The structure of Xis reveals the basis for filament formation and insight into DNA bending within a mycobacteriophage intasome

Journal of Molecular Biology

Volumn 426, Issue 2, 2014, Pages 412-422

  Singh, Shweta ^a   Plaks, Joseph G ^a   Homa, Nicholas J ^a,c   Amrich, Christopher G ^a   Héroux, Annie ^b   Hatfull, Graham F ^a   Vandemark, Andrew P ^a  

^a UNIVERSITY OF PITTSBURGH   (United States)

^b BROOKHAVEN NATIONAL LABORATORY   (United States)

^c DUKE UNIVERSITY   (United States)

Author keywords

DNA bending; DNA recombination; mycobacteriophage; structure; Xis

Indexed keywords

CURVED DNA; UNCLASSIFIED DRUG; VIRUS PROTEIN; XIS PROTEIN;

ARTICLE; BACTERIOPHAGE LAMBDA; BINDING SITE; DNA BINDING; GEL ELECTROPHORESIS; IN VITRO STUDY; MYCOBACTERIOPHAGE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; X RAY CRYSTALLOGRAPHY;

DNA BENDING; DNA RECOMBINATION; EDTA; ETHYLENEDIAMINETETRAACETIC ACID; MYCOBACTERIOPHAGE; PEG; POLYETHYLENE GLYCOL; STRUCTURE; XIS;

ATTACHMENT SITES, MICROBIOLOGICAL; BINDING SITES; DNA NUCLEOTIDYLTRANSFERASES; DNA, VIRAL; MYCOBACTERIOPHAGES; PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; PROTEIN MULTIMERIZATION; VIRAL PROTEINS;

EID: 84891829647     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2013.10.002     Document Type: Article

References (43)

1. A. Landy Dynamic, structural, and regulatory aspects of lambda site-specific recombination Annu Rev Biochem 58 1989 913 949
2. G.D. Van Duyne Lambda integrase: armed for recombination Curr Biol 15 2005 R658 R660
3. M.A. Azaro, and A. Landy λ Int and the λ Int family N.L. Craig, R. Craigie, M. Gellert, A.M. Lambowitz, Mobile DNA II 2002 American Society Microbiology Washington, DC 118 148
4. B. Franz, and A. Landy The Holliday junction intermediates of lambda integrative and excisive recombination respond differently to the bending proteins integration host factor and excisionase EMBO J 14 1995 397 406
5. S.E. Nunes-Duby, M.A. Azaro, and A. Landy Swapping DNA strands and sensing homology without branch migration in lambda site-specific recombination Curr Biol 5 1995 139 148
6. S. Kim, and A. Landy Lambda Int protein bridges between higher order complexes at two distant chromosomal loci attL and attR Science 256 1992 198 203
7. W. Bushman, S. Yin, L.L. Thio, and A. Landy Determinants of directionality in lambda site-specific recombination Cell 39 1984 699 706
8. L. Moitoso de Vargas, S. Kim, and A. Landy DNA looping generated by DNA bending protein IHF and the two domains of lambda integrase Science 244 1989 1457 1461
9. T. Ellenberger, and A. Landy A good turn for DNA: the structure of integration host factor bound to DNA Structure 5 1997 153 157
10. C.A. Robertson, and H.A. Nash Bending of the bacteriophage lambda attachment site by Escherichia coli integration host factor J Biol Chem 263 1988 3554 3557
11. S. Kim, L. Moitoso de Vargas, S.E. Nunes-Duby, and A. Landy Mapping of a higher order protein-DNA complex: two kinds of long-range interactions in lambda attL Cell 63 1990 773 781
12. J.F. Thompson, and A. Landy Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes Nucleic Acids Res 16 1988 9687 9705
13. T.E. Numrych, R.I. Gumport, and J.F. Gardner Characterization of the bacteriophage lambda excisionase (Xis) protein: the C-terminus is required for Xis-integrase cooperativity but not for DNA binding EMBO J 11 1992 3797 3806
14. Z. Wu, R.I. Gumport, and J.F. Gardner Defining the structural and functional roles of the carboxyl region of the bacteriophage lambda excisionase (Xis) protein J Mol Biol 281 1998 651 661
15. E.H. Cho, R.I. Gumport, and J.F. Gardner Interactions between integrase and excisionase in the phage lambda excisive nucleoprotein complex J Bacteriol 184 2002 5200 5203
16. M.A. Abbani, C.V. Papagiannis, M.D. Sam, D. Cascio, R.C. Johnson, and R.T. Clubb Structure of the cooperative Xis-DNA complex reveals a micronucleoprotein filament that regulates phage lambda intasome assembly Proc Natl Acad Sci USA 104 2007 2109 2114
17. M.D. Sam, C.V. Papagiannis, K.M. Connolly, L. Corselli, J. Iwahara, and J. Lee et al. Regulation of directionality in bacteriophage lambda site-specific recombination: structure of the Xis protein J Mol Biol 324 2002 791 805
18. M.H. Lee, and G.F. Hatfull Mycobacteriophage L5 integrase-mediated site-specific integration in vitro J Bacteriol 175 1993 6836 6841
19. C.E. Peña, M.H. Lee, M.L. Pedulla, and G.F. Hatfull Characterization of the mycobacteriophage L5 attachment site, attP J Mol Biol 266 1997 76 92
20. M.L. Pedulla, M.H. Lee, D.C. Lever, and G.F. Hatfull A novel host factor for integration of mycobacteriophage L5 Proc Natl Acad Sci USA 93 1996 15411 15416
21. C.E. Pena, J.M. Kahlenberg, and G.F. Hatfull Assembly and activation of site-specific recombination complexes Proc Natl Acad Sci USA 97 2000 7760 7765
22. J.A. Lewis, and G.F. Hatfull Identification and characterization of mycobacteriophage L5 excisionase Mol Microbiol 35 2000 350 360
23. J.A. Lewis, and G.F. Hatfull Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins Nucleic Acids Res 29 2001 2205 2216
24. J.A. Lewis, and G.F. Hatfull Control of directionality in L5 integrase-mediated site-specific recombination J Mol Biol 326 2003 805 821
25. G.F. Hatfull Complete genome sequences of 138 mycobacteriophages J Virol 86 2012 2382 2384
26. G.F. Hatfull, M.L. Pedulla, D. Jacobs-Sera, P.M. Cichon, A. Foley, and M.E. Ford et al. Exploring the mycobacteriophage metaproteome: phage genomics as an educational platform PLoS Genet 2 2006 e92
27. G.F. Hatfull The secret lives of mycobacteriophages Adv Virus Res 82 2012 179 288
28. C.E. Peña, J.E. Stoner, and G.F. Hatfull Positions of strand exchange in mycobacteriophage L5 integration and characterization of the attB site J Bacteriol 178 1996 5533 5536
29. G.F. Hatfull, D. Jacobs-Sera, J.G. Lawrence, W.H. Pope, D.A. Russell, and C.C. Ko et al. Comparative genomic analysis of 60 mycobacteriophage genomes: genome clustering, gene acquisition, and gene size J Mol Biol 397 2010 119 143
30. V.V. Rogov, C. Lucke, L. Muresanu, H. Wienk, I. Kleinhaus, and K. Werner et al. Solution structure and stability of the full-length excisionase from bacteriophage HK022 Eur J Biochem 270 2003 4846 4858
31. M. Abbani, M. Iwahara, and R.T. Clubb The structure of the excisionase (Xis) protein from conjugative transposon Tn916 provides insights into the regulation of heterobivalent tyrosine recombinases J Mol Biol 347 2005 11 25
32. M.D. Sam, D. Cascio, R.C. Johnson, and R.T. Clubb Crystal structure of the excisionase-DNA complex from bacteriophage lambda J Mol Biol 338 2004 229 240
33. C. Zwieb, and S. Adhya Plasmid vectors for the analysis of protein-induced DNA bending Methods Mol Biol 543 2009 547 562
34. L. Elantak, M. Ansaldi, F. Guerlesquin, V. Mejean, and X. Morelli Structural and genetic analyses reveal a key role in prophage excision for the TorI response regulator inhibitor J Biol Chem 280 2005 36802 36808
35. P.A. Rice, S. Yang, K. Mizuuchi, and H.A. Nash Crystal structure of an IHF-DNA complex: a protein-induced DNA U-turn Cell 87 1996 1295 1306
36. C.A. Ball, and R.C. Johnson Efficient excision of phage lambda from the Escherichia coli chromosome requires the Fis protein J Bacteriol 173 1991 4027 4031
37. C.A. Ball, and R.C. Johnson Multiple effects of Fis on integration and the control of lysogeny in phage lambda J Bacteriol 173 1991 4032 4038
38. M.H. Lee, L. Pascopella, W.R. Jacobs, and G.F. Hatfull Site-specific integration of mycobacteriophage L5: integration-proficient vectors for Mycobacterium smegmatis, Mycobacterium tuberculosis, and bacille Calmette-Guerin Proc Natl Acad Sci USA 88 1991 3111 3115
39. F.W. Studier Protein production by auto-induction in high density shaking cultures Protein Expression Purif 41 2005 207 234
40. Z. Otwinowski, and W. Minor Processing of X-ray diffraction data collected in oscillation mode Methods Enzymol 276 1997 307 326
41. P.D. Adams, P.V. Afonine, G. Bunkoczi, V.B. Chen, I.W. Davis, and N. Echols et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr Sect D Biol Crystallogr 66 2010 213 221
42. I.W. Davis, A. Leaver-Fay, V.B. Chen, J.N. Block, G.J. Kapral, and X. Wang et al. MolProbity: all-atom contacts and structure validation for proteins and nucleic acids Nucleic Acids Res 35 2007 W375 W383
43. J. Kim, C. Zwieb, C. Wu, and S. Adhya Bending of DNA by gene-regulatory proteins: construction and use of a DNA bending vector Gene 85 1989 15 23