Phage-encoded serine integrases and other large serine recombinases

Mobile DNA III

Volumn , Issue , 2015, Pages 253-272

  Smith, Margaret C M ^a  

^a UNIVERSITY OF YORK   (United Kingdom)

Author keywords

Biological roles; DNA binding; Domestication; Large serine recombinases; Phage life cycles; Phage encoded serine integrases; Prophage excision; Site selectivity; Site specific recombination; Staphylococcal cassette chromosomes

Indexed keywords

EID: 85103344876     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1128/9781555819217.ch11     Document Type: Chapter

References (90)

1. Grindley NDF, Whiteson KL, Rice PA. 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75:567-605.
2. Smith MCM, Thorpe HM. 2002. Diversity in the serine recombinases. Mol Microbiol 44:299-307.
3. Thorpe HM, Smith MCM. 1998. In vitro site-specific integration of bacteriophage DNA catalyzed by a recombinase of the resolvase/invertase family. Proc Natl Acad Sci USA 95:5505-5510.
4. Kim AI, Ghosh P, Aaron MA, Bibb LA, Jain S, Hatfull GF. 2003. Mycobacteriophage Bxb1 integrates into the Mycobacterium smegmatis groEL1 gene. Mol Microbiol 50:463-473.
5. Rutherford K, Yuan P, Perry K, Sharp R, Van Duyne GD. 2013. Attachment site recognition and regulation of directionality by the serine integrases. Nucleic Acids Res 41:8341-8356.
6. Van Duyne GD, Rutherford K. 2013. Large serine recombinase domain structure and attachment site binding. Crit Rev Biochem Molec Biol 48:476-491.
7. Rutherford K, Van Duyne GD. 2014. The ins and outs of serine integrase site-specific recombination. Curr Opin Struct Biol 24:125-131.
8. Adams V, Lyras D, Farrow KA, Rood JI. 2002. The clostridial mobilisable transposons. Cell Mol Life Sci 59: 2033-2043.
9. Mullany P, Roberts AP, Wang H. 2002. Mechanism of integration and excision in conjugative transposons. Cell Mol Life Sci 59:2017-2022.
10. Hanssen AM, Ericson Sollid JU. 2006. SCCmec in staphylococci: genes on the move. FEMS Immunol Med Microbiol 46:8-20.
11. Campbell AM. 1962. Episomes, p 101-145. In Caspari EW, Thoday JM (ed), Advances in Genetics. Academic Press, New York, NY.
12. Lewis JA, Hatfull GF. 2001. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucleic Acids Res 29:2205-2216.
13. Smith MCM, Brown WR, McEwan AR, Rowley PA. 2010. Site-specific recombination by phiC31 integrase and other large serine recombinases. Biochem Soc Trans 38:388-394.
14. Misiura A, Pigli YZ, Boyle-Vavra S, Daum RS, Boocock MR, Rice PA. 2013. Roles of two large serine recombinases in mobilizing the methicillin-resistance cassette SCCmec. Mol Microbiol 88:1218-1229.
15. Combes P, Till R, Bee S, Smith MCM. 2002. The streptomyces genome contains multiple pseudo-attB sites for the ΦC31-encoded site-specific recombination system. J Bacteriol 184:5746-5752.
16. Bibb LA, Hancox MI, Hatfull GF. 2005. Integration and excision by the large serine recombinase phiRv1 integrase. Mol Microbiol 55:1896-1910.
17. Ito T, Katayama Y, Asada K, Mori N, Tsutsumimoto K, Tiensasitorn C, Hiramatsu K. 2001. Structural comparison of three types of staphylococcal cassette chromosome mec integrated in the chromosome in methicillin-resistant Staphylococcus aureus. Antimicrob Agents Chemother 45:1323-1336.
18. Singh S, Rockenbach K, Dedrick RM, VanDemark AP, Hatfull GF. 2014. Cross-talk between diverse serine integrases. J Mol Biol 426:318-331.
19. Carrasco CD, Ramaswamy KS, Ramasubramanian TS, Golden JW. 1994. Anabaena xisF gene encodes a developmentally regulated site-specific recombinase. Genes Dev 8:74-83.
20. Sato T, Samori Y, Kobayashi Y. 1990. The cisA cistron of Bacillus subtilis sporulation gene spoIVC encodes a protein homologus to a site-sepcific recombinase. J Bacteriol 172:1092-1098.
21. Stragier P, Kunkel B, Kroos L, Losick R. 1989. Chromosomal rearrangement generating a composite gene for a developmental transcription factor. Science 243:507-512.
22. Golden JW, Mulligan ME, Haselkorn R. 1987. Different recombination site specificity of two developmentally regulated genome rearrangements. Nature 327:526-529.
23. Carrasco CD, Buettner JA, Golden JW. 1995. Programmed DNA rearrangement of a cyanobacteria hupL gene in heterocysts. Proc Natl Acad Sci USA 92:791-795.
24. Ramaswamy KS, Carrasco CD, Fatma T, Golden JW. 1997. Cell-type specificity of the Anabaena fdxN-element rearrangement requires xisH and xisI. Mol Microbiol 23: 1241-1249.
25. Kunkel B, Losick R, Stragier P. 1990. The Bacillus subtilis gene for the development transcription factor sigma K is generated by excision of a dispensable DNA element containing a sporulation recombinase gene. Genes Dev 4:525-535.
26. Popham DL, Stragier P. 1992. Binding of the Bacillus subtilis spoIVCA product to the recombination sites of the element interrupting the sigma-K encoding gene. Proc Natl Acad Sci USA 89:5991-5995.
27. Loessner MJ, Inman RB, Lauer P, Calendar R. 2000. Complete nucleotide sequence, molecular analysis and genome structure of bacteriophage A118 of Listeria monocytogenes: implications for phage evolution. Mol Microbiol 35:324-340.
28. Rabinovich L, Sigal N, Borovok I, Nir-Paz R, Herskovits AA. 2012. Prophage excision activates Listeria competence genes that promote phagosomal escape and virulence. Cell 150:792-802.
29. Claverys JP, Prudhomme M, Martin B. 2006. Induction of competence regulons as a general response to stress in gram-positive bacteria. Annu Rev Microbiol 60:451-475.
30. Bannam TL, Crellin PK, Rood JI. 1995. Molecular genetics of the chloramphenicol-resistance transposon Tn4451 from Clostridium perfringens: the TnpX sitespecific recombinase excises a circular transposon molecule. Mol Microbiol 16:535-551.
31. Crellin PK, Rood JI. 1997. The resolvase/invertase domain of the site-specific recombinase TnpX is functional and recognizes a target sequence that resembles the junction of the circular form of the Clostridium perfringens transposon Tn4451. J Bacteriol 179:5148-5156.
32. Wang H, Mullany P. 2000. The large resolvase TndX is required and sufficient for integration and excision of derivatives of the novel conjugative transposon Tn5397. J Bacteriol 182:6577-6583.
33. Lyras D, Rood JI. 2000. Transposition of Tn4451 and Tn4453 involves a circular intermediate that forms a promoter for the large resolvase, TnpX. Mol Microbiol 38:588-601.
34. Wang H, Smith MCM, Mullany P. 2006. The conjugative transposon Tn5397 has a strong preference for integration into its Clostridium difficile target site. J Bacteriol 188:4871-4878.
35. Katayama Y, Ito T, Hiramatsu K. 2000. A new class of genetic element, staphylococcus cassette chromosome mec, encodes methicillin resistance in Staphylococcus aureus. Antimicrob Agents Chemother 44:1549-1555.
36. Wang L, Archer GL. 2010. Roles of CcrA and CcrB in excision and integration of staphylococcal cassette chromosome mec, a Staphylococcus aureus genomic island. J Bacteriol 192:3204-3212.
37. Ito T, Katayama Y, Hiramatsu K. 1999. Cloning and nucleotide sequence determination of the entire mec DNA of pre-methicillin-resistant Staphylococcus aureus N315. Antimicrob Agents Chemother 43:1449-1458.
38. Scharn CR, Tenover FC, Goering RV. 2013. Transduction of staphylococcal cassette chromosome mec elements between strains of Staphylococcus aureus. Antimicrob Agents Chemother 57:5233-5238.
39. Li W, Kamtekar S, Xiong Y, Sarkis GJ, Grindley ND, Steitz TA. 2005. Structure of a synaptic gamma-delta resolvase tetramer covalently linked to two cleaved DNAs. Science 309:1210-1215.
40. Yang W, Steitz TA. 1995. Crystal-structure of the sitespecific recombinase gamma-delta resolvase complexed with a 34bp cleavage site. Cell 82:193-207.
41. Yuan P, Gupta K, Van Duyne GD. 2008. Tetrameric structure of a serine integrase catalytic domain. Structure 16:1275-1286.
42. Ghosh P, Kim AI, Hatfull GF. 2003. The orientation of mycobacteriophage Bxb1 integration is solely dependent on the central dinucleotide of attP and attB. Mol Cell 12: 1101-1111.
43. Ghosh P, Pannunzio NR, Hatfull GF. 2005. Synapsis in phage Bxb1 integration: selection mechanism for the correct pair of recombination sites. J Mol Biol 349: 331-348.
44. Smith MCA, Till R, Brady K, Soultanas P, Thorpe H, Smith MCM. 2004. Synapsis and DNA cleavage in ΦC31 integrase-mediated site-specific recombination. Nucleic Acids Res 32:2607-2617.
45. Zhang L, Wang L, Wang J, Ou X, Zhao G, Ding X. 2010. DNA cleavage is independent of synapsis during Streptomyces phage ΦBT1 integrase-mediated site-specific recombination. J Mol Cell Biol 2:264-275.
46. Smith MCA, Till R, Smith MCM. 2004. Switching the polarity of a bacteriophage integration system. Mol Microbiol 51:1719-1728.
47. Thorpe HM, Wilson SE, Smith MCM. 2000. Control of directionality in the site-specific recombination system of the Streptomyces phage ΦC31. Mol Microbiol 38: 232-241.
48. Rowley PA, Smith MCA, Younger E, Smith MCM. 2008. A motif in the C-terminal domain of ΦC31 integrase controls the directionality of recombination. Nucleic Acids Res 36:3879-3891.
49. Breuner A, Brondsted L, Hammer K. 1999. Novel organisation of genes involved in prophage excision identified in the temperate lactococcal bacteriophage TP901-1. J Bacteriol 181:7291-7297.
50. Zhang L, Ou X, Zhao G, Ding X. 2008. Highly efficient in vitro site-specific recombination system based on Streptomyces phage ΦBT1 integrase. J Bacteriol 190:6392-6397.
51. Ghosh P, Bibb LA, Hatfull GF. 2008. Two-step site selection for serine-integrase-mediated excision: DNA-directed integrase conformation and central dinucleotide proofreading. Proc Natl Acad Sci USA 105:3238-3243.
52. Ghosh P, Wasil LR, Hatfull GF. 2006. Control of phage Bxb1 excision by a novel recombination directionality factor. PLoS Biol 4:e186.
53. Khaleel T, Younger E, McEwan AR, Varghese AS, Smith MCM. 2011. A phage protein that binds ΦC31 integrase to switch its directionality. Mol Microbiol 80:1450-1463.
54. Matsuura M, Noguchi T, Yamaguchi D, Aida T, Asayama M, Takahashi H, Shirai M. 1996. The sre gene (ORF469) encodes a site-specific recombinase responsible for integration of the R4 phage genome. J Bacteriol 178:3374-3376.
55. Mouw KW, Rowland SJ, Gajjar MM, Boocock MR, Stark WM, Rice PA. 2008. Architecture of a serine recombinase-DNA regulatory complex. Mol Cell 30: 145-155.
56. Adams V, Lucet IS, Lyras D, Rood JI. 2004. DNA binding properties of TnpX indicate that different synapses are formed in the excision and integration of the Tn4451 family. Mol Microbiol 53:1195-1207.
57. Mandali S, Dhar G, Avliyakulov NK, Haykinson MJ, Johnson RC. 2013. The site-specific integration reaction of Listeria phage A118 integrase, a serine recombinase. Mobile DNA 4:2.
58. Rowley PA, Smith MCM. 2008. Role of the N-terminal domain of ΦC31 integrase in attB-attP synapsis. J Bacteriol 190:6918-6921.
59. McEwan AR, Raab A, Kelly SM, Feldmann J, Smith MCM. 2011. Zinc is essential for high-affinity DNA binding and recombinase activity of ΦC31 integrase. Nucleic Acids Res 39:6137-6147.
60. McEwan AR, Rowley PA, Smith MCM. 2009. DNA binding and synapsis by the large C-terminal domain of ΦC31 integrase. Nucleic Acids Res 37:4764-4773.
61. Lucet IS, Tynan FE, Adams V, Rossjohn J, Lyras D, Rood JI. 2005. Identification of the structural and functional domains of the large serine recombinase TnpX from Clostridium perfringens. J Biol Chem 280:2503-2511.
62. Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Heger A, Hetherington K, Holm L, Mistry J, Sonnhammer EL, Tate J, Punta M. 2014. Pfam: the protein families database. Nucleic Acids Res 42:D222-D230.
63. Gupta M, Till R, Smith MCM. 2007. Sequences in attB that affect the ability of ΦC31 integrase to synapse and to activate DNA cleavage. Nucleic Acids Res 35:3407-3419.
64. Singh S, Ghosh P, Hatfull GF. 2013. Attachment site selection and identity in Bxb1 serine integrase-mediated site-specific recombination. PLoS Genet 9:e1003490.
65. Bibb LA, Hatfull GF. 2002. Integration and excision of the Mycobacterium tuberculosis prophage-like element, ΦRv1. Mol Microbiol 45:1515-1526.
66. Zhang L, Zhu B, Dai R, Zhao G, Ding X. 2013. Control of directionality in Streptomyces phage ΦBT1 integrasemediated site-specific recombination. PloS One 8:e80434.
67. Lyras D, Adams V, Lucet I, Rood JI. 2004. The large resolvase TnpX is the only transposon-encoded protein required for transposition of the Tn4451/3 family of integrative mobilizable elements. Mol Microbiol 51:1787-1800.
68. Olorunniji FJ, Buck DE, Colloms SD, McEwan AR, Smith MCM, Stark WM, Rosser SJ. 2012. Gated rotation mechanism of site-specific recombination by ΦC31 integrase. Proc Natl Acad Sci USA 109:19661-19666.
69. Kuhstoss S, Rao RN. 1991. Analysis of the integration function of the streptomycete bacteriophage phic31. J Mol Biol 222:897-908.
70. Kuhstoss S, Richardson MA, Rao RN. 1991. Plasmid cloning vectors that integrate site-specifically in Streptomyces spp. Gene 97:143-146.
71. St-Pierre F, Cui L, Priest DG, Endy D, Dodd IB, Shearwin KE. 2013. One-step cloning and chromosomal integration of DNA. ACS Synth Biol 2:537-541.
72. Fogg PC, Colloms S, Rosser S, Stark M, Smith MCM. 2014. New applications for phage integrases. J Mol Biol 426:2703-2716.
73. Groth AC, Calos MP. 2004. Phage integrases: biology and applications. J Mol Biol 335:667-678.
74. Groth AC, Olivares EC, Thyagarajan B, Calos MP. 2000. A phage integrase directs efficient site-specific integration in human cells. Proc Natl Acad Sci USA 97: 5995-6000.
75. Zhang L, Zhao G, Ding X. 2011. Tandem assembly of the epothilone biosynthetic gene cluster by in vitro site-specific recombination. Sci Rep 1:141.
76. Colloms SD, Merrick CA, Olorunniji FJ, Stark WM, Smith MCM, Osbourn A, Keasling JD, Rosser SJ. 2013. Rapid metabolic pathway assembly and modification using serine integrase site-specific recombination. Nucleic Acids Res 42:e23.
77. Bonnet J, Subsoontorn P, Endy D. 2012. Rewritable digital data storage in live cells via engineered control of recombination directionality. Proc Natl Acad Sci USA 109: 8884-8889.
78. Bonnet J, Yin P, Ortiz ME, Subsoontorn P, Endy D. 2013. Amplifying genetic logic gates. Science 340:599-603.
79. Smith MCM. 2013. Conservative site-specific recombination, p 555-561. In Lennarz W (ed), The Encyclopedia of Biological Chemistry, vol 1. Academic Press, Waltham, MA.
80. Christiansen B, Johnsen MG, Stenby E, Vogensen FK, Hammer K. 1994. Characterization of the lactococcal temperate phage TP901-1 and its site-specific integration. J Bacteriol 176:1069-1076.
81. Gregory MA, Till R, Smith MCM. 2003. Integration site for Streptomyces phage ΦBT1 and the development of novel site-specific integrating vectors. J Bacteriol 185: 5320-5323.
82. Shirai M, Nara H, Sato A, Aida T, Takahashi H. 1991. Site-specific integration of the actinophage R4 genome into the chromosome of Streptomyces parvulus upon lysogenization. J Bacteriol 173:4237-4239.
83. Morita K, Yamamoto T, Fusada N, Komatsu M, Ikeda H, Hirano N, Takahashi H. 2009. The site-specific recombination system of actinophage TG1. FEMS Microbiol Lett 297:234-240.
84. Park MO, Lim KH, Kim TH, Chang HI. 2007. Characterization of site-specific recombination by the integrase MJ1 from enterococcal bacteriophage ΦFC1. J Microbiol Biotechnol 17:342-347.
85. Rashel M, Uchiyama J, Ujihara T, Takemura I, Hoshiba H, Matsuzaki S. 2008. A novel site-specific recombination system derived from bacteriophage ΦMR11. Biochem Biophys Res Commun 368:192-198.
86. Fayed B, Younger E, Taylor G, Smith MCM. 2014. A novel Streptomyces spp. integration vector derived from the S. venezuelae phage, SV1. BMC Biotechnol 14:51.
87. Kilcher S, Loessner MJ, Klumpp J. 2010. Brochothrix thermosphacta bacteriophages feature heterogeneous and highly mosaic genomes and utilize unique prophage insertion sites. J Bacteriol 192:5441-5453.
88. Lazarevic V, Dusterhoft A, Soldo B, Hilbert H, Mauel C, Karamata D. 1999. Nucleotide sequence of the Bacillus subtilis temperate bacteriophage SPβc2. Microbiology 145(Pt 5):1055-1067.
89. Fouts DE, Rasko DA, Cer RZ, Jiang L, Fedorova NB, Shvartsbeyn A, Vamathevan JJ, Tallon L, Althoff R, Arbogast TS, Fadrosh DW, Read TD, Gill SR. 2006. Sequencing Bacillus anthracis typing phages gamma and cherry reveals a common ancestry. J Bacteriol 188: 3402-3408.
90. Canchaya C, Desiere F, McShan WM, Ferretti JJ, Parkhill J, Brussow H. 2002. Genome analysis of an inducible prophage and prophage remnants integrated in the Streptococcus pyogenes strain SF370. Virology 302: 245-258.