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Journal of Virology, August 2000, p. 7691-7693, Vol. 74, No. 16
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Initial Interactions of Subgenus D Adenoviruses
with A549 Cellular Receptors: Sialic Acid versus 
v
Integrins
Niklas
Arnberg,*
Alistair H.
Kidd,
Karin
Edlund,
Farzad
Olfat, and
Göran
Wadell
Department of Virology, University of Umeå,
S-90185 Umeå, Sweden
Received 10 January 2000/Accepted 16 May 2000
 |
ABSTRACT |
Selected members of the adenovirus family have been shown to
interact with the coxsackie adenovirus receptor, 
v
integrins, and sialic acid on target cells. Initial interactions of
subgenus D adenoviruses with target cells have until now been poorly
characterized. Here, we demonstrate that adenovirus type 8 (Ad8),
Ad19a, and Ad37 use sialic acid as a functional cellular
receptor, whereas the Ad9 and Ad19 prototypes do not.
| |
TEXT |
The 51 human adenovirus (Ad)
serotypes fall into six subgenera, A through F (8, 20).
Several adenoviruses of subgenus D exhibit tropism for the human eye
(4, 5, 10, 13), but Ad8, Ad19a, and Ad37 are the only types
which are frequently associated with epidemic keratoconjunctivitis
(10, 13). Adenovirus binding to target cells is mediated by
its fiber (7, 9, 12, 18), and the cellular receptor for most
adenoviruses, including Ad9 and Ad19p of subgenus D, has been
identified recently as the coxsackie adenovirus receptor (CAR) (6,
17, 19). Ad37 was found recently to use (2
3)-linked sialic
acid as a receptor (2) instead of CAR. Ad9 has been shown to
use its penton base to interact with v integrins not
only during internalization, which is the proposed mechanism for most
adenoviruses (14), but also during attachment to target
cells (18). Here, we investigated the role of sialic acid
and v integrins during the early steps of infection for
five distinct subgenus D adenoviruses.
Sialic acid is used as a primary receptor by Ad8, Ad19a, and
Ad37.
Using 35S-labeled adenoviruses (7) in
a virus-cell binding assay (2), we found that the
binding of Ad8, Ad19a, and Ad37 to A549 cells was highly sensitive to
neuraminidase treatment of the cells (Fig.
1). We also found that
Ad9 and Ad19p binding was sensitive to neuraminidase treatment of
cells, but to a lesser extent. These results suggested that the
adenoviruses Ad8, Ad19a, and Ad37 all use sialic acid as cellular
receptors. At this point, we could not exclude the possibility that
sialic acid was also used as a receptor by Ad9 and Ad19p.
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FIG. 1.
Interaction of subgenus D adenoviruses with A549 cells.
A total of 2 × 105 A549 cells in suspension were
treated with (i) anti- 2 integrin MAb P4H9 on ice
(negative control), (ii) anti-v integrin MAbs P1F6 and
LM609 on ice, (iii) neuraminidase (Vibrio cholerae) at
37°C, or (iv) first with P1F6 and LM609 and then with neuraminidase.
The binding of 35S-labeled virions to the cells was
measured in a Wallac scintillation counter. Data are the means of three
independent experiments.
|
|
The penton base proteins of most, but not all, adenoviruses contain
v-integrin-recognizing RGD (Arg-Gly-Asp) motifs
(
1).
The
v5 integrins have
been shown to interact with most adenoviruses,
supporting their
internalization into the host cell (
15). Nucleotide
sequencing and comparison of the respective penton base proteins
revealed that they all contained the RGD motif (Fig.
2). Full-length
penton base genes of
Ad19p, Ad19a, and Ad37 were generated by
PCR (
3) and
sequenced as described earlier (
3). An incomplete
Ad9 penton
base gene was generated by PCR (
3) and sequenced
by
Cybergene (Huddinge, Sweden). The RGD-flanking region of Ad8
has been
published (
1). Other than for the regions flanking
the RGD
motifs, the Ad9, Ad19a, Ad19p, and Ad37 sequences were
highly
homologous. Function-blocking monoclonal antibodies (MAbs)
against
v integrins inhibited Ad9 and Ad19p binding to A549
cells
significantly more than the binding of Ad8, Ad37, and Ad19a to
A549 cells (Fig.
1). Cotreatment of the cells with neuraminidase
and
v MAbs had little additional effect beyond what was
achieved
with neuraminidase alone (Ad8, Ad19a, and Ad37) or with
v MAbs
alone (Ad9 and Ad19p). Taken together, these
experiments indicated
that sialic acid is a functional attachment
molecule for Ad8,
Ad19a, and Ad37, and that Ad9 and Ad19p are more
dependent on
v integrins for attachment to target cells.
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FIG. 2.
Amino acid sequences of the variable RGD-flanking
regions in the penton base of five subgenus D adenoviruses. The
conserved RGD motifs are shown in boldface, and conserved amino acids
are indicated by asterisks. The GenBank accession numbers are AF217407
(Ad9), AF217408 (Ad37), AF217409 (Ad19p), and AF217410 (Ad19a). The
sequence of Ad8 is from Albinsson and Kidd (1).
|
|
Sialic acid is a functional receptor for Ad8, Ad19a, and Ad37 but
not for Ad9 or Ad19p.
To determine the role of sialic acid and
v integrins as functional receptors for subgenus D
adenoviruses, we treated A549 cells with neuraminidase and/or
v MAbs and infected the cells with the different
adenovirus types as described earlier (2), with the
exception that the neuraminidase treatment of the cells was followed by
incubation of virus-infected cells on ice for 1 h, washing, and
warming of the cells thereafter to 37°C. Our immunofluorescence
assays indicated that infection of A549 cells with Ad8, Ad19a, and Ad37
was strongly inhibited by pretreatment of the cells with neuraminidase
(Fig. 3). The efficacy
of Ad8 infection decreased by 60% and that of Ad19a and Ad37
infection decreased by 80%, suggesting that sialic acid is a
functional receptor for these viruses. These data agree with an earlier
observation that Ad8 partially competes for Ad37 binding to
conjunctival cells (12).
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FIG. 3.
Uptake and replication of subgenus D adenoviruses in
A549 cells. A total of 2 × 105 adherent A549 cells
were treated with (i) anti-2 integrin MAb P4H9 on ice
(negative control), (ii) anti-v integrin MAbs P1F6 and
LM609 on ice, (iii) neuraminidase (V. cholerae) at 37°C,
or (iv) first with P1F6 and LM609 and then with neuraminidase. Added
virions were diluted to 5,000 fluorescent focus units (FFU) per virus
type and well, resulting in approximately 100 FFU per view field in
control wells. Data are the means of three independent
experiments.
|
|
We then assayed the ability of subgenus D adenoviruses to infect A549
cells preblocked with
v MAbs (Fig.
3).
v
MAbs did
not appreciably decrease the infectivity of Ad8, Ad19a, and
Ad37,
and the combination of neuraminidase and
v MAbs
had no additional
effect compared to neuraminidase alone. This supports
the suggestion
that sialic acid is used as a functional receptor for
Ad8, Ad19a,
and
Ad37.
Even though the binding assay indicated that sialic acid may support
Ad9 and Ad19p attachment to some extent (Fig.
1B and
C, respectively),
the infectivity assay clearly demonstrated that
a productive infection
by Ad9 or Ad19p does not require sialic
acid (Fig.
3B and C). Rather,
we found that Ad9 infectivity for
A549 cells was significantly
inhibited by
v MAbs (Fig.
3), while
Ad19p infectivity
was not inhibited. The Ad9 result agrees with
the previous finding that
preincubation of A549 cells with soluble
penton base decreased Ad9
virion binding (
18), presumably by
blocking access to
v integrins acting as receptors. The combined
treatment
of neuraminidase and
v MAbs did not further inhibit
Ad9
binding or infection compared to treatment with
v MAbs
alone.
Uniquely, the variable region of the Ad9 penton base contains
three threonines immediately upstream of the RGD motif (Fig.
2).
This is also a feature of vitronectin and fibronectin, proteins
which
interact efficiently with
v integrins. One possible
explanation
for the unusual ability of Ad9 to interact with
v integrins could
be the presence of these threonines.
Most adenoviruses have been
shown to interact with the
v5 integrin heterodimer, and the
most
efficient interaction is exhibited by Ad37 (
15). The
relative
efficiency by which Ad9 interacts with this integrin has not
been
determined, but from the data presented here and from the data
of
others (
18), we would expect this interaction to be among
the most
efficient.
It has been shown previously that Ad19p virions interact with
v5 integrins (
15). In the
binding assay we found that
v integrins were used
by Ad19p, but only to a limited extent. In
the infectivity assay
we found that Ad19p infection was independent
of
v
integrins, and a combination of neuraminidase treatment
and
v MAb preincubation had little or no effect on the entry
of Ad19p. This was unexpected, since the binding assay indicated
that
sialic acid and
v integrins together accounted for 74%
of
the total binding. In part, this may be explained by the known
interaction between Ad19p and CAR (
17). It may also be that
sialic acid and/or
v integrins are used by Ad19p for
binding
and internalization but Ad19p is less competent in replication.
The high particle/PFU ratio (1,600:1) found for Ad19p (
11)
supports
this
suggestion.
Sialic acid appears to be a functional cellular receptor for the
adenovirus types that cause epidemic keratoconjunctivitis
(i.e., Ad8,
Ad19a, and Ad37), and it is found on the surface of
many cell types.
Consequently, the reason for the limited tropism
of these viruses may
lie at a postattachment level (i.e., during
early replication), or at
an even later point, during cell-cell
spread. The latter consideration
has been neglected somewhat in
discussions of virus
tropism.
Adenoviruses have been used as vectors for gene therapy, but with
limited success (
16,
21). Here, we demonstrated that
a
selected group of adenoviruses uses sialic acid as a primary,
functional receptor. Since sialic acid is expressed on most cells,
including erythrocytes, these findings should be useful for the
application of adenovirus-based vectors in human gene
therapy.
| |
ACKNOWLEDGMENTS |
This work was supported by grants from the Swedish Medical Research
Council (K99-06X-0568820C and GT), the Swedish Cancer Foundation
(1547-B99-10X and 1547-B99-08XAC), Lions Foundation (AMP-97-128), and
the Foundation for Advanced Research at Umeå University Hospital.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Department of
Virology, University of Umeå, S-90185 Umeå, Sweden. Phone: 46 90 7852891. Fax: 46 90 129905. E-mail:
niklas.arnberg{at}climi.umu.se.
| |
REFERENCES |
| 1.
|
Albinsson, B., and A. H. Kidd.
1999.
Adenovirus type 41 lacks an RGD v-integrin binding motif on the penton base and undergoes delayed uptake in A549 cells.
Virus Res.
64:125-136[CrossRef][Medline].
|
| 2.
|
Arnberg, N.,
K. Edlund,
A. H. Kidd, and G. Wadell.
2000.
Adenovirus type 37 uses sialic acid as a cellular receptor.
J. Virol.
74:42-48[Abstract/Free Full Text].
|
| 3.
|
Arnberg, N.,
Y. Mei, and G. Wadell.
1997.
Fiber genes of adenoviruses with tropism for the eye and the genital tract.
Virology
227:239-244[CrossRef][Medline].
|
| 4.
|
Bell, S. D.,
T. Rondon Rota, and D. E. McComb.
1960.
Adenoviruses isolated from Saudi Arabia. Six new serotypes.
Am. J. Trop. Med. Hyg.
9:523-526.
|
| 5.
|
Bennett, F. M.,
B. B. Law,
W. Hamilton, and A. MacDonald.
1957.
Adenovirus eye infection in Aberdeen.
Lancet
ii:670-673.
|
| 6.
|
Bergelson, J. M.,
J. A. Cunningham,
G. Droguett,
E. A. Kurt-Jones,
A. Krithivas,
J. S. Hong,
M. S. Horwitz,
R. L. Crowell, and R. W. Finberg.
1997.
Isolation of a common receptor for coxsackie B viruses and adenoviruses 2 and 5.
Science
275:1320-1323[Abstract/Free Full Text].
|
| 7.
|
Defer, C.,
M.-T. Belin,
M.-L. Caillet-Boudin, and P. Boulanger.
1990.
Human adenovirus-host cell interactions: comparative study with members of subgroups B and C.
J. Virol.
64:3661-3673[Abstract/Free Full Text].
|
| 8.
|
de Jong, J. C.,
A. G. Wermenbol,
M. W. Verweij-Uijterwaal,
K. W. Slaterus,
P. Wertheim-Van Dillen,
G. J. J. Van Doornum,
S. H. Khoo, and J. C. Hierholzer.
1999.
Adenoviruses from human immunodeficiency virus-infected individuals, including two strains that represent new candidate serotypes Ad50 and Ad51 of species B1 and D, respectively.
J. Clin. Microbiol.
37:3940-3945[Abstract/Free Full Text].
|
| 9.
|
Gall, J.,
A. Kass-Eisler,
L. Leinwand, and E. Falck-Pedersen.
1996.
Adenovirus type 5 and 7 capsid chimera: fiber replacement alters receptor tropism without affecting primary immune neutralization epitopes.
J. Virol.
70:2116-2123[Abstract].
|
| 10.
|
Gordon, Y. J.,
K. Aoki, and P. R. Kinchington.
1996.
Adenovirus keratoconjunctivitis, p. 877-894.
In
J. S. Pepose (ed.), Ocular infections and immunity. Mosby, St. Louis, Mo.
|
| 11.
|
Green, M.,
M. Pina, and R. C. Kimes.
1967.
Biochemical purification of adenovirus multiplication. XII. Plaquing efficiencies of purified human adenoviruses.
Virology
31:562-565[CrossRef][Medline].
|
| 12.
|
Huang, S.,
V. Reddy,
N. Dasgupta, and G. R. Nemerow.
1999.
A single amino acid in the adenovirus type 37 fiber confers binding to human conjunctival cells.
J. Virol.
73:2798-2802[Abstract/Free Full Text].
|
| 13.
|
Kemp, M. C.,
J. C. Hierholzer,
C. P. Cabradilla, and J. F. Obijeski.
1983.
The changing etiology of epidemic keratoconjunctivitis. Antigenic and restriction enzyme analysis of types 19 and 37 isolated over a 10-year period.
J. Infect. Dis.
148:24-33[Medline].
|
| 14.
|
Mathias, P.,
T. Wickham,
M. Moore, and G. Nemerow.
1994.
Multiple adenovirus serotypes use v integrins for infection.
J. Virol.
68:6811-6814[Abstract/Free Full Text].
|
| 15.
|
Mathias, P.,
M. Galleno, and G. R. Nemerow.
1998.
Interactions of soluble recombinant integrin v5 with human adenoviruses.
J. Virol.
72:8669-8675[Abstract/Free Full Text].
|
| 16.
|
Pickles, R. J.,
D. McCarty,
H. Matsui,
P. J. Hart,
S. H. Randell, and R. C. Boucher.
1998.
Limited entry of adenovirus vectors into well-differentiated airway epithelium is responsible for inefficient gene transfer.
J. Virol.
72:6014-6023[Abstract/Free Full Text].
|
| 17.
|
Roelvink, P. W.,
A. Lizonova,
J. G. M. Lee,
Y. Li,
J. M. Bergelson,
R. W. Finberg,
D. E. Brough,
I. Kovesdi, and T. J. Wickham.
1998.
The coxsackie-adenovirus receptor protein can function as a cellular attachment protein for adenovirus serotypes from subgroups A, C, D, E, and F.
J. Virol.
72:7909-7915[Abstract/Free Full Text].
|
| 18.
|
Roelvink, P. W.,
I. Kovesdi, and T. J. Wickham.
1996.
Comparative analysis of adenovirus fiber-cell interaction: adenovirus type 2 (Ad2) and Ad9 utilize the same cellular fiber receptor but use different binding strategies for attachment.
J. Virol.
70:7614-7621[Abstract].
|
| 19.
|
Tomko, R. P.,
R. Xu, and L. Philipson.
1997.
HCAR and MCAR: the human and mouse cellular receptors for subgroup C adenoviruses and group B coxsackieviruses.
Proc. Natl. Acad. Sci. USA
94:3352-3356[Abstract/Free Full Text].
|
| 20.
|
Wadell, G.,
M-L. Hammarskjöld,
G. Winberg,
T. M. Varsanyi, and G. Sundell.
1980.
Genetic variability of adenoviruses.
Ann. N. Y. Acad. Sci.
354:16-42[Medline].
|
| 21.
|
Walters, R. W.,
T. Grunst,
J. M. Bergelson,
R. W. Finberg,
M. J. Welsh, and J. Zabner.
1999.
Basolateral localization of fiber receptors limits adenovirus infection from the apical surface of airway epithelia.
J. Biol. Chem.
274:10219-10226[Abstract/Free Full Text].
|
Journal of Virology, August 2000, p. 7691-7693, Vol. 74, No. 16
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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