Autophagy in diabetic nephropathy

Journal of Endocrinology

Volumn 224, Issue 1, 2015, Pages R15-R30

  Ding, Yan ^a   Choi, Mary E ^a  

^a WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

Autophagy; Diabetes mellitus; Kidney; Macroautophagy; Nephropathy

Indexed keywords

ADVANCED GLYCATION END PRODUCT; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 2; RAPAMYCIN; RESVERATROL; SILENT INFORMATION REGULATOR PROTEIN; SILENT INFORMATION REGULATOR PROTEIN T1; TRANSFORMING GROWTH FACTOR BETA; UNCLASSIFIED DRUG; TARGET OF RAPAMYCIN KINASE;

AUTOPHAGY; DIABETIC NEPHROPATHY; END STAGE RENAL DISEASE; ENDOPLASMIC RETICULUM STRESS; HUMAN; HYPOXIA; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CELL; KIDNEY FIBROSIS; MESANGIUM CELL; NON INSULIN DEPENDENT DIABETES MELLITUS; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PODOCYTE; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; ANIMAL; COMPLICATION; DIABETIC NEPHROPATHIES; GENETICS; KIDNEY; PATHOPHYSIOLOGY; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; AUTOPHAGY; DIABETES MELLITUS, TYPE 1; DIABETES MELLITUS, TYPE 2; DIABETIC NEPHROPATHIES; HUMANS; KIDNEY; SIGNAL TRANSDUCTION; TOR SERINE-THREONINE KINASES;

EID: 84919632586     PISSN: 00220795     EISSN: 14796805     Source Type: Journal    
DOI: 10.1530/JOE-14-0437     Document Type: Review

References (108)

1. Alers S, Löffler AS, Wesselborg S & Stork B 2012 Role of AMPK-mTOR-Ulk1/2 in the regulation of autophagy: cross talk, shortcuts, and feedbacks. Molecular and Cellular Biology 32 2-11. (doi:10.1128/MCB.06159-11).
2. Arias E & Cuervo AM 2010 Chaperone-mediated autophagy in protein quality control. Current Opinion in Cell Biology 23 184-189. (doi:10.1016/j.ceb.2010.10.009).
3. Barbosa Júnior Ade A, Zhou H, Hültenschmidt D, Totovic V, Jurilj N & Pfeifer U 1992 Inhibition of cellular autophagy in proximal tubular cells of the kidney in streptozotocin-diabetic and uninephrectomized rats. Virchows Archiv. B, Cell Pathology Including Molecular Pathology 61 359-366.
4. Belibi F, Zafar I, Ravichandran K, Segvic AB, Jani A, Ljubanovic DG & Edelstein CL 2011 Hypoxia-inducible factor-1α (HIF-1α) and autophagy in polycystic kidney disease (PKD). American Journal of Physiology. Renal Physiology 300 F1235-F1243. (doi:10.1152/ajprenal.00348.2010).
5. Bellot G, Garcia-Medina R, Gounon P, Chiche J, Roux D, Pouysségur J & Mazure NM 2009 Hypoxia-induced autophagy is mediated through hypoxia-inducible factor induction of BNIP3 and BNIP3L via their BH3 domains. Molecular and Cellular Biology 29 2570-2581. (doi:10.1128/ MCB.00166-09).
6. Brenner BM, Cooper ME, de Zeeuw D, Keane WF, Mitch WE, Parving HH, Remuzzi G, Snapinn SM, Zhang Z, Shahinfar S et al. 2001 Effects of losartan on renal and cardiovascular outcomes in patients with type 2 diabetes and nephropathy. New England Journal of Medicine 345 861-869. (doi:10.1056/NEJMoa011161).
7. Calcutt NA, Cooper ME, Kern TS & Schmidt AM 2009 Therapies for hyperglycaemia-induced diabetic complications: from animal models to clinical trials. Nature Reviews. Drug Discovery 8 417-429. (doi:10.1038/nrd2476).
8. Cao Y, Hao Y, Li H, Liu Q, Gao F, Liu W & Duan H 2014 Role of endoplasmic reticulum stress in apoptosis of differentiated mouse podocytes induced by high glucose. International Journal of Molecular Medicine 33 809-816. (doi:10.3892/ijmm.2014.1642).
9. Chang CC, Chang CY, Wu YT, Huang JP, Yen TH & Hung LM 2011 Resveratrol retards progression of diabetic nephropathy through modulations of oxidative stress, proinflammatory cytokines, and AMP-activated protein kinase. Journal of Biomedical Science 18 47. (doi:10.1186/1423-0127-18-47).
10. Chen Y, Liu CP, Xu KF, Mao XD, Lu YB, Fang L, Yang JW & Liu C 2008 Effect of taurine-conjugated ursodeoxycholic acid on endoplasmic reticulum stress and apoptosis induced by advanced glycation end products in cultured mouse podocytes. American Journal of Nephrology 28 1014-1022. (doi:10.1159/000148209).
11. Choi AM, Ryter SW & Levine B 2013 Autophagy in human health and disease. New England Journal of Medicine 368 651-662. (doi:10.1056/ NEJMra1205406).
12. Chuang PY, Dai Y, Liu R, He H, Kretzler M, Jim B, Cohen CD & He JC 2011 Alteration of forkhead box O (foxo4) acetylation mediates apoptosis of podocytes in diabetes mellitus. PLoS ONE 6 e23566. (doi:10.1371/ journal.pone.0023566).
13. Ding DF, You N, Wu XM, Xu JR, Hu AP, Ye XL, Zhu Q, Jiang XQ, Miao H, Liu C et al. 2010a Resveratrol attenuates renal hypertrophy in earlystage diabetes by activating AMPK. American Journal of Nephrology 31 363-374. (doi:10.1159/000300388).
14. Ding Y, Kim JK, Kim SI, Na HJ, Jun SY, Lee SJ & Choi ME 2010b TGF-β1 protects against mesangial cell apoptosis via induction of autophagy. Journal of Biological Chemistry 285 37909-37919. (doi:10.1074/jbc. M109.093724).
15. Ding Y, Kim SL, Lee SY, Koo JK, Wang Z & Choi ME 2014 Autophagy regulates TGF-β expression and suppresses kidney fibrosis induced by unilateral ureteral obstruction. Journal of theAmerican Society ofNephrology [in press]. (doi:10.1681/ASN.2013101068).
16. Fang L, Zhou Y, Cao H, Wen P, Jiang L, He W, Dai C & Yang J 2013 Autophagy attenuates diabetic glomerular damage through protection of hyperglycemia-induced podocyte injury. PLoS ONE 8 e60546. (doi:10.1371/journal.pone.0060546).
17. Fervenza FC, Fitzpatrick PM, Mertz J, Erickson SB, Liggett S, Popham S, Wochos DN, Synhavsky A, Hippler S, Larson TS et al. 2004 Acute rapamycin nephrotoxicity in native kidneys of patients with chronic glomerulopathies. Nephrology, Dialysis, Transplantation 19 1288-1292. (doi:10.1093/ndt/gfh079).
18. Fiorentino L, Cavalera M, Menini S, Marchetti V, Mavilio M, Fabrizi M, Conserva F, Casagrande V, Menghini R, Pontrelli P et al. 2013 Loss of TIMP3 underlies diabetic nephropathy via FoxO1/STAT1 interplay. EMBO Molecular Medicine 5 441-455. (doi:10.1002/emmm.201201475).
19. Forbes MS, Thornhill BA & Chevalier RL 2011 Proximal tubular injury and rapid formation of atubular glomeruli in mice with unilateral ureteral obstruction: a new look at an old model. American Journal of Physiology. Renal Physiology 301 F110-F117. (doi:10.1152/ajprenal.00022.2011).
20. Friederich M, Fasching A, Hansell P, Nordquist L & Palm F 2008 Diabetesinduced up-regulation of uncoupling protein-2 results in increased mitochondrial uncoupling in kidney proximal tubular cells. Biochimica et Biophysica Acta 1777 935-940. (doi:10.1016/j.bbabio.2008.03.030).
21. Giacco F & Brownlee M 2010 Oxidative stress and diabetic complications. Circulation Research 107 1058-1070. (doi:10.1161/CIRCRESAHA.110. 223545).
22. Gödel M, Hartleben B, Herbach N, Liu S, Zschiedrich S, Lu S, Debreczeni-Mór A, Lindenmeyer MT, Rastaldi MP, Hartleben G et al. 2011 Role of mTOR in podocyte function and diabetic nephropathy in humans and mice. Journal of Clinical Investigation 121 2197-2209. (doi:10.1172/ JCI44774).
23. Hamasaki M, Furuta N,Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y et al. 2013 Autophagosomes form at ER-mitochondria contact sites. Nature 495 389-393. (doi:10.1038/ nature11910).
24. Han K, Zhou H & Pfeifer U 1997 Inhibition and restimulation by insulin of cellular autophagy in distal tubular cells of the kidney in early diabetic rats. Kidney & Blood Pressure Research 20 258-263. (doi:10.1159/ 000174155).
25. Har R, Scholey JW, Daneman D, Mahmud FH, Dekker R, Lai V, Elia Y, Fritzler ML, Sochett EB, Reich HN et al. 2013 The effect of renal hyperfiltration on urinary inflammatory cytokines/chemokines in patients with uncomplicated type 1 diabetes mellitus. Diabetologia 56 1166-1173. (doi:10.1007/s00125-013-2857-5).
26. Hartleben B, Gödel M, Meyer-Schwesinger C, Liu S, Ulrich T, Köbler S, Wiech T, Grahammer F, Arnold SJ, Lindenmeyer MT et al. 2010 Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice. Journal of Clinical Investigation 120 1084-1096. (doi:10.1172/JCI39492).
27. Hasegawa K, Wakino S, Simic P, Sakamaki Y, Minakuchi H, Fujimura K, Hosoya K, Komatsu M, Kaneko Y, Kanda T et al. 2013 Renal tubular Sirt1 attenuates diabetic albuminuria by epigenetically suppressing Claudin-1 overexpression in podocytes. Nature Medicine 19 1496-1504. (doi:10.1038/nm.3363).
28. He C & Levine B 2010 The Beclin 1 interactome. Current Opinion in Cell Biology 22 140-149. (doi:10.1016/j.ceb.2010.01.001).
29. He W, Wang Y, Zhang MZ, You L, Davis LS, Fan H, Yang HC, Fogo AB, Zent R, Harris RC et al. 2010 Sirt1 activation protects the mouse renal medulla from oxidative injury. Journal of Clinical Investigation 120 1056-1068. (doi:10.1172/JCI41563).
30. Hu FB 2011 Globalization of diabetes. Diabetes Care 34 1249-1257. (doi:10.2337/dc11-0442).
31. Hummasti S & Hotamisligil GS 2010 Endoplasmic reticulum stress and inflammation in obesity and diabetes. Circulation Research 107 579-591. (doi:10.1161/CIRCRESAHA.110.225698).
32. Ichihara A, Suzuki F, Nakagawa T, Kaneshiro Y, Takemitsu T, Sakoda M, Nabi AH, Nishiyama A, Sugaya T, Hayashi M et al. 2006 Prorenin receptor blockade inhibits development of glomerulosclerosis in diabetic angiotensin II type 1a receptor-deficient mice. Journal of the American Society of Nephrology 17 1950-1961. (doi:10.1681/ASN.2006010029).
33. Inoki K, Mori H,Wang J, Suzuki T, Hong S, Yoshida S, Blattner SM, Ikenoue T, Rüegg MA, Hall MN et al. 2011 mTORC1 activation in podocytes is a critical step in the development of diabetic nephropathy in mice. Journal of Clinical Investigation 121 2181-2196. (doi:10.1172/JCI44771).
34. Jiang M, Liu K, Luo J & Dong Z 2010 Autophagy is a renoprotective mechanism during in vitro hypoxia and in vivo ischemia-reperfusion injury. American Journal of Pathology 176 1181-1192. (doi:10.2353/ ajpath.2010.090594).
35. Kanwar YS, Sun L, Xie P, Liu FY & Chen S 2011 A glimpse of various pathogenetic mechanisms of diabetic nephropathy. Annual Review of Pathology 6 395-423. (doi:10.1146/annurev.pathol.4.110807.092150).
36. van Kats JP, Schalekamp MA, Verdouw PD, Duncker DJ & Danser AH 2001 Intrarenal angiotensin II: interstitial and cellular levels and site of production. Kidney International 60 2311-2317. (doi:10.1046/ j.1523-1755.2001.00049.x).
37. Kim J, Kundu M, Viollet B & Guan KL 2011 AMPK and mTOR regulate autophagy through direct phosphorylation of Ulk1. Nature Cell Biology 13 132-141. (doi:10.1038/ncb2152).
38. Kim SI, Na HJ, Ding Y, Wang Z, Lee SJ & Choi ME 2012a Autophagy promotes intracellular degradation of type I collagen induced by transforming growth factor (TGF)-β1. Journal of Biological Chemistry 287 11677-11688. (doi:10.1074/jbc.M111.308460).
39. Kim WY, Nam SA, Song HC, Ko JS, Park SH, Kim HL, Choi EJ, Kim YS, Kim J & Kim YK 2012b The role of autophagy in unilateral ureteral obstruction rat model. Nephrology 17 148-159. (doi:10.1111/j.1440-1797.2011.01541.x).
40. Kim MY, Lim JH, Youn HH, Hong YA, Yang KS, Park HS, Chung S, Ko SH, Shin SJ, Choi BS et al. 2013 Resveratrol prevents renal lipotoxicity and inhibits mesangial cell glucotoxicity in a manner dependent on the AMPK-SIRT1-PGC1a axis in db/db mice. Diabetologia 56 204-217. (doi:10.1007/s00125-012-2747-2).
41. Kimura T, Takabatake Y, Takahashi A, Kaimori JY, Matsui I, Namba T, Kitamura H, Niimura F, Matsusaka T, Soga T et al. 2011 Autophagy protects the proximal tubule from degeneration and acute ischemic injury. Journal of the American Society of Nephrology 22 902-913. (doi:10.1681/ASN.2010070705).
42. Kitada M, Takeda A, Nagai T, Ito H, Kanasaki K & Koya D 2011a 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. Experimental Diabetes Research 2011 908185. (doi:10.1155/2011/908185).
43. Kitada M, Kume S, Imaizumi N & Koya D 2011b Resveratrol improves oxidative stress and protects against diabetic nephropathy through normalization of Mn-SOD dysfunction in AMPK/SIRT1-independent pathway. Diabetes 60 634-643. (doi:10.2337/db10-0386).
44. Koesters R, Kaissling B, Lehir M, Picard N, Theilig F, Gebhardt R, Glick AB, Hähnel B, Hosser H, Gröne HJ et al. 2010 Tubular overexpression of transforming growth factor-b1 induces autophagy and fibrosis but not mesenchymal transition of renal epithelial cells. American Journal of Pathology 177 632-643. (doi:10.2353/ajpath.2010.091012).
45. Koya D, Hayashi K, Kitada M, Kashiwagi A, Kikkawa R & Haneda M 2003 Effects of antioxidants in diabetes-induced oxidative stress in the glomeruli of diabetic rats. Journal of the American Society of Nephrology 14 S250-S253. (doi:10.1097/01.ASN.0000077412.07578.44).
46. Kroemer G, Mariño G & Levine B 2010 Autophagy and the integrated stress response. Molecular Cell 40 280-293. (doi:10.1016/j.molcel.2010.09.023).
47. Kume S, Uzu T, Horiike K, Chin-Kanasaki M, Isshiki K, Araki S, Sugimoto T, Haneda M, Kashiwagi A & Koya D 2010 Calorie restriction enhances cell adaptation to hypoxia through Sirt1-dependent mitochondrial autophagy in mouse aged kidney. Journal of Clinical Investigation 120 1043-1055. (doi:10.1172/JCI41376).
48. Lee MJ, Feliers D, Mariappan MM, Sataranatarajan K, Mahimainathan L, Musi N, Foretz M, Viollet B, Weinberg JM, Choudhury GG et al. 2007 A role for AMP-activated protein kinase in diabetes-induced renal hypertrophy. American Journal of Physiology. Renal Physiology 292 F617-F627. (doi:10.1152/ajprenal.00278.2006).
49. Lee IH, Cao L, Mostoslavsky R, Lombard DB, Liu J, Bruns NE, Tsokos M, Alt FW & Finkel T 2008 A role for the NAD-dependent deacetylase Sirt1 in the regulation of autophagy. PNAS 105 3374-3379. (doi:10.1073/pnas.0712145105).
50. Lee JW, Park S, Takahashi Y & Wang HG 2010 The association of AMPK with ULK1 regulates autophagy. PLoS ONE 5 e15394. (doi:10.1371/ journal.pone.0015394).
51. Lewis EJ, Hunsicker LG, Clarke WR, Berl T, Pohl MA, Lewis JB, Ritz E, Atkins RC, Rohde R, Raz I et al. 2001 Renoprotective effect of the angiotensin-receptor antagonist irbesartan in patients with nephropathy due to type 2 diabetes. New England Journal of Medicine 345 851-860. (doi:10.1056/NEJMoa011303).
52. Li C, Cai F, Yang Y, Zhao X, Wang C, Li J, Jia Y, Tang J & Liu Q 2010a Tetrahydroxystilbene glucoside ameliorates diabetic nephropathy in rats: involvement of SIRT1 and TGF-β1 pathway. European Journal of Pharmacology 649 382-389. (doi:10.1016/j.ejphar.2010.09.004).
53. Li L, Zepeda-Orozco D, Black R & Lin F 2010b Autophagy is a component of epithelial cell fate in obstructive uropathy. American Journal of Pathology 176 1767-1778. (doi:10.2353/ajpath.2010.090345).
54. Lieberthal W & Levine JS 2009 The role of the mammalian target of rapamycin (mTOR) in renal disease. Journal of the American Society of Nephrology 20 2493-2502. (doi:10.1681/ASN.2008111186).
55. Lindenmeyer MT, Rastaldi MP, Ikehata M, Neusser MA, Kretzler M, Cohen CD & Schlöndorff D 2008 Proteinuria and hyperglycemia induce endoplasmic reticulum stress. Journal of the American Society of Nephrology 19 2225-2236. (doi:10.1681/ASN.2007121313).
56. Liu S, Hartleben B, Kretz O, Wiech T, Igarashi P, Mizushima N, Walz G & Huber TB 2012 Autophagy plays a critical role in kidney tubule maintenance, aging and ischemia-reperfusion injury. Autophagy 8 826-837. (doi:10.4161/auto.19419).
57. Lloberas N, Cruzado JM, Franquesa M, Herrero-Fresneda I, Torras J, Alperovich G, Rama I, Vidal A & Grinyó JM 2006 Mammalian target of rapamycin pathway blockade slows progression of diabetic kidney disease in rats. Journal of the American Society of Nephrology 17 1395-1404. (doi:10.1681/ASN.2005050549).
58. Lu X, Roksnoer LC & Danser AH 2013 The intrarenal renin-angiotensin system: does it exist? Implications from a recent study in renal angiotensin-converting enzyme knockout mice Nephrology, Dialysis, Transplantation 28 2977-2982. (doi:10.1093/ndt/gft333).
59. Ma T, Zhu J, Chen X, Zha D, Singhal PC & Ding G 2013 High glucose induces autophagy in podocytes. Experimental Cell Research 319 779-789. (doi:10.1016/j.yexcr.2013.01.018).
60. Mijaljica D, Prescott M & Devenish RJ 2011 Microautophagy in mammalian cells: revisiting a 40-year-old conundrum. Autophagy 7 673-682. (doi:10.4161/auto.7.7.14733).
61. Mori H, Inoki K, Masutani K, Wakabayashi Y, Komai K, Nakagawa R, Guan KL & Yoshimura A 2009 The mTOR pathway is highly activated in diabetic nephropathy and rapamycin has a strong therapeutic potential. Biochemical and Biophysical Research Communications 384 471-475. (doi:10.1016/j.bbrc.2009.04.136).
62. Mortimore GE & Pösö AR 1987 Intracellular protein catabolism and its control during nutrient deprivation and supply. Annual Review of Nutrition 7 539-564. (doi:10.1146/annurev.nu.07.070187.002543).
63. Moynihan KA, Grimm AA, Plueger MM, Bernal-Mizrachi E, Ford E, Cras-Méneur C, Permutt MA & Imai S 2005 Increased dosage of mammalian Sir2 in pancreatic b cells enhances glucose-stimulated insulin secretion in mice. Cell Metabolism 2 105-117. (doi:10.1016/j.cmet.2005.07.001).
64. Muller DN, Klanke B, Feldt S, Cordasic N, Hartner A, Schmieder RE, Luft FC & Hilgers KF 2008 (Pro)renin receptor peptide inhibitor "handleregion" peptide does not affect hypertensive nephrosclerosis in Goldblatt rats. Hypertension 51 676-681. (doi:10.1161/HYPERTENSIONAHA. 107.101493).
65. Nair S & Wilding JP 2010 Sodium glucose cotransporter 2 inhibitors as a new treatment for diabetes mellitus. Journal of Clinical Endocrinology and Metabolism 95 34-42. (doi:10.1210/jc.2009-0473).
66. Nakagawa T, Tanabe K, Croker BP, Johnson RJ, Grant MB, Kosugi T & Li Q 2011 Endothelial dysfunction as a potential contributor in diabetic nephropathy. Nature Reviews. Nephrology 7 36-44. (doi:10.1038/ nrneph.2010.152).
67. Nguyen G & Muller DN 2010 The biology of the (pro)renin receptor. Journal of the American Society of Nephrology 21 18-23. (doi:10.1681/ASN. 2009030300).
68. Nishikawa T, Edelstein D, Du XL, Yamagishi S, Matsumura T, Kaneda Y, Yorek MA, Beebe D, Oates PJ, Hammes HP et al. 2000 Normalizing mitochondrial superoxide production blocks three pathways of hyperglycaemic damage. Nature 404 787-790. (doi:10.1038/35008121).
69. Noh H & King GL 2007 The role of protein kinase C activation in diabetic nephropathy. Kidney International. Supplement 106 S49-S53. (doi:10.1038/sj.ki.5002386).
70. Ohse T, Inagi R, Tanaka T, Ota T, Miyata T, Kojima I, Ingelfinger JR, Ogawa S, Fujita T & Nangaku M 2006 Albumin induces endoplasmic reticulum stress and apoptosis in renal proximal tubular cells. Kidney International 70 1447-1455. (doi:10.1038/sj.ki.5001704).
71. Oshima Y, Kinouchi K, Ichihara A, Sakoda M, Kurauchi-Mito A, Bokuda K, Narita T, Kurosawa H, Sun-Wada GH, Wada Y et al. 2011 Prorenin receptor is essential for normal podocyte structure and function. Journal of the American Society of Nephrology 22 2203-2212. (doi:10.1681/ ASN.2011020202).
72. Peng KY, Horng LY, Sung HC, Huang HC & Wu RT 2011 Hepatocyte growth factor has a role in the amelioration of diabetic vascular complications via autophagic clearance of advanced glycation end products: Dispo85E, an HGF inducer, as a potential botanical drug. Metabolism 60 888-892. (doi:10.1016/j.metabol.2010.08.009).
73. Price NL, Gomes AP, Ling AJ, Duarte FV, Martin-Montalvo A, North BJ, Agarwal B, Ye L, Ramadori G, Teodoro JS et al. 2012 SIRT1 is required for AMPKactivationand the beneficial effects of resveratrol onmitochondrial function. Cell Metabolism 15 675-690. (doi:10.1016/j.cmet.2012.04.003).
74. Qi W,MuJ, Luo ZF, Zeng W, Guo YH, Pang Q, Ye ZL, Liu L, Yuan FH & Feng B 2011 Attenuation of diabetic nephropathy in diabetes rats induced by streptozotocin by regulating the endoplasmic reticulum stress inflammatory response. Metabolism 60 594-603. (doi:10.1016/j.metabol. 2010.07.021).
75. Ravikumar B, Sarkar S, Davies JE, Futter M, Garcia-Arencibia M, Green-Thompson ZW, Jimenez-Sanchez M, Korolchuk VI, Lichtenberg M, Luo S et al. 2010 Regulation of mammalian autophagy in physiology and pathophysiology. Physiological Reviews 90 1383-1435. (doi:10.1152/physrev.00030.2009).
76. Riediger F, Quack I, Qadri F, Hartleben B, Park JK, Potthoff SA, Sohn D, Sihn G, Rousselle A, Fokuhl V et al. 2011 Prorenin receptor is essential for podocyte autophagy and survival. Journal of the American Society of Nephrology 22 2193-2202. (doi:10.1681/ASN.2011020200).
77. Rouschop KM, van den Beucken T, Dubois L, Niessen H, Bussink J, Savelkouls K, Keulers T, Mujcic H, Landuyt W, Voncken JW et al. 2010 The unfolded protein response protects human tumor cells during hypoxia through regulation of the autophagy genes MAP1LC3B and ATG5. Journal of Clinical Investigation 120 127-141. (doi:10.1172/ JCI40027).
78. Ruggenenti P, Cravedi P & Remuzzi G 2010 The RAAS in the pathogenesis and treatment of diabetic nephropathy. Nature Reviews. Nephrology 6 319-330. (doi:10.1038/nrneph.2010.58).
79. Sakaguchi M, Isono M, Isshiki K, Sugimoto T, Koya D & Kashiwagi A 2006 Inhibition of mTOR signaling with rapamycin attenuates renal hypertrophy in the early diabetic mice. Biochemical and Biophysical Research Communications 340 296-301. (doi:10.1016/j.bbrc.2005.12.012).
80. Sataranatarajan K, Mariappan MM, Lee MJ, Feliers D, Choudhury GG, Barnes JL & Kasinath BS 2007 Regulation of elongation phase of mRNA translation in diabetic nephropathy: amelioration by rapamycin. American Journal of Pathology 171 1733-1742. (doi:10.2353/ajpath. 2007.070412).
81. Satofuka S, Ichihara A, Nagai N, Noda K, Ozawa Y, Fukamizu A, Tsubota K, Itoh H, Oike Y & Ishida S 2009 (Pro)renin receptor-mediated signal transduction and tissue renin-angiotensin system contribute to diabetes-induced retinal inflammation. Diabetes 58 1625-1633. (doi:10.2337/db08-0254).
82. Shi Y & Hu FB 2014 The global implications of diabetes and cancer. Lancet 383 1947-1948. (doi:10.1016/S0140-6736(14)60886-2).
83. Sieber J, Lindenmeyer MT, Kampe K, Campbell KN, Cohen CD, Hopfer H, Mundel P & Jehle AW 2010 Regulation of podocyte survival and endoplasmic reticulum stress by fatty acids. American Journal of Physiology. Renal Physiology 299 F821-F829. (doi:10.1152/ajprenal. 00196.2010).
84. Sokolovska J, Isajevs S, Sugoka O, Sharipova J, Lauberte L, Svirina D, Rostoka E, Sjakste T, Kalvinsh I & Sjakste N 2010 Influence of metformin on GLUT1 gene and protein expression in rat streptozotocin diabetes mellitus model. Archives of Physiology and Biochemistry 116 137-145. (doi:10.3109/13813455.2010.494672).
85. Sooparb S, Price SR, Shaoguang J & Franch HA 2004 Suppression of chaperone-mediated autophagy in the renal cortex during acute diabetes mellitus. Kidney International 65 2135-2144. (doi:10.1111/j. 1523-1755.2004.00639.x).
86. Stehouwer CD 2004 Endothelial dysfunction in diabetic nephropathy: state of theartandpotential significance fornon-diabetic renaldisease.Nephrology, Dialysis, Transplantation 19 778-781. (doi:10.1093/ndt/gfh015).
87. Sun C, Zhang F, Ge X, Yan T, Chen X, Shi X & Zhai Q 2007 SIRT1 improves insulin sensitivity under insulin-resistant conditions by repressing PTP1B. Cell Metabolism 6 307-319. (doi:10.1016/j.cmet.2007.08.014).
88. Takahashi H, Ichihara A, Kaneshiro Y, Inomata K, Sakoda M, Takemitsu T, Nishiyama A & Itoh H 2007 Regression of nephropathy developed in diabetes by (pro)renin receptor blockade. Journal of the American Society of Nephrology 18 2054-2061. (doi:10.1681/ASN.2006080820).
89. Tan AL, Forbes JM & Cooper ME 2007 AGE, RAGE, and ROS in diabetic nephropathy. Seminars in Nephrology 27 130-143. (doi:10.1016/j. semnephrol.2007.01.006).
90. Tikoo K, Tripathi DN, Kabra DG, Sharma V & Gaikwad AB 2007 Intermittent fasting prevents the progression of type I diabetic nephropathy in rats and changes the expression of Sir2 and p53. FEBS Letters 581 1071-1078. (doi:10.1016/j.febslet.2007.02.006).
91. Turan B, Tuncay E & Vassort G 2012 Resveratrol and diabetic cardiac function: focus on recent in vitro and in vivo studies. Journal of Bioenergetics and Biomembranes 44 281-296. (doi:10.1007/s10863-012-9429-0).
92. Vallon V, Rose M, Gerasimova M, Satriano J, Platt KA, Koepsell H, Cunard R, Sharma K, Thomson SC & Rieg T 2013 Knockout of Na-glucose transporter SGLT2 attenuates hyperglycemia and glomerular hyperfiltration but not kidney growth or injury in diabetes mellitus. American Journal of Physiology. Renal Physiology 304 F156-F167. (doi:10. 1152/ajprenal.00409.2012).
93. Walter P & Ron D 2011 The unfolded protein response: from stress pathway to homeostatic regulation. Science 334 1081-1086. (doi:10.1126/ science.1209038).
94. Wang Z & Choi ME 2014 Autophagy in kidney health and disease. Antioxidants & Redox Signaling 20 519-537. (doi:10.1089/ars.2013.5363).
95. Wittmann S, Daniel C, Stief A, Vogelbacher R, Amann K & Hugo C 2009 Long-term treatment of sirolimus but not cyclosporine ameliorates diabetic nephropathy in the rat. Transplantation 87 1290-1299. (doi:10.1097/TP.0b013e3181a192bd).
96. Wolf G, Chen S & Ziyadeh FN 2005 From the periphery of the glomerular capillary wall toward the center of disease: podocyte injury comes of age in diabetic nephropathy. Diabetes 54 1626-1634. (doi:10.2337/ diabetes.54.6.1626).
97. Wu L, Zhang Y, Ma X, Zhang N & Qin G 2012 The effect of resveratrol on FoxO1 expression in kidneys of diabetic nephropathy rats. Molecular Biology Reports 39 9085-9093. (doi:10.1007/s11033-012-1780-z).
98. Xavier S, Gilbert V, Rastaldi MP, Krick S, Kollins D, Reddy A, Bottinger E, Cohen CD & Schlondorff D 2010 BAMBI is expressed in endothelial cells and is regulated by lysosomal/autolysosomal degradation. PLoS ONE 5 e12995. (doi:10.1371/journal.pone.0012995).
99. Xu Y, Nie L, Yin YG, Tang JL, Zhou JY, Li DD & Zhou SW 2012 Resveratrol protects against hyperglycemia-induced oxidative damage to mitochondria by activating SIRT1 in rat mesangial cells. Toxicology and Applied Pharmacology 259 395-401. (doi:10.1016/j.taap.2011.09.028).
100. Xu Y, Ruan S, Wu X, Chen H, Zheng K & Fu B 2013 Autophagy and apoptosis in tubular cells following unilateral ureteral obstruction are associated with mitochondrial oxidative stress. International Journal of Molecular Medicine 31 628-636. (doi:10.3892/ijmm.2013.1232).
101. Yadav A, Vallabu S, Arora S, Tandon P, Slahan D, Teichberg S & Singhal PC 2010 ANG II promotes autophagy in podocytes. American Journal of Physiology. Cell Physiology 299 C488-C496. (doi:10.1152/ajpcell. 00424.2009).
102. Yamahara K, Kume S, Koya D, Tanaka Y, Morita Y, Chin-Kanasaki M, Araki H, Isshiki K, Araki S, Haneda M et al. 2013 Obesity-mediated autophagy insufficiency exacerbates proteinuria-induced tubulointerstitial lesions. Journal of the American Society of Nephrology 24 1769-1781. (doi:10.1681/ASN.2012111080).
103. Yang Y, Wang J, Qin L, Shou Z, Zhao J, Wang H, Chen Y & Chen J 2007 Rapamycin prevents early steps of the development of diabetic nephropathy in rats. American Journal of Nephrology 27 495-502. (doi:10.1159/000106782).
104. Zhang J 2007 The direct involvement of Sir T1 in insulin-induced insulin receptor substrate-2 tyrosine phosphorylation. Journal of Biological Chemistry 282 34356-34364. (doi:10.1074/jbc.M706644200).
105. Zhang S, Cai G, Fu B, Feng Z, Ding R, Bai X, Liu W, Zhuo L, Sun L, Liu F et al. 2012 SIRT1 is required for the effects of rapamycin on high glucoseinducing mesangial cells senescence. Mechanisms of Ageing and Development 133 387-400. (doi:10.1016/j.mad.2012.04.005).
106. Zhang MZ, Wang Y, Paueksakon P & Harris RC 2014 Epidermal growth factor receptor inhibition slows progression of diabetic nephropathy in association with a decrease in endoplasmic reticulum stress and an increase in autophagy. Diabetes 63 2063-2072. (doi:10.2337/db13-1279).
107. Zhong Y, Wang QJ, Li X, Yan Y, Backer JM, Chait BT, Heintz N & Yue Z 2009 Distinct regulation of autophagic activity by Atg14L and Rubicon associated with Beclin 1-phosphatidylinositol-3-kinase complex. Nature Cell Biology 11 468-476. (doi:10.1038/ncb1854).
108. Zoncu R, Efeyan A & Sabatini DM 2011 mTOR: from growth signal integration to cancer, diabetes and ageing. Nature Reviews. Molecular Cell Biology 12 21-35. (doi:10.1038/nrm3025).