Carcinogen-specific gene expression profiles in short-term treated Eker and wild-type rats indicative of pathways involved in renal tumorigenesis.

Eker rats heterozygous for a dominant germline mutation in the tuberous sclerosis 2 (Tsc2) tumor suppressor gene were used as a model to study renal carcinogenesis. Eker and corresponding wild-type rats were exposed to genotoxic aristolochic acid (AA) or non-genotoxic ochratoxin A (OTA) to elucidate early carcinogen-specific gene expression changes and to test whether Eker rats are more sensitive to carcinogen-induced changes in gene expression. Male Eker and wild-type rats were gavaged daily with AA (10 mg/kg body weight) or OTA (210 microg/kg body weight). After 1, 3, 7, and 14 days of exposure, renal histopathology, tubular cell proliferation, and Affymetrix gene expression profiles from renal cortex/outer medulla were analyzed. AA-treated Eker and wild-type rats were qualitatively comparable in all variables assessed, suggesting a Tsc2-independent mechanism of action. OTA treatment resulted in slightly increased cortical pathology and significantly elevated cell proliferation in both strains, although Eker rats were more sensitive. Deregulated genes involved in the phosphatidylinositol 3-kinase-AKT-Tsc2-mammalian target of rapamycin signaling, among other important genes prominent in tumorigenesis, in conjunction with the enhanced cell proliferation and presence of preneoplastic lesions suggested involvement of Tsc2 in OTA-mediated toxicity and carcinogenicity, especially as deregulation of genes involved in this pathway was more prominent in the Tsc2 mutant Eker rat.

[1]  M. Gekle,et al.  Ochratoxin A at nanomolar concentrations: a signal modulator in renal cells. , 2005, Molecular nutrition & food research.

[2]  T. Goldsworthy,et al.  Predisposition to renal cell carcinoma due to alteration of a cancer susceptibility gene. , 1992, Science.

[3]  M. Wiessler,et al.  Activating mutations at codon 61 of the c-Ha-ras gene in thin-tissue sections of tumors induced by aristolochic acid in rats and mice. , 1991, Cancer letters.

[4]  Ronit Vogt Sionov,et al.  The cellular response to p53: the decision between life and death , 1999, Oncogene.

[5]  E. Kulinskaya,et al.  Renal tumourigenesis in male rats in response to chronic dietary ochratoxin A , 2005, Food additives and contaminants.

[6]  P. Mosesso,et al.  Ochratoxin a causes DNA damage and cytogenetic effects but no DNA adducts in rats. , 2005, Chemical research in toxicology.

[7]  J. Schlatter,et al.  Ochratoxin A induces oxidative DNA damage in liver and kidney after oral dosing to rats. , 2005, Molecular nutrition & food research.

[8]  H. Liber,et al.  Genotoxic and mutagenic effects of the diagnostic use of thallium-201 in nuclear medicine. , 1991, Mutation research.

[9]  A. Grollman,et al.  QUANTITATIVE DETERMINATION OF ARISTOLOCHIC ACID-DERIVED DNA ADDUCTS IN RATS USING 32P-POSTLABELING/POLYACRYLAMIDE GEL ELECTROPHORESIS ANALYSIS , 2006, Drug Metabolism and Disposition.

[10]  G. Thomas mTOR and cancer: reason for dancing at the crossroads? , 2006, Current opinion in genetics & development.

[11]  G. Xiao,et al.  Allelic loss at the tuberous sclerosis 2 locus in spontaneous tumors in the Eker rat , 1995, Molecular carcinogenesis.

[12]  O. Hino,et al.  Molecular genetic basis of renal carcinogenesis in the Eker rat model of tuberous sclerosis(Tsc2) , 1995, Molecular carcinogenesis.

[13]  A. Knudson,et al.  Predisposition to renal carcinoma in the Eker rat is determined by germ-line mutation of the tuberous sclerosis 2 (TSC2) gene. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[14]  J. Hayes,et al.  Reduction in antioxidant defenses may contribute to ochratoxin A toxicity and carcinogenicity. , 2006, Toxicological sciences : an official journal of the Society of Toxicology.

[15]  S. Hester,et al.  The transcriptional profile of the kidney in Tsc2 heterozygous mutant Long Evans (Eker) rats compared to wild-type. , 2004, Mutation research.

[16]  K. Artzt,et al.  Loss of function of the tuberous sclerosis 2 tumor suppressor gene results in embryonic lethality characterized by disrupted neuroepithelial growth and development. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[17]  D. Dietrich,et al.  The Presence of α2u-Globulin Is Necessary for d-Limonene Promotion of Male Rat Kidney Tumors , 1991 .

[18]  D. Dietrich,et al.  The presence of alpha 2u-globulin is necessary for d-limonene promotion of male rat kidney tumors. , 1991, Cancer Research.

[19]  B. Sopko,et al.  Human cytosolic enzymes involved in the metabolic activation of carcinogenic aristolochic acid: evidence for reductive activation by human NAD(P)H:quinone oxidoreductase. , 2003, Carcinogenesis.

[20]  T. Dingermann,et al.  A new approach to studying ochratoxin A (OTA)-induced nephrotoxicity: expression profiling in vivo and in vitro employing cDNA microarrays. , 2003, Toxicological sciences : an official journal of the Society of Toxicology.

[21]  V. Arlt,et al.  Aristolochic acid as a probable human cancer hazard in herbal remedies: a review. , 2002, Mutagenesis.

[22]  G. Boorman,et al.  Renal Lesions Induced by Ochratoxin A Exposure in the F344 Rat , 1992, Toxicologic pathology.

[23]  Tao Chen,et al.  Gene Expression Profiles Distinguish the Carcinogenic Effects of Aristolochic Acid in Target (Kidney) and Non-target (Liver) Tissues in Rats , 2006, BMC Bioinformatics.

[24]  J. Slingerland,et al.  Multiple Roles of the PI3K/PKB (Akt) Pathway in Cell Cycle Progression , 2003, Cell cycle.

[25]  Y. Kubo,et al.  A germline insertion in the tuberous sclerosis (Tsc2) gene gives rise to the Eker rat model of dominantly inherited cancer , 1995, Nature Genetics.

[26]  K. Okubo,et al.  Induction of Glia Maturation Factor-β in Proximal Tubular Cells Leads to Vulnerability to Oxidative Injury through the p38 Pathway and Changes in Antioxidant Enzyme Activities* , 2003, Journal of Biological Chemistry.

[27]  H. Ellinger-Ziegelbauer,et al.  Comparison of the expression profiles induced by genotoxic and nongenotoxic carcinogens in rat liver. , 2005, Mutation research.

[28]  Paul Tempst,et al.  Phosphorylation and Functional Inactivation of TSC2 by Erk Implications for Tuberous Sclerosisand Cancer Pathogenesis , 2005, Cell.

[29]  T. Goldsworthy,et al.  Hereditary renal cell carcinoma in the Eker rat: a unique animal model for the study of cancer susceptibility. , 1995, Toxicology Letters.

[30]  Graham M Lord,et al.  DNA adducts and p53 mutations in a patient with aristolochic acid-associated nephropathy. , 2004, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[31]  Lieng-Yi Lu,et al.  Chronic renal failure rats are highly sensitive to aristolochic acids, which are nephrotoxic and carcinogenic agents. , 2006, Cancer letters.

[32]  M. Grigorov,et al.  A toxicogenomics approach to identify new plausible epigenetic mechanisms of ochratoxin a carcinogenicity in rat. , 2006, Toxicological sciences : an official journal of the Society of Toxicology.

[33]  D. Dietrich,et al.  The role of alpha2u-globulin in ochratoxin A induced renal toxicity and tumors in F344 rats. , 1999, Toxicology letters.

[34]  U. Mengs,et al.  The carcinogenic action of aristolochic acid in rats , 1982, Archives of Toxicology.

[35]  T. Yoshino,et al.  Multicentric Castleman's disease associated with glomerular microangiopathy and MPGN-like lesion: does vascular endothelial cell-derived growth factor play causative or protective roles in renal injury? , 2004, American journal of kidney diseases : the official journal of the National Kidney Foundation.

[36]  T. Goldsworthy,et al.  Promotion by sodium barbital induces early development but does not increase the multiplicity of hereditary renal tumors in Eker rats. , 2000, Carcinogenesis.

[37]  D. Dietrich,et al.  Preneoplastic lesions in rodent kidney induced spontaneously or by non-genotoxic agents: predictive nature and comparison to lesions induced by genotoxic carcinogens. , 1991, Mutation research.

[38]  Heidrun Ellinger-Ziegelbauer,et al.  Establishment of a protocol for the gene expression analysis of laser microdissected rat kidney samples with affymetrix genechips. , 2006, Toxicology and applied pharmacology.

[39]  J. Trosko,et al.  Determination of the epigenetic effects of ochratoxin in a human kidney and a rat liver epithelial cell line. , 2002, Toxicon : official journal of the International Society on Toxinology.

[40]  Kathleen A. Hinchman,et al.  Progression , 1896, Journal of Adolescent & Adult Literacy.

[41]  May 1 , 1965 .

[42]  D. Hanahan,et al.  The Hallmarks of Cancer , 2000, Cell.

[43]  R. Yeung,et al.  The Tuberous Sclerosis Complex Genes in Tumor Development , 2004, Cancer investigation.

[44]  M. Wiessler,et al.  Aristolochic acid binds covalently to the exocyclic amino group of purine nucleotides in DNA. , 1990, Carcinogenesis.

[45]  Donghui Li,et al.  Reduced constitutive 8-oxoguanine-DNA glycosylase expression and impaired induction following oxidative DNA damage in the tuberin deficient Eker rat. , 2003, Carcinogenesis.