DDT and its metabolites alter gene expressions in human uterine cell lines through estrogen receptor-independent mechanisms

Environmental Health Perspectives

Volumn 110, Issue 12, 2002, Pages 1239-1245

  Frigo, Daniel E ^a   Burow, Matthew E ^a   Mitchell, Kamron A ^a,b   Chiang, Tung Chin ^a   McLachlan, John A ^a  

^a TULANE UNIVERSITY HEALTH SCIENCES CENTER   (United States)

^b TULANE UNIVERSITY   (United States)

Author keywords

AP 1; DDT; Early signaling; Estrogen receptor; Ishikawa cell line; Organochlorines

Indexed keywords

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHANE; 1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; ACETIC ACID DERIVATIVE; CHLORPHENOTANE; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR BETA; LUCIFERASE; TRANSCRIPTION FACTOR AP 1;

CELL LINE; CELL STIMULATION; CONTROLLED STUDY; DATA ANALYSIS; EMBRYO CELL; ENDOMETRIUM CARCINOMA; GENE ACTIVATION; GENE ACTIVITY; GENE EXPRESSION; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; KIDNEY CELL; METABOLITE; PRIORITY JOURNAL; PROMOTER REGION; REVIEW; TRANSACTIVATION; UTERUS;

EUKARYOTA;

EID: 0036908860     PISSN: 00916765     EISSN: None     Source Type: Journal    
DOI: 10.1289/ehp.021101239     Document Type: Review

References (105)

1. Ahlborg U.G. Lipworth L, Titus-Ernstoff L, Hsieh CC, Hanberg A, Baron J, Trichopoulos D, Adami HO. Organochlorine compounds in relation to breast cancer, endometrial cancer, and endometriosis: an assessment of the biological and epidemiological evidence. Crit Rev Toxicol 25;463-531 (1995).
2. Korach KS, Davis VL, Curtis SW, Bocchinfuso WP. Xenoestrogens and estrogen receptor action. In: Endocrine Toxicology (Thomas JA, Colby HD, eds). London: Taylor & Francis, 1997;181-211.
3. Schlessinger J. Cell signaling by receptor tyrosine kinases. Cell 103:211-225 (2000).
4. Hsu TC, Young MR, Cmarik J, Colburn NH. Activator protein 1 (AP-1)- and nuclear factor kappaB (NF-kappaB)-dependent transcriptional events in carcinogenesis. Free Radic Biol Med 28: 1338-1348 (2000).
5. Wisdom R. AP-1: one switch for many signals. Exp Cell Res 253:180-185 (1999).
6. Shi H, Teng CT. Characterization of a mitogen-response unit in the mouse lactoferrin gene promoter. J Biol Chem 269:12973-12980 (1994).
7. Kushner PJ, Agard DA, Greene GL, Scanlan TS, Shiau AK, Uht RM, Webb P. Estrogen receptor pathways to AP-1. J Steroid Biochem Mol Biol 74:311-317 (2000).
8. Giordano A, Avantaggiati ML. p300 and CBP: partners for life and death. J Cell Physiol 181:218-230 (1999).
9. Lee SK, Kim JH, Lee YC, Cheong J, Lee JW. Silencing mediator of retinoic acid and thyroid hormone receptors, as a novel transcriptional corepressor molecule of activating protein-1, nuclear factor-kappaB, and serum response factor. J Biol Chem 275:12470-12474 (2000).
10. Wisdom R, Johnson RS, Moore C. c-Jun regulates cell cycle progression and apoptosis by distinct mechanisms. Embo J 18:188-197 (1999).
11. Brown JR, Nigh E, Lee RJ, Ye H, Thompson MA, Saudou F, Postell RO, Greenberg ME. Fas family members induce cell cycle entry by activating cyclin D1. Mol Cell Biol 18:5609-5619 (1998).
12. Hibi M, Lin A, Smeal T, Minden A, Karin M. Identification of an oncoprotein- and UV-responsive protein kinase that binds and potentiates the c-Jun activation domain. Genes Dev 7:2135-2148 (1993).
13. Li XR, Chong AS, Wu J, Roebuck KA, Kumar A, Parrillo JE, Rapp UR, Kimberly RP, Williams JW, Xu X. Transcriptional regulation of Fas gene expression by GA-binding protein and AP-1 in T cell antigen receptor. CD3 complex-stimulated T cells. J Biol Chem 274:35203-35210 (1999).
14. Sawai H, Okazaki T, Yamamoto H, Okano H. Takeda Y, Tashima M, Sawada H, Okuma M, Ishikura H, Umehara H, et al. Requirement of AP-1 for ceramide-induced apoptosis in human leukemia HL-60 cells. J Biol Chem 270:27326-27331 (1995).
15. Wang Q, Ji Y, Wang X, Evers BM. Isolation and molecular characterization of the 5′-upstream region of the human TRAIL gene. Biochem Biophys Res Commun 276:466-471 (2000).
16. Kupfer D, Bulger WH. Interactions of chlorinated hydrocarbons with steroid hormones. Fed Proc 35:2603-2608 (1976).
17. Crews D, Willingham E, Skipper JK. Endocrine disruptors: present issues, future directions. Q Rev Biol 75:243-260 (2000).
18. Matthews J, Celius T, Halgren R, Zacharewski T. Differential estrogen receptor binding of estrogen substances: a species comparison. J Steroid Biochem Mol Biol 74:223-234 (2000).
19. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139:4252-4263 (1998).
20. Jaga K. What are the implications of the interaction between DDT and estrogen receptors in the body? Med Hypotheses 54:18-25 (2000).
21. Klotz DM, Beckman BS, Hill SM, McLachlan JA, Walters MR, Arnold SF, Identification of environmental chemicals with estrogenic activity using a combination of in vitro assays. Environ Health Perspect 104:1084-1089 (1996).
22. Gulledge CC, Burow ME, McLachlan JA. Endocrine disruption in sexual differentiation and puberty. What do pseudohermaphroditic polar bears have to do with the practice of pediatrics? Pediatr Clin N Am 48:1223-1240 (2001).
23. Fry DM, Toone CK, DDT-induced feminization of gull embryos. Science 213:922-924 (1981).
24. Tyler CR, Jobling S, Sumpter JP. Endocrine disruption in wildlife: a critical review of the evidence. Crit Rev Toxicol 28:319-361 (1988).
25. Guillette LJ Jr, Gross TS, Masson GR, Matter JM, Percival HF, Woodward AR. Developmental abnormalities of the gonad and abnormal sex hormone concentrations in juvenile alligators from contaminated and control lakes in Florida. Environ Health Perspect 102:680-688 (1994).
26. Guillete LJ Jr, Woodward AR, Crain DA, Pickford DB, Rooney AA, Percival HF. Plasma steroid concentrations and male phallus size in juvenile alligators from seven Florida lakes. Gen Comp Endocrinol 116:356-372 (1999).
27. Willingham E, Crews D. Sex reversal effects of environmentally relevant xenobiotic concentrations on the redeared slider turtle, a species with temperature-dependent sex determination. Gen Comp Endocrinol 113:429-435 (1999).
28. Wolff MS, Toniolo PG, Lee EW, Rivera M, Dubin N. Blood levels of organochlorine residues and risk of breast cancer. J Natl Cancer Inst 85:648-652 (1993).
29. Safe SH, Zacharewski T. Organochlorine exposure and risk for breast cancer. Prog Clin Biol Res 396: 133-145 (1997).
30. Cocco P. Kazerouni N, Zahm SH. Cancer mortality and environmental exposure to DDE in the United States. Environ Health Perspect 108:1-4 (2000).
31. Hruska KS, Furth PA, Seifer DB, Sharara FI, Flaws JA. Environmetal factor in infertility. Clin Obstet Gynecol 43:821-829 (2000).
32. Vandelac L, Bacon MH. Will we be taught ethics by our clones? The mutations of the living, from endocrine disruptors to genetics. Baillieres Best Pract Res Clin Obstet Gynaecol 13:571-592 (1999).
33. Rier SE, Martin DC, Bowman RE, Dmowski WP, Becker JL. Endometriosis in rhesus monkeys (Macaca mulatta) following chronic exposure to 2,3,7,8-tetrachlorodibenzo-p-dioxin. Fundam Appl Toxicol 21:433-441 (1993).
34. Korrick SA, Chen C, Damokosh AI, Ni J, Liu X, Cho SI, Altshul L, Ryan L, Xu X. Association of DDT with spontaneous abortion: a case-control study. Ann Epidemiol 11:491-496 (2001).
35. Beard J, Marshall S, Jong K, Newton R, Triplett-McBride T, Humphries B, Bronks R, 1,1,1-trichloro-2,2-bis (p-chlorophenyl)-ethane (DDT) and reduced bone mineral density. Arch Environ Health 55:177-180 (2000).
36. Skakkebaek NE, Rajpert-De Meyts E, Jorgensen N, Carlsen E, Petersen PM, Giwercman A, Andersen AG, Jensen TK, Andersson AM, Muller J. Germ cell cancer and disorders of spermatogenesis: an environmental connection? Apmis 106:3-11 (1998).
37. Metz R, Kouzarides T, Bravo R. A C-terminal domain in FosB, absent in FosB/SF and Fra-1, which is able to interact with the TATA binding proteins, is required for altered cell growth. Embo J 13:3832-3842 (1994).
38. Paech K, Webb P, Kuiper GG, Nilsson S, Gustafsson J, Kushner PJ, Scanlan TS. Differential ligand activation of estrogen receptors ERalpha and ERbeta at AP1 sites. Science 277:1508-1510 (1997).
39. Webb P, Nguyen P, Valentine C, Lopez GN, Kwok GR, McInerney E, Katzenellenbogen BS, Enmark E, Gustafsson JA, Nilsson S, et al. The estrogen receptor enhances AP-1 activity by two distinct mechanisms with different requirements for receptor transactivation functions. Mol Endocrinol 13:1672-1685 (1999).
40. Duan R, Porter W, Safe S. Estrogen-induced c-fos protooncogene expression in MCF-7 human breast cancer cells: role of estrogen receptor Sp1 complex formation. Endocrinology 139:1981-1990 (1998).
41. Duan R, Xie W, Safe S. Estrogen receptor-mediated activation of the serum response element in MCF-7 cells through MAPK-dependent phosphorylation of Elk-1. J Biol Chem 276:11590-11598 (2001).
42. Boettger-Tong HL, Murthy L, Stancel GM. Cellular pattern of c-fos induction by estradiol in the immature rat uterus. Biol Reprod 53:1398-1406 (1995).
43. Iguchi T, Fukazawa Y, Bern HA. Effects of sex hormones on oncogene expression in the vagina and on development of sexual dimorphism of the pelvis and anococcygenus muscle in the mouse. Environ Health Perspect 103(suppl 7):79-82 (1995).
44. Makela S, Santti R, Salo L, McLachlan JA. Phytoestrogens are partial estrogens agonists in the adult male mouse. Environ Health Perspect 103(suppl 7):123-127 (1995).
45. Tessier DM, Matsumura F. Increased ErbB-2 tyrosine kinase activity, MAPK phosphorylation, and cell proliferation in the prostate cancer cell line LNCaP following treatment by select pesticides. Toxicol Sci 60:38-43 (2001).
46. Ramamoorthy K, Vyhlidal C, Wang F, Chen I, Safe S, McDonnell DP, Leonard LS, Gaido KW. Additive estrogenic activities of a binary mixture of 2′,4′,6′-trichloro- and 2′,3′,4′,5′-tetrachloro-4-biphenylol. Toxicol Appl Pharmacol 147:93-100 (1997).
47. Hatakeyama M, Matsumura F. Correlation between the activation of Neu tyrosine kinase and promotion of foci formation induced by selected organochlorine compounds in the MCF-7 model system. J Biochem Mol Toxicol 13:296-302 (1999).
48. Enan E, Matsumura F. Activation of c-Neu tyrosine kinase by o,p'-DDT and beta-HCH in cell-free and intact cell preparations from MCF-7 human breast cancer cells. J Biochem Mol Toxicol 12:83-92 (1998).
49. Chuang LF, Chuang RY. Heptachlor and the mitogen-activated protein kinase module in human lymphocytes. Toxicology 128:17-23 (1998).
50. Shen K, Novak RF. DDT stimulates c-erbB2, c-met, and STATS tyrosine phosphorylation, Grb2-Sos association, MAPK phosphorylation, and proliferation of human breast epithelial cells. Biochem Biophys Res Commun 231:17-21 (1997).
51. Shen K, Novak RF. Differential effects of aroclors and DDT on growth factor gene expression and receptor tyrosine kinase activity in human breast epithelial cells. Adv Exp Med Biol 407:295-302 (1997).
52. Bagchi D, Bagchi M, Tang L, Stohs SJ. Comparative in vitro and in vivo protein kinase C activation by selected pesticides and transition metal salts. Toxiol Lett 91:31-37 (1997).
53. Shekhar PV, Werdell J, Basrur VS. Environmental estrogen stimulation of growth and estrogen receptor function in preneoplastic and cancerous human breast cell lines. J Natl Cancer Inst 89:1774-1782 (1997).
54. Mousa MA, Ganey PE, Quensen JF III, Madhukar BV, Chou K, Giesy JP, Fischer LJ, Boyd SA. Altered biologic activities of commercial polychlorinated biphenyl mixtures after microbial reductive dechlorination. Environ Health Perspect 106(suppl 6):1409-1418 (1998).
55. Barron S, Serratosa J, Tusell JM. Regulation of c-fos expression by convulsants and hexachlorocyclohexane isomers in primary cultures of cortical neurons. J Neurochem 64:1708-1714 (1995).
56. Ghosh D, Taylor JA, Greene JA, Lubahn DB. Methoxychlor stimulates estrogen-responsive messenger ribonucleic acids in mouse uterus a non-estrogen receptor (non-ER) alpha and non-ER beta mechanism. Endocrinology 140:3526-3533 (1999).
57. Das SK, Taylor JA, Korach KS, Paria BC, Dey SK, Lubahn DB. Estrogenic responses in estrogen receptor-alpha deficient mice reveal a distinct estrogen signaling pathway. Proc Natl Acad Sci USA 94:12786-12791 (1997).
58. Devanesan P, Santen RJ, Bocchinfuso WP, Korach KS, Rogan EG, Cavalieri E. Cathechol estrogen metabolites and conjugates in mammary tumors and hyperplastic tissue from estrogen receptor-alpha knock-out (ERKO)/Wnt-1 mice: implications for initiation of mammary tumors. Carcinogenesis 22:1573-1576 (2001).
59. Falconer RL, Bidleman TF, Szeto SY. Chiral pesticides in soils of the Fraser Valley, British Columbia. J Agric Food Chem 45:1946-1951 (1997).
60. Aigner EJ, Leone AD, Falconer RL. Concentrations and enantiomeric ratios of organochlorine pesticides in soils from the U.S. corn belt. Environ Sci Technol 32:1162-1168 (1998).
61. U.S.G.S. Summary Statistics for Organochlorine Compounds in Whole Fish, Vols 1992-1998. Washington, DC:U.S. Geological Survey, 2001.
62. Burow ME, Weldon CB, Chiang TC, Tang Y, Collins-Burow BM, Rolfe K, Li S, McLachlan JA, Beckman BS. Differences in protein kinase C and estrogen receptor alpha, beta expression and signaling correlate with apoptotic sensitivity of MCF-7 breast cancer cell variants. Int J Oncol 16:1179-1187 (2000).
63. Collins-Burow BM, Burow ME, Duong BN, McLachlan JA. Estrogenic and antiestrogenic activities of flavonoid phytochemicals through estrogen receptor binding-dependent and -independent mechanisms. Nutr Cancer 38:229-244 (2000).
64. Burow ME, Boue SM, Collins-Burow BM, Melnik LI, Duong BN, Carter-Wientjes CH, Li S, Wiese TE, Cleveland TE, McLachlan JA. Phytochemical glyceollins, isolated from soy, mediate antihormonal effects through estrogen receptor alpha and beta. J Clin Endocrinol Metab 86:1750-1758 (2001).
65. Burow ME, Weldon CB, Collins-Burow BM, Ramsey N, McKee A, Klippel A, McLachlan JA, Clejan S, Beckman BS. Cross-talk between phosphatidylinositol 3-kinase and sphingomyelinase pathways as a mechanism for cell survival/death decisions. J Biol Chem 275:9628-9635 (2000).
66. Burow ME, Tang Y, Collins-Burow BM, Krajewski S, Reed JC, McLachlan JA, Beckman BS. Effects of environmental estrogens on tumor necrosis factor alpha-mediated apoptosis in MCF-7 cells. Carcinogenesis 20:2057-2061 (1999).
67. Thompson EW, Paik S, Brunner N, Sommers CL, Zugmaier G, Clarke R, Shima TB, Torri J, Donahue S, Lippman ME, et al. Association of increased basement membrane invasiveness with absence of estrogen receptor and expression of vimentin in human breast cancer cell lines. J Cell Physiol 150:534-544 (1992).
68. MacGregor Schafer J, Liu H, Levenson AS, Horiguchi J, Chen Z, Jordan VC. Estrogen receptor alpha mediated induction of the transforming growth factor alpha gene by estradiol and 4-hydroxytamoxifen in MDA-MB-231 breast cancer cells. J Steroid Biochem Mol Biol 78:41-50 (2001).
69. Yoon K, Pallaroni L, Stoner M, Gaido K, Safe S. Differential activation of wild-type and variant forms of estrogen receptor alpha by synthetic and natural estrogenic compounds using a promoter containing three estrogen-responsive elements. J Steroid Biochem Mol Biol 78:25-32 (2001).
70. Tyulmenkov VV, Jernigan SC, Klinge CM. Comparison of transcriptional synergy of estrogen receptors alpha and beta from multiple tandem estrogen response elements. Mol Cell Endocrinol 165:151-161 (2000).
71. Tyulmenkov VV, Klinge CM. Estrogen receptors alpha and beta exhibit different estradiol and estrogen response element binding in the presence of nonspecific DNA. Arch Biochem Biophys 390:253-264 (2001).
72. Hall JM, McDonnell DP. The estrogen receptor beta-isoform (ERbeta) of the human estrogen receptor modulates ERalpha transcriptional activity and is a key regulator of the cellular response to estrogens and antiestrogens. Endocrinology 140:5566-5578 (1999).
73. McInerney EM, Weis KE, Sun J, Mosselman S, Katzenellenbogen BS. Transcription activation by the human estrogen receptor subtype beta (ER beta) studied with ER beta and ER alpha receptor chimeras. Endocrinology 139:4513-4522 (1998).
74. Cerillo G, Rees A, Manchanda N, Reilly C, Brogan I, White A, Needham M. The oestrogen receptor regulates NFkappaB and AP-1 activity in a cell-specific manner. J Steroid Biochem Mol Biol 67:79-88 (1998).
75. Ware GW. An Introduction to Insecticides. Minneapolis, MN:University of Minnesota Press, 2001.
76. Mitra J, Raghu K. Long-term DDT pollution in tropical soils: effect of DDT and degradation products on soil microbial activities leading to soil fertility. Bull Environ Contam Toxicol 60:585-591 (1998).
77. ATSDR. Toxicological Profile for 4,4′-DDT, 4,4′-DDE, 4,4′-DDD. Atlanta, GA:Agency for Toxic Substances and Disease Registry, 1992.
78. Sundlof SF, Forrester DJ, Thompson NP, Collopy MW. Residues of chlorinated hydrocarbons in tissues of raptors in Florida. J Wildl Dis 22:71-82 (1986).
79. Provini A, Galassi S. Polychlorinated biphenyls and chlorinated pesticides in bird eggs from Calabria (southern Italy). Ecotoxicol Environ Saf 43:91-97 (1999).
80. Flanagan L, Van Weelden K, Ammerman C, Ethier SP, Welsh J. SUM-159PT cells: a novel estrogen independent human breast cancer model system. Breast Cancer Res Treat 58:193-204 (1999).
81. Jenster G. Ligand-independent activation of the androgen receptor in prostate cancer by growth factors and cytokines. J Pathol 191:227-228 (2000).
82. Huang C, Ma WY, Young MR, Colburn N, Dong Z. Shortage of mitogen-activated protein kinase is responsible for resistance to AP-1 transactivation and transformation in mouse JB6 cells. Proc Natl Acad Sci USA 95:156-161 (1998).
83. Diel P, Schulz T, Smolnikar K, Strunck E, Vollmer G, Michna H. Ability of xeno- and phytoestrogens to modulate expression of estrogen-sensitive genes in rat uterus: estrogenicity profiles and uterotropic activity. J Steroid Biochem Mol Biol 73:1-10 (2000).
84. Wunsche W, Tenniswood MP, Schneider MR, Vollmer G. Estrogenic regulation of clusterin mRNA in normal and malignant endometrial tissue. Int J Cancer 76:684-688 (1998).
85. Strunck E, Stemmann N, Hopert A, Wunsche W, Frank K, Vollmer G. Relative binding affinity does not predict biological response to xenoestrogens in rat endometrial adenocarcinoma cells. J Steroid Biochem Mol Biol 74:73-81 (2000).
86. Das SK, Tan J, Johnson DC, Dey SK. Differential spatiotemporal regulation of lactoferrin and progesterone receptor genes in the mouse uterus by primary estrogen, catechol estrogen, and xenoestrogen. Endocrinology 139:2905-2915 (1998).
87. Shi H, Teng C. Promoter-specific activation of mouse lactoferrin gene by epidermal growth factor involves two adjacent regulatory elements. Mol Endocrinol 10:732-741 (1996).
88. Schnell N, Krems B, Entian KD. The PAR1 (YAP1/SNQ3) gene of Saccharomyces cerevisiae, a c-jun homologue, is involved in oxygen metabolism. Curr Genet 21:269-273 (1992).
89. Galan A, Garcia-Bermejo L, Vilaboa NE, de Blas E, Aller P. Uncoupling of apoptosis and Jun/AP-1 activity in human promonocytic cells treated with DNA-damaging and stress-inducing agents. Eur J Cell Biol 79:1-9 (2000).
90. Shukla GS, Shukla A, Potts RJ, Osier M, Hart BA, Chiu JF, Cadmium-mediated oxidative stress in alveolar epithelial cells induces the expression of gamma-glutamylcysteine synthetase catalytic subunit and glutathione S-transferase alpha and pi isoforms: potential role of activator protein-1. Cell Biol Toxicol 16:347-362 (2000).
91. Peverali FA, Basdra EK, Papavassiliou AG. Stretch-mediated activation of selective MAPK subtypes and potentiation of AP-1 binding in human osteoblastic cells. Mol Med 7:68-78 (2001).
92. Filardo EJ, Quinn JA, Bland KI, Frackelton AR Jr. Estrogen-induced activation of Erk-1 and Erk-2 requires the G protein-coupled receptor homolog, GPR30, and occurs via trans-activation of the epidermal growth factor receptor through release of HB-EGF. Mol Endocrinol 14:1649-1660 (2000).
93. Caldwell JD, O'Rourke ST, Morris M, Walker CH, Carr RB, Faggin BM, Mason GA. Steroid effects at the membrane level on oxytocin systems. Ann N Y Acad Sci 814:282-286 (1997).
94. Improta-Brears T, Whorton AR, Codazzi F, York JD, Meyer T, McDonnell DP. Estrogen-induced activation of mitogen-activated protein kinase requires mobilization of intracellular calcium. Proc Natl Acad Sci USA 96:4686-4991 (1999).
95. Stoica A, Katzenellenbogen BS, Martin MB. Activation of estrogen receptor-alpha by the heavy metal cadmium. Mol Endocrinol 14:545-553 (2000).
96. Alam J. Multiple elements within the 5′ distal enhancer of the mouse heme oxygenase-1 gene mediate induction by heavy metals. J Biol Chem 269:25049-25056 (1994).
97. Hague F, Matifat F, Louvet L, Brule G, Collin T. The carcinogen Cd(2+) activates InsP(3)-mediated Ca(2+) release through a specific metal ion receptor in Xenopus oocyte. Cell Signal 12:419-424 (2000).
98. Nadal A, Ropero AB, Laribi O, Maillet M, Fuentes E, Soria B. Nongenomic actions of estrogens and xenoestrogens by binding at a plasma membrane receptor unrelated to estrogen receptor alpha and estrogen receptor beta. Proc Natl Acad Sci USA 97:11603-11608 (2000).
99. Kelly MJ, Levin ER. Rapid actions of plasma membrane estrogen receptors. Trends Endocrinol Metab 12:152-156 (2001).
100. 2+ channels in smooth muscle cells. Faseb J 12:613-619 (1998).
101. Muramatsu M, Inoue S. Estrogen receptors: how do they control reproductive and nonreproductive functions? Biochem Biophys Res Commun 270:1-10 (2000).
102. Martin MB, Franke TF, Stoica GE, Chambon P, Katzenellenbogen BS, Stoica BA, McLemore MS, Olivo SE, Stoica A. A role for Akt in mediating the estrogenic functions of epidermal growth factor and insulin-like growth factor I. Endocrinology 141:4503-4511 (2000).
103. Ignar-Trowbridge DM, Nelson KG, Bidwell MC, Curtis SW, Washburn TF, McLachlan JA, Korach KS. Coupling of dual signaling pathways: epidermal growth factor action involves the estrogen receptor. Proc Natl Acad Sci USA 89:4658-4662 (1992).
104. Ignar-Trowbridge DM, Pimentel M, Parker MG, McLachlan JA, Korach KS. Peptide growth factor crosstalk with the estrogen receptor requires the A/B domain and occurs independently of protein kinase C or estradiol. Endocrinology 137:1735-1744 (1996).
105. Campbell RA, Bhat-Nakshatri P, Patel NM, Constantinidou D, Ali S, Nakshatri H. Phosphatidylinositol 3-kinase/AKT-mediated activation of estrogen receptor alpha: a new model for anti-estrogen resistance. J Biol Chem 276:9817-9824 (2001).