Microbial opsins: a family of single-component tools for optical control of neural activity.

Members of the microbial opsin gene family have emerged recently as crucial tools for “optogenetics,” a new neuroscience technology. “Optogenetics” can be defined as the integration of optics and genetics to control well-defined events (such as action potentials) within specified cells (such as a targeted class of projection neurons) in living tissues (such as the brains of freely behaving mammals). In this article, we focus on the diversity of the microbial opsin genes and the structure–function properties of their corresponding proteins.

[1]  György Váró,et al.  Characterization of the photochemical reaction cycle of proteorhodopsin. , 2003, Biophysical journal.

[2]  J. Spudich The multitalented microbial sensory rhodopsins. , 2006, Trends in microbiology.

[3]  H. Sass,et al.  Structure, dynamics, and function of bacteriorhodopsin. , 1998, Journal of protein chemistry.

[4]  Peter Hegemann,et al.  The branched photocycle of the slow-cycling channelrhodopsin-2 mutant C128T. , 2010, Journal of molecular biology.

[5]  Peter Hegemann,et al.  Algal sensory photoreceptors. , 2008, Annual review of plant biology.

[6]  H. Fukuzawa,et al.  Archaeal-type rhodopsins in Chlamydomonas: model structure and intracellular localization. , 2003, Biochemical and biophysical research communications.

[7]  G. Feng,et al.  Next-Generation Optical Technologies for Illuminating Genetically Targeted Brain Circuits , 2006, The Journal of Neuroscience.

[8]  P. Scheerer,et al.  A G protein-coupled receptor at work: the rhodopsin model. , 2009, Trends in biochemical sciences.

[9]  N. Kamo,et al.  Evidence that the long-lifetime photointermediate of s-rhodopsin is a receptor for negative phototaxis in Halobacterium halobium. , 1985, Biochemical and biophysical research communications.

[10]  P. Hegemann,et al.  The photocycle of the chloride pump halorhodopsin. II: Quantum yields and a kinetic model , 1985, The EMBO journal.

[11]  K. Deisseroth,et al.  Millisecond-timescale, genetically targeted optical control of neural activity , 2005, Nature Neuroscience.

[12]  E. Bamberg,et al.  Channelrhodopsin-2 is a leaky proton pump , 2009, Proceedings of the National Academy of Sciences.

[13]  E. Bamberg,et al.  Channelrhodopsin-1: A Light-Gated Proton Channel in Green Algae , 2002, Science.

[14]  M. Engelhard,et al.  Blue halorhodopsin from Natronobacterium pharaonis: wavelength regulation by anions. , 1994, Biochemistry.

[15]  E. Bamberg,et al.  Different modes of proton translocation by sensory rhodopsin I. , 1996, The EMBO journal.

[16]  S. Waschuk,et al.  Screening and characterization of proteorhodopsin color-tuning mutations in Escherichia coli with endogenous retinal synthesis. , 2008, Biochimica et biophysica acta.

[17]  P. Hegemann,et al.  The Photoreceptor Current of the Green Alga Chlamydomonas , 1992 .

[18]  Michael A. Henninger,et al.  High-Performance Genetically Targetable Optical Neural Silencing via Light-Driven Proton Pumps , 2010 .

[19]  B. Schobert,et al.  Halorhodopsin is a light-driven chloride pump. , 1982, The Journal of biological chemistry.

[20]  W. Stoeckenius,et al.  Photoreactions of bacteriorhodopsin , 1977, Biophysics of structure and mechanism.

[21]  H Luecke,et al.  Structure of bacteriorhodopsin at 1.55 A resolution. , 1999, Journal of molecular biology.

[22]  W. Stoeckenius,et al.  Reconstitution of purple membrane vesicles catalyzing light-driven proton uptake and adenosine triphosphate formation. , 1974, The Journal of biological chemistry.

[23]  Feng Zhang,et al.  Multimodal fast optical interrogation of neural circuitry , 2007, Nature.

[24]  D. Oesterhelt,et al.  Rhodopsin-like protein from the purple membrane of Halobacterium halobium. , 1971, Nature: New biology.

[25]  J. Spudich,et al.  Demonstration of 2:2 stoichiometry in the functional SRI-HtrI signaling complex in Halobacterium membranes by gene fusion analysis. , 2002, Biochemistry.

[26]  I. Kevrekidis,et al.  Optical imaging and control of genetically designated neurons in functioning circuits. , 2005, Annual review of neuroscience.

[27]  K. Deisseroth,et al.  Red-shifted optogenetic excitation: a tool for fast neural control derived from Volvox carteri , 2008, Nature Neuroscience.

[28]  B. Hess,et al.  Reversible photolysis of the purple complex in the purple membrane of Halobacterium halobium. , 1973, European journal of biochemistry.

[29]  E. Bamberg,et al.  Channelrhodopsin-2, a directly light-gated cation-selective membrane channel , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[30]  E. Bamberg,et al.  Light Activation of Channelrhodopsin-2 in Excitable Cells of Caenorhabditis elegans Triggers Rapid Behavioral Responses , 2005, Current Biology.

[31]  Y. Shichida,et al.  Diversity of visual pigments from the viewpoint of G protein activation—comparison with other G protein-coupled receptors , 2003, Photochemical & photobiological sciences : Official journal of the European Photochemistry Association and the European Society for Photobiology.

[32]  Michael Z. Lin,et al.  Characterization of engineered channelrhodopsin variants with improved properties and kinetics. , 2009, Biophysical journal.

[33]  Peter Hegemann,et al.  Channelrhodopsins of Volvox carteri Are Photochromic Proteins That Are Specifically Expressed in Somatic Cells under Control of Light, Temperature, and the Sex Inducer[C][W] , 2009, Plant Physiology.

[34]  Raag D. Airan,et al.  Temporally precise in vivo control of intracellular signalling , 2009, Nature.

[35]  Ernst Bamberg,et al.  Spectral characteristics of the photocycle of channelrhodopsin-2 and its implication for channel function. , 2008, Journal of molecular biology.

[36]  Itai Sharon,et al.  Widespread distribution of proteorhodopsins in freshwater and brackish ecosystems , 2010, The ISME Journal.

[37]  N. Dencher,et al.  Two photosystems controlling behavioural responses of Halobacterium halobium , 1975, Nature.

[38]  K. Deisseroth,et al.  Neural substrates of awakening probed with optogenetic control of hypocretin neurons , 2007, Nature.

[39]  E. Querol,et al.  Thr-90 Plays a Vital Role in the Structure and Function of Bacteriorhodopsin* , 2004, Journal of Biological Chemistry.

[40]  Thomas G. Oertner,et al.  Temporal Control of Immediate Early Gene Induction by Light , 2009, PloS one.

[41]  Y. Mukohata,et al.  Two possible roles of bacteriorhodopsin; a comparative study of strains of Halobacterium halobium differing in pigmentation. , 1977, Biochemical and biophysical research communications.

[42]  Murtaza Z Mogri,et al.  Targeting and Readout Strategies for Fast Optical Neural Control In Vitro and In Vivo , 2007, The Journal of Neuroscience.

[43]  D. Oesterhelt,et al.  Structure of the light-driven chloride pump halorhodopsin at 1.8 A resolution. , 2000, Science.

[44]  D. Oesterhelt,et al.  Light‐induced changes of the pH gradient and the membrane potential in H. halobium , 1976, FEBS letters.

[45]  Lars-Oliver Essen,et al.  Halorhodopsin: light-driven ion pumping made simple? , 2002, Current opinion in structural biology.

[46]  O. Béjà,et al.  Adaptation and spectral tuning in divergent marine proteorhodopsins from the eastern Mediterranean and the Sargasso Seas , 2007, The ISME Journal.

[47]  J. Spudich Variations on a molecular switch: transport and sensory signalling by archaeal rhodopsins , 1998, Molecular microbiology.

[48]  Oleg A. Sineshchekov,et al.  Two rhodopsins mediate phototaxis to low- and high-intensity light in Chlamydomonas reinhardtii , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[49]  T. Sakmar,et al.  Structure of rhodopsin and the superfamily of seven-helical receptors: the same and not the same. , 2002, Current opinion in cell biology.

[50]  T. Ishizuka,et al.  Molecular Determinants Differentiating Photocurrent Properties of Two Channelrhodopsins from Chlamydomonas* , 2009, Journal of Biological Chemistry.

[51]  K. Deisseroth,et al.  Bi-stable neural state switches , 2009, Nature Neuroscience.

[52]  Marion Leclerc,et al.  Proteorhodopsin phototrophy in the ocean , 2001, Nature.

[53]  D. Tank,et al.  Two-photon excitation of channelrhodopsin-2 at saturation , 2009, Proceedings of the National Academy of Sciences.

[54]  Dirk Trauner,et al.  Photochemical tools for remote control of ion channels in excitable cells , 2005, Nature chemical biology.

[55]  H. Chiel,et al.  Fast noninvasive activation and inhibition of neural and network activity by vertebrate rhodopsin and green algae channelrhodopsin. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[56]  Oliver P. Ernst,et al.  Channelrhodopsin-1 Initiates Phototaxis and Photophobic Responses in Chlamydomonas by Immediate Light-Induced Depolarization[W] , 2008, The Plant Cell Online.

[57]  Peter Hegemann,et al.  Glu 87 of Channelrhodopsin‐1 Causes pH‐dependent Color Tuning and Fast Photocurrent Inactivation † , 2009, Photochemistry and photobiology.

[58]  Peter Hegemann,et al.  Monitoring Light-induced Structural Changes of Channelrhodopsin-2 by UV-visible and Fourier Transform Infrared Spectroscopy* , 2008, Journal of Biological Chemistry.

[59]  T. Ishizuka,et al.  Kinetic evaluation of photosensitivity in genetically engineered neurons expressing green algae light-gated channels , 2006, Neuroscience Research.

[60]  R B Rose,et al.  Structure of an early intermediate in the M-state phase of the bacteriorhodopsin photocycle. , 2001, Biophysical journal.

[61]  K. Deisseroth,et al.  eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications , 2008, Brain cell biology.

[62]  Oded Béjà,et al.  Diversification and spectral tuning in marine proteorhodopsins , 2003, The EMBO journal.

[63]  J. Spudich,et al.  Mechanism of colour discrimination by a bacterial sensory rhodopsin , 1984, Nature.

[64]  J. Spudich,et al.  Spectroscopic and Photochemical Characterization of a Deep Ocean Proteorhodopsin* , 2003, Journal of Biological Chemistry.

[65]  E. Bamberg,et al.  General concept for ion translocation by halobacterial retinal proteins: the isomerization/switch/transfer (IST) model. , 1997, Biochemistry.

[66]  H. Kandori,et al.  Color-changing mutation in the E-F loop of proteorhodopsin. , 2009, Biochemistry.

[67]  E. Bamberg,et al.  The voltage-dependent proton pumping in bacteriorhodopsin is characterized by optoelectric behavior. , 2001, Biophysical journal.

[68]  Ernst Bamberg,et al.  Conformational changes of channelrhodopsin-2. , 2009, Journal of the American Chemical Society.

[69]  E. Bamberg,et al.  Voltage- and pH-dependent changes in vectoriality of photocurrents mediated by wild-type and mutant proteorhodopsins upon expression in Xenopus oocytes. , 2009, Journal of molecular biology.