Correlation of Histopathology, Urinary Biomarkers, and Gene Expression Responses Following Hexachloro-1:3-Butadiene–induced Acute Nephrotoxicity in Male Hanover Wistar Rats: A 28-day Time Course Study

Toxicologic Pathology

Volumn 41, Issue 5, 2013, Pages 779-794

  Maguire, David P ^a   Turton, John A ^b   Scudamore, Cheryl L ^a   Swain, Aubrey J ^c   Mcclure, Fiona J ^c   Smyth, Rosemary ^d   Pereira, Ines B ^d   Munday, Michael R ^d   York, Malcolm J ^c  

^a ROYAL VETERINARY COLLEGE   (United Kingdom)

^b UNIVERSITY COLLEGE LONDON   (United Kingdom)

^c GLAXOSMITHKLINE   (United Kingdom)

^d UNIVERSITY OF LONDON   (United Kingdom)

Author keywords

gene expression; hexachloro 1:3 butadiene; kidney injury molecule 1; rat; renal injury; urinary biomarkers; glutathione S transferase

Indexed keywords

ALBUMIN; BIOLOGICAL MARKER; GLUCOSE; GLUTATHIONE TRANSFERASE ALPHA; HEME OXYGENASE; HEXACHLOROBUTADIENE; KIDNEY INJURY MOLECULE 1; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE (PHOSPHATE) DEHYDROGENASE (QUINONE); SYNEXIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOPSY; BIOCHEMISTRY; CONTROLLED STUDY; GENE EXPRESSION; HISTOPATHOLOGY; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; MALE; NEPHROTOXICITY; NONHUMAN; PRIORITY JOURNAL; RAT;

Α-GLUTATHIONE S-TRANSFERASE; GENE EXPRESSION; HEXACHLORO-1:3-BUTADIENE; KIDNEY INJURY MOLECULE-1; RAT.; RENAL INJURY; URINARY BIOMARKERS;

ACUTE KIDNEY INJURY; ANIMALS; BIOLOGICAL MARKERS; BUTADIENES; GENE EXPRESSION; KIDNEY CORTEX; MALE; OXIDATIVE STRESS; RATS; RATS, WISTAR;

ANIMALIA; RATTUS; RATTUS NORVEGICUS;

EID: 84879480522     PISSN: 01926233     EISSN: 15331601     Source Type: Journal    
DOI: 10.1177/0192623312464306     Document Type: Article

References (48)

1. Abraham N. G. Kappas A. (2005). Heme oxygenase and the cardiovascular-renal system. Free Radic Biol Med 39, 1–25.
2. Birner G. Werner M. Ott M. M. Dekant W. (1995). Sex differences in hexachlorobutadiene biotransformation and nephrotoxicity. Toxicol Appl Pharmacol 132, 203–12.
3. Bonventre J. R. Vaidya V. S. Schmouder R. S. Feig P. Dieterle F. (2010). Next generation biomarkers for detecting kidney toxicity. Nat Biotechnol 28, 436–40.
4. Bonventre J. V. Yang L. (2010). Kidney injury molecule-1. Curr Opin Crit Care 16, 556–61.
5. Cessac A. L. Perichon M. Schaeverbeke J. Bakala H. (1993). Age-related changes in albumin binding by renal brush-border membrane vesicles. Mech Ageing Dev 70, 139–48.
6. Chiusolo A. Defazio R. Zanetti E. Mongillo M. Mori N. Cristofori P. Trevisan A. (2010). Kidney injury molecule-1 expression in rat proximal tubule after treatment with segment-specific nephrotoxicants: A tool for early screening of potential kidney toxicity. Toxicol Pathol 38, 338–45.
7. da Silva J. L. Zand B. A. Yang L. M. Sabaawy H. E. Lianos E. Abraham N. G. (2001). Heme oxygenase isoform-specific expression and distribution in the rat kidney. Kidney Int 59, 1448–57.
8. 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. (2010). Urinary clusterin, cystatin C, beta2-microglobulin and total protein as markers to detect drug-induced kidney injury. Nat Biotechnol 28, 463–69.
9. Dieterle F. Sistare F. Goodsaid F. Papaluca M. Ozer J. S. Webb C. P. Baer W. Senagore A. Schipper M. J. Vonderscher J. Sultana S. Gerhold D. L. Phillips J. A. Maurer G. Carl K. Laurie D. Harpur E. Sonee M. Ennulat D. Holder D. Andrews-Cleavenger D. Gu Y. Z. Thompson K. L. Goering P. L. Vidal J. M. Abadie E. Maciulaitis R. Jacobson-Kram D. Defelice A. F. Hausner E. A. Blank M. Thompson A. Harlow P. Throckmorton D. Xiao S. Xu N. Taylor W. Vamvakas S. Flamion B. Lima B. S. Kasper P. Pasanen M. Prasad K. Troth S. Bounous D. Robinson-Gravatt D. Betton G. Davis M. A. Akunda J. McDuffie J. E. Suter L. Obert L. Guffroy M. Pinches M. Jayadev S. Blomme E. A. Beushausen S. A. Barlow V. G. Collins N. Waring J. Honor D. Snook S. Lee J. Rossi P. Walker E. Mattes W. (2010). Renal biomarker qualification submission: A dialog between the FDA-EMEA and Predictive Safety Testing Consortium. Nat Biotechnol 28, 455–62.
10. Gautier J. C. Riefke B. Walter J. Kurth P. Mylecraine L. Guilpin V. Barlow N. Gury T. Hoffman D. Ennulat D. Schuster K. Harpur E. Pettit S. (2010). Evaluation of novel biomarkers of nephrotoxicity in two strains of rat treated with cisplatin. Toxicol Pathol 38, 943–56.
11. Gong X. Gutala R. Jaiswal A. K. (2008). Quinone oxidoreductases and vitamin K metabolism. Vitam Horm 78, 85–101.
12. Greive K. A. Nikolic-Paterson D. J. Guimaraes M. A. Nikolovski J. Pratt L. M. Mu W. Atkins R. C. Comper W. D. (2001). Glomerular permselectivity factors are not responsible for the increase in fractional clearance of albumin in rat glomerulonephritis. Am J Pathol 159, 1159–70.
13. 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. Paettit S., on behalf of the HESI Committee on Biomarkers of Nephrotoxicity. (2011). Biological qualification of biomarkers of chemical induced renal toxicity in two strains of male rat. Toxicol Sci 122, 235–52.
14. Harrison D. J. Kharbanda R. Cunningham D. S. McLellan L. I. Hayes J. D. (1989). Distribution of glutathione S-transferase isoenzymes in human kidney: Basis for possible markers of renal injury. J Clin Pathol 42, 624–28.
15. Hidaka S. Kranzlin B. Gretz N. Witzgall R. (2002). Urinary clusterin levels in the rat correlate with the severity of tubular damage and may help to differentiate between glomerular and tubular injuries. Cell Tissue Res 310, 289–96.
16. Home Office. (1989). Code of Practice for the Housing and Care of Animals used in Scientific Procedures. Her Majesty's Stationary Office, London.
17. Ichimura T. Asseldonk E. J. Humphreys B. D. Gunaratnam L. Duffield J. S. Bonventre J. V. (2008). Kidney injury molecule-1 is a phosphatidylserine receptor that confers a phagocytic phenotype on epithelial cells. J Clin Invest 118, 1657–68.
18. Ichimura T. Bonventre J. V. Bailly V. Wei H. Hession C. A. Cate R. L. Sanicola M. (1998). 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 273, 4135–42.
19. Ichimura T. Hung C. C. Yang S. A. Stevens J. L. Bonventre J. V. (2004). Kidney injury molecule-1: A tissue and urinary biomarker for nephrotoxicant-induced renal injury. Am J Physiol Renal Physiol 286, F552–63.
20. Ishola D. A. Jr van der Giezen D. M. Hahnel B. Goldschmeding R. Kriz W. Koomans H. A. Joles J. A. (2006). In mice, proteinuria and renal inflammatory responses to albumin overload are strain-dependent. Nephrol Dial Transplant 21, 591–97.
21. Kirby G. M. Bach P. H. (1995). Enhanced hexachloro-1:3-butadiene nephrotoxicity in rats with a preexisting adriamycin-induced nephrotic syndrome. Toxicol Pathol 23, 303–12.
22. Lewis R. E. Kunz A. L. Bell R. E. (1966). Error of intraperitoneal injections in rats. Lab Anim Care 16, 505–509.
23. Lisowska-Myjak B. (2010). Serum and urinary biomarkers of acute kidney injury. Blood Purif 29, 357–65.
24. Lock E. A. Ishmael J. (1979). The acute toxic effects of hexachloro-1:3-butadiene on the rat kidney. Arch Toxicol 43, 47–57.
25. Mishra J. Ma Q. Prada A. Mitsnefes M. Zahedi K. Yang J. Barasch J. Devarajan P. (2003). Identification of neutrophil gelatinase-associated lipocalin as a novel early urinary biomarker for ischemic renal injury. J Am Soc Nephrol 14, 2534–43.
26. Nioi P. Hayes J. D. (2004). Contribution of NAD(P)H:quinone oxidoreductase 1 to protection against carcinogenesis, and regulation of its gene by the Nrf2 basic-region leucine zipper and the arylhydrocarbon receptor basic helix-loop-helix transcription factors. Mutat Res 555, 149–71.
27. 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 G. L. (2010). A panel of urinary biomarkers to monitor reversibility of renal injury and a serum marker with improved potential to assess renal function. Nat Biotechnol 28, 486–94.
28. Persy V. P. Verstrepen W. A. Ysebaert D. K. De Greef K. E. De Broe M. E. (1999). Differences in osteopontin up-regulation between proximal and distal tubules after renal ischemia/reperfusion. Kidney Int 56, 601–11.
29. Pinches M. D. Betts C. J. Bickerton S. J. Burdett L. D. Thomas H. T. Derbyshire N. A. Jones H. B. Moores M. (2012a). Evaluation of novel renal biomarkers with a cisplatin model of kidney injury: Gender and dosage differences. Toxicol Pathol 40, 522–33.
30. Pinches M. D. Betts C. J. Bickerton S. J. Beattie L. Burdett L. D. Thomas H. T. Derbyshire N. A. Moores M. (2012b). Evaluation of novel urinary renal biomarkers with a cisplatin model of kidney injury: Effects of collection period. Toxicol Pathol 40, 534–40.
31. Pinches M. D. Betts C. J. Bickerton S. J. Beattie L. Burdett L. D. Thomas H. T. Derbyshire N. A. Moores M. Price S. A. (2012c). Evaluation of novel renal biomarkers with a cisplatin model of kidney injury: Methodology and reference ranges. Toxicol Pathol 40, 541–49.
32. Remuzzi A. Puntorieri S. Alfano M. Macconi D. Abbate M. Bertani T. Remuzzi G. (1992). Pathophysiologic implications of proteinuria in a rat model of progressive glomerular injury. Lab Invest 67, 572–79.
33. Rinaldi Tosi M. E. Bocanegra V. Manucha W. Gil Lorenzo A. Valles P. G. (2011). The Nrf2-Keap1 cellular defense pathway and heat shock protein 70 (Hsp70) response. Role in protection against oxidative stress in early neonatal unilateral ureteral obstruction (UUO). Cell Stress Chaperones 16, 57–68.
34. Rosenberg M. E. Silkensen J. (1995). Clusterin: Physiologic and pathophysiologic considerations. Int J Biochem Cell Biol 27, 633–45.
35. Ross D. (2004). Quinone reductases multitasking in the metabolic world. Drug Metab Rev 36, 639–54.
36. Ross D. Kepa J. K. Winski S. L. Beall H. D. Anwar A. Siegel D. (2000). NAD(P)H:quinone oxidoreductase 1 (NQO1): Chemoprotection, bioactivation, gene regulation and genetic polymorphisms. Chem Biol Interact 129, 77–97.
37. Rozell B. Hansson H. A. Guthenberg C. Tahir M. K. Mannervik B. (1993). Glutathione transferases of classes alpha, mu and pi show selective expression in different regions of rat kidney. Xenobiotica 23, 835–49.
38. Swain A. Turton J. Scudamore C. Maguire D. Pereira I. Freitas S. Smyth R. Munday M. Stamp C. Gandhi M. Sondh S. Ashall H. Francis I. Woodfine J. Bowles J. York M. (2012). Nephrotoxicity of hexachloro-1:3-butadiene in the male Hanover Wistar rat; correlation of minimal histopathological changes with biomarkers of renal injury. J Appl Toxicol 32, 417–28.
39. Swain A. Turton J. Scudamore C. L. Pereira I. Viswanathan N. Smyth R. Munday M. McClure F. Gandhi M. Sondh S. York M. (2011). Urinary biomarkers in hexachloro-1:3-butadiene-induced acute kidney injury in the female Hanover Wistar rat; correlation of alpha-glutathione S-transferase, albumin and kidney injury molecule-1 with histopathology and gene expression. J Appl Toxicol 31, 366–77.
40. Tesch G. H. (2010). Review: Serum and urine biomarkers of kidney disease: A pathophysiological perspective. Nephrology 15, 609–16.
41. 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. (2010). Kidney injury molecule-1 outperforms traditional biomarkers of kidney injury in preclinical biomarker qualification studies. Nat Biotechnol 28, 478–85.
42. Wang E. J. Snyder R. D. Fielden M. R. Smith R. J. Gu Y. Z. (2008). Validation of putative genomic biomarkers of nephrotoxicity in rats. Toxicology 246, 91–100.
43. 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. (2001). Expression of osteopontin in gentamicin-induced acute tubular necrosis and its recovery process. Kidney Int 59, 959–74.
44. Yang A. Trajkovic D. Illanes O. Ramiro-Ibanez F. (2007). Clinicopathological and tissue indicators of para-aminophenol nephrotoxicity in Sprague-Dawley rats. Toxicol Pathol 35, 521–32.
45. Yu Y. Jin H. Holder D. Ozer J.S. Villareal S. Shughrue P. Shi S. Figueroa D. J. Clouse H. Su M. Muniappa N. Troth S. P. Bailey W. Seng J. Aslamkhan A. G. Thudium D. Sistare F. D. Gerhold D. L. (2010). Urinary biomarkers trefoil factor 3 and albumin enable detection of kidney tubular injury. Nat Biotechnol 28, 470–77.
46. Zhang J. Brown R. P. Shaw M. Vaidya V. S. Zhou Y. Espandiari P. Sadrieh N. Stratmeyer M. Keenan J. Kilty C. G. Bonventre J. V. Goering P. L. (2008). Immunolocalization of Kim-1, RPA-1, and RPA-2 in kidney of gentamicin-, mercury-, or chromium-treated rats: relationship to renal distributions of iNOS and nitrotyrosine. Toxicol Pathol 36, 397–409.
47. Zhu H. Zhang L. Amin A. R. Li Y. B. (2008). Coordinated upregulation of a series of endogenous antioxidants and phase 2 enzymes as a novel strategy for protecting renal tubular cells from oxidative and electrophilic stress. Exp Bio Med 233, 753–65.
48. B.B.M., Zordoky, A., Anwar-Mohamed, M.E., Aboutabl, A.A.S., El-Kadi, Acute doxorubicin toxicity differentially alters cytochrome P450 expression and arachidonic acid metabolism in rat kidney and liver, Drug Metab Dispos, (2011), 39, 1440-1450