An Atypical AAA+ ATPase Assembly Controls Efficient Transposition through DNA Remodeling and Transposase Recruitment

Cell

Volumn 162, Issue 4, 2015, Pages 860-871

  Arias Palomo, Ernesto ^a   Berger, James M ^a  

^a JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE TRIPHOSPHATASE; ADENOSINE TRIPHOSPHATE; BACTERIAL DNA; BACTERIAL PROTEIN; CURVED DNA; DNA BINDING PROTEIN; ISTA PROTEIN; ISTB PROTEIN; OLIGOMER; TRANSPOSASE; UNCLASSIFIED DRUG; TRANSPOSON;

AMINO TERMINAL SEQUENCE; ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; DNA REPLICATION; DNA TRANSPOSITION; ELECTRON TOMOGRAPHY; ENZYME SUBUNIT; GEL PERMEATION CHROMATOGRAPHY; GEOBACILLUS STEAROTHERMOPHILUS; HYDROLYSIS; NONHUMAN; PHYLOGENY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; THIN LAYER CHROMATOGRAPHY; TRANSPOSON; X RAY CRYSTALLOGRAPHY; AMINO ACID SEQUENCE; BACTERIUM; CLASSIFICATION; ENZYMOLOGY; GENETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR MODEL; SEQUENCE ALIGNMENT;

ADENOSINE TRIPHOSPHATE; AMINO ACID SEQUENCE; BACTERIA; DNA TRANSPOSABLE ELEMENTS; DNA, BACTERIAL; DNA-BINDING PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; TRANSPOSASES;

EID: 84939215665     PISSN: 00928674     EISSN: 10974172     Source Type: Journal    
DOI: 10.1016/j.cell.2015.07.037     Document Type: Article

References (85)

1. P.D. Adams, P.V. Afonine, G. Bunkóczi, V.B. Chen, I.W. Davis, N. Echols, J.J. Headd, L.-W. Hung, G.J. Kapral, R.W. Grosse-Kunstleve, and et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr. D Biol. Crystallogr. 66 2010 213 221
2. C. Ade, A.M. Roy-Engel, and P.L. Deininger Alu elements: an intrinsic source of human genome instability Curr. Opin. Virol. 3 2013 639 645
3. A. Allué-Guardia, L. Imamovic, and M. Muniesa Evolution of a self-inducible cytolethal distending toxin type V-encoding bacteriophage from Escherichia coli O157:H7 to Shigella sonnei J. Virol. 87 2013 13665 13675
4. Y. Arakawa, M. Murakami, K. Suzuki, H. Ito, R. Wacharotayankun, S. Ohsuka, N. Kato, and M. Ohta A novel integron-like element carrying the metallo-beta-lactamase gene blaIMP Antimicrob. Agents Chemother. 39 1995 1612 1615
5. E. Arias-Palomo, V.L. O'Shea, I.V. Hood, and J.M. Berger The bacterial DnaC helicase loader is a DnaB ring breaker Cell 153 2013 438 448
6. R.K. Aziz, M. Breitbart, and R.A. Edwards Transposases are the most abundant, most ubiquitous genes in nature Nucleic Acids Res. 38 2010 4207 4217
7. J.K. Baillie, M.W. Barnett, K.R. Upton, D.J. Gerhardt, T.A. Richmond, F. De Sapio, P.M. Brennan, P. Rizzu, S. Smith, M. Fell, and et al. Somatic retrotransposition alters the genetic landscape of the human brain Nature 479 2011 534 537
8. T.A. Baker, M. Mizuuchi, and K. Mizuuchi MuB protein allosterically activates strand transfer by the transposase of phage Mu Cell 65 1991 1003 1013
9. B. Berger, and D. Haas Transposase and cointegrase: specialized transposition proteins of the bacterial insertion sequence IS21 and related elements Cell. Mol. Life Sci. 58 2001 403 419
10. C. Biémont A brief history of the status of transposable elements: from junk DNA to major players in evolution Genetics 186 2010 1085 1093
11. C. Buchrieser, R. Brosch, S. Bach, A. Guiyoule, and E. Carniel The high-pathogenicity island of Yersinia pseudotuberculosis can be inserted into any of the three chromosomal asn tRNA genes Mol. Microbiol. 30 1998 965 978
12. M. Bundo, M. Toyoshima, Y. Okada, W. Akamatsu, J. Ueda, T. Nemoto-Miyauchi, F. Sunaga, M. Toritsuka, D. Ikawa, A. Kakita, and et al. Increased l1 retrotransposition in the neuronal genome in schizophrenia Neuron 81 2014 306 313
13. V. Burland, Y. Shao, N.T. Perna, G. Plunkett, H.J. Sofia, and F.R. Blattner The complete DNA sequence and analysis of the large virulence plasmid of Escherichia coli O157:H7 Nucleic Acids Res. 26 1998 4196 4204
14. K.H. Burns, and J.D. Boeke Human transposon tectonics Cell 149 2012 740 752
15. P.S.G. Chain, E. Carniel, F.W. Larimer, J. Lamerdin, P.O. Stoutland, W.M. Regala, A.M. Georgescu, L.M. Vergez, M.L. Land, V.L. Motin, and et al. Insights into the evolution of Yersinia pestis through whole-genome comparison with Yersinia pseudotuberculosis Proc. Natl. Acad. Sci. USA 101 2004 13826 13831
16. P. Cherepanov, G.N. Maertens, and S. Hare Structural insights into the retroviral DNA integration apparatus Curr. Opin. Struct. Biol. 21 2011 249 256
17. N.G. Coufal, J.L. Garcia-Perez, G.E. Peng, G.W. Yeo, Y. Mu, M.T. Lovci, M. Morell, K.S. O'Shea, J.V. Moran, and F.H. Gage L1 retrotransposition in human neural progenitor cells Nature 460 2009 1127 1131
18. N.G. Coufal, J.L. Garcia-Perez, G.E. Peng, M.C.N. Marchetto, A.R. Muotri, Y. Mu, C.T. Carson, A. Macia, J.V. Moran, and F.H. Gage Ataxia telangiectasia mutated (ATM) modulates long interspersed element-1 (L1) retrotransposition in human neural stem cells Proc. Natl. Acad. Sci. USA 108 2011 20382 20387
19. N.L. Craig, R. Craigie, M. Gellert, and A.M. Lambowitz Mobile DNA II 2002 ASM Press Washington, DC
20. R. Craigie, and K. Mizuuchi Role of DNA topology in Mu transposition: mechanism of sensing the relative orientation of two DNA segments Cell 45 1986 793 800
21. R. Craigie, D.J. Arndt-Jovin, and K. Mizuuchi A defined system for the DNA strand-transfer reaction at the initiation of bacteriophage Mu transposition: protein and DNA substrate requirements Proc. Natl. Acad. Sci. USA 82 1985 7570 7574
22. M.J. Curcio, and K.M. Derbyshire The outs and ins of transposition: from mu to kangaroo Nat. Rev. Mol. Cell Biol. 4 2003 865 877
23. D.R. Davies, I.Y. Goryshin, W.S. Reznikoff, and I. Rayment Three-dimensional structure of the Tn5 synaptic complex transposition intermediate Science 289 2000 77 85
24. K.E. Duderstadt, K. Chuang, and J.M. Berger DNA stretching by bacterial initiators promotes replication origin opening Nature 478 2011 209 213
25. E.L.C. Dueber, J.E. Corn, S.D. Bell, and J.M. Berger Replication origin recognition and deformation by a heterodimeric archaeal Orc1 complex Science 317 2007 1210 1213
26. F. Dyda, M. Chandler, and A.B. Hickman The emerging diversity of transpososome architectures Q. Rev. Biophys. 45 2012 493 521
27. P. Emsley, and K. Cowtan Coot: model-building tools for molecular graphics Acta Crystallogr. D Biol. Crystallogr. 60 2004 2126 2132
28. E.J. Enemark, and L. Joshua-Tor Mechanism of DNA translocation in a replicative hexameric helicase Nature 442 2006 270 275
29. J.P. Erzberger, and J.M. Berger Evolutionary relationships and structural mechanisms of AAA+ proteins Annu. Rev. Biophys. Biomol. Struct. 35 2006 93 114
30. J.P. Erzberger, M.L. Mott, and J.M. Berger Structural basis for ATP-dependent DnaA assembly and replication-origin remodeling Nat. Struct. Mol. Biol. 13 2006 676 683
31. A.A. Filippov, P.V. Oleinikov, V.L. Motin, O.A. Protsenko, and G.B. Smirnov Sequencing of two Yersinia pestis IS elements, IS285 and IS100 Contrib. Microbiol. Immunol. 13 1995 306 309
32. P. Gamas, and N.L. Craig Purification and characterization of TnsC, a Tn7 transposition protein that binds ATP and DNA Nucleic Acids Res. 20 1992 2525 2532
33. E.C. Greene, and K. Mizuuchi Dynamics of a protein polymer: the assembly and disassembly pathways of the MuB transposition target complex EMBO J. 21 2002 1477 1486
34. E.C. Greene, and K. Mizuuchi Direct observation of single MuB polymers: evidence for a DNA-dependent conformational change for generating an active target complex Mol. Cell 9 2002 1079 1089
35. B. Hallet, R. Rezsöhazy, J. Mahillon, and J. Delcour IS231A insertion specificity: consensus sequence and DNA bending at the target site Mol. Microbiol. 14 1994 131 139
36. R.M. Harshey, and M. Jayaram The mu transpososome through a topological lens Crit. Rev. Biochem. Mol. Biol. 41 2006 387 405
37. A.B. Hickman, H.E. Ewis, X. Li, J.A. Knapp, T. Laver, A.-L. Doss, G. Tolun, A.C. Steven, A. Grishaev, A. Bax, and et al. Structural basis of hAT transposon end recognition by Hermes, an octameric DNA transposase from Musca domestica Cell 158 2014 353 367
38. M. Hohn, G. Tang, G. Goodyear, P.R. Baldwin, Z. Huang, P.A. Penczek, C. Yang, R.M. Glaeser, P.D. Adams, and S.J. Ludtke SPARX, a new environment for Cryo-EM image processing J. Struct. Biol. 157 2007 47 55
39. L. Holm, and C. Sander Dali: a network tool for protein structure comparison Trends Biochem. Sci. 20 1995 478 480
40. P. Hu, J. Elliott, P. McCready, E. Skowronski, J. Garnes, A. Kobayashi, R.R. Brubaker, and E. Garcia Structural organization of virulence-associated plasmids of Yersinia pestis J. Bacteriol. 180 1998 5192 5202
41. Z. Ivics, M.A. Li, L. Mátés, J.D. Boeke, A. Nagy, A. Bradley, and Z. Izsvák Transposon-mediated genome manipulation in vertebrates Nat. Methods 6 2009 415 422
42. L.M. Iyer, D.D. Leipe, E.V. Koonin, and L. Aravind Evolutionary history and higher order classification of AAA+ ATPases J. Struct. Biol. 146 2004 11 31
43. P.D. Kaufman, and D.C. Rio P element transposition in vitro proceeds by a cut-and-paste mechanism and uses GTP as a cofactor Cell 69 1992 27 39
44. H.H. Kazazian Jr. Mobile elements: drivers of genome evolution Science 303 2004 1626 1632
45. B.A. Kelch, D.L. Makino, M. O'Donnell, and J. Kuriyan How a DNA polymerase clamp loader opens a sliding clamp Science 334 2011 1675 1680
46. E.V. Koonin DnaC protein contains a modified ATP-binding motif and belongs to a novel family of ATPases including also DnaA Nucleic Acids Res. 20 1992 1997
47. P.N. Kuduvalli, J.E. Rao, and N.L. Craig Target DNA structure plays a critical role in Tn7 transposition EMBO J. 20 2001 924 932
48. E.S. Lander, L.M. Linton, B. Birren, C. Nusbaum, M.C. Zody, J. Baldwin, K. Devon, K. Dewar, M. Doyle, W. FitzHugh, et al. International Human Genome Sequencing Consortium Initial sequencing and analysis of the human genome Nature 409 2001 860 921
49. G.C. Lander, S.M. Stagg, N.R. Voss, A. Cheng, D. Fellmann, J. Pulokas, C. Yoshioka, C. Irving, A. Mulder, P.W. Lau, and et al. Appion: an integrated, database-driven pipeline to facilitate EM image processing J. Struct. Biol. 166 2009 95 102
50. G.N. Maertens, S. Hare, and P. Cherepanov The mechanism of retroviral integration from X-ray structures of its key intermediates Nature 468 2010 326 329
51. A. Maxwell, R. Craigie, and K. Mizuuchi B protein of bacteriophage mu is an ATPase that preferentially stimulates intermolecular DNA strand transfer Proc. Natl. Acad. Sci. USA 84 1987 699 703
52. B. McClintock The origin and behavior of mutable loci in maize Proc. Natl. Acad. Sci. USA 36 1950 344 355
53. J.L. Miller, S.K. Anderson, D.J. Fujita, G. Chaconas, D.L. Baldwin, and R.M. Harshey The nucleotide sequence of the B gene of bacteriophage Mu Nucleic Acids Res. 12 1984 8627 8638
54. N. Mizuno, M. Dramićanin, M. Mizuuchi, J. Adam, Y. Wang, Y.-W. Han, W. Yang, A.C. Steven, K. Mizuuchi, and S. Ramón-Maiques MuB is an AAA+ ATPase that forms helical filaments to control target selection for DNA transposition Proc. Natl. Acad. Sci. USA 110 2013 E2441 E2450
55. K. Mizuuchi Transpositional recombination: mechanistic insights from studies of mu and other elements Annu. Rev. Biochem. 61 1992 1011 1051
56. S.P. Montaño, and P.A. Rice Moving DNA around: DNA transposition and retroviral integration Curr. Opin. Struct. Biol. 21 2011 370 378
57. S.P. Montaño, Y.Z. Pigli, and P.A. Rice The μ transpososome structure sheds light on DDE recombinase evolution Nature 491 2012 413 417
58. M.L. Mott, J.P. Erzberger, M.M. Coons, and J.M. Berger Structural synergy and molecular crosstalk between bacterial helicase loaders and replication initiators Cell 135 2008 623 634
59. H.P. Müller, and H.E. Varmus DNA bending creates favored sites for retroviral integration: an explanation for preferred insertion sites in nucleosomes EMBO J. 13 1994 4704 4714
60. J. Parkhill, B.W. Wren, N.R. Thomson, R.W. Titball, M.T. Holden, M.B. Prentice, M. Sebaihia, K.D. James, C. Churcher, K.L. Mungall, and et al. Genome sequence of Yersinia pestis, the causative agent of plague Nature 413 2001 523 527
61. J. Parkhill, M. Sebaihia, A. Preston, L.D. Murphy, N. Thomson, D.E. Harris, M.T.G. Holden, C.M. Churcher, S.D. Bentley, K.L. Mungall, and et al. Comparative analysis of the genome sequences of Bordetella pertussis, Bordetella parapertussis and Bordetella bronchiseptica Nat. Genet. 35 2003 32 40
62. R.D. Perry, S.C. Straley, J.D. Fetherston, D.J. Rose, J. Gregor, and F.R. Blattner DNA sequencing and analysis of the low-Ca2+-response plasmid pCD1 of Yersinia pestis KIM5 Infect. Immun. 66 1998 4611 4623
63. J.E. Peters, and N.L. Craig Tn7: smarter than we thought Nat. Rev. Mol. Cell Biol. 2 2001 806 814
64. E.F. Pettersen, T.D. Goddard, C.C. Huang, G.S. Couch, D.M. Greenblatt, E.C. Meng, and T.E. Ferrin UCSF Chimera - a visualization system for exploratory research and analysis J. Comput. Chem. 25 2004 1605 1612
65. O.N. Podladchikova, G.G. Dikhanov, A.V. Rakin, and J. Heesemann Nucleotide sequence and structural organization of Yersinia pestis insertion sequence IS100 FEMS Microbiol. Lett. 121 1994 269 274
66. P.A. Pribil, and D.B. Haniford Target DNA bending is an important specificity determinant in target site selection in Tn10 transposition J. Mol. Biol. 330 2003 247 259
67. D. Pruss, F.D. Bushman, and A.P. Wolffe Human immunodeficiency virus integrase directs integration to sites of severe DNA distortion within the nucleosome core Proc. Natl. Acad. Sci. USA 91 1994 5913 5917
68. C. Reimmann, and D. Haas The istA gene of insertion sequence IS21 is essential for cleavage at the inner 3′ ends of tandemly repeated IS21 elements in vitro EMBO J. 9 1990 4055 4063
69. C. Reimmann, R. Moore, S. Little, A. Savioz, N.S. Willetts, and D. Haas Genetic structure, function and regulation of the transposable element IS21 Mol. Gen. Genet. 215 1989 416 424
70. J. Sakai, R.M. Chalmers, and N. Kleckner Identification and characterization of a pre-cleavage synaptic complex that is an early intermediate in Tn10 transposition EMBO J. 14 1995 4374 4383
71. A. Sancar, and J.E. Hearst Molecular matchmakers Science 259 1993 1415 1420
72. S.H. Scheres, R. Núñez-Ramírez, C.O. Sorzano, J.M. Carazo, and R. Marabini Image processing for electron microscopy single-particle analysis using XMIPP Nat. Protoc. 3 2008 977 990
73. S. Schmid, T. Seitz, and D. Haas Cointegrase, a naturally occurring, truncated form of IS21 transposase, catalyzes replicon fusion rather than simple insertion of IS21 J. Mol. Biol. 282 1998 571 583
74. S. Schmid, B. Berger, and D. Haas Target joining of duplicated insertion sequence IS21 is assisted by IstB protein in vitro J. Bacteriol. 181 1999 2286 2289
75. P. Siguier, E. Gourbeyre, and M. Chandler Bacterial insertion sequences: their genomic impact and diversity FEMS Microbiol. Rev. 38 2014 865 891
76. K.R. Simonetta, S.L. Kazmirski, E.R. Goedken, A.J. Cantor, B.A. Kelch, R. McNally, S.N. Seyedin, D.L. Makino, M. O'Donnell, and J. Kuriyan The mechanism of ATP-dependent primer-template recognition by a clamp loader complex Cell 137 2009 659 671
77. M. Speek Antisense promoter of human L1 retrotransposon drives transcription of adjacent cellular genes Mol. Cell. Biol. 21 2001 1973 1985
78. A.E. Stellwagen, and N.L. Craig Gain-of-function mutations in TnsC, an ATP-dependent transposition protein that activates the bacterial transposon Tn7 Genetics 145 1997 573 585
79. C. Suloway, J. Pulokas, D. Fellmann, A. Cheng, F. Guerra, J. Quispe, S. Stagg, C.S. Potter, and B. Carragher Automated molecular microscopy: the new Leginon system J. Struct. Biol. 151 2005 41 60
80. M.G. Surette, and G. Chaconas A protein factor which reduces the negative supercoiling requirement in the Mu DNA strand transfer reaction is Escherichia coli integration host factor J. Biol. Chem. 264 1989 3028 3034
81. M. Tang, C. Cecconi, H. Kim, C. Bustamante, and D.C. Rio Guanosine triphosphate acts as a cofactor to promote assembly of initial P-element transposase-DNA synaptic complexes Genes Dev. 19 2005 1422 1425
82. G. Tang, L. Peng, P.R. Baldwin, D.S. Mann, W. Jiang, I. Rees, and S.J. Ludtke EMAN2: an extensible image processing suite for electron microscopy J. Struct. Biol. 157 2007 38 46
83. J.M.C. Tubio, Y. Li, Y.S. Ju, I. Martincorena, S.L. Cooke, M. Tojo, G. Gundem, C.P. Pipinikas, J. Zamora, K. Raine, et al. ICGC Breast Cancer Group ICGC Bone Cancer Group ICGC Prostate Cancer Group Mobile DNA in cancer. Extensive transduction of nonrepetitive DNA mediated by L1 retrotransposition in cancer genomes Science 345 2014 1251343-1251343
84. E.M. Wolff, H.-M. Byun, H.F. Han, S. Sharma, P.W. Nichols, K.D. Siegmund, A.S. Yang, P.A. Jones, and G. Liang Hypomethylation of a LINE-1 promoter activates an alternate transcript of the MET oncogene in bladders with cancer PLoS Genet. 6 2010 e1000917
85. K. Xu, Z.Q. He, Y.M. Mao, R.Q. Sheng, and Z.J. Sheng On two transposable elements from Bacillus stearothermophilus Plasmid 29 1993 1 9