Use of frozen-hydrated axonemes to assess imaging parameters and resolution limits in cryoelectron tomography

Journal of Structural Biology

Volumn 138, Issue 1-2, 2002, Pages 47-57

  McEwen, Bruce F ^a,b   Marko, Michael ^a   Hsieh, Chyong Ere ^a   Mannella, Carmen ^a,b  

^a WADSWORTH CENTER   (United States)

^b STATE UNIVERSITY OF NEW YORK   (United States)

Author keywords

Axoneme; Cryoelectron tomography; Electron tomography; Frozen hydrated specimen

Indexed keywords

DYNEIN ADENOSINE TRIPHOSPHATASE;

AXONEME; CONFERENCE PAPER; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ELECTRON; FILTRATION; FRACTIONATION; FREEZING; HYDRATION; IMAGE ANALYSIS; MICROTUBULE; NONHUMAN; PRIORITY JOURNAL; SEA URCHIN; TOMOGRAPHY; ANIMAL; ARTICLE; CELL STRUCTURE; COMPUTER ASSISTED TOMOGRAPHY; CRYOPRESERVATION; FLAGELLUM; HISTOLOGY; IMAGE PROCESSING; METHODOLOGY; STANDARD; ULTRASTRUCTURE;

ECHINOIDEA;

ANIMALS; CELLULAR STRUCTURES; CRYOELECTRON MICROSCOPY; CRYOPRESERVATION; FLAGELLA; IMAGE PROCESSING, COMPUTER-ASSISTED; SEA URCHINS; TOMOGRAPHY, X-RAY COMPUTED;

EID: 0036414847     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/S1047-8477(02)00020-5     Document Type: Conference Paper

References (54)

1. Barnard, D.P., Turner, J.N., Frank, J., McEwen, B.F., 1992. A 360° single-axis tilt stage for the high-voltage electron microscope. J. Microsc. 167, 39-48.
2. Baumeister, W., Grimm, R., Waltz, J., 1999. Electron tomography of molecules and cells. Trends Cell Biol. 9, 81-85.
3. Bell, C.W., Fraser, C., Sale, W.S., Tang, W.-J., Gibbons, I.R., 1982. Preparation and purification of dynein. Methods Cell Biol. 24, 373-397.
4. Böhm, J., Frangakis, A.S., Hegerl, R., Nickell, S., Typke, D., Baumeister, W., 2000. Toward detecting and identifying macromolecules in a cellular context: Template matching applied to electron tomograms. Proc. Natl. Acad. Sci. USA 97, 14245-14250.
5. Bullitt, E., Rout, M.P., Kilmartin, J.V., Akey, C.W., 1997. The yeast spindle pole body is assembled around a central crystal of Spc42p. Cell 89, 1077-1086.
6. Chen, L.F., Winkler, H., Reedy, M.K., Reedy, M.C., Taylor, K.A., 2002. Molecular modeling of averaged crossbridges from tomograms of insect flight muscle. J. Struct. Biol. 138, 92-104.
7. Cheng, R.H., Hultenby, K., Haag, L., Forsell, K., Garoff, H., Hsieh, C.-E., Marko, M., 2001. Bringing together high- and low-resolution data: Electron tomography of budding enveloped alphavirus. Microsc. Microanal. 7 (Suppl. 2: Proceedings), 104-105.
8. Chiu, W., Downing, K.H., Dubochet, J., Glaeser, R.M., Heide, H.G., Knapek, E., Kopf, D.A., Lamvik, M., Lepault, J., Robertson, J.D., Zeitler, E., Zemlin, F., (International Experimental Study Group), 1986. Cryoprotection in electron microscopy. J. Microsc. 141, 85-391.
9. Crowther, R.A., DeRosier, D.J., Klug, A., 1970. The reconstruction of a three-dimensional structure from its projections and its application to electron microscopy. Proc. R. Soc. London A 317, 319-340.
10. Downing, K.H., Jontes, J., 1992. Projection map of tubulin in zinc-induced sheets at 4 Å resolution. J. Struct. Biol. 109, 152-159.
11. Dubochet, J., Sartori Blanc, N., 2001. The cell in absence of aggregation artifacts. Micron 32, 91-99.
12. Dubochet, J., Adrian, M., Chang, J.-J., LaPault, J., McDowall, A.W., 1987. Cryoelectron microscopy of vitrified specimens. In: Steinbrecht, R.A., Zierold, K. (Eds.), Cryotechniques in Biological Electron Microscopy. Springer, Berlin, pp. 114-131.
13. Dubochet, J., Adrian, M., Chang, J.-J., Homo, J.-C., Lepault, J., McDowall, A.W., Schultz, P., 1988. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 21, 129-288.
14. Frangakis, A., Hegerl, R., 2001. Noise reduction in electron tomographic reconstructions using nonlinear anisotropic diffusion. J. Struct. Biol. 135, 239-250.
15. Frank, J., Radermacher, M., Penczek, P., Zhu, J., Li, Y., Ladjadj, M., Leith, A., 1996. Spider and Web: Processing and visualization of images in 3D electron microscopy and related fields. J. Struct. Biol. 116, 190-199.
16. Frank, J., Wagenknecht, T., McEwen, B.F., Marko, M., Hsieh, C.-E., Mannella, C.A., 2002. Three-dimensional imaging of biological complexity. J. Struct. Biol. 138, 85-91.
17. Fung, J.C., Liu, W., De Ruijter, W.J., Chen, H., Abbey, C.K., Sedat, J.W., Agard, D.A., 1996. Toward fully automated high-resolution electron tomography. J. Struct. Biol. 116, 181-189.
18. Gabashvili, I.S., Agrawal, R.K., Spahn, C.M.T., Grassucci, R.A., Frank, J., Penczek, P., 2000. Solution structure of the E. coli 70S ribosome at 11.5 Å resolution. Cell 100, 537-549.
19. Gibbons, I.R., 1981. Cilia and flagella of eukaryotes. J. Cell Biol. 91, 107s-124s.
20. Goodenough, U.W., Heuser, J.E., 1985. Substructure of inner dynein arms, radial spokes, the central pair/projection complex of cilia and flagella. J. Cell Biol. 100, 2008-2018.
21. Grimm, R., Singh, H., Rachel, R., Typke, D., Zillig, W., Baumeister, W., 1998. Electron tomography of ice-embedded prokaryotic cells. Biophys. J. 74, 1013-1042.
22. Hegerl, R., Hoppe, W., 1976. Influence of electron noise on three-dimensional image reconstruction. Z. Naturforsch. 31a, 1717-1721.
23. Heide, H.-G., 1984. Observations on ice layers. Ultramicroscopy 14, 271-278.
24. Hsieh, C.-E., Marko, M., Frank, J., Mannella, C.A., 2002. Electron tomographic analysis of frozen-hydrated tissue sections. J. Struct. Biol. 138, 63-73.
25. Hsieh, C.-E., Marko, M., Rath, B.K., Fleischer, S., Wagenknecht, T., 2001. Cryo-electron tomography of isolated triad junctions from skeletal muscle. Microsc. Microanal. 7 (Suppl. 2: Proceedings), 94-95.
26. Kellenberger, E., 1991. The potential of cryofixation and freeze substitution: Observations and theoretical considerations. J. Microsc. 161, 183-203.
27. Koster, A.J., Grimm, R., Typke, D., Hegerl, R., Stoschek, A., Walz, J., Baumeister, W., 1997. Perspectives of molecular and cellular electron tomography. J. Struct. Biol. 120, 276-308.
28. Mannella, C.A., Hsieh, C.-E., Marko, M., 1999. Electron microscopic tomography of whole, frozen-hydrated rat-liver mitochondria at 400 kV. Microsc. Microanal. 5 (Suppl. 2: Proceedings), 416-417.
29. Mannella, C.A., Pfeiffer, D.R., Bradshaw, P.C., Moraru, L.I., Slepchenko, L.B., Loew, L.M., Hsieh, C.-E., Buttle, K., Marko, M., 2001. Topology of the mitochondrial inner membrane: Dynamics and bioenergetic implications. IUBMB Life 53, 2-5.
30. Marko, M., Hsieh, C.-E., Mannella, C.A., McEwen, B.F., 1999. Imaging considerations for cryo-tomography of organelles and whole cells at high accelerating voltage. Microsc. Microanal. 5 (Suppl. 2: Proceedings), 414-415.
31. Marko, M., Hsieh, C.-E., Rath, B.K., Mannella, C.A., McEwen, B.F., 2000. Electron tomography of frozen-hydrated samples. Microsc. Microanal. 6 (Suppl. 2: Proceedings), 310-311.
32. Mastronarde, D.N., O'Toole, E.T., McDonald, K.L., McIntosh, J.R., Porter, M.E., 1992. Arrangement of inner dynein arms in wild-type and mutant flagella of Chlamydomonas. J. Cell Biol. 118, 1145-1162.
33. McEwen, B.F., Frank, J., 2001. Electron tomographic and other approaches for imaging molecular machines. Curr. Opin. Neurobiol. 11, 594-600.
34. McEwen, B.F., Heagle, A.B., 1997. Electron microscopic tomography: A tool for probing the structure and function of subcellular components. J. Imaging Syst. Technol. 8, 175-187.
35. McEwen, B.F., Marko, M., 1999. Three-dimensional electron microscopy and its application to mitosis research. Methods Cell Biol. 61, 81-111.
36. McEwen, B.F., Marko, M., 2001. The emergence of electron tomography as an important tool for investigating cellular ultrastructure. J. Histochem. Cytochem. 49, 553-563.
37. McEwen, B.F., Downing, K.H., Glaeser, R.M., 1995. The relevance of dose-fractionation in tomography of radiation-sensitive specimens. Ultramicroscopy 60, 357-373.
38. McEwen, B.F., Hsieh, C.-E., Marko, M., Buttle, K., Frank, J., 1998. Cryo-electron tomography applied to sperm flagella. In: Benavides, H.A.C., Jienez, L.F. (Eds.), Proceedings of the 14th International Congress on Electron Microscopy, Cancun, vol. IV. Inst. Physics Publishing, Philadelphia, pp. 459-460.
39. McEwen, B.F., Marko, M., Hsieh, C.-E., Frank, J., 1999. The potential of cryo-electron tomography as assessed by reconstruction of sea urchin axonemes. Microsc. Microanal. 5 (Suppl. 2: Proceedings), 410-411.
40. Murray, J.M., 1986. Electron microscopy of frozen hydrated eukaryotic flagella. J. Ultrastruct. Mol. Struct. Res. 95, 196-209.
41. Nicastro, D., Frangakis, A.S., Typke, D., Baumeister, W., 2000. Cryo-electron tomography of neurospora mitochondria. J. Struct. Biol. 129, 48-56.
42. Nitsch, M., Walz, J., Typke, D., Klumpp, M., Essen, L.-O., Baumeister, W., 1998. Group II chaperonin in an open conformation examined by electron tomography. Nat. Struct. Biol. 5, 855-857.
43. Pascual-Montano, A., Taylor, K.A., Winkler, H., Pascual-Marqui, R.D., Carazo, J.-M., 2002. Quantitative self-organizing maps for clustering electron tomograms. J. Struct. Biol. 138, 114-122.
44. Penczek, P.A., 2002. Three-dimensional spectral signal-to-noise ratio for a class of reconstruction algorithms. J. Struct. Biol. 138, 34-46.
45. Penczek, P., Marko, M., Buttle, K., Frank, J., 1995. Double-tilt electron tomography. Ultramicroscopy 60, 393-410.
46. Porter, M.E., 1996. Axonemal dyneins: Assembly, organization, regulation. Curr. Opin. Cell Biol. 8, 10-17.
47. Radermacher, M., 1992. Weighted back-projection methods. In: Frank, J. (Ed.), Electron Tomography. Plenum, New York, pp. 91-115.
48. Rath, B.K., Marko, M., Radermacher, M., Frank, J., 1997. Low-dose automated electron tomography: A recent implementation. J. Struct. Biol. 120, 210-218.
49. Saxberg, B.E.H., Saxton, W.O., 1981. Quantum noise in 2D projections and 3D reconstructions. Ultramicroscopy 6, 85-90.
50. Saxton, W.O., Baumeister, W., Hahn, M., 1984. Three-dimensional reconstruction of imperfect two-dimensional crystals. Ultramicroscopy 13, 57-70.
51. Sugrue, P., Avolio, J., Satir, P., Holwill, M.E.J., 1991. Computer modeling of Tetrahymena axonemes at macromolecular resolution: Interpretation of electron micrographs. J. Cell Sci. 98, 5-16.
52. 2+ -activated contracting insect flight muscle. Cell 99, 421-431.
53. Volkmann, N., 2002. A novel three-dimensional variant of the watershed transform for segmentation of electron density maps. J. Struct. Biol. 138, 123-129.
54. Ziese, U., Janssen, A.H., Murk, J.L., Geerts, W.J.C., Krift, T., Verkleij, A.J., Koster, A.J., 2002. Automated high-throughput electron tomography by pre-calibration of image shifts. J. Microsc. 205, 187-200.