In vivo murine hepatic microRNA and mRNA expression signatures predicting the (non-)genotoxic carcinogenic potential of chemicals

Archives of Toxicology

Volumn 88, Issue 4, 2014, Pages 1023-1034

  Melis, Joost P M ^a,b   Derks, Kasper W J ^c   Pronk, Tessa E ^a   Wackers, Paul ^a,c,d   Schaap, Mirjam M ^a,b   Zwart, Edwin ^b   Van IJcken, Wilfred F J ^c   Jonker, Martijs J ^d   Breit, Timo M ^d   Pothof, Joris ^c   Van Steeg, Harry ^a,b   Luijten, Mirjam ^a,b  

^a NATIONAL INSTITUTE FOR PUBLIC HEALTH AND THE ENVIRONMENT   (Netherlands)

^b LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

^c ERASMUS MEDICAL CENTER   (Netherlands)

^d UNIVERSITY OF AMSTERDAM   (Netherlands)

Author keywords

Biomarker; Classification; Gene expression; Genotoxic and non genotoxic carcinogen; MicroRNA; Risk assessment

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 4,4' ISOPROPYLIDENEDIPHENOL; 7,12 DIMETHYLBENZ[A]ANTHRACENE; AFLATOXIN B1; AMIODARONE; BENZO[A]PYRENE; BIS(TRIBUTYLTIN) OXIDE; CARBON TETRACHLORIDE; CISPLATIN; CYCLOSPORIN A; DICLOFENAC; DIETHYLSTILBESTROL; DIISODECYL PHTHALIC ACID ESTER; DIMETHYLNITROSAMINE; ESTRADIOL; MANNITOL; MESSENGER RNA; MICRORNA; MITOMYCIN; N (2 FLUORENYL)ACETAMIDE; PHENOBARBITAL; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; RESERPINE; TOLBUTAMIDE; UNCLASSIFIED DRUG; VALPROIC ACID; CARCINOGEN; GENETIC MARKER; MUTAGENIC AGENT;

ALGORITHM; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; EXPOSURE; GENE EXPRESSION; GENE EXPRESSION PROFILING; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; PREDICTIVE VALUE; PRIORITY JOURNAL; RISK ASSESSMENT; TOXICOGENETICS; WILD TYPE; ANIMAL; C57BL MOUSE; CLASSIFICATION; DISCRIMINANT ANALYSIS; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC MARKER; LIVER; METABOLISM; PROCEDURES; REPRODUCIBILITY; TIME FACTOR; VALIDATION STUDY;

MURINAE; MUS;

ALGORITHMS; ANIMALS; CARCINOGENS; DISCRIMINANT ANALYSIS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETIC MARKERS; LIVER; MALE; MICE; MICE, INBRED C57BL; MICRORNAS; MUTAGENS; REPRODUCIBILITY OF RESULTS; RISK ASSESSMENT; RNA, MESSENGER; TIME FACTORS; TOXICOGENETICS;

EID: 84897110677     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-013-1189-z     Document Type: Article

References (49)

1. Bender K, Gottlicher M, Whiteside S, Rahmsdorf HJ, Herrlich P (1998) Sequential DNA damage-independent and -dependent activation of NF-kappaB by UV. EMBO J 17(17):5170-5181 (Pubitemid 28408483)
2. Benjamini Y, Hochberg Y (1995) Controlling the false discovery rate: a practical and powerful approach to multiple testing series b (methodological). J Roy Stat Soc 57(1):289-300
3. Chen T (2010) The role of MicroRNA in chemical carcinogenesis. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 28(2):89-124
4. Chen JS, Su IJ, Leu YW, Young KC, Sun HS (2012) Expression of T-cell lymphoma invasion and metastasis 2 (TIAM2) promotes proliferation and invasion of liver cancer. Int J Cancer 130(6):1302-1313
5. Coma S, Amin DN, Shimizu A, Lasorella A, Iavarone A, Klagsbrun M (2010) Id2 promotes tumor cell migration and invasion through transcriptional repression of semaphorin 3F. Cancer Res 70(9):3823-3832
6. Concepcion CP, Han YC, Mu P, Bonetti C, Yao E, D'Andrea A, Vidigal JA, Maughan WP, Ogrodowski P, Ventura A (2012) Intact p53-dependent responses in miR-34-deficient mice. PLoS Genet 8(7):e1002797
7. de Leeuw WC, Rauwerda H, Jonker MJ, Breit TM (2008) Salvaging affymetrix probes after probe-level re-annotation. BMC Res Notes 166
8. de Vries A, van Oostrom CT, Dortant PM, Beems RB, van Kreijl CF, Capel PJ, van Steeg H (1997) Spontaneous liver tumors and benzo[a]pyrene-induced lymphomas in XPA-deficient mice. Mol Carcinog 19(1):46-53 (Pubitemid 27237224)
9. Elamin BK, Callegari E, Gramantieri L, Sabbioni S, Negrini M (2011) MicroRNA response to environmental mutagens in liver. Mutat Res 717(1-2):67-76
10. Ellinger-Ziegelbauer H, Gmuender H, Bandenburg A, Ahr HJ (2008) Prediction of a carcinogenic potential of rat hepatocarcinogens using toxicogenomics analysis of short-term in vivo studies. Mutat Res 637(1-2):23-39 (Pubitemid 350256758)
11. Fernandez-Salguero PM, Hilbert DM, Rudikoff S, Ward JM, Gonzalez FJ (1996) Aryl-hydrocarbon receptor-deficient mice are resistant to 2,3,7,8-tetrachlorodibenzo-p-dioxin-induced toxicity. Toxicol Appl Pharmacol 140(1):173-179 (Pubitemid 26329475)
12. Fielden MR, Brennan R, Gollub J (2007) A gene expression biomarker provides early prediction and mechanistic assessment of hepatic tumor induction by nongenotoxic chemicals. Toxicol Sci 99(1):90-100 (Pubitemid 47250370)
13. Fielden MR, Nie A, McMillian M, Elangbam CS, Trela BA, Yang Y, Dunn RT, Dragan Y, Fransson-Stehen R, Bogdanffy M et al (2008) Interlaboratory evaluation of genomic signatures for predicting carcinogenicity in the rat. Toxicol Sci 103(1):28-34 (Pubitemid 351524474)
14. Fielden MR, Adai A, Dunn RT, Olaharski A, Searfoss G, Sina J, Aubrecht J, Boitier E, Nioi P, Auerbach S et al (2011) Development and evaluation of a genomic signature for the prediction and mechanistic assessment of nongenotoxic hepatocarcinogens in the rat. Toxicol Sci 124(1):54-74
15. Gao C, Pang L, Ren C, Ma T (2012) Decreased expression of Nedd4L correlates with poor prognosis in gastric cancer patient. Med Oncol 29(3):1733-1738
16. Guyton KZ, Kyle AD, Aubrecht J, Cogliano VJ, Eastmond DA, Jackson M, Keshava N, Sandy MS, Sonawane B, Zhang L et al (2009) Improving prediction of chemical carcinogenicity by considering multiple mechanisms and applying toxicogenomic approaches. Mutat Res 681(2-3):230-240
17. He L, He X, Lim LP, De SE, Xuan Z, Liang Y, Xue W, Zender L, Magnus J, Ridzon D et al (2007) A microRNA component of the p53 tumour suppressor network. Nature 447(7148):1130-1134 (Pubitemid 47014436)
18. Heneghan HM, Miller N, Kerin MJ (2010) MiRNAs as biomarkers and therapeutic targets in cancer. Curr Opin Pharmacol 10(5):543-550
19. Hernandez LG, van Steeg H, Luijten M, van Benthem J (2009) Mechanisms of non-genotoxic carcinogens and importance of a weight of evidence approach. Mutat Res 682(2-3):94-109
20. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP (2003) Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4(2):249-264
21. Jain AK, Barton MC (2012) Unmet expectations: miR-34 plays no role in p53-mediated tumor suppression in vivo. PLoS Genet 8(7):e1002859
22. Jonker MJ, Bruning O, van Iterson M, Schaap MM, van der Hoeven TV, Vrieling H, Beems RB, de Vries A, van Steeg H, Breit TM et al (2009) Finding transcriptomics biomarkers for in vivo identification of (non-)genotoxic carcinogens using wild-type and Xpa/ p53 mutant mouse models. Carcinogenesis 30(10):1805-1812
23. Jonker MJ, Melis JP, Kuiper RV, van der Hoeven TV, Wackers PF, Robinson J, van der Horst GT, Dolle ME, Vijg J, Breit TM et al (2013) Life spanning murine gene expression profiles in relation to chronological and pathological aging in multiple organs. Aging Cell 12(5):901-909
24. Kasinski AL, Slack FJ (2011) Epigenetics and genetics. MicroRNAs en route to the clinic: progress in validating and targeting micro- RNAs for cancer therapy. Nat Rev Cancer 11(12):849-864
25. Kinzler V (2002) The genetic basis of human cancer, 2nd edn. McGraw-Hill, New York
26. Lasorella A, Rothschild G, Yokota Y, Russell RG, Iavarone A (2005) Id2 mediates tumor initiation, proliferation, and angiogenesis in Rb mutant mice. Mol Cell Biol 25(9):3563-3574 (Pubitemid 40559563)
27. Lilienblum W, Dekant W, Foth H, Gebel T, Hengstler JG, Kahl R, Kramer PJ, Schweinfurth H, Wollin KM (2008) Alternative methods to safety studies in experimental animals: role in the risk assessment of chemicals under the new European Chemicals Legislation (REACH). Arch Toxicol 82(4):211-236
28. Luijten M, Muller JJA, Hernandez LG, van der Ven LTM, & van Benthem J (2012) Prediction of carcinogenic potential of substances using repeated dose toxicity data (Rep. No. 340700006/2012)
29. Malik AI, Williams A, Lemieux CL, White PA, Yauk CL (2012) Hepatic mRNA, microRNA, and miR-34a-target responses in mice after 28 days exposure to doses of benzo(a)pyrene that elicit DNA damage and mutation. Environ Mol Mutagen 53(1):10-21
30. Manuppello J, Willett C (2008) Longer rodent bioassay fails to address 2-year bioassay's flaws. Environ Health Perspect 116(12):A516-A517
31. Melis JP, Kuiper RV, Zwart E, Robinson J, Pennings JL, van Oostrom CT, Luijten M, Van SH (2013a) Slow accumulation of mutations in Xpc(-/-) mice upon induction of oxidative stress. DNA Repair (Amst) 12(12):1081-1086
32. Melis JP, Speksnijder EN, Kuiper RV, Salvatori DC, Schaap MM, Maas S, Robinson J, Verhoef A, Van BJ, Luijten M et al (2013b) Detection of genotoxic and non-genotoxic carcinogens in Xpc(- /-)p53(±) mice. Toxicol Appl Pharmacol 266(2):289-297
33. Morrison BH, Bauer JA, Lupica JA, Tang Z, Schmidt H, DiDonato JA, Lindner DJ (2007) Effect of inositol hexakisphosphate kinase 2 on transforming growth factor beta-activated kinase 1 and NFkappaB activation. J Biol Chem 282(21):15349-15356 (Pubitemid 47093294)
34. Nie AY, McMillian M, Parker JB, Leone A, Bryant S, Yieh L, Bittner A, Nelson J, Carmen A, Wan J et al (2006) Predictive toxicogenomics approaches reveal underlying molecular mechanisms of nongenotoxic carcinogenicity. Mol Carcinog 45(12):914-933 (Pubitemid 44907382)
35. Palta A, Dhiman P, Cruz SD (2012) ZBTB16-RARalpha variant of acute promyelocytic leukemia with tuberculosis: a case report and review of literature. Korean J Hematol 47(3):229-232
36. Park JY, Shigenaga MK, Ames BN (1996) Induction of cytochrome P4501A1 by 2,3,7,8-tetrachlorodibenzo-p-dioxin or indolo(3,2-b) carbazole is associated with oxidative DNA damage. Proc Natl Acad Sci USA 93(6):2322-2327 (Pubitemid 26104348)
37. Pothof J, Verkaik NS, Van IJcken W, Wiemer EA, Ta VT, Van der Horst GT, Jaspers NG, Van Gent DC, Hoeijmakers JH, Persengiev SP (2009) MicroRNA-mediated gene silencing modulates the UV-induced DNA-damage response. EMBO J 28(14):2090-2099
38. Ramirez-Herrick AM, Mullican SE, Sheehan AM, Conneely OM (2011) Reduced NR4A gene dosage leads to mixed myelodysplastic/myeloproliferative neoplasms in mice. Blood 117(9):2681-2690
39. Rickman DS, Pflueger D, Moss B, VanDoren VE, Chen CX, de la Taille A, Kuefer R, Tewari AK, Setlur SR, Demichelis F et al (2009) SLC45A3-ELK4 is a novel and frequent erythroblast transformation-specific fusion transcript in prostate cancer. Cancer Res 69(7):2734-2738
40. Silva LB, Van der Laan JW (2000) Mechanisms of nongenotoxic carcinogenesis and assessment of the human hazard. Regul Toxicol Pharmacol 32(2):135-143
41. Smyth GK (2005) Limma: linear models for microarray data. In: Gentleman R (ed) Bioinformatics and Computational Biology Solutions using R and Bioconductor. Springer, New York, pp 397-420
42. Storey JD, Tibshirani R (2003) Statistical significance for genome-wide studies. Proc Natl Acad Sci USA 100(16):9440-9445
43. Thomas RS, Bao W, Chu TM, Bessarabova M, Nikolskaya T, Nikolsky Y, Andersen ME, Wolfinger RD (2009) Use of short-term transcriptional profiles to assess the long-term cancer-related safety of environmental and industrial chemicals. Toxicol Sci 112(2):311-321
44. Uehara T, Minowa Y, Morikawa Y, Kondo C, Maruyama T, Kato I, Nakatsu N, Igarashi Y, Ono A, Hayashi H et al (2011) Prediction model of potential hepatocarcinogenicity of rat hepatocarcinogens using a large-scale toxicogenomics database. Toxicol Appl Pharmacol 255(3):297-306
45. VanKreijl CF, McAnulty PA, Beems RB, Vynckier A, van Steeg H, Fransson-Steen R, Alden CL, Forster R, Vander Laan JW, Vandenberghe J (2001) Xpa and Xpa/p53 ± knockout mice: overview of available data. Toxicol Pathol 29:117-127
46. Waters MD, Jackson M, Lea I (2010) Characterizing and predicting carcinogenicity and mode of action using conventional and toxi-cogenomics methods. Mutat Res 705(3):184-200
47. Wolfinger RD, Gibson G, Wolfinger ED, Bennett L, Hamadeh H, Bushel P, Afshari C, Paules RS (2001) Assessing gene significance from cDNA microarray expression data via mixed models. J Comput Biol 8(6):625-637 (Pubitemid 34053500)
48. Zhang Y, Liu C, Peng H, Zhang J, Feng Q (2012) IL1 receptor antagonist gene IL1-RN variable number of tandem repeats polymorphism and cancer risk: a literature review and meta-analysis. PLoS ONE 7(9):e46017
49. Zhou MI, Foy RL, Chitalia VC, Zhao J, Panchenko MV, Wang H, Cohen HT (2005) Jade-1, a candidate renal tumor suppressor that promotes apoptosis. Proc Natl Acad Sci USA 102(31):11035-11040 (Pubitemid 41105988)