Role of the endocannabinoid system in diabetes and diabetic complications

British Journal of Pharmacology

Volumn 173, Issue 7, 2016, Pages 1116-1127

  Gruden, G ^a   Barutta, F ^a   Kunos, G ^b   Pacher, P ^b  

^a UNIVERSITY OF TURIN   (Italy)

^b NATIONAL INSTITUTES OF HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIINFLAMMATORY AGENT; ANTIOXIDANT; CANNABIDIOL; CANNABINOID 1 RECEPTOR; CANNABINOID 2 RECEPTOR; ENDOCANNABINOID;

AGONISTS; ANIMAL; ANTAGONISTS AND INHIBITORS; CHRONIC DISEASE; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2; HUMAN; INSULIN RESISTANCE; METABOLISM; OBESITY; PANCREAS ISLET BETA CELL;

ANIMALS; ANTI-INFLAMMATORY AGENTS; ANTIOXIDANTS; CANNABIDIOL; CHRONIC DISEASE; DIABETES COMPLICATIONS; DIABETES MELLITUS, TYPE 2; ENDOCANNABINOIDS; HUMANS; INSULIN RESISTANCE; INSULIN-SECRETING CELLS; OBESITY; RECEPTOR, CANNABINOID, CB1; RECEPTOR, CANNABINOID, CB2;

EID: 84961775064     PISSN: 00071188     EISSN: 14765381     Source Type: Journal    
DOI: 10.1111/bph.13226     Document Type: Review

References (72)

1. Agarwal N, Pacher P, Tegeder I, Amaya F, Constantin CE, Brenner GJ, et al. (2007). Cannabinoids mediate analgesia largely via peripheral type 1 cannabinoid receptors in nociceptors. Nat Neurosci 10: 870-879.
2. Agudo J, Martin M, Roca C, Molas M, Bura AS, Zimmer A, et al. (2010). Deficiency of CB2 cannabinoid receptor in mice improves insulin sensitivity but increases food intake and obesity with age. Diabetologia 53: 2629-2640.
3. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013a). The Concise Guide to PHARMACOLOGY 2013/14: G protein-coupled receptors. Br J Pharmacol 170: 1459-1581.
4. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013b). The Concise Guide to PHARMACOLOGY 2013/14: catalytic receptors. Br J Pharmacol 170: 1676-1705.
5. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013c). The Concise Guide to PHARMACOLOGY 2013/14: transporters. Br J Pharmacol 170: 1706-1796.
6. Alexander SPH, Benson HE, Faccenda E, Pawson AJ, Sharman JL, Spedding M, et al. (2013d). The Concise Guide to PHARMACOLOGY 2013/14: enzymes. Br J Pharmacol 170: 1797-1867.
7. Barutta F, Corbelli A, Mastrocola R, Gambino R, Di Marzo V, Pinach S, et al. (2010). Cannabinoid receptor 1 blockade ameliorates albuminuria in experimental diabetic nephropathy. Diabetes 59: 1046-1054.
8. Barutta F, Piscitelli F, Pinach S, Bruno G, Gambino R, Rastaldi MP, et al. (2011). Protective role of cannabinoid receptor type 2 in a mouse model of diabetic nephropathy. Diabetes 60: 2386-2396.
9. Barutta F, Grimaldi S, Franco I, Bellini S, Gambino R, Pinach S, et al. (2014). Deficiency of cannabinoid receptor of type 2 worsens renal functional and structural abnormalities in streptozotocin-induced diabetic mice. Kidney Int 86: 979-990.
10. Blüher M, Engeli S, Klöting N, Berndt J, Fasshauer M, Bátkai S, et al. (2006). Dysregulation of the peripheral and adipose tissue endocannabinoid system in human abdominal obesity. Diabetes 55: 3053-3060.
11. Boon MR, Kooijman S, van Dam AD, Pelgrom LR, Berbée JF, Visseren CA, et al. (2014). Peripheral cannabinoid 1 receptor blockade activates brown adipose tissue and diminishes dyslipidemia and obesity. FASEB J 28: 5361-5375.
12. Buraczynska M, Wacinski P, Zukowski P, Dragan M, Ksiazek A, (2014). Common polymorphism in the cannabinoid type 1 receptor gene (CNR1) is associated with microvascular complications in type 2 diabetes. J Diabetes Complications 28: 35-39.
13. Christensen R, Kristensen PK, Bartels EM, Bliddal H, Astrup A, (2007). Efficacy and safety of the weight-loss drug rimonabant: a meta-analysis of randomised trials. Lancet 370: 1706-1713.
14. Cinar R, Godlewski G, Liu J, Tam J, Jourdan T, Mukhopadhyay B, et al. (2014). Hepatic cannabinoid-1 receptors mediate diet-induced insulin resistance by increasing de novo synthesis of long-chain ceramides. Hepatology 59: 143-153.
15. Comelli F, Bettoni I, Colombo A, Fumagalli P, Giagnoni G, Costa B, (2010). Rimonabant, a cannabinoid CB1 receptor antagonist, attenuates mechanical allodynia and counteracts oxidative stress and nerve growth factor deficit in diabetic mice. Eur J Pharmacol 637: 62-69.
16. Deveaux V, Cadoudal T, Ichigotani Y, Teixeira-Clerc F, Louvet A, Manin S, et al. (2009). Cannabinoid CB2 receptor potentiates obesity-associated inflammation, insulin resistance and hepatic steatosis. PLoS ONE 4: e5844.
17. Di Marzo V, (2012). De-liver-ance' from CB(1): a way to counteract insulin resistance? Gastroenterology 142: 1063-1066.
18. El-Remessy AB, Rajesh M, Mukhopadhyay P, Horvath B, Patel V, Al-Gayyar MM, et al. (2011). 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 54: 1567-1578.
19. Forbes JM, Cooper ME, (2013). Mechanisms of diabetic complications. Physiol Rev 93: 137-188.
20. Ge Q, Maury E, Rycken L, Gérard J, Noël L, Detry R, et al. (2013). Endocannabinoids regulate adipokine production and the immune balance of omental adipose tissue in human obesity. Int J Obes (Lond) 37: 874-880.
21. Giunti S, Barutta F, Cavallo Perin P, Gruden G, (2010). Targeting the MCP-1/CCR2 system in diabetic kidney disease. Curr Vasc Pharmacol 8: 849-860.
22. Hao E, Mukhopadhyay P, Cao Z, Erdelyi K, Holocav E, (2015). Cannabidiol protects against doxorubicin-induced cardiomyopathy by modulating mitochondrial function and biogenesis. Mol Med 21: 38-45.
23. Horváth B, Mukhopadhyay P, Haskó G, Pacher P, (2012). The endocannabinoid system and plant-derived cannabinoids in diabetes and diabetic complications. Am J Pathol 180: 432-442.
24. Howlett AC, Blume LC, Dalton GD, (2010). CB(1) cannabinoid receptors and their associated proteins. Curr Med Chem 17: 1382-1393.
25. International Diabetes Federation (2014). Diabetes-Atlas [Online]. Available at: http://www.idf.org/diabetesatlas (accessed 5/4/2015).
26. Janiak P, Poirier B, Bidouard JP, Cadrouvele C, Pierre F, Gouraud L, et al. (2007). Blockade of cannabinoid CB1 receptor improves renal function, metabolic profile, and increased survival of obese Zucker rats. Kidney Int 72: 1345-1357.
27. Jenkin KA, Verty AN, McAinch AJ, Hryciw DH, (2012). Endocannabinoids and the renal proximal tubule: an emerging role in diabetic nephropathy. Int J Biochem Cell Biol 44: 2028-2031.
28. Jenkin KA, McAinch AJ, Briffa JF, Zhang Y, Kelly DJ, Pollock CA, et al. (2013). Cannabinoid receptor 2 expression in human proximal tubule cells is regulated by albumin independent of ERK1/2 signaling. Cell Physiol Biochem 32: 1309-1319.
29. Jourdan T, Godlewski G, Cinar R, Bertola A, Szanda G, Liu J, et al. (2013). Activation of the Nlrp3 inflammasome in infiltrating macrophages by endocannabinoids mediates beta cell loss in type 2 diabetes. Nat Med 19: 1132-1140.
30. Jourdan T, Szanda G, Rosenberg A, Tam J, Earley B, Godlewski G, et al. (2014). Overactive cannabinoid 1 receptor in podocytes drives type-2 diabetic nephropathy. Proc Natl Acad Sci U S A 111: E5420-E5428.
31. Kim W, Lao Q, Shin YK, Carlson OD, Lee EK, Gorospe M, et al. (2012). Cannabinoids induce pancreatic β-cell death by directly inhibiting insulin receptor activation. Sci Signal 5: ra23.
32. Kunos G, Tam J, (2011). The case for peripheral CB1 receptor blockade in the treatment of visceral obesity and its cardiometabolic complications. Br J Pharmacol 163: 1423-1431.
33. Lim JC, Lim SK, Park MJ, Kim GY, Han HJ, Park SH, (2011). Cannabinoid receptor 1 mediates high glucose-induced apoptosis via endoplasmic reticulum stress in primary cultured rat mesangial cells. Am J Physiol Renal Physiol 301: F179-F188.
34. Liu J, Zhou L, Xiong K, Godlewski G, Mukhopadhyay B, Tam J, et al. (2012). Hepatic cannabinoid receptor-1 mediates diet-induced insulin resistance via inhibition of insulin signaling and clearance in mice. Gastroenterology 142: 1218-1228.
35. Liu WJ, Jin HY, Park JH, Baek HS, Park TS, (2010). Effect of rimonabant, the cannabinoid CB1 receptor antagonist, on peripheral nerve in streptozotocin-induced diabetic rat. Eur J Pharmacol 637: 70-76.
36. Malenczyk K, Jazurek M, Keimpema E, Silvestri C, Janikiewicz J, Mackie K, et al. (2013). CB1 cannabinoid receptors couple to focal adhesion kinase to control insulin release. J Biol Chem 288: 32685-32699.
37. Montecucco F, Burger F, Mach F, Steffens S, (2008). CB2 cannabinoid receptor agonist JWH-015 modulates human monocyte migration through defined intracellular signaling pathways. Am J Physiol Heart Circ Physiol 294: H1145-H1155.
38. Mukhopadhyay P, Pan H, Rajesh M, Bátkai S, Patel V, Harvey-White J, et al. (2010a). CB1 cannabinoid receptors promote oxidative/nitrosative stress, inflammation and cell death in a murine nephropathy model. Br J Pharmacol 160: 657-668.
39. Mukhopadhyay P, Rajesh M, Pan H, Patel V, Mukhopadhyay B, Bátkai S, et al. (2010b). Cannabinoid-2 receptor limits inflammation, oxidative/nitrosative stress, and cell death in nephropathy. Free Radic Biol Med 48: 457-467.
40. Mukhopadhyay P, Rajesh M, Batkai S, Patel V, Kashiwaya Y, Liaudet L, et al. (2010c). CB1 cannabinoid receptors promote oxidative stress and cell death in murine models of doxorubicin-induced cardiomyopathy and in human cardiomyocytes. Cardiovasc Res 85: 773-784.
41. Murumalla R, Bencharif K, Gence L, Bhattacharya A, Tallet F, Gonthier MP, et al. (2011). Effect of the cannabinoid receptor-1 antagonist SR141716A on human adipocyte inflammatory profile and differentiation. J Inflamm (Lond) 8: 33.
42. Nam DH, Lee MH, Kim JE, Song HK, Kang YS, Lee JE, et al. (2012). Blockade of cannabinoid receptor 1 improves insulin resistance, lipid metabolism, and diabetic nephropathy in db/db mice. Endocrinology 153: 1387-1396.
43. 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.
44. Pacher P, Hasko G, (2008). Endocannabinoids and cannabinoid receptors in ischaemia-reperfusion injury and preconditioning. Br J Pharmacol 160: 688-700.
45. Pacher P, Kunos G, (2013). Modulating the endocannabinoid system in human health and disease-successes and failures. FEBS J 280: 1918-1943.
46. Pacher P, Mechoulam R, (2011). Is lipid signaling through cannabinoid 2 receptors part of a protective system? Prog Lipid Res 50: 193-211.
47. Pacher P, Batkai S, Kunos G, (2006). The endocannabinoid system as an emerging target of pharmacotherapy. Pharmacol Rev 58: 389-462.
48. Pawson AJ, Sharman JL, Benson HE, Faccenda E, Alexander SP, Buneman OP, et al.; NC-IUPHAR (2014). The IUPHAR/BPS Guide to PHARMACOLOGY: an expert-driven knowledgebase of drug targets and their ligands. Nucl. Acids Res. 42 (Database Issue): D1098-D1106.
49. Peltier A, Goutman SA, Callaghan BC, (2014). Painful diabetic neuropathy. BMJ 348: g1799.
50. Quercioli A, Pataky Z, Vincenti G, Makoundou V, Di Marzo V, Montecucco F, et al. (2011). Elevated endocannabinoid plasma levels are associated with coronary circulatory dysfunction in obesity. Eur Heart J 32: 1369-1378.
51. Rajesh M, Mukhopadhyay P, Hasko G, Liaudet L, Mackie K, Pacher P, (2010). Cannabinoid-1 receptor activation induces reactive oxygen species-dependent and -independent mitogen-activated protein kinase activation and cell death in human coronary artery endothelial cells. Br J Pharmacol 160: 688-700.
52. Rajesh M, Batkai S, Kechrid M, Mukhopadhyay P, Lee WS, Horvath B, et al. (2012). Cannabinoid 1 receptor promotes cardiac dysfunction, oxidative stress, inflammation, and fibrosis in diabetic cardiomyopathy. Diabetes 61: 716-727.
53. Rohrbach K, Thomas MA, Glick S, Fung EN, Wang V, Watson L, et al. (2012). Ibipinabant attenuates β-cell loss in male Zucker diabetic fatty rats independently of its effects on body weight. Diabetes Obes Metab 14: 555-564.
54. Romero-Zerbo SY, Garcia-Gutierrez MS, Suarez J, Rivera P, Ruz-Maldonado I, Vida M, et al. (2012). Overexpression of cannabinoid CB2 receptor in the brain induces hyperglycaemia and a lean phenotype in adult mice. J Neuroendocrinol 24: 1106-1119.
55. Russell JC, Kelly SE, Diane A, Wang Y, Mangat R, Novak S, et al. (2010). Rimonabant-mediated changes in intestinal lipid metabolism and improved renal vascular dysfunction in the JCR: LA-cp rat model of prediabetic metabolic syndrome. Am J Physiol Gastrointest Liver Physiol 299: G507-G516.
56. Schaich CL, Shaltout HA, Brosnihan KB, Howlett AC, Diz DI, (2014). Acute and chronic systemic CB1 cannabinoid receptor blockade improves blood pressure regulation and metabolic profile in hypertensive (mRen2)27 rats. Physiol Rep 2 (8). pii: e12108. doi: 10.14814/phy2.12108
57. Selvarajah D, Gandhi R, Emery CJ, Tesfaye S, (2010). Randomized placebo-controlled double-blind clinical trial of cannabis-based medicinal product (Sativex) in painful diabetic neuropathy: depression is a major confounding factor. Diabetes Care 33: 128-130.
58. Silvestri C, Di Marzo V, (2013). The endocannabinoid system in energy homeostasis and the etiopathology of metabolic disorders. Cell Metab 17: 475-490.
59. Silvestri C, Ligresti A, Di Marzo V, (2011). Peripheral effects of the endocannabinoid system in energy homeostasis: adipose tissue, liver and skeletal muscle. Rev Endocr Metab Disord 12: 153-162.
60. Slavic S, Lauer D, Sommerfeld M, Kemnitz UR, Grzesiak A, Trappiel M, et al. (2013). Cannabinoid receptor 1 inhibition improves cardiac function and remodelling after myocardial infarction and in experimental metabolic syndrome. J Mol Med 91: 811-823.
61. Stanley C, O'Sullivan SE, (2014). Vascular targets for cannabinoids: animal and human studies. Br J Pharmacol 171: 1361-1378.
62. Steffens S, Pacher P, (2012). Targeting cannabinoid receptor CB(2) in cardiovascular disorders: promises and controversies. Br J Pharmacol 167: 313-323.
63. Steffens S, Pacher P, (2015). The activated endocannabinoid system in atherosclerosis: driving force or protective mechanism? Curr Drug Targets 16: 334-341.
64. Tam J, Vemuri VK, Liu J, Bátkai S, Mukhopadhyay B, Godlewski G, et al. (2010). Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J Clin Invest 120: 2953-2966.
65. Tam J, Cinar R, Liu J, Godlewski G, Wesley D, Jourdan T, et al. (2012). Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab 16: 167-179.
66. Tarabra E, Giunti S, Barutta F, Salvidio G, Burt D, Deferrari G, et al. (2009). Effect of the monocyte chemoattractant protein-1/CC chemokine receptor 2 system on nephrin expression in streptozotocin-treated mice and human cultured podocytes. Diabetes 58: 2109-2118.
67. Tedesco L, Valerio A, Dossena M, Cardile A, Ragni M, Pagano C, et al. (2010). Cannabinoid receptor stimulation impairs mitochondrial biogenesis in mouse white adipose tissue, muscle, and liver: the role of eNOS, p38 MAPK, and AMPK pathways. Diabetes 59: 2826-2836.
68. Tiyerili V, Zimmer S, Jung S, Wassmann K, Naehle CP, Lutjohann D, et al. (2010). CB1 receptor inhibition leads to decreased vascular AT1 receptor expression, inhibition of oxidative stress and improved endothelial function. Basic Res Cardiol 105: 465-477.
69. Varga ZV, Giricz Z, Liaudet L, Hasko G, Ferdinandy P, Pacher P, (2015). Interplay of oxidative, nitrosative/nitrative stress, inflammation, cell death and autophagy in diabetic cardiomyopathy. Biochim Biophys Acta 1852: 232-242.
70. Vera G, López-Miranda V, Herradón E, Martín MI, Abalo R, (2012). Characterization of cannabinoid-induced relief of neuropathic pain in rat models of type 1 and type 2 diabetes. Pharmacol Biochem Behav 102: 335-343.
71. Vincenzi F, Targa M, Corciulo C, Tabrizi MA, Merighi S, Gessi S, et al. (2013). Antinociceptive effects of the selective CB2 agonist MT178 in inflammatory and chronic rodent pain models. Pain 154: 864-873.
72. Zhang F, Challapalli SC, Smith PJ, (2009). Cannabinoid CB(1) receptor activation stimulates neurite outgrowth and inhibits capsaicin-induced Ca(2) influx in an in vitro model of diabetic neuropathy. Neuropharmacology 57: 88-89.