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

Structure

Volumn 11, Issue 2, 2003, Pages 165-174

  Tranier, Samuel ^a   Iobbi Nivol, Chantal ^b   Birck, Catherine ^a,c   Ilbert, Marianne ^b   Mortier Barrière, Isabelle ^a   Méjean, Vincent ^b   Samama, Jean Pierre ^a,c  

^a INSTITUT DE PHARMACOLOGIE ET DE BIOLOGIE STRUCTURALE   (France)

^b CNRS   (France)

^c INSTITUT DE GÉNÉTIQUE ET DE BIOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

3D domain swapping; Chaperone; Molybdoenzyme; TorD; Twin arginine translocation; X ray structure

Indexed keywords

BACTERIAL PROTEIN; CHAPERONE; DIMER; DIMETHYL SULFOXIDE; MONOMER; OXIDOREDUCTASE; PROTEIN TORD; TRIMETHYLAMINE OXIDE; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CYTOPLASM; NONHUMAN; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; SEQUENCE ALIGNMENT; SHEWANELLA;

BACTERIAL PROTEINS; MOLECULAR CHAPERONES; MULTIGENE FAMILY; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; SHEWANELLA;

BACTERIA (MICROORGANISMS); MASSILIA; NEGIBACTERIA; SHEWANELLA; SHEWANELLA MASSILIA;

EID: 0037317075     PISSN: 09692126     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0969-2126(03)00008-X     Document Type: Article

References (49)

1. Dos Santos J.P., Iobbi-Nivol C., Couillault C., Giordano G., Méjean V. Molecular analysis of the trimethylamine N-oxide (TMAO) reductase respiratory system from a Shewanella species. J. Mol. Biol. 284:1998;421-433.
2. Proctor L.M., Gunsalus R.P. Anaerobic respiratory growth of Vibrio harveyi, Vibrio fischeri and Photobacterium leiognathi with trimethylamine N-oxide, nitrate and fumarate. ecological implications Environ. Microbiol. 2:2000;399-406.
3. Shaw A.L., Hanson G.R., McEwan A.G. Cloning and sequence analysis of the dimethylsulfoxide reductase structural gene from Rhodobacter capsulatus. Biochim. Biophys. Acta. 1276:1996;176-180.
4. Mouncey N.J., Choudhary M., Kaplan S. Characterization of genes encoding dimethyl sulfoxide reductase of Rhodobacter sphaeroides 2.4.1T. an essential metabolic gene function encoded on chromosome II J. Bacteriol. 179:1997;7617-7624.
5. Barrett E.L., Kwan H.S. Bacterial reduction of trimethylamine oxide. Annu. Rev. Microbiol. 39:1985;131-149.
6. Gon S., Patte J.C., Dos Santos J.P., Méjean V. Reconstitution of the trimethylamine oxide reductase regulatory elements of Shewanella oneidensis in Escherichia coli. J. Bacteriol. 184:2002;1262-1269.
7. Méjean V., Iobbi-Nivol C., Lepelletier M., Giordano G., Chippaux M., Pascal M.C. TMAO anaerobic respiration in Escherichia coli. involvement of the tor operon Mol. Microbiol. 11:1994;1169-1179.
8. Iobbi-Nivol C., Pommier J., Simala-Grant J., Méjean V., Giordano G. High substrate specificity and induction characteristics of trimethylamine-N-oxide reductase of Escherichia coli. Biochim. Biophys. Acta. 1294:1996;77-82.
9. Czjzek M., Dos Santos J.P., Pommier J., Giordano G., Méjean V., Haser R. Crystal structure of oxidized trimethylamine N-oxide reductase from Shewanella massilia at 2.5 A resolution. J. Mol. Biol. 284:1998;435-447.
10. Gon S., Giudici-Orticoni M.T., Méjean V., Iobbi-Nivol C. Electron transfer and binding of the c-type cytochrome TorC to the trimethylamine N-oxide reductase in Escherichia coli. J. Biol. Chem. 276:2001;11545-11551.
11. Gon S., Jourlin-Castelli C., Theraulaz L., Méjean V. An unsuspected autoregulatory pathway involving apocytochrome TorC and sensor TorS in Escherichia coli. Proc. Natl. Acad. Sci. USA. 98:2001;11615-11620.
12. Pommier J., Méjean V., Giordano G., Iobbi-Nivol C. TorD, a cytoplasmic chaperone that interacts with the unfolded trimethylamine N-oxide reductase enzyme (TorA) in Escherichia coli. J. Biol. Chem. 273:1998;16615-16620.
13. Santini C.L., Ize B., Chanal A., Muller M., Giordano G., Wu L.F. A novel sec-independent periplasmic protein translocation pathway in Escherichia coli. EMBO J. 17:1998;101-112.
14. Berks B.C., Sargent F., De Leeuw E., Hinsley A.P., Stanley N.R., Jack R.L., Buchanan G., Palmer T. A novel protein transport system involved in the biogenesis of bacterial electron transfer chains. Biochim. Biophys. Acta. 1459:2000;325-330.
15. Voordouw G. A universal system for the transport of redox proteins. early roots and latest developments Biophys. Chem. 86:2000;131-140.
16. Tranier S., Mortier-Barrière I., Ilbert M., Birck C., Iobbi-Nivol C., Mejean V., Samama J.P. Characterization and multiple molecular forms of TorD from Shewanella massilia, the putative chaperone of the molybdoenzyme TorA. Protein Sci. 11:2002;2148-2157.
17. Terwilliger T.C., Berendzen J. Automated MAD and MIR structure solution. Acta Crystallogr. D Biol. Crystallogr. 55:1999;849-861.
18. Laskowski R.A., MacArthur M.W., Moss D.S., Thornton J.M. Procheck. a program to check the stereochemical quality of protein structures J. Appl. Crystallogr. 26:1993;283-291.
19. Holm L., Sander C. Mapping the protein universe. Science. 273:1996;595-603.
20. Schlunegger M.P., Bennett M.J., Eisenberg D. Oligomer formation by 3D domain swapping. a model for protein assembly and misassembly Adv. Protein Chem. 50:1997;61-122.
21. Oresnik I.J., Ladner C.L., Turner R.J. Identification of a twin-arginine leader-binding protein. Mol. Microbiol. 40:2001;323-331.
22. Shaw A.L., Leimkuhler S., Klipp W., Hanson G.R., McEwan A.G. Mutational analysis of the dimethylsulfoxide respiratory (dor) operon of Rhodobacter capsulatus. Microbiology. 145:1999;1409-1420.
23. Nicholls A., Sharp K.A., Honig B. Protein folding and association. insights from the interfacial and thermodynamic properties of hydrocarbons Proteins. 11:1991;281-296.
24. Rousseau F., Schymkowitz J.W., Wilkinson H.R., Itzhaki L.S. Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues. Proc. Natl. Acad. Sci. USA. 98:2001;5596-5601.
25. Bergdoll M., Remy M.H., Cagnon C., Masson J.M., Dumas P. Proline-dependent oligomerization with arm exchange. Structure. 5:1997;391-401.
26. Bourne Y., Watson M.H., Hickey M.J., Holmes W., Rocque W., Reed S.I., Tainer J.A. Crystal structure and mutational analysis of the human CDK2 kinase complex with cell cycle-regulatory protein CksHs1. Cell. 84:1996;863-874.
27. Raaijmakers H., Vix O., Toro I., Golz S., Kemper B., Suck D. X-ray structure of T4 endonuclease VII. a DNA junction resolvase with a novel fold and unusual domain-swapped dimer architecture EMBO J. 18:1999;1447-1458.
28. Bennett M.J., Choe S., Eisenberg D. Domain swapping. entangling alliances between proteins Proc. Natl. Acad. Sci. USA. 91:1994;3127-3131.
29. Steere B., Eisenberg D. Characterization of high-order diphtheria toxin oligomers. Biochemistry. 39:2000;15901-15909.
30. Vitagliano L., Adinolfi S., Sica F., Merlino A., Zagari A., Mazzarella L. A potential allosteric subsite generated by domain swapping in bovine seminal ribonuclease. J. Mol. Biol. 293:1999;569-577.
31. Tegoni M., Ramoni R., Bignetti E., Spinelli S., Cambillau C. Domain swapping creates a third putative combining site in bovine odorant binding protein dimer. Nat. Struct. Biol. 3:1996;863-867.
32. Berks B.C., Sargent F., Palmer T. The Tat protein export pathway. Mol. Microbiol. 35:2000;260-274.
33. Sargent F. A marriage of bacteriology with cell biology results in twin arginines. Trends Microbiol. 9:2001;196-198.
34. Hendrickson W.A., Horton J.R., LeMaster D.M. Selenomethionyl proteins produced for analysis by multiwavelength anomalous diffraction (MAD). a vehicle for direct determination of three-dimensional structure EMBO J. 9:1990;1665-1672.
35. Leslie A.G.W. Profile fitting. Helliwell J.R., Machin P.A., Papiz M.Z. Computational Aspects of Protein Crystal Analysis. Proceedings of the Daresbury Study Weekend. 1987;Daresbury Laboratory, Daresbury, UK. 39-50.pp.
36. Evans P.R. Data reduction. Sawyer L., Isaacs N., Bayley S. Data Collection and Processing. Proceedings of the CCP4 Study Weekend. 1993;Daresbury Laboratory, Daresbury, UK. 114-122.pp.
37. CCP4 The CCP4 suite. programs for protein crystallography Acta Crystallogr. D Biol Crystallogr. 50:1994;760-763.
38. Cowtan K. An automated procedure for phase improvement by density modification. Jt. CCP. 4(ESF-EACBM Newsl. Protein Crystallogr. 31):1994;34-38.
39. Brunger A.T., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S.et al. Crystallography and NMR system. a new software suite for macromolecular structure determination Acta Crystallogr. D Biol. Crystallogr. 54:1998;905-921.
40. Read R.J. Improved Fourier coefficients for maps using phases from partial structures with errors. Acta Crystallogr. A. 42:1986;140-149.
41. Roussel, A., and Cambillau, C. (1989). TURBO-FRODO. In Silicon Graphics Geometry Partner Directory (Mountain View, CA: Silicon Graphics), pp. 71-78.
42. Brunger A.T. Assessment of phase accuracy by cross validation. the free R value. Methods and applications Acta Crystallogr. D Biol. Crystallogr. 49:1993;24-36.
43. Hutchinson E.G., Thornton J.M. PROMOTIF - a program to identify and analyze structural motifs in proteins. Protein Sci. 5:1996;212-220.
44. Depautex C., Desvignes C., Leboucher P., Lemonnier M., Dagneaux D., Benoit J.P., Vachette P. LURE Annual Report. 1985-1987 (Orsay:1987;. France: LURE).
45. Boulin C., Kempf R., Koch M.H.J., McLaughlin S.M. Data appraisal, evaluation and display for synchrotron radiation experiments. hardware and software Nucl. Instrum. Methods Phys. Res. A. 249:1986;399-407.
46. Dubuisson J.M., Decamps T., Vachette P. Improved signal-to-background ratio in small-angle X-ray scattering experiments with synchrotron radiation using an evacuated cell for solutions. J. Appl. Crystallogr. 30:1997;49-54.
47. Svergun D., Barberato C., Koch M.H.J. CRYSOL - a program to evaluate X-ray solution scattering of biological macromolecules from atomic coordinates. J. Appl. Crystallogr. 28:1995;768-773.
48. Kabsch W., Sander C. Dictionary of protein secondary structure. pattern recognition of hydrogen-bonded and geometrical features Biopolymers. 22:1983;2577-2637.
49. Gouet P., Courcelle E., Stuart D.I., Metoz F. ESPript. analysis of multiple sequence alignments in PostScript Bioinformatics. 15:1999;305-308.