Nitration of indoxyl sulfate facilitates its cytotoxicity in human renal proximal tubular cells via expression of heme oxygenase-1

Biochemical and Biophysical Research Communications

Volumn 465, Issue 3, 2015, Pages 481-487

  Ishima, Yu ^a   Narisoko, Toru ^a   Kragh Hansen, Ulrich ^b   Kotani, Shunsuke ^a   Nakajima, Makoto ^a   Otagiri, Masaki ^c   Maruyama, Toru ^a  

^a KUMAMOTO UNIVERSITY   (Japan)

^b AARHUS UNIVERSITY   (Denmark)

^c SOJO UNIVERSITY   (Japan)

Author keywords

Heme oxygenase 1; Indoxyl sulfate; NADPH oxidase; Nitration; Peroxynitrite; Reactive oxygen species

Indexed keywords

HEME OXYGENASE 1; INDICAN; ORGANIC ANION TRANSPORTER; PEROXYNITRITE; REACTIVE OXYGEN METABOLITE; NITRO DERIVATIVE; PEROXYNITROUS ACID;

ARTICLE; CELL DEATH; CELL SURVIVAL; CELL VIABILITY; DRUG CYTOTOXICITY; FENTON REACTION; HUMAN; HUMAN CELL; IMMUNOFLUORESCENCE; IN VITRO STUDY; KIDNEY PROXIMAL TUBULE; KIDNEY TUBULE CELL; NITRATION; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTON NUCLEAR MAGNETIC RESONANCE; WESTERN BLOTTING; CELL LINE; CHEMISTRY; CYTOLOGY; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SYNTHESIS;

CELL LINE; CELL SURVIVAL; DOSE-RESPONSE RELATIONSHIP, DRUG; HEME OXYGENASE-1; HUMANS; INDICAN; KIDNEY TUBULES, PROXIMAL; NITRO COMPOUNDS; PEROXYNITROUS ACID;

EID: 84940935216     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2015.08.043     Document Type: Article

References (33)

1. B. Alvarez, H. Rubbo, M. Kirk, and et al. Peroxynitrite-dependent tryptophan nitration Chem. Res. Toxicol. 9 1996 390 396
2. C.C. Winterbourn Reconciling the chemistry and biology of reactive oxygen species Nat. Chem. Biol. 4 2008 278 286
3. C. Szabó, H. Ischiropoulos, and R. Radi Peroxynitrite: biochemistry, pathophysiology and development of therapeutics Nat. Rev. Drug Discov. 6 2007 662 680
4. T.S. Koskenkorva-Frank, G. Weiss, W.H. Koppenol, and et al. The complex interplay of iron metabolism, reactive oxygen species, and reactive nitrogen species: insights into the potential of various iron therapies to induce oxidative and nitrosative stress Free Radic. Biol. Med. 65 2013 1174 1194
5. K.M. Nash, A. Rockenbauer, and F.A. Villamena Reactive nitrogen species reactivities with nitrones: theoretical and experimental studies Chem. Res. Toxicol. 25 2012 1581 1597
6. J.R. Koenitzer, and B.A. Freeman Redox signaling in inflammation: interactions of endogenous electrophiles and mitochondria in cardiovascular disease Ann. N. Y. Acad. Sci. 1203 2010 45 52
7. F.J. Schopfer, P.R. Baker, and B.A. Freeman NO-dependent protein nitration: a cell signaling event or an oxidative inflammatory response? Trends Biochem. Sci. 28 2003 646 654
8. T. Sawa, M.H. Zaki, T. Okamoto, and et al. Protein S-guanylation by the biological signal 8-nitroguanosine 3',5'-cyclic monophosphate Nat. Chem. Biol. 3 2007 727 735
9. M. Feelisch Nitrated cyclic GMP as a new cellular signal Nat. Chem. Biol. 3 2007 687 688
10. T. Akaike, M. Nishida, and S. Fujii Regulation of redox signalling by an electrophilic cyclic nucleotide J. Biochem. 153 2013 131 138
11. N.K. Khoo, V. Rudolph, M.P. Cole, and et al. Activation of vascular endothelial nitric oxide synthase and heme oxygenase-1 expression by electrophilic nitro-fatty acids Free Radic. Biol. Med. 48 2010 230 239
12. L. Villacorta, L. Chang, S.R. Salvatore, and et al. Electrophilic nitro-fatty acids inhibit vascular inflammation by disrupting LPS-dependent TLR4 signalling in lipid rafts Cardiovasc. Res. 98 2013 116 124
13. N.K. Khoo, and B.A. Freeman Electrophilic nitro-fatty acids: anti-inflammatory mediators in the vascular compartment Curr. Opin. Pharmacol. 10 2010 179 184
14. K. Ikeda, H.B. Yukihiro, H. Iwai, and et al. Detection of 6-nitrotryptophan in proteins by Western blot analysis and its application for peroxynitrite-treated PC12 cells Nitric Oxide 16 2007 18 28
15. T. Nuriel, A. Hansler, and S.S. Gross Protein nitrotryptophan: formation, significance and identification J. Proteomics 74 2011 2300 2312
16. S. Fujii, T. Sawa, H. Ihara, and et al. The critical role of nitric oxide signaling, via protein S-guanylation and nitrated cyclic GMP, in the antioxidant adaptive response J. Biol. Chem. 285 2010 23970 23984
17. A. Fortuño, O. Beloqui, G. San José, and et al. Increased phagocytic nicotinamide adenine dinucleotide phosphate oxidase-dependent superoxide production in patients with early chronic kidney disease Kidney Int. Suppl. 99 2005 S71 S75
18. C.C. Sung, Y.C. Hsu, C.C. Chen, and et al. Oxidative stress and nucleic acid oxidation in patients with chronic kidney disease Oxid. Med. Cell Longev. 2013 2013 301982
19. R. Vanholder, R. De Smet, G. Glorieux, and et al. Review on uremic toxins: classification, concentration, and interindividual variability Kidney Int. 63 2003 1934 1943
20. F. Duranton, G. Cohen, R. De Smet, and et al. Normal and pathologic concentrations of uremic toxins J. Am. Soc. Nephrol. 23 2012 1258 1270
21. F.C. Barreto, D.V. Barreto, S. Liabeuf, and et al. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients Clin. J. Am. Soc. Nephrol. 4 2009 1551 1558
22. C.S. Wilcox Asymmetric dimethylarginine and reactive oxygen species: unwelcome twin visitors to the cardiovascular and kidney disease tables Hypertension 59 2012 375 381
23. R. Kissner, and W.H. Koppenol Product distribution of peroxynitrite decay as a function of pH, temperature, and concentration J. Am. Chem. Soc. 121 1999 2438 2443
24. V.B. O'Donnell, J.P. Eiserich, P.H. Chumley, and et al. Nitration of unsaturated fatty acids by nitric oxide-derived reactive nitrogen species peroxynitrite, nitrous acid, nitrogen dioxide, and nitronium ion Chem. Res. Toxicol. 12 1999 83 92
25. A. Kodama, H. Watanabe, R. Tanaka, and et al. Albumin fusion renders thioredoxin an effective anti-oxidative and anti-inflammatory agent for preventing cisplatin-induced nephrotoxicity Biochim. Biophys. Acta 1840 2014 1152 1162
26. H. Watanabe, Y. Miyamoto, M. Otagiri, and et al. Update on the pharmacokinetics and redox properties of protein-bound uremic toxins J. Pharm. Sci. 100 2011 3682 3695
27. Y. Miyamoto, H. Watanabe, M. Otagiri, and et al. New insight into the redox properties of uremic solute indoxyl sulfate as a pro- and anti-oxidant Ther. Apher. Dial. 15 2011 129 131
28. K. Shimoishi, M. Anraku, K. Kitamura, and et al. An oral adsorbent, AST-120 protects against the progression of oxidative stress by reducing the accumulation of indoxyl sulfate in the systemic circulation in renal failure Pharm. Res. 24 2007 1283 1289
29. L. Dou, N. Jourde-Chiche, V. Faure, and et al. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells J. Thromb. Haemost. 5 2007 1302 1308
30. N. Chen, W. Shao, P. Lv, and et al. Hemin-induced Erk1/2 activation and heme oxygenase-1 expression in human umbilical vein endothelial cells Free Radic. Res. 41 2007 990 996
31. P. La, A.P. Fernando, Z. Wang, and et al. Zinc protoporphyrin regulates cyclin D1 expression independent of heme oxygenase inhibition J. Biol. Chem. 284 2009 36302 36311
32. B.S. Cornblatt, L. Ye, and et al. Preclinical and clinical evaluation of sulforaphane for chemoprevention in the breast Carcinogenesis 28 2007 1485 1490
33. D. Bolati, H. Shimizu, and et al. Indoxyl sulfate, a uremic toxin, downregulates renal expression of Nrf2 through activation of NF-κB BMC Nephrol. 14 2013 56