RNAi-mediated CCR5 knockdown provides HIV-1 resistance to memory T cells in humanized BLT mice

Molecular Therapy Nucleic Acids

Volumn 4, Issue 2, 2015, Pages

  Shimizu, Saki ^a,b   Ringpis, Gene Errol ^a,b   Marsden, Matthew D ^a   Cortado, Ruth V ^a,b   Wilhalme, Holly M ^a   Elashoff, David ^a   Zack, Jerome A ^a,b   Chen, Irvin S Y ^a,b   Sung An, Dong ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

CCR5; Hematopoietic stem cells; HIV 1 Gene Therapy; Humanized mouse; shRNA

Indexed keywords

ANTIGEN P24; ANTIVIRUS AGENT; CHEMOKINE RECEPTOR CCR5; SHORT HAIRPIN RNA; SHORT HAIRPIN RNA 1005; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIVIRAL RESISTANCE; ARTICLE; BONE MARROW; CD4 CD8 RATIO; CD4+ T LYMPHOCYTE; CELL STIMULATION; CONTROLLED STUDY; DNA MODIFICATION; DOWN REGULATION; GENE SILENCING; HEMATOPOIETIC STEM CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VIVO STUDY; LIVER; LYMPHOID TISSUE; MEMORY T LYMPHOCYTE; MOUSE; NONHUMAN; PRIORITY JOURNAL; RNA INTERFERENCE; SPLEEN CELL; THYMUS; VIRAL GENE DELIVERY SYSTEM;

EID: 84927724234     PISSN: None     EISSN: 21622531     Source Type: Journal    
DOI: 10.1038/mtna.2015.3     Document Type: Article

References (49)

1. Kiem, HP, Jerome, KR, Deeks, SG and McCune, JM (2012). Hematopoietic-stemcell-based gene therapy for HIV disease. Cell Stem Cell 10: 137-147.
2. Kitchen, SG, Shimizu, S and An, DS (2011). Stem cell-based anti-HIV gene therapy. Virology 411: 260-272.
3. Hoxie, JA, June, CH (2012). Novel cell and gene therapies for HIV. Cold Spring Harb Perspect Med 2(10). doi:10.1101/cshperspect.a007179.
4. Baltimore, D (1988). Gene therapy. Intracellular immunization. Nature 335: 395-396.
5. Anderson, JS and Bauer, G (2012). Fighting HIV with stem cell therapy: one step closer to human trials? Expert Rev Anti Infect Ther 10: 1071-1073.
6. Rossi, JJ, June, CH and Kohn, DB (2007). Genetic therapies against HIV. Nat Biotechnol 25: 1444-1454.
7. Burnett, JC, Zaia, JA and Rossi, JJ (2012). Creating genetic resistance to HIV. Curr Opin Immunol 24: 625-632.
8. Hütter, G, Nowak, D, Mossner, M, Ganepola, S, Müssig, A, Allers, K et al. (2009). Longterm control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 360: 692-698.
9. 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.
10. Huang, Y, Paxton, WA, Wolinsky, SM, Neumann, AU, Zhang, L, He, T et al. (1996). The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med 2: 1240-1243.
11. Samson, M, Libert, F, Doranz, BJ, Rucker, J, Liesnard, C, Farber, CM et al. (1996). Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 382: 722-725.
12. Liu, R, Paxton, WA, Choe, S, Ceradini, D, Martin, SR, Horuk, R et al. (1996). Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 86: 367-377.
13. Dean, M, Carrington, M, Winkler, C, Huttley, GA, Smith, MW, Allikmets, R et al. (1996). Genetic restriction of HIV-1 infection and progression to AIDS by a deletion allele of the CKR5 structural gene. Hemophilia Growth and Development Study, Multicenter AIDS Cohort Study, Multicenter Hemophilia Cohort Study, San Francisco City Cohort, ALIVE Study. Science 273: 1856-1862.
14. Bai, J, Gorantla, S, Banda, N, Cagnon, L, Rossi, J and Akkina, R (2000). Characterization of anti-CCR5 ribozyme-transduced CD34+ hematopoietic progenitor cells in vitro and in a SCID-hu mouse model in vivo. Mol Ther 1: 244-254.
15. Feng, Y, Leavitt, M, Tritz, R, Duarte, E, Kang, D, Mamounas, M et al. (2000). Inhibition of CCR5-dependent HIV-1 infection by hairpin ribozyme gene therapy against CC-chemokine receptor 5. Virology 276: 271-278.
16. An, DS, Donahue, RE, Kamata, M, Poon, B, Metzger, M, Mao, SH et al. (2007). Stable reduction of CCR5 by RNAi through hematopoietic stem cell transplant in non-human primates. Proc Natl Acad Sci USA 104: 13110-13115.
17. Steinberger, P, Andris-Widhopf, J, Bühler, B, Torbett, BE and Barbas, CF 3rd (2000). Functional deletion of the CCR5 receptor by intracellular immunization produces cells that are refractory to CCR5-dependent HIV-1 infection and cell fusion. Proc Natl Acad Sci USA 97: 805-810.
18. Miller, JC, Tan, S, Qiao, G, Barlow, KA, Wang, J, Xia, DF et al. (2011). A TALE nuclease architecture for efficient genome editing. Nat Biotechnol 29: 143-148.
19. Cradick, TJ, Fine, EJ, Antico, CJ and Bao, G (2013). CRISPR/Cas9 systems targeting ß-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 41: 9584-9592.
20. Holt, N, Wang, J, Kim, K, Friedman, G, Wang, X, Taupin, V et al. (2010). Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 28: 839-847.
21. Anderson, JS, Walker, J, Nolta, JA and Bauer, G (2009). Specific transduction of HIVsusceptible cells for CCR5 knockdown and resistance to HIV infection: a novel method for targeted gene therapy and intracellular immunization. J Acquir Immune Defic Syndr 52: 152-161.
22. 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.
23. Shimizu, S, Kamata, M, Kittipongdaja, P, Chen, KN, Kim, S, Pang, S et al. (2009). Characterization of a potent non-cytotoxic shRNA directed to the HIV-1 co-receptor CCR5. Genet Vaccines Ther 7: 8.
24. Shimizu, S, Hong, P, Arumugam, B, Pokomo, L, Boyer, J, Koizumi, N et al. (2010). A highly efficient short hairpin RNA potently down-regulates CCR5 expression in systemic lymphoid organs in the hu-BLT mouse model. Blood 115: 1534-1544.
25. Liang, M, Kamata, M, Chen, KN, Pariente, N, An, DS and Chen, IS (2010). Inhibition of HIV-1 infection by a unique short hairpin RNA to chemokine receptor 5 delivered into macrophages through hematopoietic progenitor cell transduction. J Gene Med 12: 255-265.
26. Tamhane, M and Akkina, R (2008). Stable gene transfer of CCR5 and CXCR4 siRNAs by sleeping beauty transposon system to confer HIV-1 resistance. AIDS Res Ther 5: 16.
27. Qin, XF, An, DS, Chen, IS and Baltimore, D (2003). Inhibiting HIV-1 infection in human T cells by lentiviral-mediated delivery of small interfering RNA against CCR5. Proc Natl Acad Sci USA 100: 183-188.
28. Shirane, D, Sugao, K, Namiki, S, Tanabe, M, Iino, M and Hirose, K (2004). Enzymatic production of RNAi libraries from cDNAs. Nat Genet 36: 190-196.
29. O'Brien, WA, Koyanagi, Y, Namazie, A, Zhao, JQ, Diagne, A, Idler, K et al. (1990). HIV-1 tropism for mononuclear phagocytes can be determined by regions of gp120 outside the CD4-binding domain. Nature 348: 69-73.
30. Adachi, A, Gendelman, HE, Koenig, S, Folks, T, Willey, R, Rabson, A et al. (1986). Production of acquired immunodeficiency syndrome-associated retrovirus in human and nonhuman cells transfected with an infectious molecular clone. J Virol 59: 284-291.
31. Bleul, CC, Wu, L, Hoxie, JA, Springer, TA and Mackay, CR (1997). The HIV coreceptors CXCR4 and CCR5 are differentially expressed and regulated on human T lymphocytes. Proc Natl Acad Sci USA 94: 1925-1930.
32. Oswald-Richter, K, Grill, SM, Leelawong, M, Tseng, M, Kalams, SA, Hulgan, T et al. (2007). Identification of a CCR5-expressing T cell subset that is resistant to R5-tropic HIV infection. PLoS Pathog 3: e58.
33. Yang, X, Jiao, YM, Wang, R, Ji, YX, Zhang, HW, Zhang, YH et al. (2012). High CCR5 density on central memory CD4+ T cells in acute HIV-1 infection is mostly associated with rapid disease progression. PLoS ONE 7: e49526.
34. Ebert, LM and McColl, SR (2002). Up-regulation of CCR5 and CCR6 on distinct subpopulations of antigen-activated CD4+ T lymphocytes. J Immunol 168: 65-72.
35. Riley, JL, Levine, BL, Craighead, N, Francomano, T, Kim, D, Carroll, RG et al. (1998). Naïve and memory CD4 T cells differ in their susceptibilities to human immunodeficiency virus type 1 infection following CD28 costimulation: implicatip6s for transmission and pathogenesis. J Virol 72: 8273-8280.
36. Chun, TW, Finzi, D, Margolick, J, Chadwick, K, Schwartz, D and Siliciano, RF (1995). In vivo fate of HIV-1-infected T cells: quantitative analysis of the transition to stable latency. Nat Med 1: 1284-1290.
37. Finzi, D, Hermankova, M, Pierson, T, Carruth, LM, Buck, C, Chaisson, RE et al. (1997). Identification of a reservoir for HIV-1 in patients on highly active antiretroviral therapy. Science 278: 1295-1300.
38. Wong, JK, Hezareh, M, Günthard, HF, Havlir, DV, Ignacio, CC, Spina, CA et al. (1997). Recovery of replication-competent HIV despite prolonged suppression of plasma viremia. Science 278: 1291-1295.
39. Chun, TW, Stuyver, L, Mizell, SB, Ehler, LA, Mican, JA, Baseler, M et al. (1997). Presence of an inducible HIV-1 latent reservoir during highly active antiretroviral therapy. Proc Natl Acad Sci USA 94: 13193-13197.
40. Marsden, MD, Kovochich, M, Suree, N, Shimizu, S, Mehta, R, Cortado, R et al. (2012). HIV latency in the humanized BLT mouse. J Virol 86: 339-347.
41. Denton, PW, Olesen, R, Choudhary, SK, Archin, NM, Wahl, A, Swanson, MD et al. (2012). Generation of HIV latency in humanized BLT mice. J Virol 86: 630-634.
42. Ho, DD (1995). Time to hit HIV, early and hard. N Engl J Med 333: 450-451.
43. Siliciano, RF and Greene, WC (2011). HIV latency. Cold Spring Harb Perspect Med 1: a007096.
44. Coiras, M, López-Huertas, MR, Pérez-Olmeda, M and Alcamí, J (2009). Understanding HIV-1 latency provides clues for the eradication of long-term reservoirs. Nat Rev Microbiol 7: 798-812.
45. Gabriel, R, Lombardo, A, Arens, A, Miller, JC, Genovese, P, Kaeppel, C et al. (2011). An unbiased genome-wide analysis of zinc-finger nuclease specificity. Nat Biotechnol 29: 816-823.
46. Li, MJ, Bauer, G, Michienzi, A, Yee, JK, Lee, NS, Kim, J et al. (2003). Inhibition of HIV-1 infection by lentiviral vectors expressing Pol III-promoted anti-HIV RNAs. Mol Ther 8: 196-206.
47. 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.
48. Ringpis, GE, Shimizu, S, Arokium, H, Camba-Colón, J, Carroll, MV, Cortado, R et al. (2012). Engineering HIV-1-resistant T-cells from short-hairpin RNA-expressing hematopoietic stem/progenitor cells in humanized BLT mice. PLoS ONE 7: e53492.
49. Melkus, MW, Estes, JD, Padgett-Thomas, A, Gatlin, J, Denton, PW, Othieno, FA et al. (2006). Humanized mice mount specific adaptive and innate immune responses to EBV and TSST-1. Nat Med 12: 1316-1322.