Designer Nucleases: Gene-Editing Therapies using CCR5 as an Emerging Target in HIV

Author(s): Maria João Almeida, Ana Matos*.

Journal Name: Current HIV Research

Volume 17 , Issue 5 , 2019

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Acquired Immunodeficiency Syndrome (AIDS), caused by the Human Immunodeficiency Virus (HIV), is a life-threatening disorder that persists worldwide as a severe health problem. Since it was linked with the HIV attachment process, the Chemokine receptor, CCR5, has been at the development leading edge of several gene-based therapies. Given the shortcomings of the current antiretroviral treatment procedure and the non-availability of a licensed vaccine, the aptitude to modify complex genomes with Designer Nucleases has had a noteworthy impact on biotechnology. Over the last years, ZFN, TALEN and CRISPR/Cas9 gene-editing technology have appeared as a promising solution that mimics the naturally occurring CCR5/Δ32 mutation and permanently guarantees the absence of CCR5-expression on the surface of HIV target-cells, leading to a continuous resistance to the virus entry and, ultimately, proving that cellular immunization from infection could be, in fact, a conceivable therapeutic approach to finally achieve the long-awaited functional cure of HIV.

Keywords: AIDS, HIV, CCR5, designer nucleases, CCR5/Δ32 mutation, functional cure.

[1]
Berkhout B. ERTL HCJ, Weinberg MS. Gene Therapy for HIV and Chronic Infections. American Society of Gene & Cell Therapy 2015.
[2]
Deng Q, Chen Z, Shi L, Lin H. Developmental progress of CRISPR/Cas9 and its therapeutic applications for HIV-1 infection. Rev Med Virol 2018; 28(5)e1998
[http://dx.doi.org/10.1002/rmv.1998] [PMID: 30024073]
[3]
Nyamweya S, Hegedus A, Jaye A, Rowland-Jones S, Flanagan KL, Macallan DC. Comparing HIV-1 and HIV-2 infection: Lessons for viral immunopathogenesis. Rev Med Virol 2013; 23(4): 221-40.
[http://dx.doi.org/10.1002/rmv.1739] [PMID: 23444290]
[4]
Wang J, Holmes MC. Engineering hematopoietic stem cells toward a functional cure of human immunodeficiency virus infection. Cytotherapy 2016; 18(11): 1370-81.
[http://dx.doi.org/10.1016/j.jcyt.2016.07.007] [PMID: 27745602]
[5]
Mehta V, Chandramohan D, Agarwal S. Genetic Modulation Therapy Through Stem Cell Transplantation for Human Immunodeficiency Virus 1 Infection. Cureus 2017; 9(3)e1093
[http://dx.doi.org/10.7759/cureus.1093] [PMID: 28413739]
[6]
Huyghe J, Magdalena S, Vandekerckhove L. Fight fire with fire: Gene therapy strategies to cure HIV. Expert Rev Anti Infect Ther 2017; 15(8): 747-58.
[http://dx.doi.org/10.1080/14787210.2017.1353911] [PMID: 28692305]
[7]
Manjunath N, Yi G, Dang Y, Shankar P. Newer gene editing technologies toward HIV gene therapy. Viruses 2013; 5(11): 2748-66.
[http://dx.doi.org/10.3390/v5112748] [PMID: 24284874]
[8]
World Health Organization. HIV drug resistance Available at: https://www.who.int/hiv/topics/drugresistance/en/ [Accessed January 11, 2019]
[9]
Hoxie JA, June CH. Novel cell and gene therapies for HIV. Cold Spring Harb Perspect Med 2012; 2(10): 2.
[http://dx.doi.org/10.1101/cshperspect.a007179] [PMID: 23028130]
[10]
Brelot A, Chakrabarti LA. CCR5 Revisited: How Mechanisms of HIV Entry Govern AIDS Pathogenesis. J Mol Biol 2018; 430(17): 2557-89.
[http://dx.doi.org/10.1016/j.jmb.2018.06.027] [PMID: 29932942]
[11]
Science Daily. Virus. Available at: https://www.sciencedaily.com/terms/virus.htm [Accessed January 13, 2019].
[12]
AIDS Info. The HIV Life Cycle. [Accessed January 13, 2019]. Available at: https://aidsinfo.nih.gov/understanding-hiv-aids/fact-sheets/19/73/the-hiv-life-cycle
[13]
Kirchhoff F. HIV Life Cycle: Overview. Encyclopedia of AIDS 2013; 1-9.
[14]
Barmania F, Pepper MS. C-C chemokine receptor type five (CCR5): An emerging target for the control of HIV infection. Appl Transl Genomics 2013; 2: 3-16.
[http://dx.doi.org/10.1016/j.atg.2013.05.004] [PMID: 27942440]
[15]
Shi B, Li J, Shi X, et al. TALEN-Mediated Knockout of CCR5 Confers Protection Against Infection of Human Immunodeficiency Virus. J Acquir Immune Defic Syndr 2017; 74(2): 229-41.
[http://dx.doi.org/10.1097/QAI.0000000000001190] [PMID: 27749600]
[16]
Engelman A, Cherepanov P. The structural biology of HIV-1: mechanistic and therapeutic insights. Nat Rev Microbiol 2012; 10(4): 279-90.
[http://dx.doi.org/10.1038/nrmicro2747] [PMID: 22421880]
[17]
Craigie R, Bushman FD. HIV DNA integration. Cold Spring Harb Perspect Med 2012; 2(7)a006890
[http://dx.doi.org/10.1101/cshperspect.a006890] [PMID: 22762018]
[18]
Lodowski DT, Palczewski K. Chemokine receptors and other G protein-coupled receptors. Curr Opin HIV AIDS 2009; 4(2): 88-95.
[http://dx.doi.org/10.1097/COH.0b013e3283223d8d] [PMID: 19339946]
[19]
Lu M, Wu B. Structural studies of G protein-coupled receptors. IUBMB Life 2016; 68(11): 894-903.
[http://dx.doi.org/10.1002/iub.1578] [PMID: 27766738]
[20]
Hu GM, Mai TL, Chen CM. Visualizing the GPCR Network: Classification and Evolution. Sci Rep 2017; 7(1): 15495.
[http://dx.doi.org/10.1038/s41598-017-15707-9] [PMID: 29138525]
[21]
Guide to Pharmacology. G Protein-Coupled Receptors. Available at: http://www.guidetopharmacology. org/GRAC/FamilyDisplay Forward?familyId=694 [Accessed January 19, 2019].
[22]
Rosenbaum DM, Rasmussen SGF, Kobilka BK. The structure and function of G-protein-coupled receptors. Nature 2009; 459(7245): 356-63.
[http://dx.doi.org/10.1038/nature08144] [PMID: 19458711]
[23]
Allen SJ, Crown SE, Handel TM. Chemokine: receptor structure, interactions, and antagonism. Annu Rev Immunol 2007; 25: 787-820.
[http://dx.doi.org/10.1146/annurev.immunol.24.021605.090529] [PMID: 17291188]
[24]
Hughes CE, Nibbs RJB. A guide to chemokines and their receptors. FEBS J 2018; 285(16): 2944-71.
[http://dx.doi.org/10.1111/febs.14466] [PMID: 29637711]
[25]
Zlotnik A, Yoshie O, Nomiyama H. The chemokine and chemokine receptor superfamilies and their molecular evolution. Genome Biol 2006; 7(12): 243.
[http://dx.doi.org/10.1186/gb-2006-7-12-243] [PMID: 17201934]
[26]
Cartier L, Hartley O, Dubois-Dauphin M, Krause KH. Chemokine receptors in the central nervous system: role in brain inflammation and neurodegenerative diseases. Brain Res Brain Res Rev 2005; 48(1): 16-42.
[http://dx.doi.org/10.1016/j.brainresrev.2004.07.021] [PMID: 15708626]
[27]
Nomiyama H, Osada N, Yoshie O. Systematic classification of vertebrate chemokines based on conserved synteny and evolutionary history. Genes Cells 2013; 18(1): 1-16.
[http://dx.doi.org/10.1111/gtc.12013] [PMID: 23145839]
[28]
Zhang M, Zhu ZL, Gao XL, Wu JS, Liang XH, Tang YL. Functions of chemokines in the perineural invasion of tumors. (Review). Int J Oncol 2018; 52: 1019-6439.
[http://dx.doi.org/10.3892/ijo.2018.4311] [PMID: 29532850]
[29]
Allers K, Schneider T. CCR5Δ32 mutation and HIV infection: basis for curative HIV therapy. Curr Opin Virol 2015; 14: 24-9.
[http://dx.doi.org/10.1016/j.coviro.2015.06.007] [PMID: 26143158]
[30]
Bachelerie F, Ben-Baruch A, Burkhardt AM, et al. International Union of Pharmacology. LXXXIX. Update on the Extended Family of Chemokine Receptors and Introducing a New Nomenclature for Atypical Chemokine Receptors. Pharmacol Rev 2014; 66: 1-79.
[http://dx.doi.org/10.1124/pr.113.007724] [PMID: 24218476]
[31]
Pakianathan DR, Kuta EG, Artis DR, Skelton NJ, Hébert CA. Distinct but overlapping epitopes for the interaction of a CC-chemokine with CCR1, CCR3 and CCR5. Biochemistry 1997; 36(32): 9642-8.
[http://dx.doi.org/10.1021/bi970593z] [PMID: 9289016]
[32]
Blanpain C, Migeotte I, Lee B, et al. CCR5 binds multiple CC-chemokines: MCP-3 acts as a natural antagonist. Blood 1999; 94(6): 1899-905.
[http://dx.doi.org/10.1182/blood.V94.6.1899] [PMID: 10477718]
[33]
Samson M, Labbe O, Mollereau C, Vassart G, Parmentier M. Molecular cloning and functional expression of a new human CC-chemokine receptor gene. Biochemistry 1996; 35(11): 3362-7.
[http://dx.doi.org/10.1021/bi952950g] [PMID: 8639485]
[34]
Rottman JB, Ganley KP, Williams K, Wu L, Mackay CR, Ringler DJ. Cellular localization of the chemokine receptor CCR5. Correlation to cellular targets of HIV-1 infection. Am J Pathol 1997; 151(5): 1341-51.
[PMID: 9358760]
[35]
Mummidi S, Adams LM, VanCompernolle SE, et al. Production of specific mRNA transcripts, usage of an alternate promoter, and octamer-binding transcription factors influence the surface expression levels of the HIV coreceptor CCR5 on primary T cells. J Immunol 2007; 178(9): 5668-81.
[http://dx.doi.org/10.4049/jimmunol.178.9.5668] [PMID: 17442950]
[36]
Hoover KC. Intragenus (Homo) Variation in a Chemokine Receptor Gene (CCR5. PLoS One 2018; 13(10)e0204989
[37]
Mummidi S, Ahuja SS, McDaniel BL, Ahuja SK. The human CC chemokine receptor 5 (CCR5) gene. Multiple transcripts with 5′-end heterogeneity, dual promoter usage, and evidence for polymorphisms within the regulatory regions and noncoding exons. J Biol Chem 1997; 272(49): 30662-71.
[http://dx.doi.org/10.1074/jbc.272.49.30662] [PMID: 9388201]
[38]
Picton ACP, Paximadis M, Tiemessen CT. Genetic variation within the gene encoding the HIV-1 CCR5 coreceptor in two South African populations. Infect Genet Evol 2010; 10(4): 487-94.
[http://dx.doi.org/10.1016/j.meegid.2010.02.012] [PMID: 20206716]
[39]
Liu R, Paxton WA, Choe S, et al. Homozygous defect in HIV-1 coreceptor accounts for resistance of some multiply-exposed individuals to HIV-1 infection. Cell 1996; 86(3): 367-77.
[http://dx.doi.org/10.1016/S0092-8674(00)80110-5] [PMID: 8756719]
[40]
Heydarifard Z, Tabarraei A, Moradi A. Polymorphisms in CCR5Δ32 and risk of HIV-1 infection in the Southeast of Caspian Sea, Iran. Dis Markers 2017; 20174190107
[http://dx.doi.org/10.1155/2017/4190107] [PMID: 29209099]
[41]
Agrawal L, Lu X, Qingwen J, et al. Role for CCR5Delta32 protein in resistance to R5, R5X4, and X4 human immunodeficiency virus type 1 in primary CD4+ cells. J Virol 2004; 78(5): 2277-87.
[http://dx.doi.org/10.1128/JVI.78.5.2277-2287.2004] [PMID: 14963124]
[42]
Samson M, Libert F, Doranz BJ, et al. Resistance to HIV-1 infection in caucasian individuals bearing mutant alleles of the CCR-5 chemokine receptor gene. Nature 1996; 382(6593): 722-5.
[http://dx.doi.org/10.1038/382722a0] [PMID: 8751444]
[43]
Xie Y, Zhan S, Ge W, Tang P. The Potential Risks of C-C Chemokine Receptor 5-Edited Babies in Bone Development Bone Research 2019.
[44]
Dean M, Carrington M, Winkler C, et al. 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 1996; 273(5283): 1856-62.
[http://dx.doi.org/10.1126/science.273.5283.1856] [PMID: 8791590]
[45]
Smoleń-Dzirba J, Rosińska M, Janiec J, et al. HIV-1 infection in persons homozygous for CCR5-Δ32 allele: The next case and the review. AIDS Rev 2017; 19(4): 219-30.
[PMID: 28534889]
[46]
Hütter G, Nowak D, Mossner M, et al. Long-term control of HIV by CCR5 Delta32/Delta32 stem-cell transplantation. N Engl J Med 2009; 360(7): 692-8.
[http://dx.doi.org/10.1056/NEJMoa0802905] [PMID: 19213682]
[47]
Hütter G. Stem cell transplantation in strategies for curing HIV/AIDS. AIDS Res Ther 2016; 13(1): 31.
[http://dx.doi.org/10.1186/s12981-016-0114-y] [PMID: 27625700]
[48]
Kuritzkes DR. Hematopoietic stem cell transplantation for HIV cure. J Clin Invest 2016; 126(2): 432-7.
[http://dx.doi.org/10.1172/JCI80563] [PMID: 26731468]
[49]
Allers K, Hütter G, Hofmann J, et al. Evidence for the cure of HIV infection by CCR5Δ32/Δ32 stem cell transplantation. Blood 2011; 117(10): 2791-9.
[http://dx.doi.org/10.1182/blood-2010-09-309591] [PMID: 21148083]
[50]
Hütter G, Thiel E. Allogeneic transplantation of CCR5-deficient progenitor cells in a patient with HIV infection: an update after 3 years and the search for patient no. 2. AIDS 2011; 25(2): 273-4.
[http://dx.doi.org/10.1097/QAD.0b013e328340fe28] [PMID: 21173593]
[51]
Chhabra A, Ring AM, Weiskopf K, et al. Hematopoietic stem cell transplantation in immunocompetent hosts without radiation or chemotherapy. Sci Transl Med 2016; 8351ra105
[http://dx.doi.org/10.1126/scitranslmed.aae0501]
[52]
Fred Hutch. Timothy Ray Brown: the Accidental AIDS Icon. [Accessed February 14, 2019]. Available at: http://www.fredhutch.org/en/news/center-news/2015/02/aids-icon-timothy-ray-brown.html
[53]
Rezvani AR, Storb RF. Prevention of graft-vs.-host disease. Expert Opin Pharmacother 2012; 13(12): 1737-50.
[http://dx.doi.org/10.1517/14656566.2012.703652] [PMID: 22770714]
[54]
Burke BP, Boyd MP, Impey H, et al. CCR5 as a natural and modulated target for inhibition of HIV. Viruses 2013; 6(1): 54-68.
[http://dx.doi.org/10.3390/v6010054] [PMID: 24381033]
[55]
Novembre J, Galvani AP, Slatkin M. The geographic spread of the CCR5 delta32 HIV-resistance allele. PLOS biology: A Peer- Reviewed Open-Access Journal 2005; 3: e339.
[56]
Kordelas L, Verheyen J, Beelen DW, et al. Shift of HIV tropism in stem-cell transplantation with CCR5 Delta32 mutation. N Engl J Med 2014; 371(9): 880-2.
[http://dx.doi.org/10.1056/NEJMc1405805] [PMID: 25162903]
[57]
Domingo E, Sheldon J, Perales C. Viral quasispecies evolution. Microbiol Mol Biol Rev 2012; 76(2): 159-216.
[http://dx.doi.org/10.1128/MMBR.05023-11] [PMID: 22688811]
[59]
Hyde CL, Macinnes A, Sanders FA, et al. Genetic association of the CCR5 region with lipid levels in at-risk cardiovascular patients. Circ Cardiovasc Genet 2010; 3(2): 162-8.
[http://dx.doi.org/10.1161/CIRCGENETICS.109.897793] [PMID: 20130232]
[60]
Klein RS. A moving target: the multiple roles of CCR5 in infectious diseases. J Infect Dis 2008; 197(2): 183-6.
[http://dx.doi.org/10.1086/524692] [PMID: 18179384]
[61]
Glass WG, Lim JK, Cholera R, Pletnev AG, Gao JL, Murphy PM. Chemokine receptor CCR5 promotes leukocyte trafficking to the brain and survival in West Nile virus infection. J Exp Med 2005; 202(8): 1087-98.
[http://dx.doi.org/10.1084/jem.20042530] [PMID: 16230476]
[62]
Wei X, Nielsen R. CCR5-∆32 is deleterious in the homozygous state in humans. Nat Med 2019; 25(6): 909-10.
[http://dx.doi.org/10.1038/s41591-019-0459-6] [PMID: 31160814]
[63]
Kindberg E, Mickienë A, Ax C, et al. A deletion in the chemokine receptor 5 (CCR5) gene is associated with tickborne encephalitis. J Infect Dis 2008; 197(2): 266-9.
[http://dx.doi.org/10.1086/524709] [PMID: 18179389]
[64]
Houses of Parliament. Genome Editing. [Accessed March 12, 2019]. Available at: https://researchbriefings.files.parliament.uk/documents/POST-PN-0541/POST-PN-0541.pdf
[65]
Gonçalves GAR, Paiva RMA. Gene therapy: advances, challenges and perspectives. Einstein (Sao Paulo) 2017; 15(3): 369-75.
[http://dx.doi.org/10.1590/s1679-45082017rb4024] [PMID: 29091160]
[66]
Rerees HA, Es HA, Liu DR. Base editing: Precision chemistry on the genome and transcriptome of living cells. Nat Rev Genet 2018.
[67]
amfAR, Making AIDS History. The Countdown to a Cure for AIDS Available at: https://www.amfar.org/countdown/ [Accessed March 15, 2019].
[68]
Stan R, Zaia JA. Practical considerations in gene therapy for HIV cure. Curr HIV/AIDS Rep 2014; 11(1): 11-9.
[http://dx.doi.org/10.1007/s11904-013-0197-1] [PMID: 24449226]
[69]
Deeks SG, Autran B, Berkhout B, et al. Towards an HIV cure: a global scientific strategy. Nat Rev Immunol 2012; 12(8): 607-14.
[http://dx.doi.org/10.1038/nri3262] [PMID: 22814509]
[70]
Chun TW, Moir S, Fauci AS. HIV reservoirs as obstacles and opportunities for an HIV cure. Nat Immunol 2015; 16(6): 584-9.
[http://dx.doi.org/10.1038/ni.3152] [PMID: 25990814]
[71]
Nazari R, Joshi S. CCR5 as target for HIV-1 gene therapy. Curr Gene Ther 2008; 8(4): 264-72.
[http://dx.doi.org/10.2174/156652308785160674] [PMID: 18691022]
[72]
Telenti A. Safety concerns about CCR5 as an antiviral target. Curr Opin HIV AIDS 2009; 4(2): 131-5.
[http://dx.doi.org/10.1097/COH.0b013e3283223d76] [PMID: 19339952]
[73]
Zhou Y, Kurihara T, Ryseck RP, et al. Impaired macrophage function and enhanced T cell-dependent immune response in mice lacking CCR5, the mouse homologue of the major HIV-1 coreceptor. J Immunol 1998; 160(8): 4018-25.
[PMID: 9558111]
[74]
Saha SK, Saikot FK, Rahman MS, et al. Programmable molecular scissors: Applications of a new tool for genome editing in biotech. Mol Ther Nucleic Acids 2019; 14: 212-38.
[PMID: 30641475]
[75]
The National Academies of Science, Engineering and Medicine. Human Genome Editing: Science, Ethics, and Governance: Somatic Genome Editing. Washington, D.C., EUA: National Academies Press 2017.
[76]
Wang CX, Cannon PM. The clinical applications of genome editing in HIV. Blood 2016; 127(21): 2546-52.
[http://dx.doi.org/10.1182/blood-2016-01-678144] [PMID: 27053530]
[77]
Corrigan-Curay J, O’Reilly M, Kohn DB, et al. Genome editing technologies: defining a path to clinic. Mol Ther 2015; 23(5): 796-806.
[http://dx.doi.org/10.1038/mt.2015.54] [PMID: 25943494]
[78]
Singwi S, Joshi S. Potential nuclease-based strategies for HIV gene therapy. Front Biosci 2000; 5: D556-79.
[http://dx.doi.org/10.2741/Singwi] [PMID: 10799357]
[79]
Thieme. Therapeutic Genome Editing with Engineered Nucleases. [Accessed March 20, 2019]. Available at: https://www.thieme-connect.com/products/ejournals/abstract/10.5482/HAMO-16-09-0035
[80]
Kim JS. Genome editing comes of age. Nat Protoc 2016; 11(9): 1573-8.
[http://dx.doi.org/10.1038/nprot.2016.104] [PMID: 27490630]
[81]
Meng X, Noyes MB, Zhu LJ, Lawson ND, Wolfe SA. Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases. Nat Biotechnol 2008; 26(6): 695-701.
[http://dx.doi.org/10.1038/nbt1398] [PMID: 18500337]
[82]
Townsend JA, Wright DA, Winfrey RJ, et al. High-frequency modification of plant genes using engineered zinc-finger nucleases. Nature 2009; 459(7245): 442-5.
[http://dx.doi.org/10.1038/nature07845] [PMID: 19404258]
[83]
Urnov FD, Miller JC, Lee YL, et al. Highly efficient endogenous human gene correction using designed zinc-finger nucleases. Nature 2005; 435(7042): 646-51.
[http://dx.doi.org/10.1038/nature03556] [PMID: 15806097]
[84]
Miller JC, Holmes MC, Wang J, et al. An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 2007; 25(7): 778-85.
[http://dx.doi.org/10.1038/nbt1319] [PMID: 17603475]
[85]
Moscou MJ, Bogdanove AJ. A simple cipher governs DNA recognition by TAL effectors. Science 2009; 326(5959): 1501.
[http://dx.doi.org/10.1126/science.1178817] [PMID: 19933106]
[86]
Gaj T, Gersbach CA, Barbas CF III. ZFN, TALEN, and CRISPR/Cas-based methods for genome engineering. Trends Biotechnol 2013; 31(7): 397-405.
[http://dx.doi.org/10.1016/j.tibtech.2013.04.004] [PMID: 23664777]
[87]
Leukaemia Foundation. autologous stem cell transplants. Available at: https://www. leukaemia.org.au/disease-information/transplants/autologous-transplants/ [Accessed March 25, 2019].
[88]
Canadian Blood Services. Therapeutic Apheresis. Available at: https://professionaleducation.blood.ca/en/transfusion/guide-clini que/therapeutic-apheresis [Accessed March 25, 2019]
[89]
Holt N, Wang J, Kim K, et al. Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo. Nat Biotechnol 2010; 28(8): 839-47.
[http://dx.doi.org/10.1038/nbt.1663] [PMID: 20601939]
[90]
Li L, Krymskaya L, Wang J, 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(6): 1259-69.
[http://dx.doi.org/10.1038/mt.2013.65] [PMID: 23587921]
[91]
Uniprot. Keyword - Zinc-Finger. [Accessed March 22, 2019]. Available at: https://www.uniprot.org/keywords/KW-0863
[92]
Lippow SM, Aha PM, Parker MH, Blake WJ, Baynes BM, Lipovšek D. Creation of a type IIS restriction endonuclease with a long recognition sequence. Nucleic Acids Res 2009; 37(9): 3061-73.
[http://dx.doi.org/10.1093/nar/gkp182] [PMID: 19304757]
[93]
Händel EM, Cathomen T. Zinc-finger nuclease based genome surgery: it’s all about specificity. Curr Gene Ther 2011; 11(1): 28-37.
[http://dx.doi.org/10.2174/156652311794520120] [PMID: 21182467]
[94]
Cheng LT, Sun LT, Tada T. Genome editing in induced pluripotent stem cells. Genes Cells 2012; 17(6): 431-8.
[http://dx.doi.org/10.1111/j.1365-2443.2012.01599.x] [PMID: 22487259]
[95]
Urnov FD, Rebar EJ, Holmes MC, Zhang HS, Gregory PD. Genome editing with engineered zinc finger nucleases. Nat Rev Genet 2010; 11(9): 636-46.
[http://dx.doi.org/10.1038/nrg2842] [PMID: 20717154]
[96]
Bogdanove AJ, Schornack S, Lahaye T. TAL effectors: finding plant genes for disease and defense. Curr Opin Plant Biol 2010; 13(4): 394-401.
[http://dx.doi.org/10.1016/j.pbi.2010.04.010] [PMID: 20570209]
[97]
Wright DA, Li T, Yang B, Spalding MH. TALEN-mediated genome editing: prospects and perspectives. Biochem J 2014; 462(1): 15-24.
[http://dx.doi.org/10.1042/BJ20140295] [PMID: 25057889]
[98]
Mussolino C, Cathomen T. TALE nucleases: tailored genome engineering made easy. Curr Opin Biotechnol 2012; 23(5): 644-50.
[http://dx.doi.org/10.1016/j.copbio.2012.01.013] [PMID: 22342754]
[99]
Cermak T, Doyle EL, Christian M, et al. Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting. Nucleic Acids Res 2011; 39(12)e82
[http://dx.doi.org/10.1093/nar/gkr218] [PMID: 21493687]
[100]
Geissler R, Scholze H, Hahn S, et al. Transcriptional activators of human genes with programmable DNA-specificity. PLoS One 2011; 6(5)e19509
[http://dx.doi.org/10.1371/journal.pone.0019509] [PMID: 21625585]
[101]
Expanding the Genetic Editing Tool Kit: ZFNs, TALENs, and CRISPR-Cas9 [March 24, 2019] https://www.jci.org/articles/view/72992/figure/2
[102]
Doyon Y, Vo TD, Mendel MC, et al. Enhancing zinc-finger-nuclease activity with improved obligate heterodimeric architectures. Nat Methods 2011; 8(1): 74-9.
[http://dx.doi.org/10.1038/nmeth.1539] [PMID: 21131970]
[103]
Beckman Coulter – Life Sciences. What Is the Difference between Non-Homologous End Joining (NHEJ) and Homology-Directed Repair (HDR)? [Accessed March 24, 2019]. Available at: https://www.beckman.fr/support/faq/research/non-homologous-end-joining-(nhej)-and-homology-directed-repair-(hdr)-difference
[104]
Cambridge Dictionary. Specificity. [Accessed march 22, 2019]. Available at: https://dictionary.cambridge.org/dictionary/english/specificity
[105]
Chandrasegaran S. Recent advances in the use of ZFN-mediated gene editing for human gene therapy. Cell Gene Ther Insights 2017; 3(1): 33-41.
[http://dx.doi.org/10.18609/cgti.2017.005] [PMID: 29270315]
[106]
Cathomen T, Joung JK. Zinc-finger Nucleases: The Next Generation Emerges. Mol Ther 2008; 16: 1200-7.
[http://dx.doi.org/10.1038/mt.2008.114]
[107]
Cornu TI, Thibodeau-Beganny S, Guhl E, Alwin S, et al. DNA-binding Specificity Is a Major Determinant of the Activity and Toxicity of Zinc-finger Nucleases. Mol Ther 2008; 16: 352-8.
[http://dx.doi.org/10.1038/sj.mt.6300357]
[108]
Mussolino C, Cathomen T. On target? Tracing zinc-finger-nuclease specificity. Nat Methods 2011; 8(9): 725-6.
[http://dx.doi.org/10.1038/nmeth.1680] [PMID: 21878917]
[109]
Pattanayak V, Ramirez CL, Joung JK, Liu DR. Revealing off-target cleavage specificities of zinc-finger nucleases by in vitro selection. Nat Methods 2011; 8(9): 765-70.
[http://dx.doi.org/10.1038/nmeth.1670] [PMID: 21822273]
[110]
Guilinger JP, Pattanayak V, Reyon D, et al. Broad specificity profiling of TALENs results in engineered nucleases with improved DNA-cleavage specificity. Nat Methods 2014; 11(4): 429-35.
[http://dx.doi.org/10.1038/nmeth.2845] [PMID: 24531420]
[111]
Mussolino C, Alzubi J, Fine EJ, et al. TALENs facilitate targeted genome editing in human cells with high specificity and low cytotoxicity. Nucleic Acids Res 2014; 42(10): 6762-73.
[http://dx.doi.org/10.1093/nar/gku305] [PMID: 24792154]
[112]
Lin Y, Fine EJ, Zheng Z, et al. SAPTA: a new design tool for improving TALE nuclease activity. Nucleic Acids Res 2014; 42(6)e47
[http://dx.doi.org/10.1093/nar/gkt1363] [PMID: 24442582]
[113]
Juillerat A, Pessereau C, Dubois G, et al. Optimized tuning of TALEN specificity using non-conventional RVDs. Sci Rep 2015; 5: 8150.
[http://dx.doi.org/10.1038/srep08150] [PMID: 25632877]
[114]
Smith J, Berg JM, Chandrasegaran S. A detailed study of the substrate specificity of a chimeric restriction enzyme. Nucleic Acids Res 1999; 27(2): 674-81.
[http://dx.doi.org/10.1093/nar/27.2.674] [PMID: 9862996]
[115]
Szczepek M, Brondani V, Büchel J, Serrano L, Segal DJ, Cathomen T. Structure-based redesign of the dimerization interface reduces the toxicity of zinc-finger nucleases. Nat Biotechnol 2007; 25(7): 786-93.
[http://dx.doi.org/10.1038/nbt1317] [PMID: 17603476]
[116]
Wah DA, Bitinaite J, Schildkraut I, Aggarwal AK. Structure of FokI has implications for DNA cleavage. Proc Natl Acad Sci USA 1998; 95(18): 10564-9.
[http://dx.doi.org/10.1073/pnas.95.18.10564] [PMID: 9724743]
[117]
Händel EM, Alwin S, Cathomen T. Expanding or restricting the target site repertoire of zinc-finger nucleases: the inter-domain linker as a major determinant of target site selectivity. Mol Ther 2009; 17(1): 104-11.
[http://dx.doi.org/10.1038/mt.2008.233] [PMID: 19002164]
[118]
Shim G, Kim D, Park GT, Jin H, Suh SK, Oh YK. Therapeutic gene editing: delivery and regulatory perspectives. Acta Pharmacol Sin 2017; 38(6): 738-53.
[http://dx.doi.org/10.1038/aps.2017.2] [PMID: 28392568]
[119]
Kamimura K, Suda T, Zhang G, Liu D. Advances in Gene Delivery Systems. Pharmaceut Med 2011; 25(5): 293-306.
[http://dx.doi.org/10.1007/BF03256872] [PMID: 22200988]
[120]
Chira S, Jackson CS, Oprea I, et al. Progresses towards safe and efficient gene therapy vectors. Oncotarget 2015; 6(31): 30675-703.
[http://dx.doi.org/10.18632/oncotarget.5169] [PMID: 26362400]
[121]
Cox DBT, Platt RJ, Zhang F. Therapeutic genome editing: prospects and challenges. Nat Med 2015; 21(2): 121-31.
[http://dx.doi.org/10.1038/nm.3793] [PMID: 25654603]
[122]
Loske AM, Fernández F, Gómez-Lim M, Rivera AL. Genetic Transformation of Cells using Physical Methods. J Genet Syndr Gene Ther 2014; 5: 4.
[http://dx.doi.org/10.4172/2157-7412.1000237]
[123]
Nayerossadat N, Maedeh T, Ali PA. Viral and nonviral delivery systems for gene delivery. Adv Biomed Res 2012; 1: 27.
[http://dx.doi.org/10.4103/2277-9175.98152] [PMID: 23210086]
[124]
Ho BX, Loh SJH, Chan WK, Soh BS. In vivo genome editing as a therapeutic approach. Int J Mol Sci 2018; 19(9): 2721.
[http://dx.doi.org/10.3390/ijms19092721] [PMID: 30213032]
[125]
Kotterman MA, Schaffer DV. Engineering adeno-associated viruses for clinical gene therapy. Nat Rev Genet 2014; 15(7): 445-51.
[http://dx.doi.org/10.1038/nrg3742] [PMID: 24840552]
[126]
Daya S, Berns KI. Gene therapy using adeno-associated virus vectors. Clin Microbiol Rev 2008; 21(4): 583-93.
[http://dx.doi.org/10.1128/CMR.00008-08] [PMID: 18854481]
[127]
Guha TK, Wai A, Hausner G. Programmable genome editing tools and their regulation for efficient genome engineering. Comput Struct Biotechnol J 2017; 15: 146-60.
[http://dx.doi.org/10.1016/j.csbj.2016.12.006] [PMID: 28179977]
[128]
Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E. A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 2012; 337(6096): 816-21.
[http://dx.doi.org/10.1126/science.1225829] [PMID: 22745249]
[129]
Lin C. Characterization and Optimization of the CRISPR/Cas System for Applications in Genome Engineering. Harvard Library 2014.
[130]
Sorek R, Kunin V, Hugenholtz P. CRISPR--a widespread system that provides acquired resistance against phages in bacteria and archaea. Nat Rev Microbiol 2008; 6(3): 181-6.
[http://dx.doi.org/10.1038/nrmicro1793] [PMID: 18157154]
[131]
Bolotin A, Quinquis B, Sorokin A, Ehrlich SD. Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. Microbiology 2005; 151(Pt 8): 2551-61.
[http://dx.doi.org/10.1099/mic.0.28048-0] [PMID: 16079334]
[132]
Bacteriophage. https://www.britannica.com/science/bacteriophage [March 28, 2019]
[133]
Barrangou R, Fremaux C, Deveau H, et al. CRISPR provides acquired resistance against viruses in prokaryotes. Science 2007; 315(5819): 1709-12.
[http://dx.doi.org/10.1126/science.1138140] [PMID: 17379808]
[134]
There’s CRISPR in Your Yogurt. https://www.the-scientist.com/notebook/theres-crispr-in-your-yogurt-36142 [March 29, 2019].
[135]
Hao M, Cui Y, Qu X. Analysis of CRISPR-cas system in Streptococcus thermophilus and its application. Front Microbiol 2018; 9: 257.
[http://dx.doi.org/10.3389/fmicb.2018.00257] [PMID: 29515542]
[136]
Datsenko KA, Pougach K, Tikhonov A, Wanner BL, Severinov K, Semenova E. Molecular memory of prior infections activates the CRISPR/Cas adaptive bacterial immunity system. Nat Commun 2012; 3: 945.
[http://dx.doi.org/10.1038/ncomms1937] [PMID: 22781758]
[137]
Jansen R, Embden JD, Gaastra W, Schouls LM. Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 2002; 43(6): 1565-75.
[http://dx.doi.org/10.1046/j.1365-2958.2002.02839.x] [PMID: 11952905]
[138]
Mali P, Yang L, Esvelt KM, et al. RNA-guided human genome engineering via Cas9. Science 2013; 339(6121): 823-6.
[http://dx.doi.org/10.1126/science.1232033] [PMID: 23287722]
[139]
Zhang F, Wen Y, Guo X. CRISPR/Cas9 for genome editing: progress, implications and challenges. Hum Mol Genet 2014; 23(R1): R40-6.
[http://dx.doi.org/10.1093/hmg/ddu125] [PMID: 24651067]
[140]
Xiao Q, Guo D, Chen S. Application of CRISPR/Cas9-Based Gene Editing in HIV-1/AIDS Therapy. Front Cell Infect Microbiol 2019; 9: 69.
[http://dx.doi.org/10.3389/fcimb.2019.00069] [PMID: 30968001]
[141]
Allen AG, Chung CH, Atkins A, et al. Gene Editing of HIV-1 Co-receptors to Prevent and/or Cure Virus Infection. Front Microbiol 2018; 9: 2940.
[http://dx.doi.org/10.3389/fmicb.2018.02940] [PMID: 30619107]
[142]
Chylinski K, Makarova KS, Charpentier E, Koonin EV. Classification and evolution of type II CRISPR-Cas systems. Nucleic Acids Res 2014; 42(10): 6091-105.
[http://dx.doi.org/10.1093/nar/gku241] [PMID: 24728998]
[143]
Cong L, Ran FA, Cox D, et al. Multiplex genome engineering using CRISPR/Cas systems. Science 2013; 339(6121): 819-23.
[http://dx.doi.org/10.1126/science.1231143] [PMID: 23287718]
[144]
Le Rhun A, Escalera-Maurer A, Bratovič M, Charpentier E. CRISPR-Cas in Streptococcus pyogenes. RNA Biol 2019; 16(4): 380-9.
[http://dx.doi.org/10.1080/15476286.2019.1582974] [PMID: 30856357]
[145]
Hu X. CRISPR/Cas9 system and its applications in human hematopoietic cells. Blood Cells Mol Dis 2016; 62: 6-12.
[http://dx.doi.org/10.1016/j.bcmd.2016.09.003] [PMID: 27736664]
[146]
Swarts DC, Mosterd C, van Passel MWJ, Brouns SJJ. CRISPR interference directs strand specific spacer acquisition. PLoS One 2012; 7(4)e35888
[http://dx.doi.org/10.1371/journal.pone.0035888] [PMID: 22558257]
[147]
Dai WJ, Zhu LY, Yan ZY, Xu Y, Wang QL, Lu XJ. CRISPR-Cas9 for in vivo Gene Therapy: Promise and Hurdles. Mol Ther Nucleic Acids 2016; 5e349.
[http://dx.doi.org/10.1038/mtna.2016.58] [PMID: 28131272]
[148]
Lino CA, Harper JC, Carney JP, Timlin JA. Delivering CRISPR: a review of the challenges and approaches. Drug Deliv 2018; 25(1): 1234-57.
[http://dx.doi.org/10.1080/10717544.2018.1474964] [PMID: 29801422]
[149]
Lin C. Characterization and Optimization of the CRISPR/Cas System for Applications in Genome Engineering Doctoral dissertation, Office of Scholarly Communication at Harvard Medical School 2014.
[150]
Wu X, Kriz AJ, Sharp PA. Target specificity of the CRISPR-Cas9 system. Quant Biol 2014; 2(2): 59-70.
[http://dx.doi.org/10.1007/s40484-014-0030-x] [PMID: 25722925]
[151]
Ma Y, Zhang L, Huang X. Genome modification by CRISPR/Cas9. FEBS J 2014; 281(23): 5186-93.
[http://dx.doi.org/10.1111/febs.13110] [PMID: 25315507]
[152]
Saayman S, Ali SA, Morris KV, Weinberg MS. The therapeutic application of CRISPR/Cas9 technologies for HIV. Expert Opin Biol Ther 2015; 15(6): 819-30.
[http://dx.doi.org/10.1517/14712598.2015.1036736] [PMID: 25865334]
[153]
Liu C, Zhang L, Liu H, Cheng K. Delivery strategies of the CRISPR-Cas9 gene-editing system for therapeutic applications. J Control Release 2017; 266: 17-26.
[http://dx.doi.org/10.1016/j.jconrel.2017.09.012] [PMID: 28911805]
[154]
Oude Blenke E, Evers MJW, Mastrobattista E, van der Oost J. CRISPR-Cas9 gene editing: Delivery aspects and therapeutic potential. J Control Release 2016; 244(Pt B): 139-48
[http://dx.doi.org/10.1016/j.jconrel.2016.08.002] [PMID: 27498021]
[155]
Elaswad A, Khalil K, Cline D, et al. Microinjection of CRISPR/Cas9 Protein into Channel Catfish, Ictalurus punctatus, Embryos for Gene Editing. J Vis Exp 2018; 131.
[http://dx.doi.org/10.3791/56275] [PMID: 29443028]
[156]
Fact Sheets about Microinjection — the Definition, Types, Advantages and Applications [April 7, 2019]; https://medium.com/@contact_28660/fact-sheets-about-microinjection-the-definitio
[157]
Potter H. Transfection by electroporation. Curr Protoc Mol Biol 2003; Chapter 9: 3.
[PMID: 18265334]
[158]
Xu L, Wang J, Liu Y, et al. CRISPR-Edited Stem Cells in a Patient with HIV and Acute Lymphocytic Leukemia. N Engl J Med 2019; 381: 1240-1247.
[159]
Wu Z, Yang H, Colosi P. Effect of genome size on AAV vector packaging. Mol Ther 2010; 18(1): 80-6.
[http://dx.doi.org/10.1038/mt.2009.255] [PMID: 19904234]
[160]
Ran FA, Cong L, Yan WX, et al. In vivo genome editing using Staphylococcus aureus Cas9. Nature 2015; 520(7546): 186-91.
[http://dx.doi.org/10.1038/nature14299] [PMID: 25830891]
[161]
Xu CL, Ruan MZC, Mahajan VB, Tsang SH. Viral Delivery Systems for CRISPR. Viruses 2019; 11(1): 28.
[http://dx.doi.org/10.3390/v11010028] [PMID: 30621179]
[162]
Zhang Y, Ge X, Yang F, et al. Comparison of non-canonical PAMs for CRISPR/Cas9-mediated DNA cleavage in human cells. Sci Rep 2014; 4: 5405.
[http://dx.doi.org/10.1038/srep05405] [PMID: 24956376]
[163]
Zhang XH, Tee LY, Wang XG, Huang QS, Yang SH. Off-target Effects in CRISPR/Cas9-mediated Genome Engineering. Mol Ther Nucleic Acids 2015; 4e264
[http://dx.doi.org/10.1038/mtna.2015.37] [PMID: 26575098]
[164]
Labuhn M, Adams FF, Ng M, et al. Refined sgRNA efficacy prediction improves large- and small-scale CRISPR-Cas9 applications. Nucleic Acids Res 2018; 46(3): 1375-85.
[http://dx.doi.org/10.1093/nar/gkx1268] [PMID: 29267886]
[165]
Guilinger JP, Thompson DB, Liu DR. Fusion of catalytically inactive Cas9 to FokI nuclease improves the specificity of genome modification. Nat Biotechnol 2014; 32(6): 577-82.
[http://dx.doi.org/10.1038/nbt.2909] [PMID: 24770324]
[166]
Dash PK, Kaminski R, Bella R, et al. Sequential LASER ART and CRISPR Treatments Eliminate HIV-1 in a Subset of Infected Humanized Mice. Nat Commun 2019; 10(1): 2753.
[http://dx.doi.org/10.1038/s41467-019-10366-y] [PMID: 31266936]
[167]
Weeks DP, Spalding MH, Yang B. Use of designer nucleases for targeted gene and genome editing in plants. Plant Biotechnol J 2016; 14(2): 483-95.
[http://dx.doi.org/10.1111/pbi.12448] [PMID: 26261084]


Rights & PermissionsPrintExport Cite as

Article Details

VOLUME: 17
ISSUE: 5
Year: 2019
Page: [306 - 323]
Pages: 18
DOI: 10.2174/1570162X17666191025112918
Price: $58

Article Metrics

PDF: 22
HTML: 1

Special-new-year-discount