Channelrhodopsins: from phototaxis to optogenetics

Cover Page

Full Text

Open Access Open Access
Restricted Access Access granted
Restricted Access Subscription Access

Abstract

Channelrhodopsins stand out among other retinal proteins because of their capacity to generate passive ionic currents following photoactivation. Owing to that, channelrhodopsins are widely used in neuroscience and cardiology as instruments for optogenetic manipulation of the activity of excitable cells. Photocurrents generated by channelrhodopsins were first discovered in the cells of green algae in the 1970s. In this review we describe this discovery and discuss the current state of research in this field.

References

  1. Drachev, L. A., Kaulen, A. D., Ostroumov, S. A., and Skulachev, V. P. (1974) Electrogenesis by bacteriorhodopsin incorporated in a planar phospholipid membrane, FEBS Lett., 39, 43-45, doi: 10.1016/0014-5793(74)80012-8.
  2. Drachev, L. A., Kaulen, A. D., and Skulachev, V. P. (1978) Time resolution of the intermediate steps in the bacteriorhodopsin-linked electrogenesis, FEBS Lett., 87, 161-167, doi: 10.1016/0014-5793(78)80157-4.
  3. Драчев Л. А., Каулен А. Д., Скулачев В. П., Хитрина Л. В., Чекулаева Л. Н. (1981) Фазы фотоэлектрического ответа бактериородопсина, Биохимия, 46, 998-1004.
  4. Oesterhelt, D., and Stoeckenius, W. (1971) Rhodopsin-like protein from the purple membrane of Halobacterium halobium, Nature, 233, 149-152, doi: 10.1038/newbio233149a0.
  5. Балашов С. П., Литвин Ф. Ф. (1985) Фотохимические превращения бактериородопсина, Издательство МГУ, Москва.
  6. Kandori, H. (2000) Role of internal water molecules in bacteriorhodopsin, Biochim. Biophys. Acta Bioenergetics, 1460, 177-191, doi: 10.1016/s0005-2728(00)00138-9.
  7. Lanyi, J. K. (2004) Bacteriorhodopsin, Annu. Rev. Physiol., 66, 665-688, doi: 10.1146/annurev.physiol.66.032102.150049.
  8. Wickstrand, C., Nogly, P., Nango, E., Iwata, S., Standfuss, J., and Neutze, R. (2019) Bacteriorhodopsin: Structural insights revealed using X-ray lasers and synchrotron radiation, Annu. Rev. Biochem., 88, 59-83, doi: 10.1146/annurev-biochem-013118-111327.
  9. Синещеков O. A., Литвин Ф. Ф. (1974) Фототаксис микроорганизмов, его механизм и связь с фотосинтезом, Усп. соврем. биологии, 78, 58-75.
  10. Nultsch, W., and Häder, D.-P. (1988) Photomovement in motile microorganisms - II, Photochem. Photobiol., 47, 837-869, doi: 10.1111/j.1751-1097.1988.tb01668.x.
  11. Spudich, E. N., and Spudich, J. L. (1982) Control of transmembrane ion fluxes to select halorhodopsin-deficient and other energy-trunsduction mutants of Halobacterium halobium, Proc. Natl. Acad. Sci. USA, 79, 4308-4312, doi: 10.1073/pnas.79.14.4308.
  12. Bogomolni, R., and Spudich, J. L. (1982) Identification of a third rhodopsin-like pigment in phototactic Halobacterium halobium, Proc. Natl. Acad. Sci. USA, 79, 6250-6254, doi: 10.1073/pnas.79.20.6250.
  13. Spudich, J. L., and Bogomolni, R. A. (1984) Mechanism of colour discrimination by a bacterial sensory rhodopsin, Nature, 312, 509-513, doi: 10.1038/312509a0.
  14. Takahashi, T., Tomioka, H., Kamo, N., and Kobatake, Y. (1985) A photosystem other than PS370 also mediates the negative phototaxis of Halobacterium halobium, FEMS Microbiol. Lett., 28, 161-164, doi: 10.1111/j.1574-6968.1985.tb00784.x.
  15. Feinleib, M. E. H., and Curry, G. M. (1971) The relationship between stimulus intensity and oriented phototactic response (topotaxis) in Chlamydomonas, Physiol. Plantarum, 25, 346-352, doi: 10.1111/j.1399-3054.1971.tb01453.x.
  16. Kondratieva, E. N., and Gogotov, I. N. (1969) Production of hydrogen by green photosynthetic bacteria (Chloropseudomonas), Nature, 221, 83-84, doi: 10.1038/221083a0.
  17. Булычев А. А., Андрианов В. К., Курелла Г. А., Литвин Ф. Ф. (1971) Трансмембранный потенциал хлоропласта и его фотоиндуцированные изменения, Докл. Акад. Наук СССР, 197, 473-477.
  18. Синещеков О. А., Андрианов В. К., Курелла Г. А., Литвин Ф. Ф. (1976) Биоэлектрические явления у одноклеточной зеленой водоросли и их связь с фототаксисом и фотосинтезом, Физиол. растений, 23, 229-237.
  19. Синещеков O. A., Синещеков В. A., Литвин Ф. Ф. (1978) Фотоиндуцированные биоэлектрические реакции в фототаксисе одноклеточной жгутиковой водоросли, Докл. Aкад. Нaук СССР, 239, 471-474.
  20. Litvin, F. F., Sineshchekov, O. A., and Sineshchekov, V. A. (1978) Photoreceptor electric potential in the phototaxis of the alga Haematococcus pluvialis, Nature, 271, 476-478, doi: 10.1038/271476a0.
  21. Sineshchekov, O. A., Govorunova, E. G., Der, A., Keszthelyi, L., and Nultsch, W. (1992) Photoelectric responses in phototactic flagellated algae measured in cell suspension, J. Photochem. Photobiol. B Biol., 13, 119-134, doi: 10.1016/1011-1344(92)85051-U.
  22. Kreimer, G. (1994) Cell biology of phototaxis in flagellate algae, Int. Rev. Cytol., 148, 229-310, doi: 10.1016/S0074-7696(08)62409-2.
  23. Sineshchekov, O. A., Jung, K.-H., and Spudich, J. L. (2002) Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii, Proc. Natl. Acad. Sci. USA, 99, 8689-8694, doi: 10.1073/pnas.122243399.
  24. Sineshchekov, O. A., Govorunova, E. G., Jung, K.-H., Zauner, S., Maier, U.-G., and Spudich, J. L. (2005) Rhodopsin-mediated photoreception in cryptophyte flagellates, Biophys. J., 89, 4310-4319, doi: 10.1529/biophysj.105.070920.
  25. Sineshchekov, O. A., and Spudich, J. L. (2005) Sensory rhodopsin signaling in green flagellate algae. in Handbook of Photosensory Receptors, Wiley-VCH, Weinheim, pp. 25-42, doi: 10.1002/352760510X.ch2.
  26. Govorunova, E. G., Spudich, E. N., Lane, C. E., Sineshchekov, O. A., and Spudich, J. L. (2011) New channelrhodopsin with a red-shifted spectrum and rapid kinetics from Mesostigma viride, mBio, 2, e00115-00111, doi: 10.1128/mBio.00115-11.
  27. Govorunova, E. G., Sineshchekov, O. A., Li, H., Janz, R., and Spudich, J. L. (2013) Characterization of a highly efficient blue-shifted channelrhodopsin from the marine alga Platymonas subcordiformis, J. Biol. Chem., 288, 29911-29922, doi: 10.1074/jbc.M113.505495.
  28. Govorunova, E. G., Jung, K.-W., Sineshchekov, O. A., and Spudich, J. L. (2004) Chlamydomonas sensory rhodopsins A and B: Cellular content and role in photophobic responses, Biophys. J., 86, 2342-2349, doi: 10.1016/S0006-3495(04)74291-5.
  29. Foster, K.-W., and Smyth, R. D. (1980) Light antennas in phototactic algae, Microbiol. Rev., 44, 572-630, doi: 10.1128/mr.44.4.572-630.1980.
  30. Foster, K.-W., Saranak, J., Patel, N., Zarrilli, G., Okabe, M., Kline, T., and Nakanishi, K. (1984) A rhodopsin is the functional photoreceptor for phototaxis in the unicelullar eukaryote Chlamydomonas, Nature, 311, 756-759, doi: 10.1038/311756a0.
  31. Sineshchekov, O. A., Govorunova, E. G., Der, A., Keszthelyi, L., and Nultsch, W. (1994) Photoinduced electric currents in carotenoid-deficient Chlamydomonas mutants reconstituted with retinal and its analogs, Biophys. J., 66, 2073-2084, doi: 10.1016/S0006-3495(94)81002-1.
  32. Sineshchekov, O. A., and Govorunova, E. G. (1999) Rhodopsin-mediated photosensing in green flagellated algae, Trends Plant Sci., 4, 58-63, doi: 10.1016/s1360-1385(98)01370-3.
  33. Nagel, G., Ollig, D., Fuhrmann, M., Kateriya, S., Musti, A. M., Bamberg, E., and Hegemann, P. (2002) Channelrhodopsin-1: a light-gated proton channel in green algae, Science, 296, 2395-2398, doi: 10.1126/science.1072068.
  34. Nagel, G., Szellas, T., Huhn, W., Kateriya, S., Adeishvili, N., Berthold, P., Ollig, D., Hegemann, P., and Bamberg, E. (2003) Channelrhodopsin-2, a directly light-gated cation-selective membrane channel, Proc. Natl. Acad. Sci. USA, 100, 13940-13945, doi: 10.1073/pnas.1936192100.
  35. Suzuki, T., Yamasaki, K., Fujita, S., Oda, K., Iseki, M., Yoshida, K., Watanabe, M., Daiyasu, H., Toh, H., Asamizu, E., Tabata, S., Miura, K., Fukuzawa, H., Nakamura, S., and Takahashi, T. (2003) Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization, Biochem. Biophys. Res. Commun., 301, 711-717, doi: 10.1016/s0006-291x(02)03079-6.
  36. Nagel, G., Mockel, B., Buldt, G., and Bamberg, E. (1995) Functional expression of bacteriorhodopsin in oocytes allows direct measurement of voltage dependence of light induced H+ pumping, FEBS Lett., 377, 263-266, doi: 0014-5793(95)01356-3.
  37. Boyden, E. S., Zhang, F., Bamberg, E., Nagel, G., and Deisseroth, K. (2005) Millisecond-timescale, genetically targeted optical control of neural activity, Nat. Neurosci., 8, 1263-1268, doi: 10.1038/nn1525.
  38. Nagel, G., Brauner, M., Liewald, J. F., Adeishvili, N., Bamberg, E., and Gottschalk, A. (2005) Light activation of channelrhodopsin-2 in excitable cells of Caenorhabditis elegans triggers rapid behavioral responses, Curr. Biol., 15, 2279-2284, doi: 10.1016/j.cub.2005.11.032.
  39. Li, X., Gutierrez, D. V., Hanson, M. G., Han, J., Mark, M. D., Chiel, H., Hegemann, P., Landmesser, L. T., and Herlitze, S. (2005) Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin, Proc. Natl. Acad. Sci. USA, 102, 17816-17821, doi: 10.1073/pnas.0509030102.
  40. Deisseroth, K. (2011) Optogenetics, Nat. Methods, 8, 26-29, doi: 10.1038/nmeth.f.324.
  41. Yawo, H., Asano, T., Sakai, S., and Ishizuka, T. (2013) Optogenetic manipulation of neural and non-neural functions, Dev. Growth Differ., 55, 474-490, doi: 10.1111/dgd.12053.
  42. Deisseroth, K. (2015) Optogenetics: 10 years of microbial opsins in neuroscience, Nat. Neurosci., 18, 1213-1225, doi: 10.1038/nn.4091.
  43. Emiliani, V., Entcheva, E., Hedrich, R., Hegemann, P., Konrad, K. R., Lüscher, C., Mahn, M., Pan, Z.-H., Sims, R. R., Vierock, J., and Yizhar, O. (2022) Optogenetics for light control of biological systems, Nat. Rev. Methods Primers, 2, 55, doi: 10.1038/s43586-022-00136-4.
  44. Chow, B. Y., and Boyden, E. S. (2013) Optogenetics and translational medicine, Sci. Transl. Med., 5, 177ps175, doi: 10.1126/scitranslmed.3003101.
  45. Sasse, P., Funken, M., Beiert, T., and Bruegmann, T. (2019) Optogenetic termination of cardiac arrhythmia: Mechanistic enlightenment and therapeutic application? Front. Physiol., 10, 675, doi: 10.3389/fphys.2019.00675.
  46. Sahel, J. A., Boulanger-Scemama, E., Pagot, C., Arleo, A., Galluppi, F., Martel, J. N., Esposti, S. D., Delaux, A., de Saint Aubert, J. B., de Montleau, C., Gutman, E., Audo, I., Duebel, J., Picaud, S., Dalkara, D., Blouin, L., Taiel, M., and Roska, B. (2021) Partial recovery of visual function in a blind patient after optogenetic therapy, Nat. Med., 27, 1223-1229, doi: 10.1038/s41591-021-01351-4.
  47. Chow, B. Y., Han, X., Dobry, A. S., Qian, X., Chuong, A. S., Li, M., Henninger, M. A., Belfort, G. M., Lin, Y., Monahan, P. E., and Boyden, E. S. (2010) High-performance genetically targetable optical neural silencing by light-driven proton pumps, Nature, 463, 98-102, doi: 10.1038/nature08652.
  48. Govorunova, E. G., Sineshchekov, O. A., Liu, X., Janz, R., and Spudich, J. L. (2015) Natural light-gated anion channels: A family of microbial rhodopsins for advanced optogenetics, Science, 349, 647-650, doi: 10.1126/science.aaa7484.
  49. Govorunova, E. G., Sineshchekov, O. A., Li, H., Wang, Y., Brown, L. S., and Spudich, J. L. (2020) RubyACRs, non-algal anion channelrhodopsins with highly red-shifted absorption, Proc. Natl. Acad. Sci. USA, 117, 22833-22840, doi: 10.1073/pnas.2005981117.
  50. Sineshchekov, O. A., Govorunova, E. G., Li, H., and Spudich, J. L. (2017) Bacteriorhodopsin-like channelrhodopsins: Alternative mechanism for control of cation conductance, Proc. Natl. Acad. Sci. USA, 114, E9512-E9519, doi: 10.1073/pnas.1710702114.
  51. Govorunova, E. G., Gou, Y., Sineshchekov, O. A., Li, H., Lu, X., Wang, Y., Brown, L. S., St-Pierre, F., Xue, M., and Spudich, J. L. (2022) Kalium channelrhodopsins are natural light-gated potassium channels that mediate optogenetic inhibition, Nat. Neurosci., 25, 967-974, doi: 10.1038/s41593-022-01094-6.
  52. Der, A., and Keszthelyi, L. (2001) Charge motion during the photocycle of bacteriorhodopsin, Biochemistry (Moscow), 66, 1234-1248, doi: 10.1023/A:1013179101782.
  53. Sineshchekov, O. A., Govorunova, E. G., Wang, J., Li, H., and Spudich, J. L. (2013) Intramolecular proton transfer in channelrhodopsins, Biophys. J., 104, 807-817, doi: 10.1016/j.bpj.2013.01.002.
  54. Sineshchekov, O. A., Govorunova, E. G., Li, H., and Spudich, J. L. (2015) Gating mechanisms of a natural anion channelrhodopsin, Proc. Natl. Acad. Sci. USA, 112, 14236-14241, doi: 10.1073/pnas.1513602112.
  55. Sineshchekov, O. A., Govorunova, E. G., Li, H., Wang, Y., and Spudich, J. L. (2023) Sequential absorption of two photons creates a bistable form of RubyACR responsible for its strong desensitization, Proc. Natl. Acad. Sci. USA, 120, e2301521120, doi: 10.1073/pnas.2301521120.
  56. Schneider, F., Grimm, C., and Hegemann, P. (2015) Biophysics of channelrhodopsin, Annu. Rev. Biophys., 44, 167-186, doi: 10.1146/annurev-biophys-060414-034014.
  57. Deisseroth, K., and Hegemann, P. (2017) The form and function of channelrhodopsin, Science, 357, eaan5544, doi: 10.1126/science.aan5544.
  58. Govorunova, E. G., Sineshchekov, O. A., Li, H., and Spudich, J. L. (2017) Microbial rhodopsins: Diversity, mechanisms, and optogenetic applications, Annu. Rev. Biochem., 86, 845-872, doi: 10.1146/annurev-biochem-101910-144233.
  59. Govorunova, E. G., Sineshchekov, O. A., and Spudich, J. L. (2021) Emerging diversity of channelrhodopsins and their structure-function relationships, Front. Cell Neurosci., 15, 800313, doi: 10.3389/fncel.2021.800313.
  60. Boyden, E. S. (2011) A history of optogenetics: the development of tools for controlling brain circuits with light, F1000 Biol. Rep., 3, 11, doi: 10.3410/B3-11.
  61. Fenno, L., Yizhar, O., and Deisseroth, K. (2011) The development and application of optogenetics, Annu. Rev. Neurosci., 34, 389-412, doi: 10.1146/annurev-neuro-061010-113817.
  62. Hegemann, P., and Nagel, G. (2013) From channelrhodopsins to optogenetics, EMBO Mol. Med., 5, 1-4, doi: 10.1002/emmm.201202387.
  63. Boyden, E. S. (2015) Optogenetics and the future of neuroscience, Nat. Neurosci., 18, 1200-1201, doi: 10.1038/nn.4094.
  64. Richards, R., and Dempski, R. E. (2015) From phototaxis to biomedical applications: Investigating the molecular mechanism of channelrhodopsins, in Electrophysiology of Unconventional Channels and Pores (Delcour, A. H., ed) Springer International Publishing Switzerland. pp. 361-381, doi: 10.1007/978-3-319-20149-8_15.
  65. Bamberg, E., Gärtner, W., and Trauner, D. (2018) Introduction: Optogenetics and photopharmacology, Chem. Rev., 118, 10627-10628, doi: 10.1021/acs.chemrev.8b00483.
  66. Baylor, D. A., and Hodgkin, A. L. (1973) Detection and resolution of visual stimuli by turtle photoreceptors, J. Physiol., 234, 163-198, doi: 10.1113/jphysiol.1973.sp010340.
  67. Harz, H., and Hegemann, P. (1991) Rhodopsin-regulated calcium currents in Chlamydomonas, Nature, 351, 489-491, doi: 10.1038/351489a0.
  68. Braun, F. J., and Hegemann, P. (1999) Two light-activated conductances in the eye of the green alga Volvox carteri, Biophys. J., 76, 1668-1678, doi: 10.1016/S0006-3495(99)77326-1.
  69. Yoshimura, K. (1996) A novel type of mechanoreception by the flagella of Chlamydomonas, J. Exp. Biol., 199, 295-302, doi: 10.1242/jeb.199.2.295.
  70. Sineshchekov, O. A., and Govorunova, E. G. (2001) Electrical events in photomovements of green flagellated algae, in Comprehensive Series in Photosciences (Hader, D.-P., and Lebert, M., eds) Elsevier, Amsterdam, pp. 245-280, doi: 10.1016/S1568-461X(01)80013-2.
  71. Sineshchekov, O. A., Govorunova, E. G., and Spudich, J. L. (2021) Probing channelrhodopsin electrical activity in algal cell populations, in Channelrhodopsin (Dempski, R., ed) 2020/09/01 Ed., Humana, New York. pp. 85-96, doi: 10.1007/978-1-0716-0830-2_6.
  72. Kreimer, G., Overländer, C., Sineshchekov, O. A., Stolzis, H., Nultsch, W., and Melkonian, M. (1992) Functional analysis of the eyespot in Chlamydomonas reinhardtii mutant ey 627, mt-, Planta, 188, 513-521, doi: 10.1007/BF00197043.
  73. Pazour, G., Sineshchekov, O., and Witman, G. B. (1995) Mutational analysis of the phototransduction pathway of Chlamydomonas reinhardtii, J. Cell Biol., 131, 427-440, doi: 10.1083/jcb.131.2.427.
  74. Matsuda, A., Yoshimura, K., Sineshchekov, O., Hirono, M., and Kamiya, R. (1998) Isolation and characterization of novel Chlamydomonas mutants that display phototaxis but not photophobic response, Cell Motil. Cytoskeleton, 41, 353-362, doi: 10.1002/(SICI)1097-0169(1998)41:4<353::AID-CM7>3.0.CO;2-0.
  75. Govorunova, E. G., and Sineshchekov, O. A. (2003) Integration of photo- and chemosensory signaling pathways in Chlamydomonas, Planta, 216, 535-540, doi: 10.1007/s00425-002-0901-7.
  76. Govorunova, E. G., Altschuler, I. M., Häder, D. P., and Sineshchekov, O. A. (2000) A novel express bioassay for detecting toxic substances in water by recording rhodopsin-mediated photoelectric responses in Chlamydomonas cell suspensions, Photochem. Photobiol., 72, 320-326, doi: 10.1562/0031-8655(2000)072<0320:anebfd>2.0.co;2.
  77. Govorunova, E. G., and Sineshchekov, O. A. (2017) Express detection of water pollutants by photoelectric recording from algal cell suspensions, in Bioassays: Advanced Methods and Applications (Häder, D.-P., and Erzinger, G. S., eds) Elsevier, Amsterdam, pp. 289-308, doi: 10.1016/B978-0-12-811861-0.00014-0.
  78. Sineshchekov, O. A. (1991) Photoreception in unicellular flagellates: bioelectric phenomena in phototaxis, in Light in Biology and Medicine (Douglas, R. D., ed) Plenum Press, New York, pp. 523-532, doi: 10.1007/978-1-4684-5991-3_53.
  79. Синещеков, O. A. (1988) Фототаксис микроорганизмов и его роль в регуляции фотосинтеза, Фототрофные микроорганизмы (под ред. Гоготов, И. Н.) Изд-во Академии Наук СССР, Пущино, стр. 11-18.
  80. Yoshimura, K. (1994) Chromophore orientation in the photoreceptor of Chlamydomonas as probed by stimulation with polarized light, Photochem. Photobiol., 60, 594-597, doi: 10.1111/j.1751-1097.1994.tb05154.x.
  81. Mast, S. O. (1911) Light and the Behavior of Organisms, Wiley, New York, doi: 10.5962/bhl.title.4601.
  82. Morel-Laurens, N. M. L., and Feinleib, M. E. (1983) Photomovement in an "eyeless" mutant of Chlamydomonas, Photochem. Photobiol., 37, 189-194, doi: 10.1111/j.1751-1097.1983.tb04457.x.
  83. Kreimer, G., and Melkonian, M. (1990) Reflection confocal laser scanning microscopy of eyespot in flagellated green algae, Eur. J. Cell Biol., 53, 101-111, doi: 10.1016/S1434-4610(99)70032-5.
  84. Berthold, P., Tsunoda, S. P., Ernst, O. P., Mages, W., Gradmann, D., and Hegemann, P. (2008) Channelrhodopsin-1 initiates phototaxis and photophobic responses in Chlamydomonas by immediate light-induced depolarization, Plant Cell, 20, 1665-1677, doi: 10.1105/tpc.108.057919.
  85. Mittelmeier, T. M., Thompson, M. D., Ozturk, E., and Dieckmann, C. L. (2013) Independent localization of plasma membrane and chloroplast components during eyespot assembly, Eukaryot. Cell, 12, 1258-1270, doi: 10.1128/EC.00111-13.
  86. Schmidt, M., Gessner, G., Luff, M., Heiland, I., Wagner, V., Kaminski, M., Geimer, S., Eitzinger, N., Reissenweber, T., Voytsekh, O., Fiedler, M., Mittag, M., and Kreimer, G. (2006) Proteomic analysis of the eyespot of Chlamydomonas reinhardtii provides novel insights into its components and tactic movements, Plant Cell, 18, 1908-1930, doi: 10.1105/tpc.106.041749.
  87. Melkonian, M., and Robenek, H. (1980) Eyespot membranes of Chlamydomonas reinhardtii: a freeze-fracture study, J. Ultrastruct. Res., 72, 90-102, doi: 10.1016/S0022-5320(80)90138-0.
  88. Awasthi, M., Ranjan, P., Sharma, K., Veetil, S. K., and Kateriya, S. (2016) The trafficking of bacterial type rhodopsins into the Chlamydomonas eyespot and flagella is IFT mediated, Sci. Rep., 6, 34646, doi: 10.1038/srep34646.
  89. Awasthi, M., Ranjan, P., and Kateriya, S. (2018) Cytoplasmic extensions of the channelrhodopsins 1 and 2 interact in Chlamydomonas reinhardtii, J. Appl. Biotechnol. Bioeng., 5, 84-90, doi: 10.15406/jabb.2018.05.00121.
  90. Синещеков О. А., Литвин Ф. Ф. (1988 ) Механизмы фототаксиса микроорганизмов. in Молекулярные механизмы биологического действия оптического излучения (под ред. Рубин А. Б.) Наука, Москва, стр. 412-427.
  91. Witman, G. B. (1993) Chlamydomonas phototaxis, Trends Cell Biol., 3, 403-408, doi: 10.1016/0962-8924(93)90091-e.
  92. Kateriya, S., Nagel, G., Bamberg, E., and Hegemann, P. (2004) "Vision" in single-celled algae, News Physiol. Sci., 19, 133-137, doi: 10.1152/nips.01517.2004.
  93. Kreimer, G. (2009) The green algal eyespot apparatus: a primordial visual system and more? Curr. Genet., 55, 19-43, doi: 10.1007/s00294-008-0224-8.
  94. Böhm, M., and Kreimer, G. (2021) Orient in the world with a single eye: The green algal eyespot and phototaxis, in Prog. Bot. (Cánovas, F. M., Lüttge, U., Risueño, M.-C., and Pretzsch, H., eds). pp. 259-304, doi: 10.1007/124_2020_38.
  95. Sineshchekov, O. A. (1991) Electrophysiology of photomovements in flagellated algae. in Biophysics of Photoreceptors and Photomovements in Microorganisms (Lenci, F., Ghetti, F., Colombetti, G., Haeder, D.-P., and Song, P.-S., eds) Plenum Press, New York. pp. 191-202, doi: 10.1007/978-1-4684-5988-3_15.
  96. Rüffer, U., and Nultsch, W. (1990) Flagella photoresponses of Chlamydomonas cells held on micropipettes: I. Change in flagellar beat frequency, Cell Motil. Cytoskeleton, 15, 162-167, doi: 10.1002/cm.970150305.
  97. Rüffer, U., and Nultsch, W. (1991) Flagellar photoresponses of Chlamydomonas cells held on micropipettes: II. Change in flagellar beat pattern, Cell Motil. Cytoskeleton, 18, 269-278, doi: 10.1002/cm.970180404.
  98. Josef, K., Saranak, J., and Foster, K.-W. (2005) Ciliary behavior of a negatively phototactic Chlamydomonas reinhardtii, Cell Motil. Cytoskeleton, 61, 97-111, doi: 10.1002/cm.20069.
  99. Josef, K., Saranak, J., and Foster, K.-W. (2006) Linear systems analysis of the ciliary steering behavior associated with negative-phototaxis in Chlamydomonas reinhardtii, Cell Motil. Cytoskeleton, 63, 758-777, doi: 10.1002/cm.20158.
  100. Holland, E.-M., Harz, H., Uhl, R., and Hegemann, P. (1997) Control of phobic behavioral responses by rhodopsin-induced photocurrents in Chlamydomonas, Biophys. J., 73, 1395-1401, doi: 10.1016/S0006-3495(97)78171-2.
  101. Schmidt, J. A., and Eckert, R. (1976) Calcium couples flagella reversal to photostimulation in Chlamydomonas reinhardtii, Nature, 262, 713-715, doi: 10.1038/262713a0.
  102. Nultsch, W., and Häder, D.-P. (1979) Photomovement of motile microorganisms, Photochem. Photobiol., 29, 423-437, doi: 10.1111/j.1751-1097.1979.tb07072.x.
  103. Harz, H., Nonnengässer, C., and Hegemann, P. (1992) The photoreceptor current of the green alga Chlamydomonas, Phil. Trans. R. Soc. Lond. B, 338, 39-52, doi: 10.1098/rstb.1992.0127.
  104. Beck, C., and Uhl, R. (1994) On the localization of voltage-sensitive calcium channels in the flagella of Chlamydomonas reinhardtii, J. Cell Biol., 125, 1119-1125, doi: 10.1083/jcb.125.5.1119.
  105. Fujiu, K., Nakayama, Y., Yanagisawa, A., Sokabe, M., and Yoshimura, K. (2009) Chlamydomonas CAV2 encodes a voltage-dependent calcium channel required for the flagellar waveform conversion, Curr. Biol., 19, 133-139, doi: 10.1016/j.cub.2008.11.068.
  106. Sineshchekov, O. A., Litvin, F. F., and Keszthelyi, L. (1990) Two components of photoreceptor potential of the flagellated green alga Haematococcus pluvialis, Biophys. J., 57, 33-39, doi: 10.1016/S0006-3495(90)82504-2.
  107. Sineshchekov, O. A., Govorunova, E. G., and Spudich, J. L. (2009) Photosensory functions of channelrhodopsins in native algal cells, Photochem. Photobiol., 85, 556-563, doi: 10.1111/j.1751-1097.2008.00524.x.
  108. Hegemann, P., and Marwan, W. (1988) Single photons are sufficient to trigger movement responses in Chlamydomonas reinhardtii, Photochem. Photobiol., 48, 99-106, doi: 10.1111/j.1751-1097.1988.tb02793.x.
  109. Verret, F., Wheeler, G., Taylor, A. R., Farnham, G., and Brownlee, C. (2010) Calcium channels in photosynthetic eukaryotes: implications for evolution of calcium-based signalling, New Phytol., 187, 23-43, doi: 10.1111/j.1469-8137.2010.03271.x.
  110. Wagner, V., Ullmann, K., Mollwo, A., Kaminski, M., Mittag, M., and Kreimer, G. (2008) The phosphoproteome of a Chlamydomonas reinhardtii eyespot fraction includes key proteins of the light signaling pathway, Plant Physiol., 146, 772-788, doi: 10.1104/pp.107.109645.
  111. Linden, L., and G., K. (1995) Calcium modulates rapid protein phosphorilation/dephosphorilation in isolated eyespot apparatuses of the green alga Spermatozopsis similis, Planta, 197, 343-351, doi: 10.1007/BF00202656.
  112. Schlicher, U., Linden, L., Calenberg, M., and Kreimer, G. (1995) G proteins and Ca2+ modulated protein kinases of a plasma membrane enriched fraction and isolated eyespot apparatuses of Spermatozopsis similis (Chlorophycea), Eur. J. Phycol., 30, 319-330, doi: 10.1080/09670269500651111.
  113. Calenberg, M., Brohnsonn, U., Zedlacher, M., and Kreimer, G. (1998) Light- and Ca2+-modulated heteromeric GTPases in the eyespot apparatus of a flagellate green alga, Plant Cell, 10, 91-103, doi: 10.1105/tpc.10.1.91.
  114. Trippens, J., Greiner, A., Schellwat, J., Neukam, M., Rottmann, T., Lu, Y., Kateriya, S., Hegemann, P., and Kreimer, G. (2012) Phototropin influence on eyespot development and regulation of phototactic behavior in Chlamydomonas reinhardtii, Plant Cell, 24, 4687-702, doi: 10.1105/tpc.112.103523.
  115. Holland, E.-M., Braun, F.-J., Nonnengässer, C., Harz, H., and Hegemann, P. (1996) The nature of rhodopsin-triggered photocurrents in Chlamydomonas. I. Kinetics and influence of divalent ions, Biophys. J., 70, 924-931, doi: 10.1016/S0006-3495(96)79635-2.
  116. Nonnengässer, C., Holland, E.-M., Harz, H., and Hegemann, P. (1996) The nature of rhodopsin-activated photocurrents in Chlamydomonas. II. Influence of monovalent ions, Biophys. J., 70, 932-938, doi: 10.1016/S0006-3495(96)79636-4.
  117. Ritter, E., Stehfest, K., Berndt, A., Hegemann, P., and Bartl, F. J. (2008) Monitoring light-induced structural changes of Channelrhodopsin-2 by UV-visible and Fourier transform infrared spectroscopy, J. Biol. Chem., 283, 35033-35041, doi: 10.1074/jbc.M806353200.
  118. Bamann, C., Kirsch, T., Nagel, G., and Bamberg, E. (2008) Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function, J. Mol. Biol., 375, 686-694, doi: 10.1016/j.jmb.2007.10.072.
  119. Baidukova, O., Oppermann, J., Kelterborn, S., Fernandez Lahore, R. G., Schumacher, D., Evers, H., Kamrani, Y. Y., and Hegemann, P. (2022) Gating and ion selectivity of channelrhodopsins are critical for photo-activated orientation of Chlamydomonas as shown by in vivo point mutation, Nat Commun, 13, 7253, doi: 10.1038/s41467-022-35018-6.
  120. Dent, R. M., Haglund, C. M., Chin, B. L., Kobayashi, M. C., and Niyogi, K. K. (2005) Functional genomics of eukaryotic photosynthesis using insertional mutagenesis of Chlamydomonas reinhardtii, Plant Physiol., 137, 545-556, doi: 10.1104/pp.104.055244.
  121. Sizova, I., Greiner, A., Awasthi, M., Kateriya, S., and Hegemann, P. (2013) Nuclear gene targeting in Chlamydomonas using engineered zinc-finger nucleases, Plant J., 73, 873-882, doi: 10.1111/tpj.12066.
  122. Greiner, A., Kelterborn, S., Evers, H., Kreimer, G., Sizova, I., and Hegemann, P. (2017) Targeting of photoreceptor genes in Chlamydomonas reinhardtii via zinc-finger nucleases and CRISPR/Cas9, Plant Cell, 29, 2498-2518, doi: 10.1105/tpc.17.00659.
  123. Sineshchekov, O. A., Spudich, E. N., Trivedi, V. D., and Spudich, J. L. (2006) Role of the cytoplasmic domain in Anabaena sensory rhodopsin photocycling: vectoriality of Schiff base deprotonation, Biophys. J., 91, 4519-4527, doi: 10.1529/biophysj.106.093641.
  124. Tashiro, R., Sushmita, K., Hososhima, S., Sharma, S., Kateriya, S., Kandori, H., and Tsunoda, S. P. (2021) Specific residues in the cytoplasmic domain modulate photocurrent kinetics of channelrhodopsin from the alga Klebsormidium nitens, Commun. Biol., 4, 235, doi: 10.1038/s42003-021-01755-5.
  125. Böhm, M., Boness, D., Fantisch, E., Erhard, H., Frauenholz, J., Kowalzyk, Z., Marcinkowski, N., Kateriya, S., Hegemann, P., and Kreimer, G. (2019) Channelrhodopsin-1 phosphorylation changes with the phototactic behavior and responds to physiological stimuli in Chlamydomonas, Plant Cell, 31, 886-910, doi: 10.1105/tpc.18.00936.
  126. Awasthi, M., Sushmita, K., Kaushik, M. S., Ranjan, P., and Kateriya, S. (2020) Novel modular rhodopsins from green algae hold great potential for cellular optogenetic modulation across the biological model systems, Life, 10, 259, doi: 10.3390/life10110259.
  127. Rozenberg, A., Oppermann, J., Wietek, J., Fernandez Lahore, R. G., Sandaa, R. A., Bratbak, G., Hegemann, P., and Béjà, O. (2020) Lateral gene transfer of anion-conducting channelrhodopsins between green algae and giant viruses, Curr. Biol., 30, 4910-4920, doi: 10.1016/j.cub.2020.09.056.
  128. Sharma, K., Sizova, I., Sanyal, S. K., Pandey, G. K., Hegemann, P., and Kateriya, S. (2023) Deciphering the role of cytoplasmic domain of Channelrhodopsin in modulating the interactome and SUMOylome of Chlamydomonas reinhardtii, Int. J. Biol. Macromol., 243, 125135, doi: 10.1016/j.ijbiomac.2023.125135.
  129. Matasci, N., Hung, L. H., Yan, Z., Carpenter, E. J., Wickett, N. J., Mirarab, S., Nguyen, N., Warnow, T., Ayyampalayam, S., Barker, M., Burleigh, J. G., Gitzendanner, M. A., Wafula, E., Der, J. P., dePamphilis, C. W., Roure, B., Philippe, H., Ruhfel, B. R., Miles, N. W., Graham, S. W., et al. (2014) Data access for the 1,000 Plants (1KP) project, Gigascience, 3, 17, doi: 10.1186/2047-217X-3-17.
  130. Wong, G. K., Soltis, D. E., Leebens-Mack, J., Wickett, N. J., Barker, M. S., Van de Peer, Y., Graham, S. W., and Melkonian, M. (2020) Sequencing and analyzing the transcriptomes of a thousand species across the tree of life for green plants, Annu. Rev. Plant Biol., 71, 741-765, doi: 10.1146/annurev-arplant-042916-041040.
  131. Govorunova, E. G., Sineshchekov, O. A., Li, H., Wang, Y., Brown, L. S., Palmateer, A., Melkonian, M., Cheng, S., Carpenter, E., Patterson, J., Wong, G. K. S., and Spudich, J. L. (2021) Cation and anion channelrhodopsins: Sequence motifs and taxonomic distribution, MBio, 12, e0165621, doi: 10.1128/mBio.01656-21.
  132. Glock, C., Nagpal, J., and Gottschalk, A. (2015) Microbial rhodopsin optogenetic tools: Application for analyses of synaptic transmission and of neuronal network activity in behavior, Methods Mol. Biol., 1327, 87-103, doi: 10.1007/978-1-4939-2842-2_8.
  133. Tsunoda, S. P., and Hegemann, P. (2009) Glu 87 of channelrhodopsin-1 causes pH-dependent color tuning and fast photocurrent inactivation, Photochem. Photobiol., 85, 564-569, doi: 10.1111/j.1751-1097.2008.00519.x.
  134. Говорунова Е. Г., Синещеков О. А., Спудич Д. Л. (2017) Три семейства канальных родопсинов и их использование в оптогенетике, Журн. Высш. Нервной Деятельности, 67, 1-9.
  135. Watanabe, M., and Furuya, M. (1982) Phototactic behavior of individual cells of Cryptomonas sp. in response to continuous and intermittent light stimuli, Photochem. Photobiol., 35, 559-563, doi: 10.1111/j.1751-1097.1982.tb02609.x.
  136. Rhiel, E., Häder, D.-P., and Wehrmeyer, W. (1988) Photo-orientation in a freshwater Cryptomonas species, J. Photochem. Photobiol. B Biol., 2, 123-132, doi: 10.1016/1011-1344(88)85041-3.
  137. Erata, M., Kubota, M., Takahashi, T., Inouye, I., and Watanabe, M. (1995) Ultrastructure and phototactic action spectra of two genera of cryptophyte flagellate algae, Cryptomonas and Chroomonas, Protoplasma, 188, 258-266, doi: 10.1007/BF01280378.
  138. Govorunova, E. G., Sineshchekov, O. A., and Spudich, J. L. (2016) Structurally distinct cation channelrhodopsins from cryptophyte algae, Biophys. J., 110, 2302-2304, doi: S0006-3495(16)30274-0.
  139. Gradinaru, V., Zhang, F., Ramakrishnan, C., Mattis, J., Prakash, R., Diester, I., Goshen, I., Thompson, K. R., and Deisseroth, K. (2010) Molecular and cellular approaches for diversifying and extending optogenetics, Cell, 141, 154-165, doi: 10.1016/j.cell.2010.02.037.
  140. Yamauchi, Y., Konno, M., Ito, S., Tsunoda, S. P., Inoue, K., and Kandori, H. (2017) Molecular properties of a DTD channelrhodopsin from Guillardia theta, Biophys. Physicobiol., 14, 57-66, doi: 10.2142/biophysico.14.0_57.
  141. Hososhima, S., Ueno, S., Okado, S., Inoue, K. I., Konno, M., Yamauchi, Y., Inoue, K., Terasaki, H., Kandori, H., and Tsunoda, S. P. (2023) A light-gated cation channel with high reactivity to weak light, Sci Rep., 13, 7625, doi: 10.1038/s41598-023-34687-7.
  142. Sineshchekov, O. A., Govorunova, E. G., Li, H., Wang, Y., Melkonian, M., Wong, G. K.-S., Brown, L. S., and Spudich, J. L. (2020) Conductance mechanisms of rapidly desensitizing cation channelrhodopsins from cryptophyte algae, mBio, 11, e00657-20, doi: 10.1128/mBio.00657-20.
  143. Kishi, K. E., Kim, Y. S., Fukuda, M., Inoue, M., Kusakizako, T., Wang, P. Y., Ramakrishnan, C., Byrne, E. F. X., Thadhani, E., Paggi, J. M., Matsui, T. E., Yamashita, K., Nagata, T., Konno, M., Quirin, S., Lo, M., Benster, T., Uemura, T., Liu, K., Shibata, M., et al. (2022) Structural basis for channel conduction in the pump-like channelrhodopsin ChRmine, Cell, 185, 672-689.e623, doi: 10.1016/j.cell.2022.01.007.
  144. Tucker, K., Sridharan, S., Adesnik, H., and Brohawn, S. G. (2022) Cryo-EM structures of the channelrhodopsin ChRmine in lipid nanodiscs, Nat. Commun., 13, 4842, doi: 10.1038/s41467-022-32441-7.
  145. Kato, H. E., Zhang, F., Yizhar, O., Ramakrishnan, C., Nishizawa, T., Hirata, K., Ito, J., Aita, Y., Tsukazaki, T., Hayashi, S., Hegemann, P., Maturana, A. D., Ishitani, R., Deisseroth, K., and Nureki, O. (2012) Crystal structure of the channelrhodopsin light-gated cation channel, Nature, 482, 369-374, doi: 10.1038/nature10870.
  146. Volkov, O., Kovalev, K., Polovinkin, V., Borshchevskiy, V., Bamann, C., Astashkin, R., Marin, E., Popov, A., Balandin, T., Willbold, D., Buldt, G., Bamberg, E., and Gordeliy, V. (2017) Structural insights into ion conduction by channelrhodopsin 2, Science, 358, eaan8862, doi: 10.1126/science.aan8862.
  147. Oda, K., Vierock, J., Oishi, S., Rodriguez-Rozada, S., Taniguchi, R., Yamashita, K., Wiegert, J. S., Nishizawa, T., Hegemann, P., and Nureki, O. (2018) Crystal structure of the red light-activated channelrhodopsin Chrimson, Nat. Commun., 9, 3949, doi: 10.1038/s41467-018-06421-9.
  148. Marshel, J. H., Kim, Y. S., Machado, T. A., Quirin, S., Benson, B., Kadmon, J., Raja, C., Chibukhchyan, A., Ramakrishnan, C., Inoue, M., Shane, J. C., McKnight, D. J., Yoshizawa, S., Kato, H. E., Ganguli, S., and Deisseroth, K. (2019) Cortical layer-specific critical dynamics triggering perception, Science, 365, eaaw5202, doi: 10.1126/science.aaw5202.
  149. Chen, R., Gore, F., Nguyen, Q. A., Ramakrishnan, C., Patel, S., Kim, S. H., Raffiee, M., Kim, Y. S., Hsueh, B., Krook-Magnusson, E., Soltesz, I., and Deisseroth, K. (2020) Deep brain optogenetics without intracranial surgery, Nat. Biotechnol., 39, 161-164, doi: 10.1038/s41587-020-0679-9.
  150. Govorunova, E. G., Sineshchekov, O. A., Rodarte, E. M., Janz, R., Morelle, O., Melkonian, M., Wong, G. K.-S., and Spudich, J. L. (2017) The expanding family of natural anion channelrhodopsins reveals large variations in kinetics, conductance, and spectral sensitivity, Sci. Rep., 7, 43358, doi: 10.1038/srep43358.
  151. Govorunova, E. G., Sineshchekov, O. A., Hemmati, R., Janz, R., Morelle, O., Melkonian, M., Wong, G. K. S., and Spudich, J. L. (2018) Extending the time domain of neuronal silencing with cryptophyte anion channelrhodopsins, eNeuro, 5, ENEURO.0174-0118.2018, doi: 10.1523/ENEURO.0174-18.2018.
  152. Долгих Д. А., Малышев А. Ю., Саложин С. В., Некрасова О. В., Петровская Л. Е., Рощин М. В., Бородинова А. А., Фельдман Т. Б., Балабан П. М., Кирпичников М. П., Островский М. А. (2015) Анионный канальный родопсин, экспрессированный в культуре нейронов и in vivo в мозге мыши: светоиндуцированное подавление генерации потенциалов действия, Докл. Aкад. Нaук, 465, 737-740, doi: 10.7868/S086956521536030X.
  153. Mohammad, F., Stewart, J. C., Ott, S., Chlebikova, K., Chua, J. Y., Koh, T. W., Ho, J., and Claridge-Chang, A. (2017) Optogenetic inhibition of behavior with anion channelrhodopsins, Nat. Methods, 14, 271-274, doi: 10.1038/nmeth.4148.
  154. Mohamed, G. A., Cheng, R. K., Ho, J., Krishnan, S., Mohammad, F., Claridge-Chang, A., and Jesuthasan, S. (2017) Optical inhibition of larval zebrafish behaviour with anion channelrhodopsins, BMC Biol., 15, 103, doi: 10.1186/s12915-017-0430-2.
  155. Bergs, A., Schultheis, C., Fischer, E., Tsunoda, S. P., Erbguth, K., Husson, S. J., Govorunova, E. G., Spudich, J. L., Nagel, G., Gottschalk, A., and Liewald, J. F. (2018) Rhodopsin optogenetic toolbox v2.0 for light-sensitive excitation and inhibition in Caenorhabditis elegans, PLoS One, 13, e0191802, doi: 10.1371/journal.pone.0191802.
  156. Wilson, D. E., Scholl, B., and Fitzpatrick, D. (2018) Differential tuning of excitation and inhibition shapes direction selectivity in ferret visual cortex, Nature, 560, 97-101, doi: 10.1038/s41586-018-0354-1.
  157. Forli, A., Vecchia, D., Binini, N., Succol, F., Bovetti, S., Moretti, C., Nespoli, F., Mahn, M., Baker, C. A., Bolton, M. M., Yizhar, O., and Fellin, T. (2018) Two-photon bidirectional control and imaging of neuronal excitability with high spatial resolution in vivo, Cell Rep., 22, 3087-3098, doi: 10.1016/j.celrep.2018.02.063.
  158. Andrei, A. R., Debes, S., Chelaru, M., Liu, X., Rodarte, E., Spudich, J. L., Janz, R., and Dragoi, V. (2021) Heterogeneous side-effects of cortical inactivation in behaving animals, Elife, 10, e66400, doi: 10.7554/eLife.66400.
  159. Huang, S., Ding, M., Roelfsema, M. R. G., Dreyer, I., Scherzer, S., Al-Rasheid, K. A. S., Gao, S., Nagel, G., Hedrich, R., and Konrad, K. R. (2021) Optogenetic control of the guard cell membrane potential and stomatal movement by the light-gated anion channel GtACR1, Sci Adv, 7, eabg4619, doi: 10.1126/sciadv.abg4619.
  160. Zhou, Y., Ding, M., Gao, S., Yu-Strzelczyk, J., Krischke, M., Duan, X., Leide, J., Riederer, M., Mueller, M. J., Hedrich, R., Konrad, K. R., and Nagel, G. (2021) Optogenetic control of plant growth by a microbial rhodopsin, Nat. Plants, 7, 144-151, doi: 10.1038/s41477-021-00853-w.
  161. Oppermann, J., Fischer, P., Silapetere, A., Liepe, B., Rodriguez-Rozada, S., Flores-Uribe, J., Peter, E., Keidel, A., Vierock, J., Kaufmann, J., Broser, M., Luck, M., Bartl, F., Hildebrandt, P., Simon Wiegert, J., Beja, O., Hegemann, P., and Wietek, J. (2019) MerMAIDs: a family of metagenomically discovered marine anion-conducting and intensely desensitizing channelrhodopsins, Nat. Commun., 10, 3315, doi: 10.1038/s41467-019-11322-6.
  162. Malyshev, A. Y., Roshchin, M. V., Smirnova, G. R., Dolgikh, D. A., Balaban, P. M., and Ostrovsky, M. A. (2017) Chloride conducting light activated channel GtACR2 can produce both cessation of firing and generation of action potentials in cortical neurons in response to light, Neurosci. Lett., 640, 76-80, doi: 10.1016/j.neulet.2017.01.026.
  163. Messier, J. E., Chen, H., Cai, Z. L., and Xue, M. (2018) Targeting light-gated chloride channels to neuronal somatodendritic domain reduces their excitatory effect in the axon, Elife, 7, e38506, doi: 10.7554/eLife.38506.
  164. Mahn, M., Prigge, M., Ron, S., Levy, R., and Yizhar, O. (2016) Biophysical constraints of optogenetic inhibition at presynaptic terminals, Nat. Neurosci., 19, 554-556, doi: 10.1038/nn.4266.
  165. Mahn, M., Gibor, L., Patil, P., Cohen-Kashi Malina, K., Oring, S., Printz, Y., Levy, R., Lampl, I., and Yizhar, O. (2018) High-efficiency optogenetic silencing with soma-targeted anion-conducting channelrhodopsins, Nat. Commun., 9, 4125, doi: 10.1038/s41467-018-06511-8.
  166. Mardinly, A. R., Oldenburg, I. A., Pegard, N. C., Sridharan, S., Lyall, E. H., Chesnov, K., Brohawn, S. G., Waller, L., and Adesnik, H. (2018) Precise multimodal optical control of neural ensemble activity, Nat. Neurosci., 21, 881-893, doi: 10.1038/s41593-018-0139-8.
  167. Vierock, J., Peter, E., Grimm, C., Rozenberg, A., Chen, I. W., Tillert, L., Castro Scalise, A. G., Casini, M., Augustin, S., Tanese, D., Forget, B. C., Peyronnet, R., Schneider-Warme, F., Emiliani, V., Béjà, O., and Hegemann, P. (2022) WiChR, a highly potassium selective channelrhodopsin for low-light one- and two-photon inhibition of excitable cells, Sci. Adv., 8, eadd7729, doi: 10.1126/sciadv.add7729.
  168. Govorunova, E. G., Sineshchekov, O. A., Brown, L. S., Bondar, A. N., and Spudich, J. L. (2022) Structural foundations of potassium selectivity in channelrhodopsins, mBio, 13, e0303922, doi: 10.1128/mbio.03039-22.
  169. Fan, L. Z., Kim, D. K., Jennings, J. H., Tian, H., Wang, P. Y., Ramakrishnan, C., Randles, S., Sun, Y., Thadhani, E., Kim, Y. S., Quirin, S., Giocomo, L., Cohen, A. E., and Deisseroth, K. (2023) All-optical physiology resolves a synaptic basis for behavioral timescale plasticity, Cell, 186, 543-559, doi: 10.1016/j.cell.2022.12.035.

Copyright (c) 2023 Russian Academy of Sciences

This website uses cookies

You consent to our cookies if you continue to use our website.

About Cookies