Setting Up a Bioluminescence Resonance Energy Transfer High throughput Screening Assay to Search for Protein/Protein Interaction Inhibitors in Mammalian Cells
Open accessAbstract
Each step of the cell life and its response or adaptation to its environment are mediated by a network of protein/protein interactions termed "interactome." Our knowledge of this network keeps growing due to the development of sensitive techniques devoted to study these interactions. The bioluminescence resonance energy transfer (BRET) technique was primarily developed to allow the dynamic monitoring of protein/protein interactions (PPI) in living cells, and has widely been used to study receptor activation by intra- or extra-molecular conformational changes within receptors and activated complexes in mammal cells. Some interactions are described as crucial in human pathological processes, and a new class of drugs targeting them has recently emerged. The BRET method is well suited to identify inhibitors of PPI and here is described why and how to set up and optimize a high throughput screening assay based on BRET to search for such inhibitory compounds. The different parameters to take into account when developing such BRET assays in mammal cells are reviewed to give general guidelines: considerations on the targeted interaction, choice of BRET version, inducibility of the interaction, kinetic of the monitored interaction, and of the BRET reading, influence of substrate concentration, number of cells and medium composition used on the Z' factor, and expected interferences from colored or fluorescent compounds.
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
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.
Cites
Massagué, J. (1998) · Annual Review of Biochemistry · doi:10.1146/annurev.biochem.67.1.753 · Cited by 7,571 · see citing works
Energy transfer: a spectroscopic ruler.
Stryer, L., & Haugland, R. P. (1967) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.58.2.719 · Cited by 1,961 · see citing works
Engineered Luciferase Reporter from a Deep Sea Shrimp Utilizing a Novel Imidazopyrazinone Substrate
Hall, M. P., Unch, J., Binkowski, B. F., Valley, M. P., Butler, B. L., Wood, M. G., Otto, P., Zimmerman, K., Vidugiris, G. J. A., Machleidt, T., et al. (2012) · ACS Chemical Biology · doi:10.1021/cb3002478 · Cited by 1,588 · see citing works
Ecdysone-inducible gene expression in mammalian cells and transgenic mice.
No, D. B., Yao, T. P., & Evans, R. M. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.8.3346 · Cited by 852 · see citing works
Self-illuminating quantum dot conjugates for in vivo imaging
So, M., Xu, C., Loening, A. M., Gambhir, S. S., & Rao, J. (2006) · Nature Biotechnology · doi:10.1038/nbt1188 · Cited by 807 · see citing works
Codon-Optimized Gaussia Luciferase cDNA for Mammalian Gene Expression in Culture and in Vivo
Tannous, B. A., Kim, D., Fernandez, J. L., Weissleder, R., & Breakefield, X. O. (2004) · Molecular Therapy · doi:10.1016/j.ymthe.2004.10.016 · Cited by 684 · see citing works
Xu, Y. Q., Piston, D. W., & Johnson, C. H. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.1.151 · Cited by 613 · see citing works
Pfleger, K. D. G., & Eidne, K. A. (2006) · Nature Methods · doi:10.1038/nmeth841 · Cited by 571 · see citing works
Drug–target interaction prediction by random walk on the heterogeneous network
Chen, X., Liu, M.-X., & Yan, G. (2012) · Molecular BioSystems · doi:10.1039/c2mb00002d · Cited by 532 · see citing works
Algar, W. R., Tavares, A. J., & Krull, U. J. (2010) · Analytica Chimica Acta · doi:10.1016/j.aca.2010.05.026 · Cited by 511 · see citing works
Degorce, F. (2009) · Current Chemical Genomics · doi:10.2174/1875397300903010022 · Cited by 501 · see citing works
Mercier, J.-F., Salahpour, A., Angers, S., Breit, A., & Bouvier, M. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m205767200 · Cited by 474 · see citing works
Galès, C., Durm, J. J. J. V., Schaak, S., Pontier, S. M., Percherancier, Y., Audet, M., Paris, H., & Bouvier, M. (2006) · Nature Structural & Molecular Biology · doi:10.1038/nsmb1134 · Cited by 461 · see citing works
Measurement of the millisecond activation switch of G protein–coupled receptors in living cells
Vilardaga, J., Bünemann, M., Krasel, C., Castro, M., & Lohse, M. J. (2003) · Nature Biotechnology · doi:10.1038/nbt838 · Cited by 432 · see citing works
Consensus guided mutagenesis of Renilla luciferase yields enhanced stability and light output
Loening, A. M. (2006) · Protein Engineering Design and Selection · doi:10.1093/protein/gzl023 · Cited by 419 · see citing works
Terrillon, S., Durroux, T., Mouillac, B., Breit, A., Ayoub, M. A., Taulan‐Cadars, M., Jockers, R., Barberis, C., & Bouvier, M. (2003) · Molecular Endocrinology · doi:10.1210/me.2002-0222 · Cited by 323 · see citing works
Ayoub, M. A., Couturier, C., Lucas-Meunier, E., Angers, S., Fossier, P., Bouvier, M., & Jockers, R. (2002) · Journal of Biological Chemistry · doi:10.1074/jbc.m200729200 · Cited by 322 · see citing works
Self-citationUniversal strategies in research and drug discovery based on protein-fragment complementation assays
Michnick, S. W., Ear, P. H., Manderson, E. N., Remy, I., & Stefan, E. (2007) · Nature Reviews Drug Discovery · doi:10.1038/nrd2311 · Cited by 319 · see citing works
Lohse, M. J., Nuber, S., & Hoffmann, C. (2012) · Pharmacological Reviews · doi:10.1124/pr.110.004309 · Cited by 306 · see citing works
The use of resonance energy transfer in high-throughput screening: BRET versus FRET
Boute, N., Jockers, R., & Issad, T. (2002) · Trends in Pharmacological Sciences · doi:10.1016/s0165-6147(02)02062-x · Cited by 269 · see citing works
Sensitivity of MRI resonance frequency to the orientation of brain tissue microstructure
Lee, J., Shmueli, K., Fukunaga, M., van Gelderen, P., Merkle, H., Silva, A. C., & Duyn, J. H. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0910222107 · Cited by 264 · see citing works
Smith, D. S., & Eremin, S. A. (2008) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-008-1897-z · Cited by 253 · see citing works
Ayoub, M. A., Levoye, A., Delagrange, P., & Jockers, R. (2004) · Molecular Pharmacology · doi:10.1124/mol.104.000398 · Cited by 208 · see citing works
Ramsay, D., Kellett, E., McVey, M., Stephen, R. E. E. S., & Milligan, G. (2002) · Biochemical Journal · doi:10.1042/bj20020251 · Cited by 203 · see citing works
Cell-based assays: fuelling drug discovery
Michelini, E., Cevenini, L., Mezzanotte, L., Coppa, A., & Roda, A. (2010) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-010-3933-z · Cited by 197 · see citing works
The cumate gene-switch: a system for regulated expression in mammalian cells
Mullick, A., Xu, Y., Warren, R., Koutroumanis, M., Guilbault, C., Broussau, S., Malenfant, F., Bourget, L., Lamoureux, L., Lo, R., et al. (2006) · BMC Biotechnology · doi:10.1186/1472-6750-6-43 · Cited by 190 · see citing works
Hamdan, F. F., Audet, M., Garneau, P., Pelletier, J., & Bouvier, M. (2005) · SLAS Discovery · doi:10.1177/1087057105275344 · Cited by 183 · see citing works
The BRET technology and its application to screening assays
Bacart, J., Corbel, C., Jockers, R., Bach, S., & Couturier, C. (2008) · Biotechnology Journal · doi:10.1002/biot.200700222 · Cited by 178 · see citing works
Self-citationCharest, P. G., Terrillon, S., & Bouvier, M. (2005) · EMBO Reports · doi:10.1038/sj.embor.7400373 · Cited by 172 · see citing works
Radiation-Force Assisted Targeting Facilitates Ultrasonic Molecular Imaging
Zhao, S., Borden, M. A., Bloch, S. H., et al. (2004) · Molecular Imaging · doi:10.1162/1535350042380317 · Cited by 169 · see citing works
Xia, Z., Xing, Y., So, M., Koh, A. L., Sinclair, R., & Rao, J. (2008) · Analytical Chemistry · doi:10.1021/ac801562f · Cited by 168 · see citing works
Diverse strategies for tetracycline-regulated inducible gene expression.
Shockett, P. E., & Schatz, D. G. (1996) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.93.11.5173 · Cited by 150 · see citing works
Luminescent Quantum Dots: A Very Attractive and Promising Tool in Biomedicine
Weng, J., & Ren, J.-C. (2006) · Current Medicinal Chemistry · doi:10.2174/092986706776361076 · Cited by 132 · see citing works
Couturier, C., & Jockers, R. (2003) · Journal of Biological Chemistry · doi:10.1074/jbc.m302002200 · Cited by 132 · see citing works
Self-citationZhao, H. F., Doyle, T. C., Wong, R. J., Cao, Y., Stevenson, D. K., Piwnica-Worms, D. R., & Contag, C. H. (2004) · Molecular Imaging · doi:10.1162/153535004773861714 · Cited by 123 · see citing works
Milligan, G. (2004) · European Journal of Pharmaceutical Sciences · doi:10.1016/j.ejps.2003.11.010 · Cited by 119 · see citing works
Kinetics of G‐protein‐coupled receptor signals in intact cells
Lohse, M. J., Hein, P., Hoffmann, C., Nikolaev, V. O., Vilardaga, J., & Bünemann, M. (2008) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0707656 · Cited by 116 · see citing works
Interaction networks: From protein functions to drug discovery. A review
Chautard, É., Thierry‐Mieg, N., & Ricard‐Blum, S. (2008) · Pathologie Biologie · doi:10.1016/j.patbio.2008.10.004 · Cited by 116 · see citing works
Analysis of Protease Activity Using Quantum Dots and Resonance Energy Transfer
Kim, G. B., & Kim, Y. (2012) · Theranostics · doi:10.7150/thno.3476 · Cited by 113 · see citing works
De, A., Loening, A. M., & Gambhir, S. S. (2007) · Cancer Research · doi:10.1158/0008-5472.can-06-4623 · Cited by 110 · see citing works
Couturier, C., Sarkis, C., Séron, K., Belouzard, S., Chen, P. B., Lenain, A., Corset, L., Dam, J., Vauthier, V., Dubart‐Kupperschmitt, A., et al. (2007) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706671104 · Cited by 106 · see citing works
Self-citationDe, A., Ray, P., Loening, A. M., & Gambhir, S. S. (2009) · The FASEB Journal · doi:10.1096/fj.08-118919 · Cited by 106 · see citing works
Boute, N., Boubekeur, S., Lacasa, D., & Issad, T. (2003) · EMBO Reports · doi:10.1038/sj.embor.embor767 · Cited by 105 · see citing works
Pfleger, K. D. G., Dromey, J. R., Dalrymple, M. B., Lim, E. M. L., Thomas, W. G., & Eidne, K. A. (2006) · Cellular Signalling · doi:10.1016/j.cellsig.2006.01.004 · Cited by 102 · see citing works
Multiply mutated Gaussia luciferases provide prolonged and intense bioluminescence
Welsh, J. P., Patel, K. G., Manthiram, K., & Swartz, J. R. (2009) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2009.09.006 · Cited by 99 · see citing works
Yeast two-hybrid methods and their applications in drug discovery
Hamdi, A., & Colas, P. (2011) · Trends in Pharmacological Sciences · doi:10.1016/j.tips.2011.10.008 · Cited by 98 · see citing works
Ayoub, M. A., & Pfleger, K. D. G. (2009) · Current Opinion in Pharmacology · doi:10.1016/j.coph.2009.09.012 · Cited by 95 · see citing works
Sun, Y., Chen, X., & Xiao, D. (2007) · Acta Biochimica et Biophysica Sinica · doi:10.1111/j.1745-7270.2007.00258.x · Cited by 94 · see citing works
Kočan, M., See, H. B., Seeber, R. M., Eidne, K. A., & Pfleger, K. D. G. (2008) · SLAS DISCOVERY · doi:10.1177/1087057108324032 · Cited by 92 · see citing works
Superluminescent Variants of Marine Luciferases for Bioassays
Kim, S. B., Suzuki, H., Sato, M., & Tao, H. (2011) · Analytical Chemistry · doi:10.1021/ac2021882 · Cited by 90 · see citing works
Development of a BRET2 Screening Assay Using β-Arrestin 2 Mutants
Vrecl, M., Jørgensen, R., Pogačnik, A., & Heding, A. (2004) · SLAS DISCOVERY · doi:10.1177/1087057104263212 · Cited by 85 · see citing works
The cytotoxic effects of polymer-coated quantum dots and restrictions for live cell applications
Soenen, S. J., Demeester, J., Smedt, S. C. D., & Braeckmans, K. (2012) · Biomaterials · doi:10.1016/j.biomaterials.2012.03.042 · Cited by 85 · see citing works
Py, B. F., Basmaciogullari, S., Bouchet, J., Zarka, M., Moura, I. C., Benhamou, M., Monteiro, R. C., Hocini, H., Madrid, R., & Bénichou, S. (2009) · PLoS ONE · doi:10.1371/journal.pone.0005006 · Cited by 85 · see citing works
Controlling mammalian gene expression with small molecules.
Clackson, T. (1997) · Current Opinion in Chemical Biology · doi:10.1016/s1367-5931(97)80012-9 · Cited by 84 · see citing works
Boute, N., Siquier-Pernet, K., & Issad, T. (2001) · Molecular Pharmacology · doi:10.1016/s0026-895x(24)12289-4 · Cited by 83 · see citing works
Schelshorn, D. W., Joly, F., Mutel, S., Hampe, C., Breton, B., Mutel, V., & Lütjens, R. (2011) · Molecular Pharmacology · doi:10.1124/mol.111.074757 · Cited by 81 · see citing works
Majumdar, Z. K., Hickerson, R. P., Noller, H. F., & Clegg, R. M. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.06.027 · Cited by 80 · see citing works
Colorimetric detection of cholesterol with G-quadruplex-based DNAzymes and ABTS2−
Li, R., Xiong, C., Xiao, Z., et al. (2012) · Analytica Chimica Acta · doi:10.1016/j.aca.2012.02.015 · Cited by 80 · see citing works
Protein complementation assays: Approaches for the in vivo analysis of protein interactions
Morell, M., Ventura, S., & Avilés, F. X. (2009) · FEBS Letters · doi:10.1016/j.febslet.2009.03.002 · Cited by 78 · see citing works
Xia, Y.-Q., Wu, S. T., & Jemal, M. (2008) · Analytical Chemistry · doi:10.1021/ac8010846 · Cited by 78 · see citing works
Interaction networks for systems biology
Bader, S. L., Kühner, S., & Gavin, A. (2008) · FEBS Letters · doi:10.1016/j.febslet.2008.02.015 · Cited by 76 · see citing works
The role of threonine 37 in flavin reactivity of the old yellow enzyme
Xu, D., Kohli, R. M., & Massey, V. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.7.3556 · Cited by 76 · see citing works
Arai, R., Nakagawa, H., Tsumoto, K., Mahoney, W. C., Kumagai, I., Ueda, H., & Nagamune, T. (2001) · Analytical Biochemistry · doi:10.1006/abio.2000.4924 · Cited by 75 · see citing works
Development of Luciferin Analogues Bearing an Amino Group and Their Application as BRET Donors
Takakura, H., Sasakura, K., Ueno, T., Urano, Y., Terai, T., Hanaoka, K., Tsuboi, T., & Nagano, T. (2010) · Chemistry - An Asian Journal · doi:10.1002/asia.201000219 · Cited by 73 · see citing works
Subcellular Imaging of Dynamic Protein Interactions by Bioluminescence Resonance Energy Transfer
Coulon, V., Audet, M., Homburger, V., Bockaert, J., Fagni, L., Bouvier, M., & Perroy, J. (2007) · Biophysical Journal · doi:10.1529/biophysj.107.117275 · Cited by 73 · see citing works
Hickerson, R. P., Majumdar, Z. K., Baucom, A., Clegg, R. M., & Noller, H. F. (2005) · Journal of Molecular Biology · doi:10.1016/j.jmb.2005.09.010 · Cited by 72 · see citing works
Aminoluciferins as Functional Bioluminogenic Substrates of Firefly Luciferase
Takakura, H., Kojima, R., Urano, Y., Terai, T., Hanaoka, K., & Nagano, T. (2011) · Chemistry - An Asian Journal · doi:10.1002/asia.201000873 · Cited by 69 · see citing works
Accelerated Fatty Acid Oxidation in Muscle Averts Fasting-induced Hepatic Steatosis in SJL/J Mice
Guan, H.-P., Goldstein, J. L., Brown, M. S., & Liang, G. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.034397 · Cited by 65 · see citing works
Guan, R., Feng, X., Wu, X., Zhang, M., Zhang, X., Hébert, T. E., & Segaloff, D. L. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m809150200 · Cited by 64 · see citing works
Role of SUMO in RNF4-mediated Promyelocytic Leukemia Protein (PML) Degradation
Percherancier, Y., Germain-Desprez, D., Galisson, F., Mascle, X. H., Dianoux, L., Estephan, P., Chelbi‐Alix, M. K., & Aubry, M. (2009) · Journal of Biological Chemistry · doi:10.1074/jbc.m109.006387 · Cited by 62 · see citing works
Molinari, P., Casella, I., & Costa, T. (2007) · Biochemical Journal · doi:10.1042/bj20070803 · Cited by 60 · see citing works
Otto‐Duessel, M., Khankaldyyan, V., González-Gómez, I., Jensen, M. C., Laug, W. E., & Rosol, M. S. (2006) · Molecular Imaging · doi:10.2310/7290.2006.00006 · Cited by 58 · see citing works
Jarry, M., Diallo, M., Lecointre, C., Desrues, L., Tokay, T., Chatenet, D., Leprince, J., Rossi, O., Vaudry, H., Tonon, M., et al. (2010) · Biochemical Journal · doi:10.1042/bj20090867 · Cited by 57 · see citing works
Takenaka, Y., Masuda, H., Yamaguchi, A., Nishikawa, S., Shigeri, Y., Yoshida, Y., & Mizuno, H. (2008) · Gene · doi:10.1016/j.gene.2008.07.041 · Cited by 56 · see citing works
Arai, R., NAKAGAWA, H., Kitayama, A., Ueda, H., & Nagamune, T. (2002) · Journal of Bioscience and Bioengineering · doi:10.1263/jbb.94.362 · Cited by 53 · see citing works
Gainer, H., & Wray, S. (1992) · Annals of the New York Academy of Sciences · doi:10.1111/j.1749-6632.1992.tb34342.x · Cited by 52 · see citing works
See, H. B., Seeber, R. M., Kočan, M., Eidne, K. A., & Pfleger, K. D. G. (2010) · Assay and Drug Development Technologies · doi:10.1089/adt.2010.0336 · Cited by 52 · see citing works
Fruhwirth, G. O., Fernandes, L. P., Weitsman, G. E., Patel, G. S., Kelleher, M., Lawler, K., Brock, A., Poland, S. P., Matthews, D. R., Kéri, G., et al. (2011) · ChemPhysChem · doi:10.1002/cphc.201000866 · Cited by 52 · see citing works
Pfleger, K. D. G., & Eidne, K. A. (2003) · Pituitary · doi:10.1023/b:pitu.0000011175.41760.5d · Cited by 49 · see citing works
Arai, R., Nakagawa, H., Kitayama, A., Ueda, H., & Nagamune, T. (2002) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(02)80178-5 · Cited by 47 · see citing works
Kamal, M. T., Marquez, M., Vauthier, V., Leloire, A., Froguel, P., Jockers, R., & Couturier, C. (2009) · Biotechnology Journal · doi:10.1002/biot.200900016 · Cited by 46 · see citing works
Self-citationYamakawa, Y., Veda, H., Kitayama, A., & Nagamune, T. (2002) · Journal of Bioscience and Bioengineering · doi:10.1016/s1389-1723(02)80234-1 · Cited by 43 · see citing works
From protein interaction networks to novel therapeutic strategies
Jaeger, S., & Aloy, P. (2012) · IUBMB Life · doi:10.1002/iub.1040 · Cited by 43 · see citing works
Shared components of protein complexes—versatile building blocks or biochemical artefacts?
Krause, R., von Mering, C., Peer Bork, B., & Dandekar, T. (2004) · BioEssays · doi:10.1002/bies.20141 · Cited by 41 · see citing works
Matthiesen, K., & Nielsen, J. (2011) · PLoS ONE · doi:10.1371/journal.pone.0024392 · Cited by 40 · see citing works
Harikumar, K. G., Dong, M., Cheng, Z.-J. J., Pinon, D. I., Lybrand, T. P., & Miller, L. J. (2006) · Biochemistry · doi:10.1021/bi061107n · Cited by 39 · see citing works
Study of GPCR–Protein Interactions by BRET
Kočan, M., & Pfleger, K. D. G. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-126-0_20 · Cited by 38 · see citing works
Dacres, H., Dumancic, M. M., Horne, I. M., & Trowell, S. (2008) · Analytical Biochemistry · doi:10.1016/j.ab.2008.10.040 · Cited by 38 · see citing works
Hu, K., Clément, J.-F., Abrahamyan, L. G., Strebel, K., Bouvier, M., Kleiman, L., & Mouland, A. J. (2005) · Journal of Virological Methods · doi:10.1016/j.jviromet.2005.04.012 · Cited by 38 · see citing works
Monitoring interactions between G-protein-coupled receptors and β-arrestins
Pfleger, K. D. G., Dalrymple, M. B., Dromey, J. R., & Eidne, K. A. (2007) · Biochemical Society Transactions · doi:10.1042/bst0350764 · Cited by 36 · see citing works
Alvarez‐Curto, E., Pediani, J. D., & Milligan, G. (2010) · Analytical and Bioanalytical Chemistry · doi:10.1007/s00216-010-3823-4 · Cited by 36 · see citing works
In Vivo Detection of Protein–Protein Interaction in Plant Cells Using BRET
Subramanian, C., Xu, Y. Q., Johnson, C. H., & von Arnim, A. G. (2004) · Humana Press eBooks · doi:10.1385/1-59259-816-1:271 · Cited by 35 · see citing works
Corbel, C., Wang, Q., Bousserouel, H., Hamdi, A., Zhang, B., Lozach, O., Ferandin, Y., Tan, V. B. C., Guéritte, F., Colas, P., et al. (2011) · Biotechnology Journal · doi:10.1002/biot.201100138 · Cited by 35 · see citing works
Self-citationGranier, S., Terrillon, S., Pascal, R., Déméné, H., Bouvier, M., Guillon, G., & Mendre, C. (2004) · Journal of Biological Chemistry · doi:10.1074/jbc.m405089200 · Cited by 35 · see citing works
Electroanalytical Eavesdropping on Single Cell Communication
Kim, D., Koseoglu, S., Manning, B. M., et al. (2011) · Analytical Chemistry · doi:10.1021/ac200666c · Cited by 34 · see citing works
Kimura, T., Hiraoka, K., Kasahara, N., & Logg, C. R. (2010) · The Journal of Gene Medicine · doi:10.1002/jgm.1463 · Cited by 33 · see citing works
Blanquart, C., González-Yanes, C., & Issad, T. (2006) · Molecular Pharmacology · doi:10.1124/mol.106.026989 · Cited by 33 · see citing works
Zhao, H. F., Doyle, T. C., Wong, R. J., Cao, Y., Stevenson, D. K., Piwnica-Worms, D. R., & Contag, C. H. (2004) · Molecular Imaging · doi:10.1162/15353500200403181 · Cited by 33 · see citing works
Audet, M., Lagacé, M., Silversides, D. W., & Bouvier, M. (2010) · The FASEB Journal · doi:10.1096/fj.09-144816 · Cited by 32 · see citing works
MAPPIT: A protein interaction toolbox built on insights in cytokine receptor signaling
Lievens, S., Peelman, F., Bosscher, K. D., Lemmens, I. H., & Tavernier, J. H. (2011) · Cytokine & Growth Factor Reviews · doi:10.1016/j.cytogfr.2011.11.001 · Cited by 31 · see citing works
Issad, T., Boute, N., Boubekeur, S., & Lacasa, D. (2005) · Biochimie · doi:10.1016/j.biochi.2004.12.008 · Cited by 30 · see citing works
Evidence for leptin receptor isoforms heteromerization at the cell surface
Bacart, J., Leloire, A., Levoye, A., Froguel, P., Jockers, R., & Couturier, C. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.03.033 · Cited by 28 · see citing works
Self-citationMAPPIT: a cytokine receptor‐based two‐hybrid method in mammalian cells 1
Tavernier, J. H., Eyckerman, S., Lemmens, I. H., der Heyden, J. V., Vandekerckhove, J. S., & Ostade, X. V. (2002) · Clinical & Experimental Allergy · doi:10.1046/j.1365-2745.2002.01520.x · Cited by 28 · see citing works
Boubekeur, S., Boute, N., Pagésy, P., Zilberfarb, V., Christeff, N., & Issad, T. (2011) · Journal of Biological Chemistry · doi:10.1074/jbc.m111.222984 · Cited by 28 · see citing works
Otsuji, T. G., Okuda‐Ashitaka, E., Kojima, S., Akiyama, H., Ito, S., & Ohmiya, Y. (2004) · Analytical Biochemistry · doi:10.1016/j.ab.2004.03.010 · Cited by 28 · see citing works
Bioluminescence Resonance Energy Transfer as a Screening Assay: Focus on Partial and Inverse Agonism
Elster, L., Elling, C., & Heding, A. (2006) · SLAS DISCOVERY · doi:10.1177/1087057106295895 · Cited by 28 · see citing works
Comparison of enhanced bioluminescence energy transfer donors for protease biosensors
Dacres, H., Michie, M., & Trowell, S. (2012) · Analytical Biochemistry · doi:10.1016/j.ab.2012.02.028 · Cited by 27 · see citing works
Vizoso-Pinto, M. G., Pothineni, V. R., Haase, R., Woidy, M., Lotz-Havla, A. S., Gersting, S. W., Muntau, A. C., Haas, J., Sommer, M. H., Arvin, A. M., et al. (2011) · Journal of Proteome Research · doi:10.1021/pr200628s · Cited by 25 · see citing works
High-active truncated luciferase of copepod Metridia longa
Markova, S. V., Burakova, L. P., & Vysotski, E. S. (2011) · Biochemical and Biophysical Research Communications · doi:10.1016/j.bbrc.2011.11.063 · Cited by 23 · see citing works
The New Era of Bioluminescence Resonance Energy Transfer Technology
De, A. (2011) · Current Pharmaceutical Biotechnology · doi:10.2174/138920111795163922 · Cited by 23 · see citing works
Lee, K. H., Lee, S., Lee, W.-Y., Yang, H. W., & Heo, W. D. (2010) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0911262107 · Cited by 22 · see citing works
Li, F., Yu, J., Zhang, Z., Cui, Z., Wang, D., Wei, H., & Zhang, X. (2012) · Analytica Chimica Acta · doi:10.1016/j.aca.2012.02.047 · Cited by 21 · see citing works
Using BRET to study chemical compound‐induced disruptions of the p53‐HDM2 interactions in live cells
Mazars, A., & Fåhræus, R. (2010) · Biotechnology Journal · doi:10.1002/biot.200900272 · Cited by 20 · see citing works
Quinones, G. A., Miller, S. C., Bhattacharyya, S., Sobek, D., & Stéphan, J.-P. (2012) · Journal of Cellular Biochemistry · doi:10.1002/jcb.24111 · Cited by 19 · see citing works
Bimolecular Fluorescence Complementation: Illuminating Cellular Protein Interactions
Ventura, S. (2011) · Current Molecular Medicine · doi:10.2174/156652411800615117 · Cited by 17 · see citing works
Qi, Q., He, K., Liu, X., Pham, C., Meyerkord, C. L., Fu, H., & Ye, K.-N. (2012) · Oncogene · doi:10.1038/onc.2012.109 · Cited by 16 · see citing works
Oka, T., Takagi, H., Tohya, Y., Murakami, K., Takeda, N., Wakita, T., & Katayama, K. (2011) · Antiviral Research · doi:10.1016/j.antiviral.2011.02.002 · Cited by 14 · see citing works
Kang, J., Tsai‐Morris, C., & Dufau, M. L. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05337-11 · Cited by 14 · see citing works
Darbandi-Tehrani, K., Hermand, P., Carvalho, S., Dorgham, K., Couvineau, A., Lacapère, J.-J., Combadière, C., & Déterre, P. (2010) · The FASEB Journal · doi:10.1096/fj.10-156612 · Cited by 13 · see citing works
Chan, F. K.-M. (2004) · Humana Press eBooks · doi:10.1385/1-59259-762-9:371 · Cited by 11 · see citing works
Illuminating Cellular Physiology: Recent Developments
Brovko, L., & Griffiths, M. W. (2007) · Science Progress · doi:10.3184/003685007x215986 · Cited by 11 · see citing works
Laursen, L. S., & Oxvig, C. (2005) · Biochemical Pharmacology · doi:10.1016/j.bcp.2005.04.005 · Cited by 11 · see citing works
Kulahin, N., Grunnet, L. G., Lundh, M., Christensen, D. P., Jørgensen, R., Heding, A., Billestrup, N., Berezin, V., Bock, E., & Mandrup-Poulsen, T. R. (2010) · FEBS Letters · doi:10.1016/j.febslet.2010.11.043 · Cited by 10 · see citing works
A BRET assay for monitoring insulin receptor interactions and ligand pharmacology
Kulahin, N., Sanni, S. J., Slaaby, R., Nøhr, J., Gammeltoft, S., Hansen, J. L., & Jørgensen, R. (2012) · Journal of Receptors and Signal Transduction · doi:10.3109/10799893.2011.647351 · Cited by 10 · see citing works
Dinh, D. T., Qian, H., Seeber, R. M., Lim, E., Pfleger, K. D. G., Eidne, K. A., & Thomas, W. G. (2004) · Molecular Pharmacology · doi:10.1124/mol.104.004721 · Cited by 10 · see citing works
Liyan, S., Chu, T., Wang, Y., et al. (2007) · Acta Biochimica et Biophysica Sinica · doi:10.1111/j.1745-7270.2007.00321.x · Cited by 10 · see citing works
Xiao, Y.-Y., Beilstein, M. A., Wang, M.-C., Purintrapiban, J., & Forsberg, N. E. (2002) · The International Journal of Biochemistry & Cell Biology · doi:10.1016/s1357-2725(02)00122-x · Cited by 7 · see citing works
Using BRET to Detect Ligand-Specific Conformational Changes in Preformed Signalling Complexes
Audet, N., & Piñeyro, G. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-160-4_7 · Cited by 7 · see citing works
OTSUJI, T. (2004) · Analytical Biochemistry · doi:10.1016/s0003-2697(04)00224-6 · Cited by 3 · see citing works
YAMAKAWA, Y., Ueda, H., Kitayama, A., et al. (2002) · Journal of Bioscience and Bioengineering · doi:10.1263/jbb.93.537 · Cited by 3 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Modulators of Protein–Protein Interactions
Milroy, L.-G., Grossmann, T. N., Hennig, S., Brunsveld, L., & Ottmann, C. (2014) · Chemical Reviews · doi:10.1021/cr400698c · Cited by 497 · see citing works
High-Throughput Screening: today’s biochemical and cell-based approaches
Blay, V., Tolani, B., Ho, S. P., & Arkin, M. R. (2020) · Drug Discovery Today · doi:10.1016/j.drudis.2020.07.024 · Cited by 404 · see citing works
Target engagement and drug residence time can be observed in living cells with BRET
Robers, M. B., Dart, M. L., Woodroofe, C. C., Zimprich, C., Kirkland, T. A., Machleidt, T., Kupcho, K. R., Levin, S., Hartnett, J. R., Zimmerman, K., et al. (2015) · Nature Communications · doi:10.1038/ncomms10091 · Cited by 275 · see citing works
Medicinal Chemistry Strategies to Disrupt the p53–MDM2/MDMX Interaction
Lemos, A., Leão, M., Soares, J., Palmeira, A., Pinto, M. M. M., Saraiva, L., & Sousa, M. E. (2016) · Medicinal Research Reviews · doi:10.1002/med.21393 · Cited by 83 · see citing works
NanoLuc Luciferase – A Multifunctional Tool for High Throughput Antibody Screening
Boute, N., Lowe, P. R., Berger, S., Malissard, M., Robert, A., & Tesar, M. (2016) · Frontiers in Pharmacology · doi:10.3389/fphar.2016.00027 · Cited by 77 · see citing works
A platform of BRET-FRET hybrid biosensors for optogenetics, chemical screening, and in vivo imaging
Komatsu, N., Terai, K., Imanishi, A., Kamioka, Y., Sumiyama, K., Jin, T., Okada, Y., Nagai, T., & Matsuda, M. (2018) · Scientific Reports · doi:10.1038/s41598-018-27174-x · Cited by 71 · see citing works
New Pharmacological Perspectives for the Leptin Receptor in the Treatment of Obesity
Roujeau, C., Jockers, R., & Dam, J. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00167 · Cited by 70 · see citing works
Khamlichi, C. E., Reverchon, F., Hervouet, N., Blot, L., Reiter, É., & Morisset‐Lopez, S. (2019) · Molecules · doi:10.3390/molecules24030537 · Cited by 62 · see citing works
Béry, N., Cruz-Migoni, A., Bataille, C. J. R., Quevedo, C. E., Tulmin, H., Miller, A., Russell, A. J., Phillips, S. E. V., Carr, S. B., & Rabbitts, T. H. (2018) · eLife · doi:10.7554/elife.37122 · Cited by 56 · see citing works
Regulation of NF-κB by the p105-ABIN2-TPL2 complex and RelAp43 during rabies virus infection
Besson, B., Sonthonnax, F., Duchateau, M., Khalifa, Y. B., Larrous, F., Eun, H., Hourdel, V., Matondo, M., Chamot‐Rooke, J., Grailhe, R., et al. (2017) · PLoS Pathogens · doi:10.1371/journal.ppat.1006697 · Cited by 42 · see citing works
Mo, X., Luo, Y., Ivanov, A. A., Su, R., Havel, J. J., Li, Z., Khuri, F. R., Du, Y., & Fu, H. (2015) · Journal of Molecular Cell Biology · doi:10.1093/jmcb/mjv064 · Cited by 40 · see citing works
Bioluminescence Resonance Energy Transfer to Detect Protein-Protein Interactions in Live Cells
Brown, N. E., Blumer, J., & Hepler, J. R. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2425-7_30 · Cited by 37 · see citing works
Use of BRET to Study Protein–Protein Interactions In Vitro and In Vivo
Dimri, S., Basu, S., & De, A. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3724-0_5 · Cited by 32 · see citing works
Mo, X., & Fu, H. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-3673-1_17 · Cited by 28 · see citing works
Kim, J., & Grailhe, R. (2016) · Cytometry Part A · doi:10.1002/cyto.a.22870 · Cited by 24 · see citing works
Besson, B., Eun, H., Kim, S., Windisch, M. P., Bourhy, H., & Grailhe, R. (2022) · Scientific Reports · doi:10.1038/s41598-022-12851-9 · Cited by 21 · see citing works
Dimri, S., Malhotra, R., Shet, T. M., Mokal, S., Gupta, S., & De, A. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.112313 · Cited by 20 · see citing works
Materials for FRET Analysis: Beyond Traditional Dye–Dye Combinations
Sapsford, K. E., Wildt, B., Mariani, A., Yeatts, A. B., & Medintz, I. L. (2013) · Wiley eBooks · doi:10.1002/9783527656028.ch06 · Cited by 14 · see citing works
Targeting the cis ‐dimerization of LINGO ‐1 with low MW compounds affects its downstream signalling
Cobret, L., de Tauzia, M.-L., Ferent, J., Traiffort, É., Hénaoui, I. S., Godin, F., Kellenberger, E., Rognan, D., Pantel, J., Bénédetti, H., et al. (2014) · British Journal of Pharmacology · doi:10.1111/bph.12945 · Cited by 14 · see citing works
Béry, N., & Rabbitts, T. H. (2019) · Current Protocols in Cell Biology · doi:10.1002/cpcb.83 · Cited by 12 · see citing works
Protein interactions study through proximity-labeling
Béganton, B., Solassol, I., Mangé, A., & Solassol, J. (2019) · Expert Review of Proteomics · doi:10.1080/14789450.2019.1638769 · Cited by 12 · see citing works
Antonio, V. D., Palù, G., & Alvisi, G. (2021) · Microorganisms · doi:10.3390/microorganisms9050928 · Cited by 11 · see citing works
Coriano, C. G., Powell, E., & Xu, W. (2016) · Methods in molecular biology · doi:10.1007/978-1-4939-6346-1_1 · Cited by 10 · see citing works
Chou, Y., Hsu, F., Hu, D.-Y., Chen, Y., Hsu, Y., Hsu, J. T.-A., & Chau, L. (2018) · Journal of Biomedical Science · doi:10.1186/s12929-018-0411-y · Cited by 9 · see citing works
Approches nouvelles pour l’étude des interactions protéine-protéine
Béganton, B., Coyaud, É., Mangé, A., & Solassol, J. (2019) · médecine/sciences · doi:10.1051/medsci/2019035 · Cited by 8 · see citing works
Comment on “The Use of BRET to Study Receptor-Protein Interactions”
Jockers, R. (2014) · Frontiers in Endocrinology · doi:10.3389/fendo.2014.00003 · Cited by 8 · see citing works
A BRET Ca 2+ sensor enables high-throughput screening in the presence of background fluorescence
Cumberbatch, D., Mori, T., Yang, J., Mi, D., Vinson, P. N., Weaver, C. D., & Johnson, C. H. (2022) · Science Signaling · doi:10.1126/scisignal.abq7618 · Cited by 7 · see citing works
Hirai, Y., Nishino, E., & Ohmori, H. (2015) · Journal of Neurophysiology · doi:10.1152/jn.00005.2015 · Cited by 6 · see citing works
Detection of β-Arrestin-Mediated G Protein-Coupled Receptor Ubiquitination Using BRET
Nagi, K., & Shenoy, S. K. (2019) · Methods in molecular biology · doi:10.1007/978-1-4939-9158-7_6 · Cited by 6 · see citing works
Mild, J. G., Fernández, L. R., Gayet, O., Iovanna, J., Dusetti, N., & Edreira, M. M. (2018) · Molecular Biotechnology · doi:10.1007/s12033-018-0078-3 · Cited by 5 · see citing works
iBRET Screen of the ABCD1 Peroxisomal Network and Mutation-Induced Network Perturbations
Lotz-Havla, A. S., Woidy, M., Guder, P., Friedel, C. C., Klingbeil, J. M., Bulau, A., Schultze, A., Dahmen, I., Noll‐Puchta, H., Kemp, S., et al. (2021) · Journal of Proteome Research · doi:10.1021/acs.jproteome.1c00330 · Cited by 5 · see citing works
Bourque, K., Jones-Tabah, J., Mnasri, N., Martin, R., & Hébert, T. E. (2018) · Biomolecules · doi:10.3390/biom8040180 · Cited by 4 · see citing works
Stumpf, C., Wimmer, T., Lorenz, B., & Stieger, K. (2020) · PLoS ONE · doi:10.1371/journal.pone.0230344 · Cited by 4 · see citing works
Biocompatible self-illuminating sphingomyelin nanosystems for photodynamic-based cancer therapy
Abal-Sanisidro, M., Palencia‐Campos, A., Ruíz-Cañas, L., García-Fernández, J., Cañada-García, L., Batres-Ramos, S., López‐López, R., Moreno, R., Martín‐Pastor, M., Sáinz, B., et al. (2025) · Journal of Controlled Release · doi:10.1016/j.jconrel.2025.113982 · Cited by 3 · see citing works
Baiula, M. (2020) · Methods in molecular biology · doi:10.1007/978-1-0716-0884-5_4 · Cited by 3 · see citing works
Baiula, M. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1708-2_8 · Cited by 2 · see citing works
Drug Design Methods to Regulate Protein–Protein Interactions
Poluri, K. M., Gulati, K., Tripathi, D. K., & Nagar, N. (2023) · Springer eBooks · doi:10.1007/978-981-99-2423-3_6 · Cited by 2 · see citing works
Detection of Protein-protein Interactions by FRET and BRET Methods
Matoulková, E., & Vojtěšek, B. (2014) · Klinicka onkologie · doi:10.14735/amko20141s82 · Cited by 2 · see citing works
Zhuang, C., & Sheng, C. (2018) · Springer eBooks · doi:10.1007/978-981-13-0773-7_2 · Cited by 2 · see citing works
Palmer, M. A. J. (2015) · Small Molecule Medicinal Chemistry · doi:10.1002/9781118771723.ch10 · Cited by 2 · see citing works
Koshiba, T. (2015) · Biophysics and Physicobiology · doi:10.2142/biophysico.12.0_31 · Cited by 1 · see citing works
Ohmori, H. (2019) · Neuromethods · doi:10.1007/978-1-4939-9944-6_6 · Cited by 1 · see citing works
High Throughput Screening Methods for PPI Inhibitor Discovery
Doyle, S. P., Mo, X., Qian, K., Cicka, D., Niu, Q., & Fu, H. (2020) · Royal Society of Chemistry eBooks · doi:10.1039/9781788016544-00049 · Cited by 1 · see citing works
In Vivo Bioluminescence Imaging as a Tool for Drug Development
Contag, C. H. (2014) · CRC Press eBooks · doi:10.1201/b17288-30
Dose et cofacteurs des protéines Hox lors du développement des organes de vol chez les insectes
Giraud, G. (2020) · theses.fr (ABES) · doi:10.70675/50757190zb2d8z4fc2zbc96zfea34ff0071c
Evaluation of Self-Illuminating Nanoconjugates Against Pancreatic Ductal Adenocarcinoma
Abal-Sanisidro, M., Ruíz-Cañas, L., Batres-Ramos, S., Blanco, M., García-Bermejo, M. L., García-Fernández, J., Rodríguez-Cobo, L., Higuera, J. M. L., Sáinz, B., & de la Fuente, M. (2026) · International Journal of Nanomedicine · doi:10.2147/ijn.s545161
High-Throughput Polymer Design for the Biological Interface
Chittari, S. S., & Gormley, A. J. (2026) · Bioconjugate Chemistry · doi:10.1021/acs.bioconjchem.6c00447
- Authors
- Couturier, C., & Deprez, B.
- Affiliations
- Université Lille Nord de France (FR)
- Inserm (FR)
- Corresponding author
- Couturier, Cyril
- Venue
- Frontiers in Endocrinology
- Publisher
- Frontiers Media SA
- Published
- 2012
- Volume
- 3
- Pages
- 100-100
- ISSN
- 1664-2392 (ISSN-L)
- PMC
- PMC3438444
- OpenAlex
- W2001186298
- Cited by
- 52
- References
- 120
- Citations by year
- 2026: 2 · 2025: 1 · 2023: 1 · 2022: 2 · 2021: 3 · 2020: 6 · 2019: 7 · 2018: 7 · 2017: 2 · 2016: 7 · 2015: 6 · 2014: 7 · 2013: 1
- FWCI
- 1.80
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Endocrinology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HAL (submittedVersion)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › bioluminescence and chemiluminescence research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Biophysics › Advanced Fluorescence Microscopy Techniques
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Biotin and Related Studies
- Keywords
- bioluminescence resonance energy transfer, protein-protein interaction inhibitors, high-throughput screening, protein-protein interaction network, mammalian cells, Z' factor, receptor activation
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
