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Journal of Virology, January 2000, p. 1033-1037, Vol. 74, No. 2
Institut für Klinische und Molekulare
Virologie, Universität Erlangen-Nürnberg, 91054 Erlangen, Germany
Received 21 June 1999/Accepted 19 October 1999
Herpesvirus ateles is an agent indigenous to spider
monkeys (Ateles spp.) and causes fulminant lymphomas in
various New World primates. Structural and genetic relatedness led to
the classification of this virus as a member of the genus
Rhadinovirus. It is most closely related to
Herpesvirus saimiri. The 108,409-bp light DNA segment of
the herpesvirus ateles strain 73 genome has two genes for U-RNA-like
transcripts and 73 open reading frames, of which at least 6 show
significant homologies to cellular genes (encoding complement control
proteins, apoptosis-regulatory proteins, D-type cyclins, interleukin-8
receptors, and enzymes involved in nucleotide metabolism). The left
terminal region of the light DNA segment bears the putative
rhadinovirus oncogene tio.
Herpesvirus ateles strain 810 was
isolated from a primary kidney cell culture of a mature male spider
monkey (Ateles geoffroyii) imported from Guatemala
(47). This isolate, taxonomically classified as
Ateline herpesvirus 2 (AtHV-2) (49), was found to
be oncogenic in marmosets (Saguinus oedipus) and owl monkeys
(Aotus trivirgatus), which develop malignant lymphomas with
leukemia (25, 37, 46). More AtHVs (strains 73, 87, 93, and
94) were isolated from lymphocytes of Columbian spider monkeys
(Ateles paniscus) by cocultivation with permissive cell
cultures (18). Strain 73 was classified as AtHV-3
(49). Cotton-topped and white-lipped marmosets, owl monkeys (24), and distinct rabbit strains (M. D. Daniel, R. D. Hunt, N. W. King, and J. K. Ingalls,
Abstr. 3rd Int. Symp. Oncogenesis and Herpesviruses, p. 213, 1977),
infected with AtHV-3 or with AtHV strain 93 or 94 developed lymphomas
from which continuous cell lines can be established
(18). AtHV-3 was also shown to transform T lymphocytes
from S. oedipus and S. fuscicollis in vitro
(16, 17, 32).
Members of the genus Rhadinovirus have been classified by
their genetic organization. Complete genomic sequences are known for
Alcelaphine herpesvirus 1 (15), Murine
herpesvirus 68 (60), Human herpesvirus 8 (50, 54), Rhesus rhadinovirus (56), and Herpesvirus saimiri A11 (Saimiriine herpesvirus
2 [SaHV-2]) (5), the type species of the genus.
Equine herpesvirus 2 is closely genetically related to the
rhadinoviruses; however, its overall genome structure corresponds to
that of betaherpesviruses (58). All of these viruses are
clearly distinct from Epstein-Barr virus, which defines the
type species of the genus Lymphocryptovirus within the
subfamily Gammaherpesvirinae.
Since AtHV-2 and -3 and SaHV-2 have been proven unique in their ability
to transform monkey T cells to a phenotype of permanent growth in vitro
and in vivo and represent the only available model system for studying
viral T-cell lymphoma induction, I explored the genetic content of
AtHV-3. In this report, the genetic relationship of AtHV-3 to the
family of herpesviruses is established by the presentation of the
primary structure of its genome.
AtHV-3 was obtained from a frozen virus stock (18) and was
propagated on owl monkey kidney cells (10) as described
elsewhere (19). Viral DNA was digested with a restriction
endonuclease (SacI, EcoRI, PvuII, or
HindIII) and subcloned into pBluescript (Stratagene,
LaJolla, Calif.) by standard procedures. Authentic clones were
confirmed as such by hybridization with AtHV-3 DNA, partial sequencing,
and comparison with the SaHV-2 prototype sequence (5). A set
of 61 distinct overlapping clones covering the whole light DNA segment
(L-DNA) as well as several individual heavy-DNA (H-DNA) repeat clones
were obtained and sequenced by using a combination of the shotgun
and primer walking strategies. The final AtHV-3 L-DNA sequence was
generated from a total of 728,899 bases, resulting in a redundancy of
6.63 per base pair. Computer analyses were performed as described
previously (5, 15). Potential open reading frames (ORFs)
were defined by applying the following criteria: (i) a minimum of 60 amino acids in the derived polypeptide, (ii) a codon preference
like those of unambiguously identified viral genes, (iii) the presence
of a typical translational start signal, (iv) potential promoter and
transcriptional terminator elements, or (v) sequence homologies to
known reading frames of viral or cellular origin.
Earlier studies of the genome structure of AtHV revealed that its
genomic DNA is composed of a unique DNA segment of low G+C content
(L-DNA), comprising 74% of the genome, flanked by multiple copies of a
tandemly repeated element of high G+C content (H-DNA) (19).
This resembles the genome structure of SaHV-2 (9), the
prototype of the genus Rhadinovirus (5). The
unique L-DNA region of AtHV-3 was determined to have a total of 108,409 bp (36.6% G+C), while the prototypic H-DNA repeat unit was found to
contain 1,582 bp (77.1% G+C).
Sequence analysis of the standard H-DNA repeat unit of AtHV-3 uncovered
numerous internal direct and inverted repeat structures, among them an
internal 154-bp direct repeat sequence whose presence has been
suggested by endonuclease digestion data (19). The H-DNA of
SaHV-2 and AtHV-2 and -3 had been found not to be homologous by
heteroduplex analysis (19); this was confirmed here by
comparison of the AtHV-3 and SaHV-2 H-DNA sequences. The only common
motifs found are related to pac-1 and pac-2 sequences corresponding to genome cleavage recognition motifs conserved among herpesviruses (11) and to the cleavage-packaging site which defines the
genomic termini and the junctions between H- and L-DNA sequences. These junctions, which were defined by the first nucleotide that diverges from the standard H-DNA repeat unit, can be localized to a single nucleotide of H-DNA (position 1336H) at both ends of the
L-DNA. Like in SaHV-2, the far-left terminal region of L-DNA consists of H-DNA (2, 4), which in the case of AtHV-3 is not
rearranged but continuous.
Analysis of the genomic sequence of the L-DNA of AtHV-3 revealed 73 ORFs that potentially code for at least 73 proteins (Fig. 1; Table
1). Forty-eight reading frames were found
to be conserved among most herpesviruses. A minimum of 14 deduced amino
acid sequences are specific for the subfamily
Gammaherpesvirinae (ORFs 3, 10, 11, 23, 27, 28, 45, 48 to
52, 58, and 75); 6 were found in rhadinoviruses only (ORFs 1, 4, 14, 71, 72, and 73), some of which appear to be restricted to specific
virus species. Molecular piracy of cellular genes appears to be a
common feature of rhadinovirus genomes and is most apparent in the
genomes of SaHV-2 (5) and the recently isolated human
Kaposi's sarcoma-associated herpesvirus (KSHV; human herpesvirus 8 [HHV-8]) (50, 54). Analysis of the entire 108.4 kbp of the
AtHV-3 L-DNA also revealed a number of cellular homologs which might
contribute to viral pathogenicity. These include a virus-encoded
interleukin-8 receptor (IL-8R) (1), a D-type cyclin
(29, 57), FLICE-inhibitory protein (FLIP) (59),
thymidylate synthetase (TS) (23, 53), ie14/vsag
(34, 63), complement-regulatory proteins (2,
20), and two U-RNA-like transcripts (3, 39, 61) (Fig.
1; Table 1). Notably, AtHV-3 does not code for a homolog of
dihydrofolate reductase, IL-17, or CD59, which are encoded by SaHV-2.
Homologs for IL-6, macrophage-inhibitory protein 1-
0022-538X/00/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Primary Structure of the Herpesvirus
Ateles Genome
ABSTRACT
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chemokines, and viral interferon-regulatory factors, all of which
are encoded by HHV-8, were not identified. However, apparently all
identified ORFs of AtHV-3 are conserved in SaHV-2 (Table 1), with amino
acid sequence identities ranging from 30.4 to 92.5% (average, 75.1%).
A gapped alignment of their complete L-DNAs revealed an average DNA
sequence conservation of 76.4%.
View larger version (47K):
[in a new window]
FIG. 1.
Circular representation of the AtHV-3 genome. H-DNA
sequences were added to L-DNA to give a total genome size of
approximately 150 kbp as estimated by earlier studies. ORFs are shown
as directed boxes around circular restriction maps, and cellular
homologs are shaded dark gray. Areas significantly different from the
SaHV-2 genome are depicted as light-gray-shaded areas I to V. The scale
is 5 kbp/unit, with a diamond sign located every 20 kbp. ORF numbers
are given for orientation and reference to Table 1. Abbreviations:
HAUR, herpesvirus ateles U-like RNA; CCPH, complement control protein
homolog; gB, glycoprotein B; pol, DNA polymerase; ie14/vsag, viral
superantigen; TK, thymidine kinase; gH, glycoprotein H; MCP, major
capsid protein; gL, glycoprotein L; RR, ribonucleotide reductase (l,
large subunit; s, small subunit); cyclin, viral D-type cyclin; vIL-8R,
viral IL-8 receptor; FGARAT, formylglycineamide ribotide
amidotransferase.
TABLE 1.
Description of AtHV-3 ORFs and comparison to SaHV-2
and HHV-8
At least five genomic loci of AtHV-3 were found to be quite distinct from those of SaHV-2 (Fig. 1). Region I corresponds to a repetitive DNA structure within ORF73 which is present in most rhadinoviruses (5, 15, 54). The function of the ORF73 protein is not known; however, a protein encoded at an analogous position in the HHV-8 genome has been demonstrated to be a nuclear antigen expressed during latency (52). Region II is characterized by variability within the 5' noncoding region of the thymidylate synthetase (TS) gene, which has been tentatively mapped as the origin of lytic replication in SaHV-2 (55), and by the presence of an additional 168-bp repeat sequence, composed of 15.3 copies of an 11-bp unit, downstream of ORF71. Independent of this repeat insertion, ORF71 of AtHV-3 is likely to be nonfunctional due to multiple frame shifts at the 3' end of this ORF, which encodes a FLIP in other rhadinoviruses (45, 59). This appears to be a specific feature of AtHVs, since similar results were obtained for AtHV-2 after PCR amplification and sequencing of the corresponding genomic region. Region III is composed of two insertions, of 347 and 240 bp, into the AtHV-3 genome, which affect the 3' noncoding region of ORF50 and most of ORF51, respectively. Although no obvious sequence homology was detected, AtHV-3 ORF51 is a positional homolog of HHV-8 K8.1, murine herpesvirus 68 M7, bovine herpesvirus 4 BORFD1, alcelaphine herpesvirus 1 A8, and SaHV-2 ORF51. All of these ORFs code for a typical type I transmembrane glycoprotein with a high content of Ser and Thr residues and multiple N-linked glycosylation sites (NxT/S). Region IV of AtHV-3 has four deletions relative to the SaHV-2 genome: one of 177, affecting ORF12; one of 900 bp, in the gene encoding a viral IL-17 (5, 33); and two, of 632 and 84 bp, in the gene coding for the CD59 homologue in SaHV-2 (6).
Region V corresponds to a highly variable region of SaHV-2 (44) which has been shown to mediate the oncogenic and transforming phenotype (12-14, 31, 35, 42). The high degree of variability among different strains of SaHV-2 has led to their subdivision into three subgroups, A, B, and C (43). Group A, represented by the SaHV-2 prototype strain A11, encodes a single protein, termed StpA (for saimiri transformation-associated protein of group A), which has been demonstrated to be transforming in cell culture and in transgenic mice (30, 36). StpA has been shown to become phosphorylated by cellular Src and to bind to the Src SH2 domain by a phosphotyrosine-dependent mechanism (38). It has also been suggested that StpA interacts with the T-cell-specific Src family kinases Lck and Fyn (38). Group C viruses C484 and C488 encode two proteins, StpC and Tip, within this variable genomic region (7, 21). On the one hand, StpC has been shown to be transforming in cell culture (30) and to cause epithelial tumors in transgenic mice (48). It interacts directly with cellular Ras and competes with cellular Raf for binding to Ras, thereby affecting the signal transduction pathway of Ras (22, 26). On the other hand, Tip, a tyrosine kinase-interacting protein of SaHV-2 group C viruses, interacts with T-cell-specific kinases of the Src family, predominantly Lck (8, 41). Although its influence on Lck activity has been controversial (28, 40, 51, 62), Tip has been shown to associate with Lck by binding to the SH3 domain of Lck via its SH3 binding motif and, additionally, to the kinase domain of Lck via its CSKH motif (27, 28; U. Friedrich, unpublished data). In transformed monkey T cells, a spliced mRNA is transcribed within this variable genomic region of AtHV-3, which encodes the two-in-one protein Tio, a protein that exhibits homologies with both StpC and Tip (4). Homologous sequences were identified in AtHV-2, indicating a very close relationship between AtHV-2 and AtHV-3. AtHV-3-encoded Tio has been demonstrated to combine functions of Tip and StpA/B: Tio interacts with cellular Src family kinases by binding to their SH3 domains via an SH3 binding motif related to Tip and by binding to the SH2 domains of Lck, Src, and Fyn in a phosphotyrosine-dependent manner, like StpA (4). Sequence homology to StpC also suggests an additional function related to StpC; however, this has not yet been supported by experimental evidence. Tio appears to be the single rhadinovirus oncoprotein encoded in the entire AtHV-3 genome which is a multifunctional protein involved in signal transduction.
Nucleotide sequence accession numbers. The nucleotide sequences of the AtHV-3 unique L-DNA region, AtHV-3 H-DNA repeat unit, AtHV-2 ORF71, and AtHV-2 tio gene were submitted to the GenBank database and assigned accession no. AF083424, AF126541, AF133729, and AF135064, respectively.
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ACKNOWLEDGMENTS |
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I thank B. Fleckenstein and S. M. Lang for critical readings of the manuscript.
This work was supported by the Deutsche Forschungsgemeinschaft, Sonderforschungsbereich 466.
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FOOTNOTES |
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* Mailing address: Institut für Klinische und Molekulare Virologie, Friedrich-Alexander-Universität Erlangen-Nürnberg, Schlossgarten 4, D-91054 Erlangen, Germany. Phone: 49-9131-8526483. Fax: 49-9131-8526493. E-mail: jsalbrec{at}viro.med.uni-erlangen.de.
To the memory of my father.
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Journal of Virology, January 2000, p. 1033-1037, Vol. 74, No. 2
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