Gene expression analysis and urinary biomarker assays reveal activation of tubulointerstitial injury pathways in a rodent model of chronic proteinuria (Doxorubicin Nephropathy)

Nephron - Experimental Nephrology

Volumn 124, Issue 1-2, 2013, Pages 1-10

  Cianciolo, Rachel ^a,b   Yoon, Lawrence ^a   Krull, David ^a   Stokes, Alan ^a   Rodriguez, Alex ^a   Jordan, Holly ^a   Cooper, David ^a   Falls, James G ^a   Cullen, John ^a   Kimbrough, Carie ^a   Berridge, Brian ^a  

^a GLAXOSMITHKLINE   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Chronic proteinuria; Gene expression microarray; Kidney injury molecule 1; Tubulointerstitial injury; Urinary biomarker assays

Indexed keywords

ACTIVATING TRANSCRIPTION FACTOR 3; ADAMTS1 PROTEIN; ALLOGRAFT INFLAMMATORY FACTOR 1; ALPHA SMOOTH MUSCLE ACTIN; ALPHA TROPOMYOSIN; BIOLOGICAL MARKER; CALBINDIN; CATHEPSIN S; CD24 ANTIGEN; CHOLESTEROL; COLLAGEN TYPE 3; CREATININE; DECORIN; DOXORUBICIN; ENDOTHELIN RECEPTOR; HERMES ANTIGEN; KIDNEY INJURY MOLECULE 1; LIPOCORTIN 5; MEPRIN; NUCLEOPHOSMIN; OSTEOPONTIN; PROTHROMBIN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE PHOSPHATE OXIDASE 4; SERUM ALBUMIN; SOMATOMEDIN BINDING PROTEIN 1; TENASCIN; TROPOMYOSIN; UNCOUPLING PROTEIN 2; VASCULOTROPIN A; XANTHINE DEHYDROGENASE; CALCIUM BINDING PROTEIN; GLYCINE AMIDINOTRANSFERASE; MATRIX GLA PROTEIN; UNCLASSIFIED DRUG;

ALBUMIN BLOOD LEVEL; ALBUMINURIA; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CHOLESTEROL BLOOD LEVEL; CONTROLLED STUDY; CREATININE BLOOD LEVEL; DISEASE COURSE; DISEASE SEVERITY; EXTRACELLULAR MATRIX; FOCAL GLOMERULOSCLEROSIS; GENE EXPRESSION; HISTOLOGY; HISTOPATHOLOGY; KIDNEY DISEASE; KIDNEY HYPERTROPHY; KIDNEY INJURY; KIDNEY PROXIMAL TUBULE; LASER CAPTURE MICRODISSECTION; LIMIT OF DETECTION; MALE; NEPHROTOXICITY; NONHUMAN; PODOCYTE; PRIORITY JOURNAL; PROTEIN URINE LEVEL; PROTEINURIA; RAT; UPREGULATION; UREA NITROGEN BLOOD LEVEL; URINARY EXCRETION; ANIMAL CELL; ANTIBODY LABELING; CHRONIC PROTEINURIA; CREATININE URINE LEVEL; IMMUNOHISTOCHEMISTRY; MICROARRAY ANALYSIS; PROTEIN EXPRESSION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUBULOINTERSTITIAL INJURY;

ALBUMINURIA; ANIMALS; BIOLOGICAL MARKERS; CELL ADHESION MOLECULES; CHRONIC DISEASE; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; DOXORUBICIN; IMMUNOHISTOCHEMISTRY; KIDNEY DISEASES; KIDNEY TUBULES, PROXIMAL; LIPOCALINS; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OSTEOPONTIN; PROTEINURIA; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TIME FACTORS; TRANSCRIPTOME;

EID: 84890453288     PISSN: None     EISSN: 16602129     Source Type: Journal    
DOI: 10.1159/000355542     Document Type: Article

References (51)

1. Erkan E, Deverajan P, Schwartz GJ: Mitochondria are the major targets in albumininduced apoptosis in proximal tubule cells. J Am Soc Nephrol 2007; 18: 1199-1208.
2. Bertani T, Poggi A, Pozzoni R, Delaini F, Sacchi G, Thoua Y, Mecca G, Remuzzi G, Donati MB: Adriamycin-induced nephrotic syndrome in rats. Lab Invest 1982; 46: 16-22.
3. Rahman A, Carmichael D, Harris M, Roh JK: Comparative pharmacokinetics of free doxorubicin and doxorubicin entrapped cardiolipid liposomes. Cancer Res 1986; 46: 2295-2299.
4. Swain A, Turton J, Scudamore CL, Pereira I, Viswanathan N, Smyth R, Munday M, Mc- Clure F, Gandhi M, Sondh S, York M: Urinary biomarkers in hexachloro-1: 3-butadiene-induced acute kidney injury in the female Hanover Wistar rat; correlation of ?-glutathione S -transferase, albumin, and kidney injury molecule-1 with histopathology and gene expression. J Appl Toxicol 2011; 31: 366-377.
5. Cullen JM, Falls JG, Brown HR, Yoon LW, Cariello NF, Faiola B, Kimbrough CL, Jordan HL, Miller RT: Time course gene expression using laser capture microscopy-extracted bile ducts, but not hepatic parenchyma, reveals acute alpha-naphthylisothiocyanate toxicity. Toxicol Pathol 2010; 38: 715-729.
6. Gross MD, Eggen MA, Simon AM, van Pilsum JF: The purification and characterization of human kidney L -arginine: glycine amidinotransferase. Arch Biochem Biophys 1986; 251: 747-755.
7. Wang E-J, Snyder RD, Fielden MR, Smith RJ, Gu Y-Z: Validation of putative genomic biomarkers of nephrotoxicity in rats. Toxicology 2008; 246: 91-100.
8. Kastner C, Pohl M, Sendeski M, Stange G, Wagner CA, Jensen B, Patzak A, Bachmann S, Theilig F: Effects of receptor-mediated endocytosis and tubular protein composition on volume retention in experimental glomerulonephritis. Am J Phys Renal Phys 2009; 296: 902-911.
9. Bonventre JV: Kidney injruy molecule-1 (KIM-1): a urinary biomarker and much more. Nephrol Dial Transplant 2009; 24: 3265-3268.
10. Kramer AB, van Timmeren MM, Schuurs TA, Vaidya VS, Bonventre JV, van Goor H, Navis G: Reduction of proteinuria in adriamycininduced nephropathy is associated with reduction of renal kidney injury molecule (KIM-1) over time. Am J Phys Renal Phys 2009; 296:F1136-F1145.
11. Rouschop KMA, Roelofs JJTH, Claessen N, da Costa Martina P, Zwaginga J-J, Pal ST, Weening JJ, Florquin S: Protection against renal ischemia reperfusion injury by CD44 disruption. J Am Soc Nephrol 2005; 16: 2034-2043.
12. Yuen PST, Jo S-K, Holly MK, Hu X, Star RA: Ischemic and nephrotoxic acute renal failure are distinguished by their broad transcriptomic responses. Physiol Genomics 2006; 25: 375-386.
13. Basile DP, Frederich K, Chelladurai B, Leonard EC, Parrish AR: Renal ischemia reperfusion inhibits VEGF expression and induces ADAMTS-1, a novel VEGF inhibitor. Am J Phys Renal Phys 2008; 294: 928-936.
14. Wu CC, Chen J-S, Huang C-F, Chen C-C, Lu K-C, Chu P, Sytwu H-K, Lin Y-F: Approaching biomarkers of membranous nephropathy from a murine model to human disease. J Biomed Biotechnol 2011; 2011: 581928.
15. Thompson KL, Afshari CA, Amin RP, Bertram TA, Car B, Cunningham M, Kind C, Kramer J, Lawton M, Mirsky M, Naciff JM, Oreffo V, Pine PS, Sistare F: Identification of platform independent gene expression markers of cisplatin nephrotoxicity. Environ Health Perspect 2004; 112: 488-494.
16. Yoshida T, Tang S-S, Hsiao L-L, Jensen RV, Ingelfinger JR, Gullans SR: Global analysis of gene expression in renal ischemia-reperfusion in the mouse. Biochem Biophys Res Commun 2002; 291: 787-794.
17. Thukral SK, Nordone PJ, Hu R, Sullivan L, Galambos E, Fitzpatrick VD, Healy L, Bass MB, Cosenza ME, Afshari CA: Prediction of nephrotoxicant action and identification of candidate toxicity-related biomarkers. Toxicol Pathol 2005; 33: 343-355.
18. Nazeer K, Janech MG, Lin JJC, Ryan KJ, Arthur JM, Budisavljevic MN: Changes in protein profiles during the course of experimental glomerulonephritis. Am J Phys Renal Phys 2009; 296: 186-193.
19. Kieran NE, Doran PP, Connolly SB, Greenan M-C, Higgins DF, Leonard M, Godson C, Taylor CT, Henger A, Kretzler M, Burne MJ, Rabb H, Brady HR: Modification of the transcriptomic response to renal ischemia/reperfusion injury by lipoxin analog. Kidney Int 2003; 64: 480-492.
20. Huang Q, Dunn RT, Jayadev S, DiSorbo O, Pack FD, Farr SB, Stoll RE, Blanchard KT: Assessment of cisplatin-induced nephrotoxicity by microarray technology. Toxicol Sci 2001; 63: 196-207.
21. Toubas J, Beck S, Pageaud A-L, Huby A-C, Mael-Ainin M, Dussaule J-C, Chatziantoniou C, Chadjichristos CE: Alteration of connexin expression is an early signal for chronic kidney disease. Am J Phys Renal Phys 2011; 301: 24-32.
22. Yanagita M, Okuda T, Endo S, Tanaka M, Takahashi K, Sugiyama F, Kunita S, Takahashi S, Fukatsu A, Yanagisawa M, Kita T, Sakurai T: Uterine sensitization-associated gene-1 (USAG-1), a novel BMP antagonist expressed in the kidney, accelerates tubular injury. J Clin Invest 2006; 116: 70-79.
23. Amerkhanov ZG, Kashapova IY, Popov VN: The role of UCP2 and ADP/ATP antiporter in superoxide radical induced uncoupling in kidney mitochondria. Dokl Biochem Biophys 2008; 423: 328-330.
24. 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 Develop 2008; 11: 60-71.
25. Rudnicki M, Eder S, Perco P, Enrich J, Scheiber K, Koppelstatter C, Schratzberger G, Mayer B, Oberhauer R, Meyer TW, Mayer G: Gene expression profiles of human proximal tubular epithelial cells in proteinuric nephropathies. Kidney Int 2007; 71: 325-335.
26. Fiebeler A, Park J-K, Muller DN, Lindschau C, Mengel M, Merkel S, Banas B, Luft FC, Haller H: Growth arrest specific protein 6/ AxI signalling in human inflammatory renal diseases. Am J Kidney Dis 2004; 43: 286-295.
27. Basile DP, Frederich K, Alausa M, Vio CP, Liang M, Rieder MR, Greene AS, Cowley AW Jr: Identification of persistently altered gene expression in the kidney after functional recovery from ischemic acute renal failure. Am J Phys Renal Phys 2005; 288: 953-963.
28. Sanchez-Nino M, Sanz A, Ilhamo P, Lassila M, Holthofer H, Mezzano S, Aros C, Groop P, Saleem M, Mathieson P, Langham R, Kretzler M, Nair V, Lemley K, Nelson R, Mervaala E, Rastaldi MP, Ruiz-Ortega M, Martin-Ventura J, Egido J, Ortiz A: The MIF receptor CD74 in diabetic podocyte injury. J Am Soc Nephrol 2009; 20: 353-362.
29. Pigmule M, Lopez-Hellin J, Sune G, Tornavaca O, Camano S, Tejedor A, Meseguer A: Differential proteomic analysis of cyclosporine Ainduced toxicity in renal proximal tubule cells. Nephrol Dial Transplant 2009; 24: 2672-2686.
30. Shoskes DA: Effect of bioflavonoids quercetin and curcumin on ischemic renal injury: a new class of renoprotective agents. Transplantation 1998; 66: 147-152.
31. Tsubata Y, Sakatsume M, Ogawa A, Alchi B, Kaneko Y, Kuroda T, Kawachi H, Narita I, Yamamoto T, Gejyo F: Expression of allograft inflammatory factor-1 in kidneys: a novel molecular component of podocyte. Kidney Int 2006; 70: 1948-1954.
32. Schaefer L, Grone H-J, Raslik I, Robenek H, Ugorcakova J, Budny S, Schaefer RM, Kresse H: Small proteoglycans of normal adult human kidney: distinct expression patterns of decorin, biglycan, fibromodulin, and lumican. Kidney Int 2000; 58: 1557-1568.
33. Stokes MB, Holler S, Cui Y, Hudkins KL, Eitner F, Fogo A, Alpers CE: Expression of decorin, biglycan and collagen type I in human renal fibrosing disease. Kidney Int 2000; 57: 487-498.
34. Lee S, Huen S, Nishio H, Nishio S, Lee HK, Choi B-S, Ruhrberg C, Cantley LG: Distinct macrophage phenotypes contribute to kidney injury and repair. J Am Soc Nephrol 2011; 22: 317-326.
35. Oleggini R, Musante L, Menoni S, Botti G, Di Duca M, Prudenziati M, Carrea A, Ravazzolo R, Ghiggeri G: Characterization of a DNA binding site that mediates the stimulatory effect of cyclosporin-A on type III collagen expression in renal cells. Nephrol Dial Transplant 2000; 15: 778-785.
36. Tornavaca O, Sarro E, Pascual G, Bardaji B, Montero MA, Salcedo MT, Plana M, Lopez- Hellin J, Itarte E, Meseguer A: KAP degradation by calpain is associated with CK2 phosphorylation and provides a novel mechanism for cyclosporine A-induced proximal tubule injury. PLoS One 2011; 6:e25746.
37. O'Bryan T, Weiher H, Rennke HG, Kren S, Hostestter TH: Course of renal injury in the Mpv 17-deficient transgenic mice. J Am Soc Nephrol 2000; 11: 1067-1074.
38. Thijssen S, Cuypers A, Maringwa J, Smeets K, Horemans N, Lambrichts I, Van Kerkhove E: Low cadmium exposure triggers a biphasic oxidative stress response in mice kidneys. Toxicology 2007; 236: 29-41.
39. Xu EY, Perlina A, Vu H, Troth SP, Brennan RJ, Aslamkhan AG, Xu Q: Integrated pathway analysis of rat urine metabolic profiles and kidney transcriptomic profiles to elucidate the systems toxicology of model nephrotoxicants. Chem Res Toxicol 2008; 21: 1548-1561.
40. Granqvist A, Nilsson UA, Ebefors K, Haraldsson B, Nystrom J: Impaired glomerular and tubular antioxidative defense mechanisms in nephrotic syndrome. Am J Phys Renal Phys 2010; 299: 898-904.
41. Lee EM, Pollock C, Drumm K, Barden JA, Poronnik P: Effects of pathophysiological concentrations of albumin on NHE3 activity and cell proliferation in primary cultures of human proximal tubule cells. Am J Phys Renal Phys 2003; 285: 748-757.
42. Haguenauer A, Raimbault S, Masscheleyn S, del Mar Gonzalez-Barroso M, Criscuolo F, Plamondon J, Miroux B, Ricquier D, Richard D, Bouillaud F, Pecqueur C: A new renal mitochondrial carrier, KMCP1, is up-regulated during tubular cell regeneration and induction of antioxidant enzymes. J Biol Chem 2005; 280: 22036-22043.
43. Waters NJ, Waterfield CJ, Farrant RD, Holmes E, Nicholson JK: Metabonomic deconvolution of embedded toxicity: application to thioacetamide hepato- and nephrotoxicity. Chem Res Toxicol 2005; 18: 639-654.
44. Hu E, Chen Z, Fredrickson T, Gellai M, Jugus M, Contino L, Spurr N, Sims M, Halsey W, Van Horn S, Mao J, Sathe G, Brooks D: Identification of a novel kidney-specific gene downregulated in acute ischemic renal failure. Am J Phys Renal Phys 2000; 279: 426-439.
45. Sola A, Weigert A, Jung M, Vinuesa E, Brecht K, Weis N, Brune B, Borregaard N, Hotter G: Sphingosine-1-phosphate signaling induces the production of Lcn-2 by macrophages to promote kidney regeneration. J Pathol 2011; 225: 597-608.
46. Rodwell GEJ, Sonu R, Zahn JM, Lund J, Wilhelmy J, Wang L, Xiao W, Mindrinos M, Crane E, Segal E, Myers BD, Brooks JD, Davis RW, Higgins J, Owen AB, Kim SK: A transcriptional profile of aging in the human kidney. PLoS Biol 2004; 2:e427.
47. Flechner SM, Kurian SM, Head SR, Sharp SM, Whisenant TC, Zhang J, Chismar JD, Horvarth S, Mondala T, Gilmartin T, Cook DJ, Kay SA, Walker JR, Salomon DR: Kidney transplant rejection and tissue injury by gene profiling of biopsies and peripheral blood lymphocytes. Am J Transplant 2004; 4: 1475- 1489.
48. Bonventre JV, Vaidya VS, Schmouder RS, Feig P, Dieterle F: Next-generation biomarkers for detecting kidney toxicity. Nat Biotech 2010; 28: 436-440.
49. Ohse T, Tanaka T, Ota T, Miyata T, Kojima I, Ingelfinger JR, Ogawa S, Fujita T, Nangaku M: Albumin induces endoplasmic reticulum stress and apoptosis in renal proximal tubular cells. Kidney Int 2006; 70: 1447-1455.
50. Motoyoshi Y, Matsusaka T, Saito A, Pastan I, Willnow TE, Mizutani S, Ichikawa I: Megalin participates in the early injury of proximal tubule cells in glomerular disease with non-selective proteinuria. Kidney Int 2008; 74: 1262- 1269.
51. Amin RP, Vickers AE, Sistare F, Thompson KL, Roman RJ, Lawton M, Kramer J, Hamadeh HK, Collins J, Grissom S, Bennett L, Tucker CJ, Wild S, Kind C, Oreffo V, Davis JW II, Curtiss S, Naciff JM, Cunningham M, Tennant R, Stevens J, Car B, Bertram TA, Afshari CA: Identification of putative genebased markers of renal toxicity. Environ Health Perspect 2004; 112: 465-479.