Optical techniques in optogenetics

Optogenetics is an innovative technique for optical control of cells. This field has exploded over the past decade or so and has given rise to great advances in neuroscience. A variety of applications both from the basic and applied research have emerged, turning the early ideas into a powerful paradigm for cell biology, neuroscience, and medical research. This review aims at highlighting the basic concepts that are essential for a comprehensive understanding of optogenetics and some important biological/biomedical applications. Further, emphasis is placed on advancement in optogenetics-associated light-based methods for controlling gene expression, spatially controlled optogenetic stimulation and detection of cellular activities.

[1]  Mary Rowell,et al.  Attitudes Regarding Predictive Testing for Retinitis Pigmentosa , 2007, Ophthalmic genetics.

[2]  A. Vogel,et al.  Mechanisms of femtosecond laser nanosurgery of cells and tissues , 2005 .

[3]  Hajime Takano,et al.  Region-directed phototransfection reveals the functional significance of a dendritically synthesized transcription factor , 2006, Nature Methods.

[4]  Kishan Dholakia,et al.  Femtosecond cellular transfection using a nondiffracting light beam , 2007 .

[5]  Tahei Tahara,et al.  Two-photon absorption spectrum of all-trans retinal , 2003 .

[6]  Eriko Sugano,et al.  Channelrhodopsin-2 gene transduced into retinal ganglion cells restores functional vision in genetically blind rats. , 2010, Experimental eye research.

[7]  Alfred Stett,et al.  Subretinal electronic chips allow blind patients to read letters and combine them to words , 2010, Proceedings of the Royal Society B: Biological Sciences.

[8]  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.

[9]  Lief E. Fenno,et al.  The development and application of optogenetics. , 2011, Annual review of neuroscience.

[10]  Ruikang K. Wang,et al.  Phase-sensitive optical coherence tomography imaging of the tissue motion within the organ of Corti at a subnanometer scale: a preliminary study. , 2010, Journal of biomedical optics.

[11]  A. Welch,et al.  A review of the optical properties of biological tissues , 1990 .

[12]  E. Bamberg,et al.  Ultra light-sensitive and fast neuronal activation with the Ca2+-permeable channelrhodopsin CatCh , 2011, Nature Neuroscience.

[13]  Neal S Peachey,et al.  Subretinal implantation of semiconductor-based photodiodes: durability of novel implant designs. , 2002, Journal of rehabilitation research and development.

[14]  K. Ressler,et al.  Identification of cell-type-specific promoters within the brain using lentiviral vectors , 2007, Gene Therapy.

[15]  Shaochen Chen,et al.  Femtosecond laser-assisted optoporation for drug and gene delivery into single mammalian cells. , 2011, Journal of biomedical nanotechnology.

[16]  S L Jacques,et al.  CONV--convolution for responses to a finite diameter photon beam incident on multi-layered tissues. , 1997, Computer methods and programs in biomedicine.

[17]  L. Fu,et al.  Nonlinear optical endoscopy based on a double-clad photonic crystal fiber and a MEMS mirror. , 2006, Optics express.

[18]  R. Eckmiller Learning retina implants with epiretinal contacts. , 1997, Ophthalmic research.

[19]  Feng Zhang,et al.  Channelrhodopsin-2 and optical control of excitable cells , 2006, Nature Methods.

[20]  Edward S. Boyden,et al.  A history of optogenetics: the development of tools for controlling brain circuits with light , 2011, F1000 biology reports.

[21]  K. Deisseroth,et al.  Orderly recruitment of motor units under optical control in vivo , 2010, Nature Medicine.

[22]  B. Kuhlman,et al.  A genetically-encoded photoactivatable Rac controls the motility of living cells , 2009, Nature.

[23]  K. Deisseroth,et al.  Molecular and Cellular Approaches for Diversifying and Extending Optogenetics , 2010, Cell.

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

[25]  Peter Gehlbach,et al.  Intraocular adenoviral vector-mediated gene transfer in proliferative retinopathies. , 2002, Investigative ophthalmology & visual science.

[26]  D. Oesterhelt,et al.  The structure and mechanism of the family of retinal proteins from halophilic archaea. , 1998, Current opinion in structural biology.

[27]  J. Johansson,et al.  Spectroscopic method for determination of the absorption coefficient in brain tissue. , 2010, Journal of biomedical optics.

[28]  Ling Gu,et al.  Correlation of spatial intensity distribution of light reaching the retina and restoration of vision by optogenetic stimulation , 2011, BiOS.

[29]  Arup Roy,et al.  Factors affecting perceptual thresholds in epiretinal prostheses. , 2008, Investigative ophthalmology & visual science.

[30]  L. Misoguti,et al.  Degenerate two-photon absorption in all-trans retinal: nonlinear spectrum and theoretical calculations. , 2010, The journal of physical chemistry. A.

[31]  M. Berns,et al.  In-depth activation of channelrhodopsin 2-sensitized excitable cells with high spatial resolution using two-photon excitation with a near-infrared laser microbeam. , 2008, Biophysical journal.

[32]  Y Mitamura,et al.  Relationship between peripheral visual field loss and vision-related quality of life in patients with retinitis pigmentosa , 2010, Eye.

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

[34]  E. Isacoff,et al.  Scanless two-photon excitation of channelrhodopsin-2 , 2010, Nature Methods.

[35]  Andreas Möglich,et al.  From dusk till dawn: one-plasmid systems for light-regulated gene expression. , 2012, Journal of molecular biology.

[36]  Konrad Lehmann,et al.  Visual Function in Mice with Photoreceptor Degeneration and Transgenic Expression of Channelrhodopsin 2 in Ganglion Cells , 2010, The Journal of Neuroscience.

[37]  Jacob G. Bernstein,et al.  Millisecond-Timescale Optical Control of Neural Dynamics in the Nonhuman Primate Brain , 2009, Neuron.

[38]  Artium Khatchatouriants,et al.  Femtosecond infrared laser-an efficient and safe in vivo gene delivery system for prolonged expression. , 2003, Molecular therapy : the journal of the American Society of Gene Therapy.

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

[40]  D. Boas,et al.  Three dimensional Monte Carlo code for photon migration through complex heterogeneous media including the adult human head. , 2002, Optics express.

[41]  Ling Gu,et al.  Targeted microinjection into cells and retina using optoporation. , 2011, Journal of biomedical optics.

[42]  Karl Deisseroth,et al.  Optogenetics in Neural Systems , 2011, Neuron.

[43]  Hideaki E. Kato,et al.  Crystal structure of the channelrhodopsin light-gated cation channel , 2012, Nature.

[44]  Hung Cao,et al.  An Integrated μLED Optrode for Optogenetic Stimulation and Electrical Recording , 2013, IEEE Transactions on Biomedical Engineering.

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

[46]  Erika Pastrana,et al.  Optogenetics: controlling cell function with light , 2011, Nature Methods.

[47]  Feng Zhang,et al.  Molecular Tools and Approaches for Optogenetics , 2012, Biological Psychiatry.

[48]  Zhuo-Hua Pan,et al.  Ectopic Expression of Multiple Microbial Rhodopsins Restores ON and OFF Light Responses in Retinas with Photoreceptor Degeneration , 2009, The Journal of Neuroscience.

[49]  Garret D Stuber,et al.  Dissecting the neural circuitry of addiction and psychiatric disease with optogenetics , 2010, Neuropsychopharmacology.

[50]  M. Berns,et al.  Direct gene transfer into human cultured cells facilitated by laser micropuncture of the cell membrane. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[51]  Josiah P. Zayner,et al.  TULIPs: Tunable, light-controlled interacting protein tags for cell biology , 2012, Nature Methods.

[52]  Pavel Osten,et al.  Stereotaxic gene delivery in the rodent brain , 2007, Nature Protocols.

[53]  Ingrid Wilke,et al.  Laser intensity dependence of femtosecond near-infrared optoinjection. , 2007, Physical review. E, Statistical, nonlinear, and soft matter physics.

[54]  Zeger Debyser,et al.  Comparative analysis of adeno-associated viral vector serotypes 1, 2, 5, 7, and 8 in mouse brain. , 2007, Human gene therapy.

[55]  Murtaza Z Mogri,et al.  Cell Type–Specific Loss of BDNF Signaling Mimics Optogenetic Control of Cocaine Reward , 2010, Science.

[56]  B. Zemelman,et al.  Selective Photostimulation of Genetically ChARGed Neurons , 2002, Neuron.

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

[58]  Rafael Yuste,et al.  Two-photon optogenetics of dendritic spines and neural circuits in 3D , 2012, Nature Methods.

[59]  Ming Lei,et al.  Femtosecond laser-assisted microinjection into living neurons , 2008, Journal of Neuroscience Methods.

[60]  Sreekanth H. Chalasani,et al.  Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators , 2009, Nature Methods.

[61]  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.

[62]  D. Kleinfeld,et al.  ReaChR: A red-shifted variant of channelrhodopsin enables deep transcranial optogenetic excitation , 2013, Nature Neuroscience.

[63]  Toru Ishizuka,et al.  Visual Properties of Transgenic Rats Harboring the Channelrhodopsin-2 Gene Regulated by the Thy-1.2 Promoter , 2009, PloS one.

[64]  Douglas S Kim,et al.  Light-activated channels targeted to ON bipolar cells restore visual function in retinal degeneration , 2008, Nature Neuroscience.

[65]  Greg Miller,et al.  Shining New Light on Neural Circuits , 2006, Science.

[66]  Mark S Humayun,et al.  Predicting visual sensitivity in retinal prosthesis patients. , 2009, Investigative ophthalmology & visual science.

[67]  B. Zemelman,et al.  Two-photon single-cell optogenetic control of neuronal activity by sculpted light , 2010, Proceedings of the National Academy of Sciences.

[68]  Patrick Degenaar,et al.  Multi-site optical excitation using ChR2 and micro-LED array , 2010, Journal of neural engineering.

[69]  X. Breakefield,et al.  Viral vectors for gene delivery to the nervous system , 2003, Nature Reviews Neuroscience.

[70]  B Agate,et al.  Femtosecond optical transfection of cells: viability and efficiency. , 2006, Optics express.

[71]  E. Boyden,et al.  Multiple-Color Optical Activation, Silencing, and Desynchronization of Neural Activity, with Single-Spike Temporal Resolution , 2007, PloS one.

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

[73]  Ian R. Wickersham,et al.  Retrograde neuronal tracing with a deletion-mutant rabies virus , 2007, Nature Methods.

[74]  E. Zrenner Will Retinal Implants Restore Vision ? , 2002 .

[75]  Zhuo-Hua Pan,et al.  Retinal channelrhodopsin-2-mediated activity in vivo evaluated with manganese-enhanced magnetic resonance imaging , 2010, Molecular vision.

[76]  Günther Paltauf,et al.  Photomechanical processes and effects in ablation. , 2003, Chemical reviews.

[77]  Dirk Trauner,et al.  A light-gated, potassium-selective glutamate receptor for the optical inhibition of neuronal firing , 2010, Nature Neuroscience.

[78]  Hiroshi Masuhara,et al.  Nanoparticle injection to single animal cells using femtosecond laser-induced impulsive force , 2008 .

[79]  Karsten König,et al.  Cell biology: Targeted transfection by femtosecond laser , 2002, Nature.

[80]  A. Dizhoor,et al.  Ectopic Expression of a Microbial-Type Rhodopsin Restores Visual Responses in Mice with Photoreceptor Degeneration , 2006, Neuron.

[81]  Guy Salama,et al.  Imaging cellular signals in the heart in vivo: Cardiac expression of the high-signal Ca2+ indicator GCaMP2. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[82]  Karl Deisseroth,et al.  Genetic Reactivation of Cone Photoreceptors Restores Visual Responses in Retinitis Pigmentosa , 2010, Science.

[83]  Karl Deisseroth,et al.  Optical activation of lateral amygdala pyramidal cells instructs associative fear learning , 2010, Proceedings of the National Academy of Sciences.

[84]  Taner Akkin,et al.  Spectral-domain optical coherence phase microscopy for quantitative phase-contrast imaging. , 2005, Optics letters.

[85]  Karsten König,et al.  Targeted transfection of stem cells with sub-20 femtosecond laser pulses. , 2008, Optics express.

[86]  L Wang,et al.  MCML--Monte Carlo modeling of light transport in multi-layered tissues. , 1995, Computer methods and programs in biomedicine.

[87]  Samarendra K. Mohanty,et al.  Laser-assisted microinjection into targeted animal cells , 2003, Biotechnology Letters.

[88]  Christopher A. Voigt,et al.  Spatiotemporal Control of Cell Signalling Using A Light-Switchable Protein Interaction , 2009, Nature.

[89]  Hiroshi Masuhara,et al.  Gene delivery process in a single animal cell after femtosecond laser microinjection , 2009 .

[90]  V. Pieribone,et al.  Genetically Targeted Optical Electrophysiology in Intact Neural Circuits , 2013, Cell.

[91]  Ling Gu,et al.  Crystalline magnetic carbon nanoparticle assisted photothermal delivery into cells using CW near-infrared laser beam , 2014, Scientific Reports.

[92]  Jun Ohta,et al.  CMOS on-chip bio-imaging sensor with integrated micro light source array for optogenetics , 2012 .

[93]  S. Daiger,et al.  Perspective on genes and mutations causing retinitis pigmentosa. , 2007, Archives of ophthalmology.

[94]  B. Crane,et al.  Photochemistry of flavoprotein light sensors. , 2014, Nature chemical biology.

[95]  Ling Gu,et al.  Non-Scanning Fiber-Optic Near-Infrared Beam Led to Two-Photon Optogenetic Stimulation In-Vivo , 2014, PloS one.

[96]  W A Baumgartner,et al.  Etiology, pathogenesis, and experimental treatment of retinitis pigmentosa. , 2000, Medical hypotheses.

[97]  J. Fujimoto,et al.  Phase-sensitive optical coherence tomography at up to 370,000 lines per second using buffered Fourier domain mode-locked lasers. , 2007, Optics letters.

[98]  Junichi Nakai,et al.  Ca2+-sensing Transgenic Mice , 2004, Journal of Biological Chemistry.

[99]  Audrey K. Ellerbee,et al.  Spectral-domain phase microscopy. , 2004, Optics Letters.

[100]  K. Dhakal,et al.  Fiber-optic two-photon optogenetic stimulation. , 2013, Optics letters.

[101]  K. Dholakia,et al.  Fibre based cellular transfection. , 2008, Optics express.

[102]  D. Oesterhelt,et al.  Closing in on bacteriorhodopsin: progress in understanding the molecule. , 1999, Annual review of biophysics and biomolecular structure.

[103]  I. Yaroslavsky,et al.  Optical properties of selected native and coagulated human brain tissues in vitro in the visible and near infrared spectral range. , 2002, Physics in medicine and biology.

[104]  J. D. de Boer,et al.  Spectral-domain optical coherence phase and multiphoton microscopy. , 2007, Optics letters.

[105]  J. Christie,et al.  LOV to BLUF: flavoprotein contributions to the optogenetic toolkit. , 2012, Molecular plant.

[106]  Feng Zhang,et al.  An optical neural interface: in vivo control of rodent motor cortex with integrated fiberoptic and optogenetic technology , 2007, Journal of neural engineering.

[107]  M. Berns,et al.  Manipulation of mammalian cells using a single-fiber optical microbeam. , 2008, Journal of biomedical optics.

[108]  E. Muneyuki,et al.  Chloride concentration dependency of the electrogenic activity of halorhodopsin. , 1999, Biochemistry.

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

[110]  Karsten König,et al.  Optical nanoinjection of macromolecules into vital cells. , 2005, Journal of photochemistry and photobiology. B, Biology.

[111]  Vikram Kohli,et al.  Laser surgery of zebrafish (Danio rerio) embryos using femtosecond laser pulses: Optimal parameters for exogenous material delivery, and the laser's effect on short- and long-term development , 2008, BMC biotechnology.

[112]  Yei Hwan Jung,et al.  Injectable, Cellular-Scale Optoelectronics with Applications for Wireless Optogenetics , 2013, Science.

[113]  Karl Deisseroth,et al.  Functional Integration of Grafted Neural Stem Cell-Derived Dopaminergic Neurons Monitored by Optogenetics in an In Vitro Parkinson Model , 2011, PloS one.