Snf1/AMPK regulates Gcn5 occupancy, H3 acetylation and chromatin remodelling at S. cerevisiae ADY2 promoter

Biochimica et Biophysica Acta - Gene Regulatory Mechanisms

Volumn 1819, Issue 5, 2012, Pages 419-427

  Abate, Georgia ^a   Bastonini, Emanuela ^b   Braun, Katherine A ^c   Verdone, Loredana ^d   Young, Elton T ^c   Caserta, Micaela ^d  

^a SAPIENZA UNIVERSITY OF ROME   (Italy)

^b UNIVERSITY OF OXFORD   (United Kingdom)

^c UNIVERSITY OF WASHINGTON   (United States)

^d CNR   (Italy)

Author keywords

Adr1; ADY2; Cat8; Histone acetylation; Nucleosome remodeling; Snf1

Indexed keywords

HISTONE ACETYLTRANSFERASE GCN5; HISTONE H3; MESSENGER RNA; PROTEIN KINASE; SNF1 PROTEIN KINASE; UNCLASSIFIED DRUG;

ARTICLE; CHROMATIN ASSEMBLY AND DISASSEMBLY; CONTROLLED STUDY; ENZYME LOCALIZATION; GENE DELETION; HISTONE ACETYLATION; NONHUMAN; PRIORITY JOURNAL; SACCHAROMYCES CEREVISIAE; TRANSCRIPTION INITIATION;

ACETYLATION; CARBON; CHROMATIN ASSEMBLY AND DISASSEMBLY; DNA-BINDING PROTEINS; GLUCOSE; HISTONE ACETYLTRANSFERASES; HISTONES; MEMBRANE TRANSPORT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN-SERINE-THREONINE KINASES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; SIGNAL TRANSDUCTION; TRANS-ACTIVATORS; TRANSCRIPTION FACTORS; TRANSCRIPTIONAL ACTIVATION;

SACCHAROMYCES CEREVISIAE;

EID: 84857660885     PISSN: 18749399     EISSN: 18764320     Source Type: Journal    
DOI: 10.1016/j.bbagrm.2012.01.009     Document Type: Article

References (58)

1. Usaite R., Jewett M.C., Oliveira A.P., Yates J.R., Olsson L., Nielsen J. Reconstruction of the yeast Snf1 kinase regulatory network reveals its role as a global energy regulator. Mol. Syst. Biol. 2009, 5:319.
2. DeRisi J.L., Iyer V.R., Brown P.O. Exploring the metabolic and genetic control of gene expression on a genomic scale. Science 1997, 278:680-686.
3. Gancedo J.M. The early steps of glucose signalling in yeast. FEMS Microbiol. Rev. 2008, 32:673-704.
4. Schüller H.-J. Transcriptional control of nonfermentative metabolism in the yeast Saccharomyces cerevisiae. Curr. Genet. 2003, 43:139-160.
5. Papamichos-Chronakis M., Gligoris T., Tzamarias D. The Snf1 kinase controls glucose repression in yeast by modulating interactions between the Mig1 repressor and the Cyc8-Tup1 co-repressor. EMBO Rep. 2004, 5:368-372.
6. Gancedo J.M. Yeast carbon catabolite repression. Microbiol. Mol. Biol. Rev. 1998, 62:334-361.
7. Carlson M. Glucose repression in yeast. Curr. Opin. Microbiol. 1999, 2:202-207.
8. Hedbacker K., Carlson M. SNF1/AMPK pathways in yeast. Front. Biosci. 2008, 13:2408-2420.
9. Hong S.P., Carlson M. Regulation of Snf1 protein kinase in response to environmental stress. J. Biol. Chem. 2007, 282:16838-16845.
10. Treitel M.A., Kuchin S., Carlson M. Snf1 protein kinase regulates phosphorylation of the Mig1 repressor in Saccharomyces cerevisiae. Mol. Cell. Biol. 1998, 18:6273-6280.
11. Ostling J., Ronne H. Negative control of the Mig1p repressor by Snf1-dependent phosphorylation in the absence of glucose. Eur. J. Biochem. 1998, 252:162-168.
12. Lesage P., Yang X., Carlson M. Yeast Snf1 protein kinase interacts with Sip4, a C6 zinc cluster transcriptional activator: a new role for Snf1 in the glucose response. Mol. Cell. Biol. 1996, 16:1921-1928.
13. Randez-Gil F., Bojunga N., Proft M., Entian K.D. Glucose derepression of gluconeogenic enzymes in Saccharomyces cerevisiae correlates with phosphorylation of the gene activator Cat8p. Mol. Cell. Biol. 1997, 17:2502-2510.
14. Charbon G., Breunig K.D., Wattiez R., Vandenhaute J., Noel-Georis I. Key role of Ser562/661 in Snf1-dependent regulation of Cat8p in Saccharomyces cerevisiae and Kluyveromyces lactis. Mol. Cell. Biol. 2004, 24:4083-4091.
15. Young E.T., Kacherovsky N., van Riper K. Snf1 protein kinase regulates Adr1 binding to chromatin but not transcription activation. J. Biol. Chem. 2002, 277:38095-38103.
16. Kuchin S., Treich I., Carlson M. A regulatory shortcut between the Snf1 protein kinase and RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. U. S. A. 2000, 97:7916-7920.
17. Shirra M.K., Rogers S.E., Alexander D.E., Arndt K. The Snf1 protein kinase and Sit4 protein phosphatase have opposing functions in regulating TATA-binding protein association with the Saccharomyces cerevisiae INO1 promoter. Genetics 2005, 169:1957-1972.
18. Lo W.S., Duggan L., Emre N.C., Belotserkovskya R., Lane W.S., Shiekhattar R., Berger S.L. Snf1 a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science 2001, 293:1142-1146.
19. Liu Y., Xu X., Kuo M.H. Snf1p regulates Gcn5p transcriptional activity by antagonizing Spt3p. Genetics 2010, 184:91-105.
20. Ratnakumar S., Kacherovsky N., Arms E., Young E.T. Snf1 controls the activity of Adr1 through dephosphorylation of Ser230. Genetics 2009, 182:735-745.
21. Ratnakumar S., Young E.T. Snf1 dependence of peroxisomal gene expression is mediated by Adr1. J. Biol. Chem. 2010, 285:10703-10714.
22. Van Driessche B., Tafforeau L., Hentges P., Carr A.M., Vandenhaute J. Additional vectors for PCR-based gene tagging in Saccharomyces cerevisiae and Schizosaccharomyces pombe using nourseothricin resistance. Yeast 2005, 22:1061-1068.
23. Knop M., Siegers K., Pereira G., Zachariae W., Winsor B., Nasmyth K., Schiebel E. Epitope tagging of yeast genes using a PCR-based strategy: more tags and improved practical routines. Yeast 1999, 15:963-972.
24. Güldener U., Heck S., Fielder T., Beinhauer J., Hegemann J.H. A new efficient gene disruption cassette for repeated use in budding yeast. Nucleic Acids Res. 1996, 24:2519-2524.
25. Schmitt M.E., Brown T.A., Trumpower B.L. A rapid and simple method for preparation of RNA from Saccharomyces cerevisiae. Nucleic Acids Res. 1990, 18:3091-3092.
26. Hecht A., Grunstein M. Mapping DNA interaction sites of chromosomal proteins using immunoprecipitation and polymerase chain reaction. Methods Enzymol. 1999, 304:399-414.
27. Schmittgen T.D., Livak K.J. Analyzing real-time PCR data by the comparative C(T) method. Nat. Protoc. 2008, 3:1101-1108.
28. Pfaffl M.W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 2001, 29:2002-2007.
29. Wu C. The 5' ends of Drosophila heat shock genes in chromatin are hypersensitive to DNase I. Nature 1980, 286:854-860.
30. Venditti S., Camilloni G. In vivo analysis of chromatin following nystatin-mediated import of active enzymes into Saccharomyces cerevisiae. Biochim. Biophys. Acta 1994, 1219:677-689.
31. Verdone L., Cesari F., Denis C.L., Di Mauro E., Caserta M. Factors affecting Saccharomyces cerevisiae ADH2 chromatin remodeling and transcription. J. Biol. Chem. 1997, 272:30828-30834.
32. Young E.T., Dombek K.M., Tachibana C., Ideker T. Multiple pathways are co-regulated by the protein kinase Snf1 and the transcription factors Adr1 and Cat8. J. Biol. Chem. 2003, 278:26146-26158.
33. Paiva S., Devaux F., Barbosa S., Jacq C., Casal M. ADY2p is essential for the acetate permease activity in the yeast Saccharomyces cerevisiae. Yeast 2004, 21:201-210.
34. Agricola E., Verdone L., Xella B., Di Mauro E., Caserta M. Common chromatin architecture, common chromatin remodeling and common transcription kinetics of ADR1-dependent genes in Saccharomyces cerevisiae. Biochemistry 2004, 43:8878-8884.
35. Agricola E., Verdone L., Di Mauro E., Caserta M. H4 acetylation does not replace H3 acetylation in chromatin remodeling and transcription activation of ADR1-dependent genes. Mol. Microbiol. 2006, 62:1433-1446.
36. Biddick R.K., Law G.L., Young E.T. Adr1 and Cat8 mediate coactivator recruitment and chromatin remodeling at glucose-regulated genes. PLoS One 2008, 3:e1436.
37. Verdone L., Camilloni G., Di Mauro E., Caserta M. Chromatin remodeling during Saccharomyces cerevisiae ADH2 gene activation. Mol. Cell. Biol. 1996, 16:1978-1988.
38. Weake V.M., Workman J.L. Inducible gene expression: diverse regulatory mechanisms. Nat. Rev. Genet. 2010, 11:426-437.
39. Zaman S., Lippman S.I., Zhao X., Broach J.R. How Saccharomyces responds to nutrients. Annu. Rev. Genet. 2008, 42:27-81.
40. Henikoff S. Nucleosome destabilization in the epigenetic regulation of gene expression. Nat. Rev. Genet. 2008, 9:15-26.
41. Caserta M., Agricola E., Churcher M., Hiriart E., Verdone L., Di Mauro E., Travers A. A translational signature for nucleosome positioning in vivo. Nucleic Acids Res. 2009, 37:5309-5321.
42. Travers A., Hiriart E., Churcher M., Caserta M., Di Mauro E. The DNA sequence-dependence of nucleosome positioning in vivo and in vitro. J. Biomol. Struct. Dyn. 2010, 27:713-724.
43. Venters B.J., Wachi S., Mavrich T.N., Andersen B.E., Jena P., Sinnamon A.J., Jain P., Rolleri N.S., Jiang C., Hemeryck-Walsh C., Pugh B.F. A comprehensive genomic binding map of gene and chromatin regulatory proteins in Saccharomyces. Mol. Cell 2011, 41:480-492.
44. Biddick R.K., Law G.L., Chin K.K., Young E.T. The transcriptional coactivators SAGA, SWI/SNF, and mediator make distinct contributions to activation of glucose-repressed genes. J. Biol. Chem. 2008, 283:33101-33109.
45. Albert I., Mavrich T.N., Tomsho L.P., Qi J., Zanton S.J., Schuster S.C., Pugh B.F. Translational and rotational settings of H2A.Z nucleosomes across the Saccharomyces cerevisiae genome. Nature 2007, 446:572-576.
46. Ioshikhes I.P., Albert I., Zanton S.J., Pugh B.F. Nucleosome positions predicted through comparative genomics. Nat. Genet. 2006, 38:1210-1215.
47. van Oevelen C.J., van Teeffelen H.A., van Werven F.J., Timmers H.T. Snf1p-dependent Spt-Ada-Gcn5-acetyltransferase (SAGA) recruitment and chromatin remodeling activities on the HXT2 and HXT4 promoters. J. Biol. Chem. 2006, 281:4523-4531.
48. Verdone L., Wu J., van Riper K., Kacherovsky N., Vogelauer M., Young E.T., Grunstein M., Di Mauro E., Caserta M. Hyperacetylation of chromatin at the ADH2 promoter allows Adr1 to bind in repressed conditions. EMBO J. 2002, 21:1101-1111.
49. Tachibana C., Biddick R., Law G.L., Young E.T. A poised initiation complex is activated by SNF1. J. Biol. Chem. 2007, 282:37308-37315.
50. Sharma V.M., Tomar R.S., Dempsey A.E., Reese J.C. Histone deacetylases RPD3 and HOS2 regulate the transcriptional activation of DNA damage-inducible genes. Mol. Cell. Biol. 2007, 27:3199-3210.
51. Sarma N.J., Haley T.M., Barbara K.E., Buford T.D., Willis K.A., Santangelo G.M. Glucose-responsive regulators of gene expression in Saccharomyces cerevisiae function at the nuclear periphery via a reverse recruitment mechanism. Genetics 2007, 175:1127-1135.
52. Eisenmann D.M., Arndt K.M., Ricupero S.L., Rooney J.W., Winston F. Spt3 interacts with TFIID to allow normal transcription in Saccharomyces cerevisiae. Genes Dev. 1992, 6:1319-1331.
53. Collart M.A. The NOT, SPT3, and MOT1 genes functionally interact to regulate transcription at core promoters. Mol. Cell. Biol. 1996, 16:6668-6676.
54. Belotserkovskaya R., Sterner D.E., Deng M., Sayre M.H., Lieberman P.M., Berger S.L. Inhibition of TATA-binding protein function by SAGA subunits Spt3 and Spt8 at Gcn4-activated promoters. Mol. Cell. Biol. 2000, 20:634-647.
55. Mohibullah N., Hahn S. Site-specific cross-linking of TBP in vivo and in vitro reveals a direct functional interaction with the SAGA subunit Spt3. Genes Dev. 2008, 22:2994-3006.
56. Woods A., Munday M.R., Scott J., Yang X., Carlson M., Carling D. Yeast Snf1 is functionally related to mammalian AMP-activated protein kinase and regulates acetyl-CoA carboxylase in vivo. J. Biol. Chem. 1994, 269:19509-19515.
57. Shirra M.K., Patton-Vogt J., Ulrich A., Liuta-Tehlivets O., Kohlwein S.D., Henry S.A., Arndt K.M. Inhibition of acetyl coenzyme A carboxylase activity restores expression of the INO1 gene in a snf1 mutant strain of Saccharomyces cerevisiae. Mol. Cell. Biol. 2001, 21:5710-5722.
58. Bungard D., Fuerth B.J., Zeng P.Y., Faubert B., Maas N.L., Viollet B., Carling D., Thompson C.B., Jones R.G., Berger S.L. Signaling kinase AMPK activates stress-promoted transcription via histone H2B phosphorylation. Science 2010, 329:1201-1205.