Three-dimensional Structure of a Type III Glutamine Synthetase by Single-particle Reconstruction

Journal of Molecular Biology

Volumn 361, Issue 4, 2006, Pages 796-810

  van Rooyen, Jason M ^a   Abratt, Valerie R ^a   Sewell, B Trevor ^a  

^a UNIVERSITY OF CAPE TOWN   (South Africa)

Author keywords

3D reconstruction; Bacteroides fragilis; glutamine synthetase type III; single particle; structure

Indexed keywords

GLUTAMATE AMMONIA LIGASE;

AMINO ACID SEQUENCE; ARTICLE; BACTEROIDES FRAGILIS; ELECTRON MICROSCOPY; GEL FILTRATION CHROMATOGRAPHY; GEOMETRY; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN STRUCTURE; STAINING;

BACTEROIDES FRAGILIS;

EID: 33746947867     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2006.06.026     Document Type: Article

References (59)

1. Gibson III F.C., Onderdonk A.B., Kasper D.L., and Tzianabos A.O. Cellular mechanism of intraabdominal abscess formation by Bacteroides fragilis. J. Immunol. 160 (1998) 5000-5006
2. Gibson S.A., and Macfarlane G.T. Characterization of proteases formed by Bacteroides fragilis. J. Gen. Microbiol. 134 (1988) 2231-2240
3. Merrick M.J., and Edwards R.A. Nitrogen control in bacteria. Microbiol. Rev. 59 (1995) 604-622
4. Southern J.A., Parker J.R., and Woods D.R. Expression and purification of glutamine synthetase cloned from Bacteroides fragilis. J. Gen. Microbiol. 132 (1986) 2827-2835
5. Garcia-Dominguez M., Reyes J.C., and Florencio F.J. Purification and characterization of a new type of glutamine synthetase from cyanobacteria. Eur. J. Biochem. 244 (1997) 258-264
6. Amaya K.R., Kocherginskaya S.A., Mackie R.I., and Cann I.K. Biochemical and mutational analysis of glutamine synthetase type III from the rumen anaerobe Ruminococcus albus 8. J. Bacteriol. 187 (2005) 7481-7491
7. Eisenberg D., Gill H.S., Pfluegl G.M., and Rotstein S.H. Structure-function relationships of glutamine synthetases. Biochim. Biophys. Acta 1477 (2000) 122-145
8. Almassy R.J., Janson C.A., Hamlin R., Xuong N.H., and Eisenberg D. Novel subunit-subunit interactions in the structure of glutamine synthetase. Nature 323 (1986) 304-309
9. Gill H.S., Pfluegl G.M., and Eisenberg D. Multicopy crystallographic refinement of a relaxed glutamine synthetase from Mycobacterium tuberculosis highlights flexible loops in the enzymatic mechanism and its regulation. Biochemistry 41 (2002) 9863-9872
10. Kretovich W.L., Evstigneeva Z.G., Pushkin A.V., and Tsuprun V.L. Evolution of the quaternary structure of glutamine synthetase. Quad. Ric. Sci. 113 (1984) 109-115
11. Southern J.A., Parker J.R., and Woods D.R. Novel structure, properties, and inactivation of glutamine synthetase cloned from Bacteroides fragilis. J. Gen. Microbiol. 133 (1987) 2437-2446
12. Gouaux J.E., Braha O., Hobaugh M.R., Song L., Cheley S., Shustak C., and Bayley H. Subunit stoichiometry of staphylococcal alpha-hemolysin in crystals and on membranes: a heptameric transmembrane pore. Proc. Natl Acad. Sci. USA 91 (1994) 12828-12831
13. Haschemeyer R.H., and De Harven E. Electron microscopy of enzymes. Annu. Rev. Biochem. 43 (1974) 279-301
14. Denman R.B., and Wedler F.C. Association-dissociation of mammalian brain glutamine synthetase: effects of metal ions and other ligands. Arch. Biochem. Biophys. 232 (1984) 427-440
15. Maurizi M.R., and Ginsburg A. Active site ligand stabilization of quaternary structures of glutamine synthetase from Escherichia coli. J. Biol. Chem. 257 (1982) 7246-7251
16. Janson C.A., Kayne P.S., Almassy R.J., Grunstein M., and Eisenberg D. Sequence of glutamine synthetase from Salmonella typhimurium and implications for the protein structure. Gene 46 (1986) 297-300
17. Janssen P.J., Jones W.A., Jones D.T., and Woods D.R. Molecular analysis and regulation of the glnA gene of the Gram-positive anaerobe Clostridium acetobutylicum. J. Bacteriol. 170 (1988) 400-408
18. Reyes J.C., and Florencio F.J. A new type of glutamine synthetase in cyanobacteria: the protein encoded by the glnN gene supports nitrogen assimilation in Synechocystis sp. strain PCC 6803. J. Bacteriol. 176 (1994) 1260-1267
19. Wen Z.T., Peng L., and Morrison M. The glutamine synthetase of Prevotella bryantii B(1)4 is a family III enzyme (GlnN) and glutamine supports growth of mutants lacking glutamate dehydrogenase activity. FEMS Microbiol. Letters 229 (2003) 15-21
20. Goodman H.J.K., and Woods D.R. Cloning and nucleotide sequence of the Buyrivibrio fibrisolvens gene encoding a type III glutamine synthetase. J. Gen. Microbiol. 139 (1993) 1487-1493
21. Comet J.P., and Henry J. Pairwise sequence alignment using a PROSITE pattern-derived similarity score. Comput. Chem. 26 (2002) 421-436
22. Yamashita M.M., Almassy R.J., Janson C.A., Cascio D., and Eisenberg D. Refined atomic model of glutamine synthetase at 3.5 Å resolution. J. Biol. Chem. 264 (1989) 17681-17690
23. Kessel M., Frank J., and Goldfarb W. Averages of glutamine synthetase molecules as obtained with various stain and electron dose conditions. J. Supramol. Struct. 14 (1980) 405-422
24. Penczek P., Radermacher M., and Frank J. Three-dimensional reconstruction of single particles embedded in ice. Ultramicroscopy 40 (1992) 33-53
25. Valentine R.C., Shapiro B., and Stadtman E.R. Regulation of glutamine synthetase. xii. electron microscopy of the enzyme from Escherichia coli. Biochemistry 7 (1968) 2143-2152
26. Crespo J.L., Garcia-Dominguez M., and Florencio F.J. Nitrogen control of the glnN gene that codes for GS type III, the only glutamine synthetase in the cyanobacterium Pseudanabaena sp. PCC 6903. Mol. Microbiol. 30 (1998) 1101-1112
27. Southern J.A. Molecular genetic studies of Bacteroides fragilis. University of Cape Town (1986)
28. Thompson J.D., Higgins D.G., and Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22 (1994) 4673-4680
29. Sonnhammer E.L., Eddy S.R., and Durbin R. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins: Struct. Funct. Genet. 28 (1997) 405-420
30. Feng D.F., and Doolittle R.F. Progressive sequence alignment as a prerequisite to correct phylogenetic trees. J. Mol. Evol. 25 (1987) 351-360
31. Pettersen E.F., Goddard T.D., Huang C.C., Couch G.S., Greenblatt D.M., Meng E.C., and Ferrin T.E. UCSF Chimera-a visualization system for exploratory research and analysis. J. Comput. Chem. 25 (2004) 1605-1612
32. Backman K., Chen Y.-M., and Magasanik B. Physical and genetic characterization of the glnA-glnG region of the Escherichia coli chromosome. Proc. Natl Acad. Sci. USA 78 (1981) 3743-3747
33. Streicher S.L., and Tyler B. Purification of glutamine synthetase from a variety of bacteria. J. Bacteriol. 142 (1980) 69-78
34. Williams R.C., and Fisher H.W. Electron microscopy of TMV under conditions of minimal beam exposure. J. Mol. Biol. 52 (1970) 121-123
35. Crowther R.A., Henderson R., and Smith J.M. MRC image processing programs. J. Struct. Biol. 116 (1996) 9-16
36. Braig K., Otwinowski Z., Hegde R., Boisvert D.C., Joachimiak A., Horwich A.L., and Sigler P.B. The crystal structure of the bacterial chaperonin GroEL at 2.8 Å. Nature 371 (1994) 578-586
37. Frank J., Radermacher M., Penczek P., Zhu J., Li Y., Ladjadj M., and Leith A. SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116 (1996) 190-199
38. Smith J.M. Ximdisp-a visualization tool to aid structure determination from electron microscope images. J. Struct. Biol. 125 (1999) 223-228
39. Vagin A. MOLREP: an automated program for molecular replacement. J. Appl. Crystallog. 30 (1997) 1022-1025
40. Penczek P.A., Zhu J., and Frank J. A common-lines based method for determining orientations for N < 3 particle projections simultaneously. Ultramicroscopy 63 (1996) 205-218
41. Joyeux L., and Penczek P.A. Efficiency of 2D alignment methods. Ultramicroscopy 92 (2002) 33-46
42. van Heel M., and Harauz G. Resolution criteria for three dimensional reconstruction. Optik 73 (1986) 119-122
43. Wriggers W., Milligan R.A., and McCammon J.A. Situs: a package for docking crystal structures into low-resolution maps from electron microscopy. J. Struct. Biol. 125 (1999) 185-195
44. Mizuguchi K., Deane C.M., Blundell T.L., Johnson M.S., and Overington J.P. JOY: protein sequence-structure representation and analysis. Bioinformatics 14 (1998) 617-623
45. de Bakker P.I., Bateman A., Burke D.F., Miguel R.N., Mizuguchi K., Shi J., et al. HOMSTRAD: adding sequence information to structure-based alignments of homologous protein families. Bioinformatics 17 (2001) 748-749
46. McGuffin L.J., Bryson K., and Jones D.T. The PSIPRED protein structure prediction server. Bioinformatics 16 (2000) 404-405
47. Gill H.S., and Eisenberg D. The crystal structure of phosphinothricin in the active site of glutamine synthetase illuminates the mechanism of enzymatic inhibition. Biochemistry 40 (2001) 1903-1912
48. Colombo G., and Villafranca J.J. Amino acid sequence of Escherichia coli glutamine synthetase deduced from the DNA nucleotide sequence. J. Biol. Chem. 261 (1986) 10587-10591
49. Harth G., and Horwitz M.A. Expression and efficient export of enzymatically active Mycobacterium tuberculosis glutamine synthetase in Mycobacterium smegmatis and evidence that the information for export is contained within the protein. J. Biol. Chem. 272 (1997) 22728-22735
50. Gibbs C.S., Campbell K.E., and Wilson R.H. Sequence of a human glutamine synthetase cDNA. Nucleic Acids Res. 15 (1987) 6293
51. Caizzi R., Bozzetti M.P., Caggese C., and Ritossa F. Homologous nuclear genes encode cytoplasmic and mitochondrial glutamine synthetase in Drosophila melanogaster. J. Mol. Biol. 212 (1990) 17-26
52. Sato S., Nakamura Y., Kaneko T., Katoh T., Asamizu E., and Tabata S. Structural analysis of Arabidopsis thaliana chromosome 3. I. Sequence features of the regions of 4,504,864 bp covered by sixty P1 and TAC clones. DNA Res. 7 (2000) 131-135
53. Wood V., et al. The genome sequence of Schizosaccharomyces pombe. Nature 415 (2002) 871-880
54. Eisen J.A., et al. The complete genome sequence of Chlorobium tepidum TLS, a photosynthetic, anaerobic, green-sulfur bacterium. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 9509-9514
55. Reyes J.C., and Florencio F.J. A mutant lacking the glutamine synthetase gene (glnA) is impaired in the regulation of the nitrate assimilation system in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 176 (1994) 7516-7523
56. Xu J., Bjursell M.K., Himrod J., Deng S., Carmichael L.K., Chiang H.C., Hooper L.V., and Gordon J.I. A genomic view of the human-Bacteroides thetaiotaomicron symbiosis. Science 299 (2003) 2074-2076
57. Hill R.T., Parker J.R., Goodman H.J., Jones D.T., and Woods D.R. Molecular analysis of a novel glutamine synthetase of the anaerobe Bacteroides fragilis. J. Gen. Microbiol. 135 12 (1989) 3271-3279
58. Capela D., et al. Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 9877-9882
59. Chiurazzi M., Meza R., Lara M., Lahm A., Defez R., Iaccarino M., and Espin G. The Rhizobium leguminosarum biovar phaseoli glnT gene, encoding glutamine synthetase III. Gene 119 (1992) 1-8