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Article: The SV40 virus enhancer functions as a somatic hypermutation-targeting element with potential oncogenic activity.

Šenigl, Filip / Soikkeli, Anni / Prost, Salomé / Schatz, David G / Slavková, Martina / Hejnar, Jiří / Alinikula, Jukka

bioRxiv : the preprint server for biology

2024

Abstract: Simian virus 40 (SV40) is a monkey virus associated with several types of human cancers. SV40 is most frequently detected in mesotheliomas, brain and bone tumors and lymphomas, but the mechanism for SV40 tumorigenesis in humans is not clear. SV40 ... ...

Abstract	Simian virus 40 (SV40) is a monkey virus associated with several types of human cancers. SV40 is most frequently detected in mesotheliomas, brain and bone tumors and lymphomas, but the mechanism for SV40 tumorigenesis in humans is not clear. SV40 relative Merkel cell polyomavirus (MCPyV) causes Merkel cell carcinoma (MCC) in humans by expressing truncated large tumor antigen (LT) caused by APOBEC cytidine deaminase family enzymes induced mutations. AID (activation-induced cytidine deaminase), a member of the APOBEC family, is the initiator of the antibody diversification process known as somatic hypermutation (SHM) and its aberrant expression and targeting is a frequent source of lymphomagenesis. In this study, we investigated whether AID-induced mutations could cause truncation of SV40 LT. We demonstrate that the SV40 enhancer has strong SHM targeting activity in several cell types and that AID-induced mutations accumulate to SV40 LT in B cells and kidney cells and cause truncated LT expression in B cells. Our results argue that the ability of the SV40 enhancer to target SHM to LT is a potential source of LT truncation events in various cell types that could contribute to carcinogenesis.
Language	English
Publishing date	2024-01-09
Publishing country	United States
Document type	Preprint
DOI	10.1101/2024.01.09.574829
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Article ; Online: Proviruses with Long-Term Stable Expression Accumulate in Transcriptionally Active Chromatin Close to the Gene Regulatory Elements: Comparison of ASLV-, HIV- and MLV-Derived Vectors.

Miklík, Dalibor / Šenigl, Filip / Hejnar, Jiří

Viruses

2018 Volume 10, Issue 3

Abstract: Individual groups of retroviruses and retroviral vectors differ in their integration site preference and interaction with the host genome. Hence, immediately after infection genome-wide distribution of integrated proviruses is non-random. During long- ... ...

Abstract	Individual groups of retroviruses and retroviral vectors differ in their integration site preference and interaction with the host genome. Hence, immediately after infection genome-wide distribution of integrated proviruses is non-random. During long-term in vitro or persistent in vivo infection, the genomic position and chromatin environment of the provirus affects its transcriptional activity. Thus, a selection of long-term stably expressed proviruses and elimination of proviruses, which have been gradually silenced by epigenetic mechanisms, helps in the identification of genomic compartments permissive for proviral transcription. We compare here the extent and time course of provirus silencing in single cell clones of the K562 human myeloid lymphoblastoma cell line that have been infected with retroviral reporter vectors derived from avian sarcoma/leukosis virus (ASLV), human immunodeficiency virus type 1 (HIV) and murine leukaemia virus (MLV). While MLV proviruses remain transcriptionally active, ASLV proviruses are prone to rapid silencing. The HIV provirus displays gradual silencing only after an extended time period in culture. The analysis of integration sites of long-term stably expressed proviruses shows a strong bias for some genomic features-especially integration close to the transcription start sites of active transcription units. Furthermore, complex analysis of histone modifications enriched at the site of integration points to the accumulation of proviruses of all three groups in gene regulatory segments, particularly close to the enhancer loci. We conclude that the proximity to active regulatory chromatin segments correlates with stable provirus expression in various retroviral species.
MeSH term(s)	Alpharetrovirus/genetics ; Animals ; Cell Line ; Chromatin/genetics ; Enhancer Elements, Genetic ; Epigenesis, Genetic ; Gene Expression Regulation, Viral ; Gene Silencing ; Gene Targeting ; Genetic Vectors/genetics ; HIV-1/genetics ; Humans ; Leukemia Virus, Murine/genetics ; Mice ; Plasmids/genetics ; Proviruses/genetics ; RNA Stability ; Regulatory Sequences, Nucleic Acid ; Transcription Initiation Site ; Transcriptional Activation ; Virus Integration
Chemical Substances	Chromatin
Language	English
Publishing date	2018-03-08
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v10030116
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Article ; Online: Accumulation of long-term transcriptionally active integrated retroviral vectors in active promoters and enhancers.

Šenigl, Filip / Miklík, Dalibor / Auxt, Miroslav / Hejnar, Jirí

Nucleic acids research

2017 Volume 45, Issue 22, Page(s) 12752–12765

Abstract: Most retroviruses preferentially integrate into certain genomic locations and, as a result, their genome-wide integration patterns are non-random. We investigate the epigenetic landscape of integrated retroviral vectors and correlate it with the long- ... ...

Abstract	Most retroviruses preferentially integrate into certain genomic locations and, as a result, their genome-wide integration patterns are non-random. We investigate the epigenetic landscape of integrated retroviral vectors and correlate it with the long-term stability of proviral transcription. Retroviral vectors derived from the avian sarcoma/leukosis virus expressing the GFP reporter were used to transduce the human myeloid lymphoblastoma cell line K562. Because of efficient silencing of avian retrovirus in mammalian cells, only ∼3% of established clones displayed stable proviral expression. We analyzed the vector integration sites in non-selected cells and in clones selected for the GFP expression. This selection led to overrepresentation of proviruses integrated in active transcription units, with particular accumulation in promoter-proximal areas. In parallel, we investigated the integration of vectors equipped with an anti-silencing CpG island core sequence. Such modification increased the frequency of stably expressing proviruses by one order. The modified vectors are also overrepresented in active transcription units, but stably expressed in distal parts of transcriptional units further away from promoters with marked accumulation in enhancers. These results suggest that integrated retroviruses subject to gradual epigenetic silencing during long-term cultivation. Among most genomic compartments, however, active promoters and enhancers protect the adjacent retroviruses from transcriptional silencing.
MeSH term(s)	Alpharetrovirus/genetics ; Animals ; Cell Line ; CpG Islands/genetics ; Enhancer Elements, Genetic/genetics ; Epigenesis, Genetic ; Gene Silencing ; Genetic Vectors/genetics ; Humans ; K562 Cells ; Promoter Regions, Genetic/genetics ; Proviruses/genetics ; Transcription, Genetic ; Virus Integration/genetics
Language	English
Publishing date	2017-12-15
Publishing country	England
Document type	Journal Article
ZDB-ID	2205588-5
ISSN	1362-4962 ; 1746-8272 ; 0305-1048 ; 0261-3166
ISSN (online)	1362-4962 ; 1746-8272
ISSN	0305-1048 ; 0261-3166
DOI	10.1093/nar/gkx889
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Article ; Online: The Novel Avian Leukosis Virus Subgroup K Shares Its Cellular Receptor with Subgroup A.

Přikryl, David / Plachý, Jiří / Kučerová, Dana / Koslová, Anna / Reinišová, Markéta / Šenigl, Filip / Hejnar, Jiří

Journal of virology

2019 Volume 93, Issue 17

Abstract: Avian leukosis virus subgroup K (ALV-K) is composed of newly emerging isolates, which, in sequence analyses, cluster separately from the well-characterized subgroups A, B, C, D, E, and J. However, it remains unclear whether ALV-K represents an ... ...

Abstract	Avian leukosis virus subgroup K (ALV-K) is composed of newly emerging isolates, which, in sequence analyses, cluster separately from the well-characterized subgroups A, B, C, D, E, and J. However, it remains unclear whether ALV-K represents an independent ALV subgroup with regard to receptor usage, host range, and superinfection interference. In the present study, we examined the host range of the Chinese infectious isolate JS11C1, an ALV-K prototype, and we found substantial overlap of species that were either resistant or susceptible to ALV-A and JS11C1. Ectopic expression of the chicken
MeSH term(s)	Animals ; Avian Leukosis/genetics ; Avian Leukosis/metabolism ; Avian Leukosis/virology ; Avian Leukosis Virus/classification ; Avian Leukosis Virus/pathogenicity ; Avian Leukosis Virus/physiology ; Avian Proteins/genetics ; Avian Proteins/metabolism ; Cell Line ; Chickens ; Disease Susceptibility ; Fibroblasts/cytology ; Fibroblasts/metabolism ; Fibroblasts/virology ; Mesocricetus ; Receptors, Virus/genetics ; Receptors, Virus/metabolism ; Species Specificity ; Virus Internalization
Chemical Substances	Avian Proteins ; Receptors, Virus ; Tva receptor
Language	English
Publishing date	2019-08-13
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.00580-19
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Article ; Online: Knock-Out of Retrovirus Receptor Gene

Koslová, Anna / Trefil, Pavel / Mucksová, Jitka / Krchlíková, Veronika / Plachý, Jiří / Krijt, Jakub / Reinišová, Markéta / Kučerová, Dana / Geryk, Josef / Kalina, Jiří / Šenigl, Filip / Elleder, Daniel / Kožich, Viktor / Hejnar, Jiří

Viruses

2021 Volume 13, Issue 12

Abstract: The chicken Tva cell surface protein, a member of the low-density lipoprotein receptor family, has been identified as an entry receptor for avian leukosis virus of classic subgroup A and newly emerging subgroup K. Because both viruses represent an ... ...

Abstract	The chicken Tva cell surface protein, a member of the low-density lipoprotein receptor family, has been identified as an entry receptor for avian leukosis virus of classic subgroup A and newly emerging subgroup K. Because both viruses represent an important concern for the poultry industry, we introduced a frame-shifting deletion into the chicken
MeSH term(s)	Animals ; Avian Leukosis Virus/classification ; Avian Leukosis Virus/physiology ; Avian Proteins/genetics ; Avian Proteins/physiology ; Chick Embryo ; Chickens/virology ; Female ; Frameshift Mutation ; Gene Editing ; Gene Knockout Techniques ; Male ; Methylmalonic Acid/blood ; Receptors, Virus/genetics ; Receptors, Virus/physiology ; Vitamin B 12/metabolism
Chemical Substances	Avian Proteins ; Receptors, Virus ; Tva receptor ; Methylmalonic Acid (8LL8S712J7) ; Vitamin B 12 (P6YC3EG204)
Language	English
Publishing date	2021-12-14
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v13122504
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Article ; Online: Ig Enhancers Increase RNA Polymerase II Stalling at Somatic Hypermutation Target Sequences.

Tarsalainen, Alina / Maman, Yaakov / Meng, Fei-Long / Kyläniemi, Minna K / Soikkeli, Anni / Budzyńska, Paulina / McDonald, Jessica J / Šenigl, Filip / Alt, Frederic W / Schatz, David G / Alinikula, Jukka

Journal of immunology (Baltimore, Md. : 1950)

2021 Volume 208, Issue 1, Page(s) 143–154

Abstract: Somatic hypermutation (SHM) drives the genetic diversity of Ig genes in activated B cells and supports the generation of Abs with increased affinity for Ag. SHM is targeted to Ig genes by their enhancers (diversification activators [DIVACs]), but how the ...

Abstract	Somatic hypermutation (SHM) drives the genetic diversity of Ig genes in activated B cells and supports the generation of Abs with increased affinity for Ag. SHM is targeted to Ig genes by their enhancers (diversification activators [DIVACs]), but how the enhancers mediate this activity is unknown. We show using chicken DT40 B cells that highly active DIVACs increase the phosphorylation of RNA polymerase II (Pol II) and Pol II occupancy in the mutating gene with little or no accompanying increase in elongation-competent Pol II or production of full-length transcripts, indicating accumulation of stalled Pol II. DIVAC has similar effect also in human Ramos Burkitt lymphoma cells. The DIVAC-induced stalling is weakly associated with an increase in the detection of ssDNA bubbles in the mutating target gene. We did not find evidence for antisense transcription, or that DIVAC functions by altering levels of H3K27ac or the histone variant H3.3 in the mutating gene. These findings argue for a connection between Pol II stalling and
MeSH term(s)	Animals ; Antibody Diversity ; Avian Proteins/genetics ; Avian Proteins/metabolism ; B-Lymphocyte Subsets/immunology ; Burkitt Lymphoma/genetics ; Burkitt Lymphoma/immunology ; Chickens ; Cytidine Deaminase/genetics ; Enhancer Elements, Genetic/genetics ; Humans ; Immunoglobulins/genetics ; Immunoglobulins/metabolism ; Lymphocyte Activation ; Mutagenesis, Site-Directed ; Mutation/genetics ; RNA Polymerase II/genetics ; RNA Polymerase II/metabolism ; Somatic Hypermutation, Immunoglobulin ; Transcription, Genetic
Chemical Substances	Avian Proteins ; Immunoglobulins ; RNA Polymerase II (EC 2.7.7.-) ; AICDA (activation-induced cytidine deaminase) (EC 3.5.4.-) ; Cytidine Deaminase (EC 3.5.4.5)
Language	English
Publishing date	2021-12-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't
ZDB-ID	3056-9
ISSN	1550-6606 ; 0022-1767 ; 1048-3233 ; 1047-7381
ISSN (online)	1550-6606
ISSN	0022-1767 ; 1048-3233 ; 1047-7381
DOI	10.4049/jimmunol.2100923
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Article ; Online: Bookmarking the epigenome by retrovirus integration

Hejnar Jiri / Auxt Miroslav / Senigl Filip

Retrovirology, Vol 8, Iss Suppl 2, p O

2011 Volume 16

Keywords	Medicine (General) ; R5-920 ; Medicine ; R ; DOAJ:Medicine (General) ; DOAJ:Health Sciences ; Immunologic diseases. Allergy ; RC581-607
Language	English
Publishing date	2011-10-01T00:00:00Z
Publisher	BioMed Central
Document type	Article ; Online
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Article: Knock-Out of Retrovirus Receptor Gene Tva in the Chicken Confers Resistance to Avian Leukosis Virus Subgroups A and K and Affects Cobalamin (Vitamin B12)-Dependent Level of Methylmalonic Acid

Viruses. 2021 Dec. 14, v. 13, no. 12

2021

Abstract	The chicken Tva cell surface protein, a member of the low-density lipoprotein receptor family, has been identified as an entry receptor for avian leukosis virus of classic subgroup A and newly emerging subgroup K. Because both viruses represent an important concern for the poultry industry, we introduced a frame-shifting deletion into the chicken tva locus with the aim of knocking-out Tva expression and creating a virus-resistant chicken line. The tva knock-out was prepared by CRISPR/Cas9 gene editing in chicken primordial germ cells and orthotopic transplantation of edited cells into the testes of sterilized recipient roosters. The resulting tva −/− chickens tested fully resistant to avian leukosis virus subgroups A and K, both in in vitro and in vivo assays, in contrast to their susceptible tva +/+ and tva +/− siblings. We also found a specific disorder of the cobalamin/vitamin B₁₂ metabolism in the tva knock-out chickens, which is in accordance with the recently recognized physiological function of Tva as a receptor for cobalamin in complex with transcobalamin transporter. Last but not least, we bring a new example of the de novo resistance created by CRISPR/Cas9 editing of pathogen dependence genes in farm animals and, furthermore, a new example of gene editing in chicken.
Keywords	Avian leukosis virus ; CRISPR-Cas systems ; farms ; genes ; loci ; low density lipoprotein ; metabolism ; methylmalonic acid ; pathogens ; poultry industry ; surface proteins ; vitamin B12
Language	English
Dates of publication	2021-1214
Publishing place	Multidisciplinary Digital Publishing Institute
Document type	Article
ZDB-ID	2516098-9
ISSN	1999-4915
ISSN	1999-4915
DOI	10.3390/v13122504
Database	NAL-Catalogue (AGRICOLA)

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Article ; Online: Transcriptional provirus silencing as a crosstalk of de novo DNA methylation and epigenomic features at the integration site.

Senigl, Filip / Auxt, Miroslav / Hejnar, Jirí

Nucleic acids research

2012 Volume 40, Issue 12, Page(s) 5298–5312

Abstract: The autonomous transcription of integrated retroviruses strongly depends on genetic and epigenetic effects of the chromatin at the site of integration. These effects are mostly suppressive and proviral activity can be finally silenced by mechanisms, such ...

Abstract	The autonomous transcription of integrated retroviruses strongly depends on genetic and epigenetic effects of the chromatin at the site of integration. These effects are mostly suppressive and proviral activity can be finally silenced by mechanisms, such as DNA methylation and histone modifications. To address the role of the integration site at the whole-genome-scale, we performed clonal analysis of provirus silencing with an avian leucosis/sarcoma virus-based reporter vector and correlated the transcriptional silencing with the epigenomic landscape of respective integrations. We demonstrate efficient provirus silencing in human HCT116 cell line, which is strongly but not absolutely dependent on the de novo DNA methyltransferase activity, particularly of Dnmt3b. Proviruses integrated close to the transcription start sites of active genes into the regions enriched in H3K4 trimethylation display long-term stability of expression and are resistant to the transcriptional silencing after over-expression of Dnmt3a or Dnmt3b. In contrast, proviruses in the intergenic regions tend to spontaneous transcriptional silencing even in Dnmt3a(-/-) Dnmt3b(-/-) cells. The silencing of proviruses within genes is accompanied with DNA methylation of long terminal repeats, whereas silencing in intergenic regions is DNA methylation-independent. These findings indicate that the epigenomic features of integration sites are crucial for their permissivity to the proviral expression.
MeSH term(s)	Alpharetrovirus/genetics ; Cell Line, Tumor ; DNA (Cytosine-5-)-Methyltransferases/genetics ; DNA (Cytosine-5-)-Methyltransferases/metabolism ; DNA Methylation ; DNA Methyltransferase 3A ; Epigenesis, Genetic ; Gene Silencing ; Humans ; Proviruses/genetics ; Transcription, Genetic ; Virus Integration ; DNA Methyltransferase 3B
Chemical Substances	DNMT3A protein, human ; DNA (Cytosine-5-)-Methyltransferases (EC 2.1.1.37) ; DNA Methyltransferase 3A (EC 2.1.1.37)
Language	English
Publishing date	2012-02-29
Publishing country	England
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	186809-3
ISSN	1362-4962 ; 1362-4954 ; 0301-5610 ; 0305-1048
ISSN (online)	1362-4962 ; 1362-4954
ISSN	0301-5610 ; 0305-1048
DOI	10.1093/nar/gks197
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Article ; Online: Genetic Diversity of NHE1, Receptor for Subgroup J Avian Leukosis Virus, in Domestic Chicken and Wild Anseriform Species.

Reinišová, Markéta / Plachý, Jiří / Kučerová, Dana / Šenigl, Filip / Vinkler, Michal / Hejnar, Jiří

PloS one

2016 Volume 11, Issue 3, Page(s) e0150589

Abstract: J subgroup avian leukosis virus (ALV-J) infects domestic chicken, jungle fowl, and turkey and enters the host cell through a receptor encoded by tvj locus and identified as Na+/H+ exchanger 1 (NHE1). The resistance to ALV-J in a great majority of ... ...

Abstract	J subgroup avian leukosis virus (ALV-J) infects domestic chicken, jungle fowl, and turkey and enters the host cell through a receptor encoded by tvj locus and identified as Na+/H+ exchanger 1 (NHE1). The resistance to ALV-J in a great majority of examined galliform species was explained by deletions or substitutions of the critical tryptophan 38 in the first extracellular loop of NHE1, and genetic polymorphisms around this site predict the susceptibility or resistance of a given species or individual. In this study, we examined the NHE1 polymorphism in domestic chicken breeds and documented quantitative differences in their susceptibility to ALV-J in vitro. In a panel of chicken breeds assembled with the aim to cover the maximum variability encountered in domestic chickens, we found a completely uniform sequence of NHE1 extracellular loop 1 (ECL1) without any source of genetic variation for the selection of ALV-J-resistant poultry. In parallel, we studied the natural polymorphisms of NHE1 in wild ducks and geese because of recent reports on ALV-J positivity in feral Asian species. In anseriform species, we demonstrate a specific and highly conserved critical ECL1 sequence without any homologue of tryptophan 38 in accordance with the resistance of duck cells to prototype ALV-J. Last, we demonstrated that the new Asian strains of ALV-J have not evolved their envelope glycoprotein to the entry the duck cells. Our results contribute substantially to the current discussion of possible heterotransmission of ALV-J and its spill-over into the wild ducks and geese.
MeSH term(s)	Amino Acid Sequence ; Animals ; Animals, Domestic ; Animals, Wild ; Cells, Cultured ; Chick Embryo ; Chickens ; Genetic Variation ; Molecular Sequence Data ; Sequence Homology, Amino Acid ; Sodium-Hydrogen Exchangers/chemistry ; Sodium-Hydrogen Exchangers/genetics
Chemical Substances	Sodium-Hydrogen Exchangers
Language	English
Publishing date	2016-03-15
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ISSN	1932-6203
ISSN (online)	1932-6203
DOI	10.1371/journal.pone.0150589
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