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Sooty Mangabey Monkeys (Cercocebus Atys) (Cross-Neutralization/Serologic Relationship/Acquired Immunodeflciency Syndrome) PATRICIA N

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Sooty Mangabey Monkeys (Cercocebus Atys) (Cross-Neutralization/Serologic Relationship/Acquired Immunodeflciency Syndrome) PATRICIA N Proc. Nati. Acad. Sci. USA Vol. 83, pp. 5286-5290, July 1986 Medical Sciences Isolation of a T-lymphotropic retrovirus from naturally infected sooty mangabey monkeys (Cercocebus atys) (cross-neutralization/serologic relationship/acquired immunodeflciency syndrome) PATRICIA N. FULTZ*t, HAROLD M. MCCLUREt, DANIEL C. ANDERSONt, R. BRENT SWENSON*, RITA ANAND*, AND A. SRINIVASAN* *AIDS Program, Center for Infectious Diseases, Centers for Disease Control, Atlanta, GA 30333; and Divisions of tPathobiology and Immunobiology, and tClinical Medicine, Yerkes Regional Primate Research Center, Emory University, Atlanta, GA 30322 Communicated by Eliot Stellar, March 10, 1986 ABSTRACT Healthy mangabey monkeys in a colony at the ings, a virus resembling both STLV-III and HIV was isolated Yerkes Regional Primate Research Center were found to be from African green monkeys and was designated STLV- infected with a retrovirus related to human immunodeficiency IIIAGM (9). virus (HIV). Virus was isolated from peripheral blood cells of We have isolated a virus related to STLV-Il and HIV from 14 of 15 randomly selected mangabeys. All virus-positive healthy sooty mangabey monkeys (Cercocebus atys) which, animals had antibodies to the mangabey virus at the time of like African green monkeys, are indigenous to central and virus isolation and, in a retrospective study, 82% of mangabey western Africa. Because the mangabey isolate appears to be serum samples obtained in 1981 had antibodies to the virus. similar to the prototype simian virus, STLV-III, and in The newly isolated retrovirus is (Al morphologically identical to accordance with proposed nomenclature (21), we will refer to HIV by electron microscopy; (ii) serologically related to the the mangabey isolate as SIV/SMM (simian immunodeficien- human virus by enzyme immunoassay, immunoblotting exper- cy virus/sooty mangabey monkey). iments, radioimmunoprecipitation, and neutralization; and (Mi) cytopathic for human OKT41 cells. The mangabey virus MATERIALS AND METHODS also shares these properties with the simian T-lymphotropic virus type m (STLV-III) recently isolated from diseased Animals. The Yerkes Regional Primate Research Center macaques and from healthy African green monkeys (STLV- maintains a colony of approximately 88 colony-born or MAGM). However, the mangabey virus, like STLV-IIAGM, wild-caught mangabey monkeys that are used primarily for differs from both HIV and STLV-HI in that it apparently does reproductive and behavioral studies. Mangabeys also are not cause clinical immunodeflciency or disease following nat- used for experimental leprosy infection because of their ural infection of the host from which it was isolated. Compar- unique susceptibility to Mycobacterium leprae (10, 11). The ison of the virus-host interactions of these isolates may be 15 animals used in this study were selected at random from valuable in defining determinants of pathogenicity for among mangabey monkeys that are housed together in an cytopathic retroviruses. indoor/outdoor facility. The mangabeys selected from the colony were between 4 and 22 years old, and all were Acquired immunodeficiency syndrome (AIDS) is caused by colony-born except for nos. 2 and 8 (see Table 1). Blood was a retrovirus, human T-lymphotropic virus type III/ collected to obtain peripheral blood mononuclear cells lymphadenopathy-associated virus/AIDS-associated retro- (PBMC) and serum. None of the animals was neutropenic or virus (HTLV-III/LAV/ARV) or human immunodeficiency lymphopenic, and all were clinically normal at the time of virus (HIV), (1-4), that replicates in and is cytopathic for blood collection. helper T lymphocytes (OKT4' cells) (5). Recently, a related Virus Strains. LAV was the gift of L. Montagnier, J. C. virus was isolated by Daniel et al. (6) from rhesus macaques Chermann, and F. Barre-Sinoussi, and ARV-2 was obtained (Macaca mulatta) that had either immunodeficiency disease from Jay Levy. or a transmissible lymphoma. The simian isolate, termed Isolation of Virus. Virus was isolated from PBMC of simian T-lymphotropic virus type III (STLV-III), has many mangabeys by coculturing PBMC with phytohemagglutinin of the characteristics of human HIV. These common char- P-stimulated adult human leukocytes (PHA-AWBC). Cell- include a for cells with con- free supernatants from cocultures were monitored for Mg2"- acteristics (i) tropism OKT4' dependent reverse transcriptase activity as described previ- comitant cytopathology, (il) a virion morphology typical of ously (4). Culture supernatants with positive reverse retroviruses but unusual in nucleoid morphology, (iii) a transcriptase were tested for their ability to transfer infec- Mg2"-dependent reverse transcriptase enzyme, and (iv) a tivity to fresh PHA-AWBC or to established cell lines; some distinct virion protein profile. Also, serologic cross-reactivity of the initial cocultures were tested by electron microscopy was demonstrated (7, 8) when it was shown that antiserum for the presence of virus. specific for either HIV or STLV-III precipitated proteins of Cellular Tropism. The cellular tropism of SIV/SMM was the other. determined in two ways. First, PHA-AWBC were infected Although STLV-III was isolated from an Asian primate with an isolate of SIV/SMM and, periodically, the number of species, antibodies to STLV-III have also been found in serum samples obtained from a species ofmonkey commonly Abbreviations: HIV, human immunodeficiency virus; SIV, simian found in Africa. Serum samples from 42% of wild-caught immunodeficiency virus; HTLV-III, human T-lymphotropic virus African green monkeys (Cercopithecus aethiops) had anti- type III; LAV, lymphadenopathy-associated virus; ARV, AIDS- bodies to STLV-III proteins (8). Subsequent to these find- associated retrovirus; STLV-III, simian T-lymphotropic virus type III; SMM, sooty mangabey monkey; AGM, African green monkey; PBMC, peripheral blood mononuclear cells; PHA-AWBC, The publication costs of this article were defrayed in part by page charge phytohemagglutinin-stimulated adult human white blood cells; IFA, payment. This article must therefore be hereby marked "advertisement" indirect immunofluorescence assay; EIA, enzyme immunoassay; in accordance with 18 U.S.C. §1734 solely to indicate this fact. RIP, radioimmunoprecipitation. 5286 Downloaded by guest on September 25, 2021 Medical Sciences: FtIltz et al. Proc. Natl. Acad. Sci. USA 83 (1986) 5287 T-helper (T4) and T-cytotoxic/suppressor cells (T8) in the B. Culture supernatants were monitored for extracellular infected culture and in an uninfected control culture were reverse transcriptase activity on days 6, 9, 12, and 16. determined by indirect immunofluorescence assay (IFA) Neutralizing antibody activity was considered to be present if using a T-helper/suppressor ratio test kit (Becton Dickin- there was at least 80%o inhibition of reverse transcriptase son). At least 500 cells were counted for each determination. activity compared to reverse transcriptase activity in control Reverse transcriptase activity in both cultures was also cultures. assayed and, in the infected culture, peaked at >106 cpm per Nucleic Acid Hybridization. Concentrated virus, prepared reaction, while that in the control culture never exceeded from SIV/SMM-infected cell culture supernatants, was 1400 cpm. Second, the ability of isolates of SIV/SMM to lysed, spotted onto nitrocellulose filters, and hybridized to replicate in established cell lines of different lineages was genomic (-9-kilobase) HIV (clone Zr6; A.S., R.A., P. tested. Approximately 10- cpm of SIV/SMM reverse trans- Luciw, unpublished work) as described (14). High molecular criptase activity was used to infect 107 cells. Culture super- weight DNA was isolated from SIV/SMM-infected cells and natants were monitored for reverse transcriptase activity. digested with several restriction enzymes before it was used The cell line HT was provided by R. C. Gallo (National with the Zr6 cDNA clone of HIV in Southern hybridization Institutes ofHealth); HUT78 and 6D5, a subclone of1HUT78, assays (15). by J. Getchell (Centers for Disease Control); and K562, by S. McDougal (Centers for Disease Control). RESULTS Serologic Assays. Mangabey serum samples were tested at a 1:50 dilution by enzyme immunoassay (EIA) using Abbott Incidence of Disease in the Mangabey Colony. Since the Laboratories HTLV-III EIA kit, at a 1:100 dilution by mangabey colony was established at the Yerkes Primate immunoblot using H9/HTLV-III antigen, and at a 1:20 Center, there has been no apparent difference in the inci- dilution for SIV/SMM-specific antibodies by indirect IFA dence of disease in this species when compared with the using acetone-fixed, virus-infected PHA-AWBC. The second incidence of disease in other species of monkeys at the antibody was a fluorescein-labeled goat anti-monkey IgG Yerkes field station. During the past 16 years, 55% (42 (Cooper Biomedical, Malvern, PA). Metabolic labeling, animals) of the deaths in the mangabey colony resulted from immunoprecipitation, NaDodSO4/polyacrylamide gel elec- spontaneous disease problems in animals older than 1 month. trophoresis, and fluorography have been described (12). Neoplastic diseases were not found in any of these animals, Briefly, virus-infected cells were labeled with [35S]methio- and lymphadenopathy of one or more lymph node groups was nine and [35S]cysteine (200 ACi/ml; 1 Ci = 37 GBq) for 1 hr seen in only six animals. Thus, it appears that SIV/SMM and then lysed. Viral proteins were immunoprecipitated with infection
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