p21 and notch signalings in the persistently altered vagina induced by neonatal diethylstilbestrol exposure in mice

Journal of Veterinary Medical Science

Volumn 74, Issue 12, 2012, Pages 1589-1595

  Nakamura, Takeshi ^a,b   Miyagawa, Shinichi ^a   Katsu, Yoshinao ^b,c   Mizutani, Takeshi ^b   Sato, Tomomi ^d   Takeuchi, Takashi ^e   Iguchi, Taisen ^b   Ohta, Yasuhiko ^e  

^a YAMAGATA UNIVERSITY   (Japan)

^b OKAZAKI INSTITUTE FOR INTEGRATIVE BIOSCIENCE   (Japan)

^c HOKKAIDO UNIVERSITY   (Japan)

^d YOKOHAMA CITY UNIVERSITY   (Japan)

^e TOTTORI UNIVERSITY   (Japan)

Author keywords

Diethylstilbestrol; Neonatal exposure; p21 and notch signalings; Persistent vaginal changes; Vagina

Indexed keywords

BASIC HELIX LOOP HELIX TRANSCRIPTION FACTOR; CYCLIN DEPENDENT KINASE INHIBITOR 1A; DIETHYLSTILBESTROL; ESTROGEN; NOTCH RECEPTOR;

ANIMAL; ARTICLE; C57BL MOUSE; CELL PROLIFERATION; CYTOLOGY; DRUG EFFECT; EPITHELIUM CELL; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; METABOLISM; MICROARRAY ANALYSIS; MOUSE; NEWBORN; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; VAGINA;

ANIMALS; ANIMALS, NEWBORN; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; CELL PROLIFERATION; CYCLIN-DEPENDENT KINASE INHIBITOR P21; DIETHYLSTILBESTROL; EPITHELIAL CELLS; ESTROGENS, NON-STEROIDAL; FEMALE; GENE EXPRESSION REGULATION; IMMUNOHISTOCHEMISTRY; MICE; MICE, INBRED C57BL; MICROARRAY ANALYSIS; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, NOTCH; SIGNAL TRANSDUCTION; VAGINA;

MUS;

EID: 84871776872     PISSN: 09167250     EISSN: 13477439     Source Type: Journal    
DOI: 10.1292/jvms.12-0182     Document Type: Article

References (56)

1. Brugarolas, J., Chadrasekaran, C., Gordon, J., Beach, D., Jacks, T. and Hannon, G. 1995. Radiation-induced cell cycle arrest compromised by p21 deficiency. Nature 377: 552-557. [Medline] [CrossRef]
2. Deng, C., Zhang, P., Harper, J. W., Elledge, S. J. and Leder, P. 1995. Mice lacking p21CIP1/WAF1 undergo normal development, but are defective in G1 checkpoint control. Cell 82: 675-684. [Medline] [CrossRef]
3. Devgan, V., Mammucari, C., Millar, S. E., Brisken, C. and Dotto, G. P. 2005. P21WAF1/Cip1 is a negative transcriptional regulator of Wnt4 expression downstream of Notch1 activation. Genes Dev. 19: 1485-1495. [Medline] [CrossRef]
4. Dulic, V., Kaufman, W. K., Wilson, S. J., Tlsty, T. D., Lees, E., Harper, J. W., Elledge, S. J. and Reed, S. I. 1994. p53-dependent inhibition of cyclin-dependent kinase activities in human fibroblasts during radiation-induced G1 arrest. Cell 76: 1013-1023. [Medline] [CrossRef]
5. Dunn, T. B. and Green, A. W. 1963. Cysts of the epididymis, cancer of the cervix, granular cell myoblastoma, and other lesions after rogen injection in newborn mice. J. Natl. Cancer Inst. 31: 425-455. [Medline]
6. el-Deiry, W. S., Tokino, T., Velculescu, V., Levy, D., Parsons, R., Trent, J., Lin, D., Mercer, W. E., Kinzler, K. and Vogelstein, B. 1993. WAF1, a potential mediator of p53 tumor suppression. Cell 75: 817-825. [Medline] [CrossRef]
7. Forsberg, J. G. 1969. The development of atypical epithelium in the mouse uterine cervix and vaginal formix after neonatal oestradiol treatment. Br. J. Exp. Pathol. 50: 187-195. [Medline]
8. Forsberg, J. G. 1979. Developmental mechanism of estrogeninduced irreversible changes in the mouse cervicovaginal epithelium. Natl. Cancer Inst. Monogr. 51: 41-56. [Medline]
9. Gartel, A. L. and Tyner, A. L. 1999. Transcriptional regulation of the p21(WAF1/CIP1) gene. Exp. Cell Res. 246: 280-289. [Medline] [CrossRef]
10. Harper, J. W., Adami, G., Wei, N., Keyomarsi, K. and Elledge, S. 1993. The p21 cdk-interacting protein Cip1 is a potent inhibitor of G1 cyclin-dependent kinases. Cell 75: 805-816. [Medline] [CrossRef]
11. Harper, J. W., Elledge, S. J., Keyomarsi, K., Dynlacht, B., Tsai, L., Zhang, P., Dobtowolski, S., Bai, C., Connell-Crowley, L., Swindell, E., Fox, M. P. and Wei, N. 1995. Inhibition of cyclin dependent kinases by p21. Mol. Biol. Cell 6: 387-400. [Medline]
12. Hartman, J., Müller, P., Foster, J. S., Wimalasena, J., Gustafsson, J. Å. and Ström, A. 2004. HES-1 inhibits 17β-estradiol and heregulin-β1-mediated upregulation of E2F-1. Oncogene 23: 8826-8833. [Medline] [CrossRef]
13. Hatch, E. E., Herbst, A. L., Hoover, R. N., Noller, K. L., Adam, E., Kaufman, R. H., Palmer, J. R., Titus-Ernstoff, L., Hyer, M., Hartge, P. and Robboy, S. J. 2001. Incidence of squamous neoplasia of the cervix and vagina in women exposed prenatally to diethylstilbestrol (United States). Cancer Causes Control 12: 837-845. [Medline] [CrossRef]
14. Henderson, A. M., Wang, S. J., Taylor, A. C., Aitkenhead, M. and Hughes, C. C. 2001. The basic helix-loop-helix transcription factor HESR1 regulates endothelial cell tube formation. J. Biol. Chem. 276: 6169-6176. [Medline] [CrossRef]
15. Herbst, A. L. 2000. Behavior of estrogen-associated female genital tract cancer and its relation to neoplasia following intrauterine exposure to diethylstilbestrol (DES). Gynecol. Oncol. 76: 147-156. [Medline] [CrossRef]
16. Herbst, A. L., Ulfelder, H. and Poskanzer, D. C. 1971. Adenocarcinoma of the vagina, Association of maternal stilbestrol therapy with tumor appearance in young women. N. Engl. J. Med. 284: 878-881. [Medline] [CrossRef]
17. Iguchi, T. 1992. Cellular effects of early exposure to sex hormones and antihormones. Int. Rev. Cytol. 139: 1-57. [Medline] [CrossRef]
18. Iguchi, T., Takasugi, N., Bern, H. A. and Mills, K. T. 1986. Frequent occurrence of polyovular follicles in ovaries of mice exposed neonatally to diethylstilbestrol. Teratology 34: 29-35. [Medline] [CrossRef]
19. Kopan, R. and Ilagan, M. X. 2009. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137: 216-233. [Medline] [CrossRef]
20. Lathia, J. D., Mattson, M. P. and Cheng, A. 2008. Notch: from neural development to neurological disorders. J. Neurochem. 107: 1471-1481. [Medline] [CrossRef]
21. Lee, M. H., Reynisdottir, I. and Massague, G. 1995. Cloning of p57KIP2, a cyclin-dependent kinase inhibitor with unique domain structure and tissue distribution. Genes Dev. 9: 639-649. [Medline] [CrossRef]
22. Li, Y., Dowbenko, D. and Lasky, L. A. 2002. AKT/PKB phosphorylation of p21Cip/WAF1 enhances protein stability of p21Cip/ WAF1 and promotes cell survival. J. Biol. Chem. 277: 11352-11361. [Medline] [CrossRef]
23. Macleod, K. F., Sherry, N., Hannon, G., Beach, D., Tokino, T., Kinzler, K., Vogelstein, B. and Jacks, T. 1995. p53-dependent and -independent expression of p21 during cell growth, differentiation, and DNA damage. Genes Dev. 9: 935-944. [Medline] [CrossRef]
24. Maier, M. M. and Gessler, M. 2000. Comparative analysis of the human and mouse Hey1 promoter: Hey genes are new Notch target genes. Biochem. Biophys. Res. Commun. 275: 652-660. [Medline] [CrossRef]
25. Marselos, M. and Tomatis, L. 1992. Diethylstilboestrol:I, Pharmacology, toxicology and carcinogenicity in humans. Eur. J. Cancer 28A: 1182-1189. [Medline] [CrossRef]
26. Marselos, M. and Tomatis, L. 1992. Diethylstilboestrol:II, Pharmacology, toxicology and carcinogenicity in experimental animals. Eur. J. Cancer 29A: 149-155. [Medline]
27. McLachlan, J. A., Newbold, R. R. and Bullock, B. C. 1980. Long-term effects on the female mouse genital tract associated with prenatal exposure to diethylstilbestrol. Cancer Res. 40: 3988-3999. [Medline]
28. Michieli, P., Chedid, M., Lin, D., Pierce, J., Mercer, E. and Givol, D. 1994. Induction of WAF1/CIP1 by a p53-independent Pathway. Cancer Res. 54: 3391-3395. [Medline]
29. Miyagawa, S., Katsu, Y., Watanabe, H. and Iguchi, T. 2004. Estrogen-independent activation of ErbBs signaling and estrogen receptor α in the mouse vagina exposed neonatally to diethylstilbestrol. Oncogene 23: 340-349. [Medline] [CrossRef]
30. Miyagawa, S., Suzuki, A., Katsu, Y., Kobayashi, M., Goto, M., Handa, H., Watanabe, H. and Iguchi, T. 2004. Persistent gene expression in mouse vagina exposed neonatally to diethylstilbestrol. J. Mol. Endocrinol. 32: 663-677. [Medline] [CrossRef]
31. Müller, P., Merrell, K. W., Crofts, J. D., Ronnlund, C., Lin, C. Y., Gustafsson, J. Å. and Ström, A. 2009. Estrogen-dependent downregulation of hairy and enhancer of split homolog-1 gene expression in breast cancer cells is mediated via a 3' distal element. J. Endocrinol. 200: 311-319. [Medline] [CrossRef]
32. Nakamura, T., Katsu, Y., Watanabe, H. and Iguchi, T. 2008. Estrogen receptor subtypes selectively mediate female mouse reproductive abnormalities induced by neonatal exposure to estrogenic chemicals. Toxicology 253: 117-124. [Medline] [CrossRef]
33. Nakamura, T., Miyagawa, S., Katsu, Y., Watanabe, H., Mizutani, T., Sato, T., Ken-Ichirou Morohashi, K.I., Takeuchi, T., Iguchi, T. and Ohta, Y. 2012. WNT family genes and their modulation in the ovary-independent and persistent vaginal epithelial cell proliferation and keratinization induced by neonatal diethylstilbestrol exposure in mice. Toxicology 296: 13-19. [Medline] [CrossRef]
34. Newbold, R. R. and McLachlan, J. A. 1982. Vaginal adenosis and adenocarcinoma in mice exposed prenatally or neonatally to diethylstilbestrol. Cancer Res. 42: 2003-2011. [Medline]
35. Newbold, R. R., Bullock, B. C. and McLachlan, J. A. 1985. Progressive proliferative changes in the oviduct of mice following developmental exposure to diethylstilbestrol. Teratog. Carcinog. Mutagen. 5: 473-480. [Medline] [CrossRef]
36. Nicolas, M., Wolfer, A., Raj, K., Kummer, J. A., Mill, P., van-Noort, M., Hui, C. C., Clevers, H., Dotto, G. P. and Radtke, F. 2003. Notch functions as a tumor suppressor in mouse skin. Nat. Genet. 33: 416-421. [Medline] [CrossRef]
37. Niculescu, A. B., Chen, X., Smeets, M., Hengst, L., Prives, C. and Reed, S. I. 1998. Effects of p21(Cip1/Waf1) at both the G1/S and the G2/M cell cycle transitions: pRb is a critical determinant is blocking DNA replication and in preventing endoreduplication. Mol. Cell. Biol. 18: 629-643. [Medline]
38. Noda, A., Ning, Y., Venable, S. F., Pereira-Smith, O. M. and Smith, J. R. 1994. Cloning of senescent cell-derived inhibitors of DNA synthesis using an expression screen. Exp. Cell Res. 211: 90-98. [Medline] [CrossRef]
39. Ogryzko, V. V., Wong, P. and Howard, B. H. 1997. WAF1 retards S-phase progression primarily by inhibition of cyclin-dependent kinases. Mol. Cell. Biol. 17: 4877-4882. [Medline]
40. Palmer, J. R., Hatch, E. E., Rosenberg, C. L., Hartge, P., Kaufman, R. H., Titus-Ernstoff, L., Noller, K. L., Herbst, A. L., Rao, R. S., Troisi, R., Colton, T. and Hoover, R. N. 2002. Risk of breast cancer in women exposed to diethylstilbestrol in utero: preliminary results (United States). Cancer Causes Control 13: 753-758. [Medline] [CrossRef]
41. Polyak, K., Kato, J. Y., Solomon, M. J., Sherr, C. J., Massague, J., Roberts, J. M. and Koff, A. 1994. p27kip1, a cyclin-Cddk inhibitor, links transforming growth factor-β and contact inhibition to cell cycle arrest. Genes Dev. 8: 9-22. [Medline] [CrossRef]
42. Radtke, F., Fasnacht, N. and Macdonald, H. R. 2010. Notch signaling in the immune system. Immunity 32: 14-27. [Medline] [CrossRef]
43. Sasai, Y., Kageyama, R., Tagawa, Y., Shigemoto, R. and Nakanishi, S. 1992. Two mammalian helix-loop-helix factors structurally related to Drosophila hairy and Enhancer of split. Genes Dev. 6: 2620-2634. [Medline] [CrossRef]
44. Ström, A., Arai, N., Leers, J. and Gustafsson, J. Å. 2000. The hairy and enhancer of split homologue-1 (HES-1) mediates the proliferative effect of 17β-estradiol on breast cancer cell lines. Oncogene 19: 5951-5953. [Medline] [CrossRef]
45. Suzuki, A., Sugihara, A., Uchida, K., Sato, T., Ohta, Y., Katsu, Y., Watanabe, H. and Iguchi, T. 2002. Developmental effects of perinatal exposure to bisphenol-A and diethylstilbestrol on reproductive organs in female mice. Reprod. Toxicol. 16: 107-116. [Medline] [CrossRef]
46. Suzuki, A., Watanabe, H., Mizutani, T., Sato, T., Ohta, Y. and Iguchi, T. 2006. Global gene expression in mouse vaginae exposed to diethylstilbestrol at different ages. Exp. Biol. Med. (Maywood) 231: 632-640. [Medline]
47. Takasugi, N. and Bern, H. A. 1964. Tissue changes in mice with persistent vaginal cornification induced by early postnatal treatment with estrogen. J. Natl. Cancer Inst. 33: 855-865. [Medline]
48. Takasugi, N., Bern, H. A. and DeOme, K. B. 1962. Persistent vaginal cornification in mice. Science 138: 438-439. [Medline] [CrossRef]
49. Tateya, T., Imayoshi, I., Tateya, I., Ito, J. and Kageyama, R. 2011. Coorperative functions of Hes/Hey genes in auditory hair cell and supporting cell development. Dev. Biol. 352: 329-340. [Medline] [CrossRef]
50. Thelu, J., Rossio, P. and Favier, B. 2002. Notch signaling is linked to epidermal cell differentiation level in basal cell carcinoma, psoriasis and wound healing. BMC Dermatol. 2: 7. [Medline] [CrossRef]
51. Tien, A. C., Rajan, A. and Bellen, H. J. 2009. A Notch update. J. Cell Biol. 184: 621-629. [Medline] [CrossRef]
52. Toyoshima, H. and Hunter, T. 1994. p27, a novel inhibition of G1 cyclin/cdk protein kinase activity, is relayted to p21. Cell 78: 67-74. [Medline] [CrossRef]
53. Watanabe, H., Suzuki, A., Mizutani, T., Khono, S., Lubahn, D. B., Handa, H. and Iguchi, T. 2002. Genome-wide analysis of changes in early gene expression induced by oestrogen. Genes Cells 7: 497-507. [Medline] [CrossRef]
54. Watanabe, H., Suzuki, A., Kobayashi, M., Lubahn, D. B., Handa, H. and Iguchi, T. 2003. Similarities and differences in uterine gene expression patterns caused by treatment with physiological and non-physiological estrogens. J. Mol. Endocrinol. 31: 487-497. [Medline] [CrossRef]
55. Watanabe, H., Suzuki, A., Goto, M., Lubahn, D. B., Handa, H. and Iguchi, T. 2004. Tissue-specific estrogenic and non-estrogenic effects of a xenoestrogen, nonylphenol. J. Mol. Endocrinol. 33: 243-252. [Medline] [CrossRef]
56. Xiong, Y., Hannon, G., Zhang, H., Casso, D., Kobayashi, R. and Beach, D. 1993. p21 is a universal inhibitor of cyclin kinases. Nature 366: 701-704. [Medline] [CrossRef]