Transfer of R388 derivatives by a pathogenesis-associated type IV secretion system into both bacteria and human cells

Journal of Bacteriology

Volumn 193, Issue 22, 2011, Pages 6257-6265

  Fernández González, Esther ^a   de Paz, Héctor D ^a   Alperi, Anabel ^a   Agúndez, Leticia ^a   Faustmann, Marco ^b   Sangari, Félix J ^a   Dehio, Christoph ^b   Llosa, Matxalen ^a  

^a UNIVERSITY OF CANTABRIA   (Spain)

^b UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; PROTEIN TRWB; PROTEIN TRWC; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; BARTONELLA HENSELAE; DNA TRANSFER; ENDOTHELIUM CELL; HUMAN; HUMAN CELL; NONHUMAN; PLASMID; PLASMID R388; PRIORITY JOURNAL; TYPE IV SECRETION SYSTEM;

ANGIOMATOSIS, BACILLARY; BACTERIAL PROTEINS; BACTERIAL SECRETION SYSTEMS; BARTONELLA HENSELAE; CELL LINE; CONJUGATION, GENETIC; ENDOTHELIAL CELLS; ESCHERICHIA COLI; HUMANS; PLASMIDS; TRANSFECTION;

ANIMALIA; BACTERIA (MICROORGANISMS); BARTONELLA HENSELAE; ESCHERICHIA COLI;

EID: 80655146184     PISSN: 00219193     EISSN: 10985530     Source Type: Journal    
DOI: 10.1128/JB.05905-11     Document Type: Article

References (46)

1. Agúndez, L., et al. 2011. Nuclear targeting of a bacterial integrase which mediates site-specific recombination between bacterial and human target sequences. Appl. Environ. Microbiol. 77:201-210.
2. Alvarez-Martínez, C. E., and P. J. Christie. 2009. Biological diversity of prokaryotic type IV secretion systems. Microbiol. Mol. Biol. Rev. 73:775-808.
3. 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.
4. Buchanan-Wollaston, V., J. E. Passiatore, and F. Cannon. 1987. The mob and oriT mobilization functions of a bacterial plasmid promote its transfer to plants. Nature 328:172-175.
5. Cabezón, E., J. I. Sastre, and F. de la Cruz. 1997. Genetic evidence of a coupling role for the TraG protein family in bacterial conjugation. Mol. Gen. Genet. 254:400-406.
6. Cambronne, E. D., and C. R. Roy. 2006. Recognition and delivery of effector proteins into eukaryotic cells by bacterial secretion systems. Traffic 7:929-939.
7. Cascales, E., and P. J. Christie. 2004. Agrobacterium VirB10, an ATP energy sensor required for type IV secretion. Proc. Natl. Acad. Sci. U. S. A. 101: 17228-17233.
8. César, C. E., C. Machón, F. de la Cruz, and M. Llosa. 2006. A new domain of conjugative relaxase TrwC responsible for efficient oriT-specific recombination on minimal target sequences. Mol. Microbiol. 62:984-996.
9. Dehio, C. 2008. Infection-associated type IV secretion systems of Bartonella and their diverse roles in host cell interaction. Cell. Microbiol. 10:1591-1598.
10. de Paz, H. D., et al. 2010. Functional dissection of the conjugative coupling protein TrwB. J. Bacteriol. 192:2655-2669.
11. de Paz, H. D., et al. 2005. Functional interactions between type IV secretion systems involved in DNA transfer and virulence. Microbiology 151:3505-3516.
12. Draper, O., C. E. César, C. Machón, F. de la Cruz, and M. Llosa. 2005. Site-specific recombinase and integrase activities of a conjugative relaxase in recipient cells. Proc. Natl. Acad. Sci. U. S. A. 102:16385-16390.
13. Grandoso, G., et al. 2000. Two active-site tyrosyl residues of protein TrwC act sequentially at the origin of transfer during plasmid R388 conjugation. J. Mol. Biol. 295:1163-1172.
14. Grandoso, G., M. Llosa, J. C. Zabala, and F. de la Cruz. 1994. Purification and biochemical characterization of TrwC, the helicase involved in plasmid R388 conjugal DNA transfer. Eur. J. Biochem. 226:403-412.
15. Grant, S. G., J. Jessee, F. R. Bloom, and D. Hanahan. 1990. Differential plasmid rescue from transgenic mouse DNAs into Escherichia coli methylation-restriction mutants. Proc. Natl. Acad. Sci. U. S. A. 87:4645-4649.
16. Hamilton, C. M., et al. 2000. TraG from RP4 and TraG and VirD4 from Ti plasmids confer relaxosome specificity to the conjugal transfer system of pTiC58. J. Bacteriol. 182:1541-1548.
17. Heinemann, J. A., and G. F. Sprague, Jr. 1989. Bacterial conjugative plasmids mobilize DNA transfer between bacteria and yeast. Nature 340:205-209.
18. Jurik, A., et al. 2010. The coupling protein Cagbeta and its interaction partner CagZ are required for type IV secretion of the Helicobacter pylori CagA protein. Infect. Immun. 78:5244-5251.
19. Karimova, G., N. Dautin, and D. Ladant. 2005. Interaction network among Escherichia coli membrane proteins involved in cell division as revealed by bacterial two-hybrid analysis. J. Bacteriol. 187:2233-2243.
20. Karimova, G., J. Pidoux, A. Ullmann, and D. Ladant. 1998. A bacterial two-hybrid system based on a reconstituted signal transduction pathway. Proc. Natl. Acad. Sci. U. S. A. 95:5752-5756.
21. Karimova, G., A. Ullmann, and D. Ladant. 2001. Protein-protein interaction between Bacillus stearothermophilus tyrosyl-tRNA synthetase subdomains revealed by a bacterial two-hybrid system. J. Mol. Microbiol. Biotechnol. 3:73-82.
22. Lee, E. C., et al. 2001. A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73:56-65.
23. Llosa, M., S. Bolland, G. Grandoso, and F. de la Cruz. 1994. Conjugationindependent, site-specific recombination at the oriT of the IncW plasmid R388 mediated by TrwC. J. Bacteriol. 176:3210-3217. (Erratum, 176:6414.)
24. Llosa, M., F.-X. Gomis-Rüth, M. Coll, and F. de la Cruz. 2002. Bacterial conjugation: a two-step mechanism for DNA transport. Mol. Microbiol. 45:1-8.
25. Llosa, M., C. Roy, and C. Dehio. 2009. Bacterial type IV secretion systems in human disease. Mol. Microbiol. 73:141-151.
26. Llosa, M., S. Zunzunegui, and F. de la Cruz. 2003. Conjugative coupling proteins interact with cognate and heterologous VirB10-like proteins while exhibiting specificity for cognate relaxosomes. Proc. Natl. Acad. Sci. U. S. A. 100:10465-10470.
27. Luo, Z. Q., and R. R. Isberg. 2004. Multiple substrates of the Legionella pneumophila Dot/Icm system identified by interbacterial protein transfer. Proc. Natl. Acad. Sci. U. S. A. 101:841-846.
28. Martínez, E., and F. de la Cruz. 1988. Transposon Tn21 encodes a RecAindependent site-specific integration system. Mol. Gen. Genet. 211:320-325.
29. Moncalián, G., et al. 1999. Characterization of ATP and DNA binding activities of TrwB, the coupling protein essential in plasmid R388 conjugation. J. Biol. Chem. 274:36117-36124.
30. Nagai, H., et al. 2005. A C-terminal translocation signal required for Dot/ Icm-dependent delivery of the Legionella RalF protein to host cells. Proc. Natl. Acad. Sci. U. S. A. 102:826-831.
31. Quebatte, M., et al. 2010. The BatR/BatS two-component regulatory system controls the adaptive response of Bartonella henselae during human endothelial cell infection. J. Bacteriol. 192:3352-3367.
32. Sadler, J. R., M. Tecklenburg, and J. L. Betz. 1980. Plasmids containing many tandem copies of a synthetic lactose operator. Gene 8:279-300.
33. Saenz, H. L., et al. 2007. Genomic analysis of Bartonella identifies type IV secretion systems as host adaptability factors. Nat. Genet. 39:1469-1476.
34. Salgado-Pabon, W., S. Jain, N. Turner, C. van der Does, and J. P. Dillard. 2007. A novel relaxase homologue is involved in chromosomal DNA processing for type IV secretion in Neisseria gonorrhoeae. Mol. Microbiol. 66: 930-947.
35. Sambrook, J., and D. W. Russell. 2001. Molecular cloning: a laboratory manual, 3rd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
36. Schmid, M. C., et al. 2004. The VirB type IV secretion system of Bartonella henselae mediates invasion, proinflammatory activation and antiapoptotic protection of endothelial cells. Mol. Microbiol. 52:81-92.
37. Schröder, G., et al. 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.
38. Schröder, G., R. Schülein, M. Quebatte, and C. Dehio. 2011. Conjugative DNA transfer into human cells by the VirB/VirD4 type IV secretion system of the bacterial pathogen Bartonella henselae. Proc. Natl. Acad. Sci. U. S. A. 108:14643-14648.
39. Schulein, R., and C. Dehio. 2002. The VirB/VirD4 type IV secretion system of Bartonella is essential for establishing intraerythrocytic infection. Mol. Microbiol. 46:1053-1067.
40. Schulein, R., et al. 2005. A bipartite signal mediates the transfer of type IV secretion substrates of Bartonella henselae into human cells. Proc. Natl. Acad. Sci. U. S. A. 102:856-861.
41. Seubert, A., R. Hiestand, F. de la Cruz, and C. Dehio. 2003. A bacterial conjugation machinery recruited for pathogenesis. Mol. Microbiol. 49:1253-1266.
42. Truttmann, M. C., T. A. Rhomberg, and C. Dehio. 2011. Combined action of the type IV secretion effector proteins BepC and BepF promotes invasome formation of Bartonella henselae on endothelial and epithelial cells. Cell. Microbiol. 13:284-299.
43. Vayssier-Taussat, M., et al. 2010. The Trw type IV secretion system of Bartonella mediates host-specific adhesion to erythrocytes. PLoS Pathog. 6:e1000946.
44. Vergunst, A. C., et al. 2005. Positive charge is an important feature of the C-terminal transport signal of the VirB/D4-translocated proteins of Agrobacterium. Proc. Natl. Acad. Sci. U. S. A. 102:832-837.
45. Voth, D. E., et al. 2009. The Coxiella burnetii ankyrin repeat domain-containing protein family is heterogeneous, with C-terminal truncations that influence Dot/Icm-mediated secretion. J. Bacteriol. 191:4232-4242.
46. Waters, V. L. 2001. Conjugation between bacterial and mammalian cells. Nat. Genet. 29:375-376.