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Membrane protein
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PDB id
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1uyo
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Contents |
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* Residue conservation analysis
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DOI no:
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EMBO J
23:1257-1266
(2004)
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PubMed id:
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Structure of the translocator domain of a bacterial autotransporter.
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C.J.Oomen,
P.van Ulsen,
P.van Gelder,
M.Feijen,
J.Tommassen,
P.Gros.
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ABSTRACT
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Autotransporters are virulence-related proteins of Gram-negative bacteria that
are secreted via an outer-membrane-based C-terminal extension, the translocator
domain. This domain supposedly is sufficient for the transport of the N-terminal
passenger domain across the outer membrane. We present here the crystal
structure of the in vitro-folded translocator domain of the autotransporter NalP
from Neisseria meningitidis, which reveals a 12-stranded beta-barrel with a
hydrophilic pore of 10 x 12.5 A that is filled by an N-terminal alpha-helix. The
domain has pore activity in vivo and in vitro. Our data are consistent with the
model of passenger-domain transport through the hydrophilic channel within the
beta-barrel, and inconsistent with a model for transport through a central
channel formed by an oligomer of translocator domains. However, the dimensions
of the pore imply translocation of the secreted domain in an unfolded form. An
alternative model, possibly covering the transport of folded domains, is that
passenger-domain transport involves the Omp85 complex, the machinery required
for membrane insertion of outer-membrane proteins, on which autotransporters are
dependent.
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Selected figure(s)
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Figure 2.
Figure 2 Recording of NalP[  ]pores
formed in planar lipid bilayers at an applied potential of 100
mV. The recordings show conductance steps of 1.3 nS (open
arrowhead) and 0.15 nS (filled arrowhead). The horizontal
arrowhead shows the zero-conductance level.
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Figure 4.
Figure 4 Crystal structure of NalP[ ].
(A) Side view of NalP[ ]in
space group P6[1]22 shows a 12-stranded  -barrel
(blue ribbon representation) with a shear number of 14. The
hydrophobic membrane-embedded region is flanked by aromatic
residues (yellow ball-and-stick). The periplasmic side is
characterised by short turns (T0 -T5) and the extracellular side
by longer loops (L1 -L6) connecting the alternating -strands.
An  -helical
'plug' (red ribbon representation) is connected to the barrel
via T0 and positions the N-terminus of the translocator domain
(Ala 786) at the extracellular side. (B) Schematic
representation of the mixed character of the -helix
and its interactions with the -barrel
wall with the -helical
residues depicted on a helical wheel. Colour coding: positively
charged residues in blue, negatively charged residues in red,
hydrophilic residues in green and nonpolar residues in orange.
The distances between charged groups of the helix and the barrel
wall are indicated in Å. (C) Stereo top view of the NalP[ ]-barrel
in the same orientation as in (B). The barrel interior is highly
hydrophilic due to the presence of many charged amino acids
(ball-and-stick representation). (D) Topology model of NalP[
];
residues pointing outwards from the -barrel
are indicated in grey. Amino acids in -strands
are indicated as squares, in -helix
as hexagons and in loops as circles. Amino acids not visible in
the electron density of space group P6[1]22 are indicated in
blue.
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The above figures are
reprinted
from an Open Access publication published by Macmillan Publishers Ltd:
EMBO J
(2004,
23,
1257-1266)
copyright 2004.
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Figures were
selected
by the author.
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Literature references that cite this PDB file's key reference
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PubMed id
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Reference
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V.Karuppiah,
J.L.Berry,
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| |
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Channel properties of the translocator domain of the autotransporter Hbp of Escherichia coli.
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| |
Mol Membr Biol, 28,
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Y.Zhai,
K.Zhang,
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A.W.Roszak,
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and
F.Sun
(2011).
Autotransporter passenger domain secretion requires a hydrophobic cavity at the extracellular entrance of the β-domain pore.
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| |
Biochem J, 435,
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PDB code:
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C.Kim,
J.Basner,
and
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| |
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Secretion of a bacterial virulence factor is driven by the folding of a C-terminal segment.
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| |
Proc Natl Acad Sci U S A, 107,
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K.Nishimura,
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Autotransporter passenger proteins: virulence factors with common structural themes.
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UpaH is a newly identified autotransporter protein that contributes to biofilm formation and bladder colonization by uropathogenic Escherichia coli CFT073.
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| |
Infect Immun, 78,
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|
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| |
Trends Biochem Sci, 35,
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T.C.Freeman,
and
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|
| |
Bioinformatics, 26,
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C-terminal amino acid residues of the trimeric autotransporter adhesin YadA of Yersinia enterocolitica are decisive for its recognition and assembly by BamA.
|
| |
Mol Microbiol, 78,
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| |
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|
| |
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| |
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and
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Contribution of the periplasmic chaperone Skp to efficient presentation of the autotransporter IcsA on the surface of Shigella flexneri.
|
| |
J Bacteriol, 191,
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|
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K.A.Swanson,
L.D.Taylor,
S.D.Frank,
G.L.Sturdevant,
E.R.Fischer,
J.H.Carlson,
W.M.Whitmire,
and
H.D.Caldwell
(2009).
Chlamydia trachomatis polymorphic membrane protein D is an oligomeric autotransporter with a higher-order structure.
|
| |
Infect Immun, 77,
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M.E.Charbonneau,
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and
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M.Junker,
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and
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Vectorial transport and folding of an autotransporter virulence protein during outer membrane secretion.
|
| |
Mol Microbiol, 71,
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|
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|
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R.Ieva,
and
H.D.Bernstein
(2009).
Interaction of an autotransporter passenger domain with BamA during its translocation across the bacterial outer membrane.
|
| |
Proc Natl Acad Sci U S A, 106,
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|
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|
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T.A.Johnson,
J.Qiu,
A.G.Plaut,
and
T.Holyoak
(2009).
Active-site gating regulates substrate selectivity in a chymotrypsin-like serine protease the structure of haemophilus influenzae immunoglobulin A1 protease.
|
| |
J Mol Biol, 389,
559-574.
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PDB code:
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Y.H.Hu,
C.S.Liu,
J.H.Hou,
and
L.Sun
(2009).
Identification, characterization, and molecular application of a virulence-associated autotransporter from a pathogenic Pseudomonas fluorescens strain.
|
| |
Appl Environ Microbiol, 75,
4333-4340.
|
|
|
|
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|
|
C.Li,
Y.Zhu,
I.Benz,
M.A.Schmidt,
W.Chen,
A.Mulchandani,
and
C.Qiao
(2008).
Presentation of functional organophosphorus hydrolase fusions on the surface of Escherichia coli by the AIDA-I autotransporter pathway.
|
| |
Biotechnol Bioeng, 99,
485-490.
|
|
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|
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E.Yamashita,
M.V.Zhalnina,
S.D.Zakharov,
O.Sharma,
and
W.A.Cramer
(2008).
Crystal structures of the OmpF porin: function in a colicin translocon.
|
| |
EMBO J, 27,
2171-2180.
|
|
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PDB codes:
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|
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G.Duret,
M.Szymanski,
K.J.Choi,
H.J.Yeo,
and
A.H.Delcour
(2008).
The TpsB translocator HMW1B of haemophilus influenzae forms a large conductance channel.
|
| |
J Biol Chem, 283,
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|
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|
|
G.Meng,
J.W.St Geme,
and
G.Waksman
(2008).
Repetitive architecture of the Haemophilus influenzae Hia trimeric autotransporter.
|
| |
J Mol Biol, 384,
824-836.
|
|
|
PDB codes:
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|
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|
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J.P.Renn,
and
P.L.Clark
(2008).
A conserved stable core structure in the passenger domain beta-helix of autotransporter virulence proteins.
|
| |
Biopolymers, 89,
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|
|
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|
M.J.Brooks,
J.L.Sedillo,
N.Wagner,
C.A.Laurence,
W.Wang,
A.S.Attia,
E.J.Hansen,
and
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(2008).
Modular arrangement of allelic variants explains the divergence in Moraxella catarrhalis UspA protein function.
|
| |
Infect Immun, 76,
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|
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|
|
N.Ackermann,
M.Tiller,
G.Anding,
A.Roggenkamp,
and
J.Heesemann
(2008).
Contribution of trimeric autotransporter C-terminal domains of oligomeric coiled-coil adhesin (Oca) family members YadA, UspA1, EibA, and Hia to translocation of the YadA passenger domain and virulence of Yersinia enterocolitica.
|
| |
J Bacteriol, 190,
5031-5043.
|
|
|
|
|
|
|
R.Conners,
D.J.Hill,
E.Borodina,
C.Agnew,
S.J.Daniell,
N.M.Burton,
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A.R.Clarke,
L.E.Catto,
D.Lammie,
T.Wess,
R.L.Brady,
and
M.Virji
(2008).
The Moraxella adhesin UspA1 binds to its human CEACAM1 receptor by a deformable trimeric coiled-coil.
|
| |
EMBO J, 27,
1779-1789.
|
|
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PDB code:
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|
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T.C.Hoopman,
W.Wang,
C.A.Brautigam,
J.L.Sedillo,
T.J.Reilly,
and
E.J.Hansen
(2008).
Moraxella catarrhalis synthesizes an autotransporter that is an acid phosphatase.
|
| |
J Bacteriol, 190,
1459-1472.
|
|
|
|
|
|
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X.Gatsos,
A.J.Perry,
K.Anwari,
P.Dolezal,
P.P.Wolynec,
V.A.Likić,
A.W.Purcell,
S.K.Buchanan,
and
T.Lithgow
(2008).
Protein secretion and outer membrane assembly in Alphaproteobacteria.
|
| |
FEMS Microbiol Rev, 32,
995.
|
|
|
|
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|
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Y.T.Yen,
M.Kostakioti,
I.R.Henderson,
and
C.Stathopoulos
(2008).
Common themes and variations in serine protease autotransporters.
|
| |
Trends Microbiol, 16,
370-379.
|
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|
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|
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A.M.Abdallah,
N.C.Gey van Pittius,
P.A.Champion,
J.Cox,
J.Luirink,
C.M.Vandenbroucke-Grauls,
B.J.Appelmelk,
and
W.Bitter
(2007).
Type VII secretion--mycobacteria show the way.
|
| |
Nat Rev Microbiol, 5,
883-891.
|
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|
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|
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B.Clantin,
A.S.Delattre,
P.Rucktooa,
N.Saint,
A.C.Méli,
C.Locht,
F.Jacob-Dubuisson,
and
V.Villeret
(2007).
Structure of the membrane protein FhaC: a member of the Omp85-TpsB transporter superfamily.
|
| |
Science, 317,
957-961.
|
|
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PDB code:
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|
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C.M.Litwin,
M.L.Rawlins,
and
E.M.Swenson
(2007).
Characterization of an immunogenic outer membrane autotransporter protein, Arp, of Bartonella henselae.
|
| |
Infect Immun, 75,
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|
|
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|
|
|
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C.Tükel,
M.Akçelik,
M.F.de Jong,
O.Simsek,
R.M.Tsolis,
and
A.J.Bäumler
(2007).
MarT activates expression of the MisL autotransporter protein of Salmonella enterica serotype Typhimurium.
|
| |
J Bacteriol, 189,
3922-3926.
|
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J.Jose,
and
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(2007).
The autodisplay story, from discovery to biotechnical and biomedical applications.
|
| |
Microbiol Mol Biol Rev, 71,
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J.M.Davis,
L.K.Tsou,
and
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(2007).
Synthetic non-peptide mimetics of alpha-helices.
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| |
Chem Soc Rev, 36,
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L.Lin,
H.Nakano,
S.Nakamura,
S.Uchiyama,
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Y.Kobayashi,
T.Ohkubo,
and
K.Fukui
(2007).
Crystal structure of Pyrococcus horikoshii PPC protein at 1.60 A resolution.
|
| |
Proteins, 67,
505-507.
|
|
|
PDB code:
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|
|
|
|
|
|
N.Dautin,
and
H.D.Bernstein
(2007).
Protein secretion in gram-negative bacteria via the autotransporter pathway.
|
| |
Annu Rev Microbiol, 61,
89.
|
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|
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N.Dautin,
T.J.Barnard,
D.E.Anderson,
and
H.D.Bernstein
(2007).
Cleavage of a bacterial autotransporter by an evolutionarily convergent autocatalytic mechanism.
|
| |
EMBO J, 26,
1942-1952.
|
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S.Da Re,
B.Le Quéré,
J.M.Ghigo,
and
C.Beloin
(2007).
Tight modulation of Escherichia coli bacterial biofilm formation through controlled expression of adhesion factors.
|
| |
Appl Environ Microbiol, 73,
3391-3403.
|
|
|
|
|
|
|
S.L.Lipski,
C.Akimana,
J.M.Timpe,
R.M.Wooten,
and
E.R.Lafontaine
(2007).
The Moraxella catarrhalis autotransporter McaP is a conserved surface protein that mediates adherence to human epithelial cells through its N-terminal passenger domain.
|
| |
Infect Immun, 75,
314-324.
|
|
|
|
|
|
|
S.Vitovski,
and
J.R.Sayers
(2007).
Relaxed cleavage specificity of an immunoglobulin A1 protease from Neisseria meningitidis.
|
| |
Infect Immun, 75,
2875-2885.
|
|
|
|
|
|
|
S.Wilhelm,
F.Rosenau,
S.Becker,
S.Buest,
S.Hausmann,
H.Kolmar,
and
K.E.Jaeger
(2007).
Functional cell-surface display of a lipase-specific chaperone.
|
| |
Chembiochem, 8,
55-60.
|
|
|
|
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|
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T.J.Barnard,
N.Dautin,
P.Lukacik,
H.D.Bernstein,
and
S.K.Buchanan
(2007).
Autotransporter structure reveals intra-barrel cleavage followed by conformational changes.
|
| |
Nat Struct Mol Biol, 14,
1214-1220.
|
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PDB code:
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U.Grosskinsky,
M.Schütz,
M.Fritz,
Y.Schmid,
M.C.Lamparter,
P.Szczesny,
A.N.Lupas,
I.B.Autenrieth,
and
D.Linke
(2007).
A conserved glycine residue of trimeric autotransporter domains plays a key role in Yersinia adhesin A autotransport.
|
| |
J Bacteriol, 189,
9011-9019.
|
|
|
|
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|
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W.S.Jong,
C.M.ten Hagen-Jongman,
T.den Blaauwen,
D.J.Slotboom,
J.R.Tame,
D.Wickström,
J.W.de Gier,
B.R.Otto,
and
J.Luirink
(2007).
Limited tolerance towards folded elements during secretion of the autotransporter Hbp.
|
| |
Mol Microbiol, 63,
1524-1536.
|
|
|
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|
|
Y.Zhu,
I.Black,
A.W.Roszak,
and
N.W.Isaacs
(2007).
Crystallization and preliminary X-ray diffraction analysis of P30, the transmembrane domain of pertactin, an autotransporter from Bordetella pertussis.
|
| |
Acta Crystallogr Sect F Struct Biol Cryst Commun, 63,
593-595.
|
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|
|
A.Economou,
P.J.Christie,
R.C.Fernandez,
T.Palmer,
G.V.Plano,
and
A.P.Pugsley
(2006).
Secretion by numbers: Protein traffic in prokaryotes.
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PDB code:
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PDB code:
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Citation data come partly from CiteXplore and partly
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so more and more references will be included with time.
Where a reference describes a PDB structure, the PDB
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