1 Laboratory for Clinical and Epidemiological Virology, Rega Institute for Medical Research, Katholieke Universiteit Leuven, Minderbroedersstraat 10, B-3000 Leuven, Belgium
2 Unité d'Epidémiologie des Virus Oncogènes, Département EEMI, Institut Pasteur, Paris, France
Correspondence
Sonia Van Dooren
Sonia.VanDooren{at}uz.kuleuven.ac.be
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ABSTRACT |
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The GenBank/EMBL/DDBJ accession numbers for the M. arctoides MarB43 complete genome and the env and LTR sequences determined in this work are AY590142, AY141153AY141155 and AY141171AY141174, respectively.
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MAIN TEXT |
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Overall, PTLV-1 phylogeny is peculiar in that it suggests an Asian origin for PTLV-1 when phylogenetic trees are rooted with strains of other PTLV types. This observation questions the generally accepted hypothesis that the ancestor of all PTLVs originated in Africa (Salemi et al., 1999), based on the common occurrence of all different PTLV types on the African continent. Taken together, these facts create doubts about the possible origin of PTLV and the dissemination of PTLV-1 to Asia and Africa.
Full-genome sequencing and analysis of one of the most divergent STLV-1 strains of Asian origin would allow us to unravel a piece of this Asian PTLV-1 dissemination. Mahieux et al. (1997b) demonstrated that six Macaca arctoides of southeast Asian origin housed at the Strasbourg Primatology Center showed a peculiar Western blot profile with an HTLV-2-like reactivity. Sequencing of part of the tax (406 bp) region and part of the env (306 bp) region of one M. arctoides strain, Marc1, showed that this strain was the most divergent among Asian STLV-1 strains. In the present study, we sequenced the STLV-1 gp21 env and long terminal repeat (LTR) regions from four other M. arctoides strains, identified by Mahieux et al. (1997b)
[MAC912, MAC757, MAC897 and MAC11 (LTR region only)] according to the methodology described previously (Mahieux et al., 1997a
). The STLV-1 full-genome sequence was obtained from (sufficiently available) original lymphocyte DNA of M. arctoides animal B43 (MarB43), as a virus-producing cell line could not be established for Marc1. The primers and PCR conditions for amplification are available at http://www.kuleuven.be/rega/cev/TableMarB43sequencingproject.pdf. The full genome of STLV MarB43 was obtained as shown in the sequencing project represented schematically in Fig. 1
(a), after agarose-gel purification of the PCR products with a QIAquick gel extraction kit (Qiagen) and direct sequencing of both strands using the BigDye Terminator technology on an ABI 310 Genetic Analyser (Applied Biosystems). The different sequenced fragments were analysed with Sequencing Analysis software (Applied Biosystems) and assembled by using the software package Geneworks 2.5.1 (Oxford Molecular Systems). The GenBank accession number of the MarB43 complete genome is AY590142, and those of the M. arctoides env and LTR sequences are AY141153AY141155 and AY141171AY141174, respectively.
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The phylogenetic relationship between the MarB43 strain and other PTLV strains was investigated through a concatenated gag-pol-env-tax full-genome analysis (with all available PTLV full-genome sequences), and an LTR and gp21 env analysis (with more known Asian STLV-1 strains of different Macaca host species and a substantial number of STLV-1 and HTLV-1 reference strains of African and Melanesian origin from GenBank). Alignments were made in DAMBE 4.0.75 (Xia & Xie, 2001), guided by their amino acid sequence alignment, and further edited manually in Se-Al (http://evolve.zoo.ox.ac.uk). Neighbour-joining and maximum-likelihood trees were constructed according to methodology described elsewhere (Van Dooren et al., 2004
). The full-genome, LTR and env phylogenetic analyses consistently depicted MarB43 as the most divergent STLV-1 strain, clustering closer to the Asian STLV-1 strains and the Melanesian HTLV-1c strain Mel5 than to the other African or cosmopolitan STLV-1/HTLV-1 strains (env and LTR analyses shown in Fig. 2a and b
, respectively). The positioning of MarB43 within the PTLV-1 clade was analogous to the positioning of STLV-2 with respect to the HTLV-2 strains (Fig. 2a
). The PTLV-1 env and LTR phylogenetic analyses demonstrated clearly that STLV-1 strains in M. arctoides are related closely to each other, but distantly to the STLV-1 strains of other Macaca species. The remaining Asian PTLV-1 strains in the env phylogenetic analysis (Fig. 2a
) clustered according to host species in a ladder-like topology, seemingly reflecting the Macaca migration waves. STLV-1 strains in Macaca mulatta and Macaca fascicularis clustered closer to the root of the PTLV-1 part of the tree. Remarkably, these Macaca species, together with M. arctoides, are all descended from proto-fascicularis macaques, which differentiated approximately 5·5 million years ago from the silenus group (Macaca silenus, Macaca nemestrina and Sulawesi macaques) shortly after their arrival on the Asian continent (Delson, 1980
; Morales & Melnick, 1998
). M. mulatta and M. arctoides emerged 2·5 and 1·6 million years ago, respectively, and remained on the Asian northwest-to-central mainland (Delson, 1980
; Morales & Melnick, 1998
). M. fascicularis has a current habitat closer to and overlapping with that of the silenus macaques. The other STLV-1 strains located further down the Asian part of the PTLV-1 phylogenetic tree were isolated from Macaca tonkeana and M. nemestrina (in the LTR analysis only; Fig. 2b
) of the Indonesian archipelago and in the Japanese Macaca fuscata. The first two Macaca species are descended from the silenus group, which migrated soon after their arrival in Asia across the Sundaland from southern China to what is now known as the Indonesian archipelago (Morales & Melnick, 1998
). The Japanese M. fuscata probably differentiated from eastern rhesus macaques in more recent times (0·5 million years ago) (Delson, 1980
; Morales & Melnick, 1998
). The PTLV-1 topology from root to tip is thus indicative of an Asian host species migration-dependent evolution of the virus, suggestive of virushost co-evolution, known as vicariance (Holmes, 2004
), at least in the Macaca species. However, the observed degree of incongruence between the virus phylogeny and the host phylogeny creates doubts about the possibility of vicariance. The closer relationship of STLV-1 in M. mulatta and M. fascicularis to STLV-1 strains in silenus macaques (M. tonkeana and M. nemestrina) compared with STLV-1 in M. arctoides is in conflict with the host-species tree, where M. mulatta, M. fascicularis and M. arctoides all belong to the proto-fascicularis group.
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The current PTLV env phylogeny data certainly corroborate the enormous diversity of PTLV-1 observed in Asia. The STLV-1 biodiversity found to date within macaques suggests that they could have formed the reservoir species for the founding PTLV-1 in Asia. To unravel PTLV evolution further, in particular in Asia, and its relation to Africa, more PTLV strains from primates in the wild should be identified and analysed genetically, especially from Asia, to encompass a possible bias of an incomplete STLV-1 sampling pattern.
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ACKNOWLEDGEMENTS |
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Received 12 August 2004;
accepted 21 March 2005.
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