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Journal of Clinical Microbiology, April 2000, p. 1656-1660, Vol. 38, No. 4
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Identification of an Epitope Common to Genogroup 1 "Norwalk-Like Viruses"
Antony D.
Hale,1,2
Tomoyuki N.
Tanaka,3
Noritoshi
Kitamoto,4
Max
Ciarlet,1
Xi
Jiang,5
Naokazu
Takeda,6
David W. G.
Brown,2 and
Mary K.
Estes1,*
Department of Molecular Virology and
Microbiology, Baylor College of Medicine, Houston, Texas
770301; Center for Pediatric
Research, Eastern Virginia Medical School, Norfolk, Virginia
235105; Enteric and Respiratory
Virus Laboratory, Central Public Health Laboratory, London NW9 5HT,
United Kingdom2; and Department of
Microbiology, Wakayama Medical College,
Wakayama,3 School of Humanities for
Environmental Policy and Technology, Himeji Institute of Technology,
Himeji, Hyogo,4 and Department of
Virology II, National Institute of Infectious Diseases,
Tokyo,6 Japan
Received 19 October 1999/Returned for modification 24 December
1999/Accepted 31 January 2000
 |
ABSTRACT |
A panel of 10 monoclonal antibodies (MAbs) to recombinant Norwalk
virus (NV) capsid protein were tested in competition enzyme-linked immunosorbent assays. Patterns of competition indicated that these MAbs
recognize six to eight epitopes covering five nonoverlapping regions of
the capsid protein. A single epitope, recognized by NV MAbs NV3901,
NV3912, and NV2461 was found to occur in the majority of genogroup 1 (G1) but not genogroup 2 (G2) "Norwalk-like viruses" (NLVs). This
observation supports the subdivision of human NLVs into two genogroups
and provides an assay for the rapid identification of G1 NLVs in fecal specimens.
| |
TEXT |
"Norwalk-like viruses" (NLVs)
represent one of four genera within the Caliciviridae and
are a genetically and antigenically diverse group of agents that cause
acute gastroenteritis in adults and children (5, 8).
Morphologically identical viruses that are genetically related to NLVs
have also been identified in fecal specimens from cows (1,
3). Human caliciviruses have not yet been successfully grown in
tissue cultures, which has prevented the application of classical
virological methods to study these agents. However, the ability of
recombinant Norwalk virus (rNV) capsid protein to spontaneously form
virus-like particles (VLPs) when expressed in insect cells has
exponentially increased the experimental approaches available to
characterize these viruses (17). The genetic diversity of
human NLVs has also been studied by the sequencing of full and partial
genomes. Phylogenetic analyses reveal two major distinct clusters of
NLVs, designated genogroup 1 (G1) and genogroup 2 (G2) (24).
G1 NLV strains include Norwalk virus (NV), Southampton virus, Desert
Shield virus, and Chiba virus (CV). G2 NLV strains include Hawaii
virus, Lordsdale virus, Grimsby virus (GRV), Mexico virus (MXV), and
the Snow Mountain agent (4, 9, 10, 14, 15, 16, 18-20, 23).
NV VLPs are morphologically and antigenically similar to native virus,
and their atomic structure has been solved by X-ray crystallography
(21). These 38-nm particles exhibit a T=3 icosahedral symmetry, and 90 dimers of the single capsid protein form distinctive arch-like structures. The structure has a shell domain, consisting of
the N-terminal 225 residues of the 530-amino-acid capsid protein, and a
protruding (P) domain (22). The central region of the sequence forms the topmost P2 domain of the arch-like structures, and
the C terminus forms the P1 domain which connects the shell and P2
domains, comprising the body of the arch-like structures.
The process of antigenic mapping of NV began by the generation of 10 monoclonal antibodies (MAbs) to rNV VLPs (11). The MAbs
reacted by Western blotting or immunoprecipitation with either the 58K
full-length capsid protein or the C-terminal 32K product produced by
trypsin cleavage of soluble capsid protein and were classified into
three reactivity groups: group I, consisting of four MAbs (NV834,
NV142, NV101, and NV813) that recognize discontinuous epitopes on the
rNV capsid protein; group II, consisting of MAbs NV3901, NV3912, and
NV2461 that recognize continuous epitopes on the C-terminal 74 amino
acids of the capsid protein; and group III, consisting of three MAbs
(NV7411, NV8812, and NV8301) that recognize discontinuous epitopes in
the C terminus of the capsid protein (11, 12). The three
group II MAbs reacted with the 32K form by Western blotting even when
the protein was denatured by boiling prior to electrophoresis, whereas
group I MAbs NV101 and NV813 and group III MAbs only recognized the
nondenatured 32K capsid protein (11). Group I MAbs NV834 and
NV142 could not be mapped to the C-terminal region (11).
However, all 10 MAbs detected NV in the stools of NV-infected
volunteers by an enzyme-linked immunosorbent assay (ELISA) (11,
15). None of these MAbs reacted by ELISA or Western blotting with
recombinant G2 MXV VLPs (11, 15).
To further characterize the epitopes recognized by these MAbs,
competition ELISAs were performed using antibodies purified on protein
A or G columns (Pierce, Rockford, Ill.) as previously described
(2, 13). One MAb was used to coat flat-bottomed polyvinylchloride microtiter plates (Dynatech Laboratories, Inc., Alexandria, Va.) overnight at 4°C at a concentration of 2 µg/ml in
0.05 M carbonate bicarbonate buffer (pH 9.6). In separate tubes, rNV
VLPs, at a concentration of 5 to 500 ng/ml (depending on the coating
MAb), were added to decreasing concentrations of competitor MAb (5, 1, 0.5, 0.1, and 0.05 mg/ml) in phosphate-buffered saline (PBS) (pH 7.2)
containing 1% (wt/vol) BLOTTO (Carnation natural nonfat milk) and then
incubated overnight at 4°C. A control of rNV in 1% BLOTTO without
competitor MAb was also included in each plate. The antibody-coated
microtiter plates were washed twice with PBS containing 0.05% Tween 20 (PBS-T) and blocked with 5% BLOTTO for at least 30 min at 37°C.
Following two additional washes with PBS-T, 60 µl of each of the
rNV-MAb reaction mixtures was added to duplicate wells, and the plates
were incubated for 2 h at 37°C. After washing four times, 100 µl of a 1:5,000 dilution of rabbit anti-rNV hyperimmune serum in 1%
BLOTTO was added to all wells. Plates were again incubated for 2 h
at 37°C and washed four times, and a 1:5,000 dilution of goat
anti-rabbit total immunoglobulins (Igs) (IgM, IgG, and IgA) conjugated
to horseradish peroxidase (Cappel, West Chester, Pa.) was added. After
a final incubation of 1 h at 37°C and four washes with PBS-T,
100 µl of 3,3',5,5'-tetramethylbenzidine (Kirkegaard & Perry
Laboratories, Inc., Gaithersburg, Md.) was added, and the color
reaction was stopped by the addition of 100 µl of 1 M phosphoric
acid. The optical density at 450 nm (OD450) of wells was
read, and the average of duplicates was calculated. The percentage of
competition or enhanced binding was determined for all competitor MAb
concentrations based on the value of the PBS control (i.e., the value
of rNV binding to coating MAb in the absence of competitor MAb was
defined as zero). Homotypic competition was included as a positive
control for all coating MAbs.
MAbs NV3901, NV3912, and NV2461 recognize a common epitope on rNV
VLPs.
Initial experiments revealed that MAbs bound to the solid
phase had different affinities for rNV capsid protein (data not shown).
Thus, for the competition assays, the concentration of rNV VLPs used
for each coating MAb was that which produced an OD450 of
0.5 to 1.5 when no competitor MAb was present. In agreement with other
studies (2, 13), homotypic competition for the 10 MAbs was
found to vary between 50 and 90% at the highest concentration of
competitor antibody used in the ELISAs (data not shown). Significant competition was defined as at least a 50% reduction in detection signal at a concentration of 5 µg/ml of competitor antibody and when
a concentration-dependent competition effect was observed.
No significant enhanced binding was observed, and the degree of
heterotypic competition was found to vary from zero to over 90% (Fig.
1). The pattern of competition differed
depending on whether a MAb was used as a coating or as a competitor
antibody. When group III MAb NV8812 was used as the coating MAb, only
homotypic competition was observed (Fig. 1A). However, when MAb NV8812
was used as the competitor antibody, MAb NV8812 competed with itself and with six additional MAbs (NV2461, NV834, NV813, NV101, NV142, and
NV7411) (Fig. 1B). One-way competition was also observed when group I
MAb NV142 was used as the coating MAb for all other MAbs except group I
MAbs NV813 and NV834 (data not shown). Therefore, group I MAb NV142 is
unique when compared to the other group I MAbs. This phenomenon may be
due to a conformational change in the epitope recognized by the coating
antibody, leading to a reduced affinity of binding. Alternatively, the
epitopes may overlap, or one MAb may cause steric hindrance while the
other may not. For some MAb combinations, two-way competition was
observed. For example, group II MAb NV3901 competed with itself, group
II MAbs NV3912 and NV2461, and group III MAb NV7411 (Fig. 1C and D).
Group III MAb NV7411 showed a competition pattern similar to group II MAbs with the exception of the additional one-way competition of NV7411
with group I MAbs NV834 and NV813 (data not shown).
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FIG. 1.
Competition ELISAs showing homotypic and heterotypic
competition for MAb NV8812 (top) used either as coating antibody (A) or
competitor antibody (B) or MAb NV3901 (bottom) either as coating
antibody (C) or as competitor antibody (D). The 50% cutoff for
significant competition is indicated by a horizontal line.
|
|
The results of the competition ELISAs for all MAb combinations are
summarized in Fig.
2A. The patterns of
competition were
indistinguishable for a number of MAbs. Results
obtained with
group II MAbs NV3901 and NV3912 or MAb NV2461 were
identical or
similar, respectively (data not shown). Thus,
group II MAbs likely
recognize the same epitope or closely overlapping
epitopes. Results
with group I MAbs NV813, NV834, and NV101 were
also identical
except for the binding of group I MAb NV101 that was
inhibited
when group III MAb NV7411 was used as competitor antibody
(data
not shown). Since MAbs belonging to groups I and III recognize
at
least five discontinuous epitopes and two closely related discontinuous
epitopes, the precise relationship of these MAbs to one another
and to
those in group II awaits further mapping on the rNV capsid
protein. A
schematic representation of the putative six to eight
epitopes
recognized by the 10 rNV MAbs is shown in Fig.
2B. The
proposed map is
compatible with the three groups described by
Hardy et al.
(
11). In addition, group III MAb NV8812 was the
only MAb to
block binding of rNV to human intestinal epithelial
CaCo-2 cells
(
25); in the present study, this MAb appears to
recognize a
unique epitope.
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FIG. 2.
(A) Summary of epitope-mapping data. Pattern of
competition of 10 anti-rNV MAbs, both as coating and competitor
antibodies (as indicated). Combinations producing one-way competition
are indicated by hatched lines and those producing two-way competition
are indicated by black shading. MAbs are grouped according to Hardy et
al. (11), and the concentration (5 to 500 ng/ml) of rNV VLPs
used for each coating MAb is indicated at the bottom. (B) Proposed map
of the putative six to eight epitopes on rNV VLPs defined by 10 rNV
MAbs.
|
|
MAbs NV3901, NV3912, and NV2461 recognize a common epitope in G1
NLVs.
All MAbs were tested against recombinant capsid proteins of
NV, CV, GRV, and MXV by indirect ELISA as described (17),
with the exception that the plates were coated with antigen at a
concentration of 1 µg/ml. All MAbs reacted with rNV VLPs but did not
react with recombinant MXV or recombinant GRV (11,
15; data not shown). In addition, MAbs NV3901, NV3912, and
NV2461 reacted with recombinant CV VLPs, a G1 NLV exhibiting 75% amino
acid sequence identity over the entire capsid with NV, 66% amino acid
sequence identity over the region spanning amino acids 228 to 530 (the
32K soluble protein), and 82% amino acid sequence identity over the
region spanning amino acids 457 to 530 (the C-terminal 74 amino acids containing the common epitope for G1 NLVs) (11; data
not shown). The fact that these MAbs were able to detect a common
epitope present on the G1 CV was both unexpected and surprising because the NV polyclonal antigen capture ELISA that uses polyclonal antibodies to NV as capture and detection antibodies does not recognize CV. To
determine whether MAb NV3901, NV3912, or NV2461 could be used to
detect additional G1 NLVs, an antigen capture ELISA was developed essentially as described for the NV polyclonal antigen capture ELISA (6, 17) with minor modifications. Briefly, purified MAb NV3901 or rotavirus-specific MAb 3D8 (2) was used to
coat flat-bottomed polyvinylchloride microtiter plates (Dynatech
Laboratories, Inc.) at a concentration of 2 µg/ml in 0.05 M carbonate
bicarbonate buffer (pH 9.6). A 1:5,000 dilution of guinea pig
hyperimmune serum prepared against rNV VLPs (6, 17) in 1%
BLOTTO was used as the detector antibody.
A panel of 29 fecal specimens containing G1 (
n = 15) or
G2 (
n = 14) NLVs that had been characterized by reverse
transcription-PCR
and amplicon sequencing (
7) were tested in
the NV polyclonal
and MAb NV3901 antigen capture ELISAs. None of the 29 fecal specimens
reacted in the NV polyclonal antigen capture ELISA
(data not shown),
and the P
N values of the 29 fecal specimens
in the MAb NV3901
ELISA are shown in Fig.
3. Nine of 15 (60%) fecal specimens
containing
strains from the G1 NLV genetic clusters
(
7) Musgrove, Southampton,
Desert Shield, and Queens
Arms (but not Winchester) were detected
in the ELISA with MAb NV3901
(Table
1). None of the fecal specimens
containing G2 NLV strains, represented by the Hawaii virus,
Lordsdale
virus, MXV, or Leeds G2 NLV genetic clusters (
7),
reacted in
the MAb NV3901 ELISA (Table
1). The amino acid
sequence identities,
corresponding to the entire 539, 542, 544, 545, or 547 amino acids
of the capsid protein of the G1 NLV strains
tested, ranged from
63 to 70% when compared to the corresponding 530 amino acids of
the capsid protein of NV (
7). The level of
amino acid sequence
identity between NV and the G1 NLVs over the region
spanning the
C-terminal 74 amino acids of the capsid protein ranged
from 79
to 90%. The two strains from the Winchester G1 NLV genetic
cluster
failed to react in the MAb NV3901 ELISA, possibly because they
share the lowest capsid protein (63%) or C-terminal (79%) amino
acid
identity with NV. The amino acid identities of the different
G2 NLV
strains varied from 40 to 43% when compared to the corresponding
capsid region of NV (
7). Therefore, the ability of the MAb
NV3901 antigen capture ELISA to detect a subset of G1 NLVs may
possibly
reflect the greater sensitivity of PCR over antigen detection
by ELISA,
differences in virus concentration among the fecal samples
tested, or
the result of genetic variation among the different
G1 NLV genetic
clusters. The main advantage of using the MAb3901
antigen capture ELISA
to identify most G1 NLV strains over molecular
techniques such as PCR
is that large numbers of samples could
be tested in a rapid and
cost-effective manner.
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FIG. 3.
Reactivity of 29 fecal specimens containing either G1
(n = 15) or G2 NLVs (n = 14) in an
antigen ELISA based on MAb NV3901. The OD450 of MAb NV3901
(P) minus the OD450 of control rotavirus-specific MAb 3D8
(N) (2) is plotted for NLV G1 and G2. The cut off for
reactivity (P N >0.1) is indicated by a dashed line. Means are
shown as horizontal bars.
|
|
In conclusion, MAbs NV2461, NV3901, and NV3912 appear to map to a
single epitope that is common to G1 NLVs. This common epitope
is
present in monomeric forms of the 32K trypsin cleavage product
and has
been mapped to the C-terminal 74 amino acids of the capsid
(
11). Studies are underway to further map this epitope.
These
studies may allow determination of an equivalent epitope in G2
NLVs using sequence alignments directed by the rNV capsid atomic
structure (
21). Antibodies directed to the putative common
epitope
in G2 NLVs, in combination with MAb NV3901 that recognizes the
common epitope in G1 NLVs, might allow the development of a broadly
cross-reactive ELISA to rapidly and efficiently identify G1 and
G2 NLVs
in stool samples as a cause of outbreaks and sporadic
cases of
gastroenteritis
worldwide.
| |
ACKNOWLEDGMENTS |
We are extremely grateful to Sue E. Crawford, Robert L. Atmar, and
Pamela J. Glass for helpful discussions.
This work was supported by Public Health Service grant AI38036 from the
National Institute of Allergy and Infectious Diseases. Antony D. Hale
undertook this work while on a fellowship from The Pathological Society
of Great Britain and Ireland.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Division of
Molecular Virology, Baylor College of Medicine, One Baylor Plaza, Room 923E, Mailstop BCM-385, Houston, TX 77030. Phone: (713) 798-3585. Fax:
(713) 798-3586. E-mail: mestes{at}bcm.tmc.edu.
| |
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Journal of Clinical Microbiology, April 2000, p. 1656-1660, Vol. 38, No. 4
0095-1137/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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