Active state structures of a bistable visual opsin bound to G proteins.
Journal
Nature communications
ISSN: 2041-1723
Titre abrégé: Nat Commun
Pays: England
ID NLM: 101528555
Informations de publication
Date de publication:
16 Oct 2024
16 Oct 2024
Historique:
received:
10
04
2024
accepted:
04
10
2024
medline:
17
10
2024
pubmed:
17
10
2024
entrez:
16
10
2024
Statut:
epublish
Résumé
Opsins are G protein-coupled receptors (GPCRs) that have evolved to detect light stimuli and initiate intracellular signaling cascades. Their role as signal transducers is critical to light perception across the animal kingdom. Opsins covalently bind to the chromophore 11-cis retinal, which isomerizes to the all-trans isomer upon photon absorption, causing conformational changes that result in receptor activation. Monostable opsins, responsible for vision in vertebrates, release the chromophore after activation and must bind another retinal molecule to remain functional. In contrast, bistable opsins, responsible for non-visual light perception in vertebrates and for vision in invertebrates, absorb a second photon in the active state to return the chromophore and protein to the inactive state. Structures of bistable opsins in the activated state have proven elusive, limiting our understanding of how they function as bidirectional photoswitches. Here we present active state structures of a bistable opsin, jumping spider rhodopsin isoform-1 (JSR1), in complex with its downstream signaling partners, the G
Identifiants
pubmed: 39414813
doi: 10.1038/s41467-024-53208-2
pii: 10.1038/s41467-024-53208-2
doi:
Substances chimiques
Opsins
0
Rhodopsin
9009-81-8
GTP-Binding Proteins
EC 3.6.1.-
GTP-Binding Protein alpha Subunits, Gq-G11
EC 3.6.5.1
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
8928Subventions
Organisme : EC | EU Framework Programme for Research and Innovation H2020 | H2020 Priority Excellent Science | H2020 European Research Council (H2020 Excellent Science - European Research Council)
ID : 951644
Informations de copyright
© 2024. The Author(s).
Références
Terakita, A., Kawano-Yamashita, E. & Koyanagi, M. Evolution and diversity of opsins. Wiley Interdiscip. Rev. Membr. Transp. Signal. 1, 104–111 (2012).
doi: 10.1002/wmts.6
Koyanagi, M. & Terakita, A. Gq-coupled rhodopsin subfamily composed of invertebrate visual pigment and melanopsin. Photochem. Photobiol. 84, 1024–1030 (2008).
pubmed: 18513236
doi: 10.1111/j.1751-1097.2008.00369.x
Koyanagi, M. & Terakita, A. Diversity of animal opsin-based pigments and their optogenetic potential. Biochim. Biophys. Acta 1837, 710–716 (2014).
pubmed: 24041647
doi: 10.1016/j.bbabio.2013.09.003
Roberts, N. S., Hagen, J. F. D. & Johnston, R. J. The diversity of invertebrate visual opsins spanning Protostomia, Deuterostomia, and Cnidaria. Dev. Biol. 492, 187–199 (2022).
pubmed: 36272560
pmcid: 10249108
doi: 10.1016/j.ydbio.2022.10.011
Zhang, K. X. et al. Violet-light suppression of thermogenesis by opsin 5 hypothalamic neurons. Nature 585, 420–425 (2020).
pubmed: 32879486
pmcid: 8130195
doi: 10.1038/s41586-020-2683-0
Nguyen, M. T. et al. An opsin 5-dopamine pathway mediates light-dependent vascular development in the eye. Nat. Cell Biol. 21, 420–429 (2019).
pubmed: 30936473
pmcid: 6573021
doi: 10.1038/s41556-019-0301-x
Panda, S. et al. Melanopsin (Opn4) requirement for normal light-induced circadian phase shifting. Science 298, 2213–2216 (2002).
pubmed: 12481141
doi: 10.1126/science.1076848
Buhr, E. D. et al. Neuropsin (OPN5)-mediated photoentrainment of local circadian oscillators in mammalian retina and cornea. Proc. Natl. Acad. Sci. USA 112, 13093–13098 (2015).
pubmed: 26392540
pmcid: 4620855
doi: 10.1073/pnas.1516259112
Isberg, V. et al. Generic GPCR residue numbers - aligning topology maps while minding the gaps. Trends Pharm. Sci. 36, 22–31 (2015).
pubmed: 25541108
doi: 10.1016/j.tips.2014.11.001
Terakita, A. et al. Counterion displacement in the molecular evolution of the rhodopsin family. Nat. Struct. Mol. Biol. 11, 284–289 (2004).
pubmed: 14981504
doi: 10.1038/nsmb731
Varma, N. et al. Crystal structure of jumping spider rhodopsin-1 as a light sensitive GPCR. Proc. Natl. Acad. Sci. USA 116, 14547–14556 (2019).
pubmed: 31249143
pmcid: 6642406
doi: 10.1073/pnas.1902192116
Nagata, T. et al. The counterion–retinylidene Schiff base interaction of an invertebrate rhodopsin rearranges upon light activation. Commun. Biol. 2, 180 (2019).
pubmed: 31098413
pmcid: 6513861
doi: 10.1038/s42003-019-0409-3
Li, J., Edwards, P. C., Burghammer, M., Villa, C. & Schertler, G. F. Structure of bovine rhodopsin in a trigonal crystal form. J. Mol. Biol. 343, 1409–1438 (2004).
pubmed: 15491621
doi: 10.1016/j.jmb.2004.08.090
Palczewski, K. et al. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289, 739–745 (2000).
pubmed: 10926528
doi: 10.1126/science.289.5480.739
Nagata, T. et al. Depth perception from image defocus in a jumping spider. Science 335, 469–471 (2012).
pubmed: 22282813
doi: 10.1126/science.1211667
Ehrenberg, D. et al. The two-photon reversible reaction of the bistable jumping spider rhodopsin-1. Biophys. J. 116, 1248–1258 (2019).
pubmed: 30902364
pmcid: 6451042
doi: 10.1016/j.bpj.2019.02.025
Mühle, J. et al. Cyclic peptide inhibitors stabilize Gq/11 heterotrimers. Preprint at bioRxiv https://doi.org/10.1101/2023.10.24.563737 (2023).
Rodrigues, M. J. et al. Activating an invertebrate bistable opsin with the all-trans 6.11 retinal analog. Proc. Natl. Acad. Sci. USA 121, e2406814121 (2024).
pubmed: 39042699
pmcid: 11295067
doi: 10.1073/pnas.2406814121
Tsukamoto, H. & Terakita, A. Diversity and functional properties of bistable pigments. Photochem. Photobiol. Sci. 9, 1435–1443 (2010).
pubmed: 20852774
doi: 10.1039/c0pp00168f
Murakami, M. & Kouyama, T. Crystal structure of squid rhodopsin. Nature 453, 363–367 (2008).
pubmed: 18480818
doi: 10.1038/nature06925
Ota, T., Furutani, Y., Terakita, A., Shichida, Y. & Kandori, H. Structural changes in the Schiff base region of squid rhodopsin upon photoisomerization studied by low-temperature FTIR spectroscopy. Biochemistry 45, 2845–2851 (2006).
pubmed: 16503639
doi: 10.1021/bi051937l
Murakami, M. & Kouyama, T. Crystallographic analysis of the primary photochemical reaction of squid rhodopsin. J. Mol. Biol. 413, 615–627 (2011).
pubmed: 21906602
doi: 10.1016/j.jmb.2011.08.044
Murakami, M. & Kouyama, T. Crystallographic study of the LUMI intermediate of squid rhodopsin. PLoS ONE 10, e0126970 (2015).
pubmed: 26024518
pmcid: 4449009
doi: 10.1371/journal.pone.0126970
Deupi, X. et al. Stabilized G protein binding site in the structure of constitutively active metarhodopsin-II. Proc. Natl. Acad. Sci. USA 109, 119–124 (2012).
pubmed: 22198838
doi: 10.1073/pnas.1114089108
Choe, H.-W. et al. Crystal structure of metarhodopsin II. Nature 471, 651–655 (2011).
pubmed: 21389988
doi: 10.1038/nature09789
Tsai, C.-J. et al. Crystal structure of rhodopsin in complex with a mini-G
pubmed: 30255144
pmcid: 6154990
doi: 10.1126/sciadv.aat7052
Singhal, A. et al. Structural role of the T94I rhodopsin mutation in congenital stationary night blindness. EMBO Rep. 17, 1431–1440 (2016).
pubmed: 27458239
pmcid: 5048376
doi: 10.15252/embr.201642671
Jastrzebska, B., Palczewski, K. & Golczak, M. Role of bulk water in hydrolysis of the rhodopsin chromophore. J. Biol. Chem. 286, 18930–18937 (2011).
pubmed: 21460218
pmcid: 3099708
doi: 10.1074/jbc.M111.234583
Janz, J. M. & Farrens, D. L. Role of the retinal hydrogen bond network in rhodopsin Schiff base stability and hydrolysis. J. Biol. Chem. 279, 55886–55894 (2004).
pubmed: 15475355
doi: 10.1074/jbc.M408766200
Rosenbaum, D. M., Rasmussen, S. G. F. & Kobilka, B. K. The structure and function of G-protein-coupled receptors. Nature 459, 356–363 (2009).
pubmed: 19458711
pmcid: 3967846
doi: 10.1038/nature08144
Venkatakrishnan, A. J. et al. Molecular signatures of G-protein-coupled receptors. Nature 494, 185–194 (2013).
pubmed: 23407534
doi: 10.1038/nature11896
Goncalves, J. A. et al. Highly conserved tyrosine stabilizes the active state of rhodopsin. Proc. Natl. Acad. Sci. USA 107, 19861–19866 (2010).
pubmed: 21041664
pmcid: 2993422
doi: 10.1073/pnas.1009405107
Valentin-Hansen, L. et al. The arginine of the DRY motif in transmembrane segment III functions as a balancing micro-switch in the activation of the β2-adrenergic receptor. J. Biol. Chem. 287, 31973–31982 (2012).
pubmed: 22843684
pmcid: 3442529
doi: 10.1074/jbc.M112.348565
Cherezov, V. et al. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318, 1258–1265 (2007).
pubmed: 17962520
pmcid: 2583103
doi: 10.1126/science.1150577
Rasmussen, S. G. F. et al. Crystal structure of the β2 adrenergic receptor–Gs protein complex. Nature 477, 549–555 (2011).
pubmed: 21772288
pmcid: 3184188
doi: 10.1038/nature10361
Weis, W. I. & Kobilka, B. K. The molecular basis of G protein-coupled receptor activation. Annu. Rev. Biochem. 87, 897–919 (2018).
pubmed: 29925258
pmcid: 6535337
doi: 10.1146/annurev-biochem-060614-033910
Zhou, Q. et al. Common activation mechanism of class A GPCRs. ELife 8, e50279 (2019).
pubmed: 31855179
pmcid: 6954041
doi: 10.7554/eLife.50279
Pándy-Szekeres, G. et al. The G protein database, GproteinDb. Nucleic Acids Res. 50, D518–D525 (2022).
pubmed: 34570219
doi: 10.1093/nar/gkab852
Rose, A. S. et al. Position of transmembrane helix 6 determines receptor G protein coupling specificity. J. Am. Chem. Soc. 136, 11244–11247 (2014).
pubmed: 25046433
doi: 10.1021/ja5055109
Nygaard, R. et al. The dynamic process of β(2)-adrenergic receptor activation. Cell 152, 532–542 (2013).
pubmed: 23374348
pmcid: 3586676
doi: 10.1016/j.cell.2013.01.008
Yan, E. C. et al. Retinal counterion switch in the photoactivation of the G protein-coupled receptor rhodopsin. Proc. Natl. Acad. Sci. USA 100, 9262–9267 (2003).
pubmed: 12835420
pmcid: 170906
doi: 10.1073/pnas.1531970100
Hanai, S. et al. Difference FTIR spectroscopy of jumping spider rhodopsin-1 at 77 K. Biochemistry 62, 1347–1359 (2023).
pubmed: 37001008
doi: 10.1021/acs.biochem.3c00022
Westfield, G. H. et al. Structural flexibility of the Gαs α-helical domain in the β2-adrenoceptor Gs complex. Proc. Natl. Acad. Sci. USA 108, 16086–16091 (2011).
pubmed: 21914848
pmcid: 3179071
doi: 10.1073/pnas.1113645108
Tsai, C.-J. et al. Cryo-EM structure of the rhodopsin-Gαi-βγ complex reveals binding of the rhodopsin C-terminal tail to the gβ subunit. ELife 8, e46041 (2019).
pubmed: 31251171
pmcid: 6629373
doi: 10.7554/eLife.46041
Hagio, H. et al. Optogenetic manipulation of Gq- and Gi/o-coupled receptor signaling in neurons and heart muscle cells. ELife 12, e83974 (2023).
pubmed: 37589544
pmcid: 10435233
doi: 10.7554/eLife.83974
Hu, J., Adebali, O., Adar, S. & Sancar, A. Dynamic maps of UV damage formation and repair for the human genome. Proc. Natl. Acad. Sci. USA 114, 6758–6763 (2017).
pubmed: 28607063
pmcid: 5495279
doi: 10.1073/pnas.1706522114
Albeck, A., Friedman, N., Sheves, M. & Ottolenghi, M. Role of retinal isomerizations and rotations in the photocycle of bacteriorhodopsin. J. Am. Chem. Soc. 108, 4614–4618 (1986).
doi: 10.1021/ja00275a056
Sun, D. et al. Probing Gαi1 protein activation at single-amino acid resolution. Nat. Struct. Mol. Biol. 22, 686–694 (2015).
pubmed: 26258638
pmcid: 4876908
doi: 10.1038/nsmb.3070
Maeda, S. et al. Crystallization scale preparation of a stable GPCR signaling complex between constitutively active rhodopsin and G-protein. PLoS ONE 9, e98714 (2014).
pubmed: 24979345
pmcid: 4076187
doi: 10.1371/journal.pone.0098714
Abdulrahman, W. et al. A set of baculovirus transfer vectors for screening of affinity tags and parallel expression strategies. Anal. Biochem. 385, 383–385 (2009).
pubmed: 19061853
doi: 10.1016/j.ab.2008.10.044
Punjani, A., Rubinstein, J. L., Fleet, D. J. & Brubaker, M. A. cryoSPARC: algorithms for rapid unsupervised cryo-EM structure determination. Nat. Methods 14, 290–296 (2017).
pubmed: 28165473
doi: 10.1038/nmeth.4169
Kimanius, D., Dong, L., Sharov, G., Nakane, T. & Scheres, S. H. W. New tools for automated cryo-EM single-particle analysis in RELION-4.0. Biochem. J. 478, 4169–4185 (2021).
pubmed: 34783343
doi: 10.1042/BCJ20210708
Zheng, S. Q. et al. MotionCor2: anisotropic correction of beam-induced motion for improved cryo-electron microscopy. Nat. Methods 14, 331–332 (2017).
pubmed: 28250466
pmcid: 5494038
doi: 10.1038/nmeth.4193
Bepler, T. et al. Positive-unlabeled convolutional neural networks for particle picking in cryo-electron micrographs. Nat. Methods 16, 1153–1160 (2019).
pubmed: 31591578
pmcid: 6858545
doi: 10.1038/s41592-019-0575-8
Punjani, A. & Fleet, D. J. 3D variability analysis: Resolving continuous flexibility and discrete heterogeneity from single particle cryo-EM. J. Struct. Biol. 213, 107702 (2021).
pubmed: 33582281
doi: 10.1016/j.jsb.2021.107702
Rohou, A. & Grigorieff, N. CTFFIND4: Fast and accurate defocus estimation from electron micrographs. J. Struct. Biol. 192, 216–221 (2015).
pubmed: 26278980
pmcid: 6760662
doi: 10.1016/j.jsb.2015.08.008
Wagner, T. et al. SPHIRE-crYOLO is a fast and accurate fully automated particle picker for cryo-EM. Commun. Biol. 2, 218 (2019).
pubmed: 31240256
pmcid: 6584505
doi: 10.1038/s42003-019-0437-z
Ramlaul, K., Palmer, C. M., Nakane, T. & Aylett, C. H. S. Mitigating local over-fitting during single particle reconstruction with SIDESPLITTER. J. Struct. Biol. 211, 107545 (2020).
pubmed: 32534144
pmcid: 7369633
doi: 10.1016/j.jsb.2020.107545
Pettersen, E. F. et al. UCSF Chimera–a visualization system for exploratory research and analysis. J. Comput. Chem. 25, 1605–1612 (2004).
pubmed: 15264254
doi: 10.1002/jcc.20084
Adams, P. D. et al. PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr. 66, 213–221 (2010).
pubmed: 20124702
pmcid: 2815670
doi: 10.1107/S0907444909052925
Emsley, P. & Cowtan, K. Coot: model-building tools for molecular graphics. Acta Crystallogr. D Biol. Crystallogr. 60, 2126–2132 (2004).
pubmed: 15572765
doi: 10.1107/S0907444904019158
Grubbs, F. E. Procedures for detecting outlying observations in samples. Technometrics 11, 1–21 (1969).
doi: 10.1080/00401706.1969.10490657
Madeira, F. et al. Search and sequence analysis tools services from EMBL-EBI in 2022. Nucleic Acids Res. 50, W276–W279 (2022).
pubmed: 35412617
pmcid: 9252731
doi: 10.1093/nar/gkac240
Crooks, G. E., Hon, G., Chandonia, J. M. & Brenner, S. E. WebLogo: a sequence logo generator. Genome Res. 14, 1188–1190 (2004).
pubmed: 15173120
pmcid: 419797
doi: 10.1101/gr.849004
The PyMOL Molecular Graphics System, Version 2.5 Schrödinger, LLC., https://www.pymol.org/ .
Ballesteros, J. A. & Weinstein, H. in Methods in Neurosciences Vol. 25 (ed Stuart C. Sealfon) 366–428 (Academic Press, 1995).