Functional screening of guide RNAs targeting the regulatory and structural HIV-1 viral genome for a cure of AIDS

AIDS

Volumn 30, Issue 8, 2016, Pages 1163-1173

  Yin, Chaoran ^a   Zhang, Ting ^a   Li, Fang ^a   Yang, Fan ^a   Putatunda, Raj ^a   Young, Won Bin ^b   Khalili, Kamel ^a   Hu, Wenhui ^a   Zhang, Yonggang ^a  

^a TEMPLE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

CRISPR Cas9; cure; eradication; gRNA; HIV; latent reservoir

Indexed keywords

ADENINE; FIREFLY LUCIFERASE; GUIDE RNA; LENTIVIRUS VECTOR; THYMINE; VIRUS DNA; ANTI HUMAN IMMUNODEFICIENCY VIRUS AGENT; BIOLOGICAL PRODUCT; LUCIFERASE;

ACQUIRED IMMUNE DEFICIENCY SYNDROME; ARTICLE; BIOINFORMATICS; CONTROLLED STUDY; CRISPR CAS SYSTEM; DNA CLEAVAGE; GENE SEQUENCE; GENOTYPE; HEK293 CELL LINE; HIGH THROUGHPUT SCREENING; HUMAN; HUMAN CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; INDEL MUTATION; LONG TERMINAL REPEAT; LUCIFERASE ASSAY; MOLECULAR CLONING; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROVIRUS; RNA SEQUENCE; TRANSIENT TRANSFECTION; VIRAL GENE DELIVERY SYSTEM; VIRUS GENOME; VIRUS MORPHOLOGY; VIRUS REPLICATION; VIRUS TRANSCRIPTION; BIOLOGY; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETIC RECOMBINATION; GENETIC SCREENING; GENETICS; GENOTYPING TECHNIQUE; METABOLISM; REPORTER GENE; VIROLOGY; VIRUS LATENCY;

ACQUIRED IMMUNODEFICIENCY SYNDROME; ANTI-HIV AGENTS; BIOLOGICAL PRODUCTS; COMPUTATIONAL BIOLOGY; GENE EXPRESSION REGULATION, VIRAL; GENES, REPORTER; GENETIC TESTING; GENOME, VIRAL; GENOTYPING TECHNIQUES; HEK293 CELLS; HIV-1; HUMANS; LUCIFERASES; POLYMERASE CHAIN REACTION; PROVIRUSES; RECOMBINATION, GENETIC; RNA, GUIDE; VIRUS LATENCY;

EID: 84961226661     PISSN: 02699370     EISSN: 14735571     Source Type: Journal    
DOI: 10.1097/QAD.0000000000001079     Document Type: Article

References (67)

1. Hu W, Kaminski R, Yang F, Zhang Y, Cosentino L, Li F, et al. RNA-directed gene editing specifically eradicates latent and prevents new HIV-1 infection. Proc Natl Acad Sci USA 2014; 111:11461-11466.
2. Sgarbanti M, Battistini A. Therapeutics for HIV-1 reactivation from latency. Curr Opin Virol 2013; 3:394-401.
3. Halper-Stromberg A, Lu CL, Klein F, Horwitz JA, Bournazos S, Nogueira L, et al. Broadly neutralizing antibodies and viral inducers decrease rebound from HIV-1 latent reservoirs in humanized mice. Cell 2014; 158:989-999.
4. Wei DG, Chiang V, Fyne E, Balakrishnan M, Barnes T, Graupe M, et al. Histone deacetylase inhibitor romidepsin induces HIV expression in CD4 T cells from patients on suppressive antiretroviral therapy at concentrations achieved by clinical dosing. PLoS Pathog 2014; 10:e1004071.
5. R T cells to HIV by increasing the kinetics and efficiency of postentry viral events. J Virol 2014; 88:10803-10812.
6. Spivak AM, Andrade A, Eisele E, Hoh R, Bacchetti P, Bumpus NN, et al. A pilot study assessing the safety and latency-reversing activity of disulfiram in HIV-1-infected adults on anti-retroviral therapy. Clin Infect Dis 2014; 58:883-890.
7. Lee YS, Kim ST, Kim GW, Lee M, Park JS. An engineered lox sequence containing part of a long terminal repeat of HIV-1 permits Cre recombinase-mediated DNA excision. Biochem Cell Biol 2000; 78:653-658.
8. Karpinski J, Chemnitz J, Hauber I, Abi-Ghanem J, Paszkowski-Rogacz M, Surendranath V, et al. Universal Tre (uTre) recom-binase specifically targets the majority of HIV-1 isolates. J Int AIDS Soc 2014; 17:19706.
9. Hauber I, Hofmann-Sieber H, Chemnitz J, Dubrau D, Chusai-now J, Stucka R, et al. Highly significant antiviral activity of HIV-1 LTR-specific tre-recombinase in humanized mice. PLoS Pathog 2013; 9:e1003587.
10. Bedell VM, Wang Y, Campbell JM, Poshusta TL, Starker CG, Krug RG 2nd, et al. In vivo genome editing using a high-efficiency TALEN system. Nature 2012; 491:114-118.
11. Wang Y, Zhang WY, Hu S, Lan F, Lee AS, Huber B, et al. Genome editing of human embryonic stem cells and induced pluripotent stem cells with zinc finger nucleases for cellular imaging. Circ Res 2012; 111:1494-1503.
12. Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013; 339:819-823.
13. Jinek M, East A, Cheng A, Lin S, Ma E, Doudna J. RNA-pro-grammed genome editing in human cells. Elife 2013; 2:e00471.
14. Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science 2013; 339:823-826.
15. Qi LS, Larson MH, Gilbert LA, Doudna JA, Weissman JS, Arkin AP, et al. Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 2013; 152:1173-1183.
16. Aubert M, Ryu BY, Banks L, Rawlings DJ, Scharenberg AM, Jerome KR. Successful targeting and disruption of an integrated reporter lentivirus using the engineered homing endonuclease Y2 I-AniI. PLoS ONE 2011; 6:e16825.
17. Manotham K, Chattong S, Setpakdee A. Generation of CCR5-defective CD34 cells from ZFN-driven stop codon-integrated mesenchymal stem cell clones. J Biomed Sci 2015; 22:25.
18. Tebas P, Stein D, Tang WW, Frank I, Wang SQ, Lee G, et al. Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. N Engl J Med 2014; 370:901-910.
19. Li L, Krymskaya L, Wang J, Henley J, Rao A, Cao LF, et al. Genomic editing of the HIV-1 coreceptor CCR5 in adult hematopoietic stem and progenitor cells using zinc finger nucleases. Mol Ther 2013; 21:1259-1269.
20. Hutter G, Bodor J, Ledger S, Boyd M, Millington M, Tsie M, et al. CCR5 targeted cell therapy for HIV and prevention of viral escape. Viruses 2015; 7:4186-4203.
21. Ru R, Yao Y, Yu S, Yin B, Xu W, Zhao S, et al. Targeted genome engineering in human induced pluripotent stem cells by penetrating TALENs. Cell Regen (Lond) 2013; 2:5.
22. Wang W, Ye C, Liu J, Zhang D, Kimata JT, Zhou P. CCR5 gene disruption via lentiviral vectors expressing Cas9 and single guided RNA renders cells resistant to HIV-1 infection. PLoS ONE 2014; 9:e115987.
23. Ye L, Wang J, Beyer AI, Teque F, Cradick TJ, Qi Z, et al. Seamless modification of wild-type induced pluripotent stem cells to the natural CCR5Delta32 mutation confers resistance to HIV infection. Proc Natl Acad Sci USA 2014; 111:9591-9596.
24. Qu X, Wang P, Ding D, Li L, Wang H, Ma L, et al. Zinc-finger-nucleases mediate specific and efficient excision of HIV-1 proviral DNA from infected and latently infected human T cells. Nucleic Acids Res 2013; 41:7771-7782.
25. Ebina H, Kanemura Y, Misawa N, Sakuma T, Kobayashi T, Yamamoto T, et al. A high excision potential of TALENs for integrated DNA of HIV-based lentiviral vector. PLoS ONE 2015; 10:e0120047.
26. Wang X, Wang P, Fu Z, Ji H, Qu X, Zeng H, et al. Designed transcription activator-like effector proteins efficiently induced the expression of latent HIV-1 in latently infected cells. AIDS Res Hum Retroviruses 2015; 31:98-106.
27. Lee HJ, Kweon J, Kim E, Kim S, Kim JS. Targeted chromosomal duplications and inversions in the human genome using zinc finger nucleases. Genome Res 2012; 22:539-548.
28. Chen S, Oikonomou G, Chiu CN, Niles BJ, Liu J, Lee DA, et al. A large-scale in vivo analysis reveals that TALENs are significantly more mutagenic than ZFNs generated using context-dependent assembly. Nucleic Acids Res 2013; 41:2769-2778.
29. Mussolino C, Morbitzer R, Lutge F, Dannemann N, Lahaye T, Cathomen T. A novel TALE nuclease scaffold enables high genome editing activity in combination with low toxicity. Nucleic Acids Res 2011; 39:9283-9293.
30. Bogdanove AJ, Voytas DF. TAL effectors: customizable proteins for DNA targeting. Science 2011; 333:1843-1846.
31. Ebina H, Misawa N, Kanemura Y, Koyanagi Y. Harnessing the CRISPR/Cas9 system to disrupt latent HIV-1 provirus. Sci Rep 2013; 3:2510.
32. Liao HK, Gu Y, Diaz A, Marlett J, Takahashi Y, Li M, et al. Use of the CRISPR/Cas9 system as an intracellular defense against HIV-1 infection in human cells. Nat Commun 2015; 6:6413.
33. Zhu W, Lei R, Le Duff Y, Li J, Guo F, Wainberg MA, et al. The CRISPR/Cas9 system inactivates latent HIV-1 proviral DNA. Retrovirology 2015; 12:22.
34. Sena-Esteves M, Tebbets JC, Steffens S, Crombleholme T, Flake AW. Optimized large-scale production of high titer lentivirus vector pseudotypes. J Virol Methods 2004; 122:131-139.
35. Koike-Yusa H, Li Y, Tan EP, Velasco-Herrera Mdel C, Yusa K. Genome-wide recessive genetic screening in mammalian cells with a lentiviral CRISPR-guide RNA library. Nat Biotechnol 2014; 32:267-273.
36. Hu P, Li Y, Sands MS, McCown T, Kafri T. Generation of a stable packaging cell line producing high-titer PPT-deleted integration-deficient lentiviral vectors. Mol Ther Methods Clin Dev 2015; 2:15025.
37. Liu KC, Lin BS, Gao AD, Ma HY, Zhao M, Zhang R, et al. Integrase-deficient lentivirus: opportunities and challenges for human gene therapy. Curr Gene Ther 2014; 14:352-364.
38. Song J, Cai Z, White AG, Jin T, Wang X, Kadayakkara D, et al. Visualization and quantification of simian immunodeficiency virus-infected cells using noninvasive molecular imaging. J Gen Virol 2015; 96:3131-3142.
39. Madabhushi R, Gao F, Pfenning AR, Pan L, Yamakawa S, Seo J, et al. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 2015; 161:1592-1605.
40. Jadlowsky JK, Wong JY, Graham AC, Dobrowolski C, Devor RL, Adams MD, et al. Negative elongation factor is required for the maintenance of proviral latency but does not induce promoter-proximal pausing of RNA polymerase II on the HIV long terminal repeat. Mol Cell Biol 2014; 34:1911-1928.
41. Kopp JB, Klotman ME, Adler SH, Bruggeman LA, Dickie P, Marinos NJ, et al. Progressive glomerulosclerosis and enhanced renal accumulation of basement membrane components in mice transgenic for human immunodeficiency virus type 1 genes. Proc Natl Acad Sci USA 1992; 89:1577-1581.
42. Doench JG, Hartenian E, Graham DB, Tothova Z, Hegde M, Smith I, et al. Rational design of highly active sgRNAs for CRISPR-Cas9-mediated gene inactivation. Nat Biotechnol 2014; 32:1262-1267.
43. Gagnon JA, Valen E, Thyme SB, Huang P, Akhmetova L, Pauli A, et al. Efficient mutagenesis by Cas9 protein-mediated oligonu-cleotide insertion and large-scale assessment of single-guide RNAs. PLoS ONE 2014; 9:e98186.
44. Liu H, Wei Z, Dominguez A, Li Y, Wang X, Qi LS. CRISPR-ERA: a comprehensive design tool for CRISPR-mediated gene editing, repression and activation. Bioinformatics 2015; 31:3676-3678.
45. Sander JD, Cade L, Khayter C, Reyon D, Peterson RT, Joung JK, et al. Targeted gene disruption in somatic zebrafish cells using engineered TALENs. Nat Biotechnol 2011; 29:697-698.
46. Qiu P, Shandilya H, D'Alessio JM, O'Connor K, Durocher J, Gerard GF. Mutation detection using Surveyor nuclease. Bio-techniques 2004; 36:702-707.
47. Kim JM, Kim D, Kim S, Kim JS. Genotyping with CRISPR-Cas-derived RNA-guided endonucleases. Nat Commun 2014; 5:3157.
48. Dahlem TJ, Hoshijima K, Jurynec MJ, Gunther D, Starker CG, Locke AS, et al. Simple methods for generating and detecting locus-specific mutations induced with TALENs in the zebrafish genome. PLoS Genet 2012; 8:e1002861.
49. Bassett AR, Liu JL. CRISPR/Cas9 and genome editing in Drosophila. J Genet Genomics 2014; 41:7-19.
50. Guell M, Yang L, Church GM. Genome editing assessment using CRISPR genome analyzer (CRISPR-GA). Bioinformatics 2014; 30:2968-2970.
51. Brinkman EK, Chen T, Amendola M, van Steensel B. Easy quantitative assessment of genome editing by sequence trace decomposition. Nucleic Acids Res 2014; 42:e168.
52. Carrington B, Varshney GK, Burgess SM, Sood R. CRISPR-STAT: an easy and reliable PCR-based method to evaluate target-specific sgRNA activity. Nucleic Acids Res 2015; 43:e157.
53. Yu C, Zhang Y, Yao S, Wei Y. A PCR based protocol for detecting InDel mutations induced by TALENs and CRISPR/Cas9 in zebrafish. PLoS ONE 2014; 9:e98282.
54. Ramanan V, Shlomai A, Cox DB, Schwartz RE, Michailidis E, Bhatta A, et al. CRISPR/Cas9 cleavage of viral DNA efficiently suppresses hepatitis B virus. Sci Rep 2015; 5:10833.
55. Yuen KS, Chan CP, Wong NH, Ho CH, Ho TH, Lei T, et al. CRISPR/Cas9-mediated genome editing of Epstein-Barr virus in human cells. J Gen Virol 2015; 96:626-636.
56. Peng C, Lu M, Yang D. CRISPR/Cas9-based tools for targeted genome editing and replication control of HBV. Virol Sin 2015; 30:317-325.
57. Zuckermann M, Hovestadt V, Knobbe-Thomsen CB, Zapatka M, Northcott PA, Schramm K, et al. Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modelling. Nat Commun 2015; 6:7391.
58. Smith C, Gore A, Yan W, Abalde-Atristain L, Li Z, He C, et al. Whole-genome sequencing analysis reveals high specificity of CRISPR/Cas9 and TALEN-based genome editing in human iPSCs. Cell Stem Cell 2014; 15:12-13.
59. Veres A, Gosis BS, Ding Q, Collins R, Ragavendran A, Brand H, et al. 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 2014; 15:27-30.
60. Yang L, Grishin D, Wang G, Aach J, Zhang CZ, Chari R, et al. Targeted and genome-wide sequencing reveal single nucleo-tide variations impacting specificity of Cas9 in human stem cells. Nat Commun 2014; 5:5507.
61. Ran FA, Cong L, Yan WX, Scott DA, Gootenberg JS, Kriz AJ, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 2015; 520:186-191.
62. Tsai SQ, Zheng Z, Nguyen NT, Liebers M, Topkar VV, Thapar V, et al. GUIDE-seq enables genome-wide profiling of off-target cleavage by CRISPR-Cas nucleases. Nat Biotechnol 2015; 33:187-197.
63. Frock RL, Hu J, Meyers RM, Ho YJ, Kii E, Alt FW. Genome-wide detection of DNA double-stranded breaks induced by engineered nucleases. Nat Biotechnol 2015; 33:179-186.
64. Ran FA, Hsu PD, Lin CY, Gootenberg JS, Konermann S, Trevino AE, et al. Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 2013; 154:1380-1389.
65. Mali P, Aach J, Stranges PB, Esvelt KM, Moosburner M, Kosuri S, et al. CAS9 transcriptional activators for target specificity screening and paired nickases for cooperative genome engineering. Nat Biotechnol 2013; 31:833-838.
66. Wyvekens N, Topkar VV, Khayter C, Joung JK, Tsai SQ. Dimeric CRISPR RNA-guided FokI-dCas9 nucleases directed by truncated gRNAs for highly specific genome editing. Hum Gene Ther 2015; 26:425-431.
67. Tsai SQ, Wyvekens N, Khayter C, Foden JA, Thapar V, Reyon D, et al. Dimeric CRISPR RNA-guided FokI nucleases for highly specific genome editing. Nat Biotechnol 2014; 32:569-576.