An unusually high substitution rate in transplant-associated BK polyomavirus in vivo is further concentrated in HLA-C-bound viral peptides

PLoS Pathog. 2018 Oct 18;14(10):e1007368. doi: 10.1371/journal.ppat.1007368. eCollection 2018 Oct.

Abstract

Infection with human BK polyomavirus, a small double-stranded DNA virus, potentially results in severe complications in immunocompromised patients. Here, we describe the in vivo variability and evolution of the BK polyomavirus by deep sequencing. Our data reveal the highest genomic evolutionary rate described in double-stranded DNA viruses, i.e., 10(-3)-10(-5) substitutions per nucleotide site per year. High mutation rates in viruses allow their escape from immune surveillance and adaptation to new hosts. By combining mutational landscapes across viral genomes with in silico prediction of viral peptides, we demonstrate the presence of significantly more coding substitutions within predicted cognate HLA-C-bound viral peptides than outside. This finding suggests a role for HLA-C in antiviral immunity, perhaps through the action of killer cell immunoglobulin-like receptors. The present study provides a comprehensive view of viral evolution and immune escape in a DNA virus.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Substitution
  • BK Virus / genetics*
  • BK Virus / immunology
  • Genome, Viral
  • HLA-C Antigens / genetics
  • HLA-C Antigens / immunology
  • HLA-C Antigens / metabolism*
  • High-Throughput Nucleotide Sequencing
  • Humans
  • Mutation*
  • Organ Transplantation*
  • Peptide Fragments / genetics
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism*
  • Phylogeny
  • Polyomavirus Infections / genetics
  • Polyomavirus Infections / immunology
  • Polyomavirus Infections / virology*

Substances

  • HLA-C Antigens
  • Peptide Fragments

Grants and funding

This work has been published under the framework of the Laboratoire d’Excellence (LABEX) TRANSPLANTEX [ANR-11-LABX-0070_TRANSPLANTEX] and benefits from a funding from the French government, managed by the French National Research Agency (ANR) as part of the « Investments for the future » program (SB)(http://www.agence-nationale-recherche.fr/investissementsdavenir/). Additional support was received from the Strasbourg High Throughput Next Generation Sequencing facility (GENOMAX)(SB)(no URL available), the Institut National de la Santé et de la Recherche Médicale (INSERM)(SB)(www.inserm.fr), Initiative d'Excellence (IDEX) fund of the University of Strasbourg (UNISTRA)(SB)(www.unistra.fr), the Institut Universitaire de France (IUF)(SB)(http://www.iufrance.fr), projects BFU2014-58656R and BFU2017-89594R from Ministry of Economy and Competitiveness (MINECO; Spanish Government) (http://www.idi.mineco.gob.es)(FGC) and the project PROMETEO/2016/122 from the Generalitat Valenciana (FGC)(www.gva.es/). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.