Indoxyl sulfate induces oxidative stress and hypertrophy in cardiomyocytes by inhibiting the AMPK/UCP2 signaling pathway

Toxicology Letters

Volumn 234, Issue 2, 2015, Pages 110-119

  Yang, Ke ^a   Xu, Xinli ^a   Nie, Ling ^a   Xiao, Tangli ^a   Guan, Xu ^a   He, Ting ^a   Yu, Yanlin ^a   Liu, Liang ^a   Huang, Yunjian ^a   Zhang, Jingbo ^a   Zhao, Jinghong ^a  

^a THIRD MILITARY MEDICAL UNIVERSITY   (China)

Author keywords

AMPK; Cardiomyopathy; Indoxyl sulfate; Oxidative stress; Uncoupling protein 2

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; ADENYLATE KINASE; ATRIAL NATRIURETIC FACTOR; BRAIN NATRIURETIC PEPTIDE; INDICAN; MESSENGER RNA; MYOSIN HEAVY CHAIN BETA; REACTIVE OXYGEN METABOLITE; UNCOUPLING PROTEIN 2; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; ION CHANNEL; MITOCHONDRIAL PROTEIN; MITOCHONDRIAL UNCOUPLING PROTEIN 2; OXIDIZING AGENT; PROTEIN KINASE INHIBITOR;

ANIMAL CELL; ARTICLE; CELL VOLUME; CONTROLLED STUDY; DOWN REGULATION; ENZYME INHIBITION; GENE EXPRESSION; HEART HYPERTROPHY; HEART MUSCLE CELL; NEWBORN; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SIGNAL TRANSDUCTION; ANIMAL; ANTAGONISTS AND INHIBITORS; CARDIOMEGALY; CELL CULTURE; CHEMICALLY INDUCED; DOSE RESPONSE; DRUG EFFECTS; ENZYMOLOGY; GENETIC TRANSFECTION; GENETICS; METABOLISM; PATHOLOGY; SPRAGUE DAWLEY RAT; TIME;

RATTUS;

AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANIMALS, NEWBORN; CARDIOMEGALY; CELLS, CULTURED; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; INDICAN; ION CHANNELS; MITOCHONDRIAL PROTEINS; MYOCYTES, CARDIAC; OXIDANTS; OXIDATIVE STRESS; PROTEIN KINASE INHIBITORS; RATS, SPRAGUE-DAWLEY; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSFECTION;

EID: 84923352278     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2015.01.021     Document Type: Article

References (58)

1. Arsenijevic D., Onuma H., Pecqueur C., Raimbault S., Manning B.S., Miroux B., Couplan E., Alves-Guerra M.C., Goubern M., Surwit R., Bouillaud F., Richard D., Collins S., Ricquier D. Disruption of the uncoupling protein-2 gene in mice reveals a role in immunity and reactive oxygen species production. Nat. Genet. 2000, 26:435-439.
2. Barreto F.C., Barreto D.V., Liabeuf S., Meert N., Glorieux G., Temmar M., Choukroun G., Vanholder R., Massy Z.A. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin. J. Am. Soc. Nephrol. 2009, 4:1551-1558.
3. Bechmann I., Diano S., Warden C.H., Bartfai T., Nitsch R., Horvath T.L. Brain mitochondrial uncoupling protein 2 (UCP2): a protective stress signal in neuronal injury. Biochem. Pharmacol. 2002, 64:363-367.
4. Chade A.R., Lerman A., Lerman L.O. Kidney in early atherosclerosis. Hypertension 2005, 5:1042-1049.
5. Chinnappa S., Hothi S.S., Tan L.B. Is uremic cardiomyopathy a direct consequence of chronic kidney disease?. Expert Rev. Cardiovasc. Ther. 2014, 12:127-130.
6. Dou L., Jourde-Chiche N., Faure V., Cerini C., Berland Y., Dignat-George F., Brunet P. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells. J. Thromb. Haemost. 2007, 5:1302-1308.
7. Dromparis P., Paulin R., Sutendra G., Qi A.C., Bonnet S., Michelakis E.D. Uncoupling protein 2 deficiency mimics the effects of hypoxia and endoplasmic reticulum stress on mitochondria and triggers pseudohypoxic pulmonary vascular remodeling and pulmonary hypertension. Circ. Res. 2013, 113:126-136.
8. Fisslthaler B., Fleming I. Activation and signaling by the AMP-activated protein kinase in endothelial cells. Circ. Res. 2009, 105:114-127.
9. Fleury C., Neverova M., Collins S., Raimbault S., Champigny O., Levi-Meyrueis C., Bouillaud F., Seldin M.F., Surwit R.S., Ricquier D., Warden C.H. Uncoupling protein-2: a novel gene linked to obesity and hyperinsulinemia. Nat. Genet. 1997, 15:269-272.
10. Foley R.N., Parfrey P.S., Harnett J.D., Kent G.M., Murray D.C., Barre P.E. The prognostic importance of left ventricular geometry in uremic cardiomyopathy. J. Am. Soc. Nephrol. 1995, 5:2024-2031.
11. Fridell Y.W., Sanchez-Blanco A., Silvia B.A., Helfand S.L. Targeted expression of the human uncoupling protein 2 (hUCP2) to adult neurons extends life span in the fly. Cell. Metab. 2005, 1:145-152.
12. Gelasco A.K., Raymond J.R. Indoxyl sulfate induces complex redox alterations in mesangial cells. Am. J. Physiol. Renal. Physiol. 2006, 290:F1551-1558.
13. Go A.S., Chertow G.M., Fan D.J., McCulloch C.E., Hsu C.Y. Chronic kidney disease and the risks of death, cardiovascular events, and hospitalization. New Engl. J. Med. 2004, 351:1296-1305.
14. Gross M.L., Ritz E. Hypertrophy and fibrosis in the cardiomyopathy of uremia-beyond coronary heart disease. Semin. Dial. 2008, 21:308-318.
15. Ichii O., Otsuka-Kanazawa S., Nakamura T., Ueno M., Kon Y., Chen W., Rosenberg A.Z., Kopp J.B. Podocyte injury caused by indoxyl sulfate, a uremic toxin and aryl-hydrocarbon receptor ligand. PloS One 2014, 9:e108448.
16. Ito S., Yoshida M. Protein-bound uremic toxins: new culprits of cardiovascular events in chronic kidney disease patients. Toxins 2014, 6:665-678.
17. Itoh Y., Ezawa A., Kikuchi K., Tsuruta Y., Niwa T. Protein-bound uremic toxins in hemodialysis patients measured by liquid chromatography/tandem mass spectrometry and their effects on endothelial ROS production. Anal. Bioanal. Chem. 2012, 403:1841-1850.
18. Johnstone L.M., Jones C.L., Grigg L.E., Wilkinson J.L., Walker R.G., Powell H.R. Left ventricular abnormalities in children, adolescents and young adults with renal disease. Kidney Int. 1996, 50:998-1006.
19. Keith D.S., Nichols G.A., Gullion C.M., Brown J.B., Smith D.H. Longitudinal follow-up and outcomes among a population with chronic kidney disease in a large managed care organization. Arch. Intern. Med. 2004, 164:659-663.
20. Lekawanvijit S., Adrahtas A., Kelly D.J., Kompa A.R., Wang B.H., Krum H. Does indoxyl sulfate, a uraemic toxin, have direct effects on cardiac fibroblasts and myocytes?. Eur. Heart J. 2010, 31:1771-1779.
21. Lekawanvijit S., Kompa A.R., Manabe M., Wang B.H., Langham R.G., Nishijima F., Kelly D.J., Krum H. Chronic kidney disease-induced cardiac fibrosis is ameliorated by reducing circulating levels of a non-dialysable uremic toxin, indoxyl sulfate. PloS One 2012, 7:19.
22. Levin A., Singer J., Thompson C.R., Ross H., Lewis M. Prevalent left ventricular hypertrophy in the predialysis population: identifying opportunities for intervention. Am. J. Kidney Dis. 1996, 27:347-354.
23. Lim C.F., Bernard B.F., de Jong M., Docter R., Krenning E.P., Hennemann G. A furan fatty acid and indoxyl sulfate are the putative inhibitors of thyroxine hepatocyte transport in uremia. J. Clin. Endocrinol. Metab. 1993, 76:318-324.
24. London G.M. Cardiovascular disease in chronic renal failure: pathophysiologic aspects. Semin. Dial. 2003, 16:85-94.
25. 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-kappaB pathway. Circ. J. 2010, 74:2216-2224.
26. Mattiasson G., Shamloo M., Gido G., Mathi K., Tomasevic G., Yi S., Warden C.H., Castilho R.F., Melcher T., Gonzalez-Zulueta M., Nikolich K., Wieloch T. Uncoupling protein-2 prevents neuronal death and diminishes brain dysfunction after stroke and brain trauma. Nat. Med. 2003, 9:1062-1068.
27. Meert N., Schepers E., De Smet R., Argiles A., Cohen G., Deppisch R., Drueke T., Massy Z., Spasovski G., Stegmayr B., Zidek W., Jankowski J., Vanholder R. Inconsistency of reported uremic toxin concentrations. Artif. Organs 2007, 31:600-611.
28. Mitsnefes M.M., Daniels S.R., Schwartz S.M., Meyer R.A., Khoury P., Strife C.F. Severe left ventricular hypertrophy in pediatric dialysis: prevalence and predictors. Pediatr. Nephrol. 2000, 14:898-902.
29. Miyazaki H., Matsuoka H., Itabe H., Usui M., Ueda S., Okuda S., Imaizumi T. Hemodialysis impairs endothelial function via oxidative stress: effects of vitamin E-coated dialyzer. Circ. 2000, 101:1002-1006.
30. 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.
31. 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.
32. Nagata D., Hirata Y. The role of AMP-activated protein kinase in the cardiovascular system. Hypertens. Res. 2010, 33:22-28.
33. Niwa T. Role of indoxyl sulfate in the progression of chronic kidney disease and cardiovascular disease: experimental and clinical effects of oral sorbent AST-120. Ther. Apher. Dial. 2011, 15:120-124.
34. Rasic S., Kulenovic I., Haracic A., Catovic A. Left ventricular hypertrophy and risk factors for its development in uraemic patients. Bosn. J. Basic Med. Sci. 2004, 4:34-40.
35. Sarnak M.J., Levey A.S., Schoolwerth A.C., Coresh J., Culleton B., Hamm L.L., McCullough P.A., Kasiske B.L., Kelepouris E., Klag M.J., Parfrey P., Pfeffer M., Raij L., Spinosa D.J., Wilson P.W. Kidney disease as a risk factor for development of cardiovascular disease: a statement from the American Heart Association Councils on Kidney in Cardiovascular Disease, High Blood Pressure Research, Clinical Cardiology, and Epidemiology and Prevention. Circulation 2003, 108:2154-2169.
36. Schulman I.H., Zhou M.S., Raij L. Nitric oxide, angiotensin II, and reactive oxygen species in hypertension and atherogenesis. Curr. Hypertens. Rep. 2005, 7:61-67.
37. Shimoishi K., Anraku M., Kitamura K., Tasaki Y., Taguchi K., Hashimoto M., Fukunaga E., Maruyama T., Otagiri M. 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. 2007, 24:1283-1289.
38. Shin S.J., Kim H.W., Chung S., Chung H.W., Lee S.J., Kim Y.S., Bang B.K., Chang Y.S., Park C.W. Late referral to a nephrologist increases the risk of uremia-related cardiac hypertrophy in patients on hemodialysis. Nephron. Clin. Pract. 2007, 107:c139-146.
39. Siedlecki A.M., Jin X., Muslin A.J. Uremic cardiac hypertrophy is reversed by rapamycin but not by lowering of blood pressure. Kidney Int. 2009, 75:800-808.
40. Sun J., Pu Y., Wang P., Chen S., Zhao Y., Liu C., Shang Q., Zhu Z., Liu D. TRPV1-mediated UCP2 upregulation ameliorates hyperglycemia-induced endothelial dysfunction. Cardiovasc. Diabetol. 2013, 12:69.
41. Teshima Y., Akao M., Jones S.P., Marban E. Uncoupling protein-2 overexpression inhibits mitochondrial death pathway in cardiomyocytes. Circ. Res. 2003, 93:192-200.
42. Tian X.Y., Wong W.T., Xu A., Lu Y., Zhang Y., Wang L., Cheang W.S., Wang Y., Yao X., Huang Y. Uncoupling protein-2 protects endothelial function in diet-induced obese mice. Circ. Res. 2012, 110:1211-1216.
43. 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.
44. Tumur Z., Shimizu H., Enomoto A., Miyazaki H., Niwa T. Indoxyl sulfate upregulates expression of ICAM-1 and MCP-1 by oxidative stress-induced NF-kappaB activation. Am. J. Nephrol. 2010, 31:435-441.
45. Vanholder R., De Smet R., Glorieux G., Argiles A., Baurmeister U., Brunet P., Clark W., Cohen G., De Deyn P.P., Deppisch R., Descamps-Latscha B., Henle T., Jorres A., Lemke H.D., Massy Z.A., Passlick-Deetjen J., Rodriguez M., Stegmayr B., Stenvinkel P., Tetta C., Wanner C., Zidek W. Review on uremic toxins: classification, concentration, and interindividual variability. Kidney Int. 2003, 63:1934-1943.
46. Vaziri N.D., Rodriguez-Iturbe B. Mechanisms of disease: oxidative stress and inflammation in the pathogenesis of hypertension. Nat. Clin. Pract. Nephrol. 2006, 2:582-593.
47. Vincent A.M., Olzmann J.A., Brownlee M., Sivitz W.I., Russell J.W. Uncoupling proteins prevent glucose-induced neuronal oxidative stress and programmed cell death. Diabetes 2004, 53:726-734.
48. Vlahakos D.V., Hahalis G., Vassilakos P., Marathias K.P., Geroulanos S. Relationship between left ventricular hypertrophy and plasma renin activity in chronic hemodialysis patients. J. Am. Soc. Nephrol. 1997, 8:1764-1770.
49. Wang W.J., Cheng M.H., Sun M.F., Hsu S.F., Weng C.S. Indoxyl sulfate induces renin release and apoptosis of kidney mesangial cells. J. Toxicol. Sci. 2014, 39:637-643.
50. Woodcock E.A., Wang B.H., Arthur J.F., Lennard A., Matkovich S.J., Du X.J., Brown J.H., Hannan R.D. Inositol polyphosphate 1-phosphatase is a novel antihypertrophic factor. J. Biol. Chem. 2002, 277:22734-22742.
51. Xie Z., Zhang J., Wu J., Viollet B., Zou M.H. Upregulation of mitochondrial uncoupling protein-2 by the AMP-activated protein kinase in endothelial cells attenuates oxidative stress in diabetes. Diabetes 2008, 57:3222-3230.
52. Xu M.J., Song P., Shirwany N., Liang B., Xing J., Viollet B., Wang X., Zhu Y., Zou M.H. Impaired expression of uncoupling protein 2 causes defective postischemic angiogenesis in mice deficient in AMP-activated protein kinase alpha subunits. Arterioscler Thromb. Vasc. Biol. 2011, 31:1757-1765.
53. Yamakawa H., Imamura T., Matsuo T., Onitsuka H., Tsumori Y., Kato J., Kitamura K., Koiwaya Y., Eto T. Diastolic wall stress and ANG II in cardiac hypertrophy and gene expression induced by volume overload. Am. J. Physiol. Heart Circ. Physiol. 2000, 279:H2939-2946.
54. Yamamoto H., Tsuruoka S., Ioka T., Ando H., Ito C., Akimoto T., Fujimura A., Asano Y., Kusano E. Indoxyl sulfate stimulates proliferation of rat vascular smooth muscle cells. Kidney Int. 2006, 69:1780-1785.
55. 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.
56. Yisireyili M., Saito S., Abudureyimu S., Adelibieke Y., Ng H.Y., Nishijima F., Takeshita K., Murohara T., Niwa T. Indoxyl sulfate-induced activation of (pro) renin receptor promotes cell proliferation and tissue factor expression in vascular smooth muscle cells. PloS One 2014, 9:e109268.
57. Yisireyili M., Shimizu H., Saito S., Enomoto A., Nishijima F., Niwa T. Indoxyl sulfate promotes cardiac fibrosis with enhanced oxidative stress in hypertensive rats. Life Sci. 2013, 92:1180-1185.
58. Zhang Y., Li L., Hua Y., Nunn J.M., Dong F., Yanagisawa M., Ren J. Cardiac-specific knockout of ET(A) receptor mitigates low ambient temperature-induced cardiac hypertrophy and contractile dysfunction. J. Mol. Cell. Biol. 2012, 4:97-107.