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  • 1. Bachmayer, Nora
    et al.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, The Wenner-Gren Institute , Immunology.
    Sundström, Yvonne
    Hamad, Rangeen Rafik
    Berg, Louise
    Bremme, Katarina
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, The Wenner-Gren Institute , Immunology.
    Women with pre-eclampsia have an altered NKG2A and NKG2C receptor expression on peripheral blood natural killer cells.2009In: American Journal of Reproductive Immunology and Microbiology, ISSN 8755-8920, Vol. 62, no 3, p. 147-57Article in journal (Refereed)
    Abstract [en]

    PROBLEM: Preeclampsia, a pregnancy disorder, is associated with exaggerated inflammation and increased serum monokines. Uterine natural killer (NK) cells are implicated in preeclampsia pathology, but little is known regarding peripheral NK cells in the disease. METHOD OF STUDY: We examined blood NK cells at delivery in women with preeclampsia, in healthy pregnant women and in healthy non-pregnant blood donors as a reference. RESULTS: Although the percentages of both NKG2A- and NKG2C-positive NK cells were normal in preeclamptic women, the levels of NKG2A and NKG2C on NK cells were significantly up-regulated in these women. In vitro stimulation of PBMCs from healthy pregnant women and blood donors with monokines resulted in increased percentage of NKG2A(+) NK cells and increased NKG2A levels, while levels of NKG2C were decreased. CONCLUSIONS: Our results suggest that the peripheral NK-cell pool is skewed in preeclampsia and possibly under the influence of monokines like interleukin (IL)-15 and IL-12.

  • 2. Beziat, Vivien
    et al.
    Liu, Lisa L.
    Malmberg, Jenny-Ann
    Ivarsson, Martin A.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Björklund, Andreas T.
    Retiere, Christelle
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Traherne, James
    Ljungman, Per
    Schaffer, Marie
    Price, David A.
    Trowsdale, John
    Michaelsson, Jakob
    Ljunggren, Hans-Gustaf
    Malmberg, Karl-Johan
    NK cell responses to cytomegalovirus infection lead to stable imprints in the human KIR repertoire and involve activating KIRs2013In: Blood, ISSN 0006-4971, E-ISSN 1528-0020, Vol. 121, no 14, p. 2678-2688Article in journal (Refereed)
    Abstract [en]

    Human natural killer (NK) cells are functionally regulated by killer cell immunoglobulin-like receptors (KIRs) and their interactions with HLA class I molecules. As KIR expression in a given NK cell is genetically hard-wired, we hypothesized that KIR repertoire perturbations reflect expansions of unique NK-cell subsets and may be used to trace adaptation of the NK-cell compartment to virus infections. By determining the human KIR-ome at a single-cell level in more than 200 donors, we were able to analyze the magnitude of NK cell adaptation to virus infections in healthy individuals. Strikingly, infection with human cytomegalovirus (CMV), but not with other common herpesviruses, induced expansion and differentiation of KIR-expressing NK cells, visible as stable imprints in the repertoire. Education by inhibitory KIRs promoted the clonal-like expansion of NK cells, causing a bias for self-specific inhibitory KIRs. Furthermore, our data revealed a unique contribution of activating KIRs (KIR2DS4, KIR2DS2, or KIR3DS1), in addition to NKG2C, in the expansion of human NK cells. These results provide new insight into the diversity of KIR repertoire and its adaptation to virus infection, suggesting a role for both activating and inhibitory KIRs in immunity to CMV infection.

  • 3. Rasul, Abu E.
    et al.
    Nagy, Noemi
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, The Wenner-Gren Institute , Immunology.
    Adori, Monika
    Claesson, Hans-Erik
    Klein, George
    Klein, Eva
    Simultaneous detection of the two main proliferation driving EBV encoded proteins, EBNA-2 and LMP-1 in single B cells2012In: JIM - Journal of Immunological Methods, ISSN 0022-1759, E-ISSN 1872-7905, Vol. 385, no 1-2, p. 60-70Article in journal (Refereed)
    Abstract [en]

    Epstein Barr virus (EBV) is carried by almost all adults, mostly without clinical manifestations. Latent virus infection of B lymphocytes induces activation and proliferation that can be demonstrated in vitro. In healthy individuals, generation of EBV induced malignant proliferation is avoided by continuous immunological surveillance. The proliferation inducing set of the virally encoded genes is expressed exclusively in B cells in a defined differentiation window. It comprises nine EBV encoded nuclear proteins, EBNA 1-6, and three cell membrane associated proteins, LMP-1,2A and 2B, designated as latency Type III. Outside this window the expression of the viral genes is limited. Healthy carriers harbor a low number of B lymphocytes in which the viral genome is either silent or expresses one virally encoded protein, EBNA-1, latency Type I. In addition, EBV genome carrying B cells can lack either EBNA-2 or LMP-1, latency Type IIa or Type IIb respectively. These cells have no inherent proliferation capacity. Detection of both EBNA-2 and LMP-1 can identify B cells with growth potential. We devised therefore a method for their simultaneous detection in cytospin deposited cell populations. Simultaneous detection of EBNA-2 and LMP-1 was reported earlier in tissues derived from infectious mononucleosis (IM), postransplantation lymphoproliferative disorders (PTLD) and from humanized mice infected with EBV. We show for the first time the occurrence of Type IIa and Type IIb cells in cord blood lymphocyte populations infected with EBV in vitro. Further, we confirm the variation of EBNA-2 and LMP-1 expression in several Type III lines and that they vary independently in individual cells. We visualize that in Type III LCL, induced for plasmacytoid differentiation by IL-21 treatment, EBV protein expression changes to Type ha (EBNA-2 negative LMP-1 positive). We also show that when the proliferation of EBV infected cord blood lymphocyte culture is inhibited by the immunomodulator, PSK the majority of the cells express latency Type IIa pattern. These results show that by modifying the differentiation state, the proliferating EBV positive B cells can be curbed. Type IIa expression is a characteristic for EBV positive Reed-Sternberg (R/S) cells in EBV positive Hodgkin's lymphomas. For survival and proliferation, the R/S cells require the contribution of the in vivo microenvironment Consequently, Type IIa lines could not be established from Hodgkin's lymphoma in vitro. We propose that these experimental cultures can be exploited for study of the Type IIa cells.

  • 4.
    Saghafian-Hedengren, Shanie
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Theorell, Jakob
    Carvalho-Queiroz, Claudia
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Nagy, Noemi
    Persson, Jan-Olov
    Stockholm University, Faculty of Science, Department of Mathematics.
    Nilsson, Caroline
    Bryceson, Yenan T.
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Epstein-Barr Virus Coinfection in Children Boosts Cytomegalovirus-Induced Differentiation of Natural Killer Cells2013In: Journal of Virology, ISSN 0022-538X, E-ISSN 1098-5514, Vol. 87, no 24, p. 13446-13455Article in journal (Refereed)
    Abstract [en]

    During childhood, infections with cytomegalovirus (CMV) and Epstein-Barr virus (EBV) can occur in close temporal proximity. Active, as well as latent, CMV infection is associated with enlarged subsets of differentiated natural killer (NK) and cytotoxic T cells. How EBV infection may influence CMV-driven immune differentiation is not known. We found that EBV coinfection selectively influenced the NK cell compartment of CMV-seropositive (CMV+) children. Coinfected children had significantly higher proportions of peripheral-blood NKG2C(+) NK cells than CMV+ EBV- children. Ex vivo NK cell degranulation after target cell stimulation and plasma IL-15 levels were significantly higher in CMV+ children. EBV coinfection was related to the highest levels of plasma interleukin-15 (IL-15) and IL-12p70. Remarkably, in vitro EBV infection of peripheral blood mononuclear cells (PBMC) from EBV- CMV+ children increased NKG2C(+) NK cell proportions. A similar tendency was seen in cocultures of PBMC with EBV+ lymphoblastoid B-cell lines (LCL) and IL-15. After K562 challenge, NKG2C(+) NK cells excelled in regard to degranulation and production of gamma interferon, regardless of whether there was previous coculture with LCL. Taken together, our data suggest that dual latency with these herpesviruses during childhood could contribute to an in vivo environment supporting differentiation and maintenance of distinct NK cell populations. This viral imprint may affect subsequent immune responses through altered distributions of effector cells.

  • 5.
    Saghafian-Hedengren, Shanie
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Theorell, Jakob
    Carvalho-Queiroz, Claudia
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Nagy, Noémi
    Persson, Jan-Olov
    Nilsson, Caroline
    Bryceson, Yenan T.
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Epstein-Barr Virus Co-infection in Children Boosts Cytomegalovirus-induced Differentiation of Natural Killer CellsManuscript (preprint) (Other academic)
    Abstract [en]

    During childhood, infections with cytomegalovirus (CMV) and Epstein-Barr virus (EBV) can occur in close temporal proximity. Active as well as latent CMV infection is associated with enlarged subsets of differentiated NK- and cytotoxic T cells. How EBV infection may influence CMV-driven immune differentiation is not known. Here we found that EBV co-infection selectively influenced the NK-cell compartment of CMV-seropositive (CMV+) children. Co-infected children had significantly higher proportions of peripheral-blood NKG2C+ NK cells than CMV+EBV children. Ex vivo NK-cell degranulation after target cell stimulation and plasma IL-15 levels were significantly higher in CMV+ children. EBV co-infection related with the highest levels of plasma IL-15 and IL-12p70. Remarkably, in vitro EBV infection of peripheral blood mononuclear cells (PBMC) from EBVCMV+ children increased NKG2C+ NK-cell proportions. A similar tendency was seen in co-cultures of PBMC with EBV+ lymphoblastoid B-cell lines (LCL) and IL-15. Following K562 challenge, NKG2C+ NK cells excelled in regards to degranulation and production of IFN-g, regardless of previous co-culture with LCL. Taken together, our data suggest that herpesvirus interplay during childhood could contribute to an in vivo environment supporting differentiation and maintenance of distinct NK-cell populations. This viral imprint may affect subsequent immune responses through altered distributions of effector cells.

  • 6.
    Saghafian-Hedengren, Shanie
    et al.
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Sundström, Yvonne
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Nilsson, Caroline
    Linde, Annika
    Troye-Blomberg, Marita
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Berg, Louise
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Herpesvirus seropositivity in childhood associates with decreased monocyte-induced NK-cell IFN-γ production2009In: Journal of Immunology, ISSN 0022-1767, E-ISSN 1550-6606, Vol. 182, no 4, p. 2511-2517Article in journal (Refereed)
    Abstract [en]

    EBV infection is inversely associated with IgE sensitization in children, and this association is further enhanced by CMV coinfection. In mice, herpesvirus latency causes systemic innate activation and protection from bacterial coinfection, implying the importance of herpesviruses in skewing immune responses during latent infection. Early control of viral infections depends on IFN- release by NK cells, which generally requires the presence of accessory cells. We investigated IFN- production by NK cells in PBMCs from children seropositive (SP) for EBV alone, for both EBV and CMV, or seronegative for both viruses. The ability of classical (CD14++CD16–) and proinflammatory (CD14+CD16+) monocytes to induce autologous NK cell IFN- was studied by coculture experiments with enriched CD3–CD56+ cells. Transwell experiments were used to evaluate how monocytes interact with NK cells to induce IFN- synthesis. SP children had a significantly reduced proportion of IFN-+ NK cells and cognate intracellular IFN- levels, which was more pronounced in CMV-coinfected subjects. Also, resting PBMCs of SP children displayed lower proportions of proinflammatory monocytes. IFN- production by NK cells was dependent on interactions with monocytes, with the proinflammatory subset inducing the highest IFN-. Finally, SP children had markedly lower levels of plasma IFN-, concurrent with in vitro findings. Herpesvirus infections could be one contributing factor for maturation toward balanced Th1-Th2 responses. Our data indicate that early infection by herpesviruses may affect NK cell and monocyte interactions and thereby also influence the development of allergies.

  • 7.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Immune maturation in early childhood and the influence of herpesvirus infections2013Doctoral thesis, comprehensive summary (Other academic)
    Abstract [en]

    The quality of immune responses develops from birth into adulthood and in the context of the host microbial environment. The aim of this work was to study immune maturation during childhood, and how this process can be affected by the common herpesviruses; Epstein-Barr virus (EBV) and cytomegalovirus (CMV).

    In paper I we studied monocytes, an important cell type for immunity in the newborn. We showed that the neonatal monocyte subsets exist in similar frequencies as adult subsets, and have a potent capacity for pro-inflammatory cytokine production. In paper II, III and IV we studied the effects of EBV and CMV infections on immune cell function in children. In paper II we found that monocyte-induced NK-cell production of IFN-γ, and plasma IFN-γ levels, were decreased in 2-year old EBV- and/or CMV-seropositive children and mostly so in co-infected children. In paper III we found that in 5-year old children, EBV and CMV co-infection was associated with the highest levels of differentiated NKG2C+ NK cells. CMV+ children had higher plasma IFN-γ and IL-15 levels and higher NK-cell cytotoxic capacity. In vitro PBMC systems showed elevated frequencies of NKG2C+ NK cells in the presence of EBV-infected cells. In paper IV we showed that a child’s age and subsequent capacity for anti-viral cytokine production affects in vitro EBV infection in terms of B-cell proliferation and B-cell acquisition of memory phenotype. PBMC from CMV+ children had lower EBV-induced accumulation of switched memory B cells, which was connected to high prevalence of CD57+CD8+ T cells and IFN-γ production.

    Taken together, this thesis work shows that monocyte subsets at birth can give potent functional responses and that latency with EBV and CMV has a significant effect on the differentiation process and functional capacity of anti-viral effector cells during childhood. This in turn could affect responses to related or unrelated infections or even to non-invasive antigens such as allergens.

  • 8.
    Sohlberg, Ebba
    Stockholm University, Faculty of Science, The Wenner-Gren Institute , Immunology.
    Innate immune responses in cord blood,and the influence of pathological pregnancy2011Licentiate thesis, comprehensive summary (Other academic)
  • 9.
    Sohlberg, Ebba
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Saghafian-Hedengren, Shanie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Bachmayer, Nora
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Hamad, Rangeen Rafik
    Bremme, Katarina
    Holmlund, Ulrika
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Pre-Eclampsia Affects Cord Blood NK Cell Expression of Activation Receptors and Serum Cytokine Levels but Not CB Monocyte Characteristics2014In: American Journal of Reproductive Immunology, ISSN 1046-7408, E-ISSN 1600-0897, Vol. 71, no 2, p. 178-188Article in journal (Refereed)
    Abstract [en]

    ProblemMaternal immunopathology in pre-eclampsia is well studied; however, less is known regarding the immunological effects on the newborns. Increased inflammation and activation of immune cells at the fetal-maternal interface in pre-eclampsia could influence the neonatal immune compartment. Method of StudyMonocytes and natural killer (NK) cells from cord blood (CB) of children with pre-eclamptic or healthy mothers were analyzed by flow cytometry for surface markers and intracellular cytokines. In addition, serum cytokine profiles were investigated using ELISA or cytometric bead array. ResultsNeonates born to pre-eclamptic mothers had an inflammatory serum cytokine profile. While CB monocyte characteristics seemed unaffected, CB NK cells from pre-eclamptic pregnancies had higher NKp30, but borderline lower NKG2D expression. ConclusionIn utero inflammatory priming of neonatal innate immunity taking place in pre-eclamptic pregnancies might influence specific NK cell functions in newborns.

  • 10.
    Sohlberg, Ebba
    et al.
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Saghafian-Hedengren, Shanie
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Bremme, Katarina
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, The Wenner-Gren Institute, Immunology.
    Cord blood monocyte subsets are similar to adult and show potent peptidoglycan-stimulated cytokine responses2011In: Immunology, ISSN 0019-2805, E-ISSN 1365-2567, Vol. 133, no 1, p. 41-50Article in journal (Refereed)
    Abstract [en]

    P>Human monocytes can be divided into two major subpopulations, CD14++ CD16- and CD14+ CD16+ cells, which are suggested to play different roles in antimicrobial responses. In neonates, characteristics and functional responses of monocyte subsets have not previously been explored, and might contribute to the qualitative difference between neonatal and adult cytokine profiles. We report that at baseline, monocyte subsets in cord blood and adult peripheral blood are present in similar frequencies, and show similar expression of CD11c, CD80/CD86, CD163 and HLA-DR. In response to the bacterial ligand peptidoglycan, cord blood monocytes had high inherent capacity for production of the early-response cytokines with levels of tumour necrosis factor and interleukin-12p70 exceeding adult levels, and also a higher phosphorylation of p38-mitogen-activated protein kinase. The CD14+ CD16+ cells expressed more interleukin-12p70 than CD14++ CD16- cells and were present in a higher frequency in peptidoglycan-stimulated cord blood mononuclear cell cultures. Together, the behaviour of cord blood CD14+ CD16+ cells following peptidoglycan stimulation might indicate a qualitative difference between the neonatal antimicrobial response and that of the adult. In addition we found that serum factors in cord blood and adult sera affected cytokine production similarly, with the exception of tumour necrosis factor, regardless of the source of serum or cells. Overall, our data provide new insights into monocyte heterogeneity in cord blood and monocyte subset responses to a bacterial ligand at birth.

  • 11.
    Sohlberg, Ebba
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Saghafian-Hedengren, Shanie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Rasul, Eahsan
    Marchini, Giovanna
    Nilsson, Caroline
    Klein, Eva
    Nagy, Noemi
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Cytomegalovirus-Seropositive Children Show Inhibition of In Vitro EBV Infection That Is Associated with CD8(+)CD57(+) T Cell Enrichment and IFN-gamma2013In: Journal of Immunology, ISSN 0022-1767, E-ISSN 1550-6606, Vol. 191, no 11, p. 5669-5676Article in journal (Refereed)
    Abstract [en]

    EBV, a human herpesvirus, is commonly acquired during childhood and persists latently in B cells. EBV seropositivity has been connected to immunomodulatory effects such as altered T and NK cell functional responses as well as protection against early IgE sensitization; however, owing to the asymptomatic presentation during childhood little is known regarding the infection process in children of different ages. In this study, we used mononuclear cells from cord blood and from 2- and 5-y-old EBV-naive children for in vitro EBV infection. We show that the degree of EBV-induced B cell activation and expansion differs between age groups and in particular in relationship to IFN-gamma production capacity. EBV infection induced redistribution between B cell subsets with enrichment of IgD(+)CD27(+) cells (commonly referred to as non-switched memory) in infected cord blood cell cultures, and of IgD(-)CD27(+) cells (switched memory) in cell cultures from older children. We also related results to serostatus to CMV, a persistent herpesvirus that can affect differentiation status of T and NK cells. As compared with CMV- children, the EBV-induced enrichment of IgD(-)CD27(+) B cells was significantly reduced in infected cell cultures from CMV+ children. This effect was associated with high levels of IFN-gamma and frequencies of highly mature CD8(+)CD57(+) T cells in CMV+ children. Our results demonstrate that both a child's age and serostatus to CMV will have an impact on EBV-induced B cell activation and expansion, and they point to the ability of viruses with immunomodulatory functions, such as CMV, to affect immune responses within the host system.

  • 12.
    Sohlberg, Ebba
    et al.
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Saghafian-Hedengren, Shanie
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    Rasul, Eashan
    Marchini, Giovanna
    Nilsson, Caroline
    Klein, Eva
    Nagy, Noémi
    Sverremark-Ekström, Eva
    Stockholm University, Faculty of Science, Department of Molecular Biosciences, The Wenner-Gren Institute.
    CMV Seropositive Children Show Inhibition of In Vitro EBV Infection that is Associated with CD8+CD57+ T-cell Enrichment and IFN-gManuscript (preprint) (Other academic)
    Abstract [en]

    Epstein-Barr virus (EBV), a human herpesvirus, is commonly acquired during childhood and persists latently in B cells. EBV seropositivity has been connected to immune modulatory effects such as altered T- and NK-cell functional responses as well as protection against early IgE-sensitization, but due to the asymptomatic presentation during childhood little is known regarding the infection process in children of different ages. Here, we used mononuclear cells from cord blood, 2-year and 5-year old EBV-naïve children for in vitro EBV infection. We show that the degree of EBV-induced B-cell activation and expansion differs between age groups and in particular in relation to IFN-g production capacity. EBV infection induced redistribution between B-cell subsets with enrichment of IgD+CD27+ cells (commonly referred to as non-switched memory) in infected cord blood cell cultures, and of IgD-CD27+ cells (switched memory) in cell cultures of older children. We also related results to serostatus to cytomegalovirus (CMV), a persistent herpesvirus that can affect differentiation status of T- and NK cells. As compared to CMV- children, the EBV-induced enrichment of IgD-CD27+ B cells was significantly reduced in infected cell cultures from CMV+ children. This effect was associated with high levels of IFN-g  and frequencies of highly mature CD8+CD57+ T cells in CMV+ children. Our results demonstrate that both a child’s age and serostatus to CMV will have an impact on EBV-induced B-cell activation and expansion, and points to the ability of viruses with immune-modulatory functions, like CMV, to impact on immune responses within the host system.

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