Yeast Poly(A) Polymerase

Garrett Thesing '24 and Logan Spiess '23


Contents:


I. Introduction

In eukaryotes, pre-mRNA transcripts are cleaved at a consensus sequence and a tract of 100 to 250 adenine nucleotides are added to the 3' end of the nascent transcript. This process is known as polyadenylation and it is an important step in RNA processing. The addition of the poly(A) tail helps protect the transcript from degradation and aids in its export from the nucleus to the cytoplasm where it can be translated into a polypeptide. The poly(A) tail is also essential for the formation of the closed loop structure that is necessary for translation initiation in most eukaryotic mRNA transcripts. In some mRNA transcripts, there can be multiple polyadenylation sites. Because many binding sites for regulatory proteins and RNAs exist in the 3' UTR, alternative polyadenylation in this region can have a profound effect on gene expression. In some cases, alternative polyadenylation sites can occur in the coding region of a gene which can result in the production of distinct protein isoforms from the same gene.

Of the several proteins that are involved in polyadenylation, poly(A) polymerase (PAP) is the enzyme which is responsible for adding a poly(A) tail to the 3' end of pre-mRNA transcripts. It is a template-independent polymerase which belongs to the DNA polymerase beta family (Balbo and Bohm). It uses the 3' end of the nascent mRNA strand as a primer and adds adenine nucleotides non-templated. It can synthesize the poly(A) tail in a processive manner when other components of the polyadenylation machinery are bound to the RNA substrate (Wahle).


II. General Structure

Yeast poly(A) polymerase is 530 amino acids long and is composed of three domains; the N-terminal domain (residues 40-190), middle domain (residues 1-39 and 190-353) and C-terminal domain (residues 353-530) encircle a substrate binding cleft where RNA and ATP bind (Balbo and Bohm) . The N-terminal domain is homologous to the catalytic palm domain of other beta polymerases. In the active site, three aspartate residues (100, 102, 154) coordinate two catalytically-required magnesium ions (Zhelkovsky et al.). In this structure, Asp154 is mutated to Ala154 so the second magnesium ion is missing . The C-terminal domain plays an important role in holding the RNA substrate. The middle domain is thought to function similarly to the fingers domain of template-directed polymerases in that it helps to properly orient the incoming ATP in the active site (Balbo and Bohm).


III. ATP Specificity

In order for Poly(A) Polymerase to add adenines to the 3' end of the pre-mRNA transcript, it must have specificity for ATP in its active site. Asp100 and Asp 102 interact with a magnesium ion which in turn interacts with the phopsphates of ATP, helping to position it in the active site . There is a non-polar base stacking interaction between the adenine base base of ATP and the 3'-terminus of the RNA substrate . On the opposite side of the base stacking interaction, Val 234 makes Van der Waals interactions with the adenine base and ribose of ATP (Balbo and Bohm). These non-polar interactions promote purine specificity in the active site. Three water molecules buried within the complex near the active site hydrogen bond with N3, N6, and N7 of the adenine base . These specific hydrogen bonds promote specificity for ATP over GTP. The side chains of Thr 304, Met310, and Ala312 come in close contact with the C2 of adenine . This close steric contact further promotes specificity for ATP over GTP; the amino group at this position in guanine would not fit between these amino acid residues (Hodis et al.)


IV. RNA Binding

4 nucleotides at the 3' end of the Poly(A) RNA make contact with PAP. The -4 nucleotide (5'-most residue) makes contact with the surface of the enzyme while the -3, -2, and -1 (3'-terminal residue) nucleotides are in contact with the interior of the enzyme . The -1 nucleotide is positioned between Val141 and the incoming ATP . Several hydrogen bonds form between the -1 nucleotide and amino acid residues of the enzyme. The 2' hydroxyl forms a hydrogen bond with the side chain hydoxyl of Tyr87 and the phosphate group oxygen forms a hydrogen bond with Asn226 . Additionally, the -1 nucleotide is bound in the enzyme through an interaction between its 3' hydroxyl and a catalytic magnesium ion which is coordinated by Asp154 (Balbo and Bohm). As mentioned above, Asp154 is mutated to Ala154 so the magnesium ion is not present in this structure. Overall, the positioning of the Poly(A) RNA within the enzyme ensures that the incoming adenine nucleotide can be effectively added to the 3' end.


V. Closed Ternary Complex

The absence of the second catalytically-required magnesium ion inhibits the catalytic activity of the enzyme but does not affect binding of the RNA and ATP substrates. When both the RNA and ATP substrates are bound in the active site, poly(A) polymerase adopts its 'closed' substrate-bound ternary complex. There are two defined hinge regions in PAP: one between the N-terminal and middle domains (residues around 40 and 190) and one between the middle and C-terminal domains (residues around 353)(Balbo and Bohm). When PAP adopts its 'closed' conformation, movement of the domains about these hinge regions is observed: both the N-terminal and C-terminal domains rotate inward toward the middle domain.



VI. References

Balbo, Paul B, and Andrew Bohm. Mechanism of poly(A) polymerase: structure of the enzyme-MgATP-RNA ternary complex and kinetic analysis. Structure (London, England : 1993) vol. 15,9 (2007): 1117-31. doi:10.1016/j.str.2007.07.010.

Hodis, Eran, Michal Harel, David Canner, Joel L. Sussman, OCA, Alexander Berchansky, Jaime Prilusky, David S. Goodsell, Eric Martz. Poly(A) Polymerase. Proteopedia. https://proteopedia.org/wiki/index.php/Poly%28A%29_Polymerase.

Zhelkovsky, Alexander, Steffen Helming, Andrew Bohm, Claire Moore. et al. Mutations in the Middle Domain of Yeast Poly(a) Polymerase Affect Interactions with RNA but Not ATP. RNA. vol. 10, no. 4, 2004, pp. 558-564., https://doi.org/10.1261/rna.5238704

Elmar Wahle. Poly(A) Tail Length Control Is Caused by Termination of Processive Synthesis. Journal of Biological Chemistry. vol. 270, Issue 6, 1995, pp. 2800-2808, https://doi.org/10.1074/jbc.270.6.2800.

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