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Problems and outlooks of optogenetic technologies in the 21st century

[Reviews]
Irina Ivanovna Fomochkina; Leya Evgenievna Sorokina; Vitalina Igorevna Petrenko; Alexander Sergeevich Kucherenko; Server Iskanderovich Halilov; Anatoly Vladimirovich Kubyshkin; Mikhail Vladimirovich Subbotkin; Alina Alekseevna Kulanova;

Optogenetics is an innovative scientific trend, had developed in the 21st century as the integration of genetic engineering and advanced laser technologies to study the functioning of the human organism, diagnostics, and therapy of socially significant diseases. This work represents modern information and outlooks of optogenetics achievements to solve a wide range of biomedical problems. The review contains a description of the main methods of delivery, incorporation, and control of the expression of photosensitive proteins on the cell membrane. There are described characteristics of the physical and technical side of the optogenetic experiment, are indicated the key advantages and disadvantages of various techniques. The
main difficulties of optogenetic technologies, examples of technical solutions for optostimulation and registration of cellular
activity synchronically are described.

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References:
1. Deisseroth K., Feng G., Majewska A. K., Miesenböck G., Ting A. [et al.] Next-generation optical technologies for illuminating genetically targeted brain circuits. Journal of Neuroscience. 2006;26(41):10380-10386. https://doi.org/10.1523/JNEUROSCI.3863-06.2006
2. Nagel G., Szellas T., Huhn W., Kateriya S., Adeishvili N. [et al.] Channelrhodopsin-2, a directly light-gated cation-selective membrane channel. PNAS. 2003;100(24):13940-13945. https://doi.org/10.1073/pnas.1936192100
3. Boyden E. S., Zhang F., Bamberg E., Nagel G., Deisseroth K. Millisecond-timescale, genetically targeted optical control of neural activity. Nature Neuroscience. 2005;8(9):1263-1268. https://doi.org/10.1038/nn1525
4. Imamura H., Nhat K. P. H., Togawa H., Saito K., Iino R. [et al.] Visualization of ATP levels inside single living cells with fluorescence resonance energy transfer-based genetically encoded indicators. PNAS. 2009;106(37):15651-15656. https://doi.org/10.1073/pnas.0904764106
5. Zaglia T., Di Bona A., Mongillo M. A. Light Wand to Untangle the Myocardial Cell Network. Methods & Protocols. 2019;2(2):34-36. https://doi.org/10.3390/mps2020034
6. Yizhar O., Fenno L., Zhang F., Hegemann P., Diesseroth K. Microbial opsins: a family of single-component tools for optical control of neural activity. Cold Spring Harbor Protocols. 2011;3:102. https://doi.org/10.1101/pdb.top102
7. Sakmar T. P. Structure of rhodopsin and the superfamily of seven-helical receptors: the same and not the same. Current Opinion in Cell Biology. 2002;14(2):189-195. https://doi.org/10.1016/S0955-0674(02)00306-X
8. Shichida Y., Yamashita T. Diversity of visual pigments from the viewpoint of G protein activation – comparison with other G protein-coupled receptors. Photochemical and Photobiological Sciences: Official Journal of the European
Photochemistry Association and the European Society for Photobiology. 2003;2(12):1237-1246. https://doi.org/10.1039/B300434A
9. Adamantidis A. R., Zhang F., de Lecea L., Deisseroth K. Optogenetics: opsins and optical interfaces in neuroscience. Cold Spring Harbor Protocols. 2014;(8):815-822. https://doi.org/10.1101/pdb.top083329
10. Klapoetke N. C., Murata Y., Kim S. S., Pulver S. R., Birdsey B. [et al.] Independent optical excitation of distinct neural populations. Nature Methods. 2014;11(3):338-346. https://doi.org/10.1038/nmeth.2836
11. Glock C., Nagpal J., Gottschalk A. Microbial rhodopsin optogenetic tools: Application for analyses of synaptic transmission and of neuronal network activity in behavior. Methods in molecular biology. 2015;1327:87-103. https://doi.org/10.1007/978-1-4939-2842-2_8
12. Gradinaru V., Thompson K. R., Zhang F., Mogri M., Kay K. [et al.] Targeting and readout strategies for fast optical neural control in vitro and in vivo. Journal of Neuroscience. 2007;27(52):14231-14238. https://doi.org/10.1523/JNEUROSCI.3578-07.2007
13. Lin J. Y. A user’s guide to channelrhodopsin variants: features, limitations and future developments. Experimental physiology. 2011;96(1):19-25, https://doi.org/10.1113/expphysiol.2009.051961
14. Adamantidis A. R., Zhang F., Aravanis A. M., Deisseroth K., de Lecea L. Neural substrates of awakening probed with optogenetic control of hypocretin neurons.
Nature. 2007;450(7168):420-424. https://doi.org/10.1038/nature06310
15. Yizhar O., Fenno L. E., Davidson T. J., Mogri M., Deisseroth K. Optogenetics in neural systems. Neuron. 2011;71(1): 9-34. https://doi.org/10.1016/j.neuron.2011.06.004
16. Zhang F., Wang L. P., Brauner M., Liewald J. F., Kay K. [et al.] Multimodal fast optical interrogation of neural circuitry. Nature. 2007;446(7136):633-639. https://doi.org/10.1038/nature05744
17. Husson S. J., Liewald J. F., Schultheis C., Stirman J. N., Lu H. [et al.] Microbial light-activatable proton pumps as neuronal inhibitors to functionally dissect neuronal networks in C. elegans. PloS One. 2012;7(7):e40937. https://doi.org/10.1371/journal.pone.0040937
18. Han X., Qian X., Bernstein J. G., Zhou H.-H., Franzes G. T. [et al.] Millisecond-Timescale Optical Control of Neural Dynamics in the Nonhuman Primate Brain. Neuron. 2009;62(2):191-198. https://doi.org/10.1016/j.neuron.2009.03.011
19. Govorunova E. G., Koppel L. A. The road to optogenetics: microbial rhodopsins. Biochemistry (Mosc). 2016;81(9):928-940. https://doi.org/10.1134/S0006297916090029
20. Airan R. D., Thompson K. R., Fenno L. E. Temporally precise in vivo control of intracellular signalling. Nature. 2009;458:1025-1029. https://doi.org/10.1038/nature07926
21. Witten I. B., Steinberg E. E., Lee S. Y., Davidson T. J., Zalocusky K. [et al.] Recombinase-Driver Rat Lines: Tools, Techniques, and Optogenetic Application to Dopamine-Mediated Reinforcement. Neuron. 2011;72(5):721-733. https://doi.org/10.1016/j.neuron.2011.10.028
22. Madisen L., Mao T., Koch H., Zhuo J.-M., Berenyi A. [et al.] A toolbox of Cre-dependent optogenetic transgenic mice for light-induced activation and silencing. Nature Neuroscience. 2012;15(5):793–802. https://doi.org/10.1038/nn.3078
23. Carter M. E., de Lecea L. Optogenetic investigation of neural circuits in vivo. Trends in molecular medicine. 2011;17(4):197–206. https://doi.org/10.1016/j.molmed.2010.12.005
24. Sizemore R. J., Seeger-Armbruster S., Hughes S. M., ParrBrownlie L. C. Viral vector-based tools advance knowledge of basal ganglia anatomy and physiology.
Journal of Neurophysiology. 2016;115(4):2124-2146. https://doi.org/10.1152/jn.01131.2015
25. Masamizu Y., Okada T., Kawasaki K., Ishibashi H., Yuasa S. [et al.] Local and retrograde gene transfer into primate neuronal pathways via adeno-associated virus
serotype 8 and 9. Neuroscience. 2011;193:249-258. https://doi.org/10.1016/j.neuroscience.2011.06.080
26. Tervo D. G. R., Hwang B.-Y., Viswanathan S., Gaj T., Lavzin M. [et al.] Variant Permits Efficient Retrograde Access to Projection Neurons. Neuron. 2016;92(2):372-382. https://doi.org/10.1016/j.neuron.2016.09.021
27. Kühn R., Torres R. M. Cre/loxP Recombination system and gene targeting. Methods in molecular biology. 2002;180:175-204. https://doi.org/10.1385/1-59259-178-7:175
28. Dittgen T., Nimmerjahn A., Komai S., Licznerski P., Waters J. [et al.] Lentivirus-based genetic manipulations of cortical neurons and their optical and electrophysiological monitoring in vivo. PNAS. 2004;101(52):18206-18211. https://doi.org/10.1073/pnas.0407976101
29. Kim J. Y., Ash R. T., Ceballos-Diaz C., Levites Y., Golde T. E. [et al.] Viral transduction of the neonatal brain delivers controllable genetic mosaicism for visualising and manipulating neuronal circuits in vivo. The European journal of
neuroscience. 2013;37(8):1203-1220. https://doi.org/10.1111/ejn.12126
30. Arenkiel B. R., Peca J., Davison I. G. In vivo light-induced activation of neural circuitry in transgenic mice expressing channelrhodopsin-2. Neuron. 2007;54(2):205-218. https://doi.org/10.1016/j.neuron.2007.03.005
31. Zeng H., Madisen L. Mouse transgenic approaches in optogenetics. Progress in brain research. 2012;196:193-213. https://doi.org/10.1016/B978-0-444-59426-6.00010-0
32. Park J. E., Silva A. C. Generation of genetically engineered non-human primate models of brain function and neurological disorders. American journal of primatology. 2019;81(2):e22931. https://doi.org/10.1002/ajp.22931
33. Bitzenhofer S. H., Ahlbeck J., Wolff A. Layer-specific optogenetic activation of pyramidal neurons causes beta-gamma entrainment of neonatal networks. Nature communications. 2017;8:14563. https://doi.org/10.1038/ncomms14563
34. Warden M. R., Cardin J. A., Deisseroth K. Optical neural interfaces. Annual Review of Biomedical Engineering. 2014;16:103-129. https://doi.org/10.1146/annurev-bioeng-071813-104733
35. Bartic C., Battaglia F. P., Wang L., Nguyen T. T., Cabral H. [et al.] A multichannel recording system with optical stimulation for closed-loop optogenetic experiments. Methods in Molecular Biology. 2016;1408:333-344. https://doi.org/10.1007/978-1-4939-3512-3_23
36. Aravanis A. M., Wang L.-P., Zhang F., Meltzer L. A., Mogri M. Z. [et al.] An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology. Journal of Neural Engineering. 2007;4(3):43-56. https://doi.org/10.1088/1741-2560/4/3/S02
37. Kwon K. Y., Lee H.-M., Ghovanloo M., Weber A., Li W. A wireless slanted optrode array with integrated micro leds for optogenetics. In 2014 IEEE27th International conference on micro electro mechanical systems (MEMS). 2014. https://doi.org/10.1109/memsys.2014.6765765
38. Shin Y., Yoo M., Kim H.-S., Nam S.-K., Kim H.-I. [et al.] Characterization of fiber-optic light delivery and light-induced temperature changes in a rodent brain for precise optogenetic neuromodulation. Biomedical Optics Express. 2016;7(11):4450-4471. https://doi.org/10.1364/OL.37.004841
39. Cardin J. A., Carlén M., Meletis K., Knoblich U., Zhang F. [et al.] Targeted optogenetic stimulation and recording of neurons in vivo using cell-type-specific expression of Channelrhodopsin-2. Nature Protocols. 2010;5(2):247-254, https://doi.org/10.1038/nprot.2009.228
40. Wu F., Stark E., Im M., Cho I. J., Yoon E. S. [et al.] An implantable neural probe with monolithically integrated dielectric waveguide and recording electrodes for optogenetics applications. Journal of Neural Engineering. 2013;10(5):056012.
https://doi.org/10.1088/1741-2560/10/5/056012
41. Royer S., Zemelman B. V., Barbic M., Losonczy A., Buzsáki G. [et al.] Multi-array silicon probes with integrated optical fibers: light assisted perturbation and recording of local neural circuits in the behaving animal. The European Journal
of Neuroscience. 2010;31(12):2279-2291. https://doi.org/10.1111/j.1460-9568.2010.07250.x
42. Abaya T. V. F., Blair S., Tathireddy P., Rieth L., Solzbacher F. A 3D glass optrode array for optical neural stimulation. Biomedical Optics Express. 2012;3(12):3087-3104. https://doi.org/10.1364/BOE.3.003087
43. Pisanello F., Sileo L., De Vittorio M. Micro- and Nano-technologies for Optical Neural Interfaces. Frontiers in Neuroscience. 2016;10:70. https://doi.org/10.3389/fnins.2016.00070
44. Airan R. D., Thompson K. R., Fenno L. E., Bernstein H., Deisseroth K. Temporally precise in vivo control of intracellular signalling. Nature. 2009;458(7241):1025-1029. ttps://doi.org/10.1038/nature07926
45. Kastanenka K. V., Calvo-Rodriguez M., Hou S. S. Frequency-dependent exacerbation of Alzheimer’s disease neuropathophysiology. Scientific reports. 2019;9(1):8964. https://doi.org/10.1038/s41598-019-44964-z
46. Chen Y., Xiong M., Zhang S. C. Illuminating Parkinson’s therapy with optogenetics. Nature Biotechnology. 2015;33(2):149-150. https://doi.org/10.1038/nbt.3140
47. Krook-Magnuson E., Armstrong C., Oijala M., Soltesz I. On-demand optogenetic control of spontaneous seizures in temporal lobe epilepsy. Nature communications. 2013;4:1376. https://doi.org/10.1038/ncomms2376
48. Touriño C., Eban-Rothschild A., de Lecea L. Optogenetics in psychiatric diseases. Current opinion in neurobiology. 2013;23(3):430-435. https://doi.org/10.1016/j.conb.2013.03.007
49. Deisseroth K. Optogenetics and psychiatry: applications, challenges, and opportunities. Biological psychiatry. 2012;71(12):1030-2. https://doi.org/10.1016/j.biopsych.2011.12.021
50. Tye K. M., Mirzabekov J. J., Warden M. R. Dopamine neurons modulate neural encoding and expression of depression-related behaviour. Nature. 2013; 493(7433): 537–541. https://doi.org/10.1038/nature11740
51. Henriksen B. S., Marc R. E., Bernstein P. S. Optogenetics for retinal disorders. Journal of ophthalmic and vision research. 2014;9(3):374-38, https://doi.org/10.4103/2008-322X.143379
52. Berry M. H., Holt A., Salari A. Restoration of high-sensitivity and adapting vision with a cone opsin. Nature communications. 2019;10(1):1221. https://doi.org/10.1038/s41467-019-09124-x
53. Ganjawala T. H., Lu Q., Fenner M. D., Abrams G. W., Pan Z. H. Improved CoChR Variants Restore Visual Acuity and Contrast Sensitivity in a Mouse Model of Blindness under Ambient Light Conditions. Molecular therapy: the journal of the American Society of Gene Therapy. 2019;27(6):1195- 1205. https://doi.org/10.1016/j.ymthe.2019.04.002
54. Berry M. H., Holt A., Salari A. Restoration of high-sensitivity and adapting vision with a cone opsin. Nature communications. 2019;10(1):1221. https://doi.org/10.1038/s41467-019-09124-x
55. Yu L., Zhou L., Cao G. Optogenetic Modulation of Cardiac Sympathetic Nerve Activity to Prevent Ventricular Arrhythmias. Journal of the American College of Cardiology. 2017;70(22):2778-2790. https://doi.org/10.1016/j.jacc.2017.09.1107
56. Majumder R., Feola I., Teplenin A. S., de Vries A. A., Panfilov A. V. [et al.] Optogenetics enables real-time spatiotemporal control over spiral wave dynamics in an excitable cardiac system. Elife. 2018;7:e41076. https://doi.org/10.7554/eLife.41076
57. Cheng Y., Li H., Lei H. Flexible and precise control of cardiac rhythm with blue light. Biochemical and biophysical research communications. 2019;514(3):759-764. https://doi.org/10.1016/j.bbrc.2019.05.035
58. Ye H., Daoud E., Baba M., Peng R. W., Fussenegger M. A synthetic optogenetic transcription device enhances blood-glucose homeostasis in mice. Science. 2011;332(6037):1565-8. https://doi.org/10.1126/science.1203535
59. Shao J., Xue S., Yu G. Smartphone-controlled optogenetically engineered cells enable semiautomatic glucose homeostasis in diabetic mice. Science translational medicine. 2017;9(387):eaal2298. https://doi.org/10.1126/scitranslmed.aal2298
60. Mohanty S. K., Lakshminarayananan V. Optical Techniques in Optogenetics. Journal of modern optics. 2015;62(12):949–970. https://doi.org/10.1080/09500340.2015.1010620
61. Kravitz A. V., Bonci A. Optogenetics, physiology, and emotions. Frontiers in behavioral neuroscience. 2013;7:169. https://doi.org/10.3389/fnbeh.2013.00169.89
62. Packer A. M., Roska B., Häusser M. Targeting neurons and photons for optogenetics. Nature neuroscience. 2013;16(7):805-815. https://doi.org/10.1038/nn.3427

Keywords: optogenetics, opsins, ion channels, fiber optic systems, photostimulation


Founders:
Stavropol State Medical Academy
Pyatigorsk State Research Institute of Balneotherapeutics
Pyatigorsk State Pharmaceutical Academy