Altered endocannabinoid signalling after a high-fat diet in Apoe -/- mice: Relevance to adipose tissue inflammation, hepatic steatosis and insulin resistance

Diabetologia

Volumn 54, Issue 11, 2011, Pages 2900-2910

  Bartelt, A ^a   Orlando, P ^b,c   Mele, C ^b   Ligresti, A ^b   Toedter, K ^a   Scheja, L ^a   Heeren, J ^a   Di Marzo, V ^b  

^a UNIVERSITY MEDICAL CENTER HAMBURG EPPENDORF   (Germany)

^b CNR   (Italy)

^c INSTITUTE OF PROTEIN BIOCHEMISTRY   (Italy)

Author keywords

CB1 receptor; Fasting glycaemia; Inflammation; Insulin sensitivity; Liver triacylglycerols

Indexed keywords

APOLIPOPROTEIN E; CANNABINOID 1 RECEPTOR; CD68 ANTIGEN; EGF LIKE MODULE CONTAINING MUCIN LIKE HORMONE RECEPTOR LIKE 1; ENDOCANNABINOID; GLUCOSE; HORMONE RECEPTOR; INSULIN; LEPTIN; MESSENGER RNA; MONOCYTE CHEMOTACTIC PROTEIN 1; PHOSPHOLIPID; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG;

ADIPOSE TISSUE INFLAMMATION; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BODY WEIGHT; CATABOLISM; CONTROLLED STUDY; EPIDIDYMIS FAT; FATTY LIVER; GLUCOSE METABOLISM; INFLAMMATION; INSULIN RESISTANCE; LIPID DIET; LIVER LEVEL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT; WHITE ADIPOSE TISSUE; WILD TYPE;

ADIPOSE TISSUE, WHITE; ANIMALS; APOLIPOPROTEINS E; CANNABINOID RECEPTOR MODULATORS; CELLS, CULTURED; DIETARY FATS; ENDOCANNABINOIDS; FATTY LIVER; GENE EXPRESSION REGULATION; HEPATOCYTES; INFLAMMATION MEDIATORS; INSULIN RESISTANCE; LIPID METABOLISM; LIVER; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PANNICULITIS; RECEPTOR, CANNABINOID, CB1; RNA, MESSENGER; SIGNAL TRANSDUCTION; SUBCUTANEOUS FAT;

EID: 80054692396     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-011-2274-6     Document Type: Article

References (45)

1. J Heeren U Beisiegel T Grewal 2006 Apolipoprotein E recycling. Implications for dyslipidemia and atherosclerosis Arterioscler Thromb Vasc Biol 26 442 448 16373604 10.1161/01.ATV.0000201282.64751.47 1:CAS:528: DC%2BD28XisFWnt74%3D
2. GM Dallinga-Thie R Franssen HL Mooij, et al. 2010 The metabolism of triacylglycerol-rich lipoproteins revisited: new players, new insight Atherosclerosis 211 1 8 20117784 10.1016/j.atherosclerosis.2009.12.027 1:CAS:528:DC%2BC3cXos1yit78%3D
3. KS Meir E Leitersdorf 2004 Atherosclerosis in the apolipoprotein-E- deficient mouse. A decade of progress Arterioscler Thromb Vasc Biol 24 1006 1014 15087308 10.1161/01.ATV.0000128849.12617.f4 1:CAS:528:DC%2BD2cXkt1Ogsbk%3D (Pubitemid 38737824)
4. RW Mahley KH Weisgraber Y Huang 2009 Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimers disease to AIDS J Lipid Res 50 Suppl S183 S188 19106071 10.1194/jlr.R800069-JLR200
5. K Wouters PJ van Gorp V Bieghs, et al. 2008 Dietary cholesterol, rather than liver steatosis, leads to hepatic inflammation in hyperlipidemic mouse models of nonalcoholic steatohepatitis Hepatology 48 474 486 18666236 10.1002/hep.22363
6. J Joven A Rull N Ferré, et al. 2007 The results in rodent models of atherosclerosis are not interchangeable: the influence of diet and strain Atherosclerosis 195 e85 e92 17651742 10.1016/j.atherosclerosis.2007.06.012 1:CAS:528:DC%2BD2sXhtlahtbjI (Pubitemid 350087985)
7. R Zechner R Moser TC Newman SK Fried JL Breslow 1991 Apolipoprotein E gene expression in mouse 3T3-L1 adipocytes and human adipose tissue and its regulation by differentiation and lipid content J Biol Chem 266 10583 10588 1709937 1:CAS:528:DyaK3MXkt1Kkurw%3D (Pubitemid 21906841)
8. ZH Huang CA Reardon T Mazzone 2006 Endogenous ApoE expression modulates adipocyte triacylglycerol content and turnover Diabetes 55 3394 3402 17130485 10.2337/db06-0354 1:CAS:528:DC%2BD28XhtlSmsb7K (Pubitemid 44923598)
9. J Gao H Katagiri Y Ishigaki, et al. 2007 Involvement of apolipoprotein E in excess fat accumulation and insulin resistance Diabetes 56 24 33 17192461 10.2337/db06-0144 1:CAS:528:DC%2BD2sXhtVWlsbk%3D
10. A Bartelt FT Beil T Schinke, et al. 2010 Apolipoprotein E-dependent inverse regulation of vertebral bone and adipose tissue mass in C57Bl/6 mice: modulation by diet-induced obesity Bone 47 736 745 20633710 10.1016/j.bone.2010. 07.002 1:CAS:528:DC%2BC3cXhtFClsb3O
11. K Maeda H Cao K Kono, et al. 2005 Adipocyte/macrophage fatty acid binding proteins control integrated metabolic responses in obesity and diabetes Cell Metab 1 107 119 16054052 10.1016/j.cmet.2004.12.008 1:CAS:528: DC%2BD2MXit12rtb0%3D (Pubitemid 43960591)
12. H Cao K Gerhold JR Mayers MM Wiest SM Watkins GS Hotamisligil 2008 Identification of a lipokine, a lipid hormone linking adipose tissue to systemic metabolism Cell 134 933 944 18805087 10.1016/j.cell.2008.07.048 1:CAS:528:DC%2BD1cXht1Sns73K
13. A Mallat S Lotersztajn 2008 Cannabinoid receptors as novel therapeutic targets for the management of non-alcoholic steatohepatitis Diabetes Metab 34 680 684 19195630 10.1016/S1262-3636(08)74604-4 1:CAS:528:DC%2BD1MXitVyqtrw%3D
14. P Caraceni M Domenicali F Giannone M Bernardi 2009 The role of the endocannabinoid system in liver diseases Best Pract Res Clin Endocrinol Metab 23 65 77 19285261 10.1016/j.beem.2008.10.009 1:CAS:528:DC%2BD1MXjt1agsbk%3D
15. V Di Marzo JP Després 2009 CB1 antagonists for obesity-what lessons have we learned from rimonabant? Nat Rev Endocrinol 5 633 638 19844251 10.1038/nrendo.2009.197
16. KM Starowicz L Cristino I Matias, et al. 2008 Endocannabinoid dysregulation in the pancreas and adipose tissue of mice fed with a high-fat diet Obesity 16 553 565 18239598 10.1038/oby.2007.106 1:CAS:528: DC%2BD1cXivVOqtLk%3D (Pubitemid 351328005)
17. D Osei-Hyiaman M DePetrillo P Pacher, et al. 2005 Endocannabinoid activation at hepatic CB1 receptors stimulates fatty acid synthesis and contributes to diet-induced obesity J Clin Invest 115 1298 1305 15864349 1:CAS:528:DC%2BD2MXktFSktLw%3D (Pubitemid 40629049)
18. JP Després R Ross G Boka N Alméras I Lemieux 2009 ADAGIO-Lipids Investigators. Effect of rimonabant on the high-triacylglycerol/ low-HDL-cholesterol dyslipidemia, intraabdominal adiposity, and liver fat: the ADAGIO-Lipids trial Arterioscler Thromb Vasc Biol 29 416 423 19112166 10.1161/ATVBAHA.108.176362
19. MA Ruby DK Nomura CS Hudak, et al. 2008 Overactive endocannabinoid signaling impairs apolipoprotein E-mediated clearance of triacylglycerol-rich lipoproteins Proc Natl Acad Sci U S A 105 14561 14566 18794527 10.1073/pnas.0807232105 1:CAS:528:DC%2BD1cXht1Sgt77L
20. C Touriño F Oveisi J Lockney D Piomelli R Maldonado 2010 FAAH deficiency promotes energy storage and enhances the motivation for food Int J Obes (Lond) 34 557 568 10.1038/ijo.2009.262
21. D Osei-Hyiaman J Liu L Zhou, 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 3160 3169 18677409 10.1172/JCI34827 1:CAS:528:DC%2BD1cXhtV2isbvP
22. J Tam VK Vemuri J Liu, et al. 2010 Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity J Clin Invest 120 2953 2966 20664173 10.1172/JCI42551 1:CAS:528:DC%2BC3cXhtVaiurzM
23. Mancini G, Quarta C, 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. 20th Annual Symposium of the International Cannabinoid Research Society, July 23-27, Lund, Sweden
24. MJ Meredith 1988 Rat hepatocytes prepared without collagenase: prolonged retention of differentiated characteristics in culture Cell Biol Toxicol 4 405 425 2852531 10.1007/BF00117769 1:CAS:528:DyaK3cXhtlGms7s%3D (Pubitemid 19115551)
25. A Bartelt OT Bruns R Reimer, et al. 2011 Brown adipose tissue activity controls triacylglycerol clearance Nat Med 17 200 205 21258337 10.1038/nm.2297 1:CAS:528:DC%2BC3MXps1aisw%3D%3D
26. P Grimaldi P Orlando S Di Siena, et al. 2009 The endocannabinoid system and pivotal role of the CB2 receptor in mouse spermatogenesis Proc Natl Acad Sci U S A 106 11131 11136 19541620 10.1073/pnas.0812789106 1:CAS:528: DC%2BD1MXptVWgsrg%3D
27. J Folch I Ascoli M Lees JA Meath N LeBaron 1951 Preparation of lipid extracts from brain tissue J Biol Chem 191 833 841 14861228 1:STN:280: DyaG3M%2FptVOkug%3D%3D
28. L Scheja K Toedter R Mohr, et al. 2008 Liver TAG transiently decreases while PL n-3 and n-6 fatty acids are persistently elevated in insulin resistant mice Lipids 43 1039 1051 18763007 10.1007/s11745-008-3220-3 1:CAS:528: DC%2BD1cXhtlSgsb3K
29. JG Hamilton K Comai 1988 Separation of neutral lipid, free fatty acid and phospholipid classes by normal phase HPLC Lipids 23 1150 1153 3226230 10.1007/BF02535282 1:CAS:528:DyaL1MXhtlWmtLw%3D (Pubitemid 19019478)
30. G Lepage CC Roy 1986 Direct transesterification of all classes of lipids in a one-step reaction J Lipid Res 27 114 120 3958609 1:CAS:528: DyaL28XhtVGgsLg%3D (Pubitemid 16045295)
31. G Marsicano CT Wotjak SC Azad, et al. 2002 The endogenous cannabinoid system controls extinction of aversive memories Nature 418 530 534 12152079 10.1038/nature00839 1:CAS:528:DC%2BD38Xls12nur4%3D (Pubitemid 34851398)
32. ED Rosen BM Spiegelman 2006 Adipocytes as regulators of energy balance and glucose homeostasis Nature 444 847 853 17167472 10.1038/nature05483 1:CAS:528:DC%2BD28XhtlShtrzI (Pubitemid 46024991)
33. V Di Marzo 2008 The endocannabinoid system in obesity and type 2 diabetes Diabetologia 51 1356 1367 18563385 10.1007/s00125-008-1048-2 1:CAS:528:DC%2BD1cXovF2htLk%3D
34. I Matias MP Gonthier P Orlando, et al. 2006 Regulation, function, and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia J Clin Endocrinol Metab 91 3171 3180 16684820 10.1210/jc.2005-2679 1:CAS:528:DC%2BD28XosFGht7s%3D (Pubitemid 44271774)
35. JP Després I Lemieux 2006 Abdominal obesity and metabolic syndrome Nature 444 881 887 17167477 10.1038/nature05488 (Pubitemid 46024995)
36. AA Izzo F Piscitelli R Capasso, et al. 2009 Peripheral endocannabinoid dysregulation in obesity: relation to intestinal motility and energy processing induced by food deprivation and re-feeding Br J Pharmacol 158 451 461 19371345 10.1111/j.1476-5381.2009.00183.x 1:CAS:528:DC%2BD1MXhsVClsb3O
37. WI Jeong D Osei-Hyiaman O Park, et al. 2008 Paracrine activation of hepatic CB1 receptors by stellate cell-derived endocannabinoids mediates alcoholic fatty liver Cell Metab 7 227 235 18316028 10.1016/j.cmet.2007.12.007 1:CAS:528:DC%2BD1cXjt1Cgsrw%3D (Pubitemid 351285525)
38. BE Alger J Kim 2011 Supply and demand for endocannabinoids Trends Neurosci 34 304 315 21507493 10.1016/j.tins.2011.03.003 1:CAS:528: DC%2BC3MXmvFWmsLs%3D
39. TM DEon KA Pierce JJ Roix A Tyler H Chen SR Teixeira 2008 The role of adipocyte insulin resistance in the pathogenesis of obesity-related elevations in endocannabinoids Diabetes 57 1262 1268 18276766 10.2337/db07-1186
40. R Sarzani M Bordicchia P Marcucci, et al. 2009 Altered pattern of cannabinoid type 1 receptor expression in adipose tissue of dysmetabolic and overweight patients Metabolism 58 361 367 19217452 10.1016/j.metabol.2008.10.009 1:CAS:528:DC%2BD1MXitVClsLs%3D
41. MF Bennetzen TS Nielsen SK Paulsen, et al. 2010 Reduced cannabinoid receptor 1 protein in subcutaneous adipose tissue of obese Eur J Clin Invest 40 121 126 20039929 10.1111/j.1365-2362.2009.02231.x 1:CAS:528:DC%2BC3cXitlKqtb4%3D
42. M Blüher S Engeli N Klöting, et al. 2006 Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity Diabetes 55 3053 3060 17065342 10.2337/db06-0812 (Pubitemid 44923642)
43. V Di Marzo M Côté I Matias, et al. 2009 Changes in plasma endocannabinoid levels in viscerally obese men following a 1 year lifestyle modification programme and waist circumference reduction: associations with changes in metabolic risk factors Diabetologia 52 213 217 18972095 10.1007/s00125-008-1178-6 1:CAS:528:DC%2BD1MXjvFGisw%3D%3D
44. Y Akazawa S Cazanave JL Mott, et al. 2010 Palmitoleate attenuates palmitate-induced Bim and PUMA up-regulation and hepatocyte lipoapoptosis J Hepatol 52 586 593 20206402 10.1016/j.jhep.2010.01.003 1:CAS:528: DC%2BC3cXjvFKmsbk%3D
45. I Matias G Carta E Murru S Petrosino S Banni V Di Marzo 2008 Effect of polyunsaturated fatty acids on endocannabinoid and N-acyl-ethanolamine levels in mouse adipocytes Biochim Biophys Acta 1781 52 60 18054340 1:CAS:528: DC%2BD1cXhslemsr8%3D