Abstract
Since the description of human T-cell leukemia virus type I (HTLV-I) and its simian counterpart, simian T-cell leukemia virus type I (STLV-I), the possible existence of other related simian retroviruses has been raised. Here, we report a new retrovirus, STLV-II, which we have identified in spider monkeys (Ateles fusciceps), a New World primate species. Initially, a recombinant HTLV-II envelope protein (RP-IIB) was used to identify anti-STLV-II antibodies in New World monkeys by Western blot (immunoblot) assays. Subsequently, the virus was characterized by Southern blot hybridization, which showed that STLV-II and HTLV-II have a high degree of nucleotide sequence homology but have different restriction enzyme patterns. Nucleotide sequence analysis of the pX-II region of STLV-II provirus revealed 3% variation with the corresponding region of HTLV-II. Electron micrographic studies revealed HTLV-like, type C retrovirus particles outside the cell membranes of STLV-II-infected cells. This study describes the first link between HTLV-II and a simian reservoir in the New World. Further molecular studies of STLV-II infection in different species of New World monkeys, especially from the wild, may provide valuable information about the origin and intragroup relationships of South American monkeys. Spider monkeys infected with STLV-II may serve as an important animal model for HTLV-II infection in humans.
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- Abbott M. A., Poiesz B. J., Byrne B. C., Kwok S., Sninsky J. J., Ehrlich G. D. Enzymatic gene amplification: qualitative and quantitative methods for detecting proviral DNA amplified in vitro. J Infect Dis. 1988 Dec;158(6):1158–1169. doi: 10.1093/infdis/158.6.1158. [DOI] [PubMed] [Google Scholar]
- Blattner W. A., Kalyanaraman V. S., Robert-Guroff M., Lister T. A., Galton D. A., Sarin P. S., Crawford M. H., Catovsky D., Greaves M., Gallo R. C. The human type-C retrovirus, HTLV, in Blacks from the Caribbean region, and relationship to adult T-cell leukemia/lymphoma. Int J Cancer. 1982 Sep 15;30(3):257–264. doi: 10.1002/ijc.2910300302. [DOI] [PubMed] [Google Scholar]
- Chen I. S., McLaughlin J., Gasson J. C., Clark S. C., Golde D. W. Molecular characterization of genome of a novel human T-cell leukaemia virus. Nature. 1983 Oct 6;305(5934):502–505. doi: 10.1038/305502a0. [DOI] [PubMed] [Google Scholar]
- Chen I. S., McLaughlin J., Golde D. W. Long terminal repeats of human T-cell leukaemia virus II genome determine target cell specificity. Nature. 1984 May 17;309(5965):276–279. doi: 10.1038/309276a0. [DOI] [PubMed] [Google Scholar]
- Chen Y. M., Essex M. Identification of a recombinant HTLV-II envelope protein for serological detection of HTLV-II carriers. AIDS Res Hum Retroviruses. 1991 May;7(5):453–457. doi: 10.1089/aid.1991.7.453. [DOI] [PubMed] [Google Scholar]
- Chen Y. M., Lee T. H., Samuel K. P., Okayama A., Tachibana N., Miyoshi I., Papas T. S., Essex M. Antibody reactivity to different regions of human T-cell leukemia virus type 1 gp61 in infected people. J Virol. 1989 Nov;63(11):4952–4957. doi: 10.1128/jvi.63.11.4952-4957.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chen Y. M., Lee T. H., Wiktor S. Z., Shaw G. M., Murphy E. L., Blattner W. A., Essex M. Type-specific antigens for serological discrimination of HTLV-I and HTLV-II infection. Lancet. 1990 Nov 10;336(8724):1153–1155. doi: 10.1016/0140-6736(90)92769-e. [DOI] [PubMed] [Google Scholar]
- Chen Y. M., Zhang X. Q., Dahl C. E., Samuel K. P., Schooley R. T., Essex M., Papas T. S. Delineation of type-specific regions on the envelope glycoproteins of human T cell leukemia viruses. J Immunol. 1991 Oct 1;147(7):2368–2376. [PubMed] [Google Scholar]
- Clarke J. K., Attridge J. T., Dane D. S., Briggs M. A simian virus of new morphology. J Gen Virol. 1967 Oct;1(4):565–566. doi: 10.1099/0022-1317-1-4-565. [DOI] [PubMed] [Google Scholar]
- Gelmann E. P., Franchini G., Manzari V., Wong-Staal F., Gallo R. C. Molecular cloning of a unique human T-cell leukemia virus (HTLV-IIMo). Proc Natl Acad Sci U S A. 1984 Feb;81(4):993–997. doi: 10.1073/pnas.81.4.993. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gessain A., Barin F., Vernant J. C., Gout O., Maurs L., Calender A., de Thé G. Antibodies to human T-lymphotropic virus type-I in patients with tropical spastic paraparesis. Lancet. 1985 Aug 24;2(8452):407–410. doi: 10.1016/s0140-6736(85)92734-5. [DOI] [PubMed] [Google Scholar]
- Gessain A., Gallo R. C., Franchini G. Low degree of human T-cell leukemia/lymphoma virus type I genetic drift in vivo as a means of monitoring viral transmission and movement of ancient human populations. J Virol. 1992 Apr;66(4):2288–2295. doi: 10.1128/jvi.66.4.2288-2295.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Goubau P., Desmyter J., Ghesquiere J., Kasereka B. HTLV-II among pygmies. Nature. 1992 Sep 17;359(6392):201–201. doi: 10.1038/359201a0. [DOI] [PubMed] [Google Scholar]
- Hall W. W., Takahashi H., Liu C., Kaplan M. H., Scheewind O., Ijichi S., Nagashima K., Gallo R. C. Multiple isolates and characteristics of human T-cell leukemia virus type II. J Virol. 1992 Apr;66(4):2456–2463. doi: 10.1128/jvi.66.4.2456-2463.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hayami M., Ishikawa K., Komuro A., Kawamoto Y., Nozawa K., Yamamoto K., Ishida T., Hinuma Y. ATLV antibody in cynomolgus monkeys in the wild. Lancet. 1983 Sep 10;2(8350):620–620. doi: 10.1016/s0140-6736(83)90698-0. [DOI] [PubMed] [Google Scholar]
- Hinuma Y., Komoda H., Chosa T., Kondo T., Kohakura M., Takenaka T., Kikuchi M., Ichimaru M., Yunoki K., Sato I. Antibodies to adult T-cell leukemia-virus-associated antigen (ATLA) in sera from patients with ATL and controls in Japan: a nation-wide sero-epidemiologic study. Int J Cancer. 1982 Jun 15;29(6):631–635. doi: 10.1002/ijc.2910290606. [DOI] [PubMed] [Google Scholar]
- Hjelle B., Scalf R., Swenson S. High frequency of human T-cell leukemia-lymphoma virus type II infection in New Mexico blood donors: determination by sequence-specific oligonucleotide hybridization. Blood. 1990 Aug 1;76(3):450–454. [PubMed] [Google Scholar]
- Hjelle B., Wilson C., Cyrus S., Bradshaw P., Lo J., Schammel C., Wiltbank T., Alexander S. Human T-cell leukemia virus type II infection frequently goes undetected in contemporary US blood donors. Blood. 1993 Mar 15;81(6):1641–1644. [PubMed] [Google Scholar]
- Homma T., Kanki P. J., King N. W., Jr, Hunt R. D., O'Connell M. J., Letvin N. L., Daniel M. D., Desrosiers R. C., Yang C. S., Essex M. Lymphoma in macaques: association with virus of human T lymphotrophic family. Science. 1984 Aug 17;225(4663):716–718. doi: 10.1126/science.6087453. [DOI] [PubMed] [Google Scholar]
- Hooks J. J., Gibbs C. J., Jr, Chou S., Howk R., Lewis M., Gajdusek D. C. Isolation of a new simian foamy virus from a spider monkey brain culture. Infect Immun. 1973 Nov;8(5):804–813. doi: 10.1128/iai.8.5.804-813.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hunsmann G., Schneider J., Schmitt J., Yamamoto N. Detection of serum antibodies to adult T-cell leukemia virus in non-human primates and in people from Africa. Int J Cancer. 1983 Sep 15;32(3):329–332. doi: 10.1002/ijc.2910320311. [DOI] [PubMed] [Google Scholar]
- Ina Y., Gojobori T. Molecular evolution of human T-cell leukemia virus. J Mol Evol. 1990 Dec;31(6):493–499. doi: 10.1007/BF02102076. [DOI] [PubMed] [Google Scholar]
- Ishida T., Yamamoto K., Kaneko R., Tokita E., Hinuma Y. Seroepidemiological study of antibodies to adult T-cell leukemia virus-associated antigen (ATLA) in free-ranging Japanese monkeys (Macaca fuscata). Microbiol Immunol. 1983;27(3):297–301. doi: 10.1111/j.1348-0421.1983.tb03592.x. [DOI] [PubMed] [Google Scholar]
- Kalyanaraman V. S., Sarngadharan M. G., Robert-Guroff M., Miyoshi I., Golde D., Gallo R. C. A new subtype of human T-cell leukemia virus (HTLV-II) associated with a T-cell variant of hairy cell leukemia. Science. 1982 Nov 5;218(4572):571–573. doi: 10.1126/science.6981847. [DOI] [PubMed] [Google Scholar]
- Lairmore M. D., Jacobson S., Gracia F., De B. K., Castillo L., Larreategui M., Roberts B. D., Levine P. H., Blattner W. A., Kaplan J. E. Isolation of human T-cell lymphotropic virus type 2 from Guaymi Indians in Panama. Proc Natl Acad Sci U S A. 1990 Nov;87(22):8840–8844. doi: 10.1073/pnas.87.22.8840. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lal R. B., Rudolph D. L., Lairmore M. D., Khabbaz R. F., Garfield M., Coligan J. E., Folks T. M. Serologic discrimination of human T cell lymphotropic virus infection by using a synthetic peptide-based enzyme immunoassay. J Infect Dis. 1991 Jan;163(1):41–46. doi: 10.1093/infdis/163.1.41. [DOI] [PubMed] [Google Scholar]
- Lipka J. J., Bui K., Reyes G. R., Moeckli R., Wiktor S. Z., Blattner W. A., Murphy E. L., Shaw G. M., Hanson C. V., Sninsky J. J. Determination of a unique and immunodominant epitope of human T cell lymphotropic virus type I. J Infect Dis. 1990 Aug;162(2):353–357. doi: 10.1093/infdis/162.2.353. [DOI] [PubMed] [Google Scholar]
- Mann D. L., O'Brien S. J., Gilbert D. A., Reid Y., Popovic M., Read-Connole E., Gallo R. C., Gazdar A. F. Origin of the HIV-susceptible human CD4+ cell line H9. AIDS Res Hum Retroviruses. 1989 Jun;5(3):253–255. doi: 10.1089/aid.1989.5.253. [DOI] [PubMed] [Google Scholar]
- Martin R. D. Primate origins: plugging the gaps. Nature. 1993 May 20;363(6426):223–234. doi: 10.1038/363223a0. [DOI] [PubMed] [Google Scholar]
- Merl S., Kloster B., Moore J., Hubbell C., Tomar R., Davey F., Kalinowski D., Planas A., Ehrlich G., Clark D. Efficient transformation of previously activated and dividing T lymphocytes by human T cell leukemia-lymphoma virus. Blood. 1984 Nov;64(5):967–974. [PubMed] [Google Scholar]
- Miyoshi I., Fujishita M., Taguchi H., Matsubayashi K., Miwa N., Tanioka Y. Natural infection in non-human primates with adult T-cell leukemia virus or a closely related agent. Int J Cancer. 1983 Sep 15;32(3):333–336. doi: 10.1002/ijc.2910320312. [DOI] [PubMed] [Google Scholar]
- Miyoshi I., Yoshimoto S., Fujishita M., Taguchi H., Kubonishi I., Niiya K., Minezawa M. Natural adult T-cell leukemia virus infection in Japanese monkeys. Lancet. 1982 Sep 18;2(8299):658–658. doi: 10.1016/s0140-6736(82)92757-x. [DOI] [PubMed] [Google Scholar]
- Osame M., Usuku K., Izumo S., Ijichi N., Amitani H., Igata A., Matsumoto M., Tara M. HTLV-I associated myelopathy, a new clinical entity. Lancet. 1986 May 3;1(8488):1031–1032. doi: 10.1016/s0140-6736(86)91298-5. [DOI] [PubMed] [Google Scholar]
- Poiesz B. J., Ruscetti F. W., Gazdar A. F., Bunn P. A., Minna J. D., Gallo R. C. Detection and isolation of type C retrovirus particles from fresh and cultured lymphocytes of a patient with cutaneous T-cell lymphoma. Proc Natl Acad Sci U S A. 1980 Dec;77(12):7415–7419. doi: 10.1073/pnas.77.12.7415. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Popovic M., Sarngadharan M. G., Read E., Gallo R. C. Detection, isolation, and continuous production of cytopathic retroviruses (HTLV-III) from patients with AIDS and pre-AIDS. Science. 1984 May 4;224(4648):497–500. doi: 10.1126/science.6200935. [DOI] [PubMed] [Google Scholar]
- Reeves W. C., Levine P. H., Cuevas M., Quiroz E., Maloney E., Saxinger W. C. Seroepidemiology of human T cell lymphotropic virus in the Republic of Panama. Am J Trop Med Hyg. 1990 Apr;42(4):374–379. doi: 10.4269/ajtmh.1990.42.374. [DOI] [PubMed] [Google Scholar]
- Rho H. M., Poiesz B., Ruscetti F. W., Gallo R. C. Characterization of the reverse transcriptase from a new retrovirus (HTLV) produced by a human cutaneous T-cell lymphoma cell line. Virology. 1981 Jul 15;112(1):355–360. doi: 10.1016/0042-6822(81)90642-5. [DOI] [PubMed] [Google Scholar]
- Rosenblatt J. D., Gasson J. C., Glaspy J., Bhuta S., Aboud M., Chen I. S., Golde D. W. Relationship between human T cell leukemia virus-II and atypical hairy cell leukemia: a serologic study of hairy cell leukemia patients. Leukemia. 1987 Apr;1(4):397–401. [PubMed] [Google Scholar]
- Rudolph D. L., Keesling S. S., Lerche N., Yee J. A., Lal R. Dominance of HTLV type I-specific antibody responsiveness in Old World monkeys. AIDS Res Hum Retroviruses. 1991 Sep;7(9):721–722. doi: 10.1089/aid.1991.7.721. [DOI] [PubMed] [Google Scholar]
- Saxinger W., Blattner W. A., Levine P. H., Clark J., Biggar R., Hoh M., Moghissi J., Jacobs P., Wilson L., Jacobson R. Human T-cell leukemia virus (HTLV-I) antibodies in Africa. Science. 1984 Sep 28;225(4669):1473–1476. doi: 10.1126/science.6089348. [DOI] [PubMed] [Google Scholar]
- Seiki M., Hattori S., Hirayama Y., Yoshida M. Human adult T-cell leukemia virus: complete nucleotide sequence of the provirus genome integrated in leukemia cell DNA. Proc Natl Acad Sci U S A. 1983 Jun;80(12):3618–3622. doi: 10.1073/pnas.80.12.3618. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Sherman M. P., Saksena N. K., Dube D. K., Yanagihara R., Poiesz B. J. Evolutionary insights on the origin of human T-cell lymphoma/leukemia virus type I (HTLV-I) derived from sequence analysis of a new HTLV-I variant from Papua New Guinea. J Virol. 1992 Apr;66(4):2556–2563. doi: 10.1128/jvi.66.4.2556-2563.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimotohno K., Golde D. W., Miwa M., Sugimura T., Chen I. S. Nucleotide sequence analysis of the long terminal repeat of human T-cell leukemia virus type II. Proc Natl Acad Sci U S A. 1984 Feb;81(4):1079–1083. doi: 10.1073/pnas.81.4.1079. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Shimotohno K., Takahashi Y., Shimizu N., Gojobori T., Golde D. W., Chen I. S., Miwa M., Sugimura T. Complete nucleotide sequence of an infectious clone of human T-cell leukemia virus type II: an open reading frame for the protease gene. Proc Natl Acad Sci U S A. 1985 May;82(10):3101–3105. doi: 10.1073/pnas.82.10.3101. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Smith L. M., Sanders J. Z., Kaiser R. J., Hughes P., Dodd C., Connell C. R., Heiner C., Kent S. B., Hood L. E. Fluorescence detection in automated DNA sequence analysis. Nature. 1986 Jun 12;321(6071):674–679. doi: 10.1038/321674a0. [DOI] [PubMed] [Google Scholar]
- Smith S. D., Shatsky M., Cohen P. S., Warnke R., Link M. P., Glader B. E. Monoclonal antibody and enzymatic profiles of human malignant T-lymphoid cells and derived cell lines. Cancer Res. 1984 Dec;44(12 Pt 1):5657–5660. [PubMed] [Google Scholar]
- Sodroski J., Trus M., Perkins D., Patarca R., Wong-Staal F., Gelmann E., Gallo R., Haseltine W. A. Repetitive structure in the long-terminal-repeat element of a type II human T-cell leukemia virus. Proc Natl Acad Sci U S A. 1984 Aug;81(15):4617–4621. doi: 10.1073/pnas.81.15.4617. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Uchiyama T., Yodoi J., Sagawa K., Takatsuki K., Uchino H. Adult T-cell leukemia: clinical and hematologic features of 16 cases. Blood. 1977 Sep;50(3):481–492. [PubMed] [Google Scholar]
- Wang J. J., Hu C., Lee F., Shaio M. F., Chen L. K. Internalization of CD4 molecules in human T-cells demonstrated by immuno-electron microscopy. Histochemistry. 1992;97(1):51–59. doi: 10.1007/BF00271281. [DOI] [PubMed] [Google Scholar]
- Watanabe T., Seiki M., Hirayama Y., Yoshida M. Human T-cell leukemia virus type I is a member of the African subtype of simian viruses (STLV). Virology. 1986 Jan 30;148(2):385–388. doi: 10.1016/0042-6822(86)90336-3. [DOI] [PubMed] [Google Scholar]
- Watanabe T., Seiki M., Tsujimoto H., Miyoshi I., Hayami M., Yoshida M. Sequence homology of the simian retrovirus genome with human T-cell leukemia virus type I. Virology. 1985 Jul 15;144(1):59–65. doi: 10.1016/0042-6822(85)90304-6. [DOI] [PubMed] [Google Scholar]
- Yoshida M., Miyoshi I., Hinuma Y. Isolation and characterization of retrovirus from cell lines of human adult T-cell leukemia and its implication in the disease. Proc Natl Acad Sci U S A. 1982 Mar;79(6):2031–2035. doi: 10.1073/pnas.79.6.2031. [DOI] [PMC free article] [PubMed] [Google Scholar]





