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. 1995 Dec;69(12):7877–7887. doi: 10.1128/jvi.69.12.7877-7887.1995

Distribution of baboon endogenous virus among species of African monkeys suggests multiple ancient cross-species transmissions in shared habitats.

A C van der Kuyl 1, J T Dekker 1, J Goudsmit 1
PMCID: PMC189732  PMID: 7494300

Abstract

PCR amplification of baboon endogenous virus (BaEV) long terminal repeat, reverse transcriptase gene, and env fragments from 24 different species of African monkeys indicates that BaEV is less widespread than was formerly thought. Instead of being present in every species of African primates, BaEV can be found only in baboons, geladas, and mangabeys (all belonging to the Papionini tribe) and in African green monkey (Cercopithecus aethiops)subspecies. BaEV, which can be activated from baboon and gelada tissues, was most likely introduced in the germ line only recently (less than a few million years ago) and has not been inherited from a common ancestor of all extant African monkeys. Neighbor-joining and maximum-likelihood analyses of the sequences obtained showed that two distinct virus clusters can be distinguished: the first containing baboon, gelada, and African green monkey BaEV sequences and the second consisting of mandrill and mangabey BaEV sequences. This viral evolutionary tree does not follow host phylogeny, indicating the cross-species transmissions and multiple germ line fixations of the virus must have occurred in the past. BaEV sequences are found in monkeys inhabiting savannas (baboons, geladas, and African green monkeys) as well as forests (managabeys and mandrills) and cluster according to the habitats of their hosts, providing evidence for cross-species transmission in shared habitats.

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Selected References

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  1. Benveniste R. E., Lieber M. M., Livingston D. M., Sherr C. J., Todaro G. J., Kalter S. S. Infectious C-type virus isolated from a baboon placenta. Nature. 1974 Mar 1;248(5443):17–20. doi: 10.1038/248017a0. [DOI] [PubMed] [Google Scholar]
  2. Benveniste R. E., Todaro G. J. Evolution of C-type viral genes: inheritance of exogenously acquired viral genes. Nature. 1974 Dec 6;252(5483):456–459. doi: 10.1038/252456a0. [DOI] [PubMed] [Google Scholar]
  3. Benveniste R. E., Todaro G. J. Evolution of primate oncornaviruses: An endogenous virus from langurs (Presbytis spp.) with related virogene sequences in other Old World monkeys. Proc Natl Acad Sci U S A. 1977 Oct;74(10):4557–4561. doi: 10.1073/pnas.74.10.4557. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Benveniste R. E., Todaro G. J. Evolution of type C viral genes: evidence for an Asian origin of man. Nature. 1976 May 13;261(5556):101–108. doi: 10.1038/261101a0. [DOI] [PubMed] [Google Scholar]
  5. Boller K., König H., Sauter M., Mueller-Lantzsch N., Löwer R., Löwer J., Kurth R. Evidence that HERV-K is the endogenous retrovirus sequence that codes for the human teratocarcinoma-derived retrovirus HTDV. Virology. 1993 Sep;196(1):349–353. doi: 10.1006/viro.1993.1487. [DOI] [PubMed] [Google Scholar]
  6. Boom R., Sol C. J., Salimans M. M., Jansen C. L., Wertheim-van Dillen P. M., van der Noordaa J. Rapid and simple method for purification of nucleic acids. J Clin Microbiol. 1990 Mar;28(3):495–503. doi: 10.1128/jcm.28.3.495-503.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Disotell T. R., Honeycutt R. L., Ruvolo M. Mitochondrial DNA phylogeny of the Old-World monkey tribe Papionini. Mol Biol Evol. 1992 Jan;9(1):1–13. doi: 10.1093/oxfordjournals.molbev.a040700. [DOI] [PubMed] [Google Scholar]
  8. Fischinger P. J., Peebles P. T., Nomura S., Haapala D. K. Isolation of RD-114-like oncornavirus from a cat cell line. J Virol. 1973 Jun;11(6):978–985. doi: 10.1128/jvi.11.6.978-985.1973. [DOI] [PMC free article] [PubMed] [Google Scholar]
  9. Frisby D. P., Weiss R. A., Roussel M., Stehelin D. The distribution of endogenous chicken retrovirus sequences in the DNA of galliform birds does not coincide with avian phylogenetic relationships. Cell. 1979 Jul;17(3):623–634. doi: 10.1016/0092-8674(79)90270-8. [DOI] [PubMed] [Google Scholar]
  10. Herchenröder O., Renne R., Loncar D., Cobb E. K., Murthy K. K., Schneider J., Mergia A., Luciw P. A. Isolation, cloning, and sequencing of simian foamy viruses from chimpanzees (SFVcpz): high homology to human foamy virus (HFV). Virology. 1994 Jun;201(2):187–199. doi: 10.1006/viro.1994.1285. [DOI] [PubMed] [Google Scholar]
  11. Higgins D. G., Sharp P. M. CLUSTAL: a package for performing multiple sequence alignment on a microcomputer. Gene. 1988 Dec 15;73(1):237–244. doi: 10.1016/0378-1119(88)90330-7. [DOI] [PubMed] [Google Scholar]
  12. Ikeda H., Sugimura H. Fv-4 resistance gene: a truncated endogenous murine leukemia virus with ecotropic interference properties. J Virol. 1989 Dec;63(12):5405–5412. doi: 10.1128/jvi.63.12.5405-5412.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Inaguma Y., Miyashita N., Moriwaki K., Huai W. C., Jin M. L., He X. Q., Ikeda H. Acquisition of two endogenous ecotropic murine leukemia viruses in distinct Asian wild mouse populations. J Virol. 1991 Apr;65(4):1796–1802. doi: 10.1128/jvi.65.4.1796-1802.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
  14. Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
  15. Koralnik I. J., Boeri E., Saxinger W. C., Monico A. L., Fullen J., Gessain A., Guo H. G., Gallo R. C., Markham P., Kalyanaraman V. Phylogenetic associations of human and simian T-cell leukemia/lymphotropic virus type I strains: evidence for interspecies transmission. J Virol. 1994 Apr;68(4):2693–2707. doi: 10.1128/jvi.68.4.2693-2707.1994. [DOI] [PMC free article] [PubMed] [Google Scholar]
  16. Lavelle G., Foote L., Heberling R. L., Kalter S. S. Expression of baboon endogenous virus in exogenously infected baboon cells. J Virol. 1979 Apr;30(1):390–393. doi: 10.1128/jvi.30.1.390-393.1979. [DOI] [PMC free article] [PubMed] [Google Scholar]
  17. Lock L. F., Keshet E., Gilbert D. J., Jenkins N. A., Copeland N. G. Studies of the mechanism of spontaneous germline ecotropic provirus acquisition in mice. EMBO J. 1988 Dec 20;7(13):4169–4177. doi: 10.1002/j.1460-2075.1988.tb03313.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Rabin H., Benton C. V., Tainsky M. A., Rice N. R., Gilden R. V. Isolation and characterization of an endogenous type C virus of rhesus monkeys. Science. 1979 May 25;204(4395):841–842. doi: 10.1126/science.87013. [DOI] [PubMed] [Google Scholar]
  19. Rowe W. P., Kozak C. A. Germ-line reinsertions of AKR murine leukemia virus genomes in Akv-1 congenic mice. Proc Natl Acad Sci U S A. 1980 Aug;77(8):4871–4874. doi: 10.1073/pnas.77.8.4871. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Saitou N., Nei M. The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol. 1987 Jul;4(4):406–425. doi: 10.1093/oxfordjournals.molbev.a040454. [DOI] [PubMed] [Google Scholar]
  21. Saksena N. K., Herve V., Durand J. P., Leguenno B., Diop O. M., Digouette J. P., Mathiot C., Muller M. C., Love J. L., Dube S. Seroepidemiologic, molecular, and phylogenetic analyses of simian T-cell leukemia viruses (STLV-I) from various naturally infected monkey species from central and western Africa. Virology. 1994 Jan;198(1):297–310. doi: 10.1006/viro.1994.1033. [DOI] [PubMed] [Google Scholar]
  22. Sherwin S. A., Todaro G. J. A new endogenous primate type C virus isolated from the Old World monkey Colobus polykomos. Proc Natl Acad Sci U S A. 1979 Oct;76(10):5041–5045. doi: 10.1073/pnas.76.10.5041. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Shih A., Coutavas E. E., Rush M. G. Evolutionary implications of primate endogenous retroviruses. Virology. 1991 Jun;182(2):495–502. doi: 10.1016/0042-6822(91)90590-8. [DOI] [PubMed] [Google Scholar]
  24. Song K. J., Nerurkar V. R., Saitou N., Lazo A., Blakeslee J. R., Miyoshi I., Yanagihara R. Genetic analysis and molecular phylogeny of simian T-cell lymphotropic virus type I: evidence for independent virus evolution in Asia and Africa. Virology. 1994 Feb 15;199(1):56–66. doi: 10.1006/viro.1994.1097. [DOI] [PubMed] [Google Scholar]
  25. Stoye J. P., Coffin J. M. The four classes of endogenous murine leukemia virus: structural relationships and potential for recombination. J Virol. 1987 Sep;61(9):2659–2669. doi: 10.1128/jvi.61.9.2659-2669.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Todaro G. J., Benveniste R. E., Sherwin S. A., Sherr C. J. MAC-1, a new genetically transmitted type C virus of primates: "low frequency" activation from stumptail monkey cell cultures. Cell. 1978 Apr;13(4):775–782. doi: 10.1016/0092-8674(78)90227-1. [DOI] [PubMed] [Google Scholar]
  27. Todaro G. J., Sherr C. J., Benveniste R. E. Baboons and their close relatives are unusual among primates in their ability to release nondefective endogenous type C viruses. Virology. 1976 Jul 1;72(1):278–282. doi: 10.1016/0042-6822(76)90331-7. [DOI] [PubMed] [Google Scholar]
  28. York D. F., Vigne R., Verwoerd D. W., Querat G. Nucleotide sequence of the jaagsiekte retrovirus, an exogenous and endogenous type D and B retrovirus of sheep and goats. J Virol. 1992 Aug;66(8):4930–4939. doi: 10.1128/jvi.66.8.4930-4939.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. van der Kuyl A. C., Dekker J. T., Goudsmit J. Full-length proviruses of baboon endogenous virus (BaEV) and dispersed BaEV reverse transcriptase retroelements in the genome of baboon species. J Virol. 1995 Sep;69(9):5917–5924. doi: 10.1128/jvi.69.9.5917-5924.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. van der Kuyl A. C., Kuiken C. L., Dekker J. T., Goudsmit J. Phylogeny of African monkeys based upon mitochondrial 12S rRNA sequences. J Mol Evol. 1995 Feb;40(2):173–180. doi: 10.1007/BF00167111. [DOI] [PubMed] [Google Scholar]

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