The λ integrase site-specific recombination pathway

Mobile DNA III

Volumn , Issue , 2015, Pages 91-118

  Landy, Arthur ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Hexapeptide inhibitors; Holliday junction intermediates; Int tetramer complex; Integration host factor; Recombination reactions; Recombinogenic complexes; Single molecule kinetics; Int CTD; integrase site specific recombination pathway

Indexed keywords

EID: 84975116584     PISSN: None     EISSN: None     Source Type: Book    
DOI: 10.1128/9781555819217.ch4     Document Type: Chapter

References (181)

1. Campbell AM. 1962. Episomes, p 101-145. In Caspari EW, Thoday JM (ed), Advances in Genetics. Academic Press, New York, NY.
2. Nash HA. 1974. Purification of bactriophage λ Int protein. Nature 247:543-545.
3. Nash HA, Robertson CA. 1981. Purification and properties of the Escherichia coli protein factor required for λ integrative recombination. J Biol Chem 256:9246-9253.
4. Rice PA, Yang SW, Mizuuchi K, Nash HA. 1996. Crystal structure of an IHF-DNA complex: a proteininduced DNA U-turn. Cell 87:1295-1306.
5. Kostrewa D, Granzin J, Koch C, Choe HW, Labahn J, Kahmann R, Saenger W. 1991. Three-dimensional structure of the E. coli DNA-binding protein FIS. Nature 349:178-180.
6. Yuan HS, Finkel SE, Feng JA, Kaczor-Grzeskowiak M, Johnson RC, Dickerson RE. 1991. 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 88:9558-9562.
7. Stella S, Cascio D, Johnson RC. 2010. The shape of the DNA minor groove directs binding by the DNAbending protein Fis. Genes Dev 24:814-826.
8. Papagiannis CV, Sam MD, Abbani MA, Yoo D, Cascio D, Clubb RT, Johnson RC. 2007. Fis Targets Assembly of the Xis Nucleoprotein Filament to Promote Excisive Recombination by Phage Lambda. J Mol Biol 367: 328-343.
9. Rudy C, Taylor KL, Hinerfeld D, Scott JR, Churchward G. 1997. Excision of a conjugative transposon in vitro by the Int and Xis proteins of Tn 916. Nucleic Acids Res 25:4061-4066.
10. Hickman AB, Waninger S, Scocca JJ, Dyda F. 1997. Molecular organization in site-specific recombination: The catalytic domain of bacteriophage HP1 integrase at 2.7 Å resolution. Cell 89:227-237.
11. Lewis JA, Hatfull GF. 2003. Control of directionality in L5 integrase-mediated site-specific recombination. J Mol Biol 326:805-821.
12. Garcia-Russell N, Orchard SS, Segall AM. 2007. Probing nucleoid structure in bacteria using phage lambda integrase-mediated chromosome rearrangements, p 209-226. In Kelly TH, Stanley RM (ed), Methods Enzymol, vol 421. Academic Press, New York, NY.
13. Van Houdt R, Leplae R, Lima-Mendez G, Mergeay M, Toussiant A. 2012. Towards a more accurate annotation of tyrosine-based site-specific recombinases in bacterial genomes. Mobile DNA 3:6.
14. Warren D, Laxmikanthan G, Landy A. 2013. Integrase family of site-specific recombinases. Brenner's Encyclopedia of Genetics 4:100-105.
15. Van Duyne GD. 2008. Site-specific recombinases, p 303-332. In Protein-Nucleic Acid Interactions: Structural Biology. The Royal Society of Chemistry, Cambridge.
16. 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.
17. Segall AM, Craig NL. 2006. New wrinkles and folds in site-specific recombination. Mol Cell 19:433-435.
18. Grindley ND, Whiteson KL, Rice PA. 2006. Mechanisms of site-specific recombination. Annu Rev Biochem 75:567-605.
19. Rice PA. 2005. Resolving integral questions in sitespecific recombination. Nat Struct Mol Biol 12: 641-643.
20. Lee L, Sadowski PD. 2005. Strand selection by the tyrosine recombinases. Prog Nucl Acid Res Mol Biol 80: 1-42.
21. Williams KP. 2002. Integration sites for genetic elements in prokaryotic tRNA and tmRNA genes: sublocation preference of integrase subfamilies. Nucleic Acids Res 30:866-875.
22. Van Duyne GD. 2002. A structural view of tyrosine recombinase site-specific recombination, p 93-117. In Craig NL, Craigie R, Gellert M, Lambowitz AM (ed), Mobile DNA II. ASM Press, Washington DC.
23. She Q, Brügger K, Chen L. 2002. Archaeal integrative genetic elements and their impact on genome evolution. Res Microbiol 153:325-332.
24. Dutton G. 2002. Site-specific recombinases. The Scientist 16:29-31.
25. 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.
26. Kobryn K, Chaconas G. 2001. The circle is broken: telomere resolution in linear replicons. Curr Opin Microbiol 4:558-564.
27. Azaro MA, Landy A. 2002. λ Int and the λ Int family, p 118-148. In Craig NL, Craigie R, Gellert M, Lambowitz AM (ed), Mobile DNA II. ASM Press, Washington DC.
28. Rutkai E, Gyorgy A, Dorgai L, Weisberg RA. 2006. Role of secondary attachment sites in changing the specificity of site-specific recombination. J Bact 188: 3409-3411.
29. Landy A. 1989. Dynamic, structural and regulatory aspects of lambda site-specific recombination. Annu Rev Biochem 58:913-949.
30. Reese TA, Wakeman BS, Choi HS, Hufford MM, Huang SC, Zhang X, Buck MD, Jezewski A, Kambal A, Liu CY, Goel G, Murray PJ, Xavier RJ, Kaplan MH, Renne R, Speck SH, Artyomov MN, Pearce EJ, Virgin HW. 2014. Helminth infection reactivates latent γ-herpesvirus via cytokine competition at a viral promoter. Science 345:573-577.
31. Hsu PL, Landy A. 1984. Resolution of synthetic att-site Holliday structures by the integrase protein of bacteriophage λ. Nature 311:721-726.
32. Kitts PA, Nash HA. 1988. An intermediate in the phage λ site-specific recombination reaction is revealed by phosphorothioate substitution in DNA. Nucleic Acids Res 16:6839-6856.
33. Kitts PA, Nash HA. 1988. Bacteriophage λ site-specific recombination proceeds with a defined order of strandexchanges. J Mol Biol 204:95-107.
34. Mumm JP, Landy A, Gelles J. 2006. Viewing single lambda site-specific recombination events from start to finish. EMBO J 25:4586-4595.
35. Nunes-Düby S, Matsumoto L, Landy A. 1987. Sitespecific recombination intermediates trapped with suicide substrates. Cell 50:779-788.
36. Tong W, Warren D, Seah N, Laxmikanthan G, Van Duyne GD, Landy A. 2014. Mapping the Int bridges in the nucleoprotein Holliday junction intermediates of viral integrative and excisive recombination. Proc Natl Acad Sci USA 111:12366-12371.
37. Seah N, Tong W, Warren D, Van Duyne GD, Landy A. 2014. Nucleoprotein architectures regulating the directionality of viral integration and excision. Proc Natl Acad Sci USA 111:12372-12377.
38. Matovina M, Seah N, Hamilton T, Warren D, Landy A. 2010. Stoichiometric incorporation of base substitutions at specific sites in supercoiled DNA and supercoiled recombination intermediates. Nucleic Acids Res 38:e175.
39. Sun KQ. 1990. A study of DNA-DNA interactions during bacteriophage lambda integrative recombination. Ph.D. Doctoral Thesis in Biochemistry. University of Illinois at Urbana-Champaign, Champaign, IL.
40. Conway AB, Chen Y, Rice PA. 2003. Structural plasticity of the Flp-Holliday junction complex. J Mol Biol 326:425-434.
41. Chen Y, Narendra U, Iype LE, Cox MM, Rice PA. 2000. Crystal structure of a Flp recombinase-Holliday junction complex: assembly of an active oligomer by helix swapping. Mol Cell 6:885-897.
42. Gopaul DN, Guo F, Van Duyne GD. 1998. Structure of the Holliday junction intermediate in Cre-loxP sitespecific recombination. EMBO J 17:4175-4187.
43. Guo F, Gopaul DN, Van Duyne GD. 1997. Structure of Cre recombinase complexed with DNA in a site-specific recombination synapse. Nature 389:40-46.
44. Biswas T, Aihara H, Radman-Livaja M, Filman D, Landy A, Ellenberger T. 2005. A structural basis for allosteric control of DNA recombination by λ integrase. Nature 435:1059-1066.
45. Aihara H, Kwon HJ, Nunes-Düby SE, Landy A, Ellenberger T. 2003. A conformational switch controls the DNA cleavage activity of Lambda integrase. Mol Cell 12:187-198.
46. Tirumalai RS, Pargellis CA, Landy A. 1996. Identification and characterization of the NEM-sensitive site in lambda integrase. J Biol Chem 271:29599-29604.
47. Pargellis CA, Nunes-Düby SE, Moitoso de Vargas L, Landy A. 1988. Suicide recombination substrates yield covalent λ integrase-DNA complexes and lead to identification of the active site tyrosine. J Biol Chem 263: 7678-7685.
48. Tirumalai RS, Healey E, Landy A. 1997. The catalytic domain of λ site-specific recombinase. Proc Natl Acad Sci USA 94:6104-6109.
49. Sarkar D, Radman-Livaja M, Landy A. 2001. The small DNA binding domain of λ Int is a context-sensitive modulator of recombinase functions. EMBO J 20: 1203-1212.
50. Lee SY, Aihara H, Ellenberger T, Landy A. 2004. Two structural features of integrase that are critical for DNA cleavage by multimers but not by monomers. Proc Natl Acad Sci USA 101:2770-2775.
51. Cassell GD, Segall AM. 2003. Mechanism of inhibition of site-specific recombination by the Holliday junctiontrapping peptide WKHYNY: Insights into phage λ integrase-mediated strand exchnage. J Mol Biol 327: 413-429.
52. Cassell G, Klemm M, Pinilla C, Segall A. 2000. Dissection of bacteriophage λ site-specific recombination using synthetic peptide combinatorial libraries. J Mol Biol 299:1193-1202.
53. Boldt JL, Pinilla C, Segall AM. 2004. Reversible inhibitors of λ Int-mediated recombination efficiently trap Holliday junction intermediates and form the basis of a novel assay for junction resolution. J Biol Chem 279: 3472-3483.
54. Ghosh K, Lau CK, Guo F, Segall AM, Van Duyne GD. 2005. Peptide Trapping of the Holliday Junction Intermediate in Cre-loxP Site-specific Recombination. J Biol Chem 280:8290-8299.
55. Segall AM, Nash HA. 1996. Architectural flexibility in lambda site-specific recombination: three alternate conformations channel the att L site into three distinct pathways. Genes Cells 1:453-463.
56. Segall AM, Goodman SD, Nash HA. 1994. Architectural elements in nucleoprotein complexes:interchangeability of specific and non-specific DNA binding proteins. EMBO J 13:4536-4548.
57. Boldt JL, Kepple KV, Cassell GD, Segall AM. 2006. Spermidine biases the resolution of Holliday junctions by phage λ integrase. Nucl Acids Res 35:716-727.
58. Rajeev L, Segall A, Gardner J. 2007. The bacteroides NBU1 integrase performs a homology-independent strand exchange to form a Holliday junction intermediate. J Biol Chem 282:31228-31237.
59. Klemm M, Cheng C, Cassell G, Shuman S, Segall AM. 2000. Peptide inhibitors of DNA cleavage by tyrosine recombinases and topoisomerases. J Mol Biol 299: 1203-1216.
60. Gunderson CW, Boldt JL, Authement RN, Segall AM. 2009. Peptide wrwycr Inhibits the Excision of Several Prophages and Traps Holliday Junctions inside Bacteria. J Bacteriol 191:2169-2176.
61. Ranjit DK, Rideout MC, Nefzi A, Ostresh JM, Pinilla C, Segall AM. 2010. Small molecule functional analogs of peptides that inhibit λ site-specific recombination and bind Holliday junctions. Bioorg Med Chem Lett 20: 4531-4534.
62. Bankhead TM, Etzel BJ, Wolven F, Bordenave S, Boldt JL, Larsen TA, Segall AM. 2003. Mutations at residues 282, 286, and 293 of phage λ integrase exert pathwayspecific effects on synapsis and catalysis in recombination. J Bacteriol 185:2653-2666.
63. Chen Y, Rice PA. 2003. New insight into site-specific recombination from Flp recombinase-DNA structures. Annu Rev Biophys Biomol Struct 32:135-139.
64. Tal A, Arbel-Goren R, Costantino N, Court DL, Stavans J. 2014. Location of the unique integration site on an Escherichia coli chromosome by bacteriophage lambda DNA in vivo. Proc Natl Acad Sci USA 111: 7308-7312.
65. Kwon HJ, Tirumalai RS, Landy A, Ellenberger T. 1997. Flexibility in DNA recombination: structure of the λ integrase catalytic core. Science 276:126-131.
66. Sarkar D, Azaro MA, Aihara H, Papagiannis C, Tirumalai RS, Nunes-Düby SE, Johnson RC, Ellenberger T, Landy A. 2002. Differential affinity and cooperativity functions of the amino-terminal 70 residues of λ integrase. J Mol Biol 324:775-789.
67. Azaro MA, Landy A. 1997. The isomeric preference of Holliday junctions influences resolution bias by λ integrase. EMBO J 16:3744-3755.
68. Kamadurai HB, Jain R, Foster MP. 2008. Crystallization and structure determination of the corebinding domain of bacteriophage lambda integrase. Acta Crystallogr Sect F Struct Biol Cryst Commun 64: 470-473.
69. Kovach MJ, Tirumalai RS, Landy A. 2002. Site-specific photo-crosslinking of lambda Int. J Biol Chem 277: 14530-14538.
70. Tirumalai RS, Kwon H, Cardente E, Ellenberger T, Landy A. 1998. The recognition of core-type DNA sites by λ Integrase. J Mol Biol 279:513-527.
71. Ross W, Landy A. 1983. Patterns of λ Int recognition in the regions of strand exchange. Cell 33:261-272.
72. Cheng Q, Swalla BM, Beck M, Alcaraz R Jr, Gumport RI, Gardner JF. 2000. Specificity determinants for bacteriophage Hong Kong 022 integrase: analysis of mutants with relaxed core-binding specificities. Mol Microbiol 36:424-436.
73. Dorgai L, Yagil E, Weisberg RA. 1995. Identifying determinants of recombination specificity: Construction and characterization of mutant bacteriophage integrases. J Mol Biol 252:178-188.
74. Yagil E, Dorgai L, Weisberg R. 1995. Identifying determinants of recombination specificity: Construction and characterization of chimeric bacteriophage integrases. J Mol Biol 252:163-177.
75. Patsey RL, Bruist MF. 1995. Characterization of the interaction between the lambda intasome and att B. J Mol Biol 252:47-58.
76. Lange-Gustafson BJ, Nash HA. 1984. Purification and properties of Int-H, a variant protein involved in sitespecific recombination of bacteriophage λ. J Biol Chem 259:12724-12732.
77. Han YW, Gumport RI, Gardner JF. 1994. Mapping the functional domains of bacteriophage lambda integrase protein. J Mol Biol 235:908-925.
78. Tekle M, Warren DJ, Biswas T, Ellenberger T, Landy A, Nunes-Düby SE. 2002. Attenuating functions of the C-terminus of λ Integrase. J Mol Biol 324:649-665.
79. Kazmierczak RA, Swalla BM, Burgin AB, Gumport RI, Gardner JF. 2002. Regulation of site-specific recombination by the carboxyl terminus of λ integrase. Nucleic Acids Res 30:5193-5204.
80. Hazelbaker D, Radman-Livaja M, Landy A. 2005. Receipt of the C-terminal tail from a neighboring Int protomer allosterically stimulates Holliday junction resolution. J Mol Biol 351:948-955.
81. Rowley PA, Kachroo AH, Ma C-H, Maciaszek AD, Guga P, Jayaram M. 2010. Electrostatic suppression allows tyrosine site-specific recombination in the absence of a conserved catalytic arginine. J Biol Chem 285:22976-22985.
82. Grainge I, Jayaram M. 1999. The integrase family of recombinases: organization and function of the active site. Mol Microbiol 33:449-456.
83. Krogh BO, Shuman S. 2000. Catalytic mechanism of DNA topoisomerase IB. Mol Cell 5:1035-1041.
84. Krogh BO, Shuman S. 2002. Proton relay mechanism of general acid catalysis by DNA topoisomerase IB. J Biol Chem 277:5711-5714.
85. Yakovleva L, Lai J, Kool ET, Shuman S. 2006. Nonpolar nucleobase analogs illuminate requirements for site-specific DNA cleavage by vaccinia topoisomerase. J Biol Chem 281:35914-35921.
86. Van Duyne GD. 2001. A structural view of Cre-loxP site-specific recombination. Annu Rev Biophys Biomol Struct 30:87-104.
87. Chen Y, Rice PA. 2003. The role of the conserved Trp 330 in Flp-mediated recombination. Functional and structural analysis. J Biol Chem 278:24800-24807.
88. Whiteson KL, Rice PA. 2008. Binding and catalytic contributions to site recognition by flp recombinase. J Biol Chem 283:11414-11423.
89. Warren D, Laxmikanthan G, Landy A. 2008. A chimeric Cre recombinase with regulated directionality. Proc Natl Acad Sci USA 47:18278-18283.
90. Hartung M, Kisters-Woike B. 1998. Cre mutants with altered DNA binding properties. J Biol Chem 273: 22884-22891.
91. Richet E, Abcarian P, Nash HA. 1988. Synapsis of attachment sites during lambda integrative recombination involves capture of a naked DNA by a protein-DNA complex. Cell 52:9-17.
92. Wojciak JM, Sarkar D, Landy A, Clubb RT. 2002. Arm-site binding by the lambda integrase protein: solution structure and functional characterization of its amino-terminal domain. Proc Natl Acad Sci USA 99: 3434-3439.
93. Thompson JF, Landy A. 1988. Empirical estimation of protein-induced DNA bending angles: Applications to λ site-specific recombination complexes. Nucleic Acids Res 16:9687-9705.
94. Enquist LW, Kikuchi A, Weisberg RA. 1979. The role of λ integrase in integration and excision. Cold Spring Harb Symp Quant Biol 43:1115-1120.
95. Fadeev EA, Sam MD, Clubb RT. 2009. NMR structure of the amino-terminal domain of the lambda integrase protein in complex with DNA: immobilization of a flexible tail facilitates beta-sheet recognition of the major groove. J Mol Biol 388:682-690.
96. Wojciak JM, Connolly KM, Clubb RT. 1999. NMR structure of the Tn 916 integrase-DNA complex. Nat Struct Biol 6:366-373.
97. Allen MD, Yamasaki K, Ohme-Takagi M, Tateno M, Suzuki M. 1998. A novel mode of DNA recognition by a beta-sheet revealed by the solution structure of the GCC-box binding domain in complex with DNA. EMBO J 17:5484-5496.
98. Subramanya HS, Arciszewska LK, Baker RA, Bird LE, Sherratt DJ, Wigley DB. 1997. Crystal structure of the site-specific recombinase, XerD. EMBO J 16:5178-5187.
99. Nunes-Düby SE, Yu D, Landy A. 1997. Sensing homology at the strand swapping step in λ excisive recombination. J Mol Biol 272:493-508.
100. Lee SY, Radman-Livaja M, Warren D, Aihara H, Ellenberger T, Landy A. 2005. Non-equivalent interactions between amino-terminal domains of neighboring λ integrase protomers direct Holliday junction resolution. J Mol Biol 345:475-485.
101. Radman-Livaja M, Biswas T, Mierke D, Landy A. 2005. Architecture of recombination intermediates visualized by In-gel FRET of λ integrase-Holliday junctionarm-DNA complexes. Proc Natl Acad Sci USA 102: 3913-3920.
102. Miller HI, Kikuchi A, Nash HA, Weisberg RA, Friedman DI. 1979. Site-specific recombination of bacteriophage λ: the role of host gene products. Cold Spring Harb Symp Quant Biol 43:1121-1126.
103. Miller HI, Kirk M, Echols H. 1981. SOS induction and autoregulation of the him A gene for site-specific recombination in Escherichia coli. Proc Natl Acad Sci USA 78:6754-6758.
104. Moitoso de Vargas L, Kim S, Landy A. 1989. DNA looping generated by the DNA-bending protein IHF and the two domains of lambda integrase. Science 244: 1457-1461.
105. Sze CC, Laurie AD, Shingler V. 2001. In vivo and in vitro effects of integration host factor at the DmpRregulated σ 54 -dependent Po promoter. J Bacteriol 183: 2842-2851.
106. Ryan VT, Grimwade JE, Camara JE, Crooke E, Leonard AC. 2004. Escherichia coli prereplication complex assembly is regulated by dynamic interplay among Fis, IHF and DnaA. Mol Microbiol 51:1347-1359.
107. Crellin P, Sewitz S, Chalmers R. 2004. DNA looping and catalysis: The IHF-folded Arm of Tn 10 promotes conformational changes and hairpin resolution. Mol Cell 13:537-547.
108. Morse BK, Michalczyk R, Kosturko LD. 1994. Multiple molecules of integration host factor (IHF) at a single DNA binding site, the bacteriophage lambda cos 11 site. Biochimie 76:1005-1017.
109. Friedman DI. 1988. Integration host factor: a protein for all reasons. Cell 55:545-554.
110. Goosen N, van de Putte P. 1995. The regulation of transcription initiation by integration host factor. Mol Microbiol 16:1-7.
111. Nash HA, Lin ECC, Lynch AS. 1996. The HU and IHF proteins: accessory factors for complex protein-DNA assemblies. In Lin ECC, Lynch AS (ed), Regulation of Gene Expression in Escherichia coli, p. 150-179. R.G. Landes Company, Austin, TX.
112. Johnson RC, Johnson LM, Schmidt JW, Gardner JF, Higgins NP. 2005. Major nucleoid proteins in the structure and function of the Escherichia coli chromosome, p 65-132. In The Bacterial Chromosome. ASM Press, Washington DC.
113. Dame RT. 2005. The role of nucleoid-associated proteins in the organization and compaction of bacterial chromatin. Mol Microbiol 56:858-870.
114. Swinger KK, Rice PA. 2004. IHF and HU: flexible architects of bent DNA. Curr Opin Struct Biol 14: 28-35.
115. Travers A. 1997. DNA-protein interactions: IHF-the master blender. Curr Biol 7:R252-R254.
116. Rice PA. 1997. Making DNA do a U-turn: IHF and related proteins. Curr Opin Struct Biol 7:86-93.
117. Lynch TW, Read EK, Mattis AN, Gardner JF, Rice PA. 2003. Integration host factor: putting a twist on protein-DNA recognition. J Mol Biol 330:493-502.
118. Swinger KK, Lemberg KM, Zhang Y, Rice PA. 2003. Flexible DNA bending in HU-DNA cocrystal structures. EMBO J 22:3749-3760.
119. Vander Meulen KA, Saecker RM, Record MT Jr. 2008. Formation of a wrapped DNA-protein interface: experimental characterization and analysis of the large contributions of ions and water to the thermodynamics of binding IHF to H' DNA. J Mol Biol 377:9-27.
120. Dixit S, Singh-Zocchi M, Hanne J, Zocchi G. 2005. Mechanics of binding of a single integration-host-factor protein to DNA. Phy Rev Ltrs 94:118101-118104.
121. Sugimura S, Crothers DM. 2006. Stepwise binding and bending of DNA by Escherichia coli integration host factor. Proc Natl Acad Sci USA 103:18510-18514.
122. Kuznetsov SV, Sugimura S, Vivas P, Crothers DM, Ansarai A. 2006. Direct observation of DNA bending/ unbending kinetics in complex with DNA-bending protein IHF. Proc Natl Acad Sci USA 103:18515-18520.
123. Sugimura S. 2005. Kinetic and steady-state studies of binding and bending of Lambda phage DNA by integration host factor. Ph.D. Yale University, New Haven, CT.
124. Corona T, Bao Q, Christ N, Schwartz T, Li J, Droge P. 2003. Activation of site-specific DNA integration in human cells by a single chain integration host factor. Nucleic Acids Res 31:5140-5148.
125. Goodman SD, Nicholson SC, Nash HA. 1992. Deformation of DNA during site-specific recombination of bacteriophage λ: replacement of IHF protein by HU protein or sequence-directed bends. Proc Natl Acad Sci USA 89:11910-11914.
126. Goodman SD, Nash HA. 1989. Functional replacement of a protein-induced bend in a DNA recombination site. Nature 341:251-254.
127. Nunes-Düby SE, Smith-Mungo LI, Landy A. 1995. Single base-pair precision and structural rigidity in a small IHF-induced DNA loop. J Mol Biol 253:228-242.
128. Ditto MD, Roberts D, Weisberg RA. 1994. Growth phase variation of integration host factor level in Escherichia coli. J Bacteriol 176:3738-3748.
129. Murtin C, Engelhorn M, Geiselmann J, Boccard F. 1998. A quantitative UV laser footprinting analysis of the interaction of IHF with specific binding sites: Reevaluation of the effective concentration of IHF in the Cell. J Mol Biol 284:949-961.
130. Bushman W, Thompson JF, Vargas L, Landy A. 1985. Control of directionality in lambda site-specific recombination. Science 230:906-911.
131. Thompson JF, Moitoso de Vargas L, Skinner SE, Landy A. 1987. Protein-protein interactions in a higher-order structure direct lambda site-specific recombination. J Mol Biol 195:481-493.
132. Granston AE, Nash HA. 1993. Characterization of a set of integration host factor mutants deficient for DNA binding. J Mol Biol 234:45-59.
133. Nash HA, Robertson CA, Flamm E, Weisberg RA, Miller HI. 1987. Overproduction of Escherichia coli integration host factor, a protein with nonidentical subunits. J Bacteriol 169:4124-4127.
134. Aviv M, Giladi H, Schreiber G, Oppenheim AB, Glaser G. 1994. Expression of the genes coding for the Escherichia coli integration host factor are controlled by growth phase, rpoS, ppGpp and by autoregulation. Mol Microbiol 14:1021-1031.
135. Nystrom T. 1995. Glucose starvation stimulon of Escherichia coli: Role of integration host factor in starvation survival and growth phase-dependent protein synthesis. J Bacteriol 177:5707-5710.
136. Abremski K, Gottesman S. 1982. Purification of the bacteriophage λ xis gene product required for λ excisive recombination. J Biol Chem 257:9658-9662.
137. Nash HA. 1975. Integrative recombination of bacteriophage lambda DNA in vitro. Proc Natl Acad Sci USA 72:1072-1076.
138. Sam M, Papagiannis C, Connolly KM, Corselli L, Iwahara J, Lee J, Phillips M, Wojciak JM, Johnson RC, Clubb RT. 2002. Regulation of directionality in bacteriophage lambda site-specific recombination: structure of the Xis protein. J Mol Biol 324:791-805.
139. Sam MD, Cascio D, Johnson RC, Clubb RT. 2004. Crystal structure of the excisionase-DNA complex from bacteriophage lambda. J Mol Biol 338:229-240.
140. Abbani MA, Papagiannis CV, Sam MD, Cascio D, Johnson RC, Clubb RT. 2007. Structure of the cooperative excisionase (Xis)-DNA complex reveals a micronucleoprotein filament that regulates phage lambda intasome assembly. Proc Natl Acad Sci USA 104: 2109-2114.
141. Sun X, Mierke DF, Biswas T, Lee SY, Landy A, Radman-Livaja M. 2006. Architecture of the 99 bp DNA-Six-Protein regulatory complex of the λ att Site. Molecular Cell 24:569-580.
142. Thompson JF, Moitoso de Vargas L, Koch C, Kahmann R, Landy A. 1987. Cellular factors couple recombination with growth phase: characterization of a new component in the λ site-specific recombination pathway. Cell 50:901-908.
143. Finkel SE, Johnson RC. 1992. The FIS protein: it's not just for DNA inversion anymore. Mol Microbiol 6: 3257-3265.
144. Aiyar SE, McLeod SM, Ross W, Hirvonen CA, Thomas MS, Johnson RC, Gourse RL. 2002. Architecture of Fis-activated transcription complexes at the Escherichia coli rrnB P1 and rrnE P1 promoters. J Mol Biol 316: 501-516.
145. Hancock SP, Ghane T, Cascio D, Rohs R, Di Felice R, Johnson RC. 2013. Control of DNA minor groove width and Fis protein binding by the purine 2-amino group. Nucleic Acids Res 41:6750-6760.
146. Johnson RC, Bruist MF, Simon MI. 1986. Host protein requirements for in vitro site-specific DNA inversion. Cell 46:531-539.
147. Koch C, Kahmann R. 1986. Purification and properties of the Escherichia coli host factor required for inversion of the G segment in bacteriophage Mu. J Biol Chem 261:15673-15678.
148. Ball CA, Johnson RC. 1991. Efficient excision of phage λ from the Escherichia coli chromosome requires the Fis protein. J Bacteriol 173:4027-4031.
149. Numrych TE, Gumport RI, Gardner JF. 1991. A genetic analysis of Xis and FIS interactions with their binding sites in bacteriophage lambda. J Bacteriol 173:5954-5963.
150. Skoko D, Yoo D, Bai H, Schnurr B, Yan J, McLeod SM, Marko JF, Johnson RC. 2006. Mechanism of chromosome compaction and looping by the Escherichia coli nucleoid protein Fis. J Mol Biol 364:777-798.
151. Schneider R, Travers A, Kutateladze T, Muskhelishvili G. 1999. A DNA architectural protein couples cellular physiology and DNA topology in Escherichia coli. Mol Microbiol 34:953-964.
152. Dorman CJ. 2009. Nucleoid-associated proteins and bacterial physiology, p 47-64. In Laskin A, Sariaslani S, Geoffrey G (ed), Advances in Applied Microbiology, Vol 67. Academic Press, New York, NY.
153. Browning DF, Grainger DC, Busby SJW. 2010. Effects of nucleoid-associated proteins on bacterial chromosome structure and gene expression. Curr Opin Microbiol 13:773-780.
154. Ball CA, Osuna R, Ferguson KC, Johnson RC. 1992. Dramatic changes in Fis levels upon nutrient upshift in Escherichia coli. J Bacteriol 174:8043-8056.
155. Ninnemann O, Koch C, Kahmann R. 1992. The E. coli fis promoter is subject to stringent control and autoregulation. EMBO J 11:1075-1083.
156. Nilsson L, Verbeek H, Vijgenboom E, van Drunen C, Vanet A, Bosch L. 1992. FIS-dependent trans activation of stable RNA operons of Escherichia coli under various growth conditions. J Bacteriol 174:921-929.
157. Pratt TS, Steiner T, Feldman LS, Walker KA, Osuna R. 1997. Deletion analysis of the fis promoter region in Escherichia coli: Antagonistic effects of integration host factor and Fis. J Bacteriol 179:6367-6377.
158. Mallik P, Paul BJ, Rutherford ST, Gourse RL, Osuna R. 2006. DksA is required for growth phase-dependent regulation, growth rate-dependent control, and stringent control of fis expression in Escherichia coli. J Bacteriol 188:5775-5782.
159. Paul BJ, Ross W, Gaal T, Gourse RL. 2004. rRNA transcription in Escherichia coli. Annu Rev Genet 38: 749-770.
160. Walker KA, Mallik P, Pratt TS, Osuna R. 2004. The Escherichia coli fis promoter is regulated by changes in the levels of its transcription initiation nucleotide CTP. J Biol Chem 279:50818-50828.
161. Cassell G, Moision R, Rabani E, Segall A. 1999. The geometry of a synaptic intermediate in a pathway of bacteriophage λ site-specific recombination. Nucleic Acids Res 27:1145-1151.
162. Segall AM. 1998. Analysis of higher order intermediates and synapsis in the bent-L pathway of bacteriophage λ site-specific recombination. J Biol Chem 273:24258-24265.
163. Segall AM, Nash HA. 1993. Synaptic intermediates in bacteriophage lambda site-specific recombination: Integrase can align pairs of attachment sites. EMBO J 12:4567-4576.
164. Hazelbaker D, Azaro MA, Landy A. 2008. A biotin interference assay highlights two different asymmetric interaction profiles for lambda integrase arm-type binding sites in integrative versus excisive recombination. J Biol Chem 283:12402-12414.
165. Huang H, Harrison SC, Verdine GL. 2000. Trapping of a catalytic HIV reverse transcriptase template:primer complex through a disulfide bond. Chem Biol 7: 355-364.
166. Verdine GL, Norman DP. 2003. Covalent trapping of protein-DNA complexes. Annu Rev Biochem 72: 337-366.
167. Lorenz M, Diekmann S. 2001. Quantitative distance information on protein-DNA complexes determined in polyacrylamide gels by fluorescence resonance energy transfer. Electrophoresis 22:990-998.
168. Ramirez-Carrozzi VR, Kerppola TK. 2001. Long-range electrostatic interactions influence the orientation of Fos-Jun Binding at AP-1 sites. J Mol Biol 305:411-427.
169. Lilley DMJ, Wilson TJ. 2000. Fluorescence resonance energy transfer as a structural tool for nucleic acids. Curr Opin Chem Biol 4:507-517.
170. Crisona NJ, Weinberg RL, Peter BJ, Sumners DW, Cozzarelli NR. 1999. The topological mechanism of phage λ integrase. J Mol Biol 289:747-775.
171. Pollock TJ, Nash HA. 1983. Knotting of DNA caused by a genetic rearrangement: evidence for a nucleosomelike structure in site-specific recombination for bacteriophage lambda. J Mol Biol 170:1-18.
172. Nash HA, Pollock TJ. 1983. Site-specific recombination of bacteriophage lambda: The change in topological linking number associated with exchange of DNA strands. J Mol Biol 170:19-38.
173. Gottesman S, Gottesman M. 1975. Excision of prophage λ in a cell-free system. Proc Natl Acad Sci USA 72:2188-2192.
174. Numrych TE, Gumport RI, Gardner JF. 1992. 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: 3797-3806.
175. Craig NL, Craigie R, Gellert M, Lambowitz AM. 2002. Mobile DNA II. ASM Press, Washington DC.
176. King JK. 2007. Man the misinterpretant: will he discover the universal secret of sexuality encoded within him? Int J Humanit 4:1-19.
177. Craig NL, Nash HA. 1984. E. coli integration host factor binds to specific sites in DNA. Cell 39:707-716.
178. Nunes-Düby S, Azaro M, Landy A. 1995. Swapping DNA strands and sensing homology without branch migration in λ site-specific recombination. Curr Biol 5: 139-148.
179. Warren D, Sam M, Manley K, Sarkar D, Lee SY, Abbani M, Clubb RT, Landy A. 2003. Identification of the λ integrase surface that interacts with the Xis accessory protein reveals a residue that is also critical for homomeric dimer formation. Proc Natl Acad Sci USA 100:8176-8181.
180. Esposito D, Gerard GF. 2003. The Escherichia coli Fis protein stimulates bacteriophage λ integrative recombination in vitro. J. Bacteriol 185:3076-3080.
181. Ball CA, Johnson RC. 1991. Multiple effects of Fis on integration and the control of lysogeny in phage λ. J Bacteriol 173:4032-4038.