Overactive cannabinoid 1 receptor in podocytes drives type 2 diabetic nephropathy

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

Volumn 111, Issue 50, 2014, Pages E5420-E5428

  Jourdan, Tony ^a   Szandaa, Gergo ^a   Rosenberg, Avi Z ^b,c   Tam, Joseph ^a   Earley, Brian James ^a   Godlewski, Grzegorz ^a   Cinar, Resat ^a   Liu, Ziyi ^a   Liu, Jie ^a   Ju, Cynthia ^d   Pacher, Pál ^e   Kunos, George ^a  

^a NATIONAL INSTITUTES OF HEALTH   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

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

^d UNIVERSITY OF COLORADO   (United States)

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

Author keywords

Angiotensin II; Endocannabinoid; Hyperglycemia; Nephropathy; Podocyte

Indexed keywords

ANGIOTENSIN; CANNABINOID 1 RECEPTOR; DESMIN; LOSARTAN; NEPHRIN; PODOCIN; RENIN; SMALL INTERFERING RNA; AGTR1A PROTEIN, RAT; ANGIOTENSIN 1 RECEPTOR; ANGIOTENSIN II; ARACHIDONIC ACID DERIVATIVE; ARACHIDONYL-2-CHLOROETHYLAMIDE; JD5037; PYRAZOLE DERIVATIVE; SULFONAMIDE;

ALBUMINURIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL LOSS; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; DOWN REGULATION; GENE SILENCING; GLOMERULUS; GLOMERULUS FILTRATION; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; KIDNEY CORTEX; NITRATIVE STRESS; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PHARMACOLOGICAL BLOCKING; PODOCYTE; PROTEIN CONTENT; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; AGONISTS; ANALYSIS OF VARIANCE; ANIMAL; ANTAGONISTS AND INHIBITORS; BIOLOGICAL MODEL; COMPLICATION; DIABETIC NEPHROPATHIES; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; RNA INTERFERENCE; SYNTHESIS; ZUCKER RAT;

ANIMALIA; RATTUS;

ANALYSIS OF VARIANCE; ANGIOTENSIN II; ANIMALS; ARACHIDONIC ACIDS; DESMIN; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; GENE EXPRESSION REGULATION; LOSARTAN; MODELS, BIOLOGICAL; PODOCYTES; PYRAZOLES; RATS; RATS, ZUCKER; RECEPTOR, ANGIOTENSIN, TYPE 1; RECEPTOR, CANNABINOID, CB1; RNA INTERFERENCE; RNA, SMALL INTERFERING; SULFONAMIDES;

EID: 84918571992     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.1419901111     Document Type: Article

References (54)

1. Eknoyan G (2007) Obesity, diabetes, and chronic kidney disease. Curr Diab Rep 7(6):449-453.
2. Leehey DJ, Singh AK, Alavi N, Singh R (2000) Role of angiotensin II in diabetic nephropathy. Kidney Int Suppl 77:S93-S98.
3. Gorin Y, Block K (2013) Nox as a target for diabetic complications. Clin Sci (Lond) 125(8):361-382.
4. Szabo C (2009) Role of nitrosative stress in the pathogenesis of diabetic vascular dysfunction. Br J Pharmacol 156(5):713-727.
5. 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(2):432-442.
6. Pacher P, Kunos G (2013) Modulating the endocannabinoid system in human health and disease - Successes and failures. FEBS J 280(9):1918-1943.
7. Engeli S (2012) Central and peripheral cannabinoid receptors as therapeutic targets in the control of food intake and body weight. Handb Exp Pharmacol (209):357-381.
8. Barutta F, et al. (2010) Cannabinoid receptor 1 blockade ameliorates albuminuria in experimental diabetic nephropathy. Diabetes 59(4):1046-1054.
9. Nam DH, et al. (2012) Blockade of cannabinoid receptor 1 improves insulin resistance, lipid metabolism, and diabetic nephropathy in db/db mice. Endocrinology 153(3):1387-1396.
10. Janiak P, et al. (2007) Blockade of cannabinoid CB1 receptors improves renal function, metabolic profile, and increased survival of obese Zucker rats. Kidney Int 72(11):1345-1357.
11. Rohrbach K, et al. (2012) Ibipinabant attenuates innodatabeta-cell loss in male Zucker diabetic fatty rats independently of its effects on body weight. Diabetes Obes Metab 14(6):555-564.
12. Le Foll B, Gorelick DA, Goldberg SR (2009) The future of endocannabinoid-oriented clinical research after CB1 antagonists. Psychopharmacology (Berl) 205(1):171-174.
13. 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.
14. Tam J, et al. (2012) Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab 16(2):167-179.
15. Jourdan T, et al. (2013) Activation of the Nlrp3 inflammasome in infiltrating macrophages by endocannabinoids mediates beta cell loss in type 2 diabetes. Nat Med 19(9):1132-1140.
16. Hoshi S, et al. (2002) Podocyte injury promotes progressive nephropathy in zucker diabetic fatty rats. Lab Invest 82(1):25-35.
17. Coimbra TM, et al. (2000) Early events leading to renal injury in obese Zucker (fatty) rats with type II diabetes. Kidney Int 57(1):167-182.
18. Mizuno M, et al. (2006) The effect of angiotensin II receptor blockade on an end-stage renal failure model of type 2 diabetes. J Cardiovasc Pharmacol 48(4):135-142.
19. Pacher P, Nivorozhkin A, Szabó C (2006) Therapeutic effects of xanthine oxidase inhibitors: Renaissance half a century after the discovery of allopurinol. Pharmacol Rev 58(1):87-114.
20. Mangge H, et al. (2013) Uric acid best predicts metabolically unhealthy obesity with increased cardiovascular risk in youth and adults. Obesity (Silver Spring) 21(1):E71-E77.
21. Abdullah AR, Hasan HA, Raigangar VL (2009) Analysis of the relationship of leptin, high-sensitivity C-reactive protein, adiponectin, insulin, and uric acid to metabolic syndrome in lean, overweight, and obese young females. Metab Syndr Relat Disord 7(1):17-22.
22. Lassègue B, Clempus RE (2003) Vascular NAD(P)H oxidases: Specific features, expression, and regulation. Am J Physiol Regul Integr Comp Physiol 285(2):R277-R297.
23. Venkatareddy M, et al. (2014) Estimating podocyte number and density using a single histologic section. J Am Soc Nephrol 25(5):1118-1129.
24. Gruden G, Perin PC, Camussi G (2005) Insight on the pathogenesis of diabetic nephropathy from the study of podocyte and mesangial cell biology. Curr Diabetes Rev 1(1):27-40.
25. Lim SK, Park SH (2012) The high glucose-induced stimulation of B1R and B2R expression via CB(1)R activation is involved in rat podocyte apoptosis. Life Sci 91(19-20):895-906.
26. Krolewski M, Eggers PW, Warram JH (1996) Magnitude of end-stage renal disease in IDDM: A 35 year follow-up study. Kidney Int 50(6):2041-2046.
27. Larrinaga G, et al. (2010) Expression of cannabinoid receptors in human kidney. Histol Histopathol 25(9):1133-1138.
28. Mukhopadhyay B, et al. (2010) Transcriptional regulation of cannabinoid receptor-1 expression in the liver by retinoic acid acting via retinoic acid receptor-gamma. J Biol Chem 285(25):19002-19011.
29. Jourdan T, et al. (2010) CB1 antagonism exerts specific molecular effects on visceral and subcutaneous fat and reverses liver steatosis in diet-induced obese mice. Diabetes 59(4):926-934.
30. Börner C, Höllt V, Sebald W, Kraus J (2007) Transcriptional regulation of the cannabinoid receptor type 1 gene in T cells by cannabinoids. J Leukoc Biol 81(1):336-343.
31. de Zeeuw D, et al.; BEACON Trial Investigators (2013) Bardoxolone methyl in type 2 diabetes and stage 4 chronic kidney disease. N Engl J Med 369(26):2492-2503.
32. Vesely DL, et al. (1999) Elevated atrial natriuretic peptides and early renal failure in type 2 diabetic Goto-Kakizaki rats. Metabolism 48(6):771-778.
33. Suzaki Y, Ozawa Y, Kobori H (2007) Intrarenal oxidative stress and augmented angiotensinogen are precedent to renal injury in Zucker diabetic fatty rats. Int J Biol Sci 3(1):40-46.
34. Reiser J, Sever S (2013) Podocyte biology and pathogenesis of kidney disease. Annu Rev Med 64:357-366.
35. Lim SK, et al. (2012) Hyperglycemia induces apoptosis via CB1 activation through the decrease of FAAH 1 in retinal pigment epithelial cells. J Cell Physiol 227(2):569-577.
36. 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(1):35-39.
37. Komers R (2013) Renin inhibition in the treatment of diabetic kidney disease. Clin Sci (Lond) 124(9):553-566.
38. Kobori H, Kamiyama M, Harrison-Bernard LM, Navar LG (2013) Cardinal role of the intrarenal renin-angiotensin system in the pathogenesis of diabetic nephropathy. J Investig Med 61(2):256-264.
39. Matsusaka T, et al. (2014) Podocyte injury enhances filtration of liver-derived angiotensinogen and renal angiotensin II generation. Kidney Int 85(5):1068-1077.
40. Gill PS, Wilcox CS (2006) NADPH oxidases in the kidney. Antioxid Redox Signal 8(9-10):1597-1607.
41. Campbell KN, Raij L, Mundel P (2011) Role of angiotensin II in the development of nephropathy and podocytopathy of diabetes. Curr Diabetes Rev 7(1):3-7.
42. Ran J, et al. (2006) Angiotensin II infusion decreases plasma adiponectin level via its type 1 receptor in rats: An implication for hypertension-related insulin resistance. Metabolism 55(4):478-488.
43. Li L, et al. (2013) Angiotensin II reduces cardiac AdipoR1 expression through AT1 receptor/ROS/ERK1/2/c-Myc pathway. PLoS ONE 8(1):e49915.
44. Burnier M, Brunner HR (1996) Renal effects of angiotensin II receptor blockade and angiotensin-converting enzyme inhibition in healthy subjects. Exp Nephrol 4(Suppl 1):41-46.
45. Touyz RM, et al. (2007) Increased inflammatory biomarkers in hypertensive type 2 diabetic patients: Improvement after angiotensin II type 1 receptor blockade. J Am Soc Hypertens 1(3):189-199.
46. Zhang W, et al. (2012) Interleukin 6 underlies angiotensin II-induced hypertension and chronic renal damage. Hypertension 59(1):136-144.
47. Rosa AC, Rattazzi L, Miglio G, Collino M, Fantozzi R (2012) Angiotensin II induces tumor necrosis factor-α expression and release from cultured human podocytes. Inflamm Res 61(4):311-317.
48. Kagawa T, et al. (2008) Angiotensin II receptor blocker inhibits tumour necrosis factor-alpha-induced cell damage in human renal proximal tubular epithelial cells. Nephrology (Carlton) 13(4):309-315.
49. Turu G, et al. (2009) Paracrine transactivation of the CB1 cannabinoid receptor by AT1 angiotensin and other Gq/11 protein-coupled receptors. J Biol Chem 284(25):16914-16921.
50. Szekeres M, et al. (2012) Angiotensin II induces vascular endocannabinoid release, which attenuates its vasoconstrictor effect via CB1 cannabinoid receptors. J Biol Chem 287(37):31540-31550.
51. Tiyerili V, 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(4):465-477.
52. 1R heteromerization reveals a new mechanism for the pathogenic properties of angiotensin II. EMBO J 30(12):2350-2363.
53. Chorvat RJ, Berbaum J, Seriacki K, McElroy JF (2012) JD-5006 and JD-5037: Peripherally restricted (PR) cannabinoid-1 receptor blockers related to SLV-319 (Ibipinabant) as metabolic disorder therapeutics devoid of CNS liabilities. Bioorg Med Chem Lett 22(19):6173-6180.
54. Mukhopadhyay B, et al. (2011) Hyperactivation of anandamide synthesis and regulation of cell-cycle progression via cannabinoid type 1 (CB1) receptors in the regenerating liver. Proc Natl Acad Sci USA 108(15):6323-6328.