Towards a Structural Comprehension of Bacterial Type VI Secretion Systems: Characterization of the TssJ-TssM Complex of an Pathovar

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Type VI secretion systems (T6SS) are trans-envelope machines dedicated to the secretion of virulence factors into eukaryotic or prokaryotic cells, therefore required for pathogenesis and/or for competition towards neighboring bacteria. The T6SS apparatus resembles the injection device of bacteriophage T4, and is anchored to the cell envelope through a membrane complex. This membrane complex is composed of the TssL, TssM and TagL inner membrane anchored proteins and of the TssJ outer membrane lipoprotein. Here, we report the crystal structure of the enteroaggregative Escherichia coli Sci1 TssJ lipoprotein, a two four-stranded β-sheets protein that exhibits a transthyretin fold with an additional α-helical domain and a protruding loop. We showed that TssJ contacts TssM through this loop since a loop depleted mutant failed to interact with TssM in vitro or in vivo. Biophysical analysis of TssM and TssJ-TssM interaction suggest a structural model of the membrane-anchored outer shell of T6SS. Collectively, our results provide an improved understanding of T6SS assembly and encourage structure-aided drug design of novel antimicrobials targeting T6SS.

Vyšlo v časopise: Towards a Structural Comprehension of Bacterial Type VI Secretion Systems: Characterization of the TssJ-TssM Complex of an Pathovar. PLoS Pathog 7(11): e32767. doi:10.1371/journal.ppat.1002386
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.ppat.1002386

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Zdroje

1. CascalesE 2008 The Type VI secretion toolkit. EMBO Rep 9 735 741

2. SchwarzSHoodRDMougousJD 2010 What is Type VI secretion doing in all those bugs? Trends Microbiol 18 531 537

3. BernardCSBrunetYRGueguenECascalesE 2010 Nooks and crannies in Type VI secretion regulation. J Bacteriol 192 3850 60

4. RecordsAR 2011 The Type VI secretion system: A multipurpose delivery system with a phage like machinery. Mol Plant Microbe Interact 24 751 7

5. PukatzkiSMaATSturtevantDKrastinsBSarracinoD 2006 Identification of a conserved bacterial protein secretion system in Vibrio cholerae using the Dictyostelium host model system. Proc Natl Acad Sci U S A 103 1528 33

6. MaATMekalanosJJ 2010 In vivo actin cross-linking induced by Vibrio cholerae Type VI secretion system is associated with intestinal inflammation. Proc Natl Acad Sci U S A 107 4365 70

7. SchwarzSWestTEBoyerFChiangWCCarlMA 2010 Burkholderia type VI secretion systems have distinct roles in eukaryotic and bacterial cell interactions. PLoS Pathog 6 e1001068

8. RussellABHoodRDBuiNKLerouxMVollmerW 2011 Type VI secretion delivers bacteriolytic effectors to target cells. Nature 475 343 7

9. MougousJDCuffMERaunserSShenAZhouM 2006 A virulence locus of Pseudomonas aeruginosa encodes a protein secretion apparatus. Science 312 1526 1530

10. PukatzkiSMaATRevelATSturtevantDMekalanosJJ 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

11. LeimanPGBaslerMRamagopalUABonannoJBSauderJM 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

12. PukatzkiSMcAuleySBMiyataST 2009 The Type VI secretion system: translocation of effectors and effector-domains. Curr Opin Microbiol 12 11 17

13. PellLGKanelisVDonaldsonLWHowellPLDavidsonAR 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

14. KanamaruSLeimanPGKostyuchenkoVAChipmanPRMesyanzhinovVV 2002 Structure of the cell-puncturing device of bacteriophage T4. Nature 415 553 557

15. BingleLEBaileyCMPallenMJ 2008 Type VI secretion: a beginner's guide. Curr Opin Microbiol 11 3 8

16. ShalomGShawJGThomasMS 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 99

17. BonemannGPietrosiukADiemandAZentgrafHMogkA 2009 Remodelling of VipA/VipB tubules by ClpV-mediated threading is crucial for type VI protein secretion. EMBO J 28 315 325

18. KanamaruS 2009 Structural similarity of tailed phages and pathogenic bacterial secretion systems. Proc Natl Acad Sci U S A 106 4067 4068

19. MaATMcAuleySPukatzkiSMekalanosJJ 2009 Translocation of a Vibrio cholerae type VI secretion effector requires bacterial endocytosis by host cells. Cell Host Microbe 5 234 43

20. MaLSLinJSLaiEM 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

21. AschtgenMSBernardCSde BentzmannSLloubesRCascalesE 2008 SciN is an outer membrane lipoprotein required for type VI secretion in enteroaggregative Escherichia coli. J Bacteriol 190 7523 7531

22. AschtgenMSGavioliMDessenALloubesRCascalesE 2010 The SciZ protein anchors the enteroaggregative Escherichia coli Type VI secretion system to the cell wall. Mol Microbiol 75 886 899

23. AschtgenMSThomasMSCascalesE 2010 Anchoring the type VI secretion system to the peptidoglycan: TssL, TagL, TagP... what else? Virulence 1 535 540

24. ZhengJLeungKY 2007 Dissection of a type VI secretion system in Edwardsiella tarda. Mol Microbiol 66 1192 1206

25. VincentelliRCanaanSOffantJCambillauCBignonC 2005 Automated expression and solubility screening of His-tagged proteins in 96-well format. Anal Biochem 346 77 84

26. SciaraGBlangySSiponenMMc GrathSvan SinderenD 2008 A topological model of the baseplate of lactococcal phage Tuc2009. J Biol Chem 283 2716 2723

27. SulzenbacherGGruezARoig-ZamboniVSpinelliSValenciaC 2002 A medium-throughput crystallization approach. Acta Crystallogr D Biol Crystallogr 58 2109 2115

28. KrissinelEHenrickK 2007 Inference of macromolecular assemblies from crystalline state. J Mol Biol 372 774 797

29. HolmLRosenstromP 2010 Dali server: conservation mapping in 3D. Nucleic Acids Res 38 W545 549

30. EneqvistTLundbergEKarlssonAHuangSSantosCR 2004 High resolution crystal structures of piscine transthyretin reveal different binding modes for triiodothyronine and thyroxine. J Biol Chem 279 26411 26416

31. ZanottiGCendronLRamazzinaIFolliCPercudaniR 2006 Structure of zebra fish HIUase: insights into evolution of an enzyme to a hormone transporter. J Mol Biol 363 1 9

32. IzoreTPerduCJobVAttreeIFaudryE 2011 Structural characterization and membrane localization of ExsB from the Type III secretion system (T3SS) of Pseudomonas aeruginosa. J Mol Biol 413 236 246

33. DundasJOuyangZTsengJBinkowskiATurpazY 2006 CASTp: computed atlas of surface topography of proteins with structural and topographical mapping of functionally annotated residues. Nucleic Acids Res 34 W116 118

34. ColeCBarberJDBartonGJ 2008 The Jpred 3 secondary structure prediction server. Nucleic Acids Res 36 W197 201

35. SchellMAUlrichRLRibotWJBrueggemannEEHinesHB 2007 Type VI secretion is a major virulence determinant in Burkholderia mallei. Mol Microbiol 64 1466 85

36. BurtnickMNBrettPJHardingSVNgugiSARibotWJ 2011 The cluster 1 type VI secretion system is a major virulence determinant in Burkholderia pseudomallei. Infect Immun 79 1512 25

37. HoodRDSinghPHsuFGüvenerTCarlMA 2010 A type VI secretion system of Pseudomonas aeruginosa targets a toxin to bacteria. Cell Host Microbe 7 25 37

38. FronzesRSchäferEWangLSaibilHROrlovaEV 2009 Structure of a type IV secretion system core complex. Science 323 266 268

39. ChandranVFronzesRDuquerroySCroninNNavazaJ 2009 Structure of the outer membrane complex of a type IV secretion system. Nature 462 1011 1015

40. SchraidtOMarlovitsTC 2011 Three-dimensional model of Salmonella's needle complex at subnanometer resolution. Science 331 1192 1195

41. ReichowSLKorotkovKVHolWGGonenT 2010 Structure of the cholera toxin secretion channel in its closed state. Nat Struct Mol Biol 17 1226 1232

42. HardieKRLorySPugsleyAP 1996 Insertion of an outer membrane protein in Escherichia coli requires a chaperone-like protein. EMBO J 15 978 988

43. CragoAMKoronakisV 1998 Salmonella InvG forms a ring-like multimer that requires the InvH lipoprotein for outer membrane localization. Mol Microbiol 30 47 56

44. DaeflerSRusselM 1998 The Salmonella typhimurium InvH protein is an outer membrane lipoprotein required for the proper localization of InvG. Mol Microbiol 28 1367 1380

45. SpudichGMFernandezDZhouXRChristiePJ 1996 Intermolecular disulfide bonds stabilize VirB7 homodimers and VirB7/VirB9 heterodimers during biogenesis of the Agrobacterium tumefaciens T-complex transport apparatus. Proc Natl Acad Sci U S A 93 7512 7517

46. FernandezDSpudichGMZhouXRChristiePJ 1996 The Agrobacterium tumefaciens VirB7 lipoprotein is required for stabilization of VirB proteins during assembly of the T-complex transport apparatus. J Bacteriol 178 3168 3176

47. CascalesEChristiePJ 2004 Definition of a bacterial type IV secretion pathway for a DNA substrate. Science 304 1170 1173

48. ChristiePJAtmakuriKKrishnamoorthyVJakubowskiSCascalesE 2005 Biogenesis, architecture, and function of bacterial type IV secretion systems. Annu Rev Microbiol 59 451 85

49. DaviesDRCohenGH 1996 Interactions of protein antigens with antibodies. Proc Natl Acad Sci U S A 93 7 12

50. ShahianTLeeGMLazicAArnoldLAVelusamyP 2009 Inhibition of a viral enzyme by a small-molecule dimer disruptor. Nat Chem Biol 5 640 646

51. CascalesELloubesRSturgisJN 2001 The TolQ-TolR proteins energize TolA and share homologies with the flagellar motor proteins MotA-MotB. Mol Microbiol 42 795 807

52. KabschW 2010 Xds. Acta Crystallogr D Biol Crystallogr 66 125 132

53. BricogneGVonrheinCFlensburgCSchiltzMPaciorekW 2003 Generation, representation and flow of phase information in structure determination: recent developments in and around SHARP 2.0. Acta Crystallogr D Biol Crystallogr 59 2023 2030

54. CowtanK 2006 The Buccaneer software for automated model building. 1. Tracing protein chains. Acta Crystallogr D Biol Crystallogr 62 1002 1011

55. EmsleyPCowtanK 2004 Coot: model-building tools for molecular graphics. Acta Crystallogr D Biol Crystallogr 60 2126 2132

56. BlancERoversiPVonrheinCFlensburgCLeaSM 2004 Refinement of severely incomplete structures with maximum likelihood in BUSTER-TNT. Acta Crystallogr D Biol Crystallogr 60 2210 2221

57. MurshudovGVaginAADodsonEJ 1997 Refinement of Macromolecular Structures by the Maximum-Likelihood Method. Acta Crystallogr D Biol Crystallogr D 53 240 255

58. BakerNASeptDJosephSHolstMJMcCammonJA 2001 Electrostatics of nanosystems: application to microtubules and the ribosome. Proc Natl Acad Sci U S A 98 10037 10041

59. CorpetF 1988 Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16 10881 90

60. GouetPCourcelleEStuartDIMetozF 1999 ESPript: analysis of multiple sequence alignments in PostScript. Bioinformatics 15 305 8

61. DeLanoW 2002 The PyMOL Molecular Graphics System. DeLano Scientific LLC (San Carlos, CA) Available: http://www.pymol.org. Accessed 11 October 2011