The role of SIRT1 in diabetic kidney disease

Frontiers in Endocrinology

Volumn 5, Issue OCT, 2014, Pages

  Yacoub, Rabi ^a   Lee, Kyung ^a   He, John Cijiang ^a  

^a MOUNT SINAI SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Autophagy; Deacetylation; Diabetes mellitus; Diabetic kidney disease; Senescence; SIRT1; Sirtuin

Indexed keywords

SIRTUIN 1;

ADIPOSE TISSUE; ANGIOGENESIS; APOPTOSIS; AUTOPHAGY; CELL DAMAGE; CELL PROTECTION; DIABETES MELLITUS; DIABETIC KIDNEY DISEASE; ENDOTHELIUM CELL; HUMAN; HYPERGLYCEMIA; INFLAMMATION; INSULIN BLOOD LEVEL; KIDNEY DISEASE; KIDNEY FIBROSIS; KIDNEY MEDULLA; LIPID METABOLISM; MESANGIUM CELL; NONHUMAN; OXIDATIVE STRESS; PODOCYTE; PROTEIN EXPRESSION; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; SENESCENCE; SHORT SURVEY;

EID: 84929176985     PISSN: None     EISSN: 16642392     Source Type: Journal    
DOI: 10.3389/fendo.2014.00166     Document Type: Short Survey

References (91)

1. Danaei G, Finucane MM, Lu Y, Singh GM, Cowan MJ, Paciorek CJ, et al. National, regional, and global trends in fasting plasma glucose and diabetes prevalence since 1980: systematic analysis of health examination surveys and epidemiological studies with 370 country-years and 2.7 million participants. Lancet (2011) 378(9785):31-40. doi: 10.1016/S0140-6736(11)60679-X
2. Mauer M, Zinman B, Gardiner R, Suissa S, Sinaiko A, Strand T, et al. Renal and retinal effects of enalapril and losartan in type 1 diabetes. N Engl J Med (2009) 361(1):40-51. doi:10.1056/NEJMoa0808400
3. Foley RN, Collins AJ. End-stage renal disease in the United States: an update from the United States Renal Data System. J Am Soc Nephrol (2007) 18(10):2644-8. doi:10.1681/ASN.2007020220
4. Mori J, Patel VB, Ramprasath T, Alrob OA, DesAulniers J, Scholey JW, et al. Angiotensin 1-7 mediates renoprotection against diabetic nephropathy by reducing oxidative stress, inflammation, and lipotoxicity. Am J Physiol Renal Physiol (2014) 306(8):F812-21. doi:10.1152/ajprenal.00655.2013
5. Susztak K, Raff AC, Schiffer M, Bottinger EP. Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes (2006) 55(1):225-33. doi:10.2337/diabetes.55.01.06.db05-0894
6. Chuang PY, Yu Q, Fang W, Uribarri J, He JC. Advanced glycation endproducts induce podocyte apoptosis by activation of the FOXO4 transcription factor. Kidney Int (2007) 72(8):965-76. doi:10.1038/sj.ki.5002456
7. Sinclair DA, Guarente L. Extrachromosomal rDNA circles - a cause of aging in yeast. Cell (1997) 91(7):1033-42. doi:10.1016/S0092-8674(00)80493-6
8. Kaeberlein M, McVey M, Guarente L. The SIR2/3/4 complex and SIR2 alone promote longevity in Saccharomyces cerevisiae by two different mechanisms. Genes Dev (1999) 13(19):2570-80. doi:10.1101/gad.13.19.2570
9. Cohen HY, Miller C, Bitterman KJ, Wall NR, Hekking B, Kessler B, et al. Calorie restriction promotes mammalian cell survival by inducing the SIRT1 deacetylase. Science (2004) 305(5682):390-2. doi:10.1126/science.1099196
10. 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(7029):113-8. doi:10.1038/nature03354
11. Bordone L, Cohen D, Robinson A, Motta MC, van Veen E, Czopik A, et al. SIRT1 transgenic mice show phenotypes resembling calorie restriction. Aging Cell (2007) 6(6):759-67. doi:10.1111/j.1474-9726.2007.00335.x
12. Kume S, Uzu T, Horiike K, Chin-Kanasaki M, Isshiki K, Araki S, et al. Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. J Clin Invest (2010) 120(4):1043-55. doi:10.1172/JCI41376
13. Vaziri H, Dessain SK, Ng Eaton E, Imai SI, Frye RA, Pandita TK, et al. hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell (2001) 107(2):149-59. doi:10.1016/S0092-8674(01)00527-X
14. Guarente L. Sir2 links chromatin silencing, metabolism, and aging. Genes Dev (2000) 14(9):1021-6. doi:10.1101/gad.14.9.1021
15. Nath KA. The role of Sirt1 in renal rejuvenation and resistance to stress. J Clin Invest (2010) 120(4):1026-8. doi:10.1172/JCI42184
16. Barzilai N, Huffman DM, Muzumdar RH, Bartke A. The critical role of metabolic pathways in aging. Diabetes (2012) 61(6):1315-22. doi:10.2337/db11-1300
17. Hiona A, Sanz A, Kujoth GC, Pamplona R, Seo AY, Hofer T, et al. Mitochondrial DNA mutations induce mitochondrial dysfunction, apoptosis and sarcopenia in skeletal muscle of mitochondrial DNA mutator mice. PLoS One (2010) 5(7):e11468. doi:10.1371/journal.pone.0011468
18. Valle I, Alvarez-Barrientos A, Arza E, Lamas S, Monsalve M. PGC-1alpha regulates the mitochondrial antioxidant defense system in vascular endothelial cells. Cardiovasc Res (2005) 66(3):562-73. doi:10.1016/j.cardiores.2005.01.026
19. Xu Q, Xia P, Li X, Wang W, Liu Z, Gao X. Tetramethylpyrazine ameliorates high glucose-induced endothelial dysfunction by increasing mitochondrial biogenesis. PLoS One (2014) 9(2):e88243. doi:10.1371/journal.pone.0088243
20. Higashida K, Kim SH, Jung SR, Asaka M, Holloszy JO, Han DH. Effects of resveratrol and SIRT1 on PGC-1alpha activity and mitochondrial biogenesis: a reevaluation. PLoS Biol (2013) 11(7):e1001603. doi:10.1371/journal.pbio.1001603
21. Lagouge M, Argmann C, Gerhart-Hines Z, Meziane H, Lerin C, Daussin F, et al. Resveratrol improves mitochondrial function and protects against metabolic disease by activating SIRT1 and PGC-1alpha. Cell (2006) 127(6):1109-22. doi:10.1016/j.cell.2006.11.013
22. Menini S, Amadio L, Oddi G, Ricci C, Pesce C, Pugliese F, et al. Deletion of p66Shc longevity gene protects against experimental diabetic glomerulopathy by preventing diabetes-induced oxidative stress. Diabetes (2006) 55(6):1642-50. doi:10.2337/db05-1477
23. Ventura A, Luzi L, Pacini S, Baldari CT, Pelicci PG. The p66Shc longevity gene is silenced through epigenetic modifications of an alternative promoter. J Biol Chem (2002) 277(25):22370-6. doi:10.1074/jbc.M200280200
24. Vashistha H, Meggs L. Diabetic nephropathy: lessons from the mouse. Ochsner J (2013) 13(1):140-6. doi:10.1043/1524-5012-13.1.140
25. Vashistha H, Singhal PC, Malhotra A, Husain M, Mathieson P, Saleem MA, et al. Null mutations at the p66 and bradykinin 2 receptor loci induce divergent phenotypes in the diabetic kidney. Am J Physiol Renal Physiol (2012) 303(12):F1629-40. doi:10.1152/ajprenal.00246.2012
26. Zhou S, Chen HZ, Wan YZ, Zhang QJ, Wei YS, Huang S, et al. Repression of P66Shc expression by SIRT1 contributes to the prevention of hyperglycemia-induced endothelial dysfunction. Circ Res (2011) 109(6):639-48. doi:10.1161/CIRCRESAHA.111.243592
27. Marino G, Niso-Santano M, Baehrecke EH, Kroemer G. Self-consumption: the interplay of autophagy and apoptosis. Nat Rev Mol Cell Biol (2014) 15(2):81-94. doi:10.1038/nrm3735
28. Maiuri MC, Zalckvar E, Kimchi A, Kroemer G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat Rev Mol Cell Biol (2007) 8(9):741-52. doi:10.1038/nrm2239
29. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, et al. A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. Proc Natl Acad Sci USA (2008) 105(9):3374-9. doi:10.1073/pnas.0712145105
30. Hiromura K, Pippin JW, Fero ML, Roberts JM, Shankland SJ. Modulation of apoptosis by the cyclin-dependent kinase inhibitor p27(Kip1). J Clin Invest (1999) 103(5):597-604. doi:10.1172/JCI5461
31. Kitada M, Kume S, Takeda-Watanabe A, Kanasaki K, Koya D. Sirtuins and renal diseases: relationship with aging and diabetic nephropathy. Clin Sci (2013) 124(3):153-64. doi:10.1042/CS20120190
32. Tasdemir E, Maiuri MC, Galluzzi L, Vitale I, Djavaheri-Mergny M, D'Amelio M, et al. Regulation of autophagy by cytoplasmic p53. Nat Cell Biol (2008) 10(6):676-87. doi:10.1038/ncb1730
33. Salminen A, Kaarniranta K. SIRT1: regulation of longevity via autophagy. Cell Signal (2009) 21(9):1356-60. doi:10.1016/j.cellsig.2009.02.014
34. Picard F, Kurtev M, Chung N, Topark-Ngarm A, Senawong T, Machado De Oliveira R, et al. Sirt1 promotes fat mobilization in white adipocytes by repressing PPAR-gamma. Nature (2004) 429(6993):771-6. doi:10.1038/nature02583
35. Qiang L, Wang L, Kon N, Zhao W, Lee S, Zhang Y, et al. Brown remodeling of white adipose tissue by SirT1-dependent deacetylation of Ppargamma. Cell (2012) 150(3):620-32. doi:10.1016/j.cell.2012.06.027
36. Gesta S, Tseng YH, Kahn CR. Developmental origin of fat: tracking obesity to its source. Cell (2007) 131(2):242-56. doi:10.1016/j.cell.2007.10.004
37. Seale P, Conroe HM, Estall J, Kajimura S, Frontini A, Ishibashi J, et al. Prdm16 determines the thermogenic program of subcutaneous white adipose tissue in mice. J Clin Invest (2011) 121(1):96-105. doi:10.1172/JCI44271
38. Inzucchi SE, Bergenstal RM, Buse JB, Diamant M, Ferrannini E, Nauck M, et al. Management of hyperglycemia in type 2 diabetes: a patient-centered approach: position statement of the American Diabetes Association (ADA) and the European Association for the Study of Diabetes (EASD). Diabetes Care (2012) 35(6):1364-79. doi:10.2337/dc12-0413
39. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, et al. SIRT1 is required for AMPK activation and the beneficial effects of resveratrol on mitochondrial function. Cell Metab (2012) 15(5):675-90. doi:10.1016/j.cmet.2012.04.003
40. Hallows WC, Yu W, Denu JM. Regulation of glycolytic enzyme phosphoglycerate mutase-1 by Sirt1 protein-mediated deacetylation. J Biol Chem (2012) 287(6):3850-8. doi:10.1074/jbc.M111.317404
41. Purushotham A, Schug TT, Xu Q, Surapureddi S, Guo X, Li X. Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab (2009) 9(4):327-38. doi:10.1016/j.cmet.2009.02.006
42. Moynihan KA, Grimm AA, Plueger MM, Bernal-Mizrachi E, Ford E, Cras-Meneur C, et al. Increased dosage of mammalian Sir2 in pancreatic beta cells enhances glucose-stimulated insulin secretion in mice. Cell Metab (2005) 2(2):105-17. doi:10.1016/j.cmet.2005.07.001
43. Canto C, Gerhart-Hines Z, Feige JN, Lagouge M, Noriega L, Milne JC, et al. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature (2009) 458(7241):1056-60. doi:10.1038/nature07813
44. Clarke NE, Belyaev ND, Lambert DW, Turner AJ. Epigenetic regulation of angiotensin-converting enzyme 2 (ACE2) by SIRT1 under conditions of cell energy stress. Clin Sci (2014) 126(7):507-16. doi:10.1042/CS20130291
45. Wang RH, Kim HS, Xiao C, Xu X, Gavrilova O, Deng CX. Hepatic Sirt1 deficiency in mice impairs mTorc2/Akt signaling and results in hyperglycemia, oxidative damage, and insulin resistance. J Clin Invest (2011) 121(11):4477-90. doi:10.1172/JCI46243
46. Sun C, Zhang F, Ge X, Yan T, Chen X, Shi X, et al. SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metab (2007) 6(4):307-19. doi:10.1016/j.cmet.2007.08.014
47. Zhang J. The direct involvement of SirT1 in insulin-induced insulin receptor substrate-2 tyrosine phosphorylation. J Biol Chem (2007) 282(47):34356-64. doi:10.1074/jbc.M706644200
48. Chuang PY, Dai Y, Liu R, He H, Kretzler M, Jim B, et al. Alteration of forkhead box O (foxo4) acetylation mediates apoptosis of podocytes in diabetes mellitus. PLoS One (2011) 6(8):e23566. doi:10.1371/journal.pone.0023566
49. Hasegawa K, Wakino S, Simic P, Sakamaki Y, Minakuchi H, Fujimura K, et al. Renal tubular Sirt1 attenuates diabetic albuminuria by epigenetically suppressing Claudin-1 overexpression in podocytes. Nat Med (2013) 19(11):1496-504. doi:10.1038/nm.3363
50. Li J, Qu X, Ricardo SD, Bertram JF, Nikolic-Paterson DJ. Resveratrol inhibits renal fibrosis in the obstructed kidney: potential role in deacetylation of Smad3. Am J Pathol (2010) 177(3):1065-71. doi:10.2353/ajpath.2010.090923
51. Kume S, Haneda M, Kanasaki K, Sugimoto T, Araki S, Isshiki K, et al. SIRT1 inhibits transforming growth factor beta-induced apoptosis in glomerular mesangial cells via Smad7 deacetylation. J Biol Chem (2007) 282(1):151-8. doi:10.1074/jbc.M605904200
52. Kume S, Haneda M, Kanasaki K, Sugimoto T, Araki S, Isono M, et al. Silent information regulator 2 (SIRT1) attenuates oxidative stress-induced mesangial cell apoptosis via p53 deacetylation. Free Radic Biol Med (2006) 40(12):2175-82. doi:10.1016/j.freeradbiomed.2006.02.014
53. Zhuo L, Fu B, Bai X, Zhang B, Wu L, Cui J, et al. NAD blocks high glucose induced mesangial hypertrophy via activation of the sirtuins-AMPK-mTOR pathway. Cell Physiol Biochem (2011) 27(6):681-90. doi:10.1159/000330077
54. He W, Wang Y, Zhang MZ, You L, Davis LS, Fan H, et al. Sirt1 activation protects the mouse renal medulla from oxidative injury. J Clin Invest (2010) 120(4):1056-68. doi:10.1172/JCI41563
55. Zhang D, Li S, Cruz P, Kone BC. Sirtuin 1 functionally and physically interacts with disruptor of telomeric silencing-1 to regulate alpha-ENaC transcription in collecting duct. J Biol Chem (2009) 284(31):20917-26. doi:10.1074/jbc.M109.020073
56. Vasko R, Xavier S, Chen J, Lin CH, Ratliff B, Rabadi M, et al. Endothelial sirtuin 1 deficiency perpetrates nephrosclerosis through downregulation of matrix metalloproteinase-14: relevance to fibrosis of vascular senescence. J Am Soc Nephrol (2014) 25(2):276-91. doi:10.1681/ASN.2013010069
57. Wen D, Huang X, Zhang M, Zhang L, Chen J, Gu Y, et al. Resveratrol attenuates diabetic nephropathy via modulating angiogenesis. PLoS One (2013) 8(12):e82336. doi:10.1371/journal.pone.0082336
58. Miyazaki R, Ichiki T, Hashimoto T, Inanaga K, Imayama I, Sadoshima J, et al. SIRT1, a longevity gene, downregulates angiotensin II type 1 receptor expression in vascular smooth muscle cells. Arterioscler Thromb Vasc Biol (2008) 28(7):1263-9. doi:10.1161/ATVBAHA.108.166991
59. Kitada M, Takeda A, Nagai T, Ito H, Kanasaki K, Koya D. Dietary restriction ameliorates diabetic nephropathy through anti-inflammatory effects and regulation of the autophagy via restoration of Sirt1 in diabetic Wistar fatty (fa/fa) rats: a model of type 2 diabetes. Exp Diabetes Res (2011) 2011:908185. doi:10.1155/2011/908185
60. Matsusaka T, Sandgren E, Shintani A, Kon V, Pastan I, Fogo AB, et al. Podocyte injury damages other podocytes. J Am Soc Nephrol (2011) 22(7):1275-85. doi:10.1681/ASN.2010090963
61. Mundel P, Shankland SJ. Podocyte biology and response to injury. J Am Soc Nephrol (2002) 13(12):3005-15. doi:10.1097/01.ASN.0000039661.06947.FD
62. Eid AA, Gorin Y, Fagg BM, Maalouf R, Barnes JL, Block K, et al. Mechanisms of podocyte injury in diabetes: role of cytochrome P450 and NADPH oxidases. Diabetes (2009) 58(5):1201-11. doi:10.2337/db08-1536
63. Nihalani D, Susztak K. Sirt1-Claudin-1 crosstalk regulates renal function. Nat Med (2013) 19(11):1371-2. doi:10.1038/nm.3386
64. Yoshino J, Mills KF, Yoon MJ, Imai S. Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab (2011) 14(4):528-36. doi:10.1016/j.cmet.2011.08.014
65. Thomas MC, Tikellis C, Kantharidis P, Burns WC, Cooper ME, Forbes JM. The role of advanced glycation in reduced organic cation transport associated with experimental diabetes. J Pharmacol Exp Ther (2004) 311(2):456-66. doi:10.1124/jpet.104.070672
66. Chou SY, Porush JG, Faubert PF. Renal medullary circulation: hormonal control. Kidney Int (1990) 37(1):1-13. doi:10.1038/ki.1990.1
67. Brezis M, Rosen S. Hypoxia of the renal medulla - its implications for disease. N Engl J Med (1995) 332(10):647-55. doi:10.1056/NEJM199503093321006
68. Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW. Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol Cell (2010) 38(6):864-78. doi:10.1016/j.molcel.2010.05.023
69. Kim JW, Tchernyshyov I, Semenza GL, Dang CV. HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab (2006) 3(3):177-85. doi:10.1016/j.cmet.2006.02.002
70. Rane S, He M, Sayed D, Vashistha H, Malhotra A, Sadoshima J, et al. Downregulation of miR-199a derepresses hypoxia-inducible factor-1alpha and Sirtuin 1 and recapitulates hypoxia preconditioning in cardiac myocytes. Circ Res (2009) 104(7):879-86. doi:10.1161/CIRCRESAHA.108.193102
71. Chan AY, Dolinsky VW, Soltys CL, Viollet B, Baksh S, Light PE, et al. Resveratrol inhibits cardiac hypertrophy via AMP-activated protein kinase and Akt. J Biol Chem (2008) 283(35):24194-201. doi:10.1074/jbc.M802869200
72. Nakagawa T, Kosugi T, Haneda M, Rivard CJ, Long DA. Abnormal angiogenesis in diabetic nephropathy. Diabetes (2009) 58(7):1471-8. doi:10.2337/db09-0119
73. Cooper ME, Vranes D, Youssef S, Stacker SA, Cox AJ, Rizkalla B, et al. Increased renal expression of vascular endothelial growth factor (VEGF) and its receptor VEGFR-2 in experimental diabetes. Diabetes (1999) 48(11):2229-39. doi:10.2337/diabetes.48.11.2229
74. Hohenstein B, Hausknecht B, Boehmer K, Riess R, Brekken RA, Hugo CP. Local VEGF activity but not VEGF expression is tightly regulated during diabetic nephropathy in man. Kidney Int (2006) 69(9):1654-61. doi:10.1038/sj.ki.5000294
75. Suri C, Jones PF, Patan S, Bartunkova S, Maisonpierre PC, Davis S, et al. Requisite role of angiopoietin-1, a ligand for the TIE2 receptor, during embryonic angiogenesis. Cell (1996) 87(7):1171-80. doi:10.1016/S0092-8674(00)81813-9
76. Maisonpierre PC, Suri C, Jones PF, Bartunkova S, Wiegand SJ, Radziejewski C, et al. Angiopoietin-2, a natural antagonist for Tie2 that disrupts in vivo angiogenesis. Science (1997) 277(5322):55-60. doi:10.1126/science.277.5322.55
77. Mortuza R, Chen S, Feng B, Sen S, Chakrabarti S. High glucose induced alteration of SIRTs in endothelial cells causes rapid aging in a p300 and FOXO regulated pathway. PLoS One (2013) 8(1):e54514. doi:10.1371/journal.pone.0054514
78. Wada J, Makino H. Inflammation and the pathogenesis of diabetic nephropathy. Clin Sci (2013) 124(3):139-52. doi:10.1042/CS20120198
79. Sato M, Muragaki Y, Saika S, Roberts AB, Ooshima A. Targeted disruption of TGF-beta1/Smad3 signaling protects against renal tubulointerstitial fibrosis induced by unilateral ureteral obstruction. J Clin Invest (2003) 112(10):1486-94. doi:10.1172/JCI19270
80. Simonsson M, Kanduri M, Gronroos E, Heldin CH, Ericsson J. The DNA binding activities of Smad2 and Smad3 are regulated by coactivator-mediated acetylation. J Biol Chem (2006) 281(52):39870-80. doi:10.1074/jbc.M607868200
81. Inoue Y, Itoh Y, Abe K, Okamoto T, Daitoku H, Fukamizu A, et al. Smad3 is acetylated by p300/CBP to regulate its transactivation activity. Oncogene (2007) 26(4):500-8. doi:10.1038/sj.onc.1209826
82. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, et al. Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. N Engl J Med (2001) 345(12):861-9. doi:10.1056/NEJMoa011161
83. Terada Y, Kuwana H, Kobayashi T, Okado T, Suzuki N, Yoshimoto T, et al. Aldosterone-stimulated SGK1 activity mediates profibrotic signaling in the mesangium. J Am Soc Nephrol (2008) 19(2):298-309. doi:10.1681/ASN.2007050531
84. Panchapakesan U, Pollock C, Saad S. Renal epidermal growth factor receptor: its role in sodium and water homeostasis in diabetic nephropathy. Clin Exp Pharmacol Physiol (2011) 38(2):84-8. doi:10.1111/j.1440-1681.2010.05472.x
85. Hills CE, Bland R, Bennett J, Ronco PM, Squires PE. High glucose up-regulates ENaC and SGK1 expression in HCD-cells. Cell Physiol Biochem (2006) 18(6):337-46. doi:10.1159/000097611
86. Chen KH, Hung CC, Hsu HH, Jing YH, Yang CW, Chen JK. Resveratrol ameliorates early diabetic nephropathy associated with suppression of augmented TGF-beta/smad and ERK1/2 signaling in streptozotocin-induced diabetic rats. Chem Biol Interact (2011) 190(1):45-53. doi:10.1016/j.cbi.2011.01.033
87. Lee MJ, Feliers D, Sataranatarajan K, Mariappan MM, Li M, Barnes JL, et al. Resveratrol ameliorates high glucose-induced protein synthesis in glomerular epithelial cells. Cell Signal (2010) 22(1):65-70. doi:10.1016/j.cellsig.2009.09.011
88. Tikoo K, Singh K, Kabra D, Sharma V, Gaikwad A. Change in histone H3 phosphorylation, MAP kinase p38, SIR 2 and p53 expression by resveratrol in preventing streptozotocin induced type I diabetic nephropathy. Free Radic Res (2008) 42(4):397-404. doi:10.1080/10715760801998646
89. Wu L, Zhang Y, Ma X, Zhang N, Qin G. The effect of resveratrol on FoxO1 expression in kidneys of diabetic nephropathy rats. Mol Biol Rep (2012) 39(9):9085-93. doi:10.1007/s11033-012-1780-z
90. Xu Y, Nie L, Yin YG, Tang JL, Zhou JY, Li DD, et al. Resveratrol protects against hyperglycemia-induced oxidative damage to mitochondria by activating SIRT1 in rat mesangial cells. Toxicol Appl Pharmacol (2012) 259(3):395-401. doi:10.1016/j.taap.2011.09.028
91. Maeda S, Koya D, Araki S, Babazono T, Umezono T, Toyoda M, et al. Association between single nucleotide polymorphisms within genes encoding sirtuin families and diabetic nephropathy in Japanese subjects with type 2 diabetes. Clin Exp Nephrol (2011) 15(3):381-90. doi:10.1007/s10157-011-0418-0