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Macaca arctoides gammaherpesvirus 1 (strain herpesvirus Macaca arctoides): virus sequence, phylogeny and characterisation of virus-transformed macaque and rabbit cell lines

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Abstract

Herpesvirus Macaca arctoides (HVMA) has the propensity to transform macaque lymphocytes to lymphoblastoid cells (MAL-1). Inoculation of rabbits with cell-free virus-containing supernatant resulted in the development of malignant lymphomas and allowed isolation of immortalised HVMA-transformed rabbit lymphocytes (HTRL). In this study, the HVMA genome sequence (approx. 167 kbp), its organisation, and novel aspects of virus latency are presented. Ninety-one open reading frames were identified, of which 86 were non-repetitive. HVMA was identified as a Lymphocryptovirus closely related to Epstein–Barr virus, suggesting the designation as ‘Macaca arctoides gammaherpesvirus 1’ (MarcGHV-1). In situ lysis gel and Southern blot hybridisation experiments revealed that the MAL-1 cell line contains episomal and linear DNA, whereas episomal DNA is predominantly present in HTRL. Integration of viral DNA into macaque and rabbit host cell genomes was demonstrated by fluorescence in situ hybridisation on chromosomal preparations. Analysis of next-generation sequencing data confirmed this finding. Approximately 400 read pairs represent the overlap between macaque and MarcGHV-1 DNA. Both, MAL-1 cells and HTRL show characteristics of a polyclonal tumour with B- and T-lymphocyte markers. Based on analysis of viral gene expression and immunohistochemistry, the persistence of MarcGHV-1 in MAL-1 cells resemble the latency type III, whereas the expression pattern observed in HTRL was more comparable with latency type II. There was no evidence of the presence of STLV-1 proviral DNA in MAL-1 and HTRL. Due to the similarity to EBV-mediated cell transformation, MarcGHV-1 expands the available in vitro models by simian and rabbit cell lines.

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Acknowledgements

We thank the Institute of Clinical Molecular Biology (ICMB) in Kiel for providing Sanger sequencing facilities as supported in part by the DFG Cluster of Excellence “Inflammation at Interfaces” and “Future Ocean”. We thank the technicians S. Greve, T. Henke, C. Noack, C. Botz von Drathen, M. Müller, I. Görlich and Dr. N. Kosyakova for excellent technical support. The authors would like to thank Dr. K. Korn (Virological Institute, University of Erlangen-Nuremberg, Erlangen, Germany) for providing a HTLV-1-positive DNA sample with known proviral load. Furthermore, authors are indebted to Dr. L. Harder (Institute of Tumour Genetics, Kiel, Germany) and R. Bunke, M.D. (Wietze, Germany) for critical reading of the manuscript and valuable comments.

Funding

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

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Author notes

  1. Andi Krumbholz and Janine Roempke contributed equally to this study.

Authors and Affiliations

  1. Institute of Infection Medicine, University of Kiel and University Medical Center Schleswig-Holstein, Brunswiker Strasse 4, 24105, Kiel, Germany

    Andi Krumbholz, Janine Roempke, Gregor Maschkowitz & Helmut Fickenscher

  2. Institute of Human Genetics, Jena University Hospital, Friedrich Schiller University, Jena, Germany

    Thomas Liehr

  3. CF DNA sequencing, Leibniz Institute on Aging-Fritz Lipmann Institute (FLI), Jena, Germany

    Marco Groth

  4. Division of Experimental Virology, Institute of Medical Microbiology, Jena University Hospital, Friedrich Schiller University, Jena, Germany

    Astrid Meerbach, Michael Schacke, Andreas Sauerbrei, Peter Wutzler & Roland Zell

  5. Department of Pathology, Hematopathology Section and Lymph Node Registry, University of Kiel and University Medical Center Schleswig-Holstein, Kiel, Germany

    Wolfram Klapper

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  1. Andi Krumbholz
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Contributions

AK, RZ, HF, AS, AM, and PW planned the experiments; MS generated HTRL and performed initial characterisation; JR and MG performed sequencing with help of AK and RZ; these data were then analysed by JR, MG, AK, and RZ and used for phylogenetic comparisons; JR performed in situ lysis gel and Southern blot, and produced cloned MarcGHV-1 DNA for synthesis of FISH probes; chromosomal analysis and FISH were done by TL; AK, JR, and MG performed analysis of transcripts as well as STLV-1/HTLV-1 proviral DNA search; ISH and IHC were done by AK, GM and WK; AK, JR, TL and RZ wrote the paper; all authors approved the final version. Parts of this manuscript are subject of the MD thesis of JR.

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Correspondence to Andi Krumbholz.

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The authors declare no financial conflict of interest and no non-financial conflict of interest.

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Krumbholz, A., Roempke, J., Liehr, T. et al. Macaca arctoides gammaherpesvirus 1 (strain herpesvirus Macaca arctoides): virus sequence, phylogeny and characterisation of virus-transformed macaque and rabbit cell lines. Med Microbiol Immunol 208, 109–129 (2019). https://doi.org/10.1007/s00430-018-0565-y

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  • DOI: https://doi.org/10.1007/s00430-018-0565-y

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