The uremic toxin indoxyl sulfate exacerbates reactive oxygen species production and inflammation in 3T3-L1 adipose cells

Free Radical Research

Volumn 50, Issue 3, 2016, Pages 337-344

  Stockler Pinto, Milena B ^a   Saldanha, Juliana F ^a   Yi, Dan ^b   Mafra, Denise ^a   Fouque, Denis ^b,c   Soulage, Christophe O ^b  

^a FLUMINENSE FEDERAL UNIVERSITY   (Brazil)

^b UNIVERSITÉ DE LYON   (France)

^c CENTRE HOSPITALIER LYON SUD   (France)

Author keywords

Antioxidant; cardiovascular; cytokines

Indexed keywords

ALLOPURINOL; APOCYNIN; INDICAN; INTERLEUKIN 6; N(G) NITROARGININE METHYL ESTER; NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE; OXIDOREDUCTASE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE; ROTENONE; TUMOR NECROSIS FACTOR ALPHA; UREMIC TOXIN; TOXIN; TUMOR NECROSIS FACTOR;

3T3 CELL LINE; ADIPOSE TISSUE CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CELL ISOLATION; CLINICAL FEATURE; CONCENTRATION PROCESS; CONTROLLED STUDY; CYTOKINE PRODUCTION; DISEASE EXACERBATION; ENZYME ACTIVATION; ENZYME INHIBITION; HUMAN; INFLAMMATION; MOUSE; NONHUMAN; OXIDATIVE STRESS; PROTEIN SECRETION; WHITE ADIPOSE TISSUE; 3T3-L1 CELL LINE; ADIPOCYTE; ANIMAL; CHRONIC KIDNEY FAILURE; COMPLICATION; DRUG EFFECTS; METABOLISM; PATHOLOGY; SECRETION (PROCESS); UREMIA;

3T3-L1 CELLS; ADIPOCYTES; ANIMALS; INDICAN; INFLAMMATION; INTERLEUKIN-6; MICE; NADPH OXIDASE; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; RENAL INSUFFICIENCY, CHRONIC; TOXINS, BIOLOGICAL; TUMOR NECROSIS FACTOR-ALPHA; UREMIA;

EID: 84955666773     PISSN: 10715762     EISSN: 10292470     Source Type: Journal    
DOI: 10.3109/10715762.2015.1125996     Document Type: Article

References (40)

1. Home - Eutox - European Uremic Toxin (EUTox) Work Group of the ESAO and endorsed work group of the ERAEDTA. Available from: www.uremic-toxins.org [last accessed 1 Sept 2015].
2. Duranton F, Cohen G, De Smet R, Rodriguez M, Jankowski J, Vanholder R, Argiles A, et al. Normal and pathologic concentrations of uremic toxins. J Am Soc Nephrol 2012;23:1258-1270.
3. Sallée M, Dou L, Cerini C, Poitevin S, Brunet P, Burtey S. The aryl hydrocarbon receptor-activating effect of uremic toxins from tryptophan metabolism: a new concept to understand cardiovascular complications of chronic kidney disease. Toxins (Basel) 2014;6:934-949.
4. Ito S, Yoshida M. Protein-bound uremic toxins: new culprits of cardiovascular events in chronic kidney disease patients. Toxins (Basel) 2014;6:665-678.
5. Mafra D, Lobo JC, Barros AF, Koppe L, Vaziri ND, Fouque D. Role of altered intestinal microbiota in systemic inflammation and cardiovascular disease in chronic kidney disease. Future Microbiol 2014;9:399-410.
6. Cruz EF, da Cendoroglo M, Manfredi SR, Canziani ME, Quinto BMR, Grabulosa CC, et al. Effect of indoxyl sulfate on oxidative stress, apoptosis, and monocyte chemoattractant protein-1 in leukocytes. Int Sch Res Not 2014;2014:e412389.
7. Shimizu H, Hirose Y, Nishijima F, Tsubakihara Y, Miyazaki H. ROS and PDGF-beta [corrected] receptors are critically involved in indoxyl sulfate actions that promote vascular smooth muscle cell proliferation and migration. Am J Physiol Cell Physiol 2009;297:C389-C396.
8. Watanabe H, Miyamoto Y, Otagiri M, Maruyama T. Update on the pharmacokinetics and redox properties of proteinbound uremic toxins. J Pharm Sci 2011;100:3682-3695.
9. Ito S, Osaka M, Higuchi Y, Nishijima F, Ishii H, Yoshida M. Indoxyl sulfate induces leukocyte-endothelial interactions through up-regulation of E-selectin. J Biol Chem 2010;285:38869-38875.
10. Adelibieke Y, Shimizu H, Muteliefu G, Bolati D, Niwa T. Indoxyl sulfate induces endothelial cell senescence by increasing reactive oxygen species production and p53 activity. J Ren Nutr 2012;22:86-89.
11. Adesso S, Popolo A, Bianco G, Sorrentino R, Pinto A, Autore G, Marzocco S. The uremic toxin indoxyl sulphate enhances macrophage response to LPS. PLoS One 2013;8:e76778.
12. Shimizu H, Yisireyili M, Higashiyama Y, Nishijima F, Niwa T. Indoxyl sulfate upregulates renal expression of ICAM-1 via production of ROS and activation of NF-κB and p53 in proximal tubular cells. Life Sci 2013;92:143-148.
13. Gelasco AK, Raymond JR. Indoxyl sulfate induces complex redox alterations in mesangial cells. Am J Physiol Renal Physiol 2006;290:F1551-F1558.
14. Masai N, Tatebe J, Yoshino G, Morita T. Indoxyl sulfate stimulates monocyte chemoattractant protein-1 expression in human umbilical vein endothelial cells by inducing oxidative stress through activation of the NADPH oxidase-nuclear factor-kB pathway. Circ J 2010;74:2216-2224.
15. Lafontan M. Adipose tissue and adipocyte dysregulation. Diabetes Metab 2014;40:16-28.
16. Crujeiras AB, Díaz-Lagares A, Carreira MC, Amil M, Casanueva FF. Oxidative stress associated to dysfunctional adipose tissue: a potential link between obesity, type 2 diabetes mellitus and breast cancer. Free Radic Res 2013;47:243-256.
17. Bondia-Pons I, Ryan L, Martinez JA. Oxidative stress and inflammation interactions in human obesity. J Physiol Biochem 2012;68:701-711.
18. Furukawa S, Fujita T, Shimabukuro M, Iwaki M, Yamada Y, Nakajima Y, et al. Increased oxidative stress in obesity and its impact on metabolic syndrome. J Clin Invest 2004;114:1752-1761.
19. Cohen G, Glorieux G, Thornalley P, Schepers E, Meert N, Jankowski J, et al. Review on uraemic toxins III: recommendations for handling uraemic retention solutes in vitro - towards a standardized approach for research on uraemia. Nephrol Dial Transplant 2007;22:3381-3390.
20. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976;72:248-254.
21. Grotto D, Santa Maria LD, Boeira S, Valentini J, Charão MF, Moro AM, et al. Rapid quantification of malondialdehyde in plasma by high performance liquid chromatography visible detection. J Pharm Biomed Anal 2007;43:619-624.
22. Onat A, Can G. Enhanced proinflammatory state and autoimmune activation: a breakthrough to understanding chronic diseases. Curr Pharm Des 2014;20:575-584.
23. Rutkowski P, Malgorzewicz S, Slominska E, Renke M, Lysiak-Szydlowska W, Swierczynski J, Rutkowski B. Interrelationship between uremic toxicity and oxidative stress. J Ren Nutr 2006;16:190-193.
24. Motojima M, Hosokawa A, Yamato H, Muraki T, Yoshioka T. Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-kappaB and free radical in proximal tubular cells. Kidney Int 2003;63:1671-1680.
25. Muteliefu G, Enomoto A, Jiang P, Takahashi M, Niwa T. Indoxyl sulphate induces oxidative stress and the expression of osteoblast-specific proteins in vascular smooth muscle cells. Nephrol Dial Transplant 2009;24:2051-2058.
26. Tumur Z, Niwa T. Indoxyl sulfate inhibits nitric oxide production and cell viability by inducing oxidative stress in vascular endothelial cells. Am J Nephrol 2009;29:551-557.
27. Yang K, Nie L, Huang Y, Zhang J, Xiao T, Guan X, Zhao J. Amelioration of uremic toxin indoxyl sulfate-induced endothelial cell dysfunction by Klotho protein. Toxicol Lett 2012;215:77-83.
28. Yang K, Xu X, Nie L, Xiao T, Guan X, He T, et al. Indoxyl sulfate induces oxidative stress and hypertrophy in cardiomyocytes by inhibiting the AMPK/UCP2 signaling pathway. Toxicol Lett 2015;234:110-119.
29. Liu GS, Chan EC, Higuchi M, Dusting GJ, Jiang F. Redox mechanisms in regulation of adipocyte differentiation: beyond a general stress response. Cells 2012;1:976-993.
30. Mouche S, Mkaddem SB, Wang W, Katic M, Tseng YH, Carnesecchi S, et al. Reduced expression of the NADPH oxidase NOX4 is a hallmark of adipocyte differentiation. Biochim Biophys Acta 2007;1773:1015-1027.
31. Schröder K, Wandzioch K, Helmcke I, Brandes RP. Nox4 acts as a switch between differentiation and proliferation in preadipocytes. Arterioscler Thromb Vasc Biol 2009;29: 239-245.
32. Kanda Y, Hinata T, Kang SW, Watanabe Y. Reactive oxygen species mediate adipocyte differentiation in mesenchymal stem cells. Life Sci 2011;89:250-258.
33. Li Y, Mouche S, Sajic T, Veyrat-Durebex C, Supale R, Pierroz D, et al. Deficiency in the NADPH oxidase 4 predisposes towards diet-induced obesity. Int J Obes (Lond) 2012;36:1503-1513.
34. Martyn KD, Frederick LM, von Loehneysen K, Dinauer MC, Knaus UG. Functional analysis of Nox4 reveals unique characteristics compared to other NADPH oxidases. Cell Signal 2006;18:69-82.
35. von Löhneysen K, Noack D, Wood MR, Friedman JS, Knaus UG. Structural insights into Nox4 and Nox2: motifs involved in function and cellular localization. Mol Cell Biol 2010;30:961-975.
36. Brown DI, Griendling KK. Nox proteins in signal transduction. Free Radic Biol Med 2009;47:1239-1253.
37. Silverstein DM. Inflammation in chronic kidney disease: role in the progression of renal and cardiovascular disease. Pediatr Nephrol 2009;24:1445-1452.
38. Bolati D, Shimizu H, Yisireyili M, Nishijima F, Niwa T. Indoxyl sulfate, a uremic toxin, downregulates renal expression of Nrf2 through activation of NF-κB. BMC Nephrol 2013;14:56.
39. Lekawanvijit S, Adrahtas A, Kelly DJ, Kompa AR, Wang BH, Krum H. Does indoxyl sulfate, a uraemic toxin, have direct effects on cardiac fibroblasts and myocytes? Eur Heart J 2010;31:1771-1779.
40. Koppe L, Pillon NJ, Vella RE, Croze ML, Pelletier CC, Chambert S, et al. p-Cresyl sulfate promotes insulin resistance associated with CKD. J Am Soc Nephrol 2013;24:88-99.