Skip to main content

Transgenesis and Genome Engineering: A Historical Review

  • Protocol
  • First Online:
Transgenesis

Part of the book series: Methods in Molecular Biology ((MIMB,volume 2631))

Abstract

Our ability to modify DNA molecules and to introduce them into mammalian cells or embryos almost appears in parallel, starting from the 1970s of the last century. Genetic engineering techniques rapidly developed between 1970 and 1980. In contrast, robust procedures to microinject or introduce DNA constructs into individuals did not take off until 1980 and evolved during the following two decades. For some years, it was only possible to add transgenes, de novo, of different formats, including artificial chromosomes, in a variety of vertebrate species or to introduce specific mutations essentially in mice, thanks to the gene-targeting methods by homologous recombination approaches using mouse embryonic stem (ES) cells. Eventually, genome-editing tools brought the possibility to add or inactivate DNA sequences, at specific sites, at will, irrespective of the animal species involved. Together with a variety of additional techniques, this chapter will summarize the milestones in the transgenesis and genome engineering fields from the 1970s to date.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Protocol
USD 49.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 189.00
Price excludes VAT (USA)
  • Available as EPUB and PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 249.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Similar content being viewed by others

References

  1. Gordon JW, Ruddle FH (1982) Germ line transmission in transgenic mice. Prog Clin Biol Res 85 Pt B:111–124

    CAS  PubMed  Google Scholar 

  2. Palmiter RD, Chen HY, Brinster RL (1982) Differential regulation of metallothionein-thymidine kinase fusion genes in transgenic mice and their offspring. Cell 29:701–710

    CAS  PubMed  Google Scholar 

  3. Palmiter RD, Brinster RL et al (1982) Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 300:611–615

    CAS  PubMed  PubMed Central  Google Scholar 

  4. Petri W (1982) Transgenic organisms and development. Nature 299:399–400

    CAS  PubMed  Google Scholar 

  5. Ingles CJ, Shales M (1982) DNA-mediated transfer of an RNA polymerase II gene: reversion of the temperature-sensitive hamster cell cycle mutant TsAF8 by mammalian DNA. Mol Cell Biol 2:666–673

    CAS  PubMed  PubMed Central  Google Scholar 

  6. Doy CH, Gresshoff PM, Rolfe BG (1973) Biological and molecular evidence for the transgenosis of genes from bacteria to plant cells. Proc Natl Acad Sci U S A 70:723–726

    CAS  PubMed  PubMed Central  Google Scholar 

  7. Doy CH, Gresshoff PM, Rolfe BG (1973) Time-course of phenotypic expression of Escherichia coli gene Z following transgenosis in haploid Lycopersicon esculentum cells. Nat New Biol 244:90–91

    CAS  PubMed  Google Scholar 

  8. Giles KL, Whitehead H (1976) Uptake and continued metabolic activity of azotobacter within fungal protoplasts. Science 193:1125–1126

    CAS  PubMed  Google Scholar 

  9. McBride OW, Athwal RS (1976) Genetic analysis by chromosome-mediated gene transfer. In Vitro 12:777–786

    CAS  PubMed  Google Scholar 

  10. Fournier RE, Ruddle FH (1977) Stable association of the human transgenome and host murine chromosomes demonstrated with trispecific microcell hybrids. Proc Natl Acad Sci U S A 74:3937–3941

    CAS  PubMed  PubMed Central  Google Scholar 

  11. Miller CL, Ruddle FH (1978) Co-transfer of human X-linked markers into murine somatic cells via isolated metaphase chromosomes. Proc Natl Acad Sci U S A 75:3346–3350

    CAS  PubMed  PubMed Central  Google Scholar 

  12. McBride OW, Burch JW, Ruddle FH (1978) Cotransfer of thymidine kinase and galactokinase genes by chromosome-mediated gene transfer. Proc Natl Acad Sci U S A 75:914–918

    CAS  PubMed  PubMed Central  Google Scholar 

  13. Fournier RE, Juricek DK, Ruddle FH (1979) Somatic cell genetic analysis of transgenome integration. Somatic Cell Genet 5:1061–1077

    CAS  PubMed  Google Scholar 

  14. Klobutcher LA, Miller CL, Ruddle FH (1980) Chromosome-mediated gene transfer results in two classes of unstable transformants. Proc Natl Acad Sci U S A 77:3610–3614

    CAS  PubMed  PubMed Central  Google Scholar 

  15. Scangos G, Ruddle FH (1981) Mechanisms and applications of DNA-mediated gene transfer in mammalian cells – a review. Gene 14:1–10

    CAS  PubMed  Google Scholar 

  16. Bernstein A, Breitman M (1989) Genetic ablation in transgenic mice. Mol Biol Med 6:523–530

    CAS  PubMed  Google Scholar 

  17. Thomas KR, Capecchi MR (1986) Introduction of homologous DNA sequences into mammalian cells induces mutations in the cognate gene. Nature 324:34–38

    CAS  PubMed  Google Scholar 

  18. Thomas KR, Capecchi MR (1987) Site-directed mutagenesis by gene targeting in mouse embryo-derived stem cells. Cell 51:503–512

    CAS  PubMed  Google Scholar 

  19. Koller BH, Hagemann LJ, Doetschman T et al (1989) Germ-line transmission of a planned alteration made in a hypoxanthine phosphoribosyltransferase gene by homologous recombination in embryonic stem cells. Proc Natl Acad Sci U S A 86:8927–8931

    CAS  PubMed  PubMed Central  Google Scholar 

  20. Roemer K, Johnson PA, Friedmann T (1991) Knock-in and knock-out. Transgenes, development and disease: a keystone symposium sponsored by Genentech and Immunex, Tamarron, CO, USA, January 12–18, 1991. New Biol 3:331–335

    CAS  PubMed  Google Scholar 

  21. Ekker SC (2000) Morphants: a new systematic vertebrate functional genomics approach. Yeast 17:302–306

    CAS  PubMed  Google Scholar 

  22. Neilson R (1992) Proposals for the future regulation of biotechnology in Australia. Melb Univ Law Rev 18:692–698

    PubMed  Google Scholar 

  23. Mahaffee WF, Kloepper JW (1997) Bacterial communities of the rhizosphere and endorhiza associated with field-grown cucumber plants inoculated with a plant growth-promoting rhizobacterium or its genetically modified derivative. Can J Microbiol 43:344–353

    CAS  PubMed  Google Scholar 

  24. Somerville C (2000) The genetically modified organism conflict. Plant Physiol 123:1201–1202

    CAS  PubMed  PubMed Central  Google Scholar 

  25. Jensen KK, Gamborg C, Madsen KH et al (2003) Making the EU "risk window" transparent: the normative foundations of the environmental risk assessment of GMOs. Environ Biosaf Res 2:161–171

    Google Scholar 

  26. Fishman RE (1998) Patenting human beings: do sub-human creatures deserve constitutional protection? Am J Law Med 15:461–482

    Google Scholar 

  27. Birling MC, Fray MD, Kasparek P et al (2021) Importing genetically altered animals: ensuring quality. Mamm Genome. https://doi.org/10.1007/s00335-021-09908-x

  28. Lee HJ, Lee HC, Han JY (2015) Germline modification and engineering in avian species. Mol Cells 38:743–749

    CAS  PubMed  PubMed Central  Google Scholar 

  29. Chenouard V, Brusselle L, Heslan JM et al (2016) A rapid and cost-effective method for genotyping genome-edited animals: a heteroduplex mobility assay using microfluidic capillary electrophoresis. J Genet Genomics 43:341–348

    CAS  PubMed  Google Scholar 

  30. Bunton-Stasyshyn RK, Codner GF, Teboul L (2021) Screening and validation of genome-edited animals. Lab Anim. https://doi.org/10.1177/00236772211016922

  31. Kilby NJ, Snaith MR, Murray JA (1993) Site-specific recombinases: tools for genome engineering. Trends Genet 9:413–421

    CAS  PubMed  Google Scholar 

  32. Rossant J, Nagy A (1995) Genome engineering: the new mouse genetics. Nat Med 1:592–594

    CAS  PubMed  Google Scholar 

  33. Grand Moursel L, Visser M, Servant G et al (2021) CRISPRing future medicines. Expert Opin Drug Discov 16:463–473

    CAS  PubMed  Google Scholar 

  34. Stark WM, Akopian A (2003) Designer recombinases: tools to cut and paste genomic DNA sequences. Discov Med 3:34–35

    PubMed  Google Scholar 

  35. Miller JC, Holmes MC, Wang J et al (2007) An improved zinc-finger nuclease architecture for highly specific genome editing. Nat Biotechnol 25:778–785

    CAS  PubMed  Google Scholar 

  36. Modell AE, Lim D, Nguyen TM et al (2022) CRISPR-based therapeutics: current challenges and future applications. Trends Pharmacol Sci 43:151–161

    CAS  PubMed  Google Scholar 

  37. Jacques JP, Hausmann S, Kolakofsky D (1994) Paramyxovirus mRNA editing leads to G deletions as well as insertions. EMBO J 13:5496–5503

    CAS  PubMed  PubMed Central  Google Scholar 

  38. Bertoni C, Morris GE, Rando TA (2005) Strand bias in oligonucleotide-mediated dystrophin gene editing. Hum Mol Genet 14:221–233

    CAS  PubMed  Google Scholar 

  39. Mani M, Kandavelou K, Dy FJ et al (2005) Design, engineering, and characterization of zinc finger nucleases. Biochem Biophys Res Commun 335:447–457

    CAS  PubMed  Google Scholar 

  40. Sinsheimer RL (1977) Recombinant DNA. Annu Rev Biochem 46:415–438

    CAS  PubMed  Google Scholar 

  41. Jaenisch R, Mintz B (1974) Simian virus 40 DNA sequences in DNA of healthy adult mice derived from preimplantation blastocysts injected with viral DNA. Proc Natl Acad Sci U S A 71:1250–1254

    CAS  PubMed  PubMed Central  Google Scholar 

  42. Jaenisch R, Fan H, Croker B (1975) Infection of preimplantation mouse embryos and of newborn mice with leukemia virus: tissue distribution of viral DNA and RNA and leukemogenesis in the adult animal. Proc Natl Acad Sci U S A 72:4008–4012

    CAS  PubMed  PubMed Central  Google Scholar 

  43. Jaenisch R (1976) Germ line integration and Mendelian transmission of the exogenous Moloney leukemia virus. Proc Natl Acad Sci U S A 73:1260–1264

    CAS  PubMed  PubMed Central  Google Scholar 

  44. Gordon JW, Scangos GA, Plotkin DJ et al (1980) Genetic transformation of mouse embryos by microinjection of purified DNA. Proc Natl Acad Sci U S A 77:7380–7384

    CAS  PubMed  PubMed Central  Google Scholar 

  45. Capecchi MR (1980) High efficiency transformation by direct microinjection of DNA into cultured mammalian cells. Cell 22:479–488

    CAS  PubMed  Google Scholar 

  46. Gordon JW, Ruddle FH (1981) Integration and stable germ line transmission of genes injected into mouse pronuclei. Science 214:1244–1246

    CAS  PubMed  Google Scholar 

  47. Brinster RL, Chen HY, Trumbauer M, Senear AW, Warren R, Palmiter RD et al (1981) Somatic expression of herpes thymidine kinase in mice following injection of a fusion gene into eggs. Cell 27:223–231

    CAS  PubMed  PubMed Central  Google Scholar 

  48. Evans MJ, Kaufman MH (1981) Establishment in culture of pluripotential cells from mouse embryos. Nature 292:154–156

    CAS  PubMed  Google Scholar 

  49. Martin GR (1981) Isolation of a pluripotent cell line from early mouse embryos cultured in medium conditioned by teratocarcinoma stem cells. Proc Natl Acad Sci U S A 78:7634–7638

    CAS  PubMed  PubMed Central  Google Scholar 

  50. Brinster RL, Chen HY, Warren R et al (1982) Regulation of metallothionein--thymidine kinase fusion plasmids injected into mouse eggs. Nature 296:39–42

    CAS  PubMed  Google Scholar 

  51. Palmiter RD, Brinster RL, Hammer RE et al (1982) Dramatic growth of mice that develop from eggs microinjected with metallothionein-growth hormone fusion genes. Nature 300:611–615

    CAS  PubMed  PubMed Central  Google Scholar 

  52. Folger KR, Wong EA, Wahl G et al (1982) Patterns of integration of DNA microinjected into cultured mammalian cells: evidence for homologous recombination between injected plasmid DNA molecules. Mol Cell Biol 2:1372–1387

    CAS  PubMed  PubMed Central  Google Scholar 

  53. Gordon JW, Ruddle (1983) Gene transfer into mouse embryos: production of transgenic mice by pronuclear injection. Methods Enzymol 101:411–433

    CAS  PubMed  Google Scholar 

  54. Brinster RL, Palmiter RD (1984) Introduction of genes into the germ line of animals. Harvey Lect 80:1–38

    CAS  PubMed  PubMed Central  Google Scholar 

  55. Hammer RE, Palmiter RD, Brinster RL (1984) Partial correction of murine hereditary growth disorder by germ-line incorporation of a new gene. Nature 311:65–67

    CAS  PubMed  Google Scholar 

  56. Bradley A, Evans M, Kaufman MH et al (1984) Formation of germ-line chimaeras from embryo-derived teratocarcinoma cell lines. Nature 309:255–256

    CAS  PubMed  Google Scholar 

  57. Hammer RE, Pursel VG, Rexroad CE Jr et al (1985) Production of transgenic rabbits, sheep and pigs by microinjection. Nature 315:680–683

    CAS  PubMed  Google Scholar 

  58. Palmiter RD, Brinster RL (1985) Transgenic mice. Cell 41:343–345

    CAS  PubMed  Google Scholar 

  59. Brinster RL, Chen HY, Trumbauer ME et al (1985) Factors affecting the efficiency of introducing foreign DNA into mice by microinjecting eggs. Proc Natl Acad Sci U S A 82:4438–4442

    CAS  PubMed  PubMed Central  Google Scholar 

  60. Smithies O, Gregg RG, Boggs SS et al (1985) Insertion of DNA sequences into the human chromosomal beta-globin locus by homologous recombination. Nature 317:230–234

    CAS  PubMed  Google Scholar 

  61. Hogan B, Costantini F, Lacy E (1986) Manipulating the mouse embryo: a laboratory manual.. Cold Spring Harbor Laboratory Press, 1st edn. Cold Spring Harbor, New York

    Google Scholar 

  62. Hogan B, Beddington R, Costantini F, Lacy E (1994) Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press, 2nd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  63. Nagy A, Gerstenstein M, Vintersten K, Behringer R (2003) Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press, 3rd edn. Cold Spring Harbor, New York

    Google Scholar 

  64. Behringer R, Gerstenstein M, Vintersten K, Nagy A (2014) Manipulating the mouse embryo: a laboratory manual. Cold Spring Harbor Laboratory Press, 4th edn. Cold Spring Harbor, New York

    Google Scholar 

  65. Palmiter RD, Brinster RL (1986) Germ-line transformation of mice. Annu Rev Genet 20:465–499

    CAS  PubMed  PubMed Central  Google Scholar 

  66. Robertson E, Bradley A, Kuehn M, Evans M (1986) Germ-line transmission of genes introduced into cultured pluripotential cells by retroviral vector. Nature 323:445–448

    CAS  PubMed  Google Scholar 

  67. Bradley A, Robertson E (1986) Embryo-derived stem cells: a tool for elucidating the developmental genetics of the mouse. Curr Top Dev Biol 20:357–371

    CAS  PubMed  Google Scholar 

  68. Thomas KR, Folger KR, Capecchi MR (1986) High frequency targeting of genes to specific sites in the mammalian genome. Cell 144:419–428

    Google Scholar 

  69. Ishino Y, Shinagawa H, Makino K et al (1987) Nucleotide sequence of the iap gene, responsible for alkaline phosphatase isozyme conversion in Escherichia coli, and identification of the gene product. J Bacteriol 169:5429–5433

    CAS  PubMed  PubMed Central  Google Scholar 

  70. Hermans PW, van Soolingen D, Bik EM et al (1991) Insertion element IS987 from Mycobacterium bovis BCG is located in a hot-spot integration region for insertion elements in Mycobacterium tuberculosis complex strains. Infect Immun 59:2695–2705

    CAS  PubMed  PubMed Central  Google Scholar 

  71. Mojica FJ, Juez G, Rodríguez-Valera F (1993) Transcription at different salinities of Haloferax mediterranei sequences adjacent to partially modified PstI sites. Mol Microbiol 9:613–621

    CAS  PubMed  Google Scholar 

  72. Jansen R, Embden JD, Gaastra W et al (2002) Identification of genes that are associated with DNA repeats in prokaryotes. Mol Microbiol 43:1565–1575

    CAS  PubMed  Google Scholar 

  73. Brinster RL, Allen JM, Behringer RR, Gelinas RE, Palmiter RD (1988) Introns increase transcriptional efficiency in transgenic mice. Proc Natl Acad Sci U S A 85:836–840

    CAS  PubMed  PubMed Central  Google Scholar 

  74. Giraldo P, Montoliu L (2001) Size matters: use of YACs, BACs and PACs in transgenic animals. Transgenic Res 10:83–103

    CAS  PubMed  Google Scholar 

  75. Behringer RR, Mathews LS, Palmiter RD, Brinster RL (1988) Dwarf mice produced by genetic ablation of growth hormone-expressing cells. Genes Dev 2(4):453–461

    CAS  PubMed  Google Scholar 

  76. Mansour SL, Thomas KR, Capecchi MR (1988) Disruption of the proto-oncogene int-2 in mouse embryo-derived stem cells: a general strategy for targeting mutations to non-selectable genes. Nature 336:348–352

    CAS  PubMed  Google Scholar 

  77. Brinster RL, Braun RE, Lo D, Avarbock MR (1986) Targeted correction of a major histocompatibility class II E alpha gene by DNA microinjected into mouse eggs. Proc Natl Acad Sci U S A 86:7087–7091

    Google Scholar 

  78. Capecchi MR (1989) Altering the genome by homologous recombination. Science 244:1288–1292

    CAS  PubMed  Google Scholar 

  79. Thomas KR, Capecchi MR (1990) Targeted disruption of the murine int-1 proto-oncogene resulting in severe abnormalities in midbrain and cerebellar development. Nature 346:847–850

    CAS  PubMed  Google Scholar 

  80. McMahon AP, Bradley A (1990) The Wnt-1 (int-1) proto-oncogene is required for development of a large region of the mouse brain. Cell 62:1073–1085

    CAS  PubMed  Google Scholar 

  81. Eppig JT, Motenko H, Richardson JE (2015) The International Mouse Strain Resource (IMSR): cataloging worldwide mouse and ES cell line resources. Mamm Genome 26:448–455

    PubMed  PubMed Central  Google Scholar 

  82. Koopman P, Gubbay J, Vivian N et al (1991) Male development of chromosomally female mice transgenic for Sry. Nature 351:117–121

    CAS  PubMed  Google Scholar 

  83. Wright G, Carver A, Cottom D (1991) High level expression of active human alpha-1-antitrypsin in the milk of transgenic sheep. Biotechnology (N Y) 9:830–834

    CAS  PubMed  Google Scholar 

  84. Rubock MJ, Larin Z, Cook M (1990) A yeast artificial chromosome containing the mouse homeobox cluster Hox-2. Proc Natl Acad Sci U S A 87:4751–4755

    CAS  PubMed  PubMed Central  Google Scholar 

  85. Schedl A, Beermann F, Thies E et al (1992) Transgenic mice generated by pronuclear injection of a yeast artificial chromosome. Nucleic Acids Res 20:3073–3077

    CAS  PubMed  PubMed Central  Google Scholar 

  86. Strauss WM, Jaenisch R (1992) Molecular complementation of a collagen mutation in mammalian cells using yeast artificial chromosomes. EMBO J 11:417–422

    CAS  PubMed  PubMed Central  Google Scholar 

  87. Schedl A, Montoliu L, Kelsey G et al (1993) A yeast artificial chromosome covering the tyrosinase gene confers copy number-dependent expression in transgenic mice. Nature 362:258–261

    CAS  PubMed  Google Scholar 

  88. Strauss WM, Dausman J, Beard C (1993) Germ line transmission of a yeast artificial chromosome spanning the murine alpha 1(I) collagen locus. Science 259:1904–1907

    CAS  PubMed  Google Scholar 

  89. Jakobovits A, Moore AL, Green LL (1993) Germ-line transmission and expression of a human-derived yeast artificial chromosome. Nature 362:255–258

    CAS  PubMed  Google Scholar 

  90. Choi TK, Hollenbach PW, Pearson BE et al (1993) Transgenic mice containing a human heavy chain immunoglobulin gene fragment cloned in a yeast artificial chromosome. Nat Genet 4:117–1123

    CAS  PubMed  Google Scholar 

  91. Lamb BT, Sisodia SS, Lawler AM et al (1993) Introduction and expression of the 400 kilobase amyloid precursor protein gene in transgenic mice [corrected]. Nat Genet 5:22–30

    CAS  PubMed  Google Scholar 

  92. Davies NP, Rosewell IR, Richardson JC et al (1993) Creation of mice expressing human antibody light chains by introduction of a yeast artificial chromosome containing the core region of the human immunoglobulin kappa locus. Biotechnology (N Y) 11:911–914

    CAS  PubMed  Google Scholar 

  93. Gaensler KM, Kitamura M, Kan YW (1993) Germ-line transmission and developmental regulation of a 150-kb yeast artificial chromosome containing the human beta-globin locus in transgenic mice. Proc Natl Acad Sci U S A 90:11381–11385

    CAS  PubMed  PubMed Central  Google Scholar 

  94. Forget BG (1939) YAC transgenes: bigger is probably better. Proc Natl Acad Sci U S A 90:7909–7911

    Google Scholar 

  95. Linton MF, Farese RV Jr, Chiesa G (1993) Transgenic mice expressing high plasma concentrations of human apolipoprotein B100 and lipoprotein(a). J Clin Invest 92:3029–3037

    CAS  PubMed  PubMed Central  Google Scholar 

  96. Zhuang Y, Soriano P, Weintraub H (1994) The helix-loop-helix gene E2A is required for B cell formation. Cell 79:875–884

    CAS  PubMed  Google Scholar 

  97. Gu H, Marth JD, Orban PC (1994) Deletion of a DNA polymerase beta gene segment in T cells using cell type-specific gene targeting. Science 265:103–106

    CAS  PubMed  Google Scholar 

  98. Plück A (1996) Conditional mutagenesis in mice: the Cre/loxP recombination system. Int J Exp Pathol 77:269–278

    PubMed  PubMed Central  Google Scholar 

  99. Tronche F, Kellendonk C, Kretz O (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103

    CAS  PubMed  Google Scholar 

  100. Sharma S, Zhu J (2014) Immunologic applications of conditional gene modification technology in the mouse. Curr Protoc Immunol 2(105):10.34.1–10.34.13

    Google Scholar 

  101. Bradley A, Anastassiadis K, Ayadi A et al (2012) The mammalian gene function resource: the International Knockout Mouse Consortium. Mamm Genome 23:580–586

    PubMed  PubMed Central  Google Scholar 

  102. Friedel RH, Seisenberger C, Kaloff C et al (2007) EUCOMM–the European conditional mouse mutagenesis program. Brief Funct Genomic Proteomic 6:180–185

    CAS  PubMed  Google Scholar 

  103. Brown SD, Moore MW (2012) The International Mouse Phenotyping Consortium: past and future perspectives on mouse phenotyping. Mamm Genome 23:632–640

    CAS  PubMed  PubMed Central  Google Scholar 

  104. Metzger D, Clifford J, Chiba H et al (1995) Conditional site-specific recombination in mammalian cells using a ligand-dependent chimeric Cre recombinase. Proc Natl Acad Sci U S A 92:6991–6995

    CAS  PubMed  PubMed Central  Google Scholar 

  105. Birling MC, Gofflot F, Warot X (2009) Site-specific recombinases for manipulation of the mouse genome. Methods Mol Biol 561:245–263

    CAS  PubMed  Google Scholar 

  106. Kimura Y, Yanagimachi R (1995) Intracytoplasmic sperm injection in the mouse. Biol Reprod 52:709–720

    CAS  PubMed  Google Scholar 

  107. Rosenwaks Z, Pereira N (2017) The pioneering of intracytoplasmic sperm injection: historical perspectives. Reproduction 154:F71–F77

    CAS  PubMed  Google Scholar 

  108. Choulika A, Perrin A, Dujon B et al (1995) Induction of homologous recombination in mammalian chromosomes by using the I-SceI system of Saccharomyces cerevisiae. Mol Cell Biol 15:1968–1973

    CAS  PubMed  PubMed Central  Google Scholar 

  109. Epinat JC, Arnould S, Chames P et al (2003) A novel engineered meganuclease induces homologous recombination in yeast and mammalian cells. Nucleic Acids Res 31:2952–2962

    CAS  PubMed  PubMed Central  Google Scholar 

  110. Smith J, Grizot S, Arnould S (2006) A combinatorial approach to create artificial homing endonucleases cleaving chosen sequences. Nucleic Acids Res 34:e149

    PubMed  PubMed Central  Google Scholar 

  111. Fernández A, Josa S, Montoliu L (2017) A history of genome editing in mammals. Mamm Genome 28:237–246

    PubMed  Google Scholar 

  112. Campbell KH, McWhir J, Ritchie WA et al (1996) Sheep cloned by nuclear transfer from a cultured cell line. Nature 38:64–66

    Google Scholar 

  113. Gurdon JB, Elsdale TR, Fischberg M (1958) Sexually mature individuals of Xenopus laevis from the transplantation of single somatic nuclei. Nature 182:64–65

    CAS  PubMed  Google Scholar 

  114. Gurdon JB (1962) Adult frogs derived from the nuclei of single somatic cells. Dev Biol 4:256–273

    CAS  PubMed  Google Scholar 

  115. Willadsen SM (1986) Nuclear transplantation in sheep embryos. Nature 320:63–65

    CAS  PubMed  Google Scholar 

  116. Callaway E (2016) Dolly at 20: the inside story on the world’s most famous sheep. Nature 534:604–608

    CAS  PubMed  Google Scholar 

  117. Wilmut I, Schnieke AE, McWhir J (1997) Viable offspring derived from fetal and adult mammalian cells. Nature 385:810–813

    CAS  PubMed  Google Scholar 

  118. Hodgson J (1997) Dolly opens a farm full of possibilities. Nat Biotechnol 15:306

    CAS  PubMed  Google Scholar 

  119. Harris J (1997) “Goodbye Dolly?” The ethics of human cloning. J Med Ethics 23:353–360

    CAS  PubMed  PubMed Central  Google Scholar 

  120. Cibelli JB, Stice SL, Golueke PJ (1998) Cloned transgenic calves produced from nonquiescent fetal fibroblasts. Science 280:1256–1258

    CAS  PubMed  Google Scholar 

  121. Kato Y, Tani T, Sotomaru Y (1998) Eight calves cloned from somatic cells of a single adult. Science 282:2095–2098

    CAS  PubMed  Google Scholar 

  122. Wakayama T, Perry AC, Zuccotti M et al (1998) Full-term development of mice from enucleated oocytes injected with cumulus cell nuclei. Nature 294:369–374

    Google Scholar 

  123. Baguisi A, Behboodi E, Melican DT (1999) Production of goats by somatic cell nuclear transfer. Nat Biotechnol 17:456–461

    CAS  PubMed  Google Scholar 

  124. Polejaeva IA, Chen SH, Vaught TD et al (2000) Cloned pigs produced by nuclear transfer from adult somatic cells. Nature 407:86–90

    CAS  PubMed  Google Scholar 

  125. Zhou Q, Renard JP, Le Friec G (2003) Generation of fertile cloned rats by regulating oocyte activation. Science 302:1179

    CAS  PubMed  Google Scholar 

  126. Challah-Jacques M, Chesne P, Renard JP (2003) Production of cloned rabbits by somatic nuclear transfer. Cloning Stem Cells 5:295–299

    CAS  PubMed  Google Scholar 

  127. Galli C, Lagutina I, Crotti G et al (2003) Pregnancy: a cloned horse born to its dam twin. Nature 424:635

    CAS  PubMed  Google Scholar 

  128. Lee BC, Kim MK, Jang G et al (2005) Dogs cloned from adult somatic cells. Nature 437:641

    Google Scholar 

  129. Yang XW, Model P, Heintz N (1997) Homologous recombination based modification in Escherichia coli and germline transmission in transgenic mice of a bacterial artificial chromosome. Nat Biotechnol 15:859–865

    CAS  PubMed  Google Scholar 

  130. Muyrers JP, Zhang Y, Testa G et al (1999) Rapid modification of bacterial artificial chromosomes by ET-recombination. Nucleic Acids Res 27:1555–1557

    CAS  PubMed  PubMed Central  Google Scholar 

  131. Testa G, Zhang Y, Vintersten K et al (2003) Engineering the mouse genome with bacterial artificial chromosomes to create multipurpose alleles. Nat Biotechnol 21:443–447

    CAS  PubMed  Google Scholar 

  132. Van Keuren ML, Gavrilina GB, Filipiak WE et al (2009) Generating transgenic mice from bacterial artificial chromosomes: transgenesis efficiency, integration and expression outcomes. Transgenic Res 18:769–785

    CAS  PubMed  PubMed Central  Google Scholar 

  133. Ivics Z, Hackett PB, Plasterk RH et al (1997) Molecular reconstruction of sleeping beauty, a Tc1-like transposon from fish, and its transposition in human cells. Cell 91:501–510

    CAS  PubMed  Google Scholar 

  134. Izsvák Z, Ivics Z, Plasterk RH (2000) Sleeping beauty, a wide host-range transposon vector for genetic transformation in vertebrates. J Mol Biol 302:93–102

    PubMed  Google Scholar 

  135. Dupuy AJ, Clark K, Carlson CM (2002) Mammalian germ-line transgenesis by transposition. Proc Natl Acad Sci U S A 99:4495–4499

    CAS  PubMed  PubMed Central  Google Scholar 

  136. Zayed H, Izsvák Z, Walisko O et al (2004) Development of hyperactive sleeping beauty transposon vectors by mutational analysis. Mol Ther 9:292–304

    CAS  PubMed  Google Scholar 

  137. Katter K, Geurts AM, Hoffmann O et al (2013) Transposon-mediated transgenesis, transgenic rescue, and tissue-specific gene expression in rodents and rabbits. FASEB J 27:930–941

    CAS  PubMed  PubMed Central  Google Scholar 

  138. Geurts AM, Collier LS, Geurts JL et al (2006) Gene mutations and genomic rearrangements in the mouse as a result of transposon mobilization from chromosomal concatemers. PLoS Genet 29:e156

    Google Scholar 

  139. Schnieke AE, Kind AJ, Ritchie WA et al (1997) Human factor IX transgenic sheep produced by transfer of nuclei from transfected fetal fibroblasts. Science 278:2130–2133

    CAS  PubMed  Google Scholar 

  140. Cibelli JB, Stice SL, Golueke PJ et al (1998) Transgenic bovine chimeric offspring produced from somatic cell-derived stem-like cells. Nat Biotechnol 16:642–646

    CAS  PubMed  Google Scholar 

  141. Polejaeva IA (2001) Cloning pigs: advances and applications. Reprod Suppl 58:293–300

    CAS  PubMed  Google Scholar 

  142. Thomson JA, Itskovitz-Eldor J, Shapiro SS et al (1998) Embryonic stem cell lines derived from human blastocysts. Science 282:1145–1147

    CAS  PubMed  Google Scholar 

  143. Burley J (1999) The ethics of therapeutic and reproductive human cloning. Semin Cell Dev Biol 10:287–294

    CAS  PubMed  Google Scholar 

  144. Colman A, Kind A (2000) Therapeutic cloning: concepts and practicalities. Trends Biotechnol 18:192–196

    CAS  PubMed  Google Scholar 

  145. Rideout WM 3rd, Hochedlinger K, Kyba M et al (2002) Correction of a genetic defect by nuclear transplantation and combined cell and gene therapy. Cell 109:17–27

    CAS  PubMed  Google Scholar 

  146. Dozortsev D, Wakaiama T, Ermilov A et al (1998) Intracytoplasmic sperm injection in the rat. Zygote 6:143–147

    CAS  PubMed  Google Scholar 

  147. Fire A, Xu S, Montgomery MK, Kostas SA et al (1998) Potent and specific genetic interference by double-stranded RNA in Caenorhabditis elegans. Nature 39:806–811

    Google Scholar 

  148. Nasevicius A, Ekker SC (2000) Effective targeted gene ‘knockdown’ in zebrafish. Nat Genet 26:216–220

    CAS  PubMed  Google Scholar 

  149. Stainier DYR, Raz E, Lawson ND et al (2017) Guidelines for morpholino use in zebrafish. PLoS Genet 13:e1007000

    PubMed  PubMed Central  Google Scholar 

  150. Perry AC, Wakayama T, Kishikawa H et al (1999) Mammalian transgenesis by intracytoplasmic sperm injection. Science 284:1180–1183

    CAS  PubMed  Google Scholar 

  151. Chan AW, Luetjens CM, Dominko T et al (2000) TransgenICSI reviewed: foreign DNA transmission by intracytoplasmic sperm injection in rhesus monkey. Mol Reprod Dev 56:325–328

    CAS  PubMed  Google Scholar 

  152. Perry AC, Rothman A, de las Heras JI et al (2001) Efficient metaphase II transgenesis with different transgene archetypes. Nat Biotechnol 19:1071–1073

    CAS  PubMed  Google Scholar 

  153. Moreira PN, Giraldo P, Cozar P et al (2004) Efficient generation of transgenic mice with intact yeast artificial chromosomes by intracytoplasmic sperm injection. Biol Reprod 71:1943–1947

    CAS  PubMed  Google Scholar 

  154. Lavitrano M, Camaioni A, Fazio VM et al (1989) Sperm cells as vectors for introducing foreign DNA into eggs: genetic transformation of mice. Cell 57:717–723

    CAS  PubMed  Google Scholar 

  155. Maione B, Lavitrano M, Spadafora C et al (1998) Sperm-mediated gene transfer in mice. Mol Reprod Dev 50:406–409

    CAS  PubMed  Google Scholar 

  156. Smith K, Spadafora C (2005) Sperm-mediated gene transfer: applications and implications. BioEssays 27:551–562

    CAS  PubMed  Google Scholar 

  157. Lavitrano M, Busnelli M, Cerrito MG et al (2006) Sperm-mediated gene transfer. Reprod Fertil Dev 18:19–23

    CAS  PubMed  Google Scholar 

  158. García-Vázquez FA, Ruiz S, Grullón LA et al (2011) Factors affecting porcine sperm mediated gene transfer. Res Vet Sci 91:446–453

    PubMed  Google Scholar 

  159. McCreath KJ, Howcroft J, Campbell KH et al (2000) Production of gene-targeted sheep by nuclear transfer from cultured somatic cells. Nature 405:1066–1069

    CAS  PubMed  Google Scholar 

  160. Lai L, Kolber-Simonds D, Park KW et al (2002) Production of alpha-1,3-galactosyltransferase knockout pigs by nuclear transfer cloning. Science 295:1089–1092

    CAS  PubMed  Google Scholar 

  161. Polejaeva IA, Campbell KH (2000) New advances in somatic cell nuclear transfer: application in transgenesis. Theriogenology 53:117–261

    CAS  PubMed  Google Scholar 

  162. Bibikova M, Carroll D, Segal DJ et al (2001) Stimulation of homologous recombination through targeted cleavage by chimeric nucleases. Mol Cell Biol 21:289–297

    CAS  PubMed  PubMed Central  Google Scholar 

  163. Lois C, Hong EJ, Pease S et al (2002) Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors. Science 295:868–872

    CAS  PubMed  Google Scholar 

  164. Fässler R (2004) Lentiviral transgene vectors. EMBO Rep 5:28–29

    PubMed  PubMed Central  Google Scholar 

  165. Park F (2007) Lentiviral vectors: are they the future of animal transgenesis? Physiol Genomics 31:159–173

    CAS  PubMed  Google Scholar 

  166. Mojica FJ, Díez-Villaseñor C, García-Martínez J et al (2005) Intervening sequences of regularly spaced prokaryotic repeats derive from foreign genetic elements. J Mol Evol 60:174–182

    CAS  PubMed  Google Scholar 

  167. Mojica FJM, Montoliu L (2016) On the origin of CRISPR-Cas technology: from prokaryotes to mammals. Trends Microbiol 24:811–820

    CAS  PubMed  Google Scholar 

  168. Takahashi K, Yamanaka S (2006) Induction of pluripotent stem cells from mouse embryonic and adult fibroblast cultures by defined factors. Cell 126:663–676

    CAS  PubMed  Google Scholar 

  169. Hanna J, Markoulaki S, Schorderet P et al (2008) Direct reprogramming of terminally differentiated mature B lymphocytes to pluripotency. Cell 133:250–264

    CAS  PubMed  PubMed Central  Google Scholar 

  170. Su Y, Zhu J, Salman S et al (2020) Induced pluripotent stem cells from farm animals. J Anim Sci 98:skaa343

    PubMed  PubMed Central  Google Scholar 

  171. Vogel G (2007) Nobel prizes. A knockout award in medicine. Science 318:178–179

    CAS  PubMed  Google Scholar 

  172. Ying QL, Wray J, Nichols J et al (2008) The ground state of embryonic stem cell self-renewal. Nature 453:519–523

    CAS  PubMed  PubMed Central  Google Scholar 

  173. Buehr M, Meek S, Blair K (2008) Capture of authentic embryonic stem cells from rat blastocysts. Cell 135:1287–1298

    CAS  PubMed  Google Scholar 

  174. Geurts AM, Cost GJ, Freyvert Y (2009) Knockout rats via embryo microinjection of zinc-finger nucleases. Science 325:433

    CAS  PubMed  PubMed Central  Google Scholar 

  175. Rémy S, Tesson L, Ménoret S et al (2010) Zinc-finger nucleases: a powerful tool for genetic engineering of animals. Transgenic Res 19:363–371

    PubMed  Google Scholar 

  176. Meyer M, de Angelis MH, Wurst W et al (2007) Gene targeting by homologous recombination in mouse zygotes mediated by zinc-finger nucleases. Proc Natl Acad Sci U S A 107:15022–15026

    Google Scholar 

  177. Yu S, Luo J, Song Z (2011) Highly efficient modification of beta-lactoglobulin (BLG) gene via zinc-finger nucleases in cattle. Cell Res 21:1638–1640

    CAS  PubMed  PubMed Central  Google Scholar 

  178. Hauschild J, Petersen B, Santiago Y (2011) Efficient generation of a biallelic knockout in pigs using zinc-finger nucleases. Proc Natl Acad Sci U S A 108:12013–12017

    CAS  PubMed  PubMed Central  Google Scholar 

  179. Liu X, Wang Y, Tian Y et al (2014) Generation of mastitis resistance in cows by targeting human lysozyme gene to β-casein locus using zinc-finger nucleases. Proc Biol Sci 281:20133368

    PubMed  PubMed Central  Google Scholar 

  180. Lillico SG, Proudfoot C, King TJ et al (2016) Mammalian interspecies substitution of immune modulatory alleles by genome editing. Sci Rep 6:21645

    CAS  PubMed  PubMed Central  Google Scholar 

  181. Tesson L, Usal C, Ménoret S, Leung E, Niles BJ, Remy S, Santiago Y, Vincent AI, Meng X, Zhang L, Gregory PD, Anegon I, Cost GJ et al (2011) Knockout rats generated by embryo microinjection of TALENs. Nat Biotechnol 29:695–696

    CAS  PubMed  Google Scholar 

  182. Panda SK, Wefers B, Ortiz O et al (2013) Highly efficient targeted mutagenesis in mice using TALENs. Genetics 195:703–713

    CAS  PubMed  PubMed Central  Google Scholar 

  183. Carlson DF, Tan W, Lillico SG et al (2012) Efficient TALEN-mediated gene knockout in livestock. Proc Natl Acad Sci U S A 109:17382–17387

    CAS  PubMed  PubMed Central  Google Scholar 

  184. Wu H, Wang Y, Zhang Y et al (2015) TALE nickase-mediated SP110 knockin endows cattle with increased resistance to tuberculosis. Proc Natl Acad Sci U S A 112:E1530–E1539

    CAS  PubMed  PubMed Central  Google Scholar 

  185. Xin J, Yang H, Fan N et al (2013) Highly efficient generation of GGTA1 biallelic knockout inbred mini-pigs with TALENs. PLoS One 8:e84250

    PubMed  PubMed Central  Google Scholar 

  186. Cui C, Song Y, Liu J et al (2015) Gene targeting by TALEN-induced homologous recombination in goats directs production of β-lactoglobulin-free, high-human lactoferrin milk. Sci Rep 5:10482

    PubMed  PubMed Central  Google Scholar 

  187. Pease S, Saunders TL (eds) (2011) Advanced protocols for animal transgenesis. An ISTT Manual, Springer, Berlin

    Google Scholar 

  188. Colman A (2013) Profile of John Gurdon and Shinya Yamanaka, 2012 Nobel laureates in medicine or physiology. Proc Natl Acad Sci U S A 110:5740–5741

    CAS  PubMed  PubMed Central  Google Scholar 

  189. Jinek M, Chylinski K, Fonfara I, Hauer M, Doudna JA, Charpentier E (2012) A programmable dual-RNA-guided DNA endonuclease in adaptive bacterial immunity. Science 337(6096):816–821

    CAS  PubMed  PubMed Central  Google Scholar 

  190. Seruggia D, Montoliu L (2014) The new CRISPR-Cas system: RNA-guided genome engineering to efficiently produce any desired genetic alteration in animals. Transgenic Res 23:707–716

    CAS  PubMed  Google Scholar 

  191. Cong L, Ran FA, Cox D et al (2013) Multiplex genome engineering using CRISPR/Cas systems. Science 339:819–823

    CAS  PubMed  PubMed Central  Google Scholar 

  192. Mali P, Yang L, Esvelt KM et al (2013) RNA-guided human genome engineering via Cas9. Science 339:823–826

    CAS  PubMed  PubMed Central  Google Scholar 

  193. Hwang WY, Fu Y, Reyon D et al (2013) Efficient genome editing in zebrafish using a CRISPR-Cas system. Nat Biotechnol 31:227–229

    CAS  PubMed  PubMed Central  Google Scholar 

  194. Wang H, Yang H, Shivalila CS et al (2013) One-step generation of mice carrying mutations in multiple genes by CRISPR/Cas-mediated genome engineering. Cell 153:910–918

    CAS  PubMed  PubMed Central  Google Scholar 

  195. Yang H, Wang H, Shivalila CS et al (2013) One-step generation of mice carrying reporter and conditional alleles by CRISPR/Cas-mediated genome engineering. Cell 154:1370–1379

    CAS  PubMed  PubMed Central  Google Scholar 

  196. Ran FA, Hsu PD, Lin CY et al (2013) Double nicking by RNA-guided CRISPR Cas9 for enhanced genome editing specificity. Cell 154:1380–1389

    CAS  PubMed  PubMed Central  Google Scholar 

  197. Qi LS, Larson MH, Gilbert LA et al (2013) Repurposing CRISPR as an RNA-guided platform for sequence-specific control of gene expression. Cell 152:1173–1183

    CAS  PubMed  PubMed Central  Google Scholar 

  198. Gilbert LA, Larson MH, Morsut L et al (2013) CRISPR-mediated modular RNA-guided regulation of transcription in eukaryotes. Cell 154:442–451

    CAS  PubMed  PubMed Central  Google Scholar 

  199. Doudna JA, Charpentier E (2014) Genome editing. The new frontier of genome engineering with CRISPR-Cas9. Science 346:1258096

    PubMed  Google Scholar 

  200. Hai T, Teng F, Guo R et al (2014) One-step generation of knockout pigs by zygote injection of CRISPR/Cas system. Cell Res 24:372–375

    CAS  PubMed  PubMed Central  Google Scholar 

  201. Crispo M, Mulet AP, Tesson L et al (2015) Efficient generation of Myostatin knock-out sheep using CRISPR/Cas9 technology and microinjection into zygotes. PLoS One 210:e0136690

    Google Scholar 

  202. Wang Z (2015) Genome engineering in cattle: recent technological advancements. Chromosom Res 23:17–29

    CAS  Google Scholar 

  203. Guo R, Wan Y, Xu D (2016) Generation and evaluation of Myostatin knock-out rabbits and goats using CRISPR/Cas9 system. Sci Rep 6:29855

    CAS  PubMed  PubMed Central  Google Scholar 

  204. Amoasii L, Hildyard JCW, Li H et al (2018) Gene editing restores dystrophin expression in a canine model of Duchenne muscular dystrophy. Science 362:86–91

    CAS  PubMed  PubMed Central  Google Scholar 

  205. Han Y, Slivano OJ, Christie CK et al (2015) CRISPR-Cas9 genome editing of a single regulatory element nearly abolishes target gene expression in mice--brief report. Arterioscler Thromb Vasc Biol 35:312–315

    CAS  PubMed  Google Scholar 

  206. Seruggia D, Fernández A, Cantero M et al (2015) Functional validation of mouse tyrosinase non-coding regulatory DNA elements by CRISPR-Cas9-mediated mutagenesis. Nucleic Acids Res 43:4855–4867

    CAS  PubMed  PubMed Central  Google Scholar 

  207. Lupiáñez DG, Kraft K, Heinrich V et al (2015) Disruptions of topological chromatin domains cause pathogenic rewiring of gene-enhancer interactions. Cell 161:1012–1025

    PubMed  PubMed Central  Google Scholar 

  208. Yang L, Güell M, Niu D et al (2015) Genome-wide inactivation of porcine endogenous retroviruses (PERVs). Science 350:1101–1104

    CAS  PubMed  Google Scholar 

  209. Niu D, Wei HJ, Lin L et al (2017) Inactivation of porcine endogenous retrovirus in pigs using CRISPR-Cas9. Science 357:1303–1307

    CAS  PubMed  PubMed Central  Google Scholar 

  210. Fischer K, Kraner-Scheiber S, Petersen B et al (2016) Efficient production of multi-modified pigs for xenotransplantation by ‘combineering’, gene stacking and gene editing. Sci Rep 6:29081

    CAS  PubMed  PubMed Central  Google Scholar 

  211. Qin W, Dion SL, Kutny PM et al (2015) Efficient CRISPR/Cas9-mediated genome editing in mice by zygote electroporation of nuclease. Genetics 200:423–430

    CAS  PubMed  PubMed Central  Google Scholar 

  212. Lin JC, Van Eenennaam AL (2021) Electroporation-mediated genome editing of livestock zygotes. Front Genet 12:648482

    CAS  PubMed  PubMed Central  Google Scholar 

  213. Fernández A, Morín M, Muñoz-Santos D et al (2020) Simple protocol for generating and genotyping genome-edited mice with CRISPR-Cas9 reagents. Curr Protoc Mouse Biol 10:e69

    PubMed  Google Scholar 

  214. Long C, Amoasii L, Mireault AA et al (2016) Postnatal genome editing partially restores dystrophin expression in a mouse model of muscular dystrophy. Science 351:400–403

    CAS  PubMed  Google Scholar 

  215. Nelson CE, Hakim CH, Ousterout DG et al (2016) In vivo genome editing improves muscle function in a mouse model of Duchenne muscular dystrophy. Science 351:403–407

    CAS  PubMed  Google Scholar 

  216. Tabebordbar M, Zhu K, Cheng JKW et al (2016) In vivo gene editing in dystrophic mouse muscle and muscle stem cells. Science 351:407–411

    CAS  PubMed  Google Scholar 

  217. Komor AC, Kim YB, Packer MS et al (2016) Programmable editing of a target base in genomic DNA without double-stranded DNA cleavage. Nature 533:420–424

    CAS  PubMed  PubMed Central  Google Scholar 

  218. Gaudelli NM, Komor AC, Rees HA et al (2017) Programmable base editing of A•T to G•C in genomic DNA without DNA cleavage. Nature 551:464–471

    CAS  PubMed  PubMed Central  Google Scholar 

  219. Koblan LW, Doman JL, Wilson C et al (2018) Improving cytidine and adenine base editors by expression optimization and ancestral reconstruction. Nat Biotechnol 36:843–846

    CAS  PubMed  PubMed Central  Google Scholar 

  220. Finn JD, Smith AR, Patel MC et al (2018) A single administration of CRISPR/Cas9 lipid nanoparticles achieves robust and persistent in vivo genome editing. Cell Rep 22:2227–2235

    CAS  PubMed  Google Scholar 

  221. Anzalone AV, Randolph PB, Davis JR et al (2019) Search-and-replace genome editing without double-strand breaks or donor DNA. Nature 576:149–157

    CAS  PubMed  PubMed Central  Google Scholar 

  222. Ledford H, Callaway E (2020) Pioneers of revolutionary CRISPR gene editing win chemistry Nobel. Nature 586:346–347

    CAS  PubMed  Google Scholar 

  223. Gaudelli NM, Lam DK, Rees HA et al (2020) Directed evolution of adenine base editors with increased activity and therapeutic application. Nat Biotechnol 38:892–900

    CAS  PubMed  Google Scholar 

  224. Gao P, Lyu Q, Ghanam AR et al (2021) Prime editing in mice reveals the essentiality of a single base in driving tissue-specific gene expression. Genome Biol 22:83

    CAS  PubMed  PubMed Central  Google Scholar 

  225. Koblan LW, Erdos MR, Wilson C et al (2021) In vivo base editing rescues Hutchinson-Gilford progeria syndrome in mice. Nature 589:608–614

    CAS  PubMed  PubMed Central  Google Scholar 

  226. Newby GA, Yen JS, Woodard KJ et al (2021) Base editing of haematopoietic stem cells rescues sickle cell disease in mice. Nature 595:295–302

    CAS  PubMed  PubMed Central  Google Scholar 

  227. Musunuru K, Chadwick AC, Mizoguchi T et al (2021) In vivo CRISPR base editing of PCSK9 durably lowers cholesterol in primates. Nature 593:429–434

    CAS  PubMed  Google Scholar 

  228. Newby GA, Liu DR (2021) In vivo somatic cell base editing and prime editing. Mol Ther 29:3107–3124

    CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgments

This work was supported by the Spanish Ministry of Science and Innovation (MICINN) through the Grant [RTI2018-101223-B-I00] to L.M.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Lluis Montoliu .

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2023 The Author(s), under exclusive license to Springer Science+Business Media, LLC, part of Springer Nature

About this protocol

Check for updates. Verify currency and authenticity via CrossMark

Cite this protocol

Montoliu, L. (2023). Transgenesis and Genome Engineering: A Historical Review. In: Saunders, T.L. (eds) Transgenesis. Methods in Molecular Biology, vol 2631. Humana, New York, NY. https://doi.org/10.1007/978-1-0716-2990-1_1

Download citation

  • DOI: https://doi.org/10.1007/978-1-0716-2990-1_1

  • Published:

  • Publisher Name: Humana, New York, NY

  • Print ISBN: 978-1-0716-2989-5

  • Online ISBN: 978-1-0716-2990-1

  • eBook Packages: Springer Protocols

Publish with us

Policies and ethics