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Journal of Virology, December 2000, p. 11825-11831, Vol. 74, No. 24
Department of Biochemistry, School of Pharmaceutical
Sciences, University of Shizuoka, Yada, Shizuoka-shi
422-8526,1 Department of Veterinary
Public Health, Faculty of Agriculture, Tottori University, Tottori
680-8553,2 Department of Applied
Bioorganic Chemistry, Gifu University, Gifu
501-1193,4 and Institute of Medical
Science, University of Tokyo, Minato-ku, Tokyo
108-8639,6 Japan; Department of
Veterinary Science, Gluck Equine Research Center, University of
Kentucky, Lexington, Kentucky 405463; and
Department of Pathobiological Sciences, School of
Veterinary Medicine, University of Wisconsin-Madison, Madison,
Wisconsin 537065
Received 3 May 2000/Accepted 14 September 2000
The distribution of sialic acid (SA) species varies among animal
species, but the biological role of this variation is largely unknown.
Influenza viruses differ in their ability to recognize SA-galactose
(Gal) linkages, depending on the animal hosts from which they are
isolated. For example, human viruses preferentially recognize SA linked
to Gal by the Sialic acid (SA) is a generic term
for nine-carbon acidic amino sugars
(5-amino-3,5-dideoxy-D-glycero-D-galacto-nonulosonic acid). The amino group is always substituted with either an
N-acetyl or N-glycolyl group, yielding
N-acetylneuraminic (NeuAc) or
N-glycolylneuraminic (NeuGc) acid, respectively (Fig.
1), while the hydroxyl groups can be
substituted by acetyl, lactoyl, methyl, sulfate, or phosphate residues.
The distribution of specific SAs varies among animal species. For
example, bovine, equine, and swine tissues possess both NeuAc and
NeuGc, whereas human tissues possess only slight concentrations of
NeuGc (less than 0.1% of total SA) (21, 22). Although a
difference in the distribution of SAs among different animal species
has been recognized for many years (11, 22, 25, 28, 30, 34, 35,
47), its biological significance is largely unknown.
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Sialic Acid Species as a Determinant of the Host
Range of Influenza A Viruses
ABSTRACT
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
2,6(SA2,6Gal) linkage, while equine viruses favor
SA2,3Gal. However, whether a difference in relative abundance of
specific SA species (N-acetylneuraminic acid [NeuAc] and
N-glycolylneuraminic acid [NeuGc]) among different animals affects the replicative potential of influenza viruses is
uncertain. We therefore examined the requirement for the hemagglutinin (HA) for support of viral replication in horses, using viruses whose
HAs differ in receptor specificity. A virus with an HA recognizing NeuAc2,6Gal but not NeuAc2,3Gal or NeuGc2,3Gal failed to
replicate in horses, while one with an HA recognizing the
NeuGc2,3Gal moiety replicated in horses. Furthermore, biochemical
and immunohistochemical analyses and a lectin-binding assay
demonstrated the abundance of the NeuGc2,3Gal moiety in epithelial
cells of horse trachea, indicating that recognition of this moiety is
critical for viral replication in horses. Thus, these results provide
evidence of a biological effect of different SA species in different animals.
INTRODUCTION
Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
View larger version (12K):
[in a new window]
FIG. 1.
Structure of N-acetyl and
N-glycolylneuraminic acids. These SA differ at position 5 of
the pyranose ring. N-Acetylneuraminic acid is the precursor
of N-glycolyneuraminic acid; enzymatic hydroxylation of the
former results in the latter.
Influenza A viruses have been isolated from a variety of animals, including humans, pigs, horses, sea mammals, poultry, wild ducks, and other migrating waterfowl (49). Among these animals, wild waterfowl serve as the reservoir from which all influenza viruses are thought to have emerged (49). The causative viruses of the 1957 Asian and 1968 Hong Kong pandemics are in fact reassortants between human and avian influenza viruses (18, 23, 36), illustrating the introduction of avian viral genes into the human population. Despite the apparent common origin of influenza A viruses, their host range is clearly restricted. In experimental infections, avian influenza viruses replicate poorly in primates (3, 27, 38, 39), while human isolates do not replicate efficiently in ducks (13, 19, 50). There are exceptions, however, including an avian influenza virus that was directly transmitted from birds to humans in the Hong Kong outbreak of 1997 (5, 40). Although several genes are known to be involved in host range restriction of influenza viruses (37, 38, 39, 41, 45), the precise contribution(s) of each gene product has not been defined.
The hemagglutinin (HA) of influenza A viruses, a type I membrane
glycoprotein, is responsible for binding of the virus to cell surface
receptors, or sialyloligosaccharides. Although all influenza viruses
recognize oligosaccharides containing a terminal SA, the specificity of
the HA towards these molecules differs. Avian and equine influenza
viruses preferentially bind the sialic acid-2,3-galactose
(SA2,3Gal) linkage, while human influenza viruses preferentially
bind the SA2,6Gal linkage (6, 31, 32). Influenza viruses
also differ in their recognition of NeuAc, NeuGc, and
9-O-Ac-NeuAc (12). However, the importance of
differential recognition of these SA species for host range restriction
of influenza virus remains unknown.
Couceiro et al. (7) reported the presence of
sialyloligosaccharides reactive with an SA2,6Gal- but not
SA2,3Gal-specific lectin on the surface of epithelial cells of human
trachea. We recently showed that pig trachea contains
sialyloligosaccharides reactive with both SA2,6Gal- and
SA2,3Gal-specific lectins, while duck intestine, the major
replicative site of avian influenza viruses, possesses only
sialyloligosaccharides reactive with the SA2,3Gal-specific lectin
(16). These findings showed that the availability of
receptors (i.e., SA2,6Gal and SA2,3Gal moieties) in host animals
correlates with the receptor specificity of influenza viruses isolated
from the host animals. Although it is highly likely that this
phenomenon is controlled by multiple host and viral genes, these data
suggest that receptor specificity is one of the important determinants
of host range restriction among influenza viruses.
Because NeuGc is barely detectable in humans (less than 0.1% of total SA) (21, 22) but is abundant in horses (more than 97% of total SA in horse erythrocytes) (43), we reasoned that a difference in the recognition of SAs might play an important role in the host range restriction of influenza viruses. Here we show for the first time that the SA distribution in animal species does in fact influence influenza virus host range.
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MATERIALS AND METHODS |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Viruses. The viruses used in this study were obtained from repositories at St. Jude Children's Research Hospital and the University of Kentucky. They were propagated in the allantoic cavities of 11-day-old embryonated chicken eggs at 35°C for 2 days.
Genetic reassortment. Reassortant influenza viruses between A/equine/Kentucky/1/91 (H3N8) and A/Udorn/307/72 (H3N2), R2, or R3 viruses (13) were prepared in chicken embryos as previously described (48). Reassortants were biologically cloned at limiting dilutions in eggs.
Genotyping of reassortant viruses. The genotypes of the reassortant viruses were determined by partial sequence analysis of each gene using reverse transcription-PCR (17). The sequences of the oligonucleotides used as primers will be supplied upon request.
Immunologic detection of SA2,3Gal and SA2,6Gal in animal
tissues.
Horse trachea was obtained at a slaughter house in
Hokkaido, Japan, and shipped to our laboratory on ice. It was then
rinsed with phosphate-buffered saline (PBS, pH 7.2) before being cut into 3-mm3 cubes. The tissue block was embedded in OCT
compound (Miles Inc.) and frozen in liquid nitrogen. Sections of each
tissue (6 µm) were cut with a microtome cryostat, air dried, and
fixed for 15 min with cold acetone before immunostaining.
2,3Gal- or
SA2,6Gal-specific lectins (glycan determination kit; Boehringer Mannheim Biochemicals, Mannheim, Germany), we incubated each section with 50 µl of digoxigenin (DIG)-labeled Sambucus nigra
(SNA) lectin [1 µg/ml; specific for SA2,6galactose
(Gal)/N-acetylgalactosaminide (GalNac)] or Maackia
amurensis (MAA) lectin (5 µg/ml; specific for the SA2,3Gal)
for 1 h at room temperature. After three washes with cold PBS, the
sections were incubated with fluorescein- and rhodamine-conjugated
anti-DIG antibody (Boehringer Mannheim Biochemicals), respectively, for
1 h at room temperature and then, after three additional washes in
cold PBS and buffered glycerol (pH 9.0), were mounted for observation.
Control slides were incubated with PBS instead of lectin. All sections
were examined with a fluorescence microscope (BH-RFL; Olympus Optics,
Tokyo, Japan) equipped with a dark-field condenser and UV excitation.
NeuGc linked to Gal by 2,3 was also immunologically detected using a
chicken antiserum against hematoside [GM3 (NeuGc);
II3(NeuGc)LacCer] (14, 15) that reacts with
NeuGc2,3Gal in both glycoproteins and glycolipids. The reactivity of
this antiserum with tissue sections was tested as described above for
lectins except that the secondary antibodies were conjugated with biotin.
SA determination by liquid chromatography. The molecular species of SA (NeuAc or NeuGc) in gangliosides of epithelial cells in horse trachea was determined by a high-pressure liquid chromatography method using 1,2-diamino-4,5-methylenedioxybenzene (DMB), as described previously (11, 42). Epithelial cells (10 mg) were hydrolyzed with 200 µl of 25 mM sulfuric acid. The hydrolysate was reacted with DMB reagent and heated at 60°C for 2.5 h in the dark to develop the fluorescence of SA. A 10-µl aliquot of the solution was used for these determinations.
Experimental infection of ponies. The ponies used in these experiments all lacked serological evidence of prior influenza virus infection or vaccination (titers < 10) in hemagglutination inhibition tests for antibodies to H3N8 equine viruses. The different groups of ponies (three per group) were exposed to aerosolized virus (DeVilbiss Ultra-Neb 99 nebulizer) through a face mask for approximately 10 min (4). Each pony received 107 50% egg infections doses (EID50) of virus (in 5 ml). The four groups, each representing a single virus, were isolated from each other by either physical or time barriers; the ponies were kept in individual stalls. Nasopharyngeal swabs were taken daily, beginning just before infection (day 0) and continuing through day 9. The viruses in the swabs were titrated in eggs as described (19).
Virus-binding assay. To determine the receptor specificity of the viruses, a thin-layer chromatography/virus-binding assay was performed with gangliosides GM3 II3(NeuGc)LacCer, II3(NeuAc)LacCer, and II6(NeuAc)LacCer, as described previously (44).
Nucleotide sequencing. Viral RNA was isolated as in earlier studies (2), and cDNA was synthesized with reverse transcriptase and random hexamers as described (17). Direct sequencing of the PCR products was done with an autosequencer (Applied Biosystems Inc.) according to the protocol recommended by the company. The sequences of oligonucleotides used as primers will be supplied upon request.
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RESULTS |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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NeuGc2,3Gal is abundant in the epithelial cells of horse
trachea.
We first examined the prevalence of SA2,6Gal and
SA2,3Gal moieties in epithelial cells in horse trachea, using SA-Gal
linkage-specific lectins. SNA lectin, specific for SA2,6Gal
linkages, did not react with horse trachea but did react with pig
trachea (positive control) (Fig. 2). By
contrast, MAA lectin, specific for SA2,3Gal linkages, reacted with
horse trachea as well as pig trachea. These results establish the
predominance of the SA2,3Gal moiety in the replication site of
influenza virus in horses.
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2,3Gal but not the SA2,6Gal moiety was detected by the lectin assay and the
vast majority of SA in epithelial cells were NeuGc, these findings
suggested that the major SA-Gal moiety present in horse tracheal
epithelial cells is NeuGc2,3Gal. To directly detect this moiety, we
examined the reactivity of thin sections of horse trachea with a
chicken antiserum against hemtoside [GM3(NeuGc); II3(NeuGc)LacCer] (14, 15), which contains the
NeuGc2,3Gal structure. This antiserum reacts with both gangliosides
and glycoproteins possessing terminal NeuGc2,3Gal but not with
glycoconjugates possessing either NeuAc2,3Gal or NeuAc2,6Gal (Y. Suzuki, unpublished data). As shown in Fig.
4, the antiserum bound to epithelial
cells lining horse trachea but not with those of chicken trachea, which lack NeuGc (8). These results demonstrate the abundance of the NeuGc2,3Gal moiety in the epithelial cells of horse trachea.
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Equine but not human influenza viruses recognize NeuGc2,3Gal
moiety.
Although human influenza viruses have been transmitted to
pigs and vice versa (10, 24, 29, 33, 46, 51), human-to-horse transmission remains to be reported. The finding of differences in
sialyloligosaccharide species in tracheal epithelial cells between
humans (predominantly NeuAc2,6Gal) and horses (predominantly NeuGc2,3Gal) suggested that recognition not only of SA-Gal linkages but also of SA species may be responsible for lack of transmission of
human viruses to horses and vice versa. We therefore examined the
receptor specificity of these viruses. Human influenza viruses preferentially recognized the NeuAc2,6Gal moiety, whereas equine viruses preferentially recognized NeuAc2,3Gal over
NeuAc2,6Gal, as has been shown previously (31) (Fig.
5). Interestingly, equine viruses also
recognized the NeuGc2,3Gal moiety, although one virus
(A/equine/Miami/1/63 [H3N8]), which has been passaged extensively in
embryonated chicken eggs lacking NeuGc, bound poorly to this moiety.
Because the predominant SA-Gal moiety differs between the epithelial
cells of human and horse trachea (see above), these results suggest a
role for HA-sialyloligosaccharide specificity in host range restriction
of human and equine influenza viruses.
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NeuGc2,3Gal recognition is essential for viral replication in
horses.
Our recent study showed that the HA of a human influenza
virus, A/Udorn/307/72 (H3N2) (Udorn), preferentially recognizes
NeuAc2,6Gal, but not NeuAc2,3Gal or NeuGc2,3Gal (T. Ito et al,
unpublished data). However, a mutation at position 226 of this HA from
Leu to Gln (L226Q) made it preferentially recognize the NeuAc2,3Gal but not the NeuGc2,3Gal moiety. Another mutation at position 228, from Ser to Gly, thus L226Q and S228G mutations, made the HA recognize
both the NeuAc2,3Gal and NeuGc2,3Gal moieties (Table 1). These human virus HAs provided useful
tools with which to study the role of HA receptor specificity in the
host range restriction of influenza viruses. We therefore designed
experiments in which these HAs were used to examine the contributions
of receptor specificity and availability of host receptors to host
range restriction. To limit the effects of viral gene products to the
HA, we made three reassortant viruses possessing these mutant HAs, with
the remainder of the genes coming from an equine virus,
A/equine/Kentucky/1/91 (H3N8) (Eq/Ky). Udorn-Eq/Ky virus contains the
human virus Udorn HA, L226Q-Eq/Ky virus contains the Udorn L226Q mutant
HA, and L226Q/S228G-Eq/Ky virus contains the Udorn HA mutant possessing both the L226Q and S228G alterations. We then tested the replicative capacity of these reassortants, as well as the parent Eq/Ky virus, in
ponies. As expected, Eq/Ky virus, whose HA recognizes not only the
NeuAc2,3Gal but also the NeuGc2,3Gal moiety, replicated for up to
1 week (5 days in two ponies and 8 days in one pony), producing titers
ranging from 102.7 to 105.3 EID50
on day 2 (mean virus titer, 104.0 EID50) (Table
1). By contrast, Udorn-Eq/Ky virus, whose HA preferentially recognizes
the NeuAc2,6Gal over the NeuGc2,3Gal moiety, did not replicate in
ponies at all, demonstrating an essential contribution of the HA to
host range restriction. Interestingly, the L226Q-Eq/Ky virus, whose HA
preferentially recognizes the SA2,3Gal linkage with NeuAc while
binding much less avidly to the NeuGc moiety, replicated in one of
three ponies tested, but only for 2 days (101.4
EID50 at 1 day and <101.0 EID50 at
2 days postinfection). However, the L226Q/S228G-Eq/Ky virus,
whose HA recognizes both NeuAc2,3Gal and NeuGc2,3Gal moieties, replicated in all three ponies tested for as long as 1 week
(6 days in one pony and 7 days in two ponies), with titers ranging from
101.8 to 103.8 EID50. These
findings demonstrate that recognition of the NeuGc2,3Gal moiety is
critical for the efficient replication of influenza A viruses in
horses.
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DISCUSSION |
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Top
Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Although a variety of SAs are found in animals and their
distributions differ among animal species, the biological effects of
those differences remain largely unknown. Influenza A viruses differ in
their ability to recognize SA2,6Gal and SA2,3Gal, suggesting a
role for HA-SA specificity in host range restriction. Here we
demonstrate that NeuGc2,3Gal is the dominant moiety on the
epithelial cells of horse trachea and that a difference in sialyloligosaccharides, NeuAc2,6Gal (human) versus NeuGc2,3Gal (horse), on tracheal epithelial cells is a critical factor in differential viral replication. Viruses that failed to recognize the
SA2,3Gal linkage as well as NeuGc did not replicate efficiently in
horses. Thus, the absence or low abundance of a particular SA species
can serve as a host range barrier for influenza A viruses, providing an
example of biological effects related to differences in distribution of
different SAs.
Our recent studies showed that many avian influenza viruses recognize
the NeuGc2,3Gal moiety (16a). We also found that the antiserum specific for the NeuGc2,3Gal moiety reacted with
epithelial cells of duck colon crypt, although by chemical analysis the
ratio of NeuGc to NeuAc in colon epithelial cells was low (2 versus 98%). These findings would explain the transmission of an avian influenza virus to horses in China, resulting in the death of 20% of
the horse population (9).
The results of the current study demonstrate restriction of influenza
virus transmission from humans to horses. This finding explains why no
human viruses have been isolated from horses, while they have
transmitted into pigs multiple times (10, 24, 29, 46, 51).
Pig trachea contains both the SA2,6Gal and SA2,3Gal moieties
(16). In fact, pigs efficiently support the replication of
avian influenza viruses (20), which preferentially recognize
the SA2,3Gal moiety (31). These studies emphasize the
importance of the availability of receptor sialyloligosaccharides and
receptor specificity in the host range restriction of influenza viruses, which likely plays an important role in the evolution of these
viruses. Why, then, was an avian virus that binds preferentially to
SA2,3Gal transmitted to humans in Hong Kong in 1997 (5, 26,
40)? It seems that the magnitude of the contribution of receptor
specificity to host restriction depends on the combination of host
animal and virus strain. In horses, for example, the ability of the
virus to recognize a specific receptor is essential for efficient
replication, while in humans, the recognition of NeuAc2,6Gal does
not appear to be essential for replication of the virus. In support of
this notion, we found that human tracheal epithelial cells possess
sialyloligosaccharides reactive with SA2,3Gal linkage-specific lectin, although oligosaccharides reactive with SA2,6Gal-specific lectin were more prevalent (P. Gao and Y. Kawaoka, unpublished data),
suggesting that the amount of SA2,3Gal in the epithelial cells of
human trachea is sufficient for at least the initiation of viral
replication. Whether the same relationship between SA2,3Gal and
SA2,6Gal linkages extends to other human tissues, such as lung, is
unclear. However, the first available human isolates from the 1957 and
1968 pandemics preferentially recognized the SA2,6Gal moiety, even
though their HAs were derived from an avian virus (23, 36);
thus, for efficient human-to-human transmission, the viruses may need
to recognize SA2,6Gal more avidly than SA2,3Gal. In addition to
the receptor molecules on epithelial cells, sialyloligosaccharides in
body fluids may also play a role in the host range restriction of
influenza viruses. Horse serum contains 2-macroglobulin
containing 4-O-acetyl-SA. Because influenza virus
neuraminidase (NA) cannot cleave this SA from oligosaccharides,
glycoproteins containing this SA serve as a potent receptor analog
inhibitor. Thus, sialyloligosaccharides in body fluid, as well as those
on the cell surface (i.e., receptor), contribute to the evolution of
influenza viruses.
Influenza viruses possess both receptor-binding (HA) and
receptor-destroying (NA) proteins. Thus, the receptor specificity of
the HA and the substrate specificity of the NA may work in concert to
determine the efficiency of influenza virus replication. In fact, Baum
and Paulson (1) reported that the human influenza virus NA,
which was introduced from an avian virus, gradually acquired the
ability to cleave the SA2,6Gal as well as SA2,3Gal linkage. This
finding suggests that viral selection favors enzymes whose substrate
specificity matches the receptor specificity of the human virus HA
(i.e., SA2,6Gal specificity).
In this study, we focused on the receptor specificity of the HA as a critical determinant of host range restriction. Future research will need to test the possibility that other genes encoding internal proteins could also contribute to this natural barrier to unimpeded replication. For example, the NP and M genes are responsible for the attenuation of avian viruses in squirrel monkeys (45), and depending on the human influenza viruses used to prepare reassortants with avian viruses, a combination of polymerase genes was found to affect the ability of these reassortant viruses to replicate in squirrel monkeys (38, 39, 41). Thus, the mechanism responsible for host range restriction likely entails a complex interplay of viral and host gene products.
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ACKNOWLEDGMENTS |
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We thank Krisna Wells, Martha McGregor, Lynn Tudor, and Eugene Ferguson for excellent technical assistance and John Gilbert for editing the manuscript.
Support for this work came from the Ministry of Education and Culture of Japan (Y.S. and T.S.), National Institute of Allergy and Infectious Diseases, Public Health Service, research grants (Y.K.), Hatch-Kentucky Agricultural Experiment Station project no. KY014006 (T.M.C.), and the late Paul Mellon (T.M.C.).
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Pathobiological Sciences, School of Veterinary Medicine, University of Wisconsin-Madison, 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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REFERENCES |
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Abstract
Introduction
Materials and Methods
Results
Discussion
References
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Journal of Virology, December 2000, p. 11825-11831, Vol. 74, No. 24
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