Examination and reconstruction of three ancient endogenous parvovirus capsid protein gene remnants found in rodent genomes

Callaway, H. M., Subramanian, S., Urbina, C., Barnard, K., Dick, R., Bator, C. M., Hafentein, S. L., Gifford, R. J. and Parrish, C. R. (2019) Examination and reconstruction of three ancient endogenous parvovirus capsid protein gene remnants found in rodent genomes. Journal of Virology, 93(6), e01542-18. (doi: 10.1128/JVI.01542-18) (PMID:30626673) (PMCID:PMC6401472)

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Abstract

Parvovirus-derived endogenous viral elements (EVEs) have been found in the genomes of many different animal species, resulting from integration events that may have occurred from more than 50 million years ago to much more recently. Here, we further investigate the properties of autonomous parvovirus EVEs and describe their relationships to contemporary viruses. While we did not find any intact capsid protein open reading frames in the integrated viral sequences, we examined three EVEs that were repaired to form full-length sequences with relatively few changes. These sequences were found in the genomes of Rattus norvegicus (brown rat), Mus spretus (Algerian mouse), and Apodemus sylvaticus (wood mouse). The R. norvegicus sequence was not present in the genomes of the closely related species R. rattus, R. tanezumi, R. exulans, and R. everetti, indicating that it was less than 2 million years old, and the M. spretus and A. sylvaticus sequences were not found in the published genomes of other mouse species, also indicating relatively recent insertions. The M. spretus VP2 sequence assembled into capsids, which had high thermal stability, bound the sialic acid N-acetylneuraminic acid, and entered murine L cells. The 3.89-Å structure of the M. spretus virus-like particles (VLPs), determined using cryo-electron microscopy, showed similarities to rodent and porcine parvovirus capsids. The repaired VP2 sequences from R. norvegicus and A. sylvaticus did not assemble as first prepared, but chimeras combining capsid surface loops from R. norvegicus with canine parvovirus assembled, allowing some of that capsid’s structures and functions to be examined.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Gifford, Dr Robert
Authors: Callaway, H. M., Subramanian, S., Urbina, C., Barnard, K., Dick, R., Bator, C. M., Hafentein, S. L., Gifford, R. J., and Parrish, C. R.
College/School:College of Medical Veterinary and Life Sciences > School of Infection & Immunity > Centre for Virus Research
Journal Name:Journal of Virology
Publisher:American Society for Microbiology
ISSN:0022-538X
ISSN (Online):1098-5514
Published Online:09 January 2019
Copyright Holders:Copyright © 2019 American Society for Microbiology
First Published:First published in Journal of Virology 93(6): e01542-18
Publisher Policy:Reproduced in accordance with the publisher copyright policy

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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
172630010Innate Immunity and Host Species Barriers (Programme 7)Massimo PalmariniMedical Research Council (MRC)MC_UU_12014/10III - Centre for Virus Research