Nanoluciferase-based complementation assays to monitor activation, modulation and signaling of receptor tyrosine kinases (RTKs).
Dosquet, Hugo; Neirinckx, Virginie; MEYRATH, Max Marc Rogeret al.
2023 • In Chapter One - Nanoluciferase-based complementation assays to monitor activation, modulation and signaling of receptor tyrosine kinases (RTKs)
[en] Receptor tyrosine kinases (RTKs) are transmembrane receptors activated by a wide diversity of growth factors, cytokines or hormones. They ensure multiple roles in cellular processes, including proliferation, differentiation and survival. They are also crucial drivers of development and progression of multiple cancer types, and represent important drug targets. Generally, ligand binding induces dimerization of RTK monomers, which induces auto-/transphosphorylation of tyrosine residues on the intracellular tails leading to the recruitment of adaptor proteins and modifying enzymes to promote and modulate various downstream signaling pathways. This chapter details easy, rapid, sensitive and versatile methods based on split Nanoluciferase complementation technology (NanoBiT) to monitor activation and modulation of two models of RTKs (EGFR and AXL) through the measurement of their dimerization and the recruitment of the adaptor protein Grb2 (SH2 domain-containing growth factor receptor-bound protein 2) and the receptor-modifying enzyme, the ubiquitin ligase Cbl.
Disciplines :
Oncology
Author, co-author :
Dosquet, Hugo; Department of Cancer Research, NORLUX Neuro-Oncology Laboratory, Luxembourg Institute of Health (LIH), Luxembourg City, Luxembourg.
Neirinckx, Virginie; Laboratory of Nervous System Diseases and Therapy, GIGA Neuroscience, GIGA Institute, University of Liège, Liège, Belgium.
MEYRATH, Max Marc Roger ; University of Luxembourg > Luxembourg Centre for Systems Biomedicine > Translational Neuroscience > Team Rejko KRÜGER ; Department of Infection and Immunity, Immunopharmacology and Interactomics, Luxembourg Institute of Health (LIH), Esch-sur-Alzette, Luxembourg.
Wantz, May; Department of Infection and Immunity, Immunopharmacology and Interactomics, Luxembourg Institute of Health (LIH), Esch-sur-Alzette, Luxembourg.
HAAN, Serge ; University of Luxembourg > Faculty of Science, Technology and Medicine (FSTM) > Department of Life Sciences and Medicine (DLSM)
NICLOU, Simone P. ; Department of Cancer Research, NORLUX Neuro-Oncology Laboratory, Luxembourg Institute of Health (LIH), Luxembourg City, Luxembourg, Department of Biomedicine, University of Bergen, Bergen, Norway.
SZPAKOWSKA, Martyna ; Department of Infection and Immunity, Immunopharmacology and Interactomics, Luxembourg Institute of Health (LIH), Esch-sur-Alzette, Luxembourg.
Chevigné, Andy; Department of Infection and Immunity, Immunopharmacology and Interactomics, Luxembourg Institute of Health (LIH), Esch-sur-Alzette, Luxembourg. Electronic address: andy.chevigne@lih.lu.
External co-authors :
yes
Language :
English
Title :
Nanoluciferase-based complementation assays to monitor activation, modulation and signaling of receptor tyrosine kinases (RTKs).
Publication date :
2023
Main work title :
Chapter One - Nanoluciferase-based complementation assays to monitor activation, modulation and signaling of receptor tyrosine kinases (RTKs)
Abourehab, M.A.S., Alqahtani, A.M., Youssif, B.G.M., Gouda, A.M., Globally approved EGFR inhibitors: Insights into their syntheses, target kinases, biological activities, receptor interactions, and metabolism. Molecules, 26, 2021, 6677 https://doi.org/10.3390/molecules26216677.
Ahmadi, S., et al. The landscape of receptor-mediated precision cancer combination therapy via a single-cell perspective. Nature Communications, 13, 2022, 1613, 10.1038/s41467-022-29154-2.
Bhalla, S., Fattah, F.J., Williams, J.N., Macchiaroli, A., Padro, J., Pogue, M., et al. Phase 1 dose escalation and expansion study of bemcentinib (BGB324), a first-in-class, selective AXL inhibitor, with docetaxel in patients with previously treated advanced NSCLC. Journal of Clinical Oncology, 40(16 suppl.), 2022 9081–9081.
Bjorkelund, H., Gedda, L., Barta, P., Malmqvist, M., Andersson, K., Gefitinib induces epidermal growth factor receptor dimers which alters the interaction characteristics with (1)(2)(5)I-EGF. PLoS One, 6, 2011, e24739, 10.1371/journal.pone.0024739.
Cancer Genome Atlas Research, N, Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455 (2008), 1061–1068, 10.1038/nature07385.
Chong, C.R., Janne, P.A., The quest to overcome resistance to EGFR-targeted therapies in cancer. Nature Medicine 19 (2013), 1389–1400, 10.1038/nm.3388.
Cohen, P., Cross, D., Janne, P.A., Kinase drug discovery 20 years after imatinib: Progress and future directions. Nature Reviews. Drug Discovery 20 (2021), 551–569, 10.1038/s41573-021-00195-4.
da Cunha Santos, G., Shepherd, F.A., Tsao, M.S., EGFR mutations and lung cancer. Annual Review of Pathology 6 (2011), 49–69, 10.1146/annurev-pathol-011110-130206.
Dixon, A.S., et al. NanoLuc complementation reporter optimized for accurate measurement of protein interactions in cells. ACS Chemical Biology 11 (2016), 400–408, 10.1021/acschembio.5b00753.
Ekstrand, A.J., Sugawa, N., James, C.D., Collins, V.P., Amplified and rearranged epidermal growth factor receptor genes in human glioblastomas reveal deletions of sequences encoding portions of the N- and/or C-terminal tails. Proceedings of the National Academy of Sciences of the United States of America 89 (1992), 4309–4313, 10.1073/pnas.89.10.4309.
Engelman, J.A., et al. MET amplification leads to gefitinib resistance in lung cancer by activating ERBB3 signaling. Science 316 (2007), 1039–1043, 10.1126/science.1141478.
Fukuoka, M., et al. Multi-institutional randomized phase II trial of gefitinib for previously treated patients with advanced non-small-cell lung cancer (The IDEAL 1 Trial) [corrected]. Journal of Clinical Oncology 21 (2003), 2237–2246, 10.1200/JCO.2003.10.038.
Kris, M.G., et al. Efficacy of gefitinib, an inhibitor of the epidermal growth factor receptor tyrosine kinase, in symptomatic patients with non-small cell lung cancer: A randomized trial. JAMA 290 (2003), 2149–2158, 10.1001/jama.290.16.2149.
Li, S., et al. Structural basis for inhibition of the epidermal growth factor receptor by cetuximab. Cancer Cell 7 (2005), 301–311, 10.1016/j.ccr.2005.03.003.
Luis, R., et al. Nanoluciferase-based methods to monitor activation, modulation and trafficking of atypical chemokine receptors. Methods in Cell Biology 169 (2022), 279–294, 10.1016/bs.mcb.2022.03.002.
Meyer, A.S., Miller, M.A., Gertler, F.B., Lauffenburger, D.A., The receptor AXL diversifies EGFR signaling and limits the response to EGFR-targeted inhibitors in triple-negative breast cancer cells. Science Signaling, 6, 2013, ra66, 10.1126/scisignal.2004155.
Meyrath, M., Reynders, N., Uchanski, T., Chevigne, A., Szpakowska, M., Systematic reassessment of chemokine-receptor pairings confirms CCL20 but not CXCL13 and extends the spectrum of ACKR4 agonists to CCL22. Journal of Leukocyte Biology 109 (2021), 373–376, 10.1002/JLB.2AB0520-275R.
Meyrath, M, Szpakowska, M, Plesseria, JM, Domingues, O, Langlet, J, Weber, B, et al. Nanoluciferase-based cell fusion assay for rapid and high-throughput assessment of SARS-CoV-2-neutralizing antibodies in patient samples. Methods Enzymol 675 (2022), 351–381, 10.1016/bs.mie.2022.07.015.
Neirinckx, V., et al. The soluble form of pan-RTK inhibitor and tumor suppressor LRIG1 mediates downregulation of AXL through direct protein-protein interaction in glioblastoma. Neurooncology Advances, 1, 2019, vdz024, 10.1093/noajnl/vdz024.
Niederst, M.J., Engelman, J.A., Bypass mechanisms of resistance to receptor tyrosine kinase inhibition in lung cancer. Science Signaling, 6, 2013, re6, 10.1126/scisignal.2004652.
Ostrom, Q.T., et al. CBTRUS statistical report: Primary brain and other central nervous system tumors diagnosed in the United States in 2012–2016. Neuro-Oncology 21 (2019), v1–v100, 10.1093/neuonc/noz150.
Palmer, C.B., et al. Nanoluciferase-based complementation assay for systematic profiling of GPCR-GRK interactions. Methods in Cell Biology 169 (2022), 309–321, 10.1016/bs.mcb.2022.04.001.
Pawson, T., Specificity in signal transduction: From phosphotyrosine-SH2 domain interactions to complex cellular systems. Cell 116 (2004), 191–203, 10.1016/s0092-8674(03)01077-8.
Perez-Soler, R., et al. Determinants of tumor response and survival with erlotinib in patients with non–small-cell lung cancer. Journal of Clinical Oncology 22 (2004), 3238–3247, 10.1200/JCO.2004.11.057.
Pottier, C., et al. Tyrosine kinase inhibitors in cancer: Breakthrough and challenges of targeted therapy. Cancers (Basel), 12, 2020, 10.3390/cancers12030731.
Rankin, E.B., Giaccia, A.J., The receptor tyrosine kinase AXL in cancer progression. Cancers (Basel), 8, 2016, 10.3390/cancers8110103.
Robichaux, J.P., et al. Structure-based classification predicts drug response in EGFR-mutant NSCLC. Nature 597 (2021), 732–737, 10.1038/s41586-021-03898-1.
Rubin, C., Gur, G., Yarden, Y., Negative regulation of receptor tyrosine kinases: Unexpected links to c-Cbl and receptor ubiquitylation. Cell Research 15 (2005), 66–71, 10.1038/sj.cr.7290268.
Shen, Y., Chen, X., He, J., Liao, D., Zu, X., Axl inhibitors as novel cancer therapeutic agents. Life Sciences 198 (2018), 99–111, 10.1016/j.lfs.2018.02.033.
Shimomura, O., Masugi, T., Johnson, F.H., Haneda, Y., Properties and reaction mechanism of the bioluminescence system of the deep-sea shrimp Oplophorus gracilorostris. Biochemistry 17 (1978), 994–998, 10.1021/bi00599a008.
Sigismund, S., Avanzato, D., Lanzetti, L., Emerging functions of the EGFR in cancer. Molecular Oncology 12 (2018), 3–20, 10.1002/1878-0261.12155.
Stoddart, L.A., Kilpatrick, L.E., Hill, S.J., NanoBRET approaches to study ligand binding to GPCRs and RTKs. Trends in Pharmacological Sciences 39 (2018), 136–147, 10.1016/j.tips.2017.10.006.
Tan, P.K., et al. Monitoring interactions between receptor tyrosine kinases and their downstream effector proteins in living cells using bioluminescence resonance energy transfer. Molecular Pharmacology 72 (2007), 1440–1446, 10.1124/mol.107.039636.
White, C.W., Caspar, B., Vanyai, H.K., Pfleger, K.D.G., Hill, S.J., CRISPR-Mediated protein tagging with nanoluciferase to investigate native chemokine receptor function and conformational changes. Cell Chemistry & Biology 27 (2020), 499–510 e497, 10.1016/j.chembiol.2020.01.010.
White, C.W., Vanyai, H.K., See, H.B., Johnstone, E.K.M., Pfleger, K.D.G., Using nanoBRET and CRISPR/Cas9 to monitor proximity to a genome-edited protein in real-time. Scientific Reports, 7, 2017, 3187, 10.1038/s41598-017-03486-2.
Yun, C.H., et al. The T790M mutation in EGFR kinase causes drug resistance by increasing the affinity for ATP. Proceedings of the National Academy of Sciences of the United States of America 105 (2008), 2070–2075, 10.1073/pnas.0709662105.
