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Structure of Estrogen Related Receptor Gamma in complex with Bisphenol A

Ian Richardson and Myles Alderman


Contents:


I. Introduction


Estrogen-related Receptor-γ (ERRγ) is a nuclear receptor protein that has demonstrated regulatory control over genes in the breast and bone.  Despite sharing structural homology with the Estrogen Receptor family of proteins, ERRs do not bind estrogen and thus allow for transcription regulation by small lipophilic molecules which can act as agonists or inverse agonists.   

Bisphenol A (BPA) is an agonist for ERR
γ and is falsly recognized as estrogen by the protein.  Since BPA mimics the hormone, it is very tightly bound by ERRγ and thereby ensures the continuous activation of the protein.  This control over ERRγ has led to studies suggesting that BPA increases the risk of breast cancer and may be associated with a variety of health problems.  

Tamoxifen (4-hyrdoxytamoxifen) is an antagonist to the ERR family of proteins.  Tamoxifen is useful because it blocks estrogen from the cancer cells via competitive antagonism, and since some breast cancers require estrogen to grow, it thereby inhibits cancer growth.  It is commonly perscribed as hormone therapy for recovering breast cancer patients.


II. General Structure



ERRγ is composed of four chemically identical polypeptide subunits , each with 456 amino acids, and these combine to form two homodimers.  Helicies 9-10 appear to be important in dimerization. Each subunit has its own ligand binding domain (LBD) , and binding of a ligand to the LBD of one unit does not affect the binding affinity of any of the other LBDs in the protein.  With a volume of 280 cubic Angstroms, the LBD of ERRγ is extremely small - the LBD volume of classic Estrogen Receptors is much larger at 370 cubic Angstroms.  Due to the small size of ERRγ's LBD, and the fact that it is largely composed of hydrophobic residues ERRγ's LBD, and the fact that it is largely composed of hydrophobic residues , the LBD provides a favorable environment for small, hydrophobic molecules.  Thus the phenyl rings and methyl groups of BPA and Tamoxifen are strongly bound to the LBD of ERRγ.

The highly conserved portions of the DNA binding domain (DBD) and the ligand binding domain (LBD) may explain why the ERR family of proteins are constituitively active.  The core DBD is composed of two zinc fingers, specialized folds in the protein which are stabilized by two zinc atoms embedded in the protein . This core DBD is composed of an alpha helix that rests in the major groove of the DNA.  Sequence specific interactions with DNA occur via H-bonds with Lys-128, Lys-124, and Glu-121. .

Since the ERR family of proteins binds to DNA as a monomer, it is neccesary to have additional contact with the DNA to ensure sequence specific binding.  The result is a unique feature in the ERR family: the C-terminal extension (CTE) .  The CTE provides an AT-hook motif that allows sequence specific binding with the minor groove of the DNA, adjacent to the DBD.  Additional H-bonds are formed with the CTE and the DNA with Arg-179, Gly-180, Arg-182 . Once both the DBD and the CTE have been bound to DNA, a hydrophobic interaction occurs between Tyr-185 of the CTE and Leu-169 and Val-117 of the DBD . It is thought that this interaction stabilizes and combines the interactions of the DBD and the CTE.



III. Bisphenol A Binding

ERRγ has relatively high affinity for BPA. BPA - the highest of any phenol/polyphenol tested.  BPA is a small ligand and fits tightly in the LBD of ERRγ .  The strong interactions between ERRγ and BPA arise from a set of Pi stacking and hydrogen bonds.  Pi stacking occurs between the ligand and residues Tyr-326 and Phe-435 . There are additional hydrophobic interactions between the phenol rings of BPA and the hydrophobic carbon side chains of Leu-342 and Leu-345 . Hydrogen bonding occurs between BPA and Glu-275, Arg-316, Tyr-326, and Asn-346   . The hydrogen bond with Tyr-326 is enabled by a hydrogen bond between Tyr-326 and Asn-346 that pulls the Tyr-326 residue close enough to BPA to enable an interaction between them .


IV. Tamoxifen Binding

Tamoxifen is an effective breast cancer drug which works via competitive antagonism against estrogen in Estrogen Receptor Alpha (ERα), but it binds much tighter to ERRγ.  The variation in binding affinity is due to structural differences between ERRγ and ERα.  The most significant difference in the binding pocket is the Phe-435 residue in ERRγ which corrosponds to Leu-525 in ERα. This difference in amino acids is the primary reason that estrogen cannot bind to ERRγ, the steric strain from the PHE prevents it.

The binding interactions between Tamoxifen and ERRγ are comprised primarily of three hydrogen bonds.  ERRγ's Asp-273, Glu-275, and Arg-316 form hydrogen bonds with the ligand.
The binding interactions 
between Tamoxifen and ERRγ are stabilized by the prominent hyrophobic residues seen earlier in the LBD. 



VI. References

Abad, Marta C., et al. "Structural determination of estrogen-related receptor γ in the presence of phenol derivative compounds." The Journal of steroid biochemistry and molecular biology 108.1 (2008): 44-54.

Brisken, Cathrin. "Endocrine Disruptors and Breast Cancer." CHIMIA International Journal for Chemistry 62.5 (2008): 406-09. Print.

Gearhart, Micah D., Signe M.A. Holmbeck, Ronald M. Evans, H.Jane Dyson, and Peter E. Wright. "Monomeric Complex of Human Orphan Estrogen Related Receptor-2 with DNA: A Pseudo-dimer Interface Mediates Extended Half-site Recognition." Journal of Molecular Biology 327.4 (2003): 819-32. Print.


Wang, Liping, et al. "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." Journal of Biological Chemistry 281.49 (2006): 37773-37781.