Handbook of Photosensory Receptors
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1 Winslow R. Briggs John L. Spudich Handbook of Photosensory Receptors
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3 Preface XVII List of Authors XIX 1 Microbial Rhodopsins: Phylogenetic and Functional Diversity 1 John L. Spudich and Kwang-Hwan Jung 1,1 Introduction Archaeal Rhodopsins Clues to Newfound Microbial Rhodopsin Function from Primar y Sequence Comparison to Archaeal Rhodopsins Bacterial Rhodopsins Green-absorbing Proteorhodopsin ("GPR") from Monterey Bay Surfac e Plankton Blue-absorbing Proteorhodopsin ("BPR") from Hawaiian Deep Sea Plankton Anabaena Sensory Rhodopsin Other Bacterial Rhodopsins Eukaryotic Microbial Rhodopsins Fungal Rhodopsins Algal Rhodopsins Spectral Tuning A Unified Mechanism for Molecular Function? Opsin-related Proteins without the Retinal-binding Site Perspective 2 0 References Sensory Rhodopsin Signaling in Green Flagellate Algae 25 Oleg A. Sineshchekov and John L. Spudic h 2.1 Introduction Retinylidene Receptors 25 2.L2. Physiology of Algal Phototaxis and the Photophobic Response Photoelectrical Currents and their Relationship to Swimming Behavior 27
4 2.2 The Photosensory Receptors : CSRA and CSRB Genomics, Sequence, and Predicted Structure Cellular Content and Roles in Phototaxis and Photophobic Behavior Molecular Mechanism of Action Other Algae Conclusion and Future Perspectives 4 0 Acknowledgements 4 1 References Visual Pigments as Photoreceptors 43 Masato Kumauchi and Thomas Ebre y 3A Introduction General Considerations Photoreceptors and Pigments Non-photoreceptor or "Non-rod", "Non-cone" Retinal Pigments Retinal Photoisomerases The Unphotolyzed State of Vertebrate Visual Pigments Structure of Visual Pigments: the Chromophore Overall Topology of the Pigment Cytoplasmic Domain The Hydrophobic Core of Rhodopsin and the Retinal Binding Pocket The Extracellular Domain of Rhodopsin Structure of Other Visual Pigments Protonation State of Some of the Carboxylic Acids of Rhodopsin Internal Waters in Visual Pigments Is Rhodopsin a Dimer in vivo? Functional Properties of the Unphotolyzed State of a "Good" Visua l Pigment Quantum Efficiency of Visual Pigment Photochemistry Dark Noise Originating from the Photoreceptor Pigment Activation of Vertebrate Visual Pigments Introduction The Primary Event, Photoisomerization The Meta I Meta II Transition Molecular Changes upon the Formation of Meta I and Meta II Internal Water Molecules Required Steps for Rhodopsin Activation The Transmembrane Signaling Pathway The Unphotolyzed State of Invertebrate Visual Pigments Introduction Wavelength Regulation of Invertebrate Pigments Mechanism of Activation of Invertebrate Visual Pigments The Initial Photochemical Events Formation of Acid Metarhodopsin 71
5 3.5.3 Required Steps for Photolyzed Octopus Rhodopsin to Activate it s G-protein Purification of the Active Form of an Invertebrate Visual Pigment 72 Acknowledgements 72 References 72 4 Structural and Functional Aspects of the Mammalian Rod-Cell Photoreceptor Rhodopsin 77 Najmoutin G. Abdulaev and Kevin D. Ridge 4.1 Introduction Rhodopsin and Mammalian Visual Phototransduction Signal Amplification by Light-activated Rhodopsin Inactivation of Light-activated Rhodopsin Properties of Rhodopsin Isolation of Rhodopsin 80 4,3.2 Biochemical and Physicochemical Properties of Rhodopsin Post-translational Modifications in Rhodopsin Membrane Topology of Rhodopsin and Functional Domains Chromophore Binding Pocket and Photolysis of Rhodopsin Structure of Rhodopsin Crystal Structure of Rhodopsin Atomic Force Microscopy of Rhodopsin in the Disk Membrane Activation Mechanism of Rhodopsin Conclusions 8 9 Acknowledgements 90 References 90 5 A Novel Light Sensing Pathway in the Eye : Conserved Features of Inner Retinal Photoreception in Rodents, Man and Teleost Fish 93 Mark W. Hankins and Russell G. Foste r Summary Introduction A Novel Photoreceptor within the Eye Biological Clocks and their Regulation by Light Non-rod, Non-cone Photoreception in Rodents An Irradiance Detection Pathway in the Eye The Discovery of a Novel Ocular Photopigment in Mice (OP ß ) Melanopsin and Non-rod, Non-cone Photoreception A Functional Syncitium of Directly Light-sensitive Ganglion Cells Non-rod, Non-cone Photoreception in Humans Introduction Novel Photoreceptors Regulate Melatonin Novel Photoreceptors Regulate the Primary Visual Cone Pathway 10 S 5.4 Non-rod, Non-cone Photoreception in Teleost Fish Background 107
6 5.4.2 Vertebrate Ancient (VA) Opsin and Inner Retinal Photoreception i n Teleost Fish A Novel Light Response from VA-opsin- and Melanopsin-expressing Horizontal Cells Action Spectra for the HC-RSD Light Response Identify a Nove l Photopigment The Possible Function of HC-RSD Neurones Opsins can be Photosensors or Photoisomerases Placing Candidate Genes and Photopigments into Context Conclusions 114 References The Phytochromes 12 1 Shih-Long Tu and J. Clark Lagarias 6.1 Introduction Photomorphogenesis and Phytochromes The Central Dogma of Phytochrome Action Molecular Properties of Eukaryotic and Prokaryotic Phytochromes Molecular Properties of Plant Phytochromes Molecular Properties of Cyanobacterial Phytochromes Photochemical and Nonphotochemical Conversions of Phytochrome The Phytochrome Chromophore Phytochrome Photointerconversions Dark Reversion Phytochrome Biosynthesis and Turnover Phytobilin Biosynthesis in Plants and Cyanobacteria Apophytochrome Biosynthesis and Holophytochrome Assembly Phytochrome Turnover Molecular Mechanism of Phytochrome Signaling: Future Perspective Regulation of Protein-Protein Interactions by Phosphorylation Regulation of Tetrapyrrole Metabolism 143 Acknowledgements 145 References Phytochrome Signaling 151 Enamul Huq and Peter H. Quai l 7.1 Introduction Photosensory and Biological Functions of Individual Phytochromes phy Domains Involved in Signaling phy Signaling Components Second Messenger Hypothesis Genetically Identified Signaling Components phy-interacting Factors 159
7 7.4.4 Early phy-responsive Genes Biochemical Mechanism of Signal Transfer phy Signaling and Circadian Rhythms Future Prospects 16 6 Acknowledgements 16 7 References Phytochromes in Microorganisms 171 Richard D. Vierstra and Baruch Karniol 8.1 Introduction Higher Plant Phys The Discovery of Microbial Phys Phylogenetic Analysis of the Phy Superfamily Cyanobacterial Phy (Cph) Family Bacteriophytochrome (BphP) Family Fungal Phy (Fph) Family Phy-like Sequences Downstream Signal-Transduction Cascades Physiological Roles of Microbial Phys Regulation of Phototaxis Enhancement of Photosynthetic Potential Photocontrol of Pigmentation Evolution of the Phy Superfamily Perspectives 19 2 Acknowledgements 19 3 References Light-activated Intracellular Movement of Phytochrome 19 7 Eberhard Schäfer and Ferenc Nagy 9.1 Introduction The Classical Methods Spectroscopic Methods Cell Biological Methods Immunocytochemical Methods Novel Methods Intracellular Localization of PHYB in Dark and Light Intracellular Localization of PHYA in Dark and Light Intracellular Localization of PHYC, PHYD and PHYE in Dark and Light Intracellular Localization of Intragenic Mutant Phytochromes Hyposensitive, Loss-of-function Mutants Hypersensitive Mutants Protein Composition of Nuclear Speckles Associated with phyb The Function of Phytochromes Localized in Nuclei and Cytosol 207
8 9.10 Concluding Remarks 20 8 References Plant Cryptochromes : Their Genes, Biochemistry, and Physiologica l Roles 21 1 Alfred Batschaue r Summary Cryptochrome Genes and Evolution The Discovery of Cryptochromes Distribution of Cryptochromes and their Evolution Cryptochrome Domains, Cofactors and Similarities with Photolyase Biological Function of Plant Cryptochromes Control of Growth Role of Cryptochromes in Circadian Clock Entrainment and Photoperiodism Regulation of Gene Expression Localization of Cryptochromes Biochemical Properties of Cryptochromes Protein Stability Phosphorylation DNA Binding Electron Transfer Summary 24 1 Acknowledgements 24 1 References Plant Cryptochromes and Signaling 24 7 Anthony R. Cashmore 11.1 Introduction Photolyases Cryptochrome Photochemistry Cryptochrome Action Spectra Cryptochromes and Blue Light-dependent Inhibition of Cell Expansion Signaling Mutants Signaling by Cryptochrome CNT and CCT Domains Arabidopsis Cryptochromes Exist as Dimers COP1, a Signaling Partner of Arabidopsis Cryptochromes Cryptochrome and Phosphorylation Cryptochrome and Gene Expression Concluding Thoughts 25 5 References 257
9 12 Animal Cryptochromes 25 9 Russell N. Van Gelder and Aziz Sanca r 12.1 Introduction Discovery of Animal Cryptochromes Structure-Function Considerations Drosophila melanogaster Cryptochrome Mammalian Cryptochromes, Circadian Rhythmicity, and Nonvisua l Photoreception Cryptochromes of Other Animals Conclusions and Future Directions 274 References Blue Light Sensing and Signaling by the Phototropins 277 John M. Christie and Winslow R. Briggs 13.1 Introduction Phototropin Structure and Function Discovery of Phototropin Photl : a Blue Light-activated Receptor Kinase Phot2: a Second Phototropic Receptor Phototropins : Photoreceptors for Movement and More Overview of Phototropin Activation LOV Domain Structure and Function ,3.1 Light Sensing by the LOV Domains LOV is all Around Are Two LOVs Better than One? From Light Sensing to Receptor Activation LOV Connection Phototropin Autophosphorylation Phototropin Recovery Phototropin Signalling Beyond Photoreceptor Activation Phototropism Stomatal Opening Chloroplast Movement Rapid Inhibition of Hypocotyl Growth by Blue Light Future Prospects 30 0 References LOV-domain Photochemistry 305 Trevor E. Swartz and Roberto A. Bogomoln i 14.1 Introduction The Chromoprotein Ground State Structure and Spectroscopy Structure of the Chromoprotein and its Chromophore Environment FMN Electrostatic Environment within the Protein Photochemistry 312
10 Photocycle Kinetics and Structure of its Intermediates Photo-backreaction Reaction Mechanisms Adduct Formation Adduct Decay Future Perspectives 32 0 References LOV-Domain Structure, Dynamics, and Diversity 323 Sean Crosson 15.1 Overview LOV Domain Architecture and Chromophore Environment Photoexcited-State Structural Dynamics of LOV Domains Comparative Structural Analysis of LOV Domains LOV-Domain Diversity 33 0 Acknowledgements 334 References The ZEITLUPE Family of Putative Photoreceptors 33 7 Thomas F. Schultz 16.1 Introduction Circadian Clocks SCF Ubiquitin Ligases Photoperception The ZTL Gene Family ZTL FKF LKP Summary 346 References Photoreceptor Gene Families in Lower Plants 349 Noriyuki Suetsugu and Masamitsu Wad a 17.1 Introduction Cryptochromes Adiantum capillus-veneris Physcomitrella patens Chlamydomonas reinhardtii Phototropins Adiantum capillus-veneris Physcomitrella patens Chlamydomonas reinhardtii Phytochromes in Lower Plants Conventional Phytochromes Phytochrome 3 in Polypodiaceous Ferns 364
11 17.5 Concluding Remarks 36 6 Acknowledgements 366 References Neurospora Photoreceptors 37 1 Jay C. Dunlap and Jennifer J. Loros 18.1 Introduction and Overview The Photobiology of Fungi in General and Neurospora in Particular Photoresponses are Widespread Photobiology of Neurospora Light Perception - the Nature of the Primary Blue Ligh t Photoreceptor Flavins as Chromophores Genetic Dissection of the Light Response New Insights into Photoreceptors from Genomics How do the Known Photoreceptors Work? WC-1 and WC-2 contain PAS Domains and Act as a Complex WC-1 is the Blue Light Photoreceptor Post-activation Regulation of WC A Non-photobiological Role for WC-1 and the WCC VIVID, a Second Photoreceptor that Modulates Light Responses Types of Photoresponse Modulation Proof of VVD Photoreceptor Function Complexities in Light Regulatory Pathways Summary and Conclusion 38 7 References Photoactive Yellow Protein, the Xanthopsin 39 1 Michael A. van der Horst, Johnny Hendriks, Jocelyne Vreede, Sergei Yeremenko, Wins Crielaard and Klaas J. Hellingwerf 19.1 Introduction Discovery of the Photoactive Yellow Protein A Family of Photoactive Yellow Proteins : the Xanthopsins Differentiation of Function among the Xanthopsins PYP: The Prototype PAS Domain Structure Primary, Secondary, and Tertiary Structure Solution Structure vs. Crystal Structure The Xanthopsins Compared Photoactivity of the Xanthopsins The Basic Photocycle Photocycle Nomenclature Experimental Observation: Context Dependence Mutants and Hybrids Photo-activation in the Different Xanthopsins Compared 400
12 19.4 The Photocycle of Photoactive Yellow Protein Initial Events Signaling State Formation and Ground State Recovery Structural Relaxation of pr Protonation Change upon pb' Formation Structural Change upon pb Formation Recovery of the Ground State Spectral Tuning of Photoactive Yellow Protein Ground State Tuning Spectral Tuning in Photocycle Intermediates Summary and Future Perspective 41 1 References Hypericin-like Photoreceptors 41 7 Pill-Soon Song Abstract Introduction Ciliate Photoreceptors Action Spectra The Chromophores Proteins and Localization Photochemistry Photosensitization? Primary Photoprocesses Photosensory Signal Transduction Signal Generation Signal Amplification Signal Transduction Concluding Remarks 43 0 Acknowledgements 43 0 References The Antirepressor AppA uses the Novel Flavin-Binding BLUF Domain as a Blue-Light-Absorbing Photoreceptor to Control Photosystem Synthesis 433 Shinji Masuda and Carl E. Baue r 21.1 Overview Oxygen and Light Intensity Control Synthesis of the Bacteria l Photosystem PpsR is a DNA-binding Transcription Factor that Coordinates bot h Oxygen and Light Regulation Discovery of AppA, a Redox Responding, Blue Light Absorbing, Antirepressor of PpsR Mechanism of the BLUF Photocycle in AppA Other BLUF Containing Proteins Concluding Remarks 443
13 Acknowledgement 44 4 References Discovery and Characterization of Photoactivated Adenylyl Cyclase (PAC), a Novel Blue-Light Receptor Flavoprotein, from Euglena gracilis 44 7 Masakatsu Watanabe and Mineo Isek i 22.1 Introduction Action Spectroscopy PAC Discovery and its Identification as the Blue-light Receptor fo r Photoavoidance PAC Involvement in Phototaxis PAC Origin Future Prospects 45 7 Acknowledgements 45 9 References 460
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