Fis Targets Assembly of the Xis Nucleoprotein Filament to Promote Excisive Recombination by Phage Lambda

Journal of Molecular Biology

Volumn 367, Issue 2, 2007, Pages 328-343

  Papagiannis, Christie V ^a   Sam, My D ^b   Abbani, Mohamad A ^b   Yoo, Daniel ^a   Cascio, Duilio ^b   Clubb, Robert T ^b,c   Johnson, Reid C ^a,c  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

DNA architectural proteins; DNA bending; nonspecific DNA binding; site specific DNA recombination; X ray crystallography

Indexed keywords

DNA; DNA BINDING PROTEIN; FACTOR FOR INVERSION STIMULATION; NUCLEOPROTEIN; UNCLASSIFIED DRUG; XIS PROTEIN;

ARTICLE; BACTERIOPHAGE LAMBDA; BINDING AFFINITY; BINDING SITE; CROSS LINKING; CRYSTAL STRUCTURE; DNA FOOTPRINTING; GENETIC RECOMBINATION; MICROFILAMENT; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROPHAGE; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DNA BINDING; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS; STEREOCHEMISTRY;

ENTEROBACTERIA PHAGE LAMBDA;

EID: 33847128325     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.12.071     Document Type: Article

References (53)

1. Azaro M., and Landy A. Lambda integrase and the lambda Int family. In: Craig N.L., Craigie R., Gellert M., and Lambowitz A.L. (Eds). Mobile DNA II (2002), ASM Press, Washington, DC 118-148
2. Landy A. Dynamic, structural, and regulatory aspects of lambda site-specific recombination. Annu. Rev. Biochem. 58 (1989) 913-949
3. Ball C.A., and Johnson R.C. Multiple effects of Fis on integration and the control of lysogeny in phage lambda. J. Bacteriol. 173 (1991) 4032-4038
4. Esposito D., and Gerard G.F. The Escherichia coli Fis protein stimulates bacteriophage lambda integrative recombination in vitro. J. Bacteriol. 185 (2003) 3076-3080
5. Guarneros G., and Echols H. New mutants of bacteriophage lambda with a specific defect in excision from the host chromosome. J. Mol. Biol. 47 (1970) 565-574
6. Ball C.A., and Johnson R.C. Efficient excision of phage lambda from the Escherichia coli chromosome requires the Fis protein. J. Bacteriol. 173 (1991) 4027-4031
7. Thompson J.F., Moitoso de Vargas L., Koch C., Kahmann R., and Landy A. Cellular factors couple recombination with growth phase: characterization of a new component in the lambda site-specific recombination pathway. Cell 50 (1987) 901-908
8. Abremski K., and Gottesman S. Purification of the bacteriophage lambda xis gene product required for lambda excisive recombination. J. Biol. Chem. 257 (1982) 9658-9662
9. Bushman W., Yin S., Thio L.L., and Landy A. Determinants of directionality in lambda site-specific recombination. Cell 39 (1984) 699-706
10. Yin S., Bushman W., and Landy A. Interaction of the lambda site-specific recombination protein Xis with attachment site DNA. Proc. Natl Acad. Sci. USA 82 (1985) 1040-1044
11. Sam M.D., Papagiannis C.V., Connolly K.M., Corselli L., Iwahara J., Lee J., et al. Regulation of directionality in bacteriophage lambda site-specific recombination: structure of the Xis protein. J. Mol. Biol. 324 (2002) 791-805
12. Thompson J.F., and Landy A. Empirical estimation of protein-induced DNA bending angles: applications to lambda site-specific recombination complexes. Nucl. Acids Res. 16 (1988) 9687-9705
13. Sam M.D., Cascio D., Johnson R.C., and Clubb R.T. Crystal structure of the excisionase-DNA complex from bacteriophage lambda. J. Mol. Biol. 338 (2004) 229-240
14. Rogov V.V., Lucke C., Muresanu L., Wienk H., Kleinhaus I., Werner K., et al. Solution structure and stability of the full-length excisionase from bacteriophage HK022. Eur. J. Biochem. 270 (2003) 4846-4858
15. Moitoso de Vargas L., and Landy A. A switch in the formation of alternative DNA loops modulates lambda site-specific recombination. Proc. Natl Acad. Sci. USA 88 (1991) 588-592
16. Abbani, M., Papagiannis, C. V., Sam, M. D., Cascio, D., Johnson, R. C., Clubb, R. T. (2007). Structure of the cooperative Xis-DNA complex reveals a micronucleoprotein filament that regulates phage lambda intasome assembly. Proc. Natl Acad. Sci. USA. In the press.
17. Numrych T.E., Gumport R.I., and Gardner J.F. 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
18. Wu Z., Gumport R.I., and Gardner J.F. Defining the structural and functional roles of the carboxyl region of the bacteriophage lambda excisionase (Xis) protein. J. Mol. Biol. 281 (1998) 651-661
19. Warren D., Sam M.D., Manley K., Sarkar D., Lee S.Y., Abbani M., et al. Identification of the lambda integrase surface that interacts with Xis reveals a residue that is also critical for Int dimer formation. Proc. Natl Acad. Sci. USA 100 (2003) 8176-8181
20. Sarkar D., Radman-Livaja M., and Landy A. The small DNA binding domain of lambda integrase is a context-sensitive modulator of recombinase functions. EMBO J. 20 (2001) 1203-1212
21. Sarkar D., Azaro M.A., Aihara H., Papagiannis C.V., Tirumalai R., Nunes-Duby S.E., et al. Differential affinity and cooperativity functions of the amino-terminal 70 residues of lambda integrase. J. Mol. Biol. 324 (2002) 775-789
22. Cho E.H., Gumport R.I., and Gardner J.F. Interactions between integrase and excisionase in the phage lambda excisive nucleoprotein complex. J. Bacteriol. 184 (2002) 5200-5203
23. Johnson R.C., Bruist M.F., and Simon M.I. Host protein requirements for in vitro site-specific DNA inversion. Cell 46 (1986) 531-539
24. Koch C., and Kahmann R. Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J. Biol. Chem. 261 (1986) 15673-15678
25. Johnson R.C., Johnson L.M., Schmidt J.W., and Gardner J.F. Major nucleoid proteins in the structure and function of the Escherichia coli chromosome. In: Higgins N.P. (Ed). The Bacterial Chromosome (2005), ASM Press, Washington, DC 65-132
26. Skoko D., Yoo D., Bai H., Schnurr B., Yan J., McLeod S.M., et al. Mechanism of chromosome compaction and looping by the E. coli nucleoid protein Fis. J. Mol. Biol. 364 (2006) 777-798
27. Kostrewa D., Granzin J., Koch C., Choe H.W., Raghunathan S., Wolf W., et al. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature 349 (1991) 178-180
28. Yuan H.S., Finkel S.E., Feng J.A., Kaczor-Grzeskowiak M., Johnson R.C., and Dickerson R.E. The molecular structure of wild-type and a mutant Fis protein: relationship between mutational changes and recombinational enhancer function or DNA binding. Proc. Natl Acad. Sci. USA 88 (1991) 9558-9562
29. Numrych T.E., Gumport R.I., and Gardner J.F. A genetic analysis of Xis and FIS interactions with their binding sites in bacteriophage lambda. J. Bacteriol. 173 (1991) 5954-5963
30. Sun X., Mierke D.F., Biswas T., Lee S.Y., Landy A., and Radman-Livaja M. Architecture of the 99 bp DNA-six-protein regulatory complex of the lambda att site. Mol. Cell 24 (2006) 569-580
31. Leffers Jr. G.G., and Gottesman S. Lambda Xis degradation in vivo by Lon and FtsH. J. Bacteriol. 180 (1998) 1573-1577
32. Merickel S.K., Sanders E.R., Vazquez-Ibar J.L., and Johnson R.C. Subunit exchange and the role of dimer flexibility in DNA binding by the Fis protein. Biochemistry 41 (2002) 5788-5798
33. Safo M.K., Yang W.Z., Corselli L., Cramton S.E., Yuan H.S., and Johnson R.C. The transactivation region of the Fis protein that controls site-specific DNA inversion contains extended mobile beta-hairpin arms. EMBO J. 16 (1997) 6860-6873
34. Osuna R., Finkel S.E., and Johnson R.C. Identification of two functional regions in Fis: the N-terminus is required to promote Hin-mediated DNA inversion but not lambda excision. EMBO J. 10 (1991) 1593-1603
35. Dixon W.J., Hayes J.J., Levin J.R., Weidner M.F., Dombroski B.A., and Tullius T.D. Hydroxyl radical footprinting. Methods Enzymol. 208 (1991) 380-413
36. Pan C.Q., Finkel S.E., Cramton S.E., Feng J.A., Sigman D.S., and Johnson R.C. Variable structures of Fis-DNA complexes determined by flanking DNA protein contacts. J. Mol. Biol. 264 (1996) 675-695
37. Cheng Y.S., Yang W.Z., Johnson R.C., and Yuan H.S. Structural analysis of the transcriptional activation on Fis: crystal structures of six Fis mutants with different activation properties. J. Mol. Biol. 302 (2000) 1139-1151
38. Perkins-Balding D., Dias D.P., and Glasgow A.C. Location, degree, and direction of DNA bending associated with the Hin recombinational enhancer sequence and Fis-enhancer complex. J. Bacteriol. 179 (1997) 4747-4753
39. Lewis J.A., and Hatfull G.F. Control of directionality in integrase-mediated recombination: examination of recombination directionality factors (RDFs) including Xis and Cox proteins. Nucl. Acids Res. 29 (2001) 2205-2216
40. Benoff B., Yang H., Lawson C.L., Parkinson G., Liu J., Blatter E., et al. Structural basis of transcription activation: the CAP-alpha CTD-DNA complex. Science 297 (2002) 1562-1566
41. Savery N.J., Lloyd G.S., Busby S.J., Thomas M.S., Ebright R.H., and Gourse R.L. Determinants of the C-terminal domain of the Escherichia coli RNA polymerase alpha subunit important for transcription at class I cyclic AMP receptor protein-dependent promoters. J. Bacteriol. 184 (2002) 2273-2280
42. Jain D., Nickels B.E., Sun L., Hochschild A., and Darst S.A. Structure of a ternary transcription activation complex. Mol. Cell 13 (2004) 45-53
43. S selectivity of the proP (P2) promoter in Escherichia coli. Mol. Microbiol. 63 (2007) 780-796
44. Thompson J.F., and Landy A. Regulation of bacteriophage lambda site-specific recombination. In: Berg D., and Howe M. (Eds). Mobile DNA (1989), ASM Press, Washington, DC 1-22
45. Ball C.A., Osuna R., Ferguson K.C., and Johnson R.C. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J. Bacteriol. 174 (1992) 8043-8056
46. Mallik P., Paul B.J., Rutherford S.T., Gourse R.L., and Osuna R. DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli. J. Bacteriol. 188 (2006) 5775-5782
47. Maxam A.M., and Gilbert W. Sequencing end-labeled DNA with base-specific chemical cleavages. Methods Enzymol. 65 (1980) 499-560
48. Abremski K., and Gottesman S. The form of the DNA substrate required for excisive recombination of bacteriophage lambda. J. Mol. Biol. 131 (1979) 637-649
49. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (1997) 307-326
50. Kissinger C.R., Gehlhaar D.K., and Fogel D.B. Rapid automated molecular replacement by evolutionary search. Acta Crystallog. sect. D 55 (1999) 484-491
51. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
52. Jones T.A., Zou J.Y., Cowan S.W., and Kjeldgaard. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallog. sect. A 47 (1991) 110-119
53. Biswas T., Aihara H., Radman-Livaja M., Filman D., Landy A., and Ellenberger T. A structural basis for allosteric control of DNA recombination by lambda integrase. Nature 435 (2005) 1059-1066