Bacterial biosensors for evaluating potential impacts of estrogenic endocrine disrupting compounds in multiple species

Environmental Toxicology

Volumn 28, Issue 4, 2013, Pages 179-189

  Gierach, Izabela ^a,b   Shapero, Kayle ^a   Eyster, Thomas W ^a   Wood, David W ^a,b  

^a Princeton University   (United States)

^b Ohio State University   (United States)

Author keywords

Bacterial biosensor; Endocrine disruptors; Estrogen receptor; Homo sapiens; Solea solea; Sus scrofa

Indexed keywords

BACTERIAL BIOSENSOR; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR; HOMO SAPIENS; SOLEA SOLEA; SUS SCROFA;

BACTERIA; BINDING ENERGY; BIODIVERSITY; ENDOCRINOLOGY; ESCHERICHIA COLI; LIGANDS; MAMMALS;

BIOSENSORS;

4,4' ISOPROPYLIDENEDIPHENOL; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR BETA;

BIOASSAY; COLIFORM BACTERIUM; DOSE-RESPONSE RELATIONSHIP; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; GROWTH RATE; LIGAND; PHENOTYPE; PIG;

AGONIST; ANIMAL CELL; ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BINDING AFFINITY; CELL DIFFERENTIATION; CONTROLLED STUDY; ESCHERICHIA COLI; HUMAN; HUMAN CELL; LIGAND BINDING; MICROBIAL ELECTRODE; NONHUMAN; PRIORITY JOURNAL; SOLEA SOLEA; SWINE;

ANIMALS; BENZHYDRYL COMPOUNDS; BIOSENSING TECHNIQUES; ENDOCRINE DISRUPTORS; ESCHERICHIA COLI; ESTROGEN RECEPTOR BETA; FLATFISHES; HIGH-THROUGHPUT SCREENING ASSAYS; HUMANS; LIGANDS; PHENOLS; PROTEIN STRUCTURE, TERTIARY; SPECIES SPECIFICITY; SWINE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; HOMO SAPIENS; SOLEA SOLEA; SUIDAE; SUS SCROFA;

EID: 84875050741     PISSN: 15204081     EISSN: 15227278     Source Type: Journal    
DOI: 10.1002/tox.20708     Document Type: Article

References (56)

1. Arnal JF, Laurell H, Fontaine C, Billon A, Calippe B, Lenfant F, Gourdy P. 2009. Estrogen receptor actions on vascular biology and inflammation: implications in vascular pathophysiology. Climacteric 12(Suppl 1): 12-17.
2. Awais M, Sato M, Sasaki K, Umezawa Y. 2004. A genetically encoded fluorescent indicator capable of discriminating estrogen agonists from antagonists in living cells. Anal Chem 76: 2181-186.
3. Caserta D, Maranghi L, Mantovani A, Marci R, Maranghi F, Moscarini M. 2008. Impact of endocrine disruptor chemicals in gynaecology. Hum Reprod Update 14: 59-72.
4. Charles GD. 2004. In vitro models in endocrine disruptor screening. Ilar J 45: 494-501.
5. Christian RC, Liu PY, Harrington S, Ruan M, Miller VM, Fitzpatrick LA. 2006. Intimal estrogen receptor (ER)beta, but not ERalpha expression, is correlated with coronary calcification and atherosclerosis in pre- and postmenopausal women. J Clin Endocrinol Metab 91: 2713-2720.
6. Chu WL, Shiizaki K, Kawanishi M, Kondo M, Yagi T. 2009. Validation of a new yeast-based reporter assay consisting of human estrogen receptors alpha/beta and coactivator SRC-1: Application for detection of estrogenic activity in environmental samples. Environ Toxicol 24: 513-521.
7. Colborn T, vom Saal FS, Soto AM. 1993. Developmental effects of endocrine-disrupting chemicals in wildlife and humans. Environ Health Perspect 101: 378-384.
8. De Wilde A, Lieberherr M, Colin C, Pointillart A. 2004. A low dose of daidzein acts as an ERbeta-selective agonist in trabecular osteoblasts of young female piglets. J Cell Physiol 200: 253-262.
9. deFur PL. 2004. Use and role of invertebrate models in endocrine disruptor research and testing. Ilar J 45: 484-493.
10. Derbyshire V, Wood DW, Wu W, Dansereau JT, Dalgaard JZ, Belfort M. 1997. Genetic definition of a protein-splicing domain: Functional mini-inteins support structure predictions and a model for intein evolution. Proc Natl Acad Sci USA 94: 11466-11471.
11. Dobbins LL, Brain RA, Brooks BW. 2008. Comparison of the sensitivities of common in vitro and in vivo assays of estrogenic activity: Application of chemical toxicity distributions. Environ Toxicol Chem 27: 2608-2616.
12. Escande A, Pillon A, Servant N, Cravedi JP, Larrea F, Muhn P, Nicolas JC, Cavailles V, Balaguer P. 2006. Evaluation of ligand selectivity using reporter cell lines stably expressing estrogen receptor alpha or beta. Biochem Pharmacol 71: 1459-1469.
13. Fisher JS. 2004. Are all EDC effects mediated via steroid hormone receptors?. Toxicology 205: 33-41.
14. Fokialakis N, Lambrinidis G, Mitsiou DJ, Aligiannis N, Mitakou S, Skaltsounis AL, Pratsinis H, Mikros E, Alexis MN. 2004. A new class of phytoestrogens: Evaluation of the estrogenic activity of deoxybenzoins. Chem Biol 11: 397-406.
15. Gillies AR, Skretas G, Wood DW. 2008. Engineered systems for detection and discovery of nuclear hormone-like compounds. Biotechnol Prog 24: 8-16.
16. Goksoyr A. 2006. Endocrine disruptors in the marine environment: Mechanisms of toxicity and their influence on reproductive processes in fish. J Toxicol Environ Health A 69: 175-184.
17. Hartman I, Gillies AR, Arora S, Andaya C, Royapet N, Welsh WJ, Wood DW, Zauhar RJ. 2009. Application of screening methods, shape signatures and engineered biosensors in early drug discovery process. Pharm Res 26: 2247-2258.
18. Jordan VC, O'Malley BW. 2007. Selective estrogen-receptor modulators and antihormonal resistance in breast cancer. J Clin Oncol 25: 5815-5824.
19. Kim JK, Levin ER. 2006. Estrogen signaling in the cardiovascular system. Nucl Recept Signal 4: e013.
20. Kuiper GG, Lemmen JG, Carlsson B, Corton JC, Safe SH, van der Saag PT, van der Burg B, Gustafsson JA. 1998. Interaction of estrogenic chemicals and phytoestrogens with estrogen receptor beta. Endocrinology 139: 4252-4263.
21. Kurosawa T, Hiroi H, Tsutsumi O, Ishikawa T, Osuga Y, Fujiwara T, Inoue S, Muramatsu M, Momoeda M, Taketani Y. 2002. The activity of bisphenol A depends on both the estrogen receptor subtype and the cell type. Endocr J 49: 465-471.
22. Larsen BK, Bjornstad A, Sundt RC, Taban IC, Pampanin DM, Andersen OK. 2006. Comparison of protein expression in plasma from nonylphenol and bisphenol A-exposed Atlantic cod (Gadus morhua) and turbot (Scophthalmus maximus) by use of SELDI-TOF. Aquat Toxicol 78(Suppl 1): S25-S33.
23. Leanos-Castaneda O, Van Der Kraak G. 2007. Functional characterization of estrogen receptor subtypes. ERalpha and ERbeta, mediating vitellogenin production in the liver of rainbow trout. Toxicol Appl Pharmacol 224: 116-125.
24. Maffini MV, Rubin BS, Sonnenschein C, Soto AM. 2006. Endocrine disruptors and reproductive health: The case of bisphenol-A. Mol Cell Endocrinol 254-255:179-186.
25. Martinez ED, Rayasam GV, Dull AB, Walker DA, Hager GL. 2005. An estrogen receptor chimera senses ligands by nuclear translocation. J Steroid Biochem Mol Biol 97: 307-321.
26. Matsuoka M, Hiroshi I, Ushijima M, Inudo M, Honda E, Iwahara M, Cho H-S, Ishibashi Y, Arizono K. 2005. The potential contribution of phytoestrogens and organochlorine pesticides in an experimental fish diet to estrogenic activity. J Health Sci 51: 212-219.
27. Matthews J, Celius T, Halgren R, Zacharewski T. 2000. Differential estrogen receptor binding of estrogenic substances: A species comparison. J Steroid Biochem Mol Biol 74: 223-234.
28. Matthews JB, Clemons JH, Zacharewski TR. 2001. Reciprocal mutagenesis between human alpha(L349. M528) and rainbow trout (M317, I496) estrogen receptor residues demonstrates their importance in ligand binding and gene expression at different temperatures. Mol Cell Endocrinol 183: 127-139.
29. Melnick R, Lucier G, Wolfe M, Hall R, Stancel G, Prins G, Gallo M, Reuhl K, Ho SM, Brown T, Moore J, Leakey J, Haseman J, Kohn M. 2002. Summary of the National Toxicology Program's report of the endocrine disruptors low-dose peer review. Environ Health Perspect 110: 427-431.
30. Mendelsohn ME, Karas RH. 1999. The protective effects of estrogen on the cardiovascular system. N Engl J Med 340: 1801-1811.
31. Meyers MJ, Sun J, Carlson KE, Marriner GA, Katzenellenbogen BS, Katzenellenbogen JA. 2001. Estrogen receptor-beta potency-selective ligands: Structure-activity relationship studies of diarylpropionitriles and their acetylene and polar analogues. J Med Chem 44: 4230-4251.
32. Milligan SR, Khan O, Nash M. 1998. Competitive binding of xenobiotic oestrogens to rat alpha-fetoprotein and to sex steroid binding proteins in human and rainbow trout (Oncorhynchus mykiss) plasma. Gen Comp Endocrinol 112: 89-95.
33. Mori C. 2001. Possible effects of endocrine disruptors on male reproductive function. Kaibogaku Zasshi 76: 361-368.
34. Motylewska E, Stasikowska O, Melen-Mucha G. 2009. The inhibitory effect of diarylpropionitrile, a selective agonist of estrogen receptor beta, on the growth of MC38 colon cancer line. Cancer Lett 276: 68-73.
35. Nagel SC, vom Saal FS, Thayer KA, Dhar MG, Boechler M, Welshons WV. 1997. Relative binding affinity-serum modified access (RBA-SMA) assay predicts the relative in vivo bioactivity of the xenoestrogens bisphenol A and octylphenol. Environ Health Perspect 105: 70-76.
36. Nendza M, Wenzel A. 2006. Discriminating toxicant classes by mode of action. 1. (Eco)toxicity profiles. Environ Sci Pollut Res Int 13: 192-203.
37. Newbold RR, Padilla-Banks E, Jefferson WN. 2006. Adverse effects of the model environmental estrogen diethylstilbestrol are transmitted to subsequent generations. Endocrinology 147(6 Suppl): S11-S17.
38. O'Connor JC, Cook JC, Marty MS, Davis LG, Kaplan AM, Carney EW. 2002. Evaluation of Tier I screening approaches for detecting endocrine-active compounds (EACs). Crit Rev Toxicol 32: 521-549.
39. Oberdorster E, Cheek AO. 2001. Gender benders at the beach: endocrine disruption in marine and estuarine organisms. Environ Toxicol Chem 20: 23-36.
40. Okano A, Takahashi H, Takahashi M, Geshi M. 2007. Binding competition between estrogen and xenobiotic chemicals with estrogen receptors in the porcine endometrium. Chikusan Sochi Kenkyusho Kenkyu Hokoku 7: 1-7.
41. Olsen CM, Meussen-Elholm ET, Hongslo JK, Stenersen J, Tollefsen KE. 2005. Estrogenic effects of environmental chemicals: an interspecies comparison. Comp Biochem Physiol C Toxicol Pharmacol 141: 267-274.
42. Petit F, Valotaire Y, Pakdel F. 1995. Differential functional activities of rainbow trout and human estrogen receptors expressed in the yeast Saccharomyces cerevisiae. Eur J Biochem 233: 584-592.
43. Phillips KP, Foster WG, Leiss W, Sahni V, Karyakina N, Turner MC, Kacew S, Krewski D. 2008. Assessing and managing risks arising from exposure to endocrine-active chemicals. J Toxicol Environ Health B Crit Rev 11: 351-372.
44. Shi LM, Fang H, Tong W, Wu J, Perkins R, Blair RM, Branham WS, Dial SL, Moland CL, Sheehan DM. 2001. QSAR models using a large diverse set of estrogens. J Chem Inf Comput Sci 41: 186-195.
45. Skretas G, Meligova AK, Villalonga-Barber C, Mitsiou DJ, Alexis MN, Micha-Screttas M, Steele BR, Screttas CG, Wood DW. 2007. Engineered chimeric enzymes as tools for drug discovery: Generating reliable bacterial screens for the detection. Discovery, and assessment of estrogen receptor modulators. J Am Chem Soc 129: 8443-8457.
46. Skretas G, Wood DW. 2005a. A bacterial biosensor of endocrine modulators. J Mol Biol 349: 464-474.
47. Skretas G, Wood DW. 2005b. Rapid detection of subtype-selective nuclear hormone receptor binding with bacterial genetic selection. Appl Environ Microbiol 71: 8995-897.
48. Smeets JM, Rankouhi TR, Nichols KM, Komen H, Kaminski NE, Giesy JP, van den Berg M. 1999. In vitro vitellogenin production by carp (Cyprinus carpio) hepatocytes as a screening method for determining (anti)estrogenic activity of xenobiotics. Toxicol Appl Pharmacol 157: 68-76.
49. Soto AM, Maffini MV, Schaeberle CM, Sonnenschein C. 2006. Strengths and weaknesses of in vitro assays for estrogenic and androgenic activity. Best Pract Res Clin Endocrinol Metab 20: 15-33.
50. Stokes WS. 2004. Selecting appropriate animal models and experimental designs for endocrine disruptor research and testing studies. Ilar J 45: 387-393.
51. Traupe T, Stettler CD, Li H, Haas E, Bhattacharya I, Minotti R, Barton M. 2007. Distinct roles of estrogen receptors alpha and beta mediating acute vasodilation of epicardial coronary arteries. Hypertension 49: 1364-1370.
52. Tsai WT. 2006. Human health risk on environmental exposure to Bisphenol-A: A review. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 24: 225-255.
53. Vandenbergh JG. 2004. Animal models and studies of in utero endocrine disruptor effects. Ilar J 45: 438-442.
54. Whitten PL, Patisaul HB. 2001. Cross-species and interassay comparisons of phytoestrogen action. Environ Health Perspect 109(Suppl 1): 5-20.
55. Zacharewski T. 1997. In vitro bioassays for assessing estrogenic substances. Environ Sci Technol 31: 613-623.
56. Zhang JH, Chung TD, Oldenburg KR. 1999. A simple statistical parameter for use in evaluation and validation of high-throughput screening assays. J Biomol Screen 4: 67-73.