Neonatal exposure to diethylstilbestrol alters the expression of DNA methyltransferases and methylation of genomic DNA in the epididymis of mice

Endocrine Journal

Volumn 53, Issue 3, 2006, Pages 331-337

  Sato, Koji ^a,b   Fukata, Hideki ^a,b   Kogo, Yasushi ^c   Ohgane, Jun ^c   Shiota, Kunio ^c   Mori, Chisato ^a,b  

^a CHIBA UNIVERSITY   (Japan)

^b Center of Environmental Health Science for Future Generations NPO   (Japan)

^c UNIVERSITY OF TOKYO   (Japan)

Author keywords

Diethylstilbestrol; DNA methylation; DNA methyltransferase; Epididymis; Restriction landmark genomic scanning (RLGS)

Indexed keywords

DIETHYLSTILBESTROL; DNA METHYLTRANSFERASE; DNA METHYLTRANSFERASE 1; DNA METHYLTRANSFERASE 3A; DNA METHYLTRANSFERASE 3B; GENOMIC DNA; TRANSCRIPTION FACTOR SP1; TRANSCRIPTION FACTOR SP3;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CPG ISLAND; DNA METHYLATION; DRUG EFFECT; EPIDIDYMIS; GENE EXPRESSION; GENE EXPRESSION REGULATION; GENE LOCUS; MALE; MOLECULAR CLONING; MOUSE; NEWBORN; NONHUMAN; NUCLEOTIDE SEQUENCE; REAL TIME POLYMERASE CHAIN REACTION;

ANIMALS; ANIMALS, NEWBORN; CHROMOSOME MAPPING; DIETHYLSTILBESTROL; DNA (CYTOSINE-5-)-METHYLTRANSFERASE; DNA METHYLATION; EPIDIDYMIS; FEMALE; GENE EXPRESSION; MALE; MICE; MICE, INBRED C57BL; PREGNANCY; RESTRICTION MAPPING; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION;

EID: 33745621608     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.K06-009     Document Type: Article

References (40)

1. Herbst AL, Ulfelder H, Poskanzer DC (1971) Adenocarcinoma of the vagina. Association of maternal stilbestrol therapy with tumor appearance in young women. N Engl J Med 284: 878-881.
2. Newbold RR (2004) Lessons learned from perinatal exposure to diethylstilbestrol. Toxicol Appl Pharmacol 199: 142-150.
3. McLachlan JA, Newbold RR, Bullock B (1975) Reproductive tract lesions in male mice exposed prenatally to diethylstilbestrol. Science 190: 991-992.
4. Iguchi T, Takase M, Takasugi N (1986) Development of vaginal adenosis-like lesions and uterine epithelial stratification in mice exposed perinatally to diethylstilbestrol. Proc Soc Exp Biol Med 181: 59-65.
5. Newbold R (1995) Cellular and molecular effects of developmental exposure to diethylstilbestrol: implications for other environmental estrogens. Environ Health Perspect 103 (Suppl 7): 83-87.
6. Adachi T, Matsuno Y, Sugimura A, Takano K, Koh KB, Sakurai K, Shibayama T, Iguchi T, Mori C, Komiyama M (2003) ADAM7 (a disintegrin and metalloprotease 7) mRNA is suppressed in mouse epididymis by neonatal exposure to diethylstilbestrol. Mol Reprod Dev 64: 414-421.
7. Adachi T, Ono Y, Koh KB, Takashima K, Tainaka H, Matsuno Y, Nakagawa S, Todaka E, Sakurai K, Fukata H, Iguchi T, Komiyama M, Mori C (2004) Long-term alteration of gene expression without morphological change in testis after neonatal exposure to genistein in mice: toxicogenomic analysis using cDNA microarray. Food Chem Toxicol 42: 445-452.
8. Matsuno Y, Adachi T, Koh KB, Fukata H, Sugimura A, Sakurai K, Shibayama T, Iguchi T, Komiyama M, Mori C (2004) Effect of neonatal exposure to diethylstilbestrol on testicular gene expression in adult mouse: comprehensive analysis with cDNA subtraction method. Int J Androl 27: 115-122.
9. Shibayama T, Fukata H, Sakurai K, Adachi T, Komiyama M, Iguchi T, Mori C (2001) Neonatal exposure to genistein reduces expression of estrogen receptor alpha and androgen receptor in testes of adult mice. Endocr J 48: 655-663.
10. Cunningham A, Klopman G, Rosenkranz HS (1996) The carcinogenicity of diethylstilbestrol: structural evidence for a non-genotoxic mechanism. Arch Toxicol 70: 356-361.
11. Li S, Washburn KA, Moore R, Uno T, Teng C, Newbold RR, McLachlan JA, Negishi M (1997) Developmental exposure to diethylstilbestrol elicits demethylation of estrogen-responsive lactoferrin gene in mouse uterus. Cancer Res 57: 4356-4359.
12. Li S, Hansman R, Newbold R, Davis B, McLachlan JA, Barrett JC (2003) Neonatal diethylstilbestrol exposure induces persistent elevation of c-fos expression and hypomethylation in its exon-4 in mouse uterus. Mol Carcinog 38: 78-84.
13. Nakagawa T, Kanai Y, Ushijima S, Kitamura T, Kakizoe T, Hirohashi S (2005) DNA hypermethylation on multiple CpG islands associated with increased DNA methyltransferase DNMT1 protein expression during multistage urothelial carcinogenesis. J Urol 173: 1767-1771.
14. Etoh T, Kanai Y, Ushijima S, Nakagawa T, Nakanishi Y, Sasako M, Kitano S, Hirohashi S (2004) Increased DNA methyltransferase 1 (DNMT1) protein expression correlates significantly with poorer tumor differentiation and frequent DNA hypermethylation of multiple CpG islands in gastric cancers. Am J Pathol 164: 689-699.
15. Dahl C, Guldberg P (2003) DNA methylation analysis techniques. Biogerontology 4: 233-250.
16. Hatada I, Hayashizaki Y, Hirotsune S, Komatsubara H, Mukai T (1991) A genomic scanning method for higher organisms using restriction sites as landmarks. Proc Natl Acad Sci USA 88: 9523-9527.
17. La Salle S, Mertineit C, Taketo T, Moens PB, Bestor TH, Trasler JM (2004) Windows for sex-specific methylation marked by DNA methyltransferase expression profiles in mouse germ cells. Dev Biol 268: 403-415.
18. Ohgane J, Aikawa J, Ogura A, Hattori N, Ogawa T, Shiota K (1998) Analysis of CpG islands of trophoblast giant cells by restriction landmark genomic scanning. Dev Genet 22: 132-140.
19. Ohgane J, Wakayama T, Kogo Y, Senda S, Hattori N, Tanaka S, Yanagimachi R, Shiota K (2001) DNA methylation variation in cloned mice. Genesis 30: 45-50.
20. Imamura T, Ohgane J, Ito S, Ogawa T, Hattori N, Tanaka S, Shiota K (2001) CpG island of rat sphingosine kinase-1 gene: tissue-dependent DNA methylation status and multiple alternative first exons. Genomics 76: 117-125.
21. Ohsumi T, Okazaki Y, Hirotsune S, Shibata H, Muramatsu M, Suzuki H, Taga C, Watanabe S, Hayashizaki Y (1995) A spot cloning method for restriction landmark genomic scanning. Electrophoresis 16: 203-209.
22. Gardiner-Garden M, Frommer M (1987) CpG islands in vertebrate genomes. J Mol Biol 196: 261-282.
23. Lagali PS, Kakuk LE, Griesinger IB, Wong PW, Ayyagari R (2002) Identification and characterization of C6orf37, a novel candidate human retinal disease gene on chromosome 6q14. Biochem Biophys Res Commun 293: 356-365.
24. Kang DC, Gopalkrishnan RV, Wu Q, Jankowsky E, Pyle AM, Fisher PB (2002) mda-5: An interferon-inducible putative RNA helicase with double-stranded RNA-dependent ATPase activity and melanoma growth-suppressive properties. Proc Natl Acad Sci USA 99: 637-642.
25. Kishikawa S, Murata T, Kimura H, Shiota K, Yokoyama KK (2002) Regulation of transcription of the Dnmt1 gene by Sp1 and Sp3 zinc finger proteins. Eur J Biochem 269: 2961-2970.
26. Jinawath A, Miyake S, Yanagisawa Y, Akiyama Y, Yuasa Y (2005) Transcriptional regulation of the human DNA methyltransferase 3A and 3B genes by Sp3 and Sp1 zinc finger proteins. Biochem J 385: 557-564.
27. Shigeta H, Zuo W, Yang N, DiAugustine R, Teng CT (1997) The mouse estrogen receptor-related orphan receptor alpha 1: molecular cloning and estrogen responsiveness. J Mol Endocrinol 19: 299-309.
28. Sumi D, Ignarro LJ (2005) Sp1 transcription factor expression is regulated by estrogen-related receptor alpha1. Biochem Biophys Res Commun 328: 165-172.
29. Raiche J, Rodriguez-Juarez R, Pogribny I, Kovalchuk O (2004) Sex- and tissue-specific expression of maintenance and de novo DNA methyltransferases upon low dose X-irradiation in mice. Biochem Biophys Res Commun 325: 39-47.
30. Lindsay S, Bird AP (1987) Use of restriction enzymes to detect potential gene sequences in mammalian DNA. Nature 327: 336-338.
31. Shiota K, Yanagimachi R (2002) Epigenetics by DNA methylation for development of normal and cloned animals. Differentiation 69: 162-166.
32. Shiota K, Kogo Y, Ohgane J, Imamura T, Urano A, Nishino K, Tanaka S, Hattori N (2002) Epigenetic marks by DNA methylation specific to stem, germ and somatic cells in mice. Genes Cells 7: 961-969.
33. Hattori N, Abe T, Hattori N, Suzuki M, Matsuyama T, Yoshida S, Li E, Shiota K (2004) Preference of DNA methyltransferases for CpG islands in mouse embryonic stem cells. Genome Res 14: 1733-1740.
34. Wu Q, Ohsako S, Ishimura R, Suzuki JS, Tohyama C (2004) Exposure of mouse preimplantation embryos to 2,3,7,8-tetrachlorodibenzo-p-dioxin (TCDD) alters the methylation status of imprinted genes H19 and Igf2. Biol Reprod 70: 1790-1797.
35. Anway MD, Cupp AS, Uzumcu M, Skinner MK (2005) Epigenetic transgenerational actions of endocrine disruptors and male fertility. Science 308: 1466-1469.
36. Turusov VS, Trukhanova LS, Parfenov YD, Tomatis L (1992) Occurrence of tumours in the descendants of CBA male mice prenatally treated with diethylstilbestrol. Int J Cancer 50: 131-135.
37. Walker BE, Haven MI (1997) Intensity of multigenerational carcinogenesis from diethylstilbestrol in mice. Carcinogenesis 18: 791-793.
38. Newbold RR, Hanson RB, Jefferson WN, Bullock BC, Haseman J, McLachlan JA (2000) Proliferative lesions and reproductive tract tumors in male descendants of mice exposed developmentally to diethylstilbestrol. Carcinogenesis 21: 1355-1363.
39. Watson RE, Goodman JI (2002) Epigenetics and DNA methylation come of age in toxicology. Toxicol Sci 67: 11-16.
40. Fukata H, Mori C (2004) Epigenetic alteration by the chemical substances, food and environmental factors. Reprod Med Biol 3: 115-121.