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Article

Non-Random Pattern of Integration for Epstein-Barr Virus with Preference for Gene-Poor Genomic Chromosomal Regions into the Genome of Burkitt Lymphoma Cell Lines

by
Snjezana Janjetovic
1,2,
Juliane Hinke
1,3,
Saranya Balachandran
4,
Nuray Akyüz
1,
Petra Behrmann
1,
Carsten Bokemeyer
1,
Judith Dierlamm
1,* and
Eva Maria Murga Penas
1,4,*
1
Department of Oncology, Hematology and Bone Marrow Transplantation with Section Pneumology, University Clinic Hamburg-Eppendorf, 20251 Hamburg, Germany
2
Clinic of Hematology and Stem Cell Transplantation, HELIOS Clinic Berlin-Buch, 13125 Berlin, Germany
3
Department for Psychiatry, Albertinen Hospital, 22459 Hamburg, Germany
4
Institute of Human Genetics, Christian-Albrechts-University of Kiel and University Hospital Schleswig-Holstein, Campus Kiel, 24118 Kiel, Germany
*
Authors to whom correspondence should be addressed.
Viruses 2022, 14(1), 86; https://doi.org/10.3390/v14010086
Submission received: 13 November 2021 / Revised: 25 December 2021 / Accepted: 28 December 2021 / Published: 4 January 2022
(This article belongs to the Section Human Virology and Viral Diseases)
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Abstract

Background: Epstein-Barr virus (EBV) is an oncogenic virus found in about 95% of endemic Burkitt lymphoma (BL) cases. In latently infected cells, EBV DNA is mostly maintained in episomal form, but it can also be integrated into the host genome, or both forms can coexist in the infected cells. Methods: In this study, we mapped the chromosomal integration sites of EBV (EBV-IS) into the genome of 21 EBV+ BL cell lines (BL-CL) using metaphase fluorescence in situ hybridization (FISH). The data were used to investigate the EBV-IS distribution pattern in BL-CL, its relation to the genome instability, and to assess its association to common fragile sites and episomes. Results: We detected a total of 459 EBV-IS integrated into multiple genome localizations with a preference for gene-poor chromosomes. We did not observe any preferential affinity of EBV to integrate into common and rare fragile sites or enrichment of EBV-IS at the chromosomal breakpoints of the BL-CL analyzed here, as other DNA viruses do. Conclusions: We identified a non-random integration pattern into 13 cytobands, of which eight overlap with the EBV-IS in EBV-transformed lymphoblastoid cell lines and with a preference for gene- and CpGs-poor G-positive cytobands. Moreover, it has been demonstrated that the episomal form of EBV interacts in a non-random manner with gene-poor and AT-rich regions in EBV+ cell lines, which may explain the observed affinity for G-positive cytobands in the EBV integration process. Our results provide new insights into the patterns of EBV integration in BL-CL at the chromosomal level, revealing an unexpected connection between the episomal and integrated forms of EBV.
Keywords: Epstein-Barr virus; integration sites; Burkitt lymphoma cell lines Epstein-Barr virus; integration sites; Burkitt lymphoma cell lines

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MDPI and ACS Style

Janjetovic, S.; Hinke, J.; Balachandran, S.; Akyüz, N.; Behrmann, P.; Bokemeyer, C.; Dierlamm, J.; Murga Penas, E.M. Non-Random Pattern of Integration for Epstein-Barr Virus with Preference for Gene-Poor Genomic Chromosomal Regions into the Genome of Burkitt Lymphoma Cell Lines. Viruses 2022, 14, 86. https://doi.org/10.3390/v14010086

AMA Style

Janjetovic S, Hinke J, Balachandran S, Akyüz N, Behrmann P, Bokemeyer C, Dierlamm J, Murga Penas EM. Non-Random Pattern of Integration for Epstein-Barr Virus with Preference for Gene-Poor Genomic Chromosomal Regions into the Genome of Burkitt Lymphoma Cell Lines. Viruses. 2022; 14(1):86. https://doi.org/10.3390/v14010086

Chicago/Turabian Style

Janjetovic, Snjezana, Juliane Hinke, Saranya Balachandran, Nuray Akyüz, Petra Behrmann, Carsten Bokemeyer, Judith Dierlamm, and Eva Maria Murga Penas. 2022. "Non-Random Pattern of Integration for Epstein-Barr Virus with Preference for Gene-Poor Genomic Chromosomal Regions into the Genome of Burkitt Lymphoma Cell Lines" Viruses 14, no. 1: 86. https://doi.org/10.3390/v14010086

APA Style

Janjetovic, S., Hinke, J., Balachandran, S., Akyüz, N., Behrmann, P., Bokemeyer, C., Dierlamm, J., & Murga Penas, E. M. (2022). Non-Random Pattern of Integration for Epstein-Barr Virus with Preference for Gene-Poor Genomic Chromosomal Regions into the Genome of Burkitt Lymphoma Cell Lines. Viruses, 14(1), 86. https://doi.org/10.3390/v14010086

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