Mechanism of Substrate Translocation in an Alternating Access Transporter

Latorraca, Naomi R.; Fastman, Nathan M.; Venkatakrishnan, A. J.; Frommer, Wolf B.; Dror, Ron O.; Feng, Liang

doi:10.1016/j.cell.2017.03.010

Title: Mechanism of Substrate Translocation in an Alternating Access Transporter

Journal Article · Wed Mar 01 00:00:00 EST 2017 · Cell

DOI:https://doi.org/10.1016/j.cell.2017.03.010· OSTI ID:1429555

Latorraca, Naomi R.; Fastman, Nathan M.; Venkatakrishnan, A. J.; Frommer, Wolf B.; Dror, Ron O.; Feng, Liang

View Journal Article

Cite

Export

Save

Research Organization:: Carnegie Inst. of Science, Stanford, CA (United States)

Sponsoring Organization:: USDOE; National Institutes of Health (NIH); National Science Foundation (NSF); Alfred P. Sloan Foundation; Harold and Leila Y. Mathers Charitable Foundation; Stanford University

Grant/Contract Number:: FG02-04ER15542

OSTI ID:: 1429555

Alternate ID(s):: OSTI ID: 1398626; OSTI ID: 1473844

Journal Information:: Cell, Journal Name: Cell Vol. 169 Journal Issue: 1; ISSN 0092-8674

Publisher:: ElsevierCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 60 works

Citation information provided by
Web of Science

References (74)

SPFP: Speed without compromise—A mixed precision model for GPU accelerated molecular dynamics simulations Le Grand, Scott; Götz, Andreas W.; Walker, Ross C. Computer Physics Communications, Vol. 184, Issue 2 https://doi.org/10.1016/j.cpc.2012.09.022	journal	February 2013
A chemiosmotic mechanism of symport Kaback, H. Ronald Proceedings of the National Academy of Sciences, Vol. 112, Issue 5 https://doi.org/10.1073/pnas.1419325112	journal	January 2015
Solving structures of protein complexes by molecular replacement with Phaser McCoy, Airlie J. Acta Crystallographica Section D Biological Crystallography, Vol. 63, Issue 1 https://doi.org/10.1107/S0907444906045975	journal	December 2006
The Crystal Structure of a Sodium Galactose Transporter Reveals Mechanistic Insights into Na+/Sugar Symport Faham, S.; Watanabe, A.; Besserer, G. M. Science, Vol. 321, Issue 5890 https://doi.org/10.1126/science.1160406	journal	August 2008
Simple Allosteric Model for Membrane Pumps Jardetzky, Oleg Nature, Vol. 211, Issue 5052 https://doi.org/10.1038/211969a0	journal	August 1966
Mechanistic diversity in ATP-binding cassette (ABC) transporters Locher, Kaspar P. Nature Structural & Molecular Biology, Vol. 23, Issue 6 https://doi.org/10.1038/nsmb.3216	journal	June 2016
Functional role of oligomerization for bacterial and plant SWEET sugar transporter family Xuan, Y. H.; Hu, Y. B.; Chen, L. -Q. Proceedings of the National Academy of Sciences, Vol. 110, Issue 39 https://doi.org/10.1073/pnas.1311244110	journal	September 2013
CHARMM36 all-atom additive protein force field: Validation based on comparison to NMR data Huang, Jing; MacKerell, Alexander D. Journal of Computational Chemistry, Vol. 34, Issue 25 https://doi.org/10.1002/jcc.23354	journal	July 2013
Crystal structure of a eukaryotic phosphate transporter Pedersen, Bjørn P.; Kumar, Hemant; Waight, Andrew B. Nature, Vol. 496, Issue 7446 https://doi.org/10.1038/nature12042	journal	March 2013
Protonation drives the conformational switch in the multidrug transporter LmrP Masureel, Matthieu; Martens, Chloé; Stein, Richard A. Nature Chemical Biology, Vol. 10, Issue 2 https://doi.org/10.1038/nchembio.1408	journal	December 2013
Visualizing Functional Motions of Membrane Transporters with Molecular Dynamics Simulations Shaikh, Saher A.; Li, Jing; Enkavi, Giray Biochemistry, Vol. 52, Issue 4 https://doi.org/10.1021/bi301086x	journal	January 2013
Structure of sugar-bound LacY Kumar, Hemant; Kasho, Vladimir; Smirnova, Irina Proceedings of the National Academy of Sciences, Vol. 111, Issue 5 https://doi.org/10.1073/pnas.1324141111	journal	January 2014
Structural Biology of the Major Facilitator Superfamily Transporters Yan, Nieng Annual Review of Biophysics, Vol. 44, Issue 1 https://doi.org/10.1146/annurev-biophys-060414-033901	journal	June 2015
Structure of a eukaryotic SWEET transporter in a homotrimeric complex Tao, Yuyong; Cheung, Lily S.; Li, Shuo Nature, Vol. 527, Issue 7577 https://doi.org/10.1038/nature15391	journal	October 2015
Simulations of the Alternating Access Mechanism of the Sodium Symporter Mhp1 Adelman, Joshua L.; Dale, Amy L.; Zwier, Matthew C. Biophysical Journal, Vol. 101, Issue 10 https://doi.org/10.1016/j.bpj.2011.09.061	journal	November 2011
Structural basis for the facilitative diffusion mechanism by SemiSWEET transporter Lee, Yongchan; Nishizawa, Tomohiro; Yamashita, Keitaro Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms7112	journal	January 2015
Atomic-level characterization of transport cycle thermodynamics in the glycerol-3-phosphate:phosphate antiporter Moradi, Mahmoud; Enkavi, Giray; Tajkhorshid, Emad Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms9393	journal	September 2015
Modeling and simulation of ion-coupled and ATP-driven membrane proteins Faraldo-Gómez, José D.; Forrest, Lucy R. Current Opinion in Structural Biology, Vol. 21, Issue 2 https://doi.org/10.1016/j.sbi.2011.01.013	journal	April 2011
Routine Microsecond Molecular Dynamics Simulations with AMBER on GPUs. 2. Explicit Solvent Particle Mesh Ewald Salomon-Ferrer, Romelia; Götz, Andreas W.; Poole, Duncan Journal of Chemical Theory and Computation, Vol. 9, Issue 9 https://doi.org/10.1021/ct400314y	journal	August 2013
Understanding transport by the major facilitator superfamily (MFS): structures pave the way Quistgaard, Esben M.; Löw, Christian; Guettou, Fatma Nature Reviews Molecular Cell Biology, Vol. 17, Issue 2 https://doi.org/10.1038/nrm.2015.25	journal	January 2016
A General Theory of Membrane Transport From Studies of Bacteria Mitchell, Peter Nature, Vol. 180, Issue 4577 https://doi.org/10.1038/180134a0	journal	July 1957
Substrate Recognition at the Cytoplasmic and Extracellular Binding Site of the Lactose Transport Protein of Streptococcus thermophilus Veenhoff, Liesbeth M.; Poolman, Bert Journal of Biological Chemistry, Vol. 274, Issue 47 https://doi.org/10.1074/jbc.274.47.33244	journal	November 1999
Unbiased Simulations Reveal the Inward-Facing Conformation of the Human Serotonin Transporter and Na+ Ion Release Koldsø, Heidi; Noer, Pernille; Grouleff, Julie PLoS Computational Biology, Vol. 7, Issue 10 https://doi.org/10.1371/journal.pcbi.1002246	journal	October 2011
Hydrophilicity of cavities in proteins Zhang, Li; Hermans, Jan Proteins: Structure, Function, and Genetics, Vol. 24, Issue 4 https://doi.org/10.1002/(SICI)1097-0134(199604)24:4<433::AID-PROT3>3.0.CO;2-F	journal	April 1996
Inclusion of Many-Body Effects in the Additive CHARMM Protein CMAP Potential Results in Enhanced Cooperativity of α-Helix and β-Hairpin Formation Best, Robert B.; Mittal, Jeetain; Feig, Michael Biophysical Journal, Vol. 103, Issue 5 https://doi.org/10.1016/j.bpj.2012.07.042	journal	September 2012
Crystal structure of a bacterial homologue of Na+/Cl--dependent neurotransmitter transporters Yamashita, Atsuko; Singh, Satinder K.; Kawate, Toshimitsu Nature, Vol. 437, Issue 7056 https://doi.org/10.1038/nature03978	journal	July 2005
Structure of the Multidrug Transporter EmrD from Escherichia coli Yin, Y. Science, Vol. 312, Issue 5774 https://doi.org/10.1126/science.1125629	journal	May 2006
Ion-Controlled Conformational Dynamics in the Outward-Open Transition from an Occluded State of LeuT Zhao, Chunfeng; Stolzenberg, Sebastian; Gracia, Luis Biophysical Journal, Vol. 103, Issue 5 https://doi.org/10.1016/j.bpj.2012.07.044	journal	September 2012
Conformational Change in an MFS Protein: MD Simulations of LacY Holyoake, John; Sansom, Mark S. P. Structure, Vol. 15, Issue 7 https://doi.org/10.1016/j.str.2007.06.004	journal	July 2007
Conformational dynamics of ligand-dependent alternating access in LeuT Kazmier, Kelli; Sharma, Shruti; Quick, Matthias Nature Structural & Molecular Biology, Vol. 21, Issue 5 https://doi.org/10.1038/nsmb.2816	journal	April 2014
Integration, scaling, space-group assignment and post-refinement Kabsch, Wolfgang Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 133-144 https://doi.org/10.1107/S0907444909047374	journal	January 2010
Update of the CHARMM All-Atom Additive Force Field for Lipids: Validation on Six Lipid Types Klauda, Jeffery B.; Venable, Richard M.; Freites, J. Alfredo The Journal of Physical Chemistry B, Vol. 114, Issue 23 https://doi.org/10.1021/jp101759q	journal	June 2010
Biomolecular Simulation: A Computational Microscope for Molecular Biology Dror, Ron O.; Dirks, Robert M.; Grossman, J. P. Annual Review of Biophysics, Vol. 41, Issue 1 https://doi.org/10.1146/annurev-biophys-042910-155245	journal	June 2012
Allosteric Mechanisms of Molecular Machines at the Membrane: Transport by Sodium-Coupled Symporters LeVine, Michael V.; Cuendet, Michel A.; Khelashvili, George Chemical Reviews, Vol. 116, Issue 11 https://doi.org/10.1021/acs.chemrev.5b00627	journal	February 2016
Molecular simulations elucidate the substrate translocation pathway in a glutamate transporter Gu, Yan; Shrivastava, Indira H.; Amara, Susan G. Proceedings of the National Academy of Sciences, Vol. 106, Issue 8 https://doi.org/10.1073/pnas.0812299106	journal	February 2009
Glucose transport families SLC5 and SLC50 Wright, Ernest M. Molecular Aspects of Medicine, Vol. 34, Issue 2-3 https://doi.org/10.1016/j.mam.2012.11.002	journal	April 2013
Induced fit substrate binding to an archeal glutamate transporter homologue Ewers, D.; Becher, T.; Machtens, J. -P. Proceedings of the National Academy of Sciences, Vol. 110, Issue 30 https://doi.org/10.1073/pnas.1300772110	journal	July 2013
Apo-intermediate in the transport cycle of lactose permease (LacY) Madej, M. G.; Soro, S. N.; Kaback, H. R. Proceedings of the National Academy of Sciences, Vol. 109, Issue 44 https://doi.org/10.1073/pnas.1211183109	journal	September 2012
Sugar transporters for intercellular exchange and nutrition of pathogens Chen, Li-Qing; Hou, Bi-Huei; Lalonde, Sylvie Nature, Vol. 468, Issue 7323 https://doi.org/10.1038/nature09606	journal	November 2010
Multiscale Simulations Reveal Key Aspects of the Proton Transport Mechanism in the ClC-ec1 Antiporter Lee, Sangyun; Swanson, Jessica M. J.; Voth, Gregory A. Biophysical Journal, Vol. 110, Issue 6 https://doi.org/10.1016/j.bpj.2016.02.014	journal	March 2016
Crystal structure of the human glucose transporter GLUT1 Deng, Dong; Xu, Chao; Sun, Pengcheng Nature, Vol. 510, Issue 7503 https://doi.org/10.1038/nature13306	journal	May 2014
Crystal structure of a bacterial homologue of glucose transporters GLUT1–4 Sun, Linfeng; Zeng, Xin; Yan, Chuangye Nature, Vol. 490, Issue 7420 https://doi.org/10.1038/nature11524	journal	October 2012
Computational characterization of structural dynamics underlying function in active membrane transporters Li, Jing; Wen, Po-Chao; Moradi, Mahmoud Current Opinion in Structural Biology, Vol. 31 https://doi.org/10.1016/j.sbi.2015.04.001	journal	April 2015
Coupled ion binding and structural transitions along the transport cycle of glutamate transporters Verdon, Grégory; Oh, SeCheol; Serio, Ryan N. eLife, Vol. 3 https://doi.org/10.7554/eLife.02283	journal	May 2014
Transport domain unlocking sets the uptake rate of an aspartate transporter Akyuz, Nurunisa; Georgieva, Elka R.; Zhou, Zhou Nature, Vol. 518, Issue 7537 https://doi.org/10.1038/nature14158	journal	February 2015
P-Type ATPases Palmgren, Michael G.; Nissen, Poul Annual Review of Biophysics, Vol. 40, Issue 1 https://doi.org/10.1146/annurev.biophys.093008.131331	journal	June 2011
Coot model-building tools for molecular graphics Emsley, Paul; Cowtan, Kevin Acta Crystallographica Section D Biological Crystallography, Vol. 60, Issue 12, p. 2126-2132 https://doi.org/10.1107/S0907444904019158	journal	November 2004
Structures of bacterial homologues of SWEET transporters in two distinct conformations Xu, Yan; Tao, Yuyong; Cheung, Lily S. Nature, Vol. 515, Issue 7527 https://doi.org/10.1038/nature13670	journal	September 2014
Optimization of the Additive CHARMM All-Atom Protein Force Field Targeting Improved Sampling of the Backbone ϕ, ψ and Side-Chain χ ₁ and χ ₂ Dihedral Angles Best, Robert B.; Zhu, Xiao; Shim, Jihyun Journal of Chemical Theory and Computation, Vol. 8, Issue 9 https://doi.org/10.1021/ct300400x	journal	August 2012
Mechanistic picture for conformational transition of a membrane transporter at atomic resolution Moradi, M.; Tajkhorshid, E. Proceedings of the National Academy of Sciences, Vol. 110, Issue 47 https://doi.org/10.1073/pnas.1313202110	journal	November 2013
Crystal structure of a catalytic intermediate of the maltose transporter Oldham, Michael L.; Khare, Dheeraj; Quiocho, Florante A. Nature, Vol. 450, Issue 7169 https://doi.org/10.1038/nature06264	journal	November 2007
PHENIX: a comprehensive Python-based system for macromolecular structure solution Adams, Paul D.; Afonine, Pavel V.; Bunkóczi, Gábor Acta Crystallographica Section D Biological Crystallography, Vol. 66, Issue 2, p. 213-221 https://doi.org/10.1107/S0907444909052925	journal	January 2010
Protonation of Glu 135 Facilitates the Outward-to-Inward Structural Transition of Fucose Transporter Liu, Yufeng; Ke, Meng; Gong, Haipeng Biophysical Journal, Vol. 109, Issue 3 https://doi.org/10.1016/j.bpj.2015.06.037	journal	August 2015
(Pseudo-)Symmetrical Transport Forrest, L. R. Science, Vol. 339, Issue 6118 https://doi.org/10.1126/science.1228465	journal	January 2013
The structural basis of secondary active transport mechanisms Forrest, Lucy R.; Krämer, Reinhard; Ziegler, Christine Biochimica et Biophysica Acta (BBA) - Bioenergetics, Vol. 1807, Issue 2 https://doi.org/10.1016/j.bbabio.2010.10.014	journal	February 2011
Molecular Basis of Alternating Access Membrane Transport by the Sodium-Hydantoin Transporter Mhp1 Shimamura, T.; Weyand, S.; Beckstein, O. Science, Vol. 328, Issue 5977 https://doi.org/10.1126/science.1186303	journal	April 2010
Gating Topology of the Proton-Coupled Oligopeptide Symporters Fowler, Philip W.; Orwick-Rydmark, Marcella; Radestock, Sebastian Structure, Vol. 23, Issue 2 https://doi.org/10.1016/j.str.2014.12.012	journal	February 2015
Crystal structure of a phosphorylation-coupled saccharide transporter Cao, Yu; Jin, Xiangshu; Levin, Elena J. Nature, Vol. 473, Issue 7345 https://doi.org/10.1038/nature09939	journal	April 2011
Shared Molecular Mechanisms of Membrane Transporters Drew, David; Boudker, Olga Annual Review of Biochemistry, Vol. 85, Issue 1 https://doi.org/10.1146/annurev-biochem-060815-014520	journal	June 2016
CHARMM Additive All-Atom Force Field for Glycosidic Linkages between Hexopyranoses Guvench, Olgun; Hatcher, Elizabeth; Venable, Richard M. Journal of Chemical Theory and Computation, Vol. 5, Issue 9 https://doi.org/10.1021/ct900242e	journal	August 2009
Matplotlib: A 2D Graphics Environment Hunter, John D. Computing in Science & Engineering, Vol. 9, Issue 3 https://doi.org/10.1109/MCSE.2007.55	journal	January 2007
Transport of Sugars Chen, Li-Qing; Cheung, Lily S.; Feng, Liang Annual Review of Biochemistry, Vol. 84, Issue 1 https://doi.org/10.1146/annurev-biochem-060614-033904	journal	June 2015
Towards an understanding of the structural basis of ‘forbidden’ transport pathways in the Escherichia coli lactose carrier: mutations probing the energy barriers to uncoupled transport King, S. C.; Wilson, T. H. Molecular Microbiology, Vol. 4, Issue 9 https://doi.org/10.1111/j.1365-2958.1990.tb02053.x	journal	September 1990
OPM: Orientations of Proteins in Membranes database Lomize, M. A.; Lomize, A. L.; Pogozheva, I. D. Bioinformatics, Vol. 22, Issue 5 https://doi.org/10.1093/bioinformatics/btk023	journal	January 2006
The mechanism of sodium and substrate release from the binding pocket of vSGLT Watanabe, Akira; Choe, Seungho; Chaptal, Vincent Nature, Vol. 468, Issue 7326 https://doi.org/10.1038/nature09580	journal	December 2010
Complete Mapping of Substrate Translocation Highlights the Role of LeuT N-terminal Segment in Regulating Transport Cycle Cheng, Mary Hongying; Bahar, Ivet PLoS Computational Biology, Vol. 10, Issue 10 https://doi.org/10.1371/journal.pcbi.1003879	journal	October 2014
[20] Processing of X-ray diffraction data collected in oscillation mode Otwinowski, Zbyszek; Minor, Wladek Macromolecular Crystallography Part A, 307-326 https://doi.org/10.1016/S0076-6879(97)76066-X	book	January 1997
Stochastic steps in secondary active sugar transport Adelman, Joshua L.; Ghezzi, Chiara; Bisignano, Paola Proceedings of the National Academy of Sciences, Vol. 113, Issue 27 https://doi.org/10.1073/pnas.1525378113	journal	June 2016
Super-resolution biomolecular crystallography with low-resolution data Schröder, Gunnar F.; Levitt, Michael; Brunger, Axel T. Nature, Vol. 464, Issue 7292 https://doi.org/10.1038/nature08892	journal	April 2010
Flexible Gates Generate Occluded Intermediates in the Transport Cycle of LacY Stelzl, Lukas S.; Fowler, Philip W.; Sansom, Mark S. P. Journal of Molecular Biology, Vol. 426, Issue 3 https://doi.org/10.1016/j.jmb.2013.10.024	journal	February 2014
VMD: Visual molecular dynamics Humphrey, William; Dalke, Andrew; Schulten, Klaus Journal of Molecular Graphics, Vol. 14, Issue 1 https://doi.org/10.1016/0263-7855(96)00018-5	journal	February 1996
PTRAJ and CPPTRAJ: Software for Processing and Analysis of Molecular Dynamics Trajectory Data Roe, Daniel R.; Cheatham, Thomas E. Journal of Chemical Theory and Computation, Vol. 9, Issue 7 https://doi.org/10.1021/ct400341p	journal	June 2013
Crystal structure of a bacterial homologue of SWEET transporters Wang, Jing; Yan, Chuangye; Li, Yini Cell Research, Vol. 24, Issue 12 https://doi.org/10.1038/cr.2014.144	journal	November 2014
Structural basis for dynamic mechanism of nitrate/nitrite antiport by NarK Fukuda, Masahiro; Takeda, Hironori; Kato, Hideaki E. Nature Communications, Vol. 6, Issue 1 https://doi.org/10.1038/ncomms8097	journal	May 2015

Similar Records

Mechanism of Substrate Translocation in an Alternating Access Transporter

Journal Article · Wed Mar 01 00:00:00 EST 2017 · Cell · OSTI ID:1429555

Latorraca, Naomi R.; Fastman, Nathan M.; Venkatakrishnan, A. J.; +3 more

Studies of the Maltose Transport System Reveal a Mechanism for Coupling ATP Hydrolysis to Substrate Translocation without Direct Recognition of Substrate

Journal Article · Mon Oct 11 00:00:00 EDT 2010 · J. Biol. Chem. · OSTI ID:1429555

Gould, Alister D; Shilton, Brian H

Structural basis of the alternating-access mechanism in a bile acid transporter

Journal Article · Mon Apr 21 00:00:00 EDT 2014 · Nature · OSTI ID:1429555

Zhou, Xiaoming; Levin, Elena J.; Pan, Yaping; +6 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
molecular dynamics (MD) simulation
membrane protein
transporter
sugar transporter
SemiSWEET
structure

Title: Mechanism of Substrate Translocation in an Alternating Access Transporter

Citation Formats

References (74)

Similar Records

Related Subjects