Olmesartan Prevents Microalbuminuria in db/db Diabetic Mice Through Inhibition of Angiotensin II/p38/SIRT1-Induced Podocyte Apoptosis

Kidney and Blood Pressure Research

Volumn 41, Issue 6, 2016, Pages 848-864

  Gu, Junhui ^a   Yang, Ming ^a   Qi, Na ^a   Mei, Shuqin ^a   Chen, Jiejian ^a   Song, Shuwei ^a   Jing, Ying ^a   Chen, Meihan ^a   He, Liangliang ^a   Sun, Lijun ^a   Hu, Huimin ^a   Li, Lin ^a   Wüthrich, Rudolf P ^b   Wu, Ming ^a   Mei, Changlin ^a  

^a SECOND MILITARY MEDICAL UNIVERSITY   (China)

^b UNIVERSITY HOSPITAL ZURICH   (Switzerland)

Author keywords

Apoptosis; Diabetic nephropathy; Olmesartan; Podocytes; SIRT1

Indexed keywords

2 BUTYL 4 CHLORO 1 (2 CHLOROBENZYL) 5 IMIDAZOLEACETIC ACID; ADENYLATE KINASE; ALBUMIN; ANGIOTENSIN II; CREATININE; GLUCOSE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; MITOGEN ACTIVATED PROTEIN KINASE P38; NICOTINAMIDE ADENINE DINUCLEOTIDE ADENOSINE DIPHOSPHATE RIBOSYLTRANSFERASE; OLMESARTAN; PLACEBO; PROTEIN BAX; PROTEIN BCL 2; SIRTUIN 1; IMIDAZOLE DERIVATIVE; SIRT1 PROTEIN, MOUSE; TETRAZOLE DERIVATIVE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; APOPTOSIS; ARTICLE; CELL IMMORTALIZATION; CONTROLLED STUDY; DIABETES MELLITUS; DIABETIC NEPHROPATHY; DISEASE MODEL; ENZYME PHOSPHORYLATION; GLOMERULUS; GLUCOSE BLOOD LEVEL; IN VITRO STUDY; INHIBITION KINETICS; MALE; MICROALBUMINURIA; MOUSE; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; TREATMENT DURATION; WEIGHT CHANGE; ALBUMINURIA; ANIMAL; CELL LINE; DIABETIC NEPHROPATHIES; DRUG EFFECTS; INBRED MOUSE STRAIN; PATHOLOGY;

ALBUMINURIA; ANGIOTENSIN II; ANIMALS; APOPTOSIS; CELL LINE; DIABETIC NEPHROPATHIES; DISEASE MODELS, ANIMAL; IMIDAZOLES; MALE; MICE; MICE, INBRED STRAINS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PODOCYTES; SIRTUIN 1; TETRAZOLES;

EID: 84996671364     PISSN: 14204096     EISSN: 14230143     Source Type: Journal    
DOI: 10.1159/000452588     Document Type: Article

References (40)

1. Chan GC, Tang SC: Diabetic nephropathy: landmark clinical trials and tribulations. Nephrol Dial Transplant 2016;31:359-368.
2. Vivian E, Mannebach C: Therapeutic approaches to slowing the progression of diabetic nephropathy-is less best? Drugs Context 2013;2013:212249.
3. Chatzikyrkou C, Menne J: Update on the ROADMAP clinical trial report: olmesartan for the prevention or delay of microalbuminuria development in type 2 diabetes. Expert Rev Cardiovasc Ther 2012;10:1087-1092.
4. Haller H, Ito S, Izzo JL, Jr., Januszewicz A, Katayama S, Menne J, Mimran A, Rabelink TJ, Ritz E, Ruilope LM, Rump LC, Viberti G, Investigators RT: Olmesartan for the delay or prevention of microalbuminuria in type 2 diabetes. N Engl J Med 2011;364:907-917.
5. Zhang MZ, Wang S, Yang S, Yang H, Fan X, Takahashi T, Harris RC: Role of blood pressure and the renin-angiotensin system in development of diabetic nephropathy (DN) in eNOS-/- db/db mice. Am J Physiol Renal Physiol 2012;302:F433-438.
6. Liu R, Zhong Y, Li X, Chen H, Jim B, Zhou MM, Chuang PY, He JC: Role of transcription factor acetylation in diabetic kidney disease. Diabetes 2014;63:2440-2453.
7. Tesch GH, Lim AK: Recent insights into diabetic renal injury from the db/db mouse model of type 2 diabetic nephropathy. Am J Physiol Renal Physiol 2011;300:F301-310.
8. Roth M, Chen WY: Sorting out functions of sirtuins in cancer. Oncogene 2014;33:1609-1620.
9. Polak-Jonkisz D, Laszki-Szczachor K, Rehan L, Pilecki W, Filipowski H, Sobieszczanska M: Nephroprotective action of sirtuin 1 (SIRT1). J Physiol Biochem 2013;69:957-961.
10. Kim MY, Lim JH, Youn HH, Hong YA, Yang KS, Park HS, Chung S, Ko SH, Shin SJ, Choi BS, Kim HW, Kim YS, Lee JH, Chang YS, Park CW: Resveratrol prevents renal lipotoxicity and inhibits mesangial cell glucotoxicity in a manner dependent on the AMPK-SIRT1-PGC1alpha axis in db/db mice. Diabetologia 2013;56:204-217.
11. Marampon F, Gravina GL, Scarsella L, Festuccia C, Lovat F, Ciccarelli C, Zani BM, Polidoro L, Grassi D, Desideri G, Evangelista S, Ferri C: Angiotensin-converting-enzyme inhibition counteracts angiotensin II-mediated endothelial cell dysfunction by modulating the p38/SirT1 axis. J Hypertens 2013;31:1972-1983.
12. Hao CM, Haase VH: Sirtuins and their relevance to the kidney. J Am Soc Nephrol 2010;21:1620-1627.
13. Cai X, Bao L, Ren J, Li Y, Zhang Z: Grape seed procyanidin B2 protects podocytes from high glucose-induced mitochondrial dysfunction and apoptosis via the AMPK-SIRT1-PGC-1alpha axis in vitro. Food Funct 2016;7:805-815.
14. Yuan Y, Huang S, Wang W, Wang Y, Zhang P, Zhu C, Ding G, Liu B, Yang T, Zhang A: Activation of peroxisome proliferator-activated receptor-gamma coactivator 1alpha ameliorates mitochondrial dysfunction and protects podocytes from aldosterone-induced injury. Kidney Int 2012;82:771-789.
15. Zhou G, Cheung AK, Liu X, Huang Y: Valsartan slows the progression of diabetic nephropathy in db/db mice via a reduction in podocyte injury, and renal oxidative stress and inflammation. Clin Sci (Lond) 2014;126:707-720.
16. Mima A, Matsubara T, Arai H, Abe H, Nagai K, Kanamori H, Sumi E, Takahashi T, Iehara N, Fukatsu A, Kita T, Doi T: Angiotensin II-dependent Src and Smad1 signaling pathway is crucial for the development of diabetic nephropathy. Lab Invest 2006;86:927-939.
17. Rafiq K, Sherajee SJ, Hitomi H, Nakano D, Kobori H, Ohmori K, Mori H, Kobara H, Masaki T, Kohno M, Nishiyama A: Calcium channel blocker enhances beneficial effects of an angiotensin II AT1 receptor blocker against cerebrovascular-renal injury in type 2 diabetic mice. PLoS One 2013;8:e82082.
18. Sofue T, Kiyomoto H, Kobori H, Urushihara M, Nishijima Y, Kaifu K, Hara T, Matsumoto S, Ichimura A, Ohsaki H, Hitomi H, Kawachi H, Hayden MR, Whaley-Connell A, Sowers JR, Ito S, Kohno M, Nishiyama A: Early treatment with olmesartan prevents juxtamedullary glomerular podocyte injury and the onset of microalbuminuria in type 2 diabetic rats. Am J Hypertens 2012;25:604-611.
19. Ihara G, Kiyomoto H, Kobori H, Nagai Y, Ohashi N, Hitomi H, Nakano D, Pelisch N, Hara T, Mori T, Ito S, Kohno M, Nishiyama A: Regression of superficial glomerular podocyte injury in type 2 diabetic rats with overt albuminuria: effect of angiotensin II blockade. J Hypertens 2010;28:2289-2298.
20. Izuhara Y, Nangaku M, Inagi R, Tominaga N, Aizawa T, Kurokawa K, van Ypersele de Strihou C, Miyata T: Renoprotective properties of angiotensin receptor blockers beyond blood pressure lowering. J Am Soc Nephrol 2005;16:3631-3641.
21. Rafiq K, Nishiyama A, Konishi Y, Morikawa T, Kitabayashi C, Kohno M, Masaki T, Mori H, Kobori H, Imanishi M: Regression of glomerular and tubulointerstitial injuries by dietary salt reduction with combination therapy of angiotensin II receptor blocker and calcium channel blocker in Dahl salt-sensitive rats. PLoS One 2014;9:e107853.
22. Huang CY, Kuo WW, Yeh YL, Ho TJ, Lin JY, Lin DY, Chu CH, Tsai FJ, Tsai CH, Huang CY: ANG II promotes IGF-IIR expression and cardiomyocyte apoptosis by inhibiting HSF1 via JNK activation and SIRT1 degradation. Cell Death Differ 2014;21:1262-1274.
23. Yeung F, Hoberg JE, Ramsey CS, Keller MD, Jones DR, Frye RA, Mayo MW: Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J 2004;23:2369-2380.
24. Rodgers JT, Lerin C, Haas W, Gygi SP, Spiegelman BM, Puigserver P: Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature 2005;434:113-118.
25. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, Messadeq N, Milne J, Lambert P, Elliott P, Geny B, Laakso M, Puigserver P, Auwerx J: Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell 2006;127:1109-1122.
26. Papadimitriou A, Silva KC, Peixoto EB, Borges CM, Lopes de Faria JM, Lopes de Faria JB: Theobromine increases NAD(+)/Sirt-1 activity and protects the kidney under diabetic conditions. Am J Physiol Renal Physiol 2015;308:F209-225.
27. Leehey DJ, Zhang JH, Emanuele NV, Whaley-Connell A, Palevsky PM, Reilly RF, Guarino P, Fried LF, Group VN-DS: BP and Renal Outcomes in Diabetic Kidney Disease: The Veterans Affairs Nephropathy in Diabetes Trial. Clin J Am Soc Nephrol 2015;10:2159-2169.
28. Sternlicht H, Bakris GL: Management of Hypertension in Diabetic Nephropathy: How Low Should We Go? Blood Purif 2016;41:139-143.
29. Mima A, Arai H, Matsubara T, Abe H, Nagai K, Tamura Y, Torikoshi K, Araki M, Kanamori H, Takahashi T, Tominaga T, Matsuura M, Iehara N, Fukatsu A, Kita T, Doi T: Urinary Smad1 is a novel marker to predict later onset of mesangial matrix expansion in diabetic nephropathy. Diabetes 2008;57:1712-1722.
30. Adhikary L, Chow F, Nikolic-Paterson DJ, Stambe C, Dowling J, Atkins RC, Tesch GH: Abnormal p38 mitogen-activated protein kinase signalling in human and experimental diabetic nephropathy. Diabetologia 2004;47:1210-1222.
31. Hong EH, Lee SJ, Kim JS, Lee KH, Um HD, Kim JH, Kim SJ, Kim JI, Hwang SG: Ionizing radiation induces cellular senescence of articular chondrocytes via negative regulation of SIRT1 by p38 kinase. J Biol Chem 2010;285:1283-1295.
32. Tsiani E, Lekas P, Fantus IG, Dlugosz J, Whiteside C: High glucose-enhanced activation of mesangial cell p38 MAPK by ET-1, ANG II, and platelet-derived growth factor. Am J Physiol Endocrinol Metab 2002;282:E161-169.
33. Wilmer WA, Dixon CL, Hebert C: Chronic exposure of human mesangial cells to high glucose environments activates the p38 MAPK pathway. Kidney Int 2001;60:858-871.
34. Yuan Q, Zhou QY, Liu D, Yu L, Zhan L, Li XJ, Peng HY, Zhang XL, Yuan XC: Advanced glycation end-products impair Na(+)/K(+)-ATPase activity in diabetic cardiomyopathy: role of the adenosine monophosphate-activated protein kinase/sirtuin 1 pathway. Clin Exp Pharmacol Physiol 2014;41:127-133.
35. Lee MJ, Feliers D, Sataranatarajan K, Mariappan MM, Li M, Barnes JL, Choudhury GG, Kasinath BS: Resveratrol ameliorates high glucose-induced protein synthesis in glomerular epithelial cells. Cell Signal 2010;22:65-70.
36. Lee MJ, Feliers D, Mariappan MM, Sataranatarajan K, Mahimainathan L, Musi N, Foretz M, Viollet B, Weinberg JM, Choudhury GG, Kasinath BS: A role for AMP-activated protein kinase in diabetes-induced renal hypertrophy. Am J Physiol Renal Physiol 2007;292:F617-627.
37. Hawley SA, Davison M, Woods A, Davies SP, Beri RK, Carling D, Hardie DG: Characterization of the AMP-activated protein kinase kinase from rat liver and identification of threonine 172 as the major site at which it phosphorylates AMP-activated protein kinase. J Biol Chem 1996;271:27879-27887.
38. Kitada M, Kume S, Imaizumi N, Koya D: Resveratrol improves oxidative stress and protects against diabetic nephropathy through normalization of Mn-SOD dysfunction in AMPK/SIRT1-independent pathway. Diabetes 2011;60:634-643.
39. Choi JY, Ha TS, Park HY, Ahn HY: Angiotensin II suppresses adenosine monophosphate-activated protein kinase of podocytes via angiotensin II type 1 receptor and mitogen-activated protein kinase signaling. Clin Exp Nephrol 2013;17:16-23.
40. Shiota A, Shimabukuro M, Fukuda D, Soeki T, Sato H, Uematsu E, Hirata Y, Kurobe H, Maeda N, Sakaue H, Masuzaki H, Shimomura I, Sata M: Telmisartan ameliorates insulin sensitivity by activating the AMPK/SIRT1 pathway in skeletal muscle of obese db/db mice. Cardiovasc Diabetol 2012;11:139.