AMPK regulates metabolic actions of glucocorticoids by phosphorylating the glucocorticoid receptor through p38 MAPK

Molecular Endocrinology

Volumn 24, Issue 9, 2010, Pages 1748-1764

  Nader, Nancy ^a   Ng, Sinnie Sin Man ^c   Lambrou, George I ^d   Pervanidou, Panagiota ^d   Wang, Yonghong ^b   Chrousos, George P ^d   Kino, Tomoshige ^a  

^a EUNICE KENNEDY SHRIVER NATIONAL INSTITUTE OF CHILD HEALTH AND HUMAN DEVELOPMENT   (United States)

^b NATIONAL CANCER INSTITUTE   (United States)

^c and Hong Kong Branch of CAS Center for Excellence in Animal Evolution and Genetics   (Hong Kong)

^d UNIVERSITY OF ATHENS MEDICAL SCHOOL   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ADENYLATE KINASE; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; GLUCOSE; LENTIVIRUS VECTOR; LEUCINE ZIPPER PROTEIN; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38;

ADOLESCENT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BODY MASS; CARBOHYDRATE METABOLISM; CELL STRAIN 3T3; CHILD; CONTROLLED STUDY; ENZYME ACTIVATION; FATTY LIVER; GENE EXPRESSION; GLUCOSE BLOOD LEVEL; GLUCOSE METABOLISM; HORMONE ACTION; HORMONE RESPONSIVE ELEMENT; HUMAN; HUMAN CELL; MALE; METABOLIC REGULATION; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROADIPOCYTE; PROMOTER REGION; PROTEIN DNA BINDING; PROTEIN PHOSPHORYLATION; RAT; SCHOOL CHILD; SIGNAL TRANSDUCTION; TISSUE SPECIFICITY; TRANSCRIPTION REGULATION; TRANSCRIPTOMICS;

ADIPOCYTES; AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; BLOOD GLUCOSE; BODY MASS INDEX; CATALYTIC DOMAIN; DEXAMETHASONE; DOWN-REGULATION; FATTY LIVER; GENE KNOCKDOWN TECHNIQUES; GLUCOCORTICOIDS; HUMANS; LIVER; MICE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SPECIFICITY; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PHOSPHORYLATION; PHOSPHOSERINE; PROMOTER REGIONS, GENETIC; RATS; RECEPTORS, GLUCOCORTICOID; RIBONUCLEOTIDES; RNA, MESSENGER; TRANSCRIPTION FACTORS; TRANSCRIPTION, GENETIC;

RATTUS;

EID: 77956105754     PISSN: 08888809     EISSN: None     Source Type: Journal    
DOI: 10.1210/me.2010-0192     Document Type: Article

References (66)

1. Chrousos GP, Kino T 2007 Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress 10:213-219 (Pubitemid 46789478)
2. Kino T, Chrousos GP 2004 Glucocorticoid effect on gene expression. In: Steckler T, Kalin NH, Reul JMHM, eds. Handbook on stress and the brain, part 1. Amsterdam: Elsevier BV; 295-312
3. Kino T, De Martino MU, Charmandari E, Mirani M, Chrousos GP 2003 Tissue glucocorticoid resistance/hypersensitivity syndromes. J Steroid Biochem Mol Biol 85:457-467
4. Chrousos GP 2001 Glucocorticoid therapy. In: Felig P, Frohman L, eds. Endocrinology and metabolism. 4th ed. New York: McGraw-Hill; 609-632
5. Galon J, Franchimont D, Hiroi N, Frey G, Boettner A, Ehrhart-Bornstein M, O'Shea JJ, Chrousos GP, Bornstein SR 2002 Gene profiling reveals unknown enhancing and suppressive actions of glucocorticoids on immune cells. FASEB J 16:61-71 (Pubitemid 34027951)
6. Adam TC, Epel ES 2007 Stress, eating and the reward system. Physiol Behav 91:449-458
7. Dujovne CA, Azarnoff DL 1973 Clinical complications of corticosteroid therapy. A selected review. Med Clin North Am 57:1331-1342
8. van Rossum EF, Russcher H, Lamberts SW 2005 Genetic polymorphisms and multifactorial diseases: facts and fallacies revealed by the glucocorticoid receptor gene. Trends Endocrinol Metab 16:445-450 (Pubitemid 41660860)
9. Chrousos GP 2004 The glucocorticoid receptor gene, longevity, and the complex disorders of Western societies. Am J Med 117:204-207 (Pubitemid 39055875)
10. Chrousos GP, Kino T 2005 Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci STKE 2005:pe48
11. Kino T, Chrousos GP 2004 Glucocorticoid and mineralocorticoid receptors and associated diseases. Essays Biochem 40:137-155 (Pubitemid 38901170)
12. Lonard DM, Lanz RB, O'Malley BW 2007 Nuclear receptor coregulators and human disease. Endocr Rev 28:575-587 (Pubitemid 47236337)
13. Miller AL, Webb MS, Copik AJ, Wang Y, Johnson BH, Kumar R, Thompson EB 2005 p38 mitogen-activated protein kinase (MAPK) is a key mediator in glucocorticoid-induced apoptosis of lymphoid cells: correlation between p38 MAPK activation and site-specific phosphorylation of the human glucocorticoid receptor at serine 211. Mol Endocrinol 19:1569-1583 (Pubitemid 41002986)
14. Ismaili N, Garabedian MJ 2004 Modulation of glucocorticoid receptor function via phosphorylation. Ann NY Acad Sci 1024:86-101 (Pubitemid 38879595)
15. Itoh M, Adachi M, Yasui H, Takekawa M, Tanaka H, Imai K 2002 Nuclear export of glucocorticoid receptor is enhanced by c-Jun N-terminal kinase-mediated phosphorylation. Mol Endocrinol 16:2382-2392 (Pubitemid 35155548)
16. Rogatsky I, Logan SK, Garabedian MJ 1998 Antagonism of glucocorticoid receptor transcriptional activation by the c-Jun N-terminal kinase. Proc Natl Acad Sci USA 95:2050-2055 (Pubitemid 28145892)
17. Szatmáry Z, Garabedian MJ, Vilcek J 2004 Inhibition of glucocorticoid receptor-mediated transcriptional activation by p38 mitogen-activated protein (MAP) kinase. J Biol Chem 279:43708-43715 (Pubitemid 39390675)
18. Krstic MD, Rogatsky I, Yamamoto KR, Garabedian MJ 1997 Mitogen-activated and cyclin-dependent protein kinases selectively and differentially modulate transcriptional enhancement by the glucocorticoid receptor. Mol Cell Biol 17:3947-3954 (Pubitemid 27281870)
19. Wang Z, Frederick J, Garabedian MJ 2002 Deciphering the phosphorylation code of the glucocorticoid receptor in vivo. J Biol Chem 277:26573-26580
20. Webster JC, Jewell CM, Bodwell JE, Munck A, Sar M, Cidlowski JA 1997 Mouse glucocorticoid receptor phosphorylation status influences multiple functions of the receptor protein. J Biol Chem 272:9287-9293 (Pubitemid 27154940)
21. Kino T, Ichijo T, Amin ND, Kesavapany S, Wang Y, Kim N, Rao S, Player A, Zheng YL, Garabedian MJ, Kawasaki E, Pant HC, Chrousos GP 2007 Cyclin-dependent kinase 5 differentially regulates the transcriptional activity of the glucocorticoid receptor through phosphorylation: clinical implications for the nervous system response to glucocorticoids and stress. Mol Endocrinol 21:1552-1568 (Pubitemid 47001081)
22. Kino T 2007 Tissue glucocorticoid sensitivity: beyond stochastic regulation on the diverse actions of glucocorticoids. Horm Metab Res 39:420-424 (Pubitemid 46999848)
23. 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 (Pubitemid 43960587)
24. Hardie DG 2007 AMP-activated protein kinase as a drug target. Annu Rev Pharmacol Toxicol 47:185-210 (Pubitemid 46272128)
25. Kola B, Boscaro M, Rutter GA, Grossman AB, Korbonits M 2006 Expanding role of AMPK in endocrinology. Trends Endocrinol Metab 17:205-215
26. Corton JM, Gillespie JG, Hawley SA, Hardie DG 1995 5-Aminoimidazole-4- carboxamide ribonucleoside. A specific method for activating AMP-activated protein kinase in intact cells? Eur J Biochem 229:558-565
27. Sullivan JE, Brocklehurst KJ, Marley AE, Carey F, Carling D, Beri RK 1994 Inhibition of lipolysis and lipogenesis in isolated rat adipocytes with AICAR, a cell-permeable activator of AMP-activated protein kinase. FEBS Lett 353:33-36
28. Stefanelli C, Stanic I, Bonavita F, Flamigni F, Pignatti C, Guarnieri C, Caldarera CM 1998 Inhibition of glucocorticoid-induced apoptosis with 5-aminoimidazole-4-carboxamide ribonucleoside, a cell-permeable activator of AMP-activated protein kinase. Biochem Biophys Res Commun 243:821-826 (Pubitemid 28414166)
29. Lemieux K, Konrad D, Klip A, Marette A 2003 The AMP-activated protein kinase activator AICAR does not induce GLUT4 translocation to transverse tubules but stimulates glucose uptake and p38 mitogen-activated protein kinases α and β in skeletal muscle. FASEB J 17:1658-1665 (Pubitemid 37100067)
30. Xi X, Han J, Zhang JZ 2001 Stimulation of glucose transport by AMP-activated protein kinase via activation of p38 mitogen-activated protein kinase. J Biol Chem 276:41029-41034
31. Witters LA, Gao G, Kemp BE, Quistorff B 1994 Hepatic 5′-AMP- activated protein kinase: zonal distribution and relationship to acetyl-CoA carboxylase activity in varying nutritional states. Arch Biochem Biophys 308:413-419
32. Sullivan JE, Carey F, Carling D, Beri RK 1994 Characterisation of 5′-AMP-activated protein kinase in human liver using specific peptide substrates and the effects of 5′-AMP analogues on enzyme activity. Biochem Biophys Res Commun 200:1551-1556
33. Jakobsen SN, Hardie DG, Morrice N, Tornqvist HE 2001 5′-AMP- activated protein kinase phosphorylates IRS-1 on Ser-789 in mouse C2C12 myotubes in response to 5-aminoimidazole-4-carboxamide riboside. J Biol Chem 276:46912-46916
34. Kiens B 2006 Skeletal muscle lipid metabolism in exercise and insulin resistance. Physiol Rev 86:205-243
35. Hardie DG, Scott JW, Pan DA, Hudson ER 2003 Management of cellular energy by the AMP-activated protein kinase system. FEBS Lett 546:113-120
36. Postic C, Dentin R, Girard J 2004 Role of the liver in the control of carbohydrate and lipid homeostasis. Diabetes Metab 30:398-408
37. Imai E, Stromstedt PE, Quinn PG, Carlstedt-Duke J, Gustafsson JA, Granner DK 1990 Characterization of a complex glucocorticoid response unit in the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol 10:4712-4719
38. Lin B, Morris DW, Chou JY 1998 Hepatocyte nuclear factor 1α is an accessory factor required for activation of glucose-6-phosphatase gene transcription by glucocorticoids. DNA Cell Biol 17:967-974
39. Blind RD, Garabedian MJ 2008 Differential recruitment of glucocorticoid receptor phospho-isoforms to glucocorticoid-induced genes. J Steroid Biochem Mol Biol 109:150-157
40. Asselin-Labat ML, David M, Biola-Vidamment A, Lecoeuche D, Zennaro MC, Bertoglio J, Pallardy M 2004 GILZ, a new target for the transcription factor FoxO3, protects T lymphocytes from interleukin-2 withdrawal-induced apoptosis. Blood 104:215-223
41. Irusen E, Matthews JG, Takahashi A, Barnes PJ, Chung KF, Adcock IM 2002 p38 mitogen-activated protein kinase-induced glucocorticoid receptor phosphorylation reduces its activity: role in steroid-insensitive asthma. J Allergy Clin Immunol 109:649-657
42. Shi Y, Gaestel M 2002 In the cellular garden of forking paths: how p38 MAPKs signal for downstream assistance. Biol Chem 383:1519-1536
43. Behren A, Mühlen S, Acuna Sanhueza GA, Schwager C, Plinkert PK, Huber PE, Abdollahi A, Simon C 2010 Phenotype-assisted transcriptome analysis identifies FOXM1 downstream from Ras-MKK3-p38 to regulate in vitro cellular invasion. Oncogene 29:1519-1530
44. McKenna NJ, Lanz RB, O'Malley BW 1999 Nuclear receptor coregulators: cellular and molecular biology. Endocr Rev 20:321-344
45. Rosenfeld MG, Lunyak VV, Glass CK 2006 Sensors and signals: a coactivator/corepressor/epigenetic code for integrating signal-dependent programs of transcriptional response. Genes Dev 20:1405-1428
46. Eriksson JW 2007 Metabolic stress in insulin's target cells leads to ROS accumulation - a hypothetical common pathway causing insulin resistance. FEBS Lett 581:3734-3742
47. Kino T, Hurt DE, Ichijo T, Nader N, Chrousos GP 2010 Noncoding RNA gas5 is a growth arrest- and starvation-associated repressor of the glucocorticoid receptor. Sci Signal 3:ra8
48. Christ-Crain M, Kola B, Lolli F, Fekete C, Seboek D, Wittmann G, Feltrin D, Igreja SC, Ajodha S, Harvey-White J, Kunos G, Müller B, Pralong F, Aubert G, Arnaldi G, Giacchetti G, Boscaro M, Grossman AB, Korbonits M 2008 AMP-activated protein kinase mediates glucocorticoid-induced metabolic changes: a novel mechanism in Cushing's syndrome. FASEB J 22:1672-1683
49. Shimizu H, Arima H, Watanabe M, Goto M, Banno R, Sato I, Ozaki N, Nagasaki H, Oiso Y 2008 Glucocorticoids increase neuropeptide Y and agouti-related peptide gene expression via AMP-activated protein kinase signaling in the arcuate nucleus of rats. Endocrinology 149:4544-4553
50. Majzoub JA 1995 Adrenocorticotropin. In: Melmed S, ed. The pituitary. Cambridge, UK: Blackwell; 45-97
51. Iwasaki Y, Nishiyama M, Taguchi T, Kambayashi M, Asai M, Yoshida M, Nigawara T, Hashimoto K 2007 Activation of AMP-activated protein kinase stimulates proopiomelanocortin gene transcription in AtT20 corticotroph cells. Am J Physiol Endocrinol Metab 292:E1899-E1905
52. Turkish AR 2008 Nonalcoholic fatty liver disease: emerging mechanisms and consequences. Curr Opin Clin Nutr Metab Care 11:128-133
53. Musi N, Hirshman MF, Nygren J, Svanfeldt M, Bavenholm P, Rooyackers O, Zhou G, Williamson JM, Ljunqvist O, Efendic S, Moller DE, Thorell A, Goodyear LJ 2002 Metformin increases AMP-activated protein kinase activity in skeletal muscle of subjects with type 2 diabetes. Diabetes 51:2074-2081
54. Zhao G, Iyengar RR, Judd AS, Cool B, Chiou W, Kifle L, Frevert E, Sham H, Kym PR 2007 Discovery and SAR development of thienopyridones: a class of small molecule AMPK activators. Bioorg Med Chem Lett 17:3254-3257
55. Cool B, Zinker B, Chiou W, Kifle L, Cao N, Perham M, Dickinson R, Adler A, Gagne G, Iyengar R, Zhao G, Marsh K, Kym P, Jung P, Camp HS, Frevert E 2006 Identification and characterization of a small molecule AMPK activator that treats key components of type 2 diabetes and the metabolic syndrome. Cell Metab 3:403-416
56. Lee YS, Kim WS, Kim KH, Yoon MJ, Cho HJ, Shen Y, Ye JM, Lee CH, Oh WK, Kim CT, Hohnen-Behrens C, Gosby A, Kraegen EW, James DE, Kim JB 2006 Berberine, a natural plant product, activates AMP-activated protein kinase with beneficial metabolic effects in diabetic and insulin-resistant states. Diabetes 55:2256-2264
57. Kino T, Tiulpakov A, Ichijo T, Chheng L, Kozasa T, Chrousos GP 2005 G protein β interacts with the glucocorticoid receptor and suppresses its transcriptional activity in the nucleus. J Cell Biol 169:885-896
58. Daniel T, Carling D 2002 Functional analysis of mutations in the γ2 subunit of AMP-activated protein kinase associated with cardiac hypertrophy and Wolff-Parkinson-White syndrome. J Biol Chem 277:51017-51024
59. Dérijard B, Raingeaud J, Barrett T, Wu IH, Han J, Ulevitch RJ, Davis RJ 1995 Independent human MAP-kinase signal transduction pathways defined by MEK and MKK isoforms. Science 267:682-685
60. Raingeaud J, Whitmarsh AJ, Barrett T, Dérijard B, Davis RJ 1996 MKK3- and MKK6-regulated gene expression is mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Mol Cell Biol 16:1247-1255
61. Kino T, Gragerov A, Kopp JB, Stauber RH, Pavlakis GN, Chrousos GP 1999 The HIV-1 virion-associated protein vpr is a coactivator of the human glucocorticoid receptor. J Exp Med 189:51-62
62. Nader N, Chrousos GP, Kino T 2009 Circadian rhythm transcription factor CLOCK regulates the transcriptional activity of the glucocorticoid receptor by acetylating its hinge region lysine cluster: potential physiological implications. FASEB J 23:1572-1583
63. Ichijo T, Chrousos GP, Kino T 2008 Activated glucocorticoid receptor interacts with the INHAT component Set/TAF-Iβ and releases it from a glucocorticoid-responsive gene promoter, relieving repression: implications for the pathogenesis of glucocorticoid resistance in acute undifferentiated leukemia with Set-Can translocation. Mol Cell Endocrinol 283:19-31
64. Ichijo T, Voutetakis A, Cotrim AP, Bhattachryya N, Fujii M, Chrousos GP, Kino T 2005 The Smad6-histone deacetylase 3 complex silences the transcriptional activity of the glucocorticoid receptor: potential clinical implications. J Biol Chem 280:42067-42077
65. Kino T, Takatori H, Manoli I, Wang Y, Tiulpakov A, Blackman MR, Su YA, Chrousos GP, DeCherney AH, Segars JH 2009 Brx mediates the response of lymphocytes to osmotic stress through the activation of NFAT5. Sci Signal 2:ra5
66. van der Laan S, Sarabdjitsingh RA, Van Batenburg MF, Lachize SB, Li H, Dijkmans TF, Vreugdenhil E, de Kloet ER, Meijer OC 2008 Chromatin immunoprecipitation scanning identifies glucocorticoid receptor binding regions in the proximal promoter of a ubiquitously expressed glucocorticoid target gene in brain. J Neurochem 106:2515-2523