Indoxyl sulfate exacerbates low bone turnover induced by parathyroidectomy in young adult rats

Bone

Volumn 79, Issue , 2015, Pages 252-258

  Hirata, Junya ^a,b   Hirai, Kazuya ^a   Asai, Hirobumi ^a   Matsumoto, Chiho ^b   Inada, Masaki ^b   Miyaura, Chisato ^b   Yamato, Hideyuki ^a   Watanabe Akanuma, Mie ^a  

^a KUREHA CORPORATION   (Japan)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

Author keywords

Chronic kidney disease; Indole; Indoxyl sulfate; Low bone turnover; Parathyroidectomy

Indexed keywords

ALKALINE PHOSPHATASE; INDICAN; INDOLE; PARATHYROID HORMONE;

ADULT; ALKALINE PHOSPHATASE BLOOD LEVEL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BONE DENSITY; BONE LENGTH; BONE TURNOVER; CONTROLLED STUDY; ENZYME ACTIVITY; MALE; MORPHOMETRICS; NONHUMAN; OSSIFICATION; OSTEOLYSIS; PARATHYROIDECTOMY; RAT; YOUNG ADULT; ADVERSE EFFECTS; ANIMAL; BONE REMODELING; CHRONIC KIDNEY FAILURE; COMPLICATION; DISEASE MODEL; METABOLISM; PATHOPHYSIOLOGY; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; BONE DENSITY; BONE REMODELING; DISEASE MODELS, ANIMAL; INDICAN; MALE; PARATHYROID HORMONE; PARATHYROIDECTOMY; RATS; RATS, SPRAGUE-DAWLEY; RENAL INSUFFICIENCY, CHRONIC;

EID: 84933574741     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2015.06.010     Document Type: Article

References (38)

1. Moe S., Drüeke T., Cunningham J., Goodman W., Martin K., Olgaard K., et al. Kidney Disease: Improving Global Outcomes (KDIGO). Definition, evaluation, and classification of renal osteodystrophy: A position statement from Kidney Disease: Improving Global Outcomes (KDIGO). Kidney Int 2006, 69:1945-1953.
2. Kidney Disease: Improving Global Outcomes(KDIGO)CKD-MBD Work Group KDIGO clinical practice guideline for the diagnosis, evaluation, prevention and treatment of Chronic Kidney Disease-Mineral and Bone Disorder(CKD-MBD). Kidney Int 2009, 76(Suppl. 113):S1-S130.
3. Malluche H.H., Mawad H.W., Monier-Faugere M.C. Renal osteodystrophy in the first decade of the new millennium: Analysis of 630 bone biopsies in black and white patients. J Bone Miner Res 2011, 26:1368-1376.
4. Fournier A., Morinière P., Cohen Solal M.E., Boudailliez B., Achard J.M., Marie A., et al. Adynamic bone disease in uremia: May it be idiopathic? Is it an actual disease?. Nephron 1991, 58:1-12.
5. Salusky I.B., Goodman W.G. Adynamic renal osteodystrophy: Is there a problem?. J Am Soc Nephrol 2001, 12:1978-1985.
6. Couttenye M.M., D'Haese P.C., Verschoren W.J., Behets G.J., Schrooten I., De Broe M.E. Low bone turnover in patients with renal failure. Kidney Int Suppl 1999, 73:S70-S76.
7. 3, and radiology in end-stage renal disease. Kidney Int 1993, 44:1071-1077.
8. Massry S.G., Stein R., Garty J., Arieff A.I., Coburn J.W., Norman A.W., et al. Skeletal resistance to the calcemic action of parathyroid hormone in uremia: role of 1,25 (OH)2 D3. Kidney Int 1976, 9:467-474.
9. Coen G., Mazzaferro S., Ballanti P., Sardella D., Chicca S., Manni M., et al. Renal bone disease in 76 patients with varying degrees of predialysis chronic renal failure: a cross-sectional study. Nephrol Dial Transplant 1996, 11:813-819.
10. Sherrard D.J., Hercz G., Pei Y., Maloney N.A., Greenwood C., Manuel A., et al. The spectrum of bone disease in end-stage renal failure-an evolving disorder. Kidney Int 1993, 43:436-442.
11. Torres A., Lorenzo V., Hernández D., Rodríguez J.C., Concepción M.T., Rodríguez A.P., et al. Bone disease in predialysis, hemodialysis, and CAPD patients: evidence of a better bone response to PTH. Kidney Int 1995, 47:1434-1442.
12. Danese M.D., Kim J., Doan Q.V., Dylan M., Griffiths R., Chertow G.M. PTH and the risks for hip, vertebral, and pelvic fractures among patients on dialysis. Am J Kidney Dis 2006, 47:149-156.
13. Naves-Díaz M., Passlick-Deetjen J., Guinsburg A., Marelli C., Fernández-Martín J.L., Rodríguez-Puyol D., et al. Calcium, phosphorus, PTH and death rates in a large sample of dialysis patients from Latin America. The CORES Study. Nephrol Dial Transplant 2011, 26:1938-1947.
14. Vanholder R., De Smet R., Glorieux G., Argilés A., Baurmeister U., Brunet P., et al. Review on uremic toxins: Classification, concentration, and interindividual variability. Kidney Int 2003, 63:1934-1943.
15. Vanholder R., Glorieux G., De Smet R., Lameire N., Group European Uremic Toxin Work New insights in uremic toxins. Kidney Int Suppl 2003, 63:S6-S10.
16. Vanholder R., Van Laecke S., Glorieux G. What is new in uremic toxicity?. Pediatr Nephrol 2008, 23:1211-1221.
17. Vanholder R., Baurmeister U., Brunet P., Cohen G., Glorieux G., Jankowski J., et al. A bench to bedside view of uremic toxins. J Am Soc Nephrol 2008, 19:863-870.
18. King L.J., Parke D.V., Williams R.T. The metabolism of [2-14C] indole in the rat. Biochem J 1966, 98:266-277.
19. Niwa T., Ise M. Indoxyl sulfate, a circulating uremic toxin, stimulates the progression of glomerular sclerosis. J Lab Clin Med 1994, 124:96-104.
20. Barreto F.C., Barreto D.V., Liabeuf S., Meert N., Glorieux G., Temmar M., et al. Serum indoxyl sulfate is associated with vascular disease and mortality in chronic kidney disease patients. Clin J Am Soc Nephrol 2009, 4:1551-1558.
21. Atoh K., Itoh H., Haneda M. Serum indoxyl sulfate levels in patients with diabetic nephropathy: Relation to renal function. Diabetes Res Clin Pract 2009, 83:220-226.
22. Niwa T., Ise M., Miyazaki T. Progression of glomerular sclerosis in experimental uremic rats by administration of indole, a precursor of indoxyl sulfate. Am J Nephrol 1994, 14:207-212.
23. Iwasaki Y., Yamato H., Nii-Kono T., Fujieda A., Uchida M., Hosokawa A., et al. Administration of oral charcoal adsorbent (AST-120) suppresses low-turnover bone progression in uraemic rats. Nephrol Dial Transplant 2006, 21:2768-2774.
24. Nii-Kono T., Iwasaki Y., Uchida M., Fujieda A., Hosokawa A., Motojima M., et al. ndoxyl sulfate induces skeletal resistance to parathyroid hormone in cultured osteoblastic cells. Kidney Int 2007, 71:738-743.
25. Goto S., Fujii H., Hamada Y., Yoshiya K., Fukagawa M. Association between indoxyl sulfate and skeletal resistance in hemodialysis patients. Ther Apher Dial 2010, 14:417-423.
26. Kikuchi K., Itoh Y., Tateoka R., Ezawa A., Murakami K., Niwa T. 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 2010, 878:2997-3002.
27. Parfitt A.M., Drezner M.K., Glorieux F.H., Kanis J.A., Malluche H., Meunier P.J., et al. Bone histomorphometry: Standardization of nomenclature, symbols, and units. Report of the ASBMR Histomorphometry Nomenclature Committee. J Bone Miner Res 1987, 2:595-610.
28. Inami Y., Hamada C., Seto T., Hotta Y., Aruga S., Inuma J., et al. Effect of AST-120 on endothelial dysfunction in adenine-induced uremic rats. Int J Nephrol 2014, 164125. 10.1155/2014/164125.
29. Enomoto A., Takeda M., Tojo A., Sekine T., Cha S.H., Khamdang S., et al. Role of organic anion transporters in the tubular transport of indoxyl sulfate and the induction of its nephrotoxicity. J Am Soc Nephrol 2002, 13:1711-1720.
30. Iwasaki-Ishizuka Y., Yamato H., Nii-Kono T., Kurokawa K., Fukagawa M. Downregulation of parathyroid hormone receptor gene expression and osteoblastic dysfunction associated with skeletal resistance to parathyroid hormone in a rat model of renal failure with low turnover bone. Nephrol Dial Transplant 2005, 20:1904-1911.
31. Ferreira J.C., Ferrari G.O., Neves K.R., Cavallari R.T., Dominguez W.V., Dos Reis L.M., et al. Effects of dietary phosphate on adynamic bone disease in rats with chronic kidney disease - role of sclerostin?. PLoS One 2013, 8:e79721.
32. Kim Y.H., Kwak K.A., Gil H.W., Song H.Y., Hong S.Y. Indoxyl sulfate promotes apoptosis in cultured osteoblast cells. BMC Pharmacol Toxicol 2013, 14:60.
33. Motojima M., Hosokawa A., Yamato H., Muraki T., Yoshioka T. Uremic toxins of organic anions up-regulate PAI-1 expression by induction of NF-κB and free radical in proximal tubular cells. Kidney Int 2003, 63:1671-1680.
34. Owada S., Goto S., Bannai K., Hayashi H., Nishijima F., Niwa T. Indoxyl sulfate reduces superoxide scavenging activity in the kidneys of normal and uremic rats. Am J Nephrol 2008, 28:446-454.
35. Dou L., Jourde-Chiche N., Faure V., Cerini C., Berland Y., Dignat-George F., et al. The uremic solute indoxyl sulfate induces oxidative stress in endothelial cells. J Thromb Haemost 2007, 5:1302-1308.
36. Mozar A., Louvet L., Godin C., Mentaverri R., Brazier M., Kamel S., et al. Indoxyl sulphate inhibits osteoclast differentiation and function. Nephrol Dial Transplant 2012, 27:2176-2181.
37. Tanaka H., Iwasaki Y., Yamato H., Mori Y., Komaba H., Watanabe H., et al. p-Cresyl sulfate induces osteoblast dysfunction through activating JNK and p38 MAPK pathways. Bone 2013, 56:347-354.
38. Yano S., Yamaguchi T., Kanazawa I., Ogawa N., Hayashi K., Yamauchi M., et al. The uraemic toxin phenylacetic acid inhibits osteoblastic proliferation and differentiation: An implication for the pathogenesis of low turnover bone in chronic renal failure. Nephrol Dial Transplant 2007, 22:3160-3165.