Reactive oxygen species are involved in insulin-dependent regulation of autophagy in primary rat podocytes

International Journal of Biochemistry and Cell Biology

Volumn 75, Issue , 2016, Pages 23-33

  Audzeyenka, Irena ^a   Rogacka, Dorota ^a   Piwkowska, Agnieszka ^a   Rychlowski, Michal ^b   Bierla, Joanna Beata ^c   Czarnowska, Elzbieta ^c   Angielski, Stefan ^a   Jankowski, MacIej ^a,b  

^a MOSSAKOWSKI MEDICAL RESEARCH CENTRE   (Poland)

^b MEDICAL UNIVERSITY OF GDANSK   (Poland)

^c CHILDREN'S MEMORIAL HEALTH INSTITUTE   (Poland)

Author keywords

Autophagy; Filtration barrier permeability; Insulin; Podocyte; Reactive oxygen species

Indexed keywords

ALBUMIN; APOCYNIN; INSULIN; REACTIVE OXYGEN METABOLITE; RENALASE; RNA; SMALL INTERFERING RNA; ACETOPHENONE DERIVATIVE; ALBUMINOID; AUTOPHAGY RELATED PROTEIN 12; AUTOPHAGY RELATED PROTEIN 5; LC3 PROTEIN, RAT; MICROTUBULE ASSOCIATED PROTEIN; NOX4 PROTEIN, RAT; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE;

ANIMAL CELL; ANIMAL CELL CULTURE; ARTICLE; AUTOPHAGY; CELL VIABILITY; DIABETIC NEPHROPATHY; ENZYME INHIBITION; GENETIC TRANSFECTION; NONHUMAN; OXIDATIVE STRESS; PATHOGENESIS; PERMEABILITY; PODOCYTE; RAT; RNA EXTRACTION; WESTERN BLOTTING; WISTAR RAT; ANIMAL; CYTOLOGY; DEFICIENCY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENE SILENCING; GENETICS; METABOLISM;

ACETOPHENONES; ALBUMINS; ANIMALS; AUTOPHAGY; AUTOPHAGY-RELATED PROTEIN 12; AUTOPHAGY-RELATED PROTEIN 5; GENE EXPRESSION REGULATION; GENE KNOCKDOWN TECHNIQUES; INSULIN; MICROTUBULE-ASSOCIATED PROTEINS; NADPH OXIDASE; PERMEABILITY; PODOCYTES; RATS; RATS, WISTAR; REACTIVE OXYGEN SPECIES;

EID: 84961894007     PISSN: 13572725     EISSN: 18785875     Source Type: Journal    
DOI: 10.1016/j.biocel.2016.03.015     Document Type: Article

References (47)

1. W. Bechtel, M. Helmstadter, J. Balica, B. Hartleben, C. Schell, and T.B. Huber The class III phosphatidylinositol 3-kinase PIK3C3/VPS34 regulates endocytosis and autophagosome-autolysosome formation in podocytes Autophagy 9 2013 1097 1099
2. C.E. Chua, B.Q. Gan, and B.L. Tang Involvement of members of the Rab family and related small GTPases in autophagosome formation and maturation Cell. Mol. Life Sci. 68 2011 3349 3358
3. R. Coward, and A. Fornoni Insulin signaling: implications for podocyte biology in diabetic kidney disease Curr. Opin. Nephrol. Hypertens. 24 2015 104 110
4. R.J. Coward, G.I. Welsh, J. Yang, C. Tasman, R. Lennon, A. Koziell, and et al. The human glomerular podocyte is a novel target for insulin action Diabetes 54 2005 3095 3102
5. M. Dalla Vestra, A. Masiero, A.M. Roiter, A. Saller, G. Crepaldi, and P. Fioretto Is podocyte injury relevant in diabetic nephropathy? Studies in patients with type 2 diabetes Diabetes 52 2003 1031 1035
6. A. Diez-Sampedro, O. Lenz, and A. Fornoni Podocytopathy in diabetes: a metabolic and endocrine disorder Am. J. Kidney Dis. 58 2011 637 646
7. C. Ebato, T. Uchida, M. Arakawa, M. Komatsu, T. Ueno, K. Komiya, and et al. Autophagy is important in islet homeostasis and compensatory increase of beta cell mass in response to high-fat diet Cell Metab. 8 2008 325 332
8. J. Ezaki, N. Matsumoto, M. Takeda-Ezaki, M. Komatsu, K. Takahashi, Y. Hiraoka, and et al. Liver autophagy contributes to the maintenance of blood glucose and amino acid levels Autophagy 7 2011 727 736
9. C. Faul, K. Asanuma, E. Yanagida-Asanuma, K. Kim, and P. Mundel Actin up: regulation of podocyte structure and function by components of the actin cytoskeleton Trends Cell Biol. 17 2007 428 437
10. A. Goginashvili, Z. Zhang, E. Erbs, C. Spiegelhalter, P. Kessler, M. Mihlan, and et al. Insulin granules. Insulin secretory granules control autophagy in pancreatic beta cells. Science Am. Assoc. Adv. Sci. 2015 878 882
11. E. Gonzalez, E. Flier, D. Molle, D. Accili, and T.E. McGraw Hyperinsulinemia leads to uncoupled insulin regulation of the GLUT4 glucose transporter and the FoxO1 transcription factor Proc. Natl. Acad. Sci. U. S. A. 2011 10162 10167
12. G. Gruden, P.C. Perin, and G. Camussi Insight on the pathogenesis of diabetic nephropathy from the study of podocyte and mesangial cell biology Curr. Diabetes Rev. 1 2005 27 40
13. D. Han, B. Yang, L.K. Olson, A. Greenstein, S.H. Baek, K.J. Claycombe, and et al. Activation of autophagy through modulation of 5′-AMP-activated protein kinase protects pancreatic beta-cells from high glucose Biochem. J. 425 2010 541 551
14. B. Hartleben, M. Godel, C. Meyer-Schwesinger, S. Liu, T. Ulrich, S. Kobler, and et al. Autophagy influences glomerular disease susceptibility and maintains podocyte homeostasis in aging mice J. Clin. Invest. 120 2010 1084 1096
15. B. Hartleben, N. Wanner, and T.B. Huber Autophagy in glomerular health and disease Semin. Nephrol. 34 2014 42 52
16. C. He, M.C. Bassik, V. Moresi, K. Sun, Y. Wei, Z. Zou, and et al. Exercise-induced BCL2-regulated autophagy is required for muscle glucose homeostasis Nature 481 2012 511 515
17. T.B. Huber, C.L. Edelstein, B. Hartleben, K. Inoki, M. Jiang, D. Koya, and et al. Emerging role of autophagy in kidney function, diseases and aging Autophagy 2012 1009 1031
18. D.K. Johnson, K.J. Schillinger, D.M. Kwait, C.V. Hughes, E.J. McNamara, F. Ishmael, and et al. Inhibition of NADPH oxidase activation in endothelial cells by ortho-methoxy-substituted catechols Endothelium 9 2002 191 203
19. O. Lenoir, M. Jasiek, C. Henique, L. Guyonnet, B. Hartleben, T. Bork, and et al. Endothelial cell and podocyte autophagy synergistically protect from diabetes-induced glomerulosclerosis Autophagy 11 2015 1130 1145
20. L. Li, J. Tan, Y. Miao, P. Lei, and Q. Zhang ROS and autophagy: interactions and molecular regulatory mechanisms Cell. Mol. Neurobiol. 35 2015 615 621
21. H.Y. Liu, S.Y. Cao, T. Hong, J. Han, Z. Liu, and W. Cao Insulin is a stronger inducer of insulin resistance than hyperglycemia in mice with type 1 diabetes mellitus (T1DM) J. Biol. Chem. 2009 27090 27100
22. X. Liu, Y. Niu, H. Yuan, J. Huang, and L. Fu AMPK binds to Sestrins and mediates the effect of exercise to increase insulin-sensitivity through autophagy Metabolism 64 2015 658 665
23. Y. Liu, R. Palanivel, E. Rai, M. Park, T.V. Gabor, M.P. Scheid, and et al. Adiponectin stimulates autophagy and reduces oxidative stress to enhance insulin sensitivity during high-fat diet feeding in mice Diabetes 2015 36 48
24. P. Lv, J. Huang, J. Yang, Y. Deng, J. Xu, X. Zhang, and et al. Autophagy in muscle of glucose-infusion hyperglycemia rats and streptozotocin-induced hyperglycemia rats via selective activation of m-TOR or FoxO3 PLoS One 9 2014 e87254
25. A.J. Meijer, S. Lorin, E.F. Blommaart, and P. Codogno Regulation of autophagy by amino acids and MTOR-dependent signal transduction Amino Acids 2014
26. M. Miyauchi, M. Toyoda, K. Kobayashi, M. Abe, T. Kobayashi, M. Kato, and et al. Hypertrophy and loss of podocytes in diabetic nephropathy Intern. Med. 48 2009 1615 1620
27. K. Moreau, B. Ravikumar, M. Renna, C. Puri, and D.C. Rubinsztein Autophagosome precursor maturation requires homotypic fusion Cell 146 2011 303 317
28. P. Mundel, and S.J. Shankland Podocyte biology and response to injury J. Am. Soc. Nephrol. 13 2002 3005 3015
29. U. Nair, A. Jotwani, J. Geng, N. Gammoh, D. Richerson, W.L. Yen, and et al. SNARE proteins are required for macroautophagy Cell 146 2011 290 302
30. T. Oshima, F.S. Laroux, L.L. Coe, Z. Morise, S. Kawachi, P. Bauer, and et al. Interferon-gamma and interleukin-10 reciprocally regulate endothelial junction integrity and barrier function Microvasc. Res. 61 2001 130 143
31. M.E. Pagtalunan, P.L. Miller, S. Jumping-Eagle, R.G. Nelson, B.D. Myers, H.G. Rennke, and et al. Podocyte loss and progressive glomerular injury in type II diabetes J. Clin. Invest. 99 1997 342 348
32. L. Petrica, A. Vlad, G. Gluhovschi, F. Gadalean, V. Dumitrascu, C. Gluhovschi, and et al. Proximal tubule dysfunction is associated with podocyte damage biomarkers nephrin and vascular endothelial growth factor in type 2 diabetes mellitus patients: a cross-sectional study PLoS One 2014 e112538
33. A. Piwkowska, D. Rogacka, I. Audzeyenka, M. Jankowski, and S. Angielski High glucose concentration affects the oxidant-antioxidant balance in cultured mouse podocytes J. Cell. Biochem. 112 2011 1661 1672
34. A. Piwkowska, D. Rogacka, M. Kasztan, S. Angielski, and M. Jankowski Insulin increases glomerular filtration barrier permeability through dimerization of protein kinase G type Ialpha subunits Biochim. Biophys. Acta 1832 2013 791 804
35. R. Pyram, A. Kansara, M.A. Banerji, and L. Loney-Hutchinson Chronic kidney disease and diabetes Maturitas 71 2012 94 103
36. Y. Qi, Z. Xu, Q. Zhu, C. Thomas, R. Kumar, H. Feng, and et al. Myocardial loss of IRS1 and IRS2 causes heart failure and is controlled by p38alpha MAPK during insulin resistance Diabetes 2013 3887 3900
37. J. Satriano, and K. Sharma Autophagy and metabolic changes in obesity-related chronic kidney disease Nephrol. Dial. Transplant. 28 Suppl 4 2013 iv29 36
38. L. Shang, S. Chen, F. Du, S. Li, L. Zhao, and X. Wang Nutrient starvation elicits an acute autophagic response mediated by Ulk1 dephosphorylation and its subsequent dissociation from AMPK Proc. Natl. Acad. Sci. U. S. A. 108 2011 4788 4793
39. L. Shi, T. Zhang, Y. Zhou, X. Zeng, L. Ran, Q. Zhang, and et al. Dihydromyricetin improves skeletal muscle insulin sensitivity by inducing autophagy via the AMPK-PGC-1alpha-sirt3 signaling pathway Endocrine 2015
40. A. Tagawa, M. Yasuda, S. Kume, K. Yamahara, J. Nakazawa, M. Chin-Kanasaki, and et al. Impaired podocyte autophagy exacerbates proteinuria in diabetic nephropathy Diabetes 65 2016 755 767
41. T. Weide, and T.B. Huber Signaling at the slit: podocytes chat by synaptic transmission J. Am. Soc. Nephrol. 2009 1862 1864
42. J.E. Wiggins, M. Goyal, S.K. Sanden, B.L. Wharram, K.A. Shedden, D.E. Misek, and et al. Podocyte hypertrophy, adaptation, and 'decompensation' associated with glomerular enlargement and glomerulosclerosis in the aging rat: prevention by calorie restriction J. Am. Soc. Nephrol. 16 2005 2953 2966
43. K. Yamahara, M. Yasuda, S. Kume, D. Koya, H. Maegawa, and T. Uzu The role of autophagy in the pathogenesis of diabetic nephropathy J. Diabetes Res. 2013 2013 193757
44. Z. Yang, and D.J. Klionsky Mammalian autophagy: core molecular machinery and signaling regulation Curr. Opin. Cell Biol. 22 2010 124 131
45. J. Zhang, J. Ou, Y. Bashmakov, J.D. Horton, M.S. Brown, and J.L. Goldstein Insulin inhibits transcription of IRS-2 gene in rat liver through an insulin response element (IRE) that resembles IREs of other insulin-repressed genes Proc. Natl. Acad. Sci. U. S. A. 2001 3756 3761
46. Y. Zhang, M. Ye, L.J. Chen, M. Li, Z. Tang, and C. Wang Role of the ubiquitin-proteasome system and autophagy in regulation of insulin sensitivity in serum-starved 3T3-L1 adipocytes Endocr. J. 62 2015 673 686
47. L. Zhou, J. Zhang, Q. Fang, M. Liu, X. Liu, W. Jia, and et al. Autophagy-mediated insulin receptor down-regulation contributes to endoplasmic reticulum stress-induced insulin resistance Mol. Pharmacol. 76 2009 596 603