Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome

Significance Sequences derived from ancient viruses have been shown to make up a substantial part of animal genomes. Bornaviruses, a genus of nonsegmented, negative-sense RNA virus, also have left their DNA copies in the genomes of a number of vertebrate lineages. Recent studies have demonstrated th...

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Published inProceedings of the National Academy of Sciences - PNAS Vol. 111; no. 36; pp. 13175 - 13180
Main Authors Fujino, Kan, Horie, Masayuki, Honda, Tomoyuki, Merriman, Dana K., Tomonaga, Keizo
Format Journal Article
LanguageEnglish
Published United States National Academy of Sciences 09.09.2014
National Acad Sciences
Subjects
Amino Acid Sequence
Amino acids
Animals
Base Sequence
Biological Sciences
Borna Disease - transmission
Borna Disease - virology
Borna disease virus
Borna disease virus - physiology
Cell lines
Cercopithecus aethiops
Conserved Sequence - genetics
DNA
DNA-Directed DNA Polymerase - metabolism
evolution
genome
Genome - genetics
Genomes
HEK293 Cells
hosts
Humans
Infections
Molecular Sequence Data
Mononegavirales
Protein Structure, Tertiary
Proteins
Replicon - genetics
Retroviridae
Retrovirus
Ribonucleoproteins - metabolism
RNA
Sciuridae
Sciuridae - genetics
Sciuridae - virology
Small mammals
Spermophilus
Transfection
Vero Cells
vertebrates
Viral Proteins - chemistry
Viral Proteins - metabolism
virus replication
Virus Replication - genetics
Viruses
antiviral immunity
endogenous nonretroviral viruses
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Abstract Significance Sequences derived from ancient viruses have been shown to make up a substantial part of animal genomes. Bornaviruses, a genus of nonsegmented, negative-sense RNA virus, also have left their DNA copies in the genomes of a number of vertebrate lineages. Recent studies have demonstrated that some endogenous bornavirus-like elements (EBLs) may have acquired functions in their hosts as a result of exaptation. In this study, we show that protein encoded by an EBL in the genome of the thirteen-lined ground squirrel efficiently blocks infection and replication of extant bornavirus. To our knowledge, this is the first report showing that endogenous nonretroviral RNA virus elements may function in antiviral defense, providing a potential role for RNA virus endogenization in host evolution.
AbstractList Animal genomes contain endogenous viral sequences, such as endogenous retroviruses and retrotransposons. Recently, we and others discovered that nonretroviral viruses also have been endogenized in many vertebrate genomes. Bornaviruses belong to the Mononegavirales and have left endogenous fragments, called "endogenous bornavirus-like elements" (EBLs), in the genomes of many mammals. The striking features of EBLs are that they contain relatively long ORFs which have high sequence homology to the extant bornavirus proteins. Furthermore, some EBLs derived from bornavirus nucleoprotein (EBLNs) have been shown to be transcribed as mRNA and probably are translated into proteins. These features lead us to speculate that EBLs may function as cellular coopted genes. An EBLN element in the genome of the thirteen-lined ground squirrel (Ictidomys tridecemlineatus), itEBLN, encodes an ORF with 77% amino acid sequence identity to the current bornavirus nucleoprotein. In this study, we cloned itEBLN from the ground squirrel genome and investigated its involvement in Borna disease virus (BDV) replication. Interestingly, itEBLN, but not a human EBLN, colocalized with the viral factory in the nucleus and appeared to affect BDV polymerase activity by being incorporated into the viral ribonucleoprotein. Our data show that, as do certain endogenous retroviruses, itEBLN potentially may inhibit infection by related exogenous viruses in vivo.
Animal genomes contain endogenous viral sequences, such as endogenous retroviruses and retrotransposons. Recently, we and others discovered that nonretroviral viruses also have been endogenized in many vertebrate genomes. Bornaviruses belong to the Mononegavirales and have left endogenous fragments, called "endogenous bornavirus-like elements" (EBLs), in the genomes of many mammals. The striking features of EBLs are that they contain relatively long ORFs which have high sequence homology to the extant bornavirus proteins. Furthermore, some EBLs derived from bornavirus nucleoprotein (EBLNs) have been shown to be transcribed as mRNA and probably are translated into proteins. These features lead us to speculate that EBLs may function as cellular coopted genes. An EBLN element in the genome of the thirteen-lined ground squirrel (Ictidomys tridecemlineatus), itEBLN, encodes an ORF with 77% amino acid sequence identity to the current bornavirus nucleoprotein. In this study, we cloned itEBLN from the ground squirrel genome and investigated its involvement in Borna disease virus (BDV) replication. Interestingly, itEBLN, but not a human EBLN, colocalized with the viral factory in the nucleus and appeared to affect BDV polymerase activity by being incorporated into the viral ribonucleoprotein. Our data show that, as do certain endogenous retroviruses, itEBLN potentially may inhibit infection by related exogenous viruses in vivo.Animal genomes contain endogenous viral sequences, such as endogenous retroviruses and retrotransposons. Recently, we and others discovered that nonretroviral viruses also have been endogenized in many vertebrate genomes. Bornaviruses belong to the Mononegavirales and have left endogenous fragments, called "endogenous bornavirus-like elements" (EBLs), in the genomes of many mammals. The striking features of EBLs are that they contain relatively long ORFs which have high sequence homology to the extant bornavirus proteins. Furthermore, some EBLs derived from bornavirus nucleoprotein (EBLNs) have been shown to be transcribed as mRNA and probably are translated into proteins. These features lead us to speculate that EBLs may function as cellular coopted genes. An EBLN element in the genome of the thirteen-lined ground squirrel (Ictidomys tridecemlineatus), itEBLN, encodes an ORF with 77% amino acid sequence identity to the current bornavirus nucleoprotein. In this study, we cloned itEBLN from the ground squirrel genome and investigated its involvement in Borna disease virus (BDV) replication. Interestingly, itEBLN, but not a human EBLN, colocalized with the viral factory in the nucleus and appeared to affect BDV polymerase activity by being incorporated into the viral ribonucleoprotein. Our data show that, as do certain endogenous retroviruses, itEBLN potentially may inhibit infection by related exogenous viruses in vivo.
Sequences derived from ancient viruses have been shown to make up a substantial part of animal genomes. Bornaviruses, a genus of nonsegmented, negative-sense RNA virus, also have left their DNA copies in the genomes of a number of vertebrate lineages. Recent studies have demonstrated that some endogenous bornavirus-like elements (EBLs) may have acquired functions in their hosts as a result of exaptation. In this study, we show that protein encoded by an EBL in the genome of the thirteen-lined ground squirrel efficiently blocks infection and replication of extant bornavirus. To our knowledge, this is the first report showing that endogenous nonretroviral RNA virus elements may function in antiviral defense, providing a potential role for RNA virus endogenization in host evolution. Animal genomes contain endogenous viral sequences, such as endogenous retroviruses and retrotransposons. Recently, we and others discovered that nonretroviral viruses also have been endogenized in many vertebrate genomes. Bornaviruses belong to the Mononegavirales and have left endogenous fragments, called “endogenous bornavirus-like elements” (EBLs), in the genomes of many mammals. The striking features of EBLs are that they contain relatively long ORFs which have high sequence homology to the extant bornavirus proteins. Furthermore, some EBLs derived from bornavirus nucleoprotein (EBLNs) have been shown to be transcribed as mRNA and probably are translated into proteins. These features lead us to speculate that EBLs may function as cellular coopted genes. An EBLN element in the genome of the thirteen-lined ground squirrel ( Ictidomys tridecemlineatus ), itEBLN, encodes an ORF with 77% amino acid sequence identity to the current bornavirus nucleoprotein. In this study, we cloned itEBLN from the ground squirrel genome and investigated its involvement in Borna disease virus (BDV) replication. Interestingly, itEBLN, but not a human EBLN, colocalized with the viral factory in the nucleus and appeared to affect BDV polymerase activity by being incorporated into the viral ribonucleoprotein. Our data show that, as do certain endogenous retroviruses, itEBLN potentially may inhibit infection by related exogenous viruses in vivo.
Significance Sequences derived from ancient viruses have been shown to make up a substantial part of animal genomes. Bornaviruses, a genus of nonsegmented, negative-sense RNA virus, also have left their DNA copies in the genomes of a number of vertebrate lineages. Recent studies have demonstrated that some endogenous bornavirus-like elements (EBLs) may have acquired functions in their hosts as a result of exaptation. In this study, we show that protein encoded by an EBL in the genome of the thirteen-lined ground squirrel efficiently blocks infection and replication of extant bornavirus. To our knowledge, this is the first report showing that endogenous nonretroviral RNA virus elements may function in antiviral defense, providing a potential role for RNA virus endogenization in host evolution.
Author Merriman, Dana K.
Fujino, Kan
Tomonaga, Keizo
Honda, Tomoyuki
Horie, Masayuki
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  fullname: Honda, Tomoyuki
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  givenname: Dana K.
  surname: Merriman
  fullname: Merriman, Dana K.
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  givenname: Keizo
  surname: Tomonaga
  fullname: Tomonaga, Keizo
BackLink https://www.ncbi.nlm.nih.gov/pubmed/25157155$$D View this record in MEDLINE/PubMed
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Author contributions: K.F. and K.T. designed research; K.F., M.H., T.H., D.K.M., and K.T. performed research; D.K.M. contributed new reagents/analytic tools; M.H., T.H., and K.T. analyzed data; and K.F. and K.T. wrote the paper.
Edited* by John M. Coffin, Tufts University School of Medicine, Boston, MA, and approved July 24, 2014 (received for review April 17, 2014)
1Present address; Department of Microbiology II, School of Veterinary Medicine, Azabu University, Fuchinobe, Chuo-ku, Sagamihara-shi, Kanagawa 252-5201, Japan.
2Present address; Transboundary Animal Diseases Research Center, Joint Faculty of Veterinary Medicine, Kagoshima University, Kagoshima 890-0065, Japan.
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Snippet Significance Sequences derived from ancient viruses have been shown to make up a substantial part of animal genomes. Bornaviruses, a genus of nonsegmented,...
Animal genomes contain endogenous viral sequences, such as endogenous retroviruses and retrotransposons. Recently, we and others discovered that nonretroviral...
Sequences derived from ancient viruses have been shown to make up a substantial part of animal genomes. Bornaviruses, a genus of nonsegmented, negative-sense...
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StartPage 13175
SubjectTerms Amino Acid Sequence
Amino acids
Animals
Base Sequence
Biological Sciences
Borna Disease - transmission
Borna Disease - virology
Borna disease virus
Borna disease virus - physiology
Cell lines
Cercopithecus aethiops
Conserved Sequence - genetics
DNA
DNA-Directed DNA Polymerase - metabolism
evolution
genome
Genome - genetics
Genomes
HEK293 Cells
hosts
Humans
Infections
Molecular Sequence Data
Mononegavirales
Protein Structure, Tertiary
Proteins
Replicon - genetics
Retroviridae
Retrovirus
Ribonucleoproteins - metabolism
RNA
Sciuridae
Sciuridae - genetics
Sciuridae - virology
Small mammals
Spermophilus
Transfection
Vero Cells
vertebrates
Viral Proteins - chemistry
Viral Proteins - metabolism
virus replication
Virus Replication - genetics
Viruses
Title Inhibition of Borna disease virus replication by an endogenous bornavirus-like element in the ground squirrel genome
URI https://www.jstor.org/stable/43043300
http://www.pnas.org/content/111/36/13175.abstract
https://www.ncbi.nlm.nih.gov/pubmed/25157155
https://www.proquest.com/docview/1564000272
https://www.proquest.com/docview/1561470079
https://www.proquest.com/docview/1566855561
https://www.proquest.com/docview/1803090915
https://pubmed.ncbi.nlm.nih.gov/PMC4246967
Volume 111
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