Structural analysis of Mycoplasma pneumoniae by cryo-electron tomography

Journal of Structural Biology

Volumn 156, Issue 2, 2006, Pages 342-354

  Seybert, Anja ^a   Herrmann, Richard ^b   Frangakis, Achilleas S ^a  

^a EUROPEAN MOLECULAR BIOLOGY LABORATORY   (Germany)

^b UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Image processing; Template matching

Indexed keywords

CELL SURFACE PROTEIN;

ARTICLE; BIOINFORMATICS; CELL MEMBRANE; COMPLEX FORMATION; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ELECTRON; EVALUATION; HYPOTHESIS; MACROMOLECULE; MYCOPLASMA PNEUMONIAE; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; RELIABILITY; RIBOSOME; STRUCTURE ANALYSIS; TOMOGRAPHY;

ANTIGENS, SURFACE; CELL DIVISION; CELL SURFACE EXTENSIONS; CRYOELECTRON MICROSCOPY; IMAGING, THREE-DIMENSIONAL; MODELS, BIOLOGICAL; MODELS, MOLECULAR; MYCOPLASMA PNEUMONIAE; RIBOSOMES; TOMOGRAPHY, X-RAY COMPUTED;

EUKARYOTA; MYCOPLASMA; MYCOPLASMA PNEUMONIAE; MYCOPLASMATALES; PROKARYOTA;

EID: 33750512775     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2006.04.010     Document Type: Article

References (71)

1. Al-Amoudi A., Chang J.J., Leforestier A., McDowall A., Salamin L.M., Norlen L.P., Richter K., Blanc N.S., Studer D., and Dubochet J. Cryo-electron microscopy of vitreous sections. Embo. J. 23 (2004) 3583-3588
2. Al-Amoudi A., Norlen L.P., and Dubochet J. Cryo-electron microscopy of vitreous sections of native biological cells and tissues. J. Struct. Biol. 148 (2004) 131-135
3. Aloy P., Bottcher B., Ceulemans H., Leutwein C., Mellwig C., Fischer S., Gavin A.C., Bork P., Superti-Furga G., Serrano L., and Russell R.B. Structure-based assembly of protein complexes in yeast. Science 303 (2004) 2026-2029
4. Ausmees N., Kuhn J.R., and Jacobs-Wagner C. The bacterial cytoskeleton: an intermediate filament-like function in cell shape. Cell 115 (2003) 705-713
5. Balish M.F., Santurri R.T., Ricci A.M., Lee K.K., and Krause D.C. Localization of Mycoplasma pneumoniae cytadherence-associated protein HMW2 by fusion with green fluorescent protein: implications for attachment organelle structure. Mol. Microbiol. 47 (2003) 49-60
6. Baseman J.B., Cole R.M., Krause D.C., and Leith D.K. Molecular basis for cytadsorption of Mycoplasma pneumoniae. J. Bacteriol. 151 (1982) 1514-1522
7. Boatman E.S. Morphology and ultrastructure of the mycoplasmatales. In: Barile M.F., and Razin S. (Eds). The Mycoplasmas vol. 1 (1979), Academic Press, New York 63-102
8. Bohm J., Frangakis A.S., Hegerl R., Nickell S., Typke D., and Baumeister W. Toward detecting and identifying macromolecules in a cellular context: template matching applied to electron tomograms. Proc. Natl. Acad. Sci. USA 97 (2000) 14245-14250
9. Bredt W. Motility and multiplication of Mycoplasma pneumoniae. A phase contrast study. Pathol. Microbiol. (Basel) 32 (1968) 321-326
10. Bremer H., and Dennis P.P. Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt F.C. (Ed). Escherichia coli and Salmonella: Cellular and Molecular Biology vol. 2 (1996), Springer, Berlin 1527-1542
11. Carson, J.L., Hu, P.C., Collier, A.M., 1992. Cell structural and functional elements. In: Maniloff, J., McElhaney, R.N., Finch, L.R., Baseman, J.B. (Eds.), Mycoplasmas: Molecular Biology and Pathogenesis. Am. Soc. Microbiol. Washington, DC, pp. 63-72.
12. Cheutin T., O'Donohue M.F., Beorchia A., Klein C., Kaplan H., and Ploton D. Three-dimensional organization of pKi-67: a comparative fluorescence and electron tomography study using FluoroNanogold. J. Histochem. Cytochem. 51 (2003) 1411-1423
13. Crowther R.A., Amos L.A., Finch J.T., De Rosier D.J., and Klug A. Three dimensional reconstructions of spherical viruses by fourier synthesis from electron micrographs. Nature 226 (1970) 421-425
14. Dandekar T., Huynen M., Regula J.T., Ueberle B., Zimmermann C.U., Andrade M.A., Doerks T., Sanchez-Pulido L., Snel B., Suyama M., Yuan Y.P., Herrmann R., and Bork P. Re-annotating the Mycoplasma pneumoniae genome sequence: adding value, function and reading frames. Nucleic Acids Res. 28 (2000) 3278-3288
15. Dierksen K., Typke D., Hegerl R., Koster A.J., and Baumeister W. Towards automatic electron tomography. Ultramicroscopy 40 (1992) 71-87
16. Feldner J., Gobel U., and Bredt W. Mycoplasma pneumoniae adhesin localized to tip structure by monoclonal antibody. Nature 298 (1982) 765-767
17. Fisseha M., Gohlmann H.W., Herrmann R., and Krause D.C. Identification and complementation of frameshift mutations associated with loss of cytadherence in Mycoplasma pneumoniae. J. Bacteriol. 181 (1999) 4404-4410
18. Forster F., Medalia O., Zauberman N., Baumeister W., and Fass D. Retrovirus envelope protein complex structure in situ studied by cryo-electron tomography. Proc. Natl. Acad. Sci. USA 102 (2005) 4729-4734
19. Frangakis A.S., Bohm J., Forster F., Nickell S., Nicastro D., Typke D., Hegerl R., and Baumeister W. Identification of macromolecular complexes in cryoelectron tomograms of phantom cells. Proc. Natl. Acad. Sci. USA 99 (2002) 14153-14158
20. Frangakis A.S., and Forster F. Computational exploration of structural information from cryo-electron tomograms. Curr. Opin. Struct. Biol. 14 (2004) 325-331
21. Frangakis A.S., and Hegerl R. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135 (2001) 239-250
22. Gabashvili I.S., Agrawal R.K., Spahn C.M., Grassucci R.A., Svergun D.I., Frank J., and Penczek P. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100 (2000) 537-549
23. Gaietta G., Deerinck T.J., Adams S.R., Bouwer J., Tour O., Laird D.W., Sosinsky G.E., Tsien R.Y., and Ellisman M.H. Multicolor and electron microscopic imaging of connexin trafficking. Science 296 (2002) 503-507
24. Glaser, G., Hyman, H.C., Razin, S., 1992. Ribosomes. In: Maniloff, J., McElhaney, R.N., Finch, L.R.,Baseman, J.B. (Eds.), Mycoplasmas: Molecular Biology and Pathogenesis. Am. Soc. Microbiol. Washington, DC, pp. 169-177.
25. Gobel U., Speth V., and Bredt W. Filamentous structures in adherent Mycoplasma pneumoniae cells treated with nonionic detergents. J. Cell Biol. 91 (1981) 537-543
26. Grabenbauer M., Geerts W.J.C., Fernadez-Rodriguez J., Hoenger A., Koster A.J., and Nilsson T. Correlative microscopy and electron tomography of GFP through photooxidation. Nat. Methods 2 (2005) 857-862
27. Grunewald K., Desai P., Winkler D.C., Heymann J.B., Belnap D.M., Baumeister W., and Steven A.C. Three-dimensional structure of herpes simplex virus from cryo-electron tomography. Science 302 (2003) 1396-1398
28. Hayflick L. Tissue cultures and mycoplasmas. Tex. Rep. Biol. Med. 23 Suppl. 1 (1965) 285
29. Hegerl R., and Hoppe W. Influence of electron noise on three-dimensional image reconstruction. Z. Naturforschung 31a (1976) 1717-1721
30. Hegermann, J., 2003. Untersuchungen von Cytoskelett-Komponenten und Motilität bei Mycoplasma pneumoniae. Mathematisch-Naturwissenschaftliche Fakultäten. Georg-August-Universität, Göttingen (Germany).
31. Hegermann J., Herrmann R., and Mayer F. Cytoskeletal elements in the bacterium Mycoplasma pneumoniae. Naturwissenschaften 89 (2002) 453-458
32. Henderson R. The potential and limitations of neutrons, electrons and X-rays for atomic resolution microscopy of unstained biological molecules. n. 28 (1995) 171-193
33. Hu P.C., Cole R.M., Huang Y.S., Graham J.A., Gardner D.E., Collier A.M., and Clyde Jr. W.A. Mycoplasma pneumoniae infection: role of a surface protein in the attachment organelle. Science 216 (1982) 313-315
34. Jaffe J.D., Berg H.C., and Church G.M. Proteogenomic mapping as a complementary method to perform genome annotation. Proteomics 4 (2004) 59-77
35. Kammer G.M., Pollack J.D., and Klainer A.S. Scanning-beam electron microscopy of Mycoplasma pneumoniae. J. Bacteriol. 104 (1970) 499-502
36. Kenri T., Seto S., Horino A., Sasaki Y., Sasaki T., and Miyata M. Use of fluorescent-protein tagging to determine the subcellular localization of Mycoplasma pneumoniae proteins encoded by the cytadherence regulatory locus. J. Bacteriol. 186 (2004) 6944-6955
37. Keseler I.M., Collado-Vides J., Gama-Castro S., Ingraham J., Paley S., Paulsen I.T., Peralta-Gil M., and Karp P.D. EcoCyc: a comprehensive database resource for Escherichia coli. Nucleic Acids Res. 33 (2005) D334-D337
38. Kirchhoff, H., 1992. Motility. In Maniloff, J., McElhaney, R.N., Finch, L.R. and Baseman, J.B. (Eds.), Mycoplasmas: Molecular Biology and Pathogenesis. Am. Soc. Microbiol. Washington, DC, pp. 289-306.
39. Koster A.J., Chen H., Sedat J.W., and Agard D.A. Automated microscopy for electron tomography. Ultramicroscopy 46 (1992) 207-227
40. Krause D.C., and Balish M.F. Cellular engineering in a minimal microbe: structure and assembly of the terminal organelle of Mycoplasma pneumoniae. Mol. Microbiol. 51 (2004) 917-924
41. Krause D.C., Proft T., Hedreyda C.T., Hilbert H., Plagens H., and Herrmann R. Transposon mutagenesis reinforces the correlation between Mycoplasma pneumoniae cytoskeletal protein HMW2 and cytadherence. J. Bacteriol. 179 (1997) 2668-2677
42. Kurner J., Frangakis A.S., and Baumeister W. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307 (2005) 436-438
43. Layh-Schmitt G., and Herrmann R. Spatial arrangement of gene products of the P1 operon in the membrane of Mycoplasma pneumoniae. Infect. Immun. 62 (1994) 974-979
44. Layh-Schmitt G., Podtelejnikov A., and Mann M. Proteins complexed to the P1 adhesin of Mycoplasma pneumoniae. Microbiology 146 Pt. 3 (2000) 741-747
45. Lowe J., van den Ent F., and Amos L.A. Molecules of the bacterial cytoskeleton. Annu. Rev. Biophys. Biomol. Struct. 33 (2004) 177-198
46. McBride M.J. Bacterial gliding motility: multiple mechanisms for cell movement over surfaces. Annu. Rev. Microbiol. 55 (2001) 49-75
47. McEwen B.F., Downing K.H., and Glaeser R.M. The relevance of dose-fractionation in tomography of radiation-sensitive specimens. Ultramicroscopy 60 (1995) 357-373
48. McIntosh R., Nicastro D., and Mastronarde D. New views of cells in 3D: an introduction to electron tomography. Trends Cell Biol. 15 (2005) 43-51
49. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., and Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 298 (2002) 1209-1213
50. Meng K.E., and Pfister R.M. Intracellular structures of Mycoplasma pneumoniae revealed after membrane removal. J. Bacteriol. 144 (1980) 390-399
51. Miyata M., Ryu W.S., and Berg H.C. Force and velocity of Mycoplasma mobile gliding. J. Bacteriol. 184 (2002) 1827-1831
52. Miyata M., and Uenoyama A. Movement on the cell surface of the gliding bacterium, Mycoplasma mobile, is limited to its head-like structure. FEMS Microbiol. Lett. 215 (2002) 285-289
53. Nicastro D., Frangakis A.S., Typke D., and Baumeister W. Cryo-electron tomography of neurospora mitochondria. J. Struct. Biol. 129 (2000) 48-56
54. Nickell S., Kofler C., Leis A.P., and Baumeister W. A visual approach to proteomics. Nat. Rev. Mol. Cell Biol. 7 (2006) 225-230
55. Radestock U., and Bredt W. Motility of Mycoplasma pneumoniae. J. Bacteriol. 129 (1977) 1495-1501
56. Rath B.K., Marko M., Radermacher M., and Frank J. Low-dose automated electron tomography: a recent implementation. J. Struct. Biol. 120 (1997) 210-218
57. Razin S., Yogev D., and Naot Y. Molecular biology and pathogenicity of mycoplasmas. Microbiol. Mol. Biol. Rev. 62 (1998) 1094-1156
58. Regula J.T., Boguth G., Gorg A., Hegermann J., Mayer F., Frank R., and Herrmann R. Defining the mycoplasma 'cytoskeleton': the protein composition of the Triton X-100 insoluble fraction of the bacterium Mycoplasma pneumoniae determined by 2-D gel electrophoresis and mass spectrometry. Microbiology 147 (2001) 1045-1057
59. Regula J.T., Ueberle B., Boguth G., Gorg A., Schnolzer M., Herrmann R., and Frank R. Towards a two-dimensional proteome map of Mycoplasma pneumoniae. Electrophoresis 21 (2000) 3765-3780
60. Seto S., Kenri T., Tomiyama T., and Miyata M. Involvement of P1 adhesin in gliding motility of Mycoplasma pneumoniae as revealed by the inhibitory effects of antibody under optimized gliding conditions. J. Bacteriol. 187 (2005) 1875-1877
61. Seto S., Layh-Schmitt G., Kenri T., and Miyata M. Visualization of the attachment organelle and cytadherence proteins of Mycoplasma pneumoniae by immunofluorescence microscopy. J. Bacteriol. 183 (2001) 1621-1630
62. Seto S., and Miyata M. Attachment organelle formation represented by localization of cytadherence proteins and formation of the electron-dense core in wild-type and mutant strains of Mycoplasma pneumoniae. J. Bacteriol. 185 (2003) 1082-1091
63. Stevens M.K., and Krause D.C. Disulfide-linked protein associated with Mycoplasma pneumoniae cytadherence phase variation. Infect. Immun. 58 (1990) 3430-3433
64. Stevens M.K., and Krause D.C. Localization of the Mycoplasma pneumoniae cytadherence-accessory proteins HMW1 and HMW4 in the cytoskeleton like Triton shell. J. Bacteriol. 173 (1991) 1041-1050
65. Stevens M.K., and Krause D.C. Mycoplasma pneumoniae cytadherence phase-variable protein HMW3 is a component of the attachment organelle. J. Bacteriol. 174 (1992) 4265-4274
66. Uenoyama A., and Miyata M. Gliding ghosts of Mycoplasma mobile. Proc. Natl. Acad. Sci. USA 102 (2005) 12754-12758
67. Waites K.B., and Talkington D.F. Mycoplasma pneumoniae and its role as a human pathogen. Clin. Microbiol. Rev. 17 (2004) 697-728 table of contents
68. Weiner III J., Zimmerman C.U., Gohlmann H.W., and Herrmann R. Transcription profiles of the bacterium Mycoplasma pneumoniae grown at different temperatures. Nucleic Acids Res. 31 (2003) 6306-6320
69. Wilson M.H., and Collier A.M. Ultrastructural study of Mycoplasma pneumoniae in organ culture. J. Bacteriol. 125 (1976) 332-339
70. Wolgemuth C.W., Igoshin O., and Oster G. The motility of mollicutes. Biophys. J. 85 (2003) 828-842
71. Zheng Q.S., Braunfeld M.B., Sedat J.W., and Agard D.A. An improved strategy for automated electron microscopic tomography. J. Struct. Biol. 147 (2004) 91-101