Exaptation of Bornavirus-Like Nucleoprotein Elements in Afrotherians

PLoS Pathog. 2016 Aug 12;12(8):e1005785. doi: 10.1371/journal.ppat.1005785. eCollection 2016 Aug.

Abstract

Endogenous bornavirus-like nucleoprotein elements (EBLNs), the nucleotide sequence elements derived from the nucleoprotein gene of ancient bornavirus-like viruses, have been identified in many animal genomes. Here we show evidence that EBLNs encode functional proteins in their host. Some afrotherian EBLNs were observed to have been maintained for more than 83.3 million years under negative selection. Splice variants were expressed from the genomic loci of EBLNs in elephant, and some were translated into proteins. The EBLN proteins appeared to be localized to the rough endoplasmic reticulum in African elephant cells, in contrast to the nuclear localization of bornavirus N. These observations suggest that afrotherian EBLNs have acquired a novel function in their host. Interestingly, genomic sequences of the first exon and its flanking regions in these EBLN loci were homologous to those of transmembrane protein 106B (TMEM106B). The upstream region of the first exon in the EBLN loci exhibited a promoter activity, suggesting that the ability of these EBLNs to be transcribed in the host cell was gained through capturing a partial duplicate of TMEM106B. In conclusion, our results strongly support for exaptation of EBLNs to encode host proteins in afrotherians.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acid Sequence
  • Animals
  • Biological Evolution*
  • Blotting, Western
  • Bornaviridae / genetics
  • Elephants / genetics
  • Elephants / virology*
  • Endogenous Retroviruses / genetics*
  • Immunohistochemistry
  • Nucleoproteins / genetics
  • Phylogeny
  • Polymerase Chain Reaction
  • Sequence Homology, Amino Acid

Substances

  • Nucleoproteins

Grant support

This work was supported by research grants from College of Bioresource Sciences, Nihon University, and the Strategic Research Base Development Program, “International joint research and training of young researchers for zoonosis control in a globalized world”, and a matching fund subsidy from the Ministry of Education, Culture, Sports, Science and Technology of Japan (S1491007) to YK. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.