A peripheral endocannabinoid mechanism contributes to glucocorticoid-mediated metabolic syndrome

Proceedings of the National Academy of Sciences of the United States of America

Volumn 112, Issue 1, 2015, Pages 285-290

  Bowles, Nicole P ^a   Karatsoreos, Ilia N ^a,b   Li, Xiaosong ^c   Vemuri, V Kiran ^d   Wood, Jodi Anne ^d   Li, Zhiying ^a   Tamashiro, Kellie L K ^e   Schwartz, Gary J ^c   Makriyannis, Alexandros M ^d   Kunos, George ^f   Hillard, Cecilia J ^g   McEwen, Bruce S ^a   Hill, Matthew N ^a,h  

^a ROCKEFELLER UNIVERSITY   (United States)

^b WASHINGTON STATE UNIVERSITY   (United States)

^c ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

^d NORTHEASTERN UNIVERSITY   (United States)

^e JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTE ON ALCOHOL ABUSE AND ALCOHOLISM   (United States)

^g MEDICAL COLLEGE OF WISCONSIN   (United States)

^h UNIVERSITY OF CALGARY   (Canada)

Author keywords

2 AG; Anandamide; Corticosterone; Liver; Obesity

Indexed keywords

1 (2,4 DICHLOROPHENYL) 5 (4 IODOPHENYL) 4 METHYL N (1 PIPERIDYL) 1H PYRAZOLE 3 CARBOXAMIDE; ACYLGLYCEROL LIPASE; ANANDAMIDE; CANNABINOID 1 RECEPTOR; CORTICOSTEROID; ENDOCANNABINOID; FATTY ACID AMIDASE; INSULIN; LEPTIN; LIPOPROTEIN LIPASE; MESSENGER RNA; CORTICOSTERONE; GLUCOCORTICOID;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIET INDUCED OBESITY; DYSLIPIDEMIA; FATTY ACID OXIDATION; FATTY LIVER; HYPERGLYCEMIA; HYPERINSULINEMIA; HYPERLEPTINEMIA; HYPERLIPIDEMIA; HYPERPHAGIA; HYPOTHALAMUS; LIPID METABOLISM; METABOLIC SYNDROME X; MOUSE; NONHUMAN; PHENOTYPE; SIGNAL TRANSDUCTION; WEIGHT GAIN; ANIMAL; ANTAGONISTS AND INHIBITORS; ANTIBODY SPECIFICITY; C57BL MOUSE; CHEMICALLY INDUCED; DRUG EFFECTS; GENETICS; LIVER; METABOLISM; OBESITY; PATHOLOGY;

MUS;

ANIMALS; CORTICOSTERONE; DYSLIPIDEMIAS; ENDOCANNABINOIDS; GLUCOCORTICOIDS; LIVER; METABOLIC SYNDROME X; MICE, INBRED C57BL; OBESITY; ORGAN SPECIFICITY; RECEPTOR, CANNABINOID, CB1; RNA, MESSENGER; SIGNAL TRANSDUCTION;

EID: 84920450557     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1421420112     Document Type: Article

References (61)

1. Rosenzweig JL, et al.; Endocrine Society (2008) Primary prevention of cardiovascular disease and type 2 diabetes in patients at metabolic risk: An endocrine society clinical practice guideline. J Clin Endocrinol Metab 93(10):3671-3689.
2. Grundy SM, Brewer HB, Jr, Cleeman JI, Smith SC, Jr, Lenfant C; American Heart Association; National Heart, Lung, and Blood Institute (2004) Definition of metabolic syndrome: Report of the National Heart, Lung, and Blood Institute/American Heart Association conference on scientific issues related to definition. Circulation 109(3):433-438.
3. Dallman MF (2010) Stress-induced obesity and the emotional nervous system. Trends Endocrinol Metab 21(3):159-165.
4. McEwen BS (2008) Central effects of stress hormones in health and disease: Understanding the protective and damaging effects of stress and stress mediators. Eur J Pharmacol 583(2-3):174-185.
5. Wardle J, Chida Y, Gibson EL, Whitaker KL, Steptoe A (2011) Stress and adiposity: A meta-analysis of longitudinal studies. Obesity (Silver Spring) 19(4):771-778.
6. Patterson ZR, Abizaid A (2013) Stress induced obesity: Lessons from rodent models of stress. Front Neurosci 7(2013):130.
7. Trikudanathan S, McMahon GT (2008) Optimum management of glucocorticoid-treated patients. Nat Clin Pract Endocrinol Metab 4(5):262-271.
8. Hill MN, McEwen BS (2010) Involvement of the endocannabinoid system in the neurobehavioural effects of stress and glucocorticoids. Prog Neuropsychopharmacol Biol Psychiatry 34(5):791-797.
9. Campolongo P, et al. (2009) Endocannabinoids in the rat basolateral amygdala enhance memory consolidation and enable glucocorticoid modulation of memory. Proc Natl Acad Sci USA 106(12):4888-4893.
10. Coddington E, Lewis C, Rose JD, Moore FL (2007) Endocannabinoids mediate the effects of acute stress and corticosterone on sex behavior. Endocrinology 148(2):493-500.
11. Evanson NK, Tasker JG, Hill MN, Hillard CJ, Herman JP (2010) Fast feedback inhibition of the HPA axis by glucocorticoids is mediated by endocannabinoid signaling. Endocrinology 151(10):4811-4819.
12. Engeli S, et al. (2005) Activation of the peripheral endocannabinoid system in human obesity. Diabetes 54(10):2838-2843.
13. Silvestri C, Di Marzo V (2013) The endocannabinoid system in energy homeostasis and the etiopathology of metabolic disorders. Cell Metab 17(4):475-490.
14. Karatsoreos IN, et al. (2010) Endocrine and physiological changes in response to chronic corticosterone: A potential model of the metabolic syndrome in mouse. Endocrinology 151(5):2117-2127.
15. Fraser R, et al. (1999) Cortisol effects on body mass, blood pressure, and cholesterol in the general population. Hypertension 33(6):1364-1368.
16. Björntorp P, Rosmond R (2000) Neuroendocrine abnormalities in visceral obesity. Int J Obes Relat Metab Disord 24(Suppl 2):S80-S85.
17. Cassano AE, et al. (2012) Anatomic, hematologic, and biochemical features of C57BL/6NCrl mice maintained on chronic oral corticosterone. Comp Med 62(5):348-360.
18. Pecoraro N, Reyes F, Gomez F, Bhargava A, Dallman MF (2004) Chronic stress promotes palatable feeding, which reduces signs of stress: Feedforward and feedback effects of chronic stress. Endocrinology 145(8):3754-3762.
19. Dallman MF, et al. (2004) Minireview: Glucocorticoids-food intake, abdominal obesity, and wealthy nations in 2004. Endocrinology 145(6):2633-2638.
20. De Vriendt T, Moreno LA, De Henauw S (2009) Chronic stress and obesity in adolescents: Scientific evidence and methodological issues for epidemiological research. Nutr Metab Cardiovasc Dis 19(7):511-519.
21. Santana P, et al. (1995) Aldosterone and dexamethasone both stimulate energy acquisition whereas only the glucocorticoid alters energy storage. Endocrinology 136(5):2214-2222.
22. Osei-Hyiaman D, et al. (2008) Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice. J Clin Invest 118(9):3160-3169.
23. 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. Br J Pharmacol 136(4):550-557.
24. Pagotto U, et al. (2006) How many sites of action for endocannabinoids to control energy metabolism? Int J Obes (Lond) 30(Suppl 1):S39-S43.
25. Osei-Hyiaman D, et al. (2005) Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity. J Clin Invest 115(5):1298-1305.
26. Matias I, et al. (2008) Dysregulation of peripheral endocannabinoid levels in hyperglycemia and obesity: Effect of high fat diets. Mol Cell Endocrinol 286(1-2 Suppl 1):S66-S78.
27. Côté M, et al. (2007) Circulating endocannabinoid levels, abdominal adiposity and related cardiometabolic risk factors in obese men. Int J Obes (Lond) 31(4):692-699.
28. Tam J, et al. (2010) Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J Clin Invest 120(8):2953-2966.
29. Cinar R, et al. (2014) Hepatic cannabinoid-1 receptors mediate diet-induced insulin resistance by increasing de novo synthesis of long-chain ceramides. Hepatology 59(1):143-153.
30. Liu J, et al. (2012) Hepatic cannabinoid receptor-1 mediates diet-induced insulin resistance via inhibition of insulin signaling and clearance in mice. Gastroenterology 142(5):1218.e1-1228.e1.
31. Strekalova T, Spanagel R, Bartsch D, Henn FA, Gass P (2004) Stress-induced anhedonia in mice is associated with deficits in forced swimming and exploration. Neuropsychopharmacology 29(11):2007-2017.
32. Rothwell NJ, Stock MJ, York DA (1984) Effects of adrenalectomy on energy balance, diet-induced thermogenesis and brown adipose tissue in adult cafeteria-fed rats. Comp Biochem Physiol A 78(3):565-569.
33. Mantha L, Palacios E, Deshaies Y (1999) Modulation of triglyceride metabolism by glucocorticoids in diet-induced obesity. Am J Physiol 277(2 Pt 2):R455-R464.
34. Makimura H, et al. (2000) Adrenalectomy reverses obese phenotype and restores hypothalamic melanocortin tone in leptin-deficient ob/ob mice. Diabetes 49(11):1917-1923.
35. Makimura H, Mizuno TM, Beasley J, Silverstein JH, Mobbs CV (2003) Adrenalectomy stimulates hypothalamic proopiomelanocortin expression but does not correct diet-induced obesity. BMC Physiol 3:4.
36. Ravinet Trillou C, Delgorge C, Menet C, Arnone M, Soubrie P (2004) CB1 cannabinoid receptor knockout in mice leads to leanness, resistance to diet-induced obesity and enhanced leptin sensitivity. J Obes Relat Metab Disord 28(4):640-648.
37. Scerif M, et al. (2013) CB1 receptor mediates the effects of glucocorticoids on AMPK activity in the hypothalamus. J Endocrinol 219(1):79-88.
38. Di S, Malcher-Lopes R, Halmos KC, Tasker JG (2003) Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: A fast feedback mechanism. J Neurosci 23(12):4850-4857.
39. Wang J, Shen RY, Haj-Dahmane S (2012) Endocannabinoids mediate the glucocorticoid-induced inhibition of excitatory synaptic transmission to dorsal raphe serotonin neurons. J Physiol 590(Pt 22):5795-5808.
40. Wang M, et al. (2012) Acute restraint stress enhances hippocampal endocannabinoid function via glucocorticoid receptor activation. J Psychopharmacol 26(1):56-70.
41. Hill MN, et al. (2011) Recruitment of prefrontal cortical endocannabinoid signaling by glucocorticoids contributes to termination of the stress response. J Neurosci 31(29):10506-10515.
42. Dlugos A, Childs E, Stuhr KL, Hillard CJ, de Wit H (2012) Acute stress increases circulating anandamide and other N-acylethanolamines in healthy humans. Neuropsychopharmacology 37(11):2416-2427.
43. Hill MN, et al. (2013) Reductions in circulating endocannabinoid levels in individuals with post-traumatic stress disorder following exposure to the World Trade Center attacks. Psychoneuroendocrinology 38(12):2952-2961.
44. Di Marzo V, et al. (2001) Leptin-regulated endocannabinoids are involved in maintaining food intake. Nature 410(6830):822-825.
45. Jamshidi N, Taylor DA (2001) Anandamide administration into the ventromedial hypothalamus stimulates appetite in rats. Br J Pharmacol 134(6):1151-1154.
46. Verty AN, McGregor IS, Mallet PE (2005) Paraventricular hypothalamic CB(1) cannabinoid receptors are involved in the feeding stimulatory effects of Delta(9)-tetrahydrocannabinol. Neuropharmacology 49(8):1101-1109.
47. Higuchi S, et al. (2010) The cannabinoid 1-receptor silent antagonist O-2050 attenuates preference for high-fat diet and activated astrocytes in mice. J Pharmacol Sci 112(3):369-372.
48. Mahler SV, Smith KS, Berridge KC (2007) Endocannabinoid hedonic hotspot for sensory pleasure: Anandamide in nucleus accumbens shell enhances 'liking' of a sweet reward. Neuropsychopharmacology 32(11):2267-2278.
49. Soria-Gómez E, et al. (2014) The endocannabinoid system controls food intake via olfactory processes. Nat Neurosci 17(3):407-415.
50. Quarta C, et al. (2010) CB(1) signaling in forebrain and sympathetic neurons is a key determinant of endocannabinoid actions on energy balance. Cell Metab 11(4):273-285.
51. Buettner C, et al. (2008) Leptin controls adipose tissue lipogenesis via central, STAT3-independent mechanisms. Nat Med 14(6):667-675.
52. Jourdan T, et al. (2012) Antagonism of peripheral hepatic cannabinoid receptor-1 improves liver lipid metabolism in mice: Evidence from cultured explants. Hepatology 55(3):790-799.
53. Mancini GQC, Srivastava RK, Klaus S, Pagotto U, Lutz B (2010) Adipocyte-specific CB1 conditional knock-out mice: New insights in the study of obesity and metabolic syndrome. Proceedings of the 20th Annual Symposium on the Cannabinoids (International Cannabinoid Research Society, Research Triangle Park, NC), p 17.
54. Larsson H, Ahrén B (1996) Short-term dexamethasone treatment increases plasma leptin independently of changes in insulin sensitivity in healthy women. J Clin Endocrinol Metab 81(12):4428-4432.
55. Miell JP, Englaro P, Blum WF (1996) Dexamethasone induces an acute and sustained rise in circulating leptin levels in normal human subjects. Horm Metab Res 28(12):704-707.
56. Russell CD, et al. (1998) Leptin expression in adipose tissue from obese humans: Depot-specific regulation by insulin and dexamethasone. Am J Physiol 275(3 Pt 1):E507-E515.
57. Kolaczynski JW, Goldstein BJ, Considine RV (1997) Dexamethasone, OB gene, and leptin in humans; effect of exogenous hyperinsulinemia. J Clin Endocrinol Metab 82(11):3895-3897.
58. Postic C, et al. (1999) Dual roles for glucokinase in glucose homeostasis as determined by liver and pancreatic beta cell-specific gene knock-outs using Cre recombinase. J Biol Chem 274(1):305-315.
59. Patel S, et al. (2005) The postmortal accumulation of brain N-arachidonylethanolamine (anandamide) is dependent upon fatty acid amide hydrolase activity. J Lipid Res 46(2):342-349.
60. Hill MN, Miller GE, Ho WS, Gorzalka BB, Hillard CJ (2008) Serum endocannabinoid content is altered in females with depressive disorders: A preliminary report. Pharmacopsychiatry 41(2):48-53.
61. Williams J, et al. (2007) Quantitative method for the profiling of the endocannabinoid metabolome by LC-atmospheric pressure chemical ionization-MS. Anal Chem 79(15):5582-5593.