Developmental toxicity testing from animal towards embryonic stem cells

Altex

Volumn 22, Issue 2, 2005, Pages 47-57

  Pellizzer, Cristian ^a   Bremer, Susanne ^a   Hartung, Thomas ^a  

^a JOINT RESEARCH CENTRE   (Italy)

Author keywords

Alternatives to animals experiments; Developmental toxicity; Embryonic stem cells; Growth retardation; Malformations; Teratogenicity

Indexed keywords

2 ETHOXYETHANOL; ACETYLSALICYLIC ACID; ALCOHOL; ALKALINE PHOSPHATASE BONE ISOENZYME; ALPHA FETOPROTEIN; AMINOPTERIN; ANTINEOPLASTIC AGENT; BONE MORPHOGENETIC PROTEIN 4; COLCHICINE; COLLAGEN TYPE 2; HEPATOCYTE NUCLEAR FACTOR 4; HYDROXYUREA; LITHIUM; METHYLMERCURY; MYOSIN HEAVY CHAIN; MYOSIN LIGHT CHAIN; NERVE CELL ADHESION MOLECULE; NESTIN; NEUROFILAMENT PROTEIN; OCTAMER TRANSCRIPTION FACTOR 4; OSTEOCALCIN; RETINOID; TELOMERASE REVERSE TRANSCRIPTASE; THALIDOMIDE; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR GATA 4; TRANSCRIPTION FACTOR PAX6; TRANSCRIPTION FACTOR RUNX2; TRANSCRIPTION FACTOR SOX9; TRIMETHADIONE;

CONCEPTION; DOG; EMBRYO; EMBRYONIC STEM CELL; EMBRYOTOXICITY; EUROPE; EXPERIMENTAL MODEL; FERRET; FETUS; FETUS MALFORMATION; FUNCTIONAL DISEASE; GENETIC ANALYSIS; GROWTH RETARDATION; GUINEA PIG; HAMSTER; HEALTH CARE ORGANIZATION; HUMAN; IN VITRO STUDY; INTRAUTERINE GROWTH RETARDATION; LETHALITY; MARKETING; MEDICAL ASSESSMENT; MEDICAL ETHICS; MOUSE; NONHUMAN; POLICY; POSTNATAL DEVELOPMENT; PRENATAL DEVELOPMENT; PRENATAL EXPOSURE; PRIMATE; RABBIT; REPRODUCTIVE TOXICITY; RESEARCH ETHICS; REVIEW; SEXUAL MATURATION; SPECIES DIFFERENCE; SPONTANEOUS ABORTION; SWINE; TERATOGENICITY; TIME; TOXICITY TESTING; TOXICOLOGY; WORKSHOP;

ABNORMALITIES; ANIMAL TESTING ALTERNATIVES; ANIMALS; CELL DIVISION; EMBRYO; STEM CELLS; TOXICOLOGY;

EID: 22144457070     PISSN: 09467785     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Review

References (101)

1. Abe, K., Niwa, H., Iwase, K. et al. (1996). Endoderm-specific gene expression in embryonic stem cells differentiated to embryoid bodies. Exp. Cell. Res. 229, 27-34.
2. Anon (2005). The Fourth report on the statistics on the number of animals used for experimental and other scientific purposes in the Member States of the European Union. http://www.ncanl.org/English/Docs/EU%20stats.pdf (access 01/2005).
3. Anon (2003a). IP/03/969, Brussels, 9 July 2003. European Commission proposes strict ethical guidelines on EU funding of human embryonic stem cell research. http://europa.eu.int/rapid/pressReleasesAction.do?reference=IP/03/ 969&format=HTML&age d=0&Language=N&guiLanguage=en (access 01/2005).
4. Anon (2003b). EUROPEAN COMMISSION Directorate General: RESEARCH. Survey on opinions from National Ethics Committees or similar bodies, public debate and national legislation in relation to human embryonic stem cell research and use. Volume I in EU Member States. europa.eu.int/comm/research/biosociety/pdf /catalogue§emļls.pdf (access 01/2005).
5. Anon (2001a). White Paper on a Strategy for a Future Chemicals Policy. Brussels: Commission of the European Communities. http://europa.eu.int/comm/enviroment/chemicals/whitepaper.htm (accessed 6/2003).
6. Anon (2001b). OECD Guidelines for testing of chemicals, Guideline 414: Prenatal developmental toxicity study. http://www.sourceoecd.org/content/templates/co/co_main_oecdguid.htm? comm=oecdguid (accessed 30/2003).
7. Anon (2001c). OECD guideline for testing of chemicals 416: two-generation reproduction toxicity study. Update guideline, adopted 22nd January 2001.
8. Anon (2001d). OECD Guidelines for testing of chemicals, Guideline 421: Two-generation reproduction toxicity study. Updated guideline, adopted 22nd January 2001.
9. Anon (2001e). European Science Foundation Policy Briefing. Human stem cell research: scientific uncertainties and ethical dilemmas. www.esf.org/medias/ESPB14.pdf (access 01/2005).
10. Anon (2000). Frog Embryo Teratogenesis Assay-Xenopus (FETAX). http://iccvam.niehs.nih.gov/methods/fetax.htm.
11. Anon (1996). OECD Guidelines for testing of chemicals, Guideline 422: Combined repeated dose toxicity study with the reproduction/developmental toxicity screening test Original Guideline, adopted 22nd March 1996.
12. Anon (1983). OECD Guidelines for testing of chemicals, Guideline 415: One-generation reproduction toxicity study. Original Guideline, adopted 26th May 1983.
13. Asou, Y., Nifuji, A., Tsuji, K. et al. (2002). Coordinated expression of scleraxis and Sox9 genes during embryonic development of tendons and cartilage. J. Orthop. Res. 20, 827-833.
14. Assady, S., Maor, G., Amit, M. et al. (2001). Insulin production by human embryonic stem cells. Diabetes 50, 1691-1697.
15. Bain, G., Kitchens, D., Yao, M. et al. (1995). Embryonic stem cells express neuronal properties in vitro. Dev. Biol. 168, 342-357.
16. Bigot, K., de Lange, J., Archer, G. et al. (1999). The relative semi-quantitative expression as useful toxicological endpoint for identification of embryotoxic-teratogenic substances. Toxicol. In Vitro 13, 619-623.
17. Boheler, K. R., Czyz, J., Tweedie, D. et al. (2002). Differentiation of pluripotent embryonic stem cells into cardiomyocytes. Circ. Res. 91, 189-201.
18. Bremer, S. and Hartung, T. (2004). The use of embryonic stem cells for the regulatory developmental toxicity testing in vitro - The current status of test development. Curr Pharm. Des. 10, 2733-2747.
19. Bremer, S., Worth, A. P., Paparella, M. et al. (2001). Establishment of an in vitro reporter gene assay for developmental cardiac toxicity. Toxicol. In Vitro 15, 215-223.
20. Brent, R. L. and Beckman, D. A. (1990). Environmental teratogens. Bull. N Y Acad. Med. 66, 123-163.
21. Brown, N. A., Spielmann, H., Bechter, R. et al. (1995). Screening Chemicals for Reproductive Toxicity: The Current Alternatives. ATLA 23, 868-882.
22. Brown, N. A. (1987). Teratogenicity testing in vitro: status of validation studies. Arch. Toxicol. Suppl. 11, 105-114.
23. Callan, N. A. and Witter, F. R. (1990). Intrauterine growth retardation: characteristics, risk factors and gestational age. Int. J. Gynaecol. Obstet. 33, 215-220.
24. Chai, C. K. and Degenhardt, K. H. (1962). Developmental anomaties in inbred rabbits. J. Hered. 53, 174-182.
25. Chang, M. C. (1944). Artificial production of monstrosities in the rabbit. Nature 154, 150.
26. Cunliffe, V. and Smith, J. C. (1992). Ectopic mesoderm formation in Xenopus embryos caused by widespread expression of a Brachyury homologue. Nature 358, 427-430.
27. Davis, D. L., Friedler, G., Mattison, D. and Morris, R. (1992). Male-mediated teratogenesis and other reproductive effects: biologic and epidemiologic findings and a plea for clinical research. Reprod. Toxicol. 6, 289-292.
28. Desbois, C. and Karsenty, G. (1995). Osteocalcin cluster: implications for functional studies. J. Cell. Biochem. 57, 379-383.
29. Ducy, P., Zhang, R., Geoffroy, V. et al. (1997). Osf2/Cbfa1: a transcriptional activator of osteoblast differentiation. Cell 89, 747-754.
30. Eiges, R. and Benvenisty, N. (2002). A molecular view on pluripotent stem cells. FEBS Lett. 529, 135-141.
31. Fassler, R., Rohwedel, J., Maltsev, V. et al. (1996). Differentiation and integrity of cardiac muscle cells are impaired in the absence of beta 1 integrin. J. Cell. Sci. 109, 2989-2999.
32. Faustman, E. M. (1988). Short-term tests for teratogens. Mutat. Res. 205, 355-384.
33. Flynn, R. J. (1968). Exencephalia: its occurrence in untreated mice. Science 160, 898-899.
34. Green, H., Easley, K. and Iuchi, S. (2003). Marker succession during the development of keratinocytes from cultured human embryonic stem cells. Proc. Natl. Acad. Sci. USA. 100, 15625-15630.
35. Gruenwald, P. (1966). Growth of the human fetus. I. Normal growth and its variation. Am. J. Obstet. Gynecol. 94, 1112-1119.
36. Haas, J. F. and Schottenfeld, D. (1979). Risks to the offspring from parental occupational exposures. J. Occup. Med. 21, 607-613.
37. He, J. Q., Ma, Y., Lee, Y. et al. (2003). Human embryonic stem cells develop into multiple types of cardiacmyocytes: action potential characterization. Circ. Res. 93, 32-39.
38. Kalter, H. (1980). The relation between congenital malformation and prenatal mortality in experimental animals. In I. H. Porter and E. Hook (eds), Human Embryonic and Fetal Death (29-44). New York: Academic Press.
39. Kalter, H. (1968). Sporadic congenital malformations of newborn inbred mice. Teratology 1, 193-199.
40. Karnofsky, D. A. (1965). Drugs as teratogens in animals and man. Annu. Rev. Pharmacol. 10, 447-472.
41. Kaufman, D. S., Hanson, E. T., Lewis, R. L. et al. (2001). Hematopoietic colony-forming cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA. 98, 10716-10721.
42. Kehat, I., Amit, M., Gepstein, A. et al. (2003). Development of cardiomyocytes from human ES cells. Meth. Enzymol. 365, 461-473.
43. Kehat, I., Gepstein, A., Spira, A. et al. (2002). High-resolution electrophysiological assessment of human embryonic stem cell-derived cardiomyocytes: a novel in vitro model for the study of conduction. Circ. Res. 91, 659-661.
44. Khera, K. S. (1985). Maternal toxicity: a possible etiological factor in embryo-fetal deaths and fetal malformations of rodent-rabbit species. Teratology 31, 129-153.
45. Khera, K. S. (1987). Maternal toxicity in humans and animals: effects on fetal development and criteria for detection. Teratog. Carcinog. Mutagen. 7, 287-295.
46. Kimmel, G. L., Smith, K., Kochhar, D. M. and Pratt, R. M. (1982). Overview of In Vitro Teratogenicity Testing: aspects of validation and application to screening. Teratog. Carcinog. Mutagen. 2, 221-229.
47. Kolossov, E., Fleischmann, B. K., Liu, Q. et al. (1998). Functional characteristics of ES cell-derived cardiac precursor cells identified by tissue-specific expression of the green fluorescent protein. J. Cell. Biol. 143, 2045-2056.
48. Kramer, J., Hegert, C., Guan, K. et al. (2000). Embryonic stem cell-derived chondrogenic differentiation in vitro: activation by BMP-2 and BMP-4. Mech. Dev. 92, 193-205.
49. Leahy, A., Xiong, J. W., Kuhnert, F. and Stuhlmann, H. (1999). Use of developmental marker genes to define temporal and spatial patterns of differentiation during embryoid body formation. J. Exp. Zool. 284, 67-81.
50. Levenberg, S., Golub, J. S., Amit, M. et al. (2002). Endothelial cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. U S A 99, 4391-4396.
51. Leonard, B. E. (1981). Effect of psychotropic drugs administered to pregnant rats on the behaviour of the offspring. Neuropharmacology 20, 1237-1242.
52. Lints, T. J., Parsons, L. M., Hartley, L. et al. (1993). Nkx-2.5: a novel murine homeobox gene expressed in early heart progenitor cells and their myogenic descendants. Development 119, 419-431.
53. Lockhart, D. J. and Winzeler, E. A. (2000). Genomics, gene expression and DNA arrays. Nature 405, 827-836.
54. Low, J. A. and Galbraith, R. S. (1974). Pregnancy characteristics of intrauterine growth retardation. Obstet. Gynecol. 44, 122-126.
55. Lubchenco, L. O., Handman, C., Dressler, M. and Boyd, E. (1963). Intrauterine growth as estimated from liveborn birth-weight data at 24 to 42 weeks of gestation. Pediatrics 32, 793-800.
56. Lutwak-Mann, C. (1964). Observation of progeny of thalidomide-treated male rabbits. Br. Med. J. 1, 1090-1091.
57. MacLeod, P. M. (1993). Implication of the child with malformations for the family and society. In R. E Stevenson, J. G Hal and R. M Goodman (eds), Human malformations and related anomalies (Vol. I, 187-196). Oxford Monographs on Medical Genetics No. 27, Oxford University Press.
58. Maltsev, V. A., Rohwedel, J., Hescheler, J. and Wobus, A. M. (1993). Embryonic stem cells differentiate in vitro into cardiomyocytes representing sinusnodal, atrial and ventricular cell types. Mech. Dev. 44, 41-50.
59. Meyerson, M., Counter, C. M., Eaton, E. N. et al. (1997). hEST2, the putative human telomerase catalytic subunit gene, is up-regulated in tumor cells and during immortalization. Cell 90, 785-795.
60. Menezes, J. R and Luskin, M. B. (1994). Expression of neuron-specific tubulin defines a novel population in the proliferative layers of the developing telencephalon. J. Neurosci. 1, 5399-5416.
61. Metzger, J. M., Lin, W. I. and Samuelson, L. C. (1996). Vital staining of cardiac myocytes during embryonic stem cell cardiogenesis in vitro. Circ. Res. 78, 547-552.
62. Miller, H. C. (1981). Intrauterine growth retardation. An unmet challenge. Am. J. Dis. Child. 135, 944-948.
63. Mummery, C., Ward-van Oostwaard, D., Doevendans, P. et al. (2003). Differentiation of human embryonic stem cells to cardiomyocytes: role of coculture with visceral endoderm-like cells. Circulation 107, 2733-2740.
64. Nelson, B. K., Brightwell, W. S., Setzer, J. V. et al. (1981). Ethoxyethanol behavioral teratology in rats. Neurotoxicology 2, 231-249.
65. Okamoto, M., Kihara, T. and Tanimura, T. (1986). Developmental toxicity of prenatal aspirin exposure to rats. Teratology 34, 451.
66. Pandey, A. and Mann, M. (2000). Proteomics to study genes and genomes. Nature 405, 837-846.
67. Paparella, M., Kolossov, E., Fleischmann, B. K. et al. (2002). The use of quantitative image analysis in the assessment of in vitro embryotoxicity endpoints based on a novel embryonic stem cell clone with endoderm-related GFP expression. Toxicol. In Vitro 16, 589-597.
68. Pellizzer, C., Adler, S., Corvi, R. et al. (2004a). Monitoring of teratogenic effects in vitro by analysing a selected gene expression pattern. Toxicol. In Vitro 18, 325-335.
69. Pellizzer, C., Bello, E., Adler, S. et al. (2004b). Detection of tissue specific effects by Methotrexate on differentiating mouse embryonic stem cells. Birth Defects Res. B. Dev. Reprod. Toxicol. 71, 331-341.
70. Reubinoff, B. E., Pera, M. F., Fong, C. Y. et al. (2000). Embryonic stem cell lines from human blastocysts: somatic differentiation in vitro. Nat. Biotechnol. 18, 399-404.
71. Rohwedel, J., Guan, K., Zuschratter, W. et al. (1998). Loss of betal integrin function results in a retardation of myogenic, but an acceleration of neuronal, differentiation of embryonic stem cells in vitro. Dev. Biol. 201, 167-184.
72. Rosano, A., Botto, L. D., Botting, B. and Mastroiacovo, P. (2000). Infant mortality and congenital anomalies from 1950 to 1994: an international perspective. J. Epidemiol. Community. Health 54, 660-666.
73. Schardein, J. L. and Keller, K. A. (1989). Potential human developmental toxicants and the role of animal testing in their identification and characterization. Crit. Rev. Toxicol. 19, 251-339.
74. Schardein, J. L. (1983). Teartogenic risk assessment. Past, present and future. In H. Kalter (ed), Issues and Reviews in Teratology (Vol. 1, 181-214). New York: Plenum.
75. Schmidt, M. M., Guan, K. and Wobus, A. M. (2001). Lithium influences differentiation and tissue-specific gene expression of mouse embryonic stem (ES) cells in vitro. Int. J. Dev. Biol. 45, 421-429.
76. Schuldiner, M., Yanuka, O., Itskovitz-Eldor, J. et al. (2000). Effects of eight growth factors on the differentiation of cells derived from human embryonic stem cells. Proc. Natl. Acad. Sci. USA 97, 11307-11312.
77. Scholer, H. R. (1991). Octamania: the POU factors in murine development. Trends in Genet. 7, 323-329.
78. Seiler, A., Visan, A., Buesen, R. et al. (2004). Improvement of an in vitro stem cell assay for developmental toxicity: the use of molecular endpoints in the embryonic stem cell test. Reprod. Toxicol. 18, 231-240.
79. Seiler, A., Visan, A., Pohl, I. et al. (2002). Improving the embryonic stem cell test (EST) by establishing molecular endpoints of tissue specific development using murine embryonic stem cells (D3 cells). ALTEX 19 Suppl. 1, 55-63.
80. Shepard, T. H. and Fantel, A. G. (1979). Embryonic and early fetal loss. Clin. Perinatol. 6, 219-243.
81. Singec, I., Knoth, R., Ditter, M. et al. (2002). Synaptic vesicle protein synaptoporin is differently expressed by subpopulations of mouse hippocampal neurons. J. Comp. Neurol. 452, 139-153.
82. Spielmann, H., Poh, I., Doering, B. et al. (1997). The Embryonic Stem Cells Test (EST), an in vitro embryotoxicity test using two permanent cells line: 3T3 fibroblasts and embryonic stem cells. Toxicol. In Vitro 10, 119-127.
83. Staples, R. E. and Holtkamp, D. E. (1963). Effects of parental Thalidomide treatment on gestation and fetal development. Exp. Mol. Pathol. 26, 81-106.
84. Strubing, C., Ahnert-Hilger, G., Shan, J. et al. (1995). Differentiation of pluripotent embryonic stem cells into the neuronal lineage in vitro gives rise to mature inhibitory and excitatory neurons. Mech. Dev. 53, 275-287.
85. Suarez-Rodriguez, R. and Belkind-Gerson, J. (2004). Cultured nestin-positive cells from postnatal mouse small bowel differentiate ex vivo into neurons, glia, and smooth muscle. Stem Cells. 22, 1373-1385.
86. Thomson, J. A., Itskovitz-Eldor, J., Shapiro, S. S. et al. (1998). Embryonic stem cell lines derived from human blastocysts. Science 282, 1145-1147.
87. van der Jagt, K., Munn, S., Tørsløv, J. and de Bruijn, J. (2004). Alternative approaches can reduce the use of test animals under REACH. http://ihcp.jrc.cec.eu.int/DOCUMENTATION/ECB/2004/ Reducing_the_use_of_test_animals_under_REACH_IHCP_report.pdf (access 01/2005).
88. Vorhees, C. V., Butcher, R. E., Brunner, R. L. and Sobotka, T. J. (1979). A developmental test battery for neurobehavioral toxicity in rats: a preliminary analysis using monosodium glutamate calcium carrageenan, and hydroxyurea. Toxicol. Appl. Pharmacol. 50, 267-282.
89. Warkany, J. (1971). Syndromes. Am. J. Dis. Child. 121, 365-370.
90. Wiche, G., Herrmann, H., Dalton, J. M. et al. (1986). Molecular aspects of MAP-1 and MAP-2: microheterogeneity, in vitro localization and distribution in neuronal and nonneuronal cells. Ann. N. Y. Acad. Sci. 466, 180-198.
91. Wilson, J. G. (1978). Review of in vitro systems with potential for use in teratogenicity screening. J. Environ. Pathol. Toxicol. 2, 149-167.
92. Wilson, J. G. (1977). Embryotoxicity of drugs in man. In Plenum Publishing Corp (ed), Handbook of teratology, (Vol II., 309-355). New York.
93. Wilson, J. G. (1975). Reproduction and teratogenesis: current methods and suggested improvements. J. Assoc. Off. Anal. Chem. 584, 657-667.
94. Wilson, J. G. (1973). Environment and birth defects. New York: Academic Press.
95. Wobus, A. M., Kaomei, G., Shan, J. et al. (1997). Retinoic acid accelerates embryonic stem cell-derived cardiac differentiation and enhances development of ventricular cardiomyocytes. J. Mol. Cell. Cardiol. 29, 1525-1539.
96. Xiao, Y., Haase, H., Young, W. G. and Bartold, P. M. (2004). Development and transplantation of a mineralized matrix formed by osteoblasts in vitro for bone regeneration. Cell Transplant. 13, 15-25.
97. Xu, C., Police, S., Rao, N. and Carpenter, M. K. (2002). Characterization and enrichment of cardiomyocytes derived from human embryonic stem cells. Circ. Res. 91, 501-508.
98. Yoon, P. W., Olney, R. S., Khoury, M. J. et al. (1997). Contribution of birth defects and genetic diseases to pediatric hospitalizations. A population-based study. Arch. Pediatr. Adolesc. Med. 151, 1096-1103.
99. Zhang, S. C., Wernig, M., Duncan, I. D. et al. (2001). In vitro differentiation of transplantable neural precursors from human embryonic stem cells. Nat. Biotechnol. 19, 1129-1133.
100. zur Nieden, N. I., Kempka, G. and Ahr, H. J. (2003). In vitro differentiation of embryonic stem cells into mineralized osteoblasts. Differentiation 71, 18-27.
101. zur Nieden, N. I., Ruf, L. J., Kempka, G. et al. (2001). Molecular markers in embryonic stem cells. Toxicol. In Vitro 15, 455-461.