Solution structure and small angle scattering analysis of TraI (381-569)

Proteins: Structure, Function and Bioinformatics

Volumn 80, Issue 9, 2012, Pages 2250-2261

  Wright, Nathan T ^a,c   Raththagala, Madushi ^a   Hemmis, Casey W ^a   Edwards, Sheldon ^a   Curtis, Joseph E ^b   Krueger, Susan ^b   Schildbach, Joel F ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b NATIONAL INSTITUTE OF STANDARDS AND TECHNOLOGY   (United States)

^c JAMES MADISON UNIVERSITY   (United States)

Author keywords

Bacterial conjugation; NMR solution structure; SANS; SAXS; SsDNA binding protein

Indexed keywords

CARRIER PROTEIN; HELICASE; RECD HELICASE; RECQ HELICASE; SINGLE STRANDED DNA; TRAI PROTEIN[381 569]; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; BETA SHEET; BINDING SITE; CARBOXY TERMINAL SEQUENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DNA BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; SEQUENCE HOMOLOGY;

BINDING SITES; DNA HELICASES; ESCHERICHIA COLI PROTEINS; MOLECULAR DYNAMICS SIMULATION; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; SCATTERING, SMALL ANGLE;

BACTERIA (MICROORGANISMS);

EID: 84864413827     PISSN: 08873585     EISSN: 10970134     Source Type: Journal    
DOI: 10.1002/prot.24114     Document Type: Article

References (62)

1. Ochman H, Lawrence JG, Groisman EA. Lateral gene transfer and the nature of bacterial innovation. Nature 2000; 405: 299-304.
2. Lanka E, Wilkins BM. DNA processing reactions in bacterial conjugation. Annu Rev Biochem 1995; 64: 141-169.
3. Llosa M, Gomis-Ruth FX, Coll M, de la Cruz Fd F. Bacterial conjugation: a two-step mechanism for DNA transport. Mol Microbiol 2002; 45: 1-8.
4. Tatum EL, Lederberg J. Gene recombination in the bacterium Escherichia coli. J Bacteriol 1947; 53: 673-684.
5. Barlow M. What antimicrobial resistance has taught us about horizontal gene transfer. Methods Mol Biol 2009; 532: 397-411.
6. Tenover FC. Mechanisms of antimicrobial resistance in bacteria. Am J Infect Control 2006; 34( 5 Suppl 1): S3-S10; discussion S64-S73.
7. Davies J. Inactivation of antibiotics and the dissemination of resistance genes. Science 1994; 264: 375-382.
8. Yoon YG, Koob MD. Transformation of isolated mammalian mitochondria by bacterial conjugation. Nucleic Acids Res 2005; 33: e139.
9. Yoon YG, Koob MD, Yoo YH. Re-engineering the mitochondrial genomes in mammalian cells. Anat Cell Biol 2010; 43: 97-109.
10. Kunik T, Tzfira T, Kapulnik Y, Gafni Y, Dingwall C, Citovsky V. Genetic transformation of HeLa cells by Agrobacterium. Proc Natl Acad Sci USA 2001; 98: 1871-1876.
11. Waters VL. Conjugation between bacterial and mammalian cells. Nat Genet 2001; 29: 375-376.
12. Rayamajhi N, Cha SB, Kang ML, Lee SI, Lee HS, Yoo HS. Inter- and intraspecies plasmid-mediated transfer of florfenicol resistance in Enterobacteriaceae isolates from swine. Appl Environ Microbiol 2009; 75: 5700-5703.
13. Wolska KI. Horizontal DNA transfer between bacteria in the environment. Acta Microbiol Pol 2003; 52: 233-243.
14. Frost LS, Ippen-Ihler K, Skurray RA. Analysis of the sequence and gene products of the transfer region of the F sex factor. Microbiol Rev 1994; 58: 162-210.
15. Lawley TD, Klimke WA, Gubbins MJ, Frost LS. F factor conjugation is a true type IV secretion system. FEMS Microbiol Lett 2003; 224: 1-15.
16. Williams SL, Schildbach JF. TraY and integration host factor oriT binding sites and F conjugal transfer: sequence variations, but not altered spacing, are tolerated. J Bacteriol 2007; 189: 3813-3823.
17. Matson SW, Morton BS. Escherichia coli DNA helicase I catalyzes a site- and strand-specific nicking reaction at the F plasmid oriT. J Biol Chem 1991; 266: 16232-16237.
18. Luo Y, Gao Q, Deonier RC. Mutational and physical analysis of F plasmid traY protein binding to oriT. Mol Microbiol 1994; 11: 459-469.
19. Nelson WC, Howard MT, Sherman JA, Matson SW. The traY gene product and integration host factor stimulate Escherichia coli DNA helicase I-catalyzed nicking at the F plasmid oriT. J Biol Chem 1995; 270: 28374-28380.
20. Street LM, Harley MJ, Stern JC, Larkin C, Williams SL, Miller DL, Dohm JA, Rodgers ME, Schildbach JF. Subdomain organization and catalytic residues of the F factor TraI relaxase domain. Biochim Biophys Acta 2003; 1646: 86-99.
21. Larkin C, Datta S, Harley MJ, Anderson BJ, Ebie A, Hargreaves V, Schildbach JF. Inter- and intramolecular determinants of the specificity of single-stranded DNA binding and cleavage by the F factor relaxase. Structure 2005; 13: 1533-1544.
22. Larkin C, Datta S, Nezami A, Dohm JA, Schildbach JF. Crystallization and preliminary X-ray characterization of the relaxase domain of F factor TraI. Acta Crystallogr D Biol Crystallogr 2003; 59 (Part 8): 1514-1516.
23. Larkin C, Haft RJ, Harley MJ, Traxler B, Schildbach JF. Roles of active site residues and the HUH motif of the F plasmid TraI relaxase. J Biol Chem 2007; 282: 33707-33713.
24. Lahue EE, Matson SW. Escherichia coli DNA helicase I catalyzes a unidirectional and highly processive unwinding reaction. J Biol Chem 1988; 263: 3208-3215.
25. Matson SW, Ragonese H. The F-plasmid TraI protein contains three functional domains required for conjugative DNA strand transfer. J Bacteriol 2005; 187: 697-706.
26. Haft RJ, Palacios G, Nguyen T, Mally M, Gachelet EG, Zechner EL, Traxler B. General mutagenesis of F plasmid TraI reveals its role in conjugative regulation. J Bacteriol 2006; 188: 6346-6353.
27. Byrd DR, Sampson JK, Ragonese HM, Matson SW. Structure-function analysis of Escherichia coli DNA helicase I reveals non-overlapping transesterase and helicase domains. J Biol Chem 2002; 277: 42645-42653.
28. Datta S, Larkin C, Schildbach JF. Structural insights into single-stranded DNA binding and cleavage by F factor TraI. Structure 2003; 11: 1369-1379.
29. Dostal L, Schildbach JF. Single-stranded DNA binding by F TraI relaxase and helicase domains is coordinately regulated. J Bacteriol 2010; 192: 3620-3628.
30. Wright NT, Majumdar A, Schildbach JF. Chemical shift assignments for F-plasmid TraI (381-569). Biomol NMR Assign 2010; 5: 67-70.
31. Lang S, Gruber K, Mihajlovic S, Arnold R, Gruber CJ, Steinlechner S, Jehl MA, Rattei T, Frohlich KU, Zechner EL. Molecular recognition determinants for type IV secretion of diverse families of conjugative relaxases. Mol Microbiol 2010; 78: 1539-1555.
32. Chandran V, Fronzes R, Duquerroy S, Cronin N, Navaza J, Waksman G. Structure of the outer membrane complex of a type IV secretion system. Nature 2009; 462: 1011-1015.
33. Dostal L, Shao S, Schildbach JF. Tracking F plasmid TraI relaxase processing reactions provides insight into F plasmid transfer. Nucleic Acids Res 2011; 39: 2658-2670.
34. 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: 554-568.
35. Bax A. Weak alignment offers new NMR opportunities to study protein structure and dynamics. Protein Sci 2003; 12: 1-16.
36. Wright NT, Margolis JW, Margolis FL, Weber DJ. Refinement of the solution structure of rat olfactory marker protein (OMP). J Biomol NMR 2005; 33: 63-68.
37. Laskowski RA, Moss DS, Thornton JM. Main-chain bond lengths and bond angles in protein structures. J Mol Biol 1993; 231: 1049-1067.
38. Kelley LA, Sternberg MJ. Protein structure prediction on the Web: a case study using the Phyre server. Nat Protoc 2009; 4: 363-371.
39. Dostal L, Schildbach JF. Single-stranded DNA binding by F TraI relaxase and helicase domains are coordinately regulated. J Bacteriol 2010; 192: 3620-3628.
40. Datta S, Larkin C, Schildbach JF. Structural insights into single-stranded DNA binding and cleavage by F factor TraI. Structure (Camb) 2003; 11: 1369-1379.
41. Svergun DI. Determination of the regularization parameter in indirect-transform methods using perceptual criteria. J Appl Crystallogr 1992; 25: 495-503.
42. Cheng Y, McNamara DE, Miley MJ, Nash RP, Redinbo MR. Functional characterization of the multi-domain F plasmid TraI relaxase-helicase. J Biol Chem 2011; 286: 12670-12682.
43. Singleton MR, Dillingham MS, Gaudier M, Kowalczykowski SC, Wigley DB. Crystal structure of RecBCD enzyme reveals a machine for processing DNA breaks. Nature 2004; 432: 187-193.
44. Manoil C, Traxler B. Insertion of in-frame sequence tags into proteins using transposons. Methods 2000; 20: 55-61.
45. Wright NT, Varney KM, Ellis KC, Markowitz J, Gitti RK, Zimmer DB, Weber DJ. The three-dimensional solution structure of Ca(2+)-bound S100A1 as determined by NMR spectroscopy. J Mol Biol 2005; 353: 410-426.
46. 13C-edited NOESY experiment. J Biomol NMR 1993; 3: 463-470.
47. Wright NT, Prosser BL, Varney KM, Zimmer DB, Schneider MF, Weber DJ. S100A1 and calmodulin compete for the same binding site on ryanodine receptor. J Biol Chem 2008; 283: 26676-26683.
48. Kelley TGaD. SPARKY 3. San Francisco: University of San Francisco; 2005.
49. Shen Y, Delaglio F, Cornilescu G, Bax A. TALOS+: a hybrid method for predicting protein backbone torsion angles from NMR chemical shifts. J Biomol NMR 2009; 44: 213-223.
50. Schwieters CD, Clore GM. The VMD-XPLOR visualization package for NMR structure refinement. J Magn Reson 2001; 149: 239-244.
51. Schwieters CD, Kuszewski JJ, Tjandra N, Clore GM. The Xplor-NIH NMR molecular structure determination package. J Magn Reson 2003; 160: 65-73.
52. Glinka CJ, Barker JG, Hammouda B, Krueger S, Moyer JJ, Orts WJ. The 30 m small-angle neutron scattering instruments at the National Institute of Standards and Technology. J Appl Crystallogr 1998; 31: 430-445.
53. Kline SR. Reduction and analysis of SANS and USANS data using IGOR Pro. J Appl Crystallogr 2006; 39: 895-900.
54. Guinier A, Fournet G. Small Angle Scattering of X-rays. New York: John Wiley and Sons; 1955.
55. Krueger S, Gorshkova I, Brown J, Hoskins J, McKenney KH, Schwarz FP. Determination of the conformations of cAMP receptor protein and its T127L, S128A mutant with and without cAMP from small angle neutron scattering measurements. J Biol Chem 1998; 273: 20001-20006.
56. Curtis JE, Raghunandan S, Nanda H, Krueger S. SASSIE: A program to study intrinsically disordered biological molecules and macromolecular ensembles using experimental scattering restraints. Comp Phys Comm 2012; 183: 382-389.
57. Humphrey W, Dalke A, Schulten K. VMD: visual molecular dynamics. J Mol Graph 1996; 14: 33-38, 27-38.
58. Stern JC, Schildbach JF. DNA recognition by F Factor TraI36: highly sequence-specific binding of single-stranded DNA. Biochemistry 2001; 40: 11586-11595.
59. Nielsen SS, Toft KN, Snakenborg D, Jeppesen MG, Jacobsen JK, Vestergaard B, Kutter JP, Arleth L. BioXTAS RAW, a software program for high-throughput automated small-angle X-ray scattering data reduction and preliminary analysis. J Appl Cryst 2009; 42: 959-964.
60. Svergun D, Barerato C, Koch MHJ. CRYSOL-a Program to evaluate X-ray solution scattering of biological macromolecules and atomic coordinates. J Appl Crystallogr 1995; 28: 768-773.
61. Wuthrich K. NMR of proteins and nucleic acids. New York: Wiley; 1986.
62. Wright NT, Majumdar A, Schildbach JF. Chemical shift assignments for F-plasmid TraI (381-569). Biomol NMR Assign 2010; 5: 67-70.