Probing nuclear pore complex architecture with proximity-dependent biotinylation
Open accessAbstract
Significance: Proximity-dependent biotinylation (BioID) is a readily accessible method for identifying protein associations that occur in living cells. Fusion of a promiscuous biotin ligase to a bait protein for expression in live cells enables covalent biotin labeling, and thus identification, of proteins proximate to the bait. Here we used BioID to probe the organization of the nuclear pore complex, a large structure that regulates molecular transport between the nucleus and cytoplasm. These studies enhance our understanding of major subcomplexes within the nuclear pore complex and demonstrate the utility of BioID for studying the organization of large protein assemblies. Additionally, we have measured the labeling radius of BioID, thus enabling the rational application of this method and more meaningful data interpretation.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
By fusing BirA* to a bait protein with a synaptic localization signal or nuclear pore signal, BirA* expression was specifically guided to the synapse or nuclear pore complex to achieve biotinylation of the respective proteomes.
“By fusing BirA* to a bait protein with a synaptic localization signal or nuclear pore signal, BirA* expression was specifically guided to the synapse or nuclear pore complex to achieve biotinylation of the respective proteomes [167, 168].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [167]
Cites
Roux, K. J., Kim, D. I., Raida, M., & Burke, B. (2012) · Journal of Cell Biology · doi:10.1083/jcb.201112098 · Cited by 2,416 · see citing works
Self-citationIdentification and characterization of a nuclear pore complex protein
Davis, L. I., & Blobel, G. (1986) · Cell · doi:10.1016/0092-8674(86)90784-1 · Cited by 620 · see citing works
A general amphipathic α-helical motif for sensing membrane curvature
Drin, G., Casella, J.-F., Gautier, R., Boehmer, T., Schwartz, T., & Antonny, B. (2007) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1194 · Cited by 572 · see citing works
D'Angelo, M. A., Raices, M., Panowski, S. H., & Hetzer, M. W. (2009) · Cell · doi:10.1016/j.cell.2008.11.037 · Cited by 565 · see citing works
The Structure of the Nuclear Pore Complex
Hoelz, A., Debler, E., & Blobel, G. (2011) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-060109-151030 · Cited by 525 · see citing works
BioID: A Screen for Protein‐Protein Interactions
Roux, K. J., Kim, D. I., & Burke, B. E. (2013) · Current Protocols in Protein Science · doi:10.1002/0471140864.ps1923s74 · Cited by 505 · see citing works
Self-citationDisorder in the nuclear pore complex: The FG repeat regions of nucleoporins are natively unfolded
Denning, D. P., Patel, S. S., Uversky, V. N., et al. (2003) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0437902100 · Cited by 503 · see citing works
Mapping the dynamic organization of the nuclear pore complex inside single living cells
Rabut, G. E. E., Doye, V., & Ellenberg, J. (2004) · Nature Cell Biology · doi:10.1038/ncb1184 · Cited by 476 · see citing works
Self-citationFornerod, M. W. J., van Deursen, J., van Baal, S., Reynolds, A. B., Davis, D. S., Murti, K. G., Fransen, J. A. M., & Grosveld, G. C. (1997) · The EMBO Journal · doi:10.1093/emboj/16.4.807 · Cited by 475 · see citing works
Couzens, A. L., Knight, J. D. R., Kean, M. J., Teo, G., Weiss, A., Dunham, W. H., Lin, Z., Bagshaw, R. D., Sicheri, F., Pawson, T. J., et al. (2013) · Science Signaling · doi:10.1126/scisignal.2004712 · Cited by 440 · see citing works
Nuclear Pore Scaffold Structure Analyzed by Super-Resolution Microscopy and Particle Averaging
Szymborska, A., de Marco, A., Daigle, N., Cordes, V. C., Briggs, J. A. G., & Ellenberg, J. (2013) · Science · doi:10.1126/science.1240672 · Cited by 434 · see citing works
Nuclear pore complex composition: a new regulator of tissue-specific and developmental functions
Raı́ces, M., & D’Angelo, M. A. (2012) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm3461 · Cited by 373 · see citing works
Nuclear pore complexes form immobile networks and have a very low turnover in live mammalian cells
Daigle, N., Beaudouin, J., Hartnell, L. M., Imreh, G., Hallberg, E., Lippincott‐Schwartz, J., & Ellenberg, J. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200101089 · Cited by 373 · see citing works
Integrated Structural Analysis of the Human Nuclear Pore Complex Scaffold
Bui, K. H., von Appen, A., DiGuilio, A. L., Ori, A., Sparks, L., Mackmull, M., Bock, T., Hagen, W. J. H., Andrés‐Pons, A., Glavy, J. S., et al. (2013) · Cell · doi:10.1016/j.cell.2013.10.055 · Cited by 351 · see citing works
Extremely long-lived nuclear pore proteins in the rat brain
Savas, J. N., Toyama, B. H., Xu, T., Yates, J. R., & Hetzer, M. W. (2012) · Science · doi:10.1126/science.1217421 · Cited by 335 · see citing works
Belgareh‐Touzé, N., Rabut, G. E. E., Baï, S. W., et al. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200101081 · Cited by 320 · see citing works
Hülsmann, B. B., Labokha, A. A., & Görlich, D. (2012) · Cell · doi:10.1016/j.cell.2012.07.019 · Cited by 313 · see citing works
Ori, A., Banterle, N., Iskar, M., Andrés‐Pons, A., Escher, C., Bui, K. H., Sparks, L., Solis‐Mezarino, V., Rinner, O., Peer Bork, B., et al. (2013) · Molecular Systems Biology · doi:10.1038/msb.2013.4 · Cited by 308 · see citing works
Schmitt, C., von Kobbe, C., Bachi, A., Panté, N., Rodrigues, J. P., Boscheron, C., Rigaut, G., Wilm, M. S., Séraphin, B., Carmo‐Fonseca, M., et al. (1999) · The EMBO Journal · doi:10.1093/emboj/18.15.4332 · Cited by 289 · see citing works
Functional Architecture of the Nuclear Pore Complex
Grossman, E., Medalia, O., & Zwerger, M. (2012) · Annual Review of Biophysics · doi:10.1146/annurev-biophys-050511-102328 · Cited by 275 · see citing works
Amlacher, S., Sarges, P., Flemming, D., van Noort, V., Kunze, R., Devos, D. P., Arumugam, M., Bork, P., & Hurt, E. (2011) · Cell · doi:10.1016/j.cell.2011.06.039 · Cited by 269 · see citing works
Loïodice, I., Alves, A., Rabut, G. E. E., van Overbeek, M., Ellenberg, J., Sibarita, J., & Doye, V. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e03-12-0878 · Cited by 266 · see citing works
Self-citationKrull, S., Thyberg, J., Björkroth, B., et al. (2004) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-03-0165 · Cited by 237 · see citing works
A complex of nuclear pore proteins required for pore function.
Finlay, D. R., Meier, E., Bradley, P. J., et al. (1991) · The Journal of Cell Biology · doi:10.1083/jcb.114.1.169 · Cited by 235 · see citing works
Functional association of Sun1 with nuclear pore complexes
Liu, Q., Panté, N., Misteli, T., et al. (2007) · The Journal of Cell Biology · doi:10.1083/jcb.200704108 · Cited by 234 · see citing works
Mansfeld, J., Güttinger, S., Hawryluk-Gara, L. A., Panté, N., Mall, M., Galy, V., Haselmann, U., Mühlhäusser, P., Wozniak, R. W., Mattaj, I. W., et al. (2006) · Molecular Cell · doi:10.1016/j.molcel.2006.02.015 · Cited by 221 · see citing works
The human Nup107–160 nuclear pore subcomplex contributes to proper kinetochore functions
Zuccolo, M., Alves, A., Galy, V., Morchoisne‐Bolhy, S., Formstecher, É., Racine, V., Sibarita, J., Fukagawa, T., Shiekhattar, R., Yen, T. J., et al. (2007) · The EMBO Journal · doi:10.1038/sj.emboj.7601642 · Cited by 206 · see citing works
Self-citationDifferential Mitotic Phosphorylation of Proteins of the Nuclear Pore Complex
Macaulay, C., Meier, E., & Forbes, D. J. (1995) · Journal of Biological Chemistry · doi:10.1074/jbc.270.1.254 · Cited by 199 · see citing works
Proximity Interactions among Centrosome Components Identify Regulators of Centriole Duplication
Firat‐Karalar, E. N., Rauniyar, N., Yates, J. R., & Stearns, T. (2014) · Current Biology · doi:10.1016/j.cub.2014.01.067 · Cited by 194 · see citing works
Novel vertebrate nucleoporins Nup133 and Nup160 play a role in mRNA export
Vasu, S. K., Shah, S., Orjalo, A. V., et al. (2001) · The Journal of Cell Biology · doi:10.1083/jcb.200108007 · Cited by 192 · see citing works
CEP120 and SPICE1 Cooperate with CPAP in Centriole Elongation
Comartin, D., Gupta, G. D., Fussner, E., et al. (2013) · Current Biology · doi:10.1016/j.cub.2013.06.002 · Cited by 179 · see citing works
Bernad, R., van der Velde, H., Fornerod, M. W. J., & Pickersgill, H. (2004) · Molecular and Cellular Biology · doi:10.1128/mcb.24.6.2373-2384.2004 · Cited by 177 · see citing works
Grandi, P., Dang, T., Pané, N., Shevchenko, A., Mann, M., Forbes, D. J., & Hurt, E. (1997) · Molecular Biology of the Cell · doi:10.1091/mbc.8.10.2017 · Cited by 155 · see citing works
Domain-specific antibodies reveal multiple-site topology of Nup153 within the nuclear pore complex
Fahrenkrog, B., Maco, B., Fager, A. M., et al. (2002) · Journal of Structural Biology · doi:10.1016/s1047-8477(02)00524-5 · Cited by 139 · see citing works
Novel Bilobe Components in Trypanosoma brucei Identified Using Proximity-Dependent Biotinylation
Morriswood, B., Havlicek, K., Demmel, L., Yavuz, S., Sealey-Cardona, M., Vidilaseris, K., Anrather, D., Kostan, J., Djinović-Carugo, K., Roux, K. J., et al. (2013) · Eukaryotic Cell · doi:10.1128/ec.00326-12 · Cited by 138 · see citing works
Self-citationPom121 links two essential subcomplexes of the nuclear pore complex core to the membrane
Mitchell, J. M., Mansfeld, J., Capitanio, J. S., et al. (2010) · The Journal of Cell Biology · doi:10.1083/jcb.201007098 · Cited by 124 · see citing works
The N and C Termini of ZO-1 Are Surrounded by Distinct Proteins and Functional Protein Networks
Itallie, C. M. V., Aponte, A. M., Tietgens, A. J., Guček, M., Fredriksson, K., & Anderson, J. M. (2013) · Journal of Biological Chemistry · doi:10.1074/jbc.m113.466193 · Cited by 118 · see citing works
Molecular Architecture of the Transport Channel of the Nuclear Pore Complex
Solmaz, S. R., Chauhan, R., Blobel, G., & Melčák, I. (2011) · Cell · doi:10.1016/j.cell.2011.09.034 · Cited by 104 · see citing works
Itallie, C. M. V., Tietgens, A. J., Aponte, A. M., Fredriksson, K., Fanning, A. S., Guček, M., & Anderson, J. M. (2013) · Journal of Cell Science · doi:10.1242/jcs.140475 · Cited by 96 · see citing works
Nuclear transport and the mitotic apparatus: an evolving relationship
Wozniak, R. W., Burke, B. E., & Doye, V. (2010) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-010-0325-7 · Cited by 90 · see citing works
Self-citationFunctional Characterization of a Nup159p-containing Nuclear Pore Subcomplex
Belgareh‐Touzé, N., Snay-Hodge, C., Pasteau, F., et al. (1998) · Molecular Biology of the Cell · doi:10.1091/mbc.9.12.3475 · Cited by 90 · see citing works
Nucleoporins: Leaving the nuclear pore complex for a successful mitosis
Chatel, G., & Fahrenkrog, B. (2011) · Cellular Signalling · doi:10.1016/j.cellsig.2011.05.023 · Cited by 89 · see citing works
Nup214-Nup88 Nucleoporin Subcomplex Is Required for CRM1-mediated 60 S Preribosomal Nuclear Export
Bernad, R., Engelsma, D., Sanderson, H. S., et al. (2006) · Journal of Biological Chemistry · doi:10.1074/jbc.m512585200 · Cited by 88 · see citing works
MarvelD3 couples tight junctions to the MEKK1–JNK pathway to regulate cell behavior and survival
Steed, E., Elbediwy, A., Vacca, B., et al. (2014) · The Journal of Cell Biology · doi:10.1083/jcb.201304115 · Cited by 86 · see citing works
Roth, P., Xylourgidis, N., Sabri, N., Uv, A., Fornerod, M. W. J., & Samakovlis, C. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200304046 · Cited by 86 · see citing works
Gle1 Functions during mRNA Export in an Oligomeric Complex that Is Altered in Human Disease
Folkmann, A. W., Collier, S. E., Zhan, X., Aditi, A., Ohi, M. D., & Wente, S. R. (2013) · Cell · doi:10.1016/j.cell.2013.09.023 · Cited by 81 · see citing works
Kendirgi, F., Rexer, D. J., Alcázar-Román, A. R., Onishko, H. M., & Wente, S. R. (2005) · Molecular Biology of the Cell · doi:10.1091/mbc.e04-11-0998 · Cited by 80 · see citing works
Nucleoporin Domain Topology is Linked to the Transport Status of the Nuclear Pore Complex
Paulillo, S. M., Phillips, E. M., Köser, J., et al. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.06.034 · Cited by 77 · see citing works
Cytoplasmic annulate lamellae in cultured cells: composition, distribution, and mitotic behavior
Cordes, V. C., Reidenbach, S., & Franke, W. W. (1996) · Cell and Tissue Research · doi:10.1007/s004410050578 · Cited by 74 · see citing works
Sachdev, R., Sieverding, C., Flötenmeyer, M., et al. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e11-09-0761 · Cited by 70 · see citing works
Nup53 interaction with Ndc1 and Nup155 are required for nuclear pore complex assembly
Eisenhardt, N., Redolfi, J., & Antonin, W. (2013) · Journal of Cell Science · doi:10.1242/jcs.141739 · Cited by 69 · see citing works
Nup53 Is Required for Nuclear Envelope and Nuclear Pore Complex Assembly
Hawryluk-Gara, L. A., Platani, M., Santarella, R. A., et al. (2008) · Molecular Biology of the Cell · doi:10.1091/mbc.e07-08-0820 · Cited by 66 · see citing works
Vollmer, B., & Antonin, W. (2014) · Biological Chemistry · doi:10.1515/hsz-2013-0285 · Cited by 61 · see citing works
Goeres, J., Chan, P.-K., Mukhopadhyay, D., et al. (2011) · Molecular Biology of the Cell · doi:10.1091/mbc.e10-12-0953 · Cited by 61 · see citing works
The mRNA Export Factor Human Gle1 Interacts with the Nuclear Pore Complex Protein Nup155
Rayala, H. J., Kendirgi, F., Barry, D. M., Majerus, P. W., & Wente, S. R. (2003) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m300106-mcp200 · Cited by 60 · see citing works
Fifty Years of Nuclear Pores and Nucleocytoplasmic Transport Studies
Floch, A. G., Palancade, B., & Doye, V. (2014) · Methods in cell biology · doi:10.1016/b978-0-12-417160-2.00001-1 · Cited by 59 · see citing works
Self-citationThierbach, K., von Appen, A., Thoms, M., et al. (2013) · Structure · doi:10.1016/j.str.2013.07.004 · Cited by 47 · see citing works
Brill, L. M., Motamedchaboki, K., Wu, S., & Wolf, D. A. (2009) · Methods · doi:10.1016/j.ymeth.2009.02.023 · Cited by 46 · see citing works
Self-citationBilokapić, S., & Schwartz, T. (2013) · Structure · doi:10.1016/j.str.2013.02.006 · Cited by 40 · see citing works
Domain Topology of the p62 Complex Within the 3-D Architecture of the Nuclear Pore Complex
Schwarz-Herion, K., Maco, B., Sauder, U., et al. (2007) · Journal of Molecular Biology · doi:10.1016/j.jmb.2007.05.030 · Cited by 36 · see citing works
González‐Aguilera, C., & Askjaer, P. (2012) · Nucleus · doi:10.4161/nucl.21135 · Cited by 34 · see citing works
Eukaryotic Chaperonins: Lubricating the Folding of WD-repeat Proteins
Craig, E. A. (2003) · Current Biology · doi:10.1016/j.cub.2003.11.009 · Cited by 27 · see citing works
Interaction of Nup53 with Ndc1 and Nup155 is required for nuclear pore complex assembly
Eisenhardt, N., Redolfi, J., & Antonin, W. (2014) · Max Planck Institute for Plasma Physics · Cited by 19 · see citing works
Stochaj, U., Bański, P., Kodiha, M., & Matusiewicz, N. (2006) · Experimental Cell Research · doi:10.1016/j.yexcr.2006.04.007 · Cited by 14 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Efficient proximity labeling in living cells and organisms with TurboID
Branon, T. C., Bosch, J. A., Sanchez, A. D., Udeshi, N. D., Svinkina, T., Carr, S. A., Feldman, J. L., Perrimon, N., & Ting, A. Y. (2018) · Nature Biotechnology · doi:10.1038/nbt.4201 · Cited by 2,174 · see citing works
Deciphering molecular interactions by proximity labeling
Qin, W., Cho, K. F., Cavanagh, P. E., & Ting, A. Y. (2021) · Nature Methods · doi:10.1038/s41592-020-01010-5 · Cited by 671 · see citing works
Identification of an elaborate complex mediating postsynaptic inhibition
Uezu, A., Kanak, D. J., Bradshaw, T. W. A., Soderblom, E. J., Catavero, C. M., Burette, A. C., Weinberg, R. J., & Soderling, S. H. (2016) · Science · doi:10.1126/science.aag0821 · Cited by 354 · see citing works
Franjic, D., Skarica, M., Ma, S., Arellano, J. I., Tebbenkamp, A. T. N., Choi, J., Xu, C., Li, Q., Morozov, Y. M., Andrijevic, D., et al. (2022) · Neuron · doi:10.1016/j.neuron.2021.10.036 · Cited by 308 · see citing works
A molecular switch from STAT2-IRF9 to ISGF3 underlies interferon-induced gene transcription
Platanitis, E., Demiroz, D., Schneller, A., Fischer, K., Capelle, C., Hartl, M., Gossenreiter, T., Müller, M., Novatchkova, M., & Decker, T. (2019) · Nature Communications · doi:10.1038/s41467-019-10970-y · Cited by 233 · see citing works
Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau
Rayaprolu, S., Higginbotham, L., Bagchi, P., Watson, C. M., Zhang, T., Levey, A. I., Rangaraju, S., & Seyfried, N. T. (2021) · Neuropsychopharmacology · doi:10.1038/s41386-020-00840-3 · Cited by 118 · see citing works
The TRIM9/TRIM67 neuronal interactome reveals novel activators of morphogenesis
Menon, S., Goldfarb, D., Ho, C. T., Cloer, E. W., Boyer, N. P., Hardie, C., Bock, A. J., Johnson, E. C., Anil, J., Major, M. B., et al. (2021) · Molecular Biology of the Cell · doi:10.1091/mbc.e20-10-0622 · Cited by 46 · see citing works
Cancer proteome and metabolite changes linked to SHMT2
Tong, J., Krieger, J. R., Taylor, P., Bagshaw, R., Kang, J., Jeedigunta, S., Wybenga-Groot, L. E., Zhang, W., Badr, H., Mirhadi, S., et al. (2020) · PLoS ONE · doi:10.1371/journal.pone.0237981 · Cited by 24 · see citing works
- Authors
- Kim, D. I., KC, B., Zhu, W., Motamedchaboki, K., Doye, V., & Roux, K. J.
- Affiliations
- Sanford Research (US)
- Sanford Burnham Prebys Medical Discovery Institute (US)
- Centre National de la Recherche Scientifique (FR)
- University of South Dakota (US)
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2014-06-03
- Volume
- 111
- Issue
- 24
- Pages
- E2453-61
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC4066523
- OpenAlex
- W2035671523
- Cited by
- 560
- References
- 64
- Citations by year
- 2026: 39 · 2025: 49 · 2024: 57 · 2023: 42 · 2022: 50 · 2021: 59 · 2020: 82 · 2019: 51 · 2018: 42 · 2017: 29 · 2016: 34 · 2015: 21 · 2014: 2 · 2013: 1
- FWCI
- 11.75
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-12-BSV2-0008)
- National Institute of General Medical Sciences (P20GM103620, R01GM102203, R01GM102486, P20GM103548)
- National Institute of Biomedical Imaging and Bioengineering (R01EB014869)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Nuclear Structure and Function
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Biotin and Related Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Keywords
- nuclear pore complex, proximity biotinylation, BioID, protein-protein interaction, nuclear transport, nuclear envelope, protein complex structure
- MeSH terms
- Algorithms, Biotin, Cell Nucleus, Chromatography, Liquid, Cytoplasm, Humans, Ligases, Membrane Glycoproteins, Nuclear Envelope, Protein Binding, Transfection, Carbon-Nitrogen Ligases, Streptavidin, Biotinylation, Nuclear Pore, Nuclear Pore Complex Proteins, Green Fluorescent Proteins, Tandem Mass Spectrometry, HEK293 Cells
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
