Strengths and weaknesses of in vitro assays for estrogenic and androgenic activity

Best Practice and Research: Clinical Endocrinology and Metabolism

Volumn 20, Issue 1, 2006, Pages 15-33

  Soto, Ana M ^a   Maffini, Maricel V ^a   Schaeberle, Cheryl M ^a   Sonnenschein, Carlos ^a  

^a TUFTS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

A SCREEN; Alkylphenols; Antiandrogens; Antioxidants; Cell proliferation; E SCREEN; Endocrine disruptors; Endosulfan; Phthalates; Xenoestrogens

Indexed keywords

ALPHA FETOPROTEIN; ANDROGEN; ANDROGEN BINDING PROTEIN; ANDROSTENEDIONE; ANTIANDROGEN; ANTIESTROGEN; DIETHYLSTILBESTROL DERIVATIVE; ENDOCRINE DISRUPTOR; ESTRADIOL; ESTROGEN; ESTROGEN BINDING PROTEIN; ESTROGEN RECEPTOR; GESTAGEN; GLUCOCORTICOID RECEPTOR; HORMONE RECEPTOR; HYDROXYFLUTAMIDE; HYDROXYTAMOXIFEN; METHYLTESTOSTERONE; METRIBOLONE; PROGESTERONE RECEPTOR; SEX HORMONE BINDING GLOBULIN; TRENBOLONE; XENOBIOTIC AGENT;

BIOASSAY; BREAST CANCER; CANCER INCIDENCE; CELL CULTURE; CELL DIFFERENTIATION; CELL PROLIFERATION; ENDOCRINE SYSTEM; ESTROGEN ACTIVITY; GENITAL MALFORMATION; GENITAL SYSTEM; HORMONAL REGULATION; HORMONE INHIBITION; HORMONE METABOLISM; HORMONE SYNTHESIS; HUMAN; IN VITRO STUDY; NONHUMAN; RECEPTOR BINDING; REVIEW; SENSITIVITY ANALYSIS; SPERM; TESTIS CANCER; TISSUE SPECIFICITY;

ANDROGEN ANTAGONISTS; ANDROGENS; ANIMALS; BINDING, COMPETITIVE; BIOLOGICAL ASSAY; BREAST NEOPLASMS; CELL LINE; CELL LINE, TUMOR; CELL PROLIFERATION; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG EVALUATION, PRECLINICAL; ENDOCRINE DISRUPTORS; ESTROGEN ANTAGONISTS; ESTROGEN RECEPTOR ALPHA; ESTROGENS; FEMALE; GENES, REPORTER; HUMANS; MALE; RECEPTORS, ESTROGEN;

EID: 33644641663     PISSN: 1521690X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.beem.2005.09.001     Document Type: Review

References (80)

1. A.M. Soto H. Justicia J.W. Wray C. Sonnenschein p-Nonyl-phenol: An estrogenic xenobiotic released from 'modified' polystyrene Environmental Health Perspectives 92 1991 167-173
2. A.M. Soto K.L. Chung C. Sonnenschein The pesticides endosulfan, toxaphene, and dieldrin have estrogenic effects on human estrogen sensitive cells Environmental Health Perspectives 102 1994 380-383
3. A.M. Soto C. Sonnenschein K.L. Chung et al. The E-SCREEN assay as a tool to identify estrogens: An update on estrogenic environmental pollutants Environmental Health Perspectives 103 1995 113-122
4. A.M. Soto C.L. Michaelson N.V. Prechtl et al. Assay to measure estrogen and androgen agonists and antagonists J. del Mazo In Vitro Germ Cell Developmental Toxicology: From Science to Social and Industrial Demand 1998 Plenum Press Publishing Co. New York, NY 9-28
5. M. Schlumpf B. Cotton M. Conscience et al. In vitro and in vivo estrogenicity of UV screens Environmental Health Perspectives 109 2001 239-244
6. A.L. Herbst H.A. Bern Developmental Effects of Diethylstilbestrol (DES) in Pregnancy 1988 Thieme-Stratton New York, NY
7. R. Mittendorf Teratogen update: Carcinogenesis and teratogenesis associated with exposure to diethylstilbestrol (DES) in utero Teratology 51 1995 435-445
8. Wingspread consensus statement T. Colborn C. Clement Chemically Induced Alterations in Sexual and Fuctional Development: The Wildlife/Human Connection 1992 Princeton Scientific Publishing Princeton, NJ 1-8
9. E. Carlsen A. Giwercman N. Keinding N.E. Skakkebaek Evidence for the decreasing quality of semen during the past 50 years British Medical Journal 305 1992 609-612
10. A. Giwercman E. Carlsen N. Keiding N.E. Skakkebaek Evidence for increasing incidence of abnormalities of the human testis: A review Environmental Health Perspectives 101 1993 65-71
11. R.M. Sharpe N.E. Skakkebaek Are oestrogens involved in falling sperm count and disorders of the male reproductive tract? Lancet 341 1993 1392-1395
12. W. Körner U. Bolz W. Sussmuth et al. Input/output balance of estrogenic active compounds in a major municipal sewage plant in Germany Chemosphere 40 2000 1131-1142
13. T. Colborn F.S. vom Saal A.M. Soto Developmental effects of endocrine-disrupting chemicals in wildlife and humans Environmental Health Perspectives 101 1993 378-384
14. M.E. Baker K.L. Medlock D.M. Sheehan Flavonoids inhibit estrogen binding to rat alpha-fetoprotein Proceedings of the Society for Experimental Biology and Medicine 217 1998 317-321
15. D.M. Sheehan M. Young Diethylstilbestrol and estradiol binding to serum albumin and pregnancy plasma of rat and human Endocrinology 104 1979 1442-1446
16. G.G.J.M. Kuiper J.G. Lemmen B. Carlsson et al. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta Endocrinology 139 1998 4252-4263
17. S. Dupont A. Krust A. Gansmuller et al. Effect of single and compound knockouts of estrogen receptors alpha (ERalpha) and beta (ERbeta) on mouse reproductive phenotypes Development 127 2000 4277-4291
18. G.G. Kuiper B. Carlsson K. Grandien et al. Comparison of the ligand binding specificity and transcript tissue distribution of estrogen receptors alpha and beta Endocrinology 138 1997 863-870
19. K.F. Koehler L.A. Helguero L.A. Haldosen et al. Reflections on the discovery and significance of estrogen receptor beta Endocrine Reviews 26 2005 465-478
20. A.M. Norfleet C.H. Clarke B. Gametchu C.S. Watson Antibodies to the estrogen receptor-alpha modulate rapid prolactin release from rat pituitary tumor cells through plasma membrane estrogen receptors FEBS Journal 14 2004 157-165
21. C.E. Powell A.M. Soto C. Sonnenschein Identification and characterization of membrane estrogen receptor from MCF7 estrogen-target cells The Journal of Steroid Biochemistry Molecular Biology 77 2001 97-108
22. C. Sonnenschein A.M. Soto C.L. Michaelson Human serum albumin shares the properties of estrocolyone-I, the inhibitor of the proliferation of estrogen-target cells The Journal of Steroid Biochemistry Molecular Biology 59 1996 147-154
23. C.E. Powell A.M. Soto C.L. Michaelson et al. Plasma membrane-resident albumin binding protein associated with the proliferation of MCF7 serum-sensitive cells Steroids 68 2003 487-496
24. N.N. Bulayeva C.S. Watson Xenoestrogen-induced ERK-1 and ERK-2 activation via multiple membrane-initiated signaling pathways Environmental Health Perspectives 112 2004 1481-1487
25. C.S. Watson N.N. Bulayeva A.L. Wozniak C.C. Finnerty Signaling from the membrane via membrane estrogen receptor-alpha: Estrogens, xenoestrogens, and phytoestrogens Steroids 70 2005 364-371
26. C. Desbrow E.J. Routledge G.C. Brighty et al. Identification of estrogenic chemicals in STW effluent. 1. Chemical fractionation and in vitro biological screening Environmental Science and Technology 32 1998 1549-1558
27. A.M. Soto J.M. Calabro N.V. Prechtl et al. Androgenic and estrogenic activity in cattle feedlot effluent receiving water bodies of eastern Nebraska, USA Environmental Health Perspectives 112 2004 346-352
28. C. Sonnenschein A.M. Soto M.F. Fernandez et al. Development of a marker of estrogenic exposure in human serum Clinical Chemistry 41 1995 1888-1895
29. A.M. Soto M.F. Fernandez M.F. Luizzi et al. Developing a marker of exposure to xenoestrogen mixtures in human serum Environmental Health Perspectives 105 1997 647-654
30. J.M. Ibarluzea M.F. Fernández L. Santa-Marina et al. Breast cancer risk in the combined effect of environmental estrogens Cancer Causes Control 15 2004 591-600
31. R. Hertz The estrogen problem-retrospect and prospect J.A. McLachlan Estrogens in the Environment II - Influences on Development 1985 Elsevier New York, NY 1-11
32. R. Bolger T.E. Wiese K. Ervin et al. Rapid screening of environmental chemicals for estrogen receptor binding capacity Environmental Health Perspectives 106 1998 551-557
33. A.M. Soto C. Sonnenschein Mechanism of estrogen action on cellular proliferation: Evidence for indirect and negative control on cloned breast tumor cells Biochemical and Biophysical Research Communications 122 1984 1097-1103
34. G.C.A. Reiner B.S. Katzenellenbogen R.D. Bindal J.A. Katzenellenbogen Biological activity and receptor binding of a strongly interacting estrogen in human breast cancer cells Cancer Research 44 1984 2302-2308
35. J.M. Jeltsch M. Roberts C. Scatz et al. Structure of the human oestrogen-responsive gene pS2 Nucleic Acids Research 15 1987 1401-1414
36. A.M. Soto T.-M. Lin H. Justicia et al. An 'in culture' bioassay to assess the estrogenicity of xenobiotics T. Colborn C. Clement Chemically Induced Alterations in Sexual Development: The Wildlife/Human Connection 1992 Princeton Scientific Publishing Princeton, NJ 295-309
37. C.M. Markey C.L. Michaelson E.C. Veson et al. The mouse uterotropic assay: A re-evaluation of its validity in assessing the estrogenicity of bisphenol A Environmental Health Perspectives 109 2001 55-60
38. R.R. Newbold W.N. Jefferson E. Padilla-Banks et al. Cell response endpoints enhance sensitivity of the immature mouse uterotropic assay Reproductive Toxicology 15 2001 245-252
39. D. Pugazhendhi G.S. Pope P.D. Darbre Oestrogenic activity of p-hydroxybenzoic acid (common metabolite of paraben esters) and methylparaben in human breast cancer cell lines Journal of Applied Toxicology 24 2005 301-309
40. M. Pons D. Gagne J.C. Nicolas M. Mehtali A new cellular model of response to estrogens: A bioluminescent test to characterize (anti) estrogen molecules Biotechniques 9 1990 450-459
41. D. Gagne P. Balaguer E. Demirpence et al. Stable luciferase transfected cells for studying steroid receptor biological activity Journal of Bioluminescence and Chemiluminescence 9 1994 201-209
42. E. Badia M.J. Duchesne S. Fournier-Bidoz et al. Hydroxytamoxifen induces a rapid and irreversible inactivation of an estrogenic response in an MCF-7-derived cell line Cancer Research 54 1994 5860-5866
43. J. Oliva S.E. Messaoudi F. Pellestor et al. Involvement of HP1alpha protein in irreversible transcriptional inactivation by antiestrogens in breast cancer cells FEBS Letters 579 2005 4278-4286
44. S.P. Shiau A. Glasebrook S.D. Hardikar et al. Activation of the human estrogen receptor by estrogenic and antiestrogenic compounds in Saccharomyces cerevisiae: A positive selection system Gene 179 1996 205-210
45. J.R. Zysk B. Johnson B.A. Ozenberger et al. Selective uptake of estrogenic compounds by saccharomyces cerevisiae: A mechanism for antiestrogen resistance in yeast expressing the mammalian estrogen receptor Endocrinology 136 1995 1323-1326
46. K.W. Gaido L.S. Leonard S. Lovell et al. Evaluation of chemicals with endocrine modulating activity in a yeast-based steroid hormone receptor gene transcription assay Toxicology and Applied Pharmacology 143 1997 205-212
47. H.R. Andersen A.M. Andersson S.F. Arnold et al. Comparison of short-term estrogenicity tests for identification of hormone-disrupting chemicals Environmental Health Perspectives 107 supplement 1 1999 89-108
48. H. Fang W. Tong R. Perkins et al. Quantitative comparisons of in vitro assays for estrogenic activities Environmental Health Perspectives 108 2000 723-729
49. N. Rajapakse E. Silva M. Scholze A. Kortenkamp Deviation from additivity with estrogenic mixtures containing 4-nonylphenol and 4-tert-octylphenol detected in the E-SCREEN assay Environmental Science and Technology 38 2004 6343-6352
50. T.H. Rasmussen F. Nielsen H.R. Andersen et al. Assessment of xenoestrogenic exposure by a biomarker approach: Application of the E-Screen bioassay to determine estrogenic response of serum extracts Environmental Health 2 2003 12
51. J.T. Dalton A. Mukherjee Z. Zhu et al. Discovery of nonsteroidal androgens Biochemical and Biophysical Research Communications 244 1998 1-4
52. J.C. Cook L.S. Mullin S.R. Frame L.B. Biegel Investigation of a mechanism for Leydig cell tumorigenesis by linuron in rats Toxicology and Applied Pharmacology 119 1993 195-204
53. P.A. Fail S.W. Pearce S.A. Anderson et al. Endocrine and reproductive toxicity of vinclozolin (vin) in male Long-Evans hooded rats Fundamental and Applied Toxicology 15 1995 293
54. L.E. Gray Jr J.S. Ostby W.R. Kelce Developmental effects of an environmental antiandrogen: The fungicide vinclozolin alters sex differentiation of the male rat Toxicology and Applied Pharmacology 129 1994 46-52
55. W.R. Kelce C.R. Stone S.C. Laws et al. Persistent DDT metabolite p,p′-DDE is a potent androgen receptor antagonist Nature 375 1995 581-585
56. A.M. Vinggaard C. Nellemann M. Dalgaard et al. Antiandrogenic effects in vitro and in vivo of the fungicide prochloraz Toxicological Sciences 69 2002 344-353
57. W.R. Kelce E. Monosson M.P. Gamcsik et al. Environmental hormone disruptors: Evidence that vinclozolin developmental toxicity is mediated by antiandrogenic metabolites Toxicology and Applied Pharmacology 126 1994 276-285
58. A.M. Vinggaard C. Hnida J.C. Larsen Environmental polycyclic aromatic hydrocarbons affect androgen receptor activation in vitro Toxicology 145 2000 159-169
59. A.G. Saltzman R.A. Hiipakka C. Chang S. Liao Androgen repression of the production of a 29-kilodalton protein and its mRNA in the rat ventral prostate The Journal of Biological Chemistry 262 1987 432-437
60. F. Paris P. Balaguer B. Térouanne et al. Phenylphenols, biphenols, bisphenol-A and 4-tert-octylphenol exhibit alpha and beta estrogen activities and antiandrogen activity in reporter cell lines Molecular and Cellular Endocrinology 193 2002 43-49
61. H. Fang W. Tong W.S. Branham et al. Study of 202 natural, synthetic, and environmental chemicals for binding to the androgen receptor Chemical Research in Toxicology 16 2003 1338-1358
62. J.S. Horoszewicz S.S. Leong E. Kawinski et al. LNCaP model of human prostatic carcinoma Cancer Research 43 1983 1809-1818
63. J. Veldscholte M.M. Voorhorst-Ogink J. Bolt-de Vries et al. Unusual specificity of the androgen receptor in the human prostate tumor cell line LNCaP: High affinity for progestagenic and estrogenic steroids Biochimica et Biophysica Acta 1052 1990 187-194
64. J. Veldscholte C. Ris-Stalpers G.G. Kuiper et al. A mutation in the ligand binding domain of the androgen receptor of human LNCaP cells affects steroid binding characteristics and response to anti-androgens Biochemical and Biophysical Research Communications 173 1990 534-540
65. C. Sonnenschein N. Olea M.E. Pasanen A.M. Soto Negative controls of cell proliferation: Human prostate cancer cells and androgens Cancer Research 49 1989 3474-3481
66. N. Olea K. Sakabe A.M. Soto C. Sonnenschein The proliferative effect of 'anti-androgens' on the androgen-sensitive human prostate tumor cell line LNCaP Endocrinology 126 1990 1457-1463
67. A.M. Soto T.M. Lin K. Sakabe et al. Variants of the human prostate LNCaP cell line as a tool to study discrete components of the androgen-mediated proliferative response Oncology Research 7 1995 545-558
68. C.Y. Young B.T. Montgomery P.E. Andrews et al. Hormonal regulation of prostate-specific antigen messenger RNA in human prostatic adenocarcinoma cell line LNCaP Cancer Research 51 1991 3748-3752
69. B.T. Montgomery C.Y.F. Young D.L. Bilhartz et al. Hormonal regulation of prostate-specific antigen (PSA) glycoprotein in the human prostatic adenocarcinoma cell line, LNCaP Prostate 21 1992 63-73
70. J. Szelei J. Jimenez A.M. Soto et al. Androgen-induced inhibition of proliferation in human breast cancer MCF7 cells transfected with androgen receptor Endocrinology 138 1997 1406-1412
71. A.M. Soto C. Sonnenschein Cell proliferation of estrogen-sensitive cells: The case for negative control Endocrine Reviews 8 1987 44-52
72. M.V. Maffini P. Geck C.E. Powell et al. Mechanism of androgen action on cell proliferation AS3 protein as a mediator of proliferative arrest in the rat prostate Endocrinology 143 2002 2708-2714
73. P. Geck M.V. Maffini J. Szelei et al. Androgen-induced proliferative quiescence in prostate cancer: The role of AS3 as its mediator Proceedings of the National Academy of Sciences of the United States of America 97 2000 10185-10190
74. V.S. Wilson K. Bobseine C.R. Lambright L.E. Gray Jr. A novel cell line, MDA-kb2, that stably expresses an androgen- and glucocorticoid-responsive reporter for the detection of hormone receptor agonists and antagonists Toxicological Sciences 66 2002 69-81
75. B. Térouanne B. Tahiri V. Georget et al. A stable prostatic bioluminescent cell line to investigate androgen and antiandrogen effects Molecular and Cellular Endocrinology 160 2000 39-49
76. E. Sonneveld J.H. Jansen J.A.C. Riteco et al. Development of androgen- and estrogen-responsive bioassays, members of a panel of human cell line-based highly selective steroid-responsive bioassays Toxicological Sciences 83 2005 136-148
77. W. Körner A.M. Vinggaard B. Térouanne et al. Interlaboratory comparison of four in vitro assays for assessing androgenic and antiandrogenic activity of environmental chemicals Environmental Health Perspectives 112 2004 695-702
78. B. Terouanne B. Tahiri V. Georget et al. A stable prostatic bioluminescent cell line to investigate androgen and antiandrogen effects Molecular and Cellular Endocrinology 160 2000 39-49
79. EDSTAC Endocrine Disruptor Screening and Testing Advisory Committee Final Report 1998 US Environmental Protection Agency Washington, DC
80. R. Ma B. Cotton W. Lichtensteiger M. Schlumpf UV filters with antagonistic action at androgen receptors in the MDA-kb2 cell transcriptional-activational assay Toxicological Sciences 74 2003 43-50