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Article ; Online: Reduced frequency of cytotoxic CD56

Pánisová, Elena / Lünemann, Anna / Bürgler, Simone / Kotur, Monika / Lazarovici, Julien / Danu, Alina / Kaulfuss, Meike / Mietz, Juliane / Chijioke, Obinna / Münz, Christian / Busson, Pierre / Berger, Christoph / Ghez, David / Azzi, Tarik

Cancer immunology, immunotherapy : CII

2021 Volume 71, Issue 1, Page(s) 13–24

Abstract: Around 30-50% of classical Hodgkin lymphoma (cHL) cases in immunocompetent individuals from industrialized countries are associated with the B-lymphotropic Epstein-Barr virus (EBV). Although natural killer (NK) cells exhibit anti-viral and anti-tumoral ... ...

Abstract	Around 30-50% of classical Hodgkin lymphoma (cHL) cases in immunocompetent individuals from industrialized countries are associated with the B-lymphotropic Epstein-Barr virus (EBV). Although natural killer (NK) cells exhibit anti-viral and anti-tumoral functions, virtually nothing is known about quantitative and qualitative differences in NK cells in patients with EBV+ cHL vs. EBV- cHL. Here, we prospectively investigated 36 cHL patients without known immune suppression or overt immunodeficiency at diagnosis. All 10 EBV+ cHL patients and 25 out 26 EBV- cHL were seropositive for EBV antibodies, and EBV+ cHL patients presented with higher plasma EBV DNA levels compared to EBV- cHL patients. We show that the CD56
MeSH term(s)	Adult ; Aged ; Antibodies/immunology ; Antineoplastic Agents/pharmacology ; CD56 Antigen/biosynthesis ; Epstein-Barr Virus Infections/complications ; Female ; GPI-Linked Proteins/biosynthesis ; Herpesvirus 4, Human/metabolism ; Hodgkin Disease/complications ; Hodgkin Disease/metabolism ; Hodgkin Disease/therapy ; Humans ; Immunotherapy ; In Vitro Techniques ; Killer Cells, Natural/metabolism ; Leukocytes, Mononuclear/cytology ; Lymphocytes/metabolism ; Lysosomal-Associated Membrane Protein 1/biosynthesis ; Male ; Middle Aged ; Phenotype ; Prospective Studies ; Receptors, IgG/biosynthesis ; Rituximab/pharmacology
Chemical Substances	Antibodies ; Antineoplastic Agents ; CD56 Antigen ; FCGR3B protein, human ; GPI-Linked Proteins ; Lysosomal-Associated Membrane Protein 1 ; NCAM1 protein, human ; Receptors, IgG ; Rituximab (4F4X42SYQ6)
Language	English
Publishing date	2021-05-15
Publishing country	Germany
Document type	Journal Article
ZDB-ID	195342-4
ISSN	1432-0851 ; 0340-7004
ISSN (online)	1432-0851
ISSN	0340-7004
DOI	10.1007/s00262-021-02956-x
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Article ; Online: CD4 + T cells are found within endemic Burkitt lymphoma and modulate Burkitt lymphoma precursor cell viability and expression of pathogenically relevant Epstein-Barr virus genes.

Sidorov, Semjon / Fux, Lara / Steiner, Katja / Bounlom, Samyo / Traxel, Sabrina / Azzi, Tarik / Berisha, Arbeneshe / Berger, Christoph / Bernasconi, Michele / Niggli, Felix K / Perner, Yvonne / Pather, Sugeshnee / Kempf, Werner / Nadal, David / Bürgler, Simone

Cancer immunology, immunotherapy : CII

2021 Volume 71, Issue 6, Page(s) 1371–1392

Abstract: Endemic Burkitt lymphoma (eBL) is an aggressive B cell cancer characterized by an IgH/c-myc translocation and the harboring of Epstein-Barr virus (EBV). Evidence accumulates that CD4 + T cells might contribute to eBL pathogenesis. Here, we investigate ... ...

Abstract	Endemic Burkitt lymphoma (eBL) is an aggressive B cell cancer characterized by an IgH/c-myc translocation and the harboring of Epstein-Barr virus (EBV). Evidence accumulates that CD4 + T cells might contribute to eBL pathogenesis. Here, we investigate the presence of CD4 + T cells in primary eBL tissue and their potential dichotomous impact on an EBV-infected pre-eBL cell model using ex vivo material and in vitro co-cultures. In addition, we establish a novel method to study the effect of IgH/c-myc translocation in primary B cells by employing a CRISPR/Cas9 knock-in approach to introduce and tag de novo translocation. We unprecedently document that CD4 + T cells are present in primary eBL tumor tissue. Furthermore, we demonstrate that CD4 + T cells on the one hand suppress eBL development by killing pre-eBL cells lacking IgH/c-myc translocation in vitro and on the other hand indirectly promote eBL development by inducing crucial EBV Latency III to Latency I switching in pre-eBL cells. Finally, we show that while the mere presence of an IgH/c-myc translocation does not suffice to escape CD4 + T-cell-mediated killing in vitro, the CD4 + T-cell-mediated suppression of EBV's Latency III program in vivo may allow cells harboring an IgH/c-myc translocation and additional mutations to evade immune control and proliferate by means of deregulated c-myc activity, resulting in neoplasia. Thus, our study highlights the dichotomous effects of CD4 + T cells and the mechanisms involved in eBL pathogenesis, suggests mechanisms of their impact on eBL progression, and provides a novel in vitro model for further investigation of IgH/c-myc translocation.
MeSH term(s)	B-Lymphocytes/metabolism ; Burkitt Lymphoma/genetics ; Cell Survival ; Epstein-Barr Virus Infections/complications ; Epstein-Barr Virus Infections/genetics ; Herpesvirus 4, Human ; Humans
Language	English
Publishing date	2021-10-19
Publishing country	Germany
Document type	Journal Article
ZDB-ID	195342-4
ISSN	1432-0851 ; 0340-7004
ISSN (online)	1432-0851
ISSN	0340-7004
DOI	10.1007/s00262-021-03057-5
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Article ; Online: Innate immune responses against Epstein Barr virus infection.

Chijioke, Obinna / Azzi, Tarik / Nadal, David / Münz, Christian

Journal of leukocyte biology

2013 Volume 94, Issue 6, Page(s) 1185–1190

Abstract: EBV persists life-long in >95% of the human adult population. Whereas it is perfectly immune-controlled in most infected individuals, a minority develops EBV-associated diseases, primarily malignancies of B cell and epithelial cell origin. In recent ... ...

Abstract	EBV persists life-long in >95% of the human adult population. Whereas it is perfectly immune-controlled in most infected individuals, a minority develops EBV-associated diseases, primarily malignancies of B cell and epithelial cell origin. In recent years, it has become apparent that the course of primary infection determines part of the risk to develop EBV-associated diseases. Particularly, the primary symptomatic EBV infection or IM, which is caused by exaggerated T cell responses, resulting in EBV-induced lymphocytosis, predisposes for EBV-associated diseases. The role of innate immunity in the development of IM remains unknown. Therefore, it is important to understand how the innate immune response to this virus differs between symptomatic and asymptomatic primary EBV infection. Furthermore, the efficiency of innate immune compartments might determine the outcome of primary infection and could explain why some individuals are susceptible to IM. We will discuss these aspects in this review with a focus on intrinsic immunity in EBV-infected B cells, as well as innate immune responses by DCs and NK cells, which constitute promising immune compartments for the understanding of early immune control against EBV and potential targets for EBV-specific immunotherapies.
MeSH term(s)	B-Lymphocytes/immunology ; B-Lymphocytes/virology ; Dendritic Cells/immunology ; Epstein-Barr Virus Infections/immunology ; Epstein-Barr Virus Infections/therapy ; Herpesvirus 4, Human/immunology ; Humans ; Immunity, Innate ; Immunotherapy/methods ; Killer Cells, Natural/immunology ; T-Lymphocytes/immunology
Language	English
Publishing date	2013-06-28
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural ; Research Support, Non-U.S. Gov't ; Review
ZDB-ID	605722-6
ISSN	1938-3673 ; 0741-5400
ISSN (online)	1938-3673
ISSN	0741-5400
DOI	10.1189/jlb.0313173
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Article ; Online: Co-infection of Cytomegalovirus and Epstein-Barr Virus Diminishes the Frequency of CD56

Lam, Janice K P / Azzi, Tarik / Hui, K F / Wong, Aikha M G / McHugh, Donal / Caduff, Nicole / Chan, K H / Münz, Christian / Chiang, Alan K S

Frontiers in immunology

2020 Volume 11, Page(s) 1231

Abstract: Post-transplant lymphoproliferative disorder (PTLD) is a rare but potentially life-threatening complication, frequently associated with Epstein-Barr virus (EBV), which develops after solid organ or stem cell transplantation. Immunosuppression received by ...

Abstract	Post-transplant lymphoproliferative disorder (PTLD) is a rare but potentially life-threatening complication, frequently associated with Epstein-Barr virus (EBV), which develops after solid organ or stem cell transplantation. Immunosuppression received by transplant recipients has a significant impact on the development of PTLD by suppressing the function of T cells. The preferential proliferation of NKG2A-positive natural killer (NK) cells during primary symptomatic EBV infection known as infectious mononucleosis (IM) and their reactivity toward EBV-infected B cells point to a role of NK cell in the immune control of EBV. However, NK cell-mediated immune response to EBV in immunosuppressed transplant recipients who develop PTLD remains unclear. In this study, we longitudinally analyzed the phenotype and function of different NK cell subsets in a cohort of pediatric liver transplant patients who develop PTLD and compared them to those of children with IM. We found persistently elevated plasma EBV DNA levels in the PTLD patients indicating suboptimal anti-viral immune control. PTLD patients had markedly decreased frequency of CD56
MeSH term(s)	Age Factors ; Cell Degranulation/immunology ; Cell Line ; Child, Preschool ; Coinfection ; Cytomegalovirus/immunology ; Cytomegalovirus Infections/complications ; Cytomegalovirus Infections/immunology ; Cytomegalovirus Infections/virology ; Disease Susceptibility ; Epstein-Barr Virus Infections/complications ; Epstein-Barr Virus Infections/immunology ; Epstein-Barr Virus Infections/virology ; Female ; Herpesvirus 4, Human/immunology ; Humans ; Immunocompromised Host ; Immunophenotyping ; Immunosuppression ; Immunosuppressive Agents/administration & dosage ; Immunosuppressive Agents/pharmacokinetics ; Infant ; Killer Cells, Natural/immunology ; Killer Cells, Natural/metabolism ; Lymphocyte Activation/genetics ; Lymphocyte Activation/immunology ; Lymphocyte Count ; Lymphocyte Subsets/immunology ; Lymphocyte Subsets/metabolism ; Lymphoproliferative Disorders/etiology ; Male ; Organ Transplantation/adverse effects ; Receptors, KIR/metabolism ; Time Factors ; Viral Load
Chemical Substances	Immunosuppressive Agents ; Receptors, KIR
Language	English
Publishing date	2020-06-17
Publishing country	Switzerland
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2606827-8
ISSN	1664-3224 ; 1664-3224
ISSN (online)	1664-3224
ISSN	1664-3224
DOI	10.3389/fimmu.2020.01231
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Article ; Online: Correction: Immunosuppressive FK506 treatment leads to more frequent EBV-associated lymphoproliferative disease in humanized mice.

PLoS pathogens

2020 Volume 16, Issue 12, Page(s) e1009167

Abstract: This corrects the article DOI: 10.1371/journal.ppat.1008477.]. ...

Abstract	[This corrects the article DOI: 10.1371/journal.ppat.1008477.].
Language	English
Publishing date	2020-12-21
Publishing country	United States
Document type	Published Erratum
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1009167
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Article ; Online: Correction

PLoS Pathogens, Vol 16, Iss 12, p e

Immunosuppressive FK506 treatment leads to more frequent EBV-associated lymphoproliferative disease in humanized mice.

2020 Volume 1009167

Abstract: This corrects the article DOI:10.1371/journal.ppat.1008477.]. ...

Abstract	[This corrects the article DOI:10.1371/journal.ppat.1008477.].
Keywords	Immunologic diseases. Allergy ; RC581-607 ; Biology (General) ; QH301-705.5
Language	English
Publishing date	2020-12-01T00:00:00Z
Publisher	Public Library of Science (PLoS)
Document type	Article ; Online
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Article ; Online: A distinct subpopulation of human NK cells restricts B cell transformation by EBV.

Lünemann, Anna / Vanoaica, Liliana D / Azzi, Tarik / Nadal, David / Münz, Christian

Journal of immunology (Baltimore, Md. : 1950)

2013 Volume 191, Issue 10, Page(s) 4989–4995

Abstract: NK cells constitute the first line of defense against pathogens and transformed cells. They mature in secondary lymphoid organs, including tonsils, where common pathogens, such as EBV, enter the host and potentially imprint differentiating cells, which ... ...

Abstract	NK cells constitute the first line of defense against pathogens and transformed cells. They mature in secondary lymphoid organs, including tonsils, where common pathogens, such as EBV, enter the host and potentially imprint differentiating cells, which then patrol the body via the blood stream. Therefore, we set out to characterize a distinct human NK cell population in tonsils that produces high amounts of the immunomodulatory and antiviral cytokine IFN-γ. We found that the tonsilar IFN-γ(high) NK cell subset is CD56(bright)NKG2A(+)CD94(+)CD54(+)CD62L(-), is present in tonsils ex vivo and is more mature than other CD56(bright) NK cells in tonsils and less mature than other NK cells in blood, shows very low plasticity even after prolonged cytokine stimulation, accumulates in tonsils of EBV carriers, and is able to potently restrict EBV-induced transformation of B cells. Thus, we characterized a distinct and stable IFN-γ(high) NK cell subpopulation that can specifically restrict malignant transformation of EBV-infected B cells. This subset should be exploited for future development of cell-based therapeutic approaches in EBV-associated malignancies.
MeSH term(s)	B-Lymphocytes/immunology ; B-Lymphocytes/virology ; CD56 Antigen/metabolism ; Epstein-Barr Virus Infections/immunology ; Herpesvirus 4, Human/immunology ; Humans ; Intercellular Adhesion Molecule-1/metabolism ; Interferon-gamma/biosynthesis ; Interferon-gamma/metabolism ; Killer Cells, Natural/immunology ; L-Selectin/metabolism ; Lymphocyte Activation/immunology ; NK Cell Lectin-Like Receptor Subfamily C/metabolism ; NK Cell Lectin-Like Receptor Subfamily D/metabolism ; Palatine Tonsil/cytology ; Palatine Tonsil/immunology
Chemical Substances	CD56 Antigen ; NK Cell Lectin-Like Receptor Subfamily C ; NK Cell Lectin-Like Receptor Subfamily D ; Intercellular Adhesion Molecule-1 (126547-89-5) ; L-Selectin (126880-86-2) ; Interferon-gamma (82115-62-6)
Language	English
Publishing date	2013-10-09
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.1301046
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Article ; Online: Immunosuppressive FK506 treatment leads to more frequent EBV-associated lymphoproliferative disease in humanized mice.

PLoS pathogens

2020 Volume 16, Issue 4, Page(s) e1008477

Abstract: Post-transplant lymphoproliferative disorder (PTLD) is a potentially fatal complication after organ transplantation frequently associated with the Epstein-Barr virus (EBV). Immunosuppressive treatment is thought to allow the expansion of EBV-infected B ... ...

Abstract	Post-transplant lymphoproliferative disorder (PTLD) is a potentially fatal complication after organ transplantation frequently associated with the Epstein-Barr virus (EBV). Immunosuppressive treatment is thought to allow the expansion of EBV-infected B cells, which often express all eight oncogenic EBV latent proteins. Here, we assessed whether HLA-A2 transgenic humanized NSG mice treated with the immunosuppressant FK506 could be used to model EBV-PTLD. We found that FK506 treatment of EBV-infected mice led to an elevated viral burden, more frequent tumor formation and diminished EBV-induced T cell responses, indicative of reduced EBV-specific immune control. EBV latency III and lymphoproliferation-associated cellular transcripts were up-regulated in B cells from immunosuppressed animals, akin to the viral and host gene expression pattern found in EBV-PTLD. Utilizing an unbiased gene expression profiling approach, we identified genes differentially expressed in B cells of EBV-infected animals with and without FK506 treatment. Upon investigating the most promising candidates, we validated sCD30 as a marker of uncontrolled EBV proliferation in both humanized mice and in pediatric patients with EBV-PTLD. High levels of sCD30 have been previously associated with EBV-PTLD in patients. As such, we believe that humanized mice can indeed model aspects of EBV-PTLD development and may prove useful for the safety assessment of immunomodulatory therapies.
MeSH term(s)	Animals ; B-Lymphocytes/metabolism ; DNA, Viral ; Disease Models, Animal ; Epstein-Barr Virus Infections/virology ; Female ; Gene Expression Profiling/methods ; HLA-A2 Antigen ; Herpesvirus 4, Human/genetics ; Herpesvirus 4, Human/metabolism ; Herpesvirus 4, Human/pathogenicity ; Humans ; Immunocompromised Host ; Immunosuppressive Agents/pharmacology ; Lymphoproliferative Disorders/immunology ; Lymphoproliferative Disorders/virology ; Male ; Mice ; Mice, Inbred NOD ; Mice, Transgenic ; Organ Transplantation/adverse effects ; Tacrolimus/pharmacology ; Transcriptome/genetics ; Viral Load
Chemical Substances	DNA, Viral ; HLA-A2 Antigen ; Immunosuppressive Agents ; Tacrolimus (WM0HAQ4WNM)
Language	English
Publishing date	2020-04-06
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1008477
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Article ; Online: CD8+ T cells retain protective functions despite sustained inhibitory receptor expression during Epstein-Barr virus infection in vivo.

Chatterjee, Bithi / Deng, Yun / Holler, Angelika / Nunez, Nicolas / Azzi, Tarik / Vanoaica, Liliana Danusia / Müller, Anne / Zdimerova, Hana / Antsiferova, Olga / Zbinden, Andrea / Capaul, Riccarda / Dreyer, Johannes H / Nadal, David / Becher, Burkhard / Robinson, Mark D / Stauss, Hans / Münz, Christian

PLoS pathogens

2019 Volume 15, Issue 5, Page(s) e1007748

Abstract: Epstein Barr virus (EBV) is one of the most ubiquitous human pathogens in the world, persistently infecting more than 90% of the adult human population. It drives some of the strongest human CD8+ T cell responses, which can be observed during symptomatic ...

Abstract	Epstein Barr virus (EBV) is one of the most ubiquitous human pathogens in the world, persistently infecting more than 90% of the adult human population. It drives some of the strongest human CD8+ T cell responses, which can be observed during symptomatic primary infection known as infectious mononucleosis (IM). Despite high viral loads and prolonged CD8+ T cell stimulation during IM, EBV enters latency and is under lifelong immune control in most individuals that experience this disease. We investigated whether changes in T cell function, as frequently characterized by PD-1 up-regulation, occur during IM due to the prolonged exposure to high antigen levels. We readily detected the expansion of PD-1 positive CD8+ T cells together with high frequencies of Tim-3, 2B4, and KLRG1 expression during IM and in mice with reconstituted human immune system components (huNSG mice) that had been infected with a high dose of EBV. These PD-1 positive CD8+ T cells, however, retained proliferation, cytokine production, and cytotoxic abilities. Multiple subsets of CD8+ T cells expanded during EBV infection, including PD-1+Tim-3+KLRG1+ cells that express CXCR5 and TCF-1 germinal center homing and memory markers, and may also contain BATF3. Moreover, blocking the PD-1 axis compromised EBV specific immune control and resulted in virus-associated lymphomagenesis. Finally, PD-1+, Tim-3+, and KLRG1+ CD8+ T cell expansion coincided with declining viral loads during low dose EBV infection. These findings suggest that EBV infection primes PD-1 positive CD8+ T cell populations that rely on this receptor axis for the efficient immune control of this ubiquitous human tumor virus.
MeSH term(s)	Adult ; Animals ; CD8-Positive T-Lymphocytes/immunology ; CD8-Positive T-Lymphocytes/metabolism ; CD8-Positive T-Lymphocytes/virology ; Case-Control Studies ; Cytokines/metabolism ; Epstein-Barr Virus Infections/immunology ; Epstein-Barr Virus Infections/metabolism ; Epstein-Barr Virus Infections/virology ; Gene Expression Profiling ; Herpesvirus 4, Human/immunology ; Humans ; Inflammation Mediators/metabolism ; Mice ; Mice, Inbred NOD ; Mice, SCID ; Programmed Cell Death 1 Receptor/metabolism ; T-Lymphocytes, Cytotoxic/immunology ; Viral Load/immunology
Chemical Substances	Cytokines ; Inflammation Mediators ; Programmed Cell Death 1 Receptor
Language	English
Publishing date	2019-05-30
Publishing country	United States
Document type	Journal Article ; Research Support, Non-U.S. Gov't
ZDB-ID	2205412-1
ISSN	1553-7374 ; 1553-7366
ISSN (online)	1553-7374
ISSN	1553-7366
DOI	10.1371/journal.ppat.1007748
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Article ; Online: Two alternate strategies for innate immunity to Epstein-Barr virus: One using NK cells and the other NK cells and γδ T cells.

Djaoud, Zakia / Guethlein, Lisbeth A / Horowitz, Amir / Azzi, Tarik / Nemat-Gorgani, Neda / Olive, Daniel / Nadal, David / Norman, Paul J / Münz, Christian / Parham, Peter

The Journal of experimental medicine

2017 Volume 214, Issue 6, Page(s) 1827–1841

Abstract: Most humans become infected with Epstein-Barr virus (EBV), which then persists for life. Infrequently, EBV infection causes infectious mononucleosis (IM) or Burkitt lymphoma (BL). Type I EBV infection, particularly type I BL, stimulates strong responses ... ...

Abstract	Most humans become infected with Epstein-Barr virus (EBV), which then persists for life. Infrequently, EBV infection causes infectious mononucleosis (IM) or Burkitt lymphoma (BL). Type I EBV infection, particularly type I BL, stimulates strong responses of innate immune cells. Humans respond to EBV in two alternative ways. Of 24 individuals studied, 13 made strong NK and γδ T cell responses, whereas 11 made feeble γδ T cell responses but stronger NK cell responses. The difference does not correlate with sex, HLA type, or previous exposure to EBV or cytomegalovirus. Cohorts of EBV
MeSH term(s)	Adult ; Antigens, CD/metabolism ; B-Lymphocytes/immunology ; B-Lymphocytes/virology ; Butyrophilins/metabolism ; Cell Differentiation/immunology ; Cell Proliferation ; Cytomegalovirus/physiology ; Epstein-Barr Virus Infections/immunology ; Epstein-Barr Virus Infections/pathology ; Epstein-Barr Virus Infections/virology ; Genotype ; HLA Antigens/immunology ; Herpesvirus 4, Human/immunology ; Humans ; Immunity, Innate ; Killer Cells, Natural/immunology ; Lymphocyte Activation/immunology ; NK Cell Lectin-Like Receptor Subfamily K/metabolism ; Phenotype ; Receptors, Antigen, T-Cell, gamma-delta/metabolism ; Tissue Donors
Chemical Substances	Antigens, CD ; BTN3A1 protein, human ; Butyrophilins ; HLA Antigens ; KLRK1 protein, human ; NK Cell Lectin-Like Receptor Subfamily K ; Receptors, Antigen, T-Cell, gamma-delta
Language	English
Publishing date	2017-05-03
Publishing country	United States
Document type	Journal Article ; Research Support, N.I.H., Extramural
ZDB-ID	218343-2
ISSN	1540-9538 ; 0022-1007
ISSN (online)	1540-9538
ISSN	0022-1007
DOI	10.1084/jem.20161017
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