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Journal of Virology, October 2000, p. 9300-9305, Vol. 74, No. 19
Department of Veterinary Public Health, Faculty of
Agriculture, Tottori University, Tottori
680-8553,1 Department of Biochemistry,
University of Shizuoka, School of Pharmaceutical Science, Shizuoka
422-8002,2 Laboratory of Microbiology,
Department of Disease Control, Graduate School of Veterinary
Medicine, Hokkaido University, Sapporo
060-0818,3 Department of Veterinary
Microbiology, College of Agriculture, Osaka Prefecture University,
Sakai 599-6231,4 Department of
Applied Bioorganic Chemistry, Gifu University, Gifu
501-1193,6 and Institute of Medical
Science, University of Tokyo, Minato-ku, Tokyo
108-8639,7 and Department of
Pathobiological Sciences, School of Veterinary Medicine, University
of Wisconsin
Received 17 December 1999/Accepted 16 May 2000
The hemagglutinin (HA) of H3 human influenza viruses does not
support viral replication in duck intestine despite its avian origin. A
Leu-to-Gln mutation at position 226 and a Ser-to-Gly mutation at
position 228 in the HA of human A/Udorn/307/72 (H3N2) permit a
reassortant virus [human Udorn HA, with all other genes from
A/mallard/New York/6750/78 (H2N2)] to replicate in ducks. To
understand the molecular basis of this change in host range restriction, we investigated the receptor specificity of duck influenza
viruses as well as of human-duck virus reassortants. The results
indicate that the recognition of a glycoconjugate moiety possessing
N-glycolneuramic acid (NeuGc) linked to galactose by the
Influenza A viruses have been
isolated from a variety of animals, including humans, pigs, horses, sea
mammals, and birds (37). Each of the different antigenic
subtypes of influenza A viruses (H1 to H15 and N1 to N9) has been
isolated from wild aquatic birds (7, 27, 37), which appear
to serve as the reservoir for all influenza A viruses that infect
mammals (37). Despite their common origin, influenza A
viruses do not replicate indiscriminately across animal species but
rather show a clear pattern of host range restriction. For example, in
experimental infection of nonhuman primates, avian influenza viruses
replicate poorly (1, 20, 28), while human viruses replicate
well and cause influenza symptoms (20, 28); the titers of
avian and human viruses differ by 2 logs in nonhuman primates
(19). A notable exception is the direct transmission of an
avian influenza virus from birds to humans in Hong Kong in 1997 (2, 31). As one might predict, influenza viruses isolated
from ducks replicate well in duck intestine, the major replication site
in this host, whereas human viruses do not (14, 36). The
importance of the hemagglutinin (HA) and neuraminidase (NA) molecules
in the restriction of human virus replication in ducks was demonstrated
in studies in which reassortant viruses containing either the HA or NA
gene from a human virus and other genes from a duck virus failed to
replicate in ducks (8). However, the molecular mechanism of
these restrictive effects remains unknown.
Although all influenza viruses recognize oligosaccharide-containing
terminal sialic acid, the receptor specificity of the HA differs: most
avian influenza viruses preferentially bind to the sialic
acid- Sialic acid is a generic term for a nine-carbon, acidic amino
sugar
(5-amino-3,5-dideoxy-D-glycero-D-galacto-nonulosonic acid) whose amino group is replaced with either an N-acetyl or
N-glycolyl group, yielding N-acetylneuraminic
(NeuAc) or N-glycolylneuraminic (NeuGc) acid, respectively.
The hydroxyl groups can be replaced by acetyl, lactoyl, methyl,
sulfate, or phosphate residues. The distribution of specific sialic
acids differs among animal species. For example, cells from cows,
horses, and pigs express both NeuAc and NeuGc (16, 18, 22,
23), but human cells do not express NeuGc (15, 16).
Influenza viruses differ in their recognition of NeuAc, NeuGc, and
9-O-Ac-NeuAc (6), suggesting that it is not only
the type of sialic acid-galactose linkage but also the sialic acid
species that contributes to the host range restrictions of influenza A viruses.
Influenza viruses isolated from various animal species differentially
agglutinate erythrocytes from different animals (11). For
example, although all influenza viruses agglutinate human and chicken
erythrocytes, duck but not human influenza viruses agglutinate horse
erythrocytes (12). Chicken and human erythrocytes both
possess SA Human influenza A viruses do not replicate in ducks (14,
36). This host restriction appears to reside in the receptor specificity of the HA: a reassortant virus containing only the HA gene
from a human A/Udorn/307/72 (Udorn) (H3N2) virus and all remaining
genes from A/mallard/New York/6750/78 (Mal/NY) (H2N2) and its horse
Comparison of receptor specificity between duck and human influenza
A viruses.
Two mutations of the human Udorn virus HA at positions
226 (Leu to Gln) and 228 (Ser to Gly) enable a reassortant virus
possessing this HA in the context of Mal/NY viral genes to grow in duck
intestine. Since both mutations are located in the receptor binding
pocket, we analyzed the receptor specificity of the virus by comparing the binding characteristics of the wild-type human Udorn HA, its mutant
with a Leu-to-Gln substitution at position 226 (L226Q; R3 HA), and
another mutant possessing both the preceding changes and a Ser-to-Gly
substitution at position 228 (L228G; R2 HA), using thin-layer
chromatography (TLC) virus binding assays with gangliosides (Fig.
1A). Because gangliosides containing
NeuGc
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Recognition of N-Glycolylneuraminic Acid
Linked to Galactose by the
2,3 Linkage Is Associated with
Intestinal Replication of Influenza A Virus in Ducks
Madison, Madison, Wisconsin 537065
ABSTRACT
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Abstract
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References
2,3 linkage (NeuGc2,3Gal) is associated with viral replication in
duck intestine. Immunofluorescence assays with NeuGc2,3Gal-specific antiserum detected this moiety primarily on the crypt epithelial cells
of duck colon. Such recognition, together with biochemical evidence of
NeuGc in crypt cells, correlated exactly with the ability of the virus
to replicate in duck colon. These results suggest that recognition of
the NeuGc2,3-Gal moiety plays an important role in the enterotropism
of avian influenza viruses.
TEXT
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Abstract
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References
2,3-galactose (SA2,3Gal) linkage, while human influenza
viruses favor the SA2,6Gal linkage on cell surface sialyloligosaccharides (3, 24, 25). Couceiro et al.
(4) reported the presence of SA2,6Gal but not of
SA2,3Gal sialyloligosaccharides on the surface of epithelial cells
from human trachea. It was recently shown that the epithelial cells of
duck intestine contain SA2,3Gal but not SA2,6Gal
sialyloligosaccharides (13). Thus, the host range of
influenza A viruses may correspond to the presence or absence of
certain sialic acid-galactose linkages in host animals, although it is
highly likely that this phenomenon is controlled by multiple host and
viral genes.
2,6Gal, SA2,3Gal, and only NeuAc, while horse erythrocytes contain primarily NeuGc and SA2,3Gal (12).
These findings suggest that duck viruses recognize NeuGc2,3Gal
molecules, but experimental support for such an association is lacking.
2-macroglobulin-resistant R3 variant (with a Leu-to-Gln mutation at position 226 in the HA) did not replicate in duck intestine. A single additional mutation at position 228 (Ser to Gly)
endowed a nonreplicating human (HA with a Leu-to-Gln mutation at
position 226)-avian (all other genes) reassortant virus with enterotropism in ducks (21, 35). However, it was not known how these mutations convert the human virus HA to one supporting viral
replication in duck intestine. We therefore analyzed the receptor
specificities of duck and human influenza viruses and determined the
distribution of oligosaccharide molecules in duck intestine.
2,6Gal have not been found in nature, we did not examine the HA
specificity for this molecule. The human Udorn virus preferentially
recognized NeuAc2,6Gal, as previously shown (3), whereas
the Mal/NY virus bound to all three gangliosides tested,
II3(NeuGc)LacCer, II3(NeuAc)LacCer, and
II6(NeuAc)LacCer, thus recognizing NeuAc2,6Gal,
NeuAc2,3Gal, and NeuGc2,3Gal (Fig. 1A). A mutation from Leu to
Gln at position 226 (R3 virus) shifted the specificity of the human
Udorn virus HA from NeuAc2,6Gal to NeuAc2,3Gal, as previously
reported (26). However, the R3 virus preferentially
recognized NeuAc2,3Gal but recognized NeuGc2,3Gal only
marginally. Interestingly, an additional mutation from Ser to Gly at
position 228 (R2) made the virus recognize NeuGc2,3Gal equally well.
Because the mutation converted R3 virus to one that grows in duck
intestine (i.e., R2 virus) (21), these findings suggested
the importance of the recognition of NeuGc, in addition to the 2,3
linkage, for the replication of influenza virus in duck intestine.
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FIG. 1.
Comparison of receptor specificity among duck, human,
and reassortant influenza viruses. To determine the receptor
specificity of the viruses, we relied on a TLC-virus binding assay
using lacto-series gangliosides containing the type I sugar chain.
i.e., NeuAc 2,6 lactotetraosyl ceramide
[II6(NeuAc)LacCer](NeuAc2,6), NeuAc2,3,
lactotetraosyl ceramide [II3(NeuAc)LacCer](NeuAc2,3),
and NeuGc2,3 lactotetraosyl ceramide
[II3(NeuGc)LacCer](NeuGc2,3), as described previously
(33). Each ganglioside (1 nmol) was applied to a silica gel
(Polygram Sil G plate; Nagel) that was developed in
chloroform-methanol-12 mM MgCl2 (5/4/1, vol/vol/vol) and
dried. After being blocked by phosphate-buffered saline supplemented
with 1% egg albumin and 1% polyvinylpyrrolidone (solution A) at room
temperature for 2 h, the plate was incubated with purified virus
(28 hemagglutinating units) suspended in phospate-buffered
saline for 12 h at 4°C. After being washed with
phosphate-buffered saline, the plate was blocked with solution A and
incubated with a pool of 11 monoclonal antibodies at 4°C for 2 h. After being washed with phosphate-buffered saline and blocked again
with solution A, the plate was incubated at 4°C for 2 h with
horseradish peroxidase-conjugated protein A and then incubated with the
substrate solution (0.1 M citrate buffer [pH 6.0]-3%
4-chloro-1-naphthol in methanol- 3% aqueous
H2O2 [5/1/0.01, vol/vol/vol]) at room
temperature for 20 min. The binding activity of the virus was
determined by scanning the stained chromatogram at 629 nm with a TLC
scanner (CSR-9000; Shimazu, Kyoto, Japan). The results were recorded as
the relative binding reactivity of virus with gangliosides, with the
highest reactivity set at 100. (A) Receptor specificities of Udorn,
Mal/NY, and reassortant viruses possessing a mutation(s) in the Udorn
HA; (B) receptor specificities of other avian viruses.
2,3Gal. All seven duck viruses in this study, representing a variety of HA subtypes, recognized NeuGc2,3Gal, though less readily than NeuAc2,3Gal in most cases (Fig. 1B). The ability to
recognize NeuGc2,3Gal was marginal for A/duck/Ukraine/1/63 (H3N8),
as shown before (6). Since this virus has been passaged extensively in chicken eggs, which lack NeuGc (16), the lack of NeuGc recognition might be due to egg adaptation and the virus may
no longer replicate in ducks. We therefore tested its replicative potential in duck intestine. One-day-old mallards (Anas
platyrhynchos platyrhynchos) were purchased from Ridgeway
Hatcheries Inc., La Rue, Ohio) and used at 6 to 12 weeks of age. The
ducks were orally inoculated with 0.5 ml of allantoic fluid containing
107.0 50% egg infective doses (EID50) of
virus. They were sacrificed for the isolation of virus from organs at 3 days postinfection. The viruses in colon were titrated in eggs as
described previously (14). A/duck/Ukraine/1/63 (H3N8) virus
was recovered from only one of six ducks, and in the virus-positive
duck, the virus titer in colon was 101.3
EID50/g. By contrast, other duck viruses with substantial
ability to recognize NeuGc2,3Gal [e.g., A/duck/Hokkaido/8/80 (H3N8)
and Mal/NY (H2N2)] replicated well in duck intestine, with titers of
104 EID50/g. Thus, NeuGc2,3Gal recognition
does in fact seem to be associated with the efficient intestinal
replication of influenza virus in ducks. Some influenza A viruses also
recognize NeuAc2,6Gal [A/teal/Alberta/69/87 (H1N4) in the
present study; also see references 24 and
25], but the biologic significance of this capacity is unclear.
Sialyloligosaccharide analysis of the epithelial cells of duck
intestine.
The above observations demonstrating preferential
recognition of the NeuGc2,3Gal linkage by viruses able to replicate
in duck intestine prompted us to identify the glycoconjugate that possesses the NeuGc2,3Gal linkage in this organ. We recently showed
that the epithelial cells of duck intestine contain SA2,3Gal but not
SA2,6Gal, using SA-Gal linkage-specific lectins (13), but
these lectins did not allow us to distinguish between NeuAc and NeuGc.
Thus, we incubated frozen sections of duck and chicken (negative
control) intestine or MDCK cells (positive control) with chicken
antihematoside antibody (which specifically recognizes NeuGc2,3Gal
but not NeuAc2,3Gal [9]) and then with
fluorescein-conjugated anti-chicken immunoglobulin antibody. Although
it failed to react with chicken intestine (Fig.
2F), which lacks NeuGc (16),
the antiserum did react with NeuGc-containing MDCK cells (Fig. 2E), confirming its specificity. The crypt cells of duck colon (Fig. 2A)
epithelium reacted with the antiserum, demonstrating the presence of
NeuGc. The epithelial cells of duck jejunum (Fig. 2C) and cecum (Fig.
2B) were also positive (though to a lesser extent), while those of
duodenum (Fig. 2D) were not, suggesting that much higher concentrations
of NeuGc are present in the lower intestine of ducks.
|
2,3Gal, albeit as a minor species. This
limited amount of NeuGc among the total sialic acid content in duck
intestine seems reasonable, since only crypt cells reacted with
antiserum to NeuGc2,3Gal.
Preferential replication of avian influenza virus in the crypt
cells of duck intestine.
To determine whether the presence of
NeuGc in crypt cells of duck intestine is important for viral
replication, we performed immunofluorescence assays of thin sections of
duck colon infected with A/duck/Hokkaido/5/77 (H3N2) virus (Fig.
3). The pooled monoclonal antibodies to
the NS1 protein detected viral antigens mainly in the crypt cells, in
accord with a previous finding (14). Thus, NeuGc
localization is associated with the efficient replication of duck
viruses.
|
2,3Gal is associated with the efficient replication of
influenza viruses in duck intestine. The HAs of all duck viruses tested (with the exception of A/duck/Ukraine/1/63) recognized this moiety, while those of human viruses did not. The R3 virus, which efficiently recognized NeuAc2,3Gal but not NeuGc2,3Gal, failed to
replicate in duck intestine, whereas the R2 mutant, which
efficiently recognized both NeuAc2,3Gal and NeuGc2,3Gal,
replicated well (8). These findings indicate that the
recognition of NeuAc linked to galactose by the 2,3 linkage is not
sufficient to support influenza A virus replication in duck intestine.
Rather, NeuGc recognition also appears to be essential. In accord with
the receptor specificity of the HA and viral replication in ducks,
SA2,3Gal but not SA2,6Gal is predominant (13) and
NeuGc2,3Gal was found in the crypt cells of duck colon epithelium
(Fig. 2), the exclusive site of viral replication (Fig. 3). However,
duck viruses can recognize NeuAc2,3Gal, which is also present
in duck intestine. Why do other intestinal cells likely possessing
NeuAc2,3Gal fail to support viral replication? One possibility is
that molecules containing NeuGc2,3Gal serve as functional receptors,
while those possessing NeuAc2,3Gal do not. Collectively, our data
indicate the importance of both the sialic acid species and the type of
linkage between sialic acid and galactose in establishing the host
range of influenza viruses. Additional support for this hypothesis
comes from a recent study in which we show that the recognition of
NeuGc is also critical for influenza virus replication in horses
(unpublished data).
H3 human viruses isolated in 1968 recognize only NeuAc, whereas those
isolated after 1972 recognize both NeuAc and NeuGc (6). The
biologic significance of this change is unknown. Since human cells lack
NeuGc (15, 16), the acquisition of NeuGc specificity cannot
be attributed to the adaptation of the virus in humans. In light of the
present finding that recognition of NeuGc2,3Gal is associated with
viral replication in ducks and that the HA of human H3 viruses was
introduced from wild birds, we suggest that the human virus isolated in
1968 lost its ability to recognize NeuGc to accommodate its change in
linkage specificity from 2,3 (avian type) to 2,6 (human type) or
perhaps because of other (unknown) requirements for adaptation to a new
environment (i.e., human cells). During subsequent replication in
humans, the virus may have undergone further amino acid changes to
escape immunologic pressures, rendering it capable of NeuGc recognition.
This report appears to be the first to document the presence of NeuGc
in avian species. This sialic acid has not been identified in normal
human and chicken tissues (15, 16) but is commonly found in
cows, horses, and pigs (16, 18, 22, 23). Hence, equine and
swine influenza viruses would be expected to recognize both NeuGc and
NeuAc, a prediction supported by previous findings (6, 32).
Higa et al. (6) reported that two duck viruses, including
A/duck/Ukraine/1/63, failed to recognize NeuGc2,3Gal on
enzymatically modified erythrocytes, while two others reacted. The
majority of duck viruses in our study recognized NeuGc2,3Gal. One
exception was the A/duck/Ukraine/1/63 virus, which bound to this
glycoconjugate only weakly and failed to replicate well in duck
intestine, further emphasizing the essential role of NeuGc2,3Gal
recognition in the successful replication of influenza A viruses in ducks.
Couceiro et al. (4) showed that in addition to the
predominance of the NeuAc2,6Gal linkage in human tracheal epithelial cells, human bronchial mucin, which contains sialic acid primarily with
the NeuAc2,3Gal linkage (17), can potently inhibit the binding of NeuAc2,3Gal-recognizing viruses to tracheal sections. This finding suggests that a combination of a missing receptor moiety
and the presence of receptor analog inhibitors could protect humans
from infection by avian influenza viruses. Such strategies may well
prove useful in the influenza armamentarium but are not likely to
provide universal protection, as demonstrated by the direct
transmission of H5N1 avian influenza viruses from birds to humans
during the recent outbreak in Hong Kong (2, 31). By
contrast, previous studies demonstrate strict restriction of a virus
possessing the human virus HA in duck intestine (8). These
findings suggest that the extent of host range restriction controlled
by the HA appears to depend on the combination of host animal species
and virus.
In this study, we focused on the receptor specificity of the HA.
However, the genes of influenza A viruses encoding internal proteins in
addition to the HA and NA may also play roles in host range
restriction. For example, the NP and M genes can attenuate avian
influenza virus infection in squirrel monkeys (34), and depending on the human influenza viruses used to prepare reassortants with avian viruses, a combination of polymerase genes may affect viral
replication in this host animal (29, 30). Further studies are needed to fully delineate the contribution of these gene products to host range restriction.
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ACKNOWLEDGMENTS |
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We thank Martha McGregor for excellent technical assistance, Robert G. Webster for NS1 monoclonal antibodies, and John Gilbert for editing the manuscript. We also thank Mikhail Matrosovich for useful discussion.
Support for this work came from National Institute of Allergy and Infectious Diseases Public Health Service research grants.
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FOOTNOTES |
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*
Corresponding author. Mailing address: Department of
Pathobiological Sciences, School of Veterinary Medicine, University of WisconsinMadison, 2015 Linden Dr. West, Madison, WI 53706. Phone: (608) 265-4925. Fax: (608) 265-5622. E-mail:
kawaokay{at}svm.vetmed.wisc.edu.
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Journal of Virology, October 2000, p. 9300-9305, Vol. 74, No. 19
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Copyright © 2000, American Society for Microbiology. All rights reserved.
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