Immunité & Infections Virales, CNRS-UCBL UMR 5537, IFR 62 Laennec, Rue Paradin, 69372 Lyon Cedex 08, France
Correspondence
Denis Gerlier
gerlier{at}laennec.univ-lyon1.fr
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ABSTRACT |
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The first three authors contributed equally to this work.
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INTRODUCTION |
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The recently recognized key role of the innate immunity in the induction of cognate immunity (see Aderem & Ulevitch, 2000; Fearon, 2000
, for reviews) led us to explore further the possible contribution of complement in MV infection. Sissons and co-workers observed that MV Edmonston strain-infected human HeLa cells activate, in the absence of antibodies, the alternative pathway of human complement and that these cells were more sensitive to complement-mediated lysis (Sissons et al., 1979
, 1980
). To enter HeLa cells, MV uses the protein CD46 as a cellular receptor (Dörig et al., 1993
; Naniche et al., 1993a
). CD46 is a regulator of complement activation that acts as a cofactor of the soluble serine protease, Factor I, to cleave and inactivate covalently bound cell surface C3b and C4b into C3bi and C4bi (see Liszewski et al., 1991
, for review). CD46 acts preferentially on the alternative pathway (Kojima et al., 1993
) by inhibiting the amplification loop of C3b deposition (Devaux et al., 1999
). During MV infection, CD46 is down-regulated because interaction with the MV haemagglutinin (H) protein results in enhanced internalization (Krantic et al., 1995
; Naniche et al., 1993b
) and/or intracellular retention of CD46 (Yant et al., 1997
). This down-regulation was proposed to be responsible for the increased sensitivity of MV-infected cells to complement-mediated cell lysis (Schneider-Schaulies et al., 1995
; Schnorr et al., 1995
). However, only a small amount of CD46 can prevent human C3b deposition (Christiansen et al., 2000a
) and residual levels of CD46 after infection may prevent C3b deposition.
CD46 is now generally considered to function as a receptor for vaccine and laboratory-adapted strains of MV only. Instead, all strains, including wild-type MVs, use CD150 (signalling lymphocytic activation molecule, or SLAM) as a cellular receptor (Tatsuo et al., 2000b). Accordingly, MV strains are referred as CD46non-using or CD46using.
We have attempted to clarify further the molecular mechanisms of alternative complement pathway activation by MV, whichever CD46 and/or CD150 cellular receptor it uses.
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METHODS |
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Human serum (HS), isolated from ice-clotted blood of a single donor and human Factor B-depleted serum (Quidel) were stored as aliquots at 70 °C before use. IgG-depleted HS was obtained by incubating HS at 4 °C with an equal volume of protein Gagarose beads for 1 h just prior to the experiment. IgG-depleted HS was essentially non-reactive with CHO.CD46 cells and showed only residual labelling of MV-infected cells by flow cytometry. The residual anti-MV antibodies were devoid of significant neutralizing activity (data not shown). Heat-inactivated HS (30 min at 56 °C) was also used.
CHO (Chinese hamster ovary) fibroblasts CHO.CD46 (Devaux et al., 1999), simian B95a and human 293T cells were grown in Dulbecco's modified essential medium (DMEM) supplemented with 6 % foetal calf serum (FCS), 10 µg gentamicin ml1, non-essential amino acids and 10 µg adenosine, deoxyadenosine and thymidine ml1.
The Hallé strain of MV (CD46using) was produced in African green monkey Vero or human HeLa cells and purified on a sucrose gradient (Naniche et al., 1993a). The Lys-1 (Fayolle et al., 1999
) and Ma93F (Lecouturier et al., 1996
) MV strains (CD46non-using) were amplified in simian B95a cells. CHO.CD46, B95a and 293T cells were infected with MV at an m.o.i. of 0·1 or 1 for 1 h, washed and incubated with 10 µg zD-phe-L-Phe-Gly tripeptide ml1 to prevent syncytium formation (Richardson & Choppin, 1983
). The cells were used 48 h after MV infection.
Expression of MV H and F protein.
293T cells were transfected with 2 µg (unless otherwise indicated) of plasmid using Lipofectamin and OPTIMEM reagents (Invitrogen). The eukaryotic expression vectors used were pSC6-T7, pCAG-CD150, pCX2N KAH, pCX2N EdH and pCXN F encoding T7 polymerase, CD150, H from the KA MV strain (CD46non-using) and H and F from the Edmonston MV strain (CD46using), respectively (Tatsuo et al., 2000a).
Complement activation on cells.
Forty-eight hours after MV infection or 24 h after transfection, cells were harvested, washed with DMEM plus 0·05 % sodium azide (containing no FCS), then incubated for 30 min at 37 °C with IgG-depleted HS in the presence of MgCl2/EGTA unless otherwise indicated. Complement activation was stopped by rapid dilution with cold DMEM plus 0·05 % sodium azideand centrifugation at 400 g for 5 min. Following additional washing, the cells were incubated in 50 µl of an appropriate dilution of WM1 mAb at 4 °C for 30 min. Cell infection and CD46 expression were detected using murine monoclonal anti-H or -F and anti-CD46 antibodies, respectively. Immunolabelling was measured after incubation with PE-labelled anti-mouse Ig(H+L) conjugate and flow cytofluorometry as detailed elsewhere (Naniche et al., 1993a). In some experiments, CHO or CHO.CD46 cells (2·5x105) pre-loaded with MV for 1 h at 37 °C were used. After two washes to eliminate unbound virus, cells were incubated at 37 °C for 30 min with MgCl2/EGTA-supplemented IgG-depleted HS. In one experiment, the unbound virus was left and the HS was added directly to the virus/cell mixture. In some experiments, results were expressed as mean fluorescence value in arbitrary units. Fluorescence background level after incubation with the conjugate without the primary antibody remained within the ±20 % range and was therefore not subtracted. When CD46, CD55, H and F expression levels were compared after MV infection or transfection with expression vectors encoding the MV glycoproteins, the results were normalized and expressed as % expression, calculated as follow: % expression=(observed expressionbackground)/(maximal expressionbackground)x100, where maximal expression=expression level (in mean fluorescent units) observed in untreated cells for CD46 and CD55 and in MV-infected cells for H and F protein and background=fluorescence level in the absence of primary antibody (conjugate control).
MV binding after complement activation on the virus.
Purified MV Hallé was incubated for 30 min at 37 °C with MgCl2/EGTA-supplemented IgG-depleted HS (heat-inactivated or not). Complement activation was stopped by heat inactivation at 56 °C for 30 min. The virus/complement mixture was then incubated with CHO.CD46 cells. After a 1 h incubation and subsequent washing, the cells were stained for C3b and MV binding. Heat treatment did not change the MV binding properties (not shown).
Immunoprecipitation.
Cells (107) were infected with MV (m.o.i.=1) for 24 h and incubated with HS to allow activation of the alternative pathway for 20 min. After two washes in cold DMEM (without FCS) and lysis in a CHAPS/Triton X-100 buffer (50 mM Tris, pH 8, 150 mM NaCl, 2 mM MgCl2, 2 mM CaCl2, 10 g CHAPS l1, 1 % Triton X-100 and protease inhibitors), a pre-clearing step was performed with 20 µl of an irrelevant antibody, 9E10 anti-myc and anti-mouse Ig antibodies bound to protein GSepharose beads. WM1 antibody (40 µg) was then added to the lysate. After precipitation using anti-mouse Ig antibodies bound to protein GSepharose beads, bound proteins were eluted from the beads by heating at 95 °C with 30 µl of reducing Laemmli buffer and separated by PAGE. F protein and C3b -chain were detected by Western blotting using a rabbit anti-F cytoplasmic tail polyclonal antiserum and WM1 mAb, respectively.
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RESULTS |
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Activation of the alternative pathway by both CD46using and CD46non-using MV strains in the presence of a truncated CD46 proficient for complement regulation but unable to bind MV
Simian B95a cells were chosen as target cells because they express truncated simian CD46 molecules devoid of SCR1. Indeed, SCR1-deleted CD46 is unable to bind to MV, but efficiently regulates complement activation (Erlenhoefer et al., 2001; Murakami et al., 1998
). B95a cells also express the simian CD150 (Tatsuo et al., 2000b
), which enables infection by both CD46using and CD46non-using MV strains. As expected from the species cross-functionality of simian CD46 with human complement (Murakami et al., 1998
), uninfected B95a cells did not exhibit C3b deposition after incubation with HS supplemented with MgCl2/EGTA (Fig. 3
a). However, infection with either MV Hallé (CD46using) or Lys-1 strains (CD46non-using) resulted in a marked C3b deposition (Fig. 3e and i
) without any down-regulation of CD46 (Fig. 3f and j
). In contrast, CD150 was down-regulated after Lys-1 or Hallé infection (Fig. 3g and k
). In this experiment, the CD150 down-regulation induced by MV Hallé was lower than that induced by MV Lys due to the lower level of H expression (Fig. 3
, compare h and l). We therefore speculated that the complement activation was a consequence of the expression of the MV H and/or F envelope glycoproteins.
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DISCUSSION |
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How MV F protein expression results in cell surface activation of the alternative pathway is unknown. The involvement of F-specific antibodies is unlikely because similar C3b deposition was observed with HS and IgG-depleted HS (data not shown) and it would imply that F, but not H, glycoprotein elicited antibodies able to prime for complement activation. Moreover, activation through the lectin pathway is also unlikely, because, like the classical pathway, it strictly requires the presence of Ca2+ ions (Thielens et al., 2001; Turner, 1998
), which were absent in our complement activation assay carried out in the presence of MgCl2/EGTA. C3b deposition on the cell surface results from the activation of the intramolecular thioester bond of the C3b
-chain and the covalent attachment to nearby molecules (Sahu & Lambris, 2001
). The finding of F1 protein co-immunoprecipitated with the C3b
-chain indicates that during exposure to HS, some disulfide-bridged C3b
- and
-chains may become covalently linked to cell surface F1 protein. As expected, the immature F0 protein, which is less prone to be expressed at the cell surface, was not co-immunoprecipitated. Whether the formation of the C3bF complex is the primary event, which engages the uncontrolled activation of the alternative pathway, can be questioned. It seems unlikely, since the amount of F1 protein co-immunoprecipitated with the C3b
-chain was low, in contrast with what one would have expected from a direct relationship between the level of F expression and the level of C3b deposition. Furthermore, several attempts to co-immunoprecipitate C3b using anti-F antibodies have failed. C3b displays a high degree of specificity in reacting with targets with a preference for some primary OH groups on serine and threonine residues (see Sahu & Lambris, 2001
, for review). It is possible that F is substituted with oligosaccharides favouring the attachment of C3b. Historically, cell surfaces have been distinguished as being good or bad complement activators. However, the more recent discovery of the ubiquitous cell surface expression of strong complement activation regulators such as CD46 and CD55 has led to consideration that the activation properties of a cell surface are directly linked to the presence or absence of such regulators. CD46, CD55 and functionally related molecules, such as the mouse Crry1 protein, are partially species specific and, for example, mouse or hamster CD55 molecules efficiently control homologous complement but not human complement (Harris et al., 2000
). Moreover, when cells are incubated with blocking anti-CD46 antibodies, they become activators of the alternative pathway of human complement (Devaux et al., 1999
). Furthermore, the knock-down of Crry1 expression in mice results in abortion with a C3-mediated complement destruction of the foetus (Xu et al., 2000
). Since the alternative pathway was activated on F protein-expressing cells in the presence of normal amounts of CD46 and CD55, we have to speculate how F protein results in the escape of C3b from its two known regulators, CD46 and CD55. We did not observe any decrease in cell surface expression of either CD46 or CD55. A spatial sequestration of F protein (and C3b) outside CD55- and CD46-rich membrane areas is possible. It is known that, while F protein localizes in areas rich in cholesterol and glycosphingolipids, or rafts, CD46 does not (Manie et al., 2000
; Vincent et al., 2000
). But the glycosylphosphatidylinositol-anchored CD55 molecule is a constituent of rafts and fully able, when expressed alone, to control the amplification loop of the C3b deposition (Christiansen et al., 2000b
).
When the infecting virus expresses CD46using H protein, this seems to partially interfere with CD46 function, as shown by the modest increase in C3b deposition observed when expressing isolated H protein from Edmonston CD46using MV strain compared with that observed with CD46non-using KA strain H protein. Two mechanisms may contribute to this: the down-regulation of CD46 and competition between H protein and C3b for binding to CD46. The down-regulation is unlikely to be sufficient to explain the loss of C3b deposition control, since CHO cell clones expressing comparable low amounts of CD46 are fully able to prevent the C3b amplification loop (Christiansen et al., 2000a). Although the SCR2 domain of CD46 is involved in the cofactor activity (Adams et al., 1991
; Manchester et al., 1995
) and the binding to MV H protein (Buchholz et al., 1996
, 1997
; Iwata et al., 1995
; Manchester et al., 1995
), the two functions map to distinct sites (Christiansen et al., 2000a
; Liszewski et al., 2000
).
What could be the role of the C3b deposited at the virus surface? IgG-depleted HS supplemented with MgCl2/EGTA reduced virus infectivity down to 2025 % of that observed with heat-inactivated IgG-depleted HS (unpublished data) suggesting that complement activation results in partial virus inactivation. Such an inactivation occurring in vivo should hamper virus spreading throughout the body by free virus particles and favours cell-to-cell virus spreading. An antigen coupled to C3d displays a 100010 000-fold enhancement in immunogenicity (Dempsey et al., 1996). Thus, MV coating with C3b/C3bi and its natural C3d proteolytic derivative most likely contributes to the induction of a life-long-lasting, virus-specific immune response in a host who is paradoxically immunodepressed by the virus infection (Fugier-Vivier et al., 1997
; Hicks et al., 1977
; Karp, 1999
; Yamanouchi et al., 1981
).
In summary, we have shown that MV activates the alternative complement pathway with some neutralizing effect. This could play an important role, in vivo, to slow virus propagation by inactivating circulating virus and eliminating MV-infected cells, and to enhance the induction of a specific immune response by opsonizing MV antigens. A critical role of C3 in the pathology induced by gammaherpesviruses has recently been demonstrated (Kapadia et al., 2002). We propose that the activation of the alternative pathway is a primary mechanism of defence against MV infection, before the production of neutralizing anti-MV antibodies by the immune system.
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ACKNOWLEDGEMENTS |
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Received 5 December 2003;
accepted 27 January 2004.
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