IPET and FETR: Experimental approach for studying molecular structure dynamics by cryo-electron tomography of a single-molecule structure

PLoS ONE

Volumn 7, Issue 1, 2012, Pages

  Zhang, Lei ^a   Ren, Gang ^a  

^a LAWRENCE BERKELEY NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALGORITHM; ARTICLE; CHEMICAL STRUCTURE; ELECTRON TOMOGRAPHY; FOCUSED ELECTRON TOMOGRAPHY RECONSTRUCTION; IMAGE DISTORTION; IMAGE PROCESSING; IMAGE RECONSTRUCTION; INDIVIDUAL PARTICLE ELECTRON TOMOGRAPHY; MEASUREMENT ERROR; NONHUMAN; SIMULATION; STRUCTURE ANALYSIS; VALIDATION PROCESS; CHEMISTRY; COMPUTER SIMULATION; CRYOELECTRON MICROSCOPY; EVALUATION; MACROMOLECULE; METHODOLOGY; MOLECULAR DYNAMICS; PROTEIN QUATERNARY STRUCTURE; PROTEIN SECONDARY STRUCTURE; THREE DIMENSIONAL IMAGING; VALIDATION STUDY; X RAY CRYSTALLOGRAPHY;

ALGORITHMS; COMPUTER SIMULATION; CRYOELECTRON MICROSCOPY; CRYSTALLOGRAPHY, X-RAY; ELECTRON MICROSCOPE TOMOGRAPHY; IMAGE PROCESSING, COMPUTER-ASSISTED; IMAGING, THREE-DIMENSIONAL; MACROMOLECULAR SUBSTANCES; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR STRUCTURE; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, SECONDARY;

EID: 84856199455     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0030249     Document Type: Article

References (79)

1. Frauenfelder H, Chen G, Berendzen J, Fenimore PW, Jansson H, et al. (2009) A unified model of protein dynamics. Proc Natl Acad Sci U S A 106: 5129-5134.
2. Karplus M, Kuriyan J, (2005) Molecular dynamics and protein function. Proc Natl Acad Sci U S A 102: 6679-6685.
3. Milne JL, Subramaniam S, (2009) Cryo-electron tomography of bacteria: progress, challenges and future prospects. Nat Rev Microbiol 7: 666-675.
4. Koning RI, Koster AJ, (2009) Cryo-electron tomography in biology and medicine. Ann Anat.
5. Frey TG, Perkins GA, Ellisman MH, (2006) Electron tomography of membrane-bound cellular organelles. Annu Rev Biophys Biomol Struct 35: 199-224.
6. Walz J, Typke D, Nitsch M, Koster AJ, Hegerl R, et al. (1997) Electron Tomography of Single Ice-Embedded Macromolecules: Three-Dimensional Alignment and Classification. J Struct Biol 120: 387-395.
7. Liu J, Bartesaghi A, Borgnia MJ, Sapiro G, Subramaniam S, (2008) Molecular architecture of native HIV-1 gp120 trimers. Nature 455: 109-113.
8. Fernando KV, (2008) Radial averages of astigmatic TEM images. J Struct Biol 164: 49-59.
9. Schaffer B, Kothleitner G, Grogger W, (2006) EFTEM spectrum imaging at high-energy resolution. Ultramicroscopy 106: 1129-1138.
10. Ren G, Zuo JM, L-M P, (1997) Accurate Measurements of Crystal Structure Factors Using a FEG Electron Microscope Using Digital Micrographs. Micron 28: 459-467.
11. Frank J, Wagenknecht T, McEwen BF, Marko M, Hsieh CE, et al. (2002) Three-dimensional imaging of biological complexity. J Struct Biol 138: 85-91.
12. Henderson R, Baldwin JM, Downing KH, Lepault J, Zemlin F, (1986) Structure of purple membrane from Halobacterium halobium: recording, measurement and evaluation of electron micrographs at 3.5A resolution. Ultramicroscopy 19: 147-178.
13. Gil D, Carazo JM, Marabini R, (2006) On the nature of 2D crystal unbending. J Struct Biol 156: 546-555.
14. Zhang L, Ren G, (2010) Structural Determination of Heterogeneous Protein by Individual-Particle Electron Tomography- Combination of Electron Tomography and Local Refinement Reconstruction Method for High-Resolution Structural Determination of Each Individual Protein Particle. Biophysical Journal 98: 441a.
15. Jones MK, Zhang L, Catte A, Li L, Oda MN, et al. (2010) Assessment of the validity of the double superhelix model for reconstituted high density lipoproteins: a combined computational-experimental approach. J Biol Chem 285: 41161-41171.
16. Zhang L, Kaspar A, Woodnutt G, Ren G, (2010) Monitoring the Structural Changes of Conjugated Antibodies by High-Resolution Electron Microscopy and Individual-Particle Electron Tomography. Biophysical Journal 98: 440a-441a.
17. Zhang L, Cavigiolio G, Wang J, Rye KA, Oda M, et al. (2010) Structure of 9.6 nm Discoidal High-Density Lipoprotein Revealed by Individual-Particle Electron Tomography. Biophysical Journal 98: 440a.
18. Zhang L, Ren G, (2010) Determining the Dynamic Protein Structure by Individual-Particle Electron Tomography: An Individual Antibody Structure at a Nanometer Resolution. Biophysical Journal 98: 441a.
19. Hollenstein K, Frei DC, Locher KP, (2007) Structure of an ABC transporter in complex with its binding protein. Nature 446: 213-216.
20. Ludtke SJ, Baldwin PR, Chiu W, (1999) EMAN: semiautomated software for high-resolution single-particle reconstructions. J Struct Biol 128: 82-97.
21. Frank J, Radermacher M, Penczek P, Zhu J, Li Y, et al. (1996) SPIDER and WEB: processing and visualization of images in 3D electron microscopy and related fields. J Struct Biol 116: 190-199.
22. Leschziner AE, Nogales E, (2006) The orthogonal tilt reconstruction method: an approach to generating single-class volumes with no missing cone for ab initio reconstruction of asymmetric particles. J Struct Biol 153: 284-299.
23. Grimm R, Singh H, Rachel R, Typke D, Zillig W, et al. (1998) Electron tomography of ice-embedded prokaryotic cells. Biophys J 74: 1031-1042.
24. Shaikh TR, Gao H, Baxter WT, Asturias FJ, Boisset N, et al. (2008) SPIDER image processing for single-particle reconstruction of biological macromolecules from electron micrographs. Nat Protoc 3: 1941-1974.
25. Saxton WO, Baumeister W, (1982) The correlation averaging of a regularly arranged bacterial cell envelope protein. J Microsc 127: 127-138.
26. van Heel M, Stoffler-Meilicke M, (1985) Characteristic views of E. coli and B. stearothermophilus 30S ribosomal subunits in the electron microscope. Embo J 4: 2389-2395.
27. Unser M, Trus BL, Steven AC, (1987) A new resolution criterion based on spectral signal-to-noise ratios. Ultramicroscopy 23: 39-51.
28. van Heel M, Harauz G, Orlova EV, Schmidt R, Schatz M, (1996) A new generation of the IMAGIC image processing system. J Struct Biol 116: 17-24.
29. Bottcher B, Wynne SA, Crowther RA, (1997) Determination of the fold of the core protein of hepatitis B virus by electron cryomicroscopy. Nature 386: 88-91.
30. Xiang S, Carter CW Jr, Bricogne G, Gilmore CJ, (1993) Entropy maximization constrained by solvent flatness: a new method for macromolecular phase extension and map improvement. Acta Crystallogr D Biol Crystallogr 49: 193-212.
31. Jiang W, Li Z, Zhang Z, Baker ML, Prevelige PE Jr, et al. (2003) Coat protein fold and maturation transition of bacteriophage P22 seen at subnanometer resolutions. Nat Struct Biol 10: 131-135.
32. Jiang W, Baker ML, Jakana J, Weigele PR, King J, et al. (2008) Backbone structure of the infectious epsilon15 virus capsid revealed by electron cryomicroscopy. Nature 451: 1130-1134.
33. Cantele F, Zampighi L, Radermacher M, Zampighi G, Lanzavecchia S, (2007) Local refinement: an attempt to correct for shrinkage and distortion in electron tomography. J Struct Biol 158: 59-70.
34. Hue F, Johnson CL, Lartigue-Korinek S, Wang G, Buseck PR, et al. (2005) Calibration of projector lens distortions. J Electron Microsc (Tokyo) 54: 181-190.
35. Stokroos I, Oosterbaan JA, Arends J, (1983) Influence of radial TEM distortion on the accuracy of lattice parameter determinations of apatites: a comparison of four electron microscopes. J Biol Buccale 11: 339-345.
36. Henderson R, Baldwin JM, Ceska TA, Zemlin F, Beckmann E, et al. (1990) Model for the structure of bacteriorhodopsin based on high-resolution electron cryo-microscopy. J Mol Biol 213: 899-929.
37. Mastronarde DN, (2008) Correction for non-perpendicularity of beam and tilt axis in tomographic reconstructions with the IMOD package. J Microsc 230: 212-217.
38. Winkler H, (2007) 3D reconstruction and processing of volumetric data in cryo-electron tomography. J Struct Biol 157: 126-137.
39. Sandberg K, Mastronarde DN, Beylkin G, (2003) A fast reconstruction algorithm for electron microscope tomography. J Struct Biol 144: 61-72.
40. Fung JC, Liu W, de Ruijter WJ, Chen H, Abbey CK, et al. (1996) Toward fully automated high-resolution electron tomography. J Struct Biol 116: 181-189.
41. Chen H, Hughes DD, Chan TA, Sedat JW, Agard DA, (1996) IVE (Image Visualization Environment): a software platform for all three-dimensional microscopy applications. J Struct Biol 116: 56-60.
42. Mastronarde DN, (1997) Dual-axis tomography: an approach with alignment methods that preserve resolution. J Struct Biol 120: 343-352.
43. Grigorieff N, (2007) FREALIGN: high-resolution refinement of single particle structures. J Struct Biol 157: 117-125.
44. Hohn M, Tang G, Goodyear G, Baldwin PR, Huang Z, et al. (2007) SPARX, a new environment for Cryo-EM image processing. J Struct Biol 157: 47-55.
45. Zhang L, Song J, Cavigiolio G, Ishida BY, Zhang S, et al. (2011) Morphology and structure of lipoproteins revealed by an optimized negative-staining protocol of electron microscopy. J Lipid Res 52: 175-184.
46. Zhang L, Song J, Newhouse Y, Zhang S, Weisgraber KH, et al. (2010) An optimized negative-staining protocol of electron microscopy for apoE4 POPC lipoprotein. J Lipid Res 51: 1228-1236.
47. Fernandez JJ, Li S, Crowther RA, (2006) CTF determination and correction in electron cryotomography. Ultramicroscopy 106: 587-596.
48. Chen B, Ren X, Neville T, Jerome WG, Hoyt DW, et al. (2009) Apolipoprotein AI tertiary structures determine stability and phospholipid-binding activity of discoidal high-density lipoprotein particles of different sizes. Protein Sci 18: 921-935.
49. Cavigiolio G, Shao B, Geier EG, Ren G, Heinecke JW, et al. (2008) The interplay between size, morphology, stability, and functionality of high-density lipoprotein subclasses. Biochemistry 47: 4770-4779.
50. Silva RA, Huang R, Morris J, Fang J, Gracheva EO, et al. (2008) Structure of apolipoprotein A-I in spherical high density lipoproteins of different sizes. Proc Natl Acad Sci U S A 105: 12176-12181.
51. van Antwerpen R, Chen GC, Pullinger CR, Kane JP, LaBelle M, et al. (1997) Cryo-electron microscopy of low density lipoprotein and reconstituted discoidal high density lipoprotein: imaging of the apolipoprotein moiety. J Lipid Res 38: 659-669.
52. Segrest JP, Jones MK, Klon AE, Sheldahl CJ, Hellinger M, et al. (1999) A detailed molecular belt model for apolipoprotein A-I in discoidal high density lipoprotein. J Biol Chem 274: 31755-31758.
53. Herman GT, Lent A, Rowland SW, (1973) ART: mathematics and applications. A report on the mathematical foundations and on the applicability to real data of the algebraic reconstruction techniques. J Theor Biol 42: 1-32.
54. Gilbert P, (1972) Iterative methods for the three-dimensional reconstruction of an object from projections. J Theor Biol 36: 105-117.
55. Ren G, Reddy VS, Cheng A, Melnyk P, Mitra AK, (2001) Visualization of a water-selective pore by electron crystallography in vitreous ice. Proc Natl Acad Sci U S A 98: 1398-1403.
56. Ren G, Cheng A, Reddy V, Melnyk P, Mitra AK, (2000) Three-dimensional fold of the human AQP1 water channel determined at 4 A resolution by electron crystallography of two-dimensional crystals embedded in ice. J Mol Biol 301: 369-387.
57. Ren G, Rudenko G, Ludtke SJ, Deisenhofer J, Chiu W, et al. (2010) Model of human low-density lipoprotein and bound receptor based on cryoEM. Proc Natl Acad Sci U S A 107: 1059-1064.
58. Bracewell RN, Riddle AC, (1967) Inversion of Fan-Beam Scans in Radio Astronomy. Astrophysical Journal 150: 427-434.
59. Crowther RA, (1971) Procedures for three-dimensional reconstruction of spherical viruses by Fourier synthesis from electron micrographs. Philos Trans R Soc Lond B Biol Sci 261: 221-230.
60. Klug A, Crowther RA, (1972) Three-dimensional Image Reconstruction from the Viewpoint of information Theory. Nature Structural and Molecular Biology 238: 435-440.
61. Stagg SM, Lander GC, Pulokas J, Fellmann D, Cheng A, et al. (2006) Automated cryoEM data acquisition and analysis of 284742 particles of GroEL. J Struct Biol 155: 470-481.
62. Harris JR, Horne RW, (1994) Negative Staining: A Brief Assessment of Current Technical Benefits, Limitations and Future Possibilities. Micron 25: 5-13.
63. Rosenthal PB, Henderson R, (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J Mol Biol 333: 721-745.
64. Bammes BE, Jakana J, Schmid MF, Chiu W, (2010) Radiation damage effects at four specimen temperatures from 4 to 100 K. J Struct Biol 169: 331-341.
65. Unwin PN, Henderson R, (1975) Molecular structure determination by electron microscopy of unstained crystalline specimens. J Mol Biol 94: 425-440.
66. Glaeser RM, (1979) Prospects for extending the resolution limit of the electron microscope. J Microsc 117: 77-91.
67. Taylor KA, Glaeser RM, (1976) Electron microscopy of frozen hydrated biological specimens. J Ultrastruct Res 55: 448-456.
68. Conway JF, Trus BL, Booy FP, Newcomb WW, Brown JC, et al. (1993) The effects of radiation damage on the structure of frozen hydrated HSV-1 capsids. J Struct Biol 111: 222-233.
69. Glaeser RM, (1971) Limitations to significant information in biological electron microscopy as a result of radiation damage. J Ultrastruct Res 36: 466-482.
70. Chen JZ, Sachse C, Xu C, Mielke T, Spahn CM, et al. (2008) A dose-rate effect in single-particle electron microscopy. J Struct Biol 161: 92-100.
71. Baker LA, Smith EA, Bueler SA, Rubinstein JL, (2010) The resolution dependence of optimal exposures in liquid nitrogen temperature electron cryomicroscopy of catalase crystals. J Struct Biol 169: 431-437.
72. Liu H, Jin L, Koh SB, Atanasov I, Schein S, et al. (2010) Atomic structure of human adenovirus by cryo-EM reveals interactions among protein networks. Science 329: 1038-1043.
73. Cardone G, Winkler DC, Trus BL, Cheng N, Heuser JE, et al. (2007) Visualization of the herpes simplex virus portal in situ by cryo-electron tomography. Virology 361: 426-434.
74. Suloway C, Shi J, Cheng A, Pulokas J, Carragher B, et al. (2009) Fully automated, sequential tilt-series acquisition with Leginon. J Struct Biol 167: 11-18.
75. Ren G, Peng LM, (1996) The Analytic Doyle-Turner Representation of High Energy Electron Absorptive Structure Factors. Acta Physica Sinica 45: 1344-1349.
76. Peng LM, Ren G, Dudarev SL, Whelan MJ, (1996) Robust Parameterization of Elastic and Absorptive Electron Atomic Scattering Factors. Acta Cryst A 52: 257-276.
77. Cowley JM, Peng LM, Ren G, Dudarev SL, Whelan MJ, Prince E, Crystallography. IUo, editors (2006) Parameterizations of electron atomic scattering factors. International tables for crystallography: Volume C: Mathematical, physical and chemical tables. 4th ed Dordrecht Published for the International Union of Crystallography by Kluwer Academic pp. 262-284.
78. Peng LM, Ren G, Dudarev SL, Whelan MJ, (1996) Debye-Waller Factors and Absorptive Scattering Factors of Elemental Crystals. Acta Cryst A 52: 456-470.
79. Pettersen EF, Goddard TD, Huang CC, Couch GS, Greenblatt DM, et al. (2004) UCSF Chimera-a visualization system for exploratory research and analysis. J Comput Chem 25: 1605-1612.