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Homodimeric Structure and Double-stranded RNA Cleavage Activity of the RNase IIIb Domain of Human Dicer

Mary Myers '12 and Brian Thorne '12


Contents:


I. Introduction

    Dicer protein is responsible for generating short, non-coding  interfering RNAs and microRNAs duplexes from dsRNA, and is therefore critical for the RNAi pathway[1], which leads to sequence-specific translational repression of genes.  The dsRNA duplexes formed via Dicer cleavage are generated with symmetric 2–3nt 3' overhangs and 5'-phosphate and 3'-hydroxyl groups, which trigger the degradation of mRNAs with a matching  sequence.[2] Human Dicer is a large, multi domain protein about 200,000 Daltons in size, and is classified as a class 3 RNase protein. Classification is based on the observation of  two RNase III nuclease domains; RNase IIIa and RNase IIIb.  Both of these domains can be found either as fragments, or can coordinate into homodimers.  While this tutorial focuses predominately on the RNase IIIb domain of the protein, the folllowing image represents the remaining domains included in a complete dicer complex: [3]


II. General Structure

    Analysis has indicated that the nature of the single processing center in Human (Hs)-Dicer, suggests that RNase IIIb domain fragments are capable of forming intramolecular dimers, which result in two catalytic sites within the processing center; one on each end of the dimer interface.  Each catalytic site cleaves RNA phosphodiester bonds and generates ~20nt dsRNA products with 2 nt 3' overhangs. Other domains, such as the RNA Binding domain (RBD), dsRNA Binding Domain (dsRBD) and PAZ assist the cleavage reaction. The RNase IIIb domains specifically requires Mg2+ ions to catalyze the hydrolysis of the RNA phosphodiester backbone.  

    The crystal structure of RNase IIIb domain is known to a resolution of 2.0 Å. Each of the monomers that constitute the RNase IIIb homodimer possess a highly conserved structure with 62% helical composition[3] and contains 8 α-helices as well as a relatively rare 310 helix (helix 2)[5],   but has no ß-strands in its structure.  The dimerization of the monomers and the protein's specific folding result in a negatively charged valley which supports the Mg2+ ions required for cleavage.  This negative protein valley is represented in the accompanying image by the blue region within the interface of the dimer.  The charge difference within the valley provided by the positive metal ions allows the dsRNA substate to bind more readily by possibly neutralizing the repulsive charge, and in addition results in the resolution of two RNA cutting sites within each catalytic site.  Two cutting sites are necessary at each catalytic site, so that both strands of the dsRNA substrate can be processed, and the 3' overhang can be formed.

 


III. Homodimerization 

    The RNase IIIb exists in solution as a stable dimer with tight associations. The interface between the two monomers forms the base of the previously mentioned valley via interactions between the anti-parallel α3  helicies the and the α4 helicies, as well as interactions between the α7 C-terminus and α8 N-terminus within each monomer. 

     
Hydrophobic interactions are the main driving force of dimerization through the interactions of aromatic residues from both monomers in the dimer interface formed by the two anti-parallel α3 helicies 
[Phe]1706 interacts with [Thr]1717, [Leu]1732, and [Arg]1736.

-[Tyr]1714 interacts with [Ile]1711 and  [Leu]1827:  The Leucine residues increase dimer stability by associating the α9 helicies with the dimer interface.  

[Tyr]1721 interacts with [Arg]1703 and [Leu]1703
near the ends of the α3 helicies. 

 


IV. Active Site


As mentioned, two Mg2+ ions are bound by each RNase IIIb domain either at, or close to, the active site.  The two ions are differentiated as Mg-1 and Mg-2 depending on their location within the active site.  These four ions are each coordinated by eight interactions with oxygen atoms.  Mg-1 atoms directly interact with carboxylate oxygen atoms in [Asp]1810,
[Glu]1705, , ,  and [Glu]1813,  as well as three molecules of water, . [Asp]1709 interacts with one of the three coordinated water molecules that stabilize the Mg-1 ion. Mg-2 interacts directly with the carboxylate oxygen of [Asp]1709 and four water molecules .[Asp]1709 also interacts with one of the water molecules here as well . Two [Asp]1713 residues (only one shown) positioned centrally in the homodimer interact with the coordinated water molecules .  


It is presumed that the Mg-1 ion functions to activate the nucleophilic water molecule, and is positioned appropriately within the molecule for it to serve this purpose. Being near the end of the catalytic site places the nucleophile in the most stereochemically favorable area within this specific domain.  When complexed in a crystal with the enzyme, the dsRNA substrate ended up colliding with the N-terminus of the
α6 helix within the RNase IIIb domain.   Given this information, a comformational change is likely to occur either in the protein or with the dsRNA substrate; maybe even both.  When the substrate is within the dimer interface, the Mg-2 ions are closely associated with the minor groove of the RNA helix between the two cleavage sites.  A logical explanation for this observation would be to neutralize the negatively charged valley within the dimer near the active sites.[3]

    



VI. References

[1]http://www.scq.ubc.ca/wp-content/siRNA.gif

[2] Cioca, DP et al. 2003.  RNA interference is the functional pathway with therapeutic potential in huma myeloid leukemia cell lines. Gene Cancer Therapy.  Feb; 10(2): 125-33.  

 [3]Takeshita, D. et al. 2007. Homodimeric Structure and Double-stranded RNA Cleavage Activity of the C-terminal RNase III Domain of Human Dicer. The Journal of Molecular Biology 374:106-120.

[4]http://www.genecards.org/cgi-bin/carddisp.pl?gene=dicer1

[5] Blaszcyk, J. et al. 2004. Noncatalytic Assembly of Ribonuclease III with Double-Stranded RNA.  Structure 12:3 March 2004, Pages 457-466.

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