Glucose de-repression by yeast AMP-activated protein kinase SNF1 is controlled via at least two independent steps

FEBS Journal

Volumn 281, Issue 7, 2014, Pages 1901-1917

  García Salcedo, Raúl ^a,d   Lubitz, Timo ^b   Beltran, Gemma ^a,e   Elbing, Karin ^a,f   Tian, Ye ^a   Frey, Simone ^c   Wolkenhauer, Olaf ^c   Krantz, Marcus ^b   Klipp, Edda ^b   Hohmann, Stefan ^a  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b HUMBOLDT UNIVERSITY   (Germany)

^c UNIVERSITY OF ROSTOCK   (Germany)

^d UNIVERSITY OF OVIEDO   (Spain)

^e UNIVERSITAT ROVIRA I VIRGILI   (Spain)

^f LUND UNIVERSITY   (Sweden)

Author keywords

AMPK SNF1; glucose repression; metabolic regulation; quantitative analysis protein kinase

Indexed keywords

BETA FRUCTOFURANOSIDASE; FUNGAL RNA; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; PROTEIN MIG1; PROTEIN SAK1; PROTEIN SNF1; UNCLASSIFIED DRUG;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FUNGAL STRAIN; FUNGUS GROWTH; GENE DOSAGE; GLUCOSE METABOLISM; GLUCOSE REPRESSION; MATHEMATICAL MODEL; NONHUMAN; PLASMID; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; REGULATORY MECHANISM; RNA EXTRACTION; WESTERN BLOTTING;

EUKARYOTA;

AMPK/SNF1; GLUCOSE REPRESSION; METABOLIC REGULATION; QUANTITATIVE ANALYSIS PROTEIN KINASE;

GLUCOSE; KINETICS; MODELS, BIOLOGICAL; PHOSPHORYLATION; PROTEIN PHOSPHATASE 1; PROTEIN-SERINE-THREONINE KINASES; REPRESSOR PROTEINS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 84897480343     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/febs.12753     Document Type: Article

References (86)

1. Hardie DG, Ross FA, &, Hawley SA, (2012) AMPK: a nutrient and energy sensor that maintains energy homeostasis. Nat Rev Mol Cell Biol 13, 251-262.
2. Carling D, Mayer FV, Sanders MJ, &, Gamblin SJ, (2011) AMP-activated protein kinase: nature's energy sensor. Nat Chem Biol 7, 512-518.
3. Broach JR, (2012) Nutritional control of growth and development in yeast. Genetics 192, 73-105.
4. Ghillebert R, Swinnen E, Wen J, Vandesteene L, Ramon M, Norga K, Rolland F, &, Winderickx J, (2011) The AMPK/SNF1/SnRK1 fuel gauge and energy regulator: structure, function and regulation. FEBS J 278, 3978-3990.
5. Hardie DG, (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8, 774-785. (Pubitemid 47462132)
6. Hedbacker K, &, Carlson M, (2008) SNF1/AMPK pathways in yeast. Front Biosci 13, 2408-2420. (Pubitemid 351599694)
7. 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, 1-32.
8. Usaite R, Jewett MC, Oliveira AP, Yates JR III, Olsson L, &, Nielsen J, (2009) Reconstruction of the yeast Snf1 kinase regulatory network reveals its role as a global energy regulator. Mol Syst Biol 5, 319.
9. 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 USA 100, 8839-8843. (Pubitemid 36899185)
10. Nath N, McCartney RR, &, Schmidt MC, (2003) Yeast Pak1 kinase associates with and activates Snf1. Mol Cell Biol 23, 3909-3917. (Pubitemid 36597469)
11. Sutherland CM, Hawley SA, McCartney RR, Leech A, Stark MJ, Schmidt MC, &, Hardie DG, (2003) Elm1p is one of three upstream kinases for the Saccharomyces cerevisiae SNF1 complex. Curr Biol 13, 1299-1305. (Pubitemid 36953302)
12. Liu Y, Xu X, &, Carlson M, (2011) Interaction of SNF1 protein kinase with its activating kinase Sak1. Eukaryot Cell 10, 313-319.
13. Tu J, &, Carlson M, (1994) The GLC7 type 1 protein phosphatase is required for glucose repression in Saccharomyces cerevisiae. Mol Cell Biol 14, 6789-6796. (Pubitemid 24299748)
14. 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. (Pubitemid 30069253)
15. Tu J, &, Carlson M, (1995) REG1 binds to protein phosphatase type 1 and regulates glucose repression in Saccharomyces cerevisiae. EMBO J 14, 5939-5946.
16. 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. (Pubitemid 37384256)
17. Frederick DL, &, Tatchell K, (1996) The REG2 gene of Saccharomyces cerevisiae encodes a type 1 protein phosphatase-binding protein that functions with Reg1p and the Snf1 protein kinase to regulate growth. Mol Cell Biol 16, 2922-2931. (Pubitemid 26161298)
18. 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, 31052-31058.
19. Ruiz A, Liu Y, Xu X, &, Carlson M, (2012) Heterotrimer-independent regulation of activation-loop phosphorylation of Snf1 protein kinase involves two protein phosphatases. Proc Natl Acad Sci USA 109, 8652-8657.
20. 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, 6349-6354.
21. 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, 222-230.
22. Gowans GJ, &, Hardie DG, (2014) AMPK: a cellular energy sensor primarily regulated by AMP. Biochem Soc Trans 42, 71-75.
23. Gowans GJ, Hawley SA, Ross FA, &, Hardie DG, (2013) AMP is a true physiological regulator of AMP-activated protein kinase by both allosteric activation and enhancing net phosphorylation. Cell Metab 18, 556-566.
24. Carling D, Thornton C, Woods A, &, Sanders MJ, (2012) AMP-activated protein kinase: new regulation, new roles? Biochem J 445, 11-27.
25. Xiao B, Sanders MJ, Underwood E, Heath R, Mayer FV, Carmena D, Jing C, Walker PA, Eccleston JF, Haire LF, et al,. (2011) Structure of mammalian AMPK and its regulation by ADP. Nature 472, 230-233.
26. Mayer FV, Heath R, Underwood E, Sanders MJ, Carmena D, McCartney RR, Leiper FC, Xiao B, Jing C, Walker PA, et al,. (2011) ADP regulates SNF1, the Saccharomyces cerevisiae homolog of AMP-activated protein kinase. Cell Metab 14, 707-714.
27. Chandrashekarappa DG, McCartney RR, &, Schmidt MC, (2013) Ligand binding to the AMP-activated protein kinase active site mediates protection of the activation loop from dephosphorylation. J Biol Chem 288, 89-98.
28. 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. (Pubitemid 28500518)
29. Ostling J, &, Ronne H, (1998) Negative control of the Mig1p repressor by Snf1p-dependent phosphorylation in the absence of glucose. Eur J Biochem 252, 162-168. (Pubitemid 28089972)
30. 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. (Pubitemid 29335504)
31. Baker SH, Frederick DL, Bloecher A, &, Tatchell K, (1997) Alanine-scanning mutagenesis of protein phosphatase type 1 in the yeast Saccharomyces cerevisiae. Genetics 145, 615-626. (Pubitemid 27108017)
32. 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, 4485-4493. (Pubitemid 47100982)
33. 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. (Pubitemid 38618278)
34. Ahuatzi D, Herrero P, de la Cera T, &, Moreno F, (2004) The glucose-regulated nuclear localization of hexokinase 2 in Saccharomyces cerevisiae is Mig1-dependent. J Biol Chem 279, 14440-14446. (Pubitemid 38468986)
35. 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.
36. Pasula S, Jouandot D II, &, Kim JH, (2007) Biochemical evidence for glucose-independent induction of HXT expression in Saccharomyces cerevisiae. FEBS Lett 581, 3230-3234. (Pubitemid 46977369)
37. Neigeborn L, &, Carlson M, (1984) Genes affecting the regulation of SUC2 gene expression by glucose repression in Saccharomyces cerevisiae. Genetics 108, 845-858. (Pubitemid 15178605)
38. Sarokin L, &, Carlson M, (1984) Upstream region required for regulated expression of the glucose-repressible SUC2 gene of Saccharomyces cerevisiae. Mol Cell Biol 4, 2750-2757. (Pubitemid 15113614)
39. Sarokin L, &, Carlson M, (1985) Upstream region of the SUC2 gene confers regulated expression to a heterologous gene in Saccharomyces cerevisiae. Mol Cell Biol 5, 2521-2526. (Pubitemid 15249535)
40. Needham PG, &, Trumbly RJ, (2006) In vitro characterization of the Mig1 repressor from Saccharomyces cerevisiae reveals evidence for monomeric and higher molecular weight forms. Yeast 23, 1151-1166. (Pubitemid 46002046)
41. Cannon JF, (2010) Function of protein phosphatase-1, Glc7, in Saccharomyces cerevisiae. Adv Appl Microbiol 73, 27-59.
42. Zhang Y, McCartney RR, Chandrashekarappa DG, Mangat S, &, Schmidt MC, (2011) Reg1 protein regulates phosphorylation of all three Snf1 isoforms but preferentially associates with the Gal83 isoform. Eukaryot Cell 10, 1628-1636.
43. Huang D, Chun KT, Goebl MG, &, Roach PJ, (1996) Genetic interactions between REG1/HEX2 and GLC7, the gene encoding the protein phosphatase type 1 catalytic subunit in Saccharomyces cerevisiae. Genetics 143, 119-127. (Pubitemid 26136977)
44. Frey S, Sott K, Smedh M, Millat T, Dahl P, Wolkenhauer O, &, Goksor M, (2011) A mathematical analysis of nuclear intensity dynamics for Mig1-GFP under consideration of bleaching effects and background noise in Saccharomyces cerevisiae. Mol BioSyst 7, 215-223.
45. Eriksson E, Sott K, Lundqvist F, Sveningsson M, Scrimgeour J, Hanstorp D, Goksor M, &, Graneli A, (2010) A microfluidic device for reversible environmental changes around single cells using optical tweezers for cell selection and positioning. Lab Chip 10, 617-625.
46. Maiwald T, &, Timmer J, (2008) Dynamical modeling and multi-experiment fitting with PottersWheel. Bioinformatics 24, 2037-2043.
47. Hong SP, &, Carlson M, (2007) Regulation of snf1 protein kinase in response to environmental stress. J Biol Chem 282, 16838-16845. (Pubitemid 47093244)
48. Orlova M, Kanter E, Krakovich D, &, Kuchin S, (2006) Nitrogen availability and TOR regulate the Snf1 protein kinase in Saccharomyces cerevisiae. Eukaryot Cell 5, 1831-1837.
49. 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. (Pubitemid 24233479)
50. 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, 1426-1434. (Pubitemid 27012241)
51. Estruch F, Treitel MA, Yang X, &, Carlson M, (1992) N-terminal mutations modulate yeast SNF1 protein kinase function. Genetics 132, 639-650.
52. Schmidt MC, &, McCartney RR, (2000) Beta-subunits of Snf1 kinase are required for kinase function and substrate definition. EMBO J 19, 4936-4943.
53. Yang X, Jiang R, &, Carlson M, (1994) A family of proteins containing a conserved domain that mediates interaction with the yeast SNF1 protein kinase complex. EMBO J 13, 5878-5886.
54. Celenza JL, &, Carlson 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. (Pubitemid 19275974)
55. 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, 1104-1114. (Pubitemid 32417303)
56. Frohlich KU, Entian KD, &, Mecke D, (1985) The primary structure of the yeast hexokinase PII gene (HXK2) which is responsible for glucose repression. Gene 36, 105-111. (Pubitemid 15010949)
57. Lobo Z, &, Maitra PK, (1977) Genetics of yeast hexokinase. Genetics 86, 727-744. (Pubitemid 8184442)
58. Lobo Z, &, Maitra PK, (1977) Resistance to 2-deoxyglucose in yeast: a direct selection of mutants lacking glucose-phosphorylating enzymes. Mol Gen Genet 157, 297-300.
59. Fernandez-Garcia P, Pelaez R, Herrero P, &, Moreno F, (2012) Phosphorylation of yeast hexokinase 2 regulates its nucleocytoplasmic shuttling. J Biol Chem 287, 42151-42164.
60. Pelaez R, Herrero P, &, Moreno F, (2010) Functional domains of yeast hexokinase 2. Biochem J 432, 181-190.
61. Moreno F, Ahuatzi D, Riera A, Palomino CA, &, Herrero P, (2005) Glucose sensing through the Hxk2-dependent signalling pathway. Biochem Soc Trans 33, 265-268. (Pubitemid 40313817)
62. Chandrashekarappa DG, McCartney RR, &, Schmidt MC, (2011) Subunit and domain requirements for adenylate-mediated protection of Snf1 kinase activation loop from dephosphorylation. J Biol Chem 286, 44532-44541.
63. Rubenstein EM, McCartney RR, &, Schmidt MC, (2006) Regulatory domains of Snf1-activating kinases determine pathway specificity. Eukaryot Cell 5, 620-627.
64. Barrett L, Orlova M, Maziarz M, &, Kuchin S, (2012) Protein kinase A contributes to the negative control of Snf1 protein kinase in Saccharomyces cerevisiae. Eukaryot Cell 11, 119-128.
65. Jiang H, Tatchell K, Liu S, &, Michels CA, (2000) Protein phosphatase type-1 regulatory subunits Reg1p and Reg2p act as signal transducers in the glucose-induced inactivation of maltose permease in Saccharomyces cerevisiae. Mol Gen Genet 263, 411-422.
66. Jin C, Barrientos A, Epstein CB, Butow RA, &, Tzagoloff A, (2007) SIT4 regulation of Mig1p-mediated catabolite repression in Saccharomyces cerevisiae. FEBS Lett 581, 5658-5663. (Pubitemid 350179778)
67. Maeda T, Wurgler-Murphy SM, &, Saito H, (1994) A two-component system that regulates an osmosensing MAP kinase cascade in yeast. Nature 369, 242-245. (Pubitemid 24154803)
68. Maeda T, Tsai AY, &, Saito H, (1993) Mutations in a protein tyrosine phosphatase gene (PTP2) and a protein serine/threonine phosphatase gene (PTC1) cause a synthetic growth defect in Saccharomyces cerevisiae. Mol Cell Biol 13, 5408-5417. (Pubitemid 23260644)
69. Ostling J, Carlberg M, &, Ronne H, (1996) Functional domains in the Mig1 repressor. Mol Cell Biol 16, 753-761. (Pubitemid 26061644)
70. Treitel MA, &, Carlson M, (1995) Repression by SSN6-TUP1 is directed by MIG1, a repressor/activator protein. Proc Natl Acad Sci USA 92, 3132-3136.
71. Johnston M, Flick JS, &, Pexton T, (1994) Multiple mechanisms provide rapid and stringent glucose repression of GAL gene expression in Saccharomyces cerevisiae. Mol Cell Biol 14, 3834-3841. (Pubitemid 24160790)
72. Nehlin JO, Carlberg M, &, Ronne H, (1991) Control of yeast GAL genes by MIG1 repressor: a transcriptional cascade in the glucose response. EMBO J 10, 3373-3377. (Pubitemid 21905362)
73. Castermans D, Somers I, Kriel J, Louwet W, Wera S, Versele M, Janssens V, &, Thevelein JM, (2012) Glucose-induced posttranslational activation of protein phosphatases PP2A and PP1 in yeast. Cell Res 22, 1058-1077.
74. Sherman F, Fink GR, &, Hicks JB, (1986) Laboratory Course Manual for Methods in Yeast Genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
75. Elbing K, Rubenstein EM, McCartney RR, &, Schmidt MC, (2006) Subunits of the Snf1 kinase heterotrimer show interdependence for association and activity. J Biol Chem 281, 26170-26180. (Pubitemid 44401824)
76. Gari 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. (Pubitemid 27285747)
77. Gueldener U, Heinisch J, Koehler GJ, Voss D, &, Hegemann JH, (2002) A second set of loxP marker cassettes for Cre-mediated multiple gene knockouts in budding yeast. Nucleic Acids Res 30, e23.
78. Shaner NC, Campbell RE, Steinbach PA, Giepmans BN, Palmer AE, &, Tsien RY, (2004) Improved monomeric red, orange and yellow fluorescent proteins derived from Discosoma sp. red fluorescent protein. Nat Biotechnol 22, 1567-1572. (Pubitemid 40039460)
79. Carling D, Aguan K, Woods A, Verhoeven AJ, Beri RK, Brennan CH, Sidebottom C, Davison MD, &, Scott J, (1994) Mammalian AMP-activated protein kinase is homologous to yeast and plant protein kinases involved in the regulation of carbon metabolism. J Biol Chem 269, 11442-11448. (Pubitemid 24200360)
80. Goldstein A, &, Lampen JO, (1975) Beta-D-fructofuranoside fructohydrolase from yeast. Methods Enzymol 42, 504-511.
81. Hohmann S, &, Zimmermann FK, (1986) Cloning and expression on a multicopy vector of five invertase genes of Saccharomyces cerevisiae. Curr Genet 11, 217-225.
82. Lind K, &, Norbeck J, (2007) Immuno-qPCR detection of the tandem affinity purification (TAP)-tag as a sensitive and accurate tool suitable for large-scale protein quantification. Proteomics 7, 4414-4423.
83. Keating SM, Bornstein BJ, Finney A, &, Hucka M, (2006) SBMLToolbox: an SBML toolbox for MATLAB users. Bioinformatics 22, 1275-1277. (Pubitemid 43779023)
84. Akaike H, (1987) Factor analysis and AIC. Psychometrika 52, 317-332.
85. Mulholland H, &, Jones CR, (1968) Chi-squared distribution. In Fundamentals of Statistics (, Mulholland H, &, Jones CR, eds), pp. 178-200. Springer, New York.
86. Burnham KP, &, Anderson DR, (2002) Model Selection and Multimodel Inference: A Practical Information-Theoretic Approach. Springer, Heidelberg.