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Journal of Virology, January 2000, p. 584-590, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
Species Specificity of Macaque Rhadinovirus Glycoprotein
B Sequences
Marcy R.
Auerbach,
Susan C.
Czajak,
Welkin E.
Johnson,
Ronald C.
Desrosiers, and
Louis
Alexander*
New England Regional Primate Research Center,
Harvard Medical School, Department of Microbiology and Molecular
Genetics, Southborough, MA 01772-9102
Received 13 July 1999/Accepted 24 September 1999
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ABSTRACT |
All members of the Herpesviridae family contain
sequences for a highly conserved glycoprotein B (gB) gene. We
investigated the phylogenetic relationships of gB sequences from eight
independent rhadinovirus isolates obtained from three species: rhesus
(Macaca mulatta), cynomologus (Macaca
fasicularis), and pig-tailed (Macaca nemestrina)
macaques. Samples were derived from monkeys housed at four separate
facilities. Analysis of these eight independent gB sequences revealed
five regions of heterogeneity within the 823- to 829-amino-acid
polypeptides: residues 1 to 65, 120 to 185, 255 to 300, 352 to 393, and
412 to 457. The remaining regions of gB were highly conserved among the
different macaque isolates. Overall divergence among these gene
sequences ranged from 0.1 to 7.2% at the amino acid level.
Phylogenetic trees constructed with our macaque rhadinovirus gB
sequences and those derived from additional subfamilies or genera
(alpha, beta, gamma-1, and gamma-2) revealed that the macaque gB
sequences branched with other gamma-2 herpesvirus gB sequences and that
within the gamma-2 genera, the macaque gB sequences clustered as a
distinct branch. The eight macaque rhadinovirus gB sequences were all
approximately equidistant from Kaposi sarcoma-associated herpesvirus
(KSHV) gB sequences and had a shorter evolutionary distance to KSHV gB
sequences than to any other herpesvirus, including the gamma-2
herpesvirus saimiri (HVS) of New World squirrel monkeys. The macaque gB
sequences did not cluster according to the facility of origin, but did
cluster according to the species of origin, displaying less
intraspecies divergence (0.1 to 2.9%) than interspecies divergence
(3.3 to 7.2%). These results demonstrate a close relatedness of
rhadinovirus isolates from different macaque species.
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TEXT |
The gamma-2
(Rhadinovirus) genus of herpesviruses includes
Herpesvirus saimiri (HVS) (1); Human
herpesvirus 8 (HHV8) (6), also known as Kaposi's
sarcoma-associated herpesvirus (KSHV); Murine herpesvirus 68 (MHV68) (27); and Rhesus monkey
rhadinovirus (RRV) (8). These herpesviruses
have been assigned to the Rhadinovirus genus based on
biological properties, similarities of genomic organization, and the
relatedness of herpesvirus core genes (9). Glycoprotein B
(gB) is a core herpesvirus gene that is present in all known
herpesviruses (9, 23). The relatedness of gB sequences has
been used to determine phylogenetic relationships among members of
different herpesvirus subfamilies and between members of the same
herpesvirus subfamily (3, 10, 15, 24).
We have determined gB sequences from eight rhadinovirus isolates
obtained from three macaque species housed in four independent primate
centers and compared these sequences with those of previously determined herpesvirus gB sequences. In this report, we describe the phylogenetic relationships of macaque rhadinovirus isolates to each
other and to other members of the herpesvirus family.
Amplification and determination of gB sequences.
The macaques
from which rhadinovirus isolates were obtained for this study were
housed at four different primate research centers. Mm26-95
(8), Mm309-95, Mf27-97, Mf472-97, and Mf23-97 were from the
New England Regional Primate Research Center (NERPRC); Mm17577
(24) and Mn19545 were from the Oregon Regional Primate Research Center (ORPRC); Mn98126 was from the University of
Washington Regional Primate Research Center (WRPRC); and Mm492-98 was
from the Caribbean Primate Research Center (CPRC) (Table
1). The rhadinovirus isolate and gB
sequences from Mm17577 were obtained and published previously by others
(24), and those from Mm26-95 were previously published by
our laboratory (8). In order to grow macaque
rhadinovirus isolates for this study, peripheral blood mononuclear
cells from monkeys were cocultivated with rhesus fibroblast cells
as previously described (8). gB sequences from three RRV
isolates (RRV26-95, RRV492-98, and RRV309-95), two cynomologus
monkey rhadinovirus (CRV) isolates (CRV27-97 and CRV23-97), and
two pig-tailed monkey rhadinovirus (PMRV) isolates (PMRV98126
and PMRV19545) were successfully amplified directly from supernatants
of infected cells in culture. Cellular DNA from CRV472-97 cocultures
was isolated using a QIAMP Blood Kit (Qiagen, Valencia, Calif.)
following the manufacturer's protocol; this DNA served as a template
for the amplification of CRV472-97 gB sequences.
In order to amplify macaque rhadinovirus gB sequences, PCR
primers were designed within open reading frame 7 (ORF7) and ORF9
(DNA pol) which contain sequences flanking the gB gene. Previously
determined ORF7 and ORF9 sequences from KSHV (
23) and
RRV26-95
(
8) were aligned, and primers were made
corresponding to highly
conserved regions of KSHV and RRV26-95.
However, these sequences
were not absolutely conserved, and thus nine
PCR primers in different
combinations were used to amplify gB sequences
from all three
macaque species (Tables
2 and
3).
Specific primers and PCR conditions
for each macaque isolate are
presented in Tables
2 and
3. Nested
PCR was necessary for the
amplification of gB sequences from one
PMRV isolate, PMRV19545. PCR
mixtures were assembled inside a
PCR workstation in a laboratory that
was not otherwise utilized
for molecular biology or cell culture
experiments. PCR of uninfected
rhesus fibroblast cells did not produce
gB-specific fragments,
and nucleotide sequences obtained from
individual samples were
unique. Thus, our gB data from infected
macaques did not result
from contamination. For PCR, a 100-µl
reaction volume was used
in a 0.5-ml thin-walled PCR tube (Perkin-Elmer
Cetus, Norwalk,
Conn.), which included 2 U of rTth DNA polymerase XL
(Perkin-Elmer
Cetus), 20 mM deoxynucleoside triphosphates (dNTP), 0.1 µM each
primer, and 5 µl of culture supernatant or 1 µg of
cellular DNA.
PCR mixtures were preheated for 1 min at 80°C in a
heat block
before 1 mM Mg(OAC)
2, was added. The sample was
then inserted
into an Omnigene PCR cycler (Hybaid, Franklin, Mass.)
that was
preheated to 80°C, and PCR was performed. The data in this
report
are representative of two independent PCRs. Amplified gB gene
sequences were independently digested with two restriction enzymes
with
4-base recognition sites,
AluI and
RsaI (New
England Biolabs,
Beverly, Mass.), and the resulting fragments were
cloned into
a pUC18
SmaI/BAP kit (Amersham Pharmacia,
Chicago, Ill.). The
sequence of this library of random fragments was
determined using
universal M13 forward and reverse primers with
BigDye Terminator
Cycle Sequencing Ready Reaction kits (Perkin-Elmer
Cetus) and
an ABI377 DNA Sequencer (Perkin-Elmer Cetus). Sequences from
AluI
and
RsaI fragments produced contiguous
overlapping fragments of
gB sequence (contigs). gB sequence not
obtained from the
AluI
and
RsaI fragments was
determined with specific sequencing primers
that annealed near the ends
of individual contigs. In this manner,
full-length gB sequences were
obtained for five of the isolates
described in this report. For two
isolates, RRV492-98 and PMRV98126,
gB sequences were determined
directly from the PCR product, using
only the specific sequencing
primers that were designed to determine
the intervening sequences
between contigs as described above.
Using these techniques, gB
sequences of each macaque rhadinovirus
isolate were obtained for both
strands, representing two to eight
determinations per base from a
minimum of two independent PCRs.
The macaque gB sequences were edited
with Sequencer, version 3.0,
software (Gene Codes Corporation, Ann
Arbor, Mich.), and edited
gB sequences were translated to protein
sequences using MacVector,
version 5.01, software (Oxford Molecular
Group, Campbell, Calif.).
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TABLE 3.
Primers, annealing temperatures, PCR template, and
methods of sequence determination for the gB of each macaque
rhadinovirus isolatea
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Alignment of gB sequences.
An alignment of gB amino acid
sequences from macaque rhadinoviruses, including those previously
documented for RRV26-95 (8), and RRV17577 (24),
KSHV (23), and partial sequences from retroperitoneal fibromatosis tissues from Macaca mulatta, and Macaca
nemestrina (RFHVMm and RFHVMn, respectively) (3), was
constructed with ClustalW multiple alignment software which was
manually adjusted (EMBL, Heidelberg, Germany) (Fig.
1). Amino
acid sequence analysis revealed that 10 cysteine residues were
conserved at equivalent positions among the nine macaque isolates (Fig.
1). These cysteines are conserved among several gB sequences of the
documented alpha, beta, and gamma herpesviruses, including KSHV
(13, 16). Furthermore, 14 potential N-linked glycosylation
sites (N-X-S or N-X-T) were conserved among all macaque rhadinovirus
isolates presented in this study. Twelve of the 14 potential N-linked
glycosylation sites were also conserved in the KSHV gB sequence.
The KSHV gB sequence contained two additional potential N-linked
glycosylation sites that were not present in the macaque rhadinovirus
gB sequences, and these two sites were in very close proximity to each
other at residues 409 and 420 (residue numbering based on the alignment in Fig. 1). Our analysis also revealed that the full-length macaque gB
sequences contained regions of conserved sequence blocks interspersed with five regions of variability: amino acids 1 to 65, 120 to 185, 255 to 300, 352 to 393, and 412 to 457 (Fig. 1). Although amino acids 1 to
65 were variable between macaque species, this region was well
conserved within a single species. In fact, among the four RRV
isolates, residues 1 to 65 of gB were completely conserved (Fig. 1).
Conversely, these 65 amino acids were highly divergent when individual
rhadinovirus isolates from different species were compared with each
other or with KSHV (Fig. 1). Nineteen amino acid differences have been
previously described between the gB sequences of RRV26-95 and
RRV17577 between residues 279 and 551, while the remaining amino
acids were identical between the two isolates (24). Of these
19 differences, 16 were located between residues 354 and 457, which
include two of the gB variable regions (residues 352 to 393 and 412 to
457 [Fig. 1]). Our analysis revealed that RRV17577 and RRV309-95 have
identical amino acid sequences between residues 279 and 551, whereas,
RRV26-95 and RRV492-98 differ by only one amino acid in this region and
are thus divergent from RRV17577 and RRV309-95 sequences (Fig. 1). Despite the observed heterogeneity, five potential N-linked
glycosylation sites and four cysteine residues are conserved within
this region among these RRV isolates.
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FIG. 1.
Alignment of gB amino acid sequences. An alignment was
constructed with the full-length gB amino acid sequences from nine
macaque rhadinovirus isolates, including RRV (Macaca
mulatta), CRV (Macaca fasicularis), and PMRV
(Macaca nemestrina); one KSHV isolate (accession no.
AAC57085); and two partial sequences from retroperitoneal fibromatosis
tissues from Macaca mulatta (RFHMm, accession no. AAC72187)
and Macaca nemestrina (RFHMn, accession no. AAC72188).
RRV26-95 and RRV17577 gB sequences were obtained from GenBank
(accession no. AAC58686 and AAD21335, respectively). ClustalW software
was used to determine alignments of the gB sequences. The gB sequences
were compared to the RRV26-95 sequence (8) (shown on the top
line). Deletion polymorphisms between sequences are indicated by dashes
( ). Conserved cysteine residues and conserved potential N-linked
glycosylation sites (N-X-S or N-X-T) are highlighted in black. The five
variable regions (residues 1 to 65, 120 to 185, 255 to 300, 352 to 393, and 412 to 457) are highlighted in gray.
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We have included the partial gB sequences from the previously sequenced
RFHVMm and RFHVMn in the gB amino acid alignment (Fig.
1) (
3,
21). The 106-amino-acid fragment of documented RFHV
gB sequences
corresponds to residues 114 to 219 in the numbering
of our alignments
in Fig.
1. We determined that 13 of the 106
amino acids of RFHV gB
sequence which are identical to KSHV sequences
are divergent in macaque
rhadinovirus sequences (Fig.
1). Seven
of the 106 amino acids are
unique to the two RFHV gB sequences,
and 5 residues are unique to one
of the RFHV gB sequences (Fig.
1). The remaining amino acids are
identical to the macaque rhadinovirus
gB sequences (Fig.
1). There are
15 amino acid differences between
KSHV and RFHVMm, 8 differences
between KSHV and RFHVMn, and 20
to 22 differences between KSHV and the
nine macaque isolates in
our analysis (Table
4). Despite the observed heterogeneity,
one
conserved cysteine and one potential N-linked glycosylation site
are maintained in all of the macaque rhadinovirus, KSHV, and RFHV
gB
sequences (Fig.
1).
Amino acid divergence between gB sequences.
Degrees of amino
acid divergence between herpesvirus gB sequences were calculated by
using Gap analysis software (Genetics Computer Group [GCG], version
9.1; Madison, Wis.). Default gap penalties and gap extension parameters
were used to determine sequence relatedness. Although there are five
areas of heterogeneity, the overall divergence between the macaque
rhadinovirus gB sequences ranged from only 0.1 to 7.2% at the amino
acid level (Table 5). The 0.1 to 7.2%
amino acid divergence corresponds to 0.1 to 11% divergence at the
nucleotide level. The degree of synonymous changes (i.e., changes that
do not change an amino acid) is high between different macaque
rhadinovirus gB sequences. Approximately 74% of the nucleotide
substitutions between RRV26-95 and PMRV19545 are synonymous. However,
in the defined variable regions, only 25% of the nucleotide
substitutions were synonymous. Thus, the patterns of sequence variation
suggest pressure to conserve amino acids in the conserved regions and
selective advantage for amino acid changes in the variable regions. The
levels of divergence between the CRV isolates were the smallest among
the three macaque species (0.1 to 0.2%), corresponding to one to three
amino acid differences among the three CRV isolates in this study
(Table 5). Although the gB sequences of the three CRV isolates were very closely related at the amino acid level, six nucleotide
differences were observed in the CRV472-97 versus CRV23-97 comparison
and in the CRV23-97 versus CRV27-97 comparison. Our analysis also revealed that the RRV gB sequences displayed the most intraspecies diversity. Within the four RRV gB sequences presented here, amino acid
divergence ranged between 0.4 and 2.9% (Table 5). gB sequences from
all macaque rhadinovirus isolates were approximately equidistant to
KSHV, ranging from 25.3 to 27.4% in amino acid divergence (Table 5).
Phylogenetic analysis.
A phylogenetic tree was built with
previously determined gB amino acid sequences from KSHV
(23), RRV26-95 (8), and RRV17577 (24),
along with sequences from the two additional RRV isolates, three CRV
isolates, and two PMRV isolates by using PAUP* software (26). These data were manually adjusted, and a
neighbor-joining tree was constructed with KSHV serving as the outgroup
(Fig. 2). Parsimony and nucleotide
sequence analyses produced trees with identical
topologies (not shown). There is strong support (bootstrap values of
98% and higher) for the branches separating the three species of
macaque rhadinovirus gB sequences in this analysis (Fig. 2). Within the
RRV grouping, RRV26-95 clustered with RRV492-98 and RRV309-95 clustered
with RRV17577. RRV26-95 and RRV309-95 originated at the NERPRC, whereas
RRV492-98 and RRV17577 originated at the CPRC and WRPRC, respectively.
Thus, gB sequences within the RRV isolates clustered in an
origin-independent manner (Fig. 2).
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FIG. 2.
Phylogenetic analysis of gB genes from nine macaque
rhadinovirus isolates and KSHV. N, NEPRC; C, CPRC; O, ORPRC; W, WRPRC.
ClustalW software was used to align gB amino acid sequences. The
neighbor-joining method was used to generate this phylogeny by using
PAUP* software (26), with KSHV sequences serving as the
outgroup. Bootstrap values from 1,000 replications (repeated three
times) are shown for each branch point.
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To determine the relationships of the macaque rhadinovirus gB sequences
with other members of the herpesvirus family, phylogenetic
analysis was
performed with full-length aligned gB sequences from
representative
members of the alpha, beta, and gamma subfamilies
and the nine macaque
rhadinovirus isolates (Fig.
3). This
analysis
agreed with the known phylogeny of the herpesvirus subfamily
divisions
(
15).
Epstein-Barr virus (EBV),
designated as a gamma-1 (
Lymphocryptovirus)
herpesvirus
grouped within the gamma subfamily, was separate from
the gamma-2
(
Rhadinovirus) subgroup (Fig.
3). In this analysis,
the
macaque rhadinovirus isolates grouped identically to the analysis
displayed in Fig.
2. There is strong support (bootstrap values
of 80%
and higher) for the branches separating the three major
subfamilies of
herpesviruses in this analysis (Fig.
3). The macaque
rhadinovirus gB
sequences had a shorter evolutionary distance
to the KSHV gB sequence
than to any other herpesvirus (Fig.
3).
Parsimony and unweighted pair
group method by arithmetic averaging
analyses were also performed and
produced the same tree topology
(not shown), except that the positions
of HSV and MHV68 were exchanged.
Our data reveal that the macaque
rhadinovirus isolates in this
report are most closely related to KSHV
among all the herpesvirus
isolates for which significant sequence
information has been determined
(Fig.
3).
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FIG. 3.
Phylogenetic analysis of gB gene sequences from macaque
rhadinoviruses and representative alpha, beta, gamma-1, and gamma-2
herpesviruses. The alignment was created by using ClustalW software.
The neighbor-joining method was used to generate this phylogeny by
using PAUP* software (26) with alpha and beta herpesvirus gB
sequences serving as the outgroup. Bootstrap values from 1,000 replications (repeated three times) are shown for each branch point.
Branch lengths are drawn in proportion to distances. Sequences not
determined in this study were acquired from GenBank. Accession numbers
are as follows: KSHV, AAC57085; MHV68, AAB06229; HVS, P24905;
Equine herpesvirus 2, (EHV2); AAC13795; EBV, P02188;
Human simplex virus 1 (HSV1), P10211;
Varicella-zoster virus (VZV), P09257; Human
cytomegalovirus (HCMV), AAA45928; and Human herpesvirus
6 (HHV6), P36319.
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gB sequences have been utilized for estimating phylogenetic
relationships between closely related herpesvirus isolates (
10,
11). Furthermore, gB sequences have proven predictive of the
relatedness of complete herpesvirus genome sequences (
15).
Our
data reveal that macaque rhadinovirus gB sequences are very closely
related (Table
5 and Fig.
2 and
3) and suggest that the overall
structure and sequence of complete rhadinovirus genomes are likely
to
also be very closely related. Our analysis also indicates that
the
original RRV isolate, RRV26-95 (
8), contains gB sequences
very similar to those contained in other macaque rhadinoviruses
and
thus is not unusual in this
respect.
We have also included the 106-amino-acid gB sequence fragments from
RFHVMm and RFHVMn in our analysis (
3). In this region,
there
is less divergence between RFHV isolates and KSHV than between
macaque
rhadinovirus isolates and KSHV (Table
4). Based on previous
analysis of
the RFHVMm, RFHVMn, KSHV, and RRV26-95 partial DNA
pol and gB
sequences, it has been suggested that RFHV and macaque
rhadinoviruses
constitute independent phylogenetic branches and
that RFHV is more
similar to KSHV than are macaque rhadinoviruses
(
3). Our
results extending these comparisons to eight additional
macaque
rhadinovirus isolates are consistent with this interpretation.
However, additional RFHV data will be needed to confirm the
relatedness
of RFHV to macaque rhadinovirus isolates and
KSHV.
While 90% or more of adult macaques are seropositive for RRV
(
8), newborn macaques can be raised free of RRV
(
17). It
has been recently documented that cross-species
infection with
macaque rhadinoviruses does readily occur following
experimental
inoculation (
17). The NERPRC houses monkeys
according to species,
including infants that are housed with their
natural mothers.
The species specificity of gB sequences presented here
is consistent
with other findings suggesting transmission from infected
adults
or juveniles to uninfected juveniles or infants through close
contact (
17). Our data suggest that cross-species infection
in a primate center setting is not common and that macaque rhadinovirus
sequences have evolved with their specific
hosts.
The herpesvirus gB gene is a highly conserved gene that is essential
for infectivity (
5,
7,
12,
18). The data presented
here
reveal that macaque rhadinovirus gB sequences cluster in
a
species-specific manner. Heterogeneity among different macaque
rhadinovirus gB sequences from the three species in this study
is
confined to five distinct regions in the N-terminal half of
the gB
protein (Fig.
1). The first and third of these regions
(amino acids 1 to 65 and 255 to 300, respectively) correspond
to sequences in herpes
simplex virus (HSV) gB that express strain-specific
neutralizing
epitopes (
18). Furthermore, envelope functions
including
fusion, cell-to-cell spread, and syncytium formation
have been mapped
to HSV gB sequences that correspond to the second,
third, fourth, and
fifth regions of heterogeneity (amino acids
120 to 185, 255 to 300, 352 to 393, and 412 to 457) (
18). It
seems likely that these
putative functional domains of macaque
rhadinovirus gB have evolved in
a species-specific manner. Also
contained within the heterogeneous
regions are 8 of the 14 potential
N-linked glycosylation sites that are
conserved among all the
macaque rhadinovirus gB sequences. It has been
previously documented
that gB is a highly immunogenic protein (
4,
14,
22). Selected
N-linked glycosylation sites in a variable
region of simian immunodeficiency
virus (SIV) envelope (gp120 surface
protein) (
20) and of other
viruses (
2,
25) act to
shield the virus from antibody recognition
(
20). It is
possible that some of the potential N-linked sites
contained in
variable regions of macaque rhadinovirus gB sequences
are playing an
analogous role in limiting immune recognition.
It is also likely that,
as seen with SIV (
19), some of these
N-linked sites in gB
contribute to gB structure and
function.
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ACKNOWLEDGMENTS |
We thank Daniel Silva, Dong Ling Xia, and Allan McPhee for
technical assistance and Joanne Newton for manuscript preparation. We
also thank Deborah Glanister and Patrick Delio from the WRPRC, Lisa
Hoeber and Steven Kelly from the ORPRC, and Prabhat Sehgal from the
NERPRC for supplying macaque samples. We thank Jae Jung for comments on
the manuscript.
This study was supported by PHS grants AI38131 and RR00168.
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FOOTNOTES |
*
Corresponding author. Mailing address: New England
Regional Primate Research Center, Harvard Medical School, Department of Microbiology and Molecular Genetics, 1 Pine Hill Dr., Box 9102, Southborough, MA 01772-9102. Phone: (508) 624-8042. Fax: (508) 624-8190. E-mail: loualex{at}world.STD.com.
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Journal of Virology, January 2000, p. 584-590, Vol. 74, No. 1
0022-538X/0/$04.00+0
Copyright © 2000, American Society for Microbiology. All rights reserved.
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