Simian foamy virus infection of rhesus macaques in Bangladesh: Relationship of latent proviruses and transcriptionally active viruses

Journal of Virology

Volumn 87, Issue 24, 2013, Pages 13628-13639

  Soliven, Khanh ^a   Wang, Xiaoxing ^a   Small, Christopher T ^a   Feeroz, Mostafa M ^b   Lee, Eun Gyung ^a   Craig, Karen L ^a   Hasan, Kamrul ^b   Engel, Gregory A ^c   Jones Engel, Lisa ^d   Matsen, Frederick A ^a   Linial, Maxine L ^a  

^a USA   (United States)

^b JAHANGIRNAGAR UNIVERSITY   (Bangladesh)

^c SWEDISH MEDICAL CENTER   (United States)

^d UNIVERSITY OF WASHINGTON   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

APOLIPOPROTEIN B MESSENGER RNA EDITING ENZYME CATALYTIC POLYPEPTIDE 3; HYDROLASE; UNCLASSIFIED DRUG; VIRUS DNA;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BANGLADESH; BIOINFORMATICS; BLOOD CELL; BLOOD SAMPLING; CHEEK MUCOSA; CONTROLLED STUDY; DNA SEQUENCE; GENETIC TRANSCRIPTION; GENETIC VARIABILITY; LATENT VIRUS INFECTION; MOLECULAR PATHOLOGY; MOUTH MUCOSA; NONHUMAN; NUCLEOTIDE SEQUENCE; ORAL BIOPSY; PERIPHERAL BLOOD MONONUCLEAR CELL; PRIORITY JOURNAL; PROVIRUS; RETROVIRUS INFECTION; RHESUS MONKEY; RNA SEQUENCE; SEQUENCE ANALYSIS; SIMIAN FOAMY VIRUS INFECTION; STRAIN DIFFERENCE; STRUCTURAL GENE; TRANSCRIPTIONALLY ACTIVE VIRUS; UNINDEXED SEQUENCE; VIRUS FORMS; VIRUS LOAD; VIRUS MUTATION; VIRUS STRAIN; VIRUS TRANSMISSION;

ANIMALS; BANGLADESH; CHEEK; FEMALE; GENE PRODUCTS, GAG; LEUKOCYTES, MONONUCLEAR; MACACA MULATTA; MALE; PRIMATE DISEASES; PROVIRUSES; RETROVIRIDAE INFECTIONS; RNA, VIRAL; SIMIAN FOAMY VIRUS; TRANSCRIPTION, GENETIC; VIRUS LATENCY; VIRUS REPLICATION;

EID: 84888026694     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01989-13     Document Type: Article

References (43)

1. Yu SF, Sullivan MD, Linial ML. 1999. Evidence that the human foamy virus genome is DNA. J. Virol. 73:1565-1572.
2. Falcone V, Leupold J, Clotten J, Urbanyi E, Herchenröder O, Spatz W, Volk B, Bölm N, Toniolo A, Neumann-Haefelin D, Schweizer M. 1999. Sites of simian foamy virus persistence in naturally infected African green monkeys:latent provirus is ubiquitous, whereas viral replication is restricted to the oral mucosa. Virology 257:7-14.
3. Murray SM, Picker LJ, Axthelm MK, Linial ML. 2006. Expanded tissue targets for foamy virus replication with simian immunodeficiency virusinduced immunosuppression. J. Virol. 80:663-670.
4. Murray SM, Picker LJ, Axthelm MK, Hudkins K, Alpers CE, Linial ML. 2008. Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections. J. Virol. 82:5981-5985.
5. Jones-Engel L, Steinkraus KA, Murray SM, Engel GA, Grant R, Aggimarangsee N, Lee BPY-H, May C, Schillaci MA, Somgird C, Sutthipat T, Vojtech L, Zhao J-Y, Linial ML. 2007. Sensitive assays for simian foamy viruses reveal a high prevalence of infection in commensal, freeranging, Asian monkeys. J. Virol. 81:7330-7337.
6. Falcone V, Schweizer M, Neumann-Haefelin D. 2003. Replication of primate foamy viruses in natural and experimental hosts, p 161-180. In Rethwilm A (ed), Foamy viruses. Springer, Berlin, Germany.
7. Blewett EL, Black DH, Lerche NW, White G, Eberle R. 2000. Simian foamy virus infections in a baboon breeding colony. Virology 278:183-193.
8. Calattini S, Wanert F, Thierry B, Schmitt C, Bassot S, Saib A, Herrenschmidt N, Gessain A. 2006. Modes of transmission and genetic diversity of foamy viruses in a Macaca tonkeana colony. Retrovirology 3:23. doi:10.1186/1742-4690-3-23.
9. Boneva RS, Switzer WM, Spira TJ, Bhullar VB, Shanmugam V, Cong Me Lam L, Heneine W, Folks TM, Chapman LE. 2007. Clinical and virological characterization of persistent human infection with simian foamy viruses. AIDS Res. Hum. Retroviruses 23:1330-1337.
10. 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(10):e1002306. doi:10.1371/journal.ppat.1002306.
11. 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 N, 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.
12. Engel GA, Small CT, Soliven K, Feeroz MM, Wang X, Hasan K, Gunwha O, Alam S, Craig K, Jackson D, Matsen FA, IV, Linial ML, Jones-Engel L. 2013. Zoonotic simian foamy virus in Bangladesh reflects diverse patterns of transmission and co-infections among humans. Emerg. Microbes Infect. 2:e58. doi:10.1038/emi.2013.60.
13. 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.
14. Brooks JI, Merks HW, Fournier J, Boneva RS, Sandstrom PA. 2007. Characterization of blood-borne transmission of simian foamy virus. Transfusion 47:162-170.
15. Hooks JJ, Burns W, Hayashi K, Geis S, Notkins AL. 1976. Viral spread in the presence of neutralizing antibody:mechanisms of persistence in foamy virus infection. Infect. Immun. 14:1172-1178.
16. Feeroz M, Soliven K, Small C, Engel G, Pacheco M, Yee J, Wang X, Hasan K, Oh G, Levine K, Alam S, Craig K, Jackson D, Lee E-G, Barry P, Lerche N, Escalante A, Matsen F, Linial M, 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.
17. Cullen BR. 2006. Role and mechanism of action of the APOBEC3 family of antiretroviral resistance factors. J. Virol. 80:1067-1076.
18. Marin M, Rose KM, Kozak SL, Kabat D. 2003. HIV-1 Vif protein binds the editing enzyme APOBEC3G and induces its degradation. Nat. Med. 9:1398-1403.
19. Zhang A, Bogerd H, Villinger F, Das Gupta J, Dong B, Klein EA, Hackett J, Jr, Schochetman G, Cullen BR, Silverman RH. 2011. In vivo hypermutation of xenotropic murine leukemia virus-related virusDNAin peripheral blood mononuclear cells of rhesus macaque by APOBEC3 proteins. Virology 421:28-33.
20. Kirchoff V, Wong S, St JS, Pari GS. 2002. Generation of a life-expanded rhesus monkey fibroblast cell line for the growth of rhesus rhadinovirus (RRV). Arch. Virol. 147:321-333.
21. Edgar RC. 2004. MUSCLE:multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792-1797.
22. Fang F, Ding J, Minin VN, Suchard MA, Dorman KS. 2007. cBrother:relaxing parental tree assumptions for Bayesian recombination detection. Bioinformatics 23:507-508.
23. Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
24. Hasegawa M, Kishino H, Yano TA. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. J. Mol. Evol. 22:160-174.
25. Han MV, Zmasek CM. 2009. phyloXML:XML for evolutionary biology and comparative genomics. BMC Bioinform. 10:356. doi:10.1186/1471 -2105-10-356.
26. Core Team R. 2012. R:a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria.
27. Mullers E. 2013. The foamy virus Gag proteins:what makes them different? Viruses 5:1023-1041.
28. Stange A, Mannigel I, Peters K, Heinkelein M, Stanke N, Cartellieri M, Gottlinger H, Rethwilm A, Zentgraf H, Lindemann D. 2005. Characterization of prototype foamy virus gag late assembly domain motifs and their role in particle egress and infectivity. J. Virol. 79:5466-5476.
29. Patton GS, Morris SA, Chung W, Bieniasz PD, McClure MO. 2005. Identification of domains in gag important for prototypic foamy virus egress. J. Virol. 79:6392-6399.
30. Beale RCL, Petersen-Mahrt SK, Watt IN, Harris RS, Rada C, Neuberger MS. 2004. Comparison of the differential context-dependence of DNA deamination by APOBEC enzymes:correlation with mutation spectra in vivo. J. Mol. Biol. 337:585-596.
31. Calattini S, Nerrienet E, Mauclere P, Georges-Courbot MC, Saib A, Gessain A. 2004. Natural simian foamy virus infection in wild-caught gorillas, mandrills and drills from Cameroon and Gabon. J. Gen. Virol. 85:3313-3317.
32. Liu W, Worobey M, Li Y, Keele BF, Bibollet-Ruche F, Guo Y, Goepfert PA, Santiago ML, Ndjango JB, Neel C, Clifford SL, Sanz C, Kamenya S, Wilson ML, Pusey AE, Gross-Camp N, Boesch C, Smith V, Zamma K, Huffman MA, Mitani JC, Watts DP, Peeters M, Shaw GM, Switzer WM, Sharp PM, Hahn BH. 2008. Molecular ecology and natural history of simian foamy virus infection in wild-living chimpanzees. PLoS Pathog. 4:e1000097. doi:10.1371/journal.ppat.1000097.
33. Blasse A, Calvignac-Spencer S, Merkel K, Goffe AS, Boesch C, Mundry R, Leendertz FH. 2013. Mother-offspring transmission and agedependent accumulation of simian foamy virus in wild chimpanzees. J. Virol. 87:5193-5204.
34. Hussain AI, Shanmugam V, Bhullar VB, Beer BE, Vallet D, Gautier-Hion A, Wolfe ND, Karesh WB, Kilbourn AM, Tooze Z, Heneine W, Switzer WM. 2003. Screening for simian foamy virus infection by using a combined antigen Western blot assay:evidence for a wide distribution among Old World primates and identification of four new divergent viruses. Virology 309:248-257.
35. 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.
36. Bailes E, Gao F, Bibollet-Ruche F, Courgnaud V, Peeters M, Marx PA, Hahn BH, Sharp PM. 2003. Hybrid origin of SIV in chimpanzees. Science 300:1713-1716.
37. Chaipan C, Smith JL, Hu WS, Pathak VK. 2013. APOBEC3G restricts HIV-1 to a greater extent than APOBEC3F and APOBEC3DE in human primary CD4+ T cells and macrophages. J. Virol. 87:444-453.
38. Delebecque F, Suspene R, Calattini S, Casartelli N, Saib A, Froment A, Wain-Hobson S, Gessain A, Vartanian JP, Schwartz O. 2006. Restriction of foamy viruses by APOBEC cytidine deaminases. J. Virol. 80:605-614.
39. Gartner K, Wiktorowicz T, Park J, Mergia A, Rethwilm A, Scheller C. 2009. Accuracy estimation of foamy virus genome copying. Retrovirology 6:32. doi:10.1186/1742-4690-6-32.
40. Perkovic M, Schmidt S, Marino D, Russell RA, Stauch B, Hofmann H, Kopietz F, Kloke BP, Zielonka J, Strover H, Hermle J, Lindemann D, Pathak VK, Schneider G, Lochelt M, Cichutek K, Munk C. 2009. Species-specific inhibition of APOBEC3C by the prototype foamy virus protein Bet. J. Biol. Chem. 284:5819-5826.
41. Russell RA, Wiegand HL, Moore MD, Schafer A, McClure MO, Cullen BR. 2005. Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J. Virol. 79:8724-8731.
42. Jaguva Vasudevan AA, Perkovic M, Bulliard Y, Cichutek K, Trono D, Haussinger D, Munk C. 2013. Prototype foamy virus Bet impairs the dimerization and cytosolic solubility of human APOBEC3G. J. Virol. 87:9030-9040.
43. Lukic D, Hotz-Wagenblatt A, Lei J, Rathe A-M, Muhle M, Denner J, Munk C, Lochelt M. 2013. Identification of the feline foamy virus Bet domain essential for APOBEC3 counteraction. Retrovirology 10:76. doi:10.1186/1742-4690-10-76.