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Article: Epstein-Barr Virus Infection in Cancer.

Mundo, Lucia / Leoncini, Lorenzo / Accardi-Gheit, Rosita

2023 Volume 15, Issue 18

Abstract: EBV was the first human oncogenic virus identified [ ... ]. ...

Abstract	EBV was the first human oncogenic virus identified [...].
Language	English
Publishing date	2023-09-21
Publishing country	Switzerland
Document type	Editorial
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers15184659
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Article: Epstein-Barr Virus and the Pathogenesis of Diffuse Large B-Cell Lymphoma.

Ross, Aisling M / Leahy, Ciara I / Neylon, Fiona / Steigerova, Jana / Flodr, Patrik / Navratilova, Martina / Urbankova, Helena / Vrzalikova, Katerina / Mundo, Lucia / Lazzi, Stefano / Leoncini, Lorenzo / Pugh, Matthew / Murray, Paul G

Life (Basel, Switzerland)

2023 Volume 13, Issue 2

Abstract: Epstein-Barr virus (EBV), defined as a group I carcinogen by the World Health Organization (WHO), is present in the tumour cells of patients with different forms of B-cell lymphoma, including Burkitt lymphoma, Hodgkin lymphoma, post-transplant ... ...

Abstract	Epstein-Barr virus (EBV), defined as a group I carcinogen by the World Health Organization (WHO), is present in the tumour cells of patients with different forms of B-cell lymphoma, including Burkitt lymphoma, Hodgkin lymphoma, post-transplant lymphoproliferative disorders, and, most recently, diffuse large B-cell lymphoma (DLBCL). Understanding how EBV contributes to the development of these different types of B-cell lymphoma has not only provided fundamental insights into the underlying mechanisms of viral oncogenesis, but has also highlighted potential new therapeutic opportunities. In this review, we describe the effects of EBV infection in normal B-cells and we address the germinal centre model of infection and how this can lead to lymphoma in some instances. We then explore the recent reclassification of EBV+ DLBCL as an established entity in the WHO fifth edition and ICC 2022 classifications, emphasising the unique nature of this entity. To that end, we also explore the unique genetic background of this entity and briefly discuss the potential role of the tumour microenvironment in lymphomagenesis and disease progression. Despite the recent progress in elucidating the mechanisms of this malignancy, much work remains to be done to improve patient stratification, treatment strategies, and outcomes.
Language	English
Publishing date	2023-02-14
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2662250-6
ISSN	2075-1729
ISSN	2075-1729
DOI	10.3390/life13020521
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Article ; Online: Epstein-Barr virus-encoded EBNA2 downregulates ICOSL by inducing miR-24 in B-cell lymphoma.

Leopizzi, Martina / Mundo, Lucia / Messina, Elena / Campolo, Federica / Lazzi, Stefano / Angeloni, Antonio / Marchese, Cinzia / Leoncini, Lorenzo / Giordano, Carla / Slack, Frank / Trivedi, Pankaj / Anastasiadou, Eleni

Blood

2023 Volume 143, Issue 5, Page(s) 429–443

Abstract: Abstract: Hematological malignancies such as Burkitt lymphoma (BL), Hodgkin lymphoma (HL), and diffuse large B-cell lymphoma (DLBCL) cause significant morbidity in humans. A substantial number of these lymphomas, particularly HL and DLBCLs have poorer ... ...

Abstract	Abstract: Hematological malignancies such as Burkitt lymphoma (BL), Hodgkin lymphoma (HL), and diffuse large B-cell lymphoma (DLBCL) cause significant morbidity in humans. A substantial number of these lymphomas, particularly HL and DLBCLs have poorer prognosis because of their association with Epstein-Barr virus (EBV). Our earlier studies have shown that EBV-encoded nuclear antigen (EBNA2) upregulates programmed cell death ligand 1 in DLBCL and BLs by downregulating microRNA-34a. Here, we investigated whether EBNA2 affects the inducible costimulator (ICOS) ligand (ICOSL), a molecule required for efficient recognition of tumor cells by T cells through the engagement of ICOS on the latter. In virus-infected and EBNA2-transfected B-lymphoma cells, ICOSL expression was reduced. Our investigation of the molecular mechanisms revealed that this was due to an increase in microRNA-24 (miR-24) by EBNA2. By using ICOSL 3' untranslated region-luciferase reporter system, we validated that ICOSL is an authentic miR-24 target. Transfection of anti-miR-24 molecules in EBNA2-expressing lymphoma cells reconstituted ICOSL expression and increased tumor immunogenicity in mixed lymphocyte reactions. Because miR-24 is known to target c-MYC, an oncoprotein positively regulated by EBNA2, we analyzed its expression in anti-miR-24 transfected lymphoma cells. Indeed, the reduction of miR-24 in EBNA2-expressing DLBCL further elevated c-MYC and increased apoptosis. Consistent with the in vitro data, EBNA2-positive DLBCL biopsies expressed low ICOSL and high miR-24. We suggest that EBV evades host immune responses through EBNA2 by inducing miR-24 to reduce ICOSL expression, and for simultaneous rheostatic maintenance of proproliferative c-MYC levels. Overall, these data identify miR-24 as a potential therapeutically relevant target in EBV-associated lymphomas.
MeSH term(s)	Humans ; Antagomirs ; Epstein-Barr Virus Infections/complications ; Epstein-Barr Virus Infections/genetics ; Epstein-Barr Virus Infections/metabolism ; Epstein-Barr Virus Nuclear Antigens/genetics ; Epstein-Barr Virus Nuclear Antigens/metabolism ; Herpesvirus 4, Human/genetics ; Hodgkin Disease/complications ; Ligands ; Lymphoma, Large B-Cell, Diffuse/metabolism ; MicroRNAs/genetics ; Viral Proteins/metabolism
Chemical Substances	Antagomirs ; Epstein-Barr Virus Nuclear Antigens ; Ligands ; MicroRNAs ; MIRN24 microRNA, human ; Viral Proteins ; EBNA-2 protein, Human herpesvirus 4 ; ICOSLG protein, human
Language	English
Publishing date	2023-10-18
Publishing country	United States
Document type	Journal Article
ZDB-ID	80069-7
ISSN	1528-0020 ; 0006-4971
ISSN (online)	1528-0020
ISSN	0006-4971
DOI	10.1182/blood.2023021346
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Article: MicroRNA and Other Non-Coding RNAs in Epstein-Barr Virus-Associated Cancers.

Notarte, Kin Israel / Senanayake, Suranga / Macaranas, Imee / Albano, Pia Marie / Mundo, Lucia / Fennell, Eanna / Leoncini, Lorenzo / Murray, Paul

Cancers

2021 Volume 13, Issue 15

Abstract: EBV is a direct causative agent in around 1.5% of all cancers. The oncogenic properties of EBV are related to its ability to activate processes needed for cellular proliferation, survival, migration, and immune evasion. The EBV latency program is ... ...

Abstract	EBV is a direct causative agent in around 1.5% of all cancers. The oncogenic properties of EBV are related to its ability to activate processes needed for cellular proliferation, survival, migration, and immune evasion. The EBV latency program is required for the immortalization of infected B cells and involves the expression of non-coding RNAs (ncRNAs), including viral microRNAs. These ncRNAs have different functions that contribute to virus persistence in the asymptomatic host and to the development of EBV-associated cancers. In this review, we discuss the function and potential clinical utility of EBV microRNAs and other ncRNAs in EBV-associated malignancies. This review is not intended to be comprehensive, but rather to provide examples of the importance of ncRNAs.
Language	English
Publishing date	2021-08-03
Publishing country	Switzerland
Document type	Journal Article ; Review
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers13153909
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Article ; Online: Aflatoxin B1 and Epstein-Barr virus-induced CCL22 expression stimulates B cell infection.

Proceedings of the National Academy of Sciences of the United States of America

2024 Volume 121, Issue 16, Page(s) e2314426121

Abstract: Epstein-Barr Virus (EBV) infects more than 90% of the adult population worldwide. EBV infection is associated with Burkitt lymphoma (BL) though alone is not sufficient to induce carcinogenesis implying the involvement of co-factors. BL is endemic in ... ...

Abstract	Epstein-Barr Virus (EBV) infects more than 90% of the adult population worldwide. EBV infection is associated with Burkitt lymphoma (BL) though alone is not sufficient to induce carcinogenesis implying the involvement of co-factors. BL is endemic in African regions faced with mycotoxins exposure. Exposure to mycotoxins and oncogenic viruses has been shown to increase cancer risks partly through the deregulation of the immune response. A recent transcriptome profiling of B cells exposed to aflatoxin B1 (AFB1) revealed an upregulation of the Chemokine ligand 22 (CCL22) expression although the underlying mechanisms were not investigated. Here, we tested whether mycotoxins and EBV exposure may together contribute to endemic BL (eBL) carcinogenesis via immunomodulatory mechanisms involving CCL22. Our results revealed that B cells exposure to AFB1 and EBV synergistically stimulated CCL22 secretion via the activation of Nuclear Factor-kappa B pathway. By expressing EBV latent genes in B cells, we revealed that elevated levels of CCL22 result not only from the expression of the latent membrane protein LMP1 as previously reported but also from the expression of other viral latent genes. Importantly, CCL22 overexpression resulting from AFB1-exposure in vitro increased EBV infection through the activation of phosphoinositide-3-kinase pathway. Moreover, inhibiting CCL22 in vitro and in humanized mice in vivo limited EBV infection and decreased viral genes expression, supporting the notion that CCL22 overexpression plays an important role in B cell infection. These findings unravel new mechanisms that may underpin eBL development and identify novel pathways that can be targeted in drug development.
MeSH term(s)	Animals ; Mice ; Herpesvirus 4, Human/genetics ; Epstein-Barr Virus Infections/complications ; Aflatoxin B1/toxicity ; Ligands ; Burkitt Lymphoma/metabolism ; Chemokines ; Carcinogenesis
Chemical Substances	Aflatoxin B1 (9N2N2Y55MH) ; Ligands ; Chemokines
Language	English
Publishing date	2024-04-04
Publishing country	United States
Document type	Journal Article
ZDB-ID	209104-5
ISSN	1091-6490 ; 0027-8424
ISSN (online)	1091-6490
ISSN	0027-8424
DOI	10.1073/pnas.2314426121
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Article: Epigenetic Alteration of the Cancer-Related Gene TGFBI in B Cells Infected with Epstein-Barr Virus and Exposed to Aflatoxin B1: Potential Role in Burkitt Lymphoma Development.

Manara, Francesca / Jay, Antonin / Odongo, Grace Akinyi / Mure, Fabrice / Maroui, Mohamed Ali / Diederichs, Audrey / Sirand, Cecilia / Cuenin, Cyrille / Granai, Massimo / Mundo, Lucia / Hernandez-Vargas, Hector / Lazzi, Stefano / Khoueiry, Rita / Gruffat, Henri / Herceg, Zdenko / Accardi, Rosita

Cancers

2022 Volume 14, Issue 5

Abstract: Burkitt lymphoma (BL) is a malignant B cell neoplasm that accounts for almost half of pediatric cancers in sub-Saharan African countries. Although the BL endemic prevalence is attributable to the combination of Epstein-Barr virus (EBV) infection with ... ...

Abstract	Burkitt lymphoma (BL) is a malignant B cell neoplasm that accounts for almost half of pediatric cancers in sub-Saharan African countries. Although the BL endemic prevalence is attributable to the combination of Epstein-Barr virus (EBV) infection with malaria and environmental carcinogens exposure, such as the food contaminant aflatoxin B1 (AFB1), the molecular determinants underlying the pathogenesis are not fully understood. Consistent with the role of epigenetic mechanisms at the interface between the genome and environment, AFB1 and EBV impact the methylome of respectively leukocytes and B cells specifically. Here, we conducted a thorough investigation of common epigenomic changes following EBV or AFB1 exposure in B cells. Genome-wide DNA methylation profiling identified an EBV-AFB1 common signature within the TGFBI locus, which encodes for a putative tumor suppressor often altered in cancer. Subsequent mechanistic analyses confirmed a DNA-methylation-dependent transcriptional silencing of TGFBI involving the recruitment of DNMT1 methyltransferase that is associated with an activation of the NF-κB pathway. Our results reveal a potential common mechanism of B cell transformation shared by the main risk factors of endemic BL (EBV and AFB1), suggesting a key determinant of disease that could allow the development of more efficient targeted therapeutic strategies.
Language	English
Publishing date	2022-03-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2527080-1
ISSN	2072-6694
ISSN	2072-6694
DOI	10.3390/cancers14051284
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Article ; Online: Epstein-Barr virus reactivation influences clonal evolution in human herpesvirus-8-related lymphoproliferative disorders.

Granai, Massimo / Facchetti, Mattia / Mancini, Virginia / Goedhals, Jacqueline / Sherriff, Alicia / Mundo, Lucia / Bellan, Cristiana / Amato, Teresa / Sorrentino, Ester / Ungari, Marco / Raphael, Martine / Leoncini, Lorenzo / Facchetti, Fabio / Lazzi, Stefano

Histopathology

2021 Volume 79, Issue 6, Page(s) 1099–1107

Abstract: Background: Human herpesvirus-8 (HHV8) is a lymphotropic virus associated with different lymphoproliferative disorders, including primary effusion lymphoma (PEL), multicentric Castleman's disease (MCD), diffuse large B-cell lymphomas, not otherwise ... ...

Abstract	Background: Human herpesvirus-8 (HHV8) is a lymphotropic virus associated with different lymphoproliferative disorders, including primary effusion lymphoma (PEL), multicentric Castleman's disease (MCD), diffuse large B-cell lymphomas, not otherwise specified, and the rare entity known as germinotropic lymphoproliferative disorder (GLPD). In PELs and GLPD the neoplastic cells also contain Epstein-Barr virus (EBV). In addition, occasional cases with atypical and overlapping features among these entities have been recognised, suggesting that the spectrum of the HHV8-related lesions may not be fully characterised. Aims: Here, we report two cases of lymphoproliferative disorder associated with HHV8 and EBV that further expand the spectrum of HHV8/EBV-positive lymphoproliferative disease. Methods and results: Case 1 represented HHV8/EBV-positive extracavitary nodal PEL followed by pleural PEL. The striking characteristic of this case was the almost focal and intrasinusoidal localisation of the neoplastic cells and the association with Castleman's disease features. In the second case, we found the entire spectrum of HHV8-related disorders, i.e. MCD, GLPD, and PEL, coexisting in the same lymph node, underlining the variability, possible overlap and evolution among these entities. Both cases were well analysed with immunohistochemistry, determination of the EBV latency programme, and molecular analysis for clonality of immnoglobulin genes. In both patients, the disease followed an unexpected indolent course, both being still alive after 8 and 12 months, respectively. Conclusion: Our findings represent further evidence of the overlap among HHV8/EBV-positive lymphoproliferative disorders, and underline a grey zone that requires further study; they further confirm the experimental evidence that lytic EBV replication influences HHV8-related tumorigenesis.
MeSH term(s)	Aged ; Clonal Evolution ; Coinfection/virology ; Epstein-Barr Virus Infections/complications ; Epstein-Barr Virus Infections/virology ; Female ; Herpesviridae Infections/complications ; Herpesviridae Infections/virology ; Herpesvirus 4, Human/physiology ; Herpesvirus 8, Human ; Humans ; Lymphoproliferative Disorders/pathology ; Lymphoproliferative Disorders/virology ; Male ; Middle Aged ; Virus Activation
Language	English
Publishing date	2021-10-04
Publishing country	England
Document type	Case Reports ; Journal Article
ZDB-ID	131914-0
ISSN	1365-2559 ; 0309-0167
ISSN (online)	1365-2559
ISSN	0309-0167
DOI	10.1111/his.14551
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Article ; Online: How in-depth histological look may allow challenging diagnosis: The case of a primary in situ mantle cell neoplasm of the appendix.

Ambrosio, Maria Raffaella / Granai, Massimo / Lo Bello, Giuseppe / Cirami, Manuela / Mundo, Lucia / Leoncini, Lorenzo / Lazzi, Stefano

Hematological oncology

2018 Volume 36, Issue 1, Page(s) 376–378

MeSH term(s)	Adult ; Appendiceal Neoplasms/diagnostic imaging ; Appendiceal Neoplasms/metabolism ; Appendiceal Neoplasms/pathology ; Appendiceal Neoplasms/surgery ; Humans ; Lymphoma, Mantle-Cell/diagnostic imaging ; Lymphoma, Mantle-Cell/metabolism ; Lymphoma, Mantle-Cell/pathology ; Lymphoma, Mantle-Cell/surgery ; Male
Language	English
Publishing date	2018-02
Publishing country	England
Document type	Clinical Trial ; Letter
ZDB-ID	604884-5
ISSN	1099-1069 ; 0278-0232
ISSN (online)	1099-1069
ISSN	0278-0232
DOI	10.1002/hon.2418
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Article ; Online: The Binding of CD93 to Multimerin-2 Promotes Choroidal Neovascularization.

Tosi, Gian Marco / Neri, Giovanni / Barbera, Stefano / Mundo, Lucia / Parolini, Barbara / Lazzi, Stefano / Lugano, Roberta / Poletto, Evelina / Leoncini, Lorenzo / Pertile, Grazia / Mongiat, Maurizio / Dimberg, Anna / Galvagni, Federico / Orlandini, Maurizio

Investigative ophthalmology & visual science

2020 Volume 61, Issue 8, Page(s) 30

Abstract: Purpose: The purpose of this study was to investigate the involvement of CD93 and Multimerin-2 in three choroidal neovascularization (CNV) models and to evaluate their contribution in the neovascular progression of age-related macular degeneration (AMD). ...

Abstract	Purpose: The purpose of this study was to investigate the involvement of CD93 and Multimerin-2 in three choroidal neovascularization (CNV) models and to evaluate their contribution in the neovascular progression of age-related macular degeneration (AMD). Methods: Choroidal neovascular membranes collected during surgery from AMD patients were analyzed by microscopy methods. Laser-induced CNV mouse models and choroid sprouting assays (CSAs) were carried out using the CD93 knockout mouse model. An original ex vivo CSA of vascular angiogenesis, employing choroid tissues isolated from human donors, was developed. Results: In contrast to healthy choroid endothelium, hyperproliferative choroidal endothelial cells (ECs) of AMD patients expressed high levels of CD93, and Multimerin-2 was abundantly deposited along the choroidal neovasculature. CD93 knockout mice showed a significant reduced neovascularization after laser photocoagulation, and their choroidal ECs displayed a decreased ability to produce sprouts in ex vivo angiogenesis assays. Moreover, the presence of an antibody able to hamper the CD93/Multimerin-2 interaction reduced vascular sprouting in the human CSA. Conclusions: Our results demonstrate that CD93 and its interaction with Multimerin-2 play an important role in pathological vascularization of the choroid, disclosing new possibilities for therapeutic intervention to neovascular AMD.
MeSH term(s)	Angiogenesis Inhibitors/immunology ; Animals ; Antigens, Surface/metabolism ; Choroid/blood supply ; Choroid/pathology ; Choroidal Neovascularization/metabolism ; Endothelial Cells/metabolism ; Extracellular Matrix Proteins/metabolism ; Humans ; Intercellular Signaling Peptides and Proteins/metabolism ; Macular Degeneration/metabolism ; Macular Degeneration/pathology ; Membrane Glycoproteins/metabolism ; Mice ; Mice, Knockout ; Models, Biological ; Receptors, Complement/metabolism
Chemical Substances	Angiogenesis Inhibitors ; Antigens, Surface ; EMILIN3 protein, human ; Extracellular Matrix Proteins ; Intercellular Signaling Peptides and Proteins ; Membrane Glycoproteins ; Mmrn2 protein, mouse ; Receptors, Complement ; complement 1q receptor
Language	English
Publishing date	2020-07-22
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	391794-0
ISSN	1552-5783 ; 0146-0404
ISSN (online)	1552-5783
ISSN	0146-0404
DOI	10.1167/iovs.61.8.30
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Article: Metabolic Switch and Cytotoxic Effect of Metformin on Burkitt Lymphoma.

Bagaloni, Irene / Visani, Axel / Biagiotti, Sara / Ruzzo, Annamaria / Navari, Mohsen / Etebari, Maryam / Mundo, Lucia / Granai, Massimo / Lazzi, Stefano / Isidori, Alessandro / Loscocco, Federica / Li, Jiejin / Leoncini, Lorenzo / Visani, Giuseppe / Magnani, Mauro / Piccaluga, Pier Paolo

Frontiers in oncology

2021 Volume 11, Page(s) 661102

Abstract: Altered cellular energetic metabolism has recently emerged as important feature of neoplastic cells. Indeed, interfering with cancer cell metabolism might represent a suitable therapeutic strategy. In this study, we aimed to assess glucose metabolism ... ...

Abstract	Altered cellular energetic metabolism has recently emerged as important feature of neoplastic cells. Indeed, interfering with cancer cell metabolism might represent a suitable therapeutic strategy. In this study, we aimed to assess glucose metabolism activation in human lymphomas and evaluate how metformin can exert its action on lymphoma cells. We studied a large series of human lymphomas (N = 252) and an
Language	English
Publishing date	2021-09-02
Publishing country	Switzerland
Document type	Journal Article
ZDB-ID	2649216-7
ISSN	2234-943X
ISSN	2234-943X
DOI	10.3389/fonc.2021.661102
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