PKA phosphorylates and inactivates AMPKα to promote efficient lipolysis

EMBO Journal

Volumn 29, Issue 2, 2010, Pages 469-481

  Djouder, Nabil ^a   Tuerk, Roland D ^a   Suter, Marianne ^a   Salvioni, Paolo ^a   Thali, Ramon F ^a   Scholz, Roland ^a   Vaahtomeri, Kari ^b   Auchli, Yolanda ^c   Rechsteiner, Helene ^c   Brunisholz, René A ^c   Viollet, Benoit ^d,e   Mäkelä, Tomi P ^b   Wallimann, Theo ^a   Neumann, Dietbert ^a   Krek, Wilhelm ^a  

^a ETH ZURICH   (Switzerland)

^b UNIVERSITY OF HELSINKI   (Finland)

^c UNIVERSITY OF ZURICH   (Switzerland)

^d INSTITUT COCHIN   (France)

^e INSERM   (France)

Author keywords

adrenergic; Adipocytes; AMPK; Lipolysis; PKA

Indexed keywords

AMP ACTIVATED PROTEIN KINASE ALPHA; CYCLIC AMP DEPENDENT PROTEIN KINASE; HORMONE SENSITIVE LIPASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ISOPRENALINE; PROTEIN KINASE LKB1; SERINE; THREONINE; UNCLASSIFIED DRUG;

ADIPOCYTE; ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ENERGY CONSUMPTION; ENZYME ACTIVITY; LIPOLYSIS; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ADIPOCYTES; ADRENERGIC BETA-AGONISTS; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CELLS, CULTURED; CYCLIC AMP-DEPENDENT PROTEIN KINASES; FATTY ACIDS; GLYCEROL; ISOPROTERENOL; LIPOLYSIS; MICE; PHOSPHORYLATION; POINT MUTATION; PROTEIN SUBUNITS; PROTEIN-SERINE-THREONINE KINASES;

EID: 75049085233     PISSN: 02614189     EISSN: 14602075     Source Type: Journal    
DOI: 10.1038/emboj.2009.339     Document Type: Article

References (48)

1. Anthonsen MW, Ronnstrand L, Wernstedt C, Degerman E, Holm C (1998) Identification of novel phosphorylation sites in hormone-sensitive lipase that are phosphorylated in response to isoproter-enol and govern activation properties in vitro. J Biol Chem 273: 215-221
2. Bergeron R, Previs SF, Cline GW, Perret P, Russell III RR, Young LH, Shulman GI (2001) Effect of 5-aminoimidazole-4-carboxamide-1-beta-D- ribofuranoside infusion on in vivo glucose and lipid metabolism in lean and obese Zucker rats. Diabetes 50: 1076-1082
3. Brooks B, Arch JR, Newsholme EA (1982) Effects of hormones on the rate of the triacylglycerol/fatty acid substrate cycle in adipo-cytes and epididymal fat pads. FEBS Lett 146: 327-330
4. Carling D, Sanders MJ, Woods A (2008) The regulation of AMP-activated protein kinase by upstream kinases. Int J Obes (Lond) 32(Suppl 4): S55-S59
5. Collins SP, Reoma JL, Gamm DM, Uhler MD (2000) LKB1, a novel serine/threonine protein kinase and potential tumour suppressor, is phosphorylated by cAMP-dependent protein kinase (PKA) and prenylated in vivo. Biochem J 345(Pt 3): 673-680
6. 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
7. Djouder N, Metzler SC, Schmidt A, Wirbelauer C, Gstaiger M, Aebersold R, Hess D, Krek W (2007) S6K1-mediated disassembly of mitochondrial URI/PP1gamma complexes activates a negative feedback program that counters S6K1 survival signaling. Mol Cell 28: 28-40
8. Ducharme NA, Bickel PE (2008) Lipid droplets in lipogenesis and lipolysis. Endocrinology 149: 942-949
9. Duncan RE, Ahmadian M, Jaworski K, Sarkadi-Nagy E, Sul HS (2007) Regulation of lipolysis in adipocytes. Annl Rev Nutr 27: 79-101
10. Garton AJ, Campbell DG, Carling D, Hardie DG, Colbran RJ, Yeaman SJ (1989) Phosphorylation of bovine hormone-sensitive lipase by the AMP-activated protein kinase. A possible antilipo-lytic mechanism. Eur J Biochem 179: 249-254
11. Gauthier MS, Miyoshi H, Souza SC, Cacicedo JM, Saha AK, Greenberg AS, Ruderman NB (2008) AMP-activated protein ki-nase is activated as a consequence of lipolysis in the adipocyte: potential mechanism and physiological relevance. J Biol Chem 283: 16514-16524
12. Gesta S, Bluher M, Yamamoto Y, Norris AW, Berndt J, Kralisch S, Boucher J, Lewis C, Kahn CR (2006) Evidence for a role of developmental genes in the origin of obesity and body fat distribution. Proc Natl Acad Sci USA 103: 6676-6681
13. Granneman JG, Moore HP (2008) Location, location: protein trafficking and lipolysis in adipocytes. Trends Endocrinol Metab 19: 3-9
14. Guilherme A, Virbasius JV, Puri V, Czech MP (2008) Adipocyte dysfunctions linking obesity to insulin resistance and type 2 diabetes. Nat Rev Mol Cell Biol 9: 367-377
15. Hardie DG (2008) AMPK: a key regulator of energy balance in the single cell and the whole organism. Int J Obes (Lond) 32(Suppl 4): S7-12
16. Hardie DG, Hawley SA, Scott JW (2006) AMP-activated protein kinase-development of the energy sensor concept. J Physiol 574(Pt 1): 7-15
17. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG (1996) Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 271: 27879-27887
18. Holm C (2003) Molecular mechanisms regulating hormone-sensitive lipase and lipolysis. Biochem Soc Trans 31 (Pt 6): 1120-1124 (Pubitemid 38030921)
19. Hue L, Rider MH (2007) The AMP-activated protein kinase: more than an energy sensor. Essays Biochem 43: 121-137
20. Hurley RL, Barre LK, Wood SD, Anderson KA, Kemp BE, Means AR, Witters LA (2006) Regulation of AMP-activated protein kinase by multisite phosphorylation in response to agents that elevate cellular cAMP. J Biol Chem 281: 36662-36672
21. Kalderon B, Mayorek N, Berry E, Zevit N, Bar-Tana J (2000) Fatty acid cycling in the fasting rat. Am J Physiol Endocrinol Metab 279: E221-E227
22. Khoo JC, Fong WW, Steinberg D (1972) Activation of hormone-sensitive lipase from adipose tissue by cyclic AMP-dependent protein kinase. Biochem Biophys Res Commun 49: 407-413
23. Koh HJ, Hirshman MF, He H, Li Y, Manabe Y, Balschi JA, Goodyear LJ (2007) Adrenaline is a critical mediator of acute exercise-induced AMP-activated protein kinase activation in adipocytes. Biochem J 403: 473-481
24. Large V, Peroni O, Letexier D, Ray H, Beylot M (2004) Metabolism of lipids in human white adipocyte. Diabetes Metab 30: 294-309
25. Lihn AS, Jessen N, Pedersen SB, Lund S, Richelsen B (2004) AICAR stimulates adiponectin and inhibits cytokines in adipose tissue. Biochem Biophys Res Commun 316: 853-858
26. Lobo S, Wiczer BM, Bernlohr DA (2009) Functional analysis of long-chain Acyl-CoA synthetase 1 in 3T3-L1 adipocytes. J Biol Chem 284: 18347-18356
27. Martin S, Okano S, Kistler C, Fernandez-Rojo MA, Hill MM, Parton RG (2009) Spatiotemporal regulation of early lipolytic signalling in adipocytes. J Biol Chem 284: 32097-32107
28. McKnight GS, Cummings DE, Amieux PS, Sikorski MA, Brandon EP, Planas JV, Motamed K, Idzerda RL (1998) Cyclic AMP, PKA, and the physiological regulation of adiposity. Recent Prog Horm Res 53: 139-159; discussion 160-1131
29. Moule SK, Denton RM (1998) The activation of p38 MAPK by the beta-adrenergic agonist isoproterenol in rat epididymal fat cells. FEBS Lett 439: 287-290
30. Neumann D, Suter M, Tuerk R, Riek U, Wallimann T (2007) Co-expression of LKB1, MO25alpha and STRADalpha in bacteria yield the functional and active heterotrimeric complex. Mol Biotechnol 36: 220-231
31. Neumann D, Woods A, Carling D, Wallimann T, Schlattner U (2003) Mammalian AMP-activated protein kinase: functional, heterotrimeric complexes by co-expression of subunits in Escherichia coli. Protein Expr Purif 30: 230-237
32. Omar B, Zmuda-Trzebiatowska E, Manganiello V, Goransson O, Degerman E (2009) Regulation of AMP-activated protein kinase by cAMP in adipocytes: roles for phosphodiesterases, protein kinase B, protein kinase A, Epac and lipolysis. Cell Signal 21: 760-766
33. Reshef L, Hanson RW, Ballard FJ (1970) A possible physiological role for glyceroneogenesis in rat adipose tissue. J Biol Chem 245: 5979-5984
34. Reshef L, Olswang Y, Cassuto H, Blum B, Croniger CM, Kalhan SC, Tilghman SM, Hanson RW (2003) Glyceroneogenesis and the triglyceride/fatty acid cycle. J Biol Chem 278: 30413-30416
35. Rosen ED, Spiegelman BM (2006) Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444: 847-853
36. Sakamoto K, McCarthy A, Smith D, Green KA, Grahame Hardie D, Ashworth A, Alessi DR (2005) Deficiency of LKB1 in skeletal muscle prevents AMPK activation and glucose uptake during contraction. EMBO J 24: 1810-1820
37. Sanders MJ, Grondin PO, Hegarty BD, Snowden MA, Carling D (2007) Investigating the mechanism for AMP activation of the AMP-activated protein kinase cascade. Biochem J 403: 139-148 (Pubitemid 46569875)
38. Sapkota GP, Kieloch A, Lizcano JM, Lain S, Arthur JS, Williams MR, Morrice N, Deak M, Alessi DR (2001) Phosphorylation of the protein kinase mutated in Peutz-Jeghers cancer syndrome, LKB1/ STK11, at Ser431 by p90(RSK) and cAMP-dependent protein kinase, but not its farnesylation at Cys(433), is essential for LKB1 to suppress cell growth. J Biol Chem 276: 19469-19482
39. Schweiger M, Schreiber R, Haemmerle G, Lass A, Fledelius C, Jacobsen P, Tornqvist H, Zechner R, Zimmermann R (2006) Adipose triglyceride lipase and hormone-sensitive lipase are the major enzymes in adipose tissue triacylglycerol catabolism. J Biol Chem 281: 40236-40241
40. Shaw RJ, Lamia KA, Vasquez D, Koo SH, Bardeesy N, Depinho RA, Montminy M, Cantley LC (2005) The kinase LKB1 mediates glucose homeostasis in liver and therapeutic effects of metformin. Science 310: 1642-1646
41. Studier FW (2005) Protein production by auto-induction in high density shaking cultures. Protein Expr Purif 41: 207-234
42. Suter M, Riek U, Tuerk R, Schlattner U, Wallimann T, Neumann D (2006) Dissecting the role of 5-AMP for allosteric stimulation, activation, and deactivation of AMP-activated protein kinase. J Biol Chem 281: 32207-32216
43. Tanaka T, Yoshida N, Kishimoto T, Akira S (1997) Defective adipocyte differentiation in mice lacking the C/EBPbeta and/or C/EBPdelta gene. EMBO J 16: 7432-7443
44. Vaahtomeri K, Ventela E, Laajanen K, Katajisto P, Wipff PJ, Hinz B, Vallenius T, Tiainen M, Makela TP (2008) Lkb1 is required for TGFbeta-mediated myofibroblast differentiation. J Cell Sci 121(Pt 21): 3531-3540
45. Watt MJ, Holmes AG, Pinnamaneni SK, Garnham AP, Steinberg GR, Kemp BE, Febbraio MA (2006) Regulation of HSL serine phos-phorylation in skeletal muscle and adipose tissue. Am J Physiol Endocrinol Metab 290: E500-E508
46. Woods A, Vertommen D, Neumann D, Turk R, Bayliss J, Schlattner U, Wallimann T, Carling D, Rider MH (2003) Identification of phosphorylation sites in AMP-activated protein kinase (AMPK) for upstream AMPK kinases and study of their roles by site-directed mutagenesis. J Biol Chem 278: 28434-28442
47. Yin W, Mu J, Birnbaum MJ (2003) Role of AMP-activated protein kinase in cyclic AMP-dependent lipolysis In 3T3-L1 adipocytes. J Biol Chem 278: 43074-43080
48. Zimmermann R, Lass A, Haemmerle G, Zechner R (2009) Fate of fat: the role of adipose triglyceride lipase in lipolysis. Biochim Biophys Acta 1791: 494-500