Efficient proximity labeling in living cells and organisms with TurboID
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Abstract
Protein interaction networks and protein compartmentalization underlie all signaling and regulatory processes in cells. Enzyme-catalyzed proximity labeling (PL) has emerged as a new approach to study the spatial and interaction characteristics of proteins in living cells. However, current PL methods require over 18 h of labeling time or utilize chemicals with limited cell permeability or high toxicity. We used yeast display-based directed evolution to engineer two promiscuous mutants of biotin ligase, TurboID and miniTurbo, which catalyze PL with much greater efficiency than BioID or BioID2, and enable 10-min PL in cells with non-toxic and easily deliverable biotin. Furthermore, TurboID extends biotin-based PL to flies and worms.
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Promiscuous biotin ligases such as BioID and TurboID have been proven effective for intracellular labeling in vivo.
“Promiscuous biotin ligases, another major type of PL enzyme such as BioID18 and TurboID19, have been proven effective for intracellular labeling in vivo.”
From Spatiotemporally resolved mapping of extracellular proteomes via in vivo-compatible TyroID (2025) · cites this paper as [19]
BioID was used to effectively label proteins within flies or worms.
“More recently, BioID was used to effectively label proteins within flies (Drosophila melanogaster) or worms (Caenorhabditis elegans) [169].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [169]
TurboID-based proteome labeling has been successfully applied in flies and worms without much toxicity and with high labeling efficiency.
“TurboID-based proteome labeling has been successfully applied in flies and worms without much toxicity and with high labeling efficiency [169].”
From Systems-based proteomics to resolve the biology of Alzheimer’s disease beyond amyloid and tau (2021) · cites this paper as [169]
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Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
THE GENETICS OF CAENORHABDITIS ELEGANS
Brenner, S. (1974) · Genetics · doi:10.1093/genetics/77.1.71 · Cited by 14,984 · see citing works
Krogh, A., Larsson, B., von Heijne, G., & Sonnhammer, E. L. L. (2001) · Journal of Molecular Biology · doi:10.1006/jmbi.2000.4315 · Cited by 12,654 · see citing works
UniProt: the Universal Protein knowledgebase
Apweiler, R. (2003) · Nucleic Acids Research · doi:10.1093/nar/gkh131 · Cited by 7,535 · see citing works
Current protocols in molecular biology
Dudley, R. K. (1988) · FEBS Letters · doi:10.1016/0014-5793(88)80264-3 · Cited by 6,037 · see citing works
UniProt: the universal protein knowledgebase
The UniProt Consortium (2017) · Nucleic Acids Research · doi:10.1093/nar/gkw1099 · Cited by 4,436 · see citing works
The embryonic cell lineage of the nematode Caenorhabditis elegans
Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90201-4 · Cited by 4,199 · see citing works
Gene Ontology Consortium: going forward
The Gene Ontology Consortium (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1179 · Cited by 3,492 · see citing works
A subcellular map of the human proteome
Thul, P. J., Åkesson, L., Wiking, M., Mahdessian, D., Geladaki, A., Ait Blal, H., Alm, T., Asplund, A., Björk, L., Breckels, L. M., et al. (2017) · Science · doi:10.1126/science.aal3321 · Cited by 2,813 · see citing works
A Combined Transmembrane Topology and Signal Peptide Prediction Method
Käll, L., Krogh, A., & Sonnhammer, E. L. L. (2004) · Journal of Molecular Biology · doi:10.1016/j.jmb.2004.03.016 · Cited by 2,474 · see citing works
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
A Mitochondrial Protein Compendium Elucidates Complex I Disease Biology
Pagliarini, D. J., Calvo, S. E., Chang, B., Sheth, S. A., Vafai, S. B., Ong, S.-E., Walford, G. A., Sugiana, C., Boneh, A., Chen, W. K., et al. (2008) · Cell · doi:10.1016/j.cell.2008.06.016 · Cited by 1,994 · see citing works
Self-citationDirected evolution of APEX2 for electron microscopy and proximity labeling
Lam, S. S., Martell, J. D., Kamer, K. J., Deerinck, T. J., Ellisman, M. H., Mootha, V. K., & Ting, A. Y. (2014) · Nature Methods · doi:10.1038/nmeth.3179 · Cited by 1,404 · see citing works
Self-citationProteomic Mapping of Mitochondria in Living Cells via Spatially Restricted Enzymatic Tagging
Martell, J. D., Ting, A. Y., Rhee, H., Zou, P., Udeshi, N. D., Mootha, V. K., & Carr, S. A. (2012) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 1,330 · see citing works
Self-citationSultan, M., Schulz, M. H., Richard, H., Magen, A., Klingenhoff, A., Scherf, M., Seifert, M., Borodina, T., Soldatov, A., Parkhomchuk, D., et al. (2008) · Science · doi:10.1126/science.1160342 · Cited by 1,293 · see citing works
MitoCarta2.0: an updated inventory of mammalian mitochondrial proteins
Calvo, S. E., Clauser, K. R., & Mootha, V. K. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkv1003 · Cited by 1,251 · see citing works
Isolating and engineering human antibodies using yeast surface display
Chao, G., Lau, W. L., Hackel, B. J., Sazinsky, S. L., Lippow, S. M., & Wittrup, K. D. (2006) · Nature Protocols · doi:10.1038/nprot.2006.94 · Cited by 913 · see citing works
An improved smaller biotin ligase for BioID proximity labeling
Kim, D. I., Jensen, S. C., Noble, K. A., Birendra, K. C., Roux, K. H., Motamedchaboki, K., & Roux, K. J. (2016) · Molecular Biology of the Cell · doi:10.1091/mbc.e15-12-0844 · Cited by 822 · see citing works
Stack, E. C., Wang, C., Roman, K., & Hoyt, C. C. (2014) · Methods · doi:10.1016/j.ymeth.2014.08.016 · Cited by 779 · see citing works
Catalyzed reporter deposition, a novel method of signal amplification application to immunoassays
Bobrow, M. N., Harris, T. D., Shaughnessy, K. J., & Litt, G. J. (1989) · Journal of Immunological Methods · doi:10.1016/0022-1759(89)90104-x · Cited by 774 · see citing works
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Martell, J. D., Deerinck, T. J., Sancak, Y., Poulos, T. L., Mootha, V. K., Sosinsky, G. E., Ellisman, M. H., & Ting, A. Y. (2012) · Nature Biotechnology · doi:10.1038/nbt.2375 · Cited by 722 · see citing works
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Perkins, L. A., Holderbaum, L., Tao, R., Hu, Y., Sopko, R., McCall, K., Yang‐Zhou, D., Flockhart, I., Binari, R. C., Shim, H.-S., et al. (2015) · Genetics · doi:10.1534/genetics.115.180208 · Cited by 634 · see citing works
Self-citationProbing nuclear pore complex architecture with proximity-dependent biotinylation
Kim, D. I., KC, B., Zhu, W., Motamedchaboki, K., Doye, V., & Roux, K. J. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1406459111 · Cited by 560 · see citing works
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Bauer, J., Hengsbach, S., Tesari, I., Schwaiger, R., & Kraft, O. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1315147111 · Cited by 560 · see citing works
Spatially resolved proteomic mapping in living cells with the engineered peroxidase APEX2
Hung, V., Udeshi, N. D., Lam, S. S., Loh, K. H., Cox, K. J., Pedram, K., Carr, S. A., & Ting, A. Y. (2016) · Nature Protocols · doi:10.1038/nprot.2016.018 · Cited by 541 · see citing works
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Markstein, M., Pitsouli, C., Villalta, C., Celniker, S., & Perrimon, N. (2008) · Nature Genetics · doi:10.1038/ng.101 · Cited by 516 · see citing works
Self-citationAn Approach to Spatiotemporally Resolve Protein Interaction Networks in Living Cells
Lobingier, B. T., Hüttenhain, R., Eichel, K., Miller, K. B., Ting, A. Y., von Zastrow, M., & Krogan, N. J. (2017) · Cell · doi:10.1016/j.cell.2017.03.022 · Cited by 401 · see citing works
Self-citationHung, V., Lam, S. S., Udeshi, N. D., Svinkina, T., Guzman, G., Mootha, V. K., Carr, S. A., & Ting, A. Y. (2017) · eLife · doi:10.7554/elife.24463 · Cited by 378 · see citing works
Self-citationIdentification 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
RNA–protein interaction detection in living cells
Ramanathan, M., Majzoub, K., Rao, D. S., Neela, P. H., Zarnegar, B. J., Mondal, S., Roth, J. G., Gai, H., Kovalski, J. R., Siprashvili, Z., et al. (2018) · Nature Methods · doi:10.1038/nmeth.4601 · Cited by 301 · see citing works
Promiscuous protein biotinylation by Escherichia coli biotin protein ligase
Choi‐Rhee, E., Schulman, H., & Cronan, J. E. (2004) · Protein Science · doi:10.1110/ps.04911804 · Cited by 297 · see citing works
Filling the Void: Proximity-Based Labeling of Proteins in Living Cells
Kim, D. I., & Roux, K. J. (2016) · Trends in Cell Biology · doi:10.1016/j.tcb.2016.09.004 · Cited by 288 · see citing works
Multidimensional Tracking of GPCR Signaling via Peroxidase-Catalyzed Proximity Labeling
Paek, J., Kalocsay, M., Staus, D. P., Wingler, L. M., Pascolutti, R., Paulo, J. A., Gygi, S. P., & Kruse, A. C. (2017) · Cell · doi:10.1016/j.cell.2017.03.028 · Cited by 272 · see citing works
Organogenesis of the Caenorhabditis elegans Intestine
Leung, B., Hermann, G. J., & Priess, J. R. (1999) · Developmental Biology · doi:10.1006/dbio.1999.9471 · Cited by 271 · see citing works
Imaging proteins in live mammalian cells with biotin ligase and monovalent streptavidin
Howarth, M. R., & Ting, A. Y. (2008) · Nature Protocols · doi:10.1038/nprot.2008.20 · Cited by 250 · see citing works
Self-citationKaewsapsak, P., Shechner, D. M., Mallard, W., Rinn, J. L., & Ting, A. Y. (2017) · eLife · doi:10.7554/elife.29224 · Cited by 193 · see citing works
Self-citationMartell, J. D., Yamagata, M., Deerinck, T. J., Phan, S., Kwa, C. G., Ellisman, M. H., Sanes, J. R., & Ting, A. Y. (2016) · Nature Biotechnology · doi:10.1038/nbt.3563 · Cited by 179 · see citing works
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Jung, E., Moffat, J. J., Liu, J., Dravid, S. M., Gurumurthy, C. B., & Kim, W.-Y. (2017) · Nature Neuroscience · doi:10.1038/s41593-017-0013-0 · Cited by 177 · see citing works
Novel Components of the Toxoplasma Inner Membrane Complex Revealed by BioID
Chen, A. L., Kim, E. W., Toh, J. Y., Vashisht, A. A., Rashoff, A. Q., Van, C., Huang, A. S., Moon, A. S., Bell, H. N., Bentolila, L. A., et al. (2015) · mBio · doi:10.1128/mbio.02357-14 · Cited by 171 · see citing works
Nadipuram, S. M., Kim, E. W., Vashisht, A. A., Lin, A. H., Bell, H. N., Coppens, I., Wohlschlegel, J. A., & Bradley, P. J. (2016) · mBio · doi:10.1128/mbio.00808-16 · Cited by 156 · see citing works
The human cytoplasmic dynein interactome reveals novel activators of motility
Redwine, W. B., DeSantis, M. E., Hollyer, I., Htet, Z. M., Tran, P. T., Swanson, S. K., Florens, L. A., Washburn, M. P., & Reck‐Peterson, S. L. (2017) · eLife · doi:10.7554/elife.28257 · Cited by 155 · see citing works
Plasma Proteome Database as a resource for proteomics research
Muthusamy, B., Hanumanthu, G., Suresh, S., Rekha, B., Srinivas, D., Karthick, L., Vrushabendra, B. M., Sharma, S., Mishra, G., Chatterjee, P., et al. (2005) · PROTEOMICS · doi:10.1002/pmic.200401335 · Cited by 150 · see citing works
Proteomic mapping in live Drosophila tissues using an engineered ascorbate peroxidase
Chen, C., Hu, Y., Udeshi, N. D., Lau, T. Y. K., Wirtz‐Peitz, F., He, L., Ting, A. Y., Carr, S. A., & Perrimon, N. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1515623112 · Cited by 146 · see citing works
Self-citationEngineering Antibody Affinity by Yeast Surface Display
Colby, D. W., Kellogg, B. A., Graff, C. P., Yeung, Y. A., Swers, J. S., & Wittrup, K. D. (2004) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(04)88027-3 · 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
BioID identifies novel c-MYC interacting partners in cultured cells and xenograft tumors
Dingar, D., Kalkat, M., Chan, P.-K., Srikumar, T., Bailey, S. D., Tu, W. B., Coyaud, E., Ponzielli, R., Kolyar, M., Jurisica, I., et al. (2015) · Journal of Proteomics · doi:10.1016/j.jprot.2014.09.029 · Cited by 131 · see citing works
Proximity Biotinylation as a Method for Mapping Proteins Associated with mtDNA in Living Cells
Han, S., Udeshi, N. D., Deerinck, T. J., Svinkina, T., Ellisman, M. H., Carr, S. A., & Ting, A. Y. (2017) · Cell chemical biology · doi:10.1016/j.chembiol.2017.02.002 · Cited by 122 · see citing works
Self-citationLong, S., Brown, K. M., Drewry, L. L., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006379 · Cited by 122 · see citing works
Reinke, A. W., Balla, K. M., Bennett, E. J., & Troemel, E. R. (2017) · Nature Communications · doi:10.1038/ncomms14023 · Cited by 111 · see citing works
Weaver, L. H., Kwon, K., Beckett, D., & Matthews, B. W. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.111128198 · Cited by 109 · see citing works
Kehrer, J., Frischknecht, F., & Mair, G. R. (2016) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m116.058263 · Cited by 105 · see citing works
Gaji, R. Y., Johnson, D. E., Treeck, M., et al. (2015) · PLoS Pathogens · doi:10.1371/journal.ppat.1005268 · Cited by 91 · see citing works
Wood, Z. A., Weaver, L. H., Brown, P. H., Beckett, D., & Matthews, B. W. (2006) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.12.066 · Cited by 84 · see citing works
Proteomic Mapping of Mitochondria in Living Cells via Spatially Restricted Enzymatic Tagging
Rhee, H.-W., Zou, P., Udeshi, N. D., Martell, J. D., Mootha, V. K., Carr, S. A., & Ting, A. Y. (2013) · Science · doi:10.1126/science.1230593 · Cited by 83 · see citing works
Self-citationNovel insights into the composition and function of theToxoplasmaIMC sutures
Chen, A. L., Moon, A. S., Bell, H. N., Huang, A. S., Vashisht, A. A., Toh, J. Y., Lin, A. H., Nadipuram, S. M., Kim, E. W., Choi, C., et al. (2016) · Cellular Microbiology · doi:10.1111/cmi.12678 · Cited by 77 · see citing works
Pinon, V., Ravanel, S., Douce, R., et al. (2005) · PLANT PHYSIOLOGY · doi:10.1104/pp.105.070144 · Cited by 73 · see citing works
Opitz, N., Schmitt, K., Hofer-Pretz, V., Neumann, B., Krebber, H., Braus, G. H., & Valerius, O. (2017) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m116.066654 · Cited by 71 · see citing works
Lin, Q., Zhou, Z., Luo, W., Fang, M., Li, M., & Li, H. (2017) · Frontiers in Plant Science · doi:10.3389/fpls.2017.00749 · Cited by 69 · see citing works
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Reinke, A. W., Mak, R., Troemel, E. R., & Bennett, E. J. (2017) · Science Advances · doi:10.1126/sciadv.1602426 · Cited by 66 · see citing works
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Birendra, K. C., May, D. G., Benson, B. V., Kim, D. I., Shivega, W. G., Ali, M. H., Faustino, R. S., Campos, A. R., & Roux, K. J. (2017) · Molecular Biology of the Cell · doi:10.1091/mbc.e17-03-0138 · Cited by 62 · see citing works
Zhou, Q., Hu, H., & Li, Z. (2016) · Journal of Biological Chemistry · doi:10.1074/jbc.m116.726133 · Cited by 58 · see citing works
Brush, S. B., Bellon, M. R., Hijmans, R. J., et al. (2015) · Proceedings of the National Academy of Sciences · doi:10.1073/iti0115112 · Cited by 57 · see citing works
Xu, Y., & Beckett, D. (1996) · Biochemistry · doi:10.1021/bi952269e · Cited by 45 · see citing works
Dang, H. Q., Zhou, Q., Rowlett, V. W., Hu, H., Lee, K. J., Margolin, W., & Li, Z. (2017) · mBio · doi:10.1128/mbio.02120-16 · Cited by 42 · see citing works
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Eginton, C., Cressman, W. J., Bachas, S. T., et al. (2015) · Journal of Molecular Biology · doi:10.1016/j.jmb.2015.02.021 · Cited by 29 · see citing works
Ortega-Cuéllar, D., Hernández-Mendoza, A., Moreno-Arriola, E., Carvajal, K., Pérez‐Vázquez, V., González-Álvarez, R., & Velázquez-Arellano, A. (2010) · Lifestyle Genomics · doi:10.1159/000318054 · Cited by 24 · see citing works
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CP39, CP75 and CP91 are major structural components of the Dictyostelium centrosome’s core structure
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Jan, C. H., Williams, C. C., & Weissman, J. S. (2015) · Science · doi:10.1126/science.aaa8299 · Cited by 14 · see citing works
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The desmoglein 2 interactome in primary neonatal cardiomyocytes
Li, Y., Campbell, A. P., Balasubramanian, S., Zeng, X., Porter, E., Cantrell, P. S., Sun, M., Mattheyses, A. L., & Kwiatkowski, A. V. (2026) · Journal of Cell Science · doi:10.1242/jcs.264213 · Cited by 2 · see citing works
- Authors
- 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.
- Affiliations
- Massachusetts Institute of Technology (US)
- Harvard University (US)
- Stanford University (US)
- Broad Institute (US)
- Howard Hughes Medical Institute (US)
- Chan Zuckerberg Biohub San Francisco (US)
- Corresponding author
- Ting, Alice Y
- ORCID
- Venue
- Nature Biotechnology
- Published
- 2018-08-20
- Volume
- 36
- Issue
- 9
- Pages
- 880-887
- ISSN
- 0733-222X (ISSN-L)
- 1087-0156
- 1546-1696
- PMC
- PMC6126969
- OpenAlex
- W2888618670
- Cited by
- 2,174
- References
- 70
- Citations by year
- 2026: 406 · 2025: 402 · 2024: 392 · 2023: 281 · 2022: 241 · 2021: 219 · 2020: 139 · 2019: 69 · 2018: 22 · 2014: 1
- FWCI
- 62.07
- Type
- journal article
- Language
- en
- Update notices
- correction (2019-11-20)
- Open access
- green
- doi.org
- Licence
- Locations
- Nature Biotechnology (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- PubMed (publishedVersion)
- Europe PMC (PubMed Central) (acceptedVersion)
- PubMed Central (acceptedVersion)
- Digital Access to Scholarship at Harvard (DASH) (Harvard University) (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc)
- Funders
- Damon Runyon Cancer Research Foundation
- Koch Institute for Integrative Cancer Research, Massachusetts Institute of Technology
- National Institutes of Health (1dp2gm119136-01, NIH-R01)
- National Cancer Institute (U24CA210986, R01CA186568)
- National Institute of General Medical Sciences (T32GM007276, DP2 GM119136)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Biotin and Related Studies
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
- Physical Sciences › Chemistry › Organic Chemistry › Click Chemistry and Applications
- Keywords
- proximity labeling, TurboID, biotin ligase, enzyme engineering, directed evolution, yeast surface display, protein-protein interaction, protein compartmentalization, BioID, biotinylation, Drosophila, Caenorhabditis elegans, live-cell imaging
- MeSH terms
- Catalysis, Enzymes, Mutation, Saccharomyces cerevisiae, Protein Interaction Mapping, Saccharomyces cerevisiae Proteins
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