Mechanistic basis of plasmid-specific DNA binding of the F plasmid regulatory protein, TraM

Journal of Molecular Biology

Volumn 426, Issue 22, 2014, Pages 3783-3795

  Peng, Yun ^a   Lu, Jun ^a   Wong, Joyce J W ^b   Edwards, Ross A ^a   Frost, Laura S ^a   Glover, J N Mark ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

plasmid conjugation; protein DNA interactions; ribbon helix helix; TraM; X ray crystallography

Indexed keywords

TOLL LIKE RECEPTOR ADAPTOR MOLECULE 2; BACTERIAL DNA; BACTERIAL PROTEIN; CARRIER PROTEIN; ESCHERICHIA COLI PROTEIN; F FACTOR; PROTEIN BINDING; SBMA PROTEIN, E COLI; TRAM PROTEIN, BACTERIAL;

AMINO ACID SEQUENCE; ARTICLE; BINDING AFFINITY; BINDING SITE; CRYSTAL STRUCTURE; DNA BINDING; DNA HELIX; NONHUMAN; PLASMID; CHEMICAL STRUCTURE; CHEMISTRY; ESCHERICHIA COLI; GEL MOBILITY SHIFT ASSAY; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BASE SEQUENCE; BINDING SITES; CRYSTALLOGRAPHY, X-RAY; DNA, BACTERIAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; F FACTOR; MEMBRANE TRANSPORT PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; SEQUENCE HOMOLOGY, AMINO ACID; SEQUENCE HOMOLOGY, NUCLEIC ACID;

EID: 84908178889     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2014.09.018     Document Type: Article

References (34)

1. Frost LS, Koraimann G. Regulation of bacterial conjugation: balancing opportunity with adversity. Future Microbiol 2010;5:1057-71.
2. Wong JJ, Lu J, Glover JN. Relaxosome function and conjugation regulation in F-like plasmids - a structural biology perspective. Mol Microbiol 2012;85:602-17.
3. Waksman G, Fronzes R. Molecular architecture of bacterial type IV secretion systems. Trends Biochem Sci 2010;35:691-8.
4. Penfold S, Simon J, Frost L. Regulation of the expression of the traM gene of the F sex factor of Escherichia coli. Mol Microbiol 1996;20:549-58.
5. Lu J, Fekete RA, Frost LS. A rapid screen for functional mutants of TraM, an autoregulatory protein required for F conjugation. Mol Genet Genomics 2003;269:227-33.
6. Lu J, Zhao W, Frost LS. Mutational analysis of TraM correlates oligomerization and DNA binding with autoregulation and conjugative DNA transfer. J Biol Chem 2004;279:55324-33.
7. Fu YH, Tsai MM, Luo YN, Deonier RC. Deletion analysis of the F plasmid oriT locus. J Bacteriol 1991;173:1012-20.
8. Beranek A, Zettl M, Lorenzoni K, Schauer A, Manhart M, Koraimann G. Thirty-eight C-terminal amino acids of the coupling protein TraD of the F-like conjugative resistance plasmid R1 are required and sufficient to confer binding to the substrate selector protein TraM. J Bacteriol 2004;186:6999-7006.
9. Disque-Kochem C, Dreiseikelmann B. The cytoplasmic DNA-binding protein TraM binds to the inner membrane protein TraD in vitro. J Bacteriol 1997;179:6133-7.
10. Lu J, Edwards RA, Wong JJ, Manchak J, Scott PG, Frost LS, et al. Protonation-mediated structural flexibility in the F conjugation regulatory protein, TraM.EMBOJ 2006;25:2930-9.
11. Lu J, Frost LS. Mutations in the C-terminal region of TraM provide evidence for in vivo TraM-TraD interactions during F-plasmid conjugation. J Bacteriol 2005;187:4767-73.
12. Lu J, Wong JJ, Edwards RA, Manchak J, Frost LS, Glover JN. Structural basis of specific TraD-TraM recognition during F plasmid-mediated bacterial conjugation. Mol Microbiol 2008;70:89-99.
13. Mihajlovic S, Lang S, Sut MV, Strohmaier H, Gruber CJ, Koraimann G, et al. Plasmid r1 conjugative DNA processing is regulated at the coupling protein interface. J Bacteriol 2009;191:6877-87.
14. Wong JJ, Lu J, Edwards RA, Frost LS, Glover JN. Structural basis of cooperative DNA recognition by the plasmid conjugation factor, TraM. Nucleic Acids Res 2011;39:6775-88.
15. Sut MV, Mihajlovic S, Lang S, Gruber CJ, Zechner EL. Protein and DNA effectors control the TraI conjugative helicase of plasmid R1. J Bacteriol 2009;191:6888-99.
16. Ragonese H, Haisch D, Villareal E, Choi JH, Matson SW. The F plasmid-encoded TraM protein stimulates relaxosome-mediated cleavage at oriT through an interaction with TraI. Mol Microbiol 2007;63:1173-84.
17. Guogas LM, Kennedy SA, Lee JH, Redinbo MR. A novel fold in the TraI relaxase-helicase C-terminal domain is essential for conjugative DNA transfer. J Mol Biol 2009;386:554-68.
18. Verdino P, Keller W, Strohmaier H, Bischof K, Lindner H, Koraimann G. The essential transfer protein TraM binds to DNA as a tetramer. J Biol Chem 1999;274:37421-8.
19. Miller DL, Schildbach JF. Evidence for a monomeric intermediate in the reversible unfolding of F factor TraM. J Biol Chem 2003;278:10400-7.
20. Fekete RA, Frost LS. Mobilization of chimeric oriT plasmids by F and R100-1: role of relaxosome formation in defining plasmid specificity. J Bacteriol 2000;182:4022-7.
21. Seeman NC, Rosenberg JM, Rich A. Sequence-specific recognition of double helical nucleic acids by proteins. Proc Natl Acad Sci USA 1976;73:804-8.
22. Luscombe NM, Laskowski RA, Thornton JM. Amino acidbase interactions: a three-dimensional analysis of protein-DNA interactions at an atomic level. Nucleic Acids Res 2001;29:2860-74.
23. Lamoureux JS, Maynes JT, Glover JN. Recognition of 5′-YpG-3′ sequences by coupled stacking/hydrogen bonding interactions with amino acid residues. J Mol Biol 2004;335:399-408.
24. Geist C, Brantl S. TraM protein of plasmid R1: in vitro selection of the target region reveals two consensus 7 bp binding motifs spaced by a 4 bp linker of defined sequence. Plasmid 2008;59:20-35.
25. Abo T, Inamoto S, Ohtsubo E. Specific DNA binding of the TraM protein to the oriT region of plasmid R100. J Bacteriol 1991;173:6347-54.
26. Fekete RA, Frost LS. Characterizing the DNA contacts and cooperative binding of F plasmid TraM to its cognate sites at oriT. J Biol Chem 2002;277:16705-11.
27. Hanahan D. Studies on transformation of Escherichia coli with plasmids. J Mol Biol 1983;166:557-80.
28. Lu J, den Dulk-Ras A, Hooykaas PJ, Glover JN. Agrobacterium tumefaciens VirC2 enhances T-DNA transfer and virulence through its C-terminal ribbon-helix-helix DNAbinding fold. Proc Natl Acad Sci USA 2009;106:9643-8.
29. Otwinowski L, Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol 1997;276:307-26.
30. McCoy AJ, Grosse-Kunstleve RW, Adams PD, Winn MD, Storoni LC, Read RJ. Phaser crystallographic software. J Appl Crystallogr 2007;40:658-74.
31. Terwilliger TC. Using prime-and-switch phasing to reduce model bias in molecular replacement. Acta Crystallogr Sect D Biol Crystallogr 2004;60:2144-9.
32. Emsley P, Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallogr Sect D Biol Crystallogr 2004;60:2126-32.
33. Adams PD, Afonine PV, Bunkoczi G, Chen VB, Davis IW, Echols N, et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr Sect D Biol Crystallogr 2010;66:213-21.
34. Morris RJ, Perrakis A, Lamzin VS. ARP/wARP and automatic interpretation of protein electron density maps. Methods Enzymol 2003;374:229-44.