The C-tail anchored TssL subunit, an essential protein of the enteroaggregative Escherichia coli Sci-1 Type VI secretion system, is inserted by YidC

MicrobiologyOpen

Volumn 1, Issue 1, 2012, Pages 71-82

  Aschtgen, Marie Stéphanie ^a   Zoued, Abdelrahim ^a   Lloubès, Roland ^a   Journet, Laure ^a   Cascales, Eric ^a  

^a AIX MARSEILLE UNIVERSITY   (France)

Author keywords

Hcp; Inner membrane; Insertion; Protein trafficking; Topology

Indexed keywords

BACTERIAL PROTEIN; HEAT SHOCK PROTEIN 70; PROTEIN TSSL; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BACTERIAL MEMBRANE; BACTERIAL STRAIN; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; ENTEROAGGREGATIVE ESCHERICHIA COLI; GENE INSERTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; TYPE VI SECRETION SYSTEM; YIDC GENE;

EID: 84859950847     PISSN: None     EISSN: 20458827     Source Type: Journal    
DOI: 10.1002/mbo3.9     Document Type: Article

References (58)

1. Aschtgen, M. S., C. S. Bernard, S. de Bentzmann, R. Lloubès, and E. Cascales. 2008. SciN is an outer membrane lipoprotein required for Type VI secretion in enteroaggregative Escherichia coli. J. Bacteriol. 190:7523-7531.
2. Aschtgen, M. S., M. Gavioli, A. Dessen, R. Lloubès, and E. Cascales. 2010a. The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol. Microbiol. 75:886-899.
3. Aschtgen, M. S., M. S. Thomas, and E. Cascales. 2010b. Anchoring the Type VI secretion system to the cell wall: TssL, TagL, TagP,... What else? Virulence 1:535-540.
4. Bernard, C. S., Y. R. Brunet, E. Gueguen, and E. Cascales. 2010. Nooks and crannies in Type VI secretion regulation. J. Bacteriol. 192:3850-3860.
5. Bingle, L. E., C. M. Bailey, and M. J. Pallen. 2008. Type VI secretion: a beginner's guide. Curr. Opin. Microbiol. 11:3-8.
6. Bogdanov, M., W. Zhang, J. Xie, and W. Dowhan. 2005. Transmembrane protein topology mapping by the substituted cysteine accessibility method (SCAM(TM)): application to lipid-specific membrane protein topogenesis. Methods 36:148-171.
7. Borgese, N., and M. Righi. 2010. Remote origins of tail-anchored proteins. Traffic 11:877-885.
8. Boyer, F., G. Fichant, J. Berthod, Y. Vandenbrouck, and I. Attree. 2009. Dissecting the bacterial type VI secretion system by a genome wide in silico analysis: what can be learned from available microbial genomic resources? BMC Genomics. 10:104.
9. Brunet, Y., C. S. Bernard, M. Gavioli, R. Lloubès, and E. Cascales. 2011. An epigenetic switch involving overlapping Fur and DNA methylation optimizes expression of a Type VI secretion gene cluster. PLoS Genet. 7:e1002205.
10. Bönemann, G., A. Pietrosiuk, A. Diemand, H. Zentgraf, and A. Mogk. 2009. Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J. 28:315-325.
11. Bönemann, G., A. Pietrosiuk, and A. Mogk. 2010. Tubules and donuts: a type VI secretion story. Mol. Microbiol. 76:815-821.
12. Cascales, E. 2008. The type VI secretion toolkit. EMBO Rep. 9:735-741.
13. Cascales and Cambillau. 2012. Structural biology of Type VI secretion systems. Philos. Trans. R. Soc. Lond. B. Biol. Sci. In press.
14. Dalbey, R. E., P. Wang, and A. Kuhn. 2011. Assembly of bacterial inner membrane proteins. Annu. Rev. Biochem. 80:161-187.
15. de Bruin, O. M., B. N. Duplantis, J. S. Ludu, R. F. Hare, E. B. Nix, C. L. Schmerk, C. S. Robb, A. B. Boraston, K. Hueffer, and F. E. Nano. 2011. The biochemical properties of the Francisella Pathogenicity Island (FPI)-encoded proteins, IglA, IglB, IglC, PdpB and DotU, suggest roles in type VI secretion. Microbiology 157:3470-3478.
16. Erez, E., G. Stjepanovic, A. M. Zelazny, B. Brugger, I. Sinning, and E. Bibi. 2010. Genetic evidence for functional interaction of the E. coli SRP-receptor with acidic lipids in vivo. J. Biol. Chem. 285:40508-40514.
17. Felisberto-Rodrigues, C., E. Durand, M. S. Aschtgen, S. Blangy, M. Ortiz-Lombardia, B. Douzi, C. Cambillau, and E. Cascales. 2011. Towards a structural comprehension of bacterial Type VI secretion systems: characterization of the TssJ-TssM complex of an Escherichia coli pathovar. PLoS Pathog. 7:e1002386.
18. Filip, C., G. Fletcher, J. L. Wulff, and C. F. Earhart. 1973. Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent Sodium-Lauryl-Sarcosinate. J. Bacteriol. 115:717-722.
19. Filloux, A., A. Hachani, and S. Bleves. 2008. The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154:1570-1583.
20. Fontaine, F., R. T. Fuchs, and G. Storz. 2011. Membrane localization of small proteins in Escherichia coli. J. Biol. Chem. 286:32464-32474.
21. Genevaux, P., F. Schwager, C. Georgopoulos, and W. L. Kelley. 2001. The djlA gene acts synergistically with dnaJ in promoting Escherichia coli growth. J. Bacteriol. 183:5747-5750.
22. Goemaere, E. L., A. Devert, R. Lloubès, and E. Cascales. 2007. Movements of the TolR C-terminal domain depend on TolQR ionizable key residues and regulate activity of the Tol complex. J. Biol. Chem. 282:17749-17757.
23. Hatzixanthis, K., T. Palmer, and F. Sargent. 2003. A subset of bacterial inner membrane proteins integrated by the twin-arginine translocase. Mol. Microbiol. 49:1377-1390.
24. Hood, R. D., P. Singh, F. Hsu, T. Güvener, M. A. Carl, R. R. Trinidad, J. M. Silverman, B. B. Ohlson, K. G. Hicks, R. L. Plemel, M. Li, S. Schwarz, W. Y. Wang, A. J. Merz, D. R. Goodlett, and J. D. Mougous. 2010. A Type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7:25-37.
25. Jakubowski, S. J., V. Krishnamoorthy, E. Cascales, and P. J. Christie. 2004. Agrobacterium tumefaciens VirB6 domains direct the ordered export of a DNA substrate through a type IV secretion system. J. Mol. Biol. 341:961-977.
26. Jani, A. J., and P. A. Cotter. 2010. Type VI secretion: not just for pathogenesis anymore. Cell Host Microbe. 8:2-6.
27. Jobichen, C., S. Chakraborty, M. Li, J. Zheng, L. Joseph, Y. K. Mok, K. Y. Leung, and J. Sivaraman. 2010. Structural basis for the secretion of EvpC: a key type VI secretion system protein from Edwardsiella tarda. PLoS One 5:e12910.
28. Kanamaru, S., P. G. Leiman, V. A. Kostyuchenko, P. R. Chipman, V. V. Mesyanzhinov, F. Arisaka, and M. G. Rossmann. 2002. Structure of the cell-puncturing device of bacteriophage T4. Nature 415:553-557.
29. Kang, P. J., and E. A. Craig. 1990. Identification and characterization of a new Escherichia coli gene that is a dosage-dependent suppressor of a dnaK deletion mutation. J. Bacteriol. 172:2055-2064.
30. Kol, S., N. Nouwen, and A. J. Driessen. 2008. Mechanisms of YidC-mediated insertion and assembly of multimeric membrane protein complexes. J. Biol. Chem. 283:31269-31273.
31. Kuhn, A. 2009. From the Sec complex to the membrane insertase YidC. Biol. Chem. 390:701-706.
32. Leiman, P. G., M. Basler, U. A. Ramagopal, J. B. Bonanno, J. M. Sauder, S. Pukatzki, S. K. Burley, S. C. Almo, and J. J. Mekalanos. 2009. Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc. Natl. Acad. Sci. U. S. A. 106:4154-4159.
33. Leung, K. Y., B. A. Siame, H. Snowball, and Y. K. Mok. 2011. Type VI secretion regulation: crosstalk and intracellular communication. Curr. Opin. Microbiol. 14:9-15.
34. Lossi, N. S., R. Dajani, P. Freemont, and A. Filloux. 2011. Structure-function analysis of HsiF, a gp25-like component of the type VI secretion system in Pseudomonas aeruginosa. Microbiology 157:3292-3305.
35. Ma, L. S., J. S. Lin, and E. M. Lai. 2009. An IcmF family protein, ImpLM, is an integral inner membrane protein interacting with ImpKL, and its walker a motif is required for type VI secretion system-mediated Hcp secretion in Agrobacterium tumefaciens. J. Bacteriol. 191:4316-4329.
36. Mougous, J. D., M. E. Cuff, S. Raunser, A. Shen, M. Zhou, C. A. Gifford, A. L. Goodman, G. Joachimiak, C. L. Ordoñez, S. Lory, et al. 2006. A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312:1526-1530.
37. Muller, M. M., A. Vianney, J. C. Lazzaroni, R. E. Webster, and R. Portalier. 1993. Membrane topology of the Escherichia coli TolR protein required for cell envelope integrity. J. Bacteriol. 175:6059-6061.
38. Nagai, H., and T. Kubori. 2011. Type IVB secretion systems of Legionella and other Gram-negative bacteria. Front Microbiol. 2:136.
39. Oliver, D. B., and J. Beckwith. 1981. E. coli mutant pleiotropically defective in the export of secreted proteins. Cell 25:765-772.
40. Pell, L. G., V. Kanelis, L. W. Donaldson, P. L. Howell, and A. R. Davidson. 2009. The phage lambda major tail protein structure reveals a common evolution for long-tailed phages and the type VI bacterial secretion system. Proc. Natl. Acad. Sci. U. S. A. 106:4160-4165.
41. Pietrosiuk, A., E. D. Lenherr, S. Falk, G. Bönemann, J. Kopp, H. Zentgraf, I. Sinning, and A. Mogk. 2011. Molecular basis for the unique role of the AAA+ chaperone ClpV in type VI protein secretion. J. Biol. Chem. 286:30010-30021.
42. Pukatzki, S., A. T. Ma, A. T. Revel, D. Sturtevant, and J. J. Mekalanos. 2007. Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc. Natl. Acad. Sci. U. S. A. 104:15508-15513.
43. Pukatzki, S., S. B. McAuley, and S. T. Miyata. 2009. The type VI secretion system: translocation of effectors and effector-domains. Curr. Opin. Microbiol. 12:11-17.
44. Russell, A. B., R. D. Hood, N. K. Bui, M. LeRoux, W. Vollmer, and J. D. Mougous. 2011. Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475:343-347.
45. Schwarz, S., R. D. Hood, and J. D. Mougous. 2010. What is type VI secretion doing in all those bugs? Trends Microbiol. 18:531-553.
46. Segal, G., M. Feldman, and T. Zusman. 2005. The Icm/Dot type-IV secretion systems of Legionella pneumophila and Coxiella burnetii. FEMS Microbiol. Rev. 29:65-81.
47. Sexton, J. A., J. L. Miller, A. Yoneda, T. E. Kehl-Fie, and J. P. Vogel. 2004. Legionella pneumophila DotU and IcmF are required for stability of the Dot/Icm complex. Infect. Immun. 72:5983-5992.
48. Shalom, G., J. G. Shaw, and M. S. Thomas. 2007. In vivo expression technology identifies a type VI secretion system locus in Burkholderia pseudomallei that is induced upon invasion of macrophages. Microbiology 153:2689-2699.
49. Ullers, R. S., D. Ang, F. Schwager, C. Georgopoulos, and P. Genevaux. 2007. Trigger factor can antagonize both SecB and DnaK/DnaJ chaperone functions in Escherichia coli. Proc. Natl. Acad. Sci. U. S. A. 104:3101-3106.
50. van den Ent, F., andJ. Löwe. 2006. RF cloning: a restriction-free method for inserting target genes into plasmids. J. Biochem. Biophys. Methods 67:67-74.
51. van der Laan, M., E. N. Houben, N. Nouwen, J. Luirink, and A. J. Driessen. 2001. Reconstitution of Sec-dependent membrane protein insertion: nascent FtsQinteracts with YidC in a SecYEG-dependent manner. EMBO Rep 2:519-523.
52. VanRheenen, S. M., G. Duménil, and R. R. Isberg. 2004. IcmF and DotU are required for optimal effector translocation and trafficking of the Legionella pneumophila vacuole. Infect. Immun. 72:5972-5982.
53. Wang, P., and R. E. Dalbey. 2011. Inserting membrane proteins: The YidC/Oxa1/Alb3 machinery in bacteria, mitochondria, and chloroplasts. Biochim. Biophys. Acta. 1808:866-875.
54. Wexler, M., F. Sargent, R. L. Jack, N. R. Stanley, E. G. Bogsch, C. Robinson, B. C. Berks, and T. Palmer. 2000. TatD is a cytoplasmic protein with DNase activity: no requirement for TatD family proteins in sec-independent protein export. J. Biol. Chem. 275:16717-16722.
55. Xie, K., and R. E. Dalbey. 2008. Inserting proteins into the bacterial cytoplasmic membrane using the Sec and YidC translocases. Nat. Rev. Microbiol. 6:234-244.
56. Zheng, J., and K. Y. Leung. 2007. Dissection of a type VI secretion system in Edwardsiella tarda. Mol. Microbiol. 66:1192-1206.
57. Zheng, J., B. Ho, and J. J. Mekalanos. 2011. Genetic analysis of anti-amoebae and anti-bacterial activities of the Type VI secretion system in Vibrio cholerae. PLoS One 6:e23876.
58. Zusman, T., M. Feldman, E. Halperin, and G. Segal. 2004. Characterization of the icmH and icmF genes required for Legionella pneumophila intracellular growth, genes that are present in many bacteria associated with eukaryotic cells. Infect. Immun. 72:3398-3409.