Structural studies on the 2.25-MDa homomultimeric phosphoenolpyruvate synthase from Staphylothermus marinus

Journal of Structural Biology

Volumn 116, Issue 2, 1996, Pages 290-301

  Harauz, George ^a,c   Cicicopol, Christiana ^a   Hegerl, Reiner ^a   Cejka, Zdenka ^a   Goldie, Kenneth ^b   Santarius, Ute ^a   Engel, Andreas ^b   Baumeister, Wolfgang ^a  

^a MAX PLANCK INSTITUTE OF BIOCHEMISTRY   (Germany)

^b UNIVERSITY OF BASEL   (Switzerland)

^c UNIVERSITY OF GUELPH   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

PYRUVATE WATER DIKINASE; UNCLASSIFIED DRUG;

ARCHAEBACTERIUM; ARTICLE; ENZYME STRUCTURE; NONHUMAN; PRIORITY JOURNAL; ULTRASTRUCTURE;

EID: 0029977666     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1006/jsbi.1996.0044     Document Type: Article

References (72)

1. Adams, M. W. W. (1993) Enzymes and proteins from organisms that grow near and above 100°C, Annu. Rev. Microbiol. 47, 627-658.
2. Alpert, C.-A., Frank, R., Stüber, K., Deutscher, J., and Hengstenberg, W. (1985) Phosphoenolpyruvate-dependent protein kinase enzyme I of Streptococcus faecalis: Purification and properties of the enzyme and characterization of its active center, Biochemistry 24, 959-964.
3. Baumeister, W., and Lembcke, G. (1992) Structural features of archaebacterial cell envelopes, J. Bioenerg. Biomembr. 24, 567-575.
4. Bermann, K. M., and Cohn, M. (1970a) Phosphoenolpyruvate synthetase of Escherichia coli. Purification, some properties, and the role of divalent metal ions, J. Biol. Chem. 245, 5309-5318.
5. 18O exchange reaction, J. Biol. Chem. 245, 5319-5325.
6. Bremer, A., Henn, C., Engel, A., Baumeister, W., and Aebi, U. (1992) Has negative staining still a place in biomacromolecular electron microscopy? Ultramicroscopy 46, 85-111.
7. Calvo, J. M., Goodman, M., Salgo, M., and Capes, N. (1971) Salmonella locus affecting phosphoenolpyruvate synthase activity identified by a deletion analysis, J. Bacteriol. 106, 286-288.
8. Carroll, L. J., Xu, Y., Thrall, S. H., Martin, B. M., and Dunaway-Mariano, D. (1994) Substrate binding domains in pyruvate phosphate dikinase, Biochemistry 33, 1134-1142.
9. Cejka, Z., Kleinz, J., Santini, C., Hegerl, R., and Ghiretti Magaldi, A. (1992) The molecular architecture of the extracellular hemoglobin of Ophelia bicornis: Analysis of individual molecules, J. Struct. Biol. 109, 52-60.
10. Cicicopol, C., Peters, J., Kellermann, J., and Baumeister, W. (1994) Primary structure of a multimeric protein, homologous to the PEP-utilizing enzyme family and isolated from a thermophilic archaebacterium, FEBS Lett. 356, 345-350.
11. Cooper, R. A., and Kornberg, H. L. (1965) Net formation of phosphoenolpyruvate from pyruvate by Escherichia coli, Biochim. Biophys. Acta 104, 616-618.
12. Cooper, R. A., and Kornberg, H. L. (1969) Phosphoenolpyruvate synthetase, Methods Enzymol. 13, 309-314.
13. DeRosier, D., Oliver, R. M., and Reed, L. J. (1971) Crystallization and preliminary structural analysis of dihydrolipoyl transsuccinylase, the core of the 2-oxoglutarate dehydrogenase complex, Proc. Natl. Acad. Sci. USA 68, 1135-1137.
14. Ebina, S., Matsubara, K., Nagayama, K., Yamaki, M., and Gotoh, T. (1995) Carbohydrate gluing, an architectural mechanism in the supramolecular structure of an annelid giant hemoglobin, Proc. Natl. Acad. Sci. USA 92, 7367-7371.
15. Eigen, M. (with Winkler-Oswatitsch, R.) (1992) Steps towards Life: A Perspective on Evolution (P. Woolley, Trans). Oxford Univ. Press, Oxford, New York.
16. Engel, A. (1978) Molecular weight determination by scanning transmission electron microscopy, Ultramicroscopy 3, 273-281.
17. Engel, A., and Colliex, C. (1993) Application of scanning transmission electron microscopy to the study of biological structure, Curr. Opin. Biotech. 4, 403-411.
18. Eyzaguirre, J., Jansen, K., and Fuchs, G. (1982) Phosphoenolpyruvate synthetase in Methanobacterium thermoautotrophicum, Arch. Microbiol. 132, 67-74.
19. Frank, J. (1989) Image analysis of single macromolecules, Electron Microsc. Rev. 2, 53-74.
20. Frank, J. (1990) Classification of macromolecular assemblies studied as 'single particles,' Q. Rev. Biophys. 23, 281-329.
21. Frank, J., and Radermacher, M. (1992) Three-dimensional reconstruction of single particles negatively stained or in vitreous ice, Ultramicroscopy 46, 241-262.
22. Friedrich, P. (1984) Supramolecular Enzyme Organization: Quaternary Structure and Beyond, Pergamon Press, Oxford, Akadémiai Kiadó, Budapest.
23. Goodsell, D. S., and Olson, A. J. (1993) Soluble proteins: Size, shape and function, Trends Biochem. Sci. 18, 65-68.
24. Grenier, F. C., Reizer, J., Waygood, E. B., and Saier Jr., M. H. (1985) Evidence for covalently cross-linked dimers and trimers of enzyme I of the Escherichia coli phosphotransferase system, J. Bacteriol. 163, 243-247.
25. Hahn, T. (1983) International Tables for Crystallography, Vol. A, Space-Group Symmetry, The Int. Union of Crystallogr. and Reidel, Dordrecht, Holland.
26. Harauz, G., Boekema, E., and van Heel, M. (1988) Statistical image analysis of electron micrographs of ribosomal subunits, Methods Enzymol. 164, 35-49.
27. Hegerl, R. (1992) A survey of electron image processing packages, Ultramicroscopy 46, 417-423.
28. Jaenicke, R. (1991) Protein stability and molecular adaptation to extreme conditions, Eur. J. Biochem. 202, 715-728.
29. 60 capsid of heavy riboflavin synthase, Proteins: Struct. Funct. Genet. 5, 248-257.
30. Klotz, I. M., Darnall, D. W., and Langerman, N. R. (1975) Quaternary structure of proteins, in Neurath, H., Hill, R. L., and Boeder, C.-L. (Eds.), The Proteins, Vol. I, 3rd ed., pp 293-411, Academic Press, New York.
31. 60-capsid at 3.3 Å resolution, J. Mol. Biol. 203, 1045-1070.
32. Lupas, A., Koster, A. J., and Baumeister, W. (1993) Structural features of 26S and 20S proteasomes, Enzyme Protein 47, 252-273.
33. Maddox, J. (1993) The dark side of molecular biology, Nature 363, 13.
34. Marabini, R., and Carazo, J. M. (1994) Pattern recognition and classification of images of biological macromolecules using artificial neural networks, Biophys. J. 66, 1804-1814.
35. Matthews, B. W., and Bernhard, S. A. (1973) Structure and symmetry of oligomeric enzymes, Annu. Rev. Biophys. Bioeng. 2, 257-317.
36. McGuire, M., Herzberg, O., Yankie, L., Kapadia, G., Chen, C., Baker, A., and Dunaway-Mariano, D. (1995) Crystallographic studies of pyruvate phosphate dikinase, FASEB J. 9, A1433. [Abstract 1023]
37. McRee, D. E. (1993) Practical Protein Crystallography, p. 93, Academic Press, San Diego.
38. Milner, Y., Michaelis, G., and Wood, H. G. (1975) Pyruvate orthophosphate dikinase of Bacteroides symbiosus and Propionibacterium shermanii, Methods Enzymol. 42, 199-212.
39. Misset, O., Brouwer, M., and Robillard, G. T. (1980) Escherichia coli phosphoenolpyruvate-dependent phosphotransferase system. Evidence that the dimer is the active form of enzyme I, Biochemistry 19, 883-890.
40. Müller, S. A., Goldie, K. N., Büurki, R., Häring, R., and Engel, A. (1992) Factors influencing the precision of quantitative scanning transmission electron microscopy, Ultramicroscopy 46, 317-334.
41. Narindrasorasak, S., and Bridger, W. A. (1977) Phosphoenolpyruvate synthetase of Escherichia coli. Molecular weight, subunit composition, and identification of phosphohistidine in phosphoenzyme intermediate, J. Biol. Chem. 252, 3121-3127.
42. Niersbach, M., Kreuzaler, F., Geerse, R. H., Postma, P. W., and Hirsch, H. J. (1992) Cloning and nucleotide sequence of the Escherichia coli K-12 ppsA gene, encoding PEP synthase, Mol. Gen. Genet. 231, 332-336.
43. Ouzonis, C., Kyrpides, N., and Sander, C. (1995) Novel protein families in archaean genomes, Nucleic Acids Res. 23, 565-570.
44. Patnaik, R., Roof, W. D., Young, R. F., and Liao, J. C. (1992) Stimulation of glucose catabolism in Escherichia coli by a potential futile cycle, J. Bacteriol. 174, 7527-7532.
45. Peak, M. J., Peak, J. G., Stevens, F. J., Blamey, J., Mai, X., Zhou, Z. H., and Adams, M. W. W. (1994) The hyperthermophilic glycolytic enzyme enolase in the archaeon, Pyrococcus furiosus: Comparison with mesophilic enolases, Arch. Biochem. Biophys. 313, 280-286.
46. Penczek, P., Radermacher, M., and Frank, J. (1992) Three-dimensional reconstruction of single particles embedded in ice, Ultramicroscopy 40, 33-53.
47. Phipps, B. M., Hoffmann, A., Stetter, K. O., and Baumeister, W. (1991) A novel ATPase complex selectively accumulated upon heat shock is a major cellular component of thermophilic archaebacteria, The EMBO J. 10, 1711-1722.
48. Phipps, B. M., Typke, D., Hegerl, R., Volker, S., Hoffmann, A., Stetter, K. O., and Baumeister, W. (1993) Structure of a molecular chaperone from a thermophilic archaebacterium, Nature 361, 475-477.
49. Pocalyco, D. J., Carroll, L. J., Martin, B. M., Babbitt, P. C., and Dunaway-Mariano, D. (1990) Analysis of sequence homologies in plant and bacterial pyruvate phosphate dikinase, enzyme I of the bacterial phosphoenolpyruvate:sugar phosphotransferase system and other PEP-utilizing enzymes: Identification of potential catalytic and regulatory motifs, Biochemistry 29, 10757-10765.
50. Pühler, G., Weinkauf, S., Bachmann, L., Müller, S., Engel, A., Hegerl, R., and Baumeister, W. (1992) Subunit stoichiometry and three-dimensional arrangement in proteasomes from Thermoplasma acidophilum, EMBO J. 11, 1607-1616.
51. Rees, D. C., and Adams, M. W. W. (1995) Hyperthermophiles: Taking the heat and loving it, Structure 3, 251-254.
52. Reizer, J., Hoischen, C., Reizer, A., Pham, T. N., and Saier Jr., M. H. (1993) Sequence analysis and evolutionary relationships among the energy-coupling proteins Enzyme I and HPr of the bacterial phosphoenolpyruvate: sugar phosphotransferase system, Protein Sci. 2, 506-521.
53. Roeske, C. A., Kutny, R. M., Budde, R. J. A., and Chollet, R. (1988) Sequence of the phosphotreonyl regulatory site peptide from inactive maize leaf pyruvate, orthosphosphate dikinase, J. Biol. Chem. 263, 6683-6687.
54. Saibil, H. R., Zheng, D., Roseman, A. M., Hunter, A. S., Watson, G. M. F., Chen, S., auf der Mauer, A., O'Hara, B. P., Wood, S. P., Mann, N. H., Barnett, L. K., and Ellis, R. J. (1993) ATP induces large quaternary rearrangements in a cage-like chaperonin structure, Curr. Biol. 3, 265-273.
55. Saxton, W. O., and Baumeister, W. (1982) The correlation averaging of a regularly arranged bacterial cell envelope protein, J. Microsc. 127, 127-138.
56. Schäfer, T., and Schönheit, P. (1993) Gluconeogenesis from pyruvate in the hyperthermophilic archaeon Pyrococcus furiosus: Involvement of reactions of the Embden-Meyerhof pathway, Arch. Microbiol. 159, 354-363.
57. Schatz, M., and van Heel, M. G. (1990) Invariant classification of molecular views in electron micrographs, Ultramicroscopy 32, 255-264.
58. 4 metabolism in the chemoautotroph Alcaligenes eutrophus, J. Bacteriol. 159, 167-172.
59. Schurig, H., Rutkat, K., Rachel, R., and Jaenicke, R. (1995) Octameric enolase from the hyperthermophilic bacterium Thermotoga maritima: Purification, characterization, and image processing, Protein Sci. 4, 228-236.
60. Smyer, J. R., and Jeter, R. M. (1989) Characterization of phosphoenolpyruvate synthase mutants in Salmonella typhimurium, Arch. Microbiol. 153, 26-32.
61. Stryer, L. (1988) Biochemistry, 3rd ed., Freeman, New York.
62. Trent, J. D., Nimmesgern, E., Wall, J. S., Hartl, F. U. U., and Horwich, A. L. (1991) A molecular chaperone from a thermophilic archaebacterium is related to the eukaryotic protein t-complex polypeptide 1, Nature 354, 490-493.
63. van Heel, M. (1987) Similarity measures between images, Ultra-microscopy 21, 95-100.
64. van Heel, M., and Dube, P. (1994) Quaternary structure of multihexameric arthropod hemocyanins, Micron 25, 387-419.
65. van Heel, M., and Frank, J. (1981) Use of multivariate statistics in analysing the images of biological macromolecules, Ultramicroscopy 6, 187-194.
66. Verschoor, A., Frank, J., and Boublik, M. (1985) Investigation of 50S ribosomal subunit by electron microscopy and image analysis, J. Ultrastruct. Res. 92, 180-189.
67. Waygood, E. B., and Steeves, T. (1980) Enzyme I of the phosphoenolpyruvate:sugar phosphotransferase system of Escherichia coli. Purification to homogeneity and some properties, Can. J. Biochem. 58, 40-48.
68. Wenzel, T., and Baumeister, W. (1995) Conformational constraints in protein degradation by the 20S proteasome, Nature Struct. Biol. 2, 199-204.
69. Wood, H. G., O'Brien, W. E., and Michaels, G. (1977) Properties of carboxytransphosphorylase; pyruvate, phosphate dikinase; pyrophosphate-phosphofructokinase and pyrophosphate-acetate kinase and their roles in the metabolism of inorganic pyrophosphate, Adv. Enzymol. Relat. Areas Mol. Biol. 45, 85-155.
70. Wu, L.-F., and Saier, M. H., Jr. (1990) On the evolutionary origins of the bacterial phosphoenolpyruvate:sugar phosphotransferase system, Mol. Microbiol. 4, 1219-1222.
71. Wu, L.-F., Tomich, J. M., and Saier, M. H., Jr. (1990) Structure and evolution of a multidomain multiphosphoryl transfer protein. Nucleotide sequence of the fruB(HI) gene in Rhodobacter capsulatus and comparisons with homologous genes from other organisms, J. Mol. Biol. 213, 687-703.
72. Yoshida, H., and Wood, H. G., (1978) Crystalline pyruvate, phosphate dikinase from Bacteroides symbiosus, J. Biol. Chem. 253, 7650-7655.