Mechanisms of DNA transposition

Mobile DNA III

Volumn , Issue , 2015, Pages 529-553

  Hickman, Alison B ^a   Dyda, Fred ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

Chemical reactions; DNA transposition mechanisms; Genome repair; Strand transfer; Transposition pathways; Transposon insertion

Indexed keywords

EID: 85103344854     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1128/9781555819217.ch25     Document Type: Chapter

References (90)

1. Curcio MJ, Derbyshire KM. 2003. The outs and ins of transposition:From Mu to kangaroo. Nature Rev Mol Cell Biol 4:865-877.
2. Montano SP, Rice PA. 2011. Moving DNA around:DNA transposition and retroviral integration. Curr Opin Struct Biol 21:370-378.
3. Chandler M, de la Cruz F, Dyda F, Hickman AB, Moncalian G, Ton-Hoang B. 2013. Breaking and joining single-stranded DNA:the HUH endonuclease superfamily. Nature Rev Microbiol 11:525-538.
4. Yang W. 2011. Nucleases:diversity of structure, function and mechanism. Quart Rev Biophys 44:1-93.
5. Dyda F, Hickman AB, Jenkins TM, Engelman A, Craigie R, Davies DR. 1994. Crystal structure of the catalytic domain of HIV-1 integrase:Similarity to other polynucleotidyl transferases. Science 266:1981-1986.
6. Rice P, Mizuuchi K. 1995. Structure of the bacteriophage Mu transposase core:A common structural motif for DNA transposition and retroviral integration. Cell 82:209-220.
7. Yuan YW, Wessler SR. 2011. The catalytic domain of all eukaryotic cut-and-paste transposase superfamilies. Proc Natl Acad Sci USA 108:7884-7889.
8. Koonin EV, Ilyina TV. 1993. Computer-assisted dissection of rolling circle DNA replication. BioSystems 30:241-268.
9. Smith MCM, Thorpe HM. 2002. Diversity in the serine recombinases. Mol Microbiol 44:299-307.
10. Smith MCM, Brown WRA, McEwan AR, Rowley PA. 2010. Site-specific recombination by FC31 integrase and other large serine recombinases. Biochem Soc Trans 38:388-394.
11. Rajeev L, Malanowska K, Gardner JF. 2009. Challenging a paradigm:the role of DNA homology in tyrosine recombinase reactions. Microbiol Mol Biol Rev 73:300-309.
12. Beese LS, Steitz TA. 1991. Structural basis for the 3-5 exonuclease activity of Escherichia coli DNA polymerase I:a two metal ion mechanism. EMBO J 10:25-33.
13. Nowotny M, Gaidamakov SA, Crouch RJ, Yang W. 2005. Crystal structures of RNase H bound to an RNA/DNA hybrid:Substrate specificity and metaldependent catalysis. Cell 121:1005-1016.
14. Nowotny M, Yang W. 2006. Stepwise analyses of metal ions in RNase H catalysis from substrate destabilization to product release. EMBO J 25:1924-1933.
15. Rosta E, Woodcock HL, Brooks BR, Hummer G. 2009. Artificial reaction coordinate "tunneling" in freeenergy calculations:The catalytic reaction of RNase H. J Comput Chem 30:1634-1641.
16. Rosta E, Nowotny M, Yang W, Hummer G. 2011. Catalytic mechanism of RNA backbone cleavage by ribonuclease H from quantum mechanics/molecular mechanics simulations. J Am Chem Soc 133:8934-8941.
17. Mizuuchi K, Adzuma K. 1991. Inversion of the phosphate chirality at the target site of Mu DNA strand transfer:evidence for a one-step transesterification mechanism. Cell 66:129-140.
18. Engelman A, Mizuuchi K, Craigie R. 1991. HIV-1 DNA integration:mechanism of viral DNA cleavage and DNA strand transfer. Cell 67:1211-1221.
19. Kennedy AK, Haniford DB, Mizuuchi K. 2000. Single active site catalysis of the successive phosphoryl transfer steps by DNA transposases:Insights from phosphorothioate stereoselectivity. Cell 101:295-305.
20. Levchenko I, Luo L, Baker TA. 1995. Disassembly of the Mu transposase tetramer by the ClpX chaperone. Genes Dev 9:2399-2408.
21. Bolland S, Kleckner N. 1996. The three chemical steps of Tn10/IS10 transposition involve repeated utilization of a single active site. Cell 84:223-233.
22. Rosta E, Yang W, Hummer G. 2014. Calcium inhibition of Ribonuclease H1 two-metal ion catalysis. J Am Chem Soc 136:3137-3144.
23. Savilahti H, Rice PA, Mizuuchi K. 1995. The phage Mu transpososome core:DNA requirements for assembly and function. EMBO J 14:4893-4903.
24. Steitz TA, Steitz JA. 1993. A general two-metal-ion mechanism for catalytic RNA. Proc Natl Acad Sci USA 90:6498-6502.
25. Stahley MR, Strobel SA. 2005. Structural evidence for a two-metal-ion mechanism of group I intron splicing. Science 309:1587-1590.
26. Nowotny M. 2009. Retroviral integrase superfamily:the structural perspective. EMBO Reports 10:144-151.
27. Nakamura T, Zhao Y, Yamagata Y, Hua YJ, Yang W. 2012. Watching DNA polymerase ? make a phosphodiester bond. Nature 487:196-201.
28. Ton-Hoang B, Guynet C, Ronning DR, Cointin-Marty B, Dyda F, Chandler M. 2005. Transposition of ISHp608, member of an unusual family of bacterial insertion sequences. EMBO J 24:3325-3338.
29. Ronning DR, Guynet C, Ton-Hoang B, Perez ZN, Ghirlando R, Chandler M, Dyda F. 2005. Active site sharing and subterminal hairpin recognition in a new class of DNA transposases. Mol Cell 20:143-154.
30. Guynet C, Hickman AB, Barabas O, Dyda F, Chandler M, Ton-Hoang B. 2008. In vitro reconstitution of a single-stranded transposition mechanism of IS608. Mol Cell 29:302-312.
31. Barabas O, Ronning DR, Guynet C, Hickman AB, Ton-Hoang B, Chandler M, Dyda F. 2008. Mechanism of IS200/IS605 family DNA transposases:Activation and transposon-directed target site selection. Cell 132:208-220.
32. Hickman AB, James JA, Barabas O, Pasternak C, Ton-Hoang B, Chandler M, Sommer S, Dyda F. 2010. DNA recognition and the precleavage state during single-stranded DNA transposition in D. radiodurans. EMBO J 29:3840-3852.
33. He S, Hickman AB, Dyda F, Johnson NP, Chandler M, Ton-Hoang B. 2011. Reconstitution of a functional IS608 single-strand transpososome:role of non-canonical base pairing. Nucl Acids Res 39:8503-8512.
34. He S, Guynet C, Siguier P, Hickman AB, Dyda F, Chandler M, Ton-Hoang B. 2013. IS200/IS605 family single-strand transposition:mechanism of IS608 strand transfer. Nucl Acids Res 41:3302-3313.
35. Hickman AB, Ronning DR, Kotin RM, Dyda F. 2002. Structural unity among viral origin binding proteins:Crystal structure of the nuclease domain of adeno-associated virus Rep. Mol Cell 10:327-337.
36. Datta S, Larkin C, Schildbach JF. 2003. Structural insights into single-stranded DNA binding and cleavage by F factor TraI. Struct 11:1369-1379.
37. Boer R, Russi S, Guasch A, Lucas M, Blanco AG, Pérez-Luque R, Coll M, de la Cruz F. 2006. Unveiling the molecular mechanism of a conjugative relaxase:The structure of TrwC complexed with a 27-mer DNA comprising the recognition hairpin and the cleavage site. J Mol Biol 358:857-869.
38. Toleman MA, Bennett PM, Walsh TR. 2006. ISCR elements:Novel gene-capturing systems of the 21st century? Microbiol Mol Biol Rev 70:296-316.
39. Ton-Hoang B, Siguier P, Quentin Y, Onillon S, Marty B, Fichant G, Chandler M. 2012. Structuring the bacterial genome:Y1-transposases associated with REPBIME sequences. Nucl Acids Res 40:3596-3609.
40. Nunvar J, Huckova T, Licha I. 2010. Identification and characterization of repetitive extragenic palindromes (REP)-associated tyrosine transposases:implications for REP evolution and dynamics in bacterial genomes. BMC Genomics 11:44.
41. Kapitonov VV, Jurka J. 2001. Rolling-circle transposons in eukaryotes. Proc Natl Acad Sci USA 98:8714-8719.
42. Feschotte C, Wessler SR. 2001. Treasures in the attic:Rolling circle transposons discovered in eukaryotic genomes. Proc Natl Acad Sci USA 98:8923-8924.
43. Pritham EJ, Feschotte C. 2007. Massive amplification of rolling-circle transposons in the lineage of the bat Myotis lucifugus. Proc Natl Acad Sci USA 104:1895-1900.
44. Kersulyte D, Mukhopadhyay AK, Shirai M, Nakazawa T, Berg DE. 2000. Functional organization and insertion specificity of IS607, a chimeric element of Helicobacter pylori. J Bacteriol 182:5300-5308.
45. Boocock MR, Rice PA. 2013. A proposed mechanism for IS607-family serine transposases. Mobile DNA 4:24.
46. 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.
47. 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.
48. Grindley NDF, Whiteson KL, Rice PA. 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75:567-605.
49. 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.
50. Kersulyte D, Kalia A, Zhang MJ, Lee HK, Subramaniam D, Kiuduliene L, Chalkauskas H, Berg DE. 2004. Sequence organization and insertion specificity of the novel chimeric ISHp609 transposable element of Helicobacter pylori. J Bacteriol 186:7521-7528.
51. Sanderson MR, Freemont PS, Rice PA, Goldman A, Hatfull GF, Grindley NDF, Steitz TA. 1990. The crystal structure of the catalytic domain of the site-specific recombination enzyme ?d resolvase at 2.7 A ° resolution. Cell 63:1323-1329.
52. Li W, Kamtekar S, Xiong Y, Sarkis GJ, Grindley NDF, Steitz TA. 2005. Structure of a synaptic ?d resolvase tetramer covalently linked to two cleaved DNAs. Science 309:1210-1215.
53. Keenholtz RA, Rowland SJ, Boocock MR, Stark WM, Rice PA. 2011. Structural basis for catalytic activation of a serine recombinase. Struct 19:799-809.
54. Keenholtz RA, Mouw KW, Boocock MR, Li NS, Piccirilli JA, Rice PA. 2013. Arginine as a general acid catalyst in serine recombinase-mediated DNA cleavage. J Biol Chem 288:29206-29214.
55. Hickman AB, Waninger S, Scocca JJ, Dyda F. 1997. Molecular organization in site-specific recombination:The catalytic domain of bacteriophage HP1 integrase at 2.7A° resolution. Cell 89:227-237.
56. Kwon HJ, Tirumalai R, Landy A, Ellenberger T. 1997. Flexibility in DNA recombination:Structure of the lambda integrase catalytic core. Science 276:126-131.
57. Chen Y, Rice PA. 2003. New insight into site-specific recombination from Flp recombinase-DNA structures. Annu Rev Biophys Biomol Struct 32:135-159.
58. Roberts AP, Mullany P. 2009. A modular master on the move:the Tn916 family of mobile genetic elements. Trends Microbiol 17:251-258.
59. Waters JL, Salyers AA. 2013. Regulation of CTnDOT conjugative transfer is a complex and highly coordinated series of events. mBio 4:e00569-13.
60. Brochet M, Da Cunha V, Couvé E, Rusniok C, Trieu-Cuot P, Glaser P. 2009. Atypical association of DDE transposition with conjugation specifies a new family of mobile element. Mol Microbiol 71:948-959.
61. Guérillot R, Siguier P, Gourbeyre E, Chandler M, Glaser P. 2014. The diversity of prokaryotic DDE transposases of the Mutator superfamily, insertion specificity, and association with conjugation machineries. Genome Biol Evol 6:260-272.
62. Harshey RM. 2012. The Mu story:how a maverick phage moved the field forward. Mobile DNA 3:21.
63. Mizuuchi K. 1992. Transpositional recombination:Mechanistic insights from studies of Mu and other elements. Annu Rev Biochem 61:1011-1051.
64. North SH, Kirtland SE, Nakai H. 2007. Translation factor IF2 at the interface of transposition and replication by the PriA-PriC pathway. Mol Microbiol 66:1566-1578.
65. Jones JM, Nakai H. 1999. Duplex opening by primosome protein PriA for replisome assembly on a recombination intermediate. J Mol Biol 289:503-515.
66. Duval-Valentin G, Marty-Cointin B, Chandler M. 2004. Requirement of IS911 replication before integration defines a new bacterial transposition pathway. EMBO J 23:3897-3906.
67. Ton-Hoang B, Polard P, Chandler M. 1998. Efficient transposition of IS911 circles in vitro. EMBO J 17:1169-1181.
68. Polard P, Chandler M. 1995. An in vivo transposasecatalyzed single-stranded DNA circularization reaction. Genes Dev 9:2846-2858.
69. Ton-Hoang B, Bétermier M, Polard P, Chandler M. 1997. Assembly of a strong promoter following IS911 circularization and the role of circles in transposition. EMBO J 16:3357-3371.
70. Turlan C, Chandler M. 2000. Playing second fiddle:second-strand processing and liberation of transposable elements from donor DNA. Trends Microbiol 8:268-274.
71. Hickman AB, Chandler M, Dyda F. 2010. Integrating prokaryotes and eukaryotes:DNA transposases in light of structure. Crit Rev Biochem Mol Biol 45:50-69.
72. Dawson A, Finnegan DJ. 2003. Excision of the Drosophila mariner transposon Mos1:Comparison with bacterial transposition and V(D)J recombination. Mol Cell 11:225-235.
73. Claeys Bouuaert C, Chalmers R. 2010. Transposition of the human Hsmar1 transposon:rate-limiting steps and the importance of the flanking TA dinucleotide in second strand cleavage. Nucl Acids Res 38:190-202.
74. Lampe DJ, Churchill MEA, Robertson HM. 1996. A purified mariner transposase is sufficient to mediate transposition in vitro. EMBO J 15:5470-5479.
75. Beall EL, Rio DC. 1997. Drosophila P-element transposase is a novel site-specific endonuclease. Genes Dev 11:2137-2151.
76. Steiniger-White M, Rayment I, Reznikoff WS. 2004. Structure/function insights into Tn5 transposition. Curr Opin Struct Biol 14:50-57.
77. Mitra R, Fain-Thornton J, Craig NL. 2008. piggyBac can bypass DNA synthesis during cut and paste transposition. EMBO J 27:1097-1109.
78. Zhou L, Mitra R, Atkinson PW, Hickman AB, Dyda F, Craig NL. 2004. Transposition of hAT elements links transposable elements and V(D)J recombination. Nature 432:995-1001.
79. Schatz DG, Swanson PC. 2011. V(D)J recombination:Mechanisms of initiation. Annu Rev Genet 45:167-202.
80. Kapitonov VV, Jurka J. 2005. RAG1 core and V(D)J recombination signal sequences were derived from Transib transposons. PLoS Biol 3:e181.
81. Tang M, Cecconi C, Bustamante C, Rio DC. 2007. Analysis of P element transposase protein-DNA interactions during the early stages of transposition. J Biol Chem 282:29002-29012.
82. Biery MC, Lopata M, Craig NL. 2000. A minimal system for Tn7 transposition:The transposon-encoded proteins TnsA and TnsB can execute DNA breakage and joining reactions that generate circularized Tn7 species. J Mol Biol 297:25-37.
83. Choi KY, Li Y, Sarnovsky R, Craig NL. 2013. Direct interaction between the TnsA and TnsB subunits controls the heteromeric Tn7 transposase. Proc Natl Acad Sci USA 110:E2038-E2045.
84. Hickman AB, Li Y, Mathew SV, May EW, Craig NL, Dyda F. 2000. Unexpected structural diversity in DNA recombination:The restriction endonuclease connection. Mol Cell 5:1025-1034.
85. May EW, Craig NL. 1996. Switching from cut-andpaste to replicative Tn7 transposition. Science 272:401-404.
86. Davies DR, Goryshin IY, Reznikoff WS, Rayment I. 2000. Three-dimensional structure of the Tn5 synaptic complex transposition intermediate. Science 289:77-85.
87. Richardson JM, Colloms SD, Finnegan DJ, Walkinshaw MD. 2009. Molecular architecture of the Mos1 pairedend complex:The structural basis of DNA transposition in a eukaryote. Cell 138:1096-1108.
88. Hickman AB, et al. 2014. Structural basis of hAT transposon end recognition by Hermes, an octameric DNA transposase from Musca domestica. Cell 158:353-367.
89. Dyda F, Chandler M, Hickman AB. 2012. The emerging diversity of transpososome architectures. Quart Rev Biophys 45:493-521.
90. Montano SP, Pigli YZ, Rice PA. 2012. The Mu transpososome structure sheds light on DDE recombinase evolution. Nature 491:413-417.