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1 Institute for Virology and Clinic for Poultry, University of Veterinary Medicine Hannover, Bünteweg 17, 30559 Hannover, Germany
2 Institute for Animal Health, Division of Microbiology, Compton Laboratory, Compton, Newbury, Berkshire RG20 7NN, UK
Correspondence
Georg Herrler
Georg.Herrler{at}tiho-hannover.de
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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2,3-linked sialic acid. In agreement with this finding, susceptibility to infection by IBV was connected to the expression of 2,3-linked sialic acid as indicated by the reactivity with the lectin Maackia amurensis agglutinin. Here, it is discussed that binding to sialic acid may be used by IBV for primary attachment to the cell surface; tighter binding and subsequent fusion between the viral and the cellular membrane may require interaction with a second receptor. |
INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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; Yeager et al., 1992). Even though both viruses interact with the same type of protein, they differ from each other in several aspects. The human virus only recognizes human APN and the pig virus only porcine APN. In addition, they have been reported to bind to different domains of APN (Tresnan et al., 1996). Feline APN can serve as a receptor not only for feline coronavirus but also for other group 1 coronaviruses, namely TGEV, HCoV-229E and Canine coronavirus (Tresnan et al., 1996). Moreover, binding of the HCoV-229E virus results in the recruitment of APN into caveolae, where the subsequent fusion between the viral and the cellular membrane takes place (Nomura et al., 2004). On the other hand, binding of TGEV to APN has been reported to result in endocytotic uptake with the fusion reaction triggered by the low pH within the endosomes (Hansen et al., 1998). Protein receptors have also been reported for other coronaviruses: CEACAM1 for Murine hepatitis virus (MHV) (Williams et al., 1991) and angiotensin-converting enzyme 2 for the coronavirus causing severe acute respiratory syndrome (SARS) (Li et al., 2003; Wang et al., 2004). In contrast to SARS-CoV and MHV, some other group 2 coronaviruses use an entry strategy similar to that of influenza viruses, i.e. they attach to sialic acids on cell surface components. Group 2, Bovine coronavirus, Human coronavirus OC43 and Porcine hemagglutinating encephalomyelitis virus, recognize N-acetyl-9-O-acetylneuraminic acid (Vlasak et al., 1988a; Schultze et al., 1990, 1991a; Schultze & Herrler, 1992). These viruses share another characteristic feature with influenza virus: they contain a receptor-destroying enzyme, that (i) removes the receptor determinant from the viral surface and thus prevents formation of virus aggregates and (ii) removes the receptor determinant from the surface of the infected cell and thus facilitates virus release from the infected cell and spread to uninfected cells. In the case of coronaviruses, the enzyme is an acetylesterase as has also been reported for Influenza C virus (FLUCV) (Herrler et al., 1985; Vlasak et al., 1988b; Schultze et al., 1991b). Some strains of MHV may attach not only to CEACAM1 but also to O-acetylated sialic acids, resulting in increased neurovirulence (Kazi et al., 2005).
Avian Infectious bronchitis virus (IBV) belongs to group 3 coronaviruses. It is of serious economic importance for the poultry industry worldwide, since it affects the respiratory and reproductive tract as well as the renal system of chickens (reviewed by Cavanagh, 2003; Liu & Kong, 2004) causing respiratory disease, reduction in weight-gain and usually life-long decrease of egg laying performance. For this virus, the receptor on cells of its natural host has not yet been elucidated. Recently, it has been reported that feline APN may mediate infection of cultured feline cells by IBV (Miguel et al., 2002). However, this has not been confirmed for chicken cells. IBV also has a sialic acid-binding activity as evidenced by the ability of many strains to agglutinate erythrocytes (Bingham et al., 1975). This haemagglutinating activity is based on the capability of the virus to attach to 2,3-linked sialic acids on the surface of red blood cells (Schultze et al., 1992). The significance of this binding activity for virus infection has not been analysed.
Here, we show that cells become resistant to IBV infection after incubation with neuraminidase (NA). This effect was observed with two strains (Beaudette and M41) and different cell types. IBV was more sensitive to NA treatment than were Influenza A virus (FLUAV) and Sendai virus (SeV). Furthermore, sensitivity of cells to IBV infection was connected to expression of 2,3-linked sialic acids on the cell surface. Our results suggest that sialic acid serves as a receptor determinant for primary attachment of IBV to host cells.
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METHODS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Viruses.
Stock virus of the M41 strain of IBV was obtained by inoculating embryonated specific-pathogen-free (SPF) chicken eggs (Lohmann). Following incubation at 37 °C, the allantoic fluid was collected, clarified by low speed centrifugation and stored at –80 °C. Strains Beaudette-US of IBV, Atue51908 of Bovine respiratory syncytial virus (BRSV) and Z of SeV were propagated in Vero cells. Strain A/sw/Bakum/909/93(H3N2) of FLUAV was propagated in LLC-PK1 cells. Virus-containing supernatants of infected cell cultures were harvested, clarified by low speed centrifugation and stored at –80 °C.
NA treatment and virus infection of cells.
Cells grown on coverslips (12 mm diameter) were washed twice with PBS and incubated with NA from Vibrio cholerae (Dade Behring) or Streptococcus pneumoniae (Sigma-Aldrich) using MES buffer as a diluent. After gentle shaking at 37 °C for 1 h, cells were washed three times with PBS and infected by IBV-Beaudette (105 TCID50 ml–1) or any of the other viruses for 1 h at 37 °C. Following three washes with PBS, cells were incubated with medium at 37 °C. For cells infected with SeV and influenza virus, the medium was supplemented with trypsin (1 mg ml–1). Infected cells were visualized by immunofluorescence.
Cell viability assay.
Vero cells were grown in a 96-well plate. Cells were washed with PBS and incubated for 1 h at 37 °C with different concentrations of NA in MES buffer. Control cells were incubated with MES buffer alone. After a washing step, Cell Proliferation Reagent WST-1 (Roche) diluted 1 : 10 in medium was added to the cells. After incubation for 1 h at 37 °C, the absorbance was measured in an ELISA reader at 450 nm.
Virus infectivity.
Supernatants from IBV-infected cells were collected at 24 h post-infection (p.i.) and titrated on Vero cells grown in 96-well plates. Tenfold dilutions of the supernatants were applied in a volume of 200 µl per well. At 3 days p.i., the cytopathic effect in the monolayer indicated whether the cells had been infected or not by the respective dilutions. The titre was calculated according to Kärber (1931).
Immunofluorescence analysis.
Cells grown on coverslips were infected by the virus indicated. At 24 h p.i., cells were fixed with 3 % paraformaldehyde for 20 min at room temperature (BRSV-infected cells were fixed 48 h p.i.). After incubation with 0·1 M glycine for 5 min, cells were permeabilized by treatment with 0·2 % Triton X-100 for 5 min. For detection of viral antigen, samples were incubated with one of the following antibodies: an antiserum raised in SPF rabbits against IBV-Beaudette; monoclonal antibodies A38 and 124 directed against S and M proteins of IBV-M41, respectively (Mockett et al., 1984); a rabbit antiserum raised against strain WSN of FLUAV (kindly provided by Dr Klenk, Institute for Virology, Philipps-Universität Marburg, Germany); a polyclonal goat antiserum directed against parainfluenza virus 1 (Acris Antibodies); or a monoclonal antibody raised against the respiratory syncytial virus fusion protein (Serotec). For detection of 2,3-linked sialic acids, cells were incubated with Maackia amurensis agglutinin (MAA) labelled with digoxigenin (DIG Glycan Differentiation kit; Roche). Terminal galactose residues were detected by fluorescein isothiocyanate (FITC)-labelled peanut agglutinin (PNA; Sigma). Bound antibodies or DIG-labelled lectins were visualized by FITC-labelled anti-rabbit (Sigma), anti-mouse (Acris), anti-goat (Sigma) or anti-DIG antibodies (Roche).
Antibodies were incubated with cells for 1 h at room temperature followed by three washing steps with PBS. Fluorescent microscopy was performed with a Zeiss Axioplan 2 microscope and photographs were taken using a digital video camera (INTAS focus imager; INTAS).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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, incubation of cells with increasing amounts of enzyme resulted in a corresponding decrease of the yield of infectious virus released into the supernatant. Pre-treatment of the cells with 1 and 20 mU NA was sufficient to reduce the virus titres by 80 and 99 %, respectively. NA treatment was not detrimental to the cells as (i) viability of cells was unaffected by 2 mU NA and reduced only by about 15 % after treatment with 100 mU of enzyme (data not shown) and (ii) replication of BRSV in NA-treated cells was not impaired (reported below). To demonstrate that NA treatment affects an early step in the replication cycle of IBV, we compared the infection of cells incubated either prior to or after the 1 h period of virus adsorption. In an assay where the infected cells were counted after immunostaining, pre-treatment with 50 mU NA resulted in a 77 % reduction of the number of infected cells. By contrast, when the enzyme was added after having washed away the inoculum, the number of infected cells was reduced by only about 23 %. Taken together, these results suggest that sialic acids attached to cell surface components are involved in the initial stage of an IBV infection.
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, in the case of FLUAV, a distinct reduction in the number of infected cells was observed following pre-treatment with 100 mU NA. A comparable reduction in the number of SeV-infected cells was observed at as little as 20 mU of this enzyme. Infection by IBV was the most sensitive to pre-treatment with NA, 1 mU of enzyme being sufficient for a significant decrease in the number of infected cells. Cells shown in Fig. 2 were infected with an m.o.i. of 0·5. Comparable results were obtained when cells were infected with lower infectious doses. At an m.o.i. of 0·01, pre-treatment of Vero cells with 2 or 100 mU NA resulted in a reduction of the number of infected cells by 77 and 95 % in the case of IBV-Beaudette, by 53 and 86 % in the case of SeV and by 19 and 41 % in the case of FLUAV (data not shown).
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), as confirmed herein by immunofluorescence microscopy (Fig. 3, upper panel). Both cell types became resistant to infection after pre-treatment with NA (lower panel). Therefore, the Beaudette strain requires the presence of surface-bound sialic acid not only for infection of heterologous cell cultures but also for infection of cells from its natural host.
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, upper panel). Pre-treatment with NA rendered these cells resistant to infection not only by the Beaudette strain but also by IBV-M41. These results indicate that the sialic acid dependence of IBV infection is a general feature and not restricted to a certain cell type or virus strain.
Importance of 2,3-linked sialic acid for an infection by IBV
Some strains of IBV are able to agglutinate erythrocytes (Bingham et al., 1975). The haemagglutination activity has been shown to depend on 2,3-linked sialic acid present on the surface of erythrocytes (Schultze et al., 1992). To find out whether this linkage type is crucial for initiation of an IBV infection, Vero cells were treated with NA from S. pneumoniae, which has a preference for cleaving 2,3-linked sialic acid compared with 2,6-linked sialic acid. A pre-treatment with 50 mU enzyme for 1 h had the same effect as incubation with the enzyme from V. cholerae, i.e. the cells became resistant to IBV infection (not shown). In agreement with this result, the lectin from Maackia amurensis, which recognizes 2,3-linked sialic acid, bound to both CEK and Vero cells (Fig. 4, upper panel) that are sensitive to IBV-Beaudette infection. Interestingly, a subline of Vero cells, Vero E6, which is used for propagation of SARS-CoV and filoviruses (e.g. Ebola virus), was found to be resistant to IBV infection (Fig. 4, lower panel). This cell line could not be stained by the MAA lectin, indicating that it contains no or only a low amount of surface-bound 2,3-linked sialic acid. This result shows that a cell line containing 2,3-linked sialic acid is sensitive to infection by IBV, whereas a related cell line lacking this sugar type cannot be infected. A similar observation was made with CHO cells. The parental cell line CHO-E6 shows bright fluorescence after staining with the MAA lectin and it can be infected by IBV-Beaudette (Fig. 5, upper panel). A CHO cell line defective in the transport of CMP-sialic acid (CHO-Lec2) lacks surface bound 2,3-linked sialic acid as indicated by its lack of reactivity with the MAA lectin (Fig. 5, lower panel). In contrast, the CHO-Lec2 cells can be stained by PNA, which recognizes galactose residues that are often the penultimate sugars in sialylated oligosaccharides. CHO-Lec2 cells were found to be resistant to infection by IBV-Beaudette. The results shown in Figs 4 and 5 are in agreement with the data obtained previously with erythrocytes, indicating that IBV recognizes 2,3-linked sialic acid. Binding to this type of sugar is important not only for IBV-induced haemagglutination but also for infection of cultured cells.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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2,3-linked sialic acids present on the cell surface play an important role in the initial stage of an IBV infection. Resistance of NA-treated cells to infection by IBV was observed for two strains and four different cell types, indicating that the sialic acid dependence of the IBV infection is a general feature and not restricted to certain cell or virus strains. Preferential binding to 2,3-linked sialic acid has also been reported for avian influenza viruses, whereas human influenza viruses show a preference for 2,6-linked sialic acid (Rogers & Paulson, 1983). We have shown the importance of sialic acids for IBV infection with cultured cells. The initial target of avian influenza viruses and IBV in chicken is the respiratory epithelium. As 2,3-linked sialic acid is used by avian influenza viruses to initiate respiratory infection, it may also be used by IBV for infection of the respiratory tract. IBV, like avian influenza viruses, infects many non-respiratory tissues, including those of the alimentary tract, oviduct and kidney (Casais et al., 2003; Liu & Kong, 2004). In keeping with this we have demonstrated herein that 2,3-linked sialic acid is present on cultured CEK cells, which are susceptible to IBV. The broad distribution of 2,3-linked sialic acid in different organs and species rules out the possibility that this type of sugar is a major determinant of the narrow host tropism of IBV. It is likely that a step in the replication cycle following the attachment to sialylated surface components is responsible for the restriction of infection to avian species.
There are quantitative differences in the amount of sialic acid required for an IBV infection compared with an infection by influenza virus. Incubation with 20 mU NA was sufficient to render cells almost resistant to infection by IBV, whereas no effect on the susceptibility to infection by influenza virus was detectable. This result indicates that smaller amounts of sialic acid on the cell surface are sufficient for influenza virus to initiate an infection, compared with IBV. This finding suggests that influenza virus binds sialic acid with higher affinity than does IBV. The reason for this difference may be related to the fact that influenza viruses contain a receptor-destroying enzyme, whereas IBV lacks a comparable enzyme (Klenk et al., 1955). Binding to a sugar with high affinity renders a virus efficient in finding the target cell. However, a strong binding activity may also be detrimental, when the sialoglycoconjugate recognized by a virus does not serve as a receptor for infection of cells. The mucus layer covering the respiratory epithelium represents a barrier to infection by micro-organisms. Mucins are rich in sialic acid and therefore are bound by influenza viruses. This interaction prevents the virions from infecting the respiratory epithelium. The action of the viral NA inactivates these inhibitors and enables influenza A and B viruses to reach their target cells (Matrosovich et al., 2004). Similarly, the receptor-destroying enzyme of influenza virus is required at the final stage of the replication cycle (Air & Laver, 1989). By removing sialic acids from the viral and cellular surface, the NA of influenza viruses prevents the formation of virus aggregates sticking to the surface of the infected cells. In this way, the viral enzyme facilitates the spread of infection. Viruses that lack a comparable enzyme may avoid the detrimental effects described above by binding to sialic acid with lower affinity. In this way, it is easier to detach from bound sialic acids and to attach to other residues. Such a dynamic process may allow IBV to find the target cells even in the presence of inhibitors such as mucins. Interestingly, mutants of FLUAV have been isolated that lack a functional NA. These viruses have compensated the lack of the enzyme by mutations in the haemagglutinin that lower the binding affinity to sialic acid (Hughes et al., 2000).
Like influenza viruses, most group 2 coronaviruses contain a receptor-destroying enzyme (Vlasak et al., 1988b; Schultze et al., 1991b). Viruses such as Bovine coronavirus (BCoV) resemble FLUCV rather than type A or B influenza viruses, because they recognize 9-O-acetylated sialic acids and contain an acetylesterase as the receptor-destroying enzyme (Herrler et al., 1985; Vlasak et al., 1988b; Schultze et al., 1991b). This esterase releases the 9-O-acetyl group from sialic acid and thus abolishes virus binding to the respective sialoglycoconjugate. Group 1 and 3 coronaviruses lack a comparable enzyme. Among group 1 coronaviruses, a sialic acid-binding activity has been demonstrated for TGEV (Schultze et al., 1996). In addition to sialic acid, TGEV is able to interact with porcine APN. This surface protein functions as a cellular receptor for TGEV (Delmas et al., 1992). Binding to sialic acid increases the efficiency of binding, but it is not an absolute requirement for infection of cultured cells (Schwegmann-Wessels et al., 2002). Mutants or variants of TGEV that have lost the sialic acid-binding activity can be propagated in cultured cells to high titres (Krempl et al., 2000). The interaction with sialic acids appears to be required for the intestinal infection by TGEV. Mutants or variants of TGEV that have lost the sialic acid-binding activity by a single point mutation in the S protein have also lost the enteropathogenicity (Krempl et al., 1997).
IBV is a group 3 coronavirus and takes an intermediate position between group 1 and 2 coronaviruses with respect to receptor interaction. Like TGEV, IBV lacks a receptor-destroying enzyme; on the other hand, it infects cultured cells in a sialic acid-dependent fashion, thus resembling BCoV. Because of the low affinity binding to sialic acid, it is possible that IBV uses sialylated surface components for primary attachment to cells. Successful infection may require the interaction with another receptor to reinforce the attachment process and/or to trigger the transition to the subsequent fusion event between the viral and the cellular membrane. Such an entry strategy has been described for other viruses. Herpes simplex virus uses glycosaminoglycan structures on proteoglycans for primary attachment (reviewed by Compans & Herrler, 2005). Subsequently, viral surface proteins have to interact with surface proteins such as nectin-1 to accomplish virus entry. Similar to the role of porcine APN in TGEV infection, a specific cell surface protein may also be involved in the infection by IBV. Evidence for this has been provided by experiments with recombinant IBVs (Casais et al., 2003; Hodgson et al., 2004; Britton et al., 2005). Whilst the Beaudette strain infects Vero cells productively, the M41 strain does not. Both strains replicate equally well in CEK cells. Replacement of the Beaudette spike protein gene with that of M41 abolished infection of Vero cells, whilst not affecting replication in kidney cells (Casais et al., 2003). Since we have shown herein that both Vero and CEK cells have cell surface 2,3-linked sialic acid, and that this sugar is necessary for infection of CEK cells by both Beaudette and M41, this indicates that a secondary receptor is involved in the attachment process and is necessary for productive infection. Beaudette that has been adapted to growth in Vero cells by multiple passages would seem to be able to use such a secondary receptor at the surface of Vero cells, whilst M41 cannot. Some MHV strains are known to attach not only to CEACAM-1 but also to O-acetylated sialic acid. The additional binding activity affects the cell tropism, resulting in increased neurovirulence (Kazi et al., 2005).
Miguel et al. (2002) have reported that feline APN serves as a receptor for the Ark99 strain of IBV on feline cells. This has not been confirmed for other virus strains and also not for chicken cells. Whether APN or another receptor protein is involved in IBV infection of chicken remains to be explored in future experiments. Such a protein might be a determinant for the host tropism of IBV. Primary attachment to surface-bound sialic acids would help the virus to get into contact with this putative receptor.
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ACKNOWLEDGEMENTS |
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Received 1 November 2005;
accepted 25 January 2006.
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