An integrated approach for detecting embryotoxicity and developmental toxicity of environmental contaminants using in vitro alternative methods

Toxicology Letters

Volumn 230, Issue 2, 2014, Pages 356-367

  Sogorb, Miguel A ^a   Pamies, David ^a,b   de Lapuente, Joaquín ^c   Estevan, Carmen ^a,d   Estévez, Jorge ^a   Vilanova, Eugenio ^a  

^a MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

^b JOHNS HOPKINS BLOOMBERG SCHOOL OF PUBLIC HEALTH   (United States)

^c UNIVERSITY OF BARCELONA   (Spain)

^d JOINT RESEARCH CENTRE   (Italy)

Author keywords

Alternative tests; Embryonic stem cell test; Embryotoxicity; Teratogenicity; WEC; Zebrafish test

Indexed keywords

ADHERENT CELL; ARTICLE; CELL DIFFERENTIATION; CLINICAL ASSESSMENT; CYTOTOXICITY ASSAY; CYTOTOXICITY TEST; DEVELOPMENTAL STAGE; DEVELOPMENTAL TOXICITY; ECONOMIC ASPECT; EMBRYO CULTURE; EMBRYO DEVELOPMENT; EMBRYOID BODY; EMBRYONIC STEM CELL; EMBRYONIC STEM CELL TEST; EMBRYOTOXICITY; ENVIRONMENTAL EXPOSURE; EX VIVO STUDY; GENE EXPRESSION PROFILING; GENOMICS; GRANULE CELL; HUMAN; IN VITRO STUDY; MOLECULAR BIOLOGY; MOUSE MODEL; NEURAL STEM CELL; NONHUMAN; PHENOTYPIC VARIATION; PROTEOMICS; RISK ASSESSMENT; SCREENING TEST; TERATOGENICITY; TOXICITY TESTING; TOXICOKINETICS; ZEBRA FISH; ANIMAL; ANIMAL TESTING ALTERNATIVE; DRUG EFFECTS; EMBRYOLOGY; FETUS; MOUSE; POLLUTANT; RAT;

POLLUTANT;

ANIMAL TESTING ALTERNATIVES; ANIMALS; CELL DIFFERENTIATION; EMBRYONIC DEVELOPMENT; EMBRYONIC STEM CELLS; ENVIRONMENTAL POLLUTANTS; FETUS; HUMANS; IN VITRO TECHNIQUES; MICE; PROTEOMICS; RATS; ZEBRAFISH;

EID: 84907176470     PISSN: 03784274     EISSN: 18793169     Source Type: Journal    
DOI: 10.1016/j.toxlet.2014.01.037     Document Type: Article

References (75)

1. Augustine-Rauch K., Zhang C.X., Panzica-Kelly J.M. In vitro developmental toxicology assays: a review of the state of the science of rodent and zebrafish whole embryo culture and embryonic stem cell assays. Birth Defects Res. C Embryo Today 2010, 90:87-98.
2. Baek D.H., Kim T.G., Lim H.K., Kang J.W., Seong S.K., Choi S.E., Lim S.Y., Park S.H., Nam B.H., Kim E.H., Kim M.S., Park K.L. Embryotoxicity assessment of developmental neurotoxicants using a neuronal endpoint in the embryonic stem cell test. J. Appl. Toxicol. 2012, 32:617-626.
3. Barrier M., Jeffay S., Nichols H.P., Chandler K.J., Hoopes M.R., Slentz-Kesler K., Hunter E.S. Mouse embryonic stem cell adherent cell differentiation and cytotoxicity (ACDC) assay. Reprod. Toxicol. 2011, 31:383-391.
4. Belanger S.E., Rawlings J.M., Carr G.J. Use of fish embryo toxicity tests for theprediction of acute fish toxicity to chemicals. Environ. Toxicol. Chem. 2013, 32:1768-1783.
5. Brannen K.C., Panzica-Kelly J.M., Danberry T.L., Augustine-Rauch K.A. Development of a zebrafish embryo teratogenicity assay and quantitative prediction model. Birth Defects Res. B Dev. Reprod. Toxicol. 2010, 89:66-77.
6. Buesen R., Genschow E., Slawik B., Visan A., Spielmann H., Luch A., Seiler A. Embryonic stem cell test remastered: comparison between the validated EST and the new molecular FACS-EST for assessing developmental toxicity in vitro. Toxicol. Sci. 2009, 108:389-400.
7. Buzanska L., Sypecka J., Nerini-Molteni S., Compagnoni A., Hogberg H.T., del Torchio R., Domanska-Janik K., Zimmer J., Coecke S. A human stem cell-based model for identifying adverse effects of organic and inorganic chemicals on the developing nervous system. Stem Cells 2009, 27:2591-25601.
8. Chandler K.J., Barrier M., Jeffay S., Nichols H.P., Kleinstreuer N.C., Singh A.V., Reif D.M., Sipes N.S., Judson R.S., Dix D.J., Kavlock R., Hunter E.S., Knudsen T.B. Evaluation of 309 environmental chemicals using a mouse embryonic stem cell adherent cell differentiation and cytotoxicity assay. PLoS One 2011, 6:e18540.
9. Cheng S.H., Wai A.W.K., So C.H., Wu R.S.S. Cellular and molecular basis of cadmium-induced deformities in zebrafish embryos. Environ. Toxicol. Chem. 2000, 19:3024-3031.
10. Colleoni S., Galli C., Gaspar J.A., Meganathan K., Jagtap S., Hescheler J., Sachinidis A., Lazzari G. Development of a neural teratogenicity test based on human embryonic stem cells: response to retinoic acid exposure. Toxicol. Sci. 2011, 124:370-377.
11. de Jong E., Barenys M., Hermsen S.A., Verhoef A., Ossendorp B.C., Bessems J.G., Piersma A.H. Comparison of the mouse embryonic stem cell test, the rat whole embryo culture and the zebrafish embryotoxicity test as alternative methods for developmental toxicity testing of six 1,2,4-triazoles. Toxicol. Appl. Pharmacol. 2011, 253:103-111.
12. de Jong E., Doede´e A.M., Reis-Fernandes M.A., Nau H., Piersma A.H. Potency ranking of valproic acid analogues as to inhibition of cardiac differentiation of embryonic stem cells in comparison to their in vivo embryotoxicity. Reprod. Toxicol. 2011, 31:375-382.
13. de Jong E., Louisse J., Verwei M., Blaauboer B.J., van de Sandt J.J., Woutersen R.A., Rietjens I.M., Piersma A.H. Relative developmental toxicity of glycol ether alkoxy acid metabolites in the embryonic stem cell test as compared with the in vivo potency of their parent compounds. Toxicol. Sci. 2009, 110:117-124.
14. Di Guglielmo C., Lo´pez D.R., De Lapuente J., Mallafre J.M., Sua`rez M.B. Embryotoxicity of cobalt ferrite and gold nanoparticles: a first in vitro approach. Reprod. Toxicol. 2010, 30:271-276.
15. Duan J., Yu Y., Shi H., Tian L., Guo C., Huang P., Zhou X., Peng S., Sun Z. Toxic effects of silica nanoparticles on zebrafish embryos and larvae. PLoS One 2013, 8:e74606.
16. ESAC (European Centre for Validation of Alternative Methods (ECVAM) Scientific Advisory Committee) (2002), The Use of Scientifically-Validated In Vitro Tests for Embryotoxicity, Available in: http://ecvam.jrc.ec.europa.eu/.
17. Estevan C., Vilanova E., Sogorb M.A. Chlorpyrifos and its metabolites alter gene expression at non-cytotoxic concentrations in D3 mouse embryonic stem cells under in vitro differentiation: considerations for embryotoxic risk assessment. Toxicol. Lett. 2013, 217:14-22.
18. Estevan C., Pamies D., Sogorb M.A., Vilanova E. OECD guidelines and validated methods for in vivo testing of reproductive toxicity. Reproductive and Developmental Toxicology 2011, 123-133. Academic Press. R.G. Gupta (Ed.).
19. Festag M., Viertel B., Steinberg P., Sehner C. An in vitro embryotoxicity assay based on the disturbance of the differentiation of murine embryonic stem cells into endothelial cells. II. Testing of compounds. Toxicol in vitro. 2007, 21:1631-1640.
20. Flick B., Talsness C.E., Ja¨ckh R., Buesen R., Klug S. Embryotoxic potential of N-methyl-pyrrolidone (NMP) and three of its metabolites using the rat whole embryo culture system. Toxicol. Appl. Pharmacol. 2009, 237:154-167.
21. Genschow E., Spielmann H., Scholz G., Seiler A., Brown N., Piersma A., Brady M., Clemann N., Huuskonen H., Paillard F., Bremer S., Becker K. The ECVAM international validation study on in vitro embryotoxicity tests: results of the definitive phase and evaluation of prediction models, European centre for the validation of alternative methods. Alternative Laboratory Animal 2002, 30:151-176.
22. Gustafson A.L., Stedman D.B., Ball J., Hillegass J.M., Flood A., Zhang C.X., Panzica-Kelly J., Cao J., Coburn A., Enright B.P., Tornesi M.B., Hetheridge M., Augustine-Rauch K.A. Inter-laboratory assessment of a harmonized zebrafish developmental toxicology assay-progress report on phase I. Reprod. Toxicol. 2012, 33:155-164.
23. Hartung T., Hoffmann S., Stephens M. Mechanistic validation. ALTEX 2013, 30:119-130.
24. Hartung T., Luechtefeld T., Maertens A., Kleensang A. Integrated testing strategies for safety assessments. ALTEX 2013, 30:3-18.
25. Hermsen S.A., Pronk T.E., van den Brandhof E.J., van der Ven L.T., Piersma A.H. Transcriptomic analysis in the developing zebrafish embryo after compound exposure, individual gene expression and pathway regulation. Toxicol. Appl. Pharmacol. 2013, 272:161-171.
26. Hermsen S.A., Pronk T.E., van den Brandhof E.J., van der Ven L.T., Piersma A.H. Chemical class-specific gene expression changes in the zebrafish embryo after exposure to glycol ether alkoxy acids and 1,2,4-triazole antifungals. Reprod. Toxicol. 2011, 32:245-252.
27. Hoelting L., Scheinhardt B., Bondarenko O., Schildknecht S., Kapitza M., Tanavde V., Tan B., Lee Q.Y., Mecking S., Leist M., Kadereit S. A 3- dimensional human embryonic stem cell (hESC)-derived model to detect developmental neurotoxicity of nanoparticles. Arch. Toxicol. 2013, 87:721-733.
28. Hogberg H.T., Bressler J., Christian K.M., Harris G., Makri G., O'Driscoll C., Pamies D., Smirnova L., Wen Z., Hartung T. Toward a 3D model of human brain development for studying gene/environment interactions. Stem Cell Res. Ther. 2013, 4(Suppl 1N).
29. Hogberg H.T., Kinsner-Ovaskainen A., Coecke S., Hartung T., Bal-Price A.K. mRNA expression is a relevant tool to identify developmental neurotoxicants using an in vitro approach. Toxicol. Sci. 2010, 113:95-115.
30. Hogberg H.T., Kinsner-Ovaskainen A., Hartung T., Coecke S., Bal-Price A.K. Gene expression as a sensitive endpoint to evaluate cell differentiation and maturation of the developing central nervous system in primary cultures of rat cerebellar granule cells (CGCs) exposed to pesticides. Toxicol. Appl. Pharmacol. 2009, 235:268-286.
31. Kong D., Xing L., Liu R., Jiang J., Wang W., Shang L., Wei X., Hao W. Individual and combined developmental toxicity assessment of bisphenol A and genistein using the embryonic stem cell test in vitro. Food Chem. Toxicol. 2013, 60:497-505.
32. Lee K.J., Nallathamby P.D., Browning L.M., Osgood C.J., Xu X.H. In vivo imaging of transport and biocompatibility of single silver nanoparticles in early development of zebrafish embryos. ACS Nano 2007, 1:133-143.
33. Link V., Shevchenko A., Heisenberg C.P. Proteomics of early zebrafish embryos. BMC Dev. Biol. 2006, 6:1.
34. McGrath P., Li C.Q. Zebrafish: a predictive model for assessing drug-induced toxicity. Drug Discov. Today 2008, 13:394-401.
35. Minta M., Wilk I., Z˙mudzki J. Embryotoxicity of carbendazim in rat and hamster micromass cultures. Bull. Vet. Inst. Pulawy 2004, 48:481-484.
36. Moors M., Rockel T.D., Abel J., Cline J.E., Gassmann K., Schreiber T., Schuwald J., Weinmann N., Fritsche E. Human neurospheres as three-dimensional cellular systems for developmental neurotoxicity testing. Environ. Health Perspect. 2009, 117:1131-1138. Erratum in: Environmental Health Perspectives. 2009. 117:A342.
37. Neri T., Merico V., Fiordaliso F., Salio M., Rebuzzini P., Sacchi L., Bellazzi R., Redi C.A., Zuccotti M., Garagna S. The differentiation of cardiomyocytes from mouse embryonic stem cells is altered by dioxin. Toxicol. Lett. 2011, 202:226-236.
38. Organisation for Economic Co-operation and Development, 2013. Test No. 236: Fish Embryo Acute Toxicity (FET) Test. Available in: http://www.oecd-ilibrary.org/docserver/download/9713161e.pdf%3Fexpires=1380448247%26id=id%26accname=guest%26checksum=C0A2EF8CA2BBE64DC412FE1FD9D100EC.
39. Osman A.M., van Dartel D.A., Zwart E., Blokland M., Pennings J.L., Piersma A.H. Proteome profiling of mouse embryonic stem cells to define markers for cell differentiation and embryotoxicity. Reprod. Toxicol. 2010, 30:322-332.
40. Pamies D., Estevan C., Sogorb M.A., Vilanova E. Mechanism-based models in reproductive and developmental toxicology. Reproductive and Developmental Toxicology 2011, 135-216. Academic Press. R.G. Gupta (Ed.).
41. Panzica-Kelly J.M., Brannen K.C., Ma Y., Zhang C.X., Flint O.P., Lehman-McKeeman L.D., Augustine-Rauch K.A. Establishment of a molecular embryonic stem cell developmental toxicity assay. Toxicol. Sci. 2013, 131:447-457.
42. Pennings J.L., Theunissen P.T., Piersma A.H. An optimized gene set for transcriptomics based neurodevelopmental toxicity prediction in the neural embryonic stem cell test. Toxicology 2012, 300:158-167.
43. Piersma A.H., Bosgra S., van Duursen M.B., Hermsen S.A., Jonker L.R., Kroese E.D., van der Linden S.C., Man H., Roelofs M.J., Schulpen S.H., Schwarz M., Uibel F., van Vugt-Lussenburg B.M., Westerhout J., Wolterbeek A.P., van der Burg B. Evaluation of an alternative in vitro test battery for detecting reproductive toxicants. Reprod. Toxicol. 2013, 38:53-64.
44. Riebeling C., Pirow R., Becker K., Buesen R., Eikel D., Kaltenha¨user J., Meyer F., Nau H., Slawik B., Visan A., Volland J., Spielmann H., Luch A., Seiler A. The embryonic stem cell test as tool to assess structure-dependent teratogenicity: the case of valproic acid. Toxicol. Sci. 2011, 120:360-370.
45. Robinson J.F., Tonk E.C., Verhoef A., Piersma A.H. Triazole induced concentration-related gene signatures in rat whole embryo culture. Reprod. Toxicol. 2012, 34:275-283.
46. Robinson J.F., Verhoef A., van Beelen V.A., Pennings J.L., Piersma A.H. Dose-response analysis of phthalate effects on gene expression in rat whole embryo culture. Toxicol. Appl. Pharmacol. 2012, 264:32-41.
47. Robinson J.F., van Beelen V.A., Verhoef A., Renkens M.F., Luijten M., van Herwijnen M.H., Westerman A., Pennings J.L., Piersma A.H. Embryotoxicant-specific transcriptomic responses in rat postimplantation whole-embryo culture. Toxicol. Sci. 2010, 118:675-685. Erratum in: Toxicological Sciences. 2011. 120:529.
48. Romero A.C., Vilanova E., Sogorb M.A. Shortening and improving the embryonic stem cell test through the use of gene biomarkers of differentiation. J. Toxicol. 2011, 286034.
49. Rovida C., Hartung T. Re-evaluation of animal numbers and costs for in vivo tests to accomplish REACH legislation requirements for chemicals: a report by the transatlantic think tank for toxicology (t(4)). ALTEX 2009, 26:187-208.
50. Russell W.M.S., Burch R.L. The Principles of Humane Experimental Technique 1959, Methuen & Co. Ltd, London.
51. Scholz S., Renner P., Belanger S.E., Busquet F., Davi R., Demeneix B.A., Denny J.S., Le´onard M., McMaster M.E., Villeneuve D.L., Embry M.R. Alternatives to in vivo tests to detect endocrine disrupting chemicals (EDCs) in fish and amphibians-screening for estrogen androgen and thyroid hormone disruption. Crit. Rev. Toxicol. 2013, 43:45-72.
52. Scholz S., Fischer S., Gu¨ndel U., Ku¨ster E., Luckenbach T., Voelker D. The zebrafish embryo model in environmental risk assessment-applications beyond acute toxicity testing. Environ. Sci. Pollut. Res. Int. 2008, 15:394-404.
53. 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, 18:231-240.
54. Spielmann H., Seiler A., Bremer S., Hareng L., Hartung T., Ahr H., Faustman E., Haas U., Moffat G.J., Nau H., Vanparys P., Piersma A., Sintes J.R., Stuart J. The practical application of three validated in vitro embryotoxicity tests. The report and recommendations of an ECVAM/ZEBET workshop (ECVAM workshop 57). Altern. Lab. Anim. 2006, 34:527-538.
55. Spitsbergen J.M., Kent M.L. The state of the art of the zebrafish model for toxicology and toxicologic pathology research-advantages and current limitations. Toxicol. Pathol. 2003, 31:62-87.
56. Stra¨hle U., Scholz S., Geisler R., Greiner P., Hollert H., Rastegar S., Schumacher A., Selderslaghs I., Weiss C., Witters H., Braunbeck T. Zebrafish embryos as an alternative to animal experiments-a commentary on the definition of the onset of protected life stages in animal welfare regulations. Reprod. Toxicol. 2012, 33:128-132.
57. Strikwold M., Woutersen R.A., Spenkelink B., Punt A., Rietjens I.M. Relative embryotoxic potency of p-substituted phenols in the embryonic stem cell test (EST) and comparison to their toxic potency in vivo and in the whole embryo culture (WEC) assay. Toxicol. Lett. 2012, 213:235-242.
58. Suzuki N., Ando S., Yamashita N., Horie N., Saito K. Evaluation of novel high-throughput embryonic stem cell tests with new molecular markers for screening embryotoxic chemicals in vitro. Toxicol. Sci. 2011, 124:460-471.
59. Suzuki N., Yamashita N., Koseki N., Yamada T., Kimura Y., Aiba S., Toyoizumi T., Watanabe M., Ohta R., Tanaka N., Saito K. Assessment of technical protocols for novel embryonic stem cell tests with molecular markers (Hand1- and Cmya1-ESTs): a preliminary cross-laboratory performance analysis. J. Toxicol. Sci. 2012, 37:845-851.
60. Teixido´ E., Pique´ E., Go´mez-Catala´n J., Llobet J.M. Assessment of developmental delay in the zebrafish embryo teratogenicity assay. Toxicol In Vitro. 2013, 27:469-478.
61. Theunissen P.T., Pennings J.L., van Dartel D.A., Robinson J.F., Kleinjans J.C., Piersma A.H. Complementary detection of embryotoxic properties of substances in the neural and cardiac embryonic stem cell tests. Toxicol. Sci. 2013, 132:118-130.
62. Theunissen P.T., Robinson J.F., Pennings J.L., de Jong E., Claessen S.M., Kleinjans J.C., Piersma A.H. Transcriptomic concentration-response evaluation of valproic acid, cyproconazole, and hexaconazole in the neural embryonic stem cell test (ESTn). Toxicol. Sci. 2012, 125:430-438.
63. Theunissen P.T., Robinson J.F., Pennings J.L., van Herwijnen M.H., Kleinjans J.C., Piersma A.H. Compound-specific effects of diverse neurodevelopmental toxicants on global gene expression in the neural embryonic stem cell test (ESTn). Toxicol. Appl. Pharmacol. 2012, 262:240-330.
64. Theunissen P.T., Schulpen S.H., van Dartel D.A., Hermsen S.A., van Schooten F.J., Piersma A.H. An abbreviated protocol for multilineage neural differentiation of murine embryonic stem cells and its perturbation by methyl mercury. Reprod. Toxicol. 2010, 29:383-392.
65. van Dartel D.A., Pennings J.L., de la Fonteyne L.J., Brauers K.J., Claessen S., van Delft J.H., Kleinjans J.C., Piersma A.H. Evaluation of developmental toxicant identification using gene expression profiling in embryonic stem cell differentiation cultures. Toxicol. Sci. 2011, 119:126-134.
66. van Dartel D.A., Pennings J.L., Robinson J.F., Kleinjans J.C., Piersma A.H. Discriminating classes of developmental toxicants using gene expression profiling in the embryonic stem cell test. Toxicol. Lett. 2011, 201:143-151.
67. van Dartel D.A., Pennings J.L., de la Fonteyne L.J., van Herwijnen M.H., van Delft J.H., van Schooten F.J., Piersma A.H. Monitoring developmental toxicity in the embryonic stem cell test using differential gene expression of differentiation-related genes. Toxicol. Sci. 2010, 116:130-139.
68. van Dartel D.A., Pennings J.L., van Schooten F.J., Piersma A.H. Transcriptomics-based identification of developmental toxicants through their interference with cardiomyocyte differentiation of embryonic stem cells. Toxicol. Appl. Pharmacol. 2010, 243:420-428.
69. van Dartel D.A., Pennings J.L., Hendriksen P.J., van Schooten F.J., Piersma A.H. Early gene expression changes during embryonic stem cell differentiation intocardiomyocytes and their modulation by monobutyl phthalate. Reprod. Toxicol. 2009, 27:93-102.
70. van den Bulck K., Hill A., Mesens N., Diekman H., De Schaepdrijver L., Lammens L. Zebrafish developmental toxicity assay: a fishy solution to reproductive toxicity screening, or just a red herring?. Reprod. Toxicol. 2011, 32:213-219.
71. Wang Y., Fan Y., Puga A. Dioxin exposure disrupts the differentiation of mouse embryonic stem cells into cardiomyocytes. Toxicol. Sci. 2010, 115:225-237.
72. Xu B., Lee K.K., Zhang L., Gerton J.L. Stimulation of mTORC1 with l-leucine rescues defects associated with Roberts syndrome. PLoS Genet. 2013, 9:e1003857.
73. Yang L., Ho N.Y., Alshut R., Legradi J., Weiss C., Reischl M., Mikut R., Liebel U., Mu¨ller F., Stra¨hle U. Zebrafish embryos as models for embryotoxic and teratological effects of chemicals. Reprod. Toxicol. 2009, 28:245-253.
74. Yang L., Kemadjou J.R., Zinsmeister C., Bauer M., Legradi J., Mu¨ller F., Pankratz M., Ja¨kel J., Stra¨hle U. Transcriptional profiling reveals barcode-like toxicogenomic responses in the zebrafish embryo. Genome Biol. 2007, 8:R227.
75. Zhang C., Cao J., Kenyon J.R., Panzica-Kelly J.M., Gong L., Augustine-Rauch K. Development of a streamlined rat whole embryo culture assay for classifying teratogenic potential of pharmaceutical compounds. Toxicol. Sci. 2012, 127:535-546.