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Review

Embryonic stem cells and the next generation of developmental toxicity testing

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Pages 833-841 | Received 26 Apr 2017, Accepted 03 Jul 2017, Published online: 12 Jul 2017

References

  • Wilson JG. Current status of teratology. In: Wilson JG, Fraser FC, editors. General principles and etiology. Boston, MA: Springer US; 1977. p. 47–74.
  • Vargesson N. Thalidomide‐induced teratogenesis: history and mechanisms. Birth Defect Res. 2015;105:140–156.
  • Ito T, Ando H, Handa H. Teratogenic effects of thalidomide: molecular mechanisms. Cell Mol Life Sci. 2011;68:1569–1579.
  • Genschow E, Spielmann H, Scholz G, et al. The ECVAM international validation study on in vitro embryotoxicity tests: results of the definitive phase and evaluation of prediction models. Alternatives Lab Anim. 2002;30:151–176.
  • Collins FS, Gray GM, Bucher JR. Transforming environmental health protection. Science. 2008;319:906.
  • Tice RR, Austin CP, Kavlock RJ, et al. Improving the human hazard characterization of chemicals: a Tox21 update. Environ Health Perspect. 2013;121:756.
  • Tralau T, Oelgeschläger M, Gürtler R, et al. Regulatory toxicology in the twenty-first century: challenges, perspectives and possible solutions. Arch Toxicol. 2015;89:823–850.
  • Tralau T, Luch A. Drug-mediated toxicity: illuminating the ‘bad’ in the test tube by means of cellular assays? Trends Pharmacol Sci. 2012;33:353–364.
  • Trosko JE, Chang CC. Factors to consider in the use of stem cells for pharmaceutic drug development and for chemical safety assessment. Toxicology. 2010;270:18–34.
  • Bartfeld S, Clevers H. Stem cell-derived organoids and their application for medical research and patient treatment. J Mol Med. 2017;95:729–738.
  • Roberts RM, Green JA, Schulz LC. The evolution of the placenta. Reproduction. 2016;152:R179–R89.
  • Carter AM, Enders AC. Placentation in mammals: definitive placenta, yolk sac, and paraplacenta. Theriogenology. 2016;86:278–287.
  • Myren M, Mose T, Mathiesen L, et al. The human placenta–an alternative for studying foetal exposure. Toxicol In Vitro. 2007;21:1332–1340.
  • Carter AM. Animal models of human placentation–a review. Placenta. 2007;28(Suppl):A:S41-S7.
  • Li H, Rietjens IM, Louisse J, et al. Use of the ES-D3 cell differentiation assay, combined with the BeWo transport model, to predict relative in vivo developmental toxicity of antifungal compounds. Toxicol In Vitro. 2015;29:320–328.
  • Gundacker C, Neesen J, Straka E, et al. Genetics of the human placenta: implications for toxicokinetics. Arch Toxicol. 2016;90:2563–2581.
  • Nau H. Species differences in pharmacokinetics and drug teratogenesis. Environ Health Perspect. 1986;70:113.
  • Wells PG, Winn LM. Biochemical toxicology of chemical teratogenesis. Crit Rev Mol Biol. 1996;31:1–40.
  • Juchau MR. Bioactivation in chemical teratogenesis. Annu Rev Pharmacol Toxicol. 1989;29:165–187.
  • Cassina M, Salviati L, Di Gianantonio E, et al. Genetic susceptibility to teratogens: state of the art. Reprod Toxicol. 2012;34:186–191.
  • Brown LP, Flint OP, Orton TC, et al. Chemical teratogenesis: testing methods and the role of metabolism. Drug Metab Rev. 1986;17:221–260.
  • Louisse J, Beekmann K, Rietjens IM. Use of physiologically based kinetic modeling-based reverse dosimetry to predict in vivo toxicity from in vitro data. Chem Res Toxicol. 2017;30:114–125.
  • Doetschman TC, Eistetter H, Katz M, et al. The in vitro development of blastocyst-derived embryonic stem cell lines: formation of visceral yolk sac, blood islands and myocardium. Development. 1985;87:27–45.
  • Liu Y, Asakura M, Inoue H, et al. Sox17 is essential for the specification of cardiac mesoderm in embryonic stem cells. Proc Natl Acad Sci U S A. 2007;104:3859–3864.
  • Kugler J, Tharmann J, Chuva De Sousa Lopes SM, et al. A bmp reporter transgene mouse embryonic stem cell model as a tool to identify and characterize chemical teratogens. Toxicol Sci. 2015;146:374–385.
  • Zhang C, Ball J, Panzica-Kelly J, et al. In vitro developmental toxicology screens: a report on the progress of the methodology and future applications. Chem Res Toxicol. 2016;29:534–544.
  • Piersma AH, Genschow E, Verhoef A, et al. Validation of the postimplantation rat whole-embryo culture test in the international ECVAM validation study on three in vitro embryotoxicity tests. Altern Lab Anim. 2004;32:275–307.
  • Genschow E, Scholz G, Brown N, et al. Development of prediction models for three in vitro embryotoxicity tests in an ECVAM validation study. In Vitr Mol Toxicol. 1999;13:51–66.
  • Ball JS, Stedman DB, Hillegass JM, et al. Fishing for teratogens: a consortium effort for a harmonized zebrafish developmental toxicology assay. Toxicol Sci. 2014;139:210–219.
  • West PR, Weir AM, Smith AM, et al. Predicting human developmental toxicity of pharmaceuticals using human embryonic stem cells and metabolomics. Toxicol Appl Pharmacol. 2010;247:18–27.
  • Uibel F, Mühleisen A, Köhle C, et al. ReProGlo: a new stem cell-based reporter assay aimed to predict embryotoxic potential of drugs and chemicals. Reprod Toxicol. 2010;30:103–112.
  • Seiler AEM, Spielmann H. The validated embryonic stem cell test to predict embryotoxicity in vitro. Nat Protoc. 2011;6:961–978.
  • Zur Nieden NI, Kempka G, Hj A. Molecular multiple endpoint embryonic stem cell test—a possible approach to test for the teratogenic potential of compounds. Toxicol Appl Pharmacol. 2004;194:257–269.
  • Adler S, Pellizzer C, Hareng L, et al. First steps in establishing a developmental toxicity test method based on human embryonic stem cells. Toxicol In Vitro. 2008;22:200–211.
  • Jiang Y, Wang D, Zhang G, et al. Disruption of cardiogenesis in human embryonic stem cells exposed to trichloroethylene. Environ Toxicol. 2016;31:1372–1380.
  • Stiegler NV, Krug AK, Matt F, et al. Assessment of chemical-induced impairment of human neurite outgrowth by multiparametric live cell imaging in high-density cultures. Toxicol Sci. 2011;121:73–87.
  • Kameoka S, Babiarz J, Kolaja K, et al. A high-throughput screen for teratogens using human pluripotent stem cells. Toxicol Sci. 2014;137:76–90.
  • Jagtap S, Meganathan K, Gaspar J, et al. Cytosine arabinoside induces ectoderm and inhibits mesoderm expression in human embryonic stem cells during multilineage differentiation. Br J Pharmacol. 2011;162:1743–1756.
  • Meganathan K, Jagtap S, Wagh V, et al. Identification of thalidomide-specific transcriptomics and proteomics signatures during differentiation of human embryonic stem cells. PLoS One. 2012;7:e44228.
  • Jung EM, Choi YU, Kang HS, et al. Evaluation of developmental toxicity using undifferentiated human embryonic stem cells. J Appl Toxicol. 2015;35:205–218.
  • Rempel E, Hoelting L, Waldmann T, et al. A transcriptome-based classifier to identify developmental toxicants by stem cell testing: design, validation and optimization for histone deacetylase inhibitors. Arch Toxicol. 2015;89:1599–1618.
  • Pallocca G, Grinberg M, Henry M, et al. Identification of transcriptome signatures and biomarkers specific for potential developmental toxicants inhibiting human neural crest cell migration. Arch Toxicol. 2016;90:159–180.
  • Vaiserman A. Epidemiologic evidence for association between adverse environmental exposures in early life and epigenetic variation: a potential link to disease susceptibility? Clin Epigenet. 2015;7:96.
  • Heijmans BT, Tobi EW, Stein AD, et al. Persistent epigenetic differences associated with prenatal exposure to famine in humans. Proc Natl Acad Sci U S A. 2008;105:17046–17049.
  • Feinberg AP. Phenotypic plasticity and the epigenetics of human disease. Nature. 2007;447:433–440.
  • Bjornsson HT, Fallin MD, Feinberg AP. An integrated epigenetic and genetic approach to common human disease. Trends Genet. 2004;20:350–358.
  • Trosko JE. Pre-natal epigenetic influences on acute and chronic diseases later in life, such as cancer: global health crises resulting from a collision of biological and cultural evolution. Prev Nutr Food Sci. 2011;16:394–407.
  • Balmer NV, Weng MK, Zimmer B, et al. Epigenetic changes and disturbed neural development in a human embryonic stem cell-based model relating to the fetal valproate syndrome. Hum Mol Genet. 2012;21:4104–4114.
  • Duenas-Gonzalez A, Candelaria M, Perez-Plascencia C, et al. Valproic acid as epigenetic cancer drug: preclinical, clinical and transcriptional effects on solid tumors. Cancer Treat Rev. 2008;34:206–222.
  • Dix DJ, Houck KA, Martin MT, et al. The ToxCast program for prioritizing toxicity testing of environmental chemicals. Toxicol Sci. 2007;95:5–12.
  • Kavlock R, Chandler K, Houck K, et al. Update on EPA’s ToxCast program: providing high throughput decision support tools for chemical risk management. Chem Res Toxicol. 2012;25:1287–1302.
  • Kleinstreuer NC, Judson RS, Reif DM, et al. Environmental impact on vascular development predicted by high-throughput screening. Environ Health Perspect. 2011;119:1596–1603.
  • Tollefsen KE, Scholz S, Cronin MT, et al. Applying adverse outcome pathways (AOPs) to support integrated approaches to testing and assessment (IATA). Regul Toxicol Pharmacol. 2014;70:629–640.
  • Patlewicz G, Kuseva C, Kesova A, et al. Towards AOP application–implementation of an integrated approach to testing and assessment (IATA) into a pipeline tool for skin sensitization. Regul Toxicol Pharmacol. 2014;69:529–545.
  • OECD (2017). Guidance document on the reporting of defined approaches to be used within integrated approaches to testing and assessment, OECD Publishing, Paris. Available from:http://dx.doi.org/10.1787/9789264274822-en.
  • Sogorb MA, Pamies D, De Lapuente J, et al. An integrated approach for detecting embryotoxicity and developmental toxicity of environmental contaminants using in vitro alternative methods. Toxicological Lett. 2014;230:356–367.
  • Augustine‐Rauch K, Zhang CX, Panzica‐Kelly JM. A developmental toxicology assay platform for screening teratogenic liability of pharmaceutical compounds. Birth Defects Res B: Dev Reprod Toxicol. 2016;107:4–20.
  • Fritsche E, Crofton KM, Hernandez AF, et al. OECD/EFSA workshop on developmental neurotoxicity (DNT): the use of non-animal test methods for regulatory purposes. Altern Anim Ex. 2017;34:311–315.
  • Walters L. Human embryonic stem cell research: an intercultural perspective. Kennedy Inst Ethics J. 2004;14:3–38.
  • Osafune K, Caron L, Borowiak M, et al. Marked differences in differentiation propensity among human embryonic stem cell lines. Nat Biotechnol. 2008;26:313–315.
  • Takahashi K, Tanabe K, Ohnuki M, et al. Induction of pluripotent stem cells from adult human fibroblasts by defined factors. Cell. 2007;131:861–872.
  • Yu J, Vodyanik MA, Smuga-Otto K, et al. Induced pluripotent stem cell lines derived from human somatic cells. Science. 2007;318:1917–1920.
  • Inoue H, Nagata N, Kurokawa H, et al. iPS cells: a game changer for future medicine. Embo J. 2014;33:409–417.
  • Tiscornia G, Vivas EL, Belmonte JCI. Diseases in a dish: modeling human genetic disorders using induced pluripotent cells. Nat Med. 2011;17:1570–1576.
  • Wu SM, Hochedlinger K. Harnessing the potential of induced pluripotent stem cells for regenerative medicine. Nat Cell Biol. 2011;13:497–505.
  • Siller R, Naumovska E, Mathapati S, et al. Development of a rapid screen for the endodermal differentiation potential of human pluripotent stem cell lines. Sci Rep. 2016;6:37178.
  • Stacey GN, Crook JM, Hei D, et al. Banking human induced pluripotent stem cells: lessons learned from embryonic stem cells? Cell Stem Cell. 2013;13:385–388.
  • Pamies D, Bal-Price A, Simeonov A, et al. Good cell culture practice for stem cells and stem-cell-derived models. Altern Anim Ex. 2017;34:95–132.
  • Initiative ISC. Screening ethnically diverse human embryonic stem cells identifies a chromosome 20 minimal amplicon conferring growth advantage. Nat Biotechnol. 2011;29:1132–1144.
  • Akopian V, Andrews PW, Beil S, et al. Comparison of defined culture systems for feeder cell free propagation of human embryonic stem cells. In Vitro Cell Dev Biol Anim. 2010;46:247–258.
  • Merkle FT, Ghosh S, Kamitaki N, et al. Human pluripotent stem cells recurrently acquire and expand dominant negative P53 mutations. Nature. 2017;545:229–233.
  • Hoffman LM, Carpenter MK. Characterization and culture of human embryonic stem cells. Nat Biotechnol. 2005;23:699–708.
  • Lewandowski J, Kurpisz M. Techniques of human embryonic stem cell and induced pluripotent stem cell derivation. Arch Immunol Ther Exp (Warsz). 2016;64:349–370.
  • Basketter DA, Alépée N, Ashikaga T, et al. Categorization of chemicals according to their relative human skin sensitizing potency. Dermatitis. 2014;25:11–21.
  • Tsai T, Kyaw MH, Novicki D, et al. Exposure to MF59-adjuvanted influenza vaccines during pregnancy—a retrospective analysis. Vaccine. 2010;28:1877–1880.
  • Lilienblum W, Dekant W, Foth H, et al. Alternative methods to safety studies in experimental animals: role in the risk assessment of chemicals under the new European Chemicals Legislation (REACH). Arch Toxicol. 2008;82:211–236.
  • Tralau T, Luch A. Moving from rats to cellular omics in regulatory toxicology: great challenge toward sustainability or “up-shit-creek without a paddle”? Arch Toxicol. 2015;89:819–821.
  • Tralau T, Riebeling C, Pirow R, et al. Wind of change challenges toxicological regulators. Environ Health Perspect. 2012;120:1489.
  • Schenk B, Weimer M, Bremer S, et al. The ReProTect Feasibility Study, a novel comprehensive in vitro approach to detect reproductive toxicants. Reprod Toxicol. 2010;30:200–218.
  • Solter D. From teratocarcinomas to embryonic stem cells and beyond: a history of embryonic stem cell research. Nat Rev Genet. 2006;7:319–327.
  • Davila JC, Cezar GG, Thiede M, et al. Use and application of stem cells in toxicology. Toxicol Sci. 2004;79:214–223.
  • Scholz G, Pohl I, Genschow E, et al. Embryotoxicity screening using embryonic stem cells in vitro: correlation to in vivo teratogenicity. Cells Tissues Organs. 1999;165:203–211.
  • Schardein JL, Keller KA, Schwetz BA. Potential human developmental toxicants and the role of animal testing in their identification and characterization. CRC Crit Rev Toxicol. 1989;19:251–339.
  • Knight A. Systematic reviews of animal experiments demonstrate poor human clinical and toxicological utility. Alternatives Lab Anim. 2007;35:641–659.
  • Ginis I, Luo Y, Miura T, et al. Differences between human and mouse embryonic stem cells. Dev Biol. 2004;269:360–380.
  • Sato N, Sanjuan IM, Heke M, et al. Molecular signature of human embryonic stem cells and its comparison with the mouse. Dev Biol. 2003;260:404–413.
  • Hartung T, Bremer S, Casati S, et al. A modular approach to the ECVAM principles on test validity. Alternatives Lab Anim. 2004;32:467–472.

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