Opsins and their testing in heterological expression systems

Мұқаба

Дәйексөз келтіру

Толық мәтін

Аннотация

The study of photosensitive proteins as optogenetic tools for the therapeutic restoration of visual functions in heterologous expression systems is a necessary step prior to their optogenetic prosthetization in the retina. The review considers the features of opsins and factors affecting their activity in model cell systems. Particular attention is paid to G-protein-coupled opsins as promising tools for recreating the signaling cascade mechanisms of in retinal ON-bipolar cells. Based on the analysis of light-controlled responses of natural and chemical light-sensitive proteins in tests, the selection of the best, promising in gene therapy is made.

Толық мәтін

Рұқсат жабық

Авторлар туралы

Y. Chiligina

Sechenov Institute of Evolutionary Physiology and Biochemistry, Russian Academy of Sciences

Хат алмасуға жауапты Автор.
Email: julchil@mail.ru
Ресей, St. Petersburg

Әдебиет тізімі

  1. Долгих Д.А., Малышев А.Ю., Саложин С.В. Анионный канальный родопсин, экспрессированный в культуре нейронов и in vivo в мозге мыши: светоиндуцированное подавление генерации потенциалов действия // ДАН. 2015. Т. 465 (6). С. 737–740.
  2. Карпушев А.В., Чилигина Ю.А. Электрофизиологическое тестирование активации G-белок-зависимого сигнального каскада светочувствительными химерными рецепторами // Мат. III Всерос. науч. конф. с междунар. уч. “Оптогенетика+ 2023” (СПб., 6–8 апреля 2023 г.). СПб.: ИЭФБ, 2023. С. 48–49.
  3. Кирпичников М.П., Островский М.А. Оптогенетика и зрение // Вестн. РАН. 2019. Т. 89 (2). С. 125–30.
  4. Колесов Д.В., Соколинская Е.Л., Лукьянов К.А., Богданов А.М. Молекулярные инструменты направленного контроля электрической активности нервных клеток. Ч. I // Acta Naturae. 2021. Т. 13 (3). С. 52–64.
  5. Островский М.А. Молекулярная физиология зрительного пигмента родопсина: актуальные направления // Рос. физиол. журн. им. И.М. Сеченова. 2020. Т. 106 (4). С. 401–420.
  6. Петровская Л.Е., Рощин М.В., Смирнова Г.Р. и др. Бицистронная генетическая конструкция для оптогенетического протезирования рецептивного поля ганглиозной клетки дегенеративной сетчатки // ДАН. 2019. Т. 486. С. 258–261.
  7. Airan R.D., Thompson K.R., Fenno L.E. et al. Temporally precise in vivo control of intracellular signaling // Lett. Nat. 2009. V. 458. P. 1025–1029.
  8. Arshavsky V., Burns M. Current understanding of signal amplification in phototransduction // Cell. Logist. 2014. V. 4 (2). P. e28680. https://doi.org/10.4161/cl.29390
  9. Bailes H., Lucas R. Human melanopsin forms a pigment maximally sensitive to blue light (λmax ≈ 479 nm) supporting activation of Gq/11 and Gi/o signalling cascades // Proc. Biol. Sci. 2013. V. 280. P. 20122987. http://doi.org/10.1098/rspb.2012.2987
  10. Baker C., Flannery J. Innovative optogenetic strategies for vision restoration // Front. Cell. Neurosci. 2018. V. 12. P. 316. https://doi.org/10.3389/fncel.2018.00316
  11. Ballister E.R., Rodgers J., Martial F., Lucas R.J. A live cell assay of GPCR coupling allows identification of optogenetic tools for controlling Go and Gi signaling // BMC Biol. 2018. V. 16. P. 10. https://doi.org/10.1186/s12915-017-0475-2
  12. Berry M.H., Holt A., Salari A. et al. Restoration of high-sensitivity and adapting vision with a cone opsin // Nat. Com. 2019. V. 10. P. 1221. https://doi.org/10.1038/s41467-019-09124-x
  13. Bi A., Cui J., Ma Yu-P. et al. Ectopic expression of a microbial-type rhodopsin restores visual responses in mice with photoreceptor degeneration // Neuron. 2006. V. 50. P. 23–33. https://doi.org/10.1016/j.neuron.2006.02.026
  14. Bird A.C. Clinical investigation of retinitis pigmentosa // Aust. N. Z. J. Ophthalmol. 1988. V. 16. P. 189–198.
  15. Blasic J.R.Jr., Brown L.R., Robinson Ph.R. Light-dependent phosphorylation of the carboxy tail of mouse melanopsin // Cell. Mol. Life Sci. 2012. V. 69 (9). P. 1551–1562. https://doi.org/10.1007/s00018-011-0891-3
  16. Boyden E., Zhang F., Bamberg E. et al. Millisecond-timescale, genetically targeted optical control of neural activity // Nat. Neurosci. 2005. V. 8. P. 1263–1268. http://dx.doi.org/10.1038/nn1525
  17. Bünemann M., Bucheler M.M., Philipp M. et al. Activation and deactivation kinetics of alpha 2A- and alpha 2C-adrenergic receptor-activated G protein-activated inwardly rectifying K+ channel currents // J. Biol. Chem. 2001. V. 276. P. 47512–47517. https://doi.org/10.1074/jbc.m108652200
  18. Cehajic-Kapetanovic J., Eleftheriou C., Allen A.E. et al. Restoration of vision with ectopic expression of human rod opsin // Curr. Biol. 2015. V. 25. P. 2111–2122. https://doi.org/10.1016%2Fj.cub.2015.07.029
  19. Covington H.E., Lobo M.K., Maze I. et al. Antidepressant effect of optogenetic stimulation of the medial prefrontal cortex // J. Neurosci. 2010. V. 30 (48). P. 16082–16090. https://doi.org/10.1523%2FJNEUROSCI.1731-10.2010
  20. Deisseroth K., Feng G., Majewska A. et al. Next-generation optical technologies for illuminating genetically targeted brain circuits // J. Neurosci. 2006. V. 26 (41). P. 10380–10386. https://doi.org/10.1523/jneurosci.3863-06.2006
  21. Deisseroth K. Optogenetics // Nat. Methods. 2011. V. 8 (1). P. 26–29. https://doi.org/10.1038/nmeth.f.324
  22. Deisseroth K. Optogenetics: 10 years of microbial opsins in neuroscience // Nat. Neurosci. 2015. V. 8 (9). P. 1213–1225. https://doi.org/10.1038/nn.4091
  23. Dhingra A., Vardi N. “mGlu receptors in the retina” — WIREs membrane transport and signaling // Wiley Interdiscip. Rev. Membr. Transp. Signal. 2012. V. 1 (5). P. 641–653. https://doi.org/10.1002/wmts.43
  24. Doroudchi M., Greenberg K., Liu J. et al. Virally delivered channelrhodopsin-2 safely and effectively restores visual function in multiple mouse models of blindness // Mol. Ther. 2011. V. 19. P. 1220–1229. https://doi.org/10.1038/mt.2011.69
  25. Firsov M.L. Perspective for the optogenetic prosthetization of the retina // Neurosci. Behav. Physi. 2019. V. 49. P. 192–198. https://doi.org/10.1007/s11055-019-00714-2
  26. Flock T., Hauser A., Lund N. et al. Selectivity determinants of GPCR-G-protein binding // Nature. 2017. V. 545 (7654). P. 317–322. https://doi.org/10.1038/nature22070
  27. Ganjawala T.H., Lu Q., Fenner M.D. et al. Improved CoChR variants restore visual acuity and contrast sensitivity in a mouse model of blindness under ambient light conditions // Mol. Ther. 2019. V. 27 (6). P. 1195–1205. https://doi.org/10.1016/j.ymthe.2019.04.002
  28. Gaub B.M., Berry M.H., Holt A.E. et al. Restoration of visual function by expression of a light-gated mammalian ion channel in retinal ganglion cells or ON-bipolar cells // PNAS USA. 2014. V. 111 (51). P. E5574–83.
  29. Govorunova E.G., Sineshchekov O.A., Janz R. et al. Natural light-gated anion channels: a family of microbial rhodopsins for advanced optogenetics // Science. 2015. V. 349 (6248). P. 647–650. https://doi.org/10.1126/science.aaa7484
  30. Graham F.L., Russell W.C., Smiley J. et al. Characteristics of a human cell line transformed by DNA from human adenovirus type 5 // J. Gen. Virol. 1977. V. 36. P. 59–72. https://doi.org/10.1099/0022-1317-36-1-59
  31. Guido M.E., Marchese N.A., Rios M.N. et al. Non-visual opsins and novel photo-detectors in the vertebrate inner retina mediate light responses within the blue spectrum region // Cell. Mol. Neurobiol. 2022. V. 42 (1). P. 59–83. https://doi.org/10.1007/s10571-020-00997-x
  32. Hofmann K.P., Lamb T.D. Rhodopsin, light-sensor of vision // Prog. Retin. Eye Res. 2022. V. 93. P. 101116. http://dx.doi.org/10.1016/j.preteyeres.2022.101116
  33. Hommers L.G., Lohse M.J., Bünemann M. Regulation of the inward rectifying properties of G-protein-activated inwardly rectifying K+ (GIRK) channels by Gβγ subunits // J. Biol. Chem. 2003. V. 278 (2). P. 1037–1043. https://doi.org/10.1074/jbc.m205325200
  34. Kato M., Sugiyama T., Sakai K. et al. Two opsin 3-related proteins in the chicken retina and brain: a TMT-type opsin 3 is a blue-light sensor in retinal horizontal cells, hypothalamus, and cerebellum // PLoS One. 2016. V. 11 (11). P. e0163925. https://doi.org/10.1371%2Fjournal.pone.0163925
  35. Kim J.-M., Hwa J., Garriga P. Light-driven activation of beta 2-adrenergic receptor signaling by a chimeric rhodopsin containing the beta 2-adrenergic receptor cytoplasmic loops // Biochemistry. 2005. V. 44. P. 2284–2292. https://doi.org/10.1021/bi048328i
  36. Kim C.K., Adhikari A., Deisseroth K. Integration of optogenetics with complementary methodologies in systems neuroscience // Nat. Rev. Neurosci. 2017. V. 18 (4). P. 222–235. https://doi.org/10.1038/nrn.2017.15
  37. Kleinlogel S. Optogenetic user’s guide to opto-GPCRs // Front. Biosci. 2016. V. 21. P. 794–805. https://doi.org/10.2741/4421
  38. Koyanagi M., Terakita A. Diversity of animal opsin-based pigments and their optogenetic potential // Biochim. Biophys. Acta. 2014. V. 1837. P. 710–716. http://dx.doi.org/10.1016/j.bbabio.2013.09.003
  39. Kralik J., Wyk M., Stocker N., Kleinlogel S. Bipolar cell targeted optogenetic gene therapy restores parallel retinal signaling and high-level vision in the degenerated retina // Comm. Biol. 2022. V. 5. P. 1116. https://doi.org/10.1038/s42003-022-04016-1
  40. Lagali P., Balya D., Awatramani G. et al. Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration // Nat. Neurosci. 2008. V. 11. P. 667–675. https://doi.org/10.1038/nn.2117
  41. Lamb T.D. Photoreceptor physiology and evolution: cellular and molecular basis of rod and cone phototransduction // J. Physiol. 2022. V. 600 (21). P. 4585–4601.
  42. Law S., Yasuda K., Bell G., Reisine T. Gi alpha 3 and G(o) alpha selectively associate with the cloned somatostatin receptor subtype SSTR2 // J. Biol. Chem. 1993. V. 268. P. 10721–10727.
  43. Lei Q., Jones M.B., Talley E.M. et al. Activation and inhibition of G protein coupled inwardly rectifying potassium (Kir3) channels by G protein βγ subunits // PNAS USA. 2000. V. 97. P. 9771—9776. https://doi.org/10.1073%2Fpnas.97.17.9771
  44. Leemann S., Kleinlogel S. Functional optimization of light-activatable opto-GPCRs: illuminating the importance of the proximal C-terminus in G-protein specificity // Front. Cell Dev. Biol. 2023. V. 11. P. 1053022. https://doi.org/10.3389/fcell.2023.1053022
  45. Levitz J., Pantoja C., Gaub B. et al. Optical control of metabotropic glutamate receptors // Nat. Neurosci. 2013. V. 16. P. 507–516. https://doi.org/10.1038/nn.3346
  46. Lin J.Y., Lin M.Z., Steinbach P., Tsien R.Y. Characterization of engineered channelrhodopsin variants with improved properties and kinetics // Biophys. J. 2009. V. 96 (5). P. 1803–1814. https://doi.org/10.1016%2Fj.bpj.2008.11.034
  47. Lin J.Y. A user’s guide to channelrhodopsin variants: features, limitations and future developments // Exp. Physiol. 2011. V. 96. P. 19–25. https://doi.org/10.1113%2Fexpphysiol.2009.051961
  48. Mathes T. Natural resources for optogenetic tools // Optogenetics / Ed. A. Kianianmomeni. N.Y.: Springer, 2016. P. 19–36.
  49. Masseck O., Spoida K. Dalkara D. et al. Vertebrate cone opsins enable sustained and highly sensitive rapid control of Gi/o signaling in anxiety circuitry // Neuron. 2014. V. 81. P. 1263–1273. https://doi.org/10.1016/j.neuron.2014.01.041
  50. Masuho I., Ostrovskaya O., Kramer G. Distinct profiles of functional discrimination among G proteins determine the actions of G protein-coupled receptors // Sci. Signal. 2015. V. 8 (405). P. ra123. https://doi.org/10.1126/scisignal.aab4068
  51. Milligan G., Kostenis E. Heterotrimeric G-proteins: a short history // Br. J. Pharmacol. 2006. V. 147 (1). P. S46–S55. https://doi.org/10.1038/sj.bjp.0706405
  52. Nagata T., Koyanagi M., Lucas R., Terakita A. An all-trans-retinal-binding opsin peropsin as a potential dark-active and light-inactivated G protein-coupled receptor // Sci. Rep. 2018. V. 8 (3535). P. 1–7. https://doi.org/10.1038/s41598-018-21946-1
  53. Nagel G., Mockel B., Buldt G., Bamberg E. Functional expression of bacteriorhodopsin in oocytes allows direct measurement of voltage dependence of light induced H+ pumping // FEBS Lett. 1995. V. 377. P. 263–266. https://doi.org/10.1016/0014-5793(95)01356-3
  54. Nagel G., Ollig D., Fuhrmann M. et al. Channelrhodopsin-1: a light-gated proton channel in green algae // Science. 2002. V. 296 (5577). P. 2395–2398. https://doi.org/10.1126/science.1072068
  55. Nagel G., Szellas T., Huhn W. et al. Channelrhodopsin-2, a directly light-gated cation-selective membrane channel // PNAS USA. 2003. V. 100 (24). P. 940–945. https://doi.org/10.1073/pnas.1936192100
  56. Neves S.R., Ram P.T., Iyengar R. G-protein pathways // Science. 2002. V. 296 (5573). P. 1636–1639. https://doi.org/10.1126/science.1071550
  57. Oh E., Maejima T., Liu C. et al. Substitution of 5-HT1A receptor signaling by a light-activated G protein-coupled receptor // J. Biol. Chem. 2010. V. 285 (40). P. 30825–30836. https://doi.org/10.1074/jbc.m110.147298
  58. Pugh E.N., Lamb T.D. Phototransduction in vertebrate rods and cones: molecular mechanisms of amplification, recovery and light adaptation. Ch. 5 // Handbook of biological physics / Eds D.G. Stavenga, W.J. DeGrip, E.N. Pugh Jr. North-Holland, 2000. V. 3. P. 183–255.
  59. Riggsbee C.W., Deiters A. Recent advances in the photochemical control of protein function // Trends Biotechnol. 2010. V. 28 (9). P. 468–475. https://doi.org/10.1016/j.tibtech.2010.06.001
  60. Rosenbaum D.M., Rasmussen S.G., Kobilka B.K. The structure and function of G-protein-coupled receptors // Nature. 2009. V. 459 (7245). P. 356–363. https://doi.org/10.1038/nature08144
  61. Rost B.R., Schneider-Warme F., Schmitz D., Hegemann P. Optogenetic tools for subcellular applications in neuroscience // Neuron. 2017. V. 96 (3). P. 572–603. https://doi.org/10.1016/j.neuron.2017.09.047
  62. Sahel J.-A., Boulanger-Scemama E., Pagot Ch. et al. Partial recovery of visual function in a blind patient after optogenetic therapy // Nat. Med. 2021. V. 27. P. 1223–1229. https://doi.org/10.1038/s41591-021-01351-4
  63. Skylar M.S., Bruchas M.R. Optogenetic approaches for dissecting neuromodulation and GPCR signaling in neural circuits // Curr. Opin. Pharmacol. 2017. V. 32. P. 56–70. https://doi.org/10.1016/j.coph.2016.11.001
  64. Spoida K. Melanopsin variants as intrinsic optogenetic on and off switches for transient versus sustained activation of G protein pathways // Curr. Biol. 2016. V. 26. P. 1206–1212. https://doi.org/10.1016/j.cub.2016.03.007
  65. Stenkamp R.E., Filipek S., Driessen C.A. et al. Crystal structure of rhodopsin: a template for cone visual pigments and other G protein-coupled receptors // Biochim. Biophys. Acta. 2002. V. 1565 (2). P. 168–182. https://doi.org/10.1016/S0005-2736(02)00567-9
  66. Terakita A. The opsins // Genome Biol. 2005. V. 6 (3). P. 213. https://doi.org/10.1186/gb-2005-6-3-213
  67. Tian L., Kammermeier P.J. G protein coupling profile of mGluR6 and expression of G alpha proteins in retinal ON bipolar cells // Vis. Neurosci. 2006. V. 23 (6). P. 909–916. https://doi.org/10.1017/s0952523806230268
  68. Thomas P., Smart T.G. HEK293 cell line: a vehicle for the expression of recombinant proteins // J. Pharmacol. Toxicol. Meth. 2005. V. 51. P. 187—200. http://dx.doi.org/10.1016/j.vascn.2004.08.014
  69. Tomita H., Sugano E., Murayama N. et al. Restoration of the majority of the visual spectrum by using modified Volvox channelrhodopsin-1 // Mol. Ther. 2014. V. 22. P. 1434–1440. https://doi.org/10.1038/mt.2014.81
  70. Tye K.M., Deisseroth K. Optogenetic investigation of neural circuits underlying brain disease in animal models // Nat. Rev. Neurosci. 2012. V. 13 (4). P. 251–266. https://doi.org/10.1038/nrn3171
  71. Watanabe Y., Sugano E., Tabata К. et al. Development of an optogenetic gene sensitive to daylight and its implications in vision restoration // Regen. Med. 2021. V. 6 (1). P. 64. https://doi.org/10.1038/s41536-021-00177-5
  72. Wert K., Lin J.H., Tsang S.H. General pathophysiology in retinal degeneration // Dev. Ophtalmol. 2014. V. 53. P. 33–43. https://doi.org/10.1159%2F000357294
  73. Wu K., Kulbay M., Toameh D et al. Retinitis pigmentosa: novel therapeutic targets and drug development // Pharmaceutics. 2023. V. 15 (2). P. 685. https://doi.org/10.3390/pharmaceutics15020685
  74. Wyk M., Kleinlogel S.A. A visual opsin from jellyfish enables precise temporal control of G protein signaling // Nat. Comm. 2023. V. 14 (1). P. 2450. https://doi.org/10.21203/rs.3.rs-1723578/v1
  75. Wyk M., Pielecka-Fortuna J., Löwel S., Kleinlogel S. Restoring the on switch in blind retinas: opto-mGluR6, a next-generation, cell tailored optogenetic tool // PLoS Biol. 2015. V. 13 (5). P. e1002143. https://doi.org/10.1371/journal.pbio.1002143
  76. Xu Y., Orlandi C., Cao Y. et al. The TRPM1 channel in ON-bipolar cells is gated by both the α and the βγ subunits of the G-protein Go // Sci. Rep. 2016. V. 6. P. 20940.
  77. Yizhar O., Fenno L.E., Prigge M. et al. Neocortical excitation/inhibition balance in information processing and social dysfunction // Nature. 2011. V. 477. P. 172–178. https://doi.org/10.1038/nature10360

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2. Fig. 1. Scheme of the phototransduction cascade in the rod. (a) receptor activation in the light. As a result of photon absorption, receptor activation and signal transmission from the activated receptor (rhodopsin) to transducin occur; as a result of a cascade of reactions, non-selective cationic cGMP-dependent channels are closed. (b) receptor deactivation. Rhodopsin returns to the dark state as a result of sequential interactions: recoverin–rhodopsin kinase, rhodopsin kinase–activated receptor, arrestin–phosphorylated metarhodopsin, receptor blocking. (c) phosphodiesterase shutdown. RGS9-1 protein binds to the Gt*–PDE-6 complex, resulting in dissociation of the complex. R — rhodopsin, R* — activated rhodopsin, Gt — transducin, Gt* — activated transducin, GDP — guanosine diphosphate, GTP — guanosine triphosphate, PDE-6 — phosphodiesterase-6, cGMP — cyclic guanosine monophosphate, GMP — guanosine monophosphate, GC — guanylate cyclase, REC — recoverin, RK — rhodopsin kinase, Ap — arrestin, R*-P — phosphorylated metarhodopsin.

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3. Fig. 2. Scheme of TRPM1 channel activation in ON-bipolar cells. Designations: Glu — glutamate, mGluR6 — metabotropic receptor mGluR6 of ON-bipolar cells, TRPM1 — channel of transient receptor potential of subfamily M, GDP — guanosine diphosphate, GTP — guanosine triphosphate, NT — N-terminus, CT — C-terminus.

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