Oxidative stress induces claudin-2 nitration in experimental type 1 diabetic nephropathy

Free Radical Biology and Medicine

Volumn 72, Issue , 2014, Pages 162-175

  Molina Jijón, Eduardo ^a   Rodríguez Muñoz, Rafael ^a   Namorado, María Del Carmen ^a   Pedraza Chaverri, José ^b   Reyes, José L ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

Claudins; Free radicals; Glucose transporters; Oxidative stress; Protein tyrosine nitration; Renal tight junctions

Indexed keywords

ALPHA TUBULIN; BUTYLCRESOL; CLAUDIN 1; CLAUDIN 2; CLAUDIN 4; CLAUDIN 5; CLAUDIN 8; ENDOTHELIAL NITRIC OXIDE SYNTHASE; GLUCOSE; GLUCOSE TRANSPORTER; GLUCOSE TRANSPORTER 1; GLUCOSE TRANSPORTER 2; KIDNEY INJURY MOLECULE 1; LUCIGENIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; OCCLUDIN; PROTEIN KINASE C BETA; PROTEIN ZO1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; SODIUM GLUCOSE COTRANSPORTER 1; SODIUM GLUCOSE COTRANSPORTER 2; SUCCINIC ACID; SUPEROXIDE DISMUTASE; TYROSINE; XANTHINE; XANTHINE OXIDASE; CLAUDIN; CLDN2 PROTEIN, RAT; TIGHT JUNCTION PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CREATININE CLEARANCE; DIABETIC NEPHROPATHY; DISEASE ASSOCIATION; ENZYME ACTIVATION; FEMALE; FLUID INTAKE; FOOD INTAKE; GLUCOSE BLOOD LEVEL; INSULIN DEPENDENT DIABETES MELLITUS; KIDNEY CORTEX; KIDNEY DISTAL TUBULE; KIDNEY FUNCTION; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE; LIPID PEROXIDATION; MEAN ARTERIAL PRESSURE; NATRIURESIS; NITRATION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEINURIA; RAT; URINE VOLUME; ANIMAL; COMPLICATION; EXPERIMENTAL DIABETES MELLITUS; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; METABOLISM; OXIDATION REDUCTION REACTION; PHYSIOLOGY; WESTERN BLOTTING; WISTAR RAT;

ANIMALS; BLOTTING, WESTERN; CLAUDINS; DIABETES MELLITUS, EXPERIMENTAL; DIABETES MELLITUS, TYPE 1; DIABETIC NEPHROPATHIES; FEMALE; FLUORESCENT ANTIBODY TECHNIQUE; IMMUNOPRECIPITATION; OXIDATION-REDUCTION; OXIDATIVE STRESS; RATS; RATS, WISTAR; TIGHT JUNCTION PROTEINS;

EID: 84900494381     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2014.03.040     Document Type: Article

References (56)

1. R.C. Stanton Oxidative stress and diabetic kidney disease Curr. Diabetes Rep. 11 2011 330 336
2. M.L. Caramori, and M. Mauer Diabetes and nephropathy Curr. Opin. Nephrol. Hypertens. 12 2003 273 282
3. A.T. Reutens, and R.C. Atkins Epidemiology of diabetic nephropathy Contrib. Nephrol. 170 2011 1 7
4. C.E. Mogensen Glomerular filtration rate and renal plasma flow in short-term and long-term juvenile diabetes mellitus Scand. J. Clin. Lab. Invest. 28 1971 91 100
5. B. Najafian, and M. Mauer Progression of diabetic nephropathy in type 1 diabetic patients Diabetes Res. Clin. Pract. 83 2009 1 8
6. R. Komers, and M.E. Cooper Renal sodium handling in experimental diabetes: role of NO Nephrol. Dial. Transplant. 11 1996 2170 2177
7. M.S. Bitar, S. Wahid, S. Mustafa, E. Al-Saleh, G.S. Dhaunsi, and F. Al-Mulla Nitric oxide dynamics and endothelial dysfunction in type II model of genetic diabetes Eur. J. Pharmacol. 511 2005 53 64
8. T. Inoguchi, T. Sonta, H. Tsubouchi, T. Etoh, M. Kakimoto, N. Sonoda, N. Sato, N. Sekiguchi, K. Kobayashi, H. Sumimoto, H. Utsumi, and H. Nawata Protein kinase C-dependent increase in reactive oxygen species (ROS) production in vascular tissues of diabetes: role of vascular NAD(P)H oxidase J. Am. Soc. Nephrol. 14 2003 S227 S232
9. G. Wolf New insights into the pathophysiology of diabetic nephropathy: from haemodynamics to molecular pathology Eur. J. Clin. Invest. 34 2004 785 796
10. J. Hou, M. Rajagopal, and A.S. Yu Claudins and the kidney Annu. Rev. Physiol. 75 2013 479 501
11. M. Furuse, T. Hirase, M. Itoh, A. Nagafuchi, S. Yonemura, S. Tsukita, and S. Tsukita Occludin: a novel integral membrane protein localizing at tight junctions J. Cell Biol. 123 1993 1777 1788
12. M. Furuse, K. Fujita, T. Hiiragi, K. Fujimoto, and S. Tsukita Claudin-1 and -2: novel integral membrane proteins localizing at tight junctions with no sequence similarity to occludin J. Cell Biol. 141 1998 1539 1550
13. O. Kwon, B.D. Myers, R. Sibley, D. Dafoe, E. Alfrey, and W.J. Nelson Distribution of cell membrane-associated proteins along the human nephron J. Histochem. Cytochem. 46 1998 1423 1434
14. J.L. Reyes, M. Lamas, D. Martin, M. del Carmen Namorado, S. Islas, J. Luna, M. Tauc, and L. Gonzalez-Mariscal The renal segmental distribution of claudins changes with development Kidney Int. 62 2002 476 487
15. M. Lal-Nag, and P.J. Morin The claudins Genome Biol. 10 2009 235
16. K. Mineta, Y. Yamamoto, Y. Yamazaki, H. Tanaka, Y. Tada, K. Saito, A. Tamura, M. Igarashi, T. Endo, K. Takeuchi, and S. Tsukita Predicted expansion of the claudin multigene family FEBS Lett. 585 2011 606 612
17. A.S. Fanning, B.J. Jameson, L.A. Jesaitis, and J.M. Anderson The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton J. Biol. Chem. 273 1998 29745 29753
18. A.G. Howarth, and B.R. Stevenson Molecular environment of ZO-1 in epithelial and non-epithelial cells Cell Motil. Cytoskeleton 31 1995 323 332
19. K. Umeda, T. Matsui, M. Nakayama, K. Furuse, H. Sasaki, M. Furuse, and S. Tsukita Establishment and characterization of cultured epithelial cells lacking expression of ZO-1 J. Biol. Chem. 279 2004 44785 44794
20. A.H. Enck, U.V. Berger, and A.S. Yu Claudin-2 is selectively expressed in proximal nephron in mouse kidney Am. J. Physiol. Renal Physiol 281 2001 F966 F974
21. Y. Kiuchi-Saishin, S. Gotoh, M. Furuse, A. Takasuga, Y. Tano, and S. Tsukita Differential expression patterns of claudins, tight junction membrane proteins, in mouse nephron segments J. Am. Soc. Nephrol. 13 2002 875 886
22. R. Rosenthal, S. Milatz, S.M. Krug, B. Oelrich, J.D. Schulzke, S. Amasheh, D. Gunzel, and M. Fromm Claudin-2, a component of the tight junction, forms a paracellular water channel J. Cell Sci. 123 2010 1913 1921
23. L. Gonzalez-Mariscal, C. Namorado Mdel, D. Martin, G. Sierra, and J.L. Reyes The tight junction proteins claudin-7 and -8 display a different subcellular localization at Henle's loops and collecting ducts of rabbit kidney Nephrol. Dial. Transplant. 21 2006 2391 2398
24. H. Wen, D.D. Watry, M.C. Marcondes, and H.S. Fox Selective decrease in paracellular conductance of tight junctions: role of the first extracellular domain of claudin-5 Mol. Cell. Biol. 24 2004 8408 8417
25. R. Koda, L. Zhao, E. Yaoita, Y. Yoshida, S. Tsukita, A. Tamura, M. Nameta, Y. Zhang, H. Fujinaka, S. Magdeldin, B. Xu, I. Narita, and T. Yamamoto Novel expression of claudin-5 in glomerular podocytes Cell Tissue Res. 343 2011 637 648
26. 2+) disrupts intercellular junctions and actin filaments in LLC-PK1 cells Toxicol. Appl. Pharmacol. 107 1991 81 97
27. G. Jacquillet, O. Barbier, M. Cougnon, M. Tauc, M.C. Namorado, D. Martin, J.L. Reyes, and P. Poujeol Zinc protects renal function during cadmium intoxication in the rat Am. J. Physiol. Renal Physiol. 290 2006 F127 F137
28. L. Arreola-Mendoza, L.M. Del Razo, M.E. Mendoza-Garrido, D. Martin, M.C. Namorado, J.V. Calderon-Salinas, and J.L. Reyes The protective effect of alpha-tocopherol against dichromate-induced renal tight junction damage is mediated via ERK1/2 Toxicol. Lett. 191 2009 279 288
29. J.L. Reyes, E. Molina-Jijon, R. Rodriguez-Munoz, P. Bautista-Garcia, Y. Debray-Garcia, and M.D. Namorado Tight junction proteins and oxidative stress in heavy metals-induced nephrotoxicity BioMed Res. Int. 2013 2013 730789
30. T.N. Meyer, C. Schwesinger, J. Ye, B.M. Denker, and S.K. Nigam Reassembly of the tight junction after oxidative stress depends on tyrosine kinase activity J. Biol. Chem. 276 2001 22048 22055
31. H. Rincon-Choles, T.L. Vasylyeva, P.E. Pergola, B. Bhandari, K. Bhandari, J.H. Zhang, W. Wang, Y. Gorin, J.L. Barnes, and H.E. Abboud ZO-1 expression and phosphorylation in diabetic nephropathy Diabetes 55 2006 894 900
32. L. Arreola-Mendoza, J.L. Reyes, E. Melendez, D. Martin, M.C. Namorado, E. Sanchez, and L.M. Del Razo Alpha-tocopherol protects against the renal damage caused by potassium dichromate Toxicology 218 2006 237 246
33. P. Bautista-Garcia, J.L. Reyes, D. Martin, M.C. Namorado, B. Chavez-Munguia, E. Soria-Castro, O. Huber, and L. Gonzalez-Mariscal Zona occludens-2 protects against podocyte dysfunction induced by ADR in mice Am. J. Physiol. Renal Physiol. 304 2013 F77 F87
34. M.H. Zou, C. Shi, and R.A. Cohen Oxidation of the zinc-thiolate complex and uncoupling of endothelial nitric oxide synthase by peroxynitrite J. Clin. Invest. 109 2002 817 826
35. R. Gonzalez-Ramirez, S.L. Morales-Lazaro, V. Tapia-Ramirez, D. Mornet, and B. Cisneros Nuclear and nuclear envelope localization of dystrophin Dp71 and dystrophin-associated proteins (DAPs) in the C2C12 muscle cells: DAPs nuclear localization is modulated during myogenesis J. Cell. Biochem. 105 2008 735 745
36. E. Molina-Jijon, E. Tapia, C. Zazueta, M. El Hafidi, Z.L. Zatarain-Barron, R. Hernandez-Pando, O.N. Medina-Campos, G. Zarco-Marquez, I. Torres, and J. Pedraza-Chaverri Curcumin prevents Cr(VI)-induced renal oxidant damage by a mitochondrial pathway Free Radic. Biol. Med. 51 2011 1543 1557
37. M. Orozco-Ibarra, O.N. Medina-Campos, D.J. Sanchez-Gonzalez, C.M. Martinez-Martinez, E. Floriano-Sanchez, A. Santamaria, V. Ramirez, N.A. Bobadilla, and J. Pedraza-Chaverri Evaluation of oxidative stress in D-serine induced nephrotoxicity Toxicology 229 2007 123 135
38. Y. Gorin, K. Block, J. Hernandez, B. Bhandari, B. Wagner, J.L. Barnes, and H.E. Abboud Nox4 NAD(P)H oxidase mediates hypertrophy and fibronectin expression in the diabetic kidney J. Biol. Chem. 280 2005 39616 39626
39. A.B. Kramer, M.M. van Timmeren, T.A. Schuurs, V.S. Vaidya, J.V. Bonventre, H. van Goor, and G. Navis Reduction of proteinuria in adriamycin-induced nephropathy is associated with reduction of renal kidney injury molecule (Kim-1) over time Am. J. Physiol. Renal Physiol. 296 2009 F1136 F1145
40. J.V. Bonventre Kidney injury molecule-1 (KIM-1): a urinary biomarker and much more Nephrol. Dial. Transplant. 24 2009 3265 3268
41. C.J. Bailey Renal glucose reabsorption inhibitors to treat diabetes Trends Pharmacol. Sci. 32 2011 63 71
42. H. Ha, and H.B. Lee Reactive oxygen species amplify glucose signalling in renal cells cultured under high glucose and in diabetic kidney Nephrology 10 Suppl 2005 (S7-10)
43. P.F. Mount, and D.A. Power Nitric oxide in the kidney: functions and regulation of synthesis Acta Physiol. 187 2006 433 446
44. U. Forstermann, and T. Munzel Endothelial nitric oxide synthase in vascular disease: from marvel to menace Circulation 113 2006 1708 1714
45. R. Radi Nitric oxide, oxidants, and protein tyrosine nitration Proc. Natl. Acad. Sci. USA 101 2004 4003 4008
46. C.A. Berry, and F.C. Rector Jr. Mechanism of proximal NaCl reabsorption in the proximal tubule of the mammalian kidney Semin. Nephrol. 11 1991 86 97
47. V. Vallon, and S.C. Thomson Anomalous role for dietary salt in diabetes mellitus? Nat. Rev. Endocrinol. 7 2011 377 378
48. E.I. Ekinci, S. Clarke, M.C. Thomas, J.L. Moran, K. Cheong, R.J. MacIsaac, and G. Jerums Dietary salt intake and mortality in patients with type 2 diabetes Diabetes Care 34 2011 703 709
49. B. Kalyanaraman, V. Darley-Usmar, K.J. Davies, P.A. Dennery, H.J. Forman, M.B. Grisham, G.E. Mann, K. Moore, L.J. Roberts 2nd, and H. Ischiropoulos Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Free Radic. Biol. Med. 52 2012 1 6
50. H. Zhao, J. Joseph, H.M. Fales, E.A. Sokoloski, R.L. Levine, J. Vasquez-Vivar, and B. Kalyanaraman Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence Proc. Natl. Acad. Sci. USA 102 2005 5727 5732
51. M. Satoh, S. Fujimoto, Y. Haruna, S. Arakawa, H. Horike, N. Komai, T. Sasaki, K. Tsujioka, H. Makino, and N. Kashihara NAD(P)H oxidase and uncoupled nitric oxide synthase are major sources of glomerular superoxide in rats with experimental diabetic nephropathy Am. J. Physiol. Renal Physiol. 288 2005 F1144 F1152
52. A. Daiber, S. Daub, M. Bachschmid, S. Schildknecht, M. Oelze, S. Steven, P. Schmidt, A. Megner, M. Wada, T. Tanabe, T. Munzel, S. Bottari, and V. Ullrich Protein tyrosine nitration and thiol oxidation by peroxynitrite-strategies to prevent these oxidative modifications Int. J. Mol. Sci. 14 2013 7542 7570
53. C. Le Moellic, S. Boulkroun, D. Gonzalez-Nunez, I. Dublineau, F. Cluzeaud, M. Fay, M. Blot-Chabaud, and N. Farman Aldosterone and tight junctions: modulation of claudin-4 phosphorylation in renal collecting duct cells Am. J. Physiol. Cell Physiol. 289 2005 C1513 C1521
54. + absorption defends from paracellular back-leakage by claudin-8 upregulation Biochem. Biophys. Res. Commun. 378 2009 45 50
55. K. Yamauchi, T. Rai, K. Kobayashi, E. Sohara, T. Suzuki, T. Itoh, S. Suda, A. Hayama, S. Sasaki, and S. Uchida Disease-causing mutant WNK4 increases paracellular chloride permeability and phosphorylates claudins Proc. Natl. Acad. Sci. USA 101 2004 4690 4694
56. Y. Yamazaki, R. Tokumasu, H. Kimura, and S. Tsukita Role of claudin species-specific dynamics in reconstitution and remodeling of the zonula occludens Mol. Biol. Cell 22 2011 1495 1504