Glucagon-like peptide-1 receptor agonist ameliorates renal injury through its anti-inflammatory action without lowering blood glucose level in a rat model of type 1 diabetes

Diabetologia

Volumn 54, Issue 4, 2011, Pages 965-978

  Kodera, R ^a   Shikata, K ^a   Kataoka, H U ^a   Takatsuka, T ^a   Miyamoto, S ^a   Sasaki, M ^a   Kajitani, N ^a   Nishishita, S ^a   Sarai, K ^a   Hirota, D ^a   Sato, C ^a   Ogawa, D ^a   Makino, H ^a  

^a OKAYAMA UNIVERSITY   (Japan)

Author keywords

Anti inflammatory effect; Diabetic nephropathy; Exendin 4; Glomerular endothelial cells; GLP 1 receptor agonist; Intercellular adhesion molecule 1; Macrophage; Nuclear factor B; Type 1 diabetic rats

Indexed keywords

ALBUMIN; COLLAGEN TYPE 4; EXENDIN 4; GLUCAGON LIKE PEPTIDE 1; GLUCAGON LIKE PEPTIDE 1 RECEPTOR; GLUCAGON LIKE PEPTIDE 1 RECEPTOR AGONIST; GLUCOSE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERCELLULAR ADHESION MOLECULE 1; PLACEBO; RECEPTOR BLOCKING AGENT; STREPTOZOCIN; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIINFLAMMATORY ACTIVITY; ARTICLE; BLOOD PRESSURE; BODY WEIGHT; CELL INFILTRATION; CONTROLLED STUDY; CYTOKINE RELEASE; ENDOTHELIUM CELL; ENZYME ACTIVATION; GLOMERULAR DYSFUNCTION; GLOMERULAR HYPERFILTRATION; GLUCOSE BLOOD LEVEL; HISTOPATHOLOGY; IN VITRO STUDY; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY HYPERTROPHY; KIDNEY INJURY; KIDNEY PARENCHYMA; MACROPHAGE; MALE; MESANGIUM CELL; METABOLISM; MONOCYTE; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; PROTEINURIA; RAT; RENAL PROTECTION; TREATMENT DURATION; URINARY EXCRETION;

ANIMALS; BLOOD GLUCOSE; BLOTTING, WESTERN; CELL LINE; CELL LINE, TUMOR; COLLAGEN TYPE IV; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INTERCELLULAR ADHESION MOLECULE-1; MALE; NF-KAPPA B; PEPTIDES; RATS; RATS, SPRAGUE-DAWLEY; RECEPTORS, GLUCAGON; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TUMOR NECROSIS FACTOR-ALPHA; VENOMS;

EID: 79953826349     PISSN: 0012186X     EISSN: 14320428     Source Type: Journal    
DOI: 10.1007/s00125-010-2028-x     Document Type: Article

References (48)

1. de Zeeuw D, Parving HH, Henning RH (2006) Microalbuminuria as an early marker for cardiovascular disease. J Am Soc Nephrol 17:2100-2105
2. Go AS, Chertow GM, Fan D, McCulloch CE, Hsu CY (2004) Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. N Engl J Med 351:1296-1305
3. Magee GM, Bilous RW, Cardwell CR, Hunter SJ, Kee F, Fogarty DG (2009) Is hyperfiltration associated with the future risk of developing diabetic nephropathy? A meta-analysis. Diabetologia 52:691-697
4. Baynes JW (1991) Role of oxidative stress in development of complications in diabetes. Diabetes 40:405-412
5. Brownlee M, Cerami A, Vlassara H (1988) Advanced glycosylation end products in tissue and the biochemical basis of diabetic complications. N Engl J Med 318:1315-1321
6. Koya D, Jirousek MR, Lin YW, Ishii H, Kuboki K, King GL (1997) Characterization of protein kinase C beta isoform activation on the gene expression of transforming growth factor-beta, extracellular matrix components, and prostanoids in the glomeruli of diabetic rats. J Clin Invest 100:115-126 (Pubitemid 27311249)
7. Ziyadeh FN, Sharma K, Ericksen M, Wolf G (1994) Stimulation of collagen gene expression and protein synthesis in murine mesangial cells by high glucose is mediated by autocrine activation of transforming growth factor-beta. J Clin Invest 93:536-542 (Pubitemid 24072793)
8. Nelson CL, Karschimkus CS, Dragicevic G et al (2005) Systemic and vascular inflammation is elevated in early IgA and type 1 diabetic nephropathies and relates to vascular disease risk factors and renal function. Nephrol Dial Transplant 20:2420-2426 (Pubitemid 41548866)
9. Saraheimo M, Teppo AM, Forsblom C, Fagerudd J, Groop PH (2003) Diabetic nephropathy is associated with low-grade inflammation in type 1 diabetic patients. Diabetologia 46:1402-1407 (Pubitemid 37297211)
10. Furuta T, Saito T, Ootaka T et al (1993) The role of macrophages in diabetic glomerulosclerosis. Am J Kidney Dis 21:480-485 (Pubitemid 23160508)
11. Hirata K, Shikata K, Matsuda M et al (1998) Increased expression of selectins in kidneys of patients with diabetic nephropathy. Diabetologia 41:185-192 (Pubitemid 28088395)
12. Sugimoto H, Shikata K, Hirata K et al (1997) Increased expression of intercellular adhesion molecule-1 (ICAM-1) in diabetic rat glomeruli: glomerular hyperfiltration is a potential mechanism of ICAM-1 upregulation. Diabetes 46:2075-2081 (Pubitemid 27512099)
13. Okada S, Shikata K, Matsuda M et al (2003) Intercellular adhesion molecule-1-deficient mice are resistant against renal injury after induction of diabetes. Diabetes 52:2586-2593 (Pubitemid 37210549)
14. Yozai K, Shikata K, Sasaki M et al (2005) Methotrexate prevents renal injury in experimental diabetic rats via anti-inflammatory actions. J Am Soc Nephrol 16:3326-3338 (Pubitemid 46179336)
15. Tone A, Shikata K, Sasaki M et al (2005) Erythromycin ameliorates renal injury via anti-inflammatory effects in experimental diabetic rats. Diabetologia 48:2402-2411 (Pubitemid 41618933)
16. Ohga S, Shikata K, Yozai K et al (2007) Thiazolidinedione ameliorates renal injury in experimental diabetic rats through antiinflammatory effects mediated by inhibition of NF-kappaB activation. Am J Physiol Renal Physiol 292:F1141-F1150 (Pubitemid 46578056)
17. Usui H, Shikata K, Matsuda M et al (2003) HMG-CoA reductase inhibitor ameliorates diabetic nephropathy by its pleiotropic effects in rats. Nephrol Dial Transplant 18:265-272 (Pubitemid 36181675)
18. Baggio LL, Drucker DJ (2007) Biology of incretins: GLP-1 and GIP. Gastroenterology 132:2131-2157 (Pubitemid 46711096)
19. Farilla L, Hui H, Bertolotto C et al (2002) Glucagon-like peptide-1 promotes islet cell growth and inhibits apoptosis in Zucker diabetic rats. Endocrinology 143:4397-4408 (Pubitemid 35239574)
20. Nauck MA, Niedereichholz U, Ettler R et al (1997) Glucagon-like peptide 1 inhibition of gastric emptying outweighs its insulinotropic effects in healthy humans. Am J Physiol 273:E981-E988
21. Turton MD, O'Shea D, Gunn I et al (1996) A role for glucagon-like peptide-1 in the central regulation of feeding. Nature 379:69-72 (Pubitemid 26008136)
22. Orskov C, Wettergren A, Holst JJ (1993) Biological effects and metabolic rates of glucagon like peptide-1 7-36 amide and glucagon like peptide-1 7-37 in healthy subjects are indistinguishable. Diabetes 42:658-661 (Pubitemid 23127154)
23. Bullock BP, Heller RS, Habener JF (1996) Tissue distribution of messenger ribonucleic acid encoding the rat glucagon-like peptide-1 receptor. Endocrinology 137:2968-2978 (Pubitemid 26192194)
24. Schlatter P, Beglinger C, Drewe J, Gutmann H (2007) Glucagon-like peptide 1 receptor expression in primary porcine proximal tubular cells. Regul Pept 141:120-128 (Pubitemid 46482693)
25. Park CW, Kim HW, Ko SH et al (2007) Long-term treatment of glucagon-like peptide-1 analog exendin-4 ameliorates diabetic nephropathy through improving metabolic anomalies in db/db mice. J Am Soc Nephrol 18:1227-1238 (Pubitemid 46536909)
26. Hirata K, Kume S, Araki S et al (2009) Exendin-4 has an antihypertensive effect in salt-sensitive mice model. Biochem Biophys Res Commun 380:44-49
27. Etoh T, Inoguchi T, Kakimoto M et al (2003) Increased expression of NAD(P)H oxidase subunits, NOX4 and p22phox, in the kidney of streptozotocin-induced diabetic rats and its reversibity by interventive insulin treatment. Diabetologia 46:1428-1437 (Pubitemid 37297214)
28. Fong JS, Drummond KN (1968) Method for preparation of glomeruli for metabolic studies. J Lab Clin Med 71:1034-1039
29. Shigenaga MK, Gimeno CJ, Ames BN (1989) Urinary 8-hydroxy-2′- deoxyguanosine as a biological marker of in vivo oxidative DNA damage. Proc Natl Acad Sci U S A 86:9697-9701 (Pubitemid 20030700)
30. Liu H, Dear AE, Knudsen LB, Simpson RW (2009) A long-acting glucagon-like peptide-1 analogue attenuates induction of plasminogen activator inhibitor type-1 and vascular adhesion molecules. J Endocrinol 201:59-66
31. Pawluczyk IZ, Harris KP (1997) Macrophages promote prosclerotic responses in cultured rat mesangial cells: a mechanism for the initiation of glomerulosclerosis. J Am Soc Nephrol 8:1525-1536 (Pubitemid 27496470)
32. Leonarduzzi G, Scavazza A, Biasi F et al (1997) The lipid peroxidation end product 4-hydroxy-2,3-nonenal up-regulates transforming growth factor beta1 expression in the macrophage lineage: a link between oxidative injury and fibrosclerosis. Faseb J 11:851-857 (Pubitemid 27371894)
33. Ziyadeh FN, Hoffman BB, Han DC et al (2000) Long-term prevention of renal insufficiency, excess matrix gene expression, and glomerular mesangial matrix expansion by treatment with monoclonal antitransforming growth factor-beta antibody in db/db diabetic mice. Proc Natl Acad Sci U S A 97:8015-8020 (Pubitemid 30460765)
34. Sharma K, Ziyadeh FN (1995) Hyperglycemia and diabetic kidney disease. The case for transforming growth factor-beta as a key mediator. Diabetes 44:1139-1146
35. Guijarro C, Egido J (2001) Transcription factor-kappa B (NF-kappa B) and renal disease. Kidney Int 59:415-424 (Pubitemid 32157906)
36. Roebuck KA, Finnegan A (1999) Regulation of intercellular adhesion molecule-1 (CD54) gene expression. J Leukoc Biol 66:876-888 (Pubitemid 30010511)
37. Arakawa M, Mita T, Azuma K et al (2010) Inhibition of monocyte adhesion to endothelial cells and attenuation of atherosclerotic lesion by a glucagon-like peptide-1 receptor agonist, exendin-4. Diabetes 59:1030-1037
38. Gorin Y, Block K, Hernandez J et al (2005) Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney. J Biol Chem 280:39616-39626 (Pubitemid 41713921)
39. Frey RS, Ushio-Fukai M, Malik AB (2009) NADPH oxidase-dependent signaling in endothelial cells: role in physiology and pathophysiology. Antioxid Redox Signal 11:791-810
40. Sharma K, Ramachandrarao S, Qiu G et al (2008) Adiponectin regulates albuminuria and podocyte function in mice. J Clin Invest 118:1645-1656 (Pubitemid 351632369)
41. Doyle ME, Egan JM (2007) Mechanisms of action of glucagon-like peptide 1 in the pancreas. Pharmacol Ther 113:546-593 (Pubitemid 46365961)
42. Ollivier V, Parry GC, Cobb RR, de Prost D, Mackman N (1996) Elevated cyclic AMP inhibits NF-kappaB-mediated transcription in human monocytic cells and endothelial cells. J Biol Chem 271:20828-20835 (Pubitemid 26281870)
43. Kim JS, Diebold BA, Babior BM, Knaus UG, Bokoch GM (2007) Regulation of Nox1 activity via protein kinase A-mediated phosphorylation of NoxA1 and 14-3-3 binding. J Biol Chem 282:34787-34800 (Pubitemid 350232473)
44. Gutzwiller JP, Tschopp S, Bock A et al (2004) Glucagon-like peptide 1 induces natriuresis in healthy subjects and in insulin-resistant obese men. J Clin Endocrinol Metab 89:3055-3061 (Pubitemid 38766408)
45. Xu H, Barnes GT, Yang Q et al (2003) Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112:1821-1830 (Pubitemid 38063705)
46. Ross R (1999) Atherosclerosis - an inflammatory disease. N Engl J Med 340:115-126
47. Bongartz LG, Cramer MJ, Doevendans PA, Joles JA, Braam B (2005) The severe cardiorenal syndrome: 'Guyton revisited'. Eur Heart J 26:11-17
48. Nakamura A, Shikata K, Hiramatsu M et al (2005) Serum interleukin-18 levels are associated with nephropathy and atherosclerosis in Japanese patients with type 2 diabetes. Diabetes Care 28:2890-2895 (Pubitemid 43942920)