1 Department of Virology, Osaka City University Medical School, Asahimachi, Abeno-ku, Osaka 545-8585, Japan
2 Department of Pediatrics, Osaka City University Medical School, Asahimachi, Abeno-ku, Osaka 545-8585, Japan
3 Department of Immunology, Osaka Medical Center for Cancer and Cardiovascular Diseases, Osaka 537-8511, Japan
4 Department of Virology, Graduate School of Medical Sciences, Kyushu University, Fukuoka 812-8582, Japan
Correspondence
Hisashi Ogura
ogurah{at}med.osaka-cu.ac.jp
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ABSTRACT |
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INTRODUCTION |
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In contrast to the MV strains obtained from patients with acute measles, little is known about the cellular receptors used by defective variants of MV isolated from the brains of patients with subacute sclerosing panencephalitis (SSPE). These viruses have been isolated by cocultivation of brain cells with nonlymphatic cells, such as Vero (Doi et al., 1972; Kratzsch et al., 1977
; Makino et al., 1977
; Ogura et al., 1997
; Homma et al., 1982
), BSC-1 (Burnstein et al., 1974
) and human embryonic lung cells (Ueda et al., 1975
). Isolation of virus from brain tissue is usually problematic because of the limited quantity of biopsy specimens, poor quality of postmortem tissue and restricted expression of viral mRNAs and proteins in infected brains (Baczko et al., 1986
; Liebert et al., 1986
; Cattaneo et al., 1987
; Sidhu et al., 1994
). However, despite these difficulties, viruses have been isolated successfully from three cases of SSPE. Recovery of virus was more efficient in Vero cells than in B95a cells (Ogura et al., 1997
), suggesting that Vero cells express a host molecule(s) that makes them suitable for growth of SSPE strains of MV. Although the receptor-independent spread of MV in the central nervous system is proposed (Lawrence et al., 2000
), the entry receptor for MV is potentially one of the most important factors in the neurotropism and subsequent pathogenesis of SSPE. Recent studies have presented evidence supporting a role for CD46 as the receptor for MV in the brain (Buchholz et al., 1996
; Ogata et al., 1997
). Since neither Vero nor neural cells display SLAM, CD46 is a logical candidate for the SSPE strain entry receptor. However, the haemagglutinin (H) protein derived from SSPE strains does not adsorb to African green monkey erythrocytes, indicating the absence of an interaction between the SSPE H protein and CD46 (Furukawa et al., 2001
). Adaptation of the MV H protein to CD46 receptor use in cell culture could be achieved by substitution of tyrosine for asparagine at position 481 (Nielsen et al., 2001
) or substitution of glycine for serine at position 546 (Shibahara et al., 1994
; Furukawa et al., 2001
; Li & Qi, 2002
; K. Furukawa, unpublished observation). Our sequence analysis of the H genes of the Osaka-1, Osaka-2, Osaka-3 SSPE strains, including sibling viruses isolated in either B95a or Vero cells, revealed that there were no substitutions at positions 481 and 546, even after serial passage in Vero cells (Furukawa et al., 2001
). In addition, H protein sequences from Vero cell isolate Osaka-2/Fr/V and B95a cell isolate Osaka-2/Fr/B of the Osaka-2 strain, as well as the Vero cell isolate Osaka-3/Bs/V and B95a cell isolate Osaka-3/Bs/B of the Osaka-3 strain, were identical between the two sibling viruses (Furukawa et al., 2001
). The H genes from the Osaka-2/Fr/V, Osaka-2/Fr/B, Osaka-3/Bs/V and Osaka-3/Bs/B strains of MV were cloned into plasmids. After transfection of Vero cells, the H proteins were expressed on the cell surface and, in combination with the fusion (F) protein, syncytia were formed (Furukawa et al., 2001
; K. Furukawa, unpublished observation; M. Ayata, unpublished observation). Therefore, adaptation by changes in nucleotide and amino acid sequence of envelope glycoproteins cannot be the reason that the SSPE strains of MV replicate in Vero cells.
SSPE strains of MV are highly cell-associated and cell-free virions are not usually produced. These viruses replicate and spread from cell to cell by forming syncytia in Vero cells. The cell tropism of SSPE strains has not been studied because of the problems inherent in culturing SSPE strains in vitro. We have used cell-free virus-like particles, prepared by treating cells infected with MVs from patients with SSPE with cytochalasin D, to study the tropism of particles that resulted in syncytia formation on either Vero or B95a cells (Ito et al., 2002; H. Ishida, unpublished observation). Large syncytia developed after infection of both Vero and B95a cells, indicating the existence of host molecules on both cells suitable for infection and growth of SSPE strains of MV.
In this study, we have analysed the receptor use by SSPE strains of MV using the vesicular stomatitis virus (VSV) pseudotype system. The VSV pseudotype system allowed us to eliminate the internal host factors involved in virus replication that might affect cell tropism and to focus on the interaction between SSPE glycoproteins and candidate receptor molecules.
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METHODS |
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Ninety-six-well microtitre plates seeded with 2x104 adherent cells or 4x104 lymphoid cells were used for titrations, as described previously (Tatsuo et al., 2000a). At 24 h after infection, the number of GFP-expressing cells was counted using a fluorescence microscope and results were expressed as infectious units ml-1 of pseudotype virus stock. When suspension cultures were used for the assay, cells were dispersed by gentle pipetting before positive cells were counted.
Antibodies, FIP and entry blocking experiments.
IPO-3 to human SLAM (Sidorenko & Clark, 1993) was from Kamiya Biomedical. The manufacturer specifies that IPO-3 cross-reacts with the homologous molecule on lymphocytes from African green monkeys. M177 or M160 recognizes the short consensus repeat (SCR) 2 or SCR3 domain of human CD46, respectively (Seya et al., 1995
). The L77 neutralizing mAb against the MV H protein was a gift from V. ter Meulen (Institute of Virology and Immunology, University of Wurzburg, Germany). Cells were dispensed in 100 µl volumes to 96-well microplates and cultured overnight. Either antibody or FIP was added to culture wells to a final concentration of 40 or 50 µg ml-1, respectively, and, after 1 h of incubation, 50 µl of serially diluted virus stock was added to the culture. GFP-positive cells were counted 24 h later.
Flow cytometry analysis.
Cells were incubated with primary antibodies IPO-3, M177, M160 or L77, followed by staining with FITC-labelled goat anti-mouse IgG. Stained cells were analysed on a FACScan machine (Becton Dickinson). Since the CD46 homologue on B95a cells is structurally different from human CD46, it was detected by M160 antibody but not M177 (Murakami et al., 1998).
Chemical modification of cells.
To treat cell surface proteins, Vero or SK-N-SH cells were washed twice with serum-free medium and incubated with pronase (Sigma), trypsin (Sigma) or chymotrypsin (Sigma) in serum-free medium at 37 °C for 20 min. To treat carbohydrates, cells were incubated with NaIO4 (Sigma) or neuraminidase from Vibrio cholerae (Sigma) in serum-free medium at 37 °C for 1 h. For tunicamycin (Sigma) treatment, cells were incubated with the drug in complete medium at 37 °C for 8 h. Treated cells were washed twice with serum-free medium, incubated with pseudotype viruses for 1 h, washed twice again and then replenished with fresh complete medium. After 24 h of incubation, GFP-positive virus-infected cells were counted.
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RESULTS |
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To confirm the specificity of the entry through the receptor further, we used mAbs against both SLAM (IPO-3) and CD46 (M177 and M160). M177, but not M160, will block MV receptor activity (Seya et al., 1995). Optimal conditions for antibody blocking of virus entry were determined by quantifying virus entry into either CHO/SLAM or CHO/CD46 cells with the pseudotype viruses VSV
G*-Toy-F/H or VSV
G*-Nag-F/H. The entry of these pseudotype viruses through SLAM was blocked by IPO-3 but was not affected by M177 (Fig. 2
A). The entry of the same pseudotype viruses through CD46 was blocked by M177 but was not affected by M160 (Fig. 2A
). These three antibodies were used to examine blocking of the entry of SSPE pseudotype viruses into Vero cells. The pseudotype viruses with either the Toyoshima or the Nagahata envelope glycoproteins were blocked completely by M177 (Fig. 2B
). The entry of pseudotype viruses with SSPE glycoproteins was not affected by M177 or by a mixture of M177 and IPO-3 (Fig. 2B
). Both the L77 neutralizing antibody to H glycoprotein and FIP could block all pseudotype virus infection (Fig. 2B
). Neither the M160 nor the IPO-3 antibodies inhibited the entry of any pseudotype viruses into Vero cells (Fig. 2B
).
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The effect of receptor antibodies on virus entry was tested on cell lines of lymphoid origin. Results from the OCUPSN human B cell line and B95a cells are shown in Fig. 2(D, E). The entry into OCUPSN cells of the pseudotype viruses with either the Toyoshima or the Nagahata envelope glycoproteins was blocked partially by IPO-3 or a polyclonal antibody to SLAM but was not affected by M160 or M177 antibodies (Fig. 2D
). The reason why the M177 antibody could not block the entry into OCUPSN cells is unknown but the high affinity of the H protein for SLAM may account for the negative effect of the antibody to CD46 in such SLAM and CD46 double-positive cells. The L77 antibody, FIP and the cocktail of IPO-3 and M177 antibodies could block the entry into OCUPSN cells completely by the Toyoshima or Nagahata pseudotype viruses. The entry into OCUPSN cells of the pseudotype viruses with the Masusako envelope glycoproteins was blocked completely by IPO-3 or a polyclonal antibody to SLAM without addition of M177 antibody. The entry into OCUPSN cells of pseudotype viruses with SSPE glycoproteins was also blocked partially by IPO-3 or a polyclonal antibody to SLAM (Fig. 2D
). The combination of M177 antibody and IPO-3, however, did not block the entry into OCUPSN cells by the SSPE pseudotype viruses (Fig. 2D
). The results of the blocking pseudotype virus entry with either antibodies or FIP were similar in both B95a and OCUPSN cells (Fig. 2E
). The CD46 homologue on B95a cells is defective and cannot be used for entry by most MV strains (Hsu et al., 1997
; Murakami et al., 1998
). As expected, the entry into B95a cells of the pseudotype viruses expressing either the Toyoshima or the Nagahata envelope glycoproteins was blocked completely by IPO-3 or a polyclonal antibody to SLAM without adding M177 antibody to CD46 (Fig. 2E
). The entry of pseudotype viruses with SSPE glycoproteins into B95a cells was blocked partially by IPO-3 or a polyclonal antibody to SLAM (Fig. 2E
).
These results show that a third unknown receptor was expressed on the cell surface of various cell lines, including neural and lymphoid cells. A molecule on Vero cells used by SSPE strains for entry may be different from a molecule(s) found on other cell lines but it can be used only by pseudotype viruses with the SSPE glycoproteins.
Biochemical characterization of a putative third entry receptor suggests a glycoprotein
To characterize the biochemical nature of a molecule involved in the entry of SSPE strains, we examined the infectivity of pseudotype virus with the glycoproteins of the Osaka-2 strain (VSVG*-Osa2-F/H) on Vero or SK-N-SH cells that were chemically modified by various reagents. Pseudotype virus with the G protein of VSV (VSV
G*-G), which has a known phospholipid receptor, was used as a control (Schlegel et al., 1983
).
Vero cells were preincubated with pronase, trypsin or chymotrypsin at various concentrations and then infected with VSVG*-G or VSV
G*-Osa2-F/H (Fig. 4
A). Pronase treatment of cells markedly reduced the infectivity of VSV
G*-Osa2-F/H in a dose-dependent manner, while VSV
G*-G infectivity was not affected even at the highest concentration used (Fig. 4A
). Trypsin treatment had no inhibitory effect but rather increased the infectivity of VSV
G*-Osa2-F/H (Fig. 4A
). The dose-responsiveness of VSV
G*-Osa2-F/H was different from that of pseudotype virus with the Toyoshima glycoprotein. Infectivity of VSV
G*-Toy-F/H for Vero cells was reduced sharply by trypsin treatment at a concentration of 500 µg ml-1. Chymotrypsin treatment had no effect, even at concentration of 500 µg ml-1, on the infectivity of VSV
G*-Osa2-F/H (data not shown). These results suggest that the third, putative cellular receptor for SSPE strain on Vero cells is sensitive to pronase and resistant to trypsin and chymotrypsin.
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SK-N-SH cells were also pretreated by pronase, tunicamycin, NaIO4 or neuraminidase and then VSVG*-G and VSV
G*-Osa2-F/H were tested for infectivity (Fig. 4B
). Neuraminidase treatment had no effect, even at a concentration that was 10 times higher than that sufficient to abolish the susceptibility of cells to influenza virus (Takada et al., 1997
). However, the infectivity of VSV
G*-Osa2-F/H was reduced in a dose-dependent manner by the treatment of cells with pronase, tunicamycin or NaIO4. The pattern observed in SK-N-SH cells was essentially the same as that of Vero cells, indicating the similarity of the biochemical nature of the molecule in both cell lines.
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DISCUSSION |
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There are reports of successful MV infection of rat brain in vivo or rat hippocampal tissue in vitro in the absence of detectable CD46 (Duprex et al., 2000; Ehrengruber et al., 2002
). Immature rat neurons may possess alternative receptors that can be used by MV. Interferon
/
receptor-knocked out mice are also susceptible to the Edmonston strain of MV, although the transgenic addition of CD46 facilitated the lethal outcome (Mrkic et al., 1998
). These reports support the hypothesis that there are entry receptors for MV other than CD46 and SLAM. The data in our study also support the possibility that there is a third unidentified receptor for SSPE strains of MV on Vero cells. It is possible that our SSPE strains could have attained the ability to bind to the third receptor during passages on Vero cells in vitro. We have analysed recently a brain tissue obtained at autopsy from a patient with SSPE. The Osaka-2 strain was isolated from the patient 8 years before autopsy. The nucleotide sequence of MV was determined directly without culture and found that it was similar to the sequence determined from the Osaka-2 strain. Although the nucleotide sequence of the envelope glycoprotein was variable in some positions, the key amino acid sequences of the F and H proteins were not changed during 8 years in the brain (unpublished data). Therefore, it is likely that the virus used in this study, at least the Osaka-2 strain, represents the virus replicating in a brain of a patient with SSPE. An alternative explanation for the entry of pseudotype virus of SSPE into Vero cells is that, despite the lack of detection of SLAM on Vero cells (Ono et al., 2001
), there may be small amounts of SLAM that can be used very efficiently as a receptor.
Recently, Lawrence et al. (2000) proposed a mechanism by the receptor-independent spread of MV in neurons. We do not exclude such a possibility that MV may spread in differentiated cell types, such as neurons, with different mechanisms. MV glycoproteins may be sorted to the specific portion of the neuron and could serve for transmission, as demonstrated by Ehrengruber et al. (2002)
. However, these papers are not presuming a third receptor other than CD46 and SLAM and the unidentified molecule may be involved in virus spread without significant fusion. Firsching et al. (1999)
proposed such a microfusion event at sites of cell-to-cell contact. It should be noted that we have observed massive fusion in the hippocampal neurons in a hamster brain that was infected with the Osaka-2 strain of MV (Ito et al., 2002
).
We found that the yet to be identified receptor(s) may also exist on other cell lines, including human neural and lymphoid cells, since blocking experiments using mAbs against known receptors did not inhibit infection by pseudotype viruses with the SSPE glycoproteins. SLAM-independent MV entry was reported by Hashimoto et al. (2002), who used recombinant MV expressing GFP based on the wild-type IC-B strain of MV to demonstrate infection of SLAM-negative cells such as Vero cells. The infection of the original IC-B strain of MV to Vero cells was not obvious when the infection criterion was morphological change of cells (Hashimoto et al., 2002
). Pseudotype virus with such wild-type MV glycoproteins does not enter Vero cells (Tatsuo et al., 2000a
). The infectivity of the virus for SLAM-negative cells was two to three logs lower than that for SLAM-positive cells (Hashimoto et al., 2002
). The discrepancy between the two assay systems using the recombinant IC-B and the pseudotype virus with the IC-B glycoprotein is similar to the results obtained in this study using our Masusako strain. The Masusako strain was isolated originally in, and replicated in, Vero cells, while the pseudotype virus with the Masusako glycoproteins failed to enter Vero cells. The molecular basis of the ability of the parental Masusako strain of MV to grow in Vero cells after entry is not known. However, this strain is considered, along with the IC-B strain, to be a wild-type, based on the sequences of the F and H glycoproteins (Furukawa et al., 2001
; Ning et al., 2002
). Whether the receptor used by the Masusako and IC-B strains is different from that used by the SSPE strains is unknown.
Identification of all possible receptor(s) used by SSPE strains is necessary to understand how MV enters into and spreads throughout the central nervous system. Such information may provide insight into the conditions that lead to SSPE instead of the typical measles disease.
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ACKNOWLEDGEMENTS |
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Received 13 January 2003;
accepted 28 April 2003.