Effects of tamoxifen and ethynylestradiol cotreatment on uterine gene expression in immature, ovariectomized mice

Journal of Molecular Endocrinology

Volumn 45, Issue 3, 2010, Pages 161-173

  Fong, Cora J ^a,b   Burgoon, Lyle D ^a,b   Williams, Kurt J ^b   Jones, A Daniel ^a   Forgacs, Agnes L ^a   Zacharewski, Timothy R ^a,b  

^a Michigan State University   (United States)

^b MICHIGAN STATE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

COMPLEMENTARY DNA; ETHINYLESTRADIOL; TAMOXIFEN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DNA MICROARRAY; DRUG ANTAGONISM; DRUG EFFECT; EPITHELIUM CELL; FEMALE; GENE EXPRESSION; GENE IDENTIFICATION; IMMATURITY; MOUSE; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; SINGLE DRUG DOSE; UTEROTROPHY; UTERUS; UTERUS DISEASE; UTERUS WEIGHT;

AGING; ANIMALS; CHROMATOGRAPHY, LIQUID; DOSE-RESPONSE RELATIONSHIP, DRUG; ETHINYL ESTRADIOL; FEMALE; GENE EXPRESSION REGULATION; LIVER; MASS SPECTROMETRY; MICE; MICE, INBRED C57BL; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; ORGAN SIZE; OVARIECTOMY; REPRODUCIBILITY OF RESULTS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; TAMOXIFEN; TIME FACTORS; UTERUS;

EID: 77957372627     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1677/JME-09-0158     Document Type: Article

References (68)

1. Andree B, Hillemann T, Kessler-Icekson G, Schmitt-John T, Jockusch H, Arnold HH & Brand T 2000 Isolation and characterization of the novel popeye gene family expressed in skeletal muscle and heart. Developmental Biology 223 371-382. (doi:10.1006/dbio.2000.9751)
2. Bagheri-Yarmand R, Vadlamudi RK & Kumar R 2003 Activating transcription factor 4 overexpression inhibits proliferation and differentiation of mammary epithelium resulting in impaired lactation and accelerated involution. Journal Biological Chemistry 278 17421-17429. (doi:10.1074/jbc. M300761200)
3. Bamberger AM, Milde-Langosch K, Rossing E, Goemann C & Loning T 2001 Expression pattern of the AP-1 family in endometrial cancer: correlations with cell cycle regulators. Journal of Cancer Research and Clinical Oncology 127 545-550. (doi:10.1007/s004320100255) (Pubitemid 32757488)
4. Beekman C, Nichane M, De Clercq S, Maetens M, Floss T, Wurst W, Bellefroid E & Marine JC 2006 Evolutionarily conserved role of nucleostemin: controlling proliferation of stem/progenitor cells during early vertebrate development. Molecular and Cellular Biology 26 9291-9301. (doi:10.1128/MCB. 01183-06)
5. Black LJ & Goode RL 1980 Uterine bioassay of tamoxifen, trioxifene and a new estrogen antagonist (LY117018) in rats and mice. Life Sciences 26 1453-1458. (doi:10.1016/0024-3205(80)90049-1)
6. Bolt HM 1979 Metabolism of estrogens - natural and synthetic. Pharmacology & Therapeutics 4 155-181. (doi:10.1016/0163- 7258(79)90018-4)
7. Brzozowski AM, Pike AC, Dauter Z, Hubbard RE, Bonn T, Engstrom O, Ohman L, Greene GL, Gustafsson JA & Carlquist M 1997 Molecular basis of agonism and antagonism in the oestrogen receptor. Nature 389 753-758. (doi:10.1038/39645)
8. Burgoon LD, Eckel-Passow JE, Gennings C, Boverhof DR, Burt JW, Fong CJ & Zacharewski T 2005 Protocols for the assurance of microarray data quality and process control. Nucleic Acids Research 33 e172. (doi:10.1093/nar/gni167)
9. Burgoon LD, Boutros PC, Dere E & Zacharewski TR 2006 dbZach: a MIAME-compliant toxicogenomic supportive relational database. Toxicological Sciences 90 558-568. (doi:10.1093/toxsci/kfj097)
10. Castellano-Diaz E, Gonzalez-Quijano MI, Liminana JM & Diaz-Chico BN 1989 Tamoxifen decreases the estradiol induced progesterone receptors by interfering with nuclear estrogen receptor accumulation. Journal of Steroid Biochemistry 33 133-139. (doi:10.1016/0022- 4731(89)90368-3) (Pubitemid 19217926)
11. Cluff AH, Bystrom B, Klimaviciute A, Dahlqvist C, Cebers G, Malmstrom A & Ekman-Ordeberg G 2006 Prolonged labour associated with lower expression of syndecan 3 and connexin 43 in human uterine tissue. Reproductive Biology and Endocrinology 4 24. (doi:10.1186/1477-7827-4-24)
12. Das D, Peterson RC & Scovell WM 2004 High mobility group B proteins facilitate strong estrogen receptor binding to classical and half-site estrogen response elements and relax binding selectivity. Molecular Endocrinology 18 2616-2632. (doi:10.1210/me.2004-0125)
13. Diel P, Schmidt S & Vollmer G 2002 In vivo test systems for the quantitative and qualitative analysis of the biological activity of phytoestrogens. Journal of Chromatography. B, Analytical Technologies in the Biomedical and Life Sciences 777 191-202. (doi:10.1016/S1570- 0232(02)00494-4)
14. Dimitriadis E, Stoikos C, Tan YL & Salamonsen LA 2006 Interleukin 11 signaling components signal transducer and activator of transcription 3 (STAT3) and suppressor of cytokine signaling 3 (SOCS3) regulate human endometrial stromal cell differentiation. Endocrinology 147 3809-3817. (doi:10.1210/en.2006- 0264) (Pubitemid 44079385)
15. Eckel JE, Gennings C, Chinchilli VM, Burgoon LD & Zacharewski TR 2004 Empirical Bayes gene screening tool for time-course or dose - response microarray data. Journal of Biopharmaceutical Statistics 14 647-670. (doi:10.1081/BIP-200025656)
16. Eckel JE, Gennings C, Therneau TM, Burgoon LD, Boverhof DR & Zacharewski TR 2005 Normalization of two-channel microarray experiments: a semiparametric approach. Bioinformatics 21 1078-1083. (doi:10.1093/ bioinformatics/bti105) (Pubitemid 40467931)
17. Edwards DP 2000 The role of coactivators and corepressors in the biology and mechanism of action of steroid hormone receptors. Journal of Mammary Gland Biology and Neoplasia 5 307-324. (doi:10. 1023/A:1009503029176)
18. Ejskjaer K, Sorensen BS, Poulsen SS, Mogensen O, Forman A & Nexo E 2005 Expression of the epidermal growth factor system in human endometrium during the menstrual cycle. Molecular Human Reproduction 11 543-551. (doi:10.1093/molehr/gah207)
19. Fertuck KC, Eckel JE, Gennings C & Zacharewski TR 2003 Identification of temporal patterns of gene expression in the uteri of immature, ovariectomized mice following exposure to ethynylestradiol. Physiological Genomics 15 127-141. (doi:10.1152/physiolgenomics. 00058.2003)
20. Fong CJ, Burgoon LD, Williams KJ, Forgacs AL & Zacharewski TR 2007 Comparative temporal and dose-dependent morphological and transcriptional uterine effects elicited by tamoxifen and ethynylestradiol in immature, ovariectomized mice. BMC Genomics 8 151. (doi:10.1186/1471-2164-8-151)
21. Frasor J, Stossi F, Danes JM, Komm B, Lyttle CR & Katzenellenbogen BS 2004 Selective estrogen receptor modulators: discrimination of agonistic versus antagonistic activities by gene expression profiling in breast cancer cells. Cancer Research 64 1522-1533. (doi:10.1158/ 0008-5472.CAN-03-3326)
22. Geum D, Sun W, Paik SK, Lee CC & Kim K 1997 Estrogen-induced cyclin D1 and D3 gene expressions during mouse uterine cell proliferation in vivo: differential induction mechanism of cyclin D1 and D3. Molecular Reproduction and Development 46 450-458. (doi:10.1002/(SICI)1098-2795(199704)46:4<450::AID- MRD2>3. 0.CO;2-N) (Pubitemid 27149079)
23. Hamid AA, Mandai M, Fujita J, Nanbu K, Kariya M, Kusakari T, Fukuhara K & Fujii S 2003 Expression of cold-inducible RNA-binding protein in the normal endometrium, endometrial hyperplasia, and endometrial carcinoma. International Journal of Gynecological Pathology 22 240-247. (doi:10.1097/01.PGP. 0000070851.25718.EC)
24. Hodges LC, Cook JD, Lobenhofer EK, Li L, Bennett L, Bushel PR, Aldaz CM, Afshari CA & Walker CL 2003 Tamoxifen functions as a molecular agonist inducing cell cycle-associated genes in breast cancer cells. Molecular Cancer Research 1 300-311.
25. Hoogenraad CC, Wulf P, Schiefermeier N, Stepanova T, Galjart N, Small JV, Grosveld F, de Zeeuw CI & Akhmanova A 2003 Bicaudal D induces selective dynein-mediated microtubule minus end-directed transport. EMBO Journal 22 6004-6015. (doi:10.1093/emboj/cdg592) (Pubitemid 37463244)
26. Houssami N, Cuzick J & Dixon JM 2006 The prevention, detection, and management of breast cancer. Medical Journal of Australia 184 230-234.
27. Inoue A, Yoshida N, Omoto Y, Oguchi S, Yamori T, Kiyama R & Hayashi S 2002 Development of cDNA microarray for expression profiling of estrogen-responsive genes. Journal of Molecular Endocrinology 29 175-192. (doi:10.1677/jme.0.0290175)
28. Jordan VC 1993 Fourteenth Gaddum Memorial Lecture. A current view of tamoxifen for the treatment and prevention of breast cancer. British Journal of Pharmacology 110 507-517.
29. Jordan VC 2007 Chemoprevention of breast cancer with selective oestrogen-receptor modulators. Nature Reviews. Cancer 7 46-53. (doi:10.1038/nrc2048)
30. Jordan VC & Gosden B 1983 Inhibition of the uterotropic activity of estrogens and antiestrogens by the short acting antiestrogen LY117018. Endocrinology 113 463-468. (doi:10.1210/endo-113-2-463)
31. Jordan VC, Dix CJ, Naylor KE, Prestwich G & Rowsby L 1978a Nonsteroidal antiestrogens: their biological effects and potential mechanisms of action. Journal of Toxicology and Environmental Health 4 363-390. (doi:10.1080/15287397809529666)
32. Jordan VC, Rowsby L, Dix CJ & Prestwich G 1978b Dose-related effects of non-steroidal antioestrogens nad oestrogens on the measurement of cytoplasmic oestrogen receptors in the rat and mouse uterus. Journal of Endocrinology 78 71-81. (doi:10.1677/joe.0. 0780071)
33. Kedar RP, Bourne TH, Powles TJ, Collins WP, Ashley SE, Cosgrove DO & Campbell S 1994 Effects of tamoxifen on uterus and ovaries of postmenopausal women in a randomised breast cancer prevention trial. Lancet 343 1318-1321. (doi:10.1016/S0140-6736(94)92466-X) (Pubitemid 24162571)
34. Kilpatrick LM, Kola I & Salamonsen LA 1999 Transcription factors Ets1, Ets2, and Elf1 exhibit differential localization in human endometrium across the menstrual cycle and alternate isoforms in cultured endometrial cells. Biology of Reproduction 61 120-126. (doi:10.1095/biolreprod61.1.120)
35. Kirkland JL, Murthy L & Stancel GM 1993 Tamoxifen stimulates expression of the c-fos proto-oncogene in rodent uterus. Molecular Pharmacology 43 709-714.
36. Koibuchi Y, Iino Y, Uchida T, Andoh T, Horii Y, Nagasawa M, Horiguchi J, Maemura M, Takei H, Yokoe T et al. 2000 Regulation of estrogen receptor and epidermal growth factor receptor by tamoxifen under high and low estrogen environments in MCF-7 cells grown in athymic mice. Oncology Reports 7 135-140.
37. Kwekel JC, Burgoon LD, Burt JW, Harkema JR & Zacharewski TR 2005 A cross-species analysis of the rodent uterotrophic program: elucidation of conserved responses and targets of estrogen signaling. Physiological Genomics 23 327-342. (doi:10.1152/physiolgenomics.00175.2005)
38. Kwekel JC, Forgacs AL, Burgoon LD, Williams KJ & Zacharewski TR 2009 Tamoxifen-elicited uterotrophy: cross-species and cross-ligand analysis of the gene expression program. BMC Medical Genomics 2 19. (doi:10.1186/1755-8794-2-19)
39. Laping NJ, Olson BA & Zhu Y 2001 Identification of a novel nuclear guanosine triphosphate-binding protein differentially expressed in renal disease. Journal of the American Society of Nephrology 12 883-890.
40. Lee TC, Li L, Philipson L & Ziff EB 1997 Myc represses transcription of the growth arrest gene gas1. PNAS 94 12886-12891. (doi:10.1073/ pnas.94.24.12886) (Pubitemid 27518446)
41. Lemaire R, Bayle J, Mecham RP & Lafyatis R 2007 Microfibril- associated MAGP-2 stimulates elastic fiber assembly. Journal of Biological Chemistry 282 800-808. (doi:10.1074/jbc.M609692200)
42. Lewis JS & Jordan VC 2005 Selective estrogen receptor modulators (SERMs): mechanisms of anticarcinogenesis and drug resistance. Mutation Research 591 247-263. (doi:10.1016/j.mrfmmm.2005.02.028)
43. Mackay A, Jones C, Dexter T, Silva RL, Bulmer K, Jones A, Simpson P, Harris RA, Jat PS, Neville AM et al. 2003 cDNA microarray analysis of genes associated with ERBB2 (HER2/neu) overexpression in human mammary luminal epithelial cells. Oncogene 22 2680-2688. (doi:10.1038/sj.onc.1206349)
44. Massarweh S, Osborne CK, Creighton CJ, Qin L, Tsimelzon A, Huang S, Weiss H, Rimawi M & Schiff R 2008 Tamoxifen resistance in breast tumors is driven by growth factor receptor signaling with repression of classic estrogen receptor genomic function. Cancer Research 68 826-833. (doi:10.1158/0008-5472. CAN-07-2707)
45. McDonnell DP, Clemm DL, Hermann T, Goldman ME & Pike JW 1995 Analysis of estrogen receptor function in vitro reveals three distinct classes of antiestrogens. Molecular Endocrinology 9 659-669. (doi:10. 1210/me.9.6.659)
46. McInerney EM & Katzenellenbogen BS 1996 Different regions in activation function-1 of the human estrogen receptor required for antiestrogen- and estradiol-dependent transcription activation. Journal of Biological Chemistry 271 24172-24178. (doi:10.1074/jbc. 271.39.24172)
47. Mnif W, Pascussi JM, Pillon A, Escande A, Bartegi A, Nicolas JC, Cavailles V, Duchesne MJ & Balaguer P 2007 Estrogens and antiestrogens activate hPXR. Toxicology Letters 170 19-29. (doi:10. 1016/j.toxlet.2006.11.016)
48. Moggs JG, Tinwell H, Spurway T, Chang HS, Pate I, Lim FL, Moore DJ, Soames A, Stuckey R, Currie R et al. 2004 Phenotypic anchoring of gene expression changes during estrogen-induced uterine growth. Environmental Health Perspectives 112 1589-1606. (doi:10. 1289/txg.7345)
49. Naciff JM, Overmann GJ, Torontali SM, Carr GJ, Khambatta ZS, Tiesman JP, Richardson BD & Daston GP 2007 Uterine temporal response to acute exposure to 17{alpha}-ethinyl estradiol in the immature rat. Toxicological Sciences 97 467-490. (doi:10.1093/toxsci/kfm046)
50. Owens JW & Ashby J 2002 Critical review and evaluation of the uterotrophic bioassay for the identification of possible estrogen agonists and antagonists: in support of the validation of the OECD uterotrophic protocols for the laboratory rodent. Organisation for Economic Co-operation and Development. Critical Reviews in Toxicology 32 445-520. (doi:10.1080/20024091064291) (Pubitemid 35422723)
51. Parrott E, Butterworth M, Green A, White IN & Greaves P 2001 Adenomyosis - a result of disordered stromal differentiation. American Journal of Pathology 159 623-630.
52. Pike AC, Brzozowski AM, Hubbard RE, Bonn T, Thorsell AG, Engstrom O, Ljunggren J, Gustafsson JA & Carlquist M 1999 Structure of the ligand-binding domain of oestrogen receptor beta in the presence of a partial agonist and a full antagonist. EMBO Journal 18 4608-4618. (doi:10.1093/emboj/18. 17.4608)
53. Pole JC, Gold LI, Orton T, Huby R & Carmichael PL 2005 Gene expression changes induced by estrogen and selective estrogen receptor modulators in primary-cultured human endometrial cells: signals that distinguish the human carcinogen tamoxifen. Toxicology 206 91-109. (doi:10.1016/j.tox.2004. 07.005)
54. Qiao L, McKinstry R, Gupta S, Gilfor D, Windle JJ, Hylemon PB, Grant S, Fisher PB & Dent P 2002 Cyclin kinase inhibitor p21 potentiates bile acid-induced apoptosis in hepatocytes that is dependent on p53. Hepatology 36 39-48. (doi:10.1053/jhep.2002.33899)
55. Reel JR, Lamb IJ & Neal BH 1996 Survey and assessment of mammalian estrogen biological assays for hazard characterization. Fundamental and Applied Toxicology 34 288-305. (doi:10.1006/faat. 1996.0198)
56. Robertson DW, Katzenellenbogen JA, Long DJ, Rorke EA & Katzenellenbogen BS 1982 Tamoxifen antiestrogens. A comparison of the activity, pharmacokinetics, and metabolic activation of the cis and trans isomers of tamoxifen. Journal of Steroid Biochemistry 16 1-13. (doi:10.1016/0022-4731(82) 90137-6)
57. Rockett JC & Dix DJ 1999 Application of DNA arrays to toxicology. Environmental Health Perspectives 107 681-685. (doi:10.2307/ 3434462)
58. Shang Y & Brown M 2002 Molecular determinants for the tissue specificity of SERMs. Science 295 2465-2468. (doi:10.1126/science. 1068537)
59. Shiau AK, Barstad D, Loria PM, Cheng L, Kushner PJ, Agard DA & Greene GL 1998 The structural basis of estrogen receptor/coactivator recognition and the antagonism of this interaction by tamoxifen. Cell 95 927-937. (doi:10.1016/S0092-8674(00)81717-1) (Pubitemid 29019045)
60. Sourla A, Luo S, Labrie C, Belanger A & Labrie F 1997 Morphological changes induced by 6-month treatment of intact and ovari-ectomized mice with tamoxifen and the pure antiestrogen EM-800. Endocrinology 138 5605-5617. (doi:10.1210/en.138.12.5605)
61. Uetake Y, Terada Y, Matuliene J & Kuriyama R 2004 Interaction of Cep135 with a p50 dynactin subunit in mammalian centrosomes. Cell Motility and the Cytoskeleton 58 53-66. (doi:10.1002/cm.10175)
62. Vosse M, Renard F, Coibion M, Neven P, Nogaret JM & Hertens D 2002 Endometrial disorders in 406 breast cancer patients on tamoxifen: the case for less intensive monitoring. European Journal of Obstetrics, Gynecology, and Reproductive Biology 101 58-63. (doi:10.1016/S0301- 2115(01)00516-4)
63. Wang DY, McKague B, Liss SN & Edwards EA 2004 Gene expression profiles for detecting and distinguishing potential endocrine-disrupting compounds in environmental samples. Environmental Science and Technology 38 6396-6406. (doi:10.1021/es049235r)
64. Wang Y, Wang L, Iordanov H, Swietlicki EA, Zheng Q, Jiang S, Tang Y, Levin MS & Rubin DC 2006 Epimorphin(K/K) mice have increased intestinal growth, decreased susceptibility to dextran sodium sulfate colitis, and impaired spermatogenesis. Journal of Clinical Investigation 116 1535-1546. (doi:10.1172/JCI25442) (Pubitemid 43911008)
65. Weatherman RV, Chang CY, Clegg NJ, Carroll DC, Day RN, Baxter JD, McDonnell DP, Scanlan TS & Schaufele F 2002 Ligand-selective interactions of ER detected in living cells by fluorescence resonance energy transfer. Molecular Endocrinology 16 487-496. (doi:10.1210/ me.16.3.487)
66. Webb P, Nguyen P & Kushner PJ 2003 Differential SERM effects on corepressor binding dictate ERalpha activity in vivo. Journal of Biological Chemistry 278 6912-6920. (doi:10.1074/jbc.M208501200)
67. Wilker EW, van Vugt MA, Artim SA, Huang PH, Petersen CP, Reinhardt HC, Feng Y, Sharp PA, Sonenberg N, White FM et al. 2007 14-3- 3sigma controls mitotic translation to facilitate cytokinesis. Nature 446 329-332. (doi:10.1038/nature05584)
68. Yang YH & Speed T 2002 Design issues for cDNA microarray experiments.Nature Reviews. Genetics 3 579-588. (doi:10.1038/nrg863)