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Role of AMP-activated protein kinase in metabolic depression in animals

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Abstract

AMP-activated protein kinase (AMPK) is a highly conserved eukaryotic protein serine/threonine kinase that controls cellular and whole body energy homoeostasis. AMPK is activated during energy stress by a rise in AMP:ATP ratio and maintains energy balance by phosphorylating targets to switch on catabolic ATP-generating pathways, while at the same time switching off anabolic ATP-consuming processes. Metabolic depression is a strategy used by many animals to survive environmental stress and has been extensively studied across phylogeny by comparative biochemists and physiologists, but the role of AMPK has only recently been addressed. This review first deals with the evolution of AMPK in eukaryotes (excluding plants and fungi) and its regulation. Changes in adenine nucleotides and AMPK activation are described in animals during environmental energy stress, before considering the involvement of AMPK in controlling β-oxidation, fatty acid synthesis, triacylglycerol mobilization and protein synthesis. Lastly, strategies are presented to validate the role of AMPK in mediating metabolic depression by phosphorylating downstream targets.

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References

  • Ahmadian M, Abbott MJ, Tang T, Hudak CS, Kim Y, Bruss M, Hellerstein MK, Lee HY, Samuel VT, Shulman GI, Wang Y, Duncan RE, Kang C, Sul HS (2011) Desnutrin/ATGL is regulated by AMPK and is required for a brown adipose phenotype. Cell Metab 13:739–748

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Andersen MN, Rasmussen HB (2012) AMPK: a regulator of ion channels. Commun Integr Biol 5:480–484

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Apfeld J, O’Connor G, McDonagh T, DiStefano PS, Curtis R (2004) The AMP-activated protein kinase AAK-2 links energy levels and insulin-like signals to lifespan in C. elegans. Genes Dev 18:3004–3009

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Arrese EL, Patel RT, Soulages JL (2006) The main triglyceride-lipase from the insect fat body is an active phospholipase A(1): identification and characterization. J Lipid Res 47:2656–2667

    Article  CAS  PubMed  Google Scholar 

  • Atkinson DE, Walton GM (1967) Adenosine triphosphate conservation in metabolic regulation. Rat liver citrate cleavage enzyme. J Biol Chem 242:3239–3241

    CAS  PubMed  Google Scholar 

  • Bain J, Plater L, Elliott M, Shpiro N, Hastie CJ, McLauchlan H, Klevernic I, Arthur JS, Alessi DR, Cohen P (2007) The selectivity of protein kinase inhibitors: a further update. Biochem J 408:297–315

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Barber MC, Price NT, Travers MT (2005) Structure and regulation of acetyl-CoA carboxylase genes of metazoa. Biochim Biophys Acta 1733:1–28

    Article  CAS  PubMed  Google Scholar 

  • Bartrons M, Ortega E, Obach M, Calvo MN, Navarro-Sabate A, Bartrons R (2004) Activation of AMP-dependent protein kinase by hypoxia and hypothermia in the liver of frog Rana perezi. Cryobiology 49:190–194

    Article  CAS  PubMed  Google Scholar 

  • Bauwens JD, Schmuck EG, Lindholm CR, Ertel RL, Mulligan JD, Hovis I, Viollet B, Saupe KW (2011) Cold tolerance, cold-induced hyperphagia, and nonshivering thermogenesis are normal in alpha(1)-AMPK-/- mice. Am J Physiol Regul Integr Comp Physiol 301:R473–R483

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bishop T, St-Pierre J, Brand MD (2002) Primary causes of decreased mitochondrial oxygen consumption during metabolic depression in snail cells. Am J Physiol Regul Integr Comp Physiol 282:R372–R382

    Article  CAS  PubMed  Google Scholar 

  • Boutilier RG (2001) Mechanisms of cell survival in hypoxia and hypothermia. J Exp Biol 204:3171–3181

    CAS  PubMed  Google Scholar 

  • Brown JCL, Staples JF (2014) Substrate-specific changes in mitochondrial respiration in skeletal and cardiac muscle of hibernating thirteen-lined ground squirrels. J Comp Physiol B 184:401–414

    Article  CAS  PubMed  Google Scholar 

  • Brown JC, Chung DJ, Cooper AN, Staples JF (2013) Regulation of succinate-fuelled mitochondrial respiration in liver and skeletal muscle of hibernating thirteen-lined ground squirrels. J Exp Biol 216:1736–1743

    Article  PubMed  Google Scholar 

  • Bruss MD, Arias EB, Lienhard GE, Cartee GD (2005) Increased phosphorylation of Akt substrate of 160 kDa (AS160) in rat skeletal muscle in response to insulin or contractile activity. Diabetes 54:41–50

    Article  CAS  PubMed  Google Scholar 

  • Buck LT, Land SC, Hochachka PW (1993) Anoxia-tolerant hepatocytes: model system for study of reversible metabolic suppression. Am J Physiol 265:R49–R56

    CAS  PubMed  Google Scholar 

  • Burgess SC, Iizuka K, Jeoung NH, Harris RA, Kashiwaya Y, Veech RL, Kitazume T, Uyeda K (2008) Carbohydrate-response element-binding protein deletion alters substrate utilization producing an energy-deficient liver. J Biol Chem 283:1670–1678

    Article  CAS  PubMed  Google Scholar 

  • Buttgereit F, Brand MD (1995) A hierarchy of ATP-consuming processes in mammalian cells. Biochem J 312:163–167

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chung DJ, Szyszka B, Brown JC, Hüner NP, Staples JF (2013) Changes in the mitochondrial phosphoproteome during mammalia hibernation. Physiol Genomics 45:389–399

    Article  CAS  PubMed  Google Scholar 

  • Churchill TA, Storey KB (1989) Intermediary energy metabolism during dormancy and anoxia in the land snail Otala lactea. J Physiol Zool 62:1015–1030

    Article  Google Scholar 

  • Churchill TA, Storey KB (1994) Effects of dehydration on organ metabolism in the frog Pseudacris crucifer: hyperglycemic responses to dehydration mimic freezing-induced cryoprotectant production. J Comp Physiol B 164:492–498

    Article  CAS  PubMed  Google Scholar 

  • Churchill TA, Busza AL, Fuller BJ (1997) Energy metabolism in liver of anoxia-tolerant turtle species (Pseudemys scripta): a model for studying hepatic tolerance to cold hypoxia. Cryobiology 35:14–19

    Article  CAS  PubMed  Google Scholar 

  • 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 38:254–299

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Daval M, Diot-Dupuy F, Bazin R, Hainault I, Viollet B, Vaulont S, Hajduch E, Ferre P, Foufelle F (2005) Anti-lipolytic action of AMP-activated protein kinase in rodent adipocytes. J Biol Chem 280:25250–25257

    Article  CAS  PubMed  Google Scholar 

  • Donohoe PH, West TG, Boutilier RG (1998) Respiratory, metabolic, and acid-base correlates of aerobic metabolic rate reduction in overwintering frogs. Am J Physiol 274:R704–R710

    CAS  PubMed  Google Scholar 

  • English TE, Storey KB (2000) Enzymes of adenylate metabolism and their role in hibernation of the white-tailed prairie dog, Cynomys leucurus. Arch Biochem Biophys 376:91–100

    Article  CAS  PubMed  Google Scholar 

  • Florant GL, Healy JE (2012) The regulation of food intake in mammalian hibernators: a review. J Comp Physiol B 182:451–467

    Article  CAS  PubMed  Google Scholar 

  • Frerichs KU, Smith CB, Brenner M, DeGracia DJ, Krause GS, Marrone L, Dever TE, Hallenbeck JM (1998) Suppression of protein synthesis in brain during hibernation involves inhibition of protein initiation and elongation. Proc Natl Acad Sci U S A 95(24):14511–14516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Freschi L, Osseni M, Landry CR (2014) Functional divergence and evolutionary turnover in mammalian phosphoproteomes. PLoS Genet 10:e1004062

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Fulco M, Sartorelli V (2008) Comparing and contrasting the roles of AMPK and SIRT1 in metabolic tissues. Cell Cycle 7:3669–3679

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Galli GLJ, Lau GY, Richards JG (2013) Beating oxygen: chronic anoxic exposure reduces mitochondrial F1FO-ATPase activity in turtle (Trachemys scripta) heart. J Exp Biol 216:3283–3293

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gauthier MS, Miyoshi H, Souza SC, Cacicedo JM, Saha AK, Greenberg AS, Ruderman NB (2008) AMP-activated protein kinase is activated as a consequence of lipolysis in the adipocyte: potential mechanism and physiological relevance. J Biol Chem 283:16514–16524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grabek KR, Martin SL, Hindle AG (2015) Proteomics approaches shed new light on hibernation physiology. J Comp Physiol B (in press)

  • Guppy M (2004) The biochemistry of metabolic depression: a history of perceptions. Comp Biochem Physiol B: Biochem Mol Biol 139:435–442

    Article  CAS  Google Scholar 

  • Guppy M, Withers P (1999) Metabolic depression in animals: physiological perspectives and biochemical generalizations. Biol Rev Camb Philos Soc 74:1–40

    Article  CAS  PubMed  Google Scholar 

  • Guppy M, Reeves DC, Bishop T, Withers P, Buckingham JA, Brand MD (2000) Intrinsic metabolic depression in cells isolated from the hepatopancreas of estivating snails. FASEB J 14:999–1004

    CAS  PubMed  Google Scholar 

  • Gwinn DM, Shackelford DB, Egan DF, Mihaylova MM, Mery A, Vasquez DS, Turk BE, Shaw RJ (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30:214–226

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hand SC, Menze MA, Borcar A, Patil Y, Covi JA, Reynolds JA, Toner M (2011) Metabolic restructuring during energy-limited states: insights from Artemia franciscana embryos and other animals. J Insect Physiol 57:584–594

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardie DG (2007) AMP-activated/SNF1 protein kinases: conserved guardians of cellular energy. Nat Rev Mol Cell Biol 8:774–785

    Article  CAS  PubMed  Google Scholar 

  • Hardie DG (2011) AMP-activated protein kinase: an energy sensor that regulates all aspects of cell function. Genes Dev 25:1895–1908

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hardie DG (2014) AMPK–sensing energy while talking to other signaling pathways. Cell Metab 20:939–952

    Article  CAS  PubMed  Google Scholar 

  • Healy JE, Gearhart CN, Bateman JL, Handa RJ, Florant GL (2011) AMPK and ACC change with fasting and physiological condition in euthermic and hibernating golden-mantled ground squirrels (Callospermophilus lateralis). Comp Biochem Physiol A: Mol Integr Physiol 159:322–331

    Article  CAS  Google Scholar 

  • Hindle AG, Grabek KR, Epperson LE, Karimpour-Fard A, Martin SL (2014) Metabolic changes associated with the long winter fast dominate the liver proteome in 13-lined ground squirrels. Physiol Genomics 46(10):348–361

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hochachka PW, Buck LT, Doll CJ, Land SC (1996) Unifying theory of hypoxia tolerance: molecular/metabolic defense and rescue mechanisms for surviving oxygen lack. Proc Natl Acad Sci U S A 93:9493–9498

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Horman S, Browne G, Krause U, Patel J, Vertommen D, Bertrand L, Lavoinne A, Hue L, Proud C, Rider MH (2002) Activation of AMP-activated protein kinase leads to the phosphorylation of elongation factor 2 and an inhibition of protein synthesis. Curr Biol 12:1419–1423

    Article  CAS  PubMed  Google Scholar 

  • Horman S, Beauloye C, Vertommen D, Vanoverschelde JL, Hue L, Rider MH (2003) Myocardial ischemia and increased heart work modulate the phosphorylation state of eukaryotic elongation factor-2. J Biol Chem 278:41970–41976

    Article  CAS  PubMed  Google Scholar 

  • Horman S, Hussain N, Dilworth SM, Storey KB, Rider MH (2005) Evaluation of the role of AMP-activated protein kinase and its downstream targets in mammalian hibernation. Comp Biochem Physiol B: Biochem Mol Biol 142:374–382

    Article  CAS  Google Scholar 

  • Horne I, Haritos VS, Oakeshott JG (2009) Comparative and functional genomics of lipases in holometabolous insects. Insect Biochem Mol Biol 39:547–567

    Article  CAS  PubMed  Google Scholar 

  • Hue L, Rider MH (2007) The AMP-activated protein kinase: more than an energy sensor. Essays Biochem 43:121–137

    Article  CAS  PubMed  Google Scholar 

  • Inoki K, Zhu T, Guan KL (2003) TSC2 mediates cellular energy response to control cell growth and survival. Cell 115:577–590

    Article  CAS  PubMed  Google Scholar 

  • Jibb LA, Richards JG (2008) AMP-activated protein kinase activity during metabolic rate depression in the hypoxic goldfish, Carassius auratus. J Exp Biol 211:3111–3122

    Article  CAS  PubMed  Google Scholar 

  • Johnson EC, Kazgan N, Bretz CA, Forsberg LJ, Hector CE, Worthen RJ, Onyenwoke R, Brenman JE (2010) Altered metabolism and persistent starvation behaviors caused by reduced AMPK function in Drosophila. PLoS ONE 5:e12799

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Kahn BB, Alquier T, Carling D, Hardie DG (2005) AMP-activated protein kinase: ancient energy gauge provides clues to modern understanding of metabolism. Cell Metab 1:15–25

    Article  CAS  PubMed  Google Scholar 

  • Kelly DA, Storey KB (1988) Organ-specific control of glycolysis in anoxic turtles. Am J Physiol 255:R774–R779

    CAS  PubMed  Google Scholar 

  • Kennelly PJ (2014) Protein Ser/Thr/Tyr phosphorylation in the Archaea. J Biol Chem 289:9480–9487

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim M, Lee JH (2015) Identification of an AMPK Phosphorylation Site in Drosophila TSC2 (gigas) that Regulate Cell Growth. Int J Mol Sci 16:7015–7026

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Knickerbocker DL, Lutz PL (2001) Slow ATP loss and the defense of ion homeostasis in the anoxic frog brain. J Exp Biol 204:3547–3551

    CAS  PubMed  Google Scholar 

  • Kostál V, Vambera J, Bastl J (2004) On the nature of pre-freeze mortality in insects: water balance, ion homeostasis and energy charge in the adults of Pyrrhocoris apterus. J Exp Biol 207:1509–1521

    Article  PubMed  Google Scholar 

  • Kramer HF, Witczak CA, Taylor EB, Fujii N, Hirshman MF, Goodyear LJ (2006) AS160 regulates insulin- and contraction-stimulated glucose uptake in mouse skeletal muscle. J Biol Chem 281:31478–31485

    Article  CAS  PubMed  Google Scholar 

  • Krebs EG, Beavo JA (1979) Phosphorylation-dephosphorylation of enzymes. Annu Rev Biochem 48:923–959

    Article  CAS  PubMed  Google Scholar 

  • Krumschnabel G, Schwarzbaum PJ, Biasi C, Dorigatti M, Wieser W (1997) Effects of energy limitation on Ca2 + and K + homeostasis in anoxia-tolerant and anoxia-intolerant hepatocytes. Am J Physiol 273:R307–R316

    CAS  PubMed  Google Scholar 

  • Lai YC, Kviklyte S, Vertommen D, Lantier L, Foretz M, Viollet B, Hallen S, Rider MH (2014) A small-molecule benzimidazole derivative that potently activates AMPK to increase glucose transport in skeletal muscle: comparison with effects of contraction and other AMPK activators. Biochem J 460:363–375

    Article  CAS  PubMed  Google Scholar 

  • Lanaspa MA, Epperson LE, Li N, Cicerchi C, Garcia GE, Roncal-Jimenez CA, Trostel J, Jain S, Mant CT, Rivard CJ, Ishimoto T, Shimada M, Sanchez-Lozada LG, Nakagawa T, Jani A, Stenvinkel P, Martin SL, Johnson RJ (2015) Opposing activity changes in AMP deaminase and AMP-activated protein kinase in the hibernating ground squirrel. PLoS One 10:e0123509

    Article  PubMed  PubMed Central  Google Scholar 

  • Lass A, Zimmermann R, Oberer M, Zechner R (2011) Lipolysis - a highly regulated multi-enzyme complex mediates the catabolism of cellular fat stores. Prog Lipid Res 50:14–27

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lau GY, Richards JG (2011) AMP-activated protein kinase plays a role in initiating metabolic rate suppression in goldfish hepatocytes. J Comp Physiol B 181:927–939

    Article  CAS  PubMed  Google Scholar 

  • Lee Y, Kim EK (2013) AMP-activated protein kinase as a key molecular link between metabolism and clockwork. Exp Mol Med 45:e33

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Lee JH, Koh H, Kim M, Kim Y, Lee SY, Karess RE, Lee SH, Shong M, Kim JM, Kim J, Chung J (2007) Energy-dependent regulation of cell structure by AMP-activated protein kinase. Nature 447:1017–1020

    Article  CAS  PubMed  Google Scholar 

  • Lutz PL, McMahon P, Rosenthal M, Sick TJ (1984) Relationships between aerobic and anaerobic energy production in turtle brain in situ. Am J Physiol 247:R740–R744

    CAS  PubMed  Google Scholar 

  • MacDonald JA, Storey KB (1999) Regulation of ground squirrel Na+ K+-ATPase activity by reversible phosphorylation during hibernation. Biochem Biophys Res Commun 254:424–429

    Article  CAS  PubMed  Google Scholar 

  • MacRae TH (2010) Gene expression, metabolic regulation and stress tolerance during diapause. Cell Mol Life Sci 67:2405–2424

    Article  CAS  PubMed  Google Scholar 

  • Malik AI, Storey KB (2009) Activation of extracellular signal-regulated kinases during dehydration in the African clawed frog, Xenopus laevis. J Exp Biol 212:2595–2603

    Article  CAS  PubMed  Google Scholar 

  • Martinez-Atienza J, Van Ingelgem C, Roef L, Maathuis FJ (2007) Plant cyclic nucleotide signalling: facts and fiction. Plant Signal Behav 2:540–543

    Article  PubMed  PubMed Central  Google Scholar 

  • McBride A, Hardie DG (2009) AMP-activated protein kinase- a sensor of glycogen as well as AMP and ATP ? Acta Physiol (Oxf) 196:99–113

    Article  CAS  Google Scholar 

  • Mendelsohn BA, Kassebaum BL, Gitlin JD (2008) The zebrafish embryo as a dynamic model of anoxia tolerance. Dev Dyn 237:1780–1788

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Menze MA, Clavenna MJ, Hand SC (2005) Depression of cell metabolism and proliferation by membrane-permeable and -impermeable modulators: role for AMP-to-ATP ratio. Am J Physiol Regul Integr Comp Physiol 288:R501–R510

    Article  CAS  PubMed  Google Scholar 

  • Migliorini RH, Lima-Verde JS, Machado CR, Cardona GM, Garofalo MA, Kettelhut IC (1992) Control of adipose tissue lipolysis in ectotherm vertebrates. Am J Physiol 263:R857–R862

    CAS  PubMed  Google Scholar 

  • Miranda L, Horman S, De Potter I, Hue L, Jensen J, Rider MH (2008) Effects of contraction and insulin on protein synthesis, AMP-activated protein kinase and phosphorylation state of translation factors in rat skeletal muscle. Pflugers Arch 455:1129–1140

    Article  CAS  PubMed  Google Scholar 

  • Mulligan JD, Gonzalez AA, Stewart AM, Carey HV, Saupe KW (2007) Upregulation of AMPK during cold exposure occurs via distinct mechanisms in brown and white adipose tissue of the mouse. J Physiol 580:677–684

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Narbonne P, Roy R (2006) Inhibition of germline proliferation during C. elegans dauer development requires PTEN, LKB1 and AMPK signalling. Development 133:611–619

    Article  CAS  PubMed  Google Scholar 

  • Narbonne P, Roy R (2009) Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457:210–214

    Article  CAS  PubMed  Google Scholar 

  • Oakhill JS, Steel R, Chen ZP, Scott JW, Ling N, Tam S, Kemp BE (2011) AMPK is a direct adenylate charge-regulated protein kinase. Science 332:1433–1435

    Article  CAS  PubMed  Google Scholar 

  • Oakhill JS, Scott JW, Kemp BE (2012) AMPK functions as an adenylate charge-regulated protein kinase. Trends Endocrinol Metab 23:125–132

    Article  CAS  PubMed  Google Scholar 

  • Olson CS, Clegg JS (1978) Cell division during the development of Artemia salina. Dev Genes Evol 184:1–13

    Google Scholar 

  • Pagnon J, Matzaris M, Stark R, Meex RC, Macaulay SL, Brown W, O’Brien PE, Tiganis T, Watt MJ (2012) Identification and functional characterization of protein kinase A phosphorylation sites in the major lipolytic protein, adipose triglyceride lipase. Endocrinology 153:4278–4289

    Article  CAS  PubMed  Google Scholar 

  • Pan DA, Hardie DG (2002) A homologue of AMP-activated protein kinase in Drosophila melanogaster is sensitive to AMP and is activated by ATP depletion. Biochem J 367:179–186

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Papa S, Rasmo DD, Technikova-Dobrova Z, Panelli D, Signorile A, Scacco S, Petruzzella V, Papa F, Palmisano G, Gnoni A, Micelli L, Sardanelli AM (2012) Respiratory chain complex I, a main regulatory target of the cAMP/PKA pathway, is defective in different human diseases. FEBS Lett 586:568–577

    Article  PubMed  CAS  Google Scholar 

  • Patil YN, Marden B, Brand MD, Hand SC (2013) Metabolic downregulation and inhibition of carbohydrate catabolism during diapause in embryos of Artemia franciscana. Physiol Biochem Zool 86:106–118

    Article  CAS  PubMed  Google Scholar 

  • Pedler S, Fuery CJ, Withers PC, Flanigan J, Guppy M (1996) Effectors of metabolic depression in an estivating pulmonate snail (Helix aspersa): whole animal and in vitro tissue studies. J Comp Physiol B 166:375–381

    Article  CAS  PubMed  Google Scholar 

  • Pinz I, Perry D, Frederich M (2005) Activation of 5′-AMP activated protein kinase during anaerobiosis in the rock crab, Cancer irroratus. MDIBL Bull 44:31–32

    Google Scholar 

  • Plaideau C, Liu J, Hartleib-Geschwindner J, Bastin-Coyette L, Bontemps F, Oscarsson J, Hue L, Rider MH (2012) Overexpression of AMP-metabolizing enzymes controls adenine nucleotide levels and AMPK activation in HEK293T cells. FASEB J 26:2685–2694

    Article  CAS  PubMed  Google Scholar 

  • Plaideau C, Lai YC, Kviklyte S, Zanou N, Lofgren L, Andersen H, Vertommen D, Gailly P, Hue L, Bohlooly YM, Hallen S, Rider MH (2014) Effects of pharmacological AMP deaminase inhibition and Ampd1 deletion on nucleotide levels and AMPK activation in contracting skeletal muscle. Chem Biol 21:1497–1510

    Article  CAS  PubMed  Google Scholar 

  • Podrabsky JE, Hand SC (2000) Depression of protein synthesis during diapause in embryos of the annual killifish Austrofundulus limnaeus. Physiol Biochem Zool 73:799–808

    Article  CAS  PubMed  Google Scholar 

  • Podrabsky JE, Hand SC (2015) Physiological strategies during animal diapause: lessons from brine shrimp and annual killifish. J Exp Biol 218:1879–1906

    Google Scholar 

  • Podrabsky JE, Menze MA, Hand SC (2012) Long-Term survival of anoxia despite rapid ATP decline in embryos of the annual killifish Austrofundulus limnaeus. J Exp Zool A Ecol Genet Physiol 317:524–532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Proud CG (2007) Signalling to translation: how signal transduction pathways control the protein synthetic machinery. Biochem J 403:217–234

    Article  CAS  PubMed  Google Scholar 

  • Pyr Dit Ruys S, Wang X, Smith EM, Herinckx G, Hussain N, Rider MH, Vertommen D, Proud CG (2012) Identification of autophosphorylation sites in eukaryotic elongation factor-2 kinase. Biochem J 442:681–692

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ramnanan CJ, McMullen DC, Groom AG, Storey KB (2010) The regulation of AMPK signaling in a natural state of profound metabolic rate depression. Mol Cell Biochem 335:91–105

    Article  CAS  PubMed  Google Scholar 

  • Reynolds JA, Hand SC (2004) Differences in isolated mitochondria are insufficient to account for respiratory depression during diapause in artemia franciscana embryos. Physiol Biochem Zool 77:366–377

    Article  CAS  PubMed  Google Scholar 

  • Rider MH, Bertrand L, Vertommen D, Michels PA, Rousseau GG, Hue L (2004) 6-phosphofructo-2-kinase/fructose-2,6-bisphosphatase: head-to-head with a bifunctional enzyme that controls glycolysis. Biochem J 381:561–579

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rider MH, Hussain N, Horman S, Dilworth SM, Storey KB (2006) Stress-induced activation of the AMP-activated protein kinase in the freeze-tolerant frog Rana sylvatica. Cryobiology 53:297–309

    Article  CAS  PubMed  Google Scholar 

  • Rider MH, Hussain N, Dilworth SM, Storey KB (2009a) Phosphorylation of translation factors in response to anoxia in turtles, Trachemys scripta elegans: role of the AMP-activated protein kinase and target of rapamycin signalling pathways. Mol Cell Biochem 332:207–213

    Article  CAS  PubMed  Google Scholar 

  • Rider MH, Waelkens E, Derua R, Vertommen D (2009b) Fulfilling the Krebs and Beavo criteria for studying protein phosphorylation in the era of mass spectrometry-driven kinome research. Arch Physiol Biochem 115:298–310

    Article  CAS  PubMed  Google Scholar 

  • Rider MH, Hussain N, Dilworth SM, Storey JM, Storey KB (2011) AMP-activated protein kinase and metabolic regulation in cold-hardy insects. J Insect Physiol 57:1453–1462

    Article  CAS  PubMed  Google Scholar 

  • Scanes CG, Peterla TA, Campbell RM (1994) Influence of adenosine or adrenergic agonists on growth hormone stimulated lipolysis by chicken adipose tissue in vitro. Comp Biochem Physiol Pharmacol Toxicol Endocrinol 107:243–248

    Article  CAS  PubMed  Google Scholar 

  • Scott JW, Ling N, Issa SM, Dite TA, O’Brien MT, Chen ZP, Galic S, Langendorf CG, Steinberg GR, Kemp BE, Oakhill JS (2014) Small molecule drug A-769662 and AMP synergistically activate naive AMPK independent of upstream kinase signaling. Chem Biol 21:619–627

    Article  CAS  PubMed  Google Scholar 

  • Shi S, Chen Y, Siewers V, Nielsen J (2014) Improving production of malonyl coenzyme A-derived metabolites by abolishing Snf1-dependent regulation of Acc1. MBio 5:e01114–e01130

    Google Scholar 

  • 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 21:5710–5722

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Staples JF, Buck LT (2009) Matching cellular metabolic supply and demand in energy-stressed animals. Comp Biochem Physiol A: Mol Integr Physiol 153:95–105

    Article  CAS  Google Scholar 

  • Staples JF, Hochachka PW (1997) Liver energy metabolism duringhibernation in the golden-mantled ground squirrel Spermophilus lateralis. Can J Zool 74:1059–1065

    Article  Google Scholar 

  • Stenslokken KO, Ellefsen S, Stecyk JA, Dahl MB, Nilsson GE, Vaage J (2008) Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius). Am J Physiol Regul Integr Comp Physiol 295:R1803–R1814

    Article  PubMed  CAS  Google Scholar 

  • Stoll B, Gerok W, Lang F, Häussinger D (1992) Liver cell volume and protein synthesis. Biochem J 287:217–222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Storey KB, Storey JM (1986) Freeze tolerant frogs: cryoprotectants and tissue metabolism during freeze/thaw cycles. Can J Zool 64:49–56

    Article  CAS  Google Scholar 

  • Storey KB, Storey JM (2007) Tribute to P. L. Lutz: putting life on ‘pause’—molecular regulation of hypometabolism. J Exp Biol 210:1700–1714

    Article  CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (2012) Aestivation: signalling and hypometabolism. J Exp Biol 215:1425–1433

    Article  CAS  PubMed  Google Scholar 

  • Swoap SJ, Rathvon M, Gutilla M (2007) AMP does not induce torpor. Am J Physiol Regul Integr Comp Physiol 293:R468–R473

    Article  CAS  PubMed  Google Scholar 

  • van Dam TJ, Zwartkruis FJ, Bos JL, Snel B (2011) Evolution of the TOR pathway. J Mol Evol 73:209–220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • van den Thillart G, van Waarde A, Muller HJ, Erkelens C, Addinck A, Lugtenburg J (1989) Fish muscle energy metabolism measured by in vivo 31P-NMR during anoxia and recovery. Am J Physiol 256:R922–R929

    PubMed  Google Scholar 

  • Viollet B, Andreelli F, Jorgensen SB, Perrin C, Flamez D, Mu J, Wojtaszewski JF, Schuit FC, Birnbaum M, Richter E, Burcelin R, Vaulont S (2003) Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem Soc Trans 31:216–219

    Article  CAS  PubMed  Google Scholar 

  • Wegener G (1996) Flying insects: model systems in exercise physiology. Experientia 52:404–412

    Article  CAS  PubMed  Google Scholar 

  • Wegener G, Bolas NM, Thomas AG (1991) Locust flight metabolism studied in vivo by 31P NMR spectroscopy. J Comp Physiol B 161:247–256

    Article  CAS  Google Scholar 

  • Wieser W, Krumschnabel G (2001) Hierarchies of ATP-consuming processes: direct compared with indirect measurements, and comparative aspects. Biochem J 355:389–395

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • Xiao B, Heath R, Saiu P, Leiper FC, Leone P, Jing C, Walker PA, Haire L, Eccleston JF, Davis CT, Martin SR, Carling D, Gamblin SJ (2007) Structural basis for AMP binding to mammalian AMP-activated protein kinase. Nature 449:496–500

    Article  CAS  PubMed  Google Scholar 

  • 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 472:230–233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xue B, Kahn BB (2006) AMPK integrates nutrient and hormonal signals to regulate food intake and energy balance through effects in the hypothalamus and peripheral tissues. J Physiol 574:73–83

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang J, Kaasik K, Blackburn MR, Lee CC (2006) Constant darkness is a circadian metabolic signal in mammals. Nature 439:340–343

    Article  CAS  PubMed  Google Scholar 

  • Zhang BL, Ye Z, Xu RL, You XH, Qin YW, Wu H, Cao J, Zhang JL, Zheng X, Zhao XX (2014) Overexpression of G100S mutation in PRKAG2 causes Wolff-Parkinson-White syndrome in zebrafish. Clin Genet 86:287–291

    Article  CAS  PubMed  Google Scholar 

  • Zhu XJ, Dai JQ, Tan X, Zhao Y, Yang WJ (2009) Activation of an AMP-activated protein kinase is involved in post-diapause development of Artemia franciscana encysted embryos. BMC Dev Biol 9:21

    Article  PubMed  PubMed Central  CAS  Google Scholar 

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Acknowledgments

I am indebted to to Nusrat Hussain for her expert technical assistance, to Fred Opperdoes for his help with the AMPK phylogenetic analyses and to Ken Storey for our fruitful collaboration over the years. I also thank Gaëtan Herinckx for technical help and Didier Vertommen for mass spectrometry analyses. Work in the author’s laboratory was supported by the Interuniversity Attraction Poles Program—Belgian Science Policy (P6/28 and P7/13), by the Directorate General Higher Education and Scientific Research, French Community of Belgium, by the Fund for Medical Scientific Research (FNRS, Belgium) grant number 3.4518.11 and by the EXGENESIS Integrated Project (LSHM-CT-2004-005272) from the European Commission.

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  1. de Duve Institute and Université Catholique de Louvain, Avenue Hippocrate 75, 1200, Brussels, Belgium

    Mark H. Rider

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Communicated by I.D. Hume.

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Rider, M.H. Role of AMP-activated protein kinase in metabolic depression in animals. J Comp Physiol B 186, 1–16 (2016). https://doi.org/10.1007/s00360-015-0920-x

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