Cited by 667Protein Structure and DynamicsLipid Membrane Structure and BehaviorIon channel regulation and function

The DOI matches its Crossref record; 34 of the 34 references it cites were found in a registry or an index.

Solution Structure of the Integral Human Membrane Protein VDAC-1 in Detergent Micelles

Open access

Hiller, Sebastian, Garces, Robert G., Malia, Thomas J., Orekhov, Vladislav Y., Colombini, Marco, Wagner, Gerhard·2008·Science

DOI 10.1126/science.1161302PMC PMC2579273

Open this paper in CoChat — free account

Abstract

The voltage-dependent anion channel (VDAC) mediates trafficking of small molecules and ions across the eukaryotic outer mitochondrial membrane. VDAC also interacts with antiapoptotic proteins from the Bcl-2 family, and this interaction inhibits release of apoptogenic proteins from the mitochondrion. We present the nuclear magnetic resonance (NMR) solution structure of recombinant human VDAC-1 reconstituted in detergent micelles. It forms a 19-stranded β barrel with the first and last strand parallel. The hydrophobic outside perimeter of the barrel is covered by detergent molecules in a beltlike fashion. In the presence of cholesterol, recombinant VDAC-1 can form voltage-gated channels in phospholipid bilayers similar to those of the native protein. NMR measurements revealed the binding sites of VDAC-1 for the Bcl-2 protein Bcl-x L , for reduced β–nicotinamide adenine dinucleotide, and for cholesterol. Bcl-x L interacts with the VDAC barrel laterally at strands 17 and 18.

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

Crossref · 10.1126/science.1161302

Cites

34 of 34 references verified0 citation errors · 0 not checkable

Statistics

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.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

NMR with Proteins and Nucleic Acids
Wüthrich, K. (1986) · Europhysics news · doi:10.1051/epn/19861701011 · Cited by 8,028
Cell Death
Danial, N. N., & Korsmeyer, S. J. (2004) · Cell · doi:10.1016/s0092-8674(04)00046-7 · Cited by 4,651
Mitochondrial membrane permeabilization in cell death
Kroemer, G., Galluzzi, L., & Brenner, C. (2007) · Physiological Reviews · doi:10.1152/physrev.00013.2006 · Cited by 3,598
Global, In Vivo, and Site-Specific Phosphorylation Dynamics in Signaling Networks
Olsen, J. V., Blagoev, B., Gnad, F., Maček, B., Kumar, C., Mortensen, P., & Mann, M. (2006) · Cell · doi:10.1016/j.cell.2006.09.026 · Cited by 3,562
Bcl-2 family proteins regulate the release of apoptogenic cytochrome c by the mitochondrial channel VDAC
Shimizu, S., Narita, M., Tsujimoto, Y., & Tsujimoto, Y. (1999) · Nature · doi:10.1038/20959 · Cited by 2,178
Mitochondria as the central control point of apoptosis
Desagher, S., & Martinou, J. (2000) · Trends in Cell Biology · doi:10.1016/s0962-8924(00)01803-1 · Cited by 1,935
Bcl-2 proteins: regulators of apoptosis or of mitochondrial homeostasis?
Heiden, M. G. V., & Thompson, C. B. (1999) · Nature Cell Biology · doi:10.1038/70237 · Cited by 660
Reconstitution in planar lipid bilayers of a voltage-dependent anion-selective channel obtained from paramecium mitochondria
Schein, S. J., Colombini, M., & Finkelstein, A. (1976) · The Journal of Membrane Biology · doi:10.1007/bf01869662 · Cited by 509
Self-citation
VDAC: The channel at the interface between mitochondria and the cytosol
Colombini, M. (2003) · Molecular and Cellular Biochemistry · doi:10.1023/b:mcbi.0000009862.17396.8d · Cited by 500
Self-citation
A candidate for the permeability pathway of the outer mitochondrial membrane
Colombini, M. (1979) · Nature · doi:10.1038/279643a0 · Cited by 468
Self-citation

Show all 34 references

Research works printed but not linked: 1

This work was supported by NIH roadmap grant GM075879. Purchase operation and maintenance of instruments used were supported by NIH grants GM066360 GM47467 and EB002026. S.H. was supported by the Swiss National Science Foundation. V.Y.O. was supported by the Wenner-Gren Foundation Stockholm. Initial research on this project was supported by the Ludwig Foundation for Cancer Research. We thank V. Gelev from FBReagents.com Cambridge Massachusetts for custom synthesis of the 2 H-LDAO; S. Samanta for help with the electrophysiological measurements; and D. Frueh A. Koglin Z.-Y. J. Sun K. Oxenoid and S. Jenni for technical help and valuable discussions. The atomic coordinates of VDAC-1 in LDAO micelles have been deposited at the Protein Data Bank with code 2k4t.

Sorted by citations

Items 601–665 of 665

Crystalline, membrane-embedded, and fibrillar proteins investigated by solid-state NMR spectroscopy
Schneider, R. (2009) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-2601 · Cited by 1
Unlocking the Distinct Roles of the Three Mammalian VDAC Isoforms in Mitochondrial Respiration and Cancer Cell MetabolismPreprint
Rajendran, M., Rosencrans, W. M., Fitzgerald, W., Huynh, D., Beyene, B. G., Quan, B., Hwang, J., Bautista, N. A., Chou, T., Bezrukov, S. M., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.20.639106 · Cited by 1
Untersuchung sub-mitochondrialer Proteinverteilungen in unbehandelten und apoptotischen humanen Zellen mittels STED-Mikroskopie
Neumann, D. (2010) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-383
The proteomic approach to investigate Parkinson's desease: pathogenetic mechanisms and biomarkers discovery.
Alberio, T. (2010) · IrInSubria (University of Insubria)
Solution NMR-based characterization of the structure of the outer mitochondrial membrane protein Tom40 and a novel method for NMR resonance assignment of large intrinsically disordered proteins
Yao, X. (2014) · doi:10.53846/goediss-4489
Electrophysiological Techniques for Mitochondrial Channels
Schindl, R., & Weghuber, J. (2012) · InTech eBooks · doi:10.5772/37088
Database Development And Discrimination Algorithms For Membrane Protein Functions
Gromiha, M. M., Yabuki, Y., Imai, K., Horton, P., & Fukui, K. (2009) · doi:10.5281/zenodo.1057650
Targets and Strategies for the Mitochondrial Assault on Cancer
Biasutto, L., Szabó, I., & Zoratti, M. (2014) · Springer eBooks · doi:10.1007/978-94-017-8984-4_9
Isoforms of voltage-dependent anion channel of the outer mitochondrial membrane and experimental models to study their physiological role
Teplova, V. V., Odinokova, I. V., & Holmuhamedov, E. (2011) · Biochemistry (Moscow) Supplement Series A Membrane and Cell Biology · doi:10.1134/s1990747811020085
Isolation, functional characterization and crystallization of Aq_1259, an outer membrane protein with porin features, from Aquifex aeolicus
Wang, T., Langer, J. D., Peng, G., & Michel, H. (2012) · Biochimica et Biophysica Acta (BBA) - Proteins and Proteomics · doi:10.1016/j.bbapap.2012.07.004
Association between VDAC1 mRNA expression and intracellular ATP levels of cultured L-02 hepatocytes during hexavalent chromium toxicity
Yuan, Y. (2011) · AFRICAN JOURNAL OF BIOTECHNOLOGY · doi:10.5897/ajb11.3120
At the Crossroads Between Mitochondrial Metabolite Transport and Apoptosis: VDAC1 as an Emerging Cancer Drug Target
Shoshan‐Barmatz, V., Shteinfer‐Kuzmine, A., Ben-Hail, D., Arif, T., & Mizrachi, D. (2014) · Springer eBooks · doi:10.1007/978-94-017-9421-3_16
Bcl-2 Regulates Proapoptotic Calcium Signals by Interacting with the Inositol 1, 4, 5-Trisphosphate Receptor
Rong, Y. (2008) · OhioLink ETD Center (Ohio Library and Information Network)
Application of random coherence order selection in gradient-enhanced multidimensional NMR
Bostock, M. J., & Nietlispach, D. (2016) · Journal of Physics Conference Series · doi:10.1088/1742-6596/699/1/012004
The use of nuclear magnetic resonance in study of structurally dynamic membrane proteins
Phillips, M. (2016) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/68476
Proteome study of nasopharyngeal carcinoma
Feng, X. (2012) · doi:10.32657/10356/50504
Roles of periplasmic chaperones and BamA in outer membrane protein folding
Schiffrin, R. (2016) · White Rose eTheses Online (University of Leeds, The University of Sheffield, University of York)
Local mitochondrial-endolysosomal microfusion cleaves the
Brahimi-Horn, M. C., Lacas‐Gervais, S., Adaixo, R., Ilc, K., Rouleau, M., Notte, A., Dieu, M., Michels, C., Voeltzel, T., Maguer‐Satta, V., et al. (2015)
Self-citation
Structural plasticity of BCL-2 family proteins and its functional implication in apoptosis
Choi, M. (2018) · DR-NTU (Nanyang Technological University) · doi:10.32657/10356/73522
Membrane Proteins and Their Natural Environment
Popot, J. (2018) · Biological and medical physics, biomedical engineering · doi:10.1007/978-3-319-73148-3_1
Spectroscopic Studies of Membrane Protein Structure, Dynamics, and Function
Lo, R. H. (2014) · doi:10.18130/v3n231
Elucidation of protein interactions in complex samples by protein-protein cross-linking of synaptosomes
Parfentev, I. (2019) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-7615
Smart hybrid nanomaterials for biomimetic membranes
Lopes‐Rodrigues, M. (2019) · doi:10.5821/dissertation-2117-173360
Elucidation of protein-protein interactions in mitochondria by cross-linking mass spectrometry
Linden, A. (2020) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-8148
BAD Phosphorylation: A Novel Link between Apoptosis and Cancer
Polzien, L. (2011)
Molecular mechanism of thiamine pyrophosphate import into mitochondria: a molecular simulation study
Liefferinge, F. V., Krammer, E., Waeytens, J., & Prévost, M. (2021) · Journal of Computer-Aided Molecular Design · doi:10.1007/s10822-021-00414-5
DNA-Nanotube-Enabled NMR Structure Determination of Membrane Proteins
Min, J., Shih, W. M., & Bellot, G. (2013) · Springer eBooks · doi:10.1007/978-3-642-36077-0_16
In and through the membrane by solid-state NMR: investigations of the human voltage-dependent anion channel 1 and Nup98-derived FG-domains
Najbauer, E. É. (2022) · eDiss (Georg-August-Universität Göttingen) · doi:10.53846/goediss-52
References
(2013) · Elsevier eBooks · doi:10.1016/b978-0-12-388425-1.00023-3
Faculty Opinions recommendation of Facile backbone structure determination of human membrane proteins by NMR spectroscopy.
Doren, S. R. V. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.716747901.793003008
NMR Solution Structure of Opa60: a Neisserial Membrane Protein That Mediates Host Phagocytosis
Fox, D. A. (2013) · doi:10.18130/v36k1d
Faculty Opinions recommendation of Facile backbone structure determination of human membrane proteins by NMR spectroscopy.
Columbus, L. M., & Dewald, A. H. (2012) · Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature · doi:10.3410/f.716747901.792102901
Membranes, Minerals and Magnets: Application of NMR Spectroscopy to Biological Interfaces
Kent, J. E., Shin, K., & Marassi, F. M. (2022) · Royal Society of Chemistry eBooks · doi:10.1039/9781839165702-00496
Pseudocontact shift NMR data obtained from a non-canonical amino acid-linked lanthanide tag improves integral membrane protein structure predictionPreprint
Ledwitch, K. V., Künze, G., Larochelle, K., Okwei, E., Pankewitz, L., Ganguly, S., Darling, H. L., Coin, I., & Meiler, J. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.09.14.507970
NMR of Membrane Proteins
Bostock, M. J., & Nietlispach, D. (2012) · Royal Society of Chemistry eBooks · doi:10.1039/9781849731201-00271
Modular Assembly of Mitochondrial β-Barrel Proteins
Bhowmik, R., den Brave, F., & Becker, T. (2024) · Methods in molecular biology · doi:10.1007/978-1-0716-3734-0_13
NMR Analysis of Dog Erythrocytic Membrane Antigen
Kalaiselvi, G., Tirumurugaan, K. G., Raj, G. D., Vijayarani, K., & Baranidharan, R. (2024) · Asian Journal of Research in Biochemistry · doi:10.9734/ajrb/2024/v14i3286
Generation of TIM chaperone substrate complexes
Guillerm, U., Sučec, I., & Schanda, P. (2024) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/bs.mie.2024.07.051
Pore-Forming VDAC Proteins of the Outer Mitochondrial Membrane: Regulation and Pathophysiological Role (Review)
Belosludtseva, N. V., Dubinin, M. V., & Belosludtsev, K. N. (2024) · Biochemistry (Moscow) · doi:10.31857/s0320972524060075
Structural Study of Proteins Using Paramagnetic Lanthanide Probe Methods
Saio, T., & Inagaki, F. (2025) · Springer eBooks · doi:10.1007/978-981-97-6834-9_9
Structure and Dynamic Properties of Membrane Proteins using NMR
Rösner, H. I., & Kragelund, B. B. (2012) · Comprehensive physiology · doi:10.1002/j.2040-4603.2012.tb00430.x
Structural characterization of intra- and intermolecular disulfide bonds in voltage-dependent anion channel 3 (VDAC3) protein from Rattus norvegicus by high-resolution mass spectrometry
Pittalà, M. G. G., Cucina, A., Nibali, S. C., Cunsolo, V., Francesco, A. D., Battiato, G., Reina, S., Foti, S., Pinto, V. D., & Saletti, R. (2025) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-025-06074-w
Integrative NMR methods for structure determination of membrane proteins and their complexes in lipid bilayers
Veglia, G. (2025) · Elsevier eBooks · doi:10.1016/b978-0-323-99507-8.00011-1
Regulation of BAX/BAK-Dependent Cell Death Program
Kim, H. (2009) · Open Scholarship Institutional Repository (Washington University in St. Louis) · doi:10.7936/k7rb72m2
Solution NMR spectroscopy of integral membrane proteins
Chou, J. J., & Hiller, S. (2026) · Elsevier eBooks · doi:10.1016/b978-0-323-99507-8.00040-8
Self-citation
Investigation des interfaces hydrophobes de l'Aquaporine Z chez Escherichia coli
Schmidt, V. (2017) · theses.fr (ABES) · doi:10.70675/d7459d32z7439z406ez9d44z36c1b3b39c5f
Translocator protein (TSPO) functions on erythropoiesis and red blood cell infection by plasmodium falciparum
Marginedas-Freixa, I. (2017) · theses.fr (ABES) · doi:10.70675/c493d7f5zc4b3z4debzb54fza7d98f55233f
Characterization of the human mitochondrial Arginyl-tRNA synthetase and contribution to the général understanding of pathologies linked to mutations on mitochondrial aminoacyl-tRNA synthetases
González-Serrano, L. E. (2018) · doi:10.70675/b6a327bcz96b3z4d5fz815cz9c041822cd98
Role of VDAC1 hypoxic form, VDAC1-∆C, in the expression of primary cilia and tumor progression
Fabbri, L. (2019) · theses.fr (ABES) · doi:10.70675/7a53239dzc652z4ea4z8b95z4a71961c83b4
Rôle de la signalisation calcique dans les troubles métaboliques associés à la dysfonction myocardique
Lacôte, M. (2018) · theses.fr (ABES) · doi:10.70675/bc9b8426z5718z40e1zadc2zaa52fb20a6fd
Involvements of Bcl-2 family of proteins during early zebrafish development
Popgeorgiev, N. (2011) · theses.fr (ABES) · doi:10.70675/d1fa4100z5c50z4a30z9f26z0ee43285ce5f
Rôles des régulateurs de l’apoptose Bcl-wav et Nrz, au cours du développement embryonnaire du poisson zèbre
Prudent, J. (2011) · theses.fr (ABES) · doi:10.70675/1f03460cze5d6z42c6za18ez352e34a4dee4
Études structurales et fonctionnelles des récepteurs P2X7
Dunning, K. (2020) · theses.fr (ABES) · doi:10.70675/a39c429dz8340z4575z9559z7e2f57c656e9
Bcl2L10 : polymorphisme, résistance oncogénique et conséquences thérapeutique dans le cancer du sein
Quang, D. M. (2021) · theses.fr (ABES) · doi:10.70675/86dd7fafzcb40z4cedz8eb7zbb41268cd809
Etude in vivo du rôle du métabolisme énergétique et mitochondrial dans la résistance thérapeutique des leucémies aiguës myéloïdes
Bosc, C. (2020) · theses.fr (ABES) · doi:10.70675/e3489aa8z78d2z46e0z9435z78857025209c
Etude moléculaire des étapes initiales d'importation de protéines mitochondriales
Sučec, I. (2022) · theses.fr (ABES) · doi:10.70675/b93c1147zace8z4b3ezab9azaed46edfeac5
Développement de peptides ciblant VDAC pour l’étude et le traitement de maladies démyélinisantes
Jacquard, M. F. (2023) · theses.fr (ABES) · doi:10.70675/33c8bd67z22cfz47b0zb14bz58b975b2f7d4
Could the overexpression of neuroglobin, via an intravenous administration of an AAV2/9 vector, durably attenuate cerebellar ataxia in Harlequin mice by preserving mitochondrial homeostasis?
Ratcliffe, E. (2025) · theses.fr (ABES) · doi:10.70675/381af2e4zf397z4e20z8f8dz5b80b0f86450
Small molecule inhibition of voltage dependent anion channel 1 reroutes mitochondrial metabolite flux
Modaresi, S. M., Zhang, L., Saei, A. A., Degen, M., Khavani, M., Gharibi, H., Végvári, Á., Ye, Z., Zhang, J., Pavlov, E. V., et al. (2026) · Molecules and Cells · doi:10.1016/j.mocell.2026.100369
Self-citation
Solution NMR Spectroscopy for the Determination of Structures of Membrane Proteins in a Lipid Environment
Pandey, R. S., & Arora, A. (2026) · Methods in molecular biology · doi:10.1007/978-1-0716-5054-7_25
Monitoring Membrane Protein Folding Assisted by Insertases and Translocases Using AFM-Based Single-Molecule Force Spectroscopy
Serdiuk, T., Thoma, J., & Müller, D. J. (2026) · Chemical Reviews · doi:10.1021/acs.chemrev.5c00960
Elliptical β ‐barrel deformation underlies gating in VDAC1
Bergdoll, L. A., Elgeti, M., Belyaeva, J., Zlobin, A. S., Duneau, J., Hubbell, W. L., & Abramson, J. (2026) · Protein Science · doi:10.1002/pro.70677
The TOM Complex in the Outer Membrane of Mitochondria: A Supramolecular Assembly for Protein Import
Nußberger, S., Ghosh, R., & Wang, S. (2026) · Advances in experimental medicine and biology · doi:10.1007/978-3-032-26629-3_5
So similar, yet so different: α-synuclein recognition of the isoform-specific VDAC protein–lipid interfacePreprint
Rostovtseva, T. K., Rajendran, M., Rosencrans, W. M., Queralt-Martín, M., Wolfe, M. S., Bautista, N. A., Beyene, B. G., Larimi, M. G., Sodt, A. J., & Bezrukov, S. M. (2026) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.64898/2026.10.13.758914
The opioid peptide dynorphin A : Biophysical studies of peptide–receptor and peptide–membrane interactions
Björnerås, J. (2014) · KTH Publication Database DiVA (KTH Royal Institute of Technology)

Authors: Hiller, S., Garces, R. G., Malia, T. J., Orekhov, V. Y., Colombini, M., & Wagner, G.
Affiliations: Harvard University (US)
Corresponding author: Garces, Robert G.
Malia, Thomas J.
Wagner, Gerhard
ORCID: Hiller, Sebastian
Orekhov, Vladislav Y.
Colombini, Marco
Wagner, Gerhard
Venue: Science
Publisher: American Association for the Advancement of Science (AAAS)
Published: 2008-08-29
Volume: 321
Issue: 5893
Pages: 1206-1210
ISSN: 0036-8075 (ISSN-L)
1095-9203
DOI: 10.1126/science.1161302
PMC: PMC2579273
OpenAlex: W1986199954
Cited by: 667
References: 34
Citations by year: 2026: 13 · 2025: 16 · 2024: 23 · 2023: 21 · 2022: 21 · 2021: 45 · 2020: 35 · 2019: 29 · 2018: 39 · 2017: 38 · 2016: 51 · 2015: 37 · 2014: 53 · 2013: 40 · 2012: 49
FWCI: 21.42
Type: journal article
Language: en
Open access: green
www.ncbi.nlm.nih.gov
Locations: Science (publishedVersion)
PubMed (publishedVersion)
PubMed Central (acceptedVersion)
Funders: National Institute of General Medical Sciences (P41GM066360, R01GM075879, GM 075879, GM-066360, GM47467, P01GM047467)
National Institute of Biomedical Imaging and Bioengineering (EB 002026, P41EB002026)
Topics: Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Protein Structure and Dynamics
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Lipid Membrane Structure and Behavior
Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Ion channel regulation and function
Keywords: VDAC1, voltage-dependent anion channel, mitochondrial outer membrane, beta-barrel membrane proteins, detergent micelles, Bcl-xL, Bcl-2 family proteins, apoptosis, cholesterol binding, NAD+ binding, voltage-gated ion channels, protein solution structure
MeSH terms: Amino Acid Sequence, Binding Sites, Cholesterol, Detergents, Dimethylamines, Humans, Lipid Bilayers, Micelles, Molecular Sequence Data, NAD, Protein Conformation, Recombinant Proteins, Ion Channel Gating, Protein Structure, Secondary, Protein Folding, Nuclear Magnetic Resonance, Biomolecular, Voltage-Dependent Anion Channel 1, bcl-X Protein, Static Electricity, Hydrophobic and Hydrophilic Interactions

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

Solution Structure of the Integral Human Membrane Protein VDAC-1 in Detergent Micelles

Abstract

Overview

Integrity signals

Verification

Claims the paper makes

Claims other papers make about this one

Self-check

Citations

Cites

Cited by

Related

Metadata

Record

About these checks