In vivo administration of lentiviral vectors triggers a type I interferon response that restricts hepatocyte gene transfer and promotes vector clearance

Blood

Volumn 109, Issue 7, 2007, Pages 2797-2805

  Brown, Brian D ^a   Sitia, Giovanni ^b   Annoni, Andrea ^a   Hauben, Ehud ^a   Sergi, Lucia Sergi ^a   Zingale, Anna ^a   Roncarolo, Maria Grazia ^a,c   Guidotti, Luca G ^b,d   Naldini, Luigi ^a,c  

^a SAN RAFFAELE SCIENTIFIC INSTITUTE   (Italy)

^b SAN RAFFAELE HOSPITAL   (Italy)

^c VITA SALUTE SAN RAFFAELE UNIVERSITY   (Italy)

^d SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA INTERFERON; ANTIVIRUS AGENT; BETA INTERFERON; INTERFERON; LENTIVIRUS VECTOR;

ARTICLE; CONTROLLED STUDY; DENDRITIC CELL; DRUG EFFECT; GENE DELIVERY SYSTEM; GENE EXPRESSION; GENE TRANSFER; IN VIVO STUDY; LENTIVIRINAE; LIVER CELL; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL;

EID: 33947583453     PISSN: 00064971     EISSN: 00064971     Source Type: Journal    
DOI: 10.1182/blood-2006-10-049312     Document Type: Article

References (48)

1. Brown BD, Venneri MA, Zingale A, Sergi LS, Naldini L. Endogenous microRNA regulation suppresses transgene expression in hematopoietic lineages and enables stable gene transfer. Nat Med. 2006;12:585-591.
2. Di Domenico C, Villani GR, Di Napoli D, et al. Gene therapy for a mucopolysaccharidosis type I murine model with lentiviral-IDUA vector. Hum Gene Ther. 2005;16:81-90.
3. Follenzi A, Battaglia M, Lombardo A, Annoni A, Roncarolo MG, Naldini L. Targeting lentiviral vector expression to hepatocytes limits transgene-specific immune response and establishes long-term expression of human antihemophilic factor IX in mice. Blood. 2004;103:3700-3709.
4. Park F, Ohashi K, Kay MA. Therapeutic levels of human factor VIII and IX using HIV-1-based lentiviral vectors in mouse liver. Blood. 2000;96:1173-1176.
5. van der Wegen P, Louwen R, Imam AM, et al. Successful treatment of UGT1A1 deficiency in a rat model of Crigler-Najjar disease by intravenous administration of a liver-specific lentiviral vector. Mol Ther. 2006;13:374-381.
6. van Til NP, Markusic DM, van der Rijt R, et al. Kupffer cells and not liver sinusoidal endothelial cells prevent lentiviral transduction of hepatocytes. Mol Ther. 2005;11:26-34.
7. Beignon AS, McKenna K, Skoberne M, et al. Endocytosis of HIV-1 activates plasmacytoid dendritic cells via Toll-like receptor-viral RNA interactions. J Clin Invest. 2005;115:3265-3275.
8. Fonteneau JF, Larsson M, Beignon AS, et al. Human immunodeficiency virus type 1 activates plasmacytoid dendritic cells and concomitantly induces the bystander maturation of myeloid dendritic cells. J Virol. 2004;78:5223-5232.
9. Kadowaki N, Antonenko S, Lau JY, Liu YJ. Natural interferon alpha/beta-producing cells link innate and adaptive immunity. J Exp Med. 2000;192:219-226.
10. De Palma M, Naldini L. Transduction of a gene expression cassette using advanced generation lentiviral vectors. Methods Enzymol. 2002;346:514-529.
11. Hobbs MV, Weigle WO, Noonan DJ, et al. Patterns of cytokine gene expression by CD4+ T cells from young and old mice. J Immunol. 1993;150:3602-3614.
12. McClary H, Koch R, Chisari FV, Guidotti LG. Inhibition of hepatitis B virus replication during schistosoma mansoni infection in transgenic mice. J Exp Med. 2000;192:289-294.
13. De Palma M, Venneri MA, Roca C, Naldini L. Targeting exogenous genes to tumor angiogenesis by transplantation of genetically modified hematopoietic stem cells. Nat Med. 2003;9:789-795.
14. Miyahira Y, Murata K, Rodriguez D, et al. Quantification of antigen specific CD8+ T cells using an ELISPOT assay. J Immunol Methods. 1995;181:45-54.
15. Butler SL, Hansen MS, Bushman FD. A quantitative assay for HIV DNA integration in vivo. Nat Med. 2001;7:631-634.
16. Guidotti LG, Chisari FV. Noncytolytic control of viral infections by the innate and adaptive immune response. Annu Rev Immunol. 2001;19:65-91.
17. Naldini L, Blomer U, Gallay P, et al. In vivo gene delivery and stable transduction of nondividing cells by a lentiviral vector. Science. 1996;272:263-267.
18. VandenDriessche T, Thorrez L, Naldini L, et al. Lentiviral vectors containing the human immunodeficiency virus type-1 central polypurine tract can efficiently transduce nondividing hepatocytes and antigen-presenting cells in vivo. Blood. 2002;100:813-822.
19. Kang Y, Xie L, Tran DT, et al. Persistent expression of factor VIII in vivo following nonprimate lentiviral gene transfer. Blood. 2005;106:1552-1558.
20. Schauber CA, Tuerk MJ, Pacheco CD, Escarpe PA, Veres G. Lentiviral vectors pseudotyped with baculovirus gp64 efficiently transduce mouse cells in vivo and show tropism restriction against hematopoietic cell types in vitro. Gene Ther. 2004;11:266-275.
21. Liu YJ. IPC: professional type 1 interferon-producing cells and plasmacytoid dendritic cell precursors. Annu Rev Immunol. 2005;23:275-306.
22. Smed-Sorensen A, Lore K, Vasudevan J, et al. Differential susceptibility to human immunodeficiency virus type 1 infection of myeloid and plasmacytoid dendritic cells. J Virol. 2005;79:8861-8869.
23. Stark GR, Kerr IM, Williams BR, Silverman RH, Schreiber RD. How cells respond to interferons. Annu Rev Biochem. 1998;67:227-264.
24. Montoya M, Schiavoni G, Mattei F, et al. Type I interferons produced by dendritic cells promote their phenotypic and functional activation. Blood. 2002;99:3263-3271.
25. Tan PH, Beutelspacher SC, Xue SA, et al. Modulation of human dendritic-cell function following transduction with viral vectors: implications for gene therapy. Blood. 2005;105:3824-3832.
26. Janeway CA, Jr, Medzhitov R. Innate immune recognition. Annu Rev Immunol. 2002;20:197-216.
27. Hemmi H, Takeuchi O, Kawai T, et al. A Toll-like receptor recognizes bacterial DNA. Nature. 2000;408:740-745.
28. Diebold SS, Kaisho T, Hemmi H, Akira S, Reis e Sousa C. Innate antiviral responses by means of TLR7-mediated recognition of single-stranded RNA. Science. 2004;303:1529-1531.
29. Heil F, Hemmi H, Hochrein H, et al. Species-specific recognition of single-stranded RNA via toll-like receptor 7 and 8. Science. 2004;303:1526-1529.
30. Yoneyama M, Kikuchi M, Natsukawa T, et al. The RNA helicase RIG-I has an essential function in double-stranded RNA-induced innate antiviral responses. Nat Immunol. 2004;5:730-737.
31. Stetson DB, Medzhitov R. Recognition of cytosolic DNA activates an IRF3-dependent innate immune response. Immunity. 2006;24:93-103.
32. Ishii KJ, Coban C, Kato H, et al. A Toll-like receptor-independent antiviral response induced by double-stranded B-form DNA. Nat Immunol. 2006;7:40-48.
33. Zhang H, Dornadula G, Pomerantz RJ. Endogenous reverse transcription of human immunodeficiency virus type 1 in physiological microenviroments: an important stage for viral infection of nondividing cells. J Virol. 1996;70:2809-2824.
34. Brunner KT, Hurez D, McCluskey RT, Benacerraf B. Blood clearance of P32-labeled vesicular stomatitis and Newcastle disease viruses by the reticuloendothelial system in mice. J Immunol. 1960;85:99-105.
35. Shirazi Y, Pitha PM. Interferon alpha-mediated inhibition of human immunodeficiency virus type 1 provirus synthesis in T-cells. Virology. 1993;193:303-312.
36. Meylan PR, Guatelli JC, Munis JR, Richman DD, Kornbluth RS. Mechanisms for the inhibition of HIV replication by interferons-alpha, -beta, and -gamma in primary human macrophages. Virology. 1993;193:138-148.
37. Shirazi Y, Pitha PM. Alpha interferon inhibits early stages of the human immunodeficiency virus type 1 replication cycle. J Virol. 1992;66:1321-1328.
38. Peng G, Lei KJ, Jin W, Greenwell-Wild T, Wahl SM. Induction of APOBEC3 family proteins, a defensive maneuver underlying interferon-induced anti-HIV-1 activity. J Exp Med. 2006;203:41-46.
39. Asaoka K, Ikeda K, Hishinuma T, Horie-Inoue K, Takeda S, Inoue S. A retrovirus restriction factor TRIM5alpha is transcriptionally regulated by interferons. Biochem Biophys Res Commun. 2005;338:1950-1956.
40. Hensley SE, Giles-Davis W, McCoy KC, Weninger W, Ertl HC. Dendritic cell maturation, but not CD8+ T cell induction, is dependent on type I IFN signaling during vaccination with adenovirus vectors. J Immunol. 2005;175:6032-6041.
41. Ou R, Zhou S, Huang L, Moskophidis D. Critical role for alpha/beta and gamma interferons in persistence of lymphocytic choriomeningitis virus by clonal exhaustion of cytotoxic T cells. J Virol. 2001;75:8407-8423.
42. Price GE, Gaszewska-Mastarlarz A, Moskophidis D. The role of alpha/beta and gamma interferons in development of immunity to influenza A virus in mice. J Virol. 2000;74:3996-4003.
43. Marrack P, Kappler J, Mitchell T. Type I interferons keep activated T cells alive. J Exp Med. 1999;189:521-530.
44. Kolumam GA, Thomas S, Thompson LJ, Sprent J, Murali-Krishna K. Type I interferons act directly on CD8 T cells to allow clonal expansion and memory formation in response to viral infection. J Exp Med. 2005;202:637-650.
45. Curtsinger JM, Valenzuela JO, Agarwal P, Lins D, Mescher MF. Type I IFNs provide a third signal to CD8 T cells to stimulate clonal expansion and differentiation. J Immunol. 2005;174:4465-4469.
46. Mescher MF, Curtsinger JM, Agarwal P, et al. Signals required for programming effector and memory development by CD8+ T cells. Immunol Rev. 2006;211:81-92.
47. Zinkernagel RM. Localization dose and time of antigens determine immune reactivity. Semin Immunol. 2000;12:163-171.
48. Moskophidis D, Lechner F, Pircher H, Zinkernagel RM. Virus persistence in acutely infected immunocompetent mice by exhaustion of antiviral cytotoxic effector T cells. Nature. 1993;362:758-761.