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Journal of Virology, March 2001, p. 2444-2451, Vol. 75, No. 5
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.5.2444-2451.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Interaction of Coxsackievirus A21 with Its Cellular
Receptor, ICAM-1
Chuan
Xiao,1
Carol M.
Bator,1
Valorie D.
Bowman,1
Elizabeth
Rieder,2
Yongning
He,1
Benoît
Hébert,1
Jordi
Bella,1,
Timothy S.
Baker,1
Eckard
Wimmer,2
Richard J.
Kuhn,1,* and
Michael G.
Rossmann1
Department of Biological Sciences, Purdue
University, West Lafayette, Indiana 47907-1392,1
and Department of Molecular Genetics and Microbiology, School
of Medicine, State University of New York, Stony Brook, New York
11794-52222
Received 15 September 2000/Accepted 28 November 2000
 |
ABSTRACT |
Coxsackievirus A21 (CAV21), like human rhinoviruses (HRVs), is a
causative agent of the common cold. It uses the same cellular receptor,
intercellular adhesion molecule 1 (ICAM-1), as does the major group of
HRVs; unlike HRVs, however, it is stable at acid pH. The cryoelectron
microscopy (cryoEM) image reconstruction of CAV21 is consistent with
the highly homologous crystal structure of poliovirus 1; like other
enteroviruses and HRVs, CAV21 has a canyon-like depression around each
of the 12 fivefold vertices. A cryoEM reconstruction of CAV21 complexed
with ICAM-1 shows all five domains of the extracellular component of
ICAM-1. The known atomic structure of the ICAM-1 amino-terminal domains
D1 and D2 has been fitted into the cryoEM density of the complex. The
site of ICAM-1 binding within the canyon of CAV21 overlaps the site of
receptor recognition utilized by rhinoviruses and polioviruses. Interactions within this common region may be essential for triggering viral destabilization after attachment to susceptible cells.
| |
INTRODUCTION |
Enteroviruses, parechoviruses, and
human rhinoviruses (HRVs) are closely related viruses belonging to the
family Picornaviridae. Based on genome organization and RNA
sequences, the genera Rhinovirus and Enterovirus
are more closely related to each other than to the rest of the
picornaviruses (15). Whereas HRVs are labile at acid pH,
enteroviruses and parechoviruses are stable over a wider pH range. In
general, the serotypes within each genus have greater sequence
similarity to each other than they have to viruses in other genera.
Coxsackieviruses, polioviruses, some echoviruses, and some other
viruses are all classified as enteroviruses but are differentiated by
their pathogenic properties. Historically, coxsackieviruses have been
subdivided into 23 serotypes belonging to group A and 6 serotypes
belonging to group B (32, 42). These groups are
differentiated primarily by the type of lesions observed on infected
newborn mice. More recently, coxsackieviruses have been further
subdivided and assigned to distinct "clusters" within the
Enterovirus genus based on evolutionary kinship (genotypes). Accordingly, coxsackie A virus serotypes 1, 11, 13, 15, 17, and 18 to
24 and poliovirus serotypes 1 to 3 have been combined into cluster C,
although they cause different diseases (15, 38). All
cluster C coxsackie A viruses produce common cold-like symptoms, clinically indistinguishable from those of HRV infections. Furthermore, coxsackievirus A13 (CAV13), CAV18, and CAV21 have been shown to utilize
as their cellular receptor intercellular adhesion molecule 1 (ICAM-1,
or CD54) (9, 43), the same cell surface molecule as that
used by the major group of HRVs to gain entry into cells (13,
49). HRV infections cause the up-regulation of ICAM-1 and,
hence, the recruitment of leukocytes to sites of inflammation (37). Whether a similar up-regulation occurs for CAV21 is
not known at this time.
Many viruses utilize accessory cell surface molecules for cell
recognition or cell entry (11). For instance, CAV21 can
also bind to decay-accelerating factor (DAF, or CD55), although without causing an infection (44). The ICAM-1 and DAF binding
sites appear to be nonoverlapping although spatially close to each
other (45). The structures of ICAM-1 and DAF are totally
different. The extracellular component of ICAM-1 consists of five
tandem immunoglobulin superfamily (IgSF) domains, whereas DAF is
comprised of four short consensus repeat motifs and a
serine-threonine-rich region that links the protein via a
glycosyl-phosphotidylinositol linker to the plasma membrane.
The CAV21 RNA genome has about 80% amino acid sequence identity to
that of polioviruses, which utilize CD155 as their receptor (4,
19, 53), but only about 50% identity to that of HRVs (24). Although there is a slight preference for codon
usage resembling that of HRVs (24), these sequence
comparisons do not explain the receptor preference for CAV21 and
related cluster C coxsackieviruses. Similarly, the minor group of HRVs
has no obvious phylogenetic separation from the major group of HRVs, yet all minor-group HRVs utilize the low-density lipoprotein receptor to initiate infection (21).
The crystal structures of various HRVs and enteroviruses have been
determined at nearly atomic resolution. These include HRV14 (41) and HRV16 (16, 35), both of which
utilize ICAM-1 as a receptor; HRV1A (26) and HRV2
(51), which do not bind ICAM-1; coxsackievirus B3
(33), which utilizes the coxsackievirus-adenovirus receptor as well as DAF; CAV9 (20), which utilizes an
integrin as a receptor (39); and all three poliovirus
serotypes (22, 29, 54), which utilize the poliovirus
receptor, CD155 (4, 19, 53). However, the
three-dimensional atomic resolution structure of CAV21 has yet to be determined.
ICAM-1 is a cell surface molecule that normally binds to leukocyte
function-associated antigen 1 to provide adhesion between leukocytes
and endothelial cells. Apart from being recruited by viral pathogens,
such as HRVs and some coxsackieviruses, as a receptor, ICAM-1 also
binds to erythrocytes that have been infected by the malarial parasite
Plasmodium falciparum (3, 5, 34). The structure
of the two amino-terminal domains of ICAM-1, designated D1D2, has been
determined to nearly atomic resolution, in both partially
unglycosylated (3) and fully glycosylated (7, 28) forms. The amino-terminal domain D1 was found to have an "intermediate" type of IgSF fold, whereas the second domain, D2, has a constant type 2 IgSF structure (8, 18, 52). Amino acid sequence analyses (48) predict that the other three
domains also have IgSF-type folds.
The structures of glycosylated and unglycosylated, two- and five-domain
ICAM-1, when complexed with HRV16 (28, 36) or HRV14
(28), have been determined to a resolution of about 28 Å by cryoelectron microscopy (cryoEM). By fitting the known
X-ray structures of ICAM-1 and HRVs into the envelope of the cryoEM reconstructions of virus-receptor complexes, it has been possible to
determine the nature of the virus-receptor interactions. Similar results were obtained for the complex formed between poliovirus and
CD155 (4, 19, 53), although the structure of CD155 was
based upon homology modeling. In every case, the receptor is a long,
thin, flexible molecule that binds into the canyon, an
~15-Å-deep surface depression on rhinoviruses and
enteroviruses. These results are consistent with the prediction that
receptor molecules would be sufficiently thin to bind to the more
conserved residues in the canyon, at a site that is less accessible to
neutralizing antibodies (40, 41).
We report here a cryoEM image reconstruction, at a resolution of 26 Å, of CAV21 complexed with its primary receptor, ICAM-1, in
which all five domains of the receptor molecule are visible. Although
domain D1 of ICAM-1 binds to a similar site in the CAV21 canyon
vicinity as in HRVs and overlaps the site of binding of CD155 to
poliovirus, the orientation of the receptor molecule relative to the
virus is different for each type of virus. In contrast, ICAM-1 binds
similarly to different HRV serotypes regardless of whether it is
glycosylated or unglycosylated or is present as two- or five-domain structures.
| |
MATERIALS AND METHODS |
Sample preparation.
CAV21, strain Kuykendall, was obtained
from the American Type Culture Collection, Manassas, Va. (VR-850). The
virus was propagated in H1-HeLa cells two times, and CAV21-specific,
infectious cDNA was prepared and sequenced (E. Rieder and E. Wimmer,
unpublished data). CAV21 derived from the infectious cDNA was
propagated in 3.6 × 107 HeLa cells/ml, suspended in
Dulbecco minimal Eagle medium (Life Technologies) with 10% bovine
serum. The cells were infected with CAV21 at a multiplicity of
infection of 20. After adsorption at room temperature for 1 h
under mild agitation, the cells were diluted to a concentration of
3 × 106 cells/ml with fresh medium. They were allowed
to grow for 9.5 h, after which time they were harvested and lysed
with 1% Nonidet P-40. They were then briefly homogenized and
centrifuged at 4,000 × g to separate the components.
DNase (0.5 mg/ml) was added to permit digestion of nucleic acids for
1 h, followed by the addition of 0.5 mg of trypsin per ml for 10 min to digest protein. Sucrose gradient and CsCl isopycnic
ultracentrifugations were used to purify the virus. Five-domain, fully
glycosylated ICAM-1 lacking the cytoplasmic and transmembrane domains
was kindly provided by J. M. Greve (14). Plaque
reduction assays, used to determine whether the soluble receptor
blocked H1-HeLa cell infection, showed 100% inhibition at 0.46 mg of
ICAM-1 per ml.
CryoEM.
A 50-µl sample of purified CAV21 (6.2 mg/ml) was
incubated with or without (Table 1) 20 µl of 46.3-mg/ml five-domain ICAM-1 (an excess of about nine receptor
molecules per binding site on the virus) for 35 min on ice. CryoEM
specimens were prepared from 3.5-µl aliquots that were applied to
perforated carbon support electron microscope grids and vitrified in
liquid ethane (2). Micrographs were recorded on Kodak
SO-163 film in a Philips CM200 field emission gun (FEG) microscope at a
nominal magnification of 50,000 and a dose level of 18.5 e
/Å2. Micrographs were taken at
different underfocus levels (Table 1) so that useful contrast transfer
function corrections could be achieved uniformly for all resolutions.
The micrographs were digitized on a Zeiss PHODIS microdensitometer at
7-µm intervals but, for computational reasons, the pixels were
averaged to produce 14-µm pixels (2.80-Å spacing at the
specimen). Particles of the virus-receptor complex were boxed from
scanned micrographs with a radius of 130 pixels (364 Å).
A cryoEM reconstruction image of HRV16 served as an initial model for a
particle orientation search using the polar-Fourier
transform method
(
1). The final resolution for both the native
and the
complexed CAV21 density maps (Table
1) was determined
by splitting the
image data randomly into two equally sized groups
and determining
at what resolution the average agreement of phases
was less than 45°
and the correlation coefficient was less than
0.5. Although many
particle images were used in the reconstructions,
the final resolution
extended at best to only about 21 Å. The
original
Fourier-Bessel reconstruction program (
10), which was
later modified (
2), was rewritten for parallel processing
on
an IBM SP2 computer with 16 nodes to permit the calculations to
be
accomplished in a reasonable
time.
Difference map calculations and model fitting.
CryoEM image
reconstructions were made for native CAV21 and for CAV21 complexed with
five-domain ICAM-1 (Fig. 1). The size of
each map was scaled to that of a map of poliovirus 1 obtained from
X-ray diffraction coordinate data (Protein Data Bank accession number
2PLV) and calculated to approximately the same resolution. The maps
were scaled by comparing the densities within the protein shell (108- to 144-Å radii). A difference map was calculated by
subtracting the virus map from the virus-receptor map.
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FIG. 1.
Stereoview of cryoEM reconstructions showing native
CAV21 (a), complex of CAV21 with ICAM-1 domains D1 to D5 (b), complex
of HRV16 with ICAM-1 domains D1 and D2 (c), and complex of poliovirus 1 (Mahoney strain) with CD155 domains D1 to D3 (d). CAV21 is purple,
HRV16 is green, poliovirus 1 is blue, ICAM-1 is yellow, and CD155 is
red. In panel b, five domains of ICAM-1 can be seen; in panel c, only
two domains of ICAM-1 can be seen. All three domains of CD155 are
observed in panel d. One icosahedral asymmetric unit is outlined in
black on each of the four image reconstructions.
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|
The known structure of the first two ICAM-1 domains (
28)
was fitted into the difference map (Fig.
2). The slight variation
in the elbow
angle, about 6° (
28), between domains D1 and D2
for
different crystallographic determinations did not significantly
impact
the quality of fit. This was also true for the fitting
of the ICAM-1
structure into the HRV-ICAM-1 reconstruction density
map
(
28). The fitted structure was then used to compute
electron
density corresponding to an unglycosylated ICAM-1 D1D2
structure.
A further difference map between the cryoEM map and the
calculated
map identified the sites of carbohydrate attachment to the
D1D2
domains of the ICAM-1 molecule. These sites acted as fiducial
marks to obtain the best fit of the ICAM-1 structure to the difference
map. The absence of available structures with sufficient similarity
in
amino acid sequence to domains D3, D4, and D5 of ICAM-1 made
it
difficult to find useful homologous structures to fit the remaining
ICAM-1 density. The closest homologous structure (
25)
found
for domain D3 was neural cellular adhesion molecule domain D1
(Protein Data Bank accession number
2NCM [50]). In the absence
of any
better homologous structures, the previously modeled D1D2
domains of
CD155 (
19) were used to model the fourth and fifth
ICAM-1
domains.
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FIG. 2.
Stereoview of difference map between CAV21-ICAM-1 and
CAV21. The ICAM-1 difference density (green) has been fitted with the
known structure (black) of ICAM-1 (D1D2) and homologous models of D3,
D4, and D5 (see the text). Shown also is the difference density (blue)
between the observed glycosylated ICAM-1 structure and the
unglycosylated ICAM-1 structure. The N-linked Asn carbohydrate sites
are indicated in red. The correspondence of the observed locations of
the glycosylation sites and their known positions on the ICAM-1
backbone acted as a marker for accurate fitting of the ICAM-1 molecule.
Because the height of the density decreases approximately in proportion
to the distance of each domain from the virus center, the contour level
is shown at 2.00  around domains D1 and D2, 1.30 around D3, 0.80 around D4, and 0.65 around domain D5; the value is the
root-mean-square difference from the mean density of the map, which in
this case included large areas of zero density outside the cryoEM
image.
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|
Structure of CAV21.
The atomic coordinates of poliovirus 1 were used as a basis for building a model of CAV21. Residue replacement
and energy minimization were performed with the program SEGMOD
(30). The footprint of the ICAM-1 molecule on the CAV21
surface was defined by the residues on the viral surface that have any
atoms within 4 Å of any atom in the receptor.
| |
RESULTS AND DISCUSSION |
Structure of ICAM-1.
The 180-Å-long structure (Fig.
1 and 3) of the complete extracellular
component of five-domain ICAM-1 bound to CAV21 is clearly visible in
the reconstruction. However, only the first three domains were visible
in an earlier reconstruction of HRV16 complexed with five-domain ICAM-1
(28). The difference may partially reflect the use of
about 200 particle images in the present reconstruction, compared to
only 43 in the earlier reconstruction. In addition, the use of an
electron microscope fitted with an FEG provided better image
conditions because the electron beam was brighter and more
coherent than in conventional instruments. The importance of the
data collected with the FEG was confirmed in that an earlier reconstruction of the CAV21-ICAM-1 complex, obtained with a Philips 420 electron microscope (data not shown), did not show the complete ICAM-1 molecule. Some flexibility of the articulated ICAM-1 molecule is
apparent because the height of the density decreases in successive domains. If the mean height of the density in the viral capsid coat is
arbitrarily set to a value of 10, the densities in domains 1, 2, 3, 4, and 5 are 10, 10, 6, 3, and 1, respectively. Although the density
progressively decreases toward the C terminus of ICAM-1, it is
surprising that the long ICAM-1 molecule is sufficiently rigid for all
domains to remain visible even after the icosahedral averaging inherent
in the reconstruction technique has been applied. It was reported
(47) that ICAM-1 is kinked between domains 2 and 3, but
this orientation does not appear in the present reconstruction. Kirchhausen et al. (27) suggested that ICAM-1 is slightly
kinked between domains 3 and 4, an observation that is approximately consistent with the structure reported here (Fig. 1 and 3). All the
various receptor molecules utilized by picornaviruses are long, thin,
and articulated at hinges between domains. Although ICAM-1 appears to
be more rigid than expected, its properties are consistent with the
requirement that the receptor be a molecule able to flex sufficiently
to recognize additional sites on the viral surface once the first
receptor has been bound. The apparent preference for long, thin, hinged
receptor molecules may be essential for the recruitment of successive
receptors to the viral surface after the initial recognition event.
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FIG. 3.
Stereoview of a ribbon diagram of one molecule of
ICAM-1 (yellow) bound to one icosahedral asymmetric unit of CAV21.
Ribbons of VP1, VP2, and VP3 are shown in blue, green, and red,
respectively. Icosahedral symmetry axes surrounding the site of
receptor attachment are also shown.
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The glycosylation sites on ICAM-1 helped improve the accuracy by which
the known ICAM-1 D1D2 structure could be fitted to
the cryoEM density
(Fig.
2). The footprint of ICAM-1 on the homology-modeled
structure of
CAV21 is complementary in shape and charge to the
ICAM-1 binding
surface (Fig.
4). There is no evidence
for the
formation of any hydrogen bonding interactions.
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FIG. 4.
Road map of the ICAM-1 footprint on the surface of
CAV21, showing the surface amino acids (left) and exposed peptide
segments that are in contact with ICAM-1 (middle). The partial outline
of the triangular, icosahedral asymmetric unit is indicated. The canyon
is shown in gray, and the buried VP1 hydrophobic pocket is shown by the
circular broken line, with a representative drug bound. Also shown are
the amino acids of ICAM-1 in contact with the CAV21 surface (right).
Amino acids (left and right panels) are blue (basic), red (acidic),
green (hydrophobic), and yellow (polar). Virus residues (left panel)
are numbered from 1001, 2001, and 3001 in VP1, VP2, and VP3,
respectively. Note the charge complementarity and matching of
hydrophobic regions between the CAV21 and ICAM-1 binding surfaces. In
the middle panel, the peptide segments are differentiated by color.
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Location of the receptor binding site.
The interactions of
ICAM-1 with the surface of CAV21 span between the "north" and
"south" canyon rims (Fig. 4), involving 
C and the loop from E
to 
B of viral protein 1 (VP1) on the north rim, the GH loops of VP1
and VP3 on the floor, and the "puff" on the south rim. The puff is
a variably sized insertion in VP2 of picornaviruses (41).
The footprint of ICAM-1 on the surface of CAV21 and on HRV14 and HRV16
of the major-group rhinoviruses and the footprint of
CD155 on the
surface of poliovirus 1 have a common core of somewhat
conserved
residues (Fig.
5 and
6). However, the orientations of
the
receptor molecules are different for each virus-receptor complex.
Whereas in CAV21 the receptor leans very slightly to the east-southeast
(Fig.
1b), as viewed in the conventional orientation with the
fivefold
axis of the icosahedral asymmetric unit in the north,
in HRVs the
ICAM-1 receptor molecule leans to the southwest and
approaches the
icosahedral twofold axis much more closely (Fig.
1c). However, the
first domain of CD155 lies almost tangential
to the poliovirus surface,
with the subsequent domains pointing
eastward (Fig.
1d). In contrast,
the orientations of ICAM-1 (glycosylated
or unglycosylated, two domains
or five domains) with any of the
HRVs are almost exactly the same.
Similarly, in three studies
of CD155 with poliovirus (
4,
19,
53), the orientations
of the receptor were shown to be the same.
This result is surprising,
as the amino acid sequence differences
between CAV21 and poliovirus
are fewer than the differences between
HRV14 and HRV16.
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FIG. 5.
Comparison of the footprint of ICAM-1 on CAV21 (thick
black outline) with the footprints of ICAM-1 on HRV16 and HRV14 and of
CD155 on poliovirus 1 (PV1) (areas covered by small squares). Gray
shading shows the outline of the canyon, and the circular broken line
shows the site of the pocket factor underneath the canyon. Scale bar,
10 Å.
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FIG. 6.
Amino acid sequence alignments for CAV21, HRV16, HRV14,
and poliovirus 1 (PV1) in the regions that form the receptor-virus
interactions. Amino acids that have been identified as participating in
receptor interactions are colored to match the corresponding peptide
segments shown in the middle panel of Fig. 4. Lowercase letters
represent amino acids in the puff for which there was no alignment with
the other sequences; the residues could lie anywhere in this area.
Dashes represent deletions of amino acids relative to the alignment.
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The utilization of similar locations around the canyon by all of the
currently studied receptors bound to picornaviruses (Fig.
5) suggests
that this region provides an essential function in
picornavirus
infections. The presence of the receptor attachment
site within the
canyon was predicted (
41) as a position protected
from
host immune surveillance. This notion was questioned when
it was found
that the site of binding of a neutralizing antibody
extended beyond the
rims and into the canyon (
46), thus demonstrating
that the
receptor and antibody sites overlapped. Nevertheless,
because selected
neutralizing antibody escape mutations lie outside
the canyon and
because residues inside the canyon are more conserved
than those
outside the canyon, the binding affinity of the receptor
probably is
slightly dominated by residues in the canyon. This
preference is
enhanced by avidity caused by attachment of multiple
receptor molecules
to attain cell
entry.
Receptor binding to CAV21, HRVs, and poliovirus 1 is localized within
the canyon to a site adjacent to a hydrophobic pocket
within the VP1
barrel containing an as-yet-unidentified "pocket
factor" (Fig.
4 and
5) (
12,
40). It has been suggested that
the pocket
factor stabilizes the virus during transit between
hosts but is
displaced by the competition of the receptor for
its overlapping
binding site (
17,
35,
40). Thus, binding
of receptor would
destabilize the virion and initiate uncoating.
This hypothesis is
consistent with the observed degradation of
HRVs in the presence of
soluble ICAM-1 (
23) and the possible
absence of the pocket
factor in the poliovirus-CD155 complex (
4).
Virus stability.
The difficulty of determining incubation
times and temperatures needed to obtain successful virus-receptor
cryoEM images is related to the destabilizing effect of the receptor on
the virus. Thus, it is significant that kinetic analyses have shown,
both for HRVs (6) and for polioviruses (31),
that there are two distinct modes of binding whose relative abundance
varies with temperature. The binding modes observed in the cryoEM
reconstructions are likely to be the most stable intermediates,
although these may be different depending upon the virus-receptor
complex. Kolatkar et al. (28) argue that the complexes
seen for HRVs are an initial event, consistent with kinetic data
(6). In view of the probable loss of the pocket factor
from the poliovirus-receptor complex (4) and the more
extensive contact of the receptor with the viral surface, it is
possible that the poliovirus-receptor complex represents an
intermediate stage of picornavirus-receptor interaction. Thus, the
CAV21, HRV, and poliovirus interactions with their receptors might
represent sequential steps in similar processes for each virus.
| |
ACKNOWLEDGMENTS |
We thank Sharon Wilder and Cheryl Towell for help in the
preparation of the manuscript.
This work was supported by National Institutes of Health grants to
M.G.R. (AI11219) and E.W. (AI32100, AI39485, and AI15122); a National
Institutes of Health program project grant to M.G.R., R.J.K., T.S.B.,
and others (AI45976); and a National Science Foundation shared
instrument grant to T.S.B., M.G.R., and others (BIR-9112921). Support
was also provided by a Purdue University reinvestment grant.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Biological Sciences, Purdue University, West Lafayette, IN 47907-1392. Phone: (765) 494-1164. Fax: (765) 496-1189. E-mail:
rjkuhn{at}bragg.bio.purdue.edu.
Present address: School of Biological Sciences, University of
Manchester, Manchester M13 9PT, England.
| |
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Journal of Virology, March 2001, p. 2444-2451, Vol. 75, No. 5
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.5.2444-2451.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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Abstract
Introduction
