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Structural and functional studies of EpsC, a crucial component of the type 2 secretion system from Vibrio cholerae.

Korotkov KV, Krumm B, Bagdasarian M, Hol WG
J Mol Biol 363 311-21 (2006)
Cited: 39 times
EuropePMC logo PMID: 16978643

Abstract

The type 2 secretion system (T2SS) occurring in Gram-negative bacteria is composed of 12-15 different proteins which form large assemblies spanning two membranes and secreting several virulence factors in folded state across the outer membrane. The T2SS component EpsC of Vibrio cholerae plays an important role in this machinery. While anchored in the inner membrane, by far the largest part of EpsC is periplasmic, containing a so-called homology region (HR) domain and a PDZ domain. Here we report studies on the structure and function of both periplasmic domains of EpsC. The crystal structures of two variants of the PDZ domain of EpsC from V. cholerae were determined at better than 2 A resolution. Compared to the short variant, the longer variant contains an additional N-terminal helix, and reveals a significant difference in the position of helix alphaB with respect to the beta-sheet. Both our structures show that the PDZ domain of EpsC adopts a more open form than in previously reported structures of other PDZ domains. Most interestingly, in the crystals of the short EpsC-PDZ domain the peptide binding groove interacts with an alpha-helix from a neighboring subunit burying approximately 921 A2 solvent accessible surface. This makes it possible that the PDZ domain of this bacterial protein binds proteins in a manner which is altogether different from that seen in any other PDZ domain so far. We also determined that the HR domain of EpsC is primarily responsible for the interaction with the secretin EpsD, while the PDZ is not, or much less, so. This new finding, together with studies of others, leads to the suggestion that the PDZ domain of EpsC may interact with exoproteins to be secreted while the HR domain plays a key role in linking the inner-membrane sub-complex of the T2SS in V. cholerae to the outer membrane secretin.

Reviews - 2i4s mentioned but not cited (2)

  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. Structural insights into the Type II secretion nanomachine. McLaughlin LS, Haft RJ, Forest KT. Curr. Opin. Struct. Biol. 22 208-216 (2012)

Articles - 2i4s mentioned but not cited (2)

  1. Structural and functional studies on the interaction of GspC and GspD in the type II secretion system. Korotkov KV, Johnson TL, Jobling MG, Pruneda J, Pardon E, Héroux A, Turley S, Steyaert J, Holmes RK, Sandkvist M, Hol WG. PLoS Pathog. 7 e1002228 (2011)
  2. Simultaneous Optimization of Biomolecular Energy Functions on Features from Small Molecules and Macromolecules. Park H, Bradley P, Greisen P, Liu Y, Mulligan VK, Kim DE, Baker D, DiMaio F. J Chem Theory Comput 12 6201-6212 (2016)


Reviews citing this publication (9)

  1. Secretins: dynamic channels for protein transport across membranes. Korotkov KV, Gonen T, Hol WG. Trends Biochem. Sci. 36 433-443 (2011)
  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. Type II secretion system: a magic beanstalk or a protein escalator. Nivaskumar M, Francetic O. Biochim. Biophys. Acta 1843 1568-1577 (2014)
  4. On the path to uncover the bacterial type II secretion system. Douzi B, Filloux A, Voulhoux R. Philos. Trans. R. Soc. Lond., B, Biol. Sci. 367 1059-1072 (2012)
  5. The emerging contribution of sequence context to the specificity of protein interactions mediated by PDZ domains. Luck K, Charbonnier S, Travé G. FEBS Lett. 586 2648-2661 (2012)
  6. Biogenesis of Pseudomonas aeruginosa type IV pili and regulation of their function. Leighton TL, Buensuceso RN, Howell PL, Burrows LL. Environ. Microbiol. 17 4148-4163 (2015)
  7. The trans-envelope architecture and function of the type 2 secretion system: new insights raising new questions. Thomassin JL, Santos Moreno J, Guilvout I, Tran Van Nhieu G, Francetic O. Mol. Microbiol. 105 211-226 (2017)
  8. Assembly of the type II secretion system. Peter Howard S. Res. Microbiol. 164 535-544 (2013)
  9. Architecture, Function, and Substrates of the Type II Secretion System. Korotkov KV, Sandkvist M. EcoSal Plus 8 (2019)

Articles citing this publication (26)

  1. Crystal structure of the N-terminal domain of the secretin GspD from ETEC determined with the assistance of a nanobody. Korotkov KV, Pardon E, Steyaert J, Hol WG. Structure 17 255-265 (2009)
  2. Structure of the cholera toxin secretion channel in its closed state. Reichow SL, Korotkov KV, Hol WG, Gonen T. Nat. Struct. Mol. Biol. 17 1226-1232 (2010)
  3. Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system. Korotkov KV, Hol WG. Nat. Struct. Mol. Biol. 15 462-468 (2008)
  4. Docking and assembly of the type II secretion complex of Vibrio cholerae. Lybarger SR, Johnson TL, Gray MD, Sikora AE, Sandkvist M. J. Bacteriol. 191 3149-3161 (2009)
  5. Nanobody-aided structure determination of the EpsI:EpsJ pseudopilin heterodimer from Vibrio vulnificus. Lam AY, Pardon E, Korotkov KV, Hol WGJ, Steyaert J. J. Struct. Biol. 166 8-15 (2009)
  6. Deciphering the Xcp Pseudomonas aeruginosa type II secretion machinery through multiple interactions with substrates. Douzi B, Ball G, Cambillau C, Tegoni M, Voulhoux R. J. Biol. Chem. 286 40792-40801 (2011)
  7. Characterization of the PilN, PilO and PilP type IVa pilus subcomplex. Tammam S, Sampaleanu LM, Koo J, Sundaram P, Ayers M, Chong PA, Forman-Kay JD, Burrows LL, Howell PL. Mol. Microbiol. 82 1496-1514 (2011)
  8. Structure and function of PilQ, a secretin of the DNA transporter from the thermophilic bacterium Thermus thermophilus HB27. Burkhardt J, Vonck J, Averhoff B. J. Biol. Chem. 286 9977-9984 (2011)
  9. The three-dimensional structure of the cytoplasmic domains of EpsF from the type 2 secretion system of Vibrio cholerae. Abendroth J, Mitchell DD, Korotkov KV, Johnson TL, Kreger A, Sandkvist M, Hol WG. J. Struct. Biol. 166 303-315 (2009)
  10. The crystal structure of a binary complex of two pseudopilins: EpsI and EpsJ from the type 2 secretion system of Vibrio vulnificus. Yanez ME, Korotkov KV, Abendroth J, Hol WG. J. Mol. Biol. 375 471-486 (2008)
  11. Structure of the minor pseudopilin EpsH from the Type 2 secretion system of Vibrio cholerae. Yanez ME, Korotkov KV, Abendroth J, Hol WG. J. Mol. Biol. 377 91-103 (2008)
  12. A 20-residue peptide of the inner membrane protein OutC mediates interaction with two distinct sites of the outer membrane secretin OutD and is essential for the functional type II secretion system in Erwinia chrysanthemi. Login FH, Fries M, Wang X, Pickersgill RW, Shevchik VE. Mol. Microbiol. 76 944-955 (2010)
  13. Acinetobacter baumannii Is Dependent on the Type II Secretion System and Its Substrate LipA for Lipid Utilization and In Vivo Fitness. Johnson TL, Waack U, Smith S, Mobley H, Sandkvist M. J. Bacteriol. 198 711-719 (2015)
  14. Crystal structure of Legionella DotD: insights into the relationship between type IVB and type II/III secretion systems. Nakano N, Kubori T, Kinoshita M, Imada K, Nagai H. PLoS Pathog. 6 e1001129 (2010)
  15. The dimer formed by the periplasmic domain of EpsL from the Type 2 Secretion System of Vibrio parahaemolyticus. Abendroth J, Kreger AC, Hol WG. J. Struct. Biol. 168 313-322 (2009)
  16. Cysteine scanning mutagenesis and disulfide mapping analysis of arrangement of GspC and GspD protomers within the type 2 secretion system. Wang X, Pineau C, Gu S, Guschinskaya N, Pickersgill RW, Shevchik VE. J. Biol. Chem. 287 19082-19093 (2012)
  17. Solution structure of homology region (HR) domain of type II secretion system. Gu S, Kelly G, Wang X, Frenkiel T, Shevchik VE, Pickersgill RW. J. Biol. Chem. 287 9072-9080 (2012)
  18. Dynamic interplay between the periplasmic and transmembrane domains of GspL and GspM in the type II secretion system. Lallemand M, Login FH, Guschinskaya N, Pineau C, Effantin G, Robert X, Shevchik VE. PLoS ONE 8 e79562 (2013)
  19. Substrate recognition by the bacterial type II secretion system: more than a simple interaction. Pineau C, Guschinskaya N, Robert X, Gouet P, Ballut L, Shevchik VE. Mol. Microbiol. 94 126-140 (2014)
  20. Functional characterization of EpsC, a component of the type II secretion system, in the pathogenicity of Vibrio vulnificus. Hwang W, Lee NY, Kim J, Lee MA, Kim KS, Lee KH, Park SJ. Infect. Immun. 79 4068-4080 (2011)
  21. A dodecameric ring-like structure of the N0 domain of the type II secretin from enterotoxigenic Escherichia coli. Korotkov KV, Delarosa JR, Hol WGJ. J. Struct. Biol. 183 354-362 (2013)
  22. Bacterial secretins form constitutively open pores akin to general porins. Disconzi E, Guilvout I, Chami M, Masi M, Huysmans GH, Pugsley AP, Bayan N. J. Bacteriol. 196 121-128 (2014)
  23. Species-specific functioning of the Pseudomonas XcpQ secretin: role for the C-terminal homology domain and lipopolysaccharide. Bitter W, van Boxtel R, Groeneweg M, Carballo PS, Zähringer U, Tommassen J, Koster M. J. Bacteriol. 189 2967-2975 (2007)
  24. Alterations in Peptidoglycan Cross-Linking Suppress the Secretin Assembly Defect Caused by Mutation of GspA in the Type II Secretion System. Vanderlinde EM, Strozen TG, Hernández SB, Cava F, Howard SP. J. Bacteriol. 199 (2017)
  25. Assessing the impact, genomics and evolution of type II secretion across a large, medically important genus: the Legionella type II secretion paradigm. White RC, Cianciotto NP. Microb Genom 5 (2019)
  26. Regulatory Effects of CsrA in Vibrio cholerae. Butz HA, Mey AR, Ciosek AL, Crofts AA, Davies BW, Payne SM. mBio 12 (2021)


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