Novel cytomegaloviruses in free-ranging and captive great apes: Phylogenetic evidence for bidirectional horizontal transmission

Research Group Emerging Zoonoses, Robert Koch-Institut, D-13353 Berlin, Germany.
Journal of General Virology (Impact Factor: 3.18). 07/2009; 90(Pt 10):2386-94. DOI: 10.1099/vir.0.011866-0
Source: PubMed


Wild great apes often suffer from diseases of unknown aetiology. This is among the causes of population declines. Because human cytomegalovirus (HCMV) is an important pathogen, especially in immunocompromised individuals, a search for cytomegaloviruses (CMVs) in deceased wild and captive chimpanzees, gorillas and orang-utans was performed. By using a degenerate PCR targeting four conserved genes (UL54-UL57), several distinct, previously unrecognized CMVs were found for each species. Sequences of up to 9 kb were determined for ten novel CMVs, located in the UL54-UL57 block. A phylogenetic tree was inferred for the ten novel CMVs, the previously characterized chimpanzee CMV, HCMV strains and Old World and New World monkey CMVs. The primate CMVs fell into four clades, containing New World monkey, Old World monkey, orang-utan and human CMVs, respectively, plus two clades that each contained both chimpanzee and gorilla isolates (termed CG1 and CG2). The tree loci of the first four clades mirrored those for their respective hosts in the primate tree, suggesting that these CMV lineages arose through cospeciation with host lineages. The CG1 and CG2 loci corresponded to those of the gorilla and chimpanzee hosts, respectively. This was interpreted as indicating that CG1 and CG2 represented CMV lineages that had arisen cospeciationally with the gorilla and chimpanzee lineages, respectively, with subsequent transfer within each clade between the host genera. Divergence dates were estimated and found to be consistent with overall cospeciational development of major primate CMV lineages. However, CMV transmission between chimpanzees and gorillas in both directions has also occurred.

    • "We also note that this region is directly upstream of SLC23A1, a vitamin C transporter and PAIP2, a repressor of polyadenylate-binding protein PABP1. PAIP2 acts as part of innate defense against cytomegalovirus (CMV) (McKinney et al. 2013), which has been detected in wild gorilla populations (Leendertz et al. 2009). Another region identified (at P < 10 À4 ) contains several genes involved in taste reception. "
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    ABSTRACT: While population-level genomic sequence data have been gathered extensively for humans, similar data from our closest living relatives are just beginning to emerge. Examination of genomic variation within great apes offers many opportunities to increase our understanding of the forces that have differentially shaped the evolutionary history of hominid taxa. Here, we expand upon the work of the Great Ape Genome Project by analyzing medium to high coverage whole genome sequences from 14 western lowland gorillas (Gorilla gorilla gorilla), 2 eastern lowland gorillas (Gorilla beringei graueri), and a single Cross River individual (Gorilla gorilla diehli). We infer that the ancestors of western and eastern lowland gorillas diverged from a common ancestor ~261 thousand years ago (kya), and that the ancestors of the Cross River population diverged from the western lowland gorilla lineage ~68 kya. Using a diffusion approximation approach to model the genome-wide site frequency spectrum, we infer a history of western lowland gorillas that includes an ancestral population expansion of ~1.4-fold around ~970 kya and a recent ~5.6-fold contraction in population size ~23 kya. The latter may correspond to a major reduction in African equatorial forests around the Last Glacial Maximum. We also analyze patterns of variation among western lowland gorillas to identify several genomic regions with strong signatures of recent selective sweeps. We find that processes related to taste, pancreatic and saliva secretion, sodium ion transmembrane transport, and cardiac muscle function are overrepresented in genomic regions predicted to have experienced recent positive selection. © The Author(s) 2014. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution.
    No preview · Article · Dec 2014 · Molecular Biology and Evolution
    • "The presence of cross-species transmission and/or recombination between human and ape hepatitis B virus variants [28] and the close genomic similarity of human and ape hepatitis B viruses [29] calls for extensive phylogenetic investigations to understand the diversity, the evolution and the worldwide spread of this virus. Other pathogenic viruses, including adenoviruses [30] (family Adenoviridae), Lymphocryptovirus [31] and cytomegaloviruses [32] (family Herpesviridae), metapneumoviruses [16] [17] [18] (family Paramyxoviridae ), polyomaviruses [33] (family Polyomaviridae) and enteroviruses [34] (family Picornaviridae), are not exclusively human-specific and have also been detected in apes. Moreover, based on phylogenetic analyses, some of these viruses variants found in apes are remarkably closely related to human viruses, indicating the zoonotic potential of primate viruses to spread horizontally into the local human populations [30e34] "
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    ABSTRACT: Because of the close genetic relatedness between apes and humans, apes are susceptible to many human infectious agents and can serve as carriers of these pathogens. Consequently, they present a serious health hazard to humans. Moreover, many emerging infectious diseases originate in wildlife and continue to threaten human populations, especially vector-borne diseases described in great apes, such as malaria and rickettsiosis. These wild primates may be permanent reservoirs and important sources of human pathogens. In this special issue, we report that apes, including chimpanzees (Pan troglodytes), bonobos (Pan paniscus), gorillas (Gorilla gorilla and G. beringei), orangutans (Pongo pygmaeus and P. abelii), gibbons (Hylobates spp., Hoolock spp. and Nomascus spp) and siamangs (Symphalangus symphalangus syndactylus and S. s. continentis), have many bacterial, viral, fungal and parasitic species that are capable of infecting humans. Serious measures should be adopted in tropical forests and sub-tropical areas where habitat overlaps are frequent to survey and prevent infectious diseases from spreading from apes to people.
    No preview · Article · Sep 2014 · Microbial Pathogenesis
    • "There are also anecdotal reports of cross-species (zoonotic) infections of humans with simian or baboon CMVs (Huang et al., 1978; Martin et al., 1994; Michaels et al., 2001), but in two of the three cases the source of infection remained enigmatic. Moreover, phylogenetic analyses suggested interspecies transfer of CMVs between chimpanzees and gorillas (Leendertz et al., 2009; see also Chapter II.22). There is also a report of an experimental infection of laboratory mice (Mus musculus) with a field mouse (Apodemus sylvaticus) isolate (Raynaud and Barreau, 1965). "
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    ABSTRACT: Cytomegaloviruses (CMVs) are highly species specific as they replicate almost exclusively in cells of their natural host species. However, the molecular basis of species specificity remains poorly understood. In cells of a foreign host a post-penetration block to viral gene expression and genome replication appears to restrict viral replication and spread. In some cases, infected cells of a foreign host undergo programmed cell death, indicating that apoptosis acts as a cellular antiviral defence mechanism to prevent viral replication. A few recent studies suggested that mediator and effector molecules of the interferon system and antiviral defences operating at PML nuclear bodies (PML-NBs) might also be involved in restricting the host range of CMVs. Moreover, a recently isolated spontaneous mutant of murine CMV, which is capable of replicating to high titres in human cells, provided a new opportunity to study the mechanisms of CMV host species specificity. In this spontaneously adapted virus, mutations in the region encoding the viral Early1 (E1) proteins were found to be responsible for the extended host range phenotype. Further investigations of the CMV host species specificity should lead to a better understanding of the viral replication machinery, interfering host cell factors, and viral countermeasures.
    No preview · Chapter · Apr 2013
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