Specimens from wild and captive primates were collected and novel members of the genus Lymphocryptovirus (subfamily Gammaherpesvirinae) were searched for utilizing PCR for the DNA polymerase gene. Twenty-one novel viruses were detected. Together with previous findings, more than 50 distinct lymphocryptoviruses (LCVs) are now known, with hosts from six primate families (Hominidae, Hylobatidae, Cercopithecidae, Atelidae, Cebidae and Pitheciidae). Further work extended genomic sequences for 25 LCVs to 3.4–7.4 kbp. Phylogenetic trees were constructed, based on alignments of protein sequences inferred from the LCV genomic data. The LCVs fell into three major clades: Clade A, comprising New World viruses; Clade B, containing both Old World monkey viruses and hominoid viruses including Epstein–Barr virus (EBV); and Clade C, containing other hominoid viruses. By comparison with the primate tree, it was proposed that major elements of the LCV tree represented synchronous evolution with host lineages, with the earliest node in both trees being the separation of Old and New World lines, but that some virus lineages originated by interspecies transfer. From comparisons of branch lengths, it was inferred that evolutionary substitution in Clade B has proceeded more slowly than elsewhere in the LCV tree. It was estimated that in Clade B a subclade containing EBV, a gorilla virus and two chimpanzee viruses derived from an Old World monkey LCV line approximately 12 million years ago, and another subclade containing an orang-utan virus and a gibbon virus derived from a macaque LCV line approximately 1.2 million years ago.
AlbiniS.,
ZimmermannW.,
NeffF.,
EhlersB.,
HäniH.,
LiH.,
HüssyD.,
EngelsM.,
AckermannM.2003; Identification and quantification of ovine gammaherpesvirus 2 DNA in fresh and stored tissues of pigs with symptoms of porcine malignant catarrhal fever. J Clin Microbiol 41:900–904[CrossRef]
Bininda-EmondsO. R. P.,
CardilloM.,
JonesK. E.,
MacPheeR. D. E.,
BeckR. M. D.,
GrenyerR.,
PriceS. A.,
VosR. A.,
GittlemanJ. L.,
PurvisA.2007; The delayed rise of present-day mammals. Nature 446:507–512[CrossRef]
ChmielewiczB.,
GoltzM.,
LahrmannK. H.,
EhlersB.2003; Approaching virus safety in xenotransplantation: a search for unrecognized herpesviruses in pigs. Xenotransplantation 10:349–357[CrossRef]
ChoY.,
RamerJ.,
RivaillerP.,
QuinkC.,
GarberR. L.,
BeierD. R.,
WangF.2001; An Epstein–Barr-related herpesvirus from marmoset lymphomas. Proc Natl Acad Sci U S A 98:1224–1229[CrossRef]
ClearyM. L.,
EpsteinM. A.,
FinertyS.,
DorfmanR. F.,
BornkammG. W.,
KirkwoodJ. K.,
MorganA. J.,
SklarJ.1985; Individual tumors of multifocal EB virus-induced malignant lymphomas in tamarins arise from different B-cell clones. Science 228:722–724[CrossRef]
FelsensteinJ.1993phylip (phylogeny inference package) version 3.6a2. Distributed by the author Department of Genetics, University of Washington; Seattle, USA:
FujimotoK.,
TeratoK.,
MiyamotoJ.,
IshikoH.,
FujisakiM.,
ChoF.,
HonjoS.1990; Establishment of a B-lymphoblastoid cell line infected with Epstein–Barr-related virus from a cynomolgus monkey ( Macaca fascicularis ). J Med Primatol 19:21–30
GernerC. S.,
DolanA.,
McGeochD. J.2004; Phylogenetic relationships in the Lymphocryptovirus genus of the Gammaherpesvirinae. Virus Res 99:187–192[CrossRef]
KatohK.,
MisawaK.,
KumaK.,
MiyataT.2002; mafft: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 30:3059–3066[CrossRef]
LeendertzF. H.,
PauliG.,
EllerbrokH.,
Maetz-RensingK.,
BoardmanW.,
NunnC.,
EllerbrokH.,
JensenS. A.,
JunglenS.,
BoeschC.2006; Pathogens as drivers of population declines: the importance of systematic monitoring in great apes and other threatened mammals. Biol Conserv 131:325–337[CrossRef]
Mätz-RensingK.,
JentschK. D.,
RensingS.,
LangenhuyzenS.,
VerschoorE.,
NiphuisH.,
KaupF. J.2003; Fatal Herpes simplex infection in a group of common marmosets ( Callithrix jacchus ). Vet Pathol 40:405–411[CrossRef]
McGeochD. J.,
DavisonA. J.,
DolanA.,
GathererD.,
Sevilla-ReyesE. E.2008; Molecular evolution of the Herpesvirales . In Origin and Evolution of Viruses , 2nd edn. pp 447–475 Edited by
DomingoE.,
ParrishC. R.,
HollandJ. J.
London: Academic Press;
MeléndezL. V.,
HuntR. D.,
DanielM. D.,
GarcíaF. G.,
FraserC. E.1969; Herpesvirus saimiri. II. Experimentally induced malignant lymphoma in primates. Lab Anim Care 19:378–386
NeubauerR. H.,
RabinH.,
StrandB. C.,
NonoyamaM.,
Nelson-ReesW. A.1979; Establishment of a lymphoblastoid cell line and isolation of an Epstein–Barr-related virus of gorilla origin. J Virol 31:845–848
PrepensS.,
KreuzerK.-A.,
LeendertzF.,
NitscheA.,
EhlersB.2007; Discovery of herpesviruses in multi-infected primates using locked nucleic acids (LNA) and a bigenic PCR approach. Virol J 4:84[CrossRef]
RamerJ. C.,
GarberR. L.,
SteeleK. E.,
BoysonJ. F.,
O'RourkeC.,
ThomsonJ. A.2000; Fatal lymphoproliferative disease associated with a novel gammaherpesvirus in a captive population of common marmosets. Comp Med 50:59–68
RanganS. R.,
MartinL. N.,
BozelkaB. E.,
WangN.,
GormusB. J.1986; Epstein–Barr virus-related herpesvirus from a rhesus monkey ( Macaca mulatta ) with malignant lymphoma. Int J Cancer 38:425–432[CrossRef]
RasheedS.,
RongeyR. W.,
BruszweskiJ.,
Nelson-ReesW. A.,
RabinH.,
NeubauerR. H.,
EsraG.,
GardnerM. B.1977; Establishment of a cell line with associated Epstein–Barr-like virus from a leukemic orangutan. Science 198:407–409[CrossRef]
RivadeneiraE. D.,
FerrariM. G.,
JarrettR. F.,
ArmstrongA. A.,
MarkhamP.,
BirkebakT.,
TakemotoS.,
Johnson-DelaneyC.,
Pecon-SlatteryJ.other authors1999; A novel Epstein–Barr virus-like virus, HVMNE, in a Macaca nemestrina with mycosis fungoides. Blood 94:2090–2101
RivaillerP.,
ChoY. G.,
WangF.2002; Complete genomic sequence of an Epstein–Barr virus-related herpesvirus naturally infecting a new world primate: a defining point in the evolution of oncogenic lymphocryptoviruses. J Virol 76:12055–12068[CrossRef]
VasiljevaV. A.,
MarkarjanD. S.,
LapinB. A.,
YakovlevaL. A.,
IvanovM. T.,
SchekolodkinV. F.,
DzikidzeE. K.1974; Establishment of continuous cell lines from leukocytes culture of a hamadryas baboon with leukosis-reticulosis. Neoplasma 21:537–544