April 28, 2024
Molecular sensing of mechano- and ligand-dependent adhesion GPCR dissociation – Nature

Molecular sensing of mechano- and ligand-dependent adhesion GPCR dissociation – Nature

  • Nieberler, M., Kittel, R. J., Petrenko, A. G., Lin, H.-H. & Langenhan, T. in Adhesion G Protein-coupled Receptors: Molecular, Physiological and Pharmacological Principles in Health and Disease (eds Langenhan, T. & Schöneberg, T.) 83–109 (2016).

  • Gordon, W. R. et al. Mechanical allostery: evidence for a force requirement in the proteolytic activation of Notch. Dev. Cell 33, 729–736 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Meloty-Kapella, L., Shergill, B., Kuon, J., Botvinick, E. & Weinmaster, G. Notch ligand endocytosis generates mechanical pulling force dependent on dynamin, epsins, and actin. Dev. Cell 22, 1299–1312 (2012).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Langridge, P. D. & Struhl, G. Epsin-dependent ligand endocytosis activates Notch by force. Cell 171, 1383–1396 (2017).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lin, H.-H. et al. Autocatalytic cleavage of the EMR2 receptor occurs at a conserved G protein-coupled receptor proteolytic site motif. J. Biol. Chem. 279, 31823–31832 (2004).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Araç, D. et al. A novel evolutionarily conserved domain of cell‐adhesion GPCRs mediates autoproteolysis. EMBO J. 31, 1364–1378 (2012).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krasnoperov, V. G. et al. α-Latrotoxin stimulates exocytosis by the interaction with a neuronal G-protein-coupled receptor. Neuron 18, 925–937 (1997).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Gray, J. X. et al. CD97 is a processed, seven-transmembrane, heterodimeric receptor associated with inflammation. J. Immunol. 157, 5438–5447 (1996).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Scholz, N. et al. The adhesion GPCR latrophilin/CIRL shapes mechanosensation. Cell Rep. 11, 866–874 (2015).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Scholz, N. et al. Mechano-dependent signaling by latrophilin/CIRL quenches cAMP in proprioceptive neurons. eLife 6, e28360 (2017).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Dannhäuser, S. et al. Antinociceptive modulation by the adhesion GPCR CIRL promotes mechanosensory signal discrimination. eLife 9, e56738 (2020).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Lavalou, J. et al. Formation of polarized contractile interfaces by self-organized Toll-8/Cirl GPCR asymmetry. Dev. Cell 56, 1574–1588 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bassilana, F., Nash, M. & Ludwig, M.-G. Adhesion G protein-coupled receptors: opportunities for drug discovery. Nat. Rev. Drug Discov. 18, 869–884 (2019).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Hamann, J. et al. International Union of Basic and Clinical Pharmacology. XCIV. Adhesion G protein-coupled receptors. Pharmacol. Rev. 67, 338–367 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Yeung, J. et al. GPR56/ADGRG1 is a platelet collagen-responsive GPCR and hemostatic sensor of shear force. Proc. Natl Acad. Sci. USA 117, 28275–28286 (2020).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Boyden, S. E. et al. Vibratory urticaria associated with a missense variant in ADGRE2. N. Engl. J. Med. 374, 656–663 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liu, D. et al. CD97 promotes spleen dendritic cell homeostasis through the mechanosensing of red blood cells. Science 375, eabi5965 (2022).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Petersen, S. C. et al. The adhesion GPCR GPR126 has distinct, domain-dependent functions in Schwann cell development mediated by interaction with Laminin-211. Neuron 85, 755–769 (2015).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Scholz, N., Monk, K. R., Kittel, R. J. & Langenhan, T. in Adhesion G Protein-coupled Receptors: Molecular, Physiological and Pharmacological Principles in Health and Disease (eds Langenhan, T. & Schöneberg, T.) 221–247 (2016).

  • Vizurraga, A., Adhikari, R., Yeung, J., Yu, M. & Tall, G. G. Mechanisms of adhesion G protein-coupled receptor activation. J. Biol. Chem. 295, 14065–14083 (2020).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Beliu, G. et al. Tethered agonist exposure in intact adhesion/class B2 GPCRs through intrinsic structural flexibility of the GAIN domain. Mol. Cell 81, 905–921 (2021).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Stoveken, H. M., Hajduczok, A. G., Xu, L. & Tall, G. G. Adhesion G protein-coupled receptors are activated by exposure of a cryptic tethered agonist. Proc. Natl Acad. Sci. USA 112, 6194–6199 (2015).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Liebscher, I. et al. A tethered agonist within the ectodomain activates the adhesion g protein-coupled receptors GPR126 and GPR133. Cell Rep. 9, 2018–2026 (2014).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Bohnekamp, J. & Schöneberg, T. Cell adhesion receptor GPR133 couples to Gs protein. J. Biol. Chem. 286, 41912–41916 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sando, R., Jiang, X. & Südhof, T. C. Latrophilin GPCRs direct synapse specificity by coincident binding of FLRTs and teneurins. Science 363, eaav7969 (2019).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Frenster, J. D. et al. Functional impact of intramolecular cleavage and dissociation of adhesion G protein–coupled receptor GPR133 (ADGRD1) on canonical signaling. J. Biol. Chem. 296, 100798 (2021).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Qu, X. et al. Structural basis of tethered agonism of the adhesion GPCRs ADGRD1 and ADGRF1. Nature 604, 779–785 (2022).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Barros-Álvarez, X. et al. The tethered peptide activation mechanism of adhesion GPCRs. Nature 604, 757–762 (2022).

    Article 
    ADS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Xiao, P. et al. Tethered peptide activation mechanism of the adhesion GPCRs ADGRG2 and ADGRG4. Nature 604, 771–778 (2022).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Ping, Y.-Q. et al. Structural basis for the tethered peptide activation of adhesion GPCRs. Nature 604, 763–770 (2022).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Kopan, R. & Ilagan, Ma. X. G. The canonical Notch signaling pathway: unfolding the activation mechanism. Cell 137, 216–233 (2009).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Stephenson, N. L. & Avis, J. M. Direct observation of proteolytic cleavage at the S2 site upon forced unfolding of the Notch negative regulatory region. Proc. Natl Acad. Sci. USA 109, E2757–E2765 (2012).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Schroeter, E. H., Kisslinger, J. A. & Kopan, R. Notch-1 signalling requires ligand-induced proteolytic release of intracellular domain. Nature 393, 382–386 (1998).

    Article 
    ADS 
    CAS 
    PubMed 

    Google Scholar
     

  • Strooper, B. D. et al. A presenilin-1-dependent γ-secretase-like protease mediates release of Notch intracellular domain. Nature 398, 518–522 (1999).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Struhl, G. & Adachi, A. Nuclear access and action of Notch in vivo. Cell 93, 649–660 (1998).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Mumm, J. S. et al. A ligand-induced extracellular cleavage regulates γ-secretase-like proteolytic activation of Notch1. Mol. Cell 5, 197–206 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Rebay, I., Fehon, R. G. & Artavanis-Tsakonas, S. Specific truncations of Drosophila Notch define dominant activated and dominant negative forms of the receptor. Cell 74, 319–329 (1993).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Karpus, O. N. et al. Shear stress-dependent downregulation of the adhesion-G protein-coupled receptor CD97 on circulating leukocytes upon contact with its ligand CD55. J. Immunol. 190, 3740–3748 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Desai, B. S., Chadha, A. & Cook, B. The stum gene is essential for mechanical sensing in proprioceptive neurons. Science 343, 1256–1259 (2014).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • He, L., Binari, R., Huang, J., Falo-Sanjuan, J. & Perrimon, N. In vivo study of gene expression with an enhanced dual-color fluorescent transcriptional timer. eLife 8, e46181 (2019).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Krasnoperov, V. et al. Dissociation of the subunits of the calcium-independent receptor of α-latrotoxin as a result of two-step proteolysis. Biochemistry 48, 3230–3238 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Pereanu, W. & Hartenstein, V. Neural lineages of the Drosophila brain: a three-dimensional digital atlas of the pattern of lineage location and projection at the late larval stage. J. Neurosci. 26, 5534–5553 (2006).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Shearin, H. K., Quinn, C. D., Mackin, R. D., Macdonald, I. S. & Stowers, R. S. t-GRASP, a targeted GRASP for assessing neuronal connectivity. J. Neurosci. Meth. 306, 94–102 (2018).

    Article 
    CAS 

    Google Scholar
     

  • Feinberg, E. H. et al. GFP reconstitution across synaptic partners (GRASP) defines cell contacts and synapses in living nervous systems. Neuron 57, 353–363 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Ito, K., Urban, J. & Technau, G. M. Distribution, classification, and development of Drosophila glial cells in the late embryonic and early larval ventral nerve cord. Rouxs Arch. Dev. Biol. 204, 284–307 (1995).

    Article 
    PubMed 

    Google Scholar
     

  • Usui, T. et al. Flamingo, a seven-pass transmembrane cadherin, regulates planar cell polarity under the control of Frizzled. Cell 98, 585–595 (1999).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Scholz, N., Langenhan, T. & Schöneberg, T. Revisiting the classification of adhesion GPCRs. Ann. NY Acad. Sci. 1456, 80–95 (2019).

    Article 
    ADS 
    PubMed 

    Google Scholar
     

  • Blanco-Redondo, B. & Langenhan, T. Parallel genomic engineering of two Drosophila genes using orthogonal attB/attP sites. G3 8, 3109–3118 (2018).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Kawasaki, T. & Kawai, T. Toll-Like receptor signaling pathways. Front. Immunol. 5, 461 (2014).

    Article 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Sprinzak, D. et al. Cis-interactions between Notch and Delta generate mutually exclusive signalling states. Nature 465, 86–90 (2010).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Diegelmann, S., Bate, M. & Landgraf, M. Gateway cloning vectors for the LexA-based binary expression system in Drosophila. Fly 2, 236–239 (2008).

    Article 
    PubMed 

    Google Scholar
     

  • Lai, S.-L. & Lee, T. Genetic mosaic with dual binary transcriptional systems in Drosophila. Nat. Neurosci. 9, 703–709 (2006).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Struhl, G. & Adachi, A. Requirements for presenilin-dependent cleavage of notch and other transmembrane proteins. Mol. Cell 6, 625–636 (2000).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Harder, B. et al. TEV protease-mediated cleavage in Drosophila as a tool to analyze protein functions in living organisms. Biotechniques 44, 765–772 (2008).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Baas, S. et al. Sugar-free frosting, a homolog of SAD kinase, drives neural-specific glycan expression in the Drosophila embryo. Development 138, 553–563 (2011).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ayyar, S. et al. NF-κB/Rel-mediated regulation of the neural fate in Drosophila. PLoS ONE 2, e1178 (2007).

  • Pogodalla, N. et al. Drosophila ßHeavy-Spectrin is required in polarized ensheathing glia that form a diffusion-barrier around the neuropil. Nat. Commun. 12, 6357 (2021).

    Article 
    ADS 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Li, H.-H. et al. A GAL4 driver resource for developmental and behavioral studies on the larval CNS of Drosophila. Cell Rep. 8, 897–908 (2014).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Sanyal, S. Genomic mapping and expression patterns of C380, OK6 and D42 enhancer trap lines in the larval nervous system of Drosophila. Gene Expr. Patterns 9, 371–380 (2009).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Potter, C. J., Tasic, B., Russler, E. V., Liang, L. & Luo, L. The Q system: a repressible binary system for transgene expression, lineage tracing, and mosaic analysis. Cell 141, 536–548 (2010).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

  • Ljaschenko, D., Ehmann, N. & Kittel, R. J. Hebbian plasticity guides maturation of glutamate receptor fields in vivo. Cell Rep. 3, 1407–1413 (2013).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Stewart, B. A., Atwood, H. L., Renger, J. J., Wang, J. & Wu, C.-F. Improved stability of Drosophila larval neuromuscular preparations in haemolymph-like physiological solutions. J. Comp. Physiol. 175, 179–191 (1994).

    Article 
    CAS 

    Google Scholar
     

  • Schmid, A. & Sigrist, S. J. in Drosophila, Methods and Protocols 1st edn (ed. Dahmann, C.) 239–251 (2008).

  • Tyanova, S., Temu, T. & Cox, J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat. Protoc. 11, 2301–2319 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Tyanova, S. et al. The Perseus computational platform for comprehensive analysis of (prote)omics data. Nat. Methods 13, 731–740 (2016).

    Article 
    CAS 
    PubMed 

    Google Scholar
     

  • Schmied, C. & Tomancak, P. in Drosophila, Methods and Protocols 2nd edn (ed. Dahmann, C.) 189–202 (2016).

  • Tuthill, J. C. & Wilson, R. I. Parallel transformation of tactile signals in central circuits of Drosophila. Cell 164, 1046–1059 (2016).

    Article 
    CAS 
    PubMed 
    PubMed Central 

    Google Scholar
     

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