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Optogenetics: 10 Years of Microbial Opsins in Neuroscience

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Optogenetics: 10 Years of Microbial Opsins in Neuroscience HISTORICAL COMMENTARY Optogenetics: 10 years of microbial opsins in neuroscience Karl Deisseroth Over the past 10 years, the development and convergence of microbial opsin engineering, modular genetic methods for cell-type targeting and optical strategies for guiding light through tissue have enabled versatile optical control of defined cells in living systems, defining modern optogenetics. Despite widespread recognition of the importance of spatiotemporally precise causal control over cellular signaling, for nearly the first half (2005–2009) of this 10-year period, as optogenetics was being created, there were difficulties in implementation, few publications and limited biological findings. In contrast, the ensuing years have witnessed a substantial acceleration in the application domain, with the publication of thousands of discoveries and insights into the function of nervous systems and beyond. This Historical Commentary reflects on the scientific landscape of this decade-long transition. Optogenetics is the combination of genetic cross-integration that enabled optogenetics functionally completely distinct from (and and optical methods to cause or inhibit well- over the past 10 years only became possible unrelated in primary sequence to) the defined events in specific cells of living tissue under the right conditions. Each component better-known rhodopsins that mediate pho- and behaving animals1. This technology, as also continues to rapidly evolve for greater totransduction in the vertebrate eye6. Indeed, employed today to study the neural circuit precision and complexity. Indeed, these the initial evidence from Oesterhelt and underpinnings of behavior, most commonly fundamental elements of optogenetics are Stoeckenius, beginning in 1971, that micro- involves three core features: (i) microbial increasingly recruiting and bringing to bear bial organisms might also produce and use opsins, members of an ancient, but uniquely more branches of science and engineering, rhodopsin-like proteins7 was surprising and well-suited, gene family adapted from evolu- ranging from computational tools for system intriguing. Instead of coupling to intracellu- tionarily distant organisms such as algae and identification to automated optical readouts of lar second-messenger cascades to indirectly archaebacteria, with each gene encoding a behavior and neural activity to high-content influence ion channels, like their vertebrate distinct protein that directly elicits electrical anatomical data extraction methods for dis- counterparts, these microbial proteins for the current across cellular membranes in response covering structural and wiring relationships4. most part directly transduce photons into elec- to light, (ii) general methods for targeting suf- The most recent technological develop- trical current (Fig. 1a,b). This molecular feat ficiently strong and specific opsin gene expres- ments, along with experimental guidelines, provoked intense curiosity and has inspired sion to well-defined cellular elements in the challenges and limitations, have already been thousands of investigations over the decades5. brain, and (iii) general methods for guiding reviewed in detail this year4. In the present Indeed, within a few years, this discovery had sufficiently strong and precisely timed light Historical Commentary, I focus on the opto- given birth to a vibrant community that pro- to specific brain regions, cells or parts of cells genetic transition itself over the past 10 years, duced a steady output of about 100 papers while the experimental subject carries out from scientific conditions surrounding the annually for four decades extending to the behaviors of interest. early work to the major discoveries that have present day, spanning genomic, functional and None of these three components was arisen with application of this technology over structural investigations into the photocycles enabled for general optogenetic discovery the same time period, all set in the context of and mechanisms of these microbial proteins, in neuroscience 10 years ago2, or even when the development of three converging disci- and defining part of the textbook training of we suggested the new word to describe this plines that could hardly be more disparate in biologists8. emerging process a year later3, but each has origin and tradition. Three branches of this family tree have scientific origins dating back decades. The found utility in optogenetics: the bacteriorho- Developing and assembling the dopsins, the halorhodopsins and the channel- Karl Deisseroth is in the Departments of components of optogenetics rhodopsins (Fig. 1a). The naturally occurring Bioengineering and of Psychiatry and Behavioral The first of these three components has been bacteriorhodopsins (the first- discovered Sciences and the Howard Hughes Medical part of the fabric of biochemistry and physi- members of this family, which pump protons Institute, Stanford University, Stanford, California, ology for many decades: the microbial opsin out of the cell) and halorhodopsins (which USA. genes and the microbial rhodopsin proteins pump chloride ions into the cell) are typi- e-mail: [email protected] they encode5, a family of molecules (Fig. 1a) cally inhibitory in neural systems, as both of NATURE NEUROSCIENCE VOLUME 18 | NUMBER 9 | SEPTEMBER 2015 1213 HISTORICAL COMMENTARY were possible in adult non- retinal brain tis- + a Bacteriorhodopsin Halorhodopsin Channelrhodopsin b H sue, and even in the event of safe and correct 5 trafficking of these evolutionarily remote D96 proteins to the surface membrane of complex hν metazoan neurons. For these weak membrane 4 1 conductance regulators to work, high gene- 2 D85 expression and light-intensity levels would D212 7 R82 have to be attained in living nervous systems PRC 6 while simultaneously attaining cell-type speci- 3 ficity and minimizing cellular toxicity. All of + + + 2+ + H H+ Cl– Na , K , Ca , H this would have to be achieved even though neurons were well known to be highly vulner- All-trans retinal chromophore able to (and often damaged or destroyed by) c d overexpression of membrane proteins, as well 40 μm as sensitive to side effects of heat and light. H134R Motivating dedicated effort to exploration of N297Q microbial opsin-based optical control was dif- E129S BR-EYFP BR-TS-EYFP ficult in the face of these multiple unsolved T98S 10 μm problems, and the dimmest initial sparks of E162S T285N hope would turn out to mean a great deal. E140S V156K Outside neuroscience, several examples of V281K BR-TS-EYFP-ER (eBR) functional heterologous expression of opsins for light-activated ion flow had been pub- Figure 1 The biochemical foundations of the study of microbial light-activated proteins. (a) The three major classes of microbial proteins used for single-component optogenetics (adapted from ref. 5, lished in non-neural isolated-cell systems 14–16 14 Elsevier). (b) Light-activated transmembrane current mechanism of the proton pump bacteriorhodopsin for microbial opsins (beginning in the 17 (BR)5. Photon (hν) absorption initiates a conformational switch, leading to discontinuous proton early 1990s) or vertebrate opsins (beginning transfers involving Asp85, Asp96, Asp212, Arg82 and the proton release complex (PRC), and net in the late 1980s), although neuroscience or charge movement across the membrane. The core concept of single-component light-activated behavior applications were not suggested. It 8 transmembrane ion conductance had become textbook material by the 1980s (reproduced from is not known how many investigators actually ref. 5, Elsevier). (c) Elucidation of channel-type conductance. The channelrhodopsin crystal structure9 did attempt to transduce microbial opsins revealed positioning of transmembrane helices (green), the binding pocket of all-trans retinal (purple), and angstrom-scale positioning of residues lining the pore (left). In the course of testing into neurons before 2005, but even in this the pore model, structure-guided mutagenesis10 of the residues in orange (left) shifted expected one step, among the many steps required for pore electrostatics from largely negative (red, center) to largely positive (blue, right) and switched optogenetics, much can go wrong18 (Fig. 1d). ion selectivity from cation to anion (chloride) conductance13. (d) All three classes of microbial Meanwhile, over the years leading up to 2005, opsin–derived proteins suffer to some degree from formation of aggregations within metazoan host several other strategies for optical control of 18,50,51 cells , but in all cases this can be addressed with membrane trafficking motifs borrowed from targeted neurons, involving multiple simulta- mammalian channels18,50,51,90. Shown: original BR fused to enhanced yellow fluorescent protein (EYFP); upper left depicts accumulations seen with wild-type BR expression in mammalian neurons, neously delivered metazoan genes or coordi- upper right shows the effect on surface membrane expression of adding a neurite targeting motif (TS), nated delivery of both a metazoan gene and and the lower row shows the effect of combined TS and ER (endoplasmic reticulum export) motif a light-sensitive synthesized chemical, were provision (reproduced from ref. 18, Elsevier). devised19–23, perhaps by their very elegance reducing enthusiasm for another approach based entirely on a family of far more foreign these types of hyperpolarizing current make diversity is now leveraged to powerful effect microbial proteins that would seem much less it harder
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