RNA POLYMERASE II; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

EID: 77951996046     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.01675-09     Document Type: Article

References (37)

1. Abruzzi, K. C., D. A. Belostotsky, J. A. Chekanova, K. Dower, and M. Rosbash. 2006. 3′-end formation signals modulate the association of genes with the nuclear periphery as well as mRNP dot formation. EMBO J. 25: 4253-4262.
2. Acar, M., A. Becskei, and A. van Oudenaarden. 2005. Enhancement of cellular memory by reducing stochastic transitions. Nature 435:228-232. (Pubitemid 40685951)
3. Bhat, P. J., and T. V. Murthy. 2001. Transcriptional control of the GAL/ MEL regulon of yeast Saccharomyces cerevisiae: mechanism of galactose-mediated signal transduction. Mol. Microbiol. 40:1059-1066.
4. Brickner, D. G., I. Cajigas, Y. Fondufe-Mittendorf, S. Ahmed, P. C. Lee, J. Widom, and J. H. Brickner. 2007. H2A.Z-mediated localization of genes at the nuclear periphery confers epigenetic memory of previous transcriptional state. PLoS Biol. 5:e81.
5. Cabal, G. G., A. Genovesio, S. Rodriguez-Navarro, C. Zimmer, O. Gadal, A. Lesne, H. Buc, F. Feuerbach-Fournier, J. C. Olivo-Marin, E. C. Hurt, and U. Nehrbass. 2006. SAGA interacting factors confine sub-diffusion of transcribed genes to the nuclear envelope. Nature 441:770-773.
6. Casolari, J. M., C. R. Brown, S. Komili, J. West, H. Hieronymus, and P. A. Silver. 2004. Genome-wide localization of the nuclear transport machinery couples transcriptional status and nuclear organization. Cell 117:427-439.
7. Cavalli, G., and F. Thoma. 1993. Chromatin transitions during activation and repression of galactose-regulated genes in yeast. EMBO J. 12:4603-4613. (Pubitemid 23330266)
8. Chekanova, J. A., K. C. Abruzzi, M. Rosbash, and D. A. Belostotsky. 2008. Sus1, Sac3, and Thp1 mediate post-transcriptional tethering of active genes to the nuclear rim as well as to non-nascent mRNP. RNA 14:66-77.
9. Dion, M. F., T. Kaplan, M. Kim, S. Buratowski, N. Friedman, and O. J. Rando. 2007. Dynamics of replication-independent histone turnover in budding yeast. Science 315:1405-1408.
10. Ferreira, M. E., P. Prochasson, K. D. Berndt, J. L. Workman, and A. P. Wright. 2009. Activator-binding domains of the SWI/SNF chromatin remodeling complex characterized in vitro are required for its recruitment to promoters in vivo. FEBS J. 276:2557-2565.
11. Fischer, T., K. Strasser, A. Racz, S. Rodriguez-Navarro, M. Oppizzi, P. Ihrig, J. Lechner, and E. Hurt. 2002. The mRNA export machinery requires the novel Sac3p-Thp1p complex to dock at the nucleoplasmic entrance of the nuclear pores. EMBO J. 21:5843-5852. (Pubitemid 35315282)
12. Frolova, E., M. Johnston, and J. Majors. 1999. Binding of the glucose-dependent Mig1p repressor to the GAL1 and GAL4 promoters in vivo: regulation by glucose and chromatin structure. Nucleic Acids Res. 27:1350-1358. (Pubitemid 29206446)
13. Gligoris, T., G. Thireos, and D. Tzamarias. 2007. The Tup1 corepressor directs Htz1 deposition at a specific promoter nucleosome marking the GAL1 gene for rapid activation. Mol. Cell. Biol. 27:4198-4205.
14. Hawkins, K. M., and C. D. Smolke. 2006. The regulatory roles of the galactose permease and kinase in the induction response of the GAL network in Saccharomyces cerevisiae. J. Biol. Chem. 281:13485-13492.
15. Hittinger, C. T., and S. B. Carroll. 2007. Gene duplication and the adaptive evolution of a classic genetic switch. Nature 449:677-681.
16. Jani, D., S. Lutz, N. J. Marshall, T. Fischer, A. Kohler, A. M. Ellisdon, E. Hurt, and M. Stewart. 2009. Sus1, Cdc31, and the Sac3 CID region form a conserved interaction platform that promotes nuclear pore association and mRNA export. Mol. Cell 33:727-737.
17. Jiang, F., B. R. Frey, M. L. Evans, J. C. Friel, and J. E. Hopper. 2009. Gene activation by dissociation of an inhibitor from a transcriptional activation domain. Mol. Cell. Biol. 29:5604-5610.
18. Johnston, M. 1987. A model fungal gene regulatory mechanism: the GAL genes of Saccharomyces cerevisiae. Microbiol. Rev. 51:458-476.
19. Johnston, M., J. S. Flick, and T. Pexton. 1994. Multiple mechanisms provide rapid and stringent glucose repression of GAL gene expression in Saccharomyces cerevisiae. Mol. Cell. Biol. 14:3834-3841.
20. Kohler, A., M. Schneider, G. G. Cabal, U. Nehrbass, and E. Hurt. 2008. Yeast ataxin-7 links histone deubiquitination with gene gating and mRNA export. Nat. Cell Biol. 10:707-715.
21. Kundu, S., P. J. Horn, and C. L. Peterson. 2007. SWI/SNF is required for transcriptional memory at the yeast GAL gene cluster. Genes Dev. 21:997-1004. (Pubitemid 46625647)
22. Laine, J. P., B. N. Singh, S. Krishnamurthy, and M. Hampsey. 2009. A physiological role for gene loops in yeast. Genes Dev. 23:2604-2609.
23. Lei, E. P., C. A. Stern, B. Fahrenkrog, H. Krebber, T. I. Moy, U. Aebi, and P. A. Silver. 2003. Sac3 is an mRNA export factor that localizes to cytoplasmic fibrils of nuclear pore complex. Mol. Biol. Cell 14:836-847.
24. Lemieux, K., M. Larochelle, and L. Gaudreau. 2008. Variant histone H2A.Z, but not the HMG proteins Nhp6a/b, is essential for the recruitment of Swi/Snf, Mediator, and SAGA to the yeast GAL1 UAS(G). Biochem. Biophys. Res. Commun. 369:1103-1107.
25. Li, X. Y., S. R. Bhaumik, and M. R. Green. 2000. Distinct classes of yeast promoters revealed by differential TAF recruitment. Science 288:1242-1244.
26. Lohr, D. 1984. Organization of the GAL1-GAL10 intergenic control region chromatin. Nucleic Acids Res. 12:8457-8474.
27. Lohr, D., and J. Lopez. 1995. GAL4/GAL80-dependent nucleosome disruption/ deposition on the upstream regions of the yeast GAL1-10 and GAL80 genes. J. Biol. Chem. 270:27671-27678.
28. Lohr, D., P. Venkov, and J. Zlatanova. 1995. Transcriptional regulation in the yeast GAL gene family: a complex genetic network. FASEB J. 9:777-787.
29. Meyer, J., A. Walker-Jonah, and C. P. Hollenberg. 1991. Galactokinase encoded by GAL1 is a bifunctional protein required for induction of the GAL genes in Kluyveromyces lactis and is able to suppress the gal3 phenotype in Saccharomyces cerevisiae. Mol. Cell. Biol. 11:5454-5461.
30. Ramsey, S. A., J. J. Smith, D. Orrell, M. Marelli, T. W. Petersen, P. de Atauri, H. Bolouri, and J. D. Aitchison. 2006. Dual feedback loops in the GAL regulon suppress cellular heterogeneity in yeast. Nat. Genet. 38:1082-1087.
31. Schwabish, M. A., and K. Struhl. 2007. The Swi/Snf complex is important for histone eviction during transcriptional activation and RNA polymerase II elongation in vivo. Mol. Cell. Biol. 27:6987-6995.
32. Sekinger, E. A., Z. Moqtaderi, and K. Struhl. 2005. Intrinsic histone-DNA interactions and low nucleosome density are important for preferential accessibility of promoter regions in yeast. Mol. Cell 18:735-748.
33. Shcheprova, Z., S. Baldi, S. B. Frei, G. Gonnet, and Y. Barral. 2008. A mechanism for asymmetric segregation of age during yeast budding. Nature 454:728-734.
34. Taddei, A., G. Van Houwe, F. Hediger, V. Kalck, F. Cubizolles, H. Schober, and S. M. Gasser. 2006. Nuclear pore association confers optimal expression levels for an inducible yeast gene. Nature 441:774-778. (Pubitemid 43865226)
35. Tan-Wong, S. M., H. D. Wijayatilake, and N. J. Proudfoot. 2009. Gene loops function to maintain transcriptional memory through interaction with the nuclear pore complex. Genes Dev. 23:2610-2624.
36. Vodala, S., K. C. Abruzzi, and M. Rosbash. 2008. The nuclear exosome and adenylation regulate posttranscriptional tethering of yeast GAL genes to the nuclear periphery. Mol. Cell 31:104-113. (Pubitemid 351905922)
37. Zacharioudakis, I., T. Gligoris, and D. Tzamarias. 2007. A yeast catabolic enzyme controls transcriptional memory. Curr. Biol. 17:2041-2046.