Inhibition of HIV-1 infection of primary CD4+ T-cells by gene editing of CCR5 using adenovirus-delivered CRISPR/Cas9

Journal of General Virology

Volumn 96, Issue 8, 2015, Pages 2381-2393

  Li, Chang ^a,b   Guan, Xinmeng ^a,b   Du, Tao ^a   Jin, Wei ^a,b   Wu, Biao ^c   Liu, Yalan ^a   Wang, Ping ^a,b   Hu, Bodan ^a,b   Griffin, George E ^d   Shattock, Robin J ^e   Hu, Qinxue ^a,d  

^a WUHAN INSTITUTE OF VIROLOGY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c WUHAN NO 1 HOSPITAL   (China)

^d ST GEORGE'S UNIVERSITY OF LONDON   (United Kingdom)

^e IMPERIAL COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOVIRUS VECTOR; CAS9 ENDONUCLEASE; CHEMOKINE RECEPTOR CCR5; CHIMERIC PROTEIN; CRISPR ASSOCIATED PROTEIN; ENDONUCLEASE; UNCLASSIFIED DRUG; CCR5 PROTEIN, HUMAN;

AMPLICON; ARTICLE; BINDING AFFINITY; CD4+ T LYMPHOCYTE; CELL SURFACE; CHROMATIN IMMUNOPRECIPITATION; CRISPR CAS SYSTEM; GENE LOCUS; GENOME SIZE; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; IN VIVO STUDY; NEXT GENERATION SEQUENCING; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS RESISTANCE; ADENOVIRIDAE; ANIMAL; CELL LINE; GENE VECTOR; GENETICS; HIGH THROUGHPUT SEQUENCING; HUMAN; HUMAN IMMUNODEFICIENCY VIRUS INFECTION; IMMUNOLOGY; METABOLISM; PHYSIOLOGY; VIROLOGY;

ADENOVIRIDAE; HUMAN IMMUNODEFICIENCY VIRUS 1; MAMMALIA; PROKARYOTA;

ADENOVIRIDAE; ANIMALS; CD4-POSITIVE T-LYMPHOCYTES; CELL LINE; CRISPR-CAS SYSTEMS; GENETIC VECTORS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV INFECTIONS; HIV-1; HUMANS; RECEPTORS, CCR5;

EID: 84940203001     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.000139     Document Type: Article

References (74)

1. Alkhatib, G., Combadiere, C., Broder, C. C., Feng, Y., Kennedy, P. E., Murphy, P. M. & Berger, E. A. (1996). CC CKR5: a RANTES, MIP-1alpha, MIP-1beta receptor as a fusion cofactor for macrophage-tropic HIV-1. Science 272, 1955-1958.
2. Badia, R., Riveira-Muñoz, E., Clotet, B., Esté, J. A. & Ballana, E. (2014). Gene editing using a zinc-finger nuclease mimicking the CCR5D32 mutation induces resistance to CCR5-using HIV-1. J Antimicrob Chemother 69, 1755-1759.
3. Bett, A. J., Haddara, W., Prevec, L. & Graham, F. L. (1994). An efficient and flexible system for construction of adenovirus vectors with insertions or deletions in early regions 1 and 3. Proc Natl Acad Sci USA 91,8802-8806.
4. Boch, J., Scholze, H., Schornack, S., Landgraf, A., Hahn, S., Kay, S., Lahaye, T., Nickstadt, A. & Bonas, U. (2009). Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326, 1509-1512.
5. Centers for Disease Control (CDC) (1981). Pneumocystis pneumonia—Los Angeles. MMWR Morb Mortal Wkly Rep 30, 250-252
6. Cheng, A. W., Wang, H., Yang, H., Shi, L., Katz, Y., Theunissen, T. W., Rangarajan, S., Shivalila, C. S., Dadon, D. B. & Jaenisch, R. (2013). Multiplexed activation of endogenous genes by CRISPR-on, an RNA-guided transcriptional activator system. Cell Res 23, 1163-1171
7. Cheng, R., Peng, J., Yan, Y., Cao, P., Wang, J., Qiu, C., Tang, L., Liu, D., Tang, L. & other authors (2014). Efficient gene editing in adult mouse livers via adenoviral delivery of CRISPR/Cas9. FEBS Lett 588, 3954-3958
8. Chun, T. W., Nickle, D. C., Justement, J. S., Meyers, J. H., Roby, G., Hallahan, C. W., Kottilil, S., Moir, S., Mican, J. M. & other authors (2008). Persistence of HIV in gut-associated lymphoid tissue despite long-term antiretroviral therapy. J Infect Dis 197, 714-720.
9. Cong, L., Ran, F. A., Cox, D., Lin, S., Barretto, R., Habib, N., Hsu, P. D., Wu, X., Jiang, W. & other authors (2013). Multiplex genome engineering using CRISPR/Cas systems. Science 339, 819-823.
10. Corbeau, P. & Reynes, J. (2011). Immune reconstitution under antiretroviral therapy: the new challenge in HIV-1 infection. Blood 117, 5582-5590
11. Cradick, T. J., Fine, E. J., Antico, C. J. & Bao, G. (2013). CRISPR/Cas9 systems targeting b-globin and CCR5 genes have substantial off-target activity. Nucleic Acids Res 41, 9584-9592.
12. DiGiusto, D. L., Stan, R., Krishnan, A., Li, H., Rossi, J. J. & Zaia, J. A. (2013). Development of hematopoietic stem cell based gene therapy for HIV-1 infection: considerations for proof of concept studies and translation to standard medical practice. Viruses 5, 2898-2919.
13. Doench, J. G., Hartenian, E., Graham, D. B., Tothova, Z., Hegde, M., Smith, I., Sullender, M., Ebert, B. L., Xavier, R. J. & Root, D. E. (2014). Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat Biotechnol 32, 1262-1267.
14. Duan, J., Lu, G., Xie, Z., Lou, M., Luo, J., Guo, L. & Zhang, Y. (2014). Genome-wide identification of CRISPR/Cas9 off-targets in human genome. Cell Res 24, 1009-1012.
15. Ebina, H., Misawa, N., Kanemura, Y. & Koyanagi, Y. (2013). Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus. Sci Rep 3, 2510
16. Fatkenheuer, G., Nelson, M., Lazzarin, A., Konourina, I., Hoepelman, A. I., Lampiris, H., Hirschel, B., Tebas, P., Raffi, F. & other authors (2008). Subgroup analyses of maraviroc in previously treated R5 HIV-1 infection. N Engl J Med 359, 1442-1455.
17. Gaggar, A., Shayakhmetov, D. M. & Lieber, A. (2003). CD46 is a cellular receptor for group B adenoviruses. Nat Med 9, 1408-1412
18. Gilbert, L. A., Horlbeck, M. A., Adamson, B., Villalta, J. E., Chen, Y., Whitehead, E. H., Guimaraes, C., Panning, B., Ploegh, H. L. & other authors (2014). Genome-scale CRISPR-mediated control of gene repression and activation. Cell 159, 647-661.
19. Guilinger, J. P., Thompson, D. B. & Liu, D. R. (2014). Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 32, 577-582.
20. Herrera-Carrillo, E. & Berkhout, B. (2015). Potential mechanisms for cell-based gene therapy to treat HIV/AIDS. Expert Opin Ther Targets 19, 245-263
21. Holt, N., Wang, J., Kim, K., Friedman, G., Wang, X., Taupin, V., Crooks, G. M., Kohn, D. B., Gregory, P. D. & other authors (2010). Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 28, 839-847.
22. Hsu, P. D., Scott, D. A., Weinstein, J. A., Ran, F. A., Konermann, S., Agarwala, V., Li, Y., Fine, E. J., Wu, X. & other authors (2013). DNA targeting specificity of RNA-guided Cas9 nucleases. Nat Biotechnol 31, 827-832.
23. Hu, Q., Napier, K. B., Trent, J. O., Wang, Z., Taylor, S., Griffin, G. E., Peiper, S. C. & Shattock, R. J. (2005). Restricted variable residues in the C-terminal segment of HIV-1 V3 loop regulate the molecular anatomy of CCR5 utilization. J Mol Biol 350, 699-712.
24. Hu, W., Kaminski, R., Yang, F., Zhang, Y., Cosentino, L., Li, F., Luo, B., Alvarez-Carbonell, D., Garcia-Mesa, Y. & other authors (2014). RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection. Proc Natl Acad Sci U S A 111, 11461-11466
25. Huang, Y., Paxton, W. A., Wolinsky, S. M., Neumann, A. U., Zhang, L., He, T., Kang, S., Ceradini, D., Jin, Z. & other authors (1996). The role of a mutant CCR5 allele in HIV-1 transmission and disease progression. Nat Med 2, 1240-1243.
26. Hutter, G., Nowak, D., Mossner, M., Ganepola, S., Mußig, A., Allers, K., Schneider, T., Hofmann, J., Kucherer, C. & other authors (2009). Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 360, 692-698.
27. Jin, W., Li, C., Du, T., Hu, K., Huang, X. & Hu, Q. (2014). DC-SIGN plays a stronger role than DCIR in mediating HIV-1 capture and transfer. Virology 458-459, 83-92.
28. Keele, B. F., Giorgi, E. E., Salazar-Gonzalez, J. F., Decker, J. M., Pham, K. T., Salazar, M. G., Sun, C., Grayson, T., Wang, S. & other authors (2008). Identification and characterization of transmitted and early founder virus envelopes in primary HIV-1 infection. Proc Natl Acad Sci U S A 105, 7552-7557.
29. Kennedy, E. M., Kornepati, A. V., Goldstein, M., Bogerd, H. P., Poling, B. C., Whisnant, A. W., Kastan, M. B. & Cullen, B. R. (2014). Inactivation of the human papillomavirus E6 or E7 gene in cervical carcinoma cells by using a bacterial CRISPR/Cas RNA-guided endonuclease. J Virol 88, 11965-11972.
30. Kent, S. J., Reece, J. C., Petravic, J., Martyushev, A., Kramski, M., De Rose, R., Cooper, D. A., Kelleher, A. D., Emery, S. & other authors (2013). The search for an HIV cure: tackling latent infection. Lancet Infect Dis 13, 614-621.
31. Kim, H. & Kim, J. S. (2014). A guide to genome engineering with programmable nucleases. Nat Rev Genet 15, 321-334.
32. Kootstra, N. A. & Verma, I. M. (2003). Gene therapy with viral vectors. Annu Rev Pharmacol Toxicol 43, 413-439.
33. Kordelas, L., Verheyen, J., Beelen, D. W., Horn, P. A., Heinold, A., Kaiser, R., Trenschel, R., Schadendorf, D., Dittmer, U. & Esser, S. (2014). Shift of HIV tropism in stemcell transplantation with CCR5 Delta32 mutation. N Engl J Med 371, 880-882.
34. Kuscu, C., Arslan, S., Singh, R., Thorpe, J. & Adli, M. (2014). Genome-wide analysis reveals characteristics of off-target sites bound by the Cas9 endonuclease. Nat Biotechnol 32, 677-683.
35. Lewin, S. R. (2013). A cure for HIV: where we’ve been, and where we’re headed. Lancet 381, 2057-2058.
36. Lin, S. R., Yang, H. C., Kuo, Y. T., Liu, C. J., Yang, T. Y., Sung, K. C., Lin, Y. Y., Wang, H. Y., Wang, C. C. & other authors (2014a). The CRISPR/ Cas9 system facilitates clearance of the intrahepatic HBV templates in vivo. Mol Ther Nucleic Acids 3, e186.
37. Lin, Y., Cradick, T. J., Brown, M. T., Deshmukh, H., Ranjan, P., Sarode, N., Wile, B. M., Vertino, P. M., Stewart, F. J. & Bao, G. (2014b). CRISPR/Cas9 systems have off-target activity with insertions or deletions between target DNA and guide RNA sequences. Nucleic Acids Res 42, 7473-7485.
38. Luo, J., Deng, Z. L., Luo, X., Tang, N., Song, W. X., Chen, J., Sharff, K. A., Luu, H. H., Haydon, R. C. & other authors (2007). A protocol for rapid generation of recombinant adenoviruses using the AdEasy system. Nat Protoc 2, 1236-1247.
39. Maggio, I., Holkers, M., Liu, J., Janssen, J. M., Chen, X. & Gonçalves, M. A. (2014). Adenoviral vector delivery of RNA-guided CRISPR/Cas9 nuclease complexes induces targeted mutagenesis in a diverse array of human cells. Sci Rep 4, 5105
40. Mak, A. N., Bradley, P., Cernadas, R. A., Bogdanove, A. J. & Stoddard, B. L. (2012). The crystal structure of TAL effector PthXo1 bound to its DNA target. Science 335, 716-719.
41. Mali, P., Esvelt, K. M. & Church, G. M. (2013a). Cas9 as a versatile tool for engineering biology. Nat Methods 10, 957-963.
42. Mali, P., Yang, L., Esvelt, K. M., Aach, J., Guell, M., DiCarlo, J. E., Norville, J. E. & Church, G. M. (2013b). RNA-guided human genome engineering via Cas9. Science 339, 823-826.
43. Mandal, P. K., Ferreira, L. M., Collins, R., Meissner, T. B., Boutwell, C. L., Friesen, M., Vrbanac, V., Garrison, B. S., Stortchevoi, A. & other authors (2014). Efficient ablation of genes in human hematopoietic stem and effector cells using CRISPR/Cas9. Cell Stem Cell 15, 643-652.
44. Moncunill, G., Armand-Ugón, M., Pauls, E., Clotet, B. & Esté, J. A. (2008). HIV-1 escape to CCR5 coreceptor antagonism through selection of CXCR4-using variants in vitro. AIDS 22, 23-31
45. Mosier, D. E. (2009). How HIV changes its tropism: evolution and adaptation? Curr Opin HIV AIDS 4, 125-130
46. Mussolino, C., Alzubi, J., Fine, E. J., Morbitzer, R., Cradick, T. J., Lahaye, T., Bao, G. & Cathomen, T. (2014). TALENs facilitate targeted genome editing in human cells with high specificity and low cytotoxicity. Nucleic Acids Res 42, 6762-6773.
47. Parrish, N. F., Gao, F., Li, H., Giorgi, E. E., Barbian, H. J., Parrish, E. H., Zajic, L., Iyer, S. S., Decker, J. M. & other authors (2013). Phenotypic properties of transmitted founder HIV-1. Proc Natl Acad Sci U S A 110, 6626-6633.
48. Pavletich, N. P. & Pabo, C. O. (1991). Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A. Science 252, 809-817.
49. Perez, E. E., Wang, J., Miller, J. C., Jouvenot, Y., Kim, K. A., Liu, O., Wang, N., Lee, G., Bartsevich, V. V. & other authors (2008). Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases. Nat Biotechnol 26, 808-816.
50. Poveda, E. (2015). HIV tropism shift: new paradigm on cell therapy strategies for HIV cure. AIDS Rev 17, 65.
51. Qi, L. S., Larson, M. H., Gilbert, L. A., Doudna, J. A., Weissman, J. S., Arkin, A. P. & Lim, W. A. (2013). Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152, 1173-1183.
52. Ramakrishna, S., Kwaku Dad, A. B., Beloor, J., Gopalappa, R., Lee, S. K. & Kim, H. (2014). Gene disruption by cell-penetrating peptide-mediated delivery of Cas9 protein and guide RNA. Genome Res 24, 1020-1027.
53. Ran, F. A., Hsu, P. D., Lin, C. Y., Gootenberg, J. S., Konermann, S., Trevino, A. E., Scott, D. A., Inoue, A., Matoba, S. & other authors (2013). Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154, 1380-1389.
54. Richman, D. D., Margolis, D. M., Delaney, M., Greene, W. C., Hazuda, D. & Pomerantz, R. J. (2009). The challenge of finding a cure for HIV infection. Science 323, 1304-1307.
55. Saito, N., Chono, H., Shibata, H., Ageyama, N., Yasutomi, Y. & Mineno, J. (2014). CD4(+) T cells modified by the endoribonuclease MazF are safe and can Pprsist in SHIV-infected Rhesus macaques. Mol Ther Nucleic Acids 3, e168.
56. Savkovic, B., Nichols, J., Birkett, D., Applegate, T., Ledger, S., Symonds, G. & Murray, J. M. (2014). A quantitative comparison of anti-HIV gene therapy delivered to hematopoietic stem cells versus CD4+ T cells. PLOS Comput Biol 10, e1003681.
57. Seeger, C. & Sohn, J. A. (2014). Targeting hepatitis B virus with CRISPR/Cas9. Mol Ther Nucleic Acids 3, e216
58. Sendagire, H., Easterbrook, P. J., Nankya, I., Arts, E., Thomas, D. & Reynolds, S. J. (2009). The challenge of HIV-1 antiretroviral resistance in Africa in the era of HAART. AIDS Rev 11, 59-70.
59. Shalem, O., Sanjana, N. E., Hartenian, E., Shi, X., Scott, D. A., Mikkelsen, T. S., Heckl, D., Ebert, B. L., Root, D. E. & other authors (2014). Genome-scale CRISPR-Cas9 knockout screening in human cells. Science 343, 84-87.
60. Shayakhmetov, D. M., Papayannopoulou, T., Stamatoyannopoulos, G. & Lieber, A. (2000). Efficient gene transfer into human CD34(+) cells by a retargeted adenovirus vector. J Virol 74, 2567-2583
61. Smith, C., Gore, A., Yan, W., Abalde-Atristain, L., Li, Z., He, C., Wang, Y., Brodsky, R. A., Zhang, K. & other authors (2014). Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 15, 12-13.
62. Soda, Y., Shimizu, N., Jinno, A., Liu, H. Y., Kanbe, K., Kitamura, T. & Hoshino, H. (1999). Establishment of a new system for determination of coreceptor usages of HIV based on the human glioma NP-2 cell line. Biochem Biophys Res Commun 258, 313-321.
63. Stan, R. & Zaia, J. A. (2014). Practical considerations in gene therapy for HIV cure. Curr HIV/AIDS Rep 11, 11-19.
64. Tanenbaum, M. E., Gilbert, L. A., Qi, L. S., Weissman, J. S. & Vale, R. D. (2014). A protein-tagging system for signal amplification in gene expression and fluorescence imaging. Cell 159, 635-646.
65. Tebas, P., Stein, D., Tang, W. W., Frank, I., Wang, S. Q., Lee, G., Spratt, S. K., Surosky, R. T., Giedlin, M. A. & other authors (2014). Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 370, 901-910.
66. Tiscornia, G., Singer, O. & Verma, I. M. (2006). Design and cloning of lentiviral vectors expressing small interfering RNAs. Nat Protoc 1, 234-240.
67. Urnov, F. D., Miller, J. C., Lee, Y. L., Beausejour, C. M., Rock, J. M., Augustus, S., Jamieson, A. C., Porteus, M. H., Gregory, P. D. & Holmes, M. C. (2005). Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 435, 646-651
68. Veres, A., Gosis, B. S., Ding, Q., Collins, R., Ragavendran, A., Brand, H., Erdin, S., Cowan, C. A., Talkowski, M. E. & Musunuru, K. (2014). Low incidence of off-target mutations in individual CRISPR-Cas9 and TALEN targeted human stem cell clones detected by whole-genome sequencing. Cell Stem Cell 15, 27-30
69. Wagner, J. C., Platt, R. J., Goldfless, S. J., Zhang, F. & Niles, J. C. (2014). Efficient CRISPR-Cas9-mediated genome editing in Plasmodium falciparum. Nat Methods 11, 915-918.
70. Wang, J. & Quake, S. R. (2014). RNA-guided endonuclease provides a therapeutic strategy to cure latent herpesviridae infection. Proc Natl Acad Sci U S A 111, 13157-13162.
71. Wang, W., Ye, C., Liu, J., Zhang, D., Kimata, J. T. & Zhou, P. (2014). CCR5 gene disruption via lentiviral vectors expressing Cas9 and single guided RNA renders cells resistant to HIV-1 infection. PLoS One 9, e115987
72. Ye, L., Wang, J., Beyer, A. I., Teque, F., Cradick, T. J., Qi, Z., Chang, J. C., Bao, G., Muench, M. O. & other authors (2014). Seamless modification of wild-type induced pluripotent stem cells to the natural CCR5D32 mutation confers resistance to HIV infection. Proc Natl Acad Sci U S A 111, 9591-9596.
73. Yuen, K. S., Chan, C. P., Wong, N. H., Ho, C. H., Ho, T. H., Lei, T., Deng, W., Tsao, S. W., Chen, H. & other authors (2015). CRISPR/Cas9-mediated genome editing of Epstein-Barr virus in human cells. J Gen Virol 96, 626-636
74. Zhou, Y., Zhu, S., Cai, C., Yuan, P., Li, C., Huang, Y. & Wei, W. (2014). High-throughput screening of a CRISPR/Cas9 library for functional genomics in human cells. Nature 509, 487-491