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Crystal Structure of the Beta-2 Adrenergic Receptor-Gs Protien Complex

Andrew Maurer '14 and Sam McQuiston '14


Contents:


I. Introduction

The Beta-2 adrenergic receptor-Gs protien complex has been used as a model system for G-protien coupled receptors(GPCRs) since its discovery over 40 years ago. As a trans-membrane receptor, the primary function of the Beta-adrenergic receptor is to bind to extracellular adreniline and in turn activate the Gs subunit, which then dissociates and continues the messaging cascade. The exact structure of the receptor complex remained a mystery for many years due to the instability of the complex while in the detergent solution required for x-ray crystallography. This problem was worked around by binding a nanobody, Nb35, , to the Gs subunit and a lysosome, T4L , to B2AR which both increased the stability of the complex in the x-ray chromotography solution.

II. General Structure

The Beta-2 Adrenergic Receptor(B2AR) is a single poly-peptide chain which weaves inside and outside of the cellular membrane. Its secondary structure is constituted by 8 α helices, 7 of which are trans-membrane and one which runs parallel to the intracellular face of the cell membrane. It also contains three extra cellular loops, three intracellular loops, an extracellular N-terminus and intracellular C-terminus. The agonist binding site lies within the trans-membrane section of the protein. The Gs subunit is a heterotrimic G-protein, with the subunits, Gαs, and . The Gαs, which binds to GDP and GTP, is the primary functional subunit of the Gs protein which binds to and activates the adenyl-cyclase channel, continuing signal transduction. It is further divided into two sub-units , GαsRas and  GαsAH which clamp onto the guanine-nuceloside when it is bound.


III. Agonist Binding and B2AR Conformation Shift

The agonist binding site in the B2AR protein consists of the residues D130, V131, F288, F289, and N312. The primary interactions of this binding site are Hydrogen bonding between the D130 and N312 hydrogen acceptors and the agonist's proton donors, primarily in the form of hydroxyl groups. Additionally, the F288 and F289 groups help to stabilize the agonist in the binding site by providing non-polar-phenyl stacking interactions which hold the agonist in place. 

The binding of the agonist to this site results in a conformational shift in the trans-membrane helix(TM) 3 and TM 6 of B2AR , which is hypothesised to activate the Gs subunit. However, this conformational shift also results in the weakening of the association of between these helices, which makes them vulnerable to outside attack. This is thought to be one of the primary reasons for the instability of B2AR in detergent solution. The reason for Gs activation is not certain because the B2AR-Gs complex does not include a nucleotide and thus activation can not be observed.

Additional structural changes in B2AR include an eight residue shift in the TM5 helix and a change in in secondary structure of the second intracellular loop(2ICL) into an α-helix structure.
 


IV. B2AR-Gs Binding

The formation of the nucleotide-free B2AR-Gs protein complex first requires the carboxy terminus of the α5-helix in to shift away from the β6-strand in Gs (shown in next section). This shift allows for proper Gs interactions with B2AR. Gαs is composed of two GαsRas domains which activity bind to B2AR The B2AR-GαsRas interface is the primary binding site for the B2AR-Gs protein complex with a total buried surface of 2,576 A2 . A rotation of GαsRas causes a conformational change in both B2AR and GαsRas allowing for the stabilization and bond formation between them. The interaction is formed by ICL2 , TM3 TM5 , and TM6 of B2AR and α5-helix , αN-β1 junction , the top of β1-strand , and α4-helix of GαRas.
There are many specific interactions which hold B2AR and Gs together.
1.) ARG 131
, ALA 134, ILE 135, and THR 136 of 
TM3 interact with TYR 391, HIS 387, GLN 384, and ARG 380 of the α5-helix in a D/ERY motif.
2.)
SER 143 of
ICL2 and ALA 39 of αN-β1 junction ..
3.) ARG 239 of 
TM5 and THR 350 of α4-helix .
4.) ALA 271, THR 274, and LEU 275 of
TM6 and LEU 393 and GLU 392 of α5-helix .
Combined these interactions hold the B2AR-Gs complex together .
It is unknown when GDP is released during the building of the B2AR-Gs protein complex. Surprisingly there is no interaction between B2AR and Gβϒ , the second subunit of Gs. 



V. Conformational Change Allows Binding of Gs-Nucleotide

A major conformational shift in the Gs sub-unit allows GαsRas and GαsAH to bind to the Guanine nucleotide . GαsAH subunit displaces, rotating  127 degrees,  from a non-nucleotide bound state to a nucleotide bound state. The lack of the stability in the  bond with  guanine in between the GαsRas and GαsAH subunits is responsible for the flexibility of the GαsAH subunit when in the non-nucleotide-bound state.

While the GαsRas subunit is less flexible than its counterpart, it still undergoes significant conformational shift. The  α5 helix shifts 6Å towards the receptor and is rotated so the carboxyl terminal end is pointed into the B2AR core in non-nucleotide-bound state. In addition, the beta6 alpha5 loop, which interacts with the guanine ring in the active site when bound, is displaced away from the binding pocket. Although not  totally understood, the β1-α1 loop, a P-loop motif, is directly involved in the nucleotide binding

The interactions between GαsRas and Gβγ appear to be unaffected by the binding of guanine nucleotides. However, because a crystal structure of GDP-bound Gs heterotrimer has not yet been reported and the Nb35 binds to the junction of GαsRas and Gβ and could be responsible for the relative stability of the interface, the veracity of this phenomenon in biological systems can't be certain.




VI. References

Ghanouni, Pejman, Jacqueline J. Steenhuis, David L. Farren, and Brain K. Kobika. "Agonist-induced Conformational Changes in the G-protein-coupling Domain of the β2 Adrenergic Receptor." Proceedings of the Nation Academy of Sciences of the United States of America 98.11 (2001): 5997-6002. Web.

Kobilka, B., and G. Schertler. "New G-protein-coupled Receptor Crystal Structures: Insights and Limitations." Trends in Pharmacological Sciences 29.2 (2008): 79-83. Web.

Rasmussen, Søren G. F., Brian T. DeVree, Yaozhong Zou, Andrew C. Kruse, Ka Young Chung, Tong Sun Kobilka, Foon Sun Thian, Pil Seok Chae, Els Pardon, Diane Calinski, Jesper M. Mathiesen, Syed T. A. Shah, Joseph A. Lyons, Martin Caffrey, Samuel H. Gellman, Jan Steyaert, Georgios Skiniotis, William I. Weis, Roger K. Sunahara, and Brian K. Kobilka. "Crystal Structure of the β2 Adrenergic Receptor–Gs Protein Complex." Nature 477.7366 (2011): 549-55. Web.

Rasmussen, Søren G. F., Hee-Jung Choi, Daniel M. Rosenbaum, Tong Sun Kobilka, Foon Sun Thian, Patricia C. Edwards, Manfred Burghammer, Venkata R. P. Ratnala, Ruslan Sanishvili, Robert F. Fischetti, Gebhard F. X. Schertler, William I. Weis, and Brian K. Kobilka. "Crystal Structure of the Human β2 Adrenergic G-protein-coupled Receptor." Nature 450.7168 (2007): 383-87. Print.

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