Split Intein-Mediated Protein Ligation for detecting protein-protein interactions and their inhibition.

Szczegóły
Abstrakt

Tytuł:: Split Intein-Mediated Protein Ligation for detecting protein-protein interactions and their inhibition.
Autorzy:: Yao Z; Donnelly Centre, University of Toronto, Toronto, ON, Canada.
Aboualizadeh F; Donnelly Centre, University of Toronto, Toronto, ON, Canada.
Kroll J; Division of Developmental Biology, Institute of Biodynamics and Biocomplexity, Faculty of Science, Utrecht University, Utrecht, Netherlands.
Akula I; Donnelly Centre, University of Toronto, Toronto, ON, Canada.
Snider J; Donnelly Centre, University of Toronto, Toronto, ON, Canada.
Lyakisheva A; Donnelly Centre, University of Toronto, Toronto, ON, Canada.
Tang P; Donnelly Centre, University of Toronto, Toronto, ON, Canada.
Kotlyar M; Krembil Research Institute, University Health Network, Toronto, ON, Canada.
Jurisica I; Krembil Research Institute, University Health Network, Toronto, ON, Canada.; Department of Medical Biophysics, University of Toronto, Toronto, ON, Canada.; Department of Computer Science, University of Toronto, Toronto, ON, Canada.; Institute of Neuroimmunology, Slovak Academy of Sciences, Bratislava, Slovak Republic.
Boxem M; Division of Developmental Biology, Institute of Biodynamics and Biocomplexity, Faculty of Science, Utrecht University, Utrecht, Netherlands.
Stagljar I; Donnelly Centre, University of Toronto, Toronto, ON, Canada. .; Department of Biochemistry, University of Toronto, Toronto, ON, Canada. .; Department of Molecular Genetics, University of Toronto, Toronto, ON, Canada. .; Mediterranean Institute for Life Sciences, Meštrovićevo Šetalište 45, HR-21000, Split, Croatia. .
Źródło:: Nature communications [Nat Commun] 2020 May 15; Vol. 11 (1), pp. 2440. Date of Electronic Publication: 2020 May 15.
Typ publikacji:: Journal Article; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: [London] : Nature Pub. Group
MeSH Terms:: Protein Interaction Mapping*
Inteins/*genetics
Amino Acid Sequence ; Animals ; Caenorhabditis elegans/metabolism ; Drug Evaluation, Preclinical ; Enzyme-Linked Immunosorbent Assay ; HEK293 Cells ; HeLa Cells ; Humans ; Protein Binding ; Time Factors
References:: Yao, Z., Petschnigg, J., Ketteler, R. & Stagljar, I. Application guide for omics approaches to cell signaling. Nat. Chem. Biol. 11, 387–397 (2015). (PMID: 2597899610.1038/nchembio.1809)
Petschnigg, J., Snider, J. & Stagljar, I. Interactive proteomics research technologies: recent applications and advances. Curr. Opin. Biotechnol. 22, 50–58 (2011). (PMID: 2088419610.1016/j.copbio.2010.09.001)
Snider, J. et al. Fundamentals of protein interaction network mapping. Mol. Syst. Biol. 11, 848–848 (2015). (PMID: 26681426470449110.15252/msb.20156351)
Suter, B., Kittanakom, S. & Stagljar, I. Two-hybrid technologies in proteomics research. Curr. Opin. Biotechnol. 19, 316–323 (2008). (PMID: 1861954010.1016/j.copbio.2008.06.005)
Gogarten, J. P., Senejani, A. G., Zhaxybayeva, O., Olendzenski, L. & Hilario, E. Inteins: structure, function, and evolution. Annu. Rev. Microbiol. 56, 263–287 (2002). (PMID: 1214247910.1146/annurev.micro.56.012302.160741)
Shah, N. H. & Muir, T. W. Inteins: nature’s gift to protein chemists. Chem. Sci. 5, 446–461 (2014). (PMID: 2463471610.1039/C3SC52951G)
Aranko, A. S., Wlodawer, A. & Iwaï, H. Nature’s recipe for splitting inteins. Protein Eng. Des. Sel. 27, 263–271 (2014). (PMID: 25096198413356510.1093/protein/gzu028)
Wood, D. W. & Camarero, J. A. Intein applications: from protein purification and labeling to metabolic control methods. J. Biol. Chem. 289, 14512–14519 (2014). (PMID: 24700459403150910.1074/jbc.R114.552653)
Dassa, B., London, N., Stoddard, B. L., Schueler-furman, O. & Pietrokovski, S. Fractured genes: a novel genomic arrangement involving new split inteins and a new homing endonuclease family. Nucleic Acids Res. 37, 2560–2573 (2009). (PMID: 19264795267786610.1093/nar/gkp095)
Carvajal-Vallejos, P., Pallisse, Roser, Mootz, H. D. & Schmidt, S. R. Unprecedented rates and efficiencies revealed for new natural split inteins from metagenomic sources. J. Biol. Chem. 287, 28686–28696 (2012). (PMID: 22753413343655410.1074/jbc.M112.372680)
Beyer, H. M., Mikula, K. M., Li, M., Wlodawer, A. & Iwai, H. The crystal structure of the naturally split gp41-1 intein guides the engineering of orthogonal split inteins from a cis-splicing intein. FEBS J (in press) https://doi.org/10.1111/febs.15113 (2019).
Choi, J., Chen, J., Schreiber, S. L. & Clardy, J. Structure of the FKBP12-Rapamycin complex interacting with the binding domain of human FRAP. Science 273, 239–242 (1996). (PMID: 866250710.1126/science.273.5272.239)
Aranko, aS. et al. Structure-based engineering and comparison of novel split inteins for protein ligation. Mol. Biosyst. 10, 1023–1034 (2014). (PMID: 2457402610.1039/C4MB00021H)
Machleidt, T. et al. NanoBRET—a novel BRET platform for the analysis of protein-protein interactions. ACS Chem. Biol. 10, 1797–1804 (2015). (PMID: 2600669810.1021/acschembio.5b00143)
Venkatesan, K. et al. An empirical framework for binary interactome mapping. Nat. Methods 6, 83–90 (2009). (PMID: 1906090410.1038/nmeth.1280)
Lievens, S. et al. Kinase Substrate Sensor (KISS), a mammalian in situ protein interaction sensor. Mol. Cell. Proteomics 13, 3332–3342 (2014). (PMID: 25154561425648710.1074/mcp.M114.041087)
Trepte, P. et al. LuTHy: a double‐readout bioluminescence‐based two‐hybrid technology for quantitative mapping of protein–protein interactions in mammalian cells. Mol. Syst. Biol. 14, e8071 (2018). (PMID: 29997244603987010.15252/msb.20178071)
Braun, P. et al. An experimentally derived confidence score for binary protein-protein interactions. Nat. Methods 6, 91–97 (2009). (PMID: 1906090310.1038/nmeth.1281)
Lemmon, M. A. & Schlessinger, J. Cell signaling by receptor tyrosine kinases. Cell 141, 1117–1134 (2010). (PMID: 20602996291410510.1016/j.cell.2010.06.011)
Zheng, Y. et al. Temporal regulation of EGF signalling networks by the scaffold protein Shc1. Nature 499, 166–171 (2013). (PMID: 23846654493191410.1038/nature12308)
Pylayeva-Gupta, Y., Grabocka, E. & Bar-Sagi, D. RAS oncogenes: weaving a tumorigenic web. Nat. Rev. Cancer 11, 761–774 (2011). (PMID: 21993244363239910.1038/nrc3106)
Petschnigg, J. et al. The mammalian-membrane two-hybrid assay (MaMTH) for probing membrane-protein interactions in human cells. Nat. Methods 11, 585–592 (2014). (PMID: 2465814010.1038/nmeth.2895)
Yao, Z. et al. A global analysis of the receptor tyrosine kinase-protein phosphatase interactome. Mol. Cell 65, 347–360 (2017). (PMID: 28065597566346510.1016/j.molcel.2016.12.004)
Feig, L. A. & Cooper, G. M. Inhibition of NIH 3T3 cell proliferation by a mutant ras protein with preferential affinity for GDP. Mol. Cell. Biol. 8, 3235–3243 (1988). (PMID: 314540836355510.1128/MCB.8.8.3235)
Jura, N. et al. Mechanism for activation of the EGF receptor catalytic domain by the juxtamembrane segment. Cell 137, 1293–1307 (2009). (PMID: 19563760281454010.1016/j.cell.2009.04.025)
Waas, W. F. & Dalby, K. N. Transient Protein-protein interactions and a random-ordered kinetic mechanism for the phosphorylation of a transcription factor by extracellular-regulated protein kinase 2. J. Biol. Chem. 277, 12532–12540 (2002). (PMID: 1181278410.1074/jbc.M110523200)
Garai, Á. et al. Specificity of linear motifs that bind to a common mitogen-activated protein kinase docking groove. Sci. Signal. 5, ra74 (2012). (PMID: 23047924350069810.1126/scisignal.2003004)
Floyd, B. J. et al. Mitochondrial protein interaction mapping identifies regulators of respiratory chain function article mitochondrial protein interaction mapping identifies regulators of respiratory chain function. Mol. Cell 63, 621–632 (2016). (PMID: 27499296499245610.1016/j.molcel.2016.06.033)
Jackson, T. D., Palmer, C. S. & Stojanovski, D. Mitochondrial diseases caused by dysfunctional mitochondrial protein import. Biochem. Soc. Trans. 46, 1225–1238 (2018). (PMID: 3028750910.1042/BST20180239)
Kozjak-pavlovic, V. The MICOS complex of human mitochondria. Cell Tissue Res. 367, 83–93 (2017). (PMID: 2724523110.1007/s00441-016-2433-7)
Ciszak, E. M., Korotchkina, L. G., Dominiak, P. M., Sidhu, S. & Patel, M. S. Structural basis for flip-flop action of thiamin pyrophosphate- dependent enzymes revealed by human pyruvate dehydrogenase. 278, 21240–21246 (2003).
Boxem, M. et al. A protein domain-based interactome network for C. elegans early embryogenesis. Cell 134, 534–545 (2008). (PMID: 18692475259647810.1016/j.cell.2008.07.009)
Simonis, N. et al. Empirically controlled mapping of the Caenorhabditis elegans protein-protein interactome network. Nat. Methods 6, 47–54 (2009). (PMID: 19123269305792310.1038/nmeth.1279)
Yaish, P., Gazit, A., Gilon, C. & Levitzki, A. Blocking of EGF-dependent cell proliferation by EGF receptor kinase inhibitors. Science 242, 933–935 (1988). (PMID: 326370210.1126/science.3263702)
Roberts, A. W., Stilgenbauer, S., Seymour, J. F. & Huang, D. C. S. Venetoclax in patients with previously treated chronic lymphocytic leukemia. Clin. Cancer Res. 23, 4527–4534 (2017). (PMID: 2810058010.1158/1078-0432.CCR-16-0955)
Souers, A. J. et al. ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets. Nat. Med. 19, 202–208 (2013). (PMID: 2329163010.1038/nm.3048)
Stagljar, I. The power of OMICs. Biochem. Biophys. Res. Commun. 479, 607–609 (2016). (PMID: 2766366210.1016/j.bbrc.2016.09.09527663662)
Barrios-Rodiles, M. et al. High-throughput mapping of a dynamic signaling network in mammalian cells. Science 307, 1621–1625 (2005). (PMID: 1576115310.1126/science.1105776)
Lemmens, I. et al. Heteromeric MAPPIT: a novel strategy to study modification-dependent protein-protein interactions in mammalian cells. Nucleic Acids Res. 31, e75 (2003). (PMID: 1285365216765810.1093/nar/gng075)
Fields, S. & Song, O. A novel genetic system to detect protein-protein interactions. Nature 340, 245–246 (1989). (PMID: 254716310.1038/340245a0)
Galarneau, A., Primeau, M., Trudeau, L. & Michnick, S. W. β-Lactamase protein fragment complementation assays as in vivo and in vitro sensors of protein–protein interactions. Nat. Biotechnol. 20, 619–622 (2002). (PMID: 1204286810.1038/nbt0602-619)
Ramachandra, N. et al. Self-assembling protein microarrays. Science 305, 86–91 (2004). (PMID: 10.1126/science.1097639)
Shah, N. H., Eryilmaz, E., Cowburn, D. & Muir, T. W. Naturally split inteins assemble through a ‘capture and collapse’ mechanism. J. Am. Chem. Soc. 135, 18673–18681 (2013). (PMID: 24236406386579910.1021/ja4104364)
Zheng, Y., Wu, Q., Wang, C., Xu, M. Q. & Liu, Y. Mutual synergistic protein folding in split intein. Biosci. Rep. 32, 433–442 (2012). (PMID: 22681309380492810.1042/BSR20120049)
Michnick, S. W., Ear, P. H., Manderson, E. N., Remy, I. & Stefan, E. Universal strategies in research and drug discovery based on protein-fragment complementation assays. Nat. Rev. Drug Discov. 6, 569–582 (2007). (PMID: 1759908610.1038/nrd2311)
Kim, M. W. et al. Time-gated detection of protein-protein interactions with transcriptional readout. Elife 6, 1–24 (2017).
Olhovsky, M. et al. OpenFreezer: a reagent information management software system. Nat. Methods 8, 612–613 (2011). (PMID: 2179949310.1038/nmeth.1658)
Boussif, O. et al. A versatile vector for gene and oligonucleotide transfer into cells in culture and in vivo: polyethylenimine. Proc. Natl. Acad. Sci. USA 92, 7297–7301 (1995). (PMID: 763818410.1073/pnas.92.16.7297)
Kotlyar, M., Pastrello, C., Malik, Z. & Jurisica, I. IID 2018 update: context-specific physical protein-protein interactions in human, model organisms and domesticated species. Nucleic Acids Res. 47, D581–D589 (2019). (PMID: 3040759110.1093/nar/gky1037)
Kotlyar, M. et al. In silico prediction of physical protein interactions and characterization of interactome orphans. Nat. Methods 12, 79–84 (2014). (PMID: 2540200610.1038/nmeth.3178)
Brenner, S. The genetics of Caenorhabditis elegans. Genetcis 77, 71–94 (1974).
Grant Information:: PJT-165862 Canada CIHR
Entry Date(s):: Date Created: 20200517 Date Completed: 20200812 Latest Revision: 20210515
Update Code:: 20240105
PubMed Central ID:: PMC7229206
DOI:: 10.1038/s41467-020-16299-1
PMID:: 32415080
: Czasopismo naukowe

Full Text Finder

Here, to overcome many limitations accompanying current available methods to detect protein-protein interactions (PPIs), we develop a live cell method called Split Intein-Mediated Protein Ligation (SIMPL). In this approach, bait and prey proteins are respectively fused to an intein N-terminal fragment (IN) and C-terminal fragment (IC) derived from a re-engineered split intein GP41-1. The bait/prey binding reconstitutes the intein, which splices the bait and prey peptides into a single intact protein that can be detected by regular protein detection methods such as Western blot analysis and ELISA, serving as readouts of PPIs. The method is robust and can be applied not only in mammalian cell lines but in animal models such as C. elegans. SIMPL demonstrates high sensitivity and specificity, and enables exploration of PPIs in different cellular compartments and tracking of kinetic interactions. Additionally, we establish a SIMPL ELISA platform that enables high-throughput screening of PPIs and their inhibitors.

Informacja