Advertisement

AMPK in Yeast: The SNF1 (Sucrose Non-fermenting 1) Protein Kinase Complex

  • Pascual SanzEmail author
  • Rosa Viana
  • Maria Adelaida Garcia-Gimeno
Chapter
Part of the Experientia Supplementum book series (EXS, volume 107)

Abstract

In yeast, SNF1 protein kinase is the orthologue of mammalian AMPK complex. It is a trimeric complex composed of Snf1 protein kinase (orthologue of AMPKα catalytic subunit), Snf4 (orthologue of AMPKγ regulatory subunit), and a member of the Gal83/Sip1/Sip2 family of proteins (orthologues of AMPKβ subunit) that act as scaffolds and also regulate the subcellular localization of the complex. In this chapter, we review the recent literature on the characteristics of SNF1 complex subunits, the structure and regulation of the activity of the SNF1 complex, its role at the level of transcriptional regulation of relevant target genes and also at the level of posttranslational modification of targeted substrates. We also review the crosstalk of SNF1 complex activity with other key protein kinase pathways such as cAMP–PKA, TORC1, and PAS kinase.

Keywords

Snf1 Snf4 Gal83 Sip1 Sip2 Glucose repression Transcriptional regulation Protein structure analysis Response to cellular stress Posttranslational regulation Energy metabolism Protein kinase 

List of Abbreviations

AID

Autoinhibitory domain

ASC

Association with Snf1 complex

AMPK

AMP-activated protein kinase

CBS

Cystathionine-β-synthase domain

CSRE

Carbon source-responsive element

eIF2α

Eukaryotic initiation factor 2α

GBD

Glycogen-binding domain

KD

Catalytic domain

RD

Regulatory domain

Snf1

sucrose non-fermenting 1

TORC1

Target of rapamycin complex 1

PAS kinase

Protein kinase with a PAS domain

PKA

Protein kinase A

Notes

Acknowledgements

This study was supported by grants from the Spanish Ministry of Education and Science SAF2014-54604-C3-1-R and Generalitat Valenciana (PrometeoII/2014/029) to P.S.

References

  1. Abate G, Bastonini E, Braun KA, Verdone L, Young ET, Caserta M (2012) Snf1/AMPK regulates Gcn5 occupancy, H3 acetylation and chromatin remodelling at S. cerevisiae ADY2 promoter. Biochim Biophys Acta 1819(5):419–427CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ahuatzi D, Riera A, Pelaez R, Herrero P, Moreno F (2007) Hxk2 regulates the phosphorylation state of Mig1 and therefore its nucleocytoplasmic distribution. J Biol Chem 282(7):4485–4493CrossRefPubMedGoogle Scholar
  3. Alepuz PM, Cunningham KW, Estruch F (1997) Glucose repression affects ion homeostasis in yeast through the regulation of the stress-activated ENA1 gene. Mol Microbiol 26(1):91–98CrossRefPubMedGoogle Scholar
  4. Amodeo GA, Rudolph MJ, Tong L (2007) Crystal structure of the heterotrimer core of Saccharomyces cerevisiae AMPK homologue SNF1. Nature 449(7161):492–495CrossRefPubMedGoogle Scholar
  5. Ashrafi K, Lin SS, Manchester JK, Gordon JI (2000) Sip2p and its partner snf1p kinase affect aging in S. cerevisiae. Genes Dev 14(15):1872–1885PubMedPubMedCentralGoogle Scholar
  6. Bertram PG, Choi JH, Carvalho J, Chan TF, Ai W, Zheng XF (2002) Convergence of TOR-nitrogen and Snf1-glucose signaling pathways onto Gln3. Mol Cell Biol 22(4):1246–1252CrossRefPubMedPubMedCentralGoogle Scholar
  7. Calabrese MF, Rajamohan F, Harris MS, Caspers NL, Magyar R, Withka JM, Wang H, Borzilleri KA, Sahasrabudhe PV, Hoth LR, Geoghegan KF, Han S, Brown J, Subashi TA, Reyes AR, Frisbie RK, Ward J, Miller RA, Landro JA, Londregan AT, Carpino PA, Cabral S, Smith AC, Conn EL, Cameron KO, Qiu X, Kurumbail RG (2014) Structural basis for AMPK activation: natural and synthetic ligands regulate kinase activity from opposite poles by different molecular mechanisms. Structure 22(8):1161–1172CrossRefPubMedGoogle Scholar
  8. Casamayor A, Serrano R, Platara M, 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(1):39–49CrossRefPubMedGoogle Scholar
  9. Celenza JL, Carlson M (1984) Cloning and genetic mapping of SNF1, a gene required for expression of glucose-repressible genes in Saccharomyces cerevisiae. Mol Cell Biol 4(1):49–53CrossRefPubMedPubMedCentralGoogle Scholar
  10. Conrad M, Schothorst J, Kankipati HN, Van Zeebroeck G, Rubio-Texeira M, Thevelein JM (2014) Nutrient sensing and signaling in the yeast Saccharomyces cerevisiae. FEMS Microbiol Rev 38(2):254–299CrossRefPubMedPubMedCentralGoogle Scholar
  11. Cullen PJ, Sprague GF Jr (2000) Glucose depletion causes haploid invasive growth in yeast. Proc Natl Acad Sci USA 97(25):13619–13624CrossRefPubMedPubMedCentralGoogle Scholar
  12. Charbon G, Breunig KD, Wattiez R, Vandenhaute J, Noel-Georis I (2004) Key role of Ser562/661 in Snf1-dependent regulation of Cat8p in Saccharomyces cerevisiae and Kluyveromyces lactis. Mol Cell Biol 24(10):4083–4091CrossRefPubMedPubMedCentralGoogle Scholar
  13. Cherkasova V, Qiu H, Hinnebusch AG (2010) Snf1 promotes phosphorylation of the alpha subunit of eukaryotic translation initiation factor 2 by activating Gcn2 and inhibiting phosphatases Glc7 and Sit4. Mol Cell Biol 30(12):2862–2873CrossRefPubMedPubMedCentralGoogle Scholar
  14. Chida T, Ando M, Matsuki T, Masu Y, Nagaura Y, Takano-Yamamoto T, Tamura S, Kobayashi T (2013) N-Myristoylation is essential for protein phosphatases PPM1A and PPM1B to dephosphorylate their physiological substrates in cells. Biochem J 449(3):741–749CrossRefPubMedGoogle Scholar
  15. DeMille D, Badal BD, Evans JB, Mathis AD, Anderson JF, Grose JH (2015) PAS kinase is activated by direct SNF1-dependent phosphorylation and mediates inhibition of TORC1 through the phosphorylation and activation of Pbp1. Mol Biol Cell 26(3):569–582CrossRefPubMedPubMedCentralGoogle Scholar
  16. DeMille D, Bikman BT, Mathis AD, Prince JT, Mackay JT, Sowa SW, Hall TD, Grose JH (2014) A comprehensive protein-protein interactome for yeast PAS kinase 1 reveals direct inhibition of respiration through the phosphorylation of Cbf1. Mol Biol Cell 25(14):2199–2215CrossRefPubMedPubMedCentralGoogle Scholar
  17. Djouder N, Tuerk RD, Suter M, Salvioni P, Thali RF, Scholz R, Vaahtomeri K, Auchli Y, Rechsteiner H, Brunisholz RA, Viollet B, Makela TP, Wallimann T, Neumann D, Krek W (2010) PKA phosphorylates and inactivates AMPKalpha to promote efficient lipolysis. EMBO J 29(2):469–481CrossRefPubMedGoogle Scholar
  18. Fernandez-Garcia P, Pelaez R, Herrero P, Moreno F (2012) Phosphorylation of yeast hexokinase 2 regulates its nucleocytoplasmic shuttling. J Biol Chem 287(50):42151–42164CrossRefPubMedPubMedCentralGoogle Scholar
  19. Ferrer-Dalmau J, Randez-Gil F, Marquina M, Prieto JA, Casamayor A (2015) Protein kinase Snf1 is involved in the proper regulation of the unfolded protein response in Saccharomyces cerevisiae. Biochem J 468(1):33–47CrossRefPubMedGoogle Scholar
  20. Garcia-Haro L, Garcia-Gimeno MA, Neumann D, Beullens M, Bollen M, Sanz P (2010) The PP1-R6 protein phosphatase holoenzyme is involved in the glucose-induced dephosphorylation and inactivation of AMP-activated protein kinase, a key regulator of insulin secretion, in MIN6 beta cells. FASEB J 24(12):5080–5091CrossRefPubMedGoogle Scholar
  21. Grose JH, Smith TL, Sabic H, Rutter J (2007) Yeast PAS kinase coordinates glucose partitioning in response to metabolic and cell integrity signaling. EMBO J 26(23):4824–4830CrossRefPubMedPubMedCentralGoogle Scholar
  22. Grose JH, Sundwall E, Rutter J (2009) Regulation and function of yeast PAS kinase: a role in the maintenance of cellular integrity. Cell Cycle 8(12):1824–1832CrossRefPubMedPubMedCentralGoogle Scholar
  23. Hahn JS, Thiele DJ (2004) Activation of the Saccharomyces cerevisiae heat shock transcription factor under glucose starvation conditions by Snf1 protein kinase. J Biol Chem 279(7):5169–5176CrossRefPubMedGoogle Scholar
  24. Hao HX, Cardon CM, Swiatek W, Cooksey RC, Smith TL, Wilde J, Boudina S, Abel ED, McClain DA, Rutter J (2007) PAS kinase is required for normal cellular energy balance. Proc Natl Acad Sci USA 104(39):15466–15471CrossRefPubMedPubMedCentralGoogle Scholar
  25. Hardie DG, Ashford ML (2014) AMPK: regulating energy balance at the cellular and whole body levels. Physiology (Bethesda) 29(2):99–107Google Scholar
  26. Hardie DG, Carling D, Carlson M (1998) The AMP-activated/SNF1 protein kinase subfamily: metabolic sensors of the eukaryotic cell? Annu Rev Biochem 67:821–855CrossRefPubMedGoogle Scholar
  27. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR, Hardie DG (2003) Complexes between the LKB1 tumor suppressor, STRADalpha/beta and MO25alpha/beta are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2(4):28CrossRefPubMedPubMedCentralGoogle Scholar
  28. Hedbacker K, Carlson M (2006) Regulation of the nucleocytoplasmic distribution of Snf1-Gal83 protein kinase. Eukaryot Cell 5(12):1950–1956CrossRefPubMedPubMedCentralGoogle Scholar
  29. Hedbacker K, Hong SP, Carlson M (2004a) Pak1 protein kinase regulates activation and nuclear localization of Snf1-Gal83 protein kinase. Mol Cell Biol 24(18):8255–8263CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hedbacker K, Townley R, Carlson M (2004b) Cyclic AMP-dependent protein kinase regulates the subcellular localization of Snf1-Sip1 protein kinase. Mol Cell Biol 24(5):1836–1843CrossRefPubMedPubMedCentralGoogle Scholar
  31. Hong SP, Carlson M (2007) Regulation of snf1 protein kinase in response to environmental stress. J Biol Chem 282(23):16838–16845CrossRefPubMedGoogle Scholar
  32. Honigberg SM, Lee RH (1998) Snf1 kinase connects nutritional pathways controlling meiosis in Saccharomyces cerevisiae. Mol Cell Biol 18(8):4548–4555CrossRefPubMedPubMedCentralGoogle Scholar
  33. Hsu HE, Liu TN, Yeh CS, Chang TH, Lo YC, Kao CF (2015) Feedback control of Snf1 protein and its phosphorylation is necessary for adaptation to environmental stress. J Biol Chem 290(27):16786–16796CrossRefPubMedPubMedCentralGoogle Scholar
  34. Hunter T, Plowman GD (1997) The protein kinases of budding yeast: six score and more. Trends Biochem Sci 22(1):18–22CrossRefPubMedGoogle Scholar
  35. Janecek S, Svensson B, Macgregor EA (2011) Structural and evolutionary aspects of two families of non-catalytic domains present in starch and glycogen binding proteins from microbes, plants and animals. Enzym Microb Technol 49(5):429–440CrossRefGoogle Scholar
  36. Jiang R, Carlson M (1996) Glucose regulates protein interactions within the yeast SNF1 protein kinase complex. Genes Dev 10:3105–3115CrossRefPubMedGoogle Scholar
  37. 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 17:2099–2106CrossRefPubMedPubMedCentralGoogle Scholar
  38. Joseph BK, Liu HY, Francisco J, Pandya D, Donigan M, Gallo-Ebert C, Giordano C, Bata A, Nickels JT Jr (2015) Inhibition of AMP kinase by the protein phosphatase 2A heterotrimer, PP2APpp2r2d. J Biol Chem 290(17):10588–10598CrossRefPubMedPubMedCentralGoogle Scholar
  39. Kaps S, Kettner K, Migotti R, Kanashova T, Krause U, Rodel G, Dittmar G, Kriegel TM (2015) Protein kinase Ymr291w/Tda1 is essential for glucose signaling in saccharomyces cerevisiae on the level of hexokinase isoenzyme ScHxk2 phosphorylation*. J Biol Chem 290(10):6243–6255CrossRefPubMedPubMedCentralGoogle Scholar
  40. Kayikci O, Nielsen J (2015) Glucose repression in Saccharomyces cerevisiae. FEMS Yeast Res 15(6):fov068. doi: 10.1093/femsyr/fov068 CrossRefPubMedPubMedCentralGoogle Scholar
  41. Kuchin S, Treich I, Carlson M (2000) A regulatory shortcut between the Snf1 protein kinase and RNA polymerase II holoenzyme. Proc Natl Acad Sci USA 97(14):7916–7920CrossRefPubMedPubMedCentralGoogle Scholar
  42. Kuchin S, Vyas VK, Carlson M (2002) Snf1 protein kinase and the repressors Nrg1 and Nrg2 regulate FLO11, haploid invasive growth, and diploid pseudohyphal differentiation. Mol Cell Biol 22(12):3994–4000CrossRefPubMedPubMedCentralGoogle Scholar
  43. Kulkarni A, Buford TD, Rai R, Cooper TG (2006) Differing responses of Gat1 and Gln3 phosphorylation and localization to rapamycin and methionine sulfoximine treatment in Saccharomyces cerevisiae. FEMS Yeast Res 6(2):218–229CrossRefPubMedPubMedCentralGoogle Scholar
  44. Leech A, Nath N, McCartney RR, Schmidt MC (2003) Isolation of mutations in the catalytic domain of the snf1 kinase that render its activity independent of the snf4 subunit. Eukaryot Cell 2(2):265–273CrossRefPubMedPubMedCentralGoogle Scholar
  45. Lesage P, Yang X, Carlson M (1996) 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 16(5):1921–1928CrossRefPubMedPubMedCentralGoogle Scholar
  46. Li X, Wang L, Zhou XE, Ke J, de Waal PW, Gu X, Tan MH, Wang D, Wu D, Xu HE, Melcher K (2015) Structural basis of AMPK regulation by adenine nucleotides and glycogen. Cell Res 25(1):50–66CrossRefPubMedGoogle Scholar
  47. Lin SS, Manchester JK, Gordon JI (2003) Sip2, an N-myristoylated beta subunit of Snf1 kinase, regulates aging in Saccharomyces cerevisiae by affecting cellular histone kinase activity, recombination at rDNA loci, and silencing. J Biol Chem 278(15):13390–13397CrossRefPubMedGoogle Scholar
  48. 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(6):1073–1084CrossRefPubMedPubMedCentralGoogle Scholar
  49. Lo WS, 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(5532):1142–1146CrossRefPubMedGoogle Scholar
  50. Ludin K, Jiang R, Carlson M (1998) Glucose-regulated interaction of a regulatory subunit of protein phosphatase 1 with the Snf1 protein kinase in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 95(11):6245–6250CrossRefPubMedPubMedCentralGoogle Scholar
  51. Mangat S, Chandrashekarappa D, McCartney RR, Elbing K, Schmidt MC (2010) Differential roles of the glycogen-binding domains of beta subunits in regulation of the Snf1 kinase complex. Eukaryot Cell 9(1):173–183CrossRefPubMedGoogle Scholar
  52. 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, Schmidt MC, Gamblin SJ, Carling D (2011) ADP regulates SNF1, the Saccharomyces cerevisiae homolog of AMP-activated protein kinase. Cell Metab 14(5):707–714CrossRefPubMedPubMedCentralGoogle Scholar
  53. McCartney RR, Rubenstein EM, Schmidt MC (2005) Snf1 kinase complexes with different beta subunits display stress-dependent preferences for the three Snf1-activating kinases. Curr Genet 47(6):335–344CrossRefPubMedGoogle Scholar
  54. 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(39):36460–36466CrossRefPubMedGoogle Scholar
  55. Momcilovic M, Iram SH, Liu Y, Carlson M (2008) Roles of the glycogen-binding domain and Snf4 in glucose inhibition of SNF1 protein kinase. J Biol Chem 283(28):19521–19529CrossRefPubMedPubMedCentralGoogle Scholar
  56. Nayak V, Zhao K, Wyce A, Schwartz MF, Lo WS, Berger SL, Marmorstein R (2006) Structure and dimerization of the kinase domain from yeast Snf1, a member of the Snf1/AMPK protein family. Structure 14(3):477–485CrossRefPubMedGoogle Scholar
  57. Porta C, Paglino C, Mosca A (2014) Targeting PI3K/Akt/mTOR signaling in cancer. Front Oncol 4:64CrossRefPubMedPubMedCentralGoogle Scholar
  58. Roth S, Kumme J, Schuller HJ (2004) Transcriptional activators Cat8 and Sip4 discriminate between sequence variants of the carbon source-responsive promoter element in the yeast Saccharomyces cerevisiae. Curr Genet 45(3):121–128CrossRefPubMedGoogle Scholar
  59. Rubenstein EM, McCartney RR, Zhang C, Shokat KM, Shirra MK, Arndt KM, Schmidt MC (2008) Access denied: Snf1 activation loop phosphorylation is controlled by availability of the phosphorylated threonine 210 to the PP1 phosphatase. J Biol Chem 283(1):222–230CrossRefPubMedGoogle Scholar
  60. Rudolph MJ, Amodeo GA, Bai Y, Tong L (2005) Crystal structure of the protein kinase domain of yeast AMP-activated protein kinase Snf1. Biochem Biophys Res Commun 337(4):1224–1228CrossRefPubMedGoogle Scholar
  61. Ruiz A, Xu X, Carlson M (2011) Roles of two protein phosphatases, Reg1-Glc7 and Sit4, and glycogen synthesis in regulation of SNF1 protein kinase. Proc Natl Acad Sci USA 108(16):6349–6354CrossRefPubMedPubMedCentralGoogle Scholar
  62. Ruiz A, Xu X, Carlson M (2013) Ptc1 protein phosphatase 2C contributes to glucose regulation of SNF1/AMP-activated protein kinase (AMPK) in Saccharomyces cerevisiae. J Biol Chem 288(43):31052–31058CrossRefPubMedPubMedCentralGoogle Scholar
  63. Santangelo GM (2006) Glucose signaling in Saccharomyces cerevisiae. Microbiol Mol Biol Rev 70(1):253–282CrossRefPubMedPubMedCentralGoogle Scholar
  64. 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(4):1321–1328CrossRefPubMedPubMedCentralGoogle Scholar
  65. Schmidt MC, McCartney RR (2000) beta-subunits of Snf1 kinase are required for kinase function and substrate definition. EMBO J 19(18):4936–4943CrossRefPubMedPubMedCentralGoogle Scholar
  66. Shashkova S, Welkenhuysen N, Hohmann S (2015) Molecular communication: crosstalk between the Snf1 and other signaling pathways. FEMS Yeast Res 15(4):fov026CrossRefPubMedGoogle Scholar
  67. Shimobayashi M, Hall MN (2014) Making new contacts: the mTOR network in metabolism and signalling crosstalk. Nat Rev Mol Cell Biol 15(3):155–162CrossRefPubMedGoogle Scholar
  68. Shirra MK, McCartney RR, Zhang C, Shokat KM, Schmidt MC, Arndt KM (2008) A chemical genomics study identifies Snf1 as a repressor of GCN4 translation. J Biol Chem 283(51):35889–35898CrossRefPubMedPubMedCentralGoogle Scholar
  69. Shirra MK, Patton-Vogt J, Ulrich A, Liuta-Tehlivets O, Kohlwein 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(17):5710–5722CrossRefPubMedPubMedCentralGoogle Scholar
  70. Simpson-Lavy KJ, Johnston M (2013) SUMOylation regulates the SNF1 protein kinase. Proc Natl Acad Sci USA 110(43):17432–17437CrossRefPubMedPubMedCentralGoogle Scholar
  71. Smets B, Ghillebert R, De Snijder P, Binda M, Swinnen E, De Virgilio C, Winderickx J (2010) Life in the midst of scarcity: adaptations to nutrient availability in Saccharomyces cerevisiae. Curr Genet 56(1):1–32CrossRefPubMedGoogle Scholar
  72. Soontorngun N, Larochelle M, Drouin S, Robert F, Turcotte B (2007) Regulation of gluconeogenesis in Saccharomyces cerevisiae is mediated by activator and repressor functions of Rds2. Mol Cell Biol 27(22):7895–7905CrossRefPubMedPubMedCentralGoogle Scholar
  73. 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(6):2138–2146CrossRefPubMedPubMedCentralGoogle Scholar
  74. Thompson-Jaeger S, Francois J, Gaughran JP, Tatchell K (1991) Deletion of SNF1 affects the nutrient response of yeast and resembles mutations which activate the adenylate cyclase pathway. Genetics 129(3):697–706PubMedPubMedCentralGoogle Scholar
  75. Treitel MA, Carlson M (1995) Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc Natl Acad Sci USA 92(8):3132–3136CrossRefPubMedPubMedCentralGoogle Scholar
  76. Turcotte B, Liang XB, Robert F, Soontorngun N (2010) Transcriptional regulation of nonfermentable carbon utilization in budding yeast. FEMS Yeast Res 10(1):2–13CrossRefPubMedGoogle Scholar
  77. Viana R, Towler MC, Pan DA, Carling D, Viollet B, Hardie DG, Sanz P (2007) A conserved sequence immediately N-terminal to the Bateman domains in AMP-activated protein kinase gamma subunits is required for the interaction with the beta subunits. J Biol Chem 282(22):16117–16125CrossRefPubMedPubMedCentralGoogle Scholar
  78. Vincent O, Carlson M (1999) Gal83 mediates the interaction of the Snf1 kinase complex with the transcription activator Sip4. EMBO J 18(23):6672–6681CrossRefPubMedPubMedCentralGoogle Scholar
  79. Vincent O, Townley R, Kuchin S, Carlson M (2001) Subcellular localization of the Snf1 kinase is regulated by specific beta subunits and a novel glucose signaling mechanism. Genes Dev 15(9):1104–1114CrossRefPubMedPubMedCentralGoogle Scholar
  80. Wang Z, Wilson WA, Fujino MA, Roach PJ (2001) Antagonistic controls of autophagy and glycogen accumulation by Snf1p, the yeast homolog of AMP-activated protein kinase, and the cyclin- dependent kinase Pho85p. Mol Cell Biol 21(17):5742–5752CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wiatrowski HA, Van Denderen BJ, Berkey CD, Kemp BE, Stapleton D, Carlson M (2004) Mutations in the gal83 glycogen-binding domain activate the snf1/gal83 kinase pathway by a glycogen-independent mechanism. Mol Cell Biol 24(1):352–361CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wilson MA, Koutelou E, Hirsch C, Akdemir K, Schibler A, Barton MC, Dent SY (2011) Ubp8 and SAGA regulate Snf1 AMP kinase activity. Mol Cell Biol 31(15):3126–3135CrossRefPubMedPubMedCentralGoogle Scholar
  83. Wilson WA, Hawley SA, Hardie DG (1996) Glucose repression/derepression in budding yeast: SNF1 protein kinase is activated by phosphorylation under derepressing conditions, and this correlates with a high AMP:ATP ratio. Curr Biol 6(11):1426–1434CrossRefPubMedGoogle Scholar
  84. Wilson WA, Skurat AV, Probst B, de Paoli-Roach A, Roach PJ, Rutter J (2005) Control of mammalian glycogen synthase by PAS kinase. Proc Natl Acad Sci USA 102(46):16596–16601CrossRefPubMedPubMedCentralGoogle Scholar
  85. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D (2005) C(Ca2+)/calmodulin-dependent protein kinase kinase-beta acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2(1):21–33CrossRefPubMedGoogle Scholar
  86. Woods A, Johnstone SR, Dickerson K, Leiper FC, Fryer LG, Neumann D, Schlattner U, Wallimann T, Carlson M, Carling D (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13(22):2004–2008CrossRefPubMedGoogle Scholar
  87. 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(30):19509–19515PubMedGoogle Scholar
  88. Xiao B, Sanders MJ, Carmena D, Bright NJ, Haire LF, Underwood E, Patel BR, Heath RB, Walker PA, Hallen S, Giordanetto F, Martin SR, Carling D, Gamblin SJ (2013) Structural basis of AMPK regulation by small molecule activators. Nat Commun 4:3017PubMedPubMedCentralGoogle Scholar
  89. Xiao B, Sanders MJ, Underwood E, Heath R, Mayer FV, Carmena D, Jing C, Walker PA, Eccleston JF, Haire LF, Saiu P, Howell SA, Aasland R, Martin SR, Carling D, Gamblin SJ (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472(7342):230–233CrossRefPubMedPubMedCentralGoogle Scholar
  90. Yao Y, Tsuchiyama S, Yang C, Bulteau AL, He C, Robison B, Tsuchiya M, Miller D, Briones V, Tar K, Potrero A, Friguet B, Kennedy BK, Schmidt M (2015) Proteasomes, Sir2, and Hxk2 form an interconnected aging network that impinges on the AMPK/Snf1-regulated transcriptional repressor Mig1. PLoS Genet 11(1), e1004968CrossRefPubMedPubMedCentralGoogle Scholar
  91. 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(Pt 9):2814–2826CrossRefPubMedGoogle Scholar
  92. 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(28):26146–26158CrossRefPubMedGoogle Scholar
  93. Zhang J, Olsson L, Nielsen J (2010) The beta-subunits of the Snf1 kinase in Saccharomyces cerevisiae, Gal83 and Sip2, but not Sip1, are redundant in glucose derepression and regulation of sterol biosynthesis. Mol Microbiol 77(2):371–383CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2016

Authors and Affiliations

  • Pascual Sanz
    • 1
    Email author
  • Rosa Viana
    • 1
  • Maria Adelaida Garcia-Gimeno
    • 2
  1. 1.Instituto de Biomedicina de Valencia, CSIC and Centro de Investigación Biomédica en Red de Enfermedades Raras (CIBERER-ISCiii)ValenciaSpain
  2. 2.Department of BiotecnologíaEscuela Técnica Superior de Ingeniería Agronómica y del Medio Natural (ETSIAMN), Universitat Politécnica de ValenciaValenciaSpain

Personalised recommendations