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RNA Polymerase PB1-PB2 subunits from Influenza A Virus

Brittany Currey '11 and Lauren Brady '11


Contents:


I. Introduction

The influenza virus belongs to Orthomyxoviridae family, which is composed of six different RNA viruses.   The influenza A virus contains eight negative-strand RNA (vRNA) segments, all of which encode 10 different viral proteins. This is a particularly common disease in birds, mammals, and humans.  The estimated death toll in the United States on average is 50,000 people annually.  Given the more recent outbreaks with avian influenza, particularly in Asia, many fear that these viral strands will adapt to human hosts, as this has been the cause of three influenza pandemics in the last 300 years.  Symptoms include fever, headache, and nasal discharge which can give way to more obstructive pulmonary and heart problems including cardiac failure and bacterial pneumonia.  In the search for new anti-influenza pharmaceuticals, the viral RNA (vRNA) polymerase has the potential to be a strong target of study due to high conservation among strains of influenza virus. 

This vRNA polymerase is composed of three subunits: PB1, PB2, and PA. Although there is contact between PA and PB1, there are no direct interations between PA and PB2. These subunits play distinct roles within the polymerase and are all crucial for viral transcription and replication. The PB2 subunit of the RNA polymerase forms a ribonuleoprotein (RNP) complex with its eight genome segments and moves into the nucleus. Once in the nucleus, the RNP complex initiates the process of cap snatching before viral mRNA moves to the cytoplasm to undergo translation. During this process, PB2 binds cap-containing mRNA in order to produce primers for RNA synthesis.  An endonuclease from the PA subunit then cuts the cap-containing oligonucleotide pre-mRNA of the host cell allowing it to be extended into viral mRNA by the polymerase. (Cap Snatching)

Within the RNAP complex, the PB1-PB2 interface is needed for transcription initiation and is dependent on the short N-terminal fragment of PB2 (PB2-N) . Recent studies suggest that suitable small molecules may disrupt this interaction and possibly restrict viral replication, making this easily accessible site a strong drug target. 

 


II. PB1-PB2 interaction Domain

A co-precipitation assay was used to observe the interaction between the C-terminus of PB1 (PB1-C) and the N-terminus of PB2 (PB2-N) .  Residues 1-37 and 1-86 of PB2-N are required for subunit binding to PB1-C.  A stable RNAP complex was crystallized consisting of residues 678-757 of PB1-C and residues 1-37 of PB2-N.

There are two copies of PB1 and PB2 subunits, each containing three α helices. The majority of interaction energy is provided by helix 1 of PB2-N, which lies against helices 2 and 3 of PB1-C.   Helix 1 of PB1-C is positioned between all three helices of PB2-N.

Polar interactions, hydrogen bonds, and some buried apolar contacts between PB1-PB2 allow for the complex to remain tightly bound.   Within the RNAP, the PB1-PB2 interface contains the most extensive buried surface area as a result of the '3 plus 3' helix structure. The interface between PB1-C and PB2-N contains four salt bridges between Glu 2 and Lys 698 , Arg 3 and Asp 725 , Arg 3 and Lys 698 , and Glu 6 and Lys 698 .   Apolar contacts include an interaction between two PB2 residues (Ile 4 and Leu 7).   Eight hydrogen bonds between polypeptides supply further stability of the complex. 


III. PB1 and PB2 double mutants

The presence of PB2 is necessary for functionality of RNAP.  The extended shape of PB2 hinders most intermolecular contacts between its three helices.   However, deletions of Helix 1 reveal its importance as measured by vRNA synthesis, reducing production of RNA product by 90%.  When two nonpolar amino acids (Ile 4 and Leu 7, or Leu 7 and Leu 10) of helix 1 were simultaneously replaced with polar serine residues, polymerase activity was greatly reduced.  Similar replacements in PB1 (Val 715 and Ile 746, or Ile 746 and Ile 750) with serine residues not only led to the reduction in vRNA but also cRNA and mRNA.  The nearby polar residues at the protein surface (Ser 713 and Arg 754) can easily accommodate a serine deep within the hydrophobic core without preventing PB1 and PB2 binding.

 


IV. PB1 single mutants

Single amino acid replacements on PB1 did not significantly prevent PB1-PB2 binding enough to inhibit mRNA production.  The only exception was the replacement of Val 715 with a Ser (V715S) which still showed significant binding to PB2 with corresponding reduction in RNAP activity.  This altered mode of interaction has an effect on the efficiency of polymerase.  Another single mutant displaced Leu 695 and Ile 750 with an aspartate without preventing PB1-PB2 binding due to their accessibility to solvent water.


V. Conclusion

PB1 - PB2 interactions allow for the functionality of viral RNA polymerase. Helix 1 of PB2 is an important subunit that dramatically affects the activity of the RNAP when removed.  The V715S mutation does not inhibit the interaction between PB1 and PB2 but hinders the communication between PB1 and PB2 resulting in the loss of activity of RNAP.  The PB1-PB2 may be a potential target for novel anti-influenza drugs due to its importance in viral replication. 

 



VI. References

Boivin, Stéphane, Stephen Cusack, Rob Ruigrok, and Darren J. Hart. "Influenza A Virus Polymerase: Structural Insights into Replication and Host Adaptation Mechanisms." The Journal of Biological Chemistry. 10 June 2010. Web. 14 Dec. 2010. <http://www.jbc.org/content/285/37/28411.full>.

Gulligan, Delphine; Tarendeau, Franck; Resa-Infante, Patricia; Coloma, Rocío; Crepin, Thibaut; Sehr, Peter; Lewis, Joe; Ruigrok, R.W.H.; Ortin, Juan; Hart, Darren J.; Cusack, Stephen. 2008. The structural basis for cap binding by influenza virus polymerase subunit PB2. Nature Structural & Molecular Biology 15 (5): 500-506.

Honda, Ayae, Mizumoto, Kiyohisa, and Ishihama, Akira.  2002.  Minimum molecular architectures for transcription and replication of the influenza virus.  PNAS 99: 13166-13171.

Hunt, Margaret. "Virology-Influenza Virus (Orthomyxovirus)." University of South Carolina: Biomedical Sciences Graduate Program. 2009. Web 18 Nov. 2010. <http://pathmicro.med.sc.edu/mhunt/flu.htm>.

Silva, Nathan and David Marcey. "An Introduction to Jmol* Scripting*." 2007. Web 7 Dec. 2010. <http://www.callutheran.edu/Academic_Programs/Departments
/BioDev/omm/scripting/molmast.htm>.

Sugiyama, Kanako, Obayashi, Eiji, Kawaguchi, Atsushi, Suzuki, Yukari, Tame, Jeremy RH., Nagata, Kyosuke, and Park, Sam-Yong.  2009.  Structural insight into the essential PB1-PB2 subunit contact of the influenza virus RNA polymerase. EMBO Journal 28: 1803-1811.

 

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