Structure of a novel photoreceptor, the BLUF domain of AppA from Rhodobacter sphaeroides.

The flavin-binding BLUF domain of AppA represents a new class of blue light photoreceptors that are present in a number of bacterial and algal species. The dark state X-ray structure of this domain was determined at 2.3 A resolution. The domain demonstrates a new function for the common ferredoxin-like fold; two long alpha-helices flank the flavin, which is bound with its isoalloxazine ring perpendicular to a five-stranded beta-sheet. The hydrogen bond network and the overall protein topology of the BLUF domain (but not its sequence) bear some resemblance to LOV domains, a subset of PAS domains widely involved in signaling. Nearly all residues conserved in BLUF domains surround the flavin chromophore, many of which are involved in an intricate hydrogen bond network. Photoactivation may induce a rearrangement in this network via reorientation of the Gln63 side chain to form a new hydrogen bond to the flavin O4 position. This shift would also break a hydrogen bond to the Trp104 side chain, which may be critical in induction of global structural change in AppA.

[1]  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.

[2]  Thomas C. Terwilliger,et al.  Automated MAD and MIR structure solution , 1999, Acta crystallographica. Section D, Biological crystallography.

[3]  P. Nordlund,et al.  Crystal structure of common type acylphosphatase from bovine testis. , 1997, Structure.

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

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

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

[7]  D E McRee,et al.  XtalView/Xfit--A versatile program for manipulating atomic coordinates and electron density. , 1999, Journal of structural biology.

[8]  M. Fraaije,et al.  Flavoenzymes: diverse catalysts with recurrent features. , 2000, Trends in biochemical sciences.

[9]  Shinji Masuda,et al.  Light-induced structural changes of apoprotein and chromophore in the sensor of blue light using FAD (BLUF) domain of AppA for a signaling state. , 2005, Biochemistry.

[10]  Winslow R. Briggs,et al.  The Photocycle of a Flavin-binding Domain of the Blue Light Photoreceptor Phototropin* , 2001, The Journal of Biological Chemistry.

[11]  Tim J. P. Hubbard,et al.  SCOP database in 2004: refinements integrate structure and sequence family data , 2004, Nucleic Acids Res..

[12]  Z. Otwinowski,et al.  [20] Processing of X-ray diffraction data collected in oscillation mode. , 1997, Methods in enzymology.

[13]  G N Murshudov,et al.  Use of TLS parameters to model anisotropic displacements in macromolecular refinement. , 2001, Acta crystallographica. Section D, Biological crystallography.

[14]  I. Zhulin,et al.  PAS Domains: Internal Sensors of Oxygen, Redox Potential, and Light , 1999, Microbiology and Molecular Biology Reviews.

[15]  G. Murshudov,et al.  Refinement of macromolecular structures by the maximum-likelihood method. , 1997, Acta crystallographica. Section D, Biological crystallography.

[16]  E. Huala,et al.  Blue-light photoreceptors in higher plants. , 1999, Annual review of cell and developmental biology.

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

[18]  Michael Y. Galperin,et al.  Novel domains of the prokaryotic two-component signal transduction systems. , 2001, FEMS microbiology letters.

[19]  S. Kaplan,et al.  AppA, a Redox Regulator of Photosystem Formation in Rhodobacter sphaeroides 2.4.1, Is a Flavoprotein , 1998, The Journal of Biological Chemistry.

[20]  M. Ahmad,et al.  Association of flavin adenine dinucleotide with the Arabidopsis blue light receptor CRY1 , 1995, Science.

[21]  Chentao Lin,et al.  Plant blue-light receptors. , 2000, Trends in plant science.

[22]  N. Grishin,et al.  GGDEF domain is homologous to adenylyl cyclase , 2001, Proteins.

[23]  T. O’Halloran,et al.  Structure and chemistry of the copper chaperone proteins. , 2000, Current opinion in chemical biology.

[24]  James W. Murray,et al.  X-ray absorption by macromolecular crystals: the effects of wavelength and crystal composition on absorbed dose , 2004 .

[25]  Thomas C. Terwilliger,et al.  Electronic Reprint Biological Crystallography Maximum-likelihood Density Modification , 2022 .

[26]  H. Komori,et al.  DNA apophotolyase from Anacystis nidulans: 1.8 A structure, 8-HDF reconstitution and X-ray-induced FAD reduction. , 2004, Acta crystallographica. Section D, Biological crystallography.

[27]  Ron D. Appel,et al.  ExPASy: the proteomics server for in-depth protein knowledge and analysis , 2003, Nucleic Acids Res..

[28]  Chad A Brautigam,et al.  Structure of the photolyase-like domain of cryptochrome 1 from Arabidopsis thaliana. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[29]  David T. Jones,et al.  Recurrence of a binding motif? , 1993, Nature.

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

[31]  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.

[32]  J. Deisenhofer DNA photolyases and cryptochromes. , 2000, Mutation research.

[33]  J. Thornton,et al.  Diversity of protein–protein interactions , 2003, The EMBO journal.

[34]  Keith Moffat,et al.  The LOV domain family: photoresponsive signaling modules coupled to diverse output domains. , 2003, Biochemistry.

[35]  J. Christie,et al.  Blue Light Sensing in Higher Plants* , 2001, The Journal of Biological Chemistry.

[36]  S. Ghisla,et al.  Mechanisms of flavoprotein-catalyzed reactions. , 1989, European journal of biochemistry.

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