A high throughput screening system for predicting chemically-induced reproductive organ deformities

Reproductive Toxicology

Volumn 55, Issue , 2015, Pages 95-103

  van der Burg, Bart ^a   Pieterse, Bart ^a   Buist, Harrie ^d   Lewin, Geertje ^c   van der Linden, Sander C ^a   Man, Hai yen ^a   Rorije, Emiel ^b   Piersma, Aldert H ^b   Mangelsdorf, Inge ^c   Wolterbeek, Andre P M ^d   Kroese, E Dinant ^d   van Vugt Lussenburg, Barbara ^a  

^a BIODETECTION SYSTEMS B V   (Netherlands)

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

^c FRAUNHOFER INSTITUTE FOR TOXICOLOGY AND EXPERIMENTAL MEDICINE   (Germany)

^d TNO   (Netherlands)

Author keywords

Estrogen androgen reporter gene assay; High throughput screening; Mechanistic validation; Reproductive organ deformities

Indexed keywords

2 ETHYLHEXANOIC ACID; 2 METHOXYETHANOL; 2,4 DEXTRO ISOPROPYLAMINE SALT; 2,4 PYRIMETHAMINE; ACETYLSALICYLIC ACID; ANDROGEN RECEPTOR; BENOMYL; BIS(TRICHLOROMETHYL)SULFONE; CARBAMAZEPINE; CARBENDAZIM; CELLOSOLVE ACETATE; CYANAZINE; CYPROCONAZOLE; DI(N HEXYL)PHTHALATE; DIBUTYLTINDICHLORIDE; DIGLYME; FENACHLORAZOL ETHYL; GLYCOLIC ACID; HALOSULFURON METHYL; MANCOZEB; MOLINATE; PENTACHLOROPHENOL; PHTHALIC ACID BENZYL BUTYL ESTER; PROTHIOCONAZOLE; TOXIC SUBSTANCE; TRICLOPYR; UNCLASSIFIED DRUG; ANDROGEN RECEPTOR ANTAGONIST; ESTROGEN; ESTROGEN RECEPTOR ALPHA; TERATOGENIC AGENT;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ESTROGEN ACTIVITY; GENITAL MALFORMATION; HIGH THROUGHPUT SCREENING; NONHUMAN; PREDICTION; RAT; REPORTER GENE; REPRODUCTIVE TOXICITY; TOXICITY TESTING; CELL LINE; CHEMICALLY INDUCED; DRUG EFFECTS; GENITAL SYSTEM; HUMAN; METABOLISM; NEURAL TUBE DEFECT;

ANDROGEN RECEPTOR ANTAGONISTS; CELL LINE; ESTROGEN RECEPTOR ALPHA; ESTROGENS; GENITALIA; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; NEURAL TUBE DEFECTS; RECEPTORS, ANDROGEN; TERATOGENS;

EID: 84939416184     PISSN: 08906238     EISSN: 18731708     Source Type: Journal    
DOI: 10.1016/j.reprotox.2014.11.011     Document Type: Article

References (74)

1. Toxicity testing in the twenty-first century: a vision and a strategy. Committee on Toxicity and Assessment of Environmental Agents 2007, National Research Council (USA).
2. Costanza R., 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. ALTEX 2009, 26:187-208.
3. Schenk B., Weimer M., Bremer S., van der Burg B., Cortvrindt R., Freyberger A., et al. The ReProTect Feasibility Study, a novel comprehensive in vitro approach to detect reproductive toxicants. Reprod Toxicol 2010, 30:200-218.
4. Sipes N.S., Martin M.T., Reif D.M., Kleinstreuer N.C., Judson R.S., Singh A.V., et al. Predictive models of prenatal developmental toxicity from ToxCast high throughput screening data. Toxicol Sci 2011 Nov, 124(1):109-127.
5. Ankley G.T., Bennett R.S., Erickson R.J., Hoff D.J., Hornung M.W., Johnson R.D., et al. Adverse outcome pathways: a conceptual framework to support ecotoxicology research and risk assessment. Environ Toxicol Chem 2010, 29(3):730-741.
6. Van der Burg B., Winter R., Man H.-y., Vangenechten C., Weimer M., Berckmans P., et al. Optimization and prevalidation of the in vitro AR CALUX method to test androgenic and antiandrogenic activity of compounds. Reprod Toxicol 2010, 30:18-24.
7. Van der Burg B., Winter R., Weimer M., Berckmans P., Suzuki G., Gijsbers L., et al. Optimization and prevalidation of the in vitro ERα CALUX method to test estrogenic and antiestrogenic activity of compounds. Reprod Toxicol 2010, 30:73-80.
8. OECD SPSF by the European Commission: performance-based test guideline on androgen receptor transactivation assays (AR CALUX) 2013.
9. OECD SPSF by the Netherlands: U2-OS cells Transcriptional ERalpha CALUX®-assay for the detection of estrogenic and antiestrogenic chemicals for inclusion in TG455/TG457 2013.
10. Sonneveld E., Jansen H.J., Riteco J.A.C., Brouwer A., Van der Burg B. Development of androgen- and estrogen-responsive bioassays, members of a panel of human cell line-based highly selective steroid responsive bioassays. Toxicol Sci 2005, 83:136-148.
11. ® reporter gene assays for reliable high throughput toxicity screening of chemicals and complex mixtures. High throughput screening methods in toxicity testing 2013, 519-532. John Wiley and Sons, Inc., New York. P. Steinberg (Ed.).
12. Dix D.J., Houck K.A., Martin M.T., Richard A.M., Setzer R.W., Kavlock R.J. The ToxCast program for prioritizing toxicity testing of environmental chemicals. Toxicol Sci 2007, 95(January (1)):5-12.
13. Piersma A.H., Schulpen S.H.W., Uibel F., Van Vugt-Lussenburg B., Bosgra S., Hermsen S.A.B., et al. Evaluation of an alternative in vitro test battery for detecting reproductive toxicants. Reprod Toxicol 2013, 38:53-64.
14. Sonneveld E., Pieterse B., Schoonen W., Van der Burg B. Validation of in vitro screening models for progestagenic activities: inter-assay comparison and correlation with in vivo activity in rabbits. Toxicol In Vitro 2011, 25:545-554.
15. Sonneveld E., Riteco J.A.C., Jansen H.J., Pieterse B., Brouwer A., Schoonen W.G., et al. Comparison of in vitro and in vivo screening models for androgenic and estrogenic activities. Toxicol Sci 2006, 89:173-187.
16. Leist M., Hasiwa N., Rovida C., Daneshian M., Basketter D., Kimber I., et al. Consensus report on the future of animal-free systemic toxicity testing. ALTEX 2014, 31(3):341-356.
17. Willoughby C.R., Tesh J.M., Pritchard A.L., et al. Fluazifop butyl: effects upon reproductive performance of rats treated continuously throughout two generations: Lsr report no. 81/Ily282/130. Final rept. 1981, [Unpublished study received December 4].
18. Gupta U., Cook J.C., Tassinari M.S., Hurtt M.E. Comparison of developmental toxicology of aspirin (acetylsalicylic acid) in rats using selected dosing paradigms. Birth Defects Res B Dev Reprod Toxicol 2003, 68(1):27-37.
19. Saillenfait A.M1, Gallissot F., Sabaté J.P. Differential developmental toxicities of di-n-hexyl phthalate and dicyclohexyl phthalate administered orally to rats. J Appl Toxicol 2009, 29(6):510-521.
20. Borch J., Axelstad M., Vinggaard A.M., Dalgaard M. Diisobutyl phthalate has comparable anti-androgenic effects to di-n-butyl phthalate in fetal rat testis. Toxicol Lett 2006, 163:183-190.
21. Matsuura I., Saitoh T., Ashina M., Wako Y., Iwata H., Toyota N., et al. Evaluation of a two-generation reproduction toxicity study adding endpoints to detect endocrine disrupting activity using vinclozolin. J Toxicol Sci 2005, 30(December (Spec No.)):163-188.
22. Yamasaki K., Okuda H., Takeuchi T., Minobe Y. Effects of in utero through lactational exposure to dicyclohexyl phthalate and p,p'-DDE in Sprague-Dawley rats. Toxicol Lett 2009, 189(1):14-20.
23. Yamamoto M., Shirai M., Tamura A., Kobayashi T., Kohara S., Murakami M., et al. Effects of maternal exposure to a low dose of diethylstilbestrol on sexual dimorphic nucleus volume and male reproductive system in rat offspring. J Toxicol Sci 2005, 30(February (1)):7-18.
24. Nagao T., Wada K., Marumo H., Yoshimura S., Ono H. Reproductive effects of nonylphenol in rats after gavage administration: a two-generation study. Reprod Toxicol 2001, 15(May-June (3)):293-315.
25. Kam C, Stevens KR, Gallo MA. Teratologic evaluation of dithane M-45 in the Albino Rat: vol. I: Snell project # 10065-009 [Unpublished study, including letter dated December 4, 1979 from W.T. Lynch to Kent Stevens, 1980].
26. Stump D. A dietary two-generation reproductive toxicity study of sulfluramid in rats: final report: lab project number: WIL-157012: GP 95-051 1997, WIL Research Labs, Inc., 2591 pp. {OPPTS 870.3800}.
27. Aso S., Ehara H., Miyata K., Hosyuyama S., Shiraishi K., Umano T., et al. A two-generation reproductive toxicity study of butyl benzyl phthalate in rats. J Toxicol Sci 2005, 30(December (Spec No.)):39-58.
28. Christian M.S., York R.G., Hoberman A.M., Frazee J., Fisher L.C., Brown W.R., et al. Oral (drinking water) two-generation reproductive toxicity study of dibromoacetic acid (DBA) in rats. Int J Toxicol 2002, 21(July-August (4)):237-276.
29. Bernard B.K., Hoberman A.M., Brown W.R., Ranpuria A.K., Christian M.S. Oral (gavage) two-generation (one litter per generation) reproduction study of pentachlorophenol (penta) in rats. Int J Toxicol 2002, 21(July-August (4)):301-318.
30. Edwards J., Reid Y., Offer J., et al. Effect of endosulfan - technical on reproductive function of multiple generations of the rat: report no. HST 204/83768 1984, Huntingdon Research Centre plc., 422 pp.
31. Tyl R.W., Myers C.B., Marr M.C., Thomas B.F., Keimowitz A.R., Brine D.R., et al. Three-generation reproductive toxicity study of dietary bisphenol A in CD Sprague-Dawley Rats. Toxicol Sci 2002, 68:121-146.
32. Omura M., Ogata R., Kubo K., Shimasaki Y., Aou S., Oshima Y., et al. Two-generation reproductive toxicity study of tributyltin chrloide in male rats. Toxicol Sci 2001, 64:224-232.
33. Schroeder R. A teratogenicity study in rats with 2,4-d-tri-isopropanolamine: lab project number: HET K0008866-012: 89-3463 1990, Bio/Dynamics, Inc., 478 pp.
34. Chung M.K., Han S.S., Roh J.K. Synergistic embryotoxicity of combination pyrimethamine and folic acid in rats. Reprod Toxicol 1993, 7(September-October (5)):463-468.
35. Pennanen S., Tuovinen K., Huuskonen H., Komulainen H. The developmental toxicity of 2-ethylhexanoic acid in Wistar rats. Fundam Appl Toxicol 1992, 19(November (4)):505-511.
36. Nelson B.K., Setzer J.V., Brightwell W.S., Mathinos P.R., Kuczuk M.H., Weaver T.E., et al. Comparative inhalation teratogenicity of four glycol ether solvents and an amino derivative in rats. Environ Health Perspect 1984, August (57):261-271.
37. Du Pont de Nemours & Co., Inc. Supplement to the benomyl gavage teratogenicity study in the rat (HLR No. 649-80) 1985, 106 pp. [Unpublished compilation].
38. Nemec M.D. A teratology study in rats with N-1386 biocide technical 1987, WIL Research Laboratories Inc., [Study No: WIL-27038; MRID 40149101].
39. Piersma A.H., Verhoef A., te Biesebeck J.D., Pieters M., Slob W. Developmental toxicity of butyl benzyl phthalate in the rat using a multiple dose study design. Reprod Toxicol 2000, 14:417-425.
40. Gerenutti M., Clavijos de Oliviera C., Ribeiro de Miranda A.C., Mendoca Rosa R., de Sa Del Fiol F. Reproductive performance and embryotoxicity of rats exposed to carbamazepine. Rev Bras Cienc Farmaceut 2008, 44(3):509-514.
41. Alvarez L. Teratogenicity study of INE-965 in rats: lab. proj. ID 281-87 1987, Dupont Haskell Laboratory, 195 pp.
42. Tyl R.W., Pritts I.M., France K.A., Fisher L.C., Tyler T.R. Developmental toxicity evaluation of inhaled 2-ethoxyethanol acetate in Fischer 344 rats and New Zealand white rabbits. Fundam Appl Toxicol 1988, 10(January (1)):20-39.
43. Dix K., Cassidy S., Daniel D., et al. Teratology study in New Zealand white rabbits given bladex orally: SBGR.82.357 1982, Shell Research Ltd., Eng., submitted by Shell Chemical Co., [Unpublished study received February 1, 1983 under 201-279].
44. Klotzche C. Teratogenicity study in rats with SAN 619F: including dose finding teratogenicity study: project no. 04712 and 048701 1985, Research and Consulting Co., 215 pp.
45. Ema M., Kurosaka R., Amano H., Ogawa Y. Comparative developmental toxicity of butyltin trichloride, dibutyltin dichloride and tributyltin chloride in rats. J Appl Toxicol 1995, 15(4):297-302.
46. Driscoll C.D., Valentine R., Staples R.E., Chromey N.C., Kennedy G.L. Developmental toxicity of diglyme by inhalation in the rat. Drug Chem Toxicol 1998, 21(May (2)):119-136.
47. Baeder C., Mayer D., Langer K.H. HOE 070542 - substance technical (Code: Hoe 070542 OZ ZC99 0001) testing for embryotoxicity in the Wistar rat after oral administration Hoechst AG 6230 Frankfurt (M) 80, Fed. Repub. Germany 1986, MRID 40266213.
48. Du Pont de Nemours and Company (H-28746) 70% glycolic acid technical solution: developmental toxicity study in rats_Project ID: DuPont-18011-841 2009.
49. Morseth S. Rat teratology study with Nc-319 part A: dose finding study for teratology study in rats with Nc-319 technical part B: lab project number: Hl-89-318: Hla 2096-141: Rd 1061 1990, Hazleton Labs, Inc., 457 pp.
50. Booz, Allen and Hamilton, Inc. Teratologic evaluation of dithane m-45 in the albino rat, snell project #10065-009 1982, Rohm and Haas Company, Accession #246663.
51. Minor J. A teratology study in CD rats with R-4572 technical T-13266: lab project number: T-13266 1990, Ciba-Geigy Environmental Health Ctr., 236 pp.
52. Hoberman A. Developmental toxicity (embryo-fetal toxicity and teratogenic potential) study of pentachlorophenol administered orally via stomach tube to new zealand white rabbits: final report: lab project number: 2119-002 1994, [Unpublished study].
53. ToxRefDB Study_ID 4080: No citation.
54. Thompson D.J., Dyke I.L., Lower C.E., et al. Results of a teratology study on dowco 233 (3,5,6-trichloro-2-pyridyloxy) acetic acid in the rat 1979, [Unpublished study received May 1, 1981 under 464-554; submitted by Dow Chemical U.S.A.].
55. Garrison P.M., Tullis K., Aarts J.M.M.J.G., Brouwer A., Giesy J.P., Denison M.S. Fund. Appl Toxicol 1996, 30:194-203.
56. Gauggel S., Derreza-Greven C., Wimmer J., Wingfield M., Van der Burg B., Dietrich D.R. Characterization of biologically available wood combustion particles in cell culture medium. ALTEX 2012, 29(2):183-200.
57. Pieterse B., Felzel E., Winter R., van der Burg B., Brouwer A. PAH-CALUX, an optimized bioassay for carcinogenic hazard identification of polycyclic aromatic hydrocarbons (PAHs) as individual compounds and in complex mixtures. Environ Sci Technol 2013, 47:11651-11659.
58. Gijsbers L. In vitro reporter gene assays for assessment of PPAR- and Nrf2-mediated health effects of tomato and its bioactive constituents 1993, (Thesis), Wageningen University and Research Centre, ISBN 9789461735096.
59. Gijsbers L., van Eekelen H., de Haan L.H., Swier J.M., Heijnk N.L., Kloet S.K., et al. Induction of peroxisome proliferator-activated receptorα (PPARα)-mediated gene expression by tomato (Solanum lycopersicum L.) extracts. J Agric Food Chem 2013, 61:3419-3427.
60. Van der Linden S.C., von Bergh A.R.M., Van Vugt-Lussenburg B., Jonker L., Brouwer A., Teunis M., et al. Development of a panel of high throughput reporter gene assays to detect genotoxicity and oxidative stress. Mutat Res-Genet Toxicol Environ Mutagen 2013, 760:23-32.
61. Test guideline no. 455. Stably transfected human estrogen receptor-transcriptional activation assay for detection of estrogenic agonist-activity of chemicals 2009, OECD, Organisation for Economic Cooperation and Development, Paris.
62. Zhang J.H., Chung T.D., Oldenburg K.R. A simple statistical parameter for use in evaluation and validation of high throughput screening assays. J Biomol Screen 1999, 4(2):67-73.
63. Houtman C.J., Sterk S.S., Van de Heijning M.P., Brouwer A., Stephany R.W., Van der Burg B., et al. Detection of anabolic androgenic steroid abuse in doping control using in vitro reporter gene bioassays. Anal Chim Acta 2009, 637:247-258.
64. Beato M. Gene regulation by steroid hormones. Cell 1989, 56(February (3)):335-344.
65. Ojasoo T., Raynaud J.P., Doré J.C. Correspondence factor analysis of steroid libraries. Steroids 1995, 60(June (6)):458-469.
66. Sohoni P., Sumpter J.P. Several environmental oestrogens are also anti-androgens. J Endocrinol 1998, 158(September (3)):327-339.
67. Uibel F., Schwarz M. Prediction of embryotoxic potential using the ReProGlo stem cell-based Wnt reporter assay. Reprod Toxicol 2015, 55:30-49.
68. Verkaar F., van der Stelt M., Blankesteijn W.M., van der Doelen A.A., Zaman G.J. Discovery of novel small molecule activators of β-catenin signaling. PLoS ONE 2011, 6(April (4)):e19185.
69. Carr T.L., Ciurlionis R., Milicic I., Whitney K., Liguori M.J., Warder S.E., et al. Role of cytochrome P450c17α in dibromoacetic acid-induced testicular toxicity in rats. Arch Toxicol 2011, 85(May (5)):513-523.
70. Kuiper G.J.M., Lemmen J.G., Carlsson B., Corton J.C., Safe S.H., Van der Saag P.T., et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor. Endocrinology 1998, 139:4252-4426.
71. Lewin G., Escher S.E., Van der Burg B., Simetska N., Mangelsdorf I. Structural features of endocrine active chemicals - A comparison of in vivo and in vitro data. Reprod Toxicol 2015, 55:81-94.
72. Legler J., Dennekamp M., Vethaak A.D., Brouwer A., Koeman J.H., Van der Burg B., et al. Detection of estrogenic activity in sediment-associated compounds using in vitro reporter gene assays. Sci Total Environ 2002, 293:69-83.
73. Soprano D.R., Soprano K.J. Retinoids as teratogens. Annu Rev Nutr 1995, 15:111-132.
74. Wu S., Fisher J., Nacliff J., Laufersweiler M., Lester C., Daston G., et al. Framework for identifying chemicals with structural features associated with the potential to act as developmental or reproductive toxicants. Chem Res Toxicol 2013, 26:1840-1861.