Uterine temporal response to acute exposure to 17α-ethinyl estradiol in the immature rat

Toxicological Sciences

Volumn 97, Issue 2, 2007, Pages 467-490

  Naciff, Jorge M ^a   Overmann, Gary J ^a   Torontali, Suzanne M ^a   Carr, Gregory J ^a   Khambatta, Zubin S ^a   Tiesman, Jay P ^a   Richardson, Brian D ^a   Daston, George P ^a  

^a PROCTER AND GAMBLE COMPANY   (United States)

Author keywords

Estrogens; Female reproductive tract; Microarray; Temporal gene expression; Uterotrophic response

Indexed keywords

ETHINYLESTRADIOL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DNA MODIFICATION; DOWN REGULATION; DRUG EFFICACY; DRUG EXPOSURE; ENERGY METABOLISM; ESTROGEN ACTIVITY; FEMALE; GENE EXPRESSION; GENE EXPRESSION PROFILING; GENE SEQUENCE; HISTOPATHOLOGY; IMMATURITY; IMMUNITY; IN VIVO STUDY; MICROARRAY ANALYSIS; NONHUMAN; NUCLEOTIDE SEQUENCE; PHENOTYPIC VARIATION; PROTEIN SYNTHESIS; RAT; SIGNAL TRANSDUCTION; SINGLE DRUG DOSE; STUDENT T TEST; TISSUE REGENERATION; TRANSCRIPTION REGULATION; UNINDEXED SEQUENCE; UPREGULATION; UTERUS WEIGHT;

ANIMALS; BODY WEIGHT; CELL LINE; DATA INTERPRETATION, STATISTICAL; ESTROGENS; ETHINYL ESTRADIOL; FEMALE; GENE EXPRESSION; GENES, IMMEDIATE-EARLY; MALE; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SIZE; PHENOTYPE; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; UTERUS;

RATTUS;

EID: 34447578869     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfm046     Document Type: Article

References (63)

1. Anderson, J. N., Peck, E. J., Jr, and Clark, J. H. (1974). Nuclear receptor estradiol complex: A requirement for uterotrophic responses. Endocrinology 95, 174-178.
2. Batra, S. (1987). Increase by oestrogen of calcium entry and calcium channel density in uterine smooth muscle. Br. J. Pharmacol. 92 389-392.
3. Beissbarth, T., and Speed, T. P. (2004). GOstat: Find statistically over-represented Gene Ontologies within a group of genes. Bioinformatics 12, 1464-1465.
4. Brigstock, D. R. (2002). Regulation of angiogenesis and endothelial cell function by connective tissue growth factor (CTGF) and cysteine-rich 61 (CYR61). Angiogenesis 5, 153-165.
5. Britt, K. L., and Findlay, J. K. (2002). Estrogen actions in the ovary revisited. J. Endo.crinol. 175, 269-276.
6. Buhimschi, I. A., Yallampalli, C., Buhimschi, C. S., Saade, G. R., and Garfield, R. E. (2000). Distinct regulation of nitric oxide and cyclic guanosine monophosphate production by steroid hormones in the rat uterus. Mol. Hum. Reprod. 6, 404-414.
7. Butt, A. J., McNeil, C. M., Musgrove, E. A., and Sutherland, R. L. (2005). Downstream targets of growth factor and oestrogen signalling and endocrine resistance: The potential roles of c-Myc, cyclin D1 and cyclin E. Endocr. Relat. Cancer 12(Suppl. 1), S47-S59.
8. Catalano, R. D., Johnson, M. H., Campbell, E. A., Charnock-Jones, D. S., Smith, S. K., and Sharkey, A. M. (2005). Inhibition of Stat3 activation in the endometrium prevents implantation: A nonsteroidal approach to contraception. Proc. Natl. Acad. Sci. U.S.A. 102, 8585-8590.
9. Catelli, M. G., and Baulieu, E. E. (1976). Estrogen-induced changes of ribonucleic acid in the rat uterus. Mol. Cell. Endocrinol. 6 129-151.
10. Cheng, S. V., MacDonald, B. S., Clark, B. F., and Pollard, J. W. (1985). Cell growth and cell proliferation may be dissociated in the mouse uterine luminal epithelium treated with female sex steroids. Exp. Cell. Res. 160, 459-470.
11. Clark, J. H., and Mani, S. K. (1994). Actions of ovarian steroid hormones. In The Physiology of Reproduction (E. Knobil and J. Neill, Eds.), Vol. 1, 2nd ed., pp. 1011-1059. Raven Press, New York.
12. Clemetson, C. A., Verma, U. L., and De Carlo, S. J. (1977). Secretion and reabsorption of uterine luminal fluid in rats. J. Reprod. Fertil. 49, 183-187.
13. Cocchiara, R., Albeggiani, G., Di Trapani, G., Azzolina, A., Lampiasi, N., Rizzo, F., Diotallevi, L., Gianaroli, L., and Geraci D. (1992). Oestradiol enhances in vitro the histamine release induced by embryonic histamine-releasing factor (EHRF) from uterine mast cells. Hum. Reprod. 7, 1036-1041.
14. Couse, J. F., Dixon, D., Yates, M., Moore, A. B., Ma, L., Maas, R., and Korach, K. S. (2001). Estrogen receptor-alpha knockout mice exhibit resistance to the developmental effects of neonatal diethylstilbestrol exposure on the female reproductive tract. Dev. Biol. 238, 224-238.
15. Couse, J. F., and Korach, K. S. (2001). Contrasting phenotypes in reproductive tissues of female estrogen receptor null mice. Ann. NY Acad. Sci. 948, 1-8.
16. Curtis, S. H., Korach, K. S. (2000). Steroid receptor knockout models: Phenotypes and responses illustrate interactions between receptor signaling pathways in vivo. Adv. Pharmacol. 47, 357-380.
17. Currie, R. A., Orphanides, G., and Moggs, J. G. (2005). Mapping molecular responses to xenoestrogens through Gene Ontology and pathway analysis of toxicogenomic data. Reprod. Toxicol. 20, 433-440.
18. Daston, G. P., and Naciff, J. M. (2005). Gene expression changes related to growth and differentiation in the fetal and juvenile reproductive system of the female rat: Evaluation of microarray results. Reprod. Toxicol. 19, 381-394.
19. Debidda, M., Wang, L., Zang, H., Poli, V., and Zheng, Y. (2005). A role of STAT3 in Rho GTPase-regulated cell migration and proliferation. J. Biol. Chem. 280, 17275-17285.
20. Fertuck, K. C., Eckel, J. E., Gennings, C., and Zacharewski, T. R. (2003). Identification of temporal patterns of gene expression in the uteri of immature, ovariectomized mice following exposure to ethynylestradiol. Physiol. Genomics 15, 127-141.
21. Gouon-Evans, V., and Pollard, J. W. (2001). Eotaxin is required for eosinophil homing into the stroma of the pubertal and cycling uterus. Endocrinology 142, 4515-4521.
22. Gramantieri, L., Chieco, P., Giovannini, C., Lacchini,M., Trere, D., Grazi, G. L., Venturi, A., and Bolondi, L. (2005). GADD45-alpha expression in cirrhosis and hepatocellular carcinoma: Relationshipwith DNA repair and proliferation. Hum. Pathol. 36, 1154-1162.
23. Green, A. R., Parrott, E. L., Butterworth, M., Jones, P. S., Greaves, P., and White, I. N. (2001). Comparisons of the effects of tamoxifen, toremifene and raloxifene on enzyme induction and gene expression in the ovariectomised rat uterus. J. Endo.crinol. 170, 555-564.
24. Hao, G., Xie, L., and Gross, S. S. (2004). Argininosuccinate synthetase is reversibly inactivated by S-nitrosylation in vitro and in vivo. J. Biol. Chem. 279, 36192-36200.
25. Herve, M. A., Meduri, G., Petit, F. G., Domet, T. S., Lazennec, G., Mourah, S., and Perrot-Applanat, M. (2006). Regulation of the vascular endothelial growth factor (VEGF) receptor Flk-1/KDR by estradiol through VEGF in uterus. J. Endo.crinol. 188, 91-99.
26. Hewitt, S. C., Deroo, B. J., Hansen, K., Collins, J., Grissom, S., Afshari, C. A., and Korach, K.S. (2003). Estrogen receptor-dependent genomic responses in the uterus mirror the biphasic physiological response to estrogen. Mol. Endocrinol. 17, 2070-2083.
27. Hong, S. H., Nah, H. Y., Lee, J. Y., Gye, M. C., Kim, C. H., and Kim, M. K. (2004). Analysis of estrogen-regulated genes in mouse uterus using cDNA microarray and laser capture microdissection. J. Endocrinol. 181, 157-167.
28. Huang, S. S., and Huang, J. S. (2005). TGF-beta control of cell proliferation. J. Cell. Biochem. 96, 447-462.
29. Hung, H., and Pollak, M. (1995). Regulation of IGFBP-3 expression in breast cancer cells and uterus by estradiol and antiestrogens: Correlations with effects on proliferation: A review. Prog. Growth Factor Res. 6, 495-501.
30. Inoue, A., Takeuchi, S., and Takahashi, S. (2005). Insulin-like growth factor-I stimulated DNA replication in mouse endometrial stromal cells. J. Reprod. Dev. 51, 305-313.
31. Joslyn, C. A., Mniszewski, S. M., Fulmer, A., and Heaton, G. (2004). The gene ontology categorizer. Bioinformatics 20(Suppl. 1), I169-I177.
32. Kiss, R., Lenglet, G., Pasteels, J. L., and Danguy, A. (1987). Hormonal regulation of uterine epithelial cell proliferation. I. Effects of estradiol or progesterone administered separately. In Vivo 1 281-289.
33. Klinge, C. M. (2001). Estrogen receptor interaction with estrogen response elements. Nucleic Acids Res. 29, 2905-2919.
34. Koshi, R., Coutinho-Silva, R., Cascabulho, C. M., Henrique-Pons, A., Knight, G. E., Loesch, A., and Burnstock, G. (2005). Presence of the P2X(7) purinergic receptor on immune cells that invade the rat endometrium during oestrus. J. Reprod. Immunol. 66, 127-140.
35. Koos, R. D., Kazi, A. A., Roberson, M. S., and Jones, J. M. (2005). New insight into the transcriptional regulation of vascular endothelial growth factor expression in the endometrium by estrogen and relaxin. Ann. NY Acad. Sci. 1041, 233-247.
36. Krumenacker, J. S., Hyder, S. M., and Murad, F. (2001). Estradiol rapidly inhibits soluble guanylyl cyclase expression in rat uterus. Proc. Natl. Acad. Sci. USA 98, 717-722.
37. Kwekel, J. C., Burgoon, L. D., Burt, J. W., Harkema, J. R., and Zacharewski, T. R. (2005). A cross-species analysis of the rodent uterotrophic program: Elucidation of conserved responses and targets of estrogen signaling. Physiol. Genomics 23, 327-342.
38. Lee, K. W., and Cohen, P. (2002). Nuclear effects: Unexpected intracellular actions of insulin-like growth factor binding protein-3. J. Endo.crinol. 175, 33-40.
39. Lockhart, D. J., Dong, H., Byrne, M. C., Follettie, M. T., Gallo, M. V., Chee, M. S., Mittmann, M., Wang, C., Kobayashi, M., Horton, H., et al. (1996). Expression monitoring by hybridization to high-density oligonucleotide arrays. Nat. Biotechnol. 14, 1675-1680.
40. Long, J.,Wang, G., Matsuura, I., He, D., and Liu, F. (2004). Activation of Smad transcriptional activity by protein inhibitor of activated STAT3 (PIAS3). Proc. Natl. Acad. Sci. U.S.A. 101, 99-104.
41. Moggs, J. G. (2005). Molecular responses to xenoestrogens: Mechanistic insights from toxicogenomics. Toxicology 213, 177-193.
42. Moggs, J. G., Tinwell, H., Spurway, T., Chang, H. S., Pate, I., Lim, F. L., Moore, D. J., Soames, A., Stuckey, R., Currie, R., et al. (2004). Phenotypic anchoring of gene expression changes during estrogen-induced uterine growth. Environ. Health Perspect. 112 1589-1606.
43. Moyano, P., and Rotwein, P. (2004). Mini-review: Estrogen action in the uterus and insulin-like growth factor-I. Growth Horm. IGF Res. 14, 431-435 (Review).
44. Muller, R. E., and Knowler, J. T. (1984). The synthesis of ribosomal RNA and ribosomal protein and their incorporation into ribosomes in the uterus of the oestrogen-stimulated immature rat. FEBS Lett. 174 253-257.
45. Munoz-Alonso, M. J., Acosta, J. C., Richard, C., Delgado, M. D., Sedivy, J., and Leon, J. (2005). p21Cip1 and p27Kip1 induce distinct cell cycle effects and differentiation programs in myeloid leukemia cells. J. Biol. Chem. 280, 18120-18129.
46. Naciff, J. M., Jump, M. L., Torontali, S. M., Carr, G. J., Tiesman, J. P., Overmann, G. J., and Daston, G. P. (2002). Gene expression profile induced by 17alpha-ethynyl estradiol, bisphenol A, and genistein in the developing female reproductive system of the rat. Toxicol. Sci. 68, 184-199.
47. Naciff, J. M., Overmann, G. J., Torontali, S. M., Carr, G. J., Tiesman, J. P., Richardson, B. D., and Daston, G. P. (2003). Gene expression profile induced by 17 alpha-ethynyl estradiol in the prepubertal female reproductive system of the rat. Toxicol. Sci. 72, 314-330.
48. Naciff, J. M., Overmann, G. J., Torontali, S. M., Carr, G. J., Tiesman, J. P., and Daston, G. P. Impact of the phytoestrogen content of laboratory animal feed on the gene expression profile of the reproductive system in the immature female rat. Environ Health Perspect. 2004 Nov; 112(15): 1519-1526.
49. Naciff, J. M., Torontali, S. M., Overmann, G. I., Carr, G. J., Tiesman, J. P., and Daston, G. P. (2005). Evaluation of the gene expression changes induced by 17-alpha-ethynyl estradiol in the immature uterus/ ovaries of the rat using high density oligonucleotide arrays. Birth Defects Res. B Dev. Reprod. Toxicol. 74, 164-184.
50. Nilsson, S., Makela, S., Treuter, E., Tujague, M., Thomsen, J., Andersson, G., Enmark, E., Pettersson, K., Warner, M., and Gustafsson, J. A. (2001). Mechanisms of estrogen action. Physiol. Rev. 81 1535-1565.
51. Noda, S., Sawaki, M., Shiraishi, K., Yamasaki, K., and Yamaguchi, R. (2002). Age-related changes of genital systems in the female Crj:CD (SD) IGS rats during sexual maturation. J. Vet. Med. Sci. 64, 315-319.
52. O'Toole, S. A., Dunn, E., Sheppard, B. L., Sheils, O., O'Leary, J. J.,Wuttke, W., and Seidlova-Wuttke, D. (2005). Oestrogen regulated gene expression in normal and malignant endometrial tissue. Maturitas 51, 187-198.
53. Pines, J., and Hunter, T. (1992). Cyclins A and B1 in the human cell cycle. Ciba Found. Symp. 170, 187-196; discussion 196-204.
54. Pollard, J. W., Pacey, J., Cheng, S. V., and Jordan, E. G. (1987). Estrogens and cell death in murine uterine luminal epithelium. Cell Tissue Res. 249, 533-540.
55. Schulz, S. (2005). C-type natriuretic peptide and guanylyl cyclase B receptor. Peptides 26, 1024-1034.
56. Sherr, C. J. (1995). D-type cyclins. Trends Biochem. Sci. 20 187-190.
57. Stephanou, A., and Latchman, D. S. (2005). Opposing actions of STAT-1 and STAT-3. Growth Factors 23, 177-182.
58. Thurston, G., Wang, Q., Baffert, F., Rudge, J., Papadopoulos, N., Jean-Guillaume, D., Wiegand, S., Yancopoulos, G. D., and McDonald, D. M. (2005). Angiopoietin 1 causes vessel enlargement, without angiogenic sprouting, during a critical developmental period. Development 132, 3317-3326.
59. Vairapandi, M., Balliet, A. G., Hoffman, B., and Liebermann, D. A. (2002). GADD45b and GADD45g are cdc2/cyclinB1 kinase inhibitors with a role in S and G2/M cell cycle checkpoints induced by genotoxic stress. J. Cell. Physiol. 192, 327-338.
60. 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.
61. Waters, K. M., Safe, S., and Gaido, K. W. (2001). Differential gene expression in response to methoxychlor and estradiol through ERalpha, ERbeta, and AR in reproductive tissues of female mice. Toxicol. Sci. 63, 47-56.
62. Wu, X., Pang, S. T., Sahlin, L., Blanck, A., Norstedt, G., and Flores-Morales, A. (2003). Gene expression profiling of the effects of castration and estrogen treatment in the rat uterus. Biol. Reprod. 69, 1308-1317.
63. Yamada, A. T., and Nagata, T. (1993). Light and electron microscopic radioautographic studies on the RNA synthesis of peri-implanting pregnant mouse uterus during activation of receptivity for blastocyst implantation. Cell. Mol. Biol. (Noisy-le-grand) 39, 221-233.