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Molecular Medicine

, Volume 21, Issue 1, pp 87–97 | Cite as

Sirtuin 1: A Target for Kidney Diseases

  • Lili Kong
  • Hao Wu
  • Wenhua Zhou
  • Manyu Luo
  • Yi Tan
  • Lining Miao
  • Lu Cai
Review Article

Abstract

Sirtuin 1 (SIRT1) is an evolutionary conserved NAD+-dependent histone deacetylase that is necessary for caloric restriction-related lifespan extension. SIRT1, as an intracellular energy sensor, detects the concentration of intracellular NAD+ and uses this information to adapt cellular energy output to cellular energy requirements. Previous studies on SIRT1 have confirmed its beneficial effects on cellular immunity to oxidative stress, reduction of fibrosis, suppression of inflammation, inhibition of apoptosis, regulation of metabolism, induction of autophagy and regulation of blood pressure. All of the above biological processes are involved in the pathogenesis of kidney diseases. Therefore, the activation of SIRT1 may become a therapeutic target to improve the clinical outcome of kidney diseases. In this review, we give an overview of SIRT1 and its molecular targets as well as SIRT1-modulated biological processes, with a particular focus on the role of SIRT1 in kidney diseases.

Notes

Acknowledgments

The citations from the authors group were supported in part by the National Science Foundation of China (81170669 to L Miao) and the National Institutes of Health (1R01DK 091338-01A1 to L Cai). We would like to thank Amy Y Cai for assistance in making the figures for this manuscript. We would also like to express our gratitude to all the scientists participating in this work.

References

  1. 1.
    Bahari-Javan S, Sananbenesi F, Fischer A. (2014) Histone-acetylation: a link between Alzheimer’s disease and post-traumatic stress disorder? Front. Neurosci. 8:160.PubMedPubMedCentralCrossRefGoogle Scholar
  2. 2.
    Bassett SA, Barnett MP. (2014) The role of dietary histone deacetylases (HDACs) inhibitors in health and disease. Nutrients. 6:4273–301.PubMedPubMedCentralCrossRefGoogle Scholar
  3. 3.
    Yuan H, et al. (2013) Involvement of p300/CBP and epigenetic histone acetylation in TGF-beta1-mediated gene transcription in mesangial cells. Am. J. Physiol. Renal. Physiol. 304:F601–13.PubMedCrossRefGoogle Scholar
  4. 4.
    Li Y, et al. (2014) Novel role of silent information regulator 1 in acute endothelial cell oxidative stress injury. Biochim. Biophys. Acta. 1842:2246–56.PubMedCrossRefGoogle Scholar
  5. 5.
    Bugyei-Twum A, et al. (2014) High glucose induces Smad activation via the transcriptional coregulator p300 and contributes to cardiac fibrosis and hypertrophy. Cardiovasc. Diabetol 13:89.PubMedPubMedCentralCrossRefGoogle Scholar
  6. 6.
    Hwang YJ, Song J, Kim HR, Hwang KA. (2014) Oleanolic acid regulates NF-κB signaling by suppressing MafK expression in RAW 264.7 cells. BMB Rep. 47:524–9.PubMedPubMedCentralCrossRefGoogle Scholar
  7. 7.
    Lee HB, Noh H, Seo JY, Yu MR, Ha H. (2007) Histone deacetylase inhibitors: a novel class of therapeutic agents in diabetic nephropathy. Kidney Int. S61–6.CrossRefGoogle Scholar
  8. 8.
    Kume S, Thomas MC, Koya D. (2012) Nutrient sensing, autophagy, and diabetic nephropathy. Diabetes. 61:23–9.PubMedCrossRefGoogle Scholar
  9. 9.
    Michishita E, Park JY, Burneskis JM, Barrett JC, Horikawa I. (2005) Evolutionarily conserved and nonconserved cellular localizations and functions of human SIRT proteins. Mol. Biol. Cell. 16:4623–35.PubMedPubMedCentralCrossRefGoogle Scholar
  10. 10.
    Xie J, Zhang X, Zhang L. (2013) Negative regulation of inflammation by SIRT1. Pharmacol. Res. 67:60–7.PubMedCrossRefGoogle Scholar
  11. 11.
    Fuks F. (2005) DNA methylation and histone modifications: teaming up to silence genes. Curr. Opin. Genet. Dev. 15:490–5.PubMedCrossRefGoogle Scholar
  12. 12.
    Hasegawa K, et al. (2013) Renal tubular SIRT1 attenuates diabetic albuminuria by epigenetically suppressing Claudin-1 overexpression in podocytes. Nat. Med. 19:1496–504.PubMedPubMedCentralCrossRefGoogle Scholar
  13. 13.
    Rea S, et al. (2000) Regulation of chromatin structure by site-specific histone H3 methyltransferases. Nature. 406:593–9.PubMedCrossRefGoogle Scholar
  14. 14.
    Martin C, Zhang Y. (2005) The diverse functions of histone lysine methylation. Nat. Rev. Mol. Cell. Biol. 6:838–49.PubMedCrossRefGoogle Scholar
  15. 15.
    Vaziri H, et al. (2001) hSIR2(SIRT1) functions as an NAD-dependent p53 deacetylase. Cell. 107:149–59.PubMedCrossRefGoogle Scholar
  16. 16.
    Yeung F, et al. (2004) Modulation of NF-kappaB-dependent transcription and cell survival by the SIRT1 deacetylase. EMBO J. 23:2369–80.PubMedPubMedCentralCrossRefGoogle Scholar
  17. 17.
    Sadoul K, Boyault C, Pabion M, Khochbin S. (2008) Regulation of protein turnover by acetyltransferases and deacetylases. Biochimie. 90:306–12.PubMedCrossRefGoogle Scholar
  18. 18.
    Wang C, Tian L, Popov VM, Pestell RG. (2011) Acetylation and nuclear receptor action. J. Steroid. Biochem. Mol. Biol. 123:91–100.PubMedCrossRefGoogle Scholar
  19. 19.
    Xiong S, Salazar G, Patrushev N, Alexander RW. (2011) FoxO1 mediates an autofeedback loop regulating SIRT1 expression. J. Biol. Chem. 286:5289–99.PubMedCrossRefGoogle Scholar
  20. 20.
    Xu F, et al. (2014) Resveratrol prevention of diabetic nephropathy is associated with the suppression of renal inflammation and mesangial cell proliferation: possible roles of Akt/NF-kappaB pathway. Int. J. Endocrinol. 2014:289327.Google Scholar
  21. 21.
    Wen D, et al. (2013) Resveratrol attenuates diabetic nephropathy via modulating angiogenesis. PLoS One.8:e82336.PubMedPubMedCentralCrossRefGoogle Scholar
  22. 22.
    Elbe H, et al. (2015) Amelioration of streptozotocin-induced diabetic nephropathy by melatonin, quercetin, and resveratrol in rats. Hum. Exp. Toxicol. 34:100–13.PubMedCrossRefGoogle Scholar
  23. 23.
    Huang K, et al. (2013) SIRT1 resists advanced glycation end products-induced expressions of fibronectin and TGF-beta1 by activating the Nrf2/ARE pathway in glomerular mesangial cells. Free Radic. Biol. Med. 65:528–40.PubMedCrossRefGoogle Scholar
  24. 24.
    Gao R, et al. (2014) SIRT1 deletion leads to enhanced inflammation and aggravates endotoxin-induced acute kidney injury. PLoS One. 9:e98909.PubMedPubMedCentralCrossRefGoogle Scholar
  25. 25.
    Susztak K, Raff AC, Schiffer M, Bottinger EP. (2006) Glucose-induced reactive oxygen species cause apoptosis of podocytes and podocyte depletion at the onset of diabetic nephropathy. Diabetes. 55:225–33.PubMedCrossRefGoogle Scholar
  26. 26.
    Susztak K, Ciccone E, McCue P, Sharma K, Bottinger EP. (2005) Multiple metabolic hits converge on CD36 as novel mediator of tubular epithelial apoptosis in diabetic nephropathy. PLoS Med. 2:e45.PubMedPubMedCentralCrossRefGoogle Scholar
  27. 27.
    Bonventre JV. (2012) Can we target tubular damage to prevent renal function decline in diabetes? Semin. Nephrol. 32:452–62.PubMedPubMedCentralCrossRefGoogle Scholar
  28. 28.
    Ohse T, et al. (2010) De novo expression of podocyte proteins in parietal epithelial cells during experimental glomerular disease. Am. J. Physiol. Renal Physiol. 298:F702–11.PubMedCrossRefGoogle Scholar
  29. 29.
    Zhang J, et al. (2012) De novo expression of podocyte proteins in parietal epithelial cells in experimental aging nephropathy. Am. J. Physiol. Renal Physiol. 302:F571–80.PubMedCrossRefGoogle Scholar
  30. 30.
    Koda R, et al. (2014) Expression of tight junction protein claudin-1 in human crescentic glomerulonephritis. Int. J. Nephrol. 2014:598670.Google Scholar
  31. 31.
    Kim D, et al. (2014) Tamoxifen ameliorates renal tubulointerstitial fibrosis by modulation of estrogen receptor alpha-mediated transforming growth factor-beta1/Smad signaling pathway. Nephrol. Dial. Transplant. 29:2043–53.PubMedCrossRefGoogle Scholar
  32. 32.
    Wei J, et al. (2013) Knockdown of thioredoxin-interacting protein ameliorates high glucose-induced epithelial to mesenchymal transition in renal tubular epithelial cells. Cell Signal. 25:2788–96.PubMedCrossRefGoogle Scholar
  33. 33.
    Das R, et al. (2014) Upregulation of mitochondrial Nox4 mediates TGF-beta-induced apoptosis in cultured mouse podocytes. Am. J. Physiol. Renal Physiol. 306:F155–67.PubMedCrossRefGoogle Scholar
  34. 34.
    Samarakoon R, et al. (2013) Induction of renal fibrotic genes by TGF-beta1 requires EGFR activation, p53 and reactive oxygen species. Cell Signal. 25:2198–209.PubMedCrossRefGoogle Scholar
  35. 35.
    Yao Q, et al. (2008) The role of the TGF/Smad signaling pathway in peritoneal fibrosis induced by peritoneal dialysis solutions. Nephron Exp. Nephrol. 109:e71–8.PubMedCrossRefGoogle Scholar
  36. 36.
    Koutroutsos K, et al. (2014) Effect of Smad pathway activation on podocyte cell cycle regulation: an immunohistochemical evaluation. Ren. Fail. 36:1310–6.PubMedCrossRefGoogle Scholar
  37. 37.
    Liang J, Tian S, Han J, Xiong P. (2014) Resveratrol as a therapeutic agent for renal fibrosis induced by unilateral ureteral obstruction. Ren. Fail. 36:285–91.PubMedCrossRefGoogle Scholar
  38. 38.
    Li J, Qu X, Ricardo SD, Bertram JF, Nikolic-Paterson DJ. (2010) Resveratrol inhibits renal fibrosis in the obstructed kidney: potential role in deacetylation of Smad3. Am. J. Pathol. 177:1065–71.PubMedPubMedCentralCrossRefGoogle Scholar
  39. 39.
    Huang XZ, et al. (2014) SIRT1 activation ameliorates renal fibrosis by inhibiting the TGF-beta/Smad3 pathway. J. Cell. Biochem. 115:996–1005.PubMedCrossRefGoogle Scholar
  40. 40.
    Simic P, et al. (2013) SIRT1 suppresses the epithelial-to-mesenchymal transition in cancer metastasis and organ fibrosis. Cell Rep. 3:1175–86.PubMedCrossRefGoogle Scholar
  41. 41.
    Jung DS, et al. (2012) Apoptosis occurs differentially according to glomerular size in diabetic kidney disease. Nephrology Dialysis Transplantation. 27:259–66.CrossRefGoogle Scholar
  42. 42.
    Chen Y, et al. (2014) Down-regulation of PERK-ATF4-CHOP pathway by astragaloside IV is associated with the inhibition of endoplasmic reticulum stress-induced podocyte apoptosis in diabetic rats. Cell Physiol. Biochem. 3:1975–87.CrossRefGoogle Scholar
  43. 43.
    Peng J, et al. (2015) Hyperglycemia, p53, and mitochondrial pathway of apoptosis are involved in the susceptibility of diabetic models to ischemic acute kidney injury. Kidney Int. 87:137–50.PubMedCrossRefPubMedCentralGoogle Scholar
  44. 44.
    Wang W, et al. (2015) TRB3 mediates renal tubular cell apoptosis associated with proteinuria. Clin. Exp. Med. 15:167–77.PubMedCrossRefPubMedCentralGoogle Scholar
  45. 45.
    Kim D, et al. (2014) Ubiquitination-dependent CARM1 degradation facilitates Notch1-mediated podocyte apoptosis in diabetic nephropathy. Cell Signal. 26:1774–82.PubMedCrossRefPubMedCentralGoogle Scholar
  46. 46.
    Meek RL, et al. (2013) Glomerular cell death and inflammation with high-protein diet and diabetes. Nephrol. Dial. Transplant. 28:1711–20.PubMedPubMedCentralCrossRefGoogle Scholar
  47. 47.
    Kim DH, et al. (2011) SIRT1 activation by resveratrol ameliorates cisplatin-induced renal injury through deacetylation of p53. Am. J. Physiol. Renal Physiol. 301:F427–35.PubMedCrossRefPubMedCentralGoogle Scholar
  48. 48.
    Tikoo K, Singh K, Kabra D, Sharma V, Gaikwad A. (2008) 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. 42:397–404.PubMedCrossRefGoogle Scholar
  49. 49.
    Kume S, et al. (2007) SIRT1 inhibits transforming growth factor beta-induced apoptosis in glomerular mesangial cells via Smad7 deacetylation. J. Biol. Chem. 282:151–8.PubMedCrossRefGoogle Scholar
  50. 50.
    Hasegawa K, et al. (2008) SIRT1 protects against oxidative stress-induced renal tubular cell apoptosis by the bidirectional regulation of catalase expression. Biochem. Biophys. Res. Commun. 372:51–6.PubMedCrossRefGoogle Scholar
  51. 51.
    Chuang PY, et al. (20110 Alteration of forkhead box O (foxo4) acetylation mediates apoptosis of podocytes in diabetes mellitus. PLoS One. 6:e23566.PubMedPubMedCentralCrossRefGoogle Scholar
  52. 52.
    Gao F, et al. (2013) Notch pathway is involved in high glucose-induced apoptosis in podocytes via Bcl-2 and p53 pathways. J. Cell. Biochem. 114:1029–38.PubMedCrossRefGoogle Scholar
  53. 53.
    Menini S, et al. (2007) Increased glomerular cell (podocyte) apoptosis in rats with streptozotocin-induced diabetes mellitus: role in the development of diabetic glomerular disease. Diabetologia. 50:2591–9.PubMedCrossRefGoogle Scholar
  54. 54.
    Deshpande SD, et al. (2013) Transforming growth factor-beta-induced cross talk between p53 and a microRNA in the pathogenesis of diabetic nephropathy. Diabetes 62:3151–62.PubMedPubMedCentralCrossRefGoogle Scholar
  55. 55.
    Han SY, et al. (2006) Apoptosis by cyclosporine in mesangial cells. Trans-plant. Proc. 38:2244–6.CrossRefGoogle Scholar
  56. 56.
    Luo J, et al. (2001) Negative control of p53 by Sir2alpha promotes cell survival under stress. Cell. 107:137–48.PubMedCrossRefGoogle Scholar
  57. 57.
    Langley E, et al. (2002) Human SIR2 deacetylates p53 and antagonizes PML/p53-induced cellular senescence. EMBO J. 21:2383–96.PubMedPubMedCentralCrossRefGoogle Scholar
  58. 58.
    Brooks CL, Gu W. (2009) How does SIRT1 affect metabolism, senescence and cancer? Nat. Rev. Cancer. 9:123–8.PubMedCrossRefGoogle Scholar
  59. 59.
    Gross DN, van den Heuvel AP, Birnbaum MJ. (2008) The role of FoxO in the regulation of metabolism. Oncogene. 27:2320–36.PubMedCrossRefGoogle Scholar
  60. 60.
    Wang Y, Zhou Y, Graves DT. (2014) FOXO transcription factors: their clinical significance and regulation. Biomed. Res. Int. 2014:925350.Google Scholar
  61. 61.
    Brunet A, et al. (2004) Stress-dependent regulation of FOXO transcription factors by the SIRT1 deacetylase. Science. 303:2011–5.PubMedCrossRefGoogle Scholar
  62. 62.
    Nemoto S, Fergusson MM, Finkel T. (2004) Nutrient availability regulates SIRT1 through a fork-head-dependent pathway. Science. 306:2105–8.PubMedCrossRefGoogle Scholar
  63. 63.
    Pedruzzi LM, Stockler-Pinto MB, Leite M Jr, Mafra D. (2012) Nrf2-keap1 system versus NF-kappaB: the good and the evil in chronic kidney disease? Biochimie. 94:2461–6.PubMedCrossRefGoogle Scholar
  64. 64.
    Katto J, Engel N, Abbas W, Herbein G, Mahlknecht U. (2013) Transcription factor NFkappaB regulates the expression of the histone deacetylase SIRT1. Clin. Epigenetics. 5:11.PubMedPubMedCentralCrossRefGoogle Scholar
  65. 65.
    Hayden MS, Ghosh S. (2008) Shared principles in NF-kappaB signaling. Cell. 132:344–62.PubMedCrossRefGoogle Scholar
  66. 66.
    Lee HJ, et al. (2014) Febuxostat ameliorates diabetic renal injury in a streptozotocin-induced diabetic rat model. Am. J. Nephrol. 40:56–63.PubMedCrossRefGoogle Scholar
  67. 67.
    Roy MS, Janal MN, Crosby J, Donnelly R. (2015) Markers of endothelial dysfunction and inflammation predict progression of diabetic nephropathy in African Americans with type 1 diabetes. Kidney Int. 87:427–33.PubMedCrossRefGoogle Scholar
  68. 68.
    Jialal I, Major AM, Devaraj S. (2014) Global tolllike receptor 4 knockout results in decreased renal inflammation, fibrosis and podocytopathy. J. Diabetes Complications. 28:755–61.PubMedCrossRefGoogle Scholar
  69. 69.
    Wu H, et al. (2014) The role of MicroRNAs in diabetic nephropathy. J. Diabetes Res. 2014:920134.Google Scholar
  70. 70.
    Shimo T, et al. (2013) A novel nuclear factor kappaB inhibitor, dehydroxymethylepoxyquinomicin, ameliorates puromycin aminonucleoside-induced nephrosis in mice. Am. J. Nephrol. 37:302–9.PubMedCrossRefGoogle Scholar
  71. 71.
    Xie X, et al. (2012) Polydatin ameliorates experimental diabetes-induced fibronectin through inhibiting the activation of NF-kappaB signaling pathway in rat glomerular mesangial cells. Mol. Cell. Endocrinol. 362:183–93.PubMedCrossRefGoogle Scholar
  72. 72.
    Wu X, et al. (2012) Tanshinone IIA prevents uric acid nephropathy in rats through NF-kappaB inhibition. Planta. Med. 78:866–73.PubMedCrossRefGoogle Scholar
  73. 73.
    Machado RA, et al. (2012) Sodium butyrate decreases the activation of NF-kappaB reducing inflammation and oxidative damage in the kidney of rats subjected to contrast-induced nephropathy. Nephrol. Dial. Transplant. 27:3136–40.PubMedCrossRefGoogle Scholar
  74. 74.
    Du S, et al. (2009) Suppression of NF-kappaB by cyclosporin a and tacrolimus (FK506) via induction of the C/EBP family: implication for unfolded protein response. J. Immunol. 182:7201–11.PubMedCrossRefGoogle Scholar
  75. 75.
    Salminen A, Kauppinen A, Suuronen T, Kaarniranta K. (2008) SIRT1 longevity factor suppresses NF-kappaB -driven immune responses: regulation of aging via NF-kappaB acetylation? Bioessays. 30:939–42.PubMedCrossRefGoogle Scholar
  76. 76.
    Jung YJ, et al. (2012) SIRT1 overexpression decreases cisplatin-induced acetylation of NF-kappaB p65 subunit and cytotoxicity in renal proximal tubule cells. Biochem. Biophys. Res. Commun. 419:206–10.PubMedCrossRefGoogle Scholar
  77. 77.
    Kitada M, Takeda A, Nagai T, Ito H, Kanasaki K, Koya D. (2011) 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. 2011:908185.Google Scholar
  78. 78.
    Dvir-Ginzberg M, et al. (2011) Tumor necrosis factor alpha-mediated cleavage and inactivation of SIRT1 in human osteoarthritic chondrocytes. Arthritis Rheum. 63:2363–73.PubMedPubMedCentralCrossRefGoogle Scholar
  79. 79.
    Chalkiadaki A, Guarente L. (2012) High-fat diet triggers inflammation-induced cleavage of SIRT1 in adipose tissue to promote metabolic dysfunction. Cell Metab. 16:180–8.PubMedPubMedCentralCrossRefGoogle Scholar
  80. 80.
    Czura CJ, Wang H, Tracey KJ. (2001) Dual roles for HMGB1: DNA binding and cytokine. J. Endotoxin Res. 7:315–21.PubMedCrossRefGoogle Scholar
  81. 81.
    Andersson U, Erlandsson-Harris H, Yang H, Tracey KJ. (2002) HMGB1 as a DNA-binding cytokine. J. Leukoc. Biol. 72:1084–91.PubMedGoogle Scholar
  82. 82.
    Scaffidi P, Misteli T, Bianchi ME. (2002) Release of chromatin protein HMGB1 by necrotic cells triggers inflammation. Nature. 418:191–5.PubMedCrossRefGoogle Scholar
  83. 83.
    Karuppagounder V, et al. (2014) Resveratrol attenuates HMGB1 signaling and inflammation in house dust mite-induced atopic dermatitis in mice. Int. Immunopharmacol. 23:617–23.PubMedCrossRefGoogle Scholar
  84. 84.
    Rabadi MM, et al. (2015) High-mobility group box 1 is a novel deacetylation target of Sirtuin1. Kidney Int. 87:95–108.PubMedCrossRefGoogle Scholar
  85. 85.
    Mizushima N, Komatsu M. (2011) Autophagy: renovation of cells and tissues. Cell. 147:728–41.PubMedCrossRefGoogle Scholar
  86. 86.
    Kume S, et al. (2010) Calorie restriction enhances cell adaptation to hypoxia through SIRT1-dependent mitochondrial autophagy in mouse aged kidney. J. Clin. Invest. 120:1043–55.PubMedPubMedCentralCrossRefGoogle Scholar
  87. 87.
    Hartleben B, et al. (2010) Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. J. Clin. Invest. 120:1084–96.PubMedPubMedCentralCrossRefGoogle Scholar
  88. 88.
    Jiang M, Liu K, Luo J, Dong Z. (2010) Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. Am. J. Pathol. 176:1181–92.PubMedPubMedCentralCrossRefGoogle Scholar
  89. 89.
    Kimura T, et al. (2011) Autophagy protects the proximal tubule from degeneration and acute ischemic injury. J. Am. Soc. Nephrol. 22:902–13.PubMedPubMedCentralCrossRefGoogle Scholar
  90. 90.
    Periyasamy-Thandavan S, et al. (2008) Autophagy is cytoprotective during cisplatin injury of renal proximal tubular cells. Kidney Int. 74:631–40.PubMedCrossRefGoogle Scholar
  91. 91.
    Inoue K, et al. (2010) Cisplatin-induced macroautophagy occurs prior to apoptosis in proximal tubules in vivo. Clin. Exp. Nephrol. 14:112–22.PubMedCrossRefGoogle Scholar
  92. 92.
    Kaushal GP. (2012) Autophagy protects proximal tubular cells from injury and apoptosis. Kidney Int. 82:1250–3.PubMedPubMedCentralCrossRefGoogle Scholar
  93. 93.
    Lee IH, et al. (2008) A role for the NAD-dependent deacetylase SIRT1 in the regulation of autophagy. Proc. Natl. Acad. Sci. U. S. A. 105:3374–9.PubMedPubMedCentralCrossRefGoogle Scholar
  94. 94.
    Yamahara K, et al. (2013) The role of autophagy in the pathogenesis of diabetic nephropathy. J. Diabetes Res. 2013:193757.Google Scholar
  95. 95.
    Fang L, et al. (2013) Autophagy attenuates diabetic glomerular damage through protection of hyperglycemia-induced podocyte injury. PLoS One. 8:e60546.PubMedPubMedCentralCrossRefGoogle Scholar
  96. 96.
    Bellot G, et al. (2009) Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Mol. Cell. Biol. 29:2570–81.PubMedPubMedCentralCrossRefGoogle Scholar
  97. 97.
    Hariharan N, et al. (2010) Deacetylation of FoxO by SIRT1 plays an essential role in mediating starvation-induced autophagy in cardiac myocytes. Circ. Res. 107:1470–82.PubMedPubMedCentralCrossRefGoogle Scholar
  98. 98.
    Wu L, Zhang Y, Ma X, Zhang N, Qin G. (2012) The effect of resveratrol on FoxO1 expression in kidneys of diabetic nephropathy rats. Mol. Biol. Rep. 39:9085–93.PubMedCrossRefGoogle Scholar
  99. 99.
    Xia N, et al. (2013) Role of SIRT1 and FOXO factors in eNOS transcriptional activation by resveratrol. Nitric Oxide. 32:29–35.PubMedCrossRefGoogle Scholar
  100. 100.
    Csiszar A, et al. (2009) Resveratrol induces mitochondrial biogenesis in endothelial cells. Am. J. Physiol. Heart Circ. Physiol. 297:H13–20.PubMedPubMedCentralCrossRefGoogle Scholar
  101. 101.
    Nisoli E, et al. (2005) Calorie restriction promotes mitochondrial biogenesis by inducing the expression of eNOS. Science. 310:314–7.PubMedCrossRefGoogle Scholar
  102. 102.
    Yu W, Fu YC, Chen CJ, Wang X, Wang W. (2009) SIRT1: a novel target to prevent atherosclerosis. J. Cell. Biochem. 108:10–3.PubMedCrossRefGoogle Scholar
  103. 103.
    Nakagawa T, et al. (2011) Endothelial dysfunction as a potential contributor in diabetic nephropathy. Nat. Rev. Nephrol. 7:36–44.PubMedCrossRefGoogle Scholar
  104. 104.
    Zhao HJ, et al. (2006) Endothelial nitric oxide synthase deficiency produces accelerated nephropathy in diabetic mice. J. Am. Soc. Nephrol. 17:2664–9.PubMedPubMedCentralCrossRefGoogle Scholar
  105. 105.
    Nakagawa T, et al. (2007) Diabetic endothelial nitric oxide synthase knockout mice develop advanced diabetic nephropathy. J. Am. Soc. Nephrol. 18:539–50.PubMedCrossRefGoogle Scholar
  106. 106.
    Mattagajasingh I, et al. (2007) SIRT1 promotes endothelium-dependent vascular relaxation by activating endothelial nitric oxide synthase. Proc. Natl. Acad. Sci. U. S. A. 104:14855–60.PubMedPubMedCentralCrossRefGoogle Scholar
  107. 107.
    Miyazaki R, et al. (2008) SIRT1, a longevity gene, downregulates angiotensin II type 1 receptor expression in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 28:1263–9.PubMedCrossRefGoogle Scholar
  108. 108.
    Wu Z, et al. (1999) Mechanisms controlling mitochondrial biogenesis and respiration through the thermogenic coactivator PGC-1. Cell. 98:115–24.PubMedCrossRefGoogle Scholar
  109. 109.
    Rasbach KA, Schnellmann RG. (2007) Signaling of mitochondrial biogenesis following oxidant injury. J. Biol. Chem. 282:2355–62.PubMedCrossRefGoogle Scholar
  110. 110.
    Lehman JJ, et al. (2000) Peroxisome proliferator-activated receptor gamma coactivator-1 promotes cardiac mitochondrial biogenesis. J. Clin. Invest. 106:847–56.PubMedPubMedCentralCrossRefGoogle Scholar
  111. 111.
    Yuan Y, et al. (2012) Mitochondrial dysfunction accounts for aldosterone-induced epithelial-to-mesenchymal transition of renal proximal tubular epithelial cells. Free Radic. Biol. Med. 53:30–43.PubMedCrossRefGoogle Scholar
  112. 112.
    Nemoto S, Fergusson MM, Finkel T. (2005) SIRT1 functionally interacts with the metabolic regulator and transcriptional coactivator PGC-1α. J. Biol. Chem. 280:16456–60.PubMedCrossRefGoogle Scholar
  113. 113.
    Rodgers JT, et al. (2005) Nutrient control of glucose homeostasis through a complex of PGC-1alpha and SIRT1. Nature. 434:113–8.PubMedCrossRefGoogle Scholar
  114. 114.
    Yuan Y, et al. (2012) Activation of peroxisome proliferator-activated receptor-gamma coactivator 1alpha ameliorates mitochondrial dysfunction and protects podocytes from aldosterone-induced injury. Kidney Int. 82:771–89.PubMedCrossRefGoogle Scholar
  115. 115.
    Funk JA, Odejinmi S, Schnellmann RG. (2010) SRT1720 induces mitochondrial biogenesis and rescues mitochondrial function after oxidant injury in renal proximal tubule cells. J. Pharmacol. Exp. Ther. 333:593–601.PubMedPubMedCentralCrossRefGoogle Scholar
  116. 116.
    Hu CJ, Wang LY, Chodosh LA, Keith B, Simon MC. (2003) Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol. Cell. Biol. 23:9361–74.PubMedPubMedCentralCrossRefGoogle Scholar
  117. 117.
    Morita M, et al. (2003) HLF/HIF-2alpha is a key factor in retinopathy of prematurity in association with erythropoietin. EMBO J. 22:1134–46.PubMedPubMedCentralCrossRefGoogle Scholar
  118. 118.
    Warnecke C, et al. (2004) Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J. 18:1462–4.PubMedCrossRefGoogle Scholar
  119. 119.
    Haase VH. (2006) Hypoxia-inducible factors in the kidney. Am. J. Physiol. Renal Physiol. 291:F271–81.PubMedPubMedCentralCrossRefGoogle Scholar
  120. 120.
    Lim JH, Lee YM, Chun YS, Chen J, Kim JE, Park JW. (2010) Sirtuin 1 modulates cellular responses to hypoxia by deacetylating hypoxia-inducible factor 1alpha. Mol. Cell. 38:864–78.PubMedCrossRefGoogle Scholar
  121. 121.
    Dioum EM, et al. (2009) Regulation of hypoxia-inducible factor 2alpha signaling by the stress-responsive deacetylase sirtuin 1. Science. 324:1289–93.PubMedCrossRefGoogle Scholar
  122. 122.
    Yoon H, Shin SH, Shin DH, Chun YS, Park JW. (2014) Differential roles of SIRT1 in HIF-1alpha and HIF-2alpha mediated hypoxic responses. Biochem. Biophys. Res. Commun. 444:36–43.PubMedCrossRefGoogle Scholar
  123. 123.
    Walker AK, et al. (2010) Conserved role of SIRT1 orthologs in fasting-dependent inhibition of the lipid/cholesterol regulator SREBP. Genes Dev. 24:1403–17.PubMedPubMedCentralCrossRefGoogle Scholar
  124. 124.
    Li X, et al. (2007) SIRT1 deacetylates and positively regulates the nuclear receptor LXR. Mol. Cell. 28:91–106.PubMedCrossRefGoogle Scholar
  125. 125.
    Kemper JK, et al. (2009) FXR acetylation is normally dynamically regulated by p300 and SIRT1 but constitutively elevated in metabolic disease states. Cell Metab. 10:392–404.PubMedPubMedCentralCrossRefGoogle Scholar
  126. 126.
    Zhang J. (2007) The direct involvement of SIRT1 in insulin-induced insulin receptor substrate-2 tyrosine phosphorylation. J. Biol. Chem. 282:34356–64.PubMedCrossRefGoogle Scholar
  127. 127.
    Ponnusamy M, et al. (2014) Blocking sirtuin 1 and 2 inhibits renal interstitial fibroblast activation and attenuates renal interstitial fibrosis in obstructive nephropathy. J. Pharmacol. Exp. Ther. 350:243–56.PubMedPubMedCentralCrossRefGoogle Scholar
  128. 128.
    Yoshino J, Mills KF, Yoon MJ, Imai S. (2011) Nicotinamide mononucleotide, a key NAD(+) intermediate, treats the pathophysiology of diet- and age-induced diabetes in mice. Cell Metab. 14:528–36.PubMedPubMedCentralCrossRefGoogle Scholar
  129. 129.
    Bao L, et al. (2014) Grape seed proanthocyanidin extracts ameliorate podocyte injury by activating peroxisome proliferator-activated receptor-gamma coactivator 1alpha in low-dose streptozotocin-and high-carbohydrate/high-fat diet-induced diabetic rats. Food Funct. 5:1872–80.PubMedCrossRefGoogle Scholar
  130. 130.
    Chen D, et al. (2008) Tissue-specific regulation of SIRT1 by calorie restriction. Genes Dev. 22:1753–7.PubMedPubMedCentralCrossRefGoogle Scholar
  131. 131.
    Lai CH, et al. (2014) Exercise training enhanced SIRT1 longevity signaling replaces the IGF1 survival pathway to attenuate aging-induced rat heart apoptosis. Age (Dordr). 36:9706.CrossRefGoogle Scholar
  132. 132.
    Tikoo K, Lodea S, Karpe PA, Kumar S. (2014) Calorie restriction mimicking effects of roflumilast prevents diabetic nephropathy. Biochem. Biophys. Res. Commun. 450:1581–6.PubMedCrossRefGoogle Scholar
  133. 133.
    Hayashida S, et al. (2010) Fasting promotes the expression of SIRT1, an NAD+-dependent protein deacetylase, via activation of PPARalpha in mice. Mol. Cell Biochem. 339:285–92.PubMedCrossRefGoogle Scholar
  134. 134.
    Noriega LG, et al. (2011) CREB and ChREBP oppositely regulate SIRT1 expression in response to energy availability. EMBO Rep. 12:1069–76.PubMedPubMedCentralCrossRefGoogle Scholar
  135. 135.
    Motta MC, et al. (2004) Mammalian SIRT1 represses forkhead transcription factors. Cell. 116:551–63.PubMedCrossRefGoogle Scholar
  136. 136.
    Voelter-Mahlknecht S, Mahlknecht U. (2006) Cloning, chromosomal characterization and mapping of the NAD-dependent histone deacetylases gene sirtuin 1. Int. J. Mol. Med. 17:59–67.PubMedGoogle Scholar
  137. 137.
    Zhang HN, et al. (2010) Involvement of the p65/RelA subunit of NF-kappaB in TNF-alpha-induced SIRT1 expression in vascular smooth muscle cells. Biochem. Biophys. Res. Commun. 397:569–75.PubMedCrossRefPubMedCentralGoogle Scholar
  138. 138.
    Zhao Y, et al. (2013) Regulation of TREM2 expression by an NF-small ka, CyrillicB-sensitive miRNA-34a. Neuroreport. 24:318–23.PubMedPubMedCentralCrossRefGoogle Scholar
  139. 139.
    Forte E, et al. (2012) The Epstein-Barr virus (EBV)-induced tumor suppressor microRNA MiR-34a is growth promoting in EBV-infected B cells. J. Virol. 86:6889–98.PubMedPubMedCentralCrossRefGoogle Scholar
  140. 140.
    Yamakuchi M, Ferlito M, Lowenstein CJ. (2008) miR-34a repression of SIRT1 regulates apoptosis. Proc. Natl. Acad. Sci. U. S. A. 105:13421–6.PubMedPubMedCentralCrossRefGoogle Scholar
  141. 141.
    Li J, et al. (2012) Transcriptional activation of microRNA-34a by NF-kappa B in human esophageal cancer cells. BMC Mol. Biol. 13:4.PubMedPubMedCentralCrossRefGoogle Scholar
  142. 142.
    Purushotham A, et al. (2009) Hepatocyte-specific deletion of SIRT1 alters fatty acid metabolism and results in hepatic steatosis and inflammation. Cell Metab. 9:327–38.PubMedPubMedCentralCrossRefGoogle Scholar
  143. 143.
    Okazaki M, et al. (2010) PPARbeta/delta regulates the human SIRT1 gene transcription via Sp1. Endocr. J. 57:403–13.PubMedCrossRefGoogle Scholar
  144. 144.
    Han L, et al. (2010) SIRT1 is regulated by a PPARγ-SIRT1 negative feedback loop associated with senescence. Nucleic Acids Res. 38:7458–71.PubMedPubMedCentralCrossRefGoogle Scholar
  145. 145.
    Canto C, et al. (2009) AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature. 458:1056–60.PubMedPubMedCentralCrossRefGoogle Scholar
  146. 146.
    Nin V, et al. (2012) Role of deleted in breast cancer 1 (DBC1) protein in SIRT1 deacetylase activation induced by protein kinase A and AMP-activated protein kinase. J. Biol. Chem. 287:23489–501.PubMedPubMedCentralCrossRefGoogle Scholar
  147. 147.
    Hou X, et al. (2008) SIRT1 regulates hepatocyte lipid metabolism through activating AMP-activated protein kinase. J. Biol. Chem. 283:20015–26.PubMedPubMedCentralCrossRefGoogle Scholar
  148. 148.
    Lan F, Cacicedo JM, Ruderman N, Ido Y. (2008) SIRT1 modulation of the acetylation status, cytosolic localization, and activity of LKB1: possible role in AMP-activated protein kinase activation. J. Biol. Chem. 283:27628–35.PubMedPubMedCentralCrossRefGoogle Scholar
  149. 149.
    Narala SR, et al. (2008) SIRT1 acts as a nutrient-sensitive growth suppressor and its loss is associated with increased AMPK and telomerase activity. Mol. Biol. Cell. 19:1210–9.PubMedPubMedCentralCrossRefGoogle Scholar
  150. 150.
    Zhu H, et al. (2011) MicroRNA-195 promotes palmitate-induced apoptosis in cardiomyocytes by down-regulating SIRT1. Cardiovasc. Res. 92:75–84.PubMedCrossRefGoogle Scholar
  151. 151.
    Hu Y, Liu J, Wang J, Liu Q. (2011) The controversial links among calorie restriction, SIRT1, and resveratrol. Free Radic. Biol. Med. 51:250–6.PubMedCrossRefGoogle Scholar
  152. 152.
    Grozinger CM, Chao ED, Blackwell HE, Moazed D, Schreiber SL. (2001) Identification of a class of small molecule inhibitors of the sirtuin family of NAD-dependent deacetylases by phenotypic screening. J. Biol. Chem. 276:38837–43.PubMedCrossRefGoogle Scholar
  153. 153.
    Alcain FJ, Villalba JM. (2009) Sirtuin activators. Expert Opin. Ther. Pat. 19:403–14.PubMedCrossRefGoogle Scholar
  154. 154.
    Mai A, et al. (2005) Design, synthesis, and biological evaluation of sirtinol analogues as class III histone/protein deacetylase (Sirtuin) inhibitors. J. Med. Chem. 48:7789–95.PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of NephrologyThe Second Hospital of Jilin UniversityChangchunChina
  2. 2.Kosair Children’s Hospital Research Institute, Department of PediatricsUniversity of LouisvilleLouisvilleUSA
  3. 3.Department of Pharmacology and ToxicologyUniversity of LouisvilleLouisvilleUSA

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