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Increased Mortality and AIDS-Like Immunopathology in Wild Chimpanzees Infected with Sivcpz

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Increased Mortality and AIDS-Like Immunopathology in Wild Chimpanzees Infected with Sivcpz Vol 460 | 23 July 2009 | doi:10.1038/nature08200 LETTERS Increased mortality and AIDS-like immunopathology in wild chimpanzees infected with SIVcpz Brandon F. Keele1{, James Holland Jones4, Karen A. Terio5, Jacob D. Estes6, Rebecca S. Rudicell2, Michael L. Wilson7,8, Yingying Li1, Gerald H. Learn1, T. Mark Beasley3, Joann Schumacher-Stankey8, Emily Wroblewski8, Anna Mosser9, Jane Raphael9, Shadrack Kamenya9, Elizabeth V. Lonsdorf10, Dominic A. Travis11, Titus Mlengeya12, Michael J. Kinsel5, James G. Else13, Guido Silvestri14, Jane Goodall15, Paul M. Sharp16, George M. Shaw1, Anne E. Pusey8 & Beatrice H. Hahn1,2 African primates are naturally infected with over 40 different two other chimpanzees inoculated with SIVcpz in captivity6. On the simian immunodeficiency viruses (SIVs), two of which have basis of these data, it has been assumed that SIVcpz resembles other crossed the species barrier and generated human immunodefi- natural SIV infections of sooty mangabeys and African green ciency virus types 1 and 2 (HIV-1 and HIV-2)1,2. Unlike the human monkeys in its non-pathogenic phenotype. However, field and viruses, however, SIVs do not generally cause acquired immuno- molecular studies suggested otherwise7,8. Epidemiological surveys deficiency syndrome (AIDS) in their natural hosts3. Here we show showed that SIVcpz is less prevalent and much less evenly distributed that SIVcpz, the immediate precursor of HIV-1, is pathogenic among wild communities than are SIVs infecting sooty mangabeys in free-ranging chimpanzees. By following 94 members of two and African green monkeys2,7,8. Moreover, SIVcpz was found to be habituated chimpanzee communities in Gombe National Park, one of very few SIVs to have lost a highly conserved Nef function (that Tanzania, for over 9 years, we found a 10- to 16-fold higher age- is, the ability to down-modulate the T-cell receptor from the surface corrected death hazard for SIVcpz-infected (n 5 17) compared to of infected CD41 T cells) that correlates with CD41 T-cell pre- uninfected (n 5 77) chimpanzees. We also found that SIVcpz- servation in naturally infected primates9,10. Finally, evolutionary ana- infected females were less likely to give birth and had a higher lyses revealed that chimpanzees, like humans, acquired SIVcpz infant mortality rate than uninfected females. Immunohisto- relatively more recently by cross-species transmission of SIVs chemistry and in situ hybridization of post-mortem spleen and through infected monkeys on which chimpanzees prey11. lymph node samples from three infected and two uninfected Collectively these data suggested that the natural history of SIVcpz chimpanzees revealed significant CD41 T-cell depletion in all infection differs from that of other primate lentiviruses. To examine infected individuals, with evidence of high viral replication and this, we initiated a prospective study in Gombe National Park, extensive follicular dendritic cell virus trapping in one of them. Tanzania, the only field site where SIVcpz can be studied in wild- One female, who died within 3 years of acquiring SIVcpz, had living, yet habituated, chimpanzee communities2,7. histopathological findings consistent with end-stage AIDS. Gombe National Park is located on the shores of Lake Tanganyika These results indicate that SIVcpz, like HIV-1, is associated with and is home to three chimpanzee communities, termed Kasekela (,65 progressive CD41 T-cell loss, lymphatic tissue destruction and members), Mitumba (,25 members) and Kalande (10–20 members) premature death. These findings challenge the prevailing view that (Supplementary Fig. 1). The Kasekela and Mitumba chimpanzees all natural SIV infections are non-pathogenic and suggest that have been under continuous observation since the 1960s and 1980s, SIVcpz has a substantial negative impact on the health, reproduc- respectively, and their demography, social structure, reproductive tion and lifespan of chimpanzees in the wild. behaviour and individual life histories are well known12,13. The Little is known about the in vivo pathogenicity of SIVcpz because, Kalande chimpanzees are not habituated and thus much less well until recently, it has been impossible to identify and monitor infected studied. Although the three communities have distinct ranges, inter- apes in the wild2. Since the first description of SIVcpz in wild-caught actions between members occur in the form of territorial fights and chimpanzees, only seven naturally infected apes have been studied in the migration of adolescent females who typically leave their natal captivity, five of whom died as infants of unknown causes shortly group before having their first offspring. Owing to extensive habitat after they were placed in sanctuaries2. Only one naturally infected destruction surrounding the park (Supplementary Fig. 1a), the chimpanzee was subjected to virological and immunological ana- Gombe chimpanzees have become isolated from other east African lyses, and in this ape, SIVcpz infection was not associated with ape communities in recent decades. SIVcpz infection has been docu- CD41 T-cell decline, loss of T-cell function, or degenerative changes mented in all three Gombe communities7, but only the Mitumba and in lymph node architecture4–6. Similar findings were also reported for Kasekela chimpanzees have been studied systematically. 1Department of Medicine, 2Department of Microbiology, 3Department of Biostatistics, University of Alabama at Birmingham, Birmingham, Alabama 35294, USA. 4Department of Anthropology, Stanford University, Stanford, California 94305, USA. 5University of Illinois Zoological Pathology Program, Maywood, Illinois 60153, USA. 6The AIDS and Cancer Virus Program, Science Applications International Corporation-Frederick Inc., National Cancer Institute-Frederick, Frederick, Maryland 21702, USA. 7Department of Anthropology, University of Minnesota, Minneapolis, Minnesota 55455, USA. 8Jane Goodall Institute’s Center for Primate Studies, Department of Ecology, Evolution and Behavior, University of Minnesota, St Paul, Minnesota 55108, USA. 9Gombe Stream Research Centre, The Jane Goodall Institute, Kigoma, Tanzania. 10The Lester E. Fisher Center for the Study and Conservation of Apes and 11Department of Conservation and Science, Lincoln Park Zoo, Chicago, Illinois 60614, USA. 12Tanzania National Parks, Arusha, Tanzania. 13Division of Animal Resources, Yerkes National Primate Research Center, Emory University, Atlanta, Georgia 30322, USA. 14Department of Pathology and Laboratory Medicine, University of Pennsylvania School of Medicine, Philadelphia, Pennsylvania 19107, USA. 15The Jane Goodall Institute, Arlington, Virginia 22203, USA. 16Institute of Evolutionary Biology, University of Edinburgh, Edinburgh EH9 3JT, UK. {Present address: The AIDS and Cancer Virus Program, Science Applications International Corporation-Frederick Inc., National Cancer Institute-Frederick, Frederick, Maryland 21702, USA. 515 ©2009 Macmillan Publishers Limited. All rights reserved LETTERS NATURE | Vol 460 | 23 July 2009 SIVcpz testing of Gombe chimpanzees began in 2000 when non- Together, these data suggest that SIVcpz, like HIV-1, is transmitted invasive (faecal- and urine-based) assays for virus-specific antibody by both horizontal and vertical routes. and nucleic acid detection were first developed2,7. Since then, To determine whether SIVcpz infection has an impact on chim- 226 urine and 1,153 faecal samples have been collected from panzee survival, we used discrete event-history methods to model the 100 chimpanzees (median 11 samples per individual; range 1–70), including 69 from Kasekela and 25 from Mitumba (Supplementary a Table 1). Most chimpanzees were sampled at least once every year, ChimpanzeeSex ID Faecal samplesUrine samples Community 200020012002200320042005200620072008 Death and 32 individuals were followed continuously over 7 years. Urine Ch-001 F 23 10 KK 0 0 0 0 0 0 0 0 0 Ch-002 F 12 0 KK 0 0 0 0 0 0 0 0 and faecal samples were examined for SIVcpz antibodies by western Ch-003 M 18 2 KK 0 0 0 0 0 0 0 0 0 Ch-004 M 21 3 KK 0 0 0 0 0 111 blot analysis, and a subset of antibody-positive faecal samples was Ch-005 M 20 3 KK 0 0 0 0 0 0 0 0 Ch-006 M 15 2 KK 1111 1 1 1* 1* DLS 23 Jan 07 tested for viral RNA by reverse transcription polymerase chain re- Ch-007 M 10 4 KK 0 0 0 0 0 0 0 0 7,8 Ch-008 M 5 5 KK 0 0 0 DLS 6 Nov 02 action (RT–PCR) amplification . In addition, all chimpanzees were Ch-009 F 19 13 KK 0 0 0 0 0 0 0 0 Ch-010 M 11 5 KK 0 0 0 0 0 0 0 0 genotyped by amplifying mitochondrial and microsatellite markers Ch-011 F 1511 KK 0 0 0 00 DLS 1 Sep 04 8 Ch-012 F 12 8 KK 0 0 0 0 0 0* 0 0 0 from faecal DNA to verify sample identity . Using these non-invasive Ch-013 M 18 4 KK 0 0 0 0 0 0 0 0 0 Ch-014 M 12 1 KK 0 0* 0 0 0 0 0 approaches, we found 13 Kasekela and 4 Mitumba chimpanzees to be Ch-015 F 17 12 KK 0 0 0 0 0 0 0 0 antibody-positive, 14 of whom also had detectable SIVcpz RNA in Ch-016 M 14 9 KK 0 0 0 00 DOD 24 Aug 04 Ch-017 F 12 3 KK 0 0 0* 0 0 0 0 0 their faeces (Fig. 1). Nine chimpanzees were infected at first analysis, Ch-018 F 10 1 KK 0 0* 0 0 0 0 0 0 Ch-019 F 11 1 KK 0 0 0 0 0 0 0* 0 whereas eight others were identified during the course of the study Ch-020 M 15 3 KK 0 0 0 0 0 0 0 0 0 Ch-021 F11 2 (KL) KK 0 0 0 1 1 1 1 (Fig. 1a). The latter included two infants of SIVcpz-infected mothers Ch-022 F 17 2 (KL) KK 1 1 1 1 1 1 1 Ch-023 M 15 2 KK 0 0 0 0 0 0 0 0 (Ch-062 and Ch-103), as well as six individuals who acquired inci- Ch-024 F 9 10 KK 0000 DOD 3 Oct 05 Ch-025 F 16 11 KK 0 0 0 0 0 0 0 0 0 dent infections after exposure to infected community members Ch-026 F 11 6 KK 0 0 0 0 0 0 0 Ch-027 M 17 5 KK 0 0 0 0 0 0 0 0 0 (Ch-004, Ch-021, Ch-036, Ch-039, Ch-048 and Ch-052).
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