1932

Abstract

Cre- of bacteriophage P1 has become one of the most widely used tools for genetic engineering in eukaryotes. The origins of this tool date to more than 30 years ago when Nat L. Sternberg discovered the recombinase, Cre, and its specific locus of crossover, , while studying the maintenance of bacteriophage P1 as a stable plasmid. Recombinations mediated by Cre assist in cyclization of the DNA of infecting phage and in resolution of prophage multimers created by generalized recombination. Early in vitro work demonstrated that, although it shares similarities with the well-characterized bacteriophage λ integration, Cre- is in many ways far simpler in its requirements for carrying out recombination. These features would prove critical for its development as a powerful and versatile tool in genetic engineering. We review the history of the discovery and characterization of Cre- and touch upon the present direction of Cre- research.

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2015-11-09
2024-06-24
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Literature Cited

  1. Lwoff A. 1.  1953. Lysogeny. Bacteriol. Rev. 17:269–337 [Google Scholar]
  2. Lwoff A. 2.  Nobel Lecture: Interaction Among Virus, Cell, and Organism Stockholm: Nobel Media AB http://www.nobelprize.org/nobel_prizes/medicine/laureates/1965/lwoff-lecture.html [Google Scholar]
  3. Bertani G. 3.  2004. Lysogeny at mid-twentieth century: P1, P2, and other experimental systems. J. Bacteriol. 186:595–600 [Google Scholar]
  4. Lennox ES. 4.  1955. Transduction of linked genetic characters of the host by bacteriophage P1. Virology 1:190–206 [Google Scholar]
  5. Yarmolinsky MB, Sternberg N. 5.  1988. Bacteriophage P1. The Bacteriophages 1 R Calendar 291–438 New York: Plenum [Google Scholar]
  6. Łobocka MB, Rose DJ, Plunket G III, Rusin M, Samojedny A. 6.  et al. 2004. Genome of bacteriophage P1. J. Bacteriol. 186:7032–68 [Google Scholar]
  7. Ikeda H, Tomizawa J. 7.  1968. Prophage P1, an extra-chromosomal replication unit. Cold Spring Harb. Symp. Quant. Biol. 33:791–98 [Google Scholar]
  8. Jacob F, Monod J. 8.  1961. Genetic regulatory mechanisms in the synthesis of proteins. J. Mol. Biol. 3:315–56 [Google Scholar]
  9. Clerget M. 9.  1991. Site-specific recombination promoted by a short DNA segment of plasmid R1 and by a homologous segment in the terminus region of the Escherichia coli chromosome. New Biol. 3:780–88 [Google Scholar]
  10. Sternberg N, Tiemeier D, Enquist L. 10.  1977. In vitro packaging of a λ Dam vector containing EcoRI DNA fragments of Escherichia coli and phage P1. Gene 1:255–80 [Google Scholar]
  11. Sternberg N. 11.  1978. Demonstration and analysis of P1 site-specific recombination using λ-P1 hybrid phages constructed in vitro. Cold Spring Harb. Symp. Quant. Biol. 43:1143–46 [Google Scholar]
  12. Sternberg N, Hamilton D. 12.  1981. Bacteriophage P1 site-specific recombination. I. Recombination between loxP sites. J. Mol. Biol. 150:467–86 [Google Scholar]
  13. Takano T. 13.  1971. Bacterial mutant defective in plasmid formation: requirement for the lon+ allele. PNAS 68:1469–73 [Google Scholar]
  14. Chesney RH, Vapnek D, Scott JR. 14.  1978. Recombination between the plasmid prophages P1 and P7 and the E. coli chromosome. Contrib. Microbiol. Immunol. 6:78–88 [Google Scholar]
  15. Sternberg N, Coulby J. 15.  1987. Recognition and cleavage of the bacteriophage P1 packaging site (pac). I. Differential processing of the cleaved ends in vivo. J. Mol. Biol. 194:453–68 [Google Scholar]
  16. Sternberg N, Coulby J. 16.  1987. Recognition and cleavage of the bacteriophage P1 packaging site (pac). II. Functional limits of pac and location of pac cleavage termini. J. Mol. Biol. 194:469–83 [Google Scholar]
  17. Austin S, Zeise M, Sternberg N. 17.  1981. A novel role for site-specific recombination in the maintenance of bacterial replicons. Cell 25:729–36 [Google Scholar]
  18. Nash HA. 18.  1981. Integration and excision of bacteriophage λ: the mechanism of conservative site specific recombination. Annu. Rev. Genet. 15:143–67 [Google Scholar]
  19. Hoess RH, Ziese M, Sternberg N. 19.  1982. P1 site-specific recombination: nucleotide sequence of the recombining sites. PNAS 79:3398–402 [Google Scholar]
  20. Abremski K, Hoess R, Sternberg N. 20.  1983. Studies on the properties of P1 site-specific recombination: evidence for topologically unlinked productions following recombination. Cell 32:1301–11 [Google Scholar]
  21. Abremski K, Gottesman S. 21.  1981. Site-specific recombination: Xis-independent excisive recombination of bacteriophage lambda. J. Mol. Biol. 153:67–78 [Google Scholar]
  22. Reed RR. 22.  1981. Transposon-mediated site-specific recombination: a defined in vitro system. Cell 25:713–19 [Google Scholar]
  23. Abremski K, Hoess R. 23.  1984. Bacteriophage P1 site-specific recombination: purification and properties of the Cre recombinase protein. J. Biol. Chem. 259:1509–14 [Google Scholar]
  24. Hoess R, Abremski K. 24.  1984. Interaction of the bacteriophage P1 recombinase Cre with the recombining site loxP. PNAS 81:1026–29 [Google Scholar]
  25. Hoess R, Abremski K. 25.  1985. Mechanism of strand cleavage and exchange in the Cre-lox site-specific recombination system. J. Mol. Biol. 181:351–62 [Google Scholar]
  26. Hoess R, Wierzbicki A, Abremski K. 26.  1986. The role of the loxP spacer region in P1 site-specific recombination. Nucleic Acids Res. 14:2287–300 [Google Scholar]
  27. Sauer B. 27.  1996. Multiplex Cre/lox recombination permits selective site-specific DNA targeting to both a natural and an engineered site in the yeast genome. Nucleic Acids Res. 24:4608–13 [Google Scholar]
  28. Abremski K, Hoess R. 28.  1985. Phage P1 Cre-lox site-specific recombination: effects of DNA supercoiling on catenation and knotting of recombinant products. J. Mol. Biol. 184:211–20 [Google Scholar]
  29. Sternberg N. 29.  1981. Bacteriophage P1 site-specific recombination. III. Strand exchange during recombination at lox sites. J. Mol. Biol. 150:603–8 [Google Scholar]
  30. Hoess R, Wierzbicki A, Abremski K. 30.  1987. Isolation and characterization of potential intermediates in site-specific recombination. PNAS 84:6840–44 [Google Scholar]
  31. Sternberg N, Sauer B, Hoess R, Abremski K. 31.  1986. Bacteriophage P1 cre gene and its regulatory region: evidence for multiple promoters and regulation by DNA methylation. J. Mol. Biol. 187:197–212 [Google Scholar]
  32. Argos P, Landy A, Abremski K, Egan JB, Haggard-Ljungquist E. 32.  et al. 1986. The integrase family of site-specific recombinases: regional similarities and global diversity. EMBO J. 5:433–40 [Google Scholar]
  33. Abremski K, Hoess R. 33.  1992. Evidence for a second conserved arginine residue in the integrase family of recombination proteins. Protein Eng. 5:87–91 [Google Scholar]
  34. Guo F, Gopaul DN, Van Duyne GD. 34.  1997. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389:40–46 [Google Scholar]
  35. Adams DE, Bliska JB, Cozzarelli NR. 35.  1992. Cre-lox recombination in Escherichia coli cells: mechanistic differences from the in vitro reaction. J. Mol. Biol. 226:661–73 [Google Scholar]
  36. Cohen G. 36.  1983. Electron microscopy study of early lytic replication forms of bacteriophage P1 DNA. Virology 131:159–70 [Google Scholar]
  37. Barre FX, Soballe B, Michel B, Aroyo M, Robertson M. 37.  et al. 2001. Circles: the replication-recombination-chromosome segregation connection. PNAS 98:8189–95 [Google Scholar]
  38. Sternberg N, Hamilton D, Austin S, Yarmolinsky M, Hoess R. 38.  1981. Site-specific recombination and its role in the life cycle of bacteriophage P1. Cold Spring Harb. Symp. Quant. Biol. 45:297–309 [Google Scholar]
  39. Sauer B. 39.  1987. Functional expression of the cre-lox site-specific recombination system in the yeast Saccharomyces cerevisiae. Mol. Cell. Biol. 7:2087–96 [Google Scholar]
  40. Sauer B, Henderson N. 40.  1988. Site-specific recombination in mammalian cells by the Cre recombinase of bacteriophage P1. PNAS 85:5166–70 [Google Scholar]
  41. Sternberg N. 41.  1994. The P1 cloning system past and future. Mamm. Genome 5:397–404 [Google Scholar]
  42. Esposito D, Scocca JJ. 42.  1997. The integrase family of tyrosine recombinases: evolution of a conserved active site domain. Nucleic Acids Res. 25:3605–14 [Google Scholar]
  43. Begg KJ, Dewar SJ, Donachie WD. 43.  1995. A new Escherichia coli cell division gene, ftsK. J. Bacteriol. 177:6211–22 [Google Scholar]
  44. Bigot S, Sivanatan V, Possoz C, Barre FX, Cornet F. 44.  2007. FtsK, a literate chromosome segregation machine. Mol. Microbiol. 64:1434–41 [Google Scholar]
  45. Grainge I, Lesterlin C, Sherratt DJ. 45.  2011. Activation of XerCD-dif recombination by the FtsK DNA translocase. Nucleic Acids Res. 39:5140–48 [Google Scholar]
  46. Capiaux H, Lesterlin C, Pérals K, Louarn JM, Cornet F. 46.  2002. A dual role for the FtsK protein in Escherichia coli chromosome segregation. EMBO Rep. 3:532–36 [Google Scholar]
  47. Zawadzki P, May PF, Baker RA, Pinkney JN, Kapanidis AN. 47.  et al. 2013. Conformational transitions during FtsK translocase activation of individual XerCD-dif recombination complexes. PNAS 110:17302–7 [Google Scholar]
  48. Carnoy C, Roten CA. 48.  2009. The dif/Xer recombination systems in proteobacteria. PLOS ONE 4:e6531 [Google Scholar]
  49. Hsu PL, Ross W, Landy A. 49.  1980. The λ phage att site: functional limits and interaction with Int protein. Nature 285:85–91 [Google Scholar]
  50. Van Duyne GD. 50.  2001. A structural view of Cre-loxP site-specific recombination. Annu. Rev. Biophys. Biomol. Struct. 30:87–104 [Google Scholar]
  51. Pinkney JN, Zawadzki P, Mazauryic J, Arciszewska LK, Sherratt DJ, Kapanidis AN. 51.  2012. Capturing reaction paths and intermediates in Cre-loxP recombination using single molecule fluorescence. PNAS 109:20871–76 [Google Scholar]
  52. Warren D, Laxmikanthan G, Landy A. 52.  2008. A chimeric Cre recombinase with regulated directionality. PNAS 105:18278–83 [Google Scholar]
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