Eastern Chimpanzees, but Not Bonobos, Represent a Simian Immunodeficiency Virus Reservoir

Abstract

Chimpanzees in west central Africa ( Pan troglodytes troglodytes ) are endemically infected with simian immunodeficiency viruses (SIVcpz Ptt ) that have crossed the species barrier to humans and gorillas on at least five occasions, generating pandemic and nonpandemic forms of human immunodeficiency virus type 1 (HIV-1) as well as gorilla SIV (SIVgor). Chimpanzees in east Africa ( Pan troglodytes schweinfurthii ) are also infected with SIVcpz; however, their viruses (SIVcpz Pts ) have never been found in humans. To examine whether this is due to a paucity of natural infections, we used noninvasive methods to screen wild-living eastern chimpanzees in the Democratic Republic of the Congo (DRC), Uganda, and Rwanda. We also screened bonobos ( Pan paniscus ) in the DRC, a species not previously tested for SIV in the wild. Fecal samples ( n = 3,108) were collected at 50 field sites, tested for species and subspecies origin, and screened for SIVcpz antibodies and nucleic acids. Of 2,565 samples from eastern chimpanzees, 323 were antibody positive and 92 contained viral RNA. The antibody-positive samples represented 76 individuals from 19 field sites, all sampled north of the Congo River in an area spanning 250,000 km 2 . In this region, SIVcpz Pts was common and widespread, with seven field sites exhibiting infection rates of 30% or greater. The overall prevalence of SIVcpz Pts infection was 13.4% (95% confidence interval, 10.7% to 16.5%). In contrast, none of the 543 bonobo samples from six sites was antibody positive. All newly identified SIVcpz Pts strains clustered in strict accordance to their subspecies origin; however, they exhibited considerable genetic diversity, especially in protein domains known to be under strong host selection pressure. Thus, the absence of SIVcpz Pts zoonoses cannot be explained by an insufficient primate reservoir. Instead, greater adaptive hurdles may have prevented the successful colonization of humans by P. t. schweinfurthii viruses.

Origin of the HIV-1 group O epidemic in western lowland gorillas

“…1); yet, we identified SIVgor-positive gorillas only at six sites, all located in southern Cameroon. Overall, we found fewer than 2% of western lowland gorillas to be infected with SIVgor, which is much lower than the estimates of SIVcpz infection rates for central (6%) or eastern (13%) chimpanzees (4,6,16). Although it is possible that some fecal samples were too degraded to yield positive results, this possibility alone cannot explain the low SIVgor detection rates in western gorillas or the lack of infection in eastern gorillas.…”

“…Molecular epidemiological studies of SIVcpz have shown that these viruses exhibit phylogeographic clustering, apparently largely due to major rivers and other barriers that limit the migration of wild chimpanzees (4)(5)(6). This clustering has allowed us to pinpoint the probable geographic origins of two of the human virus clades (4).…”

“…We screened western lowland gorillas across a large part of their geographic range in southern Cameroon and Gabon, and also sampled both lowland and mountain subspecies of the eastern gorilla (Gorilla beringei). Although eastern and western gorillas likely diverged before the origin of SIVgor, eastern gorillas may have independently acquired SIV, because they share their habitat with the second chimpanzee subspecies, the eastern chimpanzee (Pan troglodytes schweinfurthii), which is widely and commonly infected with SIVcpz (6). Finally, to gain insight into potential barriers to cross-species transfers, we investigated the role of the host restriction factor apolipoprotein B mRNA editing enzyme, catalytic polypeptide-like 3G (APOBEC3G) in inhibiting apeto-ape, as well as ape-to-human, SIV transmission.…”

“…Of particular interest, chimpanzees (Pan troglodytes) acquired two distinct lineages of SIV from two different monkey species; all known strains of chimpanzee SIV (SIVcpz) are derived from a hybrid formed by recombination between these two viruses (3). The spread of this virus in chimpanzees appears to have occurred comparatively recently, because only two closely related subspecies in Central Africa are infected, whereas two other subspecies are not (4)(5)(6)(7)(8). Subsequently, strains of SIVcpz from one chimpanzee subspecies (Pan troglodytes troglodytes) have been subject to further transmission both to humans, leading to HIV-1, and to western gorillas (Gorilla gorilla), giving rise to gorilla SIV (SIVgor) (4,9).…”

Recapitulating Cross-Species Transmission of Simian Immunodeficiency Virus SIVcpz to Humans by Using Humanized BLT Mice

“…We first tested whether divergent strains of SIVcpz can infect hu-BLT mice. We selected 4 phylogenetically divergent SIVcpz strains to represent the inferred ancestral viruses of pandemic HIV-1 group M (SIVcpzMB897) and nonpandemic HIV-1 group N (SIVcpzEK505) (6,26), as well as SIVcpzMT145 (6) and SIVcpzBF1167 (27), whose viral lineages have not been found in humans (4,8). We included HIV-1 SUMA , a (Table 1), from which each hu-BLT mouse was inoculated intraperitoneally (i.p.)…”