Previous Article | Next Article 
Journal of Virology, January 2000, p. 518-522, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Avian Reticuloendotheliosis Virus Strain A and
Spleen Necrosis Virus Do Not Infect Human Cells
R.
Gautier,1
A.
Jiang,2
V.
Rousseau,3
R.
Dornburg,2 and
T.
Jaffredo1,*
Institut d'Embryologie Cellulaire et
Moléculaire du CNRS et du Collège de France, 94736 Nogent-sur-Marne Cedex,1 and Institut
Alfred FESSARD-CNRS UPR 2212, 91198 Gif sur Yvette
Cedex,3 France, and Division of
Infectious Diseases, Center for Human Retrovirology, Thomas Jefferson
University, Philadelphia, Pennsylvania 191072
Received 24 November 1998/Accepted 30 September 1999
 |
ABSTRACT |
Spleen necrosis virus (SNV) and
Reticuloendotheliosis virus strain A (REV-A) belong to the
family of reticuloendotheliosis viruses and are 90% sequence related.
SNV-derived retroviral vectors produced by the REV-A-based D17.2G
packaging cell line were shown to infect human cells (H.-M. Koo,
A. M. C. Brown, Y. Ron, and J. P. Dougherty, J. Virol. 65:4769-4776, 1991), while similar vectors produced by another
SNV-based packaging cell line, DSH134G, are not infectious in human
cells (reviewed by R. Dornburg, Gene Ther. 2:301-310, 1995). Here we
describe a careful reevaluation of the infectivity of vectors produced
from the most commonly used REV-A- or SNV-based packaging cells
obtained from various sources with, among them, one batch of D17.2G
packaging cells obtained from the American Type Culture Collection.
None of these packaging cells produced vectors able to infect human
cells. Thus, contrary to previously published data, we conclude that
REV-based vectors are not infectious in human cells.
| |
TEXT |
Spleen necrosis virus
(SNV) and Reticuloendotheliosis virus strain A (REV-A)
belong to the family of reticuloendotheliosis viruses (REVs), a group
of closely related amphotropic retroviruses all of which were isolated
from birds (3, 29, 35, 37, 40). REVs include chicken
syncytial virus, duck infectious anemia virus, SNV, REV-A, and its
acutely transforming variant REV-T, which contains the rel
oncogene (3, 42).
SNV and REV-A share more than 90% sequence homology, their
cis- and trans-acting sequences appear to be
exchangeable without impairment of virus replication (10),
and they have the same receptor (9, 16, 27). Although
originally isolated from avian species, REVs are more closely related
to mammalian oncoretroviruses than to other avian retroviruses by
sequence homology (21, 22, 38, 39, 43) and serological
cross-reactivity (2, 4). Superinfection experiments have
shown that SNV and REV-A belong to the same interference subgroup as
the simian type D viruses (23, 27).
Using the REV-A-based packaging cell line D17.2G (12), Koo
et al. (26) showed that REV-A-based vectors could infect
human cells as efficiently as amphotropic murine leukemia virus
(ampho-MLV). Contrary to this finding, when the SNV-based packaging
cell line DSH134G (30) was used, no infection of human cells
was observed (6). Because D17.2G and DSH134G produce REV-A
and SNV envelopes, respectively, it was not clear whether the
difference in human cell infectivity resulted from sequence differences
between the two envelopes or from a special feature imparted to the
viral particles produced from D17.2G cells.
To reevaluate the tropism of REV-based vectors, we have compared the
infectivity of vectors produced from the most commonly used SNV- or
REV-A-based packaging cell lines in human cells, i.e., the C3A2
(40) and D17.2G (12) packaging cell lines, which
express the REV-A envelope, and DSN (13) and DSH134G
(30) helper cells, which express the SNV envelope. We
demonstrate that none of these packaging cell-produced SNV vectors was
able to infect human cells. Thus, the ability of D17.2G-produced
vectors to infect human cells is probably a special feature of some
batches. The discrepancies between our results and those from other
labs are precisely discussed.
Infection of human cells with nonreplicative SNV-lacZ
vectors produced by various SNV- or REV-A-based packaging cells.
The tropism of REV-based vectors was determined by using an SNV-based
gene transfer vector which transduced the bacterial 
-galactosidase
gene (lacZ) (in the vector pCXL; 32) or
very similar SNV-based vectors carrying either a fusion gene between the phleomycin resistance gene and the lacZ gene (SNV-Sh
ble::lacZ) (R. Gautier and T. Jaffredo,
unpublished data) or a fusion gene consisting of the drosophila alcohol
dehydrogenase gene and the phleomycin resistance gene (17).
The vectors were transfected into the four most commonly used SNV- or
REV-A-based helper cells. These were the SNV-based helper cell lines
DSN (obtained from H. Temin's laboratory, University of Wisconsin;
reference 13) and DSH134G (30) and the
REV-A-based helper cell lines C3A2 (obtained from H. Temin's
laboratory; reference 41) and D17.2G (CRL 8468;
obtained from the American Type Culture Collection [ATCC]; reference
12). As a control, we also used a helper cell line
which expressed the SNV Gag-Pol proteins and the envelope of ampho-MLV
(termed DSH-ampho-MLV-env). Vectors were harvested from stably
transfected helper cell clones, and infectivity was tested in various
human cell lines, e.g., HeLa (18) or HOS (31), or
the canine cell line D17 (36). The best producer clones were selected and tested for absence of replication-competent (RC) virus by
using QT6 cells (33), an immortalized quail cell line, as
naive recipient cells. Virus was harvested from nearly confluent monolayers of packaging cells 16 to 18 h after the medium was changed. The harvested medium was centrifuged at 3,500 × g
for 10 min to remove cells and cell debris, and the virus was used for
infection of various cells.
No infection of HeLa or HOS cells was detected with vectors produced
from C3A2, D17.2G, DSN, or DSH134G helper cells (Table 1). In contrast,
DSH-ampho-MLV-env-produced vectors give titers ranging from 5 × 104 to 1 × 105 LacZ-forming units (LFU)/ml,
respectively (Table 1). D17 cells permissive for SNV and ampho-MLV
infection served as positive controls. In this cell type, vector virus
titers ranged from 105 to 106 LFU/ml (Table 1),
except for DSN cells, which are known to give lower vector virus titers
than C3A2 or D17.2G cells (13). LacZ staining was never
detected in mock-infected D17, HeLa, or HOS cells.
View this table:
[in this window]
[in a new window]
|
TABLE 1.
Titers of SNV vectorsa packaged by
different REV-A- or SNV-based helper cell lines on D17, HeLa, or
HOS cells
|
|
C3A2-produced vectors express the REV-A envelope from a plasmid
identical to that present in D17.2G cells. Neither of these
cell lines
produced a vector displaying human cell tropism. Thus,
the differences
in human cell infectivity between our results
and those of Koo et al.
(
26) is likely due to a special feature
imparted by some
batches of D17.2G packaging cells and certainly
did not result from
differences between the REV-A and SNV envelope
proteins. In addition,
when using an RC strain of SNV, those investigators
(
26) did
not find productive infection of human cells and concluded
that a
posttranscriptional block in SNV replication occurred in
these cells.
However, they did not investigate whether the virus
was integrated.
Since the SNV promoter is very strong in human
cells, it is very
unlikely that the lack of sufficient gene expression
accounted for the
lack of productive
infection.
Comparison of DSH134G- and DSH-ampho-MLV-env-produced
SNV-lacZ vector tropism for various human cells.
To
further evaluate the tropism of SNV-based vectors for human cells, we
compared the infectivity of CXL vectors produced from the solely
SNV-based DSH helper cell line with that of vectors produced from the
DSH-ampho-MLV-env helper cell line (19), which contains SNV
Gag-Pol and the ampho-MLV envelope. Vector particles produced from both
packaging lines encapsidated the SNV-based lacZ vector pCXL.
Infectivity was determined in human cell lines from various origins
(Table 2), as well as human embryo skin primary fibroblasts from a week
21 of amenorrhea female fetus used at the third passage in culture.
Human embryo tissue was obtained from voluntary or therapeutic
abortions performed in compliance with French legislation after
informed consent was obtained from the parents.
Coinciding with earlier observations (
5-7,
19), no or only
background (up to 10 LFU) infectivity in the human cells was
observed
with vectors produced by DSH134G packaging cells. Dog
D17 cells, which
served as a positive control, were infected with
titers of
10
6 LFU (Table
2). However,
CXL vectors pseudotyped with ampho-MLV
Env infected all of the human
nonhematopoietic cell lines investigated
with titers ranging from
4 · 10
3 to 10
5 LFU/ml (Table
2). The
hematopoietic cell lines KG1a (
24) and
Daudi (
25)
were poorly infected. These cells are known to express
low levels of
ampho-MLV receptors (
34). Thus, low levels of
infectivity of
these hematopoietic cells correlate with low-level
receptor expression,
coinciding with other reports (
34). This
conclusion is
further supported by recent findings that human
hematopoietic cells can
be efficiently infected with SNV when
a targeting envelope capable of
binding to a cell surface protein
is expressed on the viral surface
(
19). For example, KG1a cells
which express the CD34
receptor were infected with SNV vectors
displaying anti-CD34
single-chain antibodies with titers above
10
5
(
19). It is worthy of note that D17.2G-produced vectors
(obtained
from reference
26) infected HeLa and HPF
cells with titers similar
to those obtained with ampho-MLV
Env-pseudotyped SNV vectors,
e.g., 10
4 and 5 · 10
5 LFU/ml, while the same vector produced by D17.2G cells
originating
from the ATCC did not (data not shown).
View this table:
[in this window]
[in a new window]
|
TABLE 2.
Comparison of infection of human cells from various
origins by DSH134G- and
DSH-ampho-Env-produced SNV-lacZa
|
|
Amphotropic envelope detection on SNV-based helper cells: FACS and
immunocytochemical analyses.
Since we wanted to be sure that the
packaging cells we used were free of amphotropic contamination, we
tested the cells for the presence of ampho-MLV Env at the cell surface
by immunocytochemistry analysis. psi CRIP, an ampho-MLV-based packaging
cell line (8); D17.2G; DSH134G; and D17 cells were plated on
eight-well Lab Tek chamber slides (Nunc) with appropriate culture
media. The next day, they were fixed with 4% paraformaldehyde in
phosphate-buffered saline and incubated overnight with a 1/500 dilution
of a goat polyclonal antibody directed against ampho-MLV (Quality
Biotech) revealed with a sheep anti-goat peroxidase-coupled secondary
antibody (Biosys). Tyramide Signal Amplification (NEN Life Science) was used to increase the signal-to-noise ratio in accordance with the
manufacturer's recommendations. No staining was found on D17.2G, DSH134G, or D17 cells. As expected, the psi CRIP cells were strongly stained (Fig. 1).
View larger version (116K):
[in this window]
[in a new window]
|
FIG. 1.
Immunohistochemical detection of an MLV-related
amphotropic envelope on different cell types. Tyramide amplification
and diaminobenzidine staining were used. Panels: A, psi CRIP cells; B,
D17.2G cells (ATCC); C, DSH134G cells; D, D17 cells. Only psi CRIP
cells were strongly immunostained. Bar, 60 µm.
|
|
To further corroborate this finding, fluorescence-activated cell sorter
(FACS) analysis by the method of Kadan et al. (
20)
was
performed. This assay is based on the use of two different
cell lines:
a naive one which expresses neither SNV nor ampho-MLV
receptors
(
28) and another expressing the ampho-MLV receptor
PIT-2.
When added to these cells, ampho-MLV envelope proteins
or virions bind
to the receptor. Material bound to the cells is
recognized by
incubation with monoclonal antibody 83A25 (
15)
against the
MLV envelope for 45 min at 4°C. Cells are then incubated
with
anti-rat immunoglobulin fluorescein isothiocyanate-conjugated
antibodies (Dako) and subjected to FACS analysis. Incubation of
CERD9 (negative control) and CEAR13 (expressing PIT-2) cells with
the
supernatant from D17, D17.2G, or DSH134G cells or that of
the viral MLV
envelope 4070A was followed by detection of ampho-MLV
Env. This test
enables the detection of ampho-MLV Env present
in the culture medium.
No FACS signal could be detected at any
time with CERD9. CEAR13 gave a
very strong signal with the 4070A
envelope (positive control), but no
signal was detected with D17,
D17.2G, or DSH134G-conditioned medium
(Fig.
2). Surprisingly,
D17.2G cells,
from reference
26, displayed a strong signal in
both
tests which should be correlated with the ability of these
cells to
produce virus able to infect human cells (data not shown).
View larger version (23K):
[in this window]
[in a new window]
|
FIG. 2.
Profiles of the ampho-MLV envelope in the supernatant of
cells. Indirect immunofluorescence flow cytometry patterns on CEAR13
cells expressing the amphotropic receptor PIT-2 and CERD9 cells which
do not express it are shown. Supernatants are those of 4070A (ampho-MLV
strain 4070A envelope; positive control) and D17.2G (ATCC), DSH134G,
and D17 cells. The white profiles indicate cells stained by propidium
iodide alone. The black profiles shows cells incubated with monoclonal
antibody 83A25 against the ampho-MLV envelope (20). Only
4070A gave a strong positive signal. Two independent analysis were
performed which yielded similar results.
|
|
Taken together, these results indicate that some batches of D17.2G
cells produce an ampho-MLV Env glycoprotein which confers
the
characteristics of an amphotropic packaging cell line on D17.2G,
thus
enabling infection of human cells. This finding is further
supported by
the fact that D17.2G and psi CRIP cells display strong
inhibition of
infection by, respectively, psi CRIP- and D17.2G-produced
virus
(superinfection interference; data not shown). Since (i)
SNV and REV-A
and (ii) ampho-MLV belong to different interference
subgroups
(
37), this indicates the presence of an envelope different
from that of REVs in some D17.2G helper cell stocks. Therefore,
we
conclude that the ability of some batches of D17.2G-produced
vectors to
efficiently infect human cells is due to contamination
with ampho-MLV
Env.
The nature of the envelope present on some batches D17.2G cells has
remained elusive. It might be a fragment of ampho-MLV
Env inserted into
the SNV wild-type envelope, a complete envelope
together with that of
SNV, or a fully RC ampho-MLV. Furthermore,
we do not know whether the
D17.2G samples distributed in various
laboratories are equally
contaminated. In this respect, it is
important to note that infection
experiments performed by different
groups with the same cell types have
yielded different results.
For instance, Mikawa et al. (
32)
found that infection of NIH
3T3 cells by D17.2G-CXL (bearing a
lacZ gene) was negligible,
as previously reported
(
14). Koo et al. (
26) reported a titer
of 6 · 10
3 transducing vectors per ml of viral supernatant.
Both groups,
however, found similar titers on D17 dog cells and on HeLa
cells
(
23,
26).
The SNV envelope displays 42 to 49% amino acid sequence identity with
a prototype simian D-type virus envelope (
23,
27).
Interference experiments using molecular clones of RC strains
of SNV
and REV-A have shown that SNV and simian D-type viruses
belong to a
single receptor interference subgroup. Thus, they
appear to use the
same receptor (
23,
27). However, it has
been shown that the
other members of this interference subgroup
can infect human cells
(
37). Considering these findings, how
can the lack of human
cell infection by SNV be explained? REVs
may use the same cell surface
protein as other D-type viruses
for envelope docking but may use other
protein domains for binding.
This would explain why simian D-type
virus-infected cells are
resistant to SNV infection. Moreover, Dornburg
and coworkers have
found that the infectivity of SNV particles
displaying single-chain
antibodies was greatly enhanced when the SNV
wild-type envelope
was also present (
5,
7). It was
hypothesized that a cellular
receptor for the wild-type SNV envelope
that is homologous to
that expressed on dog D17 cells is present on
human cells but
that the human receptor is mutated, preventing
high-affinity binding
and virus entry. The single-chain antibodies
displayed on the
viral surface may anchor the vector to the cell
surface, hence
mediating interaction with the envelope and the
wild-type receptor,
enabling membrane fusion (
11). Since all
members of the simian
D-type interference subgroup except SNV infect
human cells, this
hypothesis appears the most likely. Cloning of the
receptor should
help to elucidate this
problem.
In summary, the present study clearly shows that the REVs REV-A and SNV
do not infect human cells due to the inability to
bind to a cell
surface receptor. However, vectors derived from
these viruses can
infect human cells when they are pseudotyped
with envelopes that
mediate receptor binding and membrane fusion,
e.g., that of ampho-MLV.
Thus, SNV or REV-A is suitable for the
development of a powerful,
hazard-free vector for gene
transduction.
| |
ACKNOWLEDGMENTS |
We are indebted to F. Dieterlen for her constant support and
critical reading of the manuscript. We are grateful to F.-L. Cosset for
his invaluable help in FACS analysis. We thank M. C. Labastie for
providing us with human embryo skin (obtained according to the rules
defined by the French Comité d'Ethique) and A. Burns for reading
the manuscript. We also thank C. Batejat for Tyramide Signal
Amplification staining, M.-F. Meunier for help in manuscript preparation, and F. Viala for excellent photographic assistance.
This work was supported by the Centre National de la Recherche
Scientifique, by AFM and ARC grants 587132 and 9787 to T.J. and R.G.,
and by a grant from the National Institutes of Health (1RO1AI41899-01)
to R.D. and A.J.
| |
FOOTNOTES |
*
Corresponding author. Mailing address: Institut
d'Embryologie Cellulaire et Moleculaire du CNRS et du College de
France-UPR 9064, 49 bis Av. de la Belle Gabrielle, 94736 Nogent-sur-Marne Cedex, France. Phone: (1) 45 14 15 30. Fax: (1) 48 73 43 77. E-mail: jaffredo{at}infobiogen.fr.
| |
REFERENCES |
| 1.
|
Alper, O.,
K. Yamaguchi,
J. Hitomi,
S. Honda,
T. Matsushima, and K. Abe.
1990.
The presence of c-erbB-2 gene product-related protein in culture medium conditioned by breast cancer cell line SK-BR-3.
Cell Growth Differ.
1:591-599[Abstract].
|
| 2.
|
Barbacid, M.,
E. Hunter, and S. A. Aaronson.
1979.
Avian reticuloendotheliosis viruses: evolutionary linkage with mammalian type C retroviruses.
J. Virol.
30:508-514[Abstract/Free Full Text].
|
| 3.
|
Bose, H. R.
1992.
The rel family: models for transcriptional regulation and oncogenic transformation.
Biochim. Biophys. Acta
1114:1-7[Medline].
|
| 4.
|
Charman, H. P.,
R. V. Gilden, and S. Oroszlan.
1979.
Reticuloendotheliosis virus: detection of immunological relationship to mammalian type C retroviruses.
J. Virol.
29:1221-1225[Abstract/Free Full Text].
|
| 5.
|
Chu, T.-H. T., and R. Dornburg.
1995.
Retroviral vector particles displaying the antigen-binding site of an antibody enable cell-type-specific gene transfer.
J. Virol.
69:2659-2663[Abstract].
|
| 6.
|
Chu, T.-H. T., and R. Dornburg.
1997.
Toward highly efficient cell-type-specific gene transfer with retroviral vectors displaying single-chain antibodies.
J. Virol.
71:720-725[Abstract].
|
| 7.
|
Chu, T.-H. T.,
I. Martinez,
W. C. Sheay, and R. Dornburg.
1994.
Cell targeting with retroviral vector particles containing antibody-envelope fusion proteins.
Gene Ther.
1:292-299[Medline].
|
| 8.
|
Danos, O., and R. C. Mulligan.
1988.
Safe and efficient generation of recombinant retroviruses with amphotropic and ecotropic host ranges.
Proc. Natl. Acad. Sci. USA
85:6460-6464[Abstract/Free Full Text].
|
| 9.
|
Delwart, E. L., and A. T. Panganiban.
1989.
Role of reticuloendotheliosis virus envelope glycoprotein in superinfection interference.
J. Virol.
63:272-280.
|
| 10.
|
Dornburg, R.
1995.
Reticuloendotheliosis viruses and derived vectors.
Gene Ther.
2:301-310[Medline].
|
| 11.
|
Dornburg, R.
1997.
From the natural evolution to the genetic manipulation of the host-range of retroviruses.
Biol. Chem.
378:457-468[Medline].
|
| 12.
|
Dougherty, J. P., and H. M. Temin.
1988.
Determination of the rate of base-pair substitution and insertion mutations in retrovirus replication.
J. Virol.
62:2817-2822[Abstract/Free Full Text].
|
| 13.
|
Dougherty, J. P.,
R. Wisniewski,
S. Yang,
B. W. Rhode, and H. M. Temin.
1989.
New retrovirus helper cells with almost no nucleotide sequence homology to retrovirus vectors.
J. Virol.
63:3209-3212[Abstract/Free Full Text].
|
| 14.
|
Embretson, J. E., and H. M. Temin.
1987.
Transcription from a spleen necrosis virus 5' long terminal repeat is suppressed in mouse cells.
J. Virol.
61:3454-3462[Abstract/Free Full Text].
|
| 15.
|
Evans, L. H.,
R. P. Morrison,
F. G. Malik,
J. Portis, and W. Britt.
1990.
A neutralizable epitope common to the envelope glycoproteins of ecotropic, polytropic, xenotropic, and amphotropic murine leukemia viruses.
J. Virol.
64:6176-6183[Abstract/Free Full Text].
|
| 16.
|
Federspiel, M. J.,
L. B. Crittenden, and S. H. Hughes.
1989.
Expression of avian reticuloendotheliosis virus envelope confers host resistance.
Virology
173:167-177[CrossRef][Medline].
|
| 17.
|
Gautier, R.,
D. Drocourt, and T. Jaffredo.
1996.
Generation of small fusion genes carrying phleomycin resistance and Drosophila alcohol dehydrogenase reporter properties, their application in retroviral vectors.
Exp. Cell Res.
224:291-301[CrossRef][Medline].
|
| 18.
|
Gey, G. O.,
W. D. Coffman, and M. T. Kubicek.
1952.
Tissue culture studies of the proliferative capacity of cervical carcinoma and normal epithelium.
Cancer Res.
12:264-269.
|
| 19.
|
Jiang, A.,
T.-H. T. Chu,
F. Nocken,
K. Cichutek, and R. Dornburg.
1998.
Cell-type-specific gene transfer into human cells with retroviral vectors that display single-chain antibodies.
J. Virol.
72:10148-10156[Abstract/Free Full Text].
|
| 20.
|
Kadan, M. J.,
S. Sturm,
W. F. Anderson, and M. A. Eglitis.
1992.
Detection of receptor-specific murine leukemia virus binding to cells by immunofluorescence analysis.
J. Virol.
66:2281-2287[Abstract/Free Full Text].
|
| 21.
|
Kang, C.-Y., and H. M. Temin.
1973.
Lack of sequence homology among RNAs of avian leukosis-sarcoma viruses, reticuloendotheliosis viruses, and chicken endogenous RNA-directed DNA polymerase activity.
J. Virol.
12:1314-1324[Abstract/Free Full Text].
|
| 22.
|
Kato, S.,
K. Matsuo,
N. Nishimura,
N. Takahashi, and T. Takano.
1987.
The entire nucleotide sequence of baboon endogenous virus DNA: a chimeric genome structure of murine type C and simian type D retroviruses.
Jpn. J. Genet.
62:127-137.
|
| 23.
|
Kewalramani, V. N.,
A. T. Panganiban, and M. Emerman.
1992.
Spleen necrosis virus, an avian immunosuppressive retrovirus, shares a receptor with the type D simian retroviruses.
J. Virol.
66:3026-3031[Abstract/Free Full Text].
|
| 24.
|
Klein, E.,
G. Klein,
J. J. Nadkarni,
H. Wigzell, and P. Clifford.
1968.
Surface IgM-kappa specificity on a Burkitt lymphoma cell in vivo and in derived culture lines.
Cancer Res.
28:1300-1310[Abstract/Free Full Text].
|
| 25.
|
Koeffler, H. P.
1983.
Induction of differentiation of human acute myelogenous leukemia cells: therapeutic implications.
Blood
62:709-721[Abstract/Free Full Text].
|
| 26.
|
Koo, H.-M.,
A. M. C. Brown,
Y. Ron, and J. P. Dougherty.
1991.
Spleen necrosis virus, an avian retrovirus, can infect primate cells.
J. Virol.
65:4769-4776[Abstract/Free Full Text].
|
| 27.
|
Koo, H.-M.,
J. Gu,
A. Varela-Echavarria,
Y. Ron, and J. P. Dougherty.
1992.
Reticuloendotheliosis type C and primate type D oncoretroviruses are members of the same receptor interference group.
J. Virol.
66:3448-3454[Abstract/Free Full Text].
|
| 28.
|
Kozak, S. L.,
D. C. Siess,
M. P. Kavanaugh,
A. D. Miller, and D. Kabat.
1995.
The envelope glycoprotein of an amphotropic murine retrovirus binds specifically to the cellular receptor/phosphate transporter of susceptible species.
J. Virol.
69:3433-3440[Abstract].
|
| 29.
|
Maldonado, R. L., and H. R. Bose, Jr.
1976.
Group-specific antigen shared by the members of the reticuloendotheliosis virus complex.
J. Virol.
17:983-990[Abstract/Free Full Text].
|
| 30.
|
Martinez, I., and R. Dornburg.
1995.
Improved retroviral packaging lines derived from spleen necrosis virus.
Virology
208:234-241[CrossRef][Medline].
|
| 31.
|
McAllister, R. M.,
M. B. Gardner,
A. E. Greene,
C. Bradt,
W. W. Nichols, and B. H. Landing.
1971.
Cultivating in vitro of cells derived from a human osteosarcoma.
Cancer
27:397-402[CrossRef][Medline].
|
| 32.
|
Mikawa, T.,
D. A. Fischman,
J. P. Dougherty, and A. M. C. Brown.
1991.
In vivo analysis of a new lacZ retrovirus vector suitable for cell lineage marking in avian and other species.
Exp. Cell Res.
195:516-523[CrossRef][Medline].
|
| 33.
|
Moscovici, C.,
M. G. Moscovici,
H. Jimenez,
M. C. C. Lai,
M. J. Hayman, and P. K. Vogt.
1977.
Continuous tissue culture cell lines derived from chemically induced tumors of Japanese quail.
Cell
11:95-103[CrossRef][Medline].
|
| 34.
|
Orlic, D.,
L. J. Girard,
C. T. Jordan,
S. M. Anderson,
A. P. Cline, and D. M. Bodine.
1996.
The level of mRNA encoding the amphotropic retrovirus receptor in mouse and human hematopoietic stem cells is low and correlates with the efficiency of retrovirus transduction.
Proc. Natl. Acad. Sci. USA
93:11097-11102[Abstract/Free Full Text].
|
| 35.
|
Purchase, H. G., and R. L. Witter.
1975.
The reticuloendotheliosis viruses.
Curr. Top. Microbiol. Immunol.
71:103-124[Medline].
|
| 36.
|
Quinn, L. A.,
G. E. Moore,
R. T. Morgan, and L. K. Woods.
1979.
Cell lines from human colon carcinoma with unusual cell products, double minutes, and homogeneously staining regions.
Cancer Res.
39:4914-4924[Abstract/Free Full Text].
|
| 37.
|
Sommerfelt, M. A., and R. A. Weiss.
1990.
Receptor interference groups of 20 retroviruses plating on human cells.
Virology
176:58-69[CrossRef][Medline].
|
| 38.
|
Sonigo, P.,
C. Barker,
E. Hunter, and S. Wain-Hobson.
1986.
Nucleotide sequence of Mason-Pfizer monkey virus: an immunosuppressive D-type retrovirus.
Cell
45:375-385[CrossRef][Medline].
|
| 39.
|
Thayer, R. M.,
M. D. Power,
M. L. Bryant,
M. B. Gardner,
P. J. Barr, and P. A. Luciw.
1987.
Sequence relationships of type D retroviruses which cause simian acquired immunodeficiency syndrome.
Virology
157:317-329[CrossRef][Medline].
|
| 40.
|
Varmus, H. E., and P. Brown.
1988.
Retroviruses, p. 53-108.
In
D. E. Berg, and M. M. Howe (ed.), Mobile DNA. American Society for Microbiology, Washington, D.C.
|
| 41.
|
Watanabe, S., and H. M. Temin.
1983.
Construction of a helper cell line for avian reticuloendotheliosis virus cloning vectors.
Mol. Cell. Biol.
3:2241-2249[Abstract/Free Full Text].
|
| 42.
|
Weiss, R.
1984.
Experimental biology and assay of RNA tumor viruses, p. 65-67.
In
R. Weiss, N. Teich, H. Varmus, and J. Coffin (ed.), RNA tumor viruses. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y
|
| 43.
|
Wilhelmsen, K. C.,
K. Eggleton, and H. M. Temin.
1984.
Nucleic acid sequences of the oncogene v-rel in reticuloendotheliosis virus strain T and its cellular homolog, the proto-oncogene c-rel.
J. Virol.
52:172-182[Abstract/Free Full Text].
|
Journal of Virology, January 2000, p. 518-522, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
This article has been cited by other articles:
-
Pouget, C., Gautier, R., Teillet, M.-A., Jaffredo, T.
(2006). Somite-derived cells replace ventral aortic hemangioblasts and provide aortic smooth muscle cells of the trunk. Development
133: 1013-1022
[Abstract]
[Full Text]
-
Parveen, Z., Mukhtar, M., Goodrich, A., Acheampong, E., Dornburg, R., Pomerantz, R. J.
(2004). Cross-Packaging of Human Immunodeficiency Virus Type 1 Vector RNA by Spleen Necrosis Virus Proteins: Construction of a New Generation of Spleen Necrosis Virus-Derived Retroviral Vectors. J. Virol.
78: 6480-6488
[Abstract]
[Full Text]
-
Marin, M., Tailor, C. S., Nouri, A., Kabat, D.
(2000). Sodium-Dependent Neutral Amino Acid Transporter Type 1 Is an Auxiliary Receptor for Baboon Endogenous Retrovirus. J. Virol.
74: 8085-8093
[Abstract]
[Full Text]
Top
Abstract
Text
