Spleen Necrosis Virus, an Avian Immunosuppressive Retrovirus, Shares a Receptor with the Type D Simian Retroviruses
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JOURNAL OF VIROLOGY, May 1992, p. 3026-3031 Vol. 66, No. 5
0022-538X/92/053026-06$02.00/0
Copyright C 1992, American Society for Microbiology
Spleen Necrosis Virus, an Avian Immunosuppressive Retrovirus,
Shares a Receptor with the Type D Simian Retroviruses
VINEET N. KEWALRAMANI,"12 ANTONITO T. PANGANIBAN,3 AND MICHAEL EMERMANl*
Program in Molecular Medicine and Division of Basic Sciences, Fred Hutchinson Cancer Research Center, Seattle,
Washington 981041; Department of Microbiology, University of Washington, Seattle, Washington 981952; and McArdle
Laboratory for Cancer Research, University of Wisconsin, Madison, Wisconsin 537063
Received 23 December 1991/Accepted 10 February 1992
The reticuloendotheliosis viruses (REV) are a family of highly related retroviruses isolated from gallinaceous
birds. On the basis of sequence comparison and overall genome organization, these viruses are more similar to
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the mammalian type C retroviruses than to the avian sarcoma/leukemia viruses. The envelope of a member of
the REV family, spleen necrosis virus (SNV), is about 50%o identical in amino acid sequence to the envelope of
the type D simian retroviruses. Although SNV does not productively infect primate or murine cells, the
receptor for SNY is present on a variety of human and murine cells. Moreover, interference assays show that
the receptor for SNY is the same as the receptor for the type D simian retroviruses. We propose that adaptation
of a mammalian type C virus to an avian host provided the REV progenitor.
Spleen necrosis virus (SNV) is a type C retrovirus isolated we propose that the progenitor of the avian REVs originated
from ducks that is capable of killing ducklings within a week through the adaptive radiation of a BAEV-like mammalian
of inoculation (35) and inducing immunodeficiency in older retrovirus.
animals (38). The virus is cytopathic to cultured chicken
embryo fibroblasts and can productively infect a canine cell
line (32, 33). Phylogenetically, SNV is grouped among the MATERIALS AND METHODS
avian reticuloendotheliosis virus (REV) subspecies, which Nomenclature. Plasmids have a small "p" before their
also includes the defective, transforming virus REV-T and name, while virus stocks derived from those plasmids do not
its replication-competent helper, REV-A (38). SNV and (e.g., pLXSH and LXSH). Virus stocks are designated by
REV-A share over 90% nucleic acid sequence homology the name of the plasmid used to derive the genome followed
across their genomes (24) and use a common receptor (8, 16).
in parentheses by the type of envelope protein on the virion
The predicted amino acid sequence of the envelope gene [e.g., LXSH(REV) is a retrovirus vector derived from trans-
of REV-A has been reported to have about 42% amino acid fection of pLXSH into a REV-packaging line]. Infected cells
identity with the env gene of the simian type D retroviruses are designated by the name of the cell line followed by the
and the type C baboon endogenous virus (BAEV) (18, 31). name of the virus (e.g., D17/SNV).
Assays based on infection interference demonstrate that the Plasmids. pLXSH is a murine leukemia virus (MuLV)-
simian type D retroviruses, BAEV, and the endogenous type based retroviral vector identical to pLXSN (22) except that
C feline virus RD114 use a common receptor (29). However, it contains the hygromycin B phosphotransferase (hph) gene,
the gag and pol genes of the REV family are distinct from which confers resistance to the drug hygromycin B in
those of simian type D retroviruses and instead share ho- eukaryotic cells, in place of the neo gene of pLXSN.
mology with those of mammalian type C retroviruses (2, 3, pSNV-hygro is an SNV-based vector derived from
24, 37). Despite the similarities in primary sequence of pJD216neo (11). It contains the hph gene driven by the SNV
mammalian retroviruses and REV, REV cannot produc- LTR. pPB1l1 and pSW253 are complete proviral clones of
tively infect cells of murine or primate origin (14, 19). SNV and REV-A, respectively (1, 5). pSHRM-15 encodes a
Here, we show that the REV receptor is present on both complete proviral clone of SRV-3 (25).
murine and human cell lines. These cells can be infected with Sequencing and analysis. The SNV env open reading frame
retrovirus vectors that are packaged with REV Gag, Pol, and and flanking sequences of pPB1O1 were cloned into pBlue-
Env proteins. While this work was in progress, Koo et al. scriptKS+ (Stratagene Co., La Jolla, Calif.) and pTZ18R
also reported that SNV can enter human as well as simian (Pharmacia). Subclones were generated by making nested
cells (19). Furthermore, sequence analysis of SNV env unidirectional deletions commencing from the 5' portion of
reveals a greater predicted amino acid sequence homology the env gene (17). Single-stranded DNA was produced by
with the simian type D retroviruses and BAEV than previous using M13K07 helper phage and was the substrate for Sanger
comparisons of REV-A to these simian retroviruses. Ac- dideoxy sequencing (27). Nucleotide oligomers correspond-
cordingly, preinfection of cells susceptible to REV infection ing to phage T3 and T7 RNA polymerase promoters and
with a simian type D virus will inhibit subsequent infection oligomers based on the REV-A env sequence (37) were used
of REV-A by three orders of magnitude. This interference as primers in sequencing.
suggests that REV-A and SNV use the same receptor as the Sequence analyses were performed with the software
simian type D retroviruses and BAEV. On the basis of package of the University of Wisconsin Genetics Computer
sequence similarities and utilization of a common receptor,
Group (9), using the BestFit algorithm (28) for alignment of
amino acid sequence. In all alignments, gap weight was 5.0
and gap length weight was 0.1.
*
Corresponding author. Cells. D17 cells are derived from a dog osteosarcoma, NIH
3026VOL. 66, 1992 SNV RECEPTOR 3027
3T3 tk- is a mouse fibroblast line, and HeLa cells are TABLE 1. Prevalence of SNV receptor among mammalian cells
derived from a human cervical carcinoma. B78 cells, L aprt- Hygromycin-resistant Cell
tk- cells, C3H 1OT1/2, and C3H C2C12 cells are of murine Cell linea
origin. Human primary fibroblasts were a gift of Matt
colonies transduced
by LXSH(REV) (%)b
.i.
origi
Thayer. CEMx174 cells are a T/B-cell human hybrid line,
and H9 is a human T-cell line. PA317 cells are a packaging D17 10fc Canine
line that will package viral genomes in an MuLV virion with HeLa 12 Human
HFFd 59 Human
an amphotropic envelope (21). D17.2G cells are a packaging L aprt- tk- 4 Murine
line that will package viral genomes in an REV-A virion with B78 5 Murine
an REV-A envelope (12). Unless otherwise indicated, all cell C2C12 (C3H) 5 Murine
lines were grown in Dulbecco's modified Eagle's medium 1OT1/2 (C3H) 67 Murine
(DMEM) with 10% calf serum. COS-7 cells were grown in NIH 3T3 tk-3028 KEWALRAMANI ET AL. J. VIROL.
SNV 1 MDCLTLR5AFGKVDQAKILILLVA1 9FGTTAEGYP?.LQQLWELPCDCSGGYVSSIPTYYTYSLDCGGSThYLTYGSGGSWSWGGFKQWCVFKP
I I ill 11 11 1111111 ill 11
SRV-3 1 MNFIWSLVILSQISQvQA.... ..GFGDPREAAIQQKHGKPCDCAGGYVSSPPINSLTTVSCSTHTAY.... SVTNSL ........ KWQCVSTP
V V1
100 KIIPSVQGQPGPCPSECLQIATQ.MHSTCYEKTQECTLLGKTYFTAILQKTKlGSYEDG...
., P IQASCTM.I 1'VGKPVWI PVAPVYVSDGGG
83
1111 11 III 11 II 11 III 11111
. .TTTHIGSCPCTISYDSVHASCYNHYQQCNIGNTYLTATITGDRTPAIGDGNVPTVLGTSHNLITAGCPN QWCWNSERPSVBISDGGG
190 PTDMIREESVRPEMLEIIRBSYPSVQYHPLAP PRSVD IVP PQSDI LNATNPKUAKNAWNCMLGIPIPIPT .....I LDNS
I I I 11 illlll 11 III III i 11 1 1 1 1 1
181 PQDRARDI IVNFLHERSLFPELSYYHPILEARKIAElDALDLATVHSLLNASQPSLAEDCWLCLQSGDPVPLALPYNJDTlSNFACLSNHSCP
v E o
0 vv
283 LSLPFGCNPPGSIDVSC.YAGEADNRTGIPVGYVHFTNCTSIQEVTNETSQMNTRLCPPPGVVCGNMAYTALPwPwIGcILAsIvPDISIIsGE
11 11 11 1iii 11 11 11 11
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I 1111111 III III
281 LTPPFLVQPFWFTDSNCLYAEYQNNSFDIDVGLASFTNCSSYYNVSTASKPSNS... ICAPNSSVFVCGNNKAYTYIPTNWTGSCVLATLLPDIDIIPGS
382 EPIPLPSIEYTARRHK RAVQFIPLLVGLGISGATLAGGTGLGVSVETYHKLSNQLIEDVQALSGTINDLQDQIDSLAKVVLQNRRGLDLLTAEQG
11 11 1 1 * 11 1111 11111 1 1 11111 1 111 111 1111 1 1111111111111111111
378
EPVPIPAIDHFLGKAK RAIQLIPLFVGLGITT!AVSTGAAGLGVSITQYTKLSHQLISDVQAISSTIQDIQDQVDSLAEVVLQNMGLDLLTAEQG
V W v
477 GICLAIQEKCCFYANKSGIVRDKIRKQEDLIERKRALYDNPLWSGLNGFLPYLPLLGPLFGLILFLTLGPCIMKTLTRIIHDKIQAVKS 567
1111111111111111111111 11 11 1 1 1111 1 11111 111111 1I1 11 1I
473 GICIQEKCCFYANKSGIVRDKIKNL DDIRRRRQLIDNPF TSFEGFLPYVIMPLGPLLCLLLVLSFGPIIFNKLHTFIKHQIESIQA 563
FIG. 1. Alignment of the predicted amino acids of the SNV and SRV-3 envelope proteins. The nucleic acid sequence of SNV was
translated to a one-letter amino acid code and aligned with the amino acid sequence of SRV-3 as described in Materials and Methods. Dots
along the sequences represent gaps in the alignment. Vertical lines represent identical amino acids. SNV paired cysteines are denoted by /.
SNV glycosylation sites which nearly align with SRV-3 (within 3 amino acids) are denoted by X, and the site which does not align is denoted
by 0. The cleavage between the SU and the TM proteins is marked with an asterisk. The immunosuppressive peptide is underlined.
(Table 1). Moreover, the primary human skin fibroblast conserved (10, 20). Within the simian type D retrovirus
culture gave 59% as many colonies as D17 cells. This receptor interference group, the conservation of amino acid
indicates that despite the block to productive infection of identity between the Env proteins of the different members
SNV in human cells, the receptor for SNV must exist on ranges from 48 to 87% (references 18, 23, and 34 and data not
human cells. In addition, because the colonies can be grown shown). We sequenced the env gene of an infectious molec-
for multiple generations, it is unlikely that there is a block to ular clone of SNV and determined the degree of similarity it
proviral integration. shared with the Env proteins of other retroviruses that infect
In agreement with previous reports that indicated that mammalian cells. We found that the predicted amino acid
NIH 3T3 cells could not be infected with SNV and that one sequence of SNV Env is 49% identical to that of a prototypic
of the blocks to infection may be at entry (14), we could not simian type D virus, SRV-3 (Fig. 1). When conservative
detect infection of NIH 3T3 cells with our pseudotyped amino acid changes are included in the alignment, there is
vector (Table 1). However, a survey of four other mouse 65% similarity between the two sequences. SNV Env is even
cell lines showed that each could be infected. One mouse more highly conserved with the squirrel monkey retrovirus
cell line, 1OT1/2, could be infected very efficiently by (55% amino acid identity) and the type C BAEV (54%
LXSH(REV) and gave 67% as many hygromycin-resistant identity) (Table 2). More importantly, however, the posi-
colonies as did D17 cells. The difference in sensitivity to tions and occurrences of cysteines within the SNV Env are
infection is not mouse strain specific because 10T1/2, C2C12, conserved among the Env proteins of the members of the
and L cells are derived from C3H mice. Supernatant ob- simian type D virus group as well as the Env of the type C
tained from LXSH-transformed murine clones of B78 and BAEV (Fig. 1 and Table 2). This suggests that the tertiary
1OT1/2 cells did not contain reverse transcriptase activity structures of the Env proteins determined by disulfide bonds
and was not able to transfer drug resistance to naive B78 or are probably similar among these simian viruses. In addition,
1OT1/2 cells (data not shown). This indicates that infection of there is a very strong conservation of the potential N-linked
mouse cells was not due to contamination with an ampho- glycosylation sites between SNV Env and the Env proteins
tropic or ecotropic helper. Moreover, infection of NIH 3T3 of the viruses in the simian type D retrovirus interference
cells with the same stocks used to infect B78, 1OT1/2, and the group.
other mouse cell lines yielded no drug-resistant colonies. Within Env, the transmembrane (TM) portion of the Env
Thus, the receptors for the avian retroviruses REV-A and precursor is more conserved than the surface (SU) portion
SNV are displayed on some cells of murine and human between SNV and the envelope of BAEV and the simian
origin. type D viruses (Fig. 1 and data not shown). The specific
SNV Env shares homology with Env of BAEV and simian regions of high identity within the TM portion include
type D retroviruses. Of those proteins which are common to residues designated the "immunosuppressive peptide,"
all retroviruses, the envelope (Env) protein is the least which appear in most mammalian type C and type DVOL. 66, 1992 SNV RECEPTOR 3029
TABLE 2. Similarity of type D and type C retroviral envelopes Hygror colonies/ml
to SNV envelope
No. of putative N- D17 D17/SRV-3 D17/SNV
Virus' iAnmo acid No. of aligned linked glycosylation
(%)b cysteines/total no.c sites conserved/ REV-Hygro
hyg 1.9 x 10 4 1.5 x 10 I 1.5x 101,
SRV-1 49.5 19/23 7/8
SRV-2 50.2 19/23 7/8
SRV-3 49.3 21/23 7/8 LXSH(A-MuLV)
SMRV 55.2 20/23 7/8
BAEV 53.6 20/23 6/8 EJ=SV4@ hyg C==E 6.8 x 104 5.9 x 104 6.3 x 104
GALV 29.8 9/23 3/8 FIG. 2. Interference of REV infection by preinfection of cells
Mo-MuLV 28.0 8/23 3/8 with SRV-3. Stocks of REV-hygro with REV-A helper virus and
stocks of helper-free LXSH(A-MuLV) produced from an amphotro-
a Virus sequence information was obtained from the GenBank data base pic MuLV-packaging line were prepared as described in Materials
(Los Alamos National Laboratory). SRV-1, -2, and -3 (simian retrovirus and Methods. Dilutions of each virus stock were used to infect D17
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serotypes 1, 2, and 3) and SMRV (squirrel monkey retrovirus) are type D cells, D17 cells preinfected with SRV-3, and D17 cells preinfected
retroviruses, whereas BAEV, GALV (gibbon ape leukemia virus), and
Mo-MuLV (Moloney murine leukemia virus) are type C retroviruses. with SNV. The number of hygromycin-resistant colonies per ml of
b Alignments were performed by using the BestFit algorithm (28) in the virus stock is shown. A titer of 1.5 x 101 hygromycin-resistant
University of Wisconsin Genetics Computer Group software package (9). Gap (Hygror) units per ml is estimated from three colonies in a well that
weights = 5.00; gap length weights = 0.1. was infected with 200 ,ul of virus. A representative experiment is
c These ratios reflect the number of cysteins which align against the total shown.
number of SNV cysteines under the BestFit algorithm. The mature form of
SNV Env glycoprotein contains a total of 23 residues in the SU and TM
portions of the molecule and does not contain the N-terminal secretory leader
sequence included in Fig. 1.
d Putative N-linked glycosylation sites are those tripeptides of the sequence
N-X-S or N-X-T, where X cannot be a proline residue. Sites are considered fore, in order to obtain a population of D17 cells that was
aligned when they occur within 3 residues under the amino acid alignment. uniformly infected with SRV-3, we cocultivated the nonad-
herent SRV-3-infected CEMx174 cells (CEMx174/SRV-3
cells) with a monolayer of D17 cells to produce D17/SRV-3
cells (for details, see Materials and Methods).
retroviruses, and the regions which flank the immunosup- In order to demonstrate that infected cells expressed env
pressive peptide (7, 31). In contrast, SNV displays only 28% of either SRV-3 or SNV, RNA from D17 cells, D17/SRV-3
amino acid identity with Moloney murine leukemia virus cells, and D17/SNV cells was extracted and analyzed. Hy-
(Mo-MuLV) and 30% with another type C primate retrovi- bridization of a Northern (RNA) blot using a probe from
rus, gibbon ape leukemia virus. The limited homology ob- SRV-3 probe encompassing the 5' end of the env gene shows
served with these type C viruses appears outside of the SU that the D17 cells infected with SRV-3 by cocultivation with
portion and is due to the highly conserved immunosuppres- producer cells contain two species of RNA corresponding to
sive peptide in the TM portions of the viruses (reference 31 the genomic RNA and spliced envelope RNA (data not
and data not shown). The unusual degree of similarity of shown). The ratio of envelope to genome RNA from the
SNV Env with Env of the type D retroviruses and of BAEV, infected D17/SRV-3 cells parallels the ratio of viral RNA
in fact, predicts a phylogeny that is distinct from pol-based from productively infected CEMx174/SRV-3 cells. Probing a
trees which place SNV at a closer evolutionary distance to parallel blot with a REV-specific probe showed SNV ge-
MuLVs than to the simian type D viruses or BAEV (10, 20). nomic and envelope RNA only in the D17 cells chronically
Interference of REV infection by preinfection of cells with infected with SNV (data not shown). These results demon-
SRV-3. Given the similarity in Env between SNV, BAEV, strate that neither culture was cross-contaminated.
and the simian type D viruses, we wished to determine These cells were then challenged with a REV-A-packaged
whether these viruses use the same receptor. Interference virus, REV-hygro. As shown in Fig. 2, this stock yielded 1.9
assays have been used to determine whether or not two x 104 hygromycin-resistant colonies per ml of inoculum
retroviruses use the same receptor (29, 36). Interference is when D17 cells were infected. This same stock yielded only
thought to occur by the association of the endogenously 15 hygromycin-resistant colonies per ml when it was used to
expressed Env with the cellular receptor, thus reducing the infect D17 cells that were chronically infected with SNV.
amount of receptor that may function on the cell surface This confirms previous findings that REV-A and SNV use a
(36). Preinfection of cells with SNV or REV-A will protect common receptor (8, 16).
cells from superinfection by a REV-packaged vector through The REV-hygro stock was also used to infect D17/SRV-3
the endogenous production of retroviral Env (8, 16). We cells. Preinfection of the D17 cells with SRV-3 reduced the
therefore sought to determine whether preinfection of cells number of hygromycin-resistant colonies to 15 per ml of
with SRV-3, a simian type D virus, would interfere with REV-hygro (Fig. 2). This indicates that SRV-3 interferes
subsequent infection of those cells by REV-A. with REV infection and therefore implies that both viruses
D17 cells were used as a target for this experiment because use the same receptor. In order to demonstrate that this
they are readily infectable by REV-A and SNV. D17 cells interference was specific to vectors packaged with REV
chronically infected with SNV served as the positive control proteins, the titer of an amphotropic virus stock containing
for interference of infection by a REV-packaged virion (8, the MuLV vector LXSH was determined on D17, D17/SNV,
16). On the other hand, we could not produce a population of and D17/SRV-3 cells. The titer of LXSH(MuLV) was not
D17 cells that were chronically infected with SRV-3 by significantly affected by preinfection of the D17 cells with
direct infection because the virus could not spread in the either SNV or SRV-3 (Fig. 2). This indicates that the
culture (data not shown). SRV-3 could readily infect and resistance to REV-hygro infection of D17 cells preinfected
replicate in the human lymphoid cell line CEMx174. There- with SNV or SRV-3 is specific to the challenge virus.3030 KEWALRAMANI ET AL. J. VIROL.
DISCUSSION 2. Barbacid, M., E. Hunter, and S. A. Aaronson. 1979. Avian
reticuloendotheliosis viruses: evolutionary linkage with mam-
The sequence of the env gene of SNV, an avian virus, malian type C retroviruses. J. Virol. 30:508-514.
reveals approximately 50% identity with the predicted amino 3. Charman, H. P., R. V. Gilden, and R. L. Witter. 1979. Reticu-
acid sequences of both the simian type D retroviruses and loendotheliosis virus: detection of immunological relationship to
BAEV. Cells preinfected with either SRV-3 or SNV are mammalian type C retroviruses. J. Virol. 29:1221-1225.
markedly less susceptible to superinfection when challenged 4. Chen, C., and H. Okayama. 1987. High-efficiency transforma-
by vectors packaged with REV proteins. The interference to tion of mammalian cells by plasmid DNA. Mol. Cell. Biol.
7:2745-2752.
infection suggests that these avian and simian viruses use an 5. Chen, I. S. Y., T. W. Mak, J. J. O'Rear, and H. M. Temin. 1981.
equivalent receptor. Consistent with this conclusion, we Characterization of reticuloendotheliosis virus strain T DNA
found that viral pseudotypes displaying a REV Env can and isolation of a novel variant of reticuloendotheliosis virus
infect human cells. We also find that REV-A pseudotypes strain T by molecular cloning. J. Virol. 40:800-811.
can enter some murine cells. Blocks to productive infection 6. Chomczynski, P., and N. Sacchi. 1987. Single-step method of
of the virus in these mammalian cells, therefore, must occur RNA isolation by acid guanidinium thiocyanate-phenol-chloro-
at steps in the virus life cycle beyond virus entry. form extraction. Anal. Biochem. 162:156-159.
The presence of a REV receptor on murine cells is 7. Cianciolo, G. J., T. D. Copeland, S. Oroszlan, and R. Snyder-
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somewhat surprising, because the simian type D viruses are man. 1985. Inhibition of lymphocyte proliferation by a synthetic
restricted from entering mouse cells (29, 30). On the other peptide homologous to retroviral envelope proteins. Science
230:453-455.
hand, pseudotypes made with the BAEV envelope can infect 8. Delwart, E. L., and A. T. Panganiban. 1989. Role of reticuloen-
murine cells at low efficiency (30). These inconsistencies in dotheliosis virus envelope glycoprotein in superinfection inter-
receptor tropism are probably due to subtle differences in the ference. J. Virol. 63:273-280.
Env proteins of viruses in this interference group (29). In 9. Devereux, J., P. Haeberli, and 0. Smithies. 1984. A comprehen-
addition to SNV Env and BAEV Env pseudotypes being sive set of sequence analysis programs for the VAX. Nucleic
able to enter mouse cells, the gag and pol gene products of Acids Res. 12:387-395.
the REVs and type C BAEV are more closely related to one 10. Doolittle, R. F., D. F. Feng, M. A. McClure, and M. S. Johnson.
another than they are to the type D simian retroviruses (2, 3, 1990. Retrovirus phylogeny and evolution, p. 1-23. In R.
Swanstrom and P. K. Vogt (ed.), Retrovirology. Springer-
24, 36, 37). Verlag, Berlin.
These data imply a common evolutionary origin for SNV 11. Dougherty, J. P., and H. M. Temin. 1986. High mutation rate of
and BAEV that is distinct from the presumed recombinato- a spleen necrosis virus-based retrovirus vector. Mol. Cell. Biol.
rial origin of the simian type D retroviruses, which possess a 6:4387-4395.
mouse mammary tumor virus-like Gag and Pol (18, 31). 12. Dougherty, J. P., and H. M. Temin. 1988. Determination of the
Unlike the REVs, BAEV is an endogenous virus and is rate of base-pair substitution and insertion mutations in retro-
therefore transmitted as a stable genetic element. Also, virus replication. J. Virol. 62:2817-2822.
unlike SNV, BAEV displays no apparent pathogenesis to its 13. Embretson, J. E., and H. M. Temin. 1987. Lack of competition
host (36). Because SNV is an exogenous and pathogenic results in efficient packaging of heterologous murine retroviral
RNAs and reticuloendotheliosis virus encapsidation-minus
retrovirus, we propose that the avian REVs are the result of RNAs by the reticuloendotheliosis virus helper cell line. J.
an adaptive radiation of a BAEV-like, mammalian retrovirus Virol. 61:2675-2683.
to birds. Direct transmission of BAEV to the North Ameri- 14. Embretson, J. E., and H. M. Temin. 1987. Transcription from a
can fowls which host the REV-like viruses seems unlikely, spleen necrosis virus 5' long terminal repeat is suppressed in
because both viral hosts are geographically isolated and the mouse cells. J. Virol. 61:3454-3462.
xenotropic host range of BAEV does not extend to avian 15. Emerman, M., R. Vazeux, and K. Peden. 1989. The rev gene
cells in vitro (36). Because the variability of BAEV is fixed product of the human immunodeficiency virus affects envelope-
as an endogenous element, the restriction of BAEV from specific RNA localization. Cell 57:1155-1165.
avian cells precludes the possibility of a REV being the 16. Federspiel, M. J., L. B. Crittenden, and S. H. Hughes. 1989.
direct progenitor of BAEV. This restriction also suggests the Expression of avian reticuloendotheliosis virus envelope con-
fers host resistance. Virology 173:167-177.
existence of another type C virus, related to BAEV, which 17. Henikoff, S. 1987. Unidirectional digestion with exonuclease III
was the true REV progenitor. Given the potential of retro- in DNA sequence analysis. Methods Enzymol. 155:156-165.
viruses to spread among similar host species, retroviral 18. Kato, S., K. Matsuo, N. Nishimura, N. Takahashi, and T.
transmission across animal phyla has not been previously Takano. 1987. The entire nucleotide sequence of baboon endog-
documented to have occurred in recent viral evolution. SNV enous virus DNA: a chimeric genome structure of murine type
may be exceptional in that regard. C and simian type D retroviruses. Jpn. J. Genet. 62:127-137.
19. Koo, H.-M., A. M. C. Brown, Y. Ron, and J. P. Dougherty.
ACKNOWLEDGMENTS 1991. Spleen necrosis virus, an avian retrovirus, can infect
We thank Peggy Lee, Paul Lewis, and Maxine Linial for discus- primate cells. J. Virol. 65:4769-4776.
sions and critical readings of the manuscript. V.N.K. thanks Eric 20. Lewe, G., and R. M. Flugel. 1990. Comparative analysis of the
Delwart for insightful suggestions. We thank Eric Hunter, A. Dusty retroviralpol and env protein sequences reveal different evolu-
Miller, Howard Temin, and Matt Thayer for plasmids or cells and tionary trees. Virus Genes 3:195-204.
Joe Dougherty for communicating results prior to publication. 21. Miller, A. D., and C. Buttimore. 1986. Redesign of retrovirus
This work was supported by grants R01 AI30927 (M.E.) and CA packaging cell lines to avoid recombination leading to helper
22443 (A.T.P.) from the Public Health Service. V.N.K. is supported virus production. Mol. Cell. Biol. 6:2895-2902.
by NRSA T32 GM07270 from the National Institute of General 22. Miller, A. D., and G. J. Rosman. 1989. Improved retroviral
Medical Sciences. A.T.P. is a Shaw Scholar. M.E. is a Scholar of vectors for gene transfer and expression. BioTechniques 7:980-
the American Foundation for AIDS Research. 990.
23. Oda, T., S. Ikeda, S. Watanabe, M. Hatsushika, K. Akiyama,
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