CB1 receptor mediates the effects of glucocorticoids on AMPK activity in the hypothalamus

Journal of Endocrinology

Volumn 219, Issue 1, 2013, Pages 79-88

  Scerif, Miski ^a   Füzesi, Tamás ^b   Thomas, Julia D ^a   Kola, Blerina ^a   Grossman, Ashley B ^a,d   Fekete, Csaba ^b,c   Korbonits, Márta ^a  

^a QUEEN MARY UNIVERSITY OF LONDON   (United Kingdom)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^c TUFTS MEDICAL CENTER   (United States)

^d UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

AMPK activity; CB1 receptor; Glucocorticoids

Indexed keywords

CANNABINOID 1 RECEPTOR; CORTICOSTERONE; CORTICOTROPIN; GLUCOCORTICOID; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BODY WEIGHT; CALORIC INTAKE; COMPARATIVE STUDY; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; CORTICOTROPIN BLOOD LEVEL; CUSHING SYNDROME; ENZYME ACTIVITY; HEART; HYPOTHALAMUS; INTRAABDOMINAL FAT; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SUBCUTANEOUS FAT; WEIGHT GAIN; WHITE ADIPOSE TISSUE;

AMPK ACTIVITY; CB1 RECEPTOR; GLUCOCORTICOIDS;

ADIPOSE TISSUE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; CORTICOSTERONE; CUSHING SYNDROME; DISEASE MODELS, ANIMAL; GLUCOCORTICOIDS; HYPOTHALAMUS; LIVER; MALE; MICE; MYOCARDIUM; RECEPTOR, CANNABINOID, CB1;

EID: 84884169835     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-13-0192     Document Type: Article

References (54)

1. Andersson U, Filipsson K, Abbott CR, Woods A, Smith K, Bloom SR, Carling D & Small CJ 2004 AMP-activated protein kinase plays a role in the control of food intake. Journal of Biological Chemistry 279 12005-12008. (doi:10.1074/jbc.C300557200)
2. Bell ME, Bhatnagar S, Liang J, Soriano L, Nagy TR & Dallman MF 2000 Voluntary sucrose ingestion, like corticosterone replacement, prevents the metabolic deficits of adrenalectomy. Journal of Neuroendocrinology 12 461-470. (doi:10.1046/j.1365-2826.2000.00488.x)
3. Boyle JG, Logan PJ, Jones GC, Small M, Sattar N, Connell JM, Cleland SJ & Salt IP 2011 AMP-activated protein kinase is activated in adipose tissue of individuals with type 2 diabetes treated with metformin: a randomised glycaemia-controlled crossover study. Diabetologia 54 1799-1809. (doi:10.1007/s00125-011-2126-4)
4. Butler H & Korbonits M 2009 Cannabinoids for clinicians: the rise and fall of the cannabinoid antagonists. European Journal of Endocrinology 161 655-662. (doi:10.1530/EJE-09-0511)
5. Christ-Crain M, Kola B, Lolli F, Fekete C, Seboek D, Wittmann G, Feltrin D, Igreja SC, Ajodha S, Harvey-White J et al. 2008 AMP-activated protein kinase mediates glucocorticoid-induced metabolic changes: a novel mechanism in Cushing's syndrome. FASEB Journal 22 1672-1683. (doi:10.1096/fj.07-094144)
6. Cota D, Marsicano G, Tschop M, Grubler Y, Flachskamm C, Schubert M, Auer D, Yassouridis A, Thone-Reineke C, Ortmann S et al. 2003 The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. Journal of Clinical Investigation 112 423-431. (doi:10.1172/JCI17725)
7. Dallman MF, Pecoraro N, Akana SF, la Fleur SE, Gomez F, Houshyar H, Bell ME, Bhatnagar S, Laugero KD & Manalo S 2003 Chronic stress and obesity: a new view of "comfort food". PNAS 100 11696-11701. (doi:10.1073/pnas.1934666100)
8. Di S, Malcher-Lopes R, Halmos KC & Tasker JG 2003 Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. Journal of Neuroscience 23 4850-4857.
9. Di S, Malcher-Lopes R, Marcheselli VL, Bazan NG & Tasker JG 2005 Rapid glucocorticoid-mediated endocannabinoid release and opposing regulation of glutamate and g-aminobutyric acid inputs to hypothalamic magnocellular neurons. Endocrinology 146 4292-4301. (doi:10.1210/en.2005-0610)
10. Di Marzo V, Goparaju SK, Wang L, Liu J, Batkai S, Jarai Z, Fezza F, Miura GI, Palmiter RD & Sugiura T 2001 Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410 822-825. (doi:10.1038/35071088)
11. Dzamko N, van Denderen BJ, Hevener AL, Jorgensen SB, Honeyman J, Galic S, Chen ZP, Watt MJ, Campbell DJ, Steinberg GR et al. 2010 AMPKb1 deletion reduces appetite, preventing obesity and hepatic insulin resistance. Journal of Biological Chemistry 285 115-122. (doi:10.1074/jbc.M109.056762)
12. Foretz M, Ancellin N, Andreelli F, Saintillan Y, Grondin P, Kahn A, Thorens B, Vaulont S & Viollet B 2005 Short-term overexpression of a constitutively active form of AMP-activated protein kinase in the liver leads to mild hypoglycemia and fatty liver. Diabetes 54 1331-1339. (doi:10.2337/diabetes.54.5.1331)
13. Gary-Bobo M, Elachouri G, Gallas JF, Janiak P, Marini P, Ravinet-Trillou C, Chabbert M, Cruccioli N, Pfersdorff C, Roque C et al. 2007 Rimonabant reduces obesity-associated hepatic steatosis and features of metabolic syndrome in obese Zucker fa/fa rats. Hepatology 46 122-129. (doi:10.1002/hep.21641)
14. Gauthier MS, O'Brien EL, Bigornia S, MottM, Cacicedo JM, Xu XJ, Gokce N, Apovian C & Ruderman N 2011 Decreased AMP-activated protein kinase activity is associated with increased inflammation in visceral adipose tissue and with whole-body insulin resistance in morbidly obese humans. Biochemical and Biophysical Research Communications 404 382-387. (doi:10.1016/j.bbrc.2010.11.127)
15. Geer EB, ShenW, Gallagher D, Punyanitya M, Looker HC, Post KD & Freda PU 2010 MRI assessment of lean and adipose tissue distribution in female patients with Cushing's disease. Clinical Endocrinology 73 469-475. (doi:10.1111/j.1365-2265.2010.03829.x)
16. Grundemann D, Schechinger B, Rappold GA & Schomig E 1998 Molecular identification of the corticosterone-sensitive extraneuronal catecholamine transporter. Nature Neuroscience 1 349-351. (doi:10.1038/1557)
17. Hadoke PW, Iqbal J & Walker BR 2009 Therapeutic manipulation of glucocorticoid metabolism in cardiovascular disease. British Journal of Pharmacology 156 689-712. (doi:10.1111/j.1476-5381.2008.00047.x)
18. Hawley SA, Boudeau J, Reid JL, Mustard KJ, Udd L, Makela TP, Alessi DR & Hardie DG 2003 Complexes between the LKB1 tumor suppressor, STRADa/b and MO25a/b are upstream kinases in the AMP-activated protein kinase cascade. Journal of Biology 2 28. (doi:10.1186/ 1475-4924-2-28)
19. Hiley CR 2009 Endocannabinoids and the heart. Journal of Cardiovascular Pharmacology 53 267-276. (doi:10.1097/FJC.0b013e318192671d)
20. Hiley CR & Ford WR 2004 Cannabinoid pharmacology in the cardiovascular system: potential protective mechanisms through lipid signalling. Biological Reviews of the Cambridge Philosophical Society 79 187-205. (doi:10.1017/S1464793103006201)
21. Jbilo O, Ravinet-Trillou C, Arnone M, Buisson I, Bribes E, Peleraux A, Penarier G, Soubrie P, Le Fur G, Galiegue S et al. 2005 The CB1 receptor antagonist rimonabant reverses the diet-induced obesity phenotype through the regulation of lipolysis and energy balance. FASEB Journal 19 1567-1569. (doi:10.1096/fj.04-3177fje)
22. Jourdan T, Djaouti L, Demizieux L, Gresti J, Verges B & Degrace P 2010 CB1 antagonism exerts specific molecular effects on visceral and subcutaneous fat and reverses liver steatosis in diet-induced obesemice. Diabetes 59 926-934. (doi:10.2337/db09-1482)
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 Metabolism 1 15-25. (doi:10.1016/j.cmet.2004.12.003)
24. Kirkham TC, Williams CM, Fezza F & Di Marzo V 2002 Endocannabinoid levels in rat limbic forebrain and hypothalamus in relation to fasting, feeding and satiation: stimulation of eating by 2-arachidonoyl glycerol. British Journal of Pharmacology 136 550-557. (doi:10.1038/sj. bjp.0704767)
25. Kola B & Korbonits M 2009 Shedding light on the intricate puzzle of ghrelin's effects on appetite regulation. Journal of Endocrinology 202 191-198. (doi:10.1677/JOE-09-0056)
26. Kola B,Hubina E, Tucci SA, KirkhamTC, GarciaEA,Mitchell SE,Williams LM, Hawley SA, Hardie DG, Grossman AB et al. 2005 Cannabinoids and ghrelin have both central and peripheral metabolic and cardiac effects via AMP-activated protein kinase. Journal of Biological Chemistry 280 25196-25201. (doi:10.1074/jbc.C500175200)
27. Kola B, Boscaro M, Rutter GA, Grossman AB & Korbonits M 2006 Expanding role of AMPK in endocrinology. Trends in Endocrinology and Metabolism 17 205-215. (doi:10.1016/j.tem.2006.05.006)
28. Kola B, Christ-Crain M, Lolli F, Arnaldi G, Giacchetti G, Boscaro M, Grossman AB & Korbonits M 2008 Changes in adenosine 50-monophosphate-activated protein kinase as a mechanism of visceral obesity in Cushing's syndrome. Journal of Clinical Endocrinology and Metabolism 93 4969-4973. (doi:10.1210/jc.2008-1297)
29. Ledent C, Valverde O, Cossu G, Petitet F, Aubert JF, Beslot F, Bohme GA, Imperato A, Pedrazzini T, Roques BP et al. 1999 Unresponsiveness to cannabinoids and reduced addictive effects of opiates in CB1 receptor knockoutmice. Science 283401-404. (doi:10.1126/science.283.5400.401)
30. Li Y, Xu S, Mihaylova MM, Zheng B, Hou X, Jiang B, Park O, Luo Z, Lefai E, Shyy JY et al. 2011 AMPK phosphorylates and inhibits SREBP activity to attenuate hepatic steatosis and atherosclerosis in diet-induced insulin-resistant mice. Cell Metabolism 13 376-388. (doi:10.1016/ j.cmet.2011.03.009)
31. Lindroos J, Husa J, Mitterer G, Haschemi A, Rauscher S, Haas R, Groger M, Loewe R, Kohrgruber N, Schrogendorfer KF et al. 2013 Human but not mouse adipogenesis is critically dependent on LMO3. Cell Metabolism 18 62-74. (doi:10.1016/j.cmet.2013.05.020)
32. McBrideA,Ghilagaber S,NikolaevA&HardieDG2009 The glycogen-binding domain on the AMPKb subunit allows the kinase to act as a glycogen sensor. Cell Metabolism 9 23-34. (doi:10.1016/j.cmet.2008.11.008)
33. Minokoshi Y, Alquier T, Furukawa N, Kim YB, Lee A, Xue B, Mu J, Foufelle F, Ferre P, Birnbaum MJ et al. 2004 AMP-kinase regulates food intake by responding to hormonal and nutrient signals in the hypothalamus. Nature 428 569-574. (doi:10.1038/nature02440)
34. Muiesan ML, LupiaM, Salvetti M, Grigoletto C, Sonino N, BoscaroM, Rosei EA, Mantero F & Fallo F 2003 Left ventricular structural and functional characteristics in Cushing's syndrome. Journal of the American College of Cardiology 41 2275-2279. (doi:10.1016/S0735-1097(03)00493-5)
35. O'Hare JD, Zielinski E, Cheng B, Scherer T & Buettner C 2011 Central endocannabinoid signaling regulates hepatic glucose production and systemic lipolysis. Diabetes 60 1055-1062. (doi:10.2337/db10-0962)
36. Osei-Hyiaman D, Depetrillo M, Pacher P, Liu J, Radaeva S, Batkai S, Harvey- White J, Mackie K, Offertaler L, Wang L et al. 2005 Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. Journal of Clinical Investigation 115 1298-1305. (doi:10.1172/JCI23057)
37. Osei-Hyiaman D, Liu J, Zhou L, Godlewski G, Harvey-White J, Jeong WI, Batkai S, Marsicano G, Lutz B, Buettner C et al. 2008 Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice. Journal of Clinical Investigation 118 3160-3169. (doi:10.1172/JCI34827)
38. Perwitz N, Wenzel J, Wagner I, Buning J, Drenckhan M, Zarse K, Ristow M, Lilienthal W, Lehnert H & Klein J 2010 Cannabinoid type 1 receptor blockade induces transdifferentiation towards a brown fat phenotype in white adipocytes. Diabetes, Obesity & Metabolism 12 158-166. (doi:10.1111/j.1463-1326.2009.01133.x)
39. Pivonello R, Faggiano A, Lombardi G & Colao A 2005 The metabolic syndrome and cardiovascular risk in Cushing's syndrome. Endocrinology and Metabolism Clinics of North America 34 327-339, viii. (doi:10.1016/ j.ecl.2005.01.010)
40. Puthanveetil P, Wang F, Kewalramani G, Kim MS, Hosseini-Beheshti E, Ng N, Lau W, Pulinilkunnil T, Allard M, Abrahani A et al. 2008 Cardiac glycogen accumulation after dexamethasone is regulated by AMPK. American Journal of Physiology. Heart and Circulatory Physiology 295 H1753-H1762. (doi:10.1152/ajpheart.518.2008)
41. Qi D, An D, Kewalramani G, Qi Y, Pulinilkunnil T, Abrahani A, Al-Atar U, Ghosh S, Wambolt RB, Allard MF et al. 2006 Altered cardiac fatty acid composition and utilization following dexamethasone-induced insulin resistance. American Journal of Physiology. Endocrinology and Metabolism 291 E420-E427. (doi:10.1152/ajpendo.00083.2006)
42. Rockall AG, Sohaib SA, Evans D, Kaltsas G, Isidori AM, Monson JP, Besser GM, Grossman AB & Reznek RH 2003a Computed tomography assessment of fat distribution in male and female patients with Cushing's syndrome. European Journal of Endocrinology 149 561-567. (doi:10.1530/eje.0.1490561)
43. Rockall AG, Sohaib SA, Evans D, Kaltsas G, Isidori AM, Monson JP, Besser GM, Grossman AB & Reznek RH 2003b Hepatic steatosis in Cushing's syndrome: a radiological assessment using computed tomography. European Journal of Endocrinology 149 543-548. (doi:10.1530/eje.0.1490543)
44. Russell RR III, Li J, Coven DL, Pypaert M, Zechner C, Palmeri M, Giordano FJ, Mu J, Birnbaum MJ & Young LH 2004 AMP-activated protein kinase mediates ischemic glucose uptake and prevents postischemic cardiac dysfunction, apoptosis, and injury. Journal of Clinical Investigation 114 495-503. (doi:10.1172/JCI19297)
45. 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 adenosine monophosphate-activated protein kinase signaling in the arcuate nucleus of rats. Endocrinology 149 4544-4553. (doi:10.1210/ en.2008-0229)
46. van Staa TP, Leufkens HG, Abenhaim L, Begaud B, Zhang B & Cooper C 2000 Use of oral corticosteroids in the United Kingdom. QJM 93 105-111. (doi:10.1093/qjmed/93.2.105)
47. Tam J, Liu J, Mukhopadhyay B, Cinar R, Godlewski G & Kunos G 2011 Endocannabinoids in liver disease. Hepatology 53 346-355. (doi:10.1002/hep.24077)
48. Turu G, Varnai P, Gyombolai P, Szidonya L, Offertaler L, Bagdy G, Kunos G & Hunyady L 2009 Paracrine transactivation of the CB1 cannabinoid receptor by AT1 angiotensin and other Gq/11 protein-coupled receptors. Journal of Biological Chemistry 284 16914-16921. (doi:10.1074/jbc.M109.003681)
49. Underdown NJ, Hiley CR & FordWR 2005 Anandamide reduces infarct size in rat isolated hearts subjected to ischaemia-reperfusion by a novel cannabinoid mechanism. British Journal of Pharmacology 146 809-816. (doi:10.1038/sj.bjp.0706391)
50. Viana AY, Sakoda H, Anai M, Fujishiro M, Ono H, Kushiyama A, Fukushima Y, Sato Y, Oshida Y, Uchijima Y et al. 2006 Role of hepatic AMPK activation in glucose metabolism and dexamethasone-induced regulation of AMPK expression. Diabetes Research and Clinical Practice 73 135-142. (doi:10.1016/j.diabres.2005.12.011)
51. Wang M, Hill MN, Zhang L, Gorzalka BB, Hillard CJ & Alger BE 2012 Acute restraint stress enhances hippocampal endocannabinoid function via glucocorticoid receptor activation. Journal of Psychopharmacology 26 56-70. (doi:10.1177/0269881111409606)
52. Wittmann G, Deli L, Kallo I, Hrabovszky E, Watanabe M, Liposits Z & Fekete C 2007 Distribution of type 1 cannabinoid receptor (CB1)- immunoreactive axons in the mouse hypothalamus. Journal of Comparative Neurology 503 270-279. (doi:10.1002/cne.21383)
53. Xu M, Zhao YT, Song Y, Hao TP, Lu ZZ, Han QD, Wang SQ& Zhang YY 2007 a1-Adrenergic receptors activate AMP-activated protein kinase in rat hearts. Sheng Li Xue Bao 59 175-182.
54. Zelena D, Barna I, Pinter O, Klausz B, Varga J &Makara GB 2011 Congenital absence of vasopressin and age-dependent changes in ACTH and corticosterone stress responses in rats. Stress 14 420-430. (doi:10.3109/ 10253890.2011.552991)