Abstract
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 wild-type 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, 2002; Hsu 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). Recently we demonstrated that this induction of SLAM is due to the interaction of wild-type MV with the Toll-like receptor 2, which is not a receptor for uptake of MV (Bieback et al., 2002).
Several observations with epitheloid cell lines such as the African green monkey kidney cell line Vero suggest the presence of additional uptake mechanisms or unknown receptors on such cells (Hashimoto et al., 2002; Koumomou & Wild, 2002; Nielsen et al., 2001; Takeuchi et al., 2002). We recently demonstrated that most wild-type MV and recombinant viruses expressing the envelope haemagglutinin (H) and fusion (F) proteins of these strains do not use CD46 as a receptor (Erlenhoefer et al., 2002); however, they can infect SLAM-negative Vero and Hela cells (Johnston et al., 1999), which supports the suggestion of CD46- and SLAM-independent virus uptake. Here we have demonstrated that primary human umbilical vein endothelial cells (HUVECs) and transformed human brain microvascular endothelial cells (HBMECs) do not express SLAM, either with and without treatment with inflammatory cytokines or MV. Since certain wild-type MV strains can use CD46 as a low-affinity receptor on the surface of lymphoid cells (Manchester et al., 2000), we assessed whether CD46 might be involved in virus uptake by ECs. We found that, in the absence of SLAM and in the presence of CD46-blocking antibodies, wild-type MV could effectively infect ECs, suggesting the presence of an additional non-CD46/non-SLAM cellular receptor(s) for MV.
Endothelial cell isolation and culture.HUVECs were prepared from umbilical cords obtained from the maternity ward of the University Hospital, Würzburg, as previously described (Marin et al., 2001). HUVECs were cultivated in M199 medium (Gibco) containing 25 mM HEPES, 20 % foetal calf serum (FCS; Biochrom), 5 U heparin ml-1, 30 µg endothelial cell growth supplement (ECGS; Sigma) ml-1 and 100 U penicillin/streptomycin ml-1. SV40 large T antigen-transformed HBMECs (Stins et al., 1997) were grown in RPMI 1640 medium (Gibco) containing 25 mM HEPES, GlutaMAX I (Gibco), 10 % FCS, 10 % NuSerum IV (Becton Dickinson), 1 % non-essential amino acids, 1 % vitamins, 1 mM sodium pyruvate, 5 U heparin ml-1, 30 µg ECGS ml-1 and 100 U penicillin/streptomycin ml-1. HUVECs were used up to passage 2 and HBMECs at passages 1620. For both endothelial cell types, the surface of the plastic dish was coated with 0·5 % gelatin (Sigma). The purity of the cell cultures was confirmed by staining with the lectin Ulex europaeus agglutinin 1 (Vector) and antibodies to von Willebrand factor or E-selectin (Pharmingen) after treatment of the cells with TNF-α for 6 h. Cells were regularly tested for mycoplasma using a PCR-based test kit (Sigma). Recombinant interleukin-1β (IL-1β) for the stimulation of ECs was used at a concentration of 1000 U ml-1, TNF-α at 100 U ml-1 (Strathmann), IFN-γ at 100 U ml-1 and bacterial lipopolysaccharide (LPS) at 1 µg ml-1 (Sigma).
Virus strains and antibodies.
MVs used in this study were the vaccine-like strain Edmonston (Edm) and the wild-type strains WTFb, Wü4797 (Würzburg.DEU/96/4797) and Wü5679 (Würzburg.DEU/98/5679; Erlenhoefer et al., 2002). For further details see Table 1. Edm was amplified using Vero cells and the wild-type strains using the human EpsteinBarr virus (EBV)-transformed B cell line BJAB, which does not produce EBV. Titres of all viruses were determined using the monkey EBV-transformed B cell line B95a (Kobune et al., 1990).
Table 1. Measles viruses used in this study
The anti-SLAM monoclonal antibodies (mAbs) IPO-3 and A12 were obtained from Kamiya Biomedicals and Pharmingen. The following mouse mAbs were grown and purified using protein G columns in our laboratory: anti-SLAM clone 5C6, anti-CD46 clones B97 and 13/42, anti-MV H clone K83 and anti-MV nucleocapsid (N) clone F227. Secondary FITC-conjugated goat anti-mouse and swine anti-human IgG antibodies and Alexa Fluor 488-conjugated goat anti-mouse IgG antibodies were obtained from DAKO and Molecular Probes.
Immunohistochemistry and infection inhibition assay.
For immunohistochemistry, four- or eight-chamber glass slides (Nunc) were coated with 0·5 % gelatin and 2 % glutardialdehyde and washed three times with PBS prior to seeding of the cells. Cells were fixed for 7 min with 3·7 % paraformaldehyde and permeabilized for 10 min with 0·25 % Triton X-100. Non-specific antibody binding was blocked by incubation with 10 % FCS for 45 min at 4 °C. MV infection was detected using mAb F227 to MV N (2 µg ml-1) and goat anti-mouse IgG Alexa Fluor 488-conjugated secondary antibody (Molecular Probes). Cell nuclei were stained using DAPI nucleic acid stain (Molecular Probes).
For the infection inhibition assay, cells were incubated prior to infection with mAbs to CD46 at given concentrations at 37 °C for 1 h, infected at an m.o.i. of 0·1 with MV for 1 h, washed once with PBS and further incubated in culture medium supplemented with antibody for 2 days. MV was visualized using a human MV-specific hyperimmune serum of a SSPE patient and secondary FITC-conjugated swine anti-human antibodies.
RT-PCR.
Total cellular RNA was isolated using the GeneElute Mammalian Total RNA kit (Sigma). Reverse transcription was primed with oligo(dT) primers and carried out using SuperScript II RNase H-free reverse transcriptase (Gibco). The PCR primers were: SLAM, forward 5'-CTCCTCATTGGCTGATGGATCC-3', reverse 5'-TTTATGAGCAGGTCTCCACTCC-3'; CD46, forward 5'-TCGATACATATGGAGCCTCCCG-3', reverse 5'-CTAGGCCTACTTACAAGCCTCC-3'; β-actin, forward 5'-TGACGGGGTCACCCACACTGTGCCC-3', reverse 5'-CTAGAAGCATTTGCGGTGGACGAT-3' and TLR2, forward 5'-GCCAAAGTCTTGATTGATTGG-3', reverse 5'-TTGAAGTTCTCCAGCTCCTG-3'. For the PCR, Ready To Go PCR beads (Amersham Pharmacia) were used.
Virus binding assay.
Cells (5x104) were incubated in 100 µl PBS at 37 °C for 1 h with viruses at a given m.o.i., washed with FACS buffer (Ca2+/Mg2+-free PBS containing 0·4 % BSA and 0·02 % sodium azide) and stained with mAb K83 against MV H and FITC-conjugated goat anti-mouse antibodies. Bound virus was determined by analysis with a FACScan (Becton Dickinson).
Staining of HUVECs and HBMECs with mAbs to CD46 and analysis by flow cytometry revealed a strong surface expression of CD46 by almost 100 % of the ECs (Fig. 1). In contrast, both HUVECs and HBMECs were negative after staining with the SLAM-specific mAbs IPO-3, A12 and 5C6. As a positive control for SLAM staining, we used B95a cells (Fig. 1G). Corresponding results were found by assessing SLAM expression by RT-PCR (Fig. 1HJ).
|
LPS and MV wild-type particles can activate cells via the Toll-like receptor 2 (TLR2) (Bieback et al., 2002). Therefore, we assessed the expression of TLR2 by HUVECs and HBMECs by RT-PCR. Both cell lines expressed TLR2 mRNA (Fig. 1K). Since it is possible that SLAM expression might be induced in activated ECs, as found for dendritic cells (Kruse et al., 2001) and monocytes (Bieback et al., 2002; Minagawa et al., 2001), we treated HUVECs and HBMECs with LPS, IL-1β, TNF-α and UV-inactivated wild-type MV. None of the treatments induced the expression of SLAM mRNA or surface protein in HUVECs and HBMECs (shown for IL-1β in Fig. 1C, F), whereas typical markers, such as E-selectin on both EC lines after TNF treatment and MHC class II on HUVECs after IFN-γ treatment, were induced (not shown). Also, infection of HUVECs and HBMECs with MV did not induce the expression of SLAM (not shown).
Analysis of virus binding to and infection of HUVECs and HBMECs
As the first step of the infection cycle, MV binds to its cellular receptors. The amount of bound virus can be taken as an indicator of the presence of receptors on the cell surface. We therefore analysed the binding capacity of ECs for CD46-utilizing and non-utilizing MV strains. Viruses corresponding to m.o.i.s of 1, 2·5 and 5 (titrated using B95a cells) were incubated with HUVECs and HBMECs for 1 h and viral envelope proteins present on the cell surface were quantified by flow cytometry. The vaccine strain Edm, as expected, bound very efficiently to a high percentage of HUVECs and HBMECs because of its high affinity to CD46 (Fig. 2). In contrast, the wild-type strains WTFb, Wü4797 and Wü5679 bound to only a fraction of the cells. Interestingly, the efficiency of virus binding varied substantially between the wild-type strains. Reproducibly more HUVECs and HBMECs bound strain Wü4797 (up to 40 and 60 %, respectively) than the other two wild-type strains, WTFb and Wü5679 (up to 15 and 20 %, respectively).
|
Binding data may reflect the presence of receptors on the EC surface but not necessarily the efficiency of infection of the cells. We therefore analysed the infectivity of the viral strains, which had all been titrated using B95a cells, for HUVECs and HBMECs. Cells were infected at an m.o.i. of 0·5 with Edm and the three wild-type viruses and incubated for up to 6 days. The expression of MV H on the cell surface was analysed by flow cytometry (Fig. 3). The expression of MV N in permeabilized cells was analysed by microscopy in a similar experiment after infection of cells at an m.o.i. of 0·1 (Fig. 4). All wild-type strains infected ECs with a reduced efficiency compared with the CD46-using strain Edm. To our surprise, we observed great differences in virus spread among the wild-type strains. The most pronounced infection was observed with wild-type strain Wü4797 in HUVECs. Wü4797 spread slowly but constantly in the culture (up to 60 % infection at day 6 p.i.), while strains WTFb and Wü5679 infected only approximately 20 % of the cells (Figs 3 and 4).
|
|
Infection inhibition assay with anti-CD46 antibodies
To investigate which MV strains can use CD46 on the surface of ECs as receptor, we performed an infection inhibition assay with antibodies that block the virusCD46 interaction by binding to the short consensus repeat domain 1 of CD46. As a control, we used anti-CD9 antibodies, which bind to the cell surface but do not interfere with MV infection (not shown). Infection of HUVECs and HBMECs with MV strain Edm was specifically inhibited by CD46 domain 1 antibodies (Fig. 5). In contrast, infection of cells with wild-type MV strains was not affected by the antibodies used. These data indicate a CD46-independent virus uptake of the MV wild-type strains.
|
CD46 modulation
A further test for high-affinity MV receptor interaction is receptor modulation. We and others have demonstrated previously that vaccine and laboratory strains effectively modulate CD46 (Krantic et al., 1995; Naniche et al., 1993b; Schneider-Schaulies et al., 1995a, b, 1996) and that MV wild-type strains modulate SLAM on the surface of infected cells and after contact of the cells with viral glycoproteins (Erlenhoefer et al., 2001; Tanaka et al., 2002). We infected HUVECs and HBMECs with MV strains Edm and the wild-type strains (m.o.i.=0·1) for 3 days and determined the CD46 and MV H expression by double staining and flow cytometry. The CD46 expression was evaluated by comparing the CD46-specific signals on cells of infected cultures with uninfected cultures (Fig. 6). Infection of cells with Edm led to a reduction in the CD46 signal of 2540 % depending on the target cell, whereas infection with the wild-type strains WTFb, Wü4797 and Wü5679 did not lead to a reduction in the CD46 signal.
|
Monocytes/macrophages have previously been described as not expressing SLAM. However, it was recently found that activation of PBMCs with phytohaemagglutinin, LPS or MV particles leads to the induction of SLAM on CD14-positive cells (Minagawa et al., 2001). Interestingly, not only infection with MV but also UV-inactivated MV induced SLAM on such cells (Minagawa et al., 2001). The basis for this observation was recently elucidated when we found that wild-type MV interacts with TLR2, an interaction that induces intracellular signalling via the transcription factor NF-κB and the expression of SLAM (Bieback et al., 2002). While mediating the activation of monocytes by MV, TLR2 is not an entry receptor for the virus (Bieback et al., 2002). Since ECs also express TLRs, which can be enhanced by LPS and IFN-γ (Faure et al., 2001), we asked whether treatment of the ECs with the TLR agonists LPS or MV could lead to the induction of SLAM. However, SLAM remained non-inducible on HUVECs and HBMECs.
In order to exclude a role for CD46 in the uptake of wild-type MV, we used strains that have been demonstrated to be unable to use CD46 as a receptor on the surface of transfected Chinese hamster ovary (CHO) cells (Erlenhoefer et al., 2002) and applied anti-CD46 antibodies to inhibit a potential interaction of wild-type MVs with this receptor on human ECs. The results indicated that MV wild-types can infect ECs in a CD46- and SLAM-independent manner. Receptor-independent mechanisms of virus spread, possibly as microfusion events at synapses, might circumvent the necessity for specific receptors for MV in the brain (Allen et al., 1996; Duprex et al., 1999; Lawrence et al., 2000; McQuaid et al., 1998; Meissner & Koschel, 1995; Urbanska et al., 1997), where CD46 is present on only a small proportion of cells and SLAM is not expressed (McQuaid & Cosby, 2002; Ogata et al., 1997). These findings are valid for virus spread in neurons in the brain, but not for infection of tissue culture cells with cell-free virus. The uptake of virus by ECs in tissue culture was relatively effective, which supports the assumption of a receptor-mediated process. Our data therefore suggest the presence of an additional unknown cellular receptor for MV on ECs. Our findings do not rule out the possibility that vaccine strains such as Edm may also use this additional receptor. We suggest this since, in the case of SLAM- and CD46-positive lymphocytes, virus attachment and infection with Edm can be blocked efficiently by antibodies to CD46, although Edm can also use the common MV receptor SLAM on cells in the absence of CD46 (Erlenhoefer et al., 2001, 2002). The molecular basis for this finding is not known.
It currently remains unclear why certain wild-type strains spread better on HUVECs than others. Various evidence has been accumulated indicating that subtle differences in the envelope proteins of MV can play a role in altering the tropism, virus uptake, cell-to-cell fusion and pathogenicity (Bartz et al., 1996; Bieback et al., 2002; Hsu et al., 1998; Johnston et al., 1999; Lecouturier et al., 1996; Moeller et al., 2001; Moll et al., 2001; Ohgimoto et al., 2001; Plemper et al., 2002; Shibahara et al., 1994; Takeuchi et al., 2002). To investigate the molecular basis for the differential spread of MV wild-types in cultures of HUVECs, we will further analyse the sequences of the envelope genes of the MV wild-types and intend functional studies with corresponding recombinant viruses.
We thank Dr H. W. Kreth and Dr R. Nanan, for helpful discussions, Dr D. Drenckhahn for helping to establish the primary endothelial cellculture, F. Dimpfel and S. Löffler for technical assistance and the Deutsche Forschungsgemeinschaft for financial support.References
Bartz, R., Brinckmann, U., Dunster, L. M., Rima, B., Ter Meulen, V. & Schneider-Schaulies, J. (1996). Mapping amino acids of the measles virus hemagglutinin responsible for receptor (CD46) downregulation. Virology 224, 334337.[CrossRef][Medline]
Bieback, K., Lien, E., Klagge, I. & 7 other authors (2002). The hemagglutinin protein of wildtype measles virus activates Toll-like receptor 2 signaling. J Virol 76, 87298736.
Cocks, B. G., Chang, C.-C. J., Carballido, J. M., Yssel, H., de Vries, J. E. & Aversa, G. (1995). A novel receptor involved in T-cell activation. Nature 376, 260263.[CrossRef][Medline]
Cosby, S. L. & Brankin, B. (1995). Measles virus infection of cerebral endothelial cells and effect on their adhesive properties. Vet Microbiol 44, 135139.[CrossRef][Medline]
Dörig, R. E., Marcil, A., Chopra, A. & Richardson, C. D. (1993). The human CD46 molecule is a receptor for measles virus (Edmonston strain). Cell 75, 295305.[CrossRef][Medline]
Duprex, W. P., McQuaid, S., Hangartner, L., Billeter, M. A. & Rima, B. K. (1999). Observation of measles virus cell-to-cell spread in astrocytoma cells by using a green fluorescent protein-expressing recombinant virus. J Virol 73, 95689575.
Erlenhoefer, C., Wurzer, W. J., Löffler, S., Schneider-Schaulies, S., ter Meulen, V. & Schneider-Schaulies, J. (2001). CD150 (SLAM) is a receptor for measles virus, but is not involved in viral contact-mediated proliferation inhibition. J Virol 75, 44994505.
Erlenhoefer, C., Duprex, W. P., Rima, B. K., ter Meulen, V. & Schneider-Schaulies, J. (2002). Analysis of receptor (CD46, CD150) usage by measles virus. J Gen Virol 83, 14311436.
Esolen, L. M., Takahashi, K., Johnson, R. T., Vaisberg, A., Moench, T. R., Wesselingh, S. L. & Griffin, D. E. (1995). Brain endothelial cell infection in children with acute fatal measles. J Clin Invest 96, 24782481.
Faure, E., Thomas, L., Xu, H., Medvedev, A. E., Equils, O. & Arditi, M. (2001). Bacterial lipopolysaccharide and IFN-γ induce Toll-like receptor 2 and Toll-like receptor 4 expression in human endothelial cells: role of NF-kB activation. J Immunol 166, 20182024.
Friedman, H. M., Macarak, E. J., MacGregor, R. R., Wolfe, J. & Kefalides, N. A. (1981). Virus infection of endothelial cells. J Infect Dis 143, 266273.[Medline]
Griffin, D. E. & Bellini, W. J. (1996). Measles virus. In Fields Virology, 3rd edn, pp. 12671312. Edited by B. N. Fields, D. M. Knipe & P. M. Howley. Philadelphia: LippincottRaven.
Harcourt, B. H., Rota, P. R., Hummel, K. B., Bellini, W. J. & Offermann, M. K. (1999). Induction of intercellular adhesion molecule 1 gene expression by measles virus in human umbilical vein endothelial cells. J Med Virol 57, 916.[CrossRef][Medline]
Hashimoto, K., Ono, N., Tatsuo, H., Minagawa, H., Takeda, M., Takeuchi, K. & Yanagi, Y. (2002). SLAM (CD150)-independent measles virus entry as revealed by recombinant virus expressing green fluorescent protein. J Virol 76, 67436749.
Hsu, E. C., Sarangi, F., Iorio, C. & 7 other authors (1998). A single amino acid change in the hemagglutinin protein of measles virus determines its ability to bind CD46 and reveals another receptor on marmoset B cells. J Virol 72, 29052916.
Hsu, E. C., Iorio, C., Sarangi, F., Khine, A. A. & Richardson, C. D. (2001). CDw150(SLAM) is a receptor for a lymphotropic strain of measles virus and may account for the immunosuppressive properties of this virus. Virology 279, 921.[CrossRef][Medline]
Isaacson, S. H., Asher, D. M., Godec, M. S., Gibbs, C. J. & Gajdusek, D. C. (1996). Widespread, restricted low-level measles virus infection of brain in a case of subacute sclerosing panencephalitis. Acta Neuropathol 91, 135139.[CrossRef][Medline]
Johnston, I. C. D., ter Meulen, V., Schneider-Schaulies, J. & Schneider-Schaulies, S. (1999). A recombinant measles vaccine virus expressing wild-type glycoproteins: consequences for viral spread and cell tropism. J Virol 73, 69036915.
Kimura, A., Tosaka, K. & Nakao, T. (1975). Measles rash I. Light and electron microscopic study of skin eruptions. Arch Virol 47, 295307.[CrossRef][Medline]
Kirk, J., Zhou, A. L., McQuaid, S., Cosby, S. L. & Allen, I. V. (1991). Cerebral endothelial cell infection by measles virus in subacute sclerosing panencephalitis: ultrastructural and in situ hybridization evidence. Neuropathol Appl Neurobiol 17, 289297.[Medline]
Kobune, F., Sakata, H. & Sugiura, A. (1990). Marmoset lymphoblastoid cell as a sensitive host for isolation of measles virus. J Virol 64, 700705.
Koumomou, D. W. & Wild, T. F. (2002). Adaptation of wild-type measles virus to tissue culture. J Virol 76, 15051509.
Krantic, S., Gimenez, C. & Rabourdin-Combe, C. (1995). Cell-to-cell contact via measles virus haemagglutininCD46 interaction triggers CD46 downregulation. J Gen Virol 76, 27932800.
Kruse, M., Meinl, E., Henning, G., Kuhnt, C., Berchtold, S., Berger, T., Schuler, G. & Steinkasserer, A. (2001). Signaling lymphocytic activation molecule is expressed on mature CD83+ dendritic cells and is up-regulated by IL-1b. J Immunol 167, 19891995.
Lawrence, D. M. P., Patterson, C. E., Gales, T. L., D'Orazio, J. L., Vaughn, M. M. & Rall, G. F. (2000). Measles virus spread between neurons requires cell contact but not CD46 expression, syncytium formation, or extracellular virus production. J Virol 74, 19081918.
Lecouturier, V., Fayolle, J., Caballero, M., Carabana, J., Celma, M. L., Fernandez-Munoz, R., Wild, T. F. & Buckland, R. (1996). Identification of two amino acids in the hemagglutinin glycoprotein of measles virus (MV) that govern hemadsorption, HeLa cell fusion, and CD46 downregulation: phenotypic markers that differentiate vaccine and wild-type MV strains. J Virol 70, 42004204.[Abstract]
McQuaid, S. & Cosby, S. L. (2002). An immunohistochemical study of the distribution of the measles virus receptors, CD46 and SLAM, in normal human tissues and subacute sclerosing panencephalitis. Lab Investig 82, 17.
McQuaid, S., Campbell, S., Wallace, I. J., Kirk, J. & Cosby, S. L. (1998). Measles virus infection and replication in undifferentiated and differentiated human neuronal cells in culture. J Virol 72, 52455250.
Manchester, M., Eto, D. S., Valsamakis, A., Liton, P. B., Fernandez-Munoz, R., Rota, P. A., Bellini, W. J., Forthal, D. N. & Oldstone, M. B. A. (2000). Clinical isolates of measles virus use CD46 as a cellular receptor. J Virol 74, 39673974.
Marin, V., Kaplanski, G., Grès, S., Farnarier, C. & Bongrand, P. (2001). Endothelial cell culture: protocol to obtain and cultivate human umbilical endothelial cells. J Immunol Methods 254, 183190.[CrossRef][Medline]
Meissner, N. N. & Koschel, K. (1995). Downregulation of endothelin receptor mRNA synthesis in C6 rat astrocytoma cells by persistent measles virus and canine distemper virus infections. J Virol 69, 51915194.[Abstract]
Minagawa, H., Tanaka, K., Ono, N., Tatsuo, H. & Yanagi, Y. (2001). Induction of the measles virus receptor SLAM (CD150) on monocytes. J Gen Virol 82, 29132917.
Moeller, K., Duffy, I., Duprex, P. & 7 other authors (2001). Recombinant measles viruses expressing altered hemagglutinin (H) genes: functional separation of mutations determining H antibody escape from neurovirulence. J Virol 75, 76127620.
Moench, T. R., Griffin, D. E., Obriecht, C. R., Vaisberg, A. J. & Johnson, R. T. (1988). Acute measles in patients with and without neurological involvement: distribution of measles virus antigen and RNA. J Infect Dis 158, 433442.[Medline]
Moll, M., Klenk, H.-D., Herrlerr, G. & Maisner, A. (2001). A single amino acid change in the cytoplasmic domains of measles virus glycoproteins H and F alters targeting, endocytosis, and cell fusion in polarized MadinDarby canine kidney cells. J Biol Chem 276, 1788717894.
Naniche, D., Varior-Krishnan, G., Cervoni, F., Wild, T. F., Rossi, B., Rabourdin-Combe, C. & Gerlier, D. (1993a). Human membrane cofactor protein (CD46) acts as a cellular receptor for measles virus. J Virol 67, 60256032.
Naniche, D., Wild, T. F., Rabourdin-Combe, C. & Gerlier, D. (1993b). Measles virus haemagglutinin induces down-regulation of gp57/67, a molecule involved in virus binding. J Gen Virol 74, 10731079.
Nielsen, L., Blixenkrone-Moller, M., Thylstrup, M., Hansen, N. J. V. & Bolt, G. (2001). Adaptation of wild-type measles virus to CD46 receptor usage. Arch Virol 146, 197208.[CrossRef][Medline]
Ogata, A., Czub, S., Ogata, S., Cosby, S. L., McQuaid, S., Budka, H., ter Meulen, V. & Schneider-Schaulies, J. (1997). Absence of measles virus receptor (CD46) in lesions of subacute sclerosing panencephalitis brains. Acta Neuropathol 94, 444449.[CrossRef][Medline]
Ohgimoto, S., Ohgimoto, K., Niewiesk, S. & 7 other authors (2001). The hemagglutinin protein is an important determinant for measles virus tropism for dendritic cells in vitro and immunosuppression in vivo. J Gen Virol 82, 18351844.
Ono, N., Tatsuo, H., Hidaka, Y., Aoki, T., Minagawa, H. & Yanagi, Y. (2001a). Measles virus on throat swabs from measles patients use signalling lymphocytic activation molecule (CDw150) but not CD46 as a cellular receptor. J Virol 75, 43994401.
Ono, N., Tatsuo, H., Tanaka, K., Minagawa, H. & Yanagi, Y. (2001b). V domain of human SLAM (CDw150) is essential for its function as a measles virus receptor. J Virol 75, 15941600.
Plemper, R., Hammond, A. L., Gerlier, D., Fielding, A. K. & Cattaneo, R. (2002). Strength of envelope protein interaction modulates cytopathicity of measles virus. J Virol 76, 50515061.
Polacino, P. S., Pinchuk, L. M., Sidorenko, S. P. & Clark, E. A. (1996). Immunodeficiency virus cDNA synthesis in resting T lymphocytes is regulated by T cell activation signals and dendritic cells. J Med Primatol 25, 201209.[Medline]
Punnonen, J., Cocks, B. G., Carballido, J. M., Bennett, B., Peterson, D., Aversa, G. & de Vries, J. (1997). Soluble and membrane-bound forms of signalling lymphocytic activation molecule (SLAM) induce proliferation and Ig synthesis by activated human B lymphocytes. J Exp Med 185, 9931004.
Schneider-Schaulies, J., Dunster, L. M., Kobune, F., Rima, B. & ter Meulen, V. (1995a). Differential downregulation of CD46 by measles virus strains. J Virol 69, 72577259.[Abstract]
Schneider-Schaulies, J., Schnorr, J. J., Brinckmann, U., Dunster, L. M., Baczko, K., Liebert, U. G., Schneider-Schaulies, S. & ter Meulen, V. (1995b). Receptor usage and differential downregulation of CD46 by measles virus wild-type and vaccine strains. Proc Natl Acad Sci U S A 92, 39433947.
Schneider-Schaulies, J., Schnorr, J. J., Schlender, J., Dunster, L. M., Schneider-Schaulies, S. & ter Meulen, V. (1996). Receptor (CD46) modulation and complement-mediated lysis of uninfected cells after contact with measles virus-infected cells. J Virol 70, 255263.[Abstract]
Shibahara, K., Hotta, H., Katayama, Y. & Homma, M. (1994). Increased binding activity of measles virus to monkey red blood cells after long-term passage in Vero cell cultures. J Gen Virol 75, 35113516.
Soilu-Hanninen, M., Hanninen, A., Ilonen, J., Salmi, A. & Salonen, R. (1996). Measles virus hemagglutinin mediates monocyte aggregation and increased adherence to measles-infected endothelial cells. Med Microbiol Immunol 185, 7380.[CrossRef][Medline]
Stins, F. M., Gilles, F. & Kim, K. S. (1997). Selective expression of adhesion molecules on human brain microvascular endothelial cells. J Neuroimmunol 76, 8190.[CrossRef][Medline]
Takeuchi, K., Takeda, M., Miyajima, N., Kobune, F., Tanabyashi, K. & Tashiro, M. (2002). Recombinant wild-type and Edmonston strain measles viruses bearing heterologous H proteins: role of H protein in cell fusion and host cell specificity. J Virol 76, 48914900.
Tanaka, K., Minagawa, H., Xie, M.-F. & Yanagi, Y. (2002). The measles virus hemagglutinin downregulates the cellular receptor SLAM (CD150). Arch Virol 147, 195203.[CrossRef][Medline]
Tatsuo, H., Ono, N., Tanaka, K. & Yanagi, Y. (2000). SLAM (CDw150) is a cellular receptor for measles virus. Nature 406, 893897.[CrossRef][Medline]
Urbanska, E. M., Chambers, B. J., Ljunggren, H. G., Norrby, E. & Kristensson, K. (1997). Spread of measles virus through axonal pathways into limbic structures in the brain of Tab -/- mice. J Med Virol 52, 362369.[CrossRef][Medline]
Received 4 October 2002; accepted 16 December 2002.