TraG-like proteins of type IV secretion systems: Functional dissection of the multiple activities of TraG (RP4) and TrwB (R388)

Journal of Bacteriology

Volumn 185, Issue 15, 2003, Pages 4371-4381

  Schröder, Gunnar ^a   Lanka, Erich ^a  

^a MAX PLANCK INSTITUTE FOR MOLECULAR GENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DNA; HYDROLASE; MAGNESIUM; MONOMER; NUCLEOSIDE TRIPHOSPHATASE; NUCLEOTIDE; OLIGOMER; PROTEIN; SINGLE STRANDED DNA; TRAG LIKE PROTEIN; TRWB PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BINDING SITE; CELL MEMBRANE; DNA BINDING; ENERGY; ENZYME ACTIVITY; NUCLEOTIDE SEQUENCE; PLASMID; POINT MUTATION; PRIORITY JOURNAL; SECRETION; SURFACE PLASMON RESONANCE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; BINDING, COMPETITIVE; CONJUGATION, GENETIC; DNA; DNA, SINGLE-STRANDED; DNA-BINDING PROTEINS; ESCHERICHIA COLI PROTEINS; GENE DELETION; MAGNESIUM; MEMBRANE PROTEINS; NUCLEOTIDES; POINT MUTATION; SURFACE PLASMON RESONANCE;

EID: 0037767570     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.185.15.4371-4381.2003     Document Type: Article

References (47)

1. Achtman, M., P. A. Manning, C. Edelbluth, and P. Herrlich. 1979. Export without proteolytic processing of inner and outer membrane proteins encoded by F sex factor tra cistrons in Escherichia coli minicells. Proc. Natl. Acad. Sci. USA 76:4837-4841.
2. Balzer, D., W. Pansegrau, and E. Lanka. 1994. Essential motifs of relaxase (TraI) and TraG proteins involved in conjugative transfer of plasmid RP4. J. Bacteriol. 176:4285-4295.
3. Balzer, D., G. Ziegelin, W. Pansegrau, V. Kruft, and E. Lanka. 1992. KorB protein of promiscuous plasmid RP4 recognizes inverted sequence repetitions in regions essential for conjugative plasmid transfer. Nucleic Acids Res. 20:1851-1858.
4. Bolland, S., M. Llosa, P. Avila, and F. de la Cruz. 1990. General organization of the conjugal transfer genes of the IncW plasmid R388 and interactions between R388 and IncN and IncP plasmids. J. Bacteriol. 172:5795-5802.
5. Boyer, H. W., and D. Roulland-Dussoix. 1969. A complementation analysis of the restriction and modification of DNA in Escherichia coli. J. Mol. Biol. 41:459-472.
6. 50) of an enzymatic reaction. Biochem. Pharmacol. 22:3099-3108.
7. Christie, P. J. 1997. Agrobacterium tumefaciens T-complex transport apparatus: a paradigm for a new family of multifunctional transporters in eubacteria. J. Bacteriol. 179:3085-3094.
8. Christie, P. J. 2001. Type IV secretion: intercellular transfer of macromolecules by systems ancestrally related to conjugation machines. Mol. Microbiol. 40:294-305.
9. Covarrubias, L., and F. Bolivar. 1982. Construction and characterization of new cloning vehicles. VI. Plasmid pBR329, a new derivative of pBR328 lacking the 482-base-pair inverted duplication. Gene 17:79-89.
10. Disqué-Kochem, C., and B. Dreiseikelmann. 1997. The cytoplasmic DNA-binding protein TraM binds to the inner membrane protein TraD in vitro. J. Bacteriol. 179:6133-6137.
11. Fürste, J. P., W. Pansegrau, G. Ziegelin, M. Kröger, and E. Lanka. 1989. Conjugative transfer of promiscuous IncP plasmids: interaction of plasmid-encoded products with the transfer origin. Proc. Natl. Acad. Sci. USA 86:1771-1775.
12. Gomis-Rüth, F. X., G. Moncalián, F. de la Cruz, and M. Coll. 2002. Conjugative plasmid protein TrwB, an integral membrane type IV secretion system coupling protein. Detailed structural features and mapping of the active site cleft. J. Biol. Chem. 277:7556-7566.
13. Gomis-Rüth, F. X., G. Moncalián, R. Perez-Luque, A. Gonzalez, E. Cabezón, F. de la Cruz, and M. Coll. 2001. The bacterial conjugation protein TrwB resembles ring helicases and F1-ATPase. Nature 409:637-641.
14. Hiratsuka, T. 1976. Fluorescence properties of 2′ (or 3′)-O-(2,4,6-trinitrophenyl)adenosine 5′-triphosphate and its use in the study of binding to heavy meromyosin ATPase. Biochim. Biophys. Acta 453:293-297.
15. Hiratsuka, T. 1982. Biological activities and spectroscopic properties of chromophoric and fluorescent analogs of adenine nucleosides and nucleotides, 2′,3′-O-(2,4,6-trinitrocyclohexadienylidene)adenosine derivatives. Biochim. Biophys. Acta 719:509-517.
16. Hormaeche, I., I. Alkorta, F. Moro, J. M. Valpuesta, F. M. Goñi, and F. de la Cruz. 2002. Purification and properties of TrwB, a hexameric, ATP-binding integral membrane protein essential for R388 plasmid conjugation. J. Biol. Chem. 277:46456-46462.
17. Hulme, E. C., and N. J. M. Birdsall. 1992. Strategy and tactics in receptor-binding studies, p. 63-174. In E. C. Hulme (ed.), Receptor-ligand interactions, a practical approach. Oxford University Press, Inc., New York, N.Y.
18. Krause, S., M. Bárcena, W. Pansegrau, R. Lurz, J. M. Carazo, and E. Lanka. 2000. Sequence-related protein export NTPases encoded by the conjugative transfer region of RP4 and by the cag pathogenicity island of Helicobacter pylori share similar hexameric ring structures. Proc. Natl. Acad. Sci. USA 97:3067-3072.
19. Krause, S., W. Pansegrau, R. Lurz, F. de la Cruz, and E. Lanka. 2000. Enzymology of type IV macromolecule secretion systems: the conjugative transfer regions of plasmids RP4 and R388 and the cag pathogenicity island of Helicobacter pylori encode structurally and functionally related nucleoside triphosphate hydrolases. J. Bacteriol. 182:2761-2770.
20. +-ATPase. Biochem. Biophys. Res. Commun. 297:154.
21. Kyte, J., and R. F. Doolittle. 1982. A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 157:105-132.
22. Lee, M. H., N. Kosuk, J. Bailey, B. Traxler, and C. Manoil. 1999. Analysis of F factor TraD membrane topology by use of gene fusions and trypsin-sensitive insertions. J. Bacteriol. 181:6108-6113.
23. Lessl, M., W. Pansegrau, and E. Lanka. 1992. Relationship of DNA-transfer-systems: essential transfer factors of plasmids RP4, Ti and F share common sequences. Nucleic Acids Res. 20:6099-6100.
24. Llosa, M., S. Bolland, and F. de la Cruz. 1994. Genetic organization of the conjugal DNA processing region of the IncW plasmid R388. J. Mol. Biol. 235:448-464.
25. Miller, J. H. 1972. Experiments in molecular genetics, p. 431-433. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, N.Y.
26. Moczydlowski, E. G., and P. A. Fortes. 1981. Characterization of 2′,3′-O-(2,4,6-trinitrocyclohexadienylidine)adenosine 5′-triphosphate as a fluorescent probe of the ATP site of sodium and potassium transport adenosine triphosphatase. Determination of nucleotide binding stoichiometry and ion-induced changes in affinity for ATP. J. Biol. Chem. 256:2346-2356.
27. Moncalián, G., E. Cabezón, I. Alkorta, M. Valle, F. Moro, J. M. Valpuesta, F. M. Goñi, and F. de la Cruz. 1999. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J. Biol. Chem. 274:36117-36124.
28. 2+-ATPase overexpressed in Escherichia coli. J. Biol. Chem. 269:11147-11154.
29. Panicker, M. M., and E. G. Minkley, Jr. 1992. Purification and properties of the F sex factor TraD protein, an inner membrane conjugal transfer protein. J. Biol. Chem. 267:12761-12766.
30. Pansegrau, W., D. Balzer, V. Kruft, R. Lurz, and E. Lanka. 1990. In vitro assembly of relaxosomes at the transfer origin of plasmid RP4. Proc. Natl. Acad. Sci. USA 87:6555-6559.
31. Pansegrau, W., E. Lanka, P. T. Barth, D. H. Figurski, D. G. Guiney, D. Haas, D. R. Helinski, H. Schwab, V. A. Stanisich, and C. M. Thomas. 1994. Complete nucleotide sequence of Birmingham IncP alpha plasmids. Compilation and comparative analysis. J. Mol. Biol. 239:623-663.
32. Pansegrau, W., G. Ziegelin, and E. Lanka. 1990. Covalent association of the traI gene product of plasmid RP4 with the 5′-terminal nucleotide at the relaxation nick site. J. Biol. Chem. 265:10637-10644.
33. Rabel, C., A. M. Grahn, R. Lurz, and E. Lanka. 2003. The VirB4 family of proposed traffic nucleoside triphosphatases: common motifs in plasmid RP4 TrbE are essential for conjugation and phage adsorption. J. Bacteriol. 185:1045-1058.
34. Rivas, S., S. Bolland, E. Cabezón, F. M. Goñi, and F. de la Cruz. 1997. TrwD, a protein encoded by the IncW plasmid R388, displays an ATP hydrolase activity essential for bacterial conjugation. J. Biol. Chem. 272:25583-25590.
35. Salmond, G. P. C. 1994. Secretion of extracellular virulence factors by plant pathogenic bacteria. Annu. Rev. Phytopathol. 32:181-200.
36. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, N.Y.
37. Savvides, S. N., H. J. Yeo, M. R. Beck, F. Blaesing, R. Lurz, E. Lanka, R. Buhrdorf, W. Fischer, R. Haas, and G. Waksman. 2003. VirB11 ATPases are dynamic hexameric assemblies: new insights into bacterial type IV secretion. EMBO J. 22:1969-1980.
38. Schröder, G., S. Krause, E. L. Zechner, B. Traxler, H. J. Yeo, R. Lurz, G. Waksman, and E. Lanka. 2002. TraG-like proteins of DNA transfer systems and of the Helicobacter pylori type IV secretion system: inner membrane gate for exported substrates? J. Bacteriol. 184:2767-2779.
39. Spiess, E., and R. Lurz. 2001. Electron microscopic analysis of nucleic acids and nucleic acid-protein complexes. Methods Microbiol. 20:293 -323.
40. Strack, B., M. Lessl, R. Calendar, and E. Lanka. 1992. A common sequence motif, -E-G-Y-A-T-A-, identified within the primase domains of plasmid-encoded I- and P-type DNA primases and the α protein of the Escherichia coli satellite phage P4. J. Biol. Chem. 267:13062-13072.
41. Vanoye, C. G., G. G. MacGregor, K. Dong, L. Tang, A. S. Buschmann, A. E. Hall, M. Lu, G. Giebisch, and S. C. Hebert. 2002. The carboxyl termini of K(ATP) channels bind nucleotides. J. Biol. Chem. 277:23260-23270.
42. Willetts, N., and B. M. Wilkins. 1984. Processing of plasmid DNA during bacterial conjugation. Microbiol. Rev. 48:24-41.
43. Winans, S. C., D. L. Burns, and P. J. Christie. 1996. Adaptation of a conjugal transfer system for the export of pathogenic macromolecules. Trends Microbiol. 4:64-68.
44. Yeo, H. J., S. N. Savvides, A. B. Herr, E. Lanka, and G. Waksman. 2000. Crystal structure of the hexameric traffic ATPase of the Helicobacter pylori type IV secretion system. Mol. Cell 6:1461-1472.
45. Zechner, E. L., F. de la Cruz, R. Eisenbrandt, A. M. Grahn, G. Koraimann, E. Lanka, G. Muth, W. Pansegrau, C. M. Thomas, B. M. Wilkins, and M. Zatyka. 2000. Conjugative DNA transfer processes, p. 87-173. Harwood Academic Publishers, Amsterdam, The Netherlands.
46. Ziegelin, G., W. Pansegrau, B. Strack, D. Balzer, M. Kröger, V. Kruft, and E. Lanka. 1991. Nucleotide sequence and organization of genes flanking the transfer origin of promiscuous plasmid RP4. DNA Sequence 1:303-327.
47. Ziegelin, G., E. Scherzinger, R. Lurz, and E. Lanka. 1993. Phage P4 α protein is multifunctional with origin recognition, helicase and primase activities. EMBO J. 12:3703-3708.