DNA repair during organogenesis

Mutation Research - Fundamental and Molecular Mechanisms of Mutagenesis

Volumn 509, Issue 1-2, 2002, Pages 79-91

  Vinson, Robert K ^a   Hales, Barbara F ^a  

^a MCGILL UNIVERSITY   (Canada)

Author keywords

Cell cycle checkpoint; DNA damage; DNA repair; Embryo; Organogenesis; Teratogen

Indexed keywords

DNA; GENE PRODUCT; TERATOGENIC AGENT;

CELL FUNCTION; CONGENITAL MALFORMATION; DEVELOPMENTAL STAGE; DNA DAMAGE; DNA RECOMBINATION; DNA REPAIR; DNA TRANSCRIPTION; EMBRYO; EMBRYO DEVELOPMENT; EMBRYOTOXICITY; EXCISION REPAIR; GENE DISRUPTION; GENE EXPRESSION; GENE MUTATION; GENOME; GENOTOXICITY; HUMAN; MAMMAL; MISMATCH REPAIR; MITOSIS INHIBITION; NONHUMAN; NULL ALLELE; ORGANOGENESIS; PRIORITY JOURNAL; REGULATORY MECHANISM; REVIEW;

MAMMALIA;

EID: 0037202623     PISSN: 00275107     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0027-5107(02)00223-3     Document Type: Article

References (114)

1. Ames B.N., Shigenaga M.K. Oxidants are a major contributor to aging. Ann. N.Y. Acad. Sci. 663:1992;85-96.
2. Burcham P.C. Internal hazards: baseline DNA damage by endogenous products of normal metabolism. Mutat. Res. 443:1999;11-36.
3. Wink D.A., Kasprzak K.S., Maragos C.M., Elespuru R.K., Misra M., Dunams T.M., Cebula T.A., Koch W.H., Andrews A.W., Allen J.S., Keefe L.K. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science. 254:1994;1001-1003.
4. Griffiths H.R., Mistry P., Herbert K.E., Lunec J. Molecular and cellular effects of ultraviolet light-induced genotoxicity. Crit. Rev. Clin. Lab. Sci. 35:1998;189-237.
5. Pryor W.A. Cigarette smoke radicals and the role of free radicals in chemical carcinogenicity. Environ. Health. Perspect. 105(Suppl 4):1997;875-882.
6. Courtois Y.A., Min S., Lachenal C., Jacquot-Deschamps J.M., Callais F., Festy B. Genotoxicity of organic extracts from atmospheric particles. Ann. N. Y. Acad. Sci. 534:1988;724-740.
7. Hsiao W.L., Mo Z.Y., Fang M., Shi X.M., Wang F. Cytotoxicity of PM(2.5) and PM(2.5-10) ambient air pollutants assessed by the MTT and the Comet assays. Mutat. Res. 471:2000;45-55.
8. Don Porto Carero A., Hoet P.H., Verschaeve L., Schoeters G., Nemery B. Genotoxic effects of carbon black particles, diesel exhaust particles, and urban air particulates and their extracts on a human alveolar epithelial cell line (A549) and a human monocytic cell line (THP-1). Environ. Mol. Mutagen. 37:2001;155-163.
9. Rubenchik B.L., Osinkovskaya N.D., Mikhailenko V.M., Furman M.A., Boim T.M. The carcinogenic danger of nitrite pollution of the environment. J. Environ. Pathol. Toxicol. Oncol. 10:1990;290-296.
10. Routledge M.N., Mirsky F.J., Wink D.A., Keefer L.K., Dipple A. Nitrite-induced mutations in a forward mutation assay: influence of nitrite concentration and pH. Mutat. Res. 322:1994;341-346.
11. Wang C.J., Huang H.P., Tseng T.H., Lin Y.L., Shiow S.J. N-Nitroso-N-(3-keto-1,2-butanediol)-3′-nitrotyramine: a new genotoxic agent derived from the reaction of tyrosine and glucose in the presence of sodium nitrite. Arch. Toxicol. 70:1995;10-15.
12. Lakdawalla A.A., Netrawali M.S. Mutagenicity, comutagenicity, and antimutagenicity of erythrosine (FD and C red 3), a food dye, in the Ames/Salmonella assay. Mutat. Res. 204:1988;131-139.
13. Moller P., Wallin H., Grunnet N., Risom L., Knudsen L.E. DNA damage in isolated rat hepatocytes exposed to C.I. pigment orange 5 and C.I. pigment yellow 12 by the alkaline comet assay. Teratog. Carcinog. Mutagen. 18:1998;9-16.
14. Tsuda S., Kosaka Y., Matsusaka N., Sasaki Y.F. Detection of pyrimethamine-induced DNA damage in mouse embryo and maternal organs by the modified alkaline single cell gel electrophoresis assay. Mutat. Res. 415:1998;69-77.
15. Sugimura T. Nutrition and dietary carcinogens. Carcinogenesis. 21:2000;387-395.
16. Brendel V., Brocchieri L., Sandler S.J., Clark A.J., Karlin S. Evolutionary comparisons of RecA-like proteins across all major kingdoms of living organisms. J. Mol. Evol. 44:1997;528-541.
17. Taylor E.M., Lehmann A.R. Conservation of eukaryotic DNA repair mechanisms. Int. J. Radiat. Biol. 74:1998;277-286.
18. Modrich P. Mismatch repair in replication fidelity, genetic recombination, and cancer biology. Annu. Rev. Biochem. 65:1996;101-133.
19. Wood R.D. DNA repair in eukaryotes. Annu. Rev. Biochem. 65:1996;135-167.
20. Norbury C.J., Hickson I.D. Cellular responses to DNA damage. Annu. Rev. Pharmacol. Toxicol. 41:2001;367-401.
21. Ronen A., Glickman B.W. Human DNA repair genes. Environ. Mol. Mutagen. 37:2001;241-283.
22. Friedberg E.C., Meira L.B. Database of mouse strains carrying targeted mutations in genes affected cellular responses to DNA damage Version 4. Mutat. Res. 459:2000;243-274.
23. McWhir J., Selfridge J., Harrison D.J., Squires S., Melton D.S. Mice with DNA repair gene (ERCC-1) deficiency have elevated levels of p53, liver nuclear abnormalities and die before weaning. Nat. Genet. 5:1993;217-224.
24. MacAuley A., Werb Z., Mirkes P.E. Characterization of the unusually rapid cell cycles during rat gastrulation. Development. 117:1993;873-883.
25. Matsuda Y., Tobari I. Repair capacity of fertilized mouse eggs for X-ray damage induced in sperm and mature oocytes. Mutat. Res. 210:1989;35-47.
26. Schultz R.M. The molecular foundations of the maternal to zygotic transition in the preimplantation embryo. Human Reprod. Update. 8:2002;323-331.
27. Gurtu V.E., Verma S., Grossmann A.H., Liskay R.M., Skarnes W.C., Baker S.M. Maternal effect for DNA mismatch repair in the mouse. Genetics. 160:2002;271-277.
28. Harrison R.H., Kuo H.C., Scriven P.N., Handyside A.H., Ogilvie C.M. Lack of cell cycle checkpoints in human cleavage stage embryos revealed by a clonal pattern of chromosomal mosaicism analysed by sequential multicolour FISH. Zygote. 8:2000;217-224.
29. McFadden D.E., Friedman J.M. Chromosome abnormalities in human beings. Mutat. Res. 396:1997;129-140.
30. Jackson S.P. Sensing and repairing DNA double-strand breaks. Carcinogenesis. 23:2002;687-696.
31. D.O. Ferguson, F.W. Alt, DNA double strand break repair and chromosomal translocation: Lessons from animal models, Oncogene 20 (2001) 5572-5579.
32. Pfeiffer P., Goedecke W., Obe G. Mechanisms of DNA double-strand break repair and their potential to induce chromosomal aberrations. Mutagenesis. 15:2000;289-302.
33. el-Hage S., Singh S.M. A 5-fold reduction in sister-chromatid exchange following implantation of mouse embryos is not directly related to the expression of embryonic genes responsible for oxygen radical metabolism. Mutat. Res. 232:1990;217-226.
34. Peleg L., Raz E., Ben-Ishai R. Changing capacity for DNA excision repair in mouse embryonic cells in vitro. Exp. Cell Res. 104:1977;301-307.
35. Jirakulsomchok S., Yielding K.L. DNA damage and repair in mouse embryos following treatment transplacentally with methylnitrosourea and methylmethanesulfonate. Teratog. Carcinog. Mutagen. 4:1984;523-536.
36. Loch-Caruso R., Baxter C.S. DNA damage and repair in embryonic mouse limbs exposed to teratogenic doses of methylnitrosourea. Mutat. Res. 131:1984;147-155.
37. Liu L., Wells P.G. DNA oxidation as a potential molecular mechanism mediating drug-induced birth defects: phenytoin and structurally related teratogens initiate the formation of 8-hydroxy-2′-deoxyguanosine in vitro and in vivo in murine maternal hepatic and embryonic tissues. Free Radic. Biol. Med. 19:1995;639-648.
38. Latimer J.J., Hultner M.L., Cleaver J.E., Pedersen R.A. Elevated DNA excision repair capacity in the extraembryonic mesoderm of the midgestation mouse embryo. Exp. Cell. Res. 228:1996;19-28.
39. Timson J. Hydroxyurea. Mutat. Res. 32:1975;115-132.
40. Weng Y., Sirover M.A. Developmental regulation of the base excision repair enzyme uracil DNA glycosylase in the rat. Mutat. Res. 293:1993;133-141.
41. Vinson R.K., Hales B.F. Expression and activity of the DNA repair enzyme uracil DNA glycosylase during organogenesis in the rat conceptus and following methotrexate exposure in vitro. Biochem. Pharmacol. 64:2002;711-721.
42. Shimura T., Inoue M., Taga M., Shiraishi K., Uematsu N., Takei N., Yuan Z.M., Shinohara T., Niwa O. p53-Dependent S-phase damage checkpoint and pronuclear cross talk in mouse zygotes with X-irradiated sperm. Mol. Cell. Biol. 22:2002;2220-2228.
43. Finkielstein C.V., Lewellyn A.L., Maller J.L. The midblastula transition in Xenopus embryos activates multiple pathways to prevent apoptosis in response to DNA damage. Proc. Natl. Acad. Sci. U.S.A. 98:2001;1006-1011.
44. Greenwood J., Costanzo V., Robertson K., Hensey C., Gautier J. Responses to DNA damage in Xenopus: cell death or cell cycle arrest. Novartis Found Symp. 237:2001;221-230.
45. Su T.T., Walker J., Stumpff J. Activating the DNA damage checkpoint in a developmental context. Curr. Biol. 10:2000;119-126.
46. Rees W.D., Hay S.M., Fontanier-Razzaq N.C., Amtipatis C., Harries D.N. Expression of the growth arrest genes (GAS and GADD) changes during organogenesis in the rat fetus. J. Nutr. 129:1999;1532-1536.
47. Chen G., Lee E.Y.-H.P. The product of the ATM gene is a 370-kDa nuclear phosphoprotein. J. Biol. Chem. 271:1996;33693-33697.
48. Soares H.D., Morgan J.I., McKinnon P.J. ATM expression patterns suggest a contribution from the peripheral nervous system to the phenotype of Ataxia-Telangiectasia. Neuroscience. 86:1998;1045-1054.
49. Schmid P., Lorenz A., Hameister H., Montenarh M. Expression of p53 during mouse embryogenesis. Development. 113:1991;857-865.
50. Choi J., Donehower L.A. p53 in embryonic development: maintaining a fine balance. Cell Mol. Life Sci. 55:1999;38-47.
51. Komarova E.A., Chernov M.V., Franks R., Wang K., Armin G., Zelnick C.R., Chin D.M., Bacus S.S., Stark G.R., Gudkov A.V. Transgenic mice with p53-responsive lacZ: p53 activity varies dramatically during normal development and determines radiation and drug sensitivity in vivo. EMBO J. 16:1997;1391-1400.
52. Heyer B.S., MacAuley A., Behrendtsen O., Werb Z. Hypersensitivity to DNA damage leads to increased apoptosis during early mouse development. Genes Dev. 14:2000;2072-2084.
53. de Klein A., Muijtjens M., van Os R., Verhoeven Y., Smit B., Carr A.M., Lehmann A.R., Hoeijmakers J.H.J. Targeted disruption of the cell-cycle checkpoint gene ATR leads to early embryonic lethality in mice. Curr. Biol. 10:2000;479-482.
54. Takai H., Tominaga K., Motoyama N., Minamishima Y.A., Nagahama H., Tsukiyama T., Ikeda K., Nakayama K., Nakanishi M., Nakayama K.-I. Aberrant cell cycle checkpoint function and early embryonic death in Chk1(-/-) mice. Genes Dev. 14:2000;1439-1447.
55. Keyse S.M. The induction of gene expression in mammalian cells by radiation. Semin. Cancer Biol. 4:1993;119-128.
56. Amundson S.A., Bittner M., Chen Y., Trent J., Meltzer P., Fornace A.J. Jr. Fluorescent cDNA microarray hybridization reveals complexity and heterogeneity of cellular genotoxic stress responses. Oncogene. 18:1999;3666-3672.
57. Jelinsky S.A., Samson L.D. Global response of Saccharomyces cerevisiae to an alkylating agent. Proc. Natl. Acad. Sci. U.S.A. 96:1999;1486-1491.
58. Harkin D.P., Hall P.A. Measuring a cell's response to stress: the p53 pathway. Genome Biol. 1:2000;105.
59. Amundson S.A., Bittner M., Meltzer P., Trent J., Fornace A.J. Jr. Physiological function as regulation of large transcriptional programs: the cellular response to genotoxic stress. Comp. Biochem. Physiol. B. Biochem. Mol. Biol. 129:2001;703-710.
60. Hubank M., Mayne L. Expression of the excision repair gene, ERCC3 (excision repair cross-complementing) during mouse development. Brain Res. Dev. Brain Res. 81:1994;66-76.
61. Kim N.K., Lee S.H., Sohn T.J., Roy R., Mitra S., Chung H.M., Ko J.J., Cha K.Y. Spatial expression of a DNA repair gene, N-methylpurine-DNA glycosylase (MPG) during development in mice. Anticancer Res. 20:2000;3037-3043.
62. Ou Y.C., Thompson S.A., Kirchner S.C., Kavanagh T.J., Faustman E.M. Induction of growth arrest and DNA damage-inducible genes Gadd45 and Gadd153 in primary rodent embryonic cells following exposure to methylmercury. Toxicol. Appl. Pharm. 147:1997;31-38.
63. Harrouk W., Codrington A., Vinson R., Robaire B., Hales B.F. Paternal exposure to cyclophosphamide induces DNA damage and alters the expression of DNA repair genes in the rat preimplantation embryo. Mutation Res. DNA Repair. 461:2000;229-241.
64. Vinson R.K., Hales B.F. Nucleotide excision repair gene expression in the rat conceptus during organogenesis. Mutat. Res. 486:2001;113-123.
65. Vinson R.K., Hales B.F. Expression of base excision, mismatch, and recombination repair genes in the organogenesis-stage rat conceptus and effects of exposure to a genotoxic teratogen, 4-hydroperoxycyclophosphamide. Teratology. 64:2001;283-291.
66. Ono Y., Watanabe M., Inoue Y., Ohmoto T., Akiyama K., Tsutsui K., Seki S. Developmental expression of APEX nuclease, a multifunctional DNA repair enzyme, in mouse brains. Brain Res. Dev. Brain Res. 86:1995;1-6.
67. Wilson T.M., Rivkees S.A., Deutsch W.A., Kelley M.R. Differential expression of the apurinic/apyrimidinic endonuclease (APE/ref-1) multifunctional DNA base excision repair gene during fetal development and in adult rat brain and testis. Mutat. Res. 362:1996;237-248.
68. Chen G., Lee E.Y.-H.P. The product of the ATM gene is a 370-kDa nuclear phosphoprotein. J. Biol. Chem. 271:1996;33693-33697.
69. Kim N.K., Lee S.H., Sohn T.J., Roy R., Mitra S., Chung H.M., Ko J.J., Cha K.Y. Spatial expression of a DNA repair gene, N-methylpurine-DNA glycosylase (MPG) during development in mice. Anticancer Res. 20:2000;3037-3043.
70. Nilsen H., Steinsbekk K.S., Otterlei M., Slupphaug G., Aas P.A., Krokan H.E. Analysis of uracil-DNA glycosylases from the murine UNG gene reveals differential expression in tissues and in embryonic development and a subcellular sorting pattern that differs from the human homologues. Nucl. Acids Res. 28:2000;2277-2285.
71. Meira L.B., Devaraj S., Kisby G.E., Burns D.K., Daniel R.L., Hammer R.E., Grundy S., Jialal I., Friedberg E.C. Heterozygosity for the mouse Apex gene results in phenotypes associated with oxidative stress. Cancer Res. 61:2001;5552-5557.
72. Niedernhofer L.J., Essers J., Weeda G., Beverloo B., de Wit J., Muijtjens M., Odijk H., Hoeijmakers J.H., Kanaar R. The structure-specific endonuclease Ercc1-XPF is required for targeted gene replacement in embryonic stem cells. EMBO J. 20:2001;6540-6549.
73. Rotman G., Shiloh Y. ATM: from gene to function. Hum. Mol. Genet. 7:1998;1555-1563.
74. Lee Y., Chong M.J., McKinnon P.J. Ataxia Telangiectasia mutated-dependent apoptosis after genotoxic stress in the developing nervous system is determined by cellular differentiation status. J. Neurosci. 21:2001;6687-6693.
75. Kang J., Bronson R.T., Xu Y. Targeted disruption of NBS1 reveals its roles in mouse development and DNA repair. EMBO J. 21:2002;1447-1455.
76. Zhu J., Petersen S., Tessarollo L., Nussenzweig A. Targeted disruption of the Nijmegen breakage syndrome gene NBS1 leads to early embryonic lethality in mice. Curr. Biol. 11:2001;105-109.
77. Armstrong J.F., Kaufman M.H., Harrison D.J., Clarke A.R. High-frequency developmental abnormalities in p53-deficient mice. Curr. Biol. 5:1995;931-936.
78. Sah V.P., Attardi L.D., Mulligan G.J., Williams B.O., Bronson R.T., Jacks T. A subset of p53-deficient embryos exhibit exencephaly. Nat. Genet. 10:1995;175-180.
79. Therrien J.P., Drouin R., Baril C., Drobetsky E.A. Human cells compromised for p53 function exhibit defective global and transcription-coupled nucleotide excision repair, whereas cells compromised for pRb function are defective only in global repair. Proc. Natl. Acad. Sci. U.S.A. 96:1999;15038-15043.
80. Ménissier-de Murcia J., Mark M., Wendling O., Wynshaw-Boris A., de Murcia G. Early embryonic lethality in PARP-1 ATM double-mutant mice suggests a functional synergy in cell proliferation during development. Mol. Cell. Biol. 21:2001;1828-1832.
81. Gurley K.E., Kemp C.J. Synthetic lethality between mutation in ATM and DNA-PKcs during murine embryogenesis. Curr. Biol. 11:2001;191-194.
82. Pittman D.L., Schimenti J.C. Midgestation lethality in mice deficient for the RecA-related gene Rad51d/Rad51l3. Genesis. 26:2000;167-173.
83. Murai M., Enokido Y., Inamura N., Yoshino M., Nakatsu Y., van der Horst G.T., Hoeijmakers J.H., Tanaka K., Hatanaka H. Early postnatal ataxia and abnormal cerebellar development in mice lacking Xeroderma pigmentosum Group A and Cockayne syndrome Group B DNA repair genes. Proc. Natl. Acad. Sci. U.S.A. 98:2001;13379-13384.
84. Montes de Oca Luna R., Wagner D.S., Lozano G. Rescue of early embryonic lethality in mdm2-deficient mice by deletion of p53. Nature. 378:1995;203-206.
85. Jones S.N., Roe A.E., Donehower L.A., Bradley A. Rescue of embryonic lethality in Mdm2-deficient mice by absence of p53. Nature. 378:1995;206-208.
86. Lim D.S., Hasty P. A mutation in mouse rad51 results in an early embryonic lethal that is suppressed by a mutation in p53. Mol. Cell. Biol. 16:1996;7133-7143.
87. Brugarolas J., Jacks T. Double indemnity - p53 BRCA and cancer: p53 mutation partially rescues developmental arrest in Brca1 and Brca2 null mice suggesting a role for familial breast cancer genes in DNA damage repair. Nat. Med. 3:1997;721-722.
88. Hakem R., de la Pompa J.L., Elia A., Potter J., Mak T.W. Partial rescue of Brca1 (5-6) early embryonic lethality by p53 or p21 null mutation. Nat. Genet. 16:1997;298-302.
89. Lee Y., Barnes D.E., Lindahl T., McKinnon P.J. Defective neurogenesis resulting from DNA ligase IV deficiency requires ATM. Genes Dev. 14:2000;2576-2580.
90. Nicol C.J., Harrison M.L., Laposa R.R., Gimelshtein I.L., Wells P.G. A teratologic suppressor role for p53 in benzo[α]pyrene-treated transgenic p53-deficient mice. Nat. Genet. 10:1995;181-187.
91. Norimura T., Nomoto S., Katsuki M., Gondo Y., Kondo S. p53-Dependent apoptosis suppresses radiation-induced teratogenesis. Nat. Med. 2:1996;577-580.
92. Wubah J.A., Ibrahim M.M., Gao X., Nguyen D., Pisano M.M., Knudsen T.B. Teratogen-induced eye defects mediated by p53-dependent apoptosis. Curr. Biol. 6:1996;60-69.
93. Moallem S.A., Hales B.F. The role of p53 and cell death by apoptosis and necrosis in 4-hydroperoxycyclophosphamide-induced limb malformations. Development. 125:1998;3225-3234.
94. Frenkel J., Sherman D., Fein A., Schwartz D., Almog N., Kapon A., Goldfinger N., Rotter V. Accentuated apoptosis in normally developing p53 knockout mouse embryos following genotoxic stress. Oncogene. 18:1999;2901-2907.
95. Wang B. Involvement of p53-dependent apoptosis in radiation teratogenesis and in the radioadaptive response in the late organogenesis of mice. J. Radiat. Res. (Tokyo). 42:2001;1-10.
96. Hall P.A., Lane D.P. Tumor suppressors: a developing role for p53? Curr. Biol. 7:1997;R144-R147.
97. Beckman D.A., Brent R.L. Mechanisms of teratogenesis. Ann. Rev. Pharmacol. Toxicol. 24:1984;483-500.
98. Bishop J.B., Witt K.L., Sloane R.A. Genetic toxicities of human teratogens. Mutat. Res. 396:1997;9-43.
99. Winn L.M., Wells P.G. Evidence for embryonic prostaglandin H synthase-catalyzed bioactivation and reactive oxygen species-mediated oxidation of cellular macromolecules in phenytoin and benzo[α]pyrene teratogenesis. Free Radic. Biol. Med. 22:1997;607-621.
100. Murthy V.V., Becker B.A., Steele W.J. Effects of dosage, phenobarbital, and 2-diethylaminoethyl-2,2-diphenylvalerate on the binding of cyclophosphamide and-or its metabolites to the DNA, RNA and protein of the embryo and liver in pregnant mice. Cancer Res. 33:1973;664-670.
101. Hassoun E.A., Bagchi D., Stohs S.J. Evidence of 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD)-induced tissue damage in fetal and placental tissues and changes in amniotic fluid lipid metabolites of pregnant CF1 mice. Toxicol. Lett. 76:1995;245-250.
102. Platzek T., Bochert G., Rahm U. Embryotoxicity induced by alkylating agents: 8. DNA adduct formation induced by ethylmethanesulfonate in mouse embryos. Teratog. Carcinog. Mutagen. 14:1994;65-73.
103. Bochert G., Platzek T., Rahm U., Neubert D. Embryotoxicity induced by alkylating agents: 6. DNA adduct formation induced by methylnitrosourea in mouse embryos. Arch. Toxicol. 65:1991;390-395.
104. Parman T., Wiley M.J., Wells P.G. Free radical-mediated oxidative DNA damage in the mechanism of thalidomide teratogenicity. Nat. Med. 5:1999;582-585.
105. Generoso W.M., Shourbaji A.G., Piegorsch W.W., Bishop J.B. Developmental response of zygotes exposed to similar mutagens. Mutat. Res. 250:1991;439-446.
106. Liu L., Wells P.G. DNA oxidation as a potential molecular mechanism mediating drug-induced birth defects: phenytoin and structurally related teratogens initiate the formation of 8-hydroxy-2'-deoxyguanosine in vitro and in vivo in murine hepatic and embryonic tissues. Free Radic. Biol. Med. 19:1995;639-648.
107. Wells P.G., Kim P.M., Laposa R.R., Nicol C.J., Parman T., Winn L.M. Oxidative damage in chemical teratogenesis. Mutat. Res. 396:1997;65-78.
108. Henderson G.I., Chen J.J., Schenker S. Ethanol, oxidative stress, reactive aldehydes, and the fetus. Front. Biosci. 4:1999;541-550.
109. Skalko R.G., Poche P.D., Kwasigroch T.E. The toxicology of chemical interactions during pregnancy in the mouse: caffeine and phenytoin. Toxicology. 30:1984;7-16.
110. Brill A., Torchinsky A., Carp H., Toder V. The role of apoptosis in normal and abnormal embryonic development. J. Assist. Reprod. Genet. 16:1999;512-519.
111. Nomura T. Similarity of the mechanism of chemical carcinogen-initiated teratogenesis and carcinogenesis in mice. Cancer Res. 37:1977;969-973.
112. T.B. Knudsen, Cell death, in: R.J. Kavlock, G.P. Daston (Eds.), Drug Toxicity in Embryonic Development I, Springer, Berlin, 1997, pp. 211-244.
113. Mirkes P.E. 2001 Warkany lecture: to die or not to die, the role of apoptosis in normal and abnormal mammalian development. Teratology. 65:2002;228-239.
114. Ferguson L.R., Ford J.H. Overlap between mutagens and teratogens. Mutat. Res. 396:1997;1-8.