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Genome Announc. 2017 August; 5(33): e00827-17.
Published online 2017 August 17. doi:  10.1128/genomeA.00827-17
PMCID: PMC5604784

Complete Genome Sequence of a Naturally Occurring Simian Foamy Virus Isolate from Rhesus Macaque (SFVmmu_K3T)

ABSTRACT

The full-length genome sequence of a simian foamy virus (SFVmmu_K3T), isolated from a rhesus macaque (Macaca mulatta), was obtained using high-throughput sequencing. SFVmmu_K3T consisted of 12,983 bp and had a genomic organization similar to that of other SFVs, with long terminal repeats (LTRs) and open reading frames for Gag, Pol, Env, Tas, and Bet.

GENOME ANNOUNCEMENT

Simian foamy viruses (SFVs) are highly prevalent in nonhuman primate species (1,4), and human infections can occur due to cross-species transmission (5,14). Although there is no known disease associated with SFV, infectious virus can persist life long due to the stable integration of viral DNA in the host genome (15,18). Therefore, studying the biology and gene regulation of naturally occurring SFVs may provide insight regarding the potential of the virus for cross-species transmission and human infection. Humans have frequent exposure to rhesus macaques in nonhuman primate research centers and in natural habitats in Asia. To date, there is no full-length genome sequence for SFV from rhesus macaques.

SFVmmu_K3T was isolated from a rhesus macaque (Macaca mulatta K3T), which was obtained from a domestic breeding colony in Morgan Island, SC, USA. At the FDA facility, animals were housed singly and maintained in accordance with the Guide for the Care and Use of Laboratory Animals (19) under an approved protocol by the Institute Animal Care and Use Committee. Monkey peripheral blood mononuclear cells (PBMC) were prepared by the Ficoll-Hypaque method (20) and cocultured with Mus dunni cells until extensive cytopathic effect was seen due to viral replication (21). Filtered supernatant containing high reverse transcriptase (RT) activity (passage 3) was collected, and aliquots were stored at −80°C. Ten milliliters of the virus stock was concentrated by ultracentrifugation through a 20% sucrose cushion at 141,000 × g for 2 h. The resuspended pellet was treated with DNase I to reduce host cell DNA, and nucleic acid was prepared using the QIAamp viral RNA minikit (Qiagen, Gaithersburg, MD, USA). High-throughput sequencing was done using the Illumina MiSeq version 3 system in the single-read mode (CD Genomics, Shirley, NY, USA).

Read trimming and assembly were done in our laboratory using the CLC Genomics Workbench software, version 10.0.1 (CLC bio, Denmark). The total number of reads was 1,878,772, and the average read length was 151 bases. The 12,983-bp complete viral genome sequence was obtained by mapping the raw reads (using default parameters) to SFVmcy-1/FV21, a full-length genome from a Taiwanese macaque (Macaca cyclopis), which was used as a reference genome (GenBank accession number X54482). The long terminal repeats (LTRs) were mapped separately to generate the full-length consensus genome sequence of SFVmmu_K3T. Open reading frames were identified (https://www.ncbi.nlm.nih.gov/orffinder/). The genomic structure of SFVmmu_K3T was similar to that of other SFVs encoding Gag, Pol, Env, Tas, and Bet. Nucleotide sequence analysis using NCBI BLASTN indicated 93% to 96% sequence identity with the partial sequences available for SFVs isolated from Asian rhesus macaques in the United States (22) and Bangladesh (23, 24). Additionally, a nucleotide sequence comparison with full-length SFVs of other macaque species indicated 93% identity with a Japanese macaque SFV (SFVmfu_WK1.pJM356 [25], GenBank accession number AB923518), 86% to 87% with Taiwanese macaque SFVs (SFVmcy-1/FV21 [26] and SFVmcy-2/FV34 [27], GenBank accession numbers X54482 and KF026286, respectively), and 85% with a cynomolgus macaque SFV (SFVmfa_Cy5061 [28], accession number LC094267). Biological studies are needed to investigate whether the genomic diversity is associated with differences in viral replication and transmission.

Accession number(s).

The SFVmmu_K3T sequence was deposited in DDBJ/ENA/GenBank under accession number MF280817.

ACKNOWLEDGMENTS

This article reflects the views of the authors and should not be construed to represent FDA’s views and policies. Any mention of product or trade names does not constitute recommendation for use by the U.S. FDA.

We declare no conflicts of financial or personal interest.

Footnotes

Citation Nandakumar S, Bae EH, Khan AS. 2017. Complete genome sequence of a naturally occurring simian foamy virus isolate from rhesus macaque (SFVmmu_K3T). Genome Announc 5:e00827-17. https://doi.org/10.1128/genomeA.00827-17.

REFERENCES

1. Ghersi BM, Jia H, Aiewsakun P, Katzourakis A, Mendoza P, Bausch DG, Kasper MR, Montgomery JM, Switzer WM 2015. Wide distribution and ancient evolutionary history of simian foamy viruses in New World primates. Retrovirology 12:89. doi:.10.1186/s12977-015-0214-0 [PMC free article] [PubMed] [Cross Ref]
2. Katzourakis A, Aiewsakun P, Jia H, Wolfe ND, LeBreton M, Yoder AD, Switzer WM 2014. Discovery of prosimian and afrotherian foamy viruses and potential cross species transmissions amidst stable and ancient mammalian co-evolution. Retrovirology 11:61. doi:.10.1186/1742-4690-11-61 [PMC free article] [PubMed] [Cross Ref]
3. Switzer WM, Salemi M, Shanmugam V, Gao F, Cong ME, Kuiken C, Bhullar V, Beer BE, Vallet D, Gautier-Hion A, Tooze Z, Villinger F, Holmes EC, Heneine W 2005. Ancient co-speciation of simian foamy viruses and primates. Nature 434:376–380. doi:.10.1038/nature03341 [PubMed] [Cross Ref]
4. Reid MJC, Switzer WM, Schillaci MA, Klegarth AR, Campbell E, Ragonnet-Cronin M, Joanisse I, Caminiti K, Lowenberger CA, Galdikas BMF, Hollocher H, Sandstrom PA, Brooks JI 2017. Bayesian inference reveals ancient origin of simian foamy virus in orangutans. Infect Genet Evol 51:54–66. doi:.10.1016/j.meegid.2017.03.003 [PubMed] [Cross Ref]
5. Betsem E, Rua R, Tortevoye P, Froment A, Gessain A 2011. Frequent and recent human acquisition of simian foamy viruses through apes’ bites in central Africa. PLoS Pathog 7:e1002306. doi:.10.1371/journal.ppat.1002306 [PMC free article] [PubMed] [Cross Ref]
6. Switzer WM, Tang S, Ahuka-Mundeke S, Shankar A, Hanson DL, Zheng H, Ayouba A, Wolfe ND, LeBreton M, Djoko CF, Tamoufe U, Esteban A, Heneine W, Peeters M, Wright LL, Muyembe-Tamfum JJ, Wemakoy EO, Mulembakani P, Hoff NA, Rimoin AW 2012. Novel simian foamy virus infections from multiple monkey species in women from the Democratic Republic of Congo. Retrovirology 9:100. doi:.10.1186/1742-4690-9-100 [PMC free article] [PubMed] [Cross Ref]
7. Switzer WM, Tang S, Zheng H, Shankar A, Sprinkle PS, Sullivan V, Granade TC, Heneine W 2016. Dual simian foamy virus/human immunodeficiency virus type 1 infections in persons from Cote d’Ivoire. PLoS One 11:e0157709. doi:.10.1371/journal.pone.0157709 [PMC free article] [PubMed] [Cross Ref]
8. Engel GA, Small CT, Soliven K, Feeroz MM, Wang X, Kamrul Hasan M, Oh G, Rabiul Alam SM, Craig KL, Jackson DL, Matsen FA IV, Linial ML, Jones-Engel L 2013. Zoonotic simian foamy virus in Bangladesh reflects diverse patterns of transmission and co-infection. Emerg Microbes Infect 2:e58. doi:.10.1038/emi.2013.60 [PMC free article] [PubMed] [Cross Ref]
9. Jones-Engel L, May CC, Engel GA, Steinkraus KA, Schillaci MA, Fuentes A, Rompis A, Chalise MK, Aggimarangsee N, Feeroz MM, Grant R, Allan JS, Putra A, Wandia IN, Watanabe R, Kuller L, Thongsawat S, Chaiwarith R, Kyes RC, Linial ML 2008. Diverse contexts of zoonotic transmission of simian foamy viruses in Asia. Emerg Infect Dis 14:1200–1208. doi:.10.3201/eid1408.071430 [PMC free article] [PubMed] [Cross Ref]
10. Schweizer M, Turek R, Hahn H, Schliephake A, Netzer KO, Eder G, Reinhardt M, Rethwilm A, Neumann-Haefelin D 1995. Markers of foamy virus infections in monkeys, apes, and accidentally infected humans: appropriate testing fails to confirm suspected foamy virus prevalence in humans. AIDS Res Hum Retroviruses 11:161–170. doi:.10.1089/aid.1995.11.161 [PubMed] [Cross Ref]
11. Sandstrom PA, Phan KO, Switzer WM, Fredeking T, Chapman L, Heneine W, Folks TM 2000. Simian foamy virus infection among zoo keepers. Lancet 355:551–552. doi:.10.1016/S0140-6736(99)05292-7 [PubMed] [Cross Ref]
12. Khan AS. 2009. Simian foamy virus infection in humans: prevalence and management. Expert Rev Anti Infect Ther 7:569–580. doi:.10.1586/eri.09.39 [PubMed] [Cross Ref]
13. Gessain A, Rua R, Betsem E, Turpin J, Mahieux R 2013. HTLV-3/4 and simian foamy retroviruses in humans: discovery, epidemiology, cross-species transmission and molecular virology. Virology 435:187–199. doi:.10.1016/j.virol.2012.09.035 [PubMed] [Cross Ref]
14. Mouinga-Ondémé A, Kazanji M 2013. Simian foamy virus in non-human primates and cross-species transmission to humans in Gabon: an emerging zoonotic disease in central Africa? Viruses 5:1536–1552. doi:.10.3390/v5061536 [PMC free article] [PubMed] [Cross Ref]
15. Schweizer M, Falcone V, Gänge J, Turek R, Neumann-Haefelin D 1997. Simian foamy virus isolated from an accidentally infected human individual. J Virol 71:4821–4824. [PMC free article] [PubMed]
16. Switzer WM, Bhullar V, Shanmugam V, Cong ME, Parekh B, Lerche NW, Yee JL, Ely JJ, Boneva R, Chapman LE, Folks TM, Heneine W 2004. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. J Virol 78:2780–2789. doi:.10.1128/JVI.78.6.2780-2789.2004 [PMC free article] [PubMed] [Cross Ref]
17. Meiering CD, Linial ML 2001. Historical perspective of foamy virus epidemiology and infection. Clin Microbiol Rev 14:165–176. doi:.10.1128/CMR.14.1.165-176.2001 [PMC free article] [PubMed] [Cross Ref]
18. von Laer D, Neumann-Haefelin D, Heeney JL, Schweizer M 1996. Lymphocytes are the major reservoir for foamy viruses in peripheral blood. Virology 221:240–244. doi:.10.1006/viro.1996.0371 [PubMed] [Cross Ref]
19. National Research Council 2011. Guide for the care and use of laboratory animals. National Academies Press, Washington, DC.
20. Khan AS, Kumar D 2006. Simian foamy virus infection by whole-blood transfer in rhesus macaques: potential for transfusion transmission in humans. Transfusion 46:1352–1359. doi:.10.1111/j.1537-2995.2006.00862.x [PubMed] [Cross Ref]
21. Khan AS, Sears JF, Muller J, Galvin TA, Shahabuddin M 1999. Sensitive assays for isolation and detection of simian foamy retroviruses. J Clin Microbiol 37:2678–2686. [PMC free article] [PubMed]
22. Murray SM, Picker LJ, Axthelm MK, Linial ML 2006. Expanded tissue targets for foamy virus replication with simian immunodeficiency virus-induced immunosuppression. J Virol 80:663–670. doi:.10.1128/JVI.80.2.663-670.2006 [PMC free article] [PubMed] [Cross Ref]
23. Soliven K, Wang X, Small CT, Feeroz MM, Lee EG, Craig KL, Hasan K, Engel GA, Jones-Engel L, Matsen FA, Linial ML 2013. Simian foamy virus infection of rhesus macaques in Bangladesh: relationship of latent proviruses and transcriptionally active viruses. J Virol 87:13628–13639. doi:.10.1128/JVI.01989-13 [PMC free article] [PubMed] [Cross Ref]
24. Feeroz MM, Soliven K, Small CT, Engel GA, Andreina Pacheco M, Yee JL, Wang X, Kamrul Hasan M, Oh G, Levine KL, Rabiul Alam SM, Craig KL, Jackson DL, Lee EG, Barry PA, Lerche NW, Escalante AA, Matsen FA IV, Linial ML, Jones-Engel L 2013. Population dynamics of rhesus macaques and associated foamy virus in Bangladesh. Emerg Microbes Infect 2:e29. doi:.10.1038/emi.2013.23 [PMC free article] [PubMed] [Cross Ref]
25. Yoshikawa R, Nakagawa S, Okamoto M, Miyazawa T 2014. Construction of an infectious clone of simian foamy virus of Japanese macaque (SFVjm) and phylogenetic analyses of SFVjm isolates. Gene 548:149–154. doi:.10.1016/j.gene.2014.07.025 [PubMed] [Cross Ref]
26. Kupiec JJ, Kay A, Hayat M, Ravier R, Périès J, Galibert F 1991. Sequence analysis of the simian foamy virus type 1 genome. Gene 101:185–194. doi:.10.1016/0378-1119(91)90410-D [PubMed] [Cross Ref]
27. Galvin TA, Ahmed IA, Shahabuddin M, Bryan T, Khan AS 2013. Identification of recombination in the envelope gene of simian foamy virus serotype 2 isolated from Macaca cyclopis. J Virol 87:8792–8797. doi:.10.1128/JVI.03555-12 [PMC free article] [PubMed] [Cross Ref]
28. Sakai K, Ami Y, Suzaki Y, Matano T 2016. First complete genome sequence of a simian foamy virus isolate from a cynomolgus macaque. Genome Announc 4(6):e01332-16. doi:.10.1128/genomeA.01332-16 [PMC free article] [PubMed] [Cross Ref]

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