Distinct mechanisms of endocrine disruption of DDT-related pesticides toward estrogen receptor α and estrogen-related receptor γ

Environmental Toxicology and Chemistry

Volumn 31, Issue 11, 2012, Pages 2597-2605

  Zhuang, Shulin ^a   Zhang, Jing ^a   Wen, Yuezhong ^a   Zhang, Chunlong ^b   Liu, Weiping ^a  

^a ZHEJIANG UNIVERSITY   (China)

^b UNIVERSITY OF HOUSTON CLEAR LAKE   (United States)

Author keywords

Dichlorodiphenyltrichloroethane; Endocrine disruption; Estrogen receptor; Molecular dynamics simulations

Indexed keywords

ATOMIC LEVELS; BINDING MODES; CONFORMATIONAL CHANGE; DICHLORODIPHENYLTRICHLOROETHANE; DICOFOL; ENDOCRINE DISRUPTION; ESTROGEN RECEPTOR; HUMAN ESTROGEN RECEPTORS; LIGAND BINDING DOMAIN; MOLECULAR DYNAMICS SIMULATIONS; PHENOLIC HYDROXYL; STRUCTURAL CHANGE; VAN DER WAALS INTERACTIONS;

BINDING ENERGY; CHLORINE; HYDROGEN BONDS; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PESTICIDES; PHENOLS; VAN DER WAALS FORCES;

ENDOCRINE DISRUPTERS;

1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHANE; 1,1 DICHLORO 2,2 BIS(4 CHLOROPHENYL)ETHYLENE; 4,4' HYDROXY DICHLORODIPHENYLTRICHLOROETHANE; CHLORINE; CHLORPHENOTANE; DICOFOL; ENDOCRINE DISRUPTOR; ESTROGEN RECEPTOR; ESTROGEN RECEPTOR ALPHA; ESTROGEN RECEPTOR RELATED RECEPTOR GAMMA; HYDROGEN; METHOXYCHLOR; PHENOL; UNCLASSIFIED DRUG;

BIOCHEMISTRY; CHEMICAL BINDING; DDD; DDE; DDT; ENDOCRINE DISRUPTOR; ESTROGENIC COMPOUND; LIGAND; MOLECULAR ANALYSIS; POLLUTION EFFECT; POLLUTION EXPOSURE; PUBLIC HEALTH;

ARTICLE; CHEMICAL STRUCTURE; CONFORMATIONAL TRANSITION; ENDOCRINE DISEASE; HYDROGEN BOND; LIGAND BINDING; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; MOLECULAR PROBE; MOLECULAR RECOGNITION; PRIORITY JOURNAL; SIMULATION;

DDT; DICHLORODIPHENYL DICHLOROETHYLENE; DICHLORODIPHENYLDICHLOROETHANE; ENDOCRINE DISRUPTORS; ESTROGEN RECEPTOR ALPHA; HUMANS; HYDROGEN BONDING; METHOXYCHLOR; MOLECULAR CONFORMATION; MOLECULAR DYNAMICS SIMULATION; PESTICIDES; PHENOLS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, ESTROGEN;

EID: 84867707720     PISSN: 07307268     EISSN: 15528618     Source Type: Journal    
DOI: 10.1002/etc.1986     Document Type: Article

References (37)

1. Miyashita M, Shimada T, Nakagami S, Kurihara N, Miyagawa H, Akamatsu M. 2005. Evaluation of estrogen receptor binding affinity of DDT-related compounds and their metabolites. Environmental Fate and Safety Management of Agrochemicals. Vol 899. ACS Symposium Series. American Chemical Society, Washington, DC, USA, pp 159-166.
2. Naidoo V, Katsu Y, Iguchi T. 2008. The influence of non-toxic concentrations of DDT and DDE on the old world vulture estrogen receptor alpha. Gen Comp Endocrinol 159:188-195.
3. Jaga K. 2000. What are the implications of the interaction between DDT and estrogen receptors in the body? Med Hypotheses 54:18-25.
4. Rider CV, Hartig PC, Cardon MC, Lambright CR, Bobseine KL, Guillette LJ, Gray LE, Wilson VS. 2010. Differences in sensitivity but not selectivity of xenoestrogen binding to alligator versus human estrogen receptor alpha. Environ Toxicol Chem 29:2064-2071.
5. Hoekstra PF, Burnison BK, Garrison AW, Neheli T, Muir DCG. 2006. Estrogenic activity of dicofol with the human estrogen receptor: Isomer- and enantiomer-specific implications. Chemosphere 64:174-177.
6. Li J, Li N, Ma M, Giesy JP, Wang Z. 2008. In vitro profiling of the endocrine disrupting potency of organochlorine pesticides. Toxicol Lett 183:65-71.
7. Gaido KW, Maness SC, McDonnell DP, Dehal SS, Kupfer D, Safe S. 2000. Interaction of methoxychlor and related compounds with estrogen receptors α and β, and androgen receptor: Structure-activity studies. Mol Pharmacol 58:852-858.
8. Matsushima A, Liu X, Okada H, Shimohigashi M, Shimohigashi Y. 2010. Bisphenol AF is a full agonist for the estrogen receptor ER α but a highly specific antagonist for ERβ. Environ Health Perspect 118:1267-1272.
9. Hirvonen J, Rajalin A-M, Wohlfahrt G, Adlercreutz H, Wähälä K, Aarnisalo P. 2011. Transcriptional activity of estrogen-related receptor γ (ERR γ) is stimulated by the phytoestrogen equol. J Steroid Biochem Mol Biol 123:46-57.
10. Celik L, Lund JDD, Schiøtt B. 2007. Conformational dynamics of the estrogen receptor α: Molecular dynamics simulations of the influence of binding site structure on protein dynamics. Biochemistry 46:1743-1758.
11. McGee T, Edwards J, Roitberg A. 2008. Preliminary molecular dynamic simulations of the estrogen receptor alpha ligand binding domain from antagonist to apo. Int J Environ Res Publ Health Health 5:111-114.
12. Oostenbrink BC, Pitera JW, van Lipzig MM, Meerman JH, van Gunsteren WF. 2000. Simulations of the estrogen receptor ligand-binding domain: Affinity of natural ligands and xenoestrogens. J Med Chem 43:4594-4605.
13. Zeng J, Li W, Zhao Y, Liu G, Tang Y, Jiang H. 2008. Insights into ligand selectivity in estrogen receptor isoforms: Molecular dynamics simulations and binding free energy calculations. J Phys Chem B 112:2719-2726.
14. Blizzard TA, DiNinno F, Morgan Ii JD, Chen HY, Wu JY, Kim S, Chan W, Birzin ET, Yang YT, Pai L-Y, Fitzgerald PMD, Sharma N, Li Y, Zhang Z, Hayes EC, DaSilva CA, Tang W, Rohrer SP, Schaeffer JM, Hammond ML. 2005. Estrogen receptor ligands. Part 9: Dihydrobenzoxathiin SERAMs with alkyl substituted pyrrolidine side chains and linkers. Bioorg Med Chem Lett 15:107-113.
15. Matsushima A, Kakuta Y, Teramoto T, Koshiba T, Liu X, Okada H, Tokunaga T, Kawabata S-I, Kimura M, Shimohigashi Y. 2007. Structural evidence for endocrine disruptor bisphenol a binding to human nuclear receptor ERRγ. J Biochem 142:517-524.
16. Wen Y, Li C, Fang Z, Zhuang S, Liu W. 2011. Elucidation of the enantioselective enzymatic hydrolysis of chiral herbicide dichlorprop methyl by chemical modification. J Agric Food Chem 59:1924-1930.
17. Vanquelef E, Simon S, Marquant G, Garcia E, Klimerak G, Delepine JC, Cieplak P, Dupradeau F-Y. 2011. R. E. D. Server: A web service for deriving RESP and ESP charges and building force field libraries for new molecules and molecular fragments. Nucleic Acids Res 39: (Suppl 2):W511-W517.
18. Duan Y, Wu C, Chowdhury S, Lee MC, Xiong G, Zhang W, Yang R, Cieplak P, Luo R, Lee T, Caldwell J, Wang J, Kollman P. 2003. A point-charge force field for molecular mechanics simulations of proteins based on condensed-phase quantum mechanical calculations. J Comput Chem 24:1999-2012.
19. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, Cheeseman JR, Scalmani G, Barone V, Mennucci B, Petersson GA, Nakatsuji H, Caricato M, Li X, Hratchian HP, Izmaylov AF, Bloino J, Zheng G, Sonnenberg JL, Hada M, Ehara M, Toyota K, Fukuda R, Hasegawa J, Ishida M, Nakajima T, Honda Y, Kitao O, Nakai H, Vreven T, Montgomery JA Jr, Peralta JE, Ogliaro F, Bearpark M, Heyd JJ, Brothers E, Kudin KN, Staroverov VN, Kobayashi R, Normand J, Raghavachari K, Rendell A, Burant JC, Iyengar SS, Tomasi J, Cossi M, Rega N, Millam JM, Klene M, Knox JE, Cross JB, Bakken V, Adamo C, Jaramillo J, Gomperts R, Stratmann RE, Yazyev O, Austin AJ, Cammi R, Pomelli C, Ochterski JW, Martin RL, Morokuma K, Zakrzewski VG, Voth GA, Salvador P, Dannenberg JJ, Dapprich S, Daniels AD, Farkas Ö, Foresman JB, Ortiz JV, Cioslowski J, Fox DJ. 2009. Gaussian 09, Revision A.1. Gaussian, Wallingford, CT, USA.
20. Case DA, Darden TA, Cheatham TEI, Simmerling CL, Wang J, Duke RE, Luo R, Walker RC, Zhang W, Merz KM, Roberts B, Wang B, Hayik S, Roitberg A, Seabra G, Kolossvai I, Wong KF, Paesani F, Vanicek J, Liu J, Wu X, Brozell SR, Steinbrecher T, Gohlke H, Cai Q, Ye X, Wang J, Hsieh MJ, Cui G, Roe DR, Mathews DH, Seetin MG, Sagui C, Babin V, Luchko T, Gusarov S, Kovalenko A, Kollman PA. 2010. Amber 11, University of California, San Francisco. San Francisco, CA, USA.
21. Davis IW, Leaver-Fay A, Chen VB, Block JN, Kapral GJ, Wang X, Murray LW, Arendall WB, Snoeyink J, Richardson JS, Richardson DC. 2007. MolProbity: All-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res 35:W375-W383.
22. Ryckaert JP, Ciccotti G, Berendsen HJ. 1977. Numerical integration of the cartesian equations of motion of a system with constraints: Molecular dynamics of n-alkanes. J Comput Physics 23:327-341.
23. Tom D, Darrin Y, Lee P. 1993. Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems. J Chem Phys 98:10089-10092.
24. Zhuang S, Linhananta A, Li H. 2010. Phenotypic effects of Ehlers-Danlos syndrome-associated mutation on the FnIII domain of tenascin-X. Protein Sci 19:2231-2239.
25. Hou T, Wang J, Li Y, Wang W. 2010. Assessing the performance of the MM/PBSA and MM/GBSA Methods. 1. The accuracy of binding free energy calculations based on molecular dynamics simulations. J Chem Inf Model 51:69-82.
26. Onufriev A, Bashford D, Case DA. 2004. Exploring protein native states and large-scale conformational changes with a modified generalized born model. Proteins 55:383-394.
27. Celik L, Lund JD, Schiøtt B. 2008. Exploring interactions of endocrine-disrupting compounds with different conformations of the human estrogen receptor α ligand binding domain: A molecular docking study. Chem Res Toxicol 21:2195-2206.
28. Burley S, Petsko G. 1985. Aromatic-aromatic interaction: A mechanism of protein structure stabilization. Science 229:23-28.
29. Blakaj DM, McConnell KJ, Beveridge DL, Baranger AM. 2001. Molecular dynamics and thermodynamics of protein-RNA interactions: Mutation of a conserved aromatic residue modifies stacking interactions and structural adaptation in the U1A-stem loop 2 RNA complex. J Am Chem Soc 123:2548-2551.
30. Anstead GM, Carlson KE, Katzenellenbogen JA. 1997. The estradiol pharmacophore: Ligand structure-estrogen receptor binding affinity relationships and a model for the receptor binding site. Steroids 62:268-303.
31. Kojima H, Katsura E, Takeuchi S, Niiyama K, Kobayashi K. 2004. Screening for estrogen and androgen receptor activities in 200 pesticides by in vitro reporter gene assays using chinese hamster ovary cells. Environ Health Perspect 112:524-531.
32. Tamrazi A, Carlson KE, Katzenellenbogen JA. 2003. Molecular sensors of estrogen receptor conformations and dynamics. Mol Endocrinol 17:2593-2602.
33. Nettles KW, Bruning JB, Gil G, Nowak J, Sharma SK, Hahm JB, Kulp K, Hochberg RB, Zhou H, Katzenellenbogen JA, Katzenellenbogen BS, Kim Y, Joachimiak A, Greene GL. 2008. NFκB selectivity of estrogen receptor ligands revealed by comparative crystallographic analyses. Nat Chem Biol 4:241-247.
34. Chen CW, Hurd C, Vorojeikina DP, Arnold SF, Notides AC. 1997. Transcriptional activation of the human estrogen receptor by DDT isomers and metabolites in yeast and MCF-7 cells. Biochem Pharmacol 53:1161-1172.
35. Wang L, Zuercher WJ, Consler TG, Lambert MH, Miller AB, Orband-Miller LA, McKee DD, Willson TM, Nolte RT. 2006. X-ray crystal structures of the estrogen-related receptor γ ligand binding domain in three functional states reveal the molecular basis of small molecule regulation. J Biol Chem 281:37773-37781.
36. Greschik H, Flaig R, Renaud JP, Moras D. 2004. Structural basis for the deactivation of the estrogen-related receptor γ by diethylstilbestrol or 4-hydroxytamoxifen and determinants of selectivity. J Biol Chem 279:33639-33646.
37. Leclercq G, Lacroix M, Laïos I, Laurent G. 2006. Estrogen receptor alpha: Impact of ligands on intracellular shuttling and turnover rate in breast cancer cells. Curr Cancer Drug Targets 6:39-64.