The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall

Molecular Microbiology

Volumn 75, Issue 4, 2010, Pages 886-899

  Aschtgen, Marie Stéphanie ^a   Gavioli, Marthe ^a   Dessen, Andrea ^b   Lloubès, Roland ^a   Cascales, Eric ^a  

^a CNRS   (France)

^b CNRS   (France)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; BINDING PROTEIN; GENE PRODUCT; MEMBRANE PROTEIN; PEPTIDOGLYCAN; PROTEIN SCIZ; UNCLASSIFIED DRUG; VIRULENCE FACTOR;

ARTICLE; BACTERIAL CELL WALL; BINDING ASSAY; BIOFILM; ENTEROAGGREGATIVE ESCHERICHIA COLI; FRACTIONATION; GRAM NEGATIVE BACTERIUM; IN VITRO STUDY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SECRETION; SUPERNATANT; TYPE IV SECRETION SYSTEM; VIRULENCE;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; BIOFILMS; BIOLOGICAL TRANSPORT; CELL WALL; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; HUMANS; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; PROTEIN BINDING; SEQUENCE ALIGNMENT; VIRULENCE FACTORS;

ANIMALIA; ESCHERICHIA COLI; NEGIBACTERIA;

EID: 76449118749     PISSN: 0950382X     EISSN: 13652958     Source Type: Journal    
DOI: 10.1111/j.1365-2958.2009.07028.x     Document Type: Article

References (53)

1. Arnold, K., Bordoli, L., Kopp, J. Schwede, T. (2006) The SWISS-MODEL workspace: a web-based environment for protein structure homology modelling. Bioinformatics 22 : 195 201.
2. Aschtgen, M.S., Bernard, C.S., De Bentzmann, S., Lloubès, R. Cascales, E. (2008) SciN is an outer membrane lipoprotein required for Type VI secretion in enteroaggregative Escherichia coli. J Bacteriol 190 : 7523 7531.
3. Aubert, D., Flannagan, R. Valvano, M.A. (2008) A novel sensor kinase-response regulator hybrid controls biofilm formation and type VI secretion system activity in Burkholderia cenocepacia. Infect Immun 76 : 1979 1991.
4. Bingle, L.E., Bailey, C.M. Pallen, M.J. (2008) Type VI secretion: a beginner's guide. Curr Opin Microbiol 11 : 3 8.
5. Bogdanov, M., Zhang, W., Xie, J. Dowhan, W. (2005) Transmembrane protein topology mapping by the substituted cysteine accessibility method (SCAM(TM)): application to lipid-specific membrane protein topogenesis. Methods 36 : 148 171.
6. Bönemann, G., Pietrosiuk, A., Diemand, A., Zentgraf, H. Mogk, A. (2009) Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 28 : 315 325.
7. Bouveret, E., Bénédetti, H., Rigal, A., Loret, E. Lazdunski, C. (1999) In vitro characterization of peptidoglycan-associated lipoprotein (PAL)-peptidoglycan and PAL-TolB interactions. J Bacteriol 181 : 6306 6311.
8. Boyer, F., Fichant, G., Berthod, J., Vandenbrouck, Y. Attree, I. (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. Cascales, E. (2008) The type VI secretion toolkit. EMBO Rep 9 : 735 741.
10. Cascales, E. Lloubès, R. (2004) Deletion analyses of the peptidoglycan-associated lipoprotein Pal reveals three independent binding sequences including a TolA box. Mol Microbiol 51 : 873 885.
11. Cascales, E., Bernadac, A., Gavioli, M., Lazzaroni, J.C. Lloubes, R. (2002) Pal lipoprotein of Escherichia coli plays a major role in outer membrane integrity. J Bacteriol 184 : 754 759.
12. Christie, P.J., Atmakuri, K., Krishnamoorthy, V., Jakubowski, S. Cascales, E. (2005) Biogenesis, architecture, and function of bacterial type IV secretion systems. Ann Rev Microbiol 59 : 451 485. (Pubitemid 41507439)
13. De Mot, R. Vanderleyden, J. (1994) The C-terminal sequence conservation between OmpA-related outer membrane proteins and MotB suggests a common function in both Gram-positive and Gram-negative bacteria, possibly in the interaction of these domains with peptidoglycan. Mol Microbiol 12 : 333 334.
14. Dudley, E.G., Thomson, N., Parkhill, J., Morin, N. Nataro, J.P. (2006) Proteomic and microarray characterization of the AggR regulon identifies a pheU pathogenicity island in enteroaggregative Escherichia coli. Mol Microbiol 61 : 1267 1282.
15. Enos-Berlage, J., Guvener, Z., Keenan, C. McCarter, L.L. (2005) Genetic determinants of biofilm development of opaque and translucent V. parahaemolyticus. Mol Microbiol 55 : 1160 1182.
16. Filip, C., Fletcher, G., Wulff, J.L. Earhart, C.F. (1973) Solubilization of the cytoplasmic membrane of Escherichia coli by the ionic detergent Sodium-Lauryl-Sarcosinate. J Bacteriol 115 : 717 722.
17. Filloux, A., Hachani, A. Bleves, S. (2008) The bacterial type VI secretion machine: yet another player for protein transport across membranes. Microbiology 154 : 1570 1583.
18. Goemaere, E.L., Devert, A., Lloubès, R. Cascales, E. (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.
19. Grizot, S. Buchanan, S.K. (2004) Structure of the OmpA-like domain of RmpM from Neisseria meningitidis. Mol Microbiol 51 : 1027 1037.
20. Harrington, S.M., Dudley, E.G. Nataro, J.P. (2006) Pathogenesis of enteroaggregative Escherichia coli infection. FEMS Microbiol Lett 254 : 12 18.
21. Hizukuri, Y., Morton, J.F., Yakushi, T., Kojima, S. Homma, M. (2009) The peptidoglycan-binding (PGB) domain of the Escherichia coli Pal protein can also function as the PGB domain in E. coli flagellar motor protein MotB. J Biochem 146 : 219 229.
22. Howard, S.P., Gebhart, C., Langen, G.R., Li, G. Strozen, T.G. (2006) Interactions between peptidoglycan and the ExeAB complex during assembly of the type II secretin of Aeromonas hydrophila. Mol Microbiol 59 : 1062 1072.
23. Jakubowski, S.J., Krishnamoorthy, V., Cascales, E. Christie, P.J. (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.
24. Kanamaru, S., Leiman, P.G., Kostyuchenko, V.A., Chipman, P.R., Mesyanzhinov, V.V., Arisaka, F. Rossmann, M.G. (2002) Structure of the cell-puncturing device of bacteriophage T4. Nature 415 : 553 557.
25. Khajanchi, B.K., Sha, J., Kozlova, E.V., Erova, T.E., Suarez, G., Sierra, J.C., et al. (2009) N-Acyl homoserine lactones involved in quorum sensing control type VI secretion system, biofilm formation, protease production, and in vivo virulence from a clinical isolate of Aeromonas hydrophila. Microbiology 155 : 3518 3531.
26. Koebnik, R. (1995) Proposal for a peptidoglycan-associating alpha-helical motif in the C-terminal regions of some bacterial cell-surface proteins. Mol Microbiol 16 : 1269 1270.
27. Kojima, S., Furukawa, Y., Matsunami, H., Minamino, T. Namba, K. (2008) Characterization of the periplasmic domain of MotB and implications for its role in the stator assembly of the bacterial flagellar motor. J Bacteriol 190 : 3314 3322.
28. Leduc, M., Ishidate, K., Shakibai, N. Rothfield, L. (1992) Interactions of Escherichia coli membrane lipoproteins with the murein sacculus. J Bacteriol 174 : 7982 7988.
29. Leiman, P.G., Basler, M., Ramagopal, U.A., Bonanno, J.B., Sauder, J.M., Pukatzki, S., et al. (2009) Type VI secretion apparatus and phage tail-associated protein complexes share a common evolutionary origin. Proc Natl Acad Sci USA 106 : 4154 4159.
30. Lesic, B., Starkey, M., He, J., Hazan, R. Rahme, L.G. (2009) Quorum sensing differentially regulates Pseudomonas aeruginosa type VI secretion locus I and homologous loci II and III, which are required for pathogenesis. Microbiology 155 : 2845 2855.
31. Lloubès, R., Cascales, E., Walburger, A., Bouveret, E., Lazdunski, C., Bernadac, A. Journet, L. (2001) The Tol-Pal proteins of the Escherichia coli cell envelope: an energized system required for outer membrane integrity? Res Microbiol 152 : 523 529.
32. Ma, L.S., Lin, J.S. Lai, E.M. (2009a) 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.
33. Ma, A.T., McAuley, S., Pukatzki, S. Mekalanos, J.J. (2009b) Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5 : 234 243.
34. Mattinen, L., Nissinen, R., Riipi, T., Kalkkinen, N. Pirhonen, M. (2007) Host-extract induced changes in the secretome of the plant pathogenic bacterium Pectobacterium atrosepticum. Proteomics 7 : 3527 3537.
35. Mougous, J.D., Cuff, M.E., Raunser, S., Shen, A., Zhou, M., Gifford, C.A., et al. (2006) A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 : 1526 1530.
36. Nataro, J.P. (2005) Enteroaggregative Escherichia coli pathogenesis. Curr Opin Gastroenterol 21 : 4 8.
37. Parsons, D. Heffron, F. (2005) sciS, an icmF homolog in S. enterica serovar Typhimurium, limits intracellular replication and decreases virulence. Infect Immun 73 : 4338 4345.
38. Parsons, L.M., Lin, F. Orban, J. (2006) Peptidoglycan recognition by Pal, an outer membrane lipoprotein. Biochemistry 45 : 2122 2128.
39. Pell, L.G., Kanelis, V., Donaldson, L.W., Howell, P.L. Davidson, A.R. (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 USA 106 : 4160 4165.
40. Persson, O.P., Pinhassi, J., Riemann, L., Marklund, B.I., Rhen, M., Normark, S., et al. (2009) High abundance of virulence gene homologues in marine bacteria. Environ Microbiol 11 : 1348 1357.
41. Pucciarelli, M.G. García-del Portillo, F. (2003) Protein-peptidoglycan interactions modulate the assembly of the needle complex in the Salmonella invasion-associated type III secretion system. Mol Microbiol 48 : 573 585.
42. Pukatzki, S., Ma, A.T., Sturtevant, D., Krastins, B., Sarracino, D., Nelson, W.C., et al. (2006) Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci USA 103 : 1528 1533.
43. Pukatzki, S., Ma, A.T., Revel, A.T., Sturtevant, D. Mekalanos, J.J. (2007) Type VI secretion system translocates a phage tail spike-like protein into target cells where it cross-links actin. Proc Natl Acad Sci USA 104 : 15508 15513.
44. Pukatzki, S., McAuley, S.B. Miyata, S.T. (2009) The type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 12 : 11 17.
45. Rao, P., Yamada, Y., Tan, Y. Leung, K.Y. (2004) Use of proteomics to identify novel virulence determinants that are required for E. tarda pathogenesis. Mol Microbiol 53 : 573 586.
46. Roujeinikova, A. (2008) Crystal structure of the cell wall anchor domain of MotB, a stator component of the bacterial flagellar motor: implications for peptidoglycan recognition. Proc Natl Acad Sci USA 105 : 10348 10353.
47. Sauer, K., Camper, A.K., Ehrlich, G.D., Costerton, J.W. Davies, D.G. (2002) Pseudomonas aeruginosa displays multiple phenotypes during development as a biofilm. J Bacteriol 184 : 1140 1154.
48. Shrivastava, S. Mande, S.S. (2008) Identification and functional characterization of gene components of Type VI Secretion system in bacterial genomes. PLoS One 3 : e2955.
49. Southey-Pillig, C., Davies, D. Sauer, K. (2005) Characterization of temporal protein production in Pseudomonas aeruginosa biofilms. J Bacteriol 187 : 8114 8126.
50. Suarez, G., Sierra, J., Sha, J., Wang, S., Erova, T., Fadl, A., et al. (2008) Molecular characterization of a functional type VI secretion system from a clinical isolate of Aeromonas hydrophila. Microb Pathog 44 : 344 361.
51. Suarez, G., Sierra, J., Erova, T., Sha, J., Horneman, A. Chopra, A.K. (2009) A Type VI secretion system effector protein VgrG1 from Aeromonas hydrophila that induces host cell toxicity by ADP-ribosylation of actin. J Bacteriol 192 : 155 168.
52. Weber, B., Hasic, M., Chen, C., Wai, S.N. Milton, D.L. (2009) Type VI secretion modulates quorum sensing and stress response in Vibrio anguillarum. Environ Microbiol 11 : 3018 3028.
53. Zheng, J. Leung, K.Y. (2007) Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66 : 1192 1206.