Altered metabolism and persistent starvation behaviors caused by reduced AMPK function in Drosophila

PLoS ONE

Volumn 5, Issue 9, 2010, Pages 1-11

  Johnson, Erik C ^a   Kazgan, Nevzat ^b   Bretz, Colin A ^a   Forsberg, Lawrence J ^b   Hector, Clare E ^a   Worthen, Ryan J ^b   Onyenwoke, Rob ^b   Brenman, Jay E ^b,c  

^a WAKE FOREST UNIVERSITY   (United States)

^b UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^c UNIVERSITY OF NORTH CAROLINA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE ALPHA; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE GAMMA; OXYGEN; RAPAMYCIN; SMALL INTERFERING RNA; TRIACYLGLYCEROL; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; SNF1A PROTEIN, DROSOPHILA; SNF4AGAMMA PROTEIN, DROSOPHILA;

ADAPTIVE BEHAVIOR; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DIETARY INTAKE; DROSOPHILA; ENERGY BALANCE; ENERGY CONSUMPTION; ENZYME ACTIVATION; ENZYME SUBUNIT; FORAGING BEHAVIOR; GENETIC VARIABILITY; HYPERACTIVITY; LETHALITY; LIFESPAN; LIPID STORAGE; LOCOMOTION; METABOLIC RATE; METAZOON; NONHUMAN; NUTRIENT AVAILABILITY; OXYGEN CONSUMPTION; PROTEIN EXPRESSION; PROTEIN FUNCTION; RNA INTERFERENCE; SIGNAL TRANSDUCTION; STARVATION; WILD TYPE; ANIMAL; DROSOPHILA MELANOGASTER; ENZYMOLOGY; FEEDING BEHAVIOR; FEMALE; GENETICS; LIPID METABOLISM; MALE; METABOLISM; PHYSIOLOGY;

ANIMALIA; DROSOPHILA MELANOGASTER; METAZOA;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; FEEDING BEHAVIOR; FEMALE; LIPID METABOLISM; MALE; STARVATION;

EID: 77958504514     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0012799     Document Type: Article

References (44)

1. Winder W, Thomson D (2007) Cellular energy sensing and signaling by AMPactivated protein kinase. Cell Biochem Biophys 47: 332-47.
2. Long YC, Zierath JR (2006) AMP-activated protein kinase signaling in metabolic regulation. J Clin Invest 116: 1776-83.
3. Riek U, Scholz R, Konarev P, Rufer A, Suter M, et al. (2008) Structural properties of AMP-activated protein kinase: dimerization, molecular shape, and changes upon ligand binding. J Biol Chem 283: 18331-43.
4. Birk JB, Wojtaszewski JF (2006) Predominant alpha2/beta2/gamma3 AMPK activation during exercise in human skeletal muscle. J Physiol 577: 1021-32.
5. 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: 179-86.
6. Greer EL, Brunet A (2009) Different dietary restriction regimens extend lifespan by both independent and overlapping genetic pathways in C. elegans. Aging Cell 8: 113-27.
7. Narkar VA, Downes M, Yu RT, Embler E, Wang YX, et al. (2008) AMPK and PPARdelta agonists are exercise mimetics. Cell 134: 405-15.
8. Viollet B, Lantier L, Devin-Leclerc J, Hebrard S, Amouyal C, et al. (2009) Targeting the AMPK pathway for the treatment of Type 2 diabetes. Front Biosci 14: 3380-400.
9. Mirouse V, Swick LL, Kazgan N, St Johnston D, Brenman JE (2007) LKB1 and AMPK maintain epithelial cell polarity under energetic stress. J Cell Biol 177: 387-92.
10. Broughton SJ, Piper MD, Ikeya T, Bass TM, Jacobson J, et al. (2005) Longer lifespan, altered metabolism, and stress resistance in Drosophila from ablation of cells making insulin-like ligands. Proc Natl Acad Sci USA 102: 3105-10.
11. Hector CE, Bretz CA, Zhao Y, Johnson EC (2009) Functional differences between two CRF-Related Diuretic Hormone Receptors in Drosophila. J Exp Biol 212: 3142-3147.
12. Zhao Y, Hawksworth SA, Bretz CA, Hirsh J, Johnson EC (2010) Corazonin neurons participate in sexually dimorphic circuitry that shape behavioral responses to stress in Drosophila. PLoS ONE 5: e9141.
13. Gutierrez E, Wiggins D, Fielding B, Gould AP (2007) Specialized hepatocytelike cells regulate Drosophila lipid metabolism. Nature 445: 275-80.
14. Ja WW, Carvalho GB, Mak EM, de la Rosa NN, Fang AY, et al. (2007) Prandiology of Drosophila and the CAFE assay. Proc Natl Acad Sci USA 104: 8253-6.
15. Al-Anzi B, Tracey WD Jr., Benzer S (2006) Response of Drosophila to wasabi is mediated by painless, the fly homolog of mammalian TRPA1/ANKTM1. Curr Biol 16: 1034-40.
16. Woods A, Azzout-Marniche D, Foretz M, Stein SC, Lemarchand P, et al. (2000) Characterization of the role of AMP-activated protein kinase in the regulation of glucose-activated gene expression using constitutively active and dominant negative forms of the kinase. Mol Cell Biol 20: 6704-11.
17. Nagata D, Kiyosue A, Takahashi M, Satonaka H, Tanaka K, et al. (2009) A new constitutively active mutant of AMP-activated protein kinase inhibits anoxiainduced apoptosis of vascular endothelial cell. Hypertens Res 32: 133-9.
18. Carrera AC, Alexandrov K, Roberts TM (1993) The conserved lysine of the catalytic domain of protein kinases is actively involved in the phosphotransfer reaction and not required for anchoring ATP. Proc Natl Acad Sci USA 90: 442-6.
19. Kamps MP, Sefton BM (1986) Neither arginine nor histidine can carry out the function of lysine-295 in the ATP-binding site of p60src. Mol Cell Biol 6: 751-7.
20. Nagata D, Mogi M, Walsh K (2003) AMP-activated protein kinase (AMPK) signaling in endothelial cells is essential for angiogenesis in response to hypoxic stress. J Biol Chem 278: 31000-6.
21. Dzamko N, van Denderen BJ, Hevener AL, Jørgensen SB, Honeyman J, et al. (2010) AMPK beta1 deletion reduces appetite, preventing obesity and hepatic insulin resistance. J Biol Chem 285: 115-22.
22. Schulz C, Perezgasga L, Fuller MT (2001) Genetic analysis of dPsa, the Drosophila orthologue of puromycin-sensitive aminopeptidase, suggests redundancy of aminopeptidases. Dev Genes Evol 211: 581-8.
23. Isabel G, Martin JR, Chidami S, Veenstra JA, Rosay P (2005) AKH-producing neuroendocrine cell ablation decreases trehalose and induces behavioral changes in Drosophila. Am J Physiol Regul Integr Comp Physiol 288: R531-8.
24. Lee G, Park JH (2005) Hemolymph sugar homeostasis and starvation-induced hyperactivity affected by genetic manipulations of the adipokinetic hormoneencoding gene in Drosophila melanogaster. Genetics 167: 311-23.
25. Claret M, Smith MA, Batterham RL, Selman C, Choudhury AI, et al. (2007) AMPK is essential for energy homeostasis regulation and glucose sensing by POMC and AgRP neurons. J Clin Invest 117: 2325-36.
26. Grönke S, Beller M, Fellert S, Ramakrishnan H, Jäckle H, et al. (2003) Control of fat storage by a Drosophila PAT domain protein. Curr Biol 13: 603-6.
27. Zang M, Zuccollo A, Hou X, Nagata D, Walsh K, et al. (2004) AMP-activated protein kinase is required for the lipid-lowering effect of metformin in insulinresistant human HepG2 cells. J Biol Chem 279: 47898-905.
28. Narbonne P, Roy R (2009) Caenorhabditis elegans dauers need LKB1/AMPK to ration lipid reserves and ensure long-term survival. Nature 457: 210-4.
29. Dowling RJ, Topisirovic I, Fonseca BD, Sonenberg N (2010) Dissecting the role of mTOR: Lessons from mTOR inhibitors. Biochim Biophys Acta 1804: 433-439.
30. Hennig KM, Neufeld TP (2002) Inhibition of cellular growth and proliferation by dTOR overexpression in Drosophila. Genesis 34: 107-110.
31. Alarcon CM, Heitman J, Cardenas ME (1999) Protein kinase activity and identification of a toxic effector domain of the target of rapamycin TOR proteins in yeast. Mol Biol Cell 10: 2531-2546.
32. Deshmukh AS, Treebak JT, Long YC, Viollet B, Wojtaszewski JF, et al. (2008) Role of adenosine 59-monophosphate-activated protein kinase subunits in skeletal muscle mammalian target of rapamycin signaling. Mol Endocrinol 22: 1105-12.
33. Lee H, Cho JS, Lambacher N, Lee J, Lee SJ, et al. (2008) The Caenorhabditis elegans AMP-activated protein kinase AAK-2 is phosphorylated by LKB1 and is required for resistance to oxidative stress and for normal motility and foraging behavior. J Biol Chem 283: 14988-93.
34. Spasić MR, Callaerts P, Norga KK (2008) Drosophila alicorn is a neuronal maintenance factor protecting against activity-induced retinal degeneration. J Neurosci 28: 6419-29.
35. Poels J, Spasić MR, Callaerts P, Norga KK (2009) Expanding roles for AMPactivated protein kinase in neuronal survival and autophagy. Bioessays 31: 944-52.
36. Tohyama D, Yamaguchi A (2010) A critical role of SNF1A/dAMPKalpha (Drosophila AMP-activated protein kinase alpha) in muscle on longevity and stress resistance in Drosophila melanogaster. Biochem Biophys Res Commun 394: 112-8.
37. Sullivan JE, Brocklehurst KJ, Marley AE, Carey F, Carling D, et al. (1994) Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett 353: 33-6.
38. Johnson EC, White MP (2009) Stressed-out Insects: Behavioral Modifications and Hormonal Actions. In: Hormones, Brain, Behavior. (2nd edition) Donald WPfaff, Arthur PArnold, Anne MEtgen, Susan EFahrbach, Robert TRubin, eds. Vol 2 Academic Press. pp 1069-1096.
39. Williams T, Forsberg LJ, Viollet B, Brenman JE (2009) Basal autophagy induction without AMP-activated protein kinase under low glucose conditions. Autophagy 5: 1155-65.
40. Wu Q, Wen T, Lee G, Park JH, Cai HN, et al. (2003) Developmental control of foraging and social behavior by the Drosophila neuropeptide Y-like system. Neuron 39: 147-61.
41. Melcher C, Pankratz MJ (2005) Candidate gustatory interneurons modulating feeding behavior in the Drosophila brain. PLoS Biol 3: e305.
42. Rulifson EJ, Kim SK, Nusse R (2002) Ablation of insulin-producing neurons in flies: growth and diabetic phenotypes. Science 296: 1118-20.
43. Bland ML, Lee RJ, Magallanes JM, Foskett JK, Birnbaum MJ (2010) AMPK supports growth in Drosophila by regulating muscle activity and nutrient uptake in the gut. Dev Biol. In press.
44. Greer EL, Dowlatshahi D, Banko MR, Villen J, Hoang K, et al. (2007) An AMPK-FOXO pathway mediates longevity induced by a novel method of dietary restriction in C. elegans. Curr Biol 17: 1646-56.