Modulation of Renal GLUT2 by the Cannabinoid-1 Receptor: Implications for the Treatment of Diabetic Nephropathy

Journal of the American Society of Nephrology

Volumn 29, Issue 2, 2018, Pages 434-448

  Hinden, Liad ^a   Udi, Shiran ^a   Drori, Adi ^a   Gammal, Asaad ^a   Nemirovski, Alina ^a   Hadar, Rivka ^a   Baraghithy, Saja ^a   Permyakova, Anna ^a   Geron, Matan ^a   Cohen, Merav ^a   Tsytkin Kirschenzweig, Sabina ^a   Riahi, Yael ^a   Leibowitz, Gil ^a   Nahmias, Yaakov ^a   Priel, Avi ^a   Tam, Joseph ^a  

^a HEBREW UNIVERSITY OF JERUSALEM   (Israel)

Author keywords

[No Author keywords available]

Indexed keywords

CANNABINOID 1 RECEPTOR; GLUCOSE; GLUCOSE TRANSPORTER 2; 3-(4-CHLOROPHENYL)-N-METHYL-N'-((4-CHLOROPHENYL)SULFONYL)-4-PHENYL-4,5-DIHYDRO-1H-PYRAZOLE-1-CARBOXAMIDINE; CREATININE; INSULIN; JD5037; PROTEIN KINASE C BETA; PYRAZOLE DERIVATIVE; SLC2A2 PROTEIN, MOUSE; STREPTOZOCIN; SULFONAMIDE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DIABETIC NEPHROPATHY; DOWN REGULATION; HUMAN; HUMAN CELL; KIDNEY FIBROSIS; KIDNEY FUNCTION; KIDNEY PROXIMAL TUBULE; KIDNEY STRUCTURE; KIDNEY TUBULE ABSORPTION; KIDNEY TUBULE CELL; KIDNEY TUBULE DAMAGE; KIDNEY TUBULE EPITHELIUM; MALE; MOUSE; NEPHRITIS; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; RECEPTOR BLOCKING; UPREGULATION; ALBUMINURIA; ANIMAL; ANTAGONISTS AND INHIBITORS; BLOOD; CHEMICALLY INDUCED; DOG; FIBROSIS; GENETICS; GLUCOSE BLOOD LEVEL; KNOCKOUT MOUSE; MDCK CELL LINE; METABOLISM; PANCREAS ISLET; PATHOLOGY; TRANSPORT AT THE CELLULAR LEVEL; UREA NITROGEN BLOOD LEVEL; URINE;

ALBUMINURIA; ANIMALS; BIOLOGICAL TRANSPORT; BLOOD GLUCOSE; BLOOD UREA NITROGEN; CREATININE; DIABETIC NEPHROPATHIES; DOGS; FIBROSIS; GLUCOSE; GLUCOSE TRANSPORTER TYPE 2; INSULIN; ISLETS OF LANGERHANS; KIDNEY TUBULES, PROXIMAL; MADIN DARBY CANINE KIDNEY CELLS; MALE; MICE; MICE, KNOCKOUT; PROTEIN KINASE C BETA; PYRAZOLES; STREPTOZOCIN; SULFONAMIDES;

EID: 85041457312     PISSN: 10466673     EISSN: 15333450     Source Type: Journal    
DOI: 10.1681/ASN.2017040371     Document Type: Article

References (51)

1. Randall MD, Kendall DA, O’Sullivan S: The complexities of the cardiovascular actions of cannabinoids. Br J Pharmacol 142: 20-26, 2004
2. Declèves AE, Sharma K: New pharmacological treatments for improving renal outcomes in diabetes. Nat Rev Nephrol 6: 371-380, 2010
3. Gilbertson DT, Liu J, Xue JL, Louis TA, Solid CA, Ebben JP, Collins AJ: Projecting the number of patients with end-stage renal disease in the United States to the year 2015. J Am Soc Nephrol 16: 3736-3741, 2005
4. Larkins RG, Dunlop ME: The link between hyperglycaemia and diabetic nephropathy. Diabetologia 35: 499-504, 1992
5. Wolf G, Thaiss F: Hyperglycaemia-pathophysiological aspects at the cellular level. Nephrol Dial Transplant 10: 1109-1112, 1995
6. Marks J, Carvou NJ, Debnam ES, Srai SK, Unwin RJ: Diabetes increases facilitative glucose uptake and GLUT2 expression at the rat proximal tubule brush border membrane. J Physiol 553: 137-145, 2003
7. Chichger H, Cleasby ME, Srai SK, Unwin RJ, Debnam ES, Marks J: Experimental type II diabetes and related models of impaired glucose metabolism differentially regulate glucose transporters at the proximal tubule brush border membrane. Exp Physiol 101: 731-742, 2016
8. Goestemeyer AK, Marks J, Srai SK, Debnam ES, Unwin RJ: GLUT2 protein at the rat proximal tubule brush border membrane correlates with protein kinase C (PKC)-betal and plasma glucose concentration. Diabetologia 50: 2209-2217, 2007
9. Chin E, Zhou J, Bondy C: Anatomical and developmental patterns of facilitative glucose transporter gene expression in the rat kidney. J Clin Invest 91: 1810-1815, 1993
10. Thorens B: Glucose transporters in the regulation of intestinal, renal, and liver glucose fluxes. Am J Physiol 270: G541-G553, 1996
11. Rahmoune H, Thompson PW, Ward JM, Smith CD, Hong G, Brown J: Glucose transporters in human renal proximal tubular cells isolated from the urine of patients with non-insulin-dependent diabetes. Diabetes 54: 3427-3434, 2005
12. Chin E, Zamah AM, Landau D, Grønbcek H, Flyvbjerg A, LeRoith D, Bondy CA: Changes in facilitative glucose transporter messenger ribonucleic acid levels in the diabetic rat kidney. Endocrinology 138: 1267-1275, 1997
13. Cohen M, Kitsberg D, Tsytkin S, Shulman M, Aroeti B, Nahmias Y: Live imaging of GLUT2 glucose-dependent trafficking and its inhibition in polarized epithelial cysts. Open Biol 4: 140091, 2014
14. Freitas HS, Schaan BD, David-Silva A, Sabino-Silva R, Okamoto MM, Alves-Wagner AB, Mori RC, Machado UF: SLC2A2 gene expression in kidney of diabetic rats is regulated by HNF-1alpha and HNF-3beta. Mol Cell Endocrinol 305: 63-70, 2009
15. David-Silva A, Freitas HS, Okamoto MM, Sabino-Silva R, Schaan BD, Machado UF: Hepatocyte nuclear factors 1a/4a and forkhead box A2 regulate the solute carrier 2A2 (Slc2a2) gene expression in the liver and kidney of diabetic rats. Life Sci 93: 805-813, 2013
16. Im SS, Kang SY, Kim SY, Kim HI, Kim JW, Kim KS, Ahn YH: Glucose-stimulated upregulation of GLUT2 gene is mediated by sterol response element-binding protein-1c in the hepatocytes. Diabetes 54: 1684-1691, 2005
17. Janiak P, Poirier B, Bidouard JP, Cadrouvele C, Pierre F, Gouraud L, Barbosa I, Dedio J, Maffrand JP, Le Fur G, O’Connor S, Herbert JM: Blockade of cannabinoid CB1 receptors improves renal function, metabolic profile, and increased survival of obese Zucker rats. Kidney Int 72: 1345-1357, 2007
18. Barutta F, Corbelli A, Mastrocola R, Gambino R, Di Marzo V, Pinach S, Rastaldi MP, Perin PC, Gruden G: Cannabinoid receptor 1 blockade ameliorates albuminuria in experimental diabetic nephropathy. Diabetes 59: 1046-1054, 2010
19. Jenkin KA, McAinch AJ, Grinfeld E, Hryciw DH: Role for cannabinoid receptors in human proximal tubular hypertrophy. Cell Physiol Bio-chem 26:879-886, 2010
20. Jourdan T, Szanda G, Rosenberg AZ, Tam J, Earley BJ, Godlewski G, Cinar R, Liu Z, Liu J, Ju C, Pacher P, Kunos G: Overactive cannabinoid 1 receptor in podocytes drives type 2 diabetic nephropathy. Proc Natl Acad Sci USA 111: E5420-E5428, 2014
21. Lin CL, Hsu YC, Lee PH, Lei CC, Wang JY, Huang YT, Wang SY, Wang FS: Cannabinoid receptor 1 disturbance of PPARg2 augments hyperglycemia induction of mesangial inflammation and fibrosis in renal glomeruli. J Mol Med (Berl) 92: 779-792, 2014
22. Jenkin KA, McAinch AJ, Zhang Y, Kelly DJ, Hryciw DH: Elevated cannabinoid receptor 1 and G protein-coupled receptor 55 expression in proximal tubule cells and whole kidney exposed to diabetic conditions. Clin Exp Pharmacol Physiol 42: 256-262, 2015
23. Hsu YC, Lei CC, Shih YH, Ho C, Lin CL: Induction of proteinuria by cannabinoid receptors 1 signaling activation in CB1 transgenic mice. Am J Med Sci 349: 162-168, 2015
24. Mukhopadhyay P, Pan H, Rajesh M, Bátkai S, Patel V, Harvey-White J, Mukhopadhyay B, Haskó 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 160: 657-668, 2010
25. Nam DH, Lee MH, Kim JE, Song HK, Kang YS, Lee JE, Kim HW, Cha JJ, Hyun YY, Kim SH, Han SY, Han KH, Han JY, Cha DR: Blockade of cannabinoid receptor 1 improves insulin resistance, lipid metabolism, and diabetic nephropathy in db/db mice. Endocrinology 153: 1387-1396, 2012
26. Jourdan T, Szanda G, Cinar R, Godlewski G, Holovac DJ, Park JK, Nicoloro S, Shen Y, Liu J, Rosenberg AZ, Liu Z, Czech MP, Kunos G: Developmental role of macrophage cannabinoid-1 receptor signaling in type 2 diabetes. Diabetes 66: 994-1007, 2017
27. Moreira FA, Grieb M, Lutz B: Central side-effects of therapies based on CB1 cannabinoid receptor agonists and antagonists: Focus on anxiety and depression. Best Pract Res Clin Endocrinol Metab 23: 133-144, 2009
28. Le Foll B, Gorelick DA, Goldberg SR: The future of endocannabinoid-oriented clinical research after CB1 antagonists. Psychopharmacology (Berl) 205: 171-174, 2009
29. Tam J, Cinar R, Liu J, Godlewski G, Wesley D, Jourdan T, Szanda G, Mukhopadhyay B, Chedester L, Liow JS, Innis RB, Cheng K, Rice KC, Deschamps JR, Chorvat RJ, McElroy JF, Kunos G: Peripheral cannabinoid-1 receptor inverse agonism reduces obesity by reversing leptin resistance. Cell Metab 16: 167-179, 2012
30. Tam J, Vemuri VK, Liu J, Bátkai S, Mukhopadhyay B, Godlewski G, Osei-Hyiaman D, Ohnuma S, Ambudkar SV, Pickel J, Makriyannis A, Kunos G: Peripheral CB1 cannabinoid receptor blockade improves cardiometabolic risk in mouse models of obesity. J Clin Invest 120: 2953-2966, 2010
31. Jourdan T, Godlewski G, Cinar R, Bertola A, Szanda G, Liu J, Tam J, Han T, Mukhopadhyay B, Skarulis MC, Ju C, Aouadi M, Czech MP, Kunos G: Activation of the Nlrp3 inflammasome in infiltrating macrophages by endocannabinoids mediates beta cell loss in type 2 diabetes. Nat Med 19: 1132-1140, 2013
32. Cinar R, Godlewski G, Liu J, Tam J, Jourdan T, Mukhopadhyay B, Harvey-White J, Kunos G: Hepatic cannabinoid-1 receptors mediate diet-induced insulin resistance by increasing de novo synthesis of long-chain ceramides. Hepatology 59: 143-153, 2014
33. Liu J, Zhou L, Xiong K, Godlewski G, Mukhopadhyay B, Tam J, Yin S, Gao P, Shan X, Pickel J, Bataller R, O’Hare J, Scherer T, Buettner C, Kunos G: Hepatic cannabinoid receptor-1 mediates diet-induced insulin resistance via inhibition of insulin signaling and clearance in mice. Gastroenterology 142: 1218-1228.e1, 2012
34. Kamran M, Peterson RG, Dominguez JH: Overexpression of GLUT2 gene in renal proximal tubules of diabetic Zucker rats. J Am Soc Nephrol 8: 943-948, 1997
35. Kellett GL, Brot-Laroche E: Apical GLUT2: A major pathway of intestinal sugar absorption. Diabetes 54: 3056-3062, 2005
36. Schnedl WJ, Ferber S, Johnson JH, Newgard CB: STZ transport and cytotoxicity. Specific enhancement in GLUT2-expressing cells. Diabetes 43: 1326-1333, 1994
37. Gurley SB, Clare SE, Snow KP, Hu A, Meyer TW, Coffman TM: Impact of genetic background on nephropathy in diabetic mice. Am J Physiol Renal Physiol 290: F214-F222, 2006
38. You H, Gao T, Cooper TK, Morris SM Jr., Awad AS: Arginase inhibition: A new treatment for preventing progression of established diabetic nephropathy. Am J Physiol Renal Physiol 309: F447-F455, 2015
39. Gurley SB, Mach CL, Stegbauer J, Yang J, Snow KP, Hu A, Meyer TW, Coffman TM: Influence of genetic background on albuminuria and kidney injury in Ins2(+/C96Y) (Akita) mice. Am J Physiol Renal Physiol 298: F788-F795, 2010
40. Udi S, Hinden L, Earley B, Drori A, Reuveni N, Hadar R, Cinar R, Nemirovski A, Tam J: Proximal tubular cannabinoid-1 receptor regulates obesity-induced CKD [published online ahead of print August 31, 2017]. J Am Soc Nephrol doi: 10.1681/ASN.2016101085
41. Elsner M, Guldbakke B, Tiedge M, Munday R, Lenzen S: Relative importance of transport and alkylation for pancreatic beta-cell toxicity of streptozotocin. Diabetologia 43: 1528-1533, 2000
42. Lecru L, Desterke C, Grassin-Delyle S, Chatziantoniou C, Vandermeersch S, Devocelle A, Vernochet A, Ivanovski N, Ledent C, Ferlicot S, Dalia M, Saïd M, Beaudreuil S, Charpentier B, Vazquez A, Giron-Michel J, Azzarone B, Durrbach A, François H: Cannabinoid receptor 1 is a major mediator of renal fibrosis. Kidney Int 88: 72-84, 2015
43. Kahraman S, Aydin C, Elpek GO, Dirice E, Sanlioglu AD: Diabetes-resistant NOR mice are more severely affected by streptozotocin compared to the diabetes-prone NOD mice: Correlations with liver and kidney GLUT2 expressions. J Diabetes Res 2015: 450128, 2015
44. Lauckner JE, Hille B, Mackie K: The cannabinoid agonist WIN55,212-2 increases intracellular calcium via CB1 receptor coupling to Gq/11 G proteins. Proc Natl Acad Sci U S A 102: 19144-19149, 2005
45. Hsieh TJ, Chen R, Zhang SL, Liu F, Brezniceanu ML, Whiteside CI, Fantus IG, Ingelfinger JR, Hamet P, Chan JS: Upregulation of osteo-pontin gene expression in diabetic rat proximal tubular cells revealed by microarray profiling. Kidney Int 69: 1005-1015, 2006
46. Yeh JH, Cheng HH, Huang CJ, Chung HM, Chiu HF, Yang YL, Yeh MY, Chen WC, Kao CH, Chou CT, Jan CR: Effect of anandamide on cytosolic Ca(2+) levels and proliferation in canine renal tubular cells. Basic Clin Pharmacol Toxicol 98: 416-422, 2006
47. Albertoni Borghese MF, Majowicz MP, Ortiz MC, Passalacqua MR, Sterin Speziale NB, Vidal NA: Expression and activity of SGLT2 in diabetes induced by streptozotocin: Relationship with the lipid environment. Nephron, Physiol 112: 45-52, 2009
48. Hahn K, Ejaz AA, Kanbay M, Lanaspa MA, Johnson RJ: Acute kidney injury from SGLT2 inhibitors: Potential mechanisms. Nat Rev Nephrol 12: 711-712, 2016
49. Chorvat RJ, Berbaum J, Seriacki K, McElroy JF: 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: 6173-6180, 2012
50. Tam J, Godlewski G, Earley BJ, Zhou L, Jourdan T, Szanda G, Cinar R, Kunos G: Role of adiponectin in the metabolic effects of cannabinoid type 1 receptor blockade in mice with diet-induced obesity. Am J Physiol Endocrinol Metab 306: E457-E468, 2014
51. Knani I, Earley BJ, Udi S, Nemirovski A, Hadar R, Gammal A, Cinar R, Hirsch HJ, Pollak Y, Gross I, Eldar-Geva T, Reyes-Capo DP, Han JC, Haqq AM, Gross-Tsur V, Wevrick R, Tam J: Targeting the endocanna-binoid/CB1 receptor system for treating obesity in Prader-Willi syndrome. Mol Metab 5: 1187-1199, 2016