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Cell-based in vitro models in environmental toxicology: a review

Michael Poteser
  • Department of Environmental Hygiene and Environmental Medicine, Center for Public Health, Medical University Vienna, Vienna 1190, Austria
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  • De Gruyter OnlineGoogle Scholar
Published Online: 2017-10-12 | DOI: https://doi.org/10.1515/bimo-2017-0002

Abstract

An analysis of biological effects induced by environmental toxins and exposure-related evaluation of potential risks for health and environment represent central tasks in classical biomonitoring. While epidemiological data and population surveys are clearly the methodological frontline of this scientific field, cellbased in vitro assays provide information on toxin-affected cellular pathways and mechanisms, and are important sources for the identification of relevant biomarkers. This review provides an overview on currently available in vitro methods based on cultured cells, as well as some limitations and considerations that are of specific interest in the context of environmental toxicology. Today, a large number of different endpoints can be determined to pinpoint basal and specific toxicological cellular effects. Technological progress and increasingly refined protocols are extending the possibilities of cell-based in vitro assays in environmental toxicology and promoting their increasingly important role in biomonitoring.

Keywords : in vitro assay; cell culture; environmental toxicology; basal endpoints; specific endpoints; cell viability; genotoxicity; carcinogenicity; cellular stress factors; biomonitoring

References

  • [1] Moshammer H., Why biomonitoring?, 2014, Biomonitoring, 1, 46-49.Google Scholar

  • [2] Kienhuis A.S, van de Poll M.C.G, Wortelboer H, van Herwijnen M, Gottschalk R, Dejong, C.H.C., Boorsma A, Paules R.S. Kleinjans J.C.S. et al., Parallelogram approach using rat-human in vitro and rat in vivo toxicogenomics predicts acetaminopheninduced hepatotoxicity in humans, Toxicol. Sci., 2009, 2, 544-552.Google Scholar

  • [3] Weisser K., Stübler S., Matheis W., Huisinga W., Towards toxicokinetic modelling of aluminium exposure from adjuvants in medicinal products, Regul Toxicol Pharmacol, 2017, (in press), DOI: 10.1016/j.yrtph.2017.02.018.CrossrefGoogle Scholar

  • [4] Yoshikado T., Kazuya M., Kusuhara H., Furihata K., Sugiyama Y., Quantitative analyses of the influence of parameters governing rate-determining process of hepatic elimination of drugs on the magnitudes of drug-drug interactions via hepatic OATPs and CYP3A using physiologically-based pharmacokinetic models, J. Pharm. Sci., 2017, (in press), DOI: 10.1016/j.xphs.2017.05.001.CrossrefGoogle Scholar

  • [5] Andersen M.E., Physiological modelling of organic compounds, Ann. Occup. Hyg., 1991, 3, 309-321.Google Scholar

  • [6] Miller C., George S., Niklason L., Developing a tissueengineered model of the human bronchiole, J. Tissue Eng. Regen. Med., 2010, 8, 619-627.Google Scholar

  • [7] Hoppensack A., Kazanecki C. C., Colter D., Gosiewska A., Schanz J., Walles H., Schenke-Layland K., A human in vitro model that mimics the renal proximal tubule, Tissue Eng., Part C, Methods, 2014, 7, 599-609.CrossrefGoogle Scholar

  • [8] Eilstein J., Léreaux G., Arbey E., Daronnat E., Wilkinson S., Duchè D.l., Xenobiotic metabolizing enzymes in human skin and SkinEthic reconstructed human skin models, Exp. Dermatol., 2015, 7, 547-549.Google Scholar

  • [9] Subramanian B., Rudym D., Cannizzaro C., Perrone R., Zhou J., Kaplan D. L., Tissue-engineered three-dimensional in vitro models for normal and diseased kidney, Tissue Eng., Part A, 2010, 9, 2821-2831.CrossrefGoogle Scholar

  • [10] Oesch F., Glatt H., Utesch D., Metabolic perspectives on in vitro toxicity tests, Xenobiotica, 1988, 1, 35-44.Google Scholar

  • [11] OECD, OECD Guidelines for the Testing of Chemicals, 2017, http://www.oecd.org/chemicalsafety/testing/oecdguidelinesforthetestingofchemicals.htm.Google Scholar

  • [12] Aufderheide M., Direct exposure methods for testing native atmosphere, Exp. Toxicol. Pathol., 2005, 57 Suppl. 1, 213-226.Google Scholar

  • [13] Aufderheide M., Gressmann H., A modified Ames assay reveals the mutagenicity of native cigarette mainstream smoke and its gas vapour phase, Exp. Toxicol. Pathol., 2007, 6, 383-392.CrossrefGoogle Scholar

  • [14] Neuman M.G., Cohen L.B., Steenkamp V., Pyrrolizidine alkaloids enhance alcohol-induced hepatocytotoxicity in vitro in normal human hepatocytes, Eur Rev Med Pharmacol Sci., 2017, 21: 53-68.Google Scholar

  • [15] Pellicciari C., Bottone M.G., Biggiogera M., Restructuring and extrusion of nuclear ribonucleoproteins (RNPs) during apoptosis, Gen Physiol Biophys., 1999, 18 Suppl 1: 50-2Google Scholar

  • [16] Gutierrez, E.R., Kamens, R.M., Tolocka, M., Sexton, K., Jaspers, I., A comparison of three dispersion media on the physiochamical and toxicological behaviour of TiO2 and NiO nanoparticles. Chem Biol Interact, 2015, 236: 74-81Google Scholar

  • [17] Papadimitriou J.M., van Bruggen I., Quantitative investigations of apoptosis of murine mononuclear phagocytes during mild hyperthermia, Exp Mol Pathol. 1993, 59(1):1-12.Google Scholar

  • [18] Trask O.J. Jr., Moore A., LeCluyse E.L., A micropatterned hepatocyte coculture model for assessment of liver toxicity using high-content imaging analysis. Assay Drug Dev Technol., 2014, 12: 16-27.Google Scholar

  • [19] Fricker S.P., The application of sulforhodamine B as a colorimetric endpoint in a cytotoxicity assay, Toxicol. In vitro, 1994, 4, 821-822.Google Scholar

  • [20] Orellana E. A., Kasinski A.L., Sulforhodamine B (SRB) Assay in Cell Culture to Investigate Cell Proliferation, Bio Protoc, 2016, 6 (21), DOI: 10.21769/BioProtoc.1984.CrossrefGoogle Scholar

  • [21] Skehan P., Storeng R., Scudiero D., Monks A., McMahon J., Vistica, D., Warren, J. T., Bokesch, H., Kenney, S., Boyd, M. R., New colorimetric cytotoxicity assay for anticancer-drug screening, J. Natl. Cancer Inst., 1990, 13, 1107-1112.Google Scholar

  • [22] Vichai, V., Kirtikara, K., Sulforhodamine B colorimetric assay for cytotoxicity screening, Nat. Protoc., 2006, 3, 1112-1116.CrossrefGoogle Scholar

  • [23] Soto A. M., Sonnenschein C., Chung K.L., Fernandez M.F., Olea, N., Serrano F.O., The E-SCREEN assay as a tool to identify estrogens: an update on estrogenic environmental pollutants, Environ Health Perspect.,1995, 103 Suppl. 7, 113-122.Google Scholar

  • [24] Bereiter-Hahn J., Münnich A., Woiteneck P., Dependence of energy metabolism on the density of cells in culture, Cell Struct. Funct., 1998, 2, 85-93.CrossrefGoogle Scholar

  • [25] Tario Jr, J. D., Humphrey K, Bantly A. D., Muirhead K. A., Moore, J. S., Wallace, P. K., Optimized staining and proliferation modeling methods for cell division monitoring using cell tracking dyes, J. Vis. Exp., 2012, 13 (70), e4287.Google Scholar

  • [26] Oostendorp R. A, Audet J, Miller C., Eaves C. J., Cell division tracking and expansion of hematopoietic long-term repopulating cell, Leukemia, 1999, 4, 499-501.CrossrefGoogle Scholar

  • [27] Goodpasture C., Bloom S. E., Visualization of nucleolar organizer regions in mammalian chromosomes using silver staining, Chromosoma, 1975, 1, 37-50.Google Scholar

  • [28] Viktorova T. V., Khusnutdinova E. K., Viktorov V. V., Liapunova N. A., Rafikov K. S., Analysis of chromosome aberrations and nucleolar organizer regions of chromosomes in workers producing pyromellitic dianhydride: the possibility of the adaptive role of Ag-NOR variants, Genetika, 1994, 7, 992-998.Google Scholar

  • [29] Li Q., Hacker G. W., Danscher G., Sonnleitner-Wittauer U., Grimelius L, Argyrophilic nucleolar organizer regions: A revised version of the Ag-NOR-staining technique, Histochem. Cell Biol., 1995, 2, 145-150.CrossrefGoogle Scholar

  • [30] Perani A., Gloria B., Wang D., Buffier A., Berteau O., Esteban, F., Smyth F.E., Scott A.M., Evaluation of an online biomass probe to monitor cell growth and cell death, BMC Proceedings, 2011 ,5 Suppl. 8, P16.Google Scholar

  • [31] Berridge M. V., Herst P. M., Tan A. S., Tetrazolium dyes as tools in cell biology: new insights into their cellular reduction, Biotechnol. Annu. Rev., 2005, 11, 127-152.CrossrefGoogle Scholar

  • [32] Berridge M. V., Tan A. S., Characterization of the cellular reduction of 3-(4,5- dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide (MTT): subcellular localization, substrate dependence, and involvement of mitochondrial electron transport in MTT reduction, Arch. Biochem. Biophys., 1993, 2, 474-482.CrossrefGoogle Scholar

  • [33] Levitz S. M., Diamond R. D., A rapid colorimetric assay of fungal viability with the tetrazolium salt MTT, J. Infect. Dis., 1985, 5, 938-945.CrossrefGoogle Scholar

  • [34] Roehm N. W., Rodgers G. H., Hatfield S. M, Glasebrook, A. L., An improved colorimetric assay for cell proliferation and viability utilizing the tetrazolium salt XTT, J. Immunol. Methods, 1991, 2, 257-265.CrossrefGoogle Scholar

  • [35] Galow A., Gimsa J., WST-assay data reveal a pH dependence of the mitochondrial succinate reductase in osteoblast-like cells, Data Brief, 2017, 12, 442-446.Google Scholar

  • [36] Ishiyama M., Tominaga H., Shiga M., Sasamoto K., Ohkura Y., Ueno K., A combined assay of cell viability and in vitro cytotoxicity with a highly water-soluble tetrazolium salt, neutral red and crystal violet, Biol. Pharm. Bull., 1996, 11, 1518-1520.CrossrefGoogle Scholar

  • [37] Semisch A., Hartwig A., Copper ions interfere with the reduction of the water-soluble tetrazolium salt-8, Chem. Res. Toxicol., 2014, 2, 169-171.Google Scholar

  • [38] Malich G., Markovic B., Winder C., The sensitivity and specificity of the MTS tetrazolium assay for detecting the in vitro cytotoxicity of 20 chemicals using human cell lines, Toxicology, 1997, 3, 179-192.CrossrefGoogle Scholar

  • [39] Goodwin C.J., Holt S.J., Downes S, Marshall, N. J., Microculture tetrazolium assays: a comparison between two new tetrazolium salts, XTT and MTS, J. Immunol. Methods, 1995, 1, 95-103.Google Scholar

  • [40] Hakura A., Suzuki S., Sawada S., Motooka S., Satoh T., An improvement of the Ames test using a modified human liver S9 preparation, J. Pharmacol. Toxicol. Methods, 2001, 3, 169-172.CrossrefGoogle Scholar

  • [41] Madle E., Tiedemann G., Madle S., Ott A., Kaufmann G., Comparison of S9 mix and hepatocytes as external metabolizing systems in mammalian cell cultures: cytogenetic effects of 7,12-dimethylbenzanthracene and aflatoxin B1, Environ. Mutagen., 1986, 3, 423-437.Google Scholar

  • [42] De Deken R. H., The Crabtree effect: a regulatory system in yeast, J. Gen. Microbiol., 1966, 2, 149-156.CrossrefGoogle Scholar

  • [43] Clerici E., Ciccarone P., Crabtree effect and the anaerobic glycolysis of the regenerating rat liver, Nature, 1965, 998, 762-763.Google Scholar

  • [44] Marroquin L.D., Hynes J., Dykens J.A., Jamieson J.D., Will Y., Circumventing the Crabtree effect: replacing media glucose with galactose increases susceptibility of HepG2 cells to mitochondrial toxicants, Toxicol. Sci., 2007, 2, 539-547.Google Scholar

  • [45] Mot A.I., Liddell J.R., White A.R., Crouch, P.J., Circumventing the Crabtree Effect: A method to induce lactate consumption and increase oxidative phosphorylation in cell culture, Int. J. Biochem. Cell Biol., 2016, 79, 128-138.Google Scholar

  • [46] Kim J., Dang C. V., Cancer’s molecular sweet tooth and the Warburg effect, Cancer Res., 2006, 18, 8927-8930.CrossrefGoogle Scholar

  • [47] Hugo-Wissemann D., Anundi I., Lauchart W., Viebahn R., de Groot H., Differences in glycolytic capacity and hypoxia tolerance between hepatoma cells and hepatocytes, Hepatology, 1991, 2, 297-303.CrossrefGoogle Scholar

  • [48] Kroemer G., Dallaporta B., Resche-Rigon M., The mitochondrial death/life regulator in apoptosis and necrosis, Annu. Rev. Physiol., 1998, 60, 619-642.CrossrefGoogle Scholar

  • [49] Pohl R. J., Fouts J. R., A rapid method for assaying the metabolism of 7-ethoxyresorufin by microsomal subcellular fractions, Anal. Biochem., 1980, 1, 150-155.Google Scholar

  • [50] Vehniäinen E., Schultz E., Lehtivuori H., Ihalainen J. A., Oikari A. O. J., More accuracy to the EROD measurements-the resorufin fluorescence differs between species and individuals, Aquat. Toxicol., 2012, 116-117, 102-108.Google Scholar

  • [51] Peng Y., Wu H., Zhang X., Zhang F., Qi H., Zhong Y., Wang Y., Sang H., Wang G., Sun J., A comprehensive assay for nine major cytochrome P450 enzymes activities with 16 probe reactions on human liver microsomes by a single LC/MS/MS run to support reliable in vitro inhibitory drug-drug interaction evaluation, Xenobiotica, 2015, 11, 961-977.Google Scholar

  • [52] Damkier P., Brøsen K., Quinidine as a probe for CYP3A4 activity: intrasubject variability and lack of correlation with probe-based assays for CYP1A2, CYP2C9, CYP2C19, and CYP2D6, Clin. Pharmacol. Ther., 2000, 2, 199-209.CrossrefGoogle Scholar

  • [53] Lammers L.A., Achterbergh R., Pistorius M.C.M., Bijleveld Y., de Vries E. M., Boelen A., Klümpen, H., Romijn J.A., Mathôlt R.A.A., Quantitative Method for Simultaneous Analysis of a 5-Probe Cocktail for Cytochrome P450 Enzymes, Ther. Drug Monit., 2016, 6, 761-768.Google Scholar

  • [54] Strehler B.L., Bioluminescence assay: principles and practice, Methods Biochem. Anal., 1968, 16, 99-181.Google Scholar

  • [55] Van Dyke K., Stitzel R., McClellan T., Szustkiewicz C., An automated procedure for the sensitive and specific determination of ATP, Clin. Chem., 1969, 1, 3-14.Google Scholar

  • [56] Julien O., Wells J.A., Caspases and their substrates, Cell Death Differ., 2017, 24, 1380-1389.CrossrefGoogle Scholar

  • [57] Boucher D., Duclos C., Denault J., General in vitro caspase assay procedures, Methods Mol. Biol., 2014, 1133, 3-39.CrossrefGoogle Scholar

  • [58] Payne A.M., Zorman J., Horton M., Dubey S., ter Meulen J., Vora K. A., Caspase activation as a versatile assay platform for detection of cytotoxic bacterial toxins, J. Clin. Microbiol., 2013, 9, 2970-2976.CrossrefGoogle Scholar

  • [59] Jones J., Heim R., Hare E., Stack J., Pollok B. A., Development and application of a GFP-FRET intracellular caspase assay for drug screening, J. Biomol. Screen., 5, 2000, 307-318.Google Scholar

  • [60] Hug H., Los M., Hirt W., Debatin K.M., Rhodamine 110-linked amino acids and peptides as substrates to measure caspase activity upon apoptosis induction in intact cells, Biochemistry, 1999, 42, 13906-13911.Google Scholar

  • [61] Wang Z., Liao J., Diwu Z., N-DEVD-N’-morpholinecarbonylrhodamine 110: novel caspase-3 fluorogenic substrates for cell-based apoptosis assay, Bioorg. Med. Chem. Lett., 2005, 9, 2335-2338.Google Scholar

  • [62] Vermes I., Haanen C., Steffens-Nakken H., Reutelingsperger C., A novel assay for apoptosis. Flow cytometric detection of phosphatidylserine expression on early apoptotic cells using fluorescein labelled Annexin V, J. Immunol. Methods, 1995, 1, 39-51.Google Scholar

  • [63] Crowley L.C., Marfell B.J, Scott A.P., Waterhouse N.J., Quantitation of Apoptosis and Necrosis by Annexin V Binding, Propidium Iodide Uptake, and Flow Cytometry, Cold Spring Harb. Protoc., 2016, 11, pdb.prot087288.Google Scholar

  • [64] Repetto G., del Peso A., Zurita, J.L., Neutral red uptake assay for the estimation of cell viability/cytotoxicity, Nat. Protoc., 2008, 7, 1125-1131.CrossrefGoogle Scholar

  • [65] Lévesque A., Paquet A., Pagé M., Measurement of tumor necrosis factor activity by flow cytometry, Cytometry, 1995, 2, 181-184.CrossrefGoogle Scholar

  • [66] Hed J., Dahlgren C., Rundquist I., A simple fluorescence technique to stain the plasma membrane of human neutrophils, Histochemistry, 1983, 1, 105-110.Google Scholar

  • [67] Belinsky S.A., Popp J.A, Kauffman F.C., Thurman R.G., Trypan blue uptake as a new method to investigate hepatotoxicity in periportal and pericentral regions of the liver lobule: studies with allyl alcohol in the perfused liver, J. Pharmacol. Exp. Ther., 1984, 3, 755-760.Google Scholar

  • [68] Saotome K., Morita H., Umeda M., Cytotoxicity test with simplified crystal violet staining method using microtitre plates and its application to injection drugs, Toxicol. In vitro, 1989, 4, 317-321.Google Scholar

  • [69] Lindhagen E., Nygren P., Larsson R., The fluorometric microculture cytotoxicity assay, Nat. Protoc., 2008, 8, 1364-1369.Google Scholar

  • [70] Betton G. R., Gorman N. T., Cell-mediated responses in dogs with spontaneous neoplasms. I. Detection of cell-mediated cytotoxicity by the chromium-51 release assay, J. Natl. Cancer Inst., 1978, 4, 1085-1093.Google Scholar

  • [71] Timonen T., Saksela E., A simplified isotope release assay for cell-mediated cytotoxicity against anchorage dependent target cells,, J. Immunol. Methods, 1977, 1-2, 123-132.Google Scholar

  • [72] Fassy J., Tsalkitzi K., Salavagione E., Hamouda-Tekaya N., Braud V.M., A real-time digital bio-imaging system to quantify cellular cytotoxicity as an alternative to the standard chromium-51 release assay, Immunology, 2017, 4, 489-494.Google Scholar

  • [73] Karimi M.A., Lee E., Bachmann M.H., Salicioni A.M., Behrens E.M, Kambayashi T., Baldwin C.L., Measuring cytotoxicity by bioluminescence imaging outperforms the standard chromium-51 release assay, PLoS One, 2014, 2, e89357.Google Scholar

  • [74] Valentin I., Philippe M., Lhuguenot J., Chagnon M., Uridine uptake inhibition as a cytotoxicity test for a human hepatoma cell line (HepG2 cells): comparison with the neutral red assay, Toxicology, 2001, 3, 127-139.CrossrefGoogle Scholar

  • [75] Valentin-Severin I., Laignelet L., Lhuguenot J.C., Chagnon M.C., Uridine uptake inhibition assay: an automated micromethod for the screening of cytotoxicity, Toxicology, 2002, 2-3, 207-213.CrossrefGoogle Scholar

  • [76] Decker T., Lohmann-Matthes M.L., A quick and simple method for the quantitation of lactate dehydrogenase release in measurements of cellular cytotoxicity and tumor necrosis factor (TNF) activity, J. Immunol. Methods, 1988, 1, 61-69.Google Scholar

  • [77] Gwag B.J., Canzoniero L.M., Sensi S.L., Demaro J.A., Koh J.Y., Goldberg M.P., Jacquin M., Choi D.W., Calcium ionophores can induce either apoptosis or necrosis in cultured cortical neurons, Neuroscience, 1999, 90(4), 1339-1348.Google Scholar

  • [78] Feng G., Kaplowitz N., Mechanism of staurosporine-induced apoptosis in murine hepatocytes, Am. J. Physiol. Gastrointest. Liver Physiol., 2002, 282(5), G825-834.Google Scholar

  • [79] Takei N., Endo Y., Ca2+ ionophore-induced apoptosis on cultured embryonic rat cortical neurons, Brain Res., 1994, 652(1), 65-70.Google Scholar

  • [80] Watson A.J., Askew J. N., Benson R. S., Poly(adenosine diphosphate ribose) polymerase inhibition prevents necrosis induced by H2O2 but not apoptosis, Gastroenterology, 1995, 109(2), 472-482.Google Scholar

  • [81] Cotter T.G., Glynn J.M., Echeverri F., Green D.R., The induction of apoptosis by chemotherapeutic agents occurs in all phases of the cell cycle, Anticancer Res., 1992, 12(3), 773-779.Google Scholar

  • [82] Bellomo G., Perotti M., Taddei F., Mirabelli F., Finardi G., Nicotera P., Orrenius S., Tumor necrosis factor alpha induces apoptosis in mammary adenocarcinoma cells by an increase in intranuclear free Ca2+ concentration and DNA fragmentation, Cancer Res., 1992, 52(5), 1342-1346.Google Scholar

  • [83] Tsuchida H., Takeda Y., Takei H., Shinzawa H., Takahashi T., Sendo F., In vivo regulation of rat neutrophil apoptosis occurring spontaneously or induced with TNF-alpha or cycloheximide, J. Immunol., 1995, 154(5), 2403-2412.Google Scholar

  • [84] Miller R.C., The micronucleus test as an in vivo cytogenetic method, Environ. Health Perspect., 1973, 6, 167-170.Google Scholar

  • [85] Schmid W., The micronucleus test, Mutat. Res., 1975, 31(1), 9-15.Google Scholar

  • [86] Hintzsche H., Hemmann U., Poth A., Utesch D., Lott J., Stopper H., Working Group “In vitro micronucleus test”, Gesellschaft für Umwelt-Mutationsforschung (GUM, German-speaking section of the European Environmental Mutagenesis and Genomics Society EEMGS), Fate of micronuclei and micronucleated cells, Mutat. Res., 2017, 771, 85-98.Google Scholar

  • [87] Santoro R., Ferraiuolo M., Morgano G.P., Muti P., Strano S., Comet Assay in Cancer Chemoprevention, Methods Mol. Biol., 2016, 1379, 99-105.Google Scholar

  • [88] de Lapuente J., Lourenço J., Mendo S.A., Borràs M., Martins M.G., Costa P.M., Pacheco M., The Comet Assay and its applications in the field of ecotoxicology: a mature tool that continues to expand its perspectives, Front. Genet., 2015, 6, 180.Google Scholar

  • [89] McKelvey-Martin V. J., Green M. H., Schmeze, P., Pool-Zobel B.L., De Méo M.P., Collins A., The single cell gel electrophoresis assay (comet assay): a European review, Mutat. Res., 1993, 288(1), 47-63.Google Scholar

  • [90] Geard C. R., Cytogenetic assays for genotoxic agents, Lens Eye Toxic. Res., 1992, 9(3-4), 413-428.Google Scholar

  • [91] Van Prooijen-Knegt A. C., Van Hoek J. F., Bauman J. G., Van Duijn P., Wool I.G., Van der Ploeg M., In situ hybridization of DNA sequences in human metaphase chromosomes visualized by an indirect fluorescent immunocytochemical procedure, Exp. Cell Res., 1982, 141(2), 197-407.Google Scholar

  • [92] Harréus U.A., Kleinsasser N.H., Zieger S., Wallner B., Reiter M., Schuller P., Berghaus A., Sensitivity to DNA-damage induction and chromosomal alterations in mucosa cells from patients with and without cancer of the oropharynx detected by a combination of Comet assay and fluorescence in situ hybridization, Mutat. Res., 2004, 563(2), 131-138.Google Scholar

  • [93] Rapp A., Bock C., Dittmar H., Greulich K.O., UV-A breakage sensitivity of human chromosomes as measured by COMET-FISH depends on gene density and not on the chromosome size, J. Photochem. Photobiol. 2000, B, 2-3, 109-117.CrossrefGoogle Scholar

  • [94] Latimer J.J. Kelly, C.M., Unscheduled DNA synthesis: the clinical and functional assay for global genomic DNA nucleotide excision repair, Methods Mol. Biol., 2014, 1105, 511-532.CrossrefGoogle Scholar

  • [95] Nesslany F., Unscheduled DNA synthesis (UDS) test with mammalian liver cells in vivo, Methods Mol. Biol., 2013, 1144, 373-387.Google Scholar

  • [96] Van Gompel J., Woestenborghs F., Beerens D., Mackie C., Cahill P.A., Knight A.W., Billinton N., Tweats D.J., Walmsley R.M., An assessment of the utility of the yeast GreenScreen assay in pharmaceutical screening, Mutagenesis, 2005, 20(6), 449-454.CrossrefGoogle Scholar

  • [97] Walmsley R.M., Tate M., The GADD45a-GFP GreenScreen HC assay, Methods Mol. Biol., 2012, 817, 231-250.Google Scholar

  • [98] Luzy A., Orsini N., Linget J., Bouvier G., Evaluation of the GADD45alpha-GFP GreenScreen HC assay for rapid and reliable in vitro early genotoxicity screening, J. Appl. Toxicol., 2013, 33(11), 1303-1315.Google Scholar

  • [99] Dearfield K.L., Jacobson-Kram D., Brown N.A., Williams J. R., Evaluation of a human hepatoma cell line as a target cell in genetic toxicology, Mutat. Res., 1983, 1-3, 437-449.Google Scholar

  • [100] Guillouzo A., Corlu A., Aninat C., Glaise D., Morel F., Guguen-Guillouzo C., The human hepatoma HepaRG cells: a highly differentiated model for studies of liver metabolism and toxicity of xenobiotics, Chem. Biol. Interact, 2007, 1, 66-73.Google Scholar

  • [101] Haponsaph R., Czuprynski C.J., Inhibition of the multiplication of Listeria monocytogenes in a murine hepatocyte cell line (ATCC TIB73) by IFN-gamma and TNF-alpha, Microb. Pathog., 1996, 5, 287-295.Google Scholar

  • [102] Pfeifer A.M., Cole K.E., Smoot D.T., Weston A., Groopman J.D., Shields P.G., Vignaud J.M., Juillerat M., Lipsky M.M., Trump B.F., Simian virus 40 large tumor antigen-immortalized normal human liver epithelial cells express hepatocyte characteristics and metabolize chemical carcinogens, Proc. Natl. Acad. Sci. U S A, 1993, 11, 5123-5127.CrossrefGoogle Scholar

  • [103] Melzer M.S., The Ames test as a predictive test for carcinogens, J. Environ. Pathol. Toxicol., 1979, 2(4), 1216-1217.Google Scholar

  • [104] Barbezan A.B., Martins R., Bueno J.B., Villavicencio A.L., Ames Test to Detect Mutagenicity of 2-Alkylcyclobutanones: A Review, J. Food Sci., 2017, (in press), DOI: 10.1111/1750-3841.13721.CrossrefGoogle Scholar

  • [105] Mortelmans K., Riccio E.S., The bacterial tryptophan reverse mutation assay with Escherichia coli WP2, Mutat. Res., 2000, 455(1-2), 61-69.Google Scholar

  • [106] Zeiger E., Bacterial mutation assays, Methods Mol. Biol., 2013, 1044, 3-26.Google Scholar

  • [107] Conti L., Crebelli R., Potential pitfalls associated with testing of enzyme preparations in the Salmonella/microsome assay, Regul. Toxicol. Pharmacol., 2016, 80, 291-294.Google Scholar

  • [108] McCann J., Ames B.N., Detection of carcinogens as mutagens in the Salmonella/microsome test: assay of 300 chemicals: discussion, Proc. Natl. Acad. Sci., 1976, 73(3), 950-954.Google Scholar

  • [109] Alley M.C., Uhl C.B., Lieber M.M., Improved detection of drug cytotoxicity in the soft agar colony formation assay through use of a metabolizable tetrazolium salt, Life Sci., 1982, 31(26), 3071-3078.CrossrefGoogle Scholar

  • [110] Malmberg M., Slocum H.K., Rustum Y.M., A model for mimicking the pharmacokinetics of chemotherapy drugs for evaluation of drug effects in a soft agar colony formation assay system, Sel. Cancer Ther., 1991, 7(4), 159-164.Google Scholar

  • [111] Rotem A., Janzer A., Izar B., Ji Z., Doench J.G, Garraway L.A, Struhl K., Alternative to the soft-agar assay that permits high-throughput drug and genetic screens for cellular transformation, Proc. Natl. Acad. Sci, 2015, 112(18), 5708-5713.Google Scholar

  • [112] Izar B., Rotem, A, GILA, a Replacement for the Soft-Agar Assay that Permits High-Throughput Drug and Genetic Screens for Cellular Transformation, Curr. Protocols Mol. Biol., 2016, epub, DOI: 10.1002/cpmb.28.CrossrefGoogle Scholar

  • [113] Combes R., Balls M., Curren R., Fischbach M., Fusenig N., Kirkland D., Lasne C., Landolph J., LeBoeuf R., Marquardt H. et al., Cell transformation assays as predictors of human carcinogenicity, Altern. Lab. Anim., 1999, 27, 745-767.Google Scholar

  • [114] Berwald Y., Sachs L., In vitro cell transformation with chemical carcinogens, Nature, 1963, 200, 1182-1184.Google Scholar

  • [115] Barrett J.C., Cell culture models of multistep carcinogenesis, IARC Sci. Publ., 1985, 58, 181-202.Google Scholar

  • [116] Maire M.A., Pant K., Phrakonkham P., Poth A., Schwind K.R., Rast C., Bruce S.W., Sly J.E, Bohnenberger S., Kunkelmann T., Schulz M., Vasseur P., Recommended protocol for the Syrian hamster embryo (SHE) cell transformation assay, Mutat. Res., 2012, 744(1), 76-81.Google Scholar

  • [117] Sasaki K., Bohnenberger S., Hayashi K., Kunkelmann T., Muramatsu D., Phrakonkham P., Poth A., Sakai A., Salovaara S., Tanaka N., Thomas B.C., Umeda M., Recommended protocol for the BALB/c 3T3 cell transformation assay, Mutat. Res., 2012, 744(1), 30-35.Google Scholar

  • [118] Combes R., Balls M., Curren R., Fischbach M., Fusenig N., Kirkland D., Lasne C., Landolph J., LeBoeuf R., Marquardt H., McCormick J., Müller L., Rivedal E., Sabbioni E., Tanaka N., Vasseur P., Yamasaki H., Cell Transformation Assays as Predictors of Human Carcinogenicity, Altern Lab Anim. 1999, 27: 745-67.Google Scholar

  • [119] Walker N.J., Real-time and quantitative PCR: applications to mechanism-based toxicology, J. Biochem. Mol. Toxicol., 2001, 15, 121-127.CrossrefGoogle Scholar

  • [120] Jenkins G.J., Chaleshtori M.H., Song H., Parry J.M., Mutation analysis using the restriction site mutation (RSM) assay, Mutat. Res., 1998, 405, 209-220.Google Scholar

  • [121] Steingrimsdottir H., Beare D., Cole J., Leal J.F., Kostic T., Lopez-Barea J., Dorado G., Lehmann A.R., Development of new molecular procedures for the detection of genetic alterations in man, Mutat. Res., 1996, 353, 109-121.Google Scholar

  • [122] Jenkins G.J., Suzen H.S., Sueiro R.A., Parry J.M., The restriction site mutation assay: a review of the methodology development and the current status of the technique, Mutagenesis, 1999, 14, 439-448.CrossrefGoogle Scholar

  • [123] Horikawa M., Nikaido O., Tanaka T., Nagata H., Sugahara T., Carcinogenesis in tissue culture. X. Rejoining of single-strand breaks in DNA by mammalian cells induced by chemical carcinogens (4-nitroquinoline 1-oxide and its derivative) in vitro, Exp. Cell Res., 1970, 59, 147-152.Google Scholar

  • [124] Pant K., Springer S., Bruce S., Lawlor T., Hewitt N., Aardema M.J., Vehicle and positive control values from the in vivo rodent comet assay and biomonitoring studies using human lymphocytes: historical database and influence of technical aspects, Environ. Mol. Mutagen, 2014, 55, 633-642.Google Scholar

  • [125] Mondal S., Brankow D.W., Heidelberger C., Two-stage chemical oncogenesis in cultures, of C3H/10T1/2 cells, Cancer Res., 1976, 36, 2254-2260.Google Scholar

  • [126] Weinstein I.B., Cell culture systems for studying multifactor interactions in carcinogenesis, Dev. Toxicol. Environ. Sci., 1980, 8, 149-164.Google Scholar

  • [127] Dale M.M., Easty G.C., Tchao R., Desai H., Andjargholi M., The induction of tumours in the guinea-pig with methylcholanthrene and diethylnitrosamine and their propagation in vivo and in vitro, Br. J. Cancer, 1973, 27, 445-450.Google Scholar

  • [128] Bertram J.S., Peterson A.R., Heidelberger C., Chemical oncogenesis in cultured mouse embryo cells in relation to the cell cycle, In vitro, 1975, 11, 97-106.Google Scholar

  • [129] Liamin M., Boutet-Robinet E., Jamin E.L., Fernier M., Khoury L., Kopp B., Le Ferrec E., Vignar J., Audebert M., Sparfel L., Benzo[a]pyrene-induced DNA damage associated with mutagenesis in primary human activated T lymphocytes, Biochem. Pharmacol., 2017, 137, 113-124.Google Scholar

  • [130] Colacci A., Mascolo M.G., Perdichizzi S., Quercioli D., Gazzilli A., Rotondo F., Morandi E., Guerrini A., Silingardi P., Grilli S., Vaccari M., Different sensitivity of BALB/c 3T3 cell clones in the response to carcinogens, Toxicol. In vitro, 2011, 25, 1183-1190.Google Scholar

  • [131] Watson, R.E., Goodman, J.I, Epigenetics and DNA methylation come of age in toxicology, Toxicol Sci., 2002, 1, 11-16.Google Scholar

  • [132] Kurdyukov S., Bullock, M., DNA Methylation Analysis: Choosing the Right Method, Biology (Basel), 2016, 5(1), DOI: 10.3390/biology5010003.CrossrefGoogle Scholar

  • [133] Couldrey C., Cave V., Assessing DNA methylation levels in animals: choosing the right tool for the job, Anim. Genet., 2014, 45 Suppl.1, 15-24.Google Scholar

  • [134] Lizardi P.M., Yan Q., Wajapeyee N., DNA Bisulfite Sequencing for Single-Nucleotide-Resolution DNA Methylation Detection, Cold Spring Harb Protoc., 2016, (in press), DOI: 10.1101/pdp. prot094839.CrossrefGoogle Scholar

  • [135] Spielmann H., Liebsch M., Validation successes: chemicals, Altern Lab Anim, 2002, 30 Suppl. 2, 33-40.Google Scholar

  • [136] Piersma A.H., Haakma, A.S., Hagenaars A.M., In vitro assays for the developmental toxicity of xenobiotic compounds using differentiating embryonal carcinoma cells in culture, Toxicol. In vitro, 1993, 5, 615-621.Google Scholar

  • [137] Pratt R.M., Grove R.I., Willis W.D., Prescreening for environmental teratogens using cultured mesenchymal cells from the human embryonic palate, Teratog. Carcinog. Mutagen, 1982, 3-4, 313-318.Google Scholar

  • [138] Mummery C.L., van den Brink C.E., van der Saag P.T., de Laat S.W., A short-term screening test for teratogens using differentiating neuroblastoma cells in vitro, Teratology, 1984, 2, 271-279.Google Scholar

  • [139] Steele V.E., Morrissey R.E., Elmore E.L., Gurganus-Rocha D., Wilkinson B.P., Curren R.D., Schmetter B.S., Louie A.T., Lamb, 4th, J.C, Yang L.L., Evaluation of two in vitro assays to screen for potential developmental toxicants, Fundam. Appl. Toxicol., 1988, 4, 673-684.Google Scholar

  • [140] Lu R.Z., Chen C.F., Lin H.F., Huang L.M., Jin, X.P., Preliminary validation of tumor cell attachment inhibition assay for developmental toxicants with mouse S180 cells, Biomed. Environ. Sci., 1999, 4, 253-259.Google Scholar

  • [141] Genschow E., Spielmann H., Scholz G., Pohl I., Seiler A., Clemann N., Bremer S., Becker K., Validation of the embryonic stem cell test in the international ECVAM validation study on three in vitro embryotoxicity tests, Altern. Lab. Anim., 2004, 3, 209-244.Google Scholar

  • [142] Liu H., Ren C., Liu W., Jiang X., Wang L., Zhu B., Jia W., Lin J., Tan J., Liu X., Embryotoxicity estimation of commonly used compounds with embryonic stem cell test, Mol. Med. Rep., 2017, 1, 263-271.Google Scholar

  • [143] Hong E., Jeung E., Assessment of Developmental Toxicants using Human Embryonic Stem Cells, Toxicol. Res., 2013, 4, 221-227.Google Scholar

  • [144] Scholz G., Genschow E., Pohl I., Bremer S., Paparella M., Raabe H., Southee J., Spielmann H., Prevalidation of the Embryonic Stem Cell Test (EST)-A New In vitro Embryotoxicity Test, Toxicol., In vitro, 1999, 4-5, 675-681.Google Scholar

  • [145] Umansky R., The effect of cell population density on the developmental fate of reaggregating mouse limb bud mesenchyme, Dev. Biol., 1966, 1, 31-56.Google Scholar

  • [146] Seiler A, Visan A., Buesen R., Genschow E., Spielmann H., Improvement of an in vitro stem cell assay for developmental toxicity: the use of molecular endpoints in the embryonic stem cell test, Reprod. Toxicol., 2004, 2, 231-240.Google Scholar

  • [147] Lallemand D., Ham J., Garbay S., Bakiri L., Traincard F., Jeannequin O., Pfarr C.M., Yaniv M., Stress-activated protein kinases are negatively regulated by cell density, EMBO J., 1998, 19, 5615-5626.Google Scholar

  • [148] Li X.A., Bianchi C., Sellke F.W., Rat aortic smooth muscle cell density affects activation of MAP kinase and Akt by menadione and PDGF homodimer BB, J. Surg. Res., 2001, 2, 197-204.Google Scholar

  • [149] Hines W.A., Thorburn J., Thorburn A., Cell density and contraction regulate p38 MAP kinase-dependent responses in neonatal rat cardiac myocytes, Am. J. Physiol, 1999,1 Pt 2, H331-H341.Google Scholar

  • [150] Iyanagi T., Molecular mechanism of phase I and phase II drug-metabolizing enzymes: implications for detoxification, Int Rev Cytol., 2007, 260, 35-112.Google Scholar

  • [151] Botts S., Ennulat D., Francke-Carroll S., Graham M., Maronpot R.R., Mohutsky M., Introduction to hepatic drug metabolizing enzyme induction in drug safety evaluation studies, Toxicol. Pathol., 2010, 5, 796-798.Google Scholar

  • [152] Babula P., Masarik M., Adam V., Eckschlager T., Stiborova M., Trnkova L., Skutkova H., Provaznik I., Hubalek J., Kizek R., Mammalian metallothioneins: properties and functions, Metallomics, 2012, 8, 739-750.Google Scholar

  • [153] Cherian M.G, The synthesis of metallothionein and cellular adaptation to metal toxicity in primary rat kidney epithelial cell cultures, Toxicology, 1980, 2, 225-231.Google Scholar

  • [154] Walker P.A., Kille P., Hurley A., Bury N.R., Hogstrand C., An in vitro method to assess toxicity of waterborne metals to fish, Toxicol. Appl. Pharmacol., 2008, 1, 67-77.Google Scholar

  • [155] Tian Z.Q., Xu Y.Z., Zhang Y.F., Ma G.F., He M., Wang G.Y., Effects of metallothionein-3 and metallothionein-1E gene transfection on proliferation, cell cycle, and apoptosis of esophageal cancer cells, Genet Mol. Res., 2013, 4, 4595-4603.Google Scholar

  • [156] Djuric A., Begic A., Gobeljic B., Stanojevic I., Ninkovic M., Vojvodic D., Pantelic A., Zebic G., Prokic V., Dejanovic B. et al., Oxidative stress, bioelements and androgen status in testes of rats subacutely exposed to cadmium, Food Chem. Toxicol., 2015, 86, 25-33.Google Scholar

  • [157] Giustarini D., Tsikas D., Colombo G., Milzani A., Dalle-Donne I., Fanti P., Rossi R., Pitfalls in the analysis of the physiological antioxidant glutathione (GSH) and its disulfide (GSSG) in biological samples: An elephant in the room, J. Chromatogr. B: Analyt. Technol. Biomed. Life Sci., 2016, 1019, 21-28.Google Scholar

  • [158] Ochi T., Miyaura S., Cytotoxicity of an organic hydroperoxide and cellular antioxidant defense system against hydroperoxides in cultured mammalian cells, Toxicology, 1989, 1-2, 69-82.Google Scholar

  • [159] Shukla G.S., Hussain T., Chandra S.V., Possible role of regional superoxide dismutase activity and lipid peroxide levels in cadmium neurotoxicity: in vivo and in vitro studies in growing rats, Life Sci., 1987, 19, 2215-2221.Google Scholar

  • [160] Costa Amaral, A.C., Guimarães J.F.J., Carvalho L.V.B., Castro V. S., Pereira N.C., Murata M.M., Mainenti H.R.D., Mitri S., Ribeiro P.C., Rodrigues C.F. et al., Evaluation of Genotoxic Effects of Asbestos, Biomonitoring, 2016, 3, 23-33.Google Scholar

  • [161] Calabrese E.J., Canada A.T., Catalase: its role in xenobiotic detoxification, Pharmacol Ther., 1989, 2, 297-307.Google Scholar

  • [162] Zhao M., Jiang Q., Wang W., Geng M., Wang M., Han Y., Wang, C., The Roles of Reactive Oxygen Species and Nitric Oxide in Perfluorooctanoic Acid-Induced Developmental Cardiotoxicity and l-Carnitine Mediated Protection, Int. J. Mol. Sci., 2017, 18(6), DOI: 10.3390/ijms18061229.CrossrefGoogle Scholar

  • [163] Roebuck K.A., Oxidant stress regulation of IL-8 and ICAM-1 gene expression: differential activation and binding of the transcription factors AP-1 and NF-kappaB (Review), Int. J. Mol. Med., 1999, 3, 223-230.Google Scholar

  • [164] Zhang Y., Chen F., Reactive oxygen species (ROS), troublemakers between nuclear factor-kappaB (NF-kappaB) and c-Jun NH(2)-terminal kinase (JNK), Cancer Res., 2004, 6, 1902-1905.Google Scholar

  • [165] Hartney T., Birari R., Venkataraman S., Villegas L., Martinez M., Black S.M., Stenmark, K.R, Nozik-Grayck, E., Xanthine oxidase-derived ROS upregulate Egr-1 via ERK1/2 in PA smooth muscle cells; model to test impact of extracellular ROS in chronic hypoxia, PLoS One, 2011, 6(11), e27531, DOI: 10.1371/journal.pone.0027531.CrossrefGoogle Scholar

  • [166] Zou W., Yan M., Xu W., Huo H., Sun L., Zheng Z., Liu X., Cobalt chloride induces PC12 cells apoptosis through reactive oxygen species and accompanied by AP-1 activation, J. Neurosci. Res., 2001, 6, 646-653.Google Scholar

  • [167] Li L., Prabhakaran K., Shou Y., Borowitz J.L., Isom G.E., Oxidative stress and cyclooxygenase-2 induction mediate cyanide-induced apoptosis of cortical cells, Toxicol. Appl. Pharmacol., 2002, 1, 55-63.Google Scholar

  • [168] Trejo-Solìs C., Jimenez-Farfan D., Rodriguez-Enriquez S., Fernandez-Valverde F., Cruz-Salgado A., Ruiz-Azuara L., Sotelo J., Copper compound induces autophagy and apoptosis of glioma cells by reactive oxygen species and JNK activation, BMC Cancer, 2012, 12, 156, DOI: 1186/1471-2407-12-156.Google Scholar

  • [169] Gulliver L.S.M., Xenobiotics and the Glucocorticoid Receptor, Toxicol. Appl. Pharmacol., 2017, 319, 69-79.Google Scholar

  • [170] Wallace B.D., Redinbo M.R., Xenobiotic-sensing nuclear receptors involved in drug metabolism: a structural perspective, Drug Metab. Rev., 2013, 1, 79-100.Google Scholar

  • [171] Pollard T.D., A guide to simple and informative binding assays, Mol. Biol. Cell, 2010, 23, 4061-4067.Google Scholar

  • [172] Raines R.T., Fluorescence polarization assay to quantify protein-protein interactions: an update, Methods Mol. Biol., 2015, 1278, 323-327.Google Scholar

  • [173] Stoddart L.A., White C.W., Nguyen K., Hill S.J., Pfleger K.D.G., Fluorescence- and bioluminescence-based approaches to study GPCR ligand binding, Br. J. Pharmacol., 2016, 20, 3028-3037.Google Scholar

  • [174] Kuehn H.S., Radinger M., Gilfillan A.M., Measuring mast cell mediator release, Curr. Protoc. Immunol., 2010, Chapter 7, Unit 7.38, DOI: 10.1002/0471142735.im0738s91.CrossrefGoogle Scholar

  • [175] Palmer G.W., Dibbern Jr, D.A., Burks A.W., Bannon G.A., Bock S.A., Porterfield H.S., McDermott, R.A., Dreskin S.C., Comparative potency of Ara h 1 and Ara h 2 in immunochemical and functional assays of allergenicity, Clin. Immunol., 2005, 3, 302-312.Google Scholar

  • [176] Camner P., Lundborg M., Låstbom L., Gerde P., Gross N., Jarstrand C., Experimental and calculated parameters on particle phagocytosis by alveolar macrophages, J. Appl. Physiol. 2002,(1985), 6, 2608-2616.Google Scholar

  • [177] Pinton P., Giorgi C., Siviero R., Zecchini E., Rizzuto R., Calcium and apoptosis: ER-mitochondria Ca2+ transfer in the control of apoptosis, Oncogene, 2008, 27, 6407-6418.Google Scholar

  • [178] Wang H.C., Zhou Y., Huang S.K., SHP-2 phosphatase controls aryl hydrocarbon receptor-mediated ER stress response in mast cells, Arch Toxicol., 2017, 91, 1739-1748.Google Scholar

  • [179] Grynkiewicz G., Poenie M., Tsien R.Y., A new generation of Ca2+ indicators with greatly improved fluorescence properties, J. Biol. Chem., 1985, 6, 3440-3450.Google Scholar

  • [180] Gee K.R., Brown K.A., Chen W.N., Bishop-Stewart J., Gray D., Johnson I., Chemical and physiological characterization of fluo-4 Ca2+-indicator dyes, Cell Calcium, 2000, 2, 97-106.Google Scholar

  • [181] Tay L.H., Griesbeck O., Yue D.T., Live-cell transforms between Ca2+ transients and FRET responses for a troponin-C-based Ca2+ sensor, Biophys. J., 2007, 11, 4031-4040.Google Scholar

  • [182] Nagai T., Sawano A., Park E.S., Miyawaki, A., Circularly permuted green fluorescent proteins engineered to sense Ca2+, Proc. Natl. Acad. Sci. U S A, 2001, 6, 3197-3202.Google Scholar

About the article

Received: 2017-07-18

Accepted: 2017-08-22

Published Online: 2017-10-12

Published in Print: 2017-10-26


Citation Information: Biomonitoring, Volume 4, Issue 1, Pages 11–26, ISSN (Online) 2300-4606, DOI: https://doi.org/10.1515/bimo-2017-0002.

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