Exploiting microRNA and mRNA profiles generated in vitro from carcinogen-exposed primary mouse hepatocytes for predicting in vivo genotoxicity and carcinogenicity

Mutagenesis

Volumn 31, Issue 5, 2016, Pages 603-615

  Rieswijk, Linda ^a,b   Brauers, Karen J J ^a   Coonen, Maarten L J ^a,b   Jennen, Danyel G J ^a,b   Van Breda, Simone G J ^a   Kleinjans, Jos C S ^a,b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

2,3,7,8 TETRACHLORODIBENZO PARA DIOXIN; 4 ACETYLAMINOFLUORENE; 4 CRESIDINE; 7,12 DIMETHYLBENZ[A]ANTHRACENE; 8 QUINOLINOL; AFLATOXIN; AMPICILLIN; BENZO[A]PYRENE; BIS(TRIBUTYLTIN) OXIDE; CARCINOGEN; CISPLATIN; CURCUMIN; CYCLOSPORIN A; DICLOFENAC; DIMETHYLBENZ[A]ANTHRACENE; ESTRADIOL; MESSENGER RNA; MICRORNA; PHENACETIN; PHENOBARBITAL; PHTHALIC ACID BIS(2 ETHYLHEXYL) ESTER; PIRINIXIC ACID; QUERCETIN; RESERPINE; RESORCINOL; TRIBUTYLINOXIDE; UNCLASSIFIED DRUG; PROTEIN; TRANSCRIPTOME;

ADULT; ANIMAL CELL; ARTICLE; CARCINOGENICITY; CONTROLLED STUDY; GENE EXPRESSION; GENOTOXICITY; HUMAN; IN VITRO STUDY; IN VIVO STUDY; LIVER CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; SENSITIVITY AND SPECIFICITY; ANIMAL; DRUG EFFECTS; GENETICS; METABOLISM; MUTAGEN TESTING; PROCEDURES; TOXICOGENETICS;

ANIMALS; CARCINOGENS; HEPATOCYTES; MALE; MICE; MICRORNAS; MUTAGENICITY TESTS; PROTEINS; RNA, MESSENGER; SENSITIVITY AND SPECIFICITY; TOXICOGENETICS; TRANSCRIPTOME;

EID: 84985920580     PISSN: 02678357     EISSN: 14643804     Source Type: Journal    
DOI: 10.1093/mutage/gew027     Document Type: Article

References (86)

1. Kirkland, D., Pfuhler, S., Tweats, D. et al. (2007) How to reduce false positive results when undertaking in vitro genotoxicity testing and thus avoid unnecessary follow-up animal tests: report of an ECVAM Workshop. Mutat. Res., 628, 31-55.
2. Kirkland, D., Kasper, P., Müller, L., Corvi, R., and Speit, G. (2008) Recommended lists of genotoxic and non-genotoxic chemicals for assessment of the performance of new or improved genotoxicity tests: a follow-up to an ECVAM workshop. Mutat. Res., 653, 99-108.
3. Ennever, F. K., and Lave, L. B. (2003) Implications of the lack of accuracy of the lifetime rodent bioassay for predicting human carcinogenicity. Regul. Toxicol. Pharmacol., 38, 52-57.
4. de Vries, A., van Steeg, H., and Opperhuizen, A. (2004) Transgenic mice as alternatives in carcinogenicity testing: current status. RIVM report 340700001. http://rivm.openrepository.com/rivm/bitstream/10029/8911/1/340700001.pdf (accessed July 28, 2015).
5. Piersma, A. H., Ezendam, J., Luijten, M., Muller, J. J., Rorije, E., van der Ven, L. T., and van Benthem, J. (2014) A critical appraisal of the process of regulatory implementation of novel in vivo and in vitro methods for chemical hazard and risk assessment. Crit. Rev. Toxicol., 44, 876-894.
6. Fielden, M. R., Adai, A., Dunn, R.T., II 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, 54-74.
7. Ellinger-Ziegelbauer, H., Stuart, B., Wahle, B., Bomann, W., and Ahr, H. J. (2005) Comparison of the expression profiles induced by genotoxic and nongenotoxic carcinogens in rat liver. Mutat. Res., 575, 61-84.
8. van Delft, J. H., van Agen, E., van Breda, S. G., Herwijnen, M. H., Staal, Y. C., and Kleinjans, J. C. (2004) Discrimination of genotoxic from non-genotoxic carcinogens by gene expression profiling. Carcinogenesis, 25, 1265-1276.
9. Magkoufopoulou, C., Claessen, S. M., Tsamou, M., Jennen, D. G., Kleinjans, J. C., and van Delft, J. H. (2012) A transcriptomics-based in vitro assay for predicting chemical genotoxicity in vivo. Carcinogenesis, 33, 1421-1429.
10. Van den Hof, W. F., Coonen, M. L., van Herwijnen, M., Brauers, K., Wodzig, W. K., van Delft, J. H., and Kleinjans, J. C. (2014) Classification of hepatotoxicants using HepG2 cells: a proof of principle study. Chem. Res. Toxicol., 27, 433-442.
11. Melis, J. P., Derks, K. W., Pronk, T. E. et al. (2014) In vivo murine hepatic microRNA and mRNA expression signatures predicting the (non-)genotoxic carcinogenic potential of chemicals. Arch. Toxicol., 88, 1023-1034.
12. Mathijs, K., Brauers, K. J., Jennen, D. G., Boorsma, A., van Herwijnen, M. H., Gottschalk, R. W., Kleinjans, J. C., and van Delft, J. H. (2009) Discrimination for genotoxic and nongenotoxic carcinogens by gene expression profiling in primary mouse hepatocytes improves with exposure time. Toxicol. Sci., 112, 374-384.
13. Doktorova, T Y., Yildirimman, R., Ceelen, L. et al. (2014) Testing chemical carcinogenicity by using a transcriptomics HepaRG-based model? EXCLI J. 13 623-637.
14. Herwig R., Gmuender, H., Corvi, R. et al. (2015) Inter-laboratory study of human in vitro toxicogenomics-based tests as alternative methods for evaluating chemical carcinogenicity: a bioinformatics perspective. Arch Toxicol. 2015 Nov 2. [Epub ahead of print].
15. Ambros, V. (2004) The functions of animal microRNAs. Nature, 431, 350-355.
16. Bartel, D. P. (2004) MicroRNAs: genomics, biogenesis, mechanism, and function. Cell, 116, 281-297.
17. Calin, G. A., and Croce, C. M. (2006) MicroRNA signatures in human cancers. Nat. Rev. Cancer, 6, 857-866.
18. Esquela-Kerscher, A., and Slack, F. J. (2006) Oncomirs-microRNAs with a role in cancer. Nat. Rev. Cancer, 6, 259-269.
19. Giordano, S., and Columbano, A (2013) MicroRNAs: new tools for diagnosis, prognosis, and therapy in hepatocellular carcinoma? Hepatology (Baltimore, Md) 57 840-847.
20. Sun, J., Lu, H., Wang, X., and Jin, H. (2013) MicroRNAs in hepatocellular carcinoma: regulation, function, and clinical implications. ScientificWorld-Journal, 2013, 924206.
21. Izzotti, A., and Pulliero, A. (2014) The effects of environmental chemical carcinogens on the microRNA machinery. Int. J. Hyg. Environ. Health, 217, 601-627.
22. Rieswijk, L., Brauers, K. J., Coonen, M. L., van Breda, S. G., Jennen, D. G., and Kleinjans, J. C. (2015) Evaluating microRNA profiles reveals discriminative responses following genotoxic or non-genotoxic carcinogen exposure in primary mouse hepatocytes. Mutagenesis, 30, 771-784.
23. Koufaris, C., Wright, J., Currie, R. A., and Gooderham, N. J. (2012) Hepatic microRNA profiles offer predictive and mechanistic insights after exposure to genotoxic and epigenetic hepatocarcinogens. Toxicol. Sci., 128, 532-543.
24. Ames, B. N., Lee, F. D., and Durston, W. E. (1973) An improved bacterial test system for the detection and classification of mutagens and carcinogens. Proc. Natl. Acad. Sci. U. S. A., 70, 782-786.
25. Kirkland, D., Reeve, L., Gatehouse, D., and Vanparys, P. (2011) A core in vitro genotoxicity battery comprising the Ames test plus the in vitro micronucleus test is sufficient to detect rodent carcinogens and in vivo genotoxins. Mutat. Res., 721, 27-73.
26. Mitchell, A. D., Auletta, A. E., Clive, D., Kirby, P. E., Moore, M. M., and Myhr, B. C. (1997) The L5178Y/tk+/? mouse lymphoma specific gene and chromosomal mutation assay a phase III report of the U.S. Environmental Protection Agency Gene-Tox Program. Mutat. Res., 394, 177-303.
27. Corvi, R., Albertini, S., Hartung, T., Hoffmann, S., Maurici, D., Pfuhler, S., van Benthem, J., and Vanparys, P. (2008) ECVAM retrospective validation of in vitro micronucleus test (MNT). Mutagenesis, 23, 271-283.
28. Matsushima, T., Hayashi, M., Matsuoka, A. et al. (1999) Validation study of the in vitro micronucleus test in a Chinese hamster lung cell line (CHL/IU). Mutagenesis, 14, 569-580.
29. Khynriam, D., and Prasad, S. B. (2003) Cisplatin-induced genotoxic effects and endogenous glutathione levels in mice bearing ascites Dalton's lymphoma. Mutat. Res., 526, 9-18.
30. Valentin-Severin, I., Le Hegarat, L., Lhuguenot, J. C., Le Bon, A. M., and Chagnon, M. C. (2003) Use of HepG2 cell line for direct or indirect mutagens screening: comparative investigation between comet and micronucleus assays. Mutat. Res., 536, 79-90.
31. Müller-Tegethoff, K., Kasper, P., and Müller, L. (1995) Evaluation studies on the in vitro rat hepatocyte micronucleus assay. Mutat. Res., 335, 293-307.
32. Miller, B., Pötter-Locher, F., Seelbach, A., Stopper, H., Utesch, D., and Madle, S. (1998) Evaluation of the in vitro micronucleus test as an alternative to the in vitro chromosomal aberration assay: position of the GUM Working Group on the in vitro micronucleus test. Gesellschaft für Umwelt-Mutations-forschung. Mutat. Res., 410, 81-116.
33. Cahill, P. A., Knight, A. W., Billinton, N., Barker, M. G., Walsh, L., Keenan, P. O., Williams, C. V., Tweats, D. J., and Walmsley, R. M. (2004) The Green-Screen genotoxicity assay: a screening validation programme. Mutagenesis, 19, 105-119.
34. Kirkland, D., and Speit, G. (2008) Evaluation of the ability of a battery of three in vitro genotoxicity tests to discriminate rodent carcinogens and non-carcinogens III. Appropriate follow-up testing in vivo. Mutat. Res., 654, 114-132.
35. Brambilla, G., and Martelli, A. (2009) Genotoxicity and carcinogenicity studies of analgesics, anti-inflammatory drugs and antipyretics. Pharmacol. Res., 60, 1-17.
36. Snyder, R. D., and Green, J. W. (2001) A review of the genotoxicity of marketed pharmaceuticals. Mutat. Res., 488, 151-169.
37. Westerink, W. M., Stevenson, J. C., Lauwers, A., Griffioen, G., Horbach, G. J., and Schoonen, W. G. (2009) Evaluation of the Vitotox and RadarScreen assays for the rapid assessment of genotoxicity in the early research phase of drug development. Mutat. Res., 676, 113-130.
38. Brambilla, G., and Martelli, A. (2009) Update on genotoxicity and carcinogenicity testing of 472 marketed pharmaceuticals. Mutat. Res., 681, 209-229.
39. Cao, J., Jiang, L. P., Liu, Y., Yang, G., Yao, X. F., and Zhong, L. F. (2007) Curcumin-induced genotoxicity and antigenotoxicity in HepG2 cells. Toxicon, 49, 1219-1222.
40. Harvey, J. S., Howe, J. R., Lynch, A. M., and Rees, R. W. (2005) The results of five coded compounds: genistein, metaproterenol, rotenone, p-Anisidine and resorcinol tested in the pH 6.7 Syrian hamster embryo cell morphological transformation assay. Mutagenesis, 20, 51-56.
41. Shelby, M. D., and Witt, K. L. (1995) Comparison of results from mouse bone marrow chromosome aberration and micronucleus tests. Environ. Mol. Mutagen., 25, 302-313.
42. Blakey, D., Galloway, S. M., Kirkland, D. J., and MacGregor, J. T. (2008) Regulatory aspects of genotoxicity testing: from hazard identification to risk assessment. Mutat. Res., 657, 84-90.
43. Wahnschaffe, U., Bitsch, A., Kielhorn, J., and Mangelsdorf, I. (2005) Mutagenicity testing with transgenic mice. Part I: comparison with the mouse bone marrow micronucleus test. J. Carcinog., 4, 3.
44. Lambert, I. B., Singer, T. M., Boucher, S. E., and Douglas, G. R. (2005) Detailed review of transgenic rodent mutation assays. Mutat. Res., 590, 1-280.
45. Davis, A., Barale, R., Brun, G. et al. (1987) Evaluation of the genetic and embryotoxic effects of bis(tri-n-butyltin)oxide (TBTO), a broad-spectrum pesticide, in multiple in vivo and in vitro short-Term tests. Mutat. Res., 188, 65-95.
46. Tsamou, M., Jennen, D. G., Claessen, S. M., Magkoufopoulou, C., Kleinjans, J. C., and van Delft, J. H. (2012) Performance of in vitro ?H2AX assay in HepG2 cells to predict in vivo genotoxicity. Mutagenesis, 27, 645-652.
47. International Agency for Research on Cancer (IARC) (2014) IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. http://monographs.iarc.fr/ENG/Classification/ClassificationsGroupOrder.pdf (accessed on November 14, 2014).
48. US Department of Health and Human Services, Public Health Service, National Toxicology Program (NTP) (2014) Report on Carcinogens. http://ntp.niehs.nih.gov/pubhealth/roc/roc13/index.html (accessed on November 14, 2014).
49. Mills, A., and Foureman, G. L. (1998) US EPA's IRIS pilot program: establishing IRIS as a centralized, peer-reviewed data base with agency consensus. Integrated Risk Information System. Toxicology, 127, 85-95.
50. U.S. National Library of Medicine (2014) Toxnet Toxicological Data Network (CCRIS, HSDB, ChemIDplus and Genetox). http://toxnet.nlm.nih. gov/(accessed on November 14, 2014).
51. Reddy, J. K., Rao, M. S., Azarnoff, D. L., and Sell, S. (1979) Mitogenic and carcinogenic effects of a hypolipidemic peroxisome proliferator, [4-chloro-6-(2, 3-xylidino)-2-pyrimidinylthio]acetic acid (Wy-14, 643), in rat and mouse liver. Cancer Res., 39, 152-161.
52. Mathijs, K., Kienhuis, A. S., Brauers, K. J., Jennen, D. G., Lahoz, A., Kleinjans, J. C., and van Delft, J. H. (2009) Assessing the metabolic competence of sandwich-cultured mouse primary hepatocytes. Drug Metab. Dispos., 37, 1305-1311.
53. Mathijs, K., Brauers, K. J., Jennen, D. G., Lizarraga, D., Kleinjans, J. C., and van Delft, J. H. (2010) Gene expression profiling in primary mouse hepatocytes discriminates true from false-positive genotoxic compounds. Mutagenesis, 25, 561-568.
54. Rieswijk, L., Lizarraga, D., Brauers, K. J., Kleinjans, J. C., and van Delft, J. H. (2014) Characterisation of cisplatin-induced transcriptomics responses in primary mouse hepatocytes, HepG2 cells and mouse embryonic stem cells shows conservation of regulating transcription factor networks. Mutagenesis, 29, 17-26.
55. Mosmann, T. (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J. Immunol. Methods, 65, 55-63.
56. Griffiths-Jones, S., Saini, H. K., van Dongen, S., and Enright, A. J. (2008) miRBase: tools for microRNA genomics. Nucleic Acids Res., 36, D154-D158.
57. Edgar, R., Domrachev, M., and Lash, A. E. (2002) Gene Expression Omnibus: NCBI gene expression and hybridization array data repository. Nucleic Acids Res., 30, 207-210.
58. Eijssen, L. M., Jaillard, M., Adriaens, M. E., Gaj, S., de Groot, P. J., Müller, M., and Evelo, C. T. (2013) User-friendly solutions for microarray quality control and pre-processing on ArrayAnalysis.org. Nucleic Acids Res., 41, W71-W76.
59. Chen, J. J., Hsueh, H. M., Delongchamp, R. R., Lin, C. J., and Tsai, C. A. (2007) Reproducibility of microarray data: a further analysis of microarray quality control (MAQC) data. BMC Bioinformatics, 8, 412.
60. Bourgon, R., Gentleman, R., and Huber, W. (2010) Independent filtering increases detection power for high-Throughput experiments. Proc. Natl Acad. Sci. U. S. A., 107, 9546-9551.
61. Reich, M., Liefeld, T., Gould, J., Lerner, J., Tamayo, P., and Mesirov, J. P. (2006) GenePattern 2.0. Nat. Genet., 38, 500-501.
62. Rebhan, M., Chalifa-Caspi, V., Prilusky, J., and Lancet, D. (1997) GeneCards: integrating information about genes, proteins and diseases. Trends Genet., 13, 163.
63. Jennen, D., Polman, J., Bessem, M., Coonen, M., van Delft, J., and Kleinjans, J. (2014) Drug-induced liver injury classification model based on in vitro human transcriptomics and in vivo rat clinical chemistry data. Syst Biomed., 2, 63-70.
64. Kotsiantis, S., Kanellopoulos, D., and Pintelas, P. (2006) Handling imbalanced datasets: A review. GESTS Int. Trans. Comput. Sci. Eng., 30, 25-36.
65. Chawla, N. V., Bowyer, K. W., Hall, L. O., and Kegelmeyer, W. P. (2002) SMOTE: synthetic minority over-sampling technique. J Artif. Intell. Res., 16, 321-357.
66. Ishii, H., Mimori, K., Inoue, H., et al. (2006) Fhit modulates the DNA damage checkpoint response. Cancer Res., 66, 11287-11292.
67. Okumura, H., Ishii, H., Pichiorri, F., Croce, C. M., Mori, M., and Huebner, K. (2009) Fragile gene product, Fhit, in oxidative and replicative stress responses. Cancer Sci., 100, 1145-1150.
68. Karras, J. R., Paisie, C. A., and Huebner, K. (2014) Replicative stress and the FHIT gene: roles in tumor suppression, genome stability and prevention of carcinogenesis. Cancers (Basel)., 6, 1208-1219.
69. Uehara, T., Hirode, M., Ono, A., Kiyosawa, N., Omura, K., Shimizu, T., Mizukawa, Y., Miyagishima, T., Nagao, T., and Urushidani, T. (2008) A toxicogenomics approach for early assessment of potential non-genotoxic hepatocarcinogenicity of chemicals in rats. Toxicology, 250, 15-26.
70. Momand, J., Wu, H. H., and Dasgupta, G. (2000) MDM2-master regulator of the p53 tumor suppressor protein. Gene, 242, 15-29.
71. Cisternas, F. A., Vincent, J. B., Scherer, S. W., and Ray, P. N. (2003) Cloning and characterization of human CADPS and CADPS2, new members of the Ca2+-dependent activator for secretion protein family. Genomics, 81, 279-291.
72. Gonzalez, F. J. (2002) The peroxisome proliferator-Activated receptor alpha (PPARalpha): role in hepatocarcinogenesis. Mol. Cell. Endocrinol., 193, 71-79.
73. Szalowska, E., Tesfay, H. A., van Hijum, S. A., and Kersten, S. (2014) Transcriptomic signatures of peroxisome proliferator-Activated receptor alpha (PPARalpha) in different mouse liver models identify novel aspects of its biology. BMC Genomics, 15, 1106.
74. Tamura, K., Ono, A., Miyagishima, T., Nagao, T., and Urushidani, T. (2006) Profiling of gene expression in rat liver and rat primary cultured hepatocytes treated with peroxisome proliferators. J. Toxicol. Sci., 31, 471-490.
75. Sokol, J. P., and Schiemann, W. P. (2004) Cystatin C antagonizes transforming growth factor beta signaling in normal and cancer cells. Mol. Cancer Res., 2, 183-195.
76. Sempere, L. F., Sokol, N. S., Dubrovsky, E. B., Berger, E. M., and Ambros, V. (2003) Temporal regulation of microRNA expression in Drosophila melanogaster mediated by hormonal signals and broad-complex gene activity. Dev. Biol., 259, 9-18.
77. Jones, B., Roberts, P. J., Faubion, W. A., Kominami, E., and Gores, G. J. (1998) Cystatin A expression reduces bile salt-induced apoptosis in a rat hepatoma cell line. Am. J. Physiol., 275, G723-G730.
78. Kos, J., Stabuc, B., Cimerman, N., and Brünner, N. (1998) Serum cystatin C, a new marker of glomerular filtration rate, is increased during malignant progression. Clin. Chem., 44, 2556-2557.
79. Agola, J. O., Jim, P. A., Ward, H. H., Basuray, S., and Wandinger-Ness, A. (2011) Rab GTPases as regulators of endocytosis, targets of disease and therapeutic opportunities. Clin. Genet., 80, 305-318.
80. Sui, Y., Zheng, X., and Zhao, D. (2015) Rab31 promoted hepatocellular carcinoma (HCC) progression via inhibition of cell apoptosis induced by PI3K/AKT/Bcl-2/BAX pathway. Tumour Biol., 36, 8661-8670.
81. Nakayama, K. I., and Nakayama, K. (2005) Regulation of the cell cycle by SCF-Type ubiquitin ligases. Semin. Cell Dev. Biol., 16, 323-333.
82. Wang, Z., Liu, P., Inuzuka, H., and Wei, W. (2014) Roles of F-box proteins in cancer. Nat. Rev. Cancer, 14, 233-247.
83. Tian, X., Dai, S., Sun, J., Jin, G., Jiang, S., Meng, F., Li, Y., Wu, D., and Jiang, Y. (2015) F-box Protein FBXO22 Mediates Polyubiquitination and Degradation of KLF4 to Promote Hepatocellular Carcinoma Progression. Oncotarget, 6, 22767-22775.
84. Hynds, R. E., and Giangreco, A. (2013) Concise review: the relevance of human stem cell-derived organoid models for epithelial translational medicine. Stem Cells, 31, 417-422.
85. Davidson, M. D., Ware, B. R., and Khetani, S. R. (2015) Stem cell-derived liver cells for drug testing and disease modeling. Discov. Med., 19, 349-358.
86. Soldatow, V. Y., LeCluyse, E. L., Griffith, L. G., and Rusyn, I. (2013) In vitro models for liver toxicity testing. Toxicol. Res., 2, 23-39.