The major plant-derived cannabinoid 9-tetrahydrocannabinol promotes hypertrophy and macrophage infiltration in adipose tissue

Hormone and Metabolic Research

Volumn 44, Issue 2, 2012, Pages 105-113

  Wong, A ^a   Gunasekaran, N ^a   Hancock, D P ^a   Denyer, G S ^a   Meng, L ^a   Radford, J L ^a   McGregor, I S ^a   Arnold, J C ^a  

^a UNIVERSITY OF SYDNEY   (Australia)

Author keywords

cannabis; fat; inflammation; obesity; TNF

Indexed keywords

CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; PHOSPHOENOLPYRUVATE CARBOXYKINASE (GTP); TETRAHYDROCANNABINOL; TUMOR NECROSIS FACTOR ALPHA;

ADIPOCYTE; ADIPOSE TISSUE; ANIMAL EXPERIMENT; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BODY WEIGHT; CELL INFILTRATION; CELL SIZE; CONTROLLED STUDY; DRUG EFFECT; DRUG EXPOSURE; DRUG MEGADOSE; FOOD INTAKE; GENE EXPRESSION; HYPERTROPHY; INFLAMMATION; MACROPHAGE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; REPEATED DRUG DOSE; WISTAR RAT;

ADIPOCYTES; ADIPOSE TISSUE; ANIMALS; HYPERTROPHY; IMMUNOHISTOCHEMISTRY; OBESITY; PHOSPHOENOLPYRUVATE CARBOXYKINASE (ATP); RATS; RATS, WISTAR; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA; TETRAHYDROCANNABINOL; TUMOR NECROSIS FACTOR-ALPHA;

CANNABIS; RATTUS;

EID: 84857054963     PISSN: 00185043     EISSN: 14394286     Source Type: Journal    
DOI: 10.1055/s-0031-1297940     Document Type: Article

References (82)

1. Di Marzo V, Matias I. Endocannabinoid control of food intake and energy balance. Nat Neurosci: 2005; 8 585 589 (Pubitemid 40594198)
2. Matias I, Di Marzo V. Endocannabinoids and the control of energy balance. Trends Endocrinol Metab: 2007; 18 27 37 (Pubitemid 44960014)
3. Matias I, Gonthier M P, Orlando P, Martiadis V, De Petrocellis L, Cervino C, Petrosino S, Hoareau L, Festy F, Pasquali R, Roche R, Maj M, Pagotto U, Monteleone P, Di Marzo V. Regulation, function, and dysregulation of endocannabinoids in models of adipose and beta-pancreatic cells and in obesity and hyperglycemia. J Clin Endocrinol Metab: 2006; 91 3171 3180 (Pubitemid 44271774)
4. Osei-Hyiaman D, Liu J, Zhou L, Godlewski G, Harvey-White J, Jeong W I, Batkai S, Marsicano G, Lutz B, Buettner C, Kunos G. Hepatic CB1 receptor is required for development of diet-induced steatosis, dyslipidemia, and insulin and leptin resistance in mice. J Clin Invest: 2008; 118 3160 3169
5. Johansson E, Noren K, Sjovall J, Halldin M M. Determination of delta 1-tetrahydrocannabinol in human fat biopsies from marihuana users by gas chromatography-mass spectrometry. Biomed Chromatogr: 1989; 3 35 38 (Pubitemid 19036470)
6. Kreuz D S, Axelrod J. Delta-9-tetrahydrocannabinol: localization in body fat. Science: 1973; 179 391 393
7. Rawitch A B, Rohrer R, Vardaris R M. delta-9-Tetrahydrocannabinol uptake by adipose tissue: preferential accumulation in gonadal fat organs. Gen Pharmacol: 1979; 10 525 529 (Pubitemid 10165345)
8. Gunasekaran N, Long L E, Dawson B L, Hansen G H, Richardson D P, Li K M, Arnold J C, McGregor I S. Reintoxication: the release of fat-stored delta(9)-tetrahydrocannabinol (THC) into blood is enhanced by food deprivation or ACTH exposure. Br J Pharmacol: 2009; 158 1330 1337
9. Cota D, Marsicano G, Tschop M, Grubler Y, Flachskamm C, Schubert M, Auer D, Yassouridis A, Thone-Reineke C, Ortmann S, Tomassoni F, Cervino C, Nisoli E, Linthorst A C, Pasquali R, Lutz B, Stalla G K, Pagotto U. The endogenous cannabinoid system affects energy balance via central orexigenic drive and peripheral lipogenesis. J Clin Invest: 2003; 112 423 431 (Pubitemid 38063771)
10. Deveaux V, Cadoudal T, Ichigotani Y, Teixeira-Clerc F, Louvet A, Manin S, Nhieu J T, Belot M P, Zimmer A, Even P, Cani P D, Knauf C, Burcelin R, Bertola A, Le Marchand-Brustel Y, Gual P, Mallat A, Lotersztajn S. Cannabinoid CB2 receptor potentiates obesity-associated inflammation, insulin resistance and hepatic steatosis. PLoS One: 2009; 4 e5844
11. Pertwee R G. The diverse CB1 and CB2 receptor pharmacology of three plant cannabinoids: delta9-tetrahydrocannabinol, cannabidiol and delta9- tetrahydrocannabivarin. British journal of pharmacology: 2008; 153 199 215
12. Bellocchio L, Cervino C, Vicennati V, Pasquali R, Pagotto U. Cannabinoid type 1 receptor: another arrow in the adipocytes bow. J Neuroendocrinol: 2008; 20 01 130 138 (Pubitemid 351559286)
13. Franckhauser S, Munoz S, Pujol A, Casellas A, Riu E, Otaegui P, Su B, Bosch F. Increased fatty acid re-esterification by PEPCK overexpression in adipose tissue leads to obesity without insulin resistance. Diabetes: 2002; 51 624 630 (Pubitemid 34760168)
14. Nye C K, Hanson R W, Kalhan S C. Glyceroneogenesis is the dominant pathway for triglyceride glycerol synthesis in vivo in the rat. J Biol Chem: 2008; 283 27565 27574
15. Bahceci M, Gokalp D, Bahceci S, Tuzcu A, Atmaca S, Arikan S. The correlation between adiposity and adiponectin, tumor necrosis factor alpha, interleukin-6 and high sensitivity C-reactive protein levels. Is adipocyte size associated with inflammation in adults? J Endocrinol Invest: 2007; 30 210 214 (Pubitemid 46929320)
16. Galvez B G, San Martin N, Rodriguez C. TNF-alpha is required for the attraction of mesenchymal precursors to white adipose tissue in Ob/ob mice. PLoS One: 2009; 4 e4444
17. Ryden M, Arner P. Tumour necrosis factor-alpha in human adipose tissue - from signalling mechanisms to clinical implications. J Intern Med: 2007; 262 431 438 (Pubitemid 47404374)
18. Cinti S, Mitchell G, Barbatelli G, Murano I, Ceresi E, Faloia E, Wang S, Fortier M, Greenberg A S, Obin M S. Adipocyte death defines macrophage localization and function in adipose tissue of obese mice and humans. J Lipid Res: 2005; 46 2347 2355 (Pubitemid 41532523)
19. Bluher M. The inflammatory process of adipose tissue. Pediatr Endocrinol Rev: 2008; 6 24 31
20. Daniels J S. The pathogenesis of obesity. Psychiatr Clin North Am: 1984; 7 335 347 (Pubitemid 14026616)
21. Insull W Jr. The pathology of atherosclerosis: plaque development and plaque responses to medical treatment. Am J Med: 2009; 122 S3 S14
22. Bays H E, Gonzalez-Campoy J M, Bray G A, Kitabchi A E, Bergman D A, Schorr A B, Rodbard H W, Henry R R. Pathogenic potential of adipose tissue and metabolic consequences of adipocyte hypertrophy and increased visceral adiposity. Expert Rev Cardiovasc Ther: 2008; 6 343 368
23. Shoelson S E, Herrero L, Naaz A. Obesity, inflammation, and insulin resistance. Gastroenterology: 2007; 132 2169 2180 (Pubitemid 46693756)
24. Subramanian V, Ferrante A W Jr. Obesity, inflammation, and macrophages. Nestle Nutr Workshop Ser Pediatr Program: 2009; 63 151 159; discussion 159-162, 168-259
25. Sugamura K, Sugiyama S, Nozaki T, Matsuzawa Y, Izumiya Y, Miyata K, Nakayama M, Kaikita K, Obata T, Takeya M, Ogawa H. Activated endocannabinoid system in coronary artery disease and antiinflammatory effects of cannabinoid 1 receptor blockade on macrophages. Circulation: 2009; 119 28 36
26. El-Remessy A B, Rajesh M, Mukhopadhyay P, Horvath B, Patel V, Al-Gayyar M M, Pillai B A, Pacher P. Cannabinoid 1 receptor activation contributes to vascular inflammation and cell death in a mouse model of diabetic retinopathy and a human retinal cell line. Diabetologia: 2011; 54 1567 1578
27. Dol-Gleizes F, Paumelle R, Visentin V, Mares A M, Desitter P, Hennuyer N, Gilde A, Staels B, Schaeffer P, Bono F. Rimonabant, a selective cannabinoid CB1 receptor antagonist, inhibits atherosclerosis in LDL receptor-deficient mice. Arterioscler Thromb Vasc Biol: 2009; 29 12 18
28. Han K H, Lim S, Ryu J, Lee C W, Kim Y, Kang J H, Kang S S, Ahn Y K, Park C S, Kim J J. CB1 and CB2 cannabinoid receptors differentially regulate the production of reactive oxygen species by macrophages. Cardiovasc Res: 2009; 84 378 386
29. Gonzalez-Muniesa P, Bing C, Trayhurn P. Upregulation of the expression of inflammatory and angiogenic markers in human adipocytes by a synthetic cannabinoid, JTE-907. Horm Metab Res: 2010; 42 710 717
30. Mukhopadhyay P, Rajesh M, Pan H, Patel V, Mukhopadhyay B, Batkai S, Gao B, Hasko G, Pacher P. Cannabinoid-2 receptor limits inflammation, oxidative/nitrosative stress, and cell death in nephropathy. Free Radic Biol Med: 2010; 48 457 467
31. Hao M X, Jiang L S, Fang N Y, Pu J, Hu L H, Shen L H, Song W, He B. The cannabinoid WIN55,212-2 protects against oxidized LDL-induced inflammatory response in murine macrophages. J Lipid Res: 2010; 51 2181 2190
32. Sokolic L, Long L E, Hunt G E, Arnold J C, McGregor I S. Disruptive effects of the prototypical cannabinoid Delta-tetrahydrocannabinol and the fatty acid amide inhibitor URB-597 on go/no-go auditory discrimination performance and olfactory reversal learning in rats. Behav Pharmacol: 2011; 22 191 202
33. Klein C, Karanges E, Spiro A, Wong A, Spencer J, Huynh T, Gunasekaran N, Karl T, Long L E, Huang X F, Liu K, Arnold J C, McGregor I S. Cannabidiol potentiates Delta(9)-tetrahydrocannabinol (THC) behavioural effects and alters THC pharmacokinetics during acute and chronic treatment in adolescent rats. Psychopharmacology (Berl): 2011; 218 443 457
34. Smit E, Crespo C J. Dietary intake and nutritional status of US adult marijuana users: results from the Third National Health and Nutrition Examination Survey. Public Health Nutr: 2001; 4 781 786 (Pubitemid 32566531)
35. Giuliani D, Ottani A, Ferrari F. Effects of the cannabinoid receptor agonist, HU 210, on ingestive behaviour and body weight of rats. Eur J Pharmacol: 2000; 391 275 279 (Pubitemid 30154095)
36. Damoiseaux J G, Dopp E A, Calame W, Chao D, MacPherson G G, Dijkstra C D. Rat macrophage lysosomal membrane antigen recognized by monoclonal antibody ED1. Immunology: 1994; 83 140 147 (Pubitemid 24285411)
37. Rodbell M. Metabolism of Isolated Fat Cells. I. Effects of Hormones on Glucose Metabolism and Lipolysis. J Biol Chem: 1964; 239 375 380
38. Koch J E. Delta(9)-THC stimulates food intake in Lewis rats: effects on chow, high-fat and sweet high-fat diets. Pharmacol Biochem Behav: 2001; 68 539 543
39. Williams C M, Kirkham T C. Reversal of delta 9-THC hyperphagia by SR141716 and naloxone but not dexfenfluramine. Pharmacol Biochem Behav: 2002; 71 333 340
40. Jarbe T U, DiPatrizio N V. Delta9-THC induced hyperphagia and tolerance assessment: interactions between the CB1 receptor agonist delta9-THC and the CB1 receptor antagonist SR-141716 (rimonabant) in rats. Behav Pharmacol: 2005; 16 373 380 (Pubitemid 41404808)
41. Verty A N, McGregor I S, Mallet P E. The dopamine receptor antagonist SCH 23390 attenuates feeding induced by Delta9-tetrahydrocannabinol. Brain Res: 2004; 1020 188 195 (Pubitemid 39092986)
42. Verty A N, McGregor I S, Mallet P E. Paraventricular hypothalamic CB(1) cannabinoid receptors are involved in the feeding stimulatory effects of Delta(9)-tetrahydrocannabinol. Neuropharmacology: 2005; 49 1101 1109 (Pubitemid 41608634)
43. Sofia R D, Knobloch L C. Comparative effects of various naturally occurring cannabinoids on food, sucrose and water consumption by rats. Pharmacol Biochem Behav: 1976; 4 591 599
44. McGregor I S, Issakidis C N, Prior G. Aversive effects of the synthetic cannabinoid CP 55,940 in rats. Pharmacol Biochem Behav: 1996; 53 657 664 (Pubitemid 26088545)
45. Miczek K A, Dixit B N. Behavioral and biochemical effects of chronic delta 9-tetrahydrocannabinol in rats. Psychopharmacology (Berl): 1980; 67 195 202 (Pubitemid 10132546)
46. Oviedo A, Glowa J, Herkenham M. Chronic cannabinoid administration alters cannabinoid receptor binding in rat brain: a quantitative autoradiographic study. Brain Res: 1993; 616 293 302 (Pubitemid 23200058)
47. Boucher A A, Hunt G E, Micheau J, Huang X, McGregor I S, Karl T, Arnold J C. The schizophrenia susceptibility gene neuregulin 1 modulates tolerance to the effects of cannabinoids. Int J Neuropsychopharmacol: 2011; 14 631 643
48. Boucher A A, Vivier L, Metna-Laurent M, Brayda-Bruno L, Mons N, Arnold J C, Micheau J. Chronic treatment with Delta(9)-tetrahydrocannabinol impairs spatial memory and reduces zif268 expression in the mouse forebrain. Behav Pharmacol: 2009; 20 45 55
49. McGarry J D, Dobbins R L. Fatty acids, lipotoxicity and insulin secretion. Diabetologia: 1999; 42 128 138 (Pubitemid 29064233)
50. Le Strat Y, Le Foll B. Obesity and Cannabis Use: Results From 2 Representative National Surveys. Am J Epidemiol: 2011; 174 929 933
51. Teixeira D, Pestana D, Faria A, Calhau C, Azevedo I, Monteiro R. Modulation of Adipocyte Biology by Delta(9)-Tetrahydrocannabinol. Obesity (Silver Spring): 2010; 18 2077 2085
52. Jbilo O, Ravinet-Trillou C, Arnone M, Buisson I, Bribes E, Peleraux A, Penarier G, Soubrie P, Le Fur G, Galiegue S, Casellas P. The CB1 receptor antagonist rimonabant reverses the diet-induced obesity phenotype through the regulation of lipolysis and energy balance. FASEB J: 2005; 19 1567 1569 (Pubitemid 41279033)
53. Ballard F J, Hanson R W, Leveille G A. Phosphoenolpyruvate carboxykinase and the synthesis of glyceride-glycerol from pyruvate in adipose tissue. J Biol Chem: 1967; 242 2746 2750
54. Robinson J, Newsholme E A. Glycerol kinase activities in rat heart and adipose tissue. Biochem J: 1967; 104 2C 4C
55. Olswang Y, Cohen H, Papo O, Cassuto H, Croniger C M, Hakimi P, Tilghman S M, Hanson R W, Reshef L. A mutation in the peroxisome proliferator-activated receptor gamma-binding site in the gene for the cytosolic form of phosphoenolpyruvate carboxykinase reduces adipose tissue size and fat content in mice. Proc Natl Acad Sci USA: 2002; 99 625 630 (Pubitemid 34106562)
56. Yang Q, Liu H Y, Zhang Y W, Wu W J, Tang W X. Anandamide induces cell death through lipid rafts in hepatic stellate cells. J Gastroenterol Hepatol: 2010; 25 991 1001
57. Monteiro R, de Castro P M, Calhau C, Azevedo I. Adipocyte size and liability to cell death. Obes Surg: 2006; 16 804 806 (Pubitemid 43874842)
58. Jo J, Guo J, Liu T, Mullen S, Hall K D, Cushman S W, Periwal V. Hypertrophy-driven adipocyte death overwhelms recruitment under prolonged weight gain. Biophys J: 2010; 99 3535 3544
59. Strissel K J, Stancheva Z, Miyoshi H, Perfield J W 2nd, DeFuria J, Jick Z, Greenberg A S, Obin M S. Adipocyte death, adipose tissue remodeling, and obesity complications. Diabetes: 2007; 56 2910 2918 (Pubitemid 350223625)
60. Weisberg S P, McCann D, Desai M, Rosenbaum M, Leibel R L, Ferrante A W Jr. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest: 2003; 112 1796 1808 (Pubitemid 38063703)
61. Surmi B K, Hasty A H. Macrophage infiltration into adipose tissue: initiation, propagation and remodeling. Future Lipidol: 2008; 3 545 556
62. Bouloumie A, Curat C A, Sengenes C, Lolmede K, Miranville A, Busse R. Role of macrophage tissue infiltration in metabolic diseases. Curr Opin Clin Nutr Metab Care: 2005; 8 347 354 (Pubitemid 40863045)
63. Heilbronn L K, Campbell L V. Adipose tissue macrophages, low grade inflammation and insulin resistance in human obesity. Curr Pharm Des: 2008; 14 1225 1230 (Pubitemid 351997835)
64. Xu H, Barnes G T, Yang Q, Tan G, Yang D, Chou C J, Sole J, Nichols A, Ross J S, Tartaglia L A, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest: 2003; 112 1821 1830 (Pubitemid 38063705)
65. Pausova Z. From big fat cells to high blood pressure: a pathway to obesity-associated hypertension. Curr Opin Nephrol Hypertens: 2006; 15 173 178
66. Bell-Anderson K S, Aouad L, Williams H, Sanz F R, Phuyal J, Larter C Z, Farrell G C, Caterson I D. Coordinated improvement in glucose tolerance, liver steatosis and obesity-associated inflammation by cannabinoid 1 receptor antagonism in fat Aussie mice. Int J Obes (Lond): 2011; Mar 8 [Epub ahead of print]
67. Mukhopadhyay P, Pan H, Rajesh M, Batkai S, Patel V, Harvey-White J, Mukhopadhyay B, Hasko G, Gao B, Mackie K, Pacher P. CB1 cannabinoid receptors promote oxidative/nitrosative stress, inflammation and cell death in a murine nephropathy model. Br J Pharmacol: 2010; 160 657 668
68. Gary-Bobo M, Elachouri G, Gallas J F, Janiak P, Marini P, Ravinet-Trillou C, Chabbert M, Cruccioli N, Pfersdorff C, Roque C, Arnone M, Croci T, Soubrie P, Oury-Donat F, Maffrand J P, Scatton B, Lacheretz F, Le Fur G, Herbert J M, Bensaid M. Rimonabant reduces obesity-associated hepatic steatosis and features of metabolic syndrome in obese Zucker fa/fa rats. Hepatology: 2007; 46 122 129 (Pubitemid 47171928)
69. Croci T, Landi M, Galzin A M, Marini P. Role of cannabinoid CB1 receptors and tumor necrosis factor-alpha in the gut and systemic anti-inflammatory activity of SR 141716 (rimonabant) in rodents. Br J Pharmacol: 2003; 140 115 122 (Pubitemid 37175837)
70. Kempf K, Hector J, Strate T, Schwarzloh B, Rose B, Herder C, Martin S, Algenstaedt P. Immune-mediated activation of the endocannabinoid system in visceral adipose tissue in obesity. Horm Metab Res: 2007; 39 596 600 (Pubitemid 47345235)
71. Guindon J, Hohmann A G. Cannabinoid CB2 receptors: a therapeutic target for the treatment of inflammatory and neuropathic pain. Br J Pharmacol: 2008; 153 319 334
72. Gutierrez T, Farthing J N, Zvonok A M, Makriyannis A, Hohmann A G. Activation of peripheral cannabinoid CB1 and CB2 receptors suppresses the maintenance of inflammatory nociception: a comparative analysis. Br J Pharmacol: 2007; 150 153 163 (Pubitemid 46160605)
73. Elmes S J, Jhaveri M D, Smart D, Kendall D A, Chapman V. Cannabinoid CB2 receptor activation inhibits mechanically evoked responses of wide dynamic range dorsal horn neurons in naive rats and in rat models of inflammatory and neuropathic pain. Eur J Neurosci: 2004; 20 2311 2320 (Pubitemid 39472394)
74. Quartilho A, Mata H P, Ibrahim M M, Vanderah T W, Porreca F, Makriyannis A, Malan T P Jr. Inhibition of inflammatory hyperalgesia by activation of peripheral CB2 cannabinoid receptors. Anesthesiology: 2003; 99 955 960 (Pubitemid 37186088)
75. Rajesh M, Mukhopadhyay P, Batkai S, Hasko G, Liaudet L, Huffman J W, Csiszar A, Ungvari Z, Mackie K, Chatterjee S, Pacher P. CB2-receptor stimulation attenuates TNF-alpha-induced human endothelial cell activation, transendothelial migration of monocytes, and monocyte-endothelial adhesion. Am J Physiol Heart Circ Physiol: 2007; 293 H2210 H2218 (Pubitemid 47605864)
76. Rajesh M, Mukhopadhyay P, Hasko G, Huffman J W, Mackie K, Pacher P. CB2 cannabinoid receptor agonists attenuate TNF-alpha-induced human vascular smooth muscle cell proliferation and migration. Br J Pharmacol: 2008; 153 347 357
77. OSullivan S E. Cannabinoids go nuclear: evidence for activation of peroxisome proliferator-activated receptors. Br J Pharmacol: 2007; 152 576 582
78. Tontonoz P, Hu E, Devine J, Beale E G, Spiegelman B M. PPAR gamma 2 regulates adipose expression of the phosphoenolpyruvate carboxykinase gene. Mol Cell Biol: 1995; 15 351 357 (Pubitemid 24379933)
79. Lauckner J E, Jensen J B, Chen H Y, Lu H C, Hille B, Mackie K. GPR55 is a cannabinoid receptor that increases intracellular calcium and inhibits M current. Proc Natl Acad Sci USA: 2008; 105 2699 2704 (Pubitemid 351520576)
80. Ryberg E, Larsson N, Sjogren S, Hjorth S, Hermansson N O, Leonova J, Elebring T, Nilsson K, Drmota T, Greasley P J. The orphan receptor GPR55 is a novel cannabinoid receptor. Br J Pharmacol: 2007; 152 1092 1101 (Pubitemid 350166046)
81. Ishiguro H, Onaivi E S, Horiuchi Y, Imai K, Komaki G, Ishikawa T, Suzuki M, Watanabe Y, Ando T, Higuchi S, Arinami T. Functional polymorphism in the GPR55 gene is associated with anorexia nervosa. Synapse: 2011; 65 103 108
82. Baker D, Pryce G, Davies W L, Hiley C R. In silico patent searching reveals a new cannabinoid receptor. Trends Pharmacol Sci: 2006; 27 1 4 (Pubitemid 43063115)