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Transport protein
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PDB id
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2a65
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* Residue conservation analysis
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Gene Ontology (GO) functional annotation
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Cellular component
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integral to membrane
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1 term
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Biological process
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transport
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2 terms
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Biochemical function
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symporter activity
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2 terms
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DOI no:
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Nature
437:215-223
(2005)
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PubMed id:
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Crystal structure of a bacterial homologue of Na+/Cl--dependent neurotransmitter transporters.
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A.Yamashita,
S.K.Singh,
T.Kawate,
Y.Jin,
E.Gouaux.
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ABSTRACT
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Na+/Cl--dependent transporters terminate synaptic transmission by using
electrochemical gradients to drive the uptake of neurotransmitters, including
the biogenic amines, from the synapse to the cytoplasm of neurons and glia.
These transporters are the targets of therapeutic and illicit compounds, and
their dysfunction has been implicated in multiple diseases of the nervous
system. Here we present the crystal structure of a bacterial homologue of these
transporters from Aquifex aeolicus, in complex with its substrate, leucine, and
two sodium ions. The protein core consists of the first ten of twelve
transmembrane segments, with segments 1-5 related to 6-10 by a pseudo-two-fold
axis in the membrane plane. Leucine and the sodium ions are bound within the
protein core, halfway across the membrane bilayer, in an occluded site devoid of
water. The leucine and ion binding sites are defined by partially unwound
transmembrane helices, with main-chain atoms and helix dipoles having key roles
in substrate and ion binding. The structure reveals the architecture of this
important class of transporter, illuminates the determinants of substrate
binding and ion selectivity, and defines the external and internal gates.
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Selected figure(s)
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Figure 5.
Figure 5: Extracellular and cytoplasmic gates. a, Slice
through the surface of LeuT[Aa], viewed parallel to the
membrane, showing the extracellular cavity. Connolly surface of
LeuT[Aa] is shown in beige. l-Leucine, Tyr 108, Phe 253 and the
two charged pairs (Arg 30 -Asp 404 and Arg 5 -Asp 369) are
depicted as stick models in yellow for leucine, purple for
aromatic residues, blue for arginines and red for aspartates. b,
c, Key interacting residues at the extracellular (b) and at the
cytoplasmic (c) gate.
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Figure 6.
Figure 6: Speculative transport mechanism. Schematic drawing
of a possible conformational change upon substrate/sodium ion
transport. The left panel shows the outward-facing state. TM1a
and TM6b assume the closed arrangement, whereas TM1b and TM6a
adopt the open one. The middle panel shows the
substrate-occluded state, which corresponds to the current
crystal structure. TM1a and TM6b assume the closed arrangement,
whereas TM1b and TM6a adopt a partially open one with some
residues blocking the permeation pathway. The right panel shows
the inward-facing state. TM1b and TM6a assume the closed
arrangement, whereas TM1a and TM6b adopt the closed one, to open
the pathway to the cytoplasm.
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The above figures are
reprinted
by permission from Macmillan Publishers Ltd:
Nature
(2005,
437,
215-223)
copyright 2005.
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Figures were
selected
by an automated process.
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Literature references that cite this PDB file's key reference
|
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| |
PubMed id
|
|
Reference
|
|
|
|
|
|
A.Narayanan,
M.Ridilla,
and
D.A.Yernool
(2011).
Restrained expression, a method to overproduce toxic membrane proteins by exploiting operator-repressor interactions.
|
| |
Protein Sci, 20,
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|
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|
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|
|
B.J.Thompson,
T.Jessen,
L.K.Henry,
J.R.Field,
K.L.Gamble,
P.J.Gresch,
A.M.Carneiro,
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L.C.Daws,
and
R.D.Blakely
(2011).
Transgenic elimination of high-affinity antidepressant and cocaine sensitivity in the presynaptic serotonin transporter.
|
| |
Proc Natl Acad Sci U S A, 108,
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|
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|
|
C.Mulligan,
M.Fischer,
and
G.H.Thomas
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Tripartite ATP-independent periplasmic (TRAP) transporters in bacteria and archaea.
|
| |
FEMS Microbiol Rev, 35,
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|
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C.Perez,
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and
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(2011).
Substrate specificity and ion coupling in the Na+/betaine symporter BetP.
|
| |
EMBO J, 30,
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|
|
|
PDB code:
|
|
|
|
|
|
|
|
F.Lu,
S.Li,
Y.Jiang,
J.Jiang,
H.Fan,
G.Lu,
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S.Dang,
X.Zhang,
J.Wang,
and
N.Yan
(2011).
Structure and mechanism of the uracil transporter UraA.
|
| |
Nature, 472,
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|
|
|
PDB code:
|
|
|
|
|
|
|
|
H.Bisgaard,
M.A.Larsen,
S.Mazier,
T.Beuming,
A.H.Newman,
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L.Shi,
C.J.Loland,
and
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The binding sites for benztropines and dopamine in the dopamine transporter overlap.
|
| |
Neuropharmacology, 60,
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|
|
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|
|
|
J.DeChancie,
I.H.Shrivastava,
and
I.Bahar
(2011).
The mechanism of substrate release by the aspartate transporter GltPh: insights from simulations.
|
| |
Mol Biosyst, 7,
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|
|
|
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|
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|
K.Illergård,
A.Kauko,
and
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Why are polar residues within the membrane core evolutionary conserved?
|
| |
Proteins, 79,
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|
|
|
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|
|
L.Kowalczyk,
M.Ratera,
A.Paladino,
P.Bartoccioni,
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M.Orozco,
X.Carpena,
J.L.Vázquez-Ibar,
and
M.Palacín
(2011).
Molecular basis of substrate-induced permeation by an amino acid antiporter.
|
| |
Proc Natl Acad Sci U S A, 108,
3935-3940.
|
|
|
PDB code:
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|
|
|
|
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|
|
M.Ihara,
N.Matsuura,
and
A.Yamashita
(2011).
High-resolution Native-PAGE for membrane proteins capable of fluorescence detection and hydrodynamic state evaluation.
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| |
Anal Biochem, 412,
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|
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|
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|
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|
S.Weyand,
T.Shimamura,
O.Beckstein,
M.S.Sansom,
S.Iwata,
P.J.Henderson,
and
A.D.Cameron
(2011).
The alternating access mechanism of transport as observed in the sodium-hydantoin transporter Mhp1.
|
| |
J Synchrotron Radiat, 18,
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|
|
|
|
|
|
|
T.Steinkellner,
M.Freissmuth,
H.H.Sitte,
and
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The ugly side of amphetamines: short- and long-term toxicity of 3,4-methylenedioxymethamphetamine (MDMA, 'Ecstasy'), methamphetamine and D-amphetamine.
|
| |
Biol Chem, 392,
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|
|
|
|
|
|
|
Y.Cao,
X.Jin,
E.J.Levin,
H.Huang,
Y.Zong,
M.Quick,
J.Weng,
Y.Pan,
J.Love,
M.Punta,
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W.A.Hendrickson,
J.A.Javitch,
K.R.Rajashankar,
and
M.Zhou
(2011).
Crystal structure of a phosphorylation-coupled saccharide transporter.
|
| |
Nature, 473,
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|
|
|
PDB code:
|
|
|
|
|
|
|
|
Y.Zhao,
D.S.Terry,
L.Shi,
M.Quick,
H.Weinstein,
S.C.Blanchard,
and
J.A.Javitch
(2011).
Substrate-modulated gating dynamics in a Na+-coupled neurotransmitter transporter homologue.
|
| |
Nature, 474,
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|
|
|
|
|
|
|
Z.Zhang,
C.B.Zander,
and
C.Grewer
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The C-terminal domain of the neutral amino acid transporter SNAT2 regulates transport activity through voltage-dependent processes.
|
| |
Biochem J, 434,
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|
|
|
|
|
|
|
A.Nyola,
N.K.Karpowich,
J.Zhen,
J.Marden,
M.E.Reith,
and
D.N.Wang
(2010).
Substrate and drug binding sites in LeuT.
|
| |
Curr Opin Struct Biol, 20,
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|
|
|
|
|
|
|
A.Schlessinger,
P.Matsson,
J.E.Shima,
U.Pieper,
S.W.Yee,
L.Kelly,
L.Apeltsin,
R.M.Stroud,
T.E.Ferrin,
K.M.Giacomini,
and
A.Sali
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Comparison of human solute carriers.
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| |
Protein Sci, 19,
412-428.
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|
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|
|
|
|
A.Watanabe,
S.Choe,
V.Chaptal,
J.M.Rosenberg,
E.M.Wright,
M.Grabe,
and
J.Abramson
(2010).
The mechanism of sodium and substrate release from the binding pocket of vSGLT.
|
| |
Nature, 468,
988-991.
|
|
|
PDB code:
|
|
|
|
|
|
|
|
B.Annamalai,
P.Mannangatti,
O.Arapulisamy,
S.Ramamoorthy,
and
L.D.Jayanthi
(2010).
Involvement of threonine 258 and serine 259 motif in amphetamine-induced norepinephrine transporter endocytosis.
|
| |
J Neurochem, 115,
23-35.
|
|
|
|
|
|
|
B.P.Pedersen,
J.P.Morth,
and
P.Nissen
(2010).
Structure determination using poorly diffracting membrane-protein crystals: the H+-ATPase and Na+,K+-ATPase case history.
|
| |
Acta Crystallogr D Biol Crystallogr, 66,
309-313.
|
|
|
|
|
|
|
C.J.Tsai,
and
C.Ziegler
(2010).
Coupling electron cryomicroscopy and X-ray crystallography to understand secondary active transport.
|
| |
Curr Opin Struct Biol, 20,
448-455.
|
|
|
|
|
|
|
C.L.Piscitelli,
H.Krishnamurthy,
and
E.Gouaux
(2010).
Neurotransmitter/sodium symporter orthologue LeuT has a single high-affinity substrate site.
|
| |
Nature, 468,
1129-1132.
|
|
|
|
|
|
|
C.M.Anderson,
P.D.Kidd,
and
S.Eskandari
(2010).
GATMD: γ-aminobutyric acid transporter mutagenesis database.
|
| |
Database (Oxford), 2010,
baq028.
|
|
|
|
|
|
|
C.S.Arendt,
and
B.Ullman
(2010).
Role of transmembrane domain 4 in ligand permeation by Crithidia fasciculata equilibrative nucleoside transporter 2 (CfNT2).
|
| |
J Biol Chem, 285,
6024-6035.
|
|
|
|
|
|
|
C.S.Watson,
R.A.Alyea,
K.A.Cunningham,
and
Y.J.Jeng
(2010).
Estrogens of multiple classes and their role in mental health disease mechanisms.
|
| |
Int J Womens Health, 2,
153-166.
|
|
|
|
|
|
|
C.Sogawa,
C.Mitsuhata,
K.Kumagai-Morioka,
N.Sogawa,
K.Ohyama,
K.Morita,
K.Kozai,
T.Dohi,
and
S.Kitayama
(2010).
Expression and function of variants of human catecholamine transporters lacking the fifth transmembrane region encoded by exon 6.
|
| |
PLoS One, 5,
e11945.
|
|
|
|
|
|
|
D.P.Claxton,
M.Quick,
L.Shi,
F.D.de Carvalho,
H.Weinstein,
J.A.Javitch,
and
H.S.McHaourab
(2010).
Ion/substrate-dependent conformational dynamics of a bacterial homolog of neurotransmitter:sodium symporters.
|
| |
Nat Struct Mol Biol, 17,
822-829.
|
|
|
|
|
|
|
E.Gorraitz,
M.Pastor-Anglada,
and
M.P.Lostao
(2010).
Effects of Na+ and H+ on steady-state and presteady-state currents of the human concentrative nucleoside transporter 3 (hCNT3).
|
| |
Pflugers Arch, 460,
617-632.
|
|
|
|
|
|
|
E.R.Kunji,
and
A.J.Robinson
(2010).
Coupling of proton and substrate translocation in the transport cycle of mitochondrial carriers.
|
| |
Curr Opin Struct Biol, 20,
440-447.
|
|
|
|
|
|
|
E.Zomot,
and
I.Bahar
(2010).
The sodium/galactose symporter crystal structure is a dynamic, not so occluded state.
|
| |
Mol Biosyst, 6,
1040-1046.
|
|
|
|
|
|
|
G.Christie,
H.Götzke,
and
C.R.Lowe
(2010).
Identification of a receptor subunit and putative ligand-binding residues involved in the Bacillus megaterium QM B1551 spore germination response to glucose.
|
| |
J Bacteriol, 192,
4317-4326.
|
|
|
|
|
|
|
H.H.Sitte,
and
M.Freissmuth
(2010).
The reverse operation of Na(+)/Cl(-)-coupled neurotransmitter transporters--why amphetamines take two to tango.
|
| |
J Neurochem, 112,
340-355.
|
|
|
|
|
|
|
H.P.Larsson,
X.Wang,
B.Lev,
I.Baconguis,
D.A.Caplan,
N.P.Vyleta,
H.P.Koch,
A.Diez-Sampedro,
and
S.Y.Noskov
(2010).
Evidence for a third sodium-binding site in glutamate transporters suggests an ion/substrate coupling model.
|
| |
Proc Natl Acad Sci U S A, 107,
13912-13917.
|
|
|
|
|
|
|
H.W.van Veen
(2010).
Structural biology: Last of the multidrug transporters.
|
| |
Nature, 467,
926-927.
|
|
|
|
|
|
|
H.Yu,
S.Y.Noskov,
and
B.Roux
(2010).
Two mechanisms of ion selectivity in protein binding sites.
|
| |
Proc Natl Acad Sci U S A, 107,
20329-20334.
|
|
|
|
|
|
|
J.A.Lundbaek,
S.A.Collingwood,
H.I.Ingólfsson,
R.Kapoor,
and
O.S.Andersen
(2010).
Lipid bilayer regulation of membrane protein function: gramicidin channels as molecular force probes.
|
| |
J R Soc Interface, 7,
373-395.
|
|
|
|
|
|
|
J.Andersen,
L.Olsen,
K.B.Hansen,
O.Taboureau,
F.S.Jørgensen,
A.M.Jørgensen,
B.Bang-Andersen,
J.Egebjerg,
K.Strømgaard,
and
A.S.Kristensen
(2010).
Mutational mapping and modeling of the binding site for (S)-citalopram in the human serotonin transporter.
|
| |
J Biol Chem, 285,
2051-2063.
|
|
|
|
|
|
|
J.Chillarón,
M.Font-Llitjós,
J.Fort,
A.Zorzano,
D.S.Goldfarb,
V.Nunes,
and
M.Palacín
(2010).
Pathophysiology and treatment of cystinuria.
|
| |
Nat Rev Nephrol, 6,
424-434.
|
|
|
|
|
|
|
J.Eriksen,
T.N.Jørgensen,
and
U.Gether
(2010).
Regulation of dopamine transporter function by protein-protein interactions: new discoveries and methodological challenges.
|
| |
J Neurochem, 113,
27-41.
|
|
|
|
|
|
|
K.C.Schmitt,
S.Mamidyala,
S.Biswas,
A.K.Dutta,
and
M.E.Reith
(2010).
Bivalent phenethylamines as novel dopamine transporter inhibitors: evidence for multiple substrate-binding sites in a single transporter.
|
| |
J Neurochem, 112,
1605-1618.
|
|
|
|
|
|
|
K.Karhumaa,
B.Wu,
and
M.C.Kielland-Brandt
(2010).
Conditions with high intracellular glucose inhibit sensing through glucose sensor Snf3 in Saccharomyces cerevisiae.
|
| |
J Cell Biochem, 110,
920-925.
|
|
|
|
|
|
|
K.McLuskey,
A.W.Roszak,
Y.Zhu,
and
N.W.Isaacs
(2010).
Crystal structures of all-alpha type membrane proteins.
|
| |
Eur Biophys J, 39,
723-755.
|
|
|
|
|
|
|
K.R.Vinothkumar,
and
R.Henderson
(2010).
Structures of membrane proteins.
|
| |
Q Rev Biophys, 43,
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|
|
|
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|
|
K.W.Kaufmann,
G.H.Lemmon,
S.L.Deluca,
J.H.Sheehan,
and
J.Meiler
(2010).
Practically useful: what the Rosetta protein modeling suite can do for you.
|
| |
Biochemistry, 49,
2987-2998.
|
|
|
|
|
|
|
L.Ruiz-Pavón,
P.M.Karlsson,
J.Carlsson,
D.Samyn,
B.Persson,
B.L.Persson,
and
C.Spetea
(2010).
Functionally important amino acids in the Arabidopsis thylakoid phosphate transporter: homology modeling and site-directed mutagenesis.
|
| |
Biochemistry, 49,
6430-6439.
|
|
|
|
|
|
|
L.Tang,
L.Bai,
W.H.Wang,
and
T.Jiang
(2010).
Crystal structure of the carnitine transporter and insights into the antiport mechanism.
|
| |
Nat Struct Mol Biol, 17,
492-496.
|
|
|
PDB code:
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|
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|
|
|
|
|
M.Indarte,
Y.Liu,
J.D.Madura,
and
C.K.Surratt
(2010).
Receptor-Based Discovery of a Plasmalemmal Monoamine Transporter Inhibitor via High Throughput Docking and Pharmacophore Modeling.
|
| |
ACS Chem Neurosci, 1,
223-233.
|
|
|
|
|
|
|
N.K.Karpowich,
and
D.N.Wang
(2010).
Biophysics: Transporter in the spotlight.
|
| |
Nature, 465,
171-172.
|
|
|
|
|
|
|
P.C.Gedeon,
M.Indarte,
C.K.Surratt,
and
J.D.Madura
(2010).
Molecular dynamics of leucine and dopamine transporter proteins in a model cell membrane lipid bilayer.
|
| |
Proteins, 78,
797-811.
|
|
|
|
|
|
|
P.S.Chae,
S.G.Rasmussen,
R.R.Rana,
K.Gotfryd,
R.Chandra,
M.A.Goren,
A.C.Kruse,
S.Nurva,
C.J.Loland,
Y.Pierre,
D.Drew,
J.L.Popot,
D.Picot,
B.G.Fox,
L.Guan,
U.Gether,
B.Byrne,
B.Kobilka,
and
S.H.Gellman
(2010).
Maltose-neopentyl glycol (MNG) amphiphiles for solubilization, stabilization and crystallization of membrane proteins.
|
| |
Nat Methods, 7,
1003-1008.
|
|
|
|
|
|
|
S.A.Shaikh,
and
E.Tajkhorshid
(2010).
Modeling and dynamics of the inward-facing state of a Na+/Cl- dependent neurotransmitter transporter homologue.
|
| |
PLoS Comput Biol, 6,
0.
|
|
|
|
|
|
|
S.J.Facey,
and
A.Kuhn
(2010).
Biogenesis of bacterial inner-membrane proteins.
|
| |
Cell Mol Life Sci, 67,
2343-2362.
|
|
|
|
|
|
|
S.Schulze,
S.Köster,
U.Geldmacher,
A.C.Terwisscha van Scheltinga,
and
W.Kühlbrandt
(2010).
Structural basis of Na(+)-independent and cooperative substrate/product antiport in CaiT.
|
| |
Nature, 467,
233-236.
|
|
|
PDB codes:
|
|
|
|
|
|
|
|
S.Sinning,
M.Musgaard,
M.Jensen,
K.Severinsen,
L.Celik,
H.Koldsø,
T.Meyer,
M.Bols,
H.H.Jensen,
B.Schiøtt,
and
O.Wiborg
(2010).
Binding and orientation of tricyclic antidepressants within the central substrate site of the human serotonin transporter.
|
| |
J Biol Chem, 285,
8363-8374.
|
|
|
|
|
|
|
S.Sucic,
S.Dallinger,
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PDB code:
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The residues determining differences in ion affinities among the alternative splice variants F, A, and B of the mammalian renal Na-K-Cl cotransporter (NKCC2).
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Selective amino acid substitutions convert the creatine transporter to a gamma-aminobutyric acid transporter.
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G328E and G409E sialin missense mutations similarly impair transport activity, but differentially affect trafficking.
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Mol Genet Metab, 92,
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Coupling substrate and ion binding to extracellular gate of a sodium-dependent aspartate transporter.
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Nature, 445,
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PDB codes:
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Synapse, 61,
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Localization of cocaine analog [125I]RTI 82 irreversible binding to transmembrane domain 6 of the dopamine transporter.
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J Biol Chem, 282,
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Direct evidence that two cysteines in the dopamine transporter form a disulfide bond.
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Mol Cell Biochem, 298,
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Molecular basis for substrate discrimination by glycine transporters.
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A screen for neurotransmitter transporters expressed in the visual system of Drosophila melanogaster identifies three novel genes.
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Chloride finds its place in the transport cycle.
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Antidepressant binding site in a bacterial homologue of neurotransmitter transporters.
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Nature, 448,
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PDB codes:
|
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S.Kitayama,
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[New development in study of neurotransmitter transporters]
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Nippon Yakurigaku Zasshi, 130,
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Phosphorylation of threonine residue 276 is required for acute regulation of serotonin transporter by cyclic GMP.
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