A Fosmid-Based System for the Generation of Recombinant Cercopithecine Alphaherpesvirus 2 Encoding Reporter Genes

Overview

Journal Viruses

Publisher MDPI

Specialty Microbiology

Date 2019 Nov 8

PMID 31694178

Citations 4

Authors

Ekaterina Chukhno

Sabine Gartner

Abdul Rahman Siregar

Alexander Mehr

Marie Wende

Stoyan Petkov

Jasper Gotting

Akshay Dhingra

Thomas Schulz

Stefan Pohlmann

Michael Winkler

Affiliations

Soon will be listed here.

Abstract

The transmission of Macacine alphaherpesvirus 1 (McHV-1) from macaques, the natural host, to humans causes encephalitis. In contrast, human infection with Cercopithecine alphaherpesvirus 2 (CeHV-2), a closely related alphaherpesvirus from African vervet monkeys and baboons, has not been reported and it is believed that CeHV-2 is apathogenic in humans. The reasons for the differential neurovirulence of McHV-1 and CeHV-2 have not been explored on a molecular level, in part due to the absence of systems for the production of recombinant viruses. Here, we report the generation of a fosmid-based system for rescue of recombinant CeHV-2. Moreover, we show that, in this system, recombineering can be used to equip CeHV-2 with reporter genes. The recombinant CeHV-2 viruses replicated with the same efficiency as uncloned, wt virus and allowed the identification of cell lines that are highly susceptible to CeHV-2 infection. Collectively, we report a system that allows rescue and genetic modification of CeHV-2 and likely other alphaherpesviruses. This system should aid future analysis of CeHV-2 biology.

Citing Articles

Development of rhesus macaque astrocyte cell lines supporting infection with a panel of viruses.

Reiter S, Sun T, Gartner S, Pohlmann S, Winkler M PLoS One. 2024; 19(5):e0303059.

PMID: 38743751 PMC: 11093292. DOI: 10.1371/journal.pone.0303059.

Development of immortalized rhesus macaque kidney cells supporting infection with a panel of viruses.

Reiter S, Gartner S, Decker K, Pohlmann S, Winkler M PLoS One. 2023; 18(5):e0284048.

PMID: 37146034 PMC: 10162512. DOI: 10.1371/journal.pone.0284048.

Primate Simplexviruses Differ in Tropism for Macaque Cells.

Hofmann-Winkler H, Siregar A, Esiyok N, Rodriguez-Polo I, Gartner S, Behr R Microorganisms. 2023; 11(1).

PMID: 36677317 PMC: 9864361. DOI: 10.3390/microorganisms11010026.

A Recombinant System and Reporter Viruses for Papiine Alphaherpesvirus 2.

Siregar A, Gartner S, Gotting J, Stegen P, Kaul A, Schulz T Viruses. 2022; 14(1).

PMID: 35062295 PMC: 8778148. DOI: 10.3390/v14010091.

References

Saeki Y, Ichikawa T, Saeki A, Chiocca E, Tobler K, Ackermann M . Herpes simplex virus type 1 DNA amplified as bacterial artificial chromosome in Escherichia coli: rescue of replication-competent virus progeny and packaging of amplicon vectors. Hum Gene Ther. 1999; 9(18):2787-94. DOI: 10.1089/hum.1998.9.18-2787. View

Gray W, Mahalingam R . A cosmid-based system for inserting mutations and foreign genes into the simian varicella virus genome. J Virol Methods. 2005; 130(1-2):89-94. DOI: 10.1016/j.jviromet.2005.06.013. View

Tischer B, Smith G, Osterrieder N . En passant mutagenesis: a two step markerless red recombination system. Methods Mol Biol. 2010; 634:421-30. DOI: 10.1007/978-1-60761-652-8_30. View

Kong Y, Yang T, Geller A . An efficient in vivo recombination cloning procedure for modifying and combining HSV-1 cosmids. J Virol Methods. 1999; 80(2):129-36. DOI: 10.1016/s0166-0934(99)00033-6. View

Tischer B, von Einem J, Kaufer B, Osterrieder N . Two-step red-mediated recombination for versatile high-efficiency markerless DNA manipulation in Escherichia coli. Biotechniques. 2006; 40(2):191-7. DOI: 10.2144/000112096. View

Tyler S, Peters G, Severini A . Complete genome sequence of cercopithecine herpesvirus 2 (SA8) and comparison with other simplexviruses. Virology. 2005; 331(2):429-40. DOI: 10.1016/j.virol.2004.09.042. View

Malherbe H, STRICKLAND-CHOLMLEY M . Simian herpesvirus SA8 from a baboon. Lancet. 1969; 2(7635):1427. DOI: 10.1016/s0140-6736(69)90972-6. View

Messerle M, Crnkovic I, Hammerschmidt W, Ziegler H, Koszinowski U . Cloning and mutagenesis of a herpesvirus genome as an infectious bacterial artificial chromosome. Proc Natl Acad Sci U S A. 1998; 94(26):14759-63. PMC: 25110. DOI: 10.1073/pnas.94.26.14759. View

Liu Y, Li K, Gao Y, Gao L, Zhong L, Zhang Y . Recombinant Marek's Disease Virus as a Vector-Based Vaccine against Avian Leukosis Virus Subgroup J in Chicken. Viruses. 2016; 8(11). PMC: 5127015. DOI: 10.3390/v8110301. View

10.

Wertheim J, Smith M, Smith D, Scheffler K, Kosakovsky Pond S . Evolutionary origins of human herpes simplex viruses 1 and 2. Mol Biol Evol. 2014; 31(9):2356-64. PMC: 4137711. DOI: 10.1093/molbev/msu185. View

11.

Chen S, Zhou Y, Chen Y, Gu J . fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics. 2018; 34(17):i884-i890. PMC: 6129281. DOI: 10.1093/bioinformatics/bty560. View

12.

Cunningham C, Davison A . A cosmid-based system for constructing mutants of herpes simplex virus type 1. Virology. 1993; 197(1):116-24. DOI: 10.1006/viro.1993.1572. View

13.

Liu J, Chen P, Jiang Y, Wu L, Zeng X, Tian G . A duck enteritis virus-vectored bivalent live vaccine provides fast and complete protection against H5N1 avian influenza virus infection in ducks. J Virol. 2011; 85(21):10989-98. PMC: 3194986. DOI: 10.1128/JVI.05420-11. View

14.

Luckow V, Lee S, Barry G, Olins P . Efficient generation of infectious recombinant baculoviruses by site-specific transposon-mediated insertion of foreign genes into a baculovirus genome propagated in Escherichia coli. J Virol. 1993; 67(8):4566-79. PMC: 237841. DOI: 10.1128/JVI.67.8.4566-4579.1993. View

15.

Wagner M, Koszinowski U . Mutagenesis of viral BACs with linear PCR fragments (ET recombination). Methods Mol Biol. 2004; 256:257-68. DOI: 10.1385/1-59259-753-X:257. View

16.

Dai G, Kim S, OCallaghan D, Kim S . Development of a bacterial artificial chromosome (BAC) recombineering procedure using galK-untranslated region (UTR) for the mutation of diploid genes. J Virol Methods. 2012; 182(1-2):18-26. PMC: 3388943. DOI: 10.1016/j.jviromet.2012.02.010. View

17.

Palmer A . B virus, Herpesvirus simiae: historical perspective. J Med Primatol. 1987; 16(2):99-130. View

18.

Li K, Liu Y, Liu C, Gao L, Zhang Y, Gao Y . Effects of different promoters on the protective efficacy of recombinant Marek's disease virus type 1 expressing the VP2 gene of infectious bursal disease virus. Vaccine. 2016; 34(47):5744-5750. DOI: 10.1016/j.vaccine.2016.10.008. View

19.

Bestman-Smith J, Boivin G . Drug resistance patterns of recombinant herpes simplex virus DNA polymerase mutants generated with a set of overlapping cosmids and plasmids. J Virol. 2003; 77(14):7820-9. PMC: 161916. DOI: 10.1128/jvi.77.14.7820-7829.2003. View

20.

Wild J, Hradecna Z, Szybalski W . Conditionally amplifiable BACs: switching from single-copy to high-copy vectors and genomic clones. Genome Res. 2002; 12(9):1434-44. PMC: 186656. DOI: 10.1101/gr.130502. View