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Allostery in the dengue virus NS3 helicase: Insights into the NTPase cycle from molecular simulations

Date

2018-03-01

Authors

McCullagh, Martin
Davidson, Russell
Hendrix, Josie
Geiss, Brian

Journal Title

Journal ISSN

Volume Title

Abstract

The C-terminus domain of non-structural 3 (NS3) protein of the Flaviviridae viruses (e.g. HCV, dengue, West Nile, Zika) is a nucleotide triphosphatase (NTPase) -dependent superfamily 2 (SF2) helicase that unwinds double-stranded RNA while translocating along the nucleic polymer. Due to these functions, NS3 is an important target for antiviral development yet the biophysics of this enzyme are poorly understood. Microsecond-long molecular dynamic simulations of the dengue NS3 helicase domain are reported from which allosteric effects of RNA and NTPase substrates are observed. The presence of a bound single-stranded RNA catalytically enhances the phosphate hydrolysis reaction by affecting the dynamics and positioning of waters within the hydrolysis active site. Coupled with results from the simulations, electronic structure calculations of the reaction are used to quantify this enhancement to be a 150-fold increase, in qualitative agreement with the experimental enhancement factor of 10-100. Additionally, protein-RNA interactions exhibit NTPase substrate-induced allostery, where the presence of a nucleotide (e.g. ATP or ADP) structurally perturbs residues in direct contact with the phosphodiester backbone of the RNA. Residue-residue network analyses highlight pathways of short ranged interactions that connect the two active sites. These analyses identify motif V as a highly connected region of protein structure through which energy released from either active site is hypothesized to move, thereby inducing the observed allosteric effects. These results lay the foundation for the design of novel allosteric inhibitors of NS3.

Description

Department of Chemistry

Rights Access

Subject

dengue virus
helicase
allostery
ATP hydrolysis
molecular dynamics

Citation

Associated Publications

Davidson RB, Hendrix J, Geiss BJ, McCullagh M (2018) Allostery in the dengue virus NS3 helicase: Insights into the NTPase cycle from molecular simulations. PLoS Comput Biol 14(4): e1006103. https://doi.org/10.1371/journal.pcbi.1006103