Performance of urinary and gene expression biomarkers in detecting the nephrotoxic effects of melamine and cyanuric acid following diverse scenarios of co-exposure

Food and Chemical Toxicology

Volumn 51, Issue 1, 2013, Pages 106-113

  Bandele, Omari ^a   Camacho, Luísa ^b   Ferguson, Martine ^a   Reimschuessel, Renate ^a   Stine, Cynthia ^a   Black, Thomas ^a   Olejnik, Nicholas ^a   Keltner, Zachary ^a   Scott, Michael ^a   Costa, Gonçalo Gamboa da ^b   Sprando, Robert ^a  

^a CENTER FOR DRUG EVALUATION AND RESEARCH   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

Author keywords

bead based; Biomarkers; Cyanuric acid; immunoassays; Luminex; Melamine; Nephrotoxicity

Indexed keywords

BETA 2 MICROGLOBULIN; BIOLOGICAL MARKER; CLUSTERIN; CYANURIC ACID; CYSTATIN C; KIDNEY INJURY MOLECULE 1; MELAMINE; OSTEOPONTIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DISEASE SEVERITY; FEEDING; FEMALE; GENE EXPRESSION; IMMUNOASSAY; INTERMETHOD COMPARISON; MALE; NEPHROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN URINE LEVEL; RAT; URINALYSIS;

ACUTE-PHASE PROTEINS; ANIMAL FEED; ANIMALS; BIOLOGICAL MARKERS; CELL ADHESION MOLECULES; CLUSTERIN; CYSTATIN C; ENVIRONMENTAL EXPOSURE; ENZYME-LINKED IMMUNOSORBENT ASSAY; FEMALE; GENE EXPRESSION; LIPOCALINS; MALE; OSTEOPONTIN; PROTO-ONCOGENE PROTEINS; RATS; RATS, INBRED F344; RENAL INSUFFICIENCY; TISSUE INHIBITOR OF METALLOPROTEINASE-1; TRIAZINES;

ANIMALIA; RATTUS;

EID: 84867312278     PISSN: 02786915     EISSN: 18736351     Source Type: Journal    
DOI: 10.1016/j.fct.2012.09.022     Document Type: Article

References (58)

1. Toxicological and Health Aspects of Melamine and Cyanuric Acid 2009, WHO, World Health Organization, Geneva, Switzerland.
2. Bailey W.J., Ulrich R. Molecular profiling approaches for identifying novel biomarkers. Expert Opin. Drug Saf. 2004, 3:137-151.
3. Bonventre J.V. Dedifferentiation and proliferation of surviving epithelial cells in acute renal failure. J. Am. Soc. Nephrol. 2003, 14(Suppl. 1):S55-S61.
4. Brown C.A., Jeong K.S., Poppenga R.H., Puschner B., Miller D.M., Ellis A.E., Kang K.I., Sum S., Cistola A.M., Brown S.A. Outbreaks of renal failure associated with melamine and cyanuric acid in dogs and cats in 2004 and 2007. J. Vet. Diagn. Invest. 2007, 19:525-531.
5. Camacho L., Kelly K.P., Beland F.A., Gamboa da Costa G. Gene expression of biomarkers of nephrotoxicity in F344 rats co-exposed to melamine and cyanuric acid for 7days. Toxicol. Lett. 2011, 206:166-171.
6. Choi L., Kwak M.Y., Kwak E.H., Kim D.H., Han E.Y., Roh T., Bae J.Y., Ahn I.Y., Jung J.Y., Kwon M.J., Jang D.E., Lim S.K., Kwack S.J., Han S.Y., Kang T.S., Kim S.H., Kim H.S., Lee B.M. Comparative nephrotoxicitiy induced by melamine, cyanuric acid, or a mixture of both chemicals in either Sprague-Dawley rats or renal cell lines. J. Toxicol. Environ. Health A 2010, 73:1407-1419.
7. Cianciolo R.E., Bischoff K., Ebel J.G., Van Winkle T.J., Goldstein R.E., Serfilippi L.M. Clinicopathologic, histologic, and toxicologic findings in 70 cats inadvertently exposed to pet food contaminated with melamine and cyanuric acid. J. Am. Vet. Med. Assoc. 2008, 233:729-737.
8. Dalal R.P., Goldfarb D.S. Melamine-related kidney stones and renal toxicity. Nature reviews. Nephrology 2011, 7:267-274.
9. Davis J.W., Kramer J.A. Genomic-based biomarkers of drug-induced nephrotoxicity. Expert Opin. Drug Metab. Toxicol. 2006, 2:95-101.
10. Devarajan P. Emerging biomarkers of acute kidney injury. Contrib. Nephrol. 2007, 156:203-212.
11. Dieterle F., Marrer E., Suzuki E., Grenet O., Cordier A., Vonderscher J. Monitoring kidney safety in drug development: emerging technologies and their implications. Curr. Opin. Drug Discov. Devel. 2008, 11:60-71.
12. Dieterle F., Perentes E., Cordier A., Roth D.R., Verdes P., Grenet O., Pantano S., Moulin P., Wahl D., Mahl A., End P., Staedtler F., Legay F., Carl K., Laurie D., Chibout S.D., Vonderscher J., Maurer G. Urinary clusterin, cystatin C, beta2-microglobulin and total protein as markers to detect drug-induced kidney injury. Nat. Biotechnol. 2010, 28:463-469.
13. Dobson R.L., Motlagh S., Quijano M., Cambron R.T., Baker T.R., Pullen A.M., Regg B.T., Bigalow-Kern A.S., Vennard T., Fix A., Reimschuessel R., Overmann G., Shan Y., Daston G.P. Identification and characterization of toxicity of contaminants in pet food leading to an outbreak of renal toxicity in cats and dogs. Toxicol. Sci. 2008, 106:251-262.
14. Dodiya H., Jain M., Goswami S.S. Renal toxicity of lisinopril and rosuvastatin, alone and in combination, in wistar rats. Int. J. Toxicol. 2011, 30:518-527.
15. Duarte C.G., Preuss H.G. Assessment of renal function - glomerular and tubular. Clin. Lab. Med. 1993, 13:33-52.
16. Biomarkers on a roll. Nat. Biotechnol. 2010, 28:431. Editorial.
17. Endre Z.H., Westhuyzen J. Early detection of acute kidney injury: emerging new biomarkers. Nephrology (Carlton) 2008, 13:91-98.
18. FDA, 2008. FDA, European Medicines Agency to Consider Additional Test Results When Assessing New Drug Safety Collaborative Effort by FDA and EMEA Expected to Yield Additional Safety Data. US Food and Drug Administration. http://www.fda.gov/NewsEvents/Newsroom/PressAnnouncements/2008/ucm116911.htm.
19. Ferguson M.A., Vaidya V.S., Bonventre J.V. Biomarkers of nephrotoxic acute kidney injury. Toxicology 2008, 245:182-193.
20. Filigenzi M.S., Puschner B., Aston L.S., Poppenga R.H. Diagnostic determination of melamine and related compounds in kidney tissue by liquid chromatography/tandem mass spectrometry. J. Agric. Food Chem. 2008, 56:7593-7599.
21. Gamboa da Costa G., Jacob C.C., Von Tungeln L.S., Hasbrouck N.R., Olson G.R., Hattan D.G., Reimschuessel R., Beland F.A. Dose-response assessment of nephrotoxicity from a twenty-eight-day combined-exposure to melamine and cyanuric acid in F344 rats. Toxicol. Appl. Pharmacol. 2012, 262:99-106.
22. Goodsaid F.M. Identification and measurement of genomic biomarkers of nephrotoxicity. J. Pharmacol. Toxicol. Methods 2004, 49:183-186.
23. Hammond B.G., Barbee S.J., Inoue T., Ishida N., Levinskas G.J., Stevens M.W., Wheeler A.G., Cascieri T. A review of toxicology studies on cyanurate and its chlorinated derivatives. Environ. Health Perspect. 1986, 69:287-292.
24. Harpur E., Ennulat D., Hoffman D., Betton G., Gautier J.C., Riefke B., Bounous D., Schuster K., Beushausen S., Guffroy M., Shaw M., Lock E., Pettit S., Nephrotoxicity H.C.o.B.o. Biological qualification of biomarkers of chemical-induced renal toxicity in two strains of male rat. Toxicol. Sci. 2011, 122:235-252.
25. Hayes K.R., Bradfield C.A. Advances in toxicogenomics. Chem. Res. Toxicol. 2005, 18:403-414.
26. Hoffmann D., Fuchs T.C., Henzler T., Matheis K.A., Herget T., Dekant W., Hewitt P., Mally A. Evaluation of a urinary kidney biomarker panel in rat models of acute and subchronic nephrotoxicity. Toxicology 2010, 277:49-58.
27. Humphreys B.D., Czerniak S., DiRocco D.P., Hasnain W., Cheema R., Bonventre J.V. Repair of injured proximal tubule does not involve specialized progenitors. Proc. Natl. Acad. Sci. USA 2011, 108:9226-9231.
28. Ichimura T., Bonventre J.V., Bailly V., Wei H., Hession C.A., Cate R.L., Sanicola M. Kidney injury molecule-1 (KIM-1), a putative epithelial cell adhesion molecule containing a novel immunoglobulin domain, is up-regulated in renal cells after injury. J. Biol. Chem. 1998, 273:4135-4142.
29. Ichimura T., Hung C.C., Yang S.A., Stevens J.L., Bonventre J.V. Kidney injury molecule-1: a tissue and urinary biomarker for nephrotoxicant-induced renal injury. Am. J. Physiol. Renal Physiol. 2004, 286:552-563.
30. Jacob C.C., Reimschuessel R., Von Tungeln L.S., Olson G.R., Warbritton A.R., Hattan D.G., Beland F.A., Gamboa da Costa G. Dose-response assessment of nephrotoxicity from a 7-day combined exposure to melamine and cyanuric acid in F344 rats. Toxicol. Sci. 2011, 119:391-397.
31. Kondo C., Minowa Y., Uehara T., Okuno Y., Nakatsu N., Ono A., Maruyama T., Kato I., Yamate J., Yamada H., Ohno Y., Urushidani T. Identification of genomic biomarkers for concurrent diagnosis of drug-induced renal tubular injury using a large-scale toxicogenomics database. Toxicology 2009, 265:15-26.
32. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25:402-408.
33. Marrer E., Dieterle F. Impact of biomarker development on drug safety assessment. Toxicol. Appl. Pharmacol. 2010, 243:167-179.
34. Miya M., Maeshima A., Mishima K., Sakurai N., Ikeuchi H., Kuroiwa T., Hiromura K., Yokoo H., Nojima Y. Enhancement of in vitro human tubulogenesis by endothelial cell-derived factors: implications for in vivo tubular regeneration after injury. Am. J. Physiol. Renal Physiol. 2011, 301:F387-F395.
35. Mori K., Lee H.T., Rapoport D., Drexler I.R., Foster K., Yang J., Schmidt-Ott K.M., Chen X., Li J.Y., Weiss S., Mishra J., Cheema F.H., Markowitz G., Suganami T., Sawai K., Mukoyama M., Kunis C., D'Agati V., Devarajan P., Barasch J. Endocytic delivery of lipocalin-siderophore-iron complex rescues the kidney from ischemia-reperfusion injury. J. Clin. Invest. 2005, 115:610-621.
36. Ozer J.S., Dieterle F., Troth S., Perentes E., Cordier A., Verdes P., Staedtler F., Mahl A., Grenet O., Roth D.R., Wahl D., Legay F., Holder D., Erdos Z., Vlasakova K., Jin H., Yu Y., Muniappa N., Forest T., Clouse H.K., Reynolds S., Bailey W.J., Thudium D.T., Topper M.J., Skopek T.R., Sina J.F., Glaab W.E., Vonderscher J., Maurer G., Chibout S.D., Sistare F.D., Gerhold D.L. A panel of urinary biomarkers to monitor reversibility of renal injury and a serum marker with improved potential to assess renal function. Nat. Biotechnol. 2010, 28:486-494.
37. Parikh C.R., Devarajan P. New biomarkers of acute kidney injury. Crit. Care Med. 2008, 36:S159-S165.
38. Persy V.P., Verstrepen W.A., Ysebaert D.K., De Greef K.E., De Broe M.E. Differences in osteopontin up-regulation between proximal and distal tubules after renal ischemia/reperfusion. Kidney Int. 1999, 56:601-611.
39. Price R.G. The role of NAG (N-acetyl-beta-d-glucosaminidase) in the diagnosis of kidney disease including the monitoring of nephrotoxicity. Clin. Nephrol. 1992, 38(Suppl. 1):S14-S19.
40. Puschner B., Poppenga R.H., Lowenstine L.J., Filigenzi M.S., Pesavento P.A. Assessment of melamine and cyanuric acid toxicity in cats. J. Vet. Diagn. Invest. 2007, 19:616-624.
41. Puschner B., Reimschuessel R. Toxicosis caused by melamine and cyanuric acid in dogs and cats: uncovering the mystery and subsequent global implications. Clin. Lab. Med. 2011, 31:181-199.
42. Rached E., Hoffmann D., Blumbach K., Weber K., Dekant W., Mally A. Evaluation of putative biomarkers of nephrotoxicity after exposure to ochratoxin a in vivo and in vitro. Toxicol. Sci. 2008, 103:371-381.
43. Reimschuessel R., Evans E.R., Stine C.B., Hasbrouck N., Mayer T.D., Nochetto C., Gieseker C.M. Renal crystal formation after combined or sequential oral administration of melamine and cyanuric acid. Food Chem. Toxicol. 2010, 48:2898-2906.
44. Rouse R.L., Zhang J., Stewart S.R., Rosenzweig B.A., Espandiari P., Sadrieh N.K. Comparative profile of commercially available urinary biomarkers in preclinical drug-induced kidney injury and recovery in rats. Kidney Int. 2011, 79:1186-1197.
45. Sola A., Weigert A., Jung M., Vinuesa E., Brecht K., Weis N., Brune B., Borregaard N., Hotter G. Sphingosine-1-phosphate signalling induces the production of Lcn-2 by macrophages to promote kidney regeneration. J. Pathol. 2011, 225:597-608.
46. Sprando, R.L., Reimschuessel, R., Stine, C.B., Black, T.N., Olejnik, N., Scott, M., Keltner, Z., Bandele, O.J., Ferguson, M.A., Nemser, S.M., Tkachenko, A., Evans, E., Crosby, T., Woodling, K., Loukotkova, L., Gamboa da Costa, G., in press. Timing and route of exposure affects crystal formation in melamine and cyanuric exposed male and female rats: gavage vs. feeding. Food Chem. Toxicol.
47. Srisawat, N., Murugan, R., Wen, X.Y., Singbartl, K., Clermont, G., Eiam-Ong, S., Kellum, J.A., 2010. Recovery from Acute Kidney Injury: Determinants and Predictors, Cardiorenal Syndromes in, Critical Care, pp. 284-291.
48. Thadhani R., Pascual M., Bonventre J.V. Acute renal failure. N. Engl. J. Med. 1996, 334:1448-1460.
49. Thukral S.K., Nordone P.J., Hu R., Sullivan L., Galambos E., Fitzpatrick V.D., Healy L., Bass M.B., Cosenza M.E., Afshari C.A. Prediction of nephrotoxicant action and identification of candidate toxicity-related biomarkers. Toxicol. Pathol. 2005, 33:343-355.
50. Vaidya V.S., Ferguson M.A., Bonventre J.V. Biomarkers of acute kidney injury. Annu. Rev. Pharmacol. Toxicol. 2008, 48:463-493.
51. Vaidya V.S., Ozer J.S., Dieterle F., Collings F.B., Ramirez V., Troth S., Muniappa N., Thudium D., Gerhold D., Holder D.J., Bobadilla N.A., Marrer E., Perentes E., Cordier A., Vonderscher J., Maurer G., Goering P.L., Sistare F.D., Bonventre J.V. Kidney injury molecule-1 outperforms traditional biomarkers of kidney injury in preclinical biomarker qualification studies. Nat. Biotechnol. 2010, 28:478-485.
52. Wang E.J., Snyder R.D., Fielden M.R., Smith R.J., Gu Y.Z. Validation of putative genomic biomarkers of nephrotoxicity in rats. Toxicology 2008, 246:91-100.
53. Werner M., Costa M.J., Mitchell L.G., Nayar R. Nephrotoxicity of xenobiotics. Clin. Chim. Acta 1995, 237:107-154.
54. Witzgall R., Brown D., Schwarz C., Bonventre J.V. Localization of proliferating cell nuclear antigen, vimentin, c-Fos, and clusterin in the postischemic kidney. Evidence for a heterogenous genetic response among nephron segments, and a large pool of mitotically active and dedifferentiated cells. J. Clin. Invest. 1994, 93:2175-2188.
55. Xie Y., Nishi S., Iguchi S., Imai N., Sakatsume M., Saito A., Ikegame M., Iino N., Shimada H., Ueno M., Kawashima H., Arakawa M., Gejyo F. Expression of osteopontin in gentamicin-induced acute tubular necrosis and its recovery process. Kidney Int. 2001, 59:959-974.
56. Xie Y., Sakatsume M., Nishi S., Narita I., Arakawa M., Gejyo F. Expression, roles, receptors, and regulation of osteopontin in the kidney. Kidney Int. 2001, 60:1645-1657.
57. Zhang Q., Gamboa da Costa G., Von Tungeln L.S., Jacob C.C., Brown R.P., Goering P.L. Urinary biomarker detection of melamine and cyanuric acid induced kidney injury in rats. Toxicol. Sci. 2012.
58. Zhou Y., Vaidya V.S., Brown R.P., Zhang J., Rosenzweig B.A., Thompson K.L., Miller T.J., Bonventre J.V., Goering P.L. Comparison of kidney injury molecule-1 and other nephrotoxicity biomarkers in urine and kidney following acute exposure to gentamicin, mercury, and chromium. Toxicol. Sci. 2008, 101:159-170.