90
Views
58
CrossRef citations to date
0
Altmetric
Article

The Yeast AMPK Homolog SNF1 Regulates Acetyl Coenzyme A Homeostasis and Histone Acetylation

, &
Pages 4701-4717 | Received 14 Feb 2013, Accepted 18 Sep 2013, Published online: 20 Mar 2023

REFERENCES

  • Hardie DG, Carling D, Carlson M. 1998. The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu. Rev. Biochem. 67:821–855.
  • Hardie DG. 2007. AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat. Rev. Mol. Cell Biol. 8:774–785.
  • Hedbacker K, Carlson M. 2008. SNF1/AMPK pathways in yeast. Front. Biosci. 13:2408–2420.
  • Jiang R, Carlson M. 1997. The Snf1 protein kinase and its activating subunit, Snf4, interact with distinct domains of the Sip1/Sip2/Gal83 component in the kinase complex. Mol. Cell. Biol. 17:2099–2106.
  • Hong SP, Leiper FC, Woods A, Carling D, Carlson M. 2003. Activation of yeast Snf1 and mammalian AMP-activated protein kinase by upstream kinases. Proc. Natl. Acad. Sci. U. S. A. 100:8839–8843.
  • Sutherland CM, Hawley SA, Mccartney RR, Leech A, Stark MJ, Schmidt MC, Hardie DG. 2003. Elm1p is one of the three upstream kinases for the Saccharomyces cerevisiae SNF1 complex. Curr. Biol. 13:1299–1305.
  • McCartney RR, Schmidt MC. 2001. Regulation of Snf1 kinase. Activation requires phosphorylation of threonine 210 by an upstream kinase as well as a distinct step mediated by the Snf4 subunit. J. Biol. Chem. 276:36460–36466.
  • Sanz P, Alms GR, Haystead TA, Carlson M. 2000. Regulatory interactions between the Reg1-Glc7 protein phosphatase and the Snf1 protein kinase. Mol. Cell. Biol. 20:1321–1328.
  • Ruiz A, Liu Y, Carlson M. 2012. Heterotrimer-independent regulation of activation-loop phosphorylation of Snf1 protein kinase involves two protein phosphatases. Proc. Natl. Acad. Sci. U. S. A. 109:8652–8657.
  • Mayer FV, Heath R, Underwood E, Sanders MJ, Carmena D, McCartney RR, Leiper FC, Xiao B, Jing C, Walker PA, Haire LF, Ogrodowicz R, Martin SR, Scmidt MC, Gamblin SJ, Carling D. 2011. ADP regulates SNF1, the Saccharomyces cerevisiae homolog of AMP-activated protein kinase. Cell Metab. 14:707–714.
  • Treitel MA, Kuchin S, Carlson M. 1998. Snf1 protein kinase regulates phosphorylation of the Mig1 repressor in Saccharomyces cerevisiae. Mol. Cell. Biol. 18:6273–6280.
  • Smith FC, Davies SP, Wilson WA, Carling D, Hardie DG. 1999. The SNF1 kinase complex from Saccharomyces cerevisiae phosphorylates the transcriptional repressor protein Mig1p in vitro at four sites within or near regulatory domain 1. FEBS Lett. 453:219–223.
  • DeVit MJ, Johnston M. 1999. The nuclear exportin Msn5 is required for nuclear export of the Mig1 glucose repressor of Saccharomyces cerevisiae. Curr. Biol. 9:1231–1241.
  • Papamichos-Chronakis M, Gligoris T, Tzamarias D. 2004. The Snf1 kinase controls glucose repression in yeast by modulating interactions between the Mig1 repressor and the cyc8-Tup1 co-repressor. EMBO Rep. 5:368–372.
  • Kuchin S, Treich I, Carlson M. 2000. A regulatory shortcut between the Snf1 protein kinase and RNA polymerase II holoenzyme. Proc. Natl. Acad. Sci. U. S. A. 97:7916–7920.
  • Tachibana C, Biddick R, Law GL, Young ET. 2007. A poised initiation complex is activated by SNF1. J. Biol. Chem. 282:37308–37315.
  • Lo W-S, Trievel RC, Rojas JR, Duggan L, Hsu J-Y, Allis CD, Marmorstein R, Berger SL. 2000. Phosphorylation of serine 10 in histone H3 is functionally linked in vitro and in vivo to Gcn5-mediated acetylation at lysine 14. Mol. Cell 5:917–926.
  • Lo W-S, Duggan L, Emre NC, Belotserkovskya R, Lane WS, Shiekhattar R, Berger SL. 2001. Snf1—a histone kinase that works in concert with the histone acetyltransferase Gcn5 to regulate transcription. Science 293:1142–1146.
  • Lo W-S, Gamache ER, Henry KW, Yang D, Pillus L, Berger SL. 2005. Histone H3 phosphorylation can promote TBP recruitment through distinct promoter-specific mechanisms. EMBO J. 24:997–1008.
  • Geng F, Laurent BC. 2004. Roles of SWI/SNF and HATs throughout the dynamic transcription of a yeast glucose-repressible gene. EMBO J. 23:127–137.
  • Liu Y, Xu X, Singh-Rodriguez S, Zhao Y, Kuo MH. 2005. Histone H3 Ser10 phosphorylation-independent function of Snf1 and Reg1 proteins rescues a gcn5- mutant in HIS3 expression. Mol. Cell. Biol. 25:10566–10579.
  • Abate G, Bastonini E, Braun KA, Verdone L, Young ET, Caserta M. 2012. Snf1/AMPK regulates Gcn5 occupancy, H3 acetylation and chromatin remodeling at S. cerevisiae ADY2 promoter. Biochim. Biophys. Acta 1819:419–427.
  • Witters LA, Watts TD. 1990. Yeast acetyl-CoA carboxylase: in vitro phosphorylation by mammalian and yeast protein kinases. Biochem. Biophys. Res. Commun. 169:369–376.
  • Davies SP, Carling D, Munday MR, Hardie DG. 1992. Diurnal rhythm of phosphorylation of rat liver acetyl-CoA carboxylase by the AMP-activated protein kinase, demonstrated using free-clamping. Effects of high fat diets. Eur. J. Biochem. 203:615–623.
  • Woods A, Munday MR, Scott J, Yang X, Carlson M, Carling D. 1994. Yeast SNF1 is functionally related to mammalian AMP-activated protein kinase and regulates acetyl-CoA carboxylase in vivo. J. Biol. Chem. 269:19509–19515.
  • Shirra MK, Patton-Vogt J, Ulrich A, Tehlivets OL, Kohwein SD, Henry SA, Arndt KM. 2001. Inhibition of acetyl coenzyme A carboxylase activity restores expression of the INO1 gene in a snf1 mutant strain of Saccharomyces cerevisiae. Mol. Cell. Biol. 21:5710–5722.
  • Tehlivets O, Scheuringer K, Kholwein SD. 2007. Fatty acid synthesis and elongation in yeast. Biochim. Biophys. Acta 1771:255–270.
  • Takahashi H, MacCaffery JM, Irizarry RA, Boeke JD. 2006. Nucleocytosolic acetyl-coenzyme A synthetase is required for histone acetylation and global transcription. Mol. Cell 23:207–217.
  • Friis RMN, Wu BP, Reinke SN, Hockman DJ, Sykes BD, Schultz MC. 2009. A glycolytic burst drives glucose induction of global histone acetylation by picNuA4 and SAGA. Nucleic Acids Res. 37:3969–3980.
  • Wellen KE, Hatzivassiliou G, Sachdeva UM, Bui TV, Cross JR, Thompson CB. 2009. ATP-citrate lyase links cellular metabolism to histone acetylation. Science 324:1076–1080.
  • Cai L, Sutter BM, Li B, Tu BP. 2011. Acetyl-CoA induces cell growth and proliferation by promoting the acetylation of histones at growth genes. Mol. Cell 42:426–437.
  • Galdieri L, Vancura A. 2012. Acetyl-CoA carboxylase regulates global histone acetylation. J. Biol. Chem. 28:23865–23876.
  • Blackwell JSJr, Wilkinson ST, Mosammaparast N, Pemberton LF. 2007. Mutational analysis of H3 and H4 N termini reveals distinct roles in nuclear import. J. Biol. Chem. 282:20142–20150.
  • Roberts SM, Winston F. 1997. Essential functional interactions of SAGA, a Saccharomyces cerevisiae complex of Spt, Ada, and Gcn5 proteins, with the Snf/Swi and Srb/mediator complexes. Genetics 147:451–465.
  • Lindstrom KC, Vary JCJr, Parthun MR, Delrow J, Tsukiyama T. 2006. Isw1 functions in parallel with the NuA4 and Swr1 complexes in stress-induced gene repression. Mol. Cell. Biol. 26:6117–6129.
  • Yu Y, Eriksson P, Stillman DJ. 2000. Architectural transcription factors and the SAGA complex function in parallel pathways to activate transcription. Mol. Cell. Biol. 20:2350–2357.
  • Proft M, Serrano R. 1999. Repressors and upstream repressing sequences of the stress-regulated ENA1 gene in Saccharomyces cerevisiae: bZIP protein Sko1p confers HOG-dependent osmotic regulation. Mol. Cell. Biol. 19:537–546.
  • Kaluarachchi Duffy SK, Friesen H, Baryshnikova A, Lambert J-P, Chong YT, Figeys D, Andrews B. 2012. Exploring the yeast acetylome using functional genomics. Cell 149:936–948.
  • Ye T, Elbing K, Hohmann S. 2008. The pathway by which the yeast protein kinase Snf1p controls acquisition of sodium tolerance is different from that mediating glucose regulation. Microbiology 154:2814–2826.
  • Sherman F. 1991. Getting started with yeast. Methods Enzymol. 194:3–21.
  • Garí E, Piedrafita L, Aldea M, Herrero E. 1997. A set of vectors with a tetracycline-regulatable promoter system for modulated gene expression in Saccharomyces cerevisiae. Yeast 13:837–848.
  • Gombert AK, Moreira dos Santos M, Christensen B, Nielsen J. 2001. Network identification and flux quantification in the central metabolism of Saccharomyces cerevisiae under different conditions of glucose repression. J. Bacteriol. 183:1441–1451.
  • Celenza JL, Carslson M. 1989. Mutational analysis of the Saccharomyces cerevisiae SNF1 protein kinase and evidence for functional interaction with the SNF4 protein. Mol. Cell. Biol. 9:5034–5044.
  • Sabet N, Volo S, Yu C, Madigan JP, Morse RH. 2004. Genome-wide analysis of the relationship between transcriptional regulation by Rpd3p and the histone H3 and H4 amino termini in budding yeast. Mol. Cell. Biol. 24:8823–8833.
  • Young ET, Dombek KM, Tachibana C, Ideker T. 2003. Multiple pathways are co-regulated by the protein kinase Snf1 and the transcription factors Adr1 and Cat8. J. Biol. Chem. 278:26146–26158.
  • Westholm JO, Nordberg N, Murén E, Ameur A, Komorowski J, Ronne H. 2008. Combinatorial control of gene expression by the three yeast repressors Mig1, Mig2 and Mig3. BMC Genomics 9:601. doi:10.1186/1471-2164-9-601.
  • Govind CK, Zhang F, Qiu H, Hofmeyer K, Hinnebusch AG. 2007. Gcn5 promotes acetylation, eviction, and methylation of nucleosomes in transcribed coding regions. Mol. Cell 25:31–42.
  • Lin YY, Lu JY, Zhang J, Walter W, Dang W, Wan J, Tao SC, Qian J, Zhao Y, Boeke JD, Berger SL, Zhu H. 2009. Protein acetylation microarray reveals that NuA4 controls key metabolic target regulating gluconeogenesis. Cell 136:1073–1084.
  • Lu J-Y, Lin Y-Y, Sheu J-C, Wu J-T, Lee F-J, Chen Y, Lin M-I, Chiang F-T, Tai T-Y, Berger SL, Zhao Y, Tsai K-S, Zhu H, Chuang L-M, Boeke JD. 2011. Acetylation of yeast AMPK controls intrinsic aging independently of caloric restriction. Cell 146:969–979.
  • Wittenberg C, Reed SI. 2005. Cell cycle-dependent transcription in yeast: promoters, transcription factors, and transcriptomes. Oncogene 24:2746–2755.
  • Lin YY, Qi Y, Lu JY, Pan X, Yuan DS, Zhao Y, Bader JS, Boeke JD. 2008. A comprehensive synthetic genetic interaction network governing yeast histone acetylation and deacetylation. Genes Dev. 22:2062–2074.
  • Sanz P. 2003. Snf1 protein kinase: a key player in the response to cellular stress in yeast. Biochem. Soc. Trans. 31:178–181.
  • Dubacq C, Chevalier A, Mann C. 2004. The protein kinase Snf1 is required for tolerance to the ribonucleotide reductase inhibitor hydroxyurea. Mol. Cell. Biol. 24:2560–2572.
  • Hong SP, Carlson M. 2007. Regulation of snf1 protein kinase in response to environmental stress. J. Biol. Chem. 282:16838–16845.
  • Casamayor A, Serrano R, Platara A, Casado C, Ruiz A, Arino J. 2012. The role of the Snf1 kinase in the adaptive response of Saccharomyces cerevisiae to alkaline pH stress. Biochem. J. 444:39–49.
  • Uffenbeck SR, Krebs JE. 2006. The role of chromatin structure in regulating stress-induced transcription in Saccharomyces cerevisiae. Biochem. Cell Biol. 84:477–489.
  • de Nadal E, Posas F. 2010. Multilayered control of gene expression by stress-activated protein kinases. EMBO J. 29:4–13.
  • Kurdistani SK, Tavazoie S, Grunstein M. 2004. Mapping global histone acetylation patterns to gene expression. Cell 117:721–733.
  • Pokholok DK, Harbison CT, Levine S, Cole M, Hannett NM, Lee IT, Bell GW, Walker K, Rolfe PA, Herbolshimer E, Zeitlinger J, Lewitter F, Gifford DK, Young RA. 2005. Genome-wide map of nucleosome acetylation and methylation in yeast. Cell 122:517–527.
  • van den Berg MA, de Jong-Gubbels P, Kortland CJ, van Dijken JP, Pronk JT, Steensma HY. 1996. The two acetyl-coenzyme A synthetases of Saccharomyces cerevisiae differ with respect to kinetic properties and transcriptional regulation. J. Biol. Chem. 271:28953–28959.
  • Tachibana C, Yoo JY, Tagne JB, Kacherovsky N, Lee TI, Young ET. 2005. Combined global localization analysis and transcriptome data identify genes that are directly coregulated by Adr1 and Cat8. Mol. Cell. Biol. 25:2138–2146.
  • Zaman S, Lippman SI, Schneper L, Slonim N, Broach JR. 2009. Glucose regulates transcription in yeast through a network of signaling pathways. Mol. Syst. Biol. 5:245.
  • Dion MF, Altschuler SJ, Wu LF, Rando OJ. 2005. Genomic characterization reveals a simple histone H4 acetylation code. Proc. Natl. Acad. Sci. U. S. A. 102:5501–5506.
  • Young ET, Zhang C, Shokat K, Parua PK, Braun KA. 2012. The AMP-activated protein kinase Snf1 regulates transcription factor binding, RNA polymerase II activity, and mRNA stability of glucose-repressed genes in Saccharomyces cerevisiae. J. Biol. Chem. 287:29021–29034.
  • Eriksson PR, Ganguli D, Nagarajavel V, Clark DJ. 2012. Regulation of histone gene expression in budding yeast. Genetics 191:7–20.
  • Ramaswamy V, Williams JS, Robinson KM, Sopko RL, Schultz MC. 2003. Global control of histone modification by the anaphase-promoting complex. Mol. Cell. Biol. 23:9136–9149.
  • van Oevelen CJC, van Teeffelen HAAM, van Werven FJ, Timmers HTM. 2006. Snf1p-dependent Spt-Ada-Gcn5-acetyltransferase (SAGA) recruitment and chromatin remodeling activities on the HXT2 and HXT4 promoters. J. Biol. Chem. 281:4523–4531.
  • Seker T, Moller K, Nielsen J. 2005. Analysis of acyl CoA ester intermediates of the mevalonate pathway in Saccharomyces cerevisiae. Appl. Microbiol. Biotechnol. 67:119–124.
  • Rohde JR, Cardenas ME. 2003. The Tor pathway regulates gene expression by linking nutrient sensing to histone acetylation. Mol. Cell. Biol. 23:629–635.
  • Shi L, Tu BP. 2013. Acetyl-CoA induces transcription of the key G1 cyclin CLN3 to promote entry into the cell division cycle in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. U. S. A. 110:7318–7323.
  • Katada S, Imhof A, Sassone-Corsi P. 2012. Connecting threads: epigenetics and metabolism. Cell 148:24–28.
  • Lau W-TW, Schneider KR, O'Shea EK. 1998. A genetic study of signaling processes for repression of PHO5 transcription in Saccharomyces cerevisiae. Genetics 150:1349–1359.
  • Vogelauer M, Wu J, Suka N, Grunstein M. 2000. Global histone acetylation and deacetylation in yeast. Nature 408:495–498.
  • Kim GW, Yang XJ. 2011. Comprehensive lysine acetylomes emerging from bacteria to humans. Trends Biochem. Sci. 36:211–220.
  • Lee TI, Causton HC, Holstege FC, Shen WC, Hannett N, Jennings EG, Winston F, Green MR, Young RA. 2000. Redundant roles for the TFIID and SAGA complexes in global transcription. Nature 405:701–704.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.