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Glycogen Synthase Kinase-3beta (GSK-3beta)


Ren DeBrosse '18 and Katie Kaestner '16


Contents:


I. Introduction

Model View:
Color Scheme:


Glycogen synthase kinase 3-beta (GSK-3beta) is a serine-threonine protein kinase involved in several signaling pathways regulating cell proliferation, differentiation, and apotosis. Although first discovered in glycogen metabolism and insulin response pathways, GSK-3beta plays a critical role in Wnt, Hedgehog, and Reelin signaling pathways as well. GSK-3beta's wide-ranging regulatory effects make it a focus of study for many diseases, including diabetes, Alzheimer's Disease, Parkinson's Disease, schizophrenia, and some types of cancers, among others. 

In the search for pharmaceuticals that can inhibit this kinase, the major targets for inhibition are the kinase active sites where its targets get phosphorylated and the ATP activation site. The problem with many compounds that can bind these sites is that they also bind to other necessary signaling molecules, such as cyclin-dependent kinases. In this tutorial, we present a molecule designed by the pharmaceutical company Astra-Zeneca that inhibits GSK-3beta at an ATP-binding site specific to the protein. 


II. General Structure

Here, we see the homodimer GSK-3beta in its form. Each monomer consists of a beta-strand, N-terminal domain and a ?-helical, C-terminal domain. A short helix interrupts the beta-barrel. The activation segment is responsible for the protein kinase's catalytic activity.

All protein kinases share a conserved overall fold but differ in the core sequences of their activation segments, and phosphorylation of these activation segments serve to activate many kinases.



The includes a , a , an , and a , in order from N to C terminus. The segment is flanked by DFG and APE at the N-terminal and C-terminal ends, respectively. 


III. Dimer Interface

The monomers of the homodimeric GSK-3beta protein align in an intermolecular head-to-tail fashion, where the residues Asp 260 to Val 263 at the N terminus of one monomer interacts with the residues Tyr 216 to Arg 220 through a series of at the end of the activation segment on the C terminal domain of the other monomer. Residues Ile 228, Phe 229, Gly 262, Val 263, and Leu 266 on the one monomer form a in which the hydrophobic side chain of Tyr 216 of the other monomer interacts.

Although the monomers at the  visibly possesses shape complementarity overall, direct interactions between them are few. These interactions include hydrogen bonding between the peptide carbonyls and nitrogens of , and . 


IV. Phosphorylation Sites


Kinase activity is typically regulated by the phosphorylation of a particular residue of the activation loop, called the primary phosphorylation site. The interaction between the basic residues of the N-terminal domain and the phosphorylated activation loop drives the conformational change of the loop into a substrate binding pocket. GSK-3beta, however, lacks a primary phosphorylation site and has Val 214 in the place of the phosphorylatable residue . Some protein kinases like GSK-3beta have instead what are called secondary phosphorylation sites, which do not interact with the substrate binding pocket. The residue Tyr 216 is one such site.

Tyr 216 is an important secondary phosphorylation site to GSK-3beta catalytic activity, but buries much of the protein’s accessible surface. Phosphorylation of Tyr 216 rotates its side chain from the “down” conformation in the dimer interface to the “up” conformation, thereby opening up the substrate binding pocket previously obstructed by the dimerization.




The above is an illustration of an unphosporylated GSK-3beta and a phosphorylated GSK-3beta, with AR-A014418 (represented as the space-filling molecule) bound to the substrate groove on the phosphorylated GSK-3beta (Bhat et al.) Our interactive model comes from a file that codes for unphosphorylated GSK-3beta, but here it is apparent how Tyr 216 moves out of the way to allow the ligand to bind.


V. Substrate Binding Pocket


GSK-3beta has a made up of 3 basic N-terminal residues - Arg 96 from helix beta C, Arg 180 from the activation loop, and Lys 205 from beta9 – and the peptide nitrogen of Val 214. An anion fills the pocket opened by secondary phosphorylation, neutralizing and stabilizing the basic pocket, and marks it for a residue in the substrate phosphorylated by another kinase.  Note how the substrate binding pocket is located on the periphery of the molecule for easier substrate access and recognition.

Thus, GSK-3beta uses the pocket not as a site of regulatory control like other protein kinases with primary phosphorylation sites, but exclusively as a substrate recognition site for primed, pre-phosphorylated substrates, which allows GSK-3beta to work more efficiently.


VI. ATP-mimetic Inhibitor Interaction

Here, the inhibitor designed by Astra-Zeneca is shown bound at Ser 396 (not shown due to instability of crystal structure past reside 384). The inhibitor N-(4-methoxybenzyl)-N'-(5-nitro-1,3-thiazol-2-yl)urea, or AR-A014418 as its manufacturer calls it, binds in competition with ATP to the . The inhibitor interacts with the ATP binding pocket primarily through with residues Lys 85, Glu 97, and Asp 200 and hydrogen bonding with residues and . The residue Asp 200 is a conserved catalytic residue in the DFG of the magnesium binding loop that binds a magnesium ion, which will position the ATP phosphates for transfer to serine side chains. Some additional residues are important in differentiating the selectivity of the GSK-3beta ATP binding pocket for AR-A014418 from cdk2, another protein kinase that has an ATP binding pocket similar to that of GSK-3beta. acts as a "selectivity residue", and a Glu-Arg salt bridge defines the edge of the binding pocket (Ghat et al.).


VII. References

Bhat, Ratan, Yafeng Xue, Stefan Berg, Sven Hellberg, Mats Ormö, Yvonne Nilsson, Ann-Cathrin Radesäter, Eva Jerning, Per-Olof Markgren, Thomas Borgegård, Martin Nylöf, Alfredo Giménez-Cassina, Félix Hernández, Jose J. Lucas, Javier Díaz-Nido, and Jesús Avila. 2003. Structural Insights and Biological Effects of Glycogen Synthase Kinase 3-specific Inhibitor AR-A014418. J. Biol. Chem. 278:45937-45945.

Dajani, Rana, Elizabeth Fraser, S. Mark Roe, Neville YOung, Valerie Good, Trevor C. Dale, and Laurence H. Pearl. Crystal Structure of Glycogen Synthase Kinase 3b: Structural Basis for Phosphate-Primed Substrate Specificity and Autoinhibition. 2001. Cell 105:721-732.

Nolen, Brad, Susan Taylor, and Gourisankar Ghosh. 2004. Regulation of Protein Kinases: Controlling Activity through Activation Segment Conformation. Molecular Cell 15: 661-675.


ter Haar, Ernst, Joyce T. Coll, Douglas A. Austen, Hsun-Mei Hsiao, Lora Swenson, and Jugnu Jain. 2001. Structure of GSK3b reveals a primed phosphorylation mechanism. Nature Publishing Group 8:593-596.

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