Melanocortin-induced PKA activation inhibits AMPK activity via ERK-1/2 and LKB-1 in hypothalamic GT1-7 cells

Molecular Endocrinology

Volumn 26, Issue 4, 2012, Pages 643-654

  Damm, Ellen ^a   Buech, Thomas R H ^a   Gudermann, Thomas ^a   Breit, Andreas ^a  

^a UNIVERSITY OF MUNICH   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; ALPHA INTERMEDIN; CALCIUM CALMODULIN DEPENDENT KINASE KINASE BETA; CYCLIC AMP DEPENDENT PROTEIN KINASE; MELANOCORTIN; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PHOSPHOTRANSFERASE; PROTEIN KINASE LKB1; TRANSFORMING GROWTH FACTOR BETA ACTIVATED KINASE 1; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; DEPHOSPHORYLATION; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; HYPOTHALAMUS; NONHUMAN; PRIORITY JOURNAL;

ADENYLATE KINASE; ALPHA-MSH; ANIMALS; CELL LINE; CYCLIC AMP-DEPENDENT PROTEIN KINASES; ENZYME ACTIVATION; GTP-BINDING PROTEIN ALPHA SUBUNITS, GS; HYPOTHALAMUS; MAP KINASE SIGNALING SYSTEM; MICE; MITOGEN-ACTIVATED PROTEIN KINASE 1; MITOGEN-ACTIVATED PROTEIN KINASE 3; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN-SERINE-THREONINE KINASES;

MURINAE;

EID: 84859151395     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2011-1218     Document Type: Article

References (58)

1. MacNeil DJ, Howard AD, Guan X, Fong TM, Nargund RP, Bednarek MA, Goulet MT, Weinberg DH, Strack AM, Marsh DJ, Chen HY, Shen CP, Chen AS, Rosenblum CI, MacNeil T, Tota M, MacIntyre ED, Van der Ploeg LH 2002 The role of melanocortins in body weight regulation: opportunities for the treatment of obesity. Eur J Pharmacol 450:93-109
2. Huszar D, Lynch CA, Fairchild-Huntress V, Dunmore JH, Fang Q, Berkemeier LR, Gu W, Kesterson RA, Boston BA, Cone RD, Smith FJ, Campfield LA, Burn P, Lee F 1997 Targeted disruption of the melanocortin-4 receptor results in obesity in mice. Cell 88:131-141
3. Lee YS, Challis BG, Thompson DA, Yeo GS, Keogh JM, Madonna ME, Wraight V, Sims M, Vatin V, Meyre D, Shield J, Burren C, Ibrahim Z, Cheetham T, Swift P, Blackwood A, Hung CC, Wareham NJ, Froguel P, Millhauser GL, O'Rahilly S, Farooqi IS 2006 A POMC variant implicates β-melanocyte-stimulating hormone in the control of human energy balance. Cell Metab 3:135-140
4. Tao YX, Segaloff DL 2003 Functional characterization of melanocortin-4 receptor mutations associated with childhood obesity. Endocrinology 144:4544-4551
5. Hinney A, Bettecken T, Tarnow P, Brumm H, Reichwald K, Lichtner P, Scherag A, Nguyen TT, Schlumberger P, Rief W, Vollmert C, Illig T, Wichmann HE, Schäfer H, Platzer M, Biebermann H, Meitinger T, Hebebrand J 2006 Prevalence, spectrum, and functional characterization of melanocortin-4 receptor gene mutations in a representative population-based sample and obese adults from Germany. J Clin Endocrinol Metab 91:1761-1769
6. Hinney A, Hohmann S, Geller F, Vogel C, Hess C, Wermter AK, Brokamp B, Goldschmidt H, Siegfried W, Remschmidt H, Schäfer H, Gudermann T, Hebebrand J 2003 Melanocortin-4 receptor gene: casecontrol study and transmission disequilibrium test confirm that functionally relevant mutations are compatible with a major gene effect for extreme obesity. J Clin Endocrinol Metab 88:4258-4267
7. Govaerts C, Srinivasan S, Shapiro A, Zhang S, Picard F, Clement K, Lubrano-Berthelier C, Vaisse C 2005 Obesity-associated mutations in the melanocortin 4 receptor provide novel insights into its function. Peptides 26:1909-1919
8. Vaisse C, Clement K, Guy-Grand B, Froguel P 1998 A frameshift mutation in human MC4R is associated with a dominant form of obesity. Nat Genet 20:113-114
9. Woods A, Cheung PC, Smith FC, Davison MD, Scott J, Beri RK, Carling D 1996 Characterization of AMP-activated protein kinase β and γ subunits. Assembly of the heterotrimeric complex in vitro. J Biol Chem 271:10282-10290
10. Hardie DG, Carling D 1997 The AMP-activated protein kinase-fuel gauge of the mammalian cell? Eur J Biochem 246:259-273
11. Blanco Martínez de Morentin P, González CR, Saha AK, Martins L, Diéguez C, Vidal-Puig A, Tena-Sempere M, López M 2011 Hypothalamic AMP-activated protein kinase as a mediator of whole body energy balance. Rev Endocr Metab Disord 12:127-140
12. Carling D 2004 The AMP-activated protein kinase cascade-a unifying system for energy control. Trends Biochem Sci 29:18-24
13. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferré P, Birnbaum MJ, Stuck BJ, Kahn BB 2004 AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428:569-574
14. 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
15. Mitchelhill KI, Michell BJ, House CM, Stapleton D, Dyck J, Gamble J, Ullrich C, Witters LA, Kemp BE 1997 Posttranslational modifications of the 5'-AMP-activated protein kinase β1 subunit. J Biol Chem 272:24475-24479
16. Gao G, Fernandez CS, Stapleton D, Auster AS, Widmer J, Dyck JR, Kemp BE, Witters LA 1996 Non-catalytic β-and γ-subunit isoforms of the 5'-AMP-activated protein kinase. J Biol Chem 271:8675-8681
17. Woods A, Dickerson K, Heath R, Hong SP, Momcilovic M, Johnstone SR, Carlson M, Carling D 2005 Ca2+/calmodulin-dependent protein kinase kinase-β acts upstream of AMP-activated protein kinase in mammalian cells. Cell Metab 2:21-33
18. Hawley SA, Pan DA, Mustard KJ, Ross L, Bain J, Edelman AM, Frenguelli BG, Hardie DG 2005 Calmodulin-dependent protein kinase kinase-β is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2:9-19
19. Anderson KA, Ribar TJ, Lin F, Noeldner PK, Green MF, Muehlbauer MJ, Witters LA, Kemp BE, Means AR 2008 Hypothalamic CaMKK2 contributes to the regulation of energy balance. Cell Metab 7:377-388
20. Xie M, Zhang D, Dyck JR, Li Y, Zhang H, Morishima M, Mann DL, Taffet GE, Baldini A, Khoury DS, Schneider MD 2006 A pivotal role for endogenous TGF-β-activated kinase-1 in the LKB1/ AMP-activated protein kinase energy-sensor pathway. Proc Natl Acad Sci USA 103:17378-17383
21. Momcilovic M, Hong SP, Carlson M 2006 Mammalian TAK1 activates Snf1 protein kinase in yeast and phosphorylates AMP-activated protein kinase in vitro. J Biol Chem 281:25336-25343
22. Shaw RJ, Kosmatka M, Bardeesy N, Hurley RL, Witters LA, De-Pinho RA, Cantley LC 2004 The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101:3329-3335
23. Lizcano JM, Göransson O, Toth R, Deak M, Morrice NA, Boudeau J, Hawley SA, Udd L, Mäkelä TP, Hardie DG, Alessi DR 2004 LKB1 is a master kinase that activates 13 kinases of the AMPK subfamily, including MARK/PAR-1. EMBO J 23:833-843
24. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Mäkelä TP, Alessi DR, Hardie DG 2003 Complexes between the LKB1 tumor suppressor, STRAD α/β and MO25 α/β are upstream kinases in the AMP-activated protein kinase cascade. J Biol 2:28
25. 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
26. Kimball SR, Siegfried BA, Jefferson LS 2004 Glucagon represses signaling through the mammalian target of rapamycin in rat liver by activating AMP-activated protein kinase. J Biol Chem 279:54103-54109
27. Djouder N, Tuerk RD, Suter M, Salvioni P, Thali RF, Scholz R, Vaahtomeri K, Auchli Y, Rechsteiner H, Brunisholz RA, Viollet B, Mäkelä TP, Wallimann T, Neumann D, Krek W 2010 PKA phosphorylates and inactivates AMPKα to promote efficient lipolysis. EMBO J 29:469-481
28. Hurley RL, Barré 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
29. Czyzyk TA, Sikorski MA, Yang L, McKnight GS 2008 Disruption of the RIIβ subunit of PKA reverses the obesity syndrome of Agouti lethal yellow mice. Proc Natl Acad Sci USA 105:276-281
30. Khong K, Kurtz SE, Sykes RL, Cone RD 2001 Expression of functional melanocortin-4 receptor in the hypothalamic GT1-1 cell line. Neuroendocrinology 74:193-201
31. Shinyama H, Masuzaki H, Fang H, Flier JS 2003 Regulation of melanocortin-4 receptor signaling: agonist-mediated desensitization and internalization. Endocrinology 144:1301-1314
32. Anderson RA, Zwain IH, Arroyo A, Mellon PL, Yen SS 1999 The insulin-like growth factor system in the GT1-7 GnRH neuronal cell line. Neuroendocrinology 70:353-359
33. Sanz C, Vázquez P, Navas MA, Alvarez E, Blázquez E 2008 Leptin but not neuropeptide Y up-regulated glucagon-like peptide 1 receptor expression in GT1-7 cells and rat hypothalamic slices. Metabolism 57:40-48
34. Mellon PL, Windle JJ, Goldsmith PC, Padula CA, Roberts JL, Weiner RI 1990 Immortalization of hypothalamic GnRH neurons by genetically targeted tumorigenesis. Neuron 5:1-10
35. Büch TR, Heling D, Damm E, Gudermann T, Breit A 2009 Pertussis toxin-sensitive signaling of melanocortin-4 receptors in hypothalamic GT1-7 cells defines agouti-related protein as a biased agonist. J Biol Chem 284:26411-26420
36. Ollmann MM, Wilson BD, Yang YK, Kerns JA, Chen Y, Gantz I, Barsh GS 1997 Antagonism of central melanocortin receptors in vitro and in vivo by agouti-related protein. Science 278:135-138
37. Davies SP, Carling D, Hardie DG 1989 Tissue distribution of the AMP-activated protein kinase, and lack of activation by cyclic-AMP-dependent protein kinase, studied using a specific and sensitive peptide assay. Eur J Biochem 186:123-128
38. Hwang SL, Kim HN, Jung HH, Kim JE, Choi DK, Hur JM, Lee JY, Song H, Song KS, Huh TL 2008 Beneficial effects of β-sitosterol on glucose and lipid metabolism in L6 myotube cells are mediated by AMP-activated protein kinase. Biochem Biophys Res Commun 377: 1253-1258
39. Hwang SL, Yang BK, Lee JY, Kim JH, Kim BD, Kim BH, Suh KH, Kim DY, Kim DY, Kim MS, Song H, Park BS, Huh TL 2008 Isodihydrocapsiate stimulates plasma glucose uptake by activation of AMP-activated protein kinase. Biochem Biophys Res Commun 371:289-293
40. Na LX, Zhang YL, Li Y, Liu LY, Li R, Kong T, Sun CH 2011 Curcumin improves insulin resistance in skeletal muscle of rats. Nutr Metab Cardiovasc Dis 21:526-533
41. Du J, Guan T, Zhang H, Xia Y, Liu F, Zhang Y 2008 Inhibitory crosstalk between ERK and AMPK in the growth and proliferation of cardiac fibroblasts. Biochem Biophys Res Commun 368:402-407
42. Chai B, Li JY, Zhang W, Newman E, Ammori J, Mulholland MW 2006 Melanocortin-4 receptor-mediated inhibition of apoptosis in immortalized hypothalamic neurons via mitogen-activated protein kinase. Peptides 27:2846-2857
43. Rahmouni K, Haynes WG 2001 Leptin signaling pathways in the central nervous system: interactions between neuropeptide Y and melanocortins. Bioessays 23:1095-1099
44. Minokoshi Y, Shiuchi T, Lee S, Suzuki A, Okamoto S 2008 Role of hypothalamic AMP-kinase in food intake regulation. Nutrition 24: 786-790
45. Chai B, Li JY, Zhang W, Wu X, Zhang C, Mulholland MW 2010 Melanocortin-4 receptor activation promotes insulin-stimulated mTOR signaling. Peptides 31:1888-1893
46. Kim JE, Song SE, Kim YW, Kim JY, Park SC, Park YK, Baek SH, Lee IK, Park SY 2010 Adiponectin inhibits palmitate-induced apoptosis through suppression of reactive oxygen species in endothelial cells: involvement of cAMP/protein kinase A and AMP-activated protein kinase. J Endocrinol 207:35-44
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. Hutchinson DS, Chernogubova E, Dallner OS, Cannon B, Bengtsson T 2005 β-Adrenoceptors, but not α-adrenoceptors, stimulate AMP-activated protein kinase in brown adipocytes independently of uncoupling protein-1. Diabetologia 48:2386-2395
49. 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
50. Funahashi K, Cao X, Yamauchi M, Kozaki Y, Ishiguro N, Kambe F 2009 Prostaglandin E2 negatively regulates AMP-activated protein kinase via protein kinase A signaling pathway. Prostag Oth Lipid Mediat 88:31-35
51. Chen HC, Bandyopadhyay G, Sajan MP, Kanoh Y, Standaert M, Farese Jr RV, Farese RV 2002 Activation of the ERK pathway and atypical protein kinaseCisoforms in exercise-and aminoimidazole-4-carboxamide-1-β-D-riboside (AICAR)-stimulated glucose transport. J Biol Chem 277:23554-23562
52. Breit A, Büch TR, Boekhoff I, Solinski HJ, Damm E, Gudermann T 2011 AlternativeGprotein coupling and biased agonism: new insights into melanocortin-4 receptor signalling. Mol Cell Endocrinol 331: 232-240
53. Mountjoy KG, Kong PL, Taylor JA, Willard DH, Wilkison WO 2001 Melanocortin receptor-mediated mobilization of intracellular free calcium in HEK293 cells. Physiol Genomics 5:11-19
54. Vongs A, Lynn NM, Rosenblum CI 2004 Activation ofMAPkinase by MC4-R through PI3 kinase. Regul Pept 120:113-118
55. Sutton GM, Duos B, Patterson LM, Berthoud HR 2005 Melanocortinergic modulation of cholecystokinin-induced suppression of feeding through extracellular signal-regulated kinase signaling in rat solitary nucleus. Endocrinology 146:3739-3747
56. Zheng B, Jeong JH, Asara JM, Yuan YY, Granter SR, Chin L, Cantley LC 2009 Oncogenic B-RAF negatively regulates the tumor suppressor LKB1 to promote melanoma cell proliferation. Mol Cell 33:237-247
57. Hayes MR, Leichner TM, Zhao S, Lee GS, Chowansky A, Zimmer D, De Jonghe BC, Kanoski SE, Grill HJ, Bence KK 2011 Intracellular signals mediating the food intake-suppressive effects of hindbrain glucagon-like peptide-1 receptor activation. Cell Metab 13: 320-330
58. Cheng XB, Wen JP, Yang J, Yang Y, Ning G, Li XY, Gn RH 2011 secretion is inhibited by adiponectin through activation of AMPactivated protein kinase and extracellular signal-regulated kinase. Endocrine 39:6-12