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Structure of a widely conserved type IV pilus biogenesis factor that affects the stability of secretin multimers.

Trindade MB, Job V, Contreras-Martel C, Pelicic V, Dessen A
J Mol Biol 378 1031-9 (2008)
Cited: 34 times
EuropePMC logo PMID: 18433773

Abstract

Type IV pili (Tfp) are arguably the most widespread pili in bacteria, whose biogenesis requires a complex machinery composed of as many as 18 different proteins. This includes the conserved outer membrane-localized secretin, which forms a pore through which Tfp emerge on the bacterial surface. Although, in most model species studied, secretin oligomerization and functionality requires the action of partner lipoproteins, structural information regarding these molecules is limited. We report the high-resolution crystal structure of PilW, the partner lipoprotein of the type IV pilus secretin PilQ from Neisseria meningitidis, which defines a conserved class of Tfp biogenesis proteins involved in the formation and/or stability of secretin multimers in a wide variety of bacteria. The use of the PilW structure as a blueprint reveals an area of high-level sequence conservation in homologous proteins from different pathogens that could reflect a possible secretin-binding site. These results could be exploited for the development of new broad-spectrum antibacterials interfering with the biogenesis of a widespread virulence factor.

Reviews - 2vq2 mentioned but not cited (2)

  1. Secretins: dynamic channels for protein transport across membranes. Korotkov KV, Gonen T, Hol WG. Trends Biochem. Sci. 36 433-443 (2011)
  2. Bacterial secretins: Mechanisms of assembly and membrane targeting. Silva YRO, Contreras-Martel C, Macheboeuf P, Dessen A. Protein Sci 29 893-904 (2020)

Articles - 2vq2 mentioned but not cited (6)

  1. PilF is an outer membrane lipoprotein required for multimerization and localization of the Pseudomonas aeruginosa Type IV pilus secretin. Koo J, Tammam S, Ku SY, Sampaleanu LM, Burrows LL, Howell PL. J. Bacteriol. 190 6961-6969 (2008)
  2. Self-recognition mechanism of MamA, a magnetosome-associated TPR-containing protein, promotes complex assembly. Zeytuni N, Ozyamak E, Ben-Harush K, Davidov G, Levin M, Gat Y, Moyal T, Brik A, Komeili A, Zarivach R. Proc. Natl. Acad. Sci. U.S.A. 108 E480-7 (2011)
  3. Structural and functional insights into the pilotin-secretin complex of the type II secretion system. Gu S, Rehman S, Wang X, Shevchik VE, Pickersgill RW. PLoS Pathog. 8 e1002531 (2012)
  4. Structure/function analysis of Neisseria meningitidis PilW, a conserved protein that plays multiple roles in type IV pilus biology. Szeto TH, Dessen A, Pelicic V. Infect. Immun. 79 3028-3035 (2011)
  5. Predicting drug targets by homology modelling of Pseudomonas aeruginosa proteins of unknown function. Babic N, Kovacic F. PLoS One 16 e0258385 (2021)
  6. The mechanism for polar localization of the type IVa pilus machine in Myxococcus xanthus. Herfurth M, Pérez-Burgos M, Søgaard-Andersen L. mBio 14 e0159323 (2023)


Reviews citing this publication (7)

  1. The type II secretion system: biogenesis, molecular architecture and mechanism. Korotkov KV, Sandkvist M, Hol WG. Nat. Rev. Microbiol. 10 336-351 (2012)
  2. Architecture of the type II secretion and type IV pilus machineries. Ayers M, Howell PL, Burrows LL. Future Microbiol 5 1203-1218 (2010)
  3. Biogenesis, regulation, and targeting of the type III secretion system. Izoré T, Job V, Dessen A. Structure 19 603-612 (2011)
  4. Meningococcal interactions with the host. Carbonnelle E, Hill DJ, Morand P, Griffiths NJ, Bourdoulous S, Murillo I, Nassif X, Virji M. Vaccine 27 Suppl 2 B78-89 (2009)
  5. Shuffling genes around in hot environments: the unique DNA transporter of Thermus thermophilus. Averhoff B. FEMS Microbiol. Rev. 33 611-626 (2009)
  6. Decoding the roles of pilotins and accessory proteins in secretin escort services. Koo J, Burrows LL, Howell PL. FEMS Microbiol. Lett. 328 1-12 (2012)
  7. Recent progress in structure and dynamics of dual-membrane-spanning bacterial nanomachines. Gold V, Kudryashev M. Curr. Opin. Struct. Biol. 39 1-7 (2016)

Articles citing this publication (19)

  1. Structural characterization of the type-III pilot-secretin complex from Shigella flexneri. Okon M, Moraes TF, Lario PI, Creagh AL, Haynes CA, Strynadka NC, McIntosh LP. Structure 16 1544-1554 (2008)
  2. Seventeen Sxy-dependent cyclic AMP receptor protein site-regulated genes are needed for natural transformation in Haemophilus influenzae. Sinha S, Mell JC, Redfield RJ. J. Bacteriol. 194 5245-5254 (2012)
  3. Structure and oligomerization of the PilC type IV pilus biogenesis protein from Thermus thermophilus. Karuppiah V, Hassan D, Saleem M, Derrick JP. Proteins 78 2049-2057 (2010)
  4. Pilotin-secretin recognition in the type II secretion system of Klebsiella oxytoca. Tosi T, Nickerson NN, Mollica L, Jensen MR, Blackledge M, Baron B, England P, Pugsley AP, Dessen A. Mol. Microbiol. 82 1422-1432 (2011)
  5. Outer membrane targeting of secretin PulD protein relies on disordered domain recognition by a dedicated chaperone. Nickerson NN, Tosi T, Dessen A, Baron B, Raynal B, England P, Pugsley AP. J. Biol. Chem. 286 38833-38843 (2011)
  6. Structural characterization of outer membrane components of the type IV pili system in pathogenic Neisseria. Jain S, Mościcka KB, Bos MP, Pachulec E, Stuart MC, Keegstra W, Boekema EJ, van der Does C. PLoS ONE 6 e16624 (2011)
  7. The archetype Pseudomonas aeruginosa proteins TssB and TagJ form a novel subcomplex in the bacterial type VI secretion system. Lossi NS, Manoli E, Simpson P, Jones C, Hui K, Dajani R, Coulthurst SJ, Freemont P, Filloux A. Mol. Microbiol. 86 437-456 (2012)
  8. Type IV pili of Acidithiobacillus ferrooxidans can transfer electrons from extracellular electron donors. Li Y, Li H. J. Basic Microbiol. 54 226-231 (2014)
  9. Pro-inflammatory cytokines can act as intracellular modulators of commensal bacterial virulence. Mahdavi J, Royer PJ, Sjölinder HS, Azimi S, Self T, Stoof J, Wheldon LM, Brännström K, Wilson R, Moreton J, Moir JW, Sihlbom C, Borén T, Jonsson AB, Soultanas P, Ala'Aldeen DA. Open Biol 3 130048 (2013)
  10. The biology of Neisseria adhesins. Hung MC, Christodoulides M. Biology (Basel) 2 1054-1109 (2013)
  11. A Single Amino Acid Substitution Changes the Self-Assembly Status of a Type IV Piliation Secretin. Nickerson NN, Abby SS, Rocha EP, Chami M, Pugsley AP. J. Bacteriol. 194 4951-4958 (2012)
  12. Structure-function relationships of the competence lipoprotein ComL and SSB in meningococcal transformation. Benam AV, Lång E, Alfsnes K, Fleckenstein B, Rowe AD, Hovland E, Ambur OH, Frye SA, Tønjum T. Microbiology (Reading, Engl.) 157 1329-1342 (2011)
  13. Natural transformation of Myxococcus xanthus. Wang J, Hu W, Lux R, He X, Li Y, Shi W. J. Bacteriol. 193 2122-2132 (2011)
  14. Novel Genes Related to Ceftriaxone Resistance Found among Ceftriaxone-Resistant Neisseria gonorrhoeae Strains Selected In Vitro. Gong Z, Lai W, Liu M, Hua Z, Sun Y, Xu Q, Xia Y, Zhao Y, Xie X. Antimicrob. Agents Chemother. 60 2043-2051 (2016)
  15. Crystal structure of the pilotin from the enterohemorrhagic Escherichia coli type II secretion system. Korotkov KV, Hol WG. J. Struct. Biol. 182 186-191 (2013)
  16. Comment A pilot sheds light on secretin assembly. Derrick J. Structure 16 1441-1442 (2008)
  17. Diffusion of antibiotics through the PilQ secretin in Neisseria gonorrhoeae occurs through the immature, sodium dodecyl sulfate-labile form. Nandi S, Swanson S, Tomberg J, Nicholas RA. J. Bacteriol. 197 1308-1321 (2015)
  18. The Inner Membrane Protein PilG Interacts with DNA and the Secretin PilQ in Transformation. Frye SA, Lång E, Beyene GT, Balasingham SV, Homberset H, Rowe AD, Ambur OH, Tønjum T. PLoS ONE 10 e0134954 (2015)
  19. Scaffolding Protein GspB/OutB Facilitates Assembly of the Dickeya dadantii Type 2 Secretion System by Anchoring the Outer Membrane Secretin Pore to the Inner Membrane and to the Peptidoglycan Cell Wall. Zhang S, Gu S, Rycroft P, Ruaudel F, Delolme F, Robert X, Ballut L, Pickersgill RW, Shevchik VE. mBio 13 e0025322 (2022)


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