Genome Editing B.C. (Before CRISPR): Lasting Lessons from the "Old Testament".

Genome editing with engineered nucleases, a powerful tool for understanding biological function and revealing causality, was built in a joint effort by academia and industry in 1994-2010. Use of CRISPR-Cas9 is the most recent (2013-), and facile, implementation of the resulting editing toolbox. Principles and methods of genome editing from the pre-CRISPR era remain relevant and continue to be useful.

[1]  Jens Boch,et al.  Breaking the Code of DNA Binding Specificity of TAL-Type III Effectors , 2009, Science.

[2]  M. Rudnicki,et al.  Inactivation of MyoD in mice leads to up-regulation of the myogenic HLH gene Myf-5 and results in apparently normal muscle development , 1992, Cell.

[3]  Wenyi Wei,et al.  Bypass of senescence after disruption of p21CIP1/WAF1 gene in normal diploid human fibroblasts. , 1997, Science.

[4]  Matthew J. Moscou,et al.  A Simple Cipher Governs DNA Recognition by TAL Effectors , 2009, Science.

[5]  M. Jasin,et al.  Double-strand-break-induced homologous recombination in mammalian cells. , 2001, Biochemical Society transactions.

[6]  R. Jaenisch,et al.  Efficient targeting of expressed and silent genes in human ESCs and iPSCs using zinc-finger nucleases , 2009, Nature Biotechnology.

[7]  Ignacio Anegon,et al.  Knockout Rats via Embryo Microinjection of Zinc-Finger Nucleases , 2009, Science.

[8]  Gabriela Plesa,et al.  Efficient clinical scale gene modification via zinc finger nuclease-targeted disruption of the HIV co-receptor CCR5. , 2013, Human gene therapy.

[9]  J. Doudna,et al.  A Programmable Dual-RNA–Guided DNA Endonuclease in Adaptive Bacterial Immunity , 2012, Science.

[10]  B. Dujon,et al.  Homologous recombination in plant cells is enhanced by in vivo induction of double strand breaks into DNA by a site-specific endonuclease. , 1993, Nucleic acids research.

[11]  Jac A. Nickoloff,et al.  Gene Conversion Tracts from Double-Strand Break Repair in Mammalian Cells , 1998, Molecular and Cellular Biology.

[12]  J. Byrne Generation of isogenic pluripotent stem cells. , 2008, Human molecular genetics.

[13]  J. Haber A Life Investigating Pathways That Repair Broken Chromosomes. , 2016, Annual review of genetics.

[14]  K. Kinzler,et al.  Facile methods for generating human somatic cell gene knockouts using recombinant adeno-associated viruses. , 2004, Nucleic acids research.

[15]  Le Cong,et al.  Multiplex Genome Engineering Using CRISPR/Cas Systems , 2013, Science.

[16]  Dana Carroll,et al.  Enhancing Gene Targeting with Designed Zinc Finger Nucleases , 2003, Science.

[17]  T. Morgan,et al.  SEX LIMITED INHERITANCE IN DROSOPHILA. , 2022, Science.

[18]  X. Darzacq,et al.  Mutations in the promoter of the telomerase gene TERT contribute to tumorigenesis by a two-step mechanism , 2017, Science.

[19]  A. Klug,et al.  A rapid, generally applicable method to engineer zinc fingers illustrated by targeting the HIV-1 promoter , 2001, Nature Biotechnology.

[20]  K. Makino,et al.  Unusual nucleotide arrangement with repeated sequences in the Escherichia coli K-12 chromosome , 1989, Journal of bacteriology.

[21]  S. Wolfe,et al.  Efficient targeted mutagenesis in the monarch butterfly using zinc-finger nucleases , 2013, Genome research.

[22]  Jeffrey C. Miller,et al.  An unbiased genome-wide analysis of zinc-finger nuclease specificity , 2011, Nature Biotechnology.

[23]  Shondra M Pruett-Miller,et al.  High-frequency genome editing using ssDNA oligonucleotides with zinc-finger nucleases , 2011, Nature Methods.

[24]  P. Rouet,et al.  Introduction of double-strand breaks into the genome of mouse cells by expression of a rare-cutting endonuclease. , 1994, Molecular and cellular biology.

[25]  Marcello Maresca,et al.  Obligate Ligation-Gated Recombination (ObLiGaRe): Custom-designed nuclease-mediated targeted integration through nonhomologous end joining , 2013, Genome research.

[26]  Thuy D. Vo,et al.  Rapid and efficient clathrin-mediated endocytosis revealed in genome-edited mammalian cells , 2011, Nature Cell Biology.

[27]  J. Vogel,et al.  CRISPR RNA maturation by trans-encoded small RNA and host factor RNase III , 2011, Nature.

[28]  M. Llinás,et al.  Site-specific genome editing in Plasmodium falciparum using engineered zinc-finger nucleases , 2012, Nature Methods.

[29]  Vanessa Taupin,et al.  Human hematopoietic stem/progenitor cells modified by zinc-finger nucleases targeted to CCR5 control HIV-1 in vivo , 2010, Nature Biotechnology.

[30]  K. Makino,et al.  Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product , 1987, Journal of bacteriology.

[31]  Feng Zhang,et al.  Improving cold storage and processing traits in potato through targeted gene knockout. , 2016, Plant biotechnology journal.

[32]  Ronnie J Winfrey,et al.  Rapid "open-source" engineering of customized zinc-finger nucleases for highly efficient gene modification. , 2008, Molecular cell.

[33]  R. Barrangou,et al.  CRISPR Provides Acquired Resistance Against Viruses in Prokaryotes , 2007, Science.

[34]  Ronnie J Winfrey,et al.  High frequency modification of plant genes using engineered zinc finger nucleases , 2009, Nature.

[35]  R. Barrangou,et al.  Cas9–crRNA ribonucleoprotein complex mediates specific DNA cleavage for adaptive immunity in bacteria , 2012, Proceedings of the National Academy of Sciences.

[36]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[37]  Jack W. Szostak,et al.  The double-strand-break repair model for recombination , 1983, Cell.

[38]  Dana Carroll,et al.  Stimulation of Homologous Recombination through Targeted Cleavage by Chimeric Nucleases , 2001, Molecular and Cellular Biology.

[39]  Philippe Horvath,et al.  The CRISPR/Cas bacterial immune system cleaves bacteriophage and plasmid DNA , 2010, Nature.

[40]  Matthew C. Canver,et al.  BCL11A enhancer dissection by Cas9-mediated in situ saturating mutagenesis , 2015, Nature.

[41]  Lei Zhang,et al.  Functional genomics, proteomics, and regulatory DNA analysis in isogenic settings using zinc finger nuclease-driven transgenesis into a safe harbor locus in the human genome. , 2010, Genome research.

[42]  S. Ehrlich,et al.  Clustered regularly interspaced short palindrome repeats (CRISPRs) have spacers of extrachromosomal origin. , 2005, Microbiology.

[43]  Varsha Singh,et al.  General Nature of the Genetic Code for Proteins , 2019 .

[44]  R. W. Davis,et al.  Replacement of chromosome segments with altered DNA sequences constructed in vitro. , 1979, Proceedings of the National Academy of Sciences of the United States of America.

[45]  A. Bradley,et al.  Targeted gene correction of α1-antitrypsin deficiency in induced pluripotent stem cells , 2011, Nature.

[46]  R. Jaenisch,et al.  Induced Pluripotent Stem Cells Meet Genome Editing. , 2016, Cell stem cell.

[47]  Michael R. Green,et al.  Expressing the human genome , 2001, Nature.

[48]  Jeffry D Sander,et al.  FLAsH assembly of TALeNs for high-throughput genome editing , 2022 .

[49]  Fyodor D Urnov,et al.  Targeted gene addition into a specified location in the human genome using designed zinc finger nucleases , 2007, Proceedings of the National Academy of Sciences.

[50]  Bernard Dujon,et al.  An intron-encoded protein is active in a gene conversion process that spreads an intron into a mitochondrial gene , 1985, Cell.

[51]  Y. Doyon,et al.  Precise genome modification in the crop species Zea mays using zinc-finger nucleases , 2009, Nature.

[52]  Erin L. Doyle,et al.  Efficient design and assembly of custom TALEN and other TAL effector-based constructs for DNA targeting , 2011, Nucleic acids research.

[53]  M. Noyes,et al.  Targeted gene inactivation in zebrafish using engineered zinc-finger nucleases , 2008, Nature Biotechnology.

[54]  H. Khorana,et al.  Studies on polynucleotides. XCVI. Repair replications of short synthetic DNA's as catalyzed by DNA polymerases. , 1971, Journal of molecular biology.

[55]  Deniz M. Ozata,et al.  CRISPR/Cas9-mediated genome editing induces exon skipping by alternative splicing or exon deletion , 2017, Genome Biology.

[56]  James E. DiCarlo,et al.  RNA-Guided Human Genome Engineering via Cas9 , 2013, Science.

[57]  Fyodor Urnov,et al.  Chromosomal translocations induced at specified loci in human stem cells , 2009, Proceedings of the National Academy of Sciences.

[58]  Stan J. J. Brouns,et al.  Small CRISPR RNAs Guide Antiviral Defense in Prokaryotes , 2008, Science.

[59]  B. Zeitler,et al.  Efficient targeted gene disruption in the soma and germ line of the frog Xenopus tropicalis using engineered zinc-finger nucleases , 2011, Proceedings of the National Academy of Sciences.

[60]  Isaac B. Hilton,et al.  Editing the epigenome: technologies for programmable transcription and epigenetic modulation , 2016, Nature Methods.

[61]  Jeffrey C. Miller,et al.  Highly efficient endogenous human gene correction using designed zinc-finger nucleases , 2005, Nature.

[62]  T. Hocking,et al.  Heritable Targeted Gene Disruption in Zebrafish Using Designed Zinc Finger Nucleases , 2008, Nature Biotechnology.

[63]  Adrian J. Thrasher,et al.  Molecular remission of infant B-ALL after infusion of universal TALEN gene-edited CAR T cells , 2017, Science Translational Medicine.

[64]  D. F. Carlson,et al.  Efficient nonmeiotic allele introgression in livestock using custom endonucleases , 2013, Proceedings of the National Academy of Sciences.

[65]  Prashant Mali,et al.  Gene targeting of a disease-related gene in human induced pluripotent stem and embryonic stem cells. , 2009, Cell stem cell.

[66]  K. Mullis,et al.  Primer-directed enzymatic amplification of DNA with a thermostable DNA polymerase. , 1988, Science.

[67]  G Vergnaud,et al.  CRISPR elements in Yersinia pestis acquire new repeats by preferential uptake of bacteriophage DNA, and provide additional tools for evolutionary studies. , 2005, Microbiology.

[68]  Yuri R. Bendaña,et al.  Functional footprinting of regulatory DNA , 2015, Nature Methods.

[69]  X. Yang,et al.  Long-Term Engraftment and Fetal Globin Induction upon BCL11A Gene Editing in Bone-Marrow-Derived CD34+ Hematopoietic Stem and Progenitor Cells , 2017, Molecular therapy. Methods & clinical development.

[70]  A. C. Chang,et al.  Construction of biologically functional bacterial plasmids in vitro. , 1973, Proceedings of the National Academy of Sciences of the United States of America.

[71]  N. Grishin,et al.  A putative RNA-interference-based immune system in prokaryotes: computational analysis of the predicted enzymatic machinery, functional analogies with eukaryotic RNAi, and hypothetical mechanisms of action , 2006, Biology Direct.

[72]  L. Marraffini,et al.  CRISPR Interference Limits Horizontal Gene Transfer in Staphylococci by Targeting DNA , 2008, Science.

[73]  N. Pavletich,et al.  Zinc finger-DNA recognition: crystal structure of a Zif268-DNA complex at 2.1 A , 1991, Science.

[74]  A. Klug,et al.  Targeted gene knockout in mammalian cells by using engineered zinc-finger nucleases , 2008, Proceedings of the National Academy of Sciences.

[75]  Dana Carroll,et al.  Targeted chromosomal cleavage and mutagenesis in Drosophila using zinc-finger nucleases. , 2002, Genetics.

[76]  S Chandrasegaran,et al.  Hybrid restriction enzymes: zinc finger fusions to Fok I cleavage domain. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[77]  J. Strathern,et al.  Homothallic switching of yeast mating type cassettes is initiated by a double-stranded cut in the MAT locus , 1982, Cell.

[78]  Jennifer Doudna,et al.  RNA-programmed genome editing in human cells , 2013, eLife.

[79]  Philip D. Gregory,et al.  Translating Dosage Compensation to Trisomy 21 , 2013, Nature.

[80]  A. Wolffe,et al.  Nuclear assembly, structure, and function: the use of Xenopus in vitro systems. , 1993, Experimental cell research.

[81]  Param Priya Singh,et al.  A Platform for Rapid Exploration of Aging and Diseases in a Naturally Short-Lived Vertebrate , 2015, Cell.

[82]  E. Rebar,et al.  Genome editing with engineered zinc finger nucleases , 2010, Nature Reviews Genetics.

[83]  O. Elemento,et al.  TET proteins safeguard bivalent promoters from de novo methylation in human embryonic stem cells , 2017, Nature Genetics.

[84]  D. Russell,et al.  Targeted transgene insertion into human chromosomes by adeno-associated virus vectors , 2002, Nature Biotechnology.

[85]  P. Gregory,et al.  Gene editing in human stem cells using zinc finger nucleases and integrase-defective lentiviral vector delivery , 2007, Nature Biotechnology.

[86]  Christof von Kalle,et al.  A serious adverse event after successful gene therapy for X-linked severe combined immunodeficiency. , 2003, The New England journal of medicine.

[87]  Elo Leung,et al.  A TALE nuclease architecture for efficient genome editing , 2011, Nature Biotechnology.

[88]  Mario R. Capecchi,et al.  High frequency targeting of genes to specific sites in the mammalian genome , 1986, Cell.

[89]  Eunji Kim,et al.  Targeted chromosomal deletions in human cells using zinc finger nucleases. , 2010, Genome research.

[90]  A Klug,et al.  Repetitive zinc‐binding domains in the protein transcription factor IIIA from Xenopus oocytes. , 1985, The EMBO journal.

[91]  Elo Leung,et al.  Targeted Genome Editing Across Species Using ZFNs and TALENs , 2011, Science.

[92]  G. Fink,et al.  Transformation of yeast. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[93]  F. Deist,et al.  Gene therapy of human severe combined immunodeficiency (SCID)-X1 disease. , 2000, Science.

[94]  Seung Woo Cho,et al.  Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease , 2013, Nature Biotechnology.

[95]  Francis Crick,et al.  The Genetic Code for Proteins , 1963 .

[96]  C. Pabo,et al.  Zinc finger phage: affinity selection of fingers with new DNA-binding specificities. , 1994, Science.

[97]  Namritha Ravinder,et al.  Enhanced CRISPR/Cas9-mediated precise genome editing by improved design and delivery of gRNA, Cas9 nuclease, and donor DNA. , 2017, Journal of biotechnology.

[98]  Susan Lindquist,et al.  Generation of Isogenic Pluripotent Stem Cells Differing Exclusively at Two Early Onset Parkinson Point Mutations , 2011, Cell.

[99]  Hojun Li,et al.  In vivo genome editing restores hemostasis in a mouse model of hemophilia , 2011, Nature.

[100]  J. García-Martínez,et al.  Intervening Sequences of Regularly Spaced Prokaryotic Repeats Derive from Foreign Genetic Elements , 2005, Journal of Molecular Evolution.

[101]  Jeffry D. Sander,et al.  Efficient In Vivo Genome Editing Using RNA-Guided Nucleases , 2013, Nature Biotechnology.

[102]  Yolanda Santiago,et al.  Zinc-finger nuclease-driven targeted integration into mammalian genomes using donors with limited chromosomal homology , 2010, Nucleic acids research.

[103]  General , 1970 .

[104]  J. Haber,et al.  Repair of a Site-Specific DNA Cleavage: Old-School Lessons for Cas9-Mediated Gene Editing. , 2017, ACS chemical biology.

[105]  Wei-Ting Hwang,et al.  Gene editing of CCR5 in autologous CD4 T cells of persons infected with HIV. , 2014, The New England journal of medicine.

[106]  A. James,et al.  orco mutant mosquitoes lose strong preference for humans and are not repelled by volatile DEET , 2013, Nature.

[107]  Dana Carroll,et al.  Genome engineering with targetable nucleases. , 2014, Annual review of biochemistry.

[108]  Philippe Horvath,et al.  A decade of discovery: CRISPR functions and applications , 2017, Nature Microbiology.

[109]  J. Orange,et al.  Establishment of HIV-1 resistance in CD4+ T cells by genome editing using zinc-finger nucleases , 2008, Nature Biotechnology.

[110]  R. Stewart,et al.  Induced Pluripotent Stem Cell Lines Derived from Human Somatic Cells , 2007, Science.

[111]  CRISPR/Cas9 mediated mutation of mouse IL-1α nuclear localisation sequence abolishes expression , 2017, Scientific Reports.

[112]  J. Doudna,et al.  The new frontier of genome engineering with CRISPR-Cas9 , 2014, Science.