The DOI matches its Crossref record; 2 of the 2 references it cites were found in a registry or an index.
Probing the stability and interdomain interactions in the ABC transporter OpuA using single-molecule optical tweezers
Open accessPublished version of a preprint
Abstract
Transmembrane transporter proteins are essential for maintaining cellular homeostasis and, as such, are key drug targets. Many transmembrane transporter proteins are known to undergo large structural rearrangements during their functional cycles. Despite the wealth of detailed structural and functional data available for these systems, our understanding of their dynamics and, consequently, how they function is generally limited. We introduce an innovative approach that enables us to directly measure the dynamics and stability of interdomain interactions of transmembrane proteins using optical tweezers. Focusing on the osmoregulatory ATP-binding cassette transporter OpuA from Lactococcus lactis, we examine the mechanical properties and potential interactions of its substrate-binding domains. Our measurements are performed in lipid nanodiscs, providing a native-mimicking environment for the transmembrane protein. The technique provides high spatial and temporal resolution and allows us to study the functionally relevant motions and interdomain interactions of individual transmembrane transporter proteins in real time in a lipid bilayer.
Overview
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Citations
Cites
Highly accurate protein structure prediction with AlphaFold
Jumper, J., Evans, R., Pritzel, A., Green, T., Figurnov, M., Ronneberger, O., Tunyasuvunakool, K., Bates, R., Žídek, A., Potapenko, A., et al. (2021) · Nature · doi:10.1038/s41586-021-03819-2 · Cited by 43,764
The Complex Folding Network of Single Calmodulin Molecules
Stigler, J., Ziegler, F., Gieseke, A., Gebhardt, J. C. M., & Rief, M. (2011) · Science · doi:10.1126/science.1207598 · Cited by 372
Flagged first, then by citations
Research works printed but not linked: 57
- Bustamante, 2021, Optical tweezers in single-molecule biophysics, Nat. Rev. Methods Primers, 1, 25, 10.1038/s43586-021-00021-6 · DOI
- Zaltron, 2020, Optical tweezers in single-molecule experiments, Eur. Phys. J. Plus, 135, 896, 10.1140/epjp/s13360-020-00907-6 · DOI
- Bustamante, 2020, Single-Molecule Studies of Protein Folding with Optical Tweezers, Annu. Rev. Biochem., 89, 443, 10.1146/annurev-biochem-013118-111442 · DOI
- Petrosyan, 2021, Single-Molecule Force Spectroscopy of Protein Folding, J. Mol. Biol., 433, 10.1016/j.jmb.2021.167207 · DOI
- Yu, 2012, Direct observation of multiple misfolding pathways in a single prion protein molecule, Proc. Natl. Acad. Sci. USA, 109, 5283, 10.1073/pnas.1107736109 · DOI
- Shank, 2010, The folding cooperativity of a protein is controlled by its chain topology, Nature, 465, 637, 10.1038/nature09021 · DOI
- Cecconi, 2005, Direct Observation of the Three-State Folding of a Single Protein Molecule, Science, 309, 2057, 10.1126/science.1116702 · DOI
- Foroutannejad, 2023, The cofactor-dependent folding mechanism of Drosophila cryptochrome revealed by single-molecule pulling experiments, Nat. Commun., 14, 1057, 10.1038/s41467-023-36701-y · DOI
- Pelz, 2016, Subnanometre enzyme mechanics probed by single-molecule force spectroscopy, Nat. Commun., 7, 10.1038/ncomms10848 · DOI
- Jahn, 2018, Folding and Domain Interactions of Three Orthologs of Hsp90 Studied by Single-Molecule Force Spectroscopy, Structure, 26, 96, 10.1016/j.str.2017.11.023 · DOI
- Jahn, 2014, The charged linker of the molecular chaperone Hsp90 modulates domain contacts and biological function, Proc. Natl. Acad. Sci. USA, 111, 17881, 10.1073/pnas.1414073111 · DOI
- Min, 2018, Unfolding of a ClC chloride transporter retains memory of its evolutionary history, Nat. Chem. Biol., 14, 489, 10.1038/s41589-018-0025-4 · DOI
- Kim, 2023, Robust membrane protein tweezers reveal the folding speed limit of helical membrane proteins, Elife, 12, 10.7554/eLife.85882 · DOI
- Wijesinghe, 2023, Single-Molecule Force Spectroscopy of Membrane Protein Folding, J. Mol. Biol., 435, 10.1016/j.jmb.2023.167975 · DOI
- Whited, 2014, Atomic force microscopy: A multifaceted tool to study membrane proteins and their interactions with ligands, Biochim. Biophys. Acta, 1838, 56, 10.1016/j.bbamem.2013.04.011 · DOI
- Ford, 2019, Learning the ABCs one at a time: Structure and mechanism of ABC transporters, Biochem. Soc. Trans., 47, 23, 10.1042/BST20180147 · DOI
- ter Beek, 2014, Structural diversity of ABC transporters, J. Gen. Physiol., 143, 419, 10.1085/jgp.201411164 · DOI
- van der Heide, 2002, ABC transporters: one, two or four extracytoplasmic substrate-binding sites?, EMBO Rep., 3, 938, 10.1093/embo-reports/kvf201 · DOI
- Higgins, 1981, Two periplasmic transport proteins which interact with a common membrane receptor show extensive homology: complete nucleotide sequences, Proc. Natl. Acad. Sci. USA, 78, 6038, 10.1073/pnas.78.10.6038 · DOI
- Schuurman-Wolters, 2005, Substrate specificity and ionic regulation of GlnPQ from Lactococcus lactis: An ATP-binding cassette transporter with four extracytoplasmic substrate-binding domains, J. Biol. Chem., 280, 23785, 10.1074/jbc.M500522200 · DOI
- van den Noort, 2023, The substrate-binding domains of the osmoregulatory ABC importer OpuA physically interact, Elife, 12
- Biemans-Oldehinkel, 2003, On the role of the two extracytoplasmic substrate-binding domains in the ABC transporter OpuA, EMBO J., 22, 5983, 10.1093/emboj/cdg581 · DOI
- Wood, 2001, Osmosensing and osmoregulatory compatible solute accumulation by bacteria, Comp. Biochem. Physiol. Mol. Integr. Physiol., 130, 437, 10.1016/S1095-6433(01)00442-1 · DOI
- Wood, 2011, Bacterial osmoregulation: A paradigm for the study of cellular homeostasis, Annu. Rev. Microbiol., 65, 215, 10.1146/annurev-micro-090110-102815 · DOI · Paper page
- Biemans-Oldehinkel, 2006, ABC transporter architecture and regulatory roles of accessory domains, FEBS Lett., 580, 1023, 10.1016/j.febslet.2005.11.079 · DOI
- Biemans-Oldehinkel, 2006, A sensor for intracellular ionic strength, Proc. Natl. Acad. Sci. USA, 103, 10624, 10.1073/pnas.0603871103 · DOI
- Sikkema, 2020, Gating by ionic strength and safety check by cyclic-di-AMP in the ABC transporter OpuA, Sci. Adv., 6, 10.1126/sciadv.abd7697 · DOI
- Wolters, 2010, Ligand binding and crystal structures of the substrate- binding domain of the ABC transporter OpuA, PLoS One, 5, 10.1371/journal.pone.0010361 · DOI
- Patzlaff, 2003, The ATP/substrate stoichiometry of the ATP-binding cassette (ABC) transporter OpuA, J. Biol. Chem., 278, 29546, 10.1074/jbc.M304796200 · DOI
- Karasawa, 2013, Physicochemical Factors Controlling the Activity and Energy Coupling of an Ionic Strength-gated ATP-binding Cassette (ABC) Transporter, J. Biol. Chem., 288, 29862, 10.1074/jbc.M113.499327 · DOI
- Mahmood, 2006, Ion specificity and ionic strength dependence of the osmoregulatory ABC transporter OpuA, J. Biol. Chem., 281, 29830, 10.1074/jbc.M604907200 · DOI
- Van Der Heide, 2000, Osmoregulated ABC-transport system of Lactococcus lactis senses water stress via changes in the physical state of the membrane, Proc. Natl. Acad. Sci. USA, 97, 7102, 10.1073/pnas.97.13.7102 · DOI
- van der Heide, 2001, On the osmotic signal and osmosensing mechanism of an ABC transport system for glycine betaine, EMBO J., 20, 7022, 10.1093/emboj/20.24.7022 · DOI
- Bayburt, 2010, Membrane protein assembly into Nanodiscs, FEBS Lett., 584, 1721, 10.1016/j.febslet.2009.10.024 · DOI
- Hilton, 2022, Single-molecule investigations of single-chain cellulose biosynthesis, Proc. Natl. Acad. Sci. USA, 119, 10.1073/pnas.2122770119 · DOI
- Crampton, 2010, Unravelling the design principles for single protein mechanical strength, Curr. Opin. Struct. Biol., 20, 508, 10.1016/j.sbi.2010.05.005 · DOI
- Renn, 2019, Mechanical unfolding of spectrin reveals a super-exponential dependence of unfolding rate on force, Sci. Rep., 9, 10.1038/s41598-019-46525-w · DOI
- Sheridan, 2019, How Fast Is Too Fast in Force-Probe Molecular Dynamics Simulations?, J. Phys. Chem. B, 123, 3658, 10.1021/acs.jpcb.9b01251 · DOI
- Mazal, 2018, Effect of ligand binding on a protein with a complex folding landscape, Phys. Chem. Chem. Phys., 20, 3054, 10.1039/C7CP03327C · DOI
- Bertz, 2009, Ligand Binding Mechanics of Maltose Binding Protein, J. Mol. Biol., 393, 1097, 10.1016/j.jmb.2009.08.066 · DOI
- Bauer, 2015, Nucleotides regulate the mechanical hierarchy between subdomains of the nucleotide binding domain of the Hsp70 chaperone DnaK, Proc. Natl. Acad. Sci. USA, 112, 10389, 10.1073/pnas.1504625112 · DOI
- Girstmair, 2019, The Hsp90 isoforms from S. cerevisiae differ in structure, function and client range, Nat. Commun., 10, 10.1038/s41467-019-11518-w · DOI
- Street, 2006, A molecular mechanism for osmolyte-induced protein stability, Proc. Natl. Acad. Sci. USA, 103, 13997, 10.1073/pnas.0606236103 · DOI
- Auton, 2011, Osmolyte effects on protein stability and solubility: A balancing act between backbone and side-chains, Biophys. Chem., 159, 90, 10.1016/j.bpc.2011.05.012 · DOI
- Ritchie, 2009, Reconstitution of Membrane Proteins in Phospholipid Bilayer Nanodiscs, Methods Enzymol., 464, 211, 10.1016/S0076-6879(09)64011-8 · DOI
- Florin, 1998, Photonic force microscope calibration by thermal noise analysis, Appl. Phys. Mater. Sci. Process, 66, S75, 10.1007/s003390051103 · DOI
- Abraham, 2015, Gromacs: High performance molecular simulations through multi-level parallelism from laptops to supercomputers, SoftwareX, 1–2, 19, 10.1016/j.softx.2015.06.001 · DOI · Paper page
- Best, 2012, Optimization of the additive CHARMM all-atom protein force field targeting improved sampling of the backbone φ, ψ and side-chain χ1 and χ2 Dihedral Angles, J. Chem. Theor. Comput., 8, 3257, 10.1021/ct300400x · DOI
- Hess, 2008, P-LINCS: A parallel linear constraint solver for molecular simulation, J. Chem. Theor. Comput., 4, 116, 10.1021/ct700200b · DOI
- Bussi, 2007, Canonical sampling through velocity rescaling, J. Chem. Phys., 126
- Parrinello, 1981, Polymorphic transitions in single crystals: A new molecular dynamics method, J. Appl. Phys., 52, 7182, 10.1063/1.328693 · DOI
- Darden, 1993, Particle mesh Ewald: An N·log(N) method for Ewald sums in large systems, J. Chem. Phys., 98, 10089, 10.1063/1.464397 · DOI
- Mirdita, 2022, ColabFold: making protein folding accessible to all, Nat. Methods, 19, 679, 10.1038/s41592-022-01488-1 · DOI · Paper page
- Wenner, 2002, Salt dependence of the elasticity and overstretching transition of single DNA molecules, Biophys. J., 82, 3160, 10.1016/S0006-3495(02)75658-0 · DOI
- Franz, 2020, Advances in molecular simulations of protein mechanical properties and function, Curr. Opin. Struct. Biol., 61, 132, 10.1016/j.sbi.2019.12.015 · DOI
- Zhuang, 2022, Implementation of Telescoping Boxes in Adaptive Steered Molecular Dynamics, J. Chem. Theor. Comput., 18, 4649, 10.1021/acs.jctc.2c00498 · DOI
- Virtanen, 2020, SciPy 1.0: fundamental algorithms for scientific computing in Python, Nat. Methods, 17, 261, 10.1038/s41592-019-0686-2 · DOI · Paper page
Metadata
- Authors
- van der Sleen, L., Stevens, J. A., Marrink, S. J., Poolman, B., & Tych, K.
- Affiliations
- University of Groningen (NL)
- Corresponding author
- Poolman, Bert
- Venue
- Cell Reports
- Publisher
- Elsevier BV
- Published
- 2024-04
- Volume
- 43
- Issue
- 4
- Pages
- 114110
- ISSN
- 2211-1247 (ISSN-L)
- OpenAlex
- W4394728395
- Cited by
- 12
- References
- 2
- Citations by year
- 2026: 5 · 2025: 5 · 2024: 1
- FWCI
- 1.75
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- Locations
- Cell Reports (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc)
- SSRN Electronic Journal (acceptedVersion)
- PubMed (publishedVersion)
- University of Groningen research database (University of Groningen / Centre for Information Technology) (publishedVersion, cc-by)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
- Funders
- NWO (OCENW.KLEIN.526)
- Topics
- Physical Sciences › Physics and Astronomy › Atomic and Molecular Physics, and Optics › Force Microscopy Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
- Health Sciences › Medicine › Oncology › Drug Transport and Resistance Mechanisms
- Keywords
- OpuA, ABC transporters, domain-domain interactions, protein stability, substrate-binding domain, osmoregulation, Lactococcus lactis, lipid nanodiscs, single-molecule force spectroscopy, optical tweezers, protein mechanical properties
- MeSH terms
- Protein Domains, Single Molecule Imaging, Bacterial Proteins, Lipid Bilayers, Protein Binding, Lactococcus lactis, ATP-Binding Cassette Transporters, Optical Tweezers, Protein Stability
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review