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Journal of Virology, November 2001, p. 11218-11221, Vol. 75, No. 22
Department of Pathology, Harvard Medical
School, Boston, Massachusetts 02115
Received 16 May 2001/Accepted 20 August 2001
Several herpesviruses encode Fc receptors that may play a role in
preventing antibody-mediated clearance of the virus in vivo. Human
cytomegalovirus (HCMV) induces an Fc-binding activity in cells upon
infection, but the gene that encodes this Fc-binding protein has not
been identified. Here, we demonstrate that the HCMV AD169 open reading
frame TRL11 and its identical copy, IRL11, encode a type I membrane
glycoprotein that possesses IgG Fc-binding capabilities.
Many herpesviruses encode proteins
that interfere with the humoral and cellular immune response (18,
29). Presumably, these immune evasion gene products are
important for allowing the virus to replicate in a host that already
has a battery of specific antiviral defenses in place. Herpes simplex
virus type 1 (HSV-1) and HSV-2, murine cytomegalovirus (MCMV) and
varicella-zoster virus produce molecules that bind to the Fc portion of
host immunoglobulins (6, 12, 17, 28). These virally
encoded Fc receptors (v-FcRs) may prevent antiviral immunoglobulin G
(IgG) from neutralizing free virus and engaging in antibody-dependent
cytotoxic activity against infected cells (19). The
well-characterized HSV-1 v-FcR is a heterodimer of the gE and gI
glycoproteins and is able to inhibit complement activation
and antibody-dependent cell-mediated cytotoxicity in in vitro
experiments (8, 9). In a mouse model of HSV-1 infection, a
functional v-FcR was necessary for viral evasion of antibody-mediated
clearance (23). For MCMV, the role of the v-FcR has not
been well defined. An MCMV strain lacking the v-FcR gene
(fcr-1 or m138) replicated to low titers in mice with
and without B cells (7). Thus, m138 could be important for
aspects of MCMV in vivo replication that are unrelated to the binding
of IgG Fc.
Human cytomegalovirus (HCMV) induces an Fc-binding activity in infected
cells (3, 10, 14, 21, 25). Although there is a large
amount of data regarding alphaherpesvirus-encoded Fc receptors, it is
not known whether the Fc-binding molecule induced during HCMV infection
is encoded by the virus or by the host. Flow cytometry has been used to
demonstrate that the Fc-binding molecule in HCMV-infected cells is
present at the cell surface, while immunofluorescence data indicates
that Fc-binding activity can also be detected within the infected cell
(10, 14, 20). HCMV-infected cells can bind IgG from
several different species; they can also bind all subtypes of human
IgG, but not other human Ig isotypes (1, 20, 22).
Additional immunoelectron microscopy data indicates that an Fc-binding
activity may be present in the tegument of HCMV virions
(27). Although attempts have been made to characterize
biochemically the protein or proteins that are responsible for the
Fc-binding activity in infected cells, the gene that encodes the
HCMV-induced FcR has not been identified (27, 30). The
goal of this study was to identify and characterize the Fc-binding
protein(s) induced by HCMV. We demonstrate that the HCMV
open reading frame (ORF) TRL11/IRL11 encodes a glycoprotein of 34 kDa that binds to IgG Fc.
In order to identify the Fc-binding protein(s) induced by HCMV, the
following approach was taken. Human foreskin fibroblasts (HFFs) (number
of passages, 10 to 20) were infected with HCMV AD169 at a
multiplicity of infection of 5. Infected cells were metabolically
labeled with Expre35S35S
protein labeling mix (NEN) for 30 min at various times postinfection (p.i.) (2). The cells were then lysed in a buffer
containing: 0.5% NP-40, 150 mM NaCl, 2 mM CaCl2,
50 mM Tris-Cl (pH 7.4), 1 mM phenylmethylsulfonylfluoride, and 10 µM
leupeptin, and the debris was removed by centrifugation. After
preclearing of lysates with streptavidin-agarose (Pierce), human IgG Fc
or a human IgG1 myeloma protein (Calbiochem) that had been biotinylated
with NHS-LC-biotin (Pierce) was added at a concentration of 10 µg/ml.
The biotinylated IgG proteins (Fcbiotin and
IgG1biotin, respectively) and material bound to
them were retrieved by the addition of streptavidin-agarose (30 µl of
a 50% [vol/vol] slurry) and washed several times. Bound proteins
were released by the addition of sodium dodecyl sulfate (SDS) sample
buffer, and were analyzed by SDS-polyacrylamide gel electrophoresis
(PAGE) and autoradiography (15, 24).
A protein of approximately 34 kDa was immunoprecipitated by
Fcbiotin specifically in AD169-infected cells
(Fig. 1A, lanes 5 to 8). The Fc-binding
protein was detected as early as 12 h p.i. (evident in longer
exposures of the autoradiogram shown in Fig. 1A), and expression levels
were highest at 72 h p.i. An additional species of approximately
63 kDa was also retrieved from infected cell lysates. The heterogeneous
migration pattern of the 34-kDa species suggested that it may be a
glycoprotein. Indeed, digestion with PNGaseF (New England
Biolabs) reduced the molecular mass of the 34 kDa protein to
approximately 24 kDa (Fig. 2B, lanes 1 and 3), consistent with the presence of at least 3 N-linked glycans and a core polypeptide molecular mass of 24 kDa. The size of the 63 kDa
protein was reduced to 33 kDa upon PNGaseF digestion, consistent with
the presence of approximately 10 N-linked glycans. We conclude that
HCMV infection induces the expression of an Fc-binding
glycoprotein with a molecular mass of 34 kDa and the
expression of an additional, highly glycosylated, Fc-binding protein of
63 kDa. Both the 34-kDa and the 63-kDa glycoproteins were
also retrieved using IgG1biotin, indicating that
both glycoproteins are capable of binding to the Fc portion
of whole IgG (data not shown).
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.22.11218-11221.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
Human Cytomegalovirus Open Reading Frame
TRL11/IRL11 Encodes an Immunoglobulin G Fc-Binding Protein
ABSTRACT
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FIG. 1.
Infection of HFFs with HCMV AD169 induces the
expression of IgG Fc-binding proteins. Cells were pulse-labeled and
immunoprecipitations were performed. Lane 1, material
immunoprecipitated with IgG Fc (Fc) from a lysate of mock-infected
cells; lane 2, material immunoprecipitated with biotinylated IgG Fc
(Fcbiotin) from a lysate of mock-infected cells; lane 3, material immunoprecipitated from a lysate of HCMV-infected cells
48 h p.i. using IgG Fc; lanes 4, 5, 6, 7, and 8, material
immunoprecipitated at, respectively, 12, 24, 48, 72, and 96 h p.i.
from lysates for HCMV-infected cells using Fcbiotin. The
asterisk indicates a polypeptide retrieved nonspecifically and in
variable amounts when using Fcbiotin. Positions of
prestained molecular size standards (Gibco BRL) shown in this figure
are meant to represent approximate molecular sizes only. More accurate
estimates of the molecular sizes of the proteins of interest (described
in the text) were determined using other molecular size standards (data
not shown).
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FIG. 2.
HCMV AD169 ORF TRL11/IRL11 encodes the 34-kDa
Fc-binding protein present in HCMV-infected cells. (A) Results of
immunoprecipitation experiments with tagged constructs. For lanes 1 and
2, HFFs were pulse-labeled and immunopreciptiations were performed with
Fcbiotin. For lanes 3 to 10, 293 cells were pulse-labeled,
and immunoprecipitations were performed from equal amounts of lysate
using either an anti-HA antibody (lanes 3 to 6) or Fcbiotin
(lanes 7 to 10). Lane 1, mock-infected HFFs; lane 2, HCMV-infected HFFs
(48 h p.i.); lanes 3 and 7, 293 cells transfected with pcDNA3.1
construct containing untagged GFP (negative control); lanes 4 and 8, 293 cells transfected with pcDNA3.1 construct containing US8-HA (US8);
lanes 5 and 9, 293 cells transfected with pcDNA3.1 construct containing
UL130-HA (UL130); lanes 6 and 10, 293 cells transfected with pcDNA3.1
construct containing TR11/IRL11-HA (TRL11). (B) Results of
immunoprecipitation experiments with untagged construct. Cells were
pulse-labeled, and immunoprecipitations were performed with
Fcbiotin. Half of the bound material was treated with
PNGase F. Lane 1, HCMV-infected HFFs (48 p.i.) not treated; lane 2, 293 cells transfected with a construct containing untagged TR11/IRL11 and
not treated; lane 3, HCMV-infected HFFs (48 h p.i.) treated with
PNGaseF; lane 4, 293 cells transfected with a construct containing
untagged TR11/IRL11 and treated with PNGaseF. The asterisks indicate a
polypeptide retrieved nonspecifically and in variable amounts when
using Fcbiotin. The arrows at the right indicate the
positions of the 63-kDa and the deglycosylated 33-kDa forms of the
additional Fc-binding protein present in HCMV-infected cells. The
positions of prestained molecular size standards (Gibco BRL) shown in
this figure are meant to represent approximate molecular sizes only.
More accurate estimates of the molecular masses of the proteins of
interest (described in the text) were determined using other molecular
size standards (data not shown).
Using the size of the polypeptide backbone and the estimated number of
glycosylation sites observed for the 34 kDa Fc-binding protein, we
compiled a list of HCMV AD169 ORFs that fit these properties (Table
1). We chose to investigate viral genes
because several herpesviruses encode Fc receptors and HCMV encodes a
variety of other proteins involved in immune evasion (19,
29). An HCMV strain (RV798) that carries a deletion encompassing
US2-11, a region encoding several gene products that interfere with
major histocompatibility complex (MHC) class I processing, was
used to rule out several candidate ORFs in that region of the HCMV genome (data not shown) (13). Those ORFs most consistent
with the observed properties of the 34 kDa Fc-binding protein were amplified from AD169 genomic DNA by PCR with specific primers that
incorporated an influenza virus hemagglutinin (HA) epitope tag
at the C terminus and were cloned into the pcDNA3.1 mammalian expression vector (Invitrogen) by standard procedures
(26). Sequence analysis was used to verify that no
mutations had arisen as a consequence of PCR amplification. We note
that the AD169 genome contains a second, identical copy of
TRL11, designated IRL11 (5).
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The various ORF-HA constructs were transfected into 293 cells using LipofectAMINE (Life Technologies) according to the manufacturer's specifications. One day after transfection, cells were pulse-labeled for 15 min and lysed as described above. Equal amounts of radiolabeled lysate were subjected to immunoprecipitation using Fcbiotin or the anti-HA monoclonal antibody 12CA5. A construct expressing untagged green fluorescent protein (GFP) was used as a negative control for immunoprecipitations from 293 transfectant lysates (Fig. 2A, lanes 3 and 7). Cells transfected with HA-tagged versions of US8 (an HCMV-encoded type I membrane glycoprotein) or with the candidate ORF UL130 produced proteins reactive with the anti-HA antibody but were not immunoprecipitated by Fcbiotin (Fig. 2A, lanes 4 and 5 and lanes 8 and 9). However, cells transfected with the tagged version of TRL11/IRL11 produced a protein that was retrieved by anti-HA and Fcbiotin (Fig. 2A, lanes 6 and 10). The difference in size between the 34 kDa Fc-binding protein from HCMV-infected cells and the tagged version of gpTRL11/IRL11 is likely due to the additional amino acids of the HA tag. The difference in the amount of material present in the anti-HA and Fcbiotin immunoprecipitates likely reflects a difference in the affinities of the 12CA5 antibody for the HA tag and of the Fcbiotin for the gpTRL11/IRL11 molecule.
In order to provide additional evidence that TRL11/IRL11 encodes the 34 kDa Fc-binding protein seen in HCMV-infected cells, an untagged version of TRL11/IRL11 was amplified by PCR and cloned into pcDNA3.1. Transfection of the untagged TRL11/IRL11 construct into 293 cells followed by pulse-labeling and immunoprecipitation using Fcbiotin yielded a protein that comigrated with the 34-kDa Fc-binding protein from HCMV-infected cells in SDS-PAGE (Fig. 2B, lanes 1 and 2), and comigration was also observed after digestion with PNGaseF (Fig. 2B, lanes 3 and 4). Cells transfected with the untagged TRL11/IRL11 construct also produced a protein that bound to IgG1biotin, indicating that gpTRL11/IRL11 can interact with the Fc region of whole IgG (data not shown). We conclude that the HCMV ORF TRL11/IRL11 encodes an Fc-binding protein present in infected cells. Importantly, gpTRL11/IRL11 is capable of binding to IgG Fc in the absence of any other viral protein (Fig. 2A and B). However, these data do not formally rule out the possibility that gpTRL11/IRL11 may form a complex with another viral or human protein to form a functional Fc receptor that may have a specificity or affinity different from that of gpTRL11/IRL11 alone.
The ORFs that encode the Fc-binding protein, TRL11 and IRL11, are
identical in sequence to one another and are located, respectively, in the terminal repeat long (TRL) and internal repeat long (IRL) regions of the AD169 genome (Fig. 3). The
234-aa protein encoded by TRL11/IRL11 is a predicted type I membrane
glycoprotein with three N-glycosylation sites and has a
predicted cytoplasmic tail of 31 aa. We note the presence of a
consensus motif for engagement of the endocytic machinery
(DXXXLL) located in the predicted cytoplasmic tail (Fig. 3)
(11, 16). The amino acid sequence of TRL11/IRL11 does not
show homology to any of the known herpesvirus v-FcRs, suggesting that
different herpesviruses have evolved the ability to bind to host IgG Fc
at multiple times in the past. The protein sequence of TRL11/IRL11
shows limited similarity to the UL153 ORF of the Towne strain of HCMV
and is a member of the RL11 gene family of AD169, which comprises a set
of ORFs that are moderately similar (4, 5). However,
TRL11/IRL11 does not bear any obvious homology to other proteins
presently in the databases.
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The identification of gpTRL11/IRL11 as an HCMV-encoded IgG Fc-binding protein adds to the lengthy list of HCMV gene products that interact with molecules important for immune system function (29). With the availability of a gene that encodes an HCMV IgG Fc-binding protein, it will now be possible to characterize its interaction with IgG Fc and its potential role as a v-FcR that may be involved in evasion of the antibody response by HCMV.
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ACKNOWLEDGMENTS |
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This work was supported by the National Institutes of Health (R37-AI33456 and P01-AI42257). B.N.L. is a Howard Hughes Medical Institute predoctoral fellow, and R.S.T. is a Novartis Fellow of the Life Sciences Research Foundation.
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FOOTNOTES |
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* Corresponding author. Mailing address: Department of Pathology, Harvard Medical School, 200 Longwood Ave., Boston, MA 02115. Phone: (617) 432-4776. Fax: (617) 432-4775. E-mail: ploegh{at}hms.harvard.edu.
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REFERENCES |
|---|
|
Top
Abstract
Text
References
|
|---|
| 1. |
Antonsson, A., and P. J. Johansson.
2001.
Binding of human and animal immunoglobulins to the IgG Fc receptor induced by human cytomegalovirus.
J. Gen. Virol.
82:1137-1145 |
| 2. | Beersma, M. F., M. J. Bijlmakers, and H. L. Ploegh. 1993. Human cytomegalovirus down-regulates HLA class I expression by reducing the stability of class I H chains. J. Immunol. 151:4455-4464[Abstract]. |
| 3. | Beersma, M. F. C. 1993. Ph.D thesis. University of Amsterdam, Amsterdam, The Netherlands. |
| 4. | Cha, T. A., E. Tom, G. W. Kemble, G. M. Duke, E. S. Mocarski, and R. R. Spaete. 1996. Human cytomegalovirus clinical isolates carry at least 19 genes not found in laboratory strains. J. Virol. 70:78-83[Abstract]. |
| 5. | Chee, M. S., A. T. Bankier, S. Beck, R. Bohni, C. M. Brown, R. Cerny, T. C. A. Horsnell. Hutchison, III, T. Kouzarides, J. A. Martignetti, et al. 1990. Analysis of the protein-coding content of the sequence of human cytomegalovirus strain AD169. Curr. Top. Microbiol. Immunol. 154:125-169[Medline]. |
| 6. | Costa, J., C. Yee, Y. Nakamura, and A. Rabson. 1978. Characteristics of the Fc receptor induced by herpes simplex virus. Intervirology 10:32-39[Medline]. |
| 7. |
Crnkovic-Mertens, I.,
M. Messerle,
I. Milotic,
U. Szepan,
N. Kucic,
A. Krmpotic,
S. Jonjic, and U. H. Koszinowski.
1998.
Virus attenuation after deletion of the cytomegalovirus Fc receptor gene is not due to antibody control.
J. Virol.
72:1377-1382 |
| 8. |
Dubin, G.,
E. Socolof,
I. Frank, and H. M. Friedman.
1991.
Herpes simplex virus type 1 Fc receptor protects infected cells from antibody-dependent cellular cytotoxicity.
J. Virol.
65:7046-7050 |
| 9. |
Frank, I., and H. M. Friedman.
1989.
A novel function of the herpes simplex virus type 1 Fc receptor: participation in bipolar bridging of antiviral immunoglobulin G.
J. Virol.
63:4479-4488 |
| 10. |
Furukawa, T.,
E. Hornberger,
S. Sakuma, and S. A. Plotkin.
1975.
Demonstration of immunoglobulin G receptors induced by human cytomegalovirus.
J. Clin. Microbiol.
2:332-336 |
| 11. | Heilker, R., M. Spiess, and P. Crottet. 1999. Recognition of sorting signals by clathrin adaptors. Bioessays 21:558-567[CrossRef][Medline]. |
| 12. |
Johnson, D. C., and V. Feenstra.
1987.
Identification of a novel herpes simplex virus type 1-induced glycoprotein which complexes with gE and binds immunoglobulin.
J. Virol.
61:2208-2216 |
| 13. | Jones, T. R., L. K. Hanson, L. Sun, J. S. Slater, R. M. Stenberg, and A. E. Campbell. 1995. Multiple independent loci within the human cytomegalovirus unique short region down-regulate expression of major histocompatibility complex class I heavy chains. J. Virol. 69:4830-4841[Abstract]. |
| 14. |
Keller, R.,
R. Peitchel,
J. N. Goldman, and M. Goldman.
1976.
An IgG-Fc receptor induced in cytomegalovirus-infected human fibroblasts.
J. Immunol.
116:772-777 |
| 15. | Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685[CrossRef][Medline]. |
| 16. | Letourneur, F., and R. D. Klausner. 1992. A novel di-leucine motif and a tyrosine-based motif independently mediate lysosomal targeting and endocytosis of CD3 chains. Cell 69:1143-1157[CrossRef][Medline]. |
| 17. | Litwin, V., M. Sandor, and C. Grose. 1990. Cell surface expression of the varicella-zoster virus glycoproteins and Fc receptor. Virology 178:263-272[CrossRef][Medline]. |
| 18. | Loenen, W. A., C. A. Bruggeman, and E. J. Wiertz. 2001. Immune evasion by human cytomegalovirus: lessons in immunology and cell biology. Semin. Immunol. 13:41-49[CrossRef][Medline]. |
| 19. | Lubinski, J., T. Nagashunmugam, and H. M. Friedman. 1998. Viral interference with antibody and complement. Semin. Cell Dev. Biol. 9:329-337[CrossRef][Medline]. |
| 20. | MacCormac, L. P., and J. E. Grundy. 1996. Human cytomegalovirus induces an Fc gamma receptor (Fc gammaR) in endothelial cells and fibroblasts that is distinct from the human cellular Fc gammaRs. J. Infect. Dis. 174:1151-1161[Medline]. |
| 21. | Mackowiak, P. A., and M. Marling-Cason. 1987. Immunoreactivity of cytomegalovirus-induced Fc receptors. Microbiol. Immunol. 31:427-434[Medline]. |
| 22. |
Murayama, T.,
S. Natsuume-Sakai,
K. Shimokawa, and T. Furukawa.
1986.
Fc receptor(s) induced by human cytomegalovirus bind differentially with human immunoglobulin G subclasses.
J. Gen. Virol.
67:1475-1478 |
| 23. |
Nagashunmugam, T.,
J. Lubinski,
L. Wang,
L. T. Goldstein,
B. S. Weeks,
P. Sundaresan,
E. H. Kang,
G. Dubin, and H. M. Friedman.
1998.
In vivo immune evasion mediated by the herpes simplex virus type 1 immunoglobulin G Fc receptor.
J. Virol.
72:5351-5359 |
| 24. | Ploegh, H. L. 1995. One-dimensional isoelectric focusing of proteins in slab gels, p. 10.12.11-10.12.18. In J. E. Coligan, B. M. Dunn, H. L. Ploegh, D. W. Speicher, and P. T. Wingfield (ed.), Current protocols in protein science, vol. 1. John Wiley and Sons, Inc., New York, N.Y. |
| 25. |
Rahman, A. A.,
M. Teschner,
K. K. Sethi, and H. Brandis.
1976.
Appearance of IgG (Fc) receptor(s) on cultured human fibroblasts infected with human cytomegalovirus.
J. Immunol.
117:253-258 |
| 26. | Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y. |
| 27. |
Stannard, L. M., and D. R. Hardie.
1991.
An Fc receptor for human immunoglobulin G is located within the tegument of human cytomegalovirus.
J. Virol.
65:3411-3415 |
| 28. |
Thale, R.,
P. Lucin,
K. Schneider,
M. Eggers, and U. H. Koszinowski.
1994.
Identification and expression of a murine cytomegalovirus early gene coding for an Fc receptor.
J. Virol.
68:7757-7765 |
| 29. | Tortorella, D., B. E. Gewurz, M. H. Furman, D. J. Schust, and H. L. Ploegh. 2000. Viral subversion of the immune system. Annu. Rev. Immunol. 18:861-926[CrossRef][Medline]. |
| 30. |
Xu, B.,
T. Murayama,
K. Ishida, and T. Furukawa.
1989.
Characterization of IgG Fc receptors induced by human cytomegalovirus.
J. Gen. Virol.
70:893-900 |
Journal of Virology, November 2001, p. 11218-11221, Vol. 75, No. 22
0022-538X/01/$04.00+0 DOI: 10.1128/JVI.75.22.11218-11221.2001
Copyright © 2001, American Society for Microbiology. All rights reserved.
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