A characteristic back support structure in the bisphenol A-binding pocket in the human nuclear receptor ERRγ

PLoS ONE

Volumn 9, Issue 6, 2014, Pages

  Liu, Xiaohui ^a   Matsushima, Ayami ^a   Shimohigashi, Miki ^b   Shimohigashi, Yasuyuki ^a  

^a KYUSHU UNIVERSITY   (Japan)

^b FUKUOKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

4,4' ISOPROPYLIDENEDIPHENOL; AFIMOXIFENE; ALANINE; ALANINE 431; ARGININE; ASPARAGINE; ASPARAGINE 346; GLUTAMIC ACID; GLUTAMIC ACID 275; HISTIDINE; HISTIDINE 434; ISOLEUCINE; ISOLEUCINE 310; ISOLEUCINE 349; LEUCIN 265; LEUCIN 268; LEUCIN 324; LEUCIN 342; LEUCIN 345; LEUCINE; LYSINE; LYSINE 430; NUCLEAR RECEPTOR ESTROGEN RELATED RECEPTOR GAMMA; STEROID RECEPTOR; TYROSINE; TYROSINE 326; TYROSINE 330; UNCLASSIFIED DRUG; UNINDEXED DRUG; VALINE; VALINE 313; 4-CUMYLPHENOL; AMINO ACID; BENZHYDRYL DERIVATIVE; ESRRG PROTEIN, HUMAN; ESTROGEN RECEPTOR; LIGAND; LUCIFERASE; MUTANT PROTEIN; PHENOL DERIVATIVE; PROTEIN BINDING; TAMOXIFEN; TRITIUM;

ALPHA HELIX; AMINO ACID SUBSTITUTION; ARTICLE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; HUMAN; HYDROGEN BOND; LIGAND BINDING; MOLECULAR INTERACTION; NONHUMAN; PROTEIN ASSEMBLY; PROTEIN STRUCTURE; STRUCTURE ANALYSIS; ANALOGS AND DERIVATIVES; BINDING COMPETITION; CHEMICAL STRUCTURE; CHEMISTRY; HELA CELL LINE; METABOLISM; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; REPORTER GENE; STRUCTURE ACTIVITY RELATION;

AMINO ACID SUBSTITUTION; AMINO ACIDS; BENZHYDRYL COMPOUNDS; BINDING SITES; BINDING, COMPETITIVE; GENES, REPORTER; HELA CELLS; HUMANS; LIGANDS; LUCIFERASES; MODELS, MOLECULAR; MUTANT PROTEINS; PHENOLS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ESTROGEN; STRUCTURE-ACTIVITY RELATIONSHIP; TAMOXIFEN; TRITIUM;

EID: 84903641544     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0101252     Document Type: Article

References (36)

1. Takayanagi S, Tokunaga T, Liu X, Okada H, Matsushima A, et al. (2006) Endocrine disruptor bisphenol A strongly binds to human estrogen-related receptor gamma (ERRgamma) with high constitutive activity. Toxicol Lett 167: 95-105. doi: 10.1016/j.toxlet.2006.08.012. PubMed: 17049190.
2. Okada H, Tokunaga T, Liu X, Takayanagi S, Matsushima A, et al. (2008) Direct evidence revealing structural elements essential for the high binding ability of bisphenol A to human estrogen-related receptor γ (ERRγ). Environ Health Perspect 116: 32-38. doi: 10.1289/ehp.10587. PubMed: 18197296.
3. Horard B, Vanacker JM (2003) Estrogen receptor-related receptors: orphan receptors desperately seeking a ligand. J Mol Endocrinol 31: 349-357. doi: 10.1677/jme.0.0310349. PubMed: 14664699.
4. Takeda Y, Liu X, Sumiyoshi M, Matsushima A, Shimohigashi M, et al. (2009) Placenta expressing the greatest quantity of bisphenol A receptor ERRγ among the human reproductive tissues: Predominant expression of type-1 ERRγ isoform. J Biochem 146: 113-122. doi: 10.1093/jb/mvp049. PubMed: 19304792.
5. Kojo H, Tajima K, Fukagawa M, Isogai T, Nishimura S (2006) A novel estrogen receptor-related protein γ splice variant lacking a DNA binding domain exon modulates transcriptional activity of a moderated range of nuclear receptors. J Steroid Biochem Mol Biol 98: 181-192. doi: 10.1016/j.jsbmb.2005.10. 004. PubMed: 16460929.
6. Giguère V (2008) Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 29: 677-696. doi: 10.1210/er.2008-0017. PubMed: 18664648.
7. Poidatz D, Dos Santos E, Brulé A, De Mazancourt P, Dieudonné MN (2012) Estrogen-related receptor gamma modulates energy metabolism target genes in human trophoblast. Placenta 33: 688-695. doi: 10.1016/j.placenta.2012.06.002. PubMed: 22763271.
8. Lui K, Huang Y, Choi HL, Yu S, Wong KB, et al. (2006) Molecular cloning and functional study of rat estrogen receptor-related receptor gamma in rat prostatic cells. Prostate 66: 1600-1619. doi: 10.1002/pros.20429. PubMed: 169273302.
9. National Toxicology Program (NTP) (2008) U.S. Department of Health and Human Services, National Institute of Environmental Health Sciences, National Institutes of Health. Draft NTP brief on bisphenol A Peer Revies. Available on the NTP web site: http://aseh.net/teaching-research/teaching-unit-better-living- through-chemistry/historical-sources/lesson-4-1/National%20Toxicology%20Program- BPADraftBrief-4.14.08.pdf
10. Viberg H, Lee I (2012) A single exposure to bisphenol A alters the levels of important neuroproteins in adult male and female mice. Neurotoxicolo 33: 1390-1395. doi: 10.1016/j.neuro.2012.09.002. PubMed: 22981971.
11. vom Saal FS, Cooke PS, Buchanan DL, Palanza P, Thayer KA, et al. (1998) A physiologically based approach to the study of bisphenol A and other estrogenic chemicals on the size of reproductive organs, daily sperm production, and behavior. Toxicol Ind Health 14: 239-260. doi: 10.1177/074823379801400115. PubMed: 9460178.
12. Kubo K, Arai O, Omura M, Watanabe R, Ogata R, et al. (2003) Low dose effects of bisphenol A on sexual differentiation of the brain and behavior in rats. Neurosci Res 45: 345-356. doi: 10.1016/S0168-0102(02)00251-1. PubMed: 12631470.
13. vom Saal FS, Hughes C (2005) An extensive new literature concerning low-dose effects of bisphenol A shows the need for a new risk assessment. Environ Health Perspect 113: 926-933. doi: 10.1289/ehp.7713. PubMed: 16079060.
14. Kamrin MA (2007) The "low dose" hypothesis: validity and implications for human risk. Int J Toxicol 26: 13-23. doi: 10.1080/ 10915810601117968. PubMed: 17365142.
15. Kunz N, Camm EJ, Somm E, Lodygensky G, Darbre S, et al. (2011) Developmental and metabolic brain alterations in rats exposed to bisphenol A during gestation and lactation. Int. J Dev Neurosci 29: 37-43. doi: 10.1016/j.ijdevneu.2010.09.009. PubMed: 20955774.
16. Yan S, Song W, Chen Y, Hong K, Rubinstein J, et al. (2013) Low-dose bisphenol A and estrogen increase ventricular arrhythmias following ischemia-reperfusion in female rat hearts. Food Chem Toxicol 56: 75-80. doi: 10.1016/j.fct.2013.02.011. PubMed: 23429042.
17. Kundakovic M, Gudsnuk K, Franks B, Madrid J, Miller RL, et al. (2013) Sex-specific epigenetic disruption and behavioural changes following low-dose in utero bisphenol A exposure. Proc Natl Acad Sci U S A. doi: 10.1073/pnas. 1214056110. PubMed: 23457122.
18. Cao J, Rebuli ME, Rogers J, Todd KL, Leyrer SM, et al. (2013) Prenatal bisphenol a exposure alters sex-specific estrogen receptor expression in the neonatal rat hypothalamus and amygdala. Toxicol Sci 133: 157-173. doi: 10.1093/toxsci/kft035. PubMed: 23457122.
19. Giguere V (2002) To ERR in the estrogen pathway. Trends Endocrinol Metab 13: 220-225. doi: 10.1016/S1043-2760(02)00592-1. PubMed: 12185669.
20. Horard B, Vanacker JM (2003) Estrogen receptor-related receptors: orphan receptors desperately seeking a ligand. J Mol Endocrinol 31: 349-357. doi: 10.1677/jme.0.0310349. PubMed: 14664699.
21. Greschik H, Wurtz JM, Sanglier S, Bourguet W, van Dorsselaer, et al. (2002) Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3. Mol Cell 9: 303-313. doi: 10.1016/S1097-2765(02)00444-6. PubMed: 11864604.
22. Matsushima A, Kakuta Y, Teramoto T, Koshiba T, Liu X, et al. (2007) Structural evidence for endocrine disruptor bisphenol A binding to human nuclear receptor ERRγ. J Biochem 142: 517-524. doi: 10.1093/jb/mvm158.PubMed: 17761695.
23. Matsushima A, Teramoto T, Okada H, Liu X, Tokunaga T, et al. (2008) ERRc tethers strongly bisphenol A and 4-a-cumylphenol in an induced-fit manner. Biochem Biophys Res Commun 373: 408-413. doi: 10.1016/j.bbrc.2008.06.050. PubMed: 18582436.
24. Liu X, Matsushima A, Nakamura M, Costa T, Nose T, et al. (2012) Fine spatial assembly for construction of the phenol-binding pocket to capture bisphenol A in the human nuclear receptor estrogen-related receptor c. J Biochem 151: 403-415. doi: 10.1093/jb/mvs008. PubMed: 22298789.
25. Liu X, Matsushima A, Okada H, Tokunaga T, Isozaki K, et al. (2007) Receptor binding characteristics of endocrine disruptor bisphenol A for the human nuclear receptor of estrogen-related receptor c (ERRc): Chief and corroborative hydrogen bonds of bisphenol A phenol-hydroxyl group with Arg316 and Glu275 residues. FEBS J 274: 6340-6351. doi: 10.1111/j.1742-4658.2007.06152. x.PubMed: 18005256.
26. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254. doi: 10.1016/0003-2697(76)90527-3. PubMed: 942051.
27. Nakai M, Tabira Y, Asai D, Yakabe Y, Shimyozu T, et al. (1999) Binding characteristics of dialkyl phthalates for the estrogen receptor. Biochem Biophys Res Commun 254: 311-314. doi: 10.1006/bbrc.1998.9928. PubMed: 9918834.
28. Pichon MF, Milgrom E (1973) Competitive protein binding assay of progesterone without chromatography. Steroids 21: 335-346. doi: 10.1016/ 0039-128X(73)90028-7. PubMed: 4693730.
29. Scatchard G (1948) The attractions of proteins for small molecules and ions. Ann NY Acad Sci 51: 660-672. dio: 10.1111/j.1749-6632.1949.tb27297.x.
30. DeLean A, Munson PJ, Rodbard D (1978) Simultaneous analysis of families of sigmoidal curves: application to bioassay, radioligand assay, and physiological dose-response curves. Am J Physiol 235: E97-E102. PubMed: 686171.
31. Berger J, Hauber J, Hauber R, Geiger R, Cullen BR (1988) Secreted placental alkaline phosphatase: a powerful new quantitative indicator of gene expression in eukaryotic cells. Gene 66: 1-10. doi: 10.1016/0378-1119(88)90219- 3. PubMed: 3417148.
32. Sambrook J, Russell DW (2001) Molecular Cloning: A Laboratory Manual, 3rd edn. Cold Springs Harbor Laboratory Press, Cold Springs Harbor, NY.
33. Dirr H, Reinemer P, Huber R (1994) Refined Crystal Structure of Porcine Class Pi Glutathione S-Transferase (pGST P1-1) at 2.1 Å Resolution. J Mol Biol 243: 72-92. doi: 10.1006/jmbi.1994.1631. PubMed: 7932743.
34. Coward P, Lee D, Hull MV, Lehmann JM (2001) 4-Hydroxytamoxifen binds to and deactivates the estrogen-related receptor gamma. Proc Natl Acad Sci USA 98: 8880-8884. doi: 10.1073/pnas.151244398. PubMed: 11447273.
35. Wang L, Zuercher WJ, Consler TG, Lambert MH, Miller AB, et al. (2006) Xray crystal structures of the estrogen-related receptor-ligand binding domain in three functional states reveal the molecular basis of small molecule regulation. J Biol Chem 281: 37773-37781. doi: 10.1074/jbc.M608410200. PubMed: 16990259.
36. Greschik H, Wurtz JM, Sanglier S, Bourguet W, van Dorsselaer A, et al. (2002) Structural and functional evidence for ligand-independent transcriptional activation by the estrogen-related receptor 3. Mol Cell 9: 303-313. doi: 10.1016/S1097-2765(02)00444-6. PubMed: 11864604.