The in situ architecture of Escherichia coli ribosomal RNA derived by electron spectroscopic imaging and three-dimensional reconstruction

Journal of Microscopy

Volumn 188, Issue 1, 1997, Pages 24-35

  Beniac, D R ^a   Czarnota, G J ^b   Rutherford, B L ^b   Ottensmeyer, F P ^b   Harauz, G ^a  

^a UNIVERSITY OF GUELPH   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

Author keywords

3D reconstruction; Electron spectroscopic imaging; Image analysis; Quaternions; Ribosomal RNA; Ribosomes

Indexed keywords

IMAGE RECONSTRUCTION; REPAIR; RNA; SPECTROSCOPIC ANALYSIS;

3D RECONSTRUCTION; ELECTRON SPECTROSCOPIC IMAGING; IMAGE-ANALYSIS; PHOSPHATE BACKBONE; QUATERNION; RIBOSOMAL RNA; RIBOSOMAL SUBUNITS; RIBOSOME; THREE-DIMENSIONAL RECONSTRUCTION; TWO-DIMENSIONS;

ESCHERICHIA COLI;

RIBOSOME RNA;

ARTICLE; ELECTRON MICROSCOPY; ESCHERICHIA COLI; IMAGE ANALYSIS; IMAGE RECONSTRUCTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RNA STRUCTURE; SPECTROSCOPY; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING;

EID: 0030707855     PISSN: 00222720     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2818.1997.2370795.x     Document Type: Article

References (78)

1. Adamson-Sharpe, K.M. & Ottensmeyer, F.P. (1981) Spatial resolution and detection sensitivity in microanalysis by electron energy loss selected imaging. J. Microsc. 122, 309-314.
2. Agrawal, R.K., Penczek, P., Grassucci, R.A., Li, Y., Leith, A., Nierhaus, K.H. & Frank, J. (1996) Direct visualization of A-, P-, and E-site transfer RNAs in the Escherichia coli ribosomes. Science, 271, 1000-1002.
3. Andrews, D.W., Walter, P. & Ottensmeyer, F.P. (1987) Evidence for an extended 7SL RNA structure in the signal recognition particle. EMBO J. 6, 3471-3477.
4. Aoyama, K., Ogawa, K., Kimura, Y. & Fujiyoshi, Y. (1995) A method for 2D crystallization of soluble proteins at liquid-liquid interface. Ultramicroscopy, 57, 345-354.
5. Avila-Sakar, A.J., Guan, T.-L., Arad, T., Schmid, M.F., Loke, T.W., Yonath, A., Piefke, J., Franceschi, F. & Chiu, W. (1994) Electron cryomicroscopy of Bacillus stearothermophilus 50S ribosomal subunits crystallized on phospholipid monolayers. J. Mol. Biol. 239, 689-697.
6. Baumeister, W. (1982) Towards higher resolution in biomolecular electron microscopy. Ultramicroscopy, 9, 151-158.
7. Bazett-Jones, D.P. (1993) Empirical basis for phosphorus mapping in DNA:protein complexes by electron spectroscopic imaging. Microbeam Anal. J. 2, 69-79.
8. Bazett-Jones, D.P., Leblanc, B., Herfort, M. & Moss, T. (1994) Short-range DNA looping by the Xenopus HMG-box transcription factor. xUBF. Science. 264, 1134-1137.
9. Bazett-Jones, D.P., Locklear, L. & Rattner, J. (1988) Electron spectroscopic imaging of DNA. J. Ultrastruct. Mol. Struct. Res. 99, 48-58.
10. Bazett-Jones, D.P., Mendez, E., Czarnota, G.J., Ottensmeyer, F.P. & Allfrey, V.G. (1996) Visualisation of unfolded nucleosomes associated with transcribing chromatin. Nucleic Acids Res. 24, 321-329.
11. Bazett-Jones, D.P. & Ottensmeyer, F.P. (1981) Phosphorus distribution in the nucleosome. Science, 211, 169-170.
12. Beniac, D.R., Czarnota, G.J., Bartlett, T.A., Rutherford, B.L., Ottensmeyer, F.P. & Harauz, G. (1997a) Challenges of three-dimensional reconstruction of ribonucleoprotein complexes from electron spectroscopic images - Reconstructing ribosomal RNA. Scan. Electron Microsc. Suppl. 11, in press.
13. Beniac, D.R., Czarnota, G.J., Rutherford, B.L., Ottensmeyer, F.P. & Harauz, G. (1997b) Three-dimensional architecture of Thermomyces lanuginosus small subunit ribosomal RNA. Micron, 28, 13-20.
14. Beniac, D.R. & Harauz, G. (1993) Visualisation of E. coli ribosomal RNA in situ by electron spectroscopic imaging and image averaging. Micron, 24, 163-171.
15. Beniac, D.R. & Harauz, G. (1995) Structures of small subunit ribosomal RNAs in situ from Escherichia coli and Thermomyces lanuginosus. Mol. Cell. Biochem. 148, 165-181.
16. Beniac, D.R., Luckevich, M.D., Czarnota, G.J., Tompkins, T.A., Ridsdale, R.A., Ottensmeyer, F.P., Moscarello, M.A. & Harauz, G. (1997c) Three-dimensional structure of myelin basic protein. I. Reconstruction via angular reconstitution of randomly oriented single particles. J. Biol. Chem. 272, 4261-4268.
17. Boublik, M., Mandiyan, V., Tumminia, S., Hainfeld, J.F. & Wall, J.S. (1990) Structural analysis of ribosomal particles from Escherichia coli by scanning transmission electron microscopy. Proc. XIIth International Congress for Electron Microscopy, Vol. 3 (ed. by L. D. Peachey and D. B. Williams), pp. 134-135. San Francisco Press, San Francisco.
18. Boublik, M., Oostergetel, G.T., Frankland, B. & Ottensmeyer, F.P. (1984) Topographical mapping of ribosomal RNAs in situ by electron spectroscopic imaging. Proc. 42nd Annual Meeting of the Electron Microscopy Society of America (ed. by G. W. Bailey), pp. 690-691. San Francisco Press, San Francisco.
19. Boublik, M. & Wall, J. (1992) Structure of rRNA in the ribosome. Proc. 50th Annual Meeting of the Electron Microscopy Society of America (ed. by G. W. Bailey, J. Bentley and J. A. Small), pp. 462-463. San Francisco Press, San Francisco.
20. Bremer, A., Henn, C., Engel, A., Baumeister, W. & Aebi, U. (1992) Has negative staining still a place in biomacromolecular electron microscopy? Ultramicroscopy, 46, 85-111.
21. Brimacombe, R. (1995) The structure of ribosomal RNA: a three-dimensional jigsaw puzzle. Eur. J. Biochem. 230, 365-383.
22. Capel, M.S., Kjeldgaard, M., Engelman, D. & Moore, P. (1988) Positions of, S2, S13, S16, S17, S19 and S21 in the 30S ribosomal subunit of Escherichia coli. J. Mol. Biol. 200, 65-87.
23. Czarnota, G.J., Andrews, D.W., Farrow, N.A. & Ottensmeyer, F.P. (1994) A structure for the signal sequence binding protein SRP54: 3D reconstruction from STEM images of single molecules. J. Struct. Biol. 113, 35-46.
24. Czarnota, G.J. & Ottensmeyer, F.P. (1996) Structural states of the nucleosome. J. Biol. Chem. 271, 3677-3683.
25. Egerton, R.F. (1988) A simple parameterization scheme for innershell cross sections. Proc. 46th Annual Meeting of the Electron Microscopy Society of America (ed. by G. W. Bailey), pp. 532-533. San Francisco Press, San Francisco.
26. Egerton, R.F. (1996) Electron Energy-Loss Spectroscopy in the Electron Microscope, 2nd edn. Plenum Press, New York.
27. Engel, A. & Colliex, C. (1993) Application of scanning transmission electron microscopy to the study of biological structure. Curr. Opin. Biotechnol. 4, 403-411.
28. Engel, A. & Meyer, J. (1980) Preparation of unstained protein structures for mass determination by electron scattering. J. Ultrastruct. Res. 72, 212-222.
29. Farrow, N.A. & Ottensmeyer, F.P. (1992) A posteriori determination of relative projection directions of arbitrarily oriented macromolecules. J. Opt. Soc. Am. A, 9, 1749-1760.
30. Farrow, N.A. & Ottensmeyer, F.P. (1993) Automatic 3D alignment of projection images of randomly oriented objects. Ultramicroscopy. 52, 141-156, 1993.
31. Fiori, C.E., Leapman, R.D., Swyt, C.R. & Andrews, S.B. (1988) Quantitative x-ray mapping of biological sections. Ultramicroscopy. 24, 237-250.
32. Fowler, W. E. & Aebi, U. (1983) Preparation of single molecules and supramolecular complexes for high resolution metal shadowing. J. Ultrastruct. Res. 83, 319-334.
33. Frank, J. (1996) Three-Dimensional Electron Microscopy of Macromolecular Assemblies. Academic Press, New York.
34. Frank, J. & Penczek, P. (1995) On the correction of the contrast transfer function in biological electron microscopy. Optik, 98, 125-129.
35. Frank, J., Verschoor, A., Li, Y., Zhu, J., Lata, R.K., Radermacher, M., Penczek, P., Grassucci, R., Agrawal, R.K. & Srivastava, S. (1995a) A model of the translational apparatus based on a three-dimensional reconstruction of the Escherichia coli ribosome. Biochem. Cell Biol. 73, 757-765.
36. Frank, J., Zhu, J., Penezek, P., Li, Y., Srivastava, S., Verschoor, A., Radermacher, M., Grassucci, R., Lata, R.K. & Agrawal, R.K. (1995b) A model of protein synthesis based on cryo-electron microscopy of the E. coli ribosome. Nature, 376, 441-444.
37. Harauz, G. & Ottensmeyer, F.P. (1984) Nucleosome reconstruction via phosphorus mapping. Science, 226, 936-940.
38. Harauz, G., Stöffler-Meilicke, M. & van Heel, M. (1987) Characteristic views of prokaryotic 50S ribosomal subunits. J. Mol. Evol. 26, 347-357.
39. Harauz, G. & van Heel, M. (1986) Exact filters for general geometry three-dimensional reconstruction. Optik, 73, 146-156.
40. Harris, J.R. (1997) Negative Staining and Cryoelectron Microscopy. Bios Scientific Publishers, Oxford.
41. van Heel, M. (1987a) Similarity measures between images. Ultramicroscopy. 21, 95-100.
42. van Heel, M. (1987b) Angular reconstitution: a posteriori assignment of projection directions for 3D reconstruction. Ultramicroscopy 21, 111-124.
43. van Heel, M., Harauz, G., Orlova, E.V., Schmidt, R. & Schatz, M. (1996) The next generation of the IMAGIC image processing system. J. Struct. Biol. 116, 17-24.
44. van Heel, M. & Stöffler-Meilicke, M. (1985) Characteristic views of E. coli and B. stearothermophilus 30S ribosomal subunits in the electron microscope. EMBO J. 4, 2389-2395.
45. Heng, Y.-M., Simon, G.T., Boublik, M. & Ottensmeyer, F.P. (1990) Experimental ionization cross-sections of phosphorus and calcium by electron spectroscopic imaging. J. Microsc. 160, 161-171.
46. Korn, A.P. (1980) Dark field electron microscopy of the 30S subunit of the E. coli ribosome. Ultramicroscopy 5, 513-520.
47. Korn, A.P., Spitnik-Elson, P., Elson, D. & Ottensmeyer, F.P. (1983) Specific visualization of ribosomal RNA in the intact ribosome by electron spectroscopic imaging. Eur. J. Cell Biol. 31, 334-340.
48. Kühlbrandt, W. & Unwin, P.N.T. (1982) Distribution of RNA and protein in crystalline eukaryotic ribosomes. J. Mol. Biol. 156, 431-448.
49. Lata, K.R., Agrawal, R.K., Penczek, P., Grassucci, R., Zhu, J. & Frank, J. (1996) Three-dimensional reconstruction of the Escherichia coli 30S ribosomal subunit in ice. J. Mol. Biol. 262, 43-52.
50. LeFurgey, A., Davilla, S.D., Kopf, D.A., Sommer, J.R. & Ingram, P. (1992) Real-time quantitative elemental analysis and mapping: microchemical imaging in cell physiology. J. Microsc. 165, 191-223.
51. Malhotra, A., Gabb, H.A. & Harvey, S.C. (1993) Modeling large nucleic acids. Curr. Opin. Struct. Biol. 3, 241-246.
52. Malhotra, A. & Harvey, S.C. (1994) A quantitative model of the Escherichia coli 16S RNA in the 30S ribosomal subunit. J. Mol. Biol. 240, 308-340.
53. May, R.P., Nowotny, V., Nowotny, P., Voss, H. & Nierhaus, K.H. (1992) Inter-protein distances within the large subunit from Escherichia coli ribosomes. EMBO J. 11, 373-378.
54. Moore, P.B. (1988) The ribosome returns. Nature, 31, 223-227.
55. Mueller, F., Döring, T., Erdemir, T., Greuer, B., Jünke, N., Osswald, M., Rinke-Appel, J., Stade, K., Thamm, S. & Brimacombe, R. (1995) Getting closer to an understanding of the three-dimensional structure of ribosomal RNA. Biochem. Cell Biol. 73, 767-773.
56. Nierhaus, K.H. (1991) The assembly of prokaryotic ribosomes. Biochimie, 73, 739-755.
57. Ottensmeyer, F.P. (1982) Scattered electrons in microscopy and microanalysis. Science, 215, 461-466.
58. Ottensmeyer, F.P. (1984) Electron spectroscopic imaging: parallel energy filtering and microanalysis in the fixed-beam electron microscope. J. Ultrastruct. Res. 88, 121-134.
59. Ottensmeyer, F.P. (1986a) Elemental mapping by energy filtration: advantages, limitations, and compromises. Ann. N.Y. Acad. Sci. 483, 339-353.
60. Ottensmeyer, F.P. (1986b) Scattered electrons in biological structure determination. Examining the Submicron World (ed. by R. Feder and W. MacGowan), pp. 137-151. Plenum, New York.
61. Ottensmeyer, F.P. & Andrew, J.W. (1980) High resolution microanalysis of biological specimens by electron energy loss spectroscopy and by electron spectroscopic imaging. J. Ultrastruct. Res. 72, 336-348.
62. Penczek, P., Grassucci, R.A. & Frank, J. (1994) The ribosome at improved resolution: new techniques for merging and orientation refinement in 3D cryo-electron microscopy of biological particles. Ultramicroscopy, 53, 251-270.
63. Radermacher, M., Wagenknecht, T., Verschoor, A. & Frank, J. (1985) A new reconstruction scheme applied to the 50S ribosomal subunit of E. coli. J. Microsc. 141, RP1-RP2.
64. Shuman, H., Chang, C.-F., Buhle, E.L. Jr. & Somlyo, A.P. (1986) Electron energy-loss spectroscopy: quantitation and imaging. Ann. N.Y. Acad. Sci. 483, 295-310.
65. Somlyo, A.V., Shuman, H. & Somlyo, A.P. (1981) Electron probe analysis of cardiac, skeletal, and vascular smooth muscle. Microprobe Analysis of Biological Systems (ed. by T. E. Hutchison and A. P. Somlyo). pp. 103-126. Academic Press, New York.
66. Stade, K., Jünke, N. & Brimacombe, R. (1995) Mapping the path of the nascent chain through the 23S rRNA in the 50S ribosomal subunit. Nucleic Acids Res. 23, 2371-2380.
67. Stark, H., Mueller, F., Orlova, E.V., Schatz, M., Duve, P., Erdemir, T., Zemlin, F., Brimacombe, R. & van Heel, M. (1995) The 70S Escherichia coli ribosome at 23 Å resolution: fitting the ribosomal RNA. Structure. 3, 815-821.
68. Stark, H., Orlova, E.V., Rinke-Appel. J., Jünke, N., Mueller, F., Rodnina, M., Wintermeyer, W., Brimacombe, R. & van Heel, M. (1997) Arrangement of tRNAs in pre- and posttranslocational ribosomes revealed by electron cryomicroscopy. Cell, 88, 19-28.
69. Stöffler, G. & Stöffler-Meilicke, M. (1983) Ultrastructure of macromolecular complexes studied with antibodies. Modern Methods in Protein Chemistry (ed. by H. Tschesche). pp. 409-455. Walter de Gruyter, Berlin.
70. Stöffler, G. & Wittmann, H.-G (1971) Ribosomal proteins XXV. Immunological studies on Escherichia coli ribosomal proteins. J. Mol. Biol. 62, 407-409.
71. Stöffler-Meilicke, M. & Stöffler, G. (1990) Topography of the ribosomal proteins from Escherichia coli within the intact subunits as determined by immunoelectron microscopy and protein-protein cross-linking. The Ribosome, Structure, Function, and Evolution (ed. by W. E. Hill, A. Dahlberg, R. A. Garrett, P. B. Moore, D. Schlessinger and J. R. Warner), pp. 123-133. American Society for Microbiology, Washington, DC.
72. Stöffler-Meilicke, M., Stöffler, G., Odom, O.W., Zinn, A., Kramer, G. & Hardesty, B. (1981) Localization of 3′ ends of 5S and 23S rRNAs in reconstituted subunits of Escherichia coli ribosomes. Proc. Natl. Acad. Sci. USA, 78, 5538-5542.
73. Svergun, D.I., Pedersen, J., Serdyuk, I.N. & Koch, M.H.J. (1994) Solution scattering from 50S ribosomal subunit resolves inconsistency between electron microscopic models. Proc. Natl. Acad. Sci. USA, 91, 11826-11830.
74. Tumminia, S.J., Hellmann, W., Wall, J.S. & Boublik, M. (1994) Visualization of protein-nucleic acid interactions involved in the in vitro assembly of the Escherichia coli 50S ribosomal subunit. J. Mol. Biol. 235, 1239-1250.
75. Tumminia, S.J., Mandiyan, V., Wall, J.S. & Boublik, M. (1991) Heterogeneity of Escherichia coli ribosomes established by scanning transmission electron microscopy. Biochimie, 73, 919-925.
76. Vainshtein, B.K. & Goncharov, A.B. (1986) Determination of the spatial orientation of arbitrarily arranged identical particles of an unknown structure from their projections. Proc. XIth International Congress on Electron Microscopy. Kyoto (ed. by T. Imura, S. Maruse and T. Suzuki), pp. 459-460. Japanese Society for Electron Microscopy. Tokyo.
77. Walleczek, J., Schüler, D., Stöffler-Melicke, M., Brimacombe, R. & Stöffler, G. (1988) A model for the spatial arrangement of the proteins in the large subunit of the Escherichia coli ribosome. EMBO J. 11, 3571-3576.
78. Wildhaber, I., Gross, H., Engel, A. & Baumeister, W. (1985) The effects of air-drying and freeze-drying on the structure of a regular protein layer. Ultramicroscopy. 16, 411-422.