PDBsum entry 1p9w

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Protein transport PDB id
Protein chain
384 a.a. *
Waters ×25
* Residue conservation analysis
PDB id:
Name: Protein transport
Title: Crystal structure of vibrio cholerae putative ntpase epse
Structure: General secretion pathway protein e. Chain: a. Fragment: n-terminal truncation of residues 1-90. Synonym: type ii traffic warden atpase, cholera toxin secretion protein epse. Engineered: yes
Source: Vibrio cholerae. Organism_taxid: 666. Gene: epse or vc2732. Expressed in: escherichia coli. Expression_system_taxid: 562.
2.70Å     R-factor:   0.238     R-free:   0.284
Authors: M.A.Robien,B.E.Krumm,M.Sandkvist,W.G.J.Hol
Key ref:
M.A.Robien et al. (2003). Crystal structure of the extracellular protein secretion NTPase EpsE of Vibrio cholerae. J Mol Biol, 333, 657-674. PubMed id: 14556751 DOI: 10.1016/j.jmb.2003.07.015
12-May-03     Release date:   14-Oct-03    
Go to PROCHECK summary

Protein chain
Pfam   ArchSchema ?
P37093  (GSPE_VIBCH) -  Type II secretion system protein E
503 a.a.
384 a.a.*
Key:    PfamA domain  PfamB domain  Secondary structure  CATH domain
* PDB and UniProt seqs differ at 2 residue positions (black crosses)

 Gene Ontology (GO) functional annotation 
  GO annot!
  Cellular component     type II protein secretion system complex   1 term 
  Biological process     transport   2 terms 
  Biochemical function     protein transporter activity     2 terms  


DOI no: 10.1016/j.jmb.2003.07.015 J Mol Biol 333:657-674 (2003)
PubMed id: 14556751  
Crystal structure of the extracellular protein secretion NTPase EpsE of Vibrio cholerae.
M.A.Robien, B.E.Krumm, M.Sandkvist, W.G.Hol.
Type II secretion systems consist of an assembly of 12-15 Gsp proteins responsible for transporting a variety of virulence factors across the outer membrane in several pathogenic bacteria. In Vibrio cholerae, the major virulence factor cholera toxin is secreted by the Eps Type II secretion apparatus consisting of 14 Eps proteins. One of these, EpsE, is a cytoplasmic putative NTPase essential for the functioning of the Eps system and member of the GspE subfamily of Type II secretion ATPases. The crystal structure of a truncated form of EpsE in nucleotide-liganded and unliganded state has been determined, and reveals a two-domain architecture with the four characteristic sequence "boxes" of the GspE subfamily clustering around the nucleotide-binding site of the C-domain. This domain contains two C-terminal subdomains not reported before in this superfamily of NTPases. One of these subdomains contains a four-cysteine motif that appears to be involved in metal binding as revealed by anomalous difference density. The EpsE subunits form a right-handed helical arrangement in the crystal with extensive and conserved contacts between the C and N domains of neighboring subunits. Combining the most conserved interface with the quaternary structure of the C domain in a distant homolog, a hexameric model for EpsE is proposed which may reflect the assembly of this critical protein in the Type II secretion system. The nucleotide ligand contacts both domains in this model. The N2-domain-containing surface of the hexamer appears to be highly conserved in the GspE family and most likely faces the inner membrane interacting with other members of the Eps system.
  Selected figure(s)  
Figure 6.
Figure 6. Superposition of EpsE with its homolog HP0525. (A) Superposition of the N2 domain (cyan) of EpsE and the N domain (light red) of the structure of HP0525. Dotted lines are shown in positions where the EpsE sequence could not be placed into electron density. (B) Superposition of the C domains of EpsE and the C domain (light red) of HP0525. The C1 domain of EpsE is dark blue, the C[M] domain yellow, and the C2 domain green. The position of ADP bound to HP0525 is red and the AMPPNP bound to EpsE is cyan. Dotted lines connect residues of the C[M] domain bridging residues 415-419 that were not modeled due to weak electron density. (C) Superposition of the experimental structure of EpsE ("open" configuration, dark blue), and the structure of HP0525 ("closed" configuration, light red). The C domains of the two structures are superimposed, in order to demonstrate the relative position of the corresponding N domains in the two proteins.
Figure 7.
Figure 7. Hexameric ring model of EpsE. (A) View from the proposed membrane-facing side (left), side view (middle) and the cytoplasmic face (right) of the hexameric ring model of EpsE constructed as described in the text. One monomer is shown with the domains colored as follows: N2, cyan; C1, dark blue; C[M], yellow; and C2, green. The other five monomers are colored in a lighter shade of the same colors. This Figure was prepared using GRASP[56.] and RASTER 3D. [55.] (B) Same views as in (A), but with the surface colored by sequence conservation.
  The above figures are reprinted by permission from Elsevier: J Mol Biol (2003, 333, 657-674) copyright 2003.  
  Figures were selected by an automated process.  

Literature references that cite this PDB file's key reference

  PubMed id Reference
22466878 K.V.Korotkov, M.Sandkvist, and W.G.Hol (2012).
The type II secretion system: biogenesis, molecular architecture and mechanism.
  Nat Rev Microbiol, 10, 336-351.  
21210168 I.Rose, G.Biuković, P.Aderhold, V.Müller, G.Grüber, and B.Averhoff (2011).
Identification and characterization of a unique, zinc-containing transport ATPase essential for natural transformation in Thermus thermophilus HB27.
  Extremophiles, 15, 191-202.  
21255118 M.D.Gray, M.Bagdasarian, W.G.Hol, and M.Sandkvist (2011).
In vivo cross-linking of EpsG to EpsL suggests a role for EpsL as an ATPase-pseudopilin coupling protein in the Type II secretion system of Vibrio cholerae.
  Mol Microbiol, 79, 786-798.  
20722599 M.Ayers, P.L.Howell, and L.L.Burrows (2010).
Architecture of the type II secretion and type IV pilus machineries.
  Future Microbiol, 5, 1203-1218.  
19646531 J.Abendroth, A.C.Kreger, and W.G.Hol (2009).
The dimer formed by the periplasmic domain of EpsL from the Type 2 Secretion System of Vibrio parahaemolyticus.
  J Struct Biol, 168, 313-322.
PDB code: 2w7v
19324092 J.Abendroth, D.D.Mitchell, K.V.Korotkov, T.L.Johnson, A.Kreger, M.Sandkvist, and W.G.Hol (2009).
The three-dimensional structure of the cytoplasmic domains of EpsF from the type 2 secretion system of Vibrio cholerae.
  J Struct Biol, 166, 303-315.
PDB codes: 2vma 2vmb 3c1q
18832308 F.Senf, J.Tommassen, and M.Koster (2008).
Polar secretion of proteins via the Xcp type II secretion system in Pseudomonas aeruginosa.
  Microbiology, 154, 3025-3032.  
18438417 K.V.Korotkov, and W.G.Hol (2008).
Structure of the GspK-GspI-GspJ complex from the enterotoxigenic Escherichia coli type 2 secretion system.
  Nat Struct Mol Biol, 15, 462-468.
PDB code: 3ci0
18249533 L.Craig, and J.Li (2008).
Type IV pili: paradoxes in form and function.
  Curr Opin Struct Biol, 18, 267-277.  
18022192 M.E.Yanez, K.V.Korotkov, J.Abendroth, and W.G.Hol (2008).
The crystal structure of a binary complex of two pseudopilins: EpsI and EpsJ from the type 2 secretion system of Vibrio vulnificus.
  J Mol Biol, 375, 471-486.
PDB code: 2ret
18241884 M.E.Yanez, K.V.Korotkov, J.Abendroth, and W.G.Hol (2008).
Structure of the minor pseudopilin EpsH from the Type 2 secretion system of Vibrio cholerae.
  J Mol Biol, 377, 91.
PDB code: 2qv8
18223089 V.Jakovljevic, S.Leonardy, M.Hoppert, and L.Søgaard-Andersen (2008).
PilB and PilT are ATPases acting antagonistically in type IV pilus function in Myxococcus xanthus.
  J Bacteriol, 190, 2411-2421.  
17255937 A.Yamagata, and J.A.Tainer (2007).
Hexameric structures of the archaeal secretion ATPase GspE and implications for a universal secretion mechanism.
  EMBO J, 26, 878-890.
PDB codes: 2oap 2oaq
17462024 B.Zolghadr, S.Weber, Z.Szabó, A.J.Driessen, and S.V.Albers (2007).
Identification of a system required for the functional surface localization of sugar binding proteins with class III signal peptides in Sulfolobus solfataricus.
  Mol Microbiol, 64, 795-806.  
17159897 J.L.Camberg, T.L.Johnson, M.Patrick, J.Abendroth, W.G.Hol, and M.Sandkvist (2007).
Synergistic stimulation of EpsE ATP hydrolysis by EpsL and acidic phospholipids.
  EMBO J, 26, 19-27.  
17355871 K.A.Satyshur, G.A.Worzalla, L.S.Meyer, E.K.Heiniger, K.G.Aukema, A.M.Misic, and K.T.Forest (2007).
Crystal structures of the pilus retraction motor PilT suggest large domain movements and subunit cooperation drive motility.
  Structure, 15, 363-376.
PDB codes: 2ewv 2eww 2eyu 2gsz
17172325 K.Nakasugi, R.Alexova, C.J.Svenson, and B.A.Neilan (2007).
Functional analysis of PilT from the toxic cyanobacterium Microcystis aeruginosa PCC 7806.
  J Bacteriol, 189, 1689-1697.  
17435791 M.Tomich, P.J.Planet, and D.H.Figurski (2007).
The tad locus: postcards from the widespread colonization island.
  Nat Rev Microbiol, 5, 363-375.  
17434972 S.A.Tripathi, and R.K.Taylor (2007).
Membrane association and multimerization of TcpT, the cognate ATPase ortholog of the Vibrio cholerae toxin-coregulated-pilus biogenesis apparatus.
  J Bacteriol, 189, 4401-4409.  
17630971 S.J.Shiue, I.L.Chien, N.L.Chan, W.M.Leu, and N.T.Hu (2007).
Mutation of a key residue in the type II secretion system ATPase uncouples ATP hydrolysis from protein translocation.
  Mol Microbiol, 65, 401-412.  
17355860 S.N.Savvides (2007).
Secretion superfamily ATPases swing big.
  Structure, 15, 255-257.  
17623846 T.Prakash, K.S.Sandhu, N.K.Singh, Y.Bhasin, C.Ramakrishnan, and S.K.Brahmachari (2007).
Structural assessment of glycyl mutations in invariantly conserved motifs.
  Proteins, 69, 617-632.  
16956883 F.H.Login, and V.E.Shevchik (2006).
The single transmembrane segment drives self-assembly of OutC and the formation of a functional type II secretion system in Erwinia chrysanthemi.
  J Biol Chem, 281, 33152-33162.  
16172129 R.F.Collins, K.Beis, B.R.Clarke, R.C.Ford, M.Hulley, J.H.Naismith, and C.Whitfield (2006).
Periplasmic protein-protein contacts in the inner membrane protein Wzc form a tetrameric complex required for the assembly of Escherichia coli group 1 capsules.
  J Biol Chem, 281, 2144-2150.  
16525507 S.J.Shiue, K.M.Kao, W.M.Leu, L.Y.Chen, N.L.Chan, and N.T.Hu (2006).
XpsE oligomerization triggered by ATP binding, not hydrolysis, leads to its association with XpsL.
  EMBO J, 25, 1426-1435.  
16420372 S.P.Howard, C.Gebhart, G.R.Langen, G.Li, and T.G.Strozen (2006).
Interactions between peptidoglycan and the ExeAB complex during assembly of the type II secretin of Aeromonas hydrophila.
  Mol Microbiol, 59, 1062-1072.  
16448494 T.L.Johnson, J.Abendroth, W.G.Hol, and M.Sandkvist (2006).
Type II secretion: from structure to function.
  FEMS Microbiol Lett, 255, 175-186.  
15948950 J.A.Sexton, H.J.Yeo, and J.P.Vogel (2005).
Genetic analysis of the Legionella pneumophila DotB ATPase reveals a role in type IV secretion system protein export.
  Mol Microbiol, 57, 70-84.  
15601709 J.L.Camberg, and M.Sandkvist (2005).
Molecular analysis of the Vibrio cholerae type II secretion ATPase EpsE.
  J Bacteriol, 187, 249-256.  
15629932 K.G.Aukema, E.M.Kron, T.J.Herdendorf, and K.T.Forest (2005).
Functional dissection of a conserved motif within the pilus retraction protein PilT.
  J Bacteriol, 187, 611-618.  
16091031 L.L.Burrows (2005).
Weapons of mass retraction.
  Mol Microbiol, 57, 878-888.  
15659660 P.Chiang, M.Habash, and L.L.Burrows (2005).
Disparate subcellular localization patterns of Pseudomonas aeruginosa Type IV pilus ATPases involved in twitching motility.
  J Bacteriol, 187, 829-839.  
16153176 P.J.Christie, K.Atmakuri, V.Krishnamoorthy, S.Jakubowski, and E.Cascales (2005).
Biogenesis, architecture, and function of bacterial type IV secretion systems.
  Annu Rev Microbiol, 59, 451-485.  
16162504 Y.Chen, S.J.Shiue, C.W.Huang, J.L.Chang, Y.L.Chien, N.T.Hu, and N.L.Chan (2005).
Structure and function of the XpsE N-terminal domain, an essential component of the Xanthomonas campestris type II secretion system.
  J Biol Chem, 280, 42356-42363.
PDB codes: 2d27 2d28
15103158 K.T.Forest, K.A.Satyshur, G.A.Worzalla, J.K.Hansen, and T.J.Herdendorf (2004).
The pilus-retraction protein PilT: ultrastructure of the biological assembly.
  Acta Crystallogr D Biol Crystallogr, 60, 978-982.  
The most recent references are shown first. Citation data come partly from CiteXplore and partly from an automated harvesting procedure. Note that this is likely to be only a partial list as not all journals are covered by either method. However, we are continually building up the citation data so more and more references will be included with time. Where a reference describes a PDB structure, the PDB code is shown on the right.