Preclinical in vivo evaluation of the safety of a multi-shRNA-based gene therapy against HIV-1

Molecular Therapy Nucleic Acids

Volumn 2, Issue SEP, 2013, Pages e120-

  Centlivre, Mireille ^a,c   Legrand, Nicolas ^b,d   Klamer, Sofieke ^b   Liu, Ying Poi ^a   Von Eije, Karin Jasmijn ^a   Bohne, Martino ^b   Siteur van Rijnstra, Esther ^b   Weijer, Kees ^b   Blom, Bianca ^b   Voermans, Carlijn ^b   Spits, Hergen ^b   Berkhout, Ben ^a  

^a ACADEMIC MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF AMSTERDAM   (Netherlands)

^c SORBONNE UNIVERSITÉ   (France)

^d Axenis S A S   (France)

Author keywords

Combinational RNA; Gene therapy; HIV 1; Humanized mouse model; RNA interference

Indexed keywords

CAPSID PROTEIN; INTEGRASE; LENTIVIRUS VECTOR; PROTEINASE; REV PROTEIN; SHORT HAIRPIN RNA; TRANSACTIVATOR PROTEIN;

ANIMAL EXPERIMENT; ANTIVIRAL ACTIVITY; ARTICLE; CELL MATURATION; CONTROLLED STUDY; DRUG SAFETY; FRIEDMAN TEST; GENE EXPRESSION; GENE TARGETING; GENE THERAPY; HEMATOPOIESIS; HEMATOPOIETIC STEM CELL; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNE SYSTEM; IN VITRO STUDY; IN VIVO STUDY; MOUSE; NEWBORN; NONHUMAN; OPEN READING FRAME; PRIORITY JOURNAL; RNA INTERFERENCE; VIRAL GENE DELIVERY SYSTEM; VIRUS CAPSID; VIRUS GENOME; VIRUS STRAIN;

EID: 84890379963     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2013.48     Document Type: Article

References (53)

1. Yukl, SA, Shergill, AK, McQuaid, K, Gianella, S, Lampiris, H, Hare, CB et al. (2010). Effect of raltegravir-containing intensification on HIV burden and T-cell activation in multiple gut sites of HIV-positive adults on suppressive antiretroviral therapy. AIDS 24: 2451-2460.
2. Llibre, JM, Buzón, MJ, Massanella, M, Esteve, A, Dahl, V, Puertas, MC et al. (2012). Treatment intensification with raltegravir in subjects with sustained HIV-1 viraemia suppression: a randomized 48-week study. Antivir Ther (Lond) 17: 355-364.
3. Siliciano, JD, Kajdas, J, Finzi, D, Quinn, TC, Chadwick, K, Margolick, JB et al. (2003). Long-term follow-up studies confirm the stability of the latent reservoir for HIV-1 in resting CD4+ T cells. Nat Med 9: 727-728. (Pubitemid 36749221)
4. Hütter, G, Nowak, D, Mossner, M, Ganepola, S, Müssig, A, Alters, K et al. (2009). Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 360: 692-698.
5. Allers, K, Hütter, G, Hofmann, J, Loddenkemper, C, Rieger, K, Thiel, E et al. (2011). Evidence for the cure of HIV infection by CCR5?32/?32 stem cell transplantation. Blood 117: 2791-2799.
6. Berkhout, B (2009). Toward a durable anti-HIV gene therapy based on RNA interference. Ann NY Acad Sci 1175: 3-14.
7. Berkhout, B and ter Brake, O (2009). Towards a durable RNAi gene therapy for HIV-AIDS. Expert Opin Biol Ther 9: 161-170.
8. Burnett, JC, Zaia, JA and Rossi, JJ (2012). Creating genetic resistance to HIV. Curr Opin Immunol 24: 625-632.
9. Fire, A, Xu, S, Montgomery, MK, Kostas, SA, Driver, SE and Mello, CC (1998). Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 391: 806-811. (Pubitemid 28099681)
10. ter Brake, O, Konstantinova, P, Ceylan, M and Berkhout, B (2006). Silencing of HIV-1 with RNA interference: a multiple shRNA approach. Mol Ther 14: 883-892. (Pubitemid 44743127)
11. ter Brake, O, Legrand, N, von Eije, KJ, Centlivre, M, Spits, H, Weijer, K et al. (2009). Evaluation of safety and efficacy of RNAi against HIV-1 in the human immune system (Rag-2(-/-)gammac(-/-)) mouse model. Gene Ther 16: 148-153.
12. Wang, GP, Levine, BL, Binder, GK, Berry, CC, Malani, N, McGarrity, G et al. (2009). Analysis of lentiviral vector integration in HIV+ study subjects receiving autologous infusions of gene modified CD4+ T cells. Mol Ther 17: 844-850.
13. Kumar, P, Ban, HS, Kim, SS, Wu, H, Pearson, T, Greiner, DL et al. (2008). T cell-specific siRNA delivery suppresses HIV-1 infection in humanized mice. Cell 134: 577-586.
14. Anderson, J, Li, MJ, Palmer, B, Remling, L, Li, S, Yam, P et al. (2007). Safety and efficacy of a lentiviral vector containing three anti-HIV genes-CCR5 ribozyme, tat-rev siRNA, and TAR decoy-in SCID-hu mouse-derived T cells. Mol Ther 15: 1182-1188. (Pubitemid 46813622)
15. Legrand, N, Cupedo, T, van Lent, AU, Ebeli, MJ, Weijer, K, Hanke, T et al. (2006). Transient accumulation of human mature thymocytes and regulatory T cells with CD28 superagonist in "human immune system" Rag2(-/-)gammac(-/-) mice. Blood 108: 238-245. (Pubitemid 43990634)
16. Manz, MG (2007). Human-hemato-lymphoid-system mice: opportunities and challenges. Immunity 26: 537-541.
17. Shultz, LD, Ishikawa, F and Greiner, DL (2007). Humanized mice in translational biomedical research. Nat Rev Immunol 7: 118-130. (Pubitemid 46174859)
18. Gimeno, R, Weijer, K, Voordouw, A, Uittenbogaart, CH, Legrand, N, Alves, NL et al. (2004). Monitoring the effect of gene silencing by RNA interference in human CD34+ cells injected into newborn RAG2-/- gammac-/- mice: functional inactivation of p53 in developing T cells. Blood 104: 3886-3893. (Pubitemid 39620134)
19. Traggiai, E, Chicha, L, Mazzucchelli, L, Bronz, L, Piffaretti, JC, Lanzavecchia, A et al. (2004). Development of a human adaptive immune system in cord blood cell-transplanted mice. Science 304: 104-107. (Pubitemid 38451466)
20. Ishikawa, F, Yasukawa, M, Lyons, B, Yoshida, S, Miyamoto, T, Yoshimoto, G et al. (2005). Development of functional human blood and immune systems in NOD/SCID/IL2 receptor {gamma} chain(null) mice. Blood 106: 1565-1573. (Pubitemid 41208567)
21. Denton, PW and Garcia, JV (2011). Humanized mouse models of HIV infection. AIDS Rev 13: 135-148.
22. Berges, BK and Rowan, MR (2011). The utility of the new generation of humanized mice to study HIV-1 infection: transmission, prevention, pathogenesis, and treatment. Retrovirology 8: 65.
23. Sato, K and Koyanagi, Y (2011). The mouse is out of the bag: insights and perspectives on HIV-1-infected humanized mouse models. Exp Biol Med (Maywood) 236: 977-985.
24. Van Duyne, R, Cardenas, J, Easley, R, Wu, W, Kehn-Hall, K, Klase, Z et al. (2008). Effect of transcription peptide inhibitors on HIV-1 replication. Virology 376: 308-322.
25. Denton, PW, Estes, JD, Sun, Z, Othieno, FA, Wei, BL, Wege, AK et al. (2008). Antiretroviral pre-exposure prophylaxis prevents vaginal transmission of HIV-1 in humanized BLT mice. PLoS Med 5: e16.
26. ter Brake, O, 't Hooft, K, Liu, YP, Centlivre, M, von Eije, KJ and Berkhout, B (2008). Lentiviral vector design for multiple shRNA expression and durable HIV-1 inhibition. Mol Ther 16: 557-564. (Pubitemid 351314996)
27. von Eije, KJ, ter Brake, O and Berkhout, B (2009). Stringent testing identifies highly potent and escape-proof anti-HIV short hairpin RNAs. J Gene Med 11: 459-467.
28. von Eije, KJ, ter Brake, O and Berkhout, B (2008). Human immunodeficiency virus type 1 escape is restricted when conserved genome sequences are targeted by RNA interference. J Virol 82: 2895-2903.
29. van Lent, AU, Centlivre, M, Nagasawa, M, Karrich, JJ, Pouw, SM, Weijer, K et al. (2010). In vivo modulation of gene expression by lentiviral transduction in "human immune system" Rag2-/- gamma c -/- mice. Methods Mol Biol 595: 87-115.
30. Knoepfel, S, Centlivre, M, Liu, YP, Boutimah, F and Berkhout, B (2012). Selection of RNAi-based inhibitors for anti-HIV gene therapy. World J Virol 1: 79-90.
31. Eekels, JJ, Pasternak, AO, Schut, AM, Geerts, D, Jeeninga, RE and Berkhout, B (2012). A competitive cell growth assay for the detection of subtle effects of gene transduction on cell proliferation. Gene Ther 19: 1058-1064.
32. O'Neill, HC (1991). Prothymocyte seeding in the thymus. Immunol Lett 27: 1-6; discussion 7.
33. Tan, JB, Visan, I, Yuan, JS and Guidos, CJ (2005). Requirement for Notch1 signals at sequential early stages of intrathymic T cell development. Nat Immunol 6: 671-679. (Pubitemid 41716740)
34. Haddad, R, Guimiot, F, Six, E, Jourquin, F, Setterblad, N, Kahn, E et al. (2006). Dynamics of thymus-colonizing cells during human development. Immunity 24: 217-230. (Pubitemid 43214590)
35. Boudreau, RL, Monteys, AM and Davidson, BL (2008). Minimizing variables among hairpin-based RNAi vectors reveals the potency of shRNAs. RNA 14: 1834-1844.
36. McBride, JL, Boudreau, RL, Harper, SQ, Staber, PD, Monteys, AM, Martins, I et al. (2008). Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: implications for the therapeutic development of RNAi. Proc Natl Acad Sci USA 105: 5868-5873. (Pubitemid 351758464)
37. Castanotto, D, Sakurai, K, Lingeman, R, Li, H, Shively, L, Aagaard, L et al. (2007). Combinatorial delivery of small interfering RNAs reduces RNAi efficacy by selective incorporation into RISC. Nucleic Acids Res 35: 5154-5164. (Pubitemid 47394199)
38. Grimm, D, Streetz, KL, Jopling, CL, Storm, TA, Pandey, K, Davis, CR et al. (2006). Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441: 537-541. (Pubitemid 44050158)
39. Vickers, TA, Lima, WF, Nichols, JG and Crooke, ST (2007). Reduced levels of Ago2 expression result in increased siRNA competition in mammalian cells. Nucleic Acids Res 35: 6598-6610. (Pubitemid 350111625)
40. Kanellopoulou, C, Muljo, SA, Kung, AL, Ganesan, S, Drapkin, R, Jenuwein, T et al. (2005). Dicer-deficient mouse embryonic stem cells are defective in differentiation and centromeric silencing. Genes Dev 19: 489-501. (Pubitemid 40256280)
41. Xiao, C and Rajewsky, K (2009). MicroRNA control in the immune system: basic principles. Cell 136: 26-36.
42. Centlivre, M, Zhou, X, Pouw, SM, Weijer, K, Kleibeuker, W, Das, AT et al. (2010). Autoregulatory lentiviral vectors allow multiple cycles of doxycycline-inducible gene expression in human hematopoietic cells in vivo. Gene Ther 17: 14-25.
43. Walker, JE, Chen, RX, McGee, J, Nacey, C, Pollard, RB, Abedi, M et al. (2012). Generation of an HIV-1-resistant immune system with CD34(+) hematopoietic stem cells transduced with a triple-combination anti-HIV lentiviral vector. J Virol 86: 5719-5729.
44. Ringpis, GE, Shimizu, S, Arokium, H, Camba-Colón, J, Carroll, MV, Cortado, R et al. (2012). Engineering HIV-1-resistantT-cellsfrom short-hairpin RNA-expressing hematopoietic stem/progenitor cells in humanized BLT mice. PLoS ONE 7: e53492.
45. DiGiusto, DL, Krishnan, A, Li, L, Li, H, Li, S, Rao, A et al. (2010). RNA-based gene therapy for HIV with lentiviral vector-modified CD34(+) cells in patients undergoing transplantation for AIDS-related lymphoma. Sci Transl Med 2: 36ra43.
46. Burnett, JC, Rossi, JJ and Tiemann, K (2011). Current progress of siRNA/shRNA therapeutics in clinical trials. Biotechnol J 6: 1130-1146.
47. Legrand, N, Huntington, ND, Nagasawa, M, Bakker, AQ, Schotte, R, Strick-Marchand, H et al. (2011). Functional CD47/signal regulatory protein alpha (SIRP(alpha)) interaction is required for optimal human T- and natural killer- (NK) cell homeostasis in vivo. Proc Natl Acad Sci USA 108: 13224-13229.
48. Dull, T, Zufferey, R, Kelly, M, Mandel, RJ, Nguyen, M, Trono, D eta l. (1998). A third-generation lentivirus vector with a conditional packaging system. J Virol 72: 8463-8471. (Pubitemid 28471781)
49. Seppen, J, Rijnberg, M, Cooreman, MP and Oude Elferink, RP (2002). Lentiviral vectors for efficient transduction of isolated primary quiescent hepatocytes. J Hepatol 36: 459-465. (Pubitemid 34407332)
50. Weijer, K, Uittenbogaart, CH, Voordouw, A, Couwenberg, F, Seppen, J, Blom, B et al. (2002). Intrathymic and extrathymic development of human plasmacytoid dendritic cell precursors in vivo. Blood 99: 2752-2759. (Pubitemid 34525362)
51. Shultz, LD, Lyons, BL, Burzenski, LM, Gott, B, Chen, X, Chaleff, S et al. (2005). Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 174: 6477-6489. (Pubitemid 40663843)
52. Takenaka, K, Prasolava, TK, Wang, JC, Mortin-Toth, SM, Khalouei, S, Gan, OI et al. (2007). Polymorphism in Sirpa modulates engraftment of human hematopoietic stem cells. Nat Immunol 8: 1313-1323. (Pubitemid 350138972)
53. Oldenborg, PA, Zheleznyak, A, Fang, YF, Lagenaur, CF, Gresham, HD and Lindberg, FP (2000). Role of CD47 as a marker of self on red blood cells. Science 288: 2051-2054. (Pubitemid 30397687)