Modulating signalling lifetime to optimise a prototypical animal opsin for optogenetic applications.

Arrestin Deactivation G-protein GPCR Kinetics Opsin Optogenetics Rhodopsin

Journal

Pflugers Archiv : European journal of physiology
ISSN: 1432-2013
Titre abrégé: Pflugers Arch
Pays: Germany
ID NLM: 0154720

Informations de publication

Date de publication:
01 Dec 2023
Historique:
received: 09 06 2023
accepted: 02 11 2023
revised: 01 11 2023
medline: 1 12 2023
pubmed: 1 12 2023
entrez: 30 11 2023
Statut: aheadofprint

Résumé

Animal opsins are light activated G-protein-coupled receptors, capable of optogenetic control of G-protein signalling for research or therapeutic applications. Animal opsins offer excellent photosensitivity, but their temporal resolution can be limited by long photoresponse duration when expressed outside their native cellular environment. Here, we explore methods for addressing this limitation for a prototypical animal opsin (human rod opsin) in HEK293T cells. We find that the application of the canonical rhodopsin kinase (GRK1)/visual arrestin signal termination mechanism to this problem is complicated by a generalised suppressive effect of GRK1 expression. This attenuation can be overcome using phosphorylation-independent mutants of arrestin, especially when these are tethered to the opsin protein. We further show that point mutations targeting the Schiff base stability of the opsin can also reduce signalling lifetime. Finally, we apply one such mutation (E122Q) to improve the temporal fidelity of restored visual responses following ectopic opsin expression in the inner retina of a mouse model of retinal degeneration (rd1). Our results reveal that these two strategies (targeting either arrestin binding or Schiff-base hydrolysis) can produce more time-delimited opsin signalling under heterologous expression and establish the potential of this approach to improve optogenetic performance.

Identifiants

pubmed: 38036775
doi: 10.1007/s00424-023-02879-9
pii: 10.1007/s00424-023-02879-9
doi:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : Human Frontiers Science Program
ID : RGP0034/2014

Informations de copyright

© 2023. The Author(s).

Références

Airan RD, Thompson KR, Fenno LE, Bernstein H, Deisseroth K (2009) Temporally precise in vivo control of intracellular signalling. Nature 458:1025–1029. https://doi.org/10.1038/nature07926
Bailes HJ, Lucas RJ (2013) Human melanopsin forms a pigment maximally sensitive to blue light ( λ
doi: 10.1098/rspb.2012.2987 pubmed: 23554393 pmcid: 3619500
Bailes HJ, Zhuang L-Y, Lucas RJ (2012) Reproducible and sustained regulation of gαs signalling using a metazoan opsin as an optogenetic tool. Plos One 7:e30774. https://doi.org/10.1371/journal.pone.0030774
doi: 10.1371/journal.pone.0030774 pubmed: 22292038 pmcid: 3265508
Baker CK, Flannery JG (2018) Innovative optogenetic strategies for vision restoration. Frontiers in Cellular Neuroscience 12:316. https://doi.org/10.3389/fncel.2018.00316
Ballister ER, Rodgers J, Martial F, Lucas RJ (2018) A live cell assay of GPCR coupling allows identification of optogenetic tools for controlling Go and Gi signaling. BMC Biol 16:10. https://doi.org/10.1186/s12915-017-0475-2
doi: 10.1186/s12915-017-0475-2 pubmed: 29338718 pmcid: 5771134
Bartl FJ, Ritter E, Hofmann KP (2001) Signaling states of rhodopsin. J Biol Chem 276:30161–30166. https://doi.org/10.1074/jbc.M101506200
doi: 10.1074/jbc.M101506200 pubmed: 11384968
Benovic JL, Kühn H, Weyand I, Codina J, Caron MG, Lefkowitz RJ (1987) Functional desensitization of the isolated beta-adrenergic receptor by the beta-adrenergic receptor kinase: potential role of an analog of the retinal protein arrestin (48-kDa protein). Proc Natl Acad Sci 84:8879–8882. https://doi.org/10.1073/pnas.84.24.8879
doi: 10.1073/pnas.84.24.8879 pubmed: 2827157 pmcid: 299654
Benovic JL, Mayor F, Somers RL, Caron MG, Lefkowitz RJ (1986) Light-dependent phosphorylation of rhodopsin by β-adrenergic receptor kinase. Nature 321:869–872. https://doi.org/10.1038/321869a0
doi: 10.1038/321869a0 pubmed: 3014340
Berry MH, Holt A, Salari A, Veit J, Visel M, Levitz J, Aghi K, Gaub BM, Sivyer B, Flannery JG, Isacoff EY (2019) Restoration of high-sensitivity and adapting vision with a cone opsin. Nat Commun 10:1221.  https://doi.org/10.1038/s41467-019-09124-x
Castiglione GM, Schott RK, Hauser FE, Chang BSW (2018) Convergent selection pressures drive the evolution of rhodopsin kinetics at high altitudes via nonparallel mechanisms: CONVERGENCE IN HIGH-ALTITUDE RHODOPSINS. Evolution 72:170–186. https://doi.org/10.1111/evo.13396
doi: 10.1111/evo.13396 pubmed: 29143302
Cehajic-Kapetanovic J, Eleftheriou C, Allen AE, Milosavljevic N, Pienaar A, Bedford R, Davis KE, Bishop PN, Lucas RJ (2015) Restoration of vision with ectopic expression of human rod opsin. Curr Biol 25:2111–2122. https://doi.org/10.1016/j.cub.2015.07.029
doi: 10.1016/j.cub.2015.07.029 pubmed: 26234216 pmcid: 4540256
Chang B, Hawes NL, Hurd RE, Davisson MT, Nusinowitz S, Heckenlively JR (2002) Retinal degeneration mutants in the mouse. Vision Res 42:517–525. https://doi.org/10.1016/S0042-6989(01)00146-8
doi: 10.1016/S0042-6989(01)00146-8 pubmed: 11853768
Chaudhury D, Walsh JJ, Friedman AK, Juarez B, Ku SM, Koo JW, Ferguson D, Tsai H-C, Pomeranz L, Christoffel DJ, Nectow AR, Ekstrand M, Domingos A, Mazei-Robison MS, Mouzon E, Lobo MK, Neve RL, Friedman JM, Russo SJ, Deisseroth K, Nestler EJ, Han M-H (2013) Rapid regulation of depression-related behaviours by control of midbrain dopamine neurons. Nature 493:532–536. https://doi.org/10.1038/nature11713
doi: 10.1038/nature11713 pubmed: 23235832
Chen C-K, Burns ME, Spencer M, Niemi GA, Chen J, Hurley JB, Baylor DA, Simon MI (1999) Abnormal photoresponses and light-induced apoptosis in rods lacking rhodopsin kinase. Proc Natl Acad Sci USA 96:3718–3722. https://doi.org/10.1073/pnas.96.7.3718
doi: 10.1073/pnas.96.7.3718 pubmed: 10097103 pmcid: 22360
Chen W, Li C, Liang W, Li Y, Zou Z, Xie Y, Liao Y, Yu L, Lin Q, Huang M, Li Z, Zhu X (2022) The roles of optogenetics and technology in neurobiology: a review. Front Aging Neurosci 14:867863.  https://doi.org/10.3389/fnagi.2022.867863
Chen X, Zaro JL, Shen W-C (2013) Fusion protein linkers: property, design and functionality. Adv Drug Deliv Rev 65:1357–1369. https://doi.org/10.1016/j.addr.2012.09.039
doi: 10.1016/j.addr.2012.09.039 pubmed: 23026637
Cheng MY, Wang EH, Woodson WJ, Wang S, Sun G, Lee AG, Arac A, Fenno LE, Deisseroth K, Steinberg GK (2014) Optogenetic neuronal stimulation promotes functional recovery after stroke. Proc Natl Acad Sci 111:12913–12918. https://doi.org/10.1073/pnas.1404109111
doi: 10.1073/pnas.1404109111 pubmed: 25136109 pmcid: 4156770
Copits BA, Gowrishankar R, O’Neill PR, Li J-N, Girven KS, Yoo JJ, Meshik X, Parker KE, Spangler SM, Elerding AJ, Brown BJ, Shirley SE, Ma KKL, Vasquez AM, Stander MC, Kalyanaraman V, Vogt SK, Samineni VK, Patriarchi T, Tian L, Gautam N, Sunahara RK, Gereau RW, Bruchas MR (2021) A photoswitchable GPCR-based opsin for presynaptic inhibition. Neuron 109:1791-1809.e11. https://doi.org/10.1016/j.neuron.2021.04.026
doi: 10.1016/j.neuron.2021.04.026 pubmed: 33979635 pmcid: 8194251
Deisseroth K (2015) Optogenetics: 10 years of microbial opsins in neuroscience. Nat Neurosci 18:1213–1225. https://doi.org/10.1038/nn.4091
doi: 10.1038/nn.4091 pubmed: 26308982 pmcid: 4790845
Doroudchi MM, Greenberg KP, Liu J, Silka KA, Boyden ES, Lockridge JA, Arman AC, Janani R, Boye SE, Boye SL, Gordon GM, Matteo BC, Sampath AP, Hauswirth WW, Horsager A (2011) Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness. Mol Ther 19:1220–1229. https://doi.org/10.1038/mt.2011.69
doi: 10.1038/mt.2011.69 pubmed: 21505421 pmcid: 3129568
Eickelbeck D, Rudack T, Tennigkeit SA, Surdin T, Karapinar R, Schwitalla J, Mücher B, Shulman M, Scherlo M, Althoff P, Mark MD, Gerwert K, Herlitze S (2020) Lamprey Parapinopsin (“UVLamP”): a Bistable UV-sensitive optogenetic switch for ultrafast control of GPCR pathways. ChemBioChem 21:612–617. https://doi.org/10.1002/cbic.201900485
doi: 10.1002/cbic.201900485 pubmed: 31468691
Farrow K, Masland RH (2011) Physiological clustering of visual channels in the mouse retina. J Neurophysiol 105:1516–1530. https://doi.org/10.1152/jn.00331.2010
doi: 10.1152/jn.00331.2010 pubmed: 21273316 pmcid: 3075295
Gaub BM, Berry MH, Holt AE, Isacoff EY, Flannery JG (2015) Optogenetic vision restoration using rhodopsin for enhanced sensitivity. Mol Ther 23:1562–1571. https://doi.org/10.1038/mt.2015.121
doi: 10.1038/mt.2015.121 pubmed: 26137852 pmcid: 4817926
Gilhooley MJ, Lindner M, Palumaa T, Hughes S, Peirson SN, Hankins MW (2022) A systematic comparison of optogenetic approaches to visual restoration. Mol Ther - Methods Clin Dev 25:111–123. https://doi.org/10.1016/j.omtm.2022.03.003
doi: 10.1016/j.omtm.2022.03.003 pubmed: 35402632 pmcid: 8956963
Goncalves JA, South K, Ahuja S, Zaitseva E, Opefi CA, Eilers M, Vogel R, Reeves PJ, Smith SO (2010) Highly conserved tyrosine stabilizes the active state of rhodopsin. Proc Natl Acad Sci 107:19861–19866. https://doi.org/10.1073/pnas.1009405107
doi: 10.1073/pnas.1009405107 pubmed: 21041664 pmcid: 2993422
Govorunova EG, Sineshchekov OA, Li H, Spudich JL (2017) Microbial rhodopsins: diversity, mechanisms, and optogenetic applications. Annu Rev Biochem 86:845–872. https://doi.org/10.1146/annurev-biochem-101910-144233
doi: 10.1146/annurev-biochem-101910-144233 pubmed: 28301742 pmcid: 5747503
Gurevich VV, Gurevich EV (2010) Custom-designed proteins as novel therapeutic tools? The case of arrestins. Expert Rev Mol Med 12:e13. https://doi.org/10.1017/S1462399410001444
doi: 10.1017/S1462399410001444 pubmed: 20412604 pmcid: 2933791
Gurevich VV, Gurevich EV (2019) GPCR signaling regulation: the role of GRKs and arrestins. Front Pharmacol 10:125.  https://doi.org/10.3389/fphar.2019.00125
Heck M, Schädel SA, Maretzki D, Bartl FJ, Ritter E, Palczewski K, Hofmann KP (2003) Signaling states of rhodopsin. J Biol Chem 278:3162–3169. https://doi.org/10.1074/jbc.M209675200
doi: 10.1074/jbc.M209675200 pubmed: 12427735
Hickey DG, Davies WIL, Hughes S, Rodgers J, Thavanesan N, MacLaren RE, Hankins MW (2021) Chimeric human opsins as optogenetic light sensitisers. J Exp Biol 224:jeb240580.  https://doi.org/10.1242/jeb.240580
Imai H, Kefalov V, Sakurai K, Chisaka O, Ueda Y, Onishi A, Morizumi T, Fu Y, Ichikawa K, Nakatani K, Honda Y, Chen J, Yau K-W, Shichida Y (2007) Molecular properties of rhodopsin and rod function. J Biol Chem 282:6677–6684. https://doi.org/10.1074/jbc.M610086200
doi: 10.1074/jbc.M610086200 pubmed: 17194706
Kawano-Yamashita E, Koyanagi M, Wada S, Tsukamoto H, Nagata T, Terakita A (2015) Activation of transducin by bistable pigment parapinopsin in the pineal organ of lower vertebrates. PLoS ONE 10:e0141280. https://doi.org/10.1371/journal.pone.0141280
doi: 10.1371/journal.pone.0141280 pubmed: 26492337 pmcid: 4619617
Kim JH, Lee S-R, Li L-H, Park H-J, Park J-H, Lee KY, Kim M-K, Shin BA, Choi S-Y (2011) High cleavage efficiency of a 2A peptide derived from porcine teschovirus-1 in human cell lines, zebrafish and mice. Plos One 6:e18556. https://doi.org/10.1371/journal.pone.0018556
doi: 10.1371/journal.pone.0018556 pubmed: 21602908 pmcid: 3084703
Koyanagi M, Terakita A (2014) Diversity of animal opsin-based pigments and their optogenetic potential. Biochim Biophys Acta (BBA) Bioenerg 1837:710–716. https://doi.org/10.1016/j.bbabio.2013.09.003
doi: 10.1016/j.bbabio.2013.09.003
Kralik J, van Wyk M, Stocker N, Kleinlogel S (2022) Bipolar cell targeted optogenetic gene therapy restores parallel retinal signaling and high-level vision in the degenerated retina. Commun Biol 5:1116.  https://doi.org/10.1038/s42003-022-04016-1
Krasel C, Bünemann M, Lorenz K, Lohse MJ (2005) β-Arrestin binding to the β2-adrenergic receptor requires both receptor phosphorylation and receptor activation *. J Biol Chem 280:9528–9535. https://doi.org/10.1074/jbc.M413078200
doi: 10.1074/jbc.M413078200 pubmed: 15634674
Kühn H, Wilden U (1987) Deactivation of Photoactivated rhodopsin by rhodopsin-kinase and arrestin. Journal of Receptor Research 7:283–298. https://doi.org/10.3109/10799898709054990
doi: 10.3109/10799898709054990 pubmed: 3040978
Kuwayama S, Imai H, Hirano T, Terakita A, Shichida Y (2002) Conserved Proline residue at position 189 in cone visual pigments as a determinant of molecular properties different from rhodopsins. Biochemistry 41:15245–15252. https://doi.org/10.1021/bi026444k
doi: 10.1021/bi026444k pubmed: 12484762
Lagali PS, Balya D, Awatramani GB, Münch TA, Kim DS, Busskamp V, Cepko CL, Roska B (2008) Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration. Nat Neurosci 11:667–675. https://doi.org/10.1038/nn.2117
doi: 10.1038/nn.2117 pubmed: 18432197
Leemann S, Kleinlogel S (2023) Functional optimization of light-activatable Opto-GPCRs: Illuminating the importance of the proximal C-terminus in G-protein specificity. Front Cell Dev Biol 11:1053022.  https://doi.org/10.3389/fcell.2023.1053022
Li G, Huang Z, Zhang C, Dong B-J, Guo R-H, Yue H-W, Yan L-T, Xing X-H (2016) Construction of a linker library with widely controllable flexibility for fusion protein design. Appl Microbiol Biotechnol 100:215–225. https://doi.org/10.1007/s00253-015-6985-3
doi: 10.1007/s00253-015-6985-3 pubmed: 26394862
Macé E, Caplette R, Marre O, Sengupta A, Chaffiol A, Barbe P, Desrosiers M, Bamberg E, Sahel J-A, Picaud S, Duebel J, Dalkara D (2015) Targeting channelrhodopsin-2 to ON-bipolar cells with vitreally administered AAV restores ON and OFF visual responses in blind mice. Mol Ther 23:7–16. https://doi.org/10.1038/mt.2014.154
doi: 10.1038/mt.2014.154 pubmed: 25095892
Masseck OA, Spoida K, Dalkara D, Maejima T, Rubelowski JM, Wallhorn L, Deneris ES, Herlitze S (2014) Vertebrate cone opsins enable sustained and highly sensitive rapid control of G i/o signaling in anxiety circuitry. Neuron 81:1263–1273. https://doi.org/10.1016/j.neuron.2014.01.041
doi: 10.1016/j.neuron.2014.01.041 pubmed: 24656249
Masuho I, Martemyanov KA, Lambert NA (2015) Monitoring G protein activation in cells with BRET. In: Filizola M (ed) G Protein-Coupled Receptors in Drug Discovery. Springer, New York, New York, NY, pp 107–113
doi: 10.1007/978-1-4939-2914-6_8
Masuho I, Ostrovskaya O, Kramer GM, Jones CD, Xie K, Martemyanov KA (2015) Distinct profiles of functional discrimination among G proteins determine the actions of G protein–coupled receptors. Sci Signal 8:ra123.  https://doi.org/10.1126/scisignal.aab4068
Morgans CW, Zhang J, Jeffrey BG, Nelson SM, Burke NS, Duvoisin RM, Brown RL (2009) TRPM1 is required for the depolarizing light response in retinal ON-bipolar cells. Proc Natl Acad Sci USA 106:19174–19178. https://doi.org/10.1073/pnas.0908711106
doi: 10.1073/pnas.0908711106 pubmed: 19861548 pmcid: 2776419
Morri M, Sanchez-Romero I, Tichy A-M, Kainrath S, Gerrard EJ, Hirschfeld PP, Schwarz J, Janovjak H (2018) Optical functionalization of human Class A orphan G-protein-coupled receptors. Nat Commun 9:1950. https://doi.org/10.1038/s41467-018-04342-1
doi: 10.1038/s41467-018-04342-1 pubmed: 29769519 pmcid: 5956105
Petrs-Silva H, Dinculescu A, Li Q, Deng W-T, Pang J, Min S-H, Chiodo V, Neeley AW, Govindasamy L, Bennett A, Agbandje-McKenna M, Zhong L, Li B, Jayandharan GR, Srivastava A, Lewin AS, Hauswirth WW (2011) Novel properties of tyrosine-mutant AAV2 vectors in the mouse retina. Mol Ther 19:293–301. https://doi.org/10.1038/mt.2010.234
doi: 10.1038/mt.2010.234 pubmed: 21045809
Pittler SJ, Baehr W (1991) Identification of a nonsense mutation in the rod photoreceptor cGMP phosphodiesterase beta-subunit gene of the rd mouse. Proc Natl Acad Sci 88:8322–8326. https://doi.org/10.1073/pnas.88.19.8322
doi: 10.1073/pnas.88.19.8322 pubmed: 1656438 pmcid: 52500
Pugh EN, Lamb TD (2000) Chapter 5 Phototransduction in vertebrate rods and cones: Molecular mechanisms of amplification, recovery and light adaptation. In: Stavenga DG, DeGrip WJ, Pugh EN (eds) Handbook of Biological Physics (vol 3). Elsevier, Amsterdam pp 183–255
Rodgers J, Bano-Otalora B, Belle MDC, Paul S, Hughes R, Wright P, McDowell R, Milosavljevic N, Orlowska-Feuer P, Martial FP, Wynne J, Ballister ER, Storchi R, Allen AE, Brown T, Lucas RJ (2021) Using a bistable animal opsin for switchable and scalable optogenetic inhibition of neurons. EMBO Reports 22:e51866
doi: 10.15252/embr.202051866 pubmed: 33655694 pmcid: 8097317
Rost BR, Schneider-Warme F, Schmitz D, Hegemann P (2017) Optogenetic tools for subcellular applications in neuroscience. Neuron 96:572–603. https://doi.org/10.1016/j.neuron.2017.09.047
doi: 10.1016/j.neuron.2017.09.047 pubmed: 29096074
Sahel J-A, Boulanger-Scemama E, Pagot C, Arleo A, Galluppi F, Martel JN, Esposti SD, Delaux A, de Saint Aubert J-B, de Montleau C, Gutman E, Audo I, Duebel J, Picaud S, Dalkara D, Blouin L, Taiel M, Roska B (2021) Partial recovery of visual function in a blind patient after optogenetic therapy. Nat Med 27:1223–1229. https://doi.org/10.1038/s41591-021-01351-4
doi: 10.1038/s41591-021-01351-4 pubmed: 34031601
Sakai K, Shichida Y, Imamoto Y, Yamashita T (2022) Creation of photocyclic vertebrate rhodopsin by single amino acid substitution. eLife 11:e75979. https://doi.org/10.7554/eLife.75979
doi: 10.7554/eLife.75979 pubmed: 35199641 pmcid: 8871353
Samaranayake S, Song X, Vishnivetskiy SA, Chen J, Gurevich EV, Gurevich VV (2018) Enhanced mutant compensates for defects in rhodopsin phosphorylation in the presence of endogenous arrestin-1. Front Mol Neurosci 11:203.  https://doi.org/10.3389/fnmol.2018.00203
Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675. https://doi.org/10.1038/nmeth.2089
doi: 10.1038/nmeth.2089 pubmed: 22930834 pmcid: 5554542
Shi G, Yau K-W, Chen J, Kefalov VJ (2007) Signaling properties of a short-wave cone visual pigment and its role in phototransduction. J Neurosci 27:10084–10093. https://doi.org/10.1523/JNEUROSCI.2211-07.2007
doi: 10.1523/JNEUROSCI.2211-07.2007 pubmed: 17881515 pmcid: 6672674
Sivaramakrishnan S, Spudich JA (2011) Systematic control of protein interaction using a modular ER/K α-helix linker. Proc Natl Acad Sci 108:20467–20472. https://doi.org/10.1073/pnas.1116066108
doi: 10.1073/pnas.1116066108 pubmed: 22123984 pmcid: 3251109
Song X, Seo J, Baameur F, Vishnivetskiy SA, Chen Q, Kook S, Kim M, Brooks EK, Altenbach C, Hong Y, Hanson SM, Palazzo MC, Chen J, Hubbell WL, Gurevich EV, Gurevich VV (2013) Rapid degeneration of rod photoreceptors expressing self-association-deficient arrestin-1 mutant. Cell Signal 25:2613–2624. https://doi.org/10.1016/j.cellsig.2013.08.022
doi: 10.1016/j.cellsig.2013.08.022 pubmed: 24012956
Soper C, Wicker E, Kulick CV, N’Gouemo P, Forcelli PA (2016) Optogenetic activation of superior colliculus neurons suppresses seizures originating in diverse brain networks. Neurobiol Dis 87:102–115. https://doi.org/10.1016/j.nbd.2015.12.012
doi: 10.1016/j.nbd.2015.12.012 pubmed: 26721319
Stefanik MT, Moussawi K, Kupchik YM, Smith KC, Miller RL, Huff ML, Deisseroth K, Kalivas PW, LaLumiere RT (2013) Optogenetic inhibition of cocaine seeking in rats. Addict Biol 18:50–53. https://doi.org/10.1111/j.1369-1600.2012.00479.x
doi: 10.1111/j.1369-1600.2012.00479.x pubmed: 22823160
Violin JD, DeWire SM, Barnes WG, Lefkowitz RJ (2006) G protein-coupled receptor kinase and β-arrestin-mediated desensitization of the angiotensin ii type 1A receptor elucidated by diacylglycerol dynamics *. J Biol Chem 281:36411–36419. https://doi.org/10.1074/jbc.M607956200
doi: 10.1074/jbc.M607956200 pubmed: 17008309
Violin JD, DiPilato LM, Yildirim N, Elston TC, Zhang J, Lefkowitz RJ (2008) beta2-adrenergic receptor signaling and desensitization elucidated by quantitative modeling of real time cAMP dynamics. J Biol Chem 283:2949–2961. https://doi.org/10.1074/jbc.M707009200
doi: 10.1074/jbc.M707009200 pubmed: 18045878
Vishnivetskiy SA, Chen Q, Palazzo MC, Brooks EK, Altenbach C, Iverson TM, Hubbell WL, Gurevich VV (2013) Engineering visual arrestin-1 with special functional characteristics. J Biol Chem 288:3394–3405. https://doi.org/10.1074/jbc.M112.445437
doi: 10.1074/jbc.M112.445437 pubmed: 23250748
Vogel R, Siebert F, Mathias G, Tavan P, Fan G, Sheves M (2003) Deactivation of rhodopsin in the transition from the signaling state meta II to meta III involves a thermal isomerization of the retinal chromophore CN double bond. Biochemistry 42:9863–9874. https://doi.org/10.1021/bi034684+
doi: 10.1021/bi034684+ pubmed: 12924935
Wagdi A, Malan D, Sathyanarayanan U, Beauchamp JS, Vogt M, Zipf D, Beiert T, Mansuroglu B, Dusend V, Meininghaus M, Schneider L, Kalthof B, Wiegert JS, König GM, Kostenis E, Patejdl R, Sasse P, Bruegmann T (2022) Selective optogenetic control of Gq signaling using human Neuropsin. Nat Commun 13:1765. https://doi.org/10.1038/s41467-022-29265-w
doi: 10.1038/s41467-022-29265-w pubmed: 35365606 pmcid: 8975936
Wichert S, Fokianos K, Strimmer K (2004) Identifying periodically expressed transcripts in microarray time series data. Bioinformatics 20:5–20. https://doi.org/10.1093/bioinformatics/btg364
doi: 10.1093/bioinformatics/btg364 pubmed: 14693803
Wilden U, Kuehn H (1982) Light-dependent phosphorylation of rhodopsin: number of phosphorylation sites. Biochemistry 21:3014–3022. https://doi.org/10.1021/bi00541a032
doi: 10.1021/bi00541a032 pubmed: 6980670
van Wyk M, Kleinlogel S (2023) A visual opsin from jellyfish enables precise temporal control of G protein signalling. Nature Communications 14:2450.  https://doi.org/10.1038/s41467-023-38231-z
Yamashita T, Terakita A, Shichida Y (2000) Distinct roles of the second and third cytoplasmic loops of bovine rhodopsin in G protein activation. J Biol Chem 275:34272–34279. https://doi.org/10.1074/jbc.M002954200
doi: 10.1074/jbc.M002954200 pubmed: 10930404
Ye H, Baba MD-E, Peng R-W, Fussenegger M (2011) A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science 332:1565–1568. https://doi.org/10.1126/science.1203535
doi: 10.1126/science.1203535 pubmed: 21700876

Auteurs

Jessica Rodgers (J)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK. jessica.rodgers@manchester.ac.uk.

Phillip Wright (P)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK.

Edward R Ballister (ER)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK.
Department of Biomedical Engineering, Columbia University, New York, NY, 10027, USA.
Department of Microbiology and Immunology, Vagelos College of Physicians and Surgeons of Columbia University, New York, 10032, NY, USA.

Rebecca B Hughes (RB)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK.

Riccardo Storchi (R)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK.

Jonathan Wynne (J)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK.

Franck P Martial (FP)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK.

Robert J Lucas (RJ)

Centre for Biological Timing, Division of Neuroscience, Faculty of Biology, Medicine and Health, University of Manchester, Manchester, M13 9PT, UK. robert.lucas@manchester.ac.uk.

Classifications MeSH