A novel protein fold and extreme domain swapping in the dimeric TorD chaperone from Shewanella massilia.

TorD is the cytoplasmic chaperone involved in the maturation of the molybdoenzyme TorA prior to the translocation of the folded protein into the periplasm. The X-ray structure at 2.4 A resolution of the TorD dimer reveals extreme domain swapping between the two subunits. The all-helical architecture of the globular domains within the intertwined molecular dimer shows no similarity with known protein structures. According to sequence similarities, this new fold probably represents the architecture of the chaperones associated with the bacterial DMSO/TMAO reductases and also that of proteins of yet unknown functions. The occurrence of multiple oligomeric forms and the chaperone activity of both monomeric and dimeric TorD raise questions about the possible biological role of domain swapping in this protein.

[1]  C. Birck,et al.  Characterization and multiple molecular forms of TorD from Shewanella massilia, the putative chaperone of the molybdoenzyme TorA , 2002, Protein science : a publication of the Protein Society.

[2]  G. Giordano,et al.  Crystal structure of oxidized trimethylamine N-oxide reductase from Shewanella massilia at 2.5 A resolution. , 1998, Journal of molecular biology.

[3]  Axel T. Brunger,et al.  Assessment of Phase Accuracy by Cross Validation: the Free R Value. Methods and Applications , 1993 .

[4]  D. Eisenberg,et al.  Characterization of high-order diphtheria toxin oligomers. , 2000, Biochemistry.

[5]  D. Svergun,et al.  CRYSOL : a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates , 1995 .

[6]  A. McEwan,et al.  Mutational analysis of the dimethylsulfoxide respiratory (dor) operon of Rhodobacter capsulatus. , 1999, Microbiology.

[7]  K. Sharp,et al.  Protein folding and association: Insights from the interfacial and thermodynamic properties of hydrocarbons , 1991, Proteins.

[8]  L Mazzarella,et al.  A potential allosteric subsite generated by domain swapping in bovine seminal ribonuclease. , 1999, Journal of molecular biology.

[9]  W A Hendrickson,et al.  Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD): a vehicle for direct determination of three‐dimensional structure. , 1990, The EMBO journal.

[10]  D. Suck,et al.  X‐ray structure of T4 endonuclease VII: a DNA junction resolvase with a novel fold and unusual domain‐swapped dimer architecture , 1999, The EMBO journal.

[11]  E. L. Barrett,et al.  Bacterial reduction of trimethylamine oxide. , 1985, Annual review of microbiology.

[12]  G. Giordano,et al.  TorD, A Cytoplasmic Chaperone That Interacts with the Unfolded Trimethylamine N-Oxide Reductase Enzyme (TorA) in Escherichia coli * , 1998, The Journal of Biological Chemistry.

[13]  C. Jourlin-Castelli,et al.  An unsuspected autoregulatory pathway involving apocytochrome TorC and sensor TorS in Escherichia coli , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[14]  B. Berks,et al.  A novel protein transport system involved in the biogenesis of bacterial electron transfer chains. , 2000, Biochimica et biophysica acta.

[15]  D Eisenberg,et al.  Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly. , 1997, Advances in protein chemistry.

[16]  Collaborative Computational,et al.  The CCP4 suite: programs for protein crystallography. , 1994, Acta crystallographica. Section D, Biological crystallography.

[17]  J. Thornton,et al.  PROCHECK: a program to check the stereochemical quality of protein structures , 1993 .

[18]  D. Eisenberg,et al.  Domain swapping: entangling alliances between proteins. , 1994, Proceedings of the National Academy of Sciences of the United States of America.

[19]  T. Creighton,et al.  Protein Folding , 1992 .

[20]  F. Sargent.  A marriage of bacteriology with cell biology results in twin arginines. , 2001, Trends in microbiology.

[21]  John A Tainer,et al.  Crystal Structure and Mutational Analysis of the Human CDK2 Kinase Complex with Cell Cycle–Regulatory Protein CksHs1 , 1996, Cell.

[22]  A. McEwan,et al.  Cloning and sequence analysis of the dimethylsulfoxide reductase structural gene from Rhodobacter capsulatus. , 1996, Biochimica et biophysica acta.

[23]  P. Vachette,et al.  Improved Signal-to-Background Ratio in Small-Angle X-ray Scattering Experiments with Synchrotron Radiation using an Evacuated Cell for Solutions , 1997 .

[24]  P. Dumas,et al.  Proline-dependent oligomerization with arm exchange. , 1997, Structure.

[25]  R J Read,et al.  Crystallography & NMR system: A new software suite for macromolecular structure determination. , 1998, Acta crystallographica. Section D, Biological crystallography.

[26]  G. Giordano,et al.  TMAO anaerobic respiration in Escherichia coli: involvement of the tor operon , 1994, Molecular microbiology.

[27]  J. Thornton,et al.  PROMOTIF—A program to identify and analyze structural motifs in proteins , 1996, Protein science : a publication of the Protein Society.

[28]  C. Boulin,et al.  Data appraisal, evaluation and display for synchrotron radiation experiments: Hardware and software , 1986 .

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

[30]  W. Kabsch,et al.  Dictionary of protein secondary structure: Pattern recognition of hydrogen‐bonded and geometrical features , 1983, Biopolymers.

[31]  S Kaplan,et al.  Characterization of genes encoding dimethyl sulfoxide reductase of Rhodobacter sphaeroides 2.4.1T: an essential metabolic gene function encoded on chromosome II , 1997, Journal of bacteriology.

[32]  C. Cambillau,et al.  Domain swapping creates a third putative combining site in bovine odorant binding protein dimer , 1996, Nature Structural Biology.

[33]  A universal system for the transport of redox proteins: early roots and latest developments. , 2000, Biophysical chemistry.

[34]  R. Gunsalus,et al.  Anaerobic respiratory growth of Vibrio harveyi, Vibrio fischeri and Photobacterium leiognathi with trimethylamine N-oxide, nitrate and fumarate: ecological implications. , 2000, Environmental microbiology.

[35]  R. Read.  Improved Fourier Coefficients for Maps Using Phases from Partial Structures with Errors , 1986 .

[36]  G. Giordano,et al.  Molecular analysis of the trimethylamine N-oxide (TMAO) reductase respiratory system from a Shewanella species. , 1998, Journal of molecular biology.

[37]  I. Oresnik,et al.  Identification of a twin‐arginine leader‐binding protein , 2001, Molecular microbiology.

[38]  V. Méjean,et al.  Electron Transfer and Binding of the c-Type Cytochrome TorC to the Trimethylamine N-Oxide Reductase in Escherichia coli * , 2001, The Journal of Biological Chemistry.

[39]  G. Giordano,et al.  A novel Sec‐independent periplasmic protein translocation pathway in Escherichia coli , 1998, The EMBO journal.

[40]  L. Itzhaki,et al.  Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues , 2001, Proceedings of the National Academy of Sciences of the United States of America.

[41]  G. Giordano,et al.  High substrate specificity and induction characteristics of trimethylamine-N-oxide reductase of Escherichia coli. , 1996, Biochimica et biophysica acta.

[42]  B. Berks,et al.  The Tat protein export pathway , 2000, Molecular microbiology.

[43]  Patrice Gouet,et al.  ESPript: analysis of multiple sequence alignments in PostScript , 1999, Bioinform..

[44]  V. Méjean,et al.  Reconstitution of the Trimethylamine Oxide Reductase Regulatory Elements of Shewanella oneidensis in Escherichia coli , 2002, Journal of bacteriology.

[45]  C Sander,et al.  Mapping the Protein Universe , 1996, Science.