Induction of the measles virus receptor SLAM (CD150) on monocytes

Minagawa, Hiroko; Tanaka, Kotaro; Ono, Nobuyuki; Tatsuo, Hironobu; Yanagi, Yusuke

doi:10.1099/0022-1317-82-12-2913

Cited by 82 publications

(83 citation statements)

References 37 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…CHO-CD150 [24], Vero-CD150 cells [47], THP-1 and the Epstein-Barr virus-transformed B-lymphoblastic cell lines (BLCL-OUW, BLCL-GR, BLCL-WH, BLCL-JP) [30,48] were cultured as described [10,18,49].…”

Section: Cellsmentioning

confidence: 99%

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4⁺ T cells but are incapable of cross‐presentation

et al. 2011

View full text Add to dashboard Cite

Langerhans cells (LCs) are a subset of DCs that reside in the upper respiratory tract and are ideally suited to sense respiratory virus infections. Measles virus (MV) is a highly infectious lymphotropic and myelotropic virus that enters the host via the respiratory tract. Here, we show that human primary LCs are capable of capturing MV through the C-type lectin Langerin. Both immature and mature LCs presented MV-derived antigens in the context of HLA class II to MV-specific CD4 1 T cells. Immature LCs were not susceptible to productive infection by MV and did not present endogenous viral antigens in the context of HLA class I. In contrast, mature LCs could be infected by MV and presented de novo synthesized viral antigens to MV-specific CD8 1 T cells. Notably, neither immature nor mature LCs were able to cross-present exogenous UV-inactivated MV or MV-infected apoptotic cells. The lack of direct infection of immature LCs, and the inability of both immature and mature LCs to crosspresent MV antigens, suggest that human LCs may not be directly involved in priming MV-specific CD8 1 T cells. Immune activation of LCs seems a prerequisite for MV infection of LCs and subsequent CD8 1 T-cell priming via the endogenous antigen presentation pathway. Eur. J. Immunol. 2011. 41: 2619-2631 DOI 10.1002 Immunity to infection 2619 molecules, a process referred to as cross-presentation which is thought to be important in both viral and tumor immunity [2,3]. It is becoming evident that different DC subsets have specialized functions in anti-viral immunity, e.g. by inducing preferentially CD4 1 or CD8 1 T-cell responses or by inducing innate immunity against pathogens [4,5]. Langerhans cells (LCs) are a subset of DCs that are, in humans, characterized by expression of CD1a, the C-type lectin Langerin and the presence of Birbeck granules [6]. LCs reside in the epidermis and stratified epithelial tissues [7][8][9]. Recently, we have shown that LCs form a barrier against HIV-1; LCs capture HIV-1 through Langerin, resulting in internalization of HIV-1 into Birbeck granules and preventing subsequent HIV-1 transmission [10]. However, little is known about the role of human LCs and Langerin in antigen presentation.Capture of exogenous antigens by LCs leads to induction of CD4 1 T-cell responses [11][12][13]. However, the ability of LCs to cross-present exogenous antigens to CD8 1 T cells has been debated [14][15][16][17]. Klechevsky et al. [13] have shown that in vitrogenerated human LCs from either CD34 1 cells or monocytes are capable of cross-presenting influenza-virus proteins to CD8 1 T cells. However, these in vitro-generated LCs might be different from primary immature LCs.Here, we have investigated the antigen capture and presentation capacity of human primary LCs during measles virus (MV) infection. MV is the causative agent of measles, which remains an important cause of morbidity and mortality in developing countries. MV is a lymphotropic and myelotropic virus and DCs have been implicated in its transmission [18,19]. MV is on...

show abstract

Section: Cellsmentioning

confidence: 99%

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4⁺ T cells but are incapable of cross‐presentation

et al. 2011

View full text Add to dashboard Cite

show abstract

“…Recently, the signalling lymphocytic activation molecule (SLAM, CD150) has been identified as a common receptor interacting with MV vaccine as well as wild-type strains (Erlenhoefer et al, 2001(Erlenhoefer et al, , 2002Hsu et al, 2001; Ono et al, 2001a, b;Tatsuo et al, 2000). SLAM is expressed on human B cell lines, primary activated B and T cells, memory cells and activated monocytes and monocyte-derived dendritic cells (Cocks et al, 1995;Minagawa et al, 2001;Ohgimoto et al, 2001;Polacino et al, 1996;Punnonen et al, 1997), and its usage as a receptor can explain the tropism of wild-type MV for such cells, but not for epithelial, endothelial and neural cells, such as neurons, oligodendrocytes and astrocytes, which do not express SLAM (McQuaid & Cosby, 2002). On monocytes, the expression of SLAM is induced after infection with MV or treatment with UV-inactivated MV (Minagawa et al, 2001).…”

Section: Introductionmentioning

confidence: 99%

“…SLAM is expressed on human B cell lines, primary activated B and T cells, memory cells and activated monocytes and monocyte-derived dendritic cells (Cocks et al, 1995;Minagawa et al, 2001;Ohgimoto et al, 2001;Polacino et al, 1996;Punnonen et al, 1997), and its usage as a receptor can explain the tropism of wild-type MV for such cells, but not for epithelial, endothelial and neural cells, such as neurons, oligodendrocytes and astrocytes, which do not express SLAM (McQuaid & Cosby, 2002). On monocytes, the expression of SLAM is induced after infection with MV or treatment with UV-inactivated MV (Minagawa et al, 2001). Recently we demonstrated that this induction of SLAM is due to the interaction of wildtype MV with the Toll-like receptor 2, which is not a receptor for uptake of MV (Bieback et al, 2002).…”

Section: Introductionmentioning

confidence: 99%

CD46- and CD150-independent endothelial cell infection with wild-type measles viruses

Andrés¹,

Obojes²,

Kim

et al. 2003

Journal of General Virology

View full text Add to dashboard Cite

Measles virus (MV) infects endothelial cells of the skin, the brain and other organs during acute or persistent infections. Endothelial cells are supposed to play an important role in virus spread from the blood stream to surrounding tissues. CD46 and CD150 (signalling lymphocytic activation molecule, SLAM) have been described as cellular receptors for certain MV strains. We found that human umbilical vein and brain microvascular endothelial cells (HUVECs and HBMECs) were CD46-positive, but did not express SLAM. Wild-type MV strains, which do not use CD46 as a receptor at the surface of transfected Chinese hamster ovary cells, infected HUVECs and HBMECs to varying extents in a strain-dependent way. This infection was not inhibited by antibodies to CD46. These data suggest the presence of an additional unidentified receptor for MV uptake and spread in human endothelial cells. INTRODUCTIONAfter acute infection of the upper respiratory tract, measles virus (MV) is rapidly transported to draining lymph nodes forming giant cells in the reticulo-endothelial system. MV then establishes a systemic infection and spreads to different organs, including the skin. In these organs, virus replicates primarily in endothelial cells (ECs), epithelial cells and monocytes/macrophages (Griffin & Bellini, 1996). ECs of dermal capillaries (Kimura et al., 1975) and small vessels throughout the body show clear evidence of MV infection. This appears to play a central role in pathogenesis, leading to changes in the skin, conjunctivae, mucous membranes and the brain (Cosby & Brankin, 1995), accompanied by vascular dilatation, increased vascular permeability, mononuclear cell infiltration and infection of surrounding tissues. In rare cases, the EC infection may extend to a severe haemorrhagic infection with confluent haemorrhagic skin eruptions and intravascular coagulopathy, so-called haemorrhagic or black measles. Brain ECs and capillary endothelium of lymph nodes and the thymus have been found to be infected in fatal cases of acute measles (Esolen et al., 1995; Moench et al., 1988). In subacute sclerosing panencephalitis (SSPE) patients, brain ECs appear to be infected in addition to various neural cells (Allen et al., 1996;Isaacson et al., 1996;Kirk et al., 1991).Following the identification of CD46 as a receptor for MV vaccine and laboratory strains (Dörig et al., 1993;Naniche et al., 1993a), evidence has accumulated that many wildtype isolates do not use CD46 as a receptor. Recently, the signalling lymphocytic activation molecule (SLAM, CD150) has been identified as a common receptor interacting with MV vaccine as well as wild-type strains (Erlenhoefer et al., 2001(Erlenhoefer et al., , 2002Hsu et al., 2001; Ono et al., 2001a, b;Tatsuo et al., 2000). SLAM is expressed on human B cell lines, primary activated B and T cells, memory cells and activated monocytes and monocyte-derived dendritic cells (Cocks et al., 1995;Minagawa et al., 2001;Ohgimoto et al., 2001;Polacino et al., 1996;Punnonen et al., 1997), and its usage as a receptor c...

show abstract

“…MV targets CD150 + haematopoetic cells (Condack et al, 2007; de Swart et al, 2007), and in experimentally infected macaques, mucosal DCs replicate MV in vivo (de Swart et al, 2007). DCs are generated from precursors and they mature upon MV exposure in vitro (Dubois et al, 2001;Fugier-Vivier et al, 1997;Grosjean et al, 1997;Kaiserlian et al, 1997;Schnorr et al, 1997;Servet-Delprat et al, 2000), this involves toll-like receptor (TLR) signalling and type I interferon (IFN) (Minagawa et al, 2001;Schnorr et al, 1997;Servet-Delprat et al, 2000;Shingai et al, 2007). MV-matured DCs (MV-DCs) fail to promote allogenic T cell expansion, which results from signalling by the viral glycoproteins expressed on the DC surface to T cells (Kerdiles et al, 2006;Schneider-Schaulies & Dittmer, 2006;Schneider-Schaulies et al, 2003;Servet-Delprat et al, 2003).…”

mentioning

confidence: 99%

Measles virus modulates chemokine release and chemotactic responses of dendritic cells

Abt

Gassert

Schneider‐Schaulies

2009

Journal of General Virology

View full text Add to dashboard Cite

Interference with dendritic cell (DC) maturation and function is considered to be central to measles virus (MV)-induced immunosuppression. Temporally ordered production of chemokines and switches in chemokine receptor expression are essential for pathogen-driven DC maturation as they are prerequisites for chemotaxis and T cell recruitment. We found that MV infection of immature monocyte-derived DCs induced transcripts specific for CCL-1, -2, -3, -5, -17 and -22, CXCL-10 and CXCL-11, yet did not induce and CCL-20 at the mRNA and protein level. Within 24 h post-infection, T cell attraction was not detectably impaired by these cells. MV infection failed to promote the switch from CCR5 to CCR7 expression and this correlated with chemotactic responses of MV-matured DC cultures to CCL-3 rather than to CCL-19. Moreover, the chemotaxis of MV-infected DCs to either chemokine was compromised, indicating that MV also interferes with this property independently of chemokine receptor modulation. Hallmarks of measles virus (MV)-induced immuno-suppression include lymphopenia and proliferative unresponsiveness of peripheral blood lymphocytes to mitogens (Griffin et al., 1994;Schneider-Schaulies & ter Meulen, 2002). The ability of myeloid dendritic cells (DCs) to both initiate T cell activation and mediate viral transport to secondary lymphatics has determined that they are central to MV-specific immunity and immunosuppression (Pollara et al., 2005;Steinman et al., 2003). MV targets CD150 + haematopoetic cells (Condack et al., 2007; de Swart et al., 2007), and in experimentally infected macaques, mucosal DCs replicate MV in vivo (de Swart et al., 2007). DCs are generated from precursors and they mature upon MV exposure in vitro (Dubois et al., 2001;Fugier-Vivier et al., 1997;Grosjean et al., 1997;Kaiserlian et al., 1997;Schnorr et al., 1997;Servet-Delprat et al., 2000), this involves toll-like receptor (TLR) signalling and type I interferon (IFN) (Minagawa et al., 2001;Schnorr et al., 1997;Servet-Delprat et al., 2000;Shingai et al., 2007). MV-matured DCs (MV-DCs) fail to promote allogenic T cell expansion, which results from signalling by the viral glycoproteins expressed on the DC surface to T cells (Kerdiles et al., 2006;Schneider-Schaulies & Dittmer, 2006;Schneider-Schaulies et al., 2003;Servet-Delprat et al., 2003).Maturing DCs change their responsiveness from initially pro-inflammatory to lymphoid-type chemokines (reflected by a switch from CCR5 to CCR7 surface expression) which allows egress from peripheral sites where they respond to CCR5-binding chemokines, such as CCL-3, and migration towards secondary lymphatics in response to CCR7-binding chemokines, such as CCL-19 (Caux et al., 2002;Sallusto et al., 1998;Sozzani et al., 1998); alterations in chemokine release also occur (Piqueras et al., 2006). DC chemotaxis is targeted during immune evasion by vaccinia virus, human cytomegalovirus (HCMV), herpes simplex virus (HSV) and influenza A virus (Humrich et al., 2007;Moutaftsi et al., 2004;Prechtel et al., 2005;Salentin e...

show abstract

Induction of the measles virus receptor SLAM (CD150) on monocytes

Cited by 82 publications

References 37 publications

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4⁺ T cells but are incapable of cross‐presentation

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4⁺ T cells but are incapable of cross‐presentation

CD46- and CD150-independent endothelial cell infection with wild-type measles viruses

Measles virus modulates chemokine release and chemotactic responses of dendritic cells

Contact Info

Product

Resources

About

Induction of the measles virus receptor SLAM (CD150) on monocytes

Cited by 82 publications

References 37 publications

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4+ T cells but are incapable of cross‐presentation

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4+ T cells but are incapable of cross‐presentation

CD46- and CD150-independent endothelial cell infection with wild-type measles viruses

Measles virus modulates chemokine release and chemotactic responses of dendritic cells

Contact Info

Product

Resources

About

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4⁺ T cells but are incapable of cross‐presentation

Human Langerhans cells capture measles virus through Langerin and present viral antigens to CD4⁺ T cells but are incapable of cross‐presentation