Lentiviruses as gene transfer agents for delivery to non-dividing cells

Current Opinion in Biotechnology

Volumn 9, Issue 5, 1998, Pages 457-463

  Naldini, Luigi ^a  

^a CELL GENESYS INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLASMID VECTOR;

BRAIN; CELL DIVISION; DRUG SAFETY; GENE EXPRESSION; GENE SEQUENCE; GENE TARGETING; GENE THERAPY; GENE TRANSFER; GENETIC TRANSDUCTION; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS; LENTIVIRINAE; LIVER; MUSCLE; NONHUMAN; PRIORITY JOURNAL; RETINA; REVIEW; TISSUE; TRANSGENE;

HUMAN IMMUNODEFICIENCY VIRUS; LENTIVIRUS; PRIMATES;

EID: 0032191380     PISSN: 09581669     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0958-1669(98)80029-3     Document Type: Article

References (71)

1. Verma IM, Somia N. Gene therapy promises, problems and prospects. Nature. 389:1997;239-242. of special interest.
2. Anderson WF. Human gene therapy. of special interest Nature. 392:1998;25-30 With [1], two thorough, updated reviews that cover the field of gene therapy from vector biology to clinical applications and ethical issues, and convey the perspective of two of its founding fathers and most outspoken leaders.
3. 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 Cel Biol. 10:1990;4239-4242.
4. Roe T, Reynolds TC, Yu G, Brown PO. Integration of murine leukemia virus DNA depends on mitosis. EMBO J. 12:1993;2099-2108.
5. Weinberg JB, Matthews TJ, Cullen BR, Malim MH. Productive human immunodeficiency virus type 1 (HIV-1) infection of nonproliferating human monocytes. J Exp Med. 174:1991;1477-1482.
6. Lewis PF, Hensel M, Emerman M. Human immunodeficiency virus infection of cell arrested in the cell cycle. EMBO J. 11:1992;3053-3058.
7. Lewis PF, Emerman M. Passage through mitosis is required for oncoretroviruses but not for the human immunodeficiency virus. J Virol. 68:1994;510-516.
8. Bukrinsky MI, Haggerty S, Dempsey MP, Sharova N, Adzhubel A, Spitz L, Lewis P, Goldfarb D, Emerman M, Stevenson M. A nuclear localization signal within HIV-1 matrix protein that governs infection of non-dividing cells. Nature. 365:1993;666-669.
9. Heinzinger NK, Bukinsky MI, Haggerty SA, Ragland AM, Kewalromani V, Lee MA, Gendelman HE, Ratner L, Stevenson M, Emerman M. The Vpr protein of human immunodeficiency virus type 1 influences nuclear localization of viral nucleic acids in nondividing host cells. Proc Natl Acad Sci USA. 91:1994;7311-7315.
10. Popov S, Rexach M, Zybart G, Reiling N, Lee MA, Ratner L, Lane CM, Moore MS, Blobel G, Bukrinsky M. Viral protein R regulates nuclear import of the HIV-1 pre-integration complex. EMBO J. 17:1998;909-917.
11. Gallay P, Swingler S, Aiken C, Trono D. HIV-1 infection of nondividing cells: C-terminal tyrosine phosphorylation of the viral matrix protein is a key regulator. Cell. 80:1995;379-388.
12. Gallay P, Swingler S, Song J, Bushman F, Trono D. HIV nuclear import is governed by the phosphotyrosine-mediated binding of matrix to the core domain of integrase. Cell. 83:1995;569-576.
13. Gallay P, Chin D, Hope TJ, Trono D. HIV-1 infection of nondividing cells mediated through the reconition of integrase by the import/karyopherin pathway. Proc Natl Acad Sci USA. 94:1997;9825-9830.
14. + cells by a recombinant human immunodeficiency virus retroviral vector. J Clin Invest. 88:1991;1043-1047.
15. Poznansky M, Lever A, Bergeron, Haseltine W, Sodroski J. Gene transfer into human lymphocytes by a defective human immunodeficiency virus type 1 vector. J Virol. 65:1991;532-536.
16. Buchschacher GLJ, Panganiban AT. Human immunodeficiency virus vectors for inducible expression of foreign genes. J Virol. 66:1992;2731-2739.
17. Parolin C, Dorfman T, Palu G, Gottlinger H, Sodroski J. Analysis in human immunodeficiency virus type 1 vectors of cis-acting sequences that affect gene transfer into human lymphocytes. J Virol. 68:1994;3888-3895.
18. Naldini L, Blömer U, Gallay P, Ory D, Mulligan R, Gage FH, Verma IM, Trono D. In vivo genes delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 272:1996;263-267.
19. Naldini L, Blömer U, Gage FH, Trono D, Verma IM. Efficient transfer, integration, and sustained long-term expression of the transgene in adult rat brains injected with a lentiviral vector. Proc Natl Acad Sci USA. 93:1996;11382-11388.
20. Reiser J, Harmison G, Kluepfel-Stahl S, Brady RO, Karlsson S, Schubert M. Transduction of nondividing cells pseudotyped defective high-titer HIV type 1 particles. Proc Natl Acad Sci USA. 93:1996;15266-15271.
21. Poeschla E, Corbeau P, Wong-Staal F. Development of HIV vectors for anti-HIV gene therapy. Proc Natl Acad Sci USA. 93:1996;11395-11399.
22. Goldman MJ, Lee P-S, Yang J-S, Wilson JM. Lentiviral vectors for gene therapy of cystic fibrosis. Hum Gene Ther. 8:1997;2261-2268.
23. of special interest Zufferey R, Nagy D, Mandel RJ, Naldini L, Trono D. Multiply attenuated lentiviral vector achieves efficient gene delivery in vivo. of outstanding interest Nat Biotechnol. 15:1997;871-875 See annotation to [24].
24. of outstanding interest Kim VN, Mitrophanous K, Kingsman SM, Kingsman AJ. Minimal requirement for a lentivirus vector based on human immunodeficiency virus type 1. of special interest J Virol. 72:1998;811-816 Both of the above papers report a systematic analysis of individual and combined deletions of the four accessory genes of HIV from the packaging construct of HIV-based vectors. They show that, unexpectedly, all four gene products can be eliminated without affecting the efficiency of gene transfer in vitro [23,24] and into brain neurons in vivo [23]. These modifications yielded a second generation of HIV-derived vectors of much improved biosafety and acceptability.
25. Blömer U, Naldini L, Kafri T, Trono D, Verma IM, Gage FH. Highly efficient and sustained gene transfer in adult neurons with a lentivirus vector. of special interest J Virol. 71:1997;6641-6649 Efficiency of gene transfer, duration of transgene expression, and local immune response were compared after intracerebral injection of four different vector systems derived from HIV, MLV, AAV and adenovirus. The results suggest that lifelong expression of an exogenous gene can be achieved in normal animals without detectable pathological consequences by a single injection of HIV-derived vector.
26. Kafri T, Blömer U, Peterson DA, Gage FH, Verma IM. Sustained expression of genes delivered directly into liver and muscle by lentiviral vectors. of outstanding interest Nat Genet. 17:1997;314-317 Successful transduction of the liver and skeletal muscles of adult rats is reported after intraparenchimal injection of HIV-based vectors. Transgene expression was sustained for more than 22 weeks in the liver, and eight weeks in the muscle, in both cases the longest time tested, without signs of inflammation or immune reaction at the site of injection. The results indicate that lentiviral vectors are efficient and versatile gene transfer agents for in vivo delivery.
27. Miyoshi H, Takahashi M, Gage FH, Verma IM. Stable and efficient gene transfer into the retina using an HIV-based lentiviral vector. of outstanding interest Proc Natl Acad Sci USA. 94:1997;10319-10323 Stable and efficient gene delivery is reported in the retina after injection of HIV-derived vectors into the subretinal space of rats. The use of the rhodopsin promoter yielded a specific pattern of transgene expression in the photoreceptor cells. This work opens the way to the testing of therapeutic gene transfer in models of retinal disease, and indicates the potential of lentiviral vectors for tissue-specific expression.
28. Poeschla EF, Wong-Staal DJ, Looney L. Efficient transduction of nondividing human cells by feline immunodeficiency virus lentiviral vectors. of outstanding interest Nat Med. 4:1998;354-357 Vectors derived from the FIV virus and pseudotyped with VSV transduced efficiently non-dividing human primary cells in vitro. Although LTR-directed expression of FIV was very poor in human cells, promoter substitution enabled high level expression of FIV proteins. The results indicate that the only important blocks to FIV infection of human cells are receptor recognition and the transcriptional activity of the LTR. This work confirms the value of lentiviral vectors as gene transfer agents and may provide an alternative pathway to their clinical testing.
29. Burns JC, Friedmann T, Driever W, Burrascano M, Yee JK. Vesicular stomatitis virus G glycoprotein pseudotyped retroviral vectors: concentration to very high titer and efficient gene transfer into mammalian and non-mammalian cells. Proc Natl Acad Sci USA. 90:1993;8033-8037.
30. Lever A, Gottlinger H, Haseltine W, Sodroski J. Identification of a sequence required for efficient packaging of human immunodeficiency virus type 1 RNA into virions. J Virol. 63:1989;4085-4087.
31. Aldovini A, Young RA. Mutations of RNA and protein sequences involved in human immunodeficiency virus type 1 packaging result in production of noninfectious virus. J Virol. 64:1990;1920-1926.
32. Luban J, Goff SP. Mutational analysis of cis-acting packaging signals in human immunodeficiency virus type 1 RNA. J Virol. 68:1994;3784-3793.
33. Berkowitz RD, Hammarskjold ML, Helga-Maria C, Rekosh D, Goff SP. 5′ regions of HIV-1 RNAs are not sufficient for encapsidation: implications for the HIV-1 packaging signal. Virol. 212:1995;718-723.
34. Kaye JF, Richardson JH, Lever AML. Cis-acting sequences involved in human immunodeficiency virus type 1 RNA packaging. J Virol. 69:1995;6588-6592.
35. McBride MS, Panganiban A. The human immunodeficiency virus type 1 encapsidation site is a multipartite RNA element composed of functional hairpin structures. J Virol. 70:1996;2963-2973.
36. McBribe MS, Panganiban A. Position dependence of functional hairpins important for human immunodeficiency virus type 1 RNA encapsidation in vivo. J Virol. 71:1997;20050-20058.
37. McBride MS, Schwartz MD, Panganiban A. Efficient encapsidation of human immunodeficiency virus type 1 vectors and further characterization of cis elements required for encapsidation. J Virol. 71:1997;4544-4554.
38. De Guzman RN, Rong Wu Z, Stalling CC, Pappalardo L, Borer PN, Summers MF. Structure of the HIV-1 nucleocapsid protein bound to the SL3 Y-RNA recognition element. Science. 279:1998;384-388.
39. + T lymphocytes. J Virol. 66:1992;6489-6495.
40. von Schwedler U, Song J, Aiken C, Trono D. Vif is crucial for immunodeficiency virus type 1 proviral DNA synthesis is infected cells. J Virol. 67:1993;4945-4955.
41. Klimkait T, Strebel K, Hoggan MD, Martin MA, Orenstein JM. The human immunodeficiency virus type 1-specific protein vpu is required for efficient virus maturation and release. J Virol. 64:1990;621-629.
42. Gottlinger HG, Dorfman T, Cohen E, Haseltine WA. Vpu protein of immunodeficiency virus type 1 enhances the release of capsids produced by gag gene constructs of widely divergent retroviruses. Proc Natl Acad Sci USA. 90:1993;7381-7385.
43. Garcia JV, Miller AD. Serine phosphorylation independent downregulation of cell-surface CD4 by net. Nature. 350:1991;508-551.
44. Miller MD, Warmerdam MT, Gaston I, Greene WC, Feinberg MB. The human immunodeficiency virus type 1 nef gene product: a positive factor for viral infection and replication in primary lymphocytes and macrophages. J Exp Med. 179:1994;101-113.
45. Aiken C. Pseudotyping human immunodeficiency virus type 1 (HIV-1) by the glycoprotein of vesicular stomatitis virus targets HIV-1 energy to an endocytic pathway and suppresses both the requirement for Nef and the sensitivity to cyclosporin A. J Virol. 71:1997;5871-5877.
46. Levy DN, Fernandes LS, Williams WV, Weiner DB. Induction of cell differentiation by human immunodeficiency virus 1 vpr. Cell. 72:1993;541-550.
47. 2 accumulation by a mechanism which differs from DNA damage checkpoint control. J Virol. 70:1996;2324-2331.
48. Goh WC, Rogel ME, Kinsey CM, Michael SF, Fultz PN, Nowak MA, Hahn BH, Emerman M. HIV-1 Vpr increases viral expression by manipulation of the cell cycle: a mechanism for selection of Vpr in vivo. Nat Med. 4:1998;65-71.
49. Desrosiers RC, Lifson JD, Gibbs JS, Czajak SC, Howe AYM, Arthur LO, Johnson RP. Identification of highly attenuated mutants of simian immunodeficiency virus. J Virol. 72:1998;1431-1437.
50. Lang SM, Weeger M, Strahl-Henning C, Coulibaly C, Hunsmann G, Muller J, Muller-Hermalink H, Fuchs D, Wachter H, Daniel MM, et al. Importance of vpr for infection of rhesus monkey with simian immuunodeficiency virus. J Virol. 67:1993;902-912.
51. Aldrovandi GM, Zack JA. Replication and pathogenicity of HIV type 1 accessory gene mutants in SCID-hu mice. J Virol. 70:1996;1505-1507.
52. Kirchhoff F, Greenough TC, Brettler DB, Sullivan JL, Desrosiers RC. Absence of intact nef sequences in a long-term survivor with nonprogressive HIV-1 infection. N Engl J Med. 332:1995;228-232.
53. Deacon NJ, Tsykin A, Solomon A, Smith K, Ludford-Menting M, Hooker DJ, McPhee DA, Greenway AL, Ellett A, Chaatfield C, et al. Genomic structure of an attenuated quasi species of HIV-1 from a blood transfusion donor and recipients. Science. 270:1995;988-991.
54. Wang B, Ge YC, Palasanthiran P, Xiang S, Ziegler J, Dwyer DE, Randle C, Dowton D, Cunningham A, Saksena NK. Gene defects clustered at the C-terminus of the vpr gene of HIV-1 in long-term nonprogressing mother and child pair: in vivo evolution of vpr quasispecies in blood and plasma. Virology. 223:1996;224-232.
55. Daniel MD, Kirchhoff F, Czajak SC, Sehgal PK, Desrosiers RC. Protective effect of a live-attenuated SIV vaccine with a deletion in the nef gene. Science. 258:1992;1938-1941.
56. Wyand MS, Manson KH, Lackner AA, Desrosiers RC. Resistance of neonatal monkeys to live attenuated vaccine strains of simian immunodeficiency virus. Nat Med. 3:1997;32-36.
57. Wei P, Garber ME, Fang SM, Fischer WH, Jones KA. A novel CDK9-associated C-type cyclin interacts directly with HIV-1 Tat and mediates its high-affinity, loop-specific binding to TAR RNA. Cell. 92:1998;451-462.
58. Srinivasakumar N, Chazal N, Helga-Maria C, Prasad S, Hammarskjold M, Rekosh D. The effect of viral regulatory protein expression on gene delivery by human immunodeficiency virus type 1 vectors produced in stable packaging cell lines. J Virol. 71:1997;5841-5848.
59. Dull T, Zufferey R, Kelly M, Mandel RJ, Nguyen M, Trono D, Naldini L. A third generation lentiviral vector with a conditional packaging system. J Virol. 1998;. in press.
60. Miyoshi H, Blomer U, Takahashi M, Gage FH, Verma IM. Development of a self-inactivating lentivirus vector. J Virol. 10:1998;. in press.
61. Collins KL, Chen BK, Kalams SA, Walker BD, Baltimore D. HIV-1 Nef protein protects infected primary cells against killing by cytotoxic T lymphocytes. Nature. 391:1998;397-401.
62. Carroll R, Lin JT, Dacquel EJ, Mosca JD, Burke DS, St Louis DC. A human immunodeficiency virus type 1 (HIV-1)-based retroviral vector system utilizing stable HIV-1 packaging cell lines. J Virol. 68:1994;6047-6051.
63. Corbeau P, Kraus G, Wong-Staal F. Transduction of human macrophages using a stable HIV-1/HIV-2-derived gene delivery system. Gene Ther. 5:1998;99-104.
64. Yu H, Rabson AB, Kaul M, Ron Y, Dougherty JP. Inducible human immunodeficiency virus type 1 packaging cell lines. J Virol. 70:1996;4530-4537.
65. Zufferey R, Dull T, Mandel RJ, Bukovsky A, Quiroz D, Naldini L, Trono D. Self-inactivating lentiviral vector for safe and efficient in vivo gene delivery. J Virol. 1998;. in press.
66. Blomer U, Kafri T, Randolph-Moore L, Verma IM, Gage FH. Bcl-xL protects adult septal cholinergic neurons from axotomized cell death. of outstanding interest Proc Natl Acad Sci USA. 95:1998;2603-2608 A single injection of lentiviral vector encoding the human nerve growth factor gene or the chicken anti-apoptotic gene Bcl-xL into the septum spared most neurons from cell death when the fimbria fornix was transected. This is the first reported experimental evidence that local gene delivery by lentiviral vectors in the CNS is adequate to achieve a therapeutic benefit.
67. Korin YD, Zack JA. Progression to the G1b phase of the cell cycle is required for completion of human immunodeficiency virus type 1 reverse transcription in T cells. J Virol. 72:1998;3161-3168.
68. + T cells requires a cyclosporin A-sensitive pathway. J Immunol. 158:1997;512-517.
69. Schuitemaker H, Kootstra NA, Fouchier RAM, Hooibrink B, Miedema F. Productive HIV-1 infection of macrophages restricted to the cell fraction with proliferative capacity. EMBO J. 13:1994;5929-5936.
70. + cells with a human immunodeficiency virus type 1-based retroviral vector pseudotyped with vesicular stomatitis virus envelope glycoprotein G. J Virol. 70:1996;2581-2585.
71. Weiss RA. Transgenic pigs and virus adaptation. Nature. 391:1998;327-328.