Chronic kidney disease-induced cardiac fibrosis is ameliorated by reducing circulating levels of a non-dialysable uremic toxin, indoxyl sulfate

PLoS ONE

Volumn 7, Issue 7, 2012, Pages

  Lekawanvijit, Suree ^a   Kompa, Andrew R ^a,b   Manabe, Minako ^c   Wang, Bing H ^a   Langham, Robyn G ^b,d   Nishijima, Fuyuhiko ^c   Kelly, Darren J ^b   Krum, Henry ^a  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF MELBOURNE   (Australia)

^c KUREHA CORPORATION   (Japan)

^d ST VINCENT S HOSPITAL   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SMOOTH MUSCLE ACTIN; AST 120; ATRIAL NATRIURETIC FACTOR; CONNECTIVE TISSUE GROWTH FACTOR; HEMOGLOBIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDICAN; INTERLEUKIN 1BETA; INTERLEUKIN 6; MESSENGER RNA; TRANSFORMING GROWTH FACTOR BETA;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHRONIC KIDNEY DISEASE; CONTROLLED STUDY; CREATININE CLEARANCE; ECHOCARDIOGRAPHY; GLOMERULUS FILTRATION RATE; HEART FUNCTION; HEART HEMODYNAMICS; HEART LEFT VENTRICLE ENDDIASTOLIC PRESSURE; HEART LEFT VENTRICLE ENDSYSTOLIC VOLUME; HEART MUSCLE FIBROSIS; HEART STROKE VOLUME; HEART WEIGHT; HEMOGLOBIN BLOOD LEVEL; LEFT VENTRICULAR DIASTOLIC DYSFUNCTION; MALE; NEPHRECTOMY; NONHUMAN; PATHOPHYSIOLOGY; PROTEIN EXPRESSION; PROTEIN PHOSPHORYLATION; RAT;

ANIMALS; CARBON; CARDIOMYOPATHIES; FIBROSIS; INDICAN; MALE; OXIDES; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RENAL INSUFFICIENCY, CHRONIC;

RATTUS;

EID: 84864044989     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0041281     Document Type: Article

References (51)

1. United States Renal Data Systems. USRDS 2007 Annual Data Report:Atlas of End-Stage Renal Disease in the United States. Bethesda, MD: National Institute of Health, National Institute of Diabetes and Digestive and Kidney Diseases.
2. Sarnak MJ, Levey AS, Schoolwerth AC, Coresh J, Culleton B, et al (2003) 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 108: 2154-2169.
3. Amann K, Buzello M, Simonaviciene A, Miltenberger-Miltenyi G, Koch A, et al. (2000) Capillary/myocyte mismatch in the heart in renal failure-a role for erythropoietin? Nephrol Dial Transplant 15: 964-969.
4. Vlahakos DV, Hahalis G, Vassilakos P, Marathias KP, Geroulanos S, (1997) Relationship between left ventricular hypertrophy and plasma renin activity in chronic hemodialysis patients. J Am Soc Nephrol 8: 1764-1770.
5. Zoccali C, Mallamaci F, Tripepi G, Parlongo S, Cutrupi S, et al. (2002) Norepinephrine and concentric hypertrophy in patients with end-stage renal disease. Hypertension 40: 41-46.
6. Gross ML, Ritz E, (2008) Hypertrophy and fibrosis in the cardiomyopathy of uremia-beyond coronary heart disease. Semin Dial 21: 308-318.
7. Go AS, Yang J, Ackerson LM, Lepper K, Robbins S, et al. (2006) Hemoglobin level, chronic kidney disease, and the risks of death and hospitalization in adults with chronic heart failure: the Anemia in Chronic Heart Failure: Outcomes and Resource Utilization (ANCHOR) Study. Circulation 113: 2713-2723.
8. Upadhyay A, Larson MG, Guo CY, Vasan RS, Lipinska I, et al. (2011) Inflammation, kidney function and albuminuria in the Framingham Offspring cohort. Nephrol Dial Transplant 26: 920-926.
9. Zoccali C, Bode-Boger S, Mallamaci F, Benedetto F, Tripepi G, et al. (2001) Plasma concentration of asymmetrical dimethylarginine and mortality in patients with end-stage renal disease: a prospective study. Lancet 358: 2113-2117.
10. Hampl H, Hennig L, Rosenberger C, Amirkhalily M, Gogoll L, et al. (2005) Effects of optimized heart failure therapy and anemia correction with epoetin beta on left ventricular mass in hemodialysis patients. Am J Nephrol 25: 211-220.
11. Tornig J, Amann K, Ritz E, Nichols C, Zeier M, et al. (1996) Arteriolar wall thickening, capillary rarefaction and interstitial fibrosis in the heart of rats with renal failure:the effects of ramipril, nifedipine and moxonidine. J Am Soc Nephrol 7: 667-675.
12. Cice G, Ferrara L, D'Andrea A, D'Isa S, Di Benedetto A, et al. (2003) Carvedilol increases two-year survivalin dialysis patients with dilated cardiomyopathy: a prospective, placebo-controlled trial. J Am Coll Cardiol 41: 1438-1444.
13. Cannella G, Paoletti E, Delfino R, Peloso G, Rolla D, et al. (1997) Prolonged therapy with ACE inhibitors induces a regression of left ventricular hypertrophy of dialyzed uremic patients independently from hypotensive effects. Am J Kidney Dis 30: 659-664.
14. Wikoff WR, Anfora AT, Liu J, Schultz PG, Lesley SA, et al. (2009) Metabolomics analysis reveals large effects of gut microflora on mammalian blood metabolites. Proc Natl Acad Sci U S A 106: 3698-3703.
15. Stanfel LA, Gulyassy PF, Jarrard EA, (1986) Determination of indoxyl sulfate in plasma of patients with renal failure by use of ion-pairing liquid chromatography. Clin Chem 32: 938-942.
16. Niwa T, Ise M, (1994) Indoxyl sulfate, a circulating uremic toxin, stimulates the progression of glomerular sclerosis. J Lab Clin Med 124: 96-104.
17. Miyazaki T, Aoyama I, Ise M, Seo H, Niwa T, (2000) An oral sorbent reduces overload of indoxyl sulphate and gene expression of TGF-beta1 in uraemic rat kidneys. Nephrol Dial Transplant 15: 1773-1781.
18. Lekawanvijit S, Adrahtas A, Kelly DJ, Kompa AR, Wang BH, et al. (2010) Does indoxyl sulfate, a uraemic toxin, have direct effects on cardiac fibroblasts and myocytes? Eur Heart J 31: 1771-1779.
19. Glassock RJ, Pecoits-Filho R, Barberato SH, (2009) Left ventricular mass in chronic kidney disease and ESRD. Clin J Am Soc Nephrol 4: S79-91.
20. Herzog CA, Mangrum JM, Passman R, (2008) Sudden cardiac death and dialysis patients. Semin Dial 21: 300-307.
21. Nitta K, Akiba T, Uchida K, Otsubo S, Otsubo Y, et al. (2004) Left ventricular hypertrophy is associated with arterial stiffness and vascular calcification in hemodialysis patients. Hypertens Res 27: 47-52.
22. Nitta K, Akiba T, Suzuki K, Uchida K, Ogawa T, et al. (2004) Assessment of coronary artery calcification in hemodialysis patients using multi-detector spiral CT scan. Hypertens Res 27: 527-533.
23. Foley RN, Parfrey PS, Sarnak MJ, (1998) Epidemiology of cardiovascular disease in chronic renal disease. J Am Soc Nephrol 9: S16-23.
24. Niwa T, (2010) Uremic toxicity of indoxyl sulfate. Nagoya J Med Sci 72: 1-11.
25. Maeda K, Hamada C, Hayashi T, Shou I, Wakabayashi M, et al. (2009) Long-term effects of the oral adsorbent, AST-120, in patients with chronic renal failure. J Int Med Res 37: 205-213.
26. Niwa T, Nomura T, Sugiyama S, Miyazaki T, Tsukushi S, et al. (1997) The protein metabolite hypothesis, a model for the progression of renal failure: an oral adsorbent lowers indoxyl sulfate levels in undialyzed uremic patients. Kidney Int pp. S23-28.
27. Ueda H, Shibahara N, Takagi S, Inoue T, Katsuoka Y, (2008) AST-120 treatment in pre-dialysis period affects the prognosis in patients on hemodialysis. Ren Fail 30: 856-860.
28. Iida S, Kohno K, Yoshimura J, Ueda S, Usui M, et al. (2006) Carbonic-adsorbent AST-120 reduces overload of indoxyl sulfate and the plasma level of TGF-beta1 in patients with chronic renal failure. Clin Exp Nephrol 10: 262-267.
29. Tamada S, Asai T, Kuwabara N, Iwai T, Uchida J, et al. (2006) Molecular mechanisms and therapeutic strategies of chronic renal injury: the role of nuclear factor kappaB activation in the development of renal fibrosis. J Pharmacol Sci 100: 17-21.
30. Motojima M, Hosokawa A, Yamato H, Muraki T, Yoshioka T, (2003) Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-kappaB and free radical in proximal tubular cells. Kidney Int 63: 1671-1680.
31. Nakai K, Fujii H, Kono K, Goto S, Fukagawa M, et al. (2011) Effects of AST-120 on left ventricular mass in predialysis patients. Am J Nephrol 33: 218-223.
32. Nakamura T, Kawagoe Y, Matsuda T, Ueda Y, Shimada N, et al. (2004) Oral ADSORBENT AST-120 decreases carotid intima-media thickness and arterial stiffness in patients with chronic renal failure. Kidney Blood Press Res 27: 121-126.
33. Shibahara H, Shibahara N, (2010) Cardiorenal protective effect of the oral uremic toxin absorbent AST-120 in chronic heart disease patients with moderate CKD. J Nephrol 23: 535-540.
34. Barreto FC, Barreto DV, Liabeuf S, Meert N, Glorieux G, et al. (2009) Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin J Am Soc Nephrol 4: 1551-1558.
35. Shimizu H, Bolati D, Adijiang A, Muteliefu G, Enomoto A, et al. (2011) NF-kappaB plays an important role in indoxyl sulfate-induced cellular senescence, fibrotic gene expression, and inhibition of proliferation in proximal tubular cells. Am J Physiol Cell Physiol 301: C1201-1212.
36. Sasaki CY, Barberi TJ, Ghosh P, Longo DL, (2005) Phosphorylation of RelA/p65 on serine 536 defines an I{kappa}B{alpha}-independent NF-{kappa}B pathway. J Biol Chem 280: 34538-34547.
37. Kobayashi N, Maeda A, Horikoshi S, Shirato I, Tomino Y, et al. (2002) Effects of oral adsorbent AST-120 (Kremezin) on renal function and glomerular injury in early-stage renal failure of subtotal nephrectomized rats. Nephron 91: 480-485.
38. Aoyama I, Shimokata K, Niwa T, (2002) An oral adsorbent downregulates renal expression of genes that promote interstitial inflammation and fibrosis in diabetic rats. Nephron 92: 635-651.
39. Aoyama I, Shimokata K, Niwa T, (2000) Oral adsorbent AST-120 ameliorates interstitial fibrosis and transforming growth factor-beta(1) expression in spontaneously diabetic (OLETF) rats. Am J Nephrol 20: 232-241.
40. Stenvinkel P, (2006) Inflammation in end-stage renal disease: the hidden enemy. Nephrology (Carlton) 11: 36-41.
41. Mann DL, (2002) Inflammatory mediators and the failing heart: past, present, and the foreseeable future. Circ Res 91: 988-998.
42. Iyngkaran P, Tuck KL, Ma J, Ho P, Lekawanvijit S, et al. (2009) Do all protein bound renal toxins exert physiological effects on cardiac cells? Heart Lung and Circulation 18: S250-S251.
43. Kikuchi K, Itoh Y, Tateoka R, Ezawa A, Murakami K, et al. (2010) Metabolomic search for uremic toxins as indicators of the effect of an oral sorbent AST-120 by liquid chromatography/tandem mass spectrometry. J Chromatogr B Analyt Technol Biomed Life Sci 878: 2997-3002.
44. London GM, Pannier B, Guerin AP, Blacher J, Marchais SJ, et al. (2001) Alterations of left ventricular hypertrophy in and survival of patients receiving hemodialysis: follow-up of an interventional study. J Am Soc Nephrol 12: 2759-2767.
45. Phrommintikul A, Tran L, Kompa A, Wang B, Adrahtas A, et al. (2008) Effects of a Rho kinase inhibitor on pressure overload induced cardiac hypertrophy and associated diastolic dysfunction. Am J Physiol Heart Circ Physiol 294: H1804-1814.
46. Kompa AR, Wang BH, Phrommintikul A, Ho PY, Kelly DJ, et al. (2010) Chronic urotensin II receptor antagonist treatment does not alter hypertrophy or fibrosis in a rat model of pressure-overload hypertrophy. Peptides 31: 1523-1530.
47. Kelly DJ, Wilkinson-Berka JL, Allen TJ, Cooper ME, Skinner SL, (1998) A new model of diabetic nephropathy with progressive renal impairment in the transgenic (mRen-2)27 rat (TGR). Kidney Int 54: 343-352.
48. Owada S, Goto S, Bannai K, Hayashi H, Nishijima F, et al. (2008) Indoxyl sulfate reduces superoxide scavenging activity in the kidneys of normal and uremic rats. Am J Nephrol 28: 446-454.
49. Tran L, Kompa AR, Kemp W, Phrommintikul A, Wang BH, et al. (2010) Chronic urotensin-II infusion induces diastolic dysfunction and enhances collagen production in rats. Am J Physiol Heart Circ Physiol 298: H608-613.
50. Campbell DJ, Somaratne JB, Jenkins AJ, Prior DL, Yii M, et al. (2011) Differences in myocardial structure and coronary microvasculature between men and women with coronary artery disease. Hypertension 57: 186-192.
51. Kompa AR, See F, Lewis DA, Adrahtas A, Cantwell DM, et al. (2008) Long-term but not short-term p38 mitogen-activated protein kinase inhibition improves cardiac function and reduces cardiac remodeling post-myocardial infarction. J Pharmacol Exp Ther 325: 741-750.