Structural characterization and membrane localization of ExsB from the type III secretion system (T3SS) of pseudomonas aeruginosa

Journal of Molecular Biology

Volumn 413, Issue 1, 2011, Pages 236-246

  Izoré, Thierry ^a,b,c   Perdu, Caroline ^b,c,d,e   Job, Viviana ^a,b,c   Attree, Ina ^b,c,d,e   Faudry, Eric ^b,c,d,e   Dessen, Andréa ^a,b,c  

^a INSTITUT DE BIOLOGIE STRUCTURALE   (France)

^b DIF   (France)

^c CNRS   (France)

^d UNIV GRENOBLE ALPES   (France)

^e INSERM   (France)

Author keywords

DDM; dodecyl maltoside; EGTA; ESRF; ethylene glycol bis( aminoethyl ether) N,N tetraacetic acid; European Synchrotron Radiation Facility; maltose binding protein; MBP; OMR; outer membrane ring; SAD; single anomalous dispersion; T3SS; type III secretion system

Indexed keywords

BACTERIAL PROTEIN; EXSB PROTEIN; LIPOPROTEIN; SECRETIN; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CELL FRACTIONATION; CRYSTAL STRUCTURE; MOLECULAR RECOGNITION; NONHUMAN; OUTER MEMBRANE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; PSEUDOMONAS AERUGINOSA; SHIGELLA; TYPE III SECRETION SYSTEM;

PSEUDOMONAS AERUGINOSA; SHIGELLA; YERSINIA;

EID: 80053296817     PISSN: 00222836     EISSN: 10898638     Source Type: Journal    
DOI: 10.1016/j.jmb.2011.07.043     Document Type: Article

References (52)

1. Lister P.D., Wolter D.J., and Hanson N.D Antibacterial-resistant Pseudomonas aeruginosa: clinical impact and complex regulation of chromosomally encoded resistance mechanisms Clin. Microbiol. Rev. 22 2009 582 610
2. Izoré T., Job V., and Dessen A Biogenesis, regulation, and targeting of the type III secretion system Structure 19 2011 603 612
3. Blocker A.J., Deane J.E., Veenendaal A.K., Roversi P., Hodgkinson J.L., Johnson S., and Lea S.M What's the point of the type III secretion system needle? Proc. Natl Acad. Sci. USA 105 2008 6507 6513 (Pubitemid 351754539)
4. Cornelis G.R The type III secretion injectisome Nat. Rev., Microbiol. 4 2006 811 825 (Pubitemid 44593948)
5. Marlovits T.C., and Stebbins C.E Type III secretion systems shape up as they ship out Curr. Opin. Microbiol. 13 2009 1 6
6. Matteï P.-J., Faudry E., Job V., Izoré T., Attree I., and Dessen A Membrane targeting and pore formation by the type III secretion system translocon FEBS. J. 278 2011 414 426
7. Galán J.E Common themes in the design and function of bacterial effectors Cell Host Microbe 5 2009 571 579
8. Goure J., Broz P., Attree O., Cornelis G.R., and Attree I Protective anti-V antibodies inhibit Pseudomonas and Yersinia translocon assembly within host membranes J. Infect. Dis. 192 2005 218 225 (Pubitemid 40993391)
9. Hauser A.R The type III secretion system of Pseudomonas aeruginosa: infection by injection Nat. Rev., Microbiol. 7 2009 654 665
10. Worrall L.J., Lameignere E., and Strynadka N.C Structural overview of the bacterial injectisome Curr. Opin. Microbiol. 14 2011 3 8
11. Deane J.E., Abrusci P., Johnson S., and Lea S.M Timing is everything: the regulation of type III secretion Cell. Mol. Life Sci. 67 2010 1065 1075
12. Hodgkinson J.L., Horsley A., Stabat D., Simon M., Johnson S., and da Fonseca P.C.A. Three-dimensional reconstruction of the Shigella T3SS transmembrane regions reveals 12-fold symmetry and novel features throughout Nat. Struct. Mol. Biol. 5 2009 477 485
13. Reichow S.L., Korotkov K.V., Hol W.G.J., and Gonen T Structure of the cholera toxin secretion channel in its closed state Nat. Struct. Mol. Biol. 17 2010 1226 1233
14. Schraidt O., Lefebre M.D., Brunner M.J., Schmied W.H., Schmidt A., and Radics J. Topology and organization of the Salmonella typhimurium type III secretion needle complex components PLoS. Pathog. 6 2010 e1000824
15. Spreter T., Yip C.K., Sanowar S., Andre I., Kimbrough T.G., and Vuckovic M. A conserved structural motif mediates formation of the periplasmic rings in the type III secretion system Nat. Struct. Mol. Biol. 5 2009 468 476
16. Burghout P., Beckers F., de Wit E., van Boxtel R., Cornelis G.R., Tommassen J., and Koster M Role of the pilot protein YscW in the biogenesis of the YscC secretin in Yersinia enterocolitica J. Bacteriol. 186 2004 5366 5375 (Pubitemid 39038138)
17. Crago A.M., and Koronakis V. Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization Mol. Microbiol. 30 1998 47 56 (Pubitemid 28446619)
18. Daefler S., and Russel M The Salmonella typhimurium InvH protein is an outer membrane lipoprotein required for the proper localization of InvG Mol. Microbiol. 28 1998 1367 1380 (Pubitemid 28293558)
19. Nakano N., Kubori T., Knoshita M., Imada K., and Nagai H Crystal structure of Legionella DotD: insights into the relationship between type IVb and type II/III secretion systems PloS. Pathog. 6 2010 e1001129
20. Balasingham S.V., Collins R.F., Assalkhou R., Homberset H., Frye S.A., Derrick J.P., and Tonjum T Interactions between the lipoprotein PilP and the secretin PilQ in Neisseria meningitidis J. Bacteriol. 189 2007 5716 5727 (Pubitemid 47206418)
21. Jain S., Moscicka K.B., Bos M.P., Pachulec E., Stuart M.C.A., and Keegstra W. Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria PloS. ONE. 6 2011 e16624
22. Koo J., Tammam S., Ku S.-Y., Sampaleanu L.M., Burrows L.L., and Howell P.L PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa type IV pilus secretin J. Bacteriol. 190 2008 6961 6969
23. Guilvout I., Chami M., Engel A., Pugsley A.P., and Bayan N Bacterial outer membrane secretin PulD assembles and inserts into the inner membrane in the absence of its pilotin EMBO. J. 25 2006 5241 5249 (Pubitemid 44764134)
24. Hardie K.R., Lory S., and Pugsley A.P Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein EMBO. J. 15 1996 978 988 (Pubitemid 26077825)
25. Hardie K.R., Seydel A., Guilvout I., and Pugsley A.P The secretin-specific chaperone-like protein of the general secretory pathway: separation of proteolytic protection and piloting functions Mol. Microbiol. 5 1996 967 976 (Pubitemid 26411340)
26. Lario P.I., Pfuetzner R.A., Frey E.A., Creagh L., Haynes C., Maurelli A.T., and Strynadka N.C Structure and biochemical analysis of a secretin pilot protein EMBO. J. 24 2005 1111 1121 (Pubitemid 40516595)
27. Okon M., Moraes T.F., Lario P.I., Creagh A.L., Haynes C.A., Strynadka N.C., and McIntosh L.P Structural characterization of the type III pilot-secretin complex from Shigella flexneri Structure 16 2008 1544 1554
28. Schuch R., and Maurelli A.T MxiM and MxiJ, base elements of the Mxi-Spa type III secretion system of Shigella, interact with and stabilize the MxiD secretin in the cell envelope J. Bacteriol. 183 2001 6991 6998 (Pubitemid 33121830)
29. Bayan N., Guilvout I., and Pugsley A.P Secretins take shape Mol. Microbiol. 60 2006 1 4 (Pubitemid 43363282)
30. Remans K., Vercammen K., Bodilis J., and Cornelis P Genome-wide analysis and literature-based survey of lipoproteins in Pseudomonas aeruginosa Microbiology 156 2010 2597 2607
31. Viarre V., Cascales E., Ball G., Michel G.P., Filloux A., and Voulhoux R HxcQ liposecretin is self-piloted to the outer membrane by its N-terminal lipid anchor J. Biol. Chem. 284 2009 33815 33823
32. Troisfontaines P., and Cornelis G.R Type III secretion: more systems than you think Physiology 20 2005 326 339 (Pubitemid 41457398)
33. Juncker A.S., Willenbrock H., Von Heijne G., Brunak S., Nielsen H., and Krogh A Prediction of lipoprotein signal peptides in Gram-negative bacteria Protein Sci. 12 2003 1652 1662 (Pubitemid 36910046)
34. 2+ dependecy, is related to ExsB of Pseudomonas aeruginosa J. Bacteriol. 177 1995 4230 4237
35. Brutinel E.D., Vakulskas C.A., and Yahr T.L ExsD inhibits expression of the Pseudomonas aeruginosa type III secretion system by disrupting ExsA self-association and DNA binding activity J. Bacteriol. 192 2010 1479 1486
36. Thibault J., Faudry E., Ebel C., Attree I., and Elsen S Anti-activator ExsD forms a 1:1 complex with ExsA to inhibit transcription of type III secretion operons J. Biol. Chem. 284 2009 15762 15770
37. Goranson J., Hovey A.K., and Franck D.W Functional analysis of exsC and exsB in regulation of exoenzyme S production by Pseudomonas aeruginosa J. Bacteriol. 179 1997 1646 1654 (Pubitemid 27100454)
38. 2+ and host cell contact proceeds through two distinct signaling pathways Infect. Immun. 74 2006 3334 3341 (Pubitemid 43794521)
39. Sigal C.T., Zhou W., Buser C.A., McLaughlin S., and Resh M.D Amino-terminal basic residues of Src mediate membrane binding through electrostatic interaction with acidic phospholipids Proc. Natl Acad. Sci. USA 91 1994 12253 12257 (Pubitemid 24368643)
40. Bentham M., Mazaleyrat S., and Harris M Role of myristoylation and N-terminal basic residues in membrane association of the human immunodeficiency virus type 1 Nef protein J. Gen. Virol. 87 2006 563 571
41. Laskowski R.A SURFNET: a program for visualizing molecular surfaces, cavities, and intermolecular interactions J. Mol. Graphics 13 1995 323 330
42. Golovanov A.P., Balasingham S., Tzitzilonis C., Goult B.T., Lian L.-Y., and Homberset H. The solution structure of a domain from the Neisseria meningitidis lipoprotein PilP reveals a new Δ-sandwich fold J. Mol. Biol. 364 2006 186 195 (Pubitemid 44649250)
43. Carbonnelle E., Helaine S., Prouvensier L., Nassif X., and Pelicic V Type IV pilus biogenesis in Neisseria meningitidis: PilW is involved in a step occurring after pilus assembly, essential for fibre stability and function Mol. Microbiol. 55 2005 54 64 (Pubitemid 40127884)
44. Trindade M.B., Job V., Contreras-Martel C., Pelicic V., and Dessen A. Structure of a widely conserved type IV pilus biogenesis factor which affects the stability of secretin multimers J. Mol. Biol. 378 2008 1031 1039
45. Kim K., Oh J., Han D., Kim E.E., Lee B.C., and Kim Y Crystal structure of PilF: functional implication in the type 4 pilus biogenesis in Pseudomonas aeruginosa Biochem. Biophys. Res. Commun. 340 2006 1028 1038 (Pubitemid 43083382)
46. Dacheux D., Attree I., Schneider C., and Toussaint B Cell death of human polymorphonuclear neutrophils induced by a Pseudomonas aeruginosa cystic fibrosis isolate requires a functional type III secretion system Infect. Immun. 67 1999 6164 6167 (Pubitemid 29508152)
47. Goure J., Pastor A., Faudry E., Chabert J., Dessen A., and Attree I The V antigen of Pseudomonas aeruginosa is required for assembly of the functional PopB/PopD translocation pore in host cell membranes Infect. Immun. 72 2004 4741 4750 (Pubitemid 38989335)
48. Kabsch W XDS Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 125 132
49. Adams P.D., Afonine P.V., Bukoczi G., Chen V.B., Davis I.W., and Echols N. PHENIX: a comprehensive Python-based system for macromolecular structure solution Acta Crystallogr., Sect. D: Biol. Crystallogr. 66 2010 213 221
50. Storoni L., McCoy A., and Read R Likelihood-enhanced fast rotation functions Acta Crystallogr., Sect. D: Biol. Crystallogr. 57 2004 1373 1382
51. Emsley P., and Cowtan K Coot: model-building tools for molecular graphics Acta Crystallogr., Sect. D: Biol. Crystallogr. 60 2004 2126 2132 (Pubitemid 41742764)
52. Murshudov G., Vagin A., and Dodson E Refinement of macromolecular structures by the maximum-likelihood method Acta Crystallogr., Sect. D: Biol. Crystallogr. 53 1997 240 255 (Pubitemid 27235885)