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Article: PARP1 as an Epigenetic Modulator: Implications for the Regulation of Host-Viral Dynamics.

Sobotka, Asher A / Tempera, Italo

2024 Volume 13, Issue 2

Abstract: The principal understanding of the Poly(ADP-ribose) polymerase (PARP) regulation of genomes has been focused on its role in DNA repair; however, in the past few years, an additional role for PARPs and PARylation has emerged in regulating viral-host ... ...

Abstract	The principal understanding of the Poly(ADP-ribose) polymerase (PARP) regulation of genomes has been focused on its role in DNA repair; however, in the past few years, an additional role for PARPs and PARylation has emerged in regulating viral-host interactions. In particular, in the context of DNA virus infection, PARP1-mediated mechanisms of gene regulations, such as the involvement with cellular protein complexes responsible for the folding of the genome into the nucleus, the formation of chromatin loops connecting distant regulatory genomic regions, and other methods of transcriptional regulation, provide additional ways through which PARPs can modulate the function of both the host and the viral genomes during viral infection. In addition, potential viral amplification of the activity of PARPs on the host genome can contribute to the pathogenic effect of viral infection, such as viral-driven oncogenesis, opening the possibility that PARP inhibition may represent a potential therapeutic approach to target viral infection. This review will focus on the role of PARPs, particularly PARP1, in regulating the infection of DNA viruses.
Language	English
Publishing date	2024-01-30
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2695572-6
ISSN	2076-0817
ISSN	2076-0817
DOI	10.3390/pathogens13020131
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Article ; Online: Host factor KAP1 coordinates temporal control between transcription and replication.

Preston-Alp, Sarah / Tempera, Italo

Trends in microbiology

2023 Volume 32, Issue 2, Page(s) 122–123

Abstract: Temporal control of transcription and replication is necessary for efficient Epstein-Barr virus reactivation. Xu et al. identified the KAP1/EA-D/ATM axis as a critical regulator of these processes. This discovery illuminates the collaboration between ... ...

Abstract	Temporal control of transcription and replication is necessary for efficient Epstein-Barr virus reactivation. Xu et al. identified the KAP1/EA-D/ATM axis as a critical regulator of these processes. This discovery illuminates the collaboration between host and viral factors as an essential interaction for viral reactivation.
MeSH term(s)	Humans ; Epstein-Barr Virus Infections ; Herpesvirus 4, Human/genetics ; Virus Replication/genetics
Language	English
Publishing date	2023-12-29
Publishing country	England
Document type	Journal Article
ZDB-ID	1158963-2
ISSN	1878-4380 ; 0966-842X
ISSN (online)	1878-4380
ISSN	0966-842X
DOI	10.1016/j.tim.2023.12.003
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Zs.A 3738: Show issues

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Article ; Online: Three-Dimensional Chromatin Structure of the EBV Genome: A Crucial Factor in Viral Infection.

Caruso, Lisa Beatrice / Maestri, Davide / Tempera, Italo

Viruses

2023 Volume 15, Issue 5

Abstract: Epstein-Barr Virus (EBV) is a human gamma-herpesvirus that is widespread worldwide. To this day, about 200,000 cancer cases per year are attributed to EBV infection. EBV is capable of infecting both B cells and epithelial cells. Upon entry, viral DNA ... ...

Abstract	Epstein-Barr Virus (EBV) is a human gamma-herpesvirus that is widespread worldwide. To this day, about 200,000 cancer cases per year are attributed to EBV infection. EBV is capable of infecting both B cells and epithelial cells. Upon entry, viral DNA reaches the nucleus and undergoes a process of circularization and chromatinization and establishes a latent lifelong infection in host cells. There are different types of latency all characterized by different expressions of latent viral genes correlated with a different three-dimensional architecture of the viral genome. There are multiple factors involved in the regulation and maintenance of this three-dimensional organization, such as CTCF, PARP1, MYC and Nuclear Lamina, emphasizing its central role in latency maintenance.
MeSH term(s)	Humans ; Herpesvirus 4, Human/genetics ; Epstein-Barr Virus Infections ; Virus Latency/genetics ; Gene Expression Regulation, Viral ; Genome, Viral ; Chromatin
Chemical Substances	Chromatin
Language	English
Publishing date	2023-04-29
Publishing country	Switzerland
Document type	Journal Article ; Review ; Research Support, N.I.H., Extramural
ZDB-ID	2516098-9
ISSN	1999-4915 ; 1999-4915
ISSN (online)	1999-4915
ISSN	1999-4915
DOI	10.3390/v15051088
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Article ; Online: Oncogenic Viruses as Entropic Drivers of Cancer Evolution.

Tempera, Italo / Lieberman, Paul M

Frontiers in virology

2021 Volume 1

Abstract: Viral infection is an indisputable causal factor for nearly 17% of all human cancers. However, the diversity and complexity of oncogenic mechanisms raises new questions as to the mechanistic role of viruses in cancer. Classical viral oncogenes have been ... ...

Abstract	Viral infection is an indisputable causal factor for nearly 17% of all human cancers. However, the diversity and complexity of oncogenic mechanisms raises new questions as to the mechanistic role of viruses in cancer. Classical viral oncogenes have been identified for all tumor-associated viruses. These oncogenes can have multiple oncogenic activities that may or may not be utilized in a particular tumor cell. In addition, stochastic events, like viral mutation and integration, as well as heritable host susceptibilities and immune deficiencies are also implicated in tumorigenesis. A more contemporary view of tumor biology highlights the importance of evolutionary forces that select for phenotypes better adapted to a complex and changing environment. Given the challenges of prioritizing singular mechanistic causes, it may be necessary to integrate concepts from evolutionary theory and systems biology to better understand viral cancer-driving forces. Here, we propose that viral infection provides a biological "entropy" that increases genetic variation and phenotypic plasticity, accelerating the main driving forces of cancer cell evolution. Viruses can also influence the evolutionary selection criteria by altering the tumor microenvironment and immune signaling. Utilizing concepts from cancer cell evolution, population genetics, thermodynamics, and systems biology may provide new perspectives on viral oncogenesis and identify novel therapeutic strategies for treating viruses and cancer.
Language	English
Publishing date	2021-11-15
Publishing country	Switzerland
Document type	Journal Article
ISSN	2673-818X
ISSN (online)	2673-818X
DOI	10.3389/fviro.2021.753366
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Article ; Online: The three-dimensional structure of the EBV genome plays a crucial role in regulating viral gene expression in EBVaGC.

Maestri, Davide / Napoletani, Giorgia / Kossenkov, Andrew / Preston-Alp, Sarah / Caruso, Lisa B / Tempera, Italo

Nucleic acids research

2023 Volume 51, Issue 22, Page(s) 12092–12110

Abstract: Epstein-Barr virus (EBV) establishes lifelong asymptomatic infection by replication of its chromatinized episomes with the host genome. EBV exhibits different latency-associated transcriptional repertoires, each with distinct three-dimensional structures. ...

Abstract	Epstein-Barr virus (EBV) establishes lifelong asymptomatic infection by replication of its chromatinized episomes with the host genome. EBV exhibits different latency-associated transcriptional repertoires, each with distinct three-dimensional structures. CTCF, Cohesin and PARP1 are involved in maintaining viral latency and establishing episome architecture. Epstein-Barr virus-associated gastric cancer (EBVaGC) represents 1.3-30.9% of all gastric cancers globally. EBV-positive gastric cancers exhibit an intermediate viral transcription profile known as 'Latency II', expressing specific viral genes and noncoding RNAs. In this study, we investigated the impact of PARP1 inhibition on CTCF/Cohesin binding in Type II latency. We observed destabilization of the binding of both factors, leading to a disrupted three-dimensional architecture of the episomes and an altered viral gene expression. Despite sharing the same CTCF binding profile, Type I, II and III latencies exhibit different 3D structures that correlate with variations in viral gene expression. Additionally, our analysis of H3K27ac-enriched interactions revealed differences between Type II latency episomes and a link to cellular transformation through docking of the EBV genome at specific sites of the Human genome, thus promoting oncogene expression. Overall, this work provides insights into the role of PARP1 in maintaining active latency and novel mechanisms of EBV-induced cellular transformation.
MeSH term(s)	Humans ; Epstein-Barr Virus Infections/virology ; Gene Expression ; Genome, Viral ; Herpesvirus 4, Human/genetics ; Stomach Neoplasms/genetics ; Stomach Neoplasms/virology ; Virus Latency/genetics ; Gene Expression Regulation, Viral
Language	English
Publishing date	2023-10-27
Publishing country	England
Document type	Journal Article
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/gkad936
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Zs.A 1067: Show issues

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Article ; Online: Epstein-Barr Virus-Encoded Latent Membrane Protein 1 and B-Cell Growth Transformation Induce Lipogenesis through Fatty Acid Synthase.

Hulse, Michael / Johnson, Sarah M / Boyle, Sarah / Caruso, Lisa Beatrice / Tempera, Italo

Journal of virology

2021 Volume 95, Issue 4

Abstract: Latent membrane protein 1 (LMP1) is the major transforming protein of Epstein-Barr virus (EBV) and is critical for EBV-induced B-cell ... ...

Abstract	Latent membrane protein 1 (LMP1) is the major transforming protein of Epstein-Barr virus (EBV) and is critical for EBV-induced B-cell transformation
MeSH term(s)	B-Lymphocytes/pathology ; B-Lymphocytes/virology ; Cell Line, Tumor ; Cell Transformation, Neoplastic ; Cellular Reprogramming ; Epstein-Barr Virus Infections/virology ; Fatty Acid Synthase, Type I/metabolism ; Herpesvirus 4, Human/physiology ; Humans ; Lipogenesis ; Viral Matrix Proteins/metabolism
Chemical Substances	EBV-associated membrane antigen, Epstein-Barr virus ; Viral Matrix Proteins ; FASN protein, human (EC 2.3.1.85) ; Fatty Acid Synthase, Type I (EC 2.3.1.85)
Language	English
Publishing date	2021-01-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/JVI.01857-20
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Zs.A 609: Show issues

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Article ; Online: Human Cytomegalovirus Utilizes Multiple Viral Proteins to Regulate the Basement Membrane Protein Nidogen 1.

Kuan, Man I / Caruso, Lisa B / Zavala, Anamaria G / Rana, Pranav S J B / O'Dowd, John M / Tempera, Italo / Fortunato, Elizabeth A

Journal of virology

2022 Volume 96, Issue 20, Page(s) e0133622

Abstract: Nidogen 1 (NID1) is an important basement membrane protein secreted by many cell types. We previously found that human cytomegalovirus (HCMV) infection rapidly induced chromosome 1 breaks and that the basement membrane protein NID1, encoded near the 1q42 ...

Abstract	Nidogen 1 (NID1) is an important basement membrane protein secreted by many cell types. We previously found that human cytomegalovirus (HCMV) infection rapidly induced chromosome 1 breaks and that the basement membrane protein NID1, encoded near the 1q42 break site, was downregulated. We have now determined that the specific breaks in and of themselves did not regulate NID1, rather interactions between several viral proteins and the cellular machinery and DNA regulated NID1. We screened a battery of viral proteins present by 24 hours postinfection (hpi) when regulation was induced, including components of the incoming virion and immediate early (IE) proteins. Adenovirus (Ad) delivery of the tegument proteins pp71 and UL35 and the IE protein IE1 influenced steady-state (ss) NID1 levels. IE1's mechanism of regulation was unclear, while UL35 influenced proteasomal regulation of ss NID1. Real-time quantitative PCR (RT-qPCR) experiments determined that pp71 downregulated
MeSH term(s)	Humans ; Cytomegalovirus/physiology ; Viral Proteins/metabolism ; CCCTC-Binding Factor/genetics ; Gene Expression Regulation, Viral ; Immediate-Early Proteins/genetics ; Immediate-Early Proteins/metabolism ; Basement Membrane/metabolism
Chemical Substances	Viral Proteins ; nidogen ; CCCTC-Binding Factor ; Immediate-Early Proteins
Language	English
Publishing date	2022-10-11
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't ; Research Support, N.I.H., Extramural
ZDB-ID	80174-4
ISSN	1098-5514 ; 0022-538X
ISSN (online)	1098-5514
ISSN	0022-538X
DOI	10.1128/jvi.01336-22
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Zs.A 609: Show issues

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Article: PARP1 Inhibition Halts EBV+ Lymphoma Progression by Disrupting the EBNA2/MYC Axis.

Napoletani, Giorgia / Soldan, Samantha S / Kannan, Toshitha / Preston-Alp, Sarah / Vogel, Peter / Maestri, Davide / Caruso, Lisa Beatrice / Kossenkov, Andrew / Sobotka, Asher / Lieberman, Paul M / Tempera, Italo

bioRxiv : the preprint server for biology

2023

Abstract: PARP1 has been shown to regulate EBV latency. However, the therapeutic effect of PARP1 inhibitors on EBV+ lymphomagenesis has not yet been explored. Here, we show that PARPi BMN-673 has a potent anti-tumor effect on EBV-driven LCL in a mouse xenograft ... ...

Abstract	PARP1 has been shown to regulate EBV latency. However, the therapeutic effect of PARP1 inhibitors on EBV+ lymphomagenesis has not yet been explored. Here, we show that PARPi BMN-673 has a potent anti-tumor effect on EBV-driven LCL in a mouse xenograft model. We found that PARP1 inhibition induces a dramatic transcriptional reprogramming of LCLs driven largely by the reduction of the
Language	English
Publishing date	2023-07-07
Publishing country	United States
Document type	Preprint
DOI	10.1101/2023.07.05.547847
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Article ; Online: Decitabine disrupts EBV genomic epiallele DNA methylation patterns around CTCF binding sites to increase chromatin accessibility and lytic transcription in gastric cancer.

Preston-Alp, Sarah / Caruso, Lisa Beatrice / Su, Chenhe / Keith, Kelsey / Soldan, Samantha S / Maestri, Davide / Madzo, Jozef / Kossenkov, Andrew / Napoletani, Giorgia / Gewurz, Benjamin / Lieberman, Paul M / Tempera, Italo

mBio

2023 Volume 14, Issue 5, Page(s) e0039623

Abstract: Importance: Epstein-Barr virus (EBV) latency is controlled by epigenetic silencing by DNA methylation [5-methyl cytosine (5mC)], histone modifications, and chromatin looping. However, how they dictate the transcriptional program in EBV-associated ... ...

Abstract	Importance: Epstein-Barr virus (EBV) latency is controlled by epigenetic silencing by DNA methylation [5-methyl cytosine (5mC)], histone modifications, and chromatin looping. However, how they dictate the transcriptional program in EBV-associated gastric cancers remains incompletely understood. EBV-associated gastric cancer displays a 5mC hypermethylated phenotype. A potential treatment for this cancer subtype is the DNA hypomethylating agent, which induces EBV lytic reactivation and targets hypermethylation of the cellular DNA. In this study, we identified a heterogeneous pool of EBV epialleles within two tumor-derived gastric cancer cell lines that are disrupted with a hypomethylating agent. Stochastic DNA methylation patterning at critical regulatory regions may be an underlying mechanism for spontaneous reactivation. Our results highlight the critical role of epigenetic modulation on EBV latency and life cycle, which is maintained through the interaction between 5mC and the host protein CCCTC-binding factor.
MeSH term(s)	Humans ; Chromatin ; Herpesvirus 4, Human/physiology ; CCCTC-Binding Factor/genetics ; CCCTC-Binding Factor/metabolism ; DNA Methylation ; Epstein-Barr Virus Infections ; Decitabine/metabolism ; Stomach Neoplasms ; Virus Latency/genetics ; DNA/metabolism ; Genomics ; Binding Sites
Chemical Substances	Chromatin ; CCCTC-Binding Factor ; Decitabine (776B62CQ27) ; DNA (9007-49-2)
Language	English
Publishing date	2023-08-22
Publishing country	United States
Document type	Journal Article
ZDB-ID	2557172-2
ISSN	2150-7511 ; 2161-2129
ISSN (online)	2150-7511
ISSN	2161-2129
DOI	10.1128/mbio.00396-23
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Article ; Online: Epigenetic regulation of EBV persistence and oncogenesis.

Tempera, Italo / Lieberman, Paul M

Seminars in cancer biology

2014 Volume 26, Page(s) 22–29

Abstract: Epigenetic mechanisms play a fundamental role in generating diverse and heritable patterns of viral and cellular gene expression. Epstein-Barr virus (EBV) can adopt a variety of gene expression programs that are necessary for long-term viral persistence ... ...

Abstract	Epigenetic mechanisms play a fundamental role in generating diverse and heritable patterns of viral and cellular gene expression. Epstein-Barr virus (EBV) can adopt a variety of gene expression programs that are necessary for long-term viral persistence and latency in multiple host-cell types and conditions. The latent viral genomes assemble into chromatin structures with different histone and DNA modifications patterns that control viral gene expression. Variations in nucleosome organization and chromatin conformations can also influence gene expression by coordinating physical interactions between different regulatory elements. The viral-encoded and host-cell factors that control these epigenetic features are beginning to be understood at the genome-wide level. These epigenetic regulators can also influence viral pathogenesis by expanding tissue tropism, evading immune detection, and driving host-cell carcinogenesis. Here, we review some of the recent findings and perspectives on how the EBV epigenome plays a central role in viral latency and viral-associated carcinogenesis.
MeSH term(s)	Cell Transformation, Neoplastic ; Cell Transformation, Viral ; Chromatin/genetics ; Chromatin/metabolism ; DNA Methylation ; Epigenesis, Genetic ; Epstein-Barr Virus Infections/complications ; Epstein-Barr Virus Infections/virology ; Gene Expression Regulation, Viral ; Genome, Viral ; Herpesvirus 4, Human/physiology ; Histones/metabolism ; Humans ; Insulator Elements ; Neoplasms/etiology ; Replication Origin ; Virus Latency/genetics
Chemical Substances	Chromatin ; Histones
Language	English
Publishing date	2014-01-24
Publishing country	England
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Review
ZDB-ID	1033980-2
ISSN	1096-3650 ; 1044-579X
ISSN (online)	1096-3650
ISSN	1044-579X
DOI	10.1016/j.semcancer.2014.01.003
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