Foamy virus vectors for gene transfer

Expert Opinion on Biological Therapy

Volumn 9, Issue 11, 2009, Pages 1427-1436

  Trobridge, Grant D ^a  

^a Fred Hutchinson Cancer Research Center   (United States)

Author keywords

Foamy virus; Gene therapy; Hematopoietic stem cell; Retroviral vector; Spumaretrovirus

Indexed keywords

FOAMY VIRUS VECTOR; GAG PROTEIN; POL PROTEIN; UNCLASSIFIED DRUG; VIRUS ENVELOPE PROTEIN; VIRUS VECTOR;

CELL CYCLE; CELL DIFFERENTIATION; DRUG MECHANISM; DRUG SAFETY; DRUG TARGETING; GENE INSERTION; GENE TRANSFER; GENETIC TRANSDUCTION; HEMATOPOIETIC STEM CELL TRANSPLANTATION; HUMAN; NONHUMAN; REVIEW; SPUMA VIRUS; TARGET CELL; VIRAL GENE DELIVERY SYSTEM; VIRAL GENE THERAPY; VIRUS REPLICATION;

ANIMALS; DOGS; GENE THERAPY; GENE TRANSFER TECHNIQUES; GENETIC VECTORS; HUMANS; MODELS, ANIMAL; SPUMAVIRUS; TRANSDUCTION, GENETIC;

ANIMALIA; HUMAN SPUMARETROVIRUS; MAMMALIA; PRIMATES;

EID: 70350633843     PISSN: 14712598     EISSN: None     Source Type: Journal    
DOI: 10.1517/14712590903246388     Document Type: Review

References (101)

1. Switzer WM, Salemi M, Shanmugam V, et al. Ancient co-speciation of simian foamy viruses and primates. Nature 2005;434(7031):376-380 (Pubitemid 40469179)
2. Wick G, Grubeck-Loebenstein B, Trieb K, et al. Human foamy virus antigens in thyroid tissue of Graves' disease patients. Int Arch Allergy Immunol 1992;99(1):153-156 (Pubitemid 23010368)
3. Schweizer M, Turek R, Hahn H, et al. 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 1995;11(1):161-170 • Definitive study showing that FVs are not endemic in human populations.
4. Heneine W, Switzer WM, Sandstrom P, et al. Identification of a human population infected with simian foamy viruses [see comments]. Nat Med 1998;4(4):403-407 (Pubitemid 28212754)
5. Switzer WM, Bhullar V, Shanmugam V, et al. Frequent simian foamy virus infection in persons occupationally exposed to nonhuman primates. J Virol 2004;78(6):2780-2789 (Pubitemid 38314337)
6. Linial M. Why aren't foamy viruses pathogenic? Trends Microbiol 2000;8(6):284-289
7. Meiering CD, Linial ML. Historical perspective of foamy virus epidemiology and infection. Clin Microbiol Rev 2001;14(1):165-176 (Pubitemid 32096212)
8. Donahue RE, Kessler SW, Bodine D, et al. Helper virus induced T cell lymphoma in nonhuman primates after retroviral mediated gene transfer. J Exp Med 1992;176(4):1125-1135
9. Murray SM, Picker LJ, Axthelm MK, et al. Replication in a superficial epithelial cell niche explains the lack of pathogenicity of primate foamy virus infections. J Virol 2008;82(12):5981-5985
10. Murray SM, Linial ML. Foamy virus infection in primates. J Med Primatol 2006;35(4-5):225-235
11. Boneva RS, Switzer WM, Spira TJ, et al. Clinical and virological characterization of persistent human infection with simian foamy viruses. AIDS Res Hum Retroviruses 2007;23(11):1330-1337
12. Boneva RS, Grindon AJ, Orton SL, et al. Simian foamy virus infection in a blood donor. Transfusion 2002;42(7):886-891
13. Lochelt M, Zentgraf H, Flugel RM. Construction of an infectious DNA clone of the full-length human spumaretrovirus genome and mutagenesis of the bel 1 gene. Virology 1991;184(1):43-54
14. Lochelt M, Yu SF, Linial ML, Flugel RM. The human foamy virus internal promoter is required for efficient gene expression and infectivity. Virology 1995;206(1):601-610
15. Rethwilm A, Erlwein O, Baunach G, et al. The transcriptional transactivator of human foamy virus maps to the bel 1 genomic region. Proc Natl Acad Sci USA 1991;88(3):941-945 (Pubitemid 21916140)
16. Venkatesh LK, Theodorakis PA, Chinnadurai G. Distinct cis-acting regions in U3 regulate trans-activation of the human spumaretrovirus long terminal repeat by the viral bel1 gene product. Nucleic Acids Res 1991;19(13):3661-3666 (Pubitemid 21912732)
17. Trobridge GD, Russell DW. Helper-free foamy virus vectors. Hum Gene Ther 1998;9(17):2517-2525
18. Heinkelein M, Schmidt M, Fischer N, et al. Characterization of a cis-acting sequence in the Pol region required to transfer human foamy virus vectors. J Virol 1998;72(8):6307-6314 (Pubitemid 28323940)
19. Lochelt M, Romen F, Bastone P, et al. The antiretroviral activity of APOBEC3 is inhibited by the foamy virus accessory Bet protein. Proc Natl Acad Sci USA 2005;102(22):7982-7987 (Pubitemid 40781049)
20. Bock M, Heinkelein M, Lindemann D, Rethwilm A. Cells expressing the human foamy virus (HFV) accessory Bet protein are resistant to productive HFV superinfection. Virology 1998;250(1):194-204 (Pubitemid 28471775)
21. Moebes A, Enssle J, Bieniasz PD, et al. Human foamy virus reverse transcription that occurs late in the viral replication cycle. J Virol 1997;71(10):7305-7311 (Pubitemid 27391668)
22. Yu SF, Baldwin DN, Gwynn SR, et al. Human foamy virus replication: a pathway distinct from that of retroviruses and hepadnaviruses. Science 1996;271(5255):1579-1582 •• Demonstrated the unique replication strategy of FVs.
23. Yu SF, Sullivan MD, Linial ML. Evidence that the human foamy virus genome is DNA. J Virol 1999;73(2):1565-1572
24. Zack JA, Arrigo SJ, Weitsman SR, et al. HIV-1 entry into quiescent primary lymphocytes: molecular analysis reveals a labile, latent viral structure. Cell 1990;61(2):213-222 (Pubitemid 20149353)
25. Enssle J, Jordan I, Mauer B, Rethwilm A. Foamy virus reverse transcriptase is expressed independently from the Gag protein. Proc Natl Acad Sci USA 1996;93(9):4137-4141 (Pubitemid 26144253)
26. Trobridge G, Josephson N, Vassilopoulos G, et al. Improved foamy virus vectors with minimal viral sequences. Mol Ther 2002;6(3):321-328 • Describes current-generation FV vectors. (Pubitemid 36305333)
27. Schmidt M, Rethwilm A. Replicating foamy virus-based vectors directing high level expression of foreign genes. Virology 1995;210(1):167-178 • First description of FV vectors.
28. Nestler U, Heinkelein M, Lucke M, et al. Foamy virus vectors for suicide gene therapy. Gene Ther 1997;4(11):1270-1277 (Pubitemid 27493891)
29. Heinkelein M, Dressler M, Jarmy G, et al. Improved primate foamy virus vectors and packaging constructs. J Virol 2002;76(8):3774-3783 • Describes current-generation FV vectors. (Pubitemid 34250542)
30. Wu M, Chari S, Yanchis T, Mergia A. cis-Acting sequences required for simian foamy virus type 1 vectors. J Virol 1998;72(4):3451-3454 (Pubitemid 28175598)
31. Park J, Nadeau PE, Mergia A. A minimal genome simian foamy virus type 1 vector system with efficient gene transfer. Virology 2002;302(2):236-244 (Pubitemid 35373852)
32. Bastone P, Bravo IG, Lochelt M. Feline foamy virus-mediated marker gene transfer: identification of essential genetic elements and influence of truncated and chimeric proteins. Virology 2006;348(1):190-199
33. Bastone P, Romen F, Liu W, et al. Construction and characterization of efficient, stable and safe replication-deficient foamy virus vectors. Gene Ther 2007;14(7):613-620 (Pubitemid 46444535)
34. Achong BG, Mansell PW, Epstein MA, Clifford P. An unusual virus in cultures from a human nasopharyngeal carcinoma. J Natl Cancer Inst 1971;46(2):299-307
35. Herchenroder O, Renne R, Loncar D, et al. Isolation, cloning, and sequencing of simian foamy viruses from chimpanzees (SFVcpz): high homology to human foamy virus (HFV). Virology 1994;201(2):187-199
36. Schweizer M, Neumann-Haefelin D. Phylogenetic analysis of primate foamy viruses by comparison of pol sequences. Virology 1995;207(2):577-582
37. Zucali JR, Ciccarone T, Kelley V, et al. Transduction of umbilical cord blood CD34+ NOD/SCID-repopulating cells by simian foamy virus type 1 (SFV-1) vector. Virology 2002;302(2):229-235 (Pubitemid 35373851)
38. Russell DW, Miller AD. Foamy virus vectors. Journal of virology 1996;70(1):217-222
39. Hirata RK, Miller AD, Andrews RG, Russell DW. Transduction of hematopoietic cells by foamy virus vectors. Blood 1996;88(9):3654-3661 (Pubitemid 26365605)
40. Peters K, Barg N, Gartner K, Rethwilm A. Complex effects of foamy virus central purine-rich regions on viral replication. Virology 2008;373(1):51-60
41. Wiktorowicz T, Peters K, Armbruster N, et al. Generation of an improved foamy virus vector by dissection of cis-acting sequences. J Gen Virol 2009;90(Pt 2):481-487
42. Bastone P, Lochelt M. Kinetics and characteristics of replication-competent revertants derived from self-inactivating foamy virus vectors. Gene Ther 2004;11(5):465-473 (Pubitemid 38313167)
43. Schenk T, Enssle J, Fischer N, Rethwilm A. Replication of a foamy virus mutant with a constitutively active U3 promoter and deleted accessory genes. J Gen Virol 1999;80(Pt 7):1591-1598 (Pubitemid 29319849)
44. Trobridge GD, Allen JM, Peterson L, et al. Foamy and lentiviral vectors transduce canine long-term repopulating cells at similar efficiency. Hum Gene Ther 2009;20:519-523
45. Kiem HP, Allen J, Trobridge G, et al. Foamy virus-mediated gene transfer to canine repopulating cells. Blood 2007;109(1):65-70 •• First demonstration of FV vector-mediated efficient gene transfer to large animal hematopoietic repopulating cells. (Pubitemid 46053045)
46. Patton GS, Erlwein O, McClure MO. Cell-cycle dependence of foamy virus vectors. J Gen Virol 2004;85(Pt 10):2925-2930 (Pubitemid 39360035)
47. Duda A, Luftenegger D, Pietschmann T, Lindemann D. Characterization of the prototype foamy virus envelope glycoprotein receptor-binding domain. J Virol 2006;80(16):8158-8167 (Pubitemid 44182316)
48. Hill CL, Bieniasz PD, McClure MO. Properties of human foamy virus relevant to its development as a vector for gene therapy. J Gen Virol 1999;80(Pt 8):2003-2009
49. Pietschmann T, Heinkelein M, Heldmann M, et al. Foamy virus capsids require the cognate envelope protein for particle export. J Virol 1999;73(4):2613-2621 (Pubitemid 29135645)
50. Baldwin DN, Linial ML. The roles of Pol and Env in the assembly pathway of human foamy virus [see comments]. J Virol 1998;72(5):3658-3665
51. Fischer N, Heinkelein M, Lindemann D, et al. Foamy virus particle formation. J Virol 1998;72(2):1610-1615
52. Vassilopoulos G, Trobridge G, Josephson NC, Russell DW. Gene transfer into murine hematopoietic stem cells with helper-free foamy virus vectors. Blood 2001;98(3):604-609 • First demonstration that FV vectors efficiently transduce mouse HSCs.
53. Takeuchi Y, Liong SH, Bieniasz PD, et al. Sensitization of rhabdo-, lenti-, and spumaviruses to human serum by galactosyl(alpha1-3)galactosylation. J Virol 1997;71(8):6174-6178 (Pubitemid 27304959)
54. Lindemann D, Bock M, Schweizer M, Rethwilm A. Efficient pseudotyping of murine leukemia virus particles with chimeric human foamy virus envelope proteins. J Virol 1997;71(6):4815-4820 (Pubitemid 27204176)
55. Sun Z, Zeng Y, Li Y, et al. Lentiviral FANCA vectors pseudotyped with a modified foamy viral envelope corrects murine Fanca-/- hematopoietic stem cells with reduced toxicity and higher efficiency [abstract]. Mol Ther 2009;17(Supplement1):S292
56. Chiu YL, Greene WC. The APOBEC3 cytidine deaminases: an innate defensive network opposing exogenous retroviruses and endogenous retroelements. Annu Rev Immunol 2008;26:317-353
57. Baumann JG. Intracellular restriction factors in mammalian cells: an ancient defense system finds a modern foe. Curr HIV Res 2006;4(2):141-168
58. de Vries W, Haasnoot J, van der Velden J, et al. Increased virus replication in mammalian cells by blocking intracellular innate defense responses. Gene Ther 2008;15(7):545-552
59. Mangeat B, Trono D. Lentiviral vectors and antiretroviral intrinsic immunity. Hum Gene Ther 2005;16(8):913-920 (Pubitemid 41153860)
60. Brown BD, Sitia G, Annoni A, et al. In vivo administration of lentiviral vectors triggers a type I interferon response that restricts hepatocyte gene transfer and promotes vector clearance. Blood 2007;109(7):2797-2805
61. Perkovic M, Schmidt S, Marino D, et al. Species-specific inhibition of APOBEC3C by the prototype foamy virus protein bet. J Biol Chem 2009;284(9):5819-5826
62. Munk C, Beck T, Zielonka J, et al. Functions, structure, and read-through alternative splicing of feline APOBEC3 genes. Genome Biol 2008;9(3):R48 (Pubitemid 351944021)
63. Russell RA, Wiegand HL, Moore MD, et al. Foamy virus Bet proteins function as novel inhibitors of the APOBEC3 family of innate antiretroviral defense factors. J Virol 2005;79(14):8724-8731
64. Gartner K, Wiktorowicz T, Park J, et al. Accuracy estimation of foamy virus genome copying. Retrovirology 2009;6:32
65. Yap MW, Lindemann D, Stanke N, et al. Restriction of foamy viruses by primate Trim5alpha. J Virol 2008;82(11):5429-5439 (Pubitemid 351705250)
66. Samuel CE. Antiviral actions of interferons. Clin Microbiol Rev 2001;14(4):778-809, table of contents
67. Rhodes-Feuillette A, Saal F, Lasneret J, et al. Studies on in vitro interferon induction capacity and interferon sensitivity of simian foamy viruses. Arch Virol 1987;97(1-2):77-84
68. Sabile A, Rhodes-Feuillette A, Jaoui FZ, et al. In vitro studies on interferon-inducing capacity and sensitivity to IFN of human foamy virus. Res Virol 1996;147(1):29-37
69. Tan J, Qiao W, Wang J, et al. IFP35 is involved in the antiviral function of interferon by association with the viral tas transactivator of bovine foamy virus. J Virol 2008;82(9):4275-4283 (Pubitemid 351563665)
70. Santoni de Sio FR, Gritti A, Cascio P, et al. Lentiviral vector gene transfer is limited by the proteasome at postentry steps in various types of stem cells. Stem Cells 2008;26(8):2142-2152
71. Santoni de Sio FR, Cascio P, Zingale A, et al. Proteasome activity restricts lentiviral gene transfer into hematopoietic stem cells and is down-regulated by cytokines that enhance transduction. Blood 2006;107(11):4257-4265 (Pubitemid 43801349)
72. Miller DG, Adam MA, Miller AD. Gene transfer by retrovirus vectors occurs only in cells that are actively replicating at the time of infection. Mol Cell Biol 1990;10(8):4239-4242 (Pubitemid 20227308)
73. Lewis PF, Emerman M. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J Virol 1994;68(1):510-516 (Pubitemid 24974657)
74. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science 1996;272(5259):263-267
75. Trobridge G, Russell DW. Cell cycle requirements for transduction by foamy virus vectors compared to those of oncovirus and lentivirus vectors. J Virol 2004;78(5):2327-2335 • Definitive study characterizing the cell cycle requirements of FV vectors. (Pubitemid 38228926)
76. Park F, Ohashi K, Chiu W, et al. Efficient lentiviral transduction of liver requires cell cycling in vivo. Nat Genet 2000;24(1):49-52 (Pubitemid 30041419)
77. Yamashita M, Emerman M. Retroviral infection of non-dividing cells: old and new perspectives. Virology 2006;344(1):88-93 (Pubitemid 41814454)
78. Bieniasz PD, Weiss RA, McClure MO. Cell cycle dependence of foamy retrovirus infection. J Virol 1995;69(11):7295-7299
79. Lehmann-Che J, Renault N, Giron ML, et al. Centrosomal latency of incoming foamy viruses in resting cells. PLoS Pathog 2007;3(5):e74 (Pubitemid 46827954)
80. Caprariello AV, Miller RH, Selkirk SM. Foamy virus as a gene transfer vector to the central nervous system. Gene Ther 2009;16(3):448-452
81. Varmus HE, Weiss RA, Friis RR, et al. Detection of avian tumor virus-specific nucleotide sequences in avian cell DNAs (reassociation kinetics-RNA tumor viruses-gas antigen-Rous sarcoma virus, chick cells). Proc Natl Acad Sci USA 1972;69(1):20-24
82. Nienhuis AW, Dunbar CE, Sorrentino BP. Genotoxicity of retroviral integration in hematopoietic cells. Mol Ther 2006;13(6):1031-1049 (Pubitemid 43779188)
83. Josephson NC, Vassilopoulos G, Trobridge GD, et al. Transduction of human NOD/SCID-repopulating cells with both lymphoid and myeloid potential by foamy virus vectors. Proc Natl Acad Sci USA 2002;99(12):8295-8300 • First demonstration that FV vectors efficiently transduce pluripotent human SRCs. (Pubitemid 34651046)
84. Neves M, Peries J, Saib A. Study of human foamy virus proviral integration in chronically infected murine cells. Res Virol 1998;149(6):393-401 (Pubitemid 29487142)
85. Trobridge GD, Miller DG, Jacobs MA, et al. Foamy virus vector integration sites in normal human cells. Proc Natl Acad Sci USA 2006;103(5):1498-1503 •• Detailed large-scale analysis of FV vector integration sites in normal human cells.
86. Wu X, Li Y, Crise B, Burgess SM. Transcription start regions in the human genome are favored targets for MLV integration. Science 2003;300(5626):1749- 1751 (Pubitemid 36712571)
87. Schroder AR, Shinn P, Chen H, et al. HIV-1 integration in the human genome favors active genes and local hotspots. Cell 2002;110(4):521-529 (Pubitemid 35232295)
88. Nowrouzi A, Dittrich M, Klanke C, et al. Genome-wide mapping of foamy virus vector integrations into a human cell line. J Gen Virol 2006;87(Pt 5):1339-1347
89. Hendrie PC, Huo Y, Stolitenko RB, Russell DW. A rapid and quantitative assay for measuring neighboring gene activation by vector proviruses. Mol Ther 2008;16(3):534-540 (Pubitemid 351314993)
90. Park J, Nadeau P, Zucali JR, et al. Inhibition of simian immunodeficiency virus by foamy virus vectors expressing siRNAs. Virology 2005;343(2):275-282 (Pubitemid 41599883)
91. Taylor JA, Vojtech L, Bahner I, et al. Foamy virus vectors expressing anti-HIV transgenes efficiently block HIV-1 replication. Mol Ther 2008;16(1):46-51
92. Gharwan H, Hirata RK, Wang P, et al. Transduction of human embryonic stem cells by foamy virus vectors. Mol Ther 2007;15(10):1827-1833 (Pubitemid 47434190)
93. Rothenaigner I, Kramer S, Meggendorfer M, et al. Transduction of human neural progenitor cells with foamy virus vectors for differentiation-dependent gene expression. Gene Ther 2009;16(3):349-358
94. Josephson NC, Trobridge G, Russell DW. Transduction of long-term and mobilized peripheral blood-derived NOD/SCID repopulating cells by foamy virus vectors. Hum Gene Ther 2004;15(1):87-92 (Pubitemid 38147191)
95. Leurs C, Jansen M, Pollok KE, et al. Comparison of three retroviral vector systems for transduction of nonobese diabetic/severe combined immunodeficiency mice repopulating human CD34(+) cord blood cells. Hum Gene Ther 2003;14(6):509-519 (Pubitemid 36442706)
96. Horn PA, Keyser KA, Peterson LJ, et al. Efficient lentiviral gene transfer to canine repopulating cells using an overnight transduction protocol. Blood 2004;103(10):3710-3716
97. Beard BC, Keyser KA, Trobridge GD, et al. Unique integration profiles in a canine model of long-term repopulating cells transduced with gammaretrovirus, lentivirus, or foamy virus. Hum Gene Ther 2007;18(5):423-434
98. Bauer TR Jr, Allen JM, Hai M, et al. Successful treatment of canine leukocyte adhesion deficiency by foamy virus vectors. Nat Med 2008;14(1):93-97 •• First demonstration of FV vector therapeutic gene transfer in a large animal model.
99. Si Y, Pulliam AC, Linka Y, et al. Overnight transduction with foamyviral vectors restores the long-term repopulating activity of Fancc-/- stem cells. Blood 2008;112(12):4458-4465
100. Liu W, Liu Z, Liu L, et al. A novel human foamy virus mediated gene transfer of GAD67 reduces neuropathic pain following spinal cord injury. Neurosci Lett 2008;432(1):13-18
101. Wei BL, Denton PW, O'Neill E, et al. Inhibition of lysosome and proteasome function enhances human immunodeficiency virus type 1 infection. J Virol 2005;79(9):5705-5712 (Pubitemid 40548239)