Light‐generated Paramagnetic Intermediates in BLUF Domains †

Blue‐light sensitive photoreceptory BLUF domains are flavoproteins, which regulate various, mostly stress‐related processes in bacteria and eukaryotes. The photoreactivity of the flavin adenine dinucleotide (FAD) cofactor in three BLUF domains from Rhodobacter sphaeroides, Synechocystis sp. PCC 6803 and Escherichia coli have been studied at low temperature using time‐resolved electron paramagnetic resonance. Photoinduced flavin triplet states and radical‐pair species have been detected on a microsecond time scale. Differences in the electronic structures of the FAD cofactors as reflected by altered zero‐field splitting parameters of the triplet states could be correlated with changes in the amino‐acid composition of the various BLUF domains’ cofactor binding pockets. For the generation of the light‐induced, spin‐correlated radical‐pair species in the BLUF domain from Synechocystis sp. PCC 6803, a tyrosine residue near the flavin’s isoalloxazine moiety plays a critical role.

[1]  E. Getzoff,et al.  Origin of light-induced spin-correlated radical pairs in cryptochrome. , 2010, The journal of physical chemistry. B.

[2]  P. Hegemann,et al.  The role of key amino acids in the photoactivation pathway of the Synechocystis Slr1694 BLUF domain. , 2009, Biochemistry.

[3]  R. Bittl,et al.  New roles of flavoproteins in molecular cell biology: Blue‐light active flavoproteins studied by electron paramagnetic resonance , 2009, The FEBS journal.

[4]  R. Shoeman,et al.  Structure and mechanism of a bacterial light-regulated cyclic nucleotide phosphodiesterase , 2009, Nature.

[5]  R. Hengge,et al.  The BLUF-EAL protein YcgF acts as a direct anti-repressor in a blue-light response of Escherichia coli. , 2009, Genes & development.

[6]  P. Saalfrank,et al.  Serine in BLUF domains displays spectral importance in computational models. , 2009, Journal of photochemistry and photobiology. B, Biology.

[7]  K. Gardner,et al.  Structure and insight into blue light-induced changes in the BlrP1 BLUF domain. , 2009, Biochemistry.

[8]  E. Getzoff,et al.  Direct observation of a photoinduced radical pair in a cryptochrome blue-light photoreceptor. , 2009, Angewandte Chemie.

[9]  M. Ikeuchi,et al.  Formation of interacting spins on flavosemiquinone and tyrosine radical in photoreaction of a blue light sensor BLUF protein TePixD. , 2008, Biochemistry.

[10]  Peter Hegemann,et al.  Hydrogen bond switching among flavin and amino acid side chains in the BLUF photoreceptor observed by ultrafast infrared spectroscopy. , 2008, Biophysical journal.

[11]  H. Schwalbe,et al.  Influence of a Joining Helix on the BLUF Domain of the YcgF Photoreceptor from Escherichia coli , 2008, Chembiochem : a European journal of chemical biology.

[12]  Marco Bocola,et al.  A conclusive mechanism of the photoinduced reaction cascade in blue light using flavin photoreceptors. , 2008, Journal of the American Chemical Society.

[13]  E. Wolf,et al.  Human and Drosophila Cryptochromes Are Light Activated by Flavin Photoreduction in Living Cells , 2008, PLoS biology.

[14]  Alexander V Nemukhin,et al.  Molecular models predict light-induced glutamine tautomerization in BLUF photoreceptors. , 2008, Biophysical journal.

[15]  P. Hore,et al.  Role of exchange and dipolar interactions in the radical pair model of the avian magnetic compass. , 2008, Biophysical journal.

[16]  R. Bittl,et al.  Studies of Organic Protein Cofactors Using Electron Paramagnetic Resonance , 2007 .

[17]  A. Losi,et al.  Flavin‐based Blue‐light Photosensors: A Photobiophysics Update , 2007, Photochemistry and photobiology.

[18]  M. Groot,et al.  Ultrafast spectroscopy of biological photoreceptors. , 2007, Current opinion in structural biology.

[19]  P. Hegemann,et al.  Photo dynamics of BLUF domain mutant H44R of AppA from Rhodobacter sphaeroides , 2007 .

[20]  R. Bittl,et al.  The Signaling State of Arabidopsis Cryptochrome 2 Contains Flavin Semiquinone* , 2007, Journal of Biological Chemistry.

[21]  Filip Vandenbussche,et al.  Cryptochrome Blue Light Photoreceptors Are Activated through Interconversion of Flavin Redox States* , 2007, Journal of Biological Chemistry.

[22]  P. Hegemann,et al.  Absorption and emission spectroscopic characterization of blue-light receptor Slr1694 from Synechocystis sp. PCC6803. , 2007, Journal of photochemistry and photobiology. B, Biology.

[23]  Keith Moffat,et al.  Crystal structures of the Synechocystis photoreceptor Slr1694 reveal distinct structural states related to signaling. , 2006, Biochemistry.

[24]  Ilme Schlichting,et al.  Crystal structures of the AppA BLUF domain photoreceptor provide insights into blue light-mediated signal transduction. , 2006, Journal of molecular biology.

[25]  P. Hegemann,et al.  Hydrogen-bond switching through a radical pair mechanism in a flavin-binding photoreceptor. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[26]  P. Hegemann,et al.  Photodynamics of the small BLUF protein BlrB from Rhodobacter sphaeroides. , 2006, Journal of photochemistry and photobiology. B, Biology.

[27]  K. Hasegawa,et al.  Light induced structural changes of a full-length protein and its BLUF domain in YcgF(Blrp), a blue-light sensing protein that uses FAD (BLUF). , 2006, Biochemistry.

[28]  K. Hellingwerf,et al.  The Solution Structure of the AppA BLUF Domain: Insight into the Mechanism of Light‐Induced Signaling , 2006, Chembiochem : a European journal of chemical biology.

[29]  Ilme Schlichting,et al.  Structure of a bacterial BLUF photoreceptor: insights into blue light-mediated signal transduction. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[30]  P. Hegemann,et al.  Absorption and fluorescence spectroscopic characterization of BLUF domain of AppA from Rhodobacter sphaeroides , 2005 .

[31]  Keith Moffat,et al.  Structure of a novel photoreceptor, the BLUF domain of AppA from Rhodobacter sphaeroides. , 2005, Biochemistry.

[32]  Masakatsu Watanabe,et al.  Biochemical and functional characterization of BLUF-type flavin-binding proteins of two species of cyanobacteria. , 2005, Journal of biochemistry.

[33]  M. Ikeuchi,et al.  Structure of a cyanobacterial BLUF protein, Tll0078, containing a novel FAD-binding blue light sensor domain. , 2005, Journal of molecular biology.

[34]  T. Todo,et al.  The cryptochromes , 2005, Genome Biology.

[35]  R. Bittl,et al.  Transient radical pairs studied by time-resolved EPR. , 2005, Biochimica et biophysica acta.

[36]  K. Hellingwerf,et al.  Photocycle of the flavin-binding photoreceptor AppA, a bacterial transcriptional antirepressor of photosynthesis genes. , 2005, Biochemistry.

[37]  G. Jeschke.  EPR techniques for studying radical enzymes. , 2004, Biochimica et biophysica acta.

[38]  P. Hegemann,et al.  On the reaction mechanism of adduct formation in LOV domains of the plant blue-light receptor phototropin. , 2004, Journal of the American Chemical Society.

[39]  R. Bittl,et al.  The photoinduced triplet of flavins and its protonation states. , 2004, Journal of the American Chemical Society.

[40]  K. Hasegawa,et al.  Light-induced structural changes in a putative blue-light receptor with a novel FAD binding fold sensor of blue-light using FAD (BLUF); Slr1694 of synechocystis sp. PCC6803. , 2004, Biochemistry.

[41]  G. Klug,et al.  Blue Light Perception in Bacteria , 2004, Photosynthesis Research.

[42]  M. A. van der Horst,et al.  Initial Characterization of the Primary Photochemistry of AppA, a Blue-light–using Flavin Adenine Dinucleotide–domain Containing Transcriptional Antirepressor Protein from Rhodobacter sphaeroides: A Key Role for Reversible Intramolecular Proton Transfer from the Flavin Adenine Dinucleotide Chromopho , 2003, Photochemistry and photobiology.

[43]  G. Tollin,et al.  Spectroscopic and mutational analysis of the blue-light photoreceptor AppA: a novel photocycle involving flavin stacking with an aromatic amino acid. , 2003, Biochemistry.

[44]  Aziz Sancar,et al.  Structure and function of DNA photolyase and cryptochrome blue-light photoreceptors. , 2003, Chemical reviews.

[45]  P. Hegemann,et al.  Crystal structures and molecular mechanism of a light-induced signaling switch: The Phot-LOV1 domain from Chlamydomonas reinhardtii. , 2003, Biophysical journal.

[46]  P. Hegemann,et al.  Phot-LOV1: photocycle of a blue-light receptor domain from the green alga Chlamydomonas reinhardtii. , 2003, Biophysical journal.

[47]  A. Bacher,et al.  DETECTION AND CHARACTERIZATION OF A LIGHT-INDUCED NEUTRAL FLAVIN RADICAL IN A C450A MUTANT OF PHOTOTROPIN* , 2003 .

[48]  Mark Gomelsky,et al.  BLUF: a novel FAD-binding domain involved in sensory transduction in microorganisms. , 2002, Trends in biochemical sciences.

[49]  Carl E. Bauer,et al.  AppA Is a Blue Light Photoreceptor that Antirepresses Photosynthesis Gene Expression in Rhodobacter sphaeroides , 2002, Cell.

[50]  W. Lubitz,et al.  Radicals, radical pairs and triplet states in photosynthesis. , 2002, Accounts of chemical research.

[51]  Keith Moffat,et al.  Photoexcited Structure of a Plant Photoreceptor Domain Reveals a Light-Driven Molecular Switch Article, publication date, and citation information can be found at www.plantcell.org/cgi/doi/10.1105/tpc.010475. , 2002, The Plant Cell Online.

[52]  Masakatsu Watanabe,et al.  A blue-light-activated adenylyl cyclase mediates photoavoidance in Euglena gracilis , 2002, Nature.

[53]  T. Todo,et al.  Photoactivation of the flavin cofactor in Xenopus laevis (6–4) photolyase: Observation of a transient tyrosyl radical by time-resolved electron paramagnetic resonance , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  W. Lubitz,et al.  Tryptophan and tyrosine radicals in ribonucleotide reductase: a comparative high-field EPR study at 94 GHz. , 2001, Biochemistry.

[55]  W. Eisenreich,et al.  An optomechanical transducer in the blue light receptor phototropin from Avena sativa , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[56]  S. Weber,et al.  The electronic structure of the flavin cofactor in DNA photolyase. , 2001, Journal of the American Chemical Society.

[57]  A. Popov,et al.  Spin dynamics in strongly coupled spin-correlated radical pairs: Stochastic modulation of the exchange interaction and ST−1 mixing in different magnetic fields , 2001 .

[58]  J. Christie,et al.  Photochemical and mutational analysis of the FMN-binding domains of the plant blue light receptor, phototropin. , 2000, Biochemistry.

[59]  I. Horne,et al.  Domain Structure, Oligomeric State, and Mutational Analysis of PpsR, the Rhodobacter sphaeroides Repressor of Photosystem Gene Expression , 2000, Journal of bacteriology.

[60]  A. Sancar,et al.  Cryptochrome: the second photoactive pigment in the eye and its role in circadian photoreception. , 2000, Annual review of biochemistry.

[61]  J. Christie,et al.  LOV (light, oxygen, or voltage) domains of the blue-light photoreceptor phototropin (nph1): binding sites for the chromophore flavin mononucleotide. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[62]  Jeffrey C. Hall,et al.  CRY, a Drosophila Clock and Light-Regulated Cryptochrome, Is a Major Contributor to Circadian Rhythm Resetting and Photosensitivity , 1998, Cell.

[63]  A. Sancar,et al.  Vitamin B2-based blue-light photoreceptors in the retinohypothalamic tract as the photoactive pigments for setting the circadian clock in mammals. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[64]  P. Oeller,et al.  Arabidopsis NPH1: a protein kinase with a putative redox-sensing domain. , 1997, Science.

[65]  A. Cashmore,et al.  HY4 gene of A. thaliana encodes a protein with characteristics of a blue-light photoreceptor , 1993, Nature.

[66]  K. Möbius,et al.  Light-induced triplet electron transfer in cyclohexene-bridged porphyrin–quinones detected by time-resolved electron paramagnetic resonance spectroscopy , 1993 .

[67]  J. Norris,et al.  Transient EPR of light-induced radical pairs in plant photosystem I: observation of quantum beats , 1991 .

[68]  J. Petersen,et al.  Anisotropic electron spin polarization of correlated spin pairs in photosynthetic reaction centers , 1989 .

[69]  D. A. Hunter,et al.  Electron paramagnetic resonance of spin-correlated radical pairs in photosynthetic reactions , 1987 .

[70]  J. Norris,et al.  Spin-polarized electron paramagnetic resonance spectra of radical pairs in micelles: observation of electron spin-spin interactions , 1987 .

[71]  D. A. Hunter,et al.  Electron spin resonance of spin-correlated radical pairs , 1987 .

[72]  T. Shiga,et al.  TRIPLET STATE STUDIES OF FLAVINS BY ELECTRON PARAMAGNETIC RESONANCE—I , 1964 .

[73]  J. S. Hyde,et al.  Paramagnetic resonance in triplet naphthalene at liquid helium temperatures , 1963 .