Molecular dynamics study of HIV-1 RT-DNA-nevirapine complexes explains NNRTI inhibition and resistance by connection mutations

Proteins. 2014 May;82(5):815-29. doi: 10.1002/prot.24460. Epub 2013 Nov 22.

Abstract

HIV-1 reverse transcriptase (RT) is a multifunctional enzyme that is targeted by nucleoside analogs (NRTIs) and non-nucleoside RT inhibitors (NNRTIs). NNRTIs are allosteric inhibitors of RT, and constitute an integral part of several highly active antiretroviral therapy regimens. Under selective pressure, HIV-1 acquires resistance against NNRTIs primarily by selecting mutations around the NNRTI pocket. Complete RT sequencing of clinical isolates revealed that spatially distal mutations arising in connection and the RNase H domain also confer NNRTI resistance and contribute to NRTI resistance. However, the precise structural mechanism by which the connection domain mutations confer NNRTI resistance is poorly understood. We performed 50-ns molecular dynamics (MD) simulations, followed by essential dynamics, free-energy landscape analyses, and network analyses of RT-DNA, RT-DNA-nevirapine (NVP), and N348I/T369I mutant RT-DNA-NVP complexes. MD simulation studies revealed altered global motions and restricted conformational landscape of RT upon NVP binding. Analysis of protein structure network parameters demonstrated a dissortative hub pattern in the RT-DNA complex and an assortative hub pattern in the RT-DNA-NVP complex suggesting enhanced rigidity of RT upon NVP binding. The connection subdomain mutations N348I/T369I did not induce any significant structural change; rather, these mutations modulate the conformational dynamics and alter the long-range allosteric communication network between the connection subdomain and NNRTI pocket. Insights from the present study provide a structural basis for the biochemical and clinical findings on drug resistance caused by the connection and RNase H mutations.

Keywords: N348I; RNase H; T369I; allosteric communication; connection mutations; drug resistance; protein structural network.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Biocatalysis
  • Catalytic Domain
  • DNA, Viral
  • Drug Resistance, Viral / genetics*
  • HIV Reverse Transcriptase / antagonists & inhibitors*
  • HIV Reverse Transcriptase / chemistry*
  • HIV-1 / enzymology
  • HIV-1 / genetics
  • Molecular Dynamics Simulation*
  • Mutation / genetics*
  • Nevirapine / chemistry*
  • Protein Structure, Tertiary
  • Reverse Transcriptase Inhibitors / chemistry*
  • Thermodynamics

Substances

  • DNA, Viral
  • Reverse Transcriptase Inhibitors
  • Nevirapine
  • reverse transcriptase, Human immunodeficiency virus 1
  • HIV Reverse Transcriptase