Electron holography of biological samples

Micron

Volumn 39, Issue 3, 2008, Pages 229-256

  Simon, P ^a   Lichte, H ^b   Formanek, P ^b   Lehmann, M ^b,d   Huhle, R ^b   Carrillo Cabrera, W ^a   Harscher, A ^c   Ehrlich, H ^b  

^a MAX PLANCK INSTITUTE FOR CHEMICAL PHYSICS OF SOLIDS   (Germany)

^b DRESDEN UNIVERSITY OF TECHNOLOGY   (Germany)

^c Retina Implant AG   (Germany)

^d TECHNISCHE UNIVERSITÄT BERLIN   (Germany)

Author keywords

Biological objects; Biominerals; Collagen; Ferritin; In line electron holography; Magnetic and electric dipole fields; Magnetotactic bacteria; Off axis electron holography; S layer protein; Tobacco mosaic virus; Transmission electron microscopy

Indexed keywords

COLLAGEN; MAGNETIC FIELDS; TRANSMISSION ELECTRON MICROSCOPY; VIRUSES;

BIOLOGICAL OBJECTS; BIOMINERALS; INLINE ELECTRON HOLOGRAPHY; MAGNETIC AND ELECTRIC DIPOLE FIELDS; MAGNETOTACTIC BACTERIA; OFF AXIS ELECTRON HOLOGRAPHY; S-LAYER PROTEINS;

ELECTRON HOLOGRAPHY;

MINERAL;

BACILLUS; BACTERIOPHAGE; ELECTRON; HOLOGRAPHY; MAGNETISM; METHODOLOGY; REVIEW; SEMLIKI FOREST ALPHAVIRUS; TOBACCO MOSAIC VIRUS; TRANSMISSION ELECTRON MICROSCOPY; ULTRASTRUCTURE;

BACILLUS; ELECTRONS; HOLOGRAPHY; MAGNETICS; MICROSCOPY, ELECTRON, TRANSMISSION; MINERALS; SEMLIKI FOREST VIRUS; SIPHOVIRIDAE; TOBACCO MOSAIC VIRUS;

BACTERIA (MICROORGANISMS); SEMLIKI FOREST VIRUS; TOBACCO MOSAIC VIRUS;

EID: 39549109261     PISSN: 09684328     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.micron.2006.11.012     Document Type: Review

References (96)

1. Angert I., Majorovits E., and Schröder R.R. Zero-loss image formation and modified contrast transfer theory in EFTEM. Ultramicroscopy 81 3-4 (2000) 203-222
2. Aoyama K., Ishizuka K., and Tanji T. Observation of biological macromolecules by electron holography. J. Electr. Microsc. 40 (1991) 235
3. Aoyama K., Lai G., and Ru Q. Electron holographic observation of thin biological filaments. J. Electr. Microsc. 43 (1994) 39-41
4. Aoyama K., and Ru Q. Electron holographic observation for biological specimens: electron holography of bio-specimens. J. Microsc. 182 (1996) 177-185
5. Asawa Y., Aoki K., Ohya K., Ohshima H., and Takano Y. Appearance of electron-dense segments: indication of possible conformational changes of premineralizing collagen fibrils in the osteoid of rat bones. J. Electr. Microsc. 53 4 (2004) 423-433
6. Baumeister W., Barth M., Hegerl R., Guckenberger R., Hahn M., and Saxton W.O. 3-Dimensional structure of the regular surface-layer (HPI layer) of Deinococcus radiodurans. J. Mol. Biol. 187 2 (1986) 241-253
7. Boot-Handford R.P., and Tuckwell D.S. Fibrillar collagen: the key to vertebrate evolution? A tale of molecular incest. BioEssays 25 (2003) 142-151
8. Bremer A., Henn C., Engel A., Baumeister W., and Aebi U. Has negative staining still a place in biomacromolecular electron microscopy. Ultramicroscopy 46 (1992) 85-111
9. Brink J., Gross H., Tittmann P., Sherman M.B., and Chiu W. Reduction of charging in protein electron cryomicroscopy. J. Microsc. 191 (1998) 67-73
10. Browning N.D., Stahlberg H., Evans J.E., Nicotra G., Chou H.-T., Kirkland A.I., and Hetherington C. Application of aberration corrected TEM and STEM to biological specimens. Proc. Int. Congr. Microsc., IMC16. Sapporo, Japan, Vol. 1 (2006) p. RT-11
11. Busch S., Dolhaine H., DuChesne A., Heinz S., Hochrein O., Laeri F., Podebrand O., Vietze U., Weiland T., and Kniep R. Biomimetic morphogenesis of fluorapatite-gelatin composites: fractal growth, the question of intrinsic electric fields, core/shell assemblies, hollow spheres and reorganization of denatured collagen. Eur. J. Inorg. Chem. 10 (1999) 1643-1653
12. Chapman J.A., Tzaphlidou M., Meek K.M., and Kadler K.E. The collagen fibril-a model system for studying the staining and fixation of a protein. Electr. Microsc. Rev. 3 (1990) 143-182
13. Cheong G.W., Typke D., and Baumeister W. Projection structure of the surface layer of Methanoplanus limicola at 10 angstrom resolution obtained by electron cryomicroscopy. J. Struct. Biol. 117 (1996) 138-144
14. Danev R., and Nagayama K. Complex observation in electron microscopy. II. Direct visualization of phases and amplitudes of exit wave functions. J. Phys. Soc. Jpn. 70 3 (2001) 696-702
15. Danev R., Okawara H., Usuda N., Kametani K., and Nagayama K. A novel phase-contrast transmission electron microscopy producing high-contrast topographic images of weak objects. J. Biol. Phys. 28 4 (2002) 627-635
16. Dunin-Borkowski R.E., McCartney M.R., Frankel R.B., Bazylinski D.A., Posfai M., and Buseck P.R. Magnetic microstructure of magnetotactic bacteria by electron holography. Science 282 5395 (1998) 1868-1870
17. Ehrlich H., Hanke T., Simon P., Göbel C., Heinemann S., Born R., and Worch H. Demineralisation of natural silica based biomaterials: new strategy for the isolation of organic frameworks. BIOmaterialien 6 4 (2005) 297-302
18. Ehrlich H., Douglas T., Scharnweber D., Hanke T., Born R., Bierbaum S., and Worch H. Hydroxyapatite crystal growth on modified collagen I-templates in a model dual membrane diffusion system. Z. Anorg. Allg. Chem. 631 (2005) 1825-1830
19. Fink H.W., Schmid H., Ermanntraut E., and Schulz T. Electron holography of individual DNA. J. Opt. Soc. Am. A 14 (1997) 2168-2172
20. Formanek P., Lenk A., Lichte H., Linck M., Matzeck C., Lehmann M., and Simon P. Electron holography: applications to materials questions. Annu. Rev. Mater. Res. 37 (2007) 539-588
21. Frank J. Three-Dimensional Electron Microscopy of Macromolecular Assemblies (2006), Oxford University Press, New York
22. Fujiyoshi Y., and Uyeda N. Direct imaging of a double-strand DNA molecule. Ultramicroscopy 7 (1981) 189
23. Gábor D. A new microscopic principle. Nature 161 4098 (1948) 777-778
24. Gelse K., Poeschl E., and Aigner T. Collagens-structure, function, and biosynthesis. Adv. Drug Deliv. Rev. 55 (2003) 1531-1546
25. Giraud Gille M.M., Mosser G., Helary C., and Eglin D. Bone matrix like assemblies of collagen: from liquid crystals to gels and biomimetic materials. Micron 36 (2005) 602-608
26. Glaeser R.M., and Taylor K.A. Radiation-damage relative to transmission electron-microscopy of biological specimens at low-temperature-review. J. Microsc. 112 (1978) 127-138
27. Grubb D.T. Radiation damage of organic materials in the transmission electron microscope. Ultramicroscopy 12 (1984) 279-280
28. Gutsmann T., Fantner G.E., Venturoni M., Ekani-Nkodo A., Thompson J.B., Kindt J.H., Morse D.E., Kuchnir-Fygenson D., and Hansma P.K. Evidence that collagen fibrils in tendons are inhomogeneously structured in a tuberlike manner. Biophys. J. 84 (2003) 2593-2598
29. Habelitz S., Balooch M., Marshall S.J., Balooch G., and Marschall G.W. In situ atomic force microscopy of partially demineralized human dentin collagen fibrils. J. Struct. Biol. 138 (2002) 227-236
30. Han K.F., Sedat J.W., and Agard D.A. Mechanism of image-formation for thick biological specimens-exit wave-front reconstruction and electron-energy-loss spectroscopic imaging. J. Microsc. 178 (1995) 107-119
31. Handlin D.L., and Thomas E.L. Phase contrast imaging of styrene-isoprene and styrene-butadiene block copolymers. Macromolecules 16 (1983) 1514-1525
32. Harris J.R. The negative staining carbon-film procedure-technical considerations and a survey of macromolecular applications. Micron Microsc. Acta 22 (1991) 341-359
33. Harris J.R., and Scheffler D. Routine preparation of air-dried negatively stained and unstained specimens on holey carbon support films: a review of applications. Micron 33 5 (2002) 461-480
34. Harscher, A., 1999. Electron holography of biological objects: basics and examples of applications. Ph.D. Thesis. University of Tübingen, Germany.
35. He G., and George A. Dentin matrix protein 1 immobilized on type I collagen fibrils facilitates apatite deposition in vitro. Biol. Chem. 279 (2004) 11649-11656
36. Holmes D.F., Graham H.K., Trotterb J.A., and Kadler K.E. STEM/TEM studies of collagen fibril assembly. Micron 32 (2001) 273-285
37. Huhle, R., McCartney, M., Goldberg, R., 2001. Experiences with a Turn Holder for Magnetic Samples in Off-axis Electron Holography. Dreiländertagung für Elektronenmikroskopie, Innsbruck, Austria, Conf. Abstracts, p. 76.
38. Kaneko Y., Danev R., Nitta K., and Nagayama K. Intact carboxysomes in a cyano-bacterial cell visualized by Hilbert differential contrast transmission electron microscopy. J. Electr. Microsc. 54 (2005) 79-85
39. Kaneko Y., Danev R., Nagayama K., and Nakamoto H. In vivo subcellular ultrastructures recognized with Hilbert differential contrast transmission electron microscopy. J. Bacter. 188 (2006) 805-808
40. Kawasaki T., Endo J., Matsuda T., Osakabe N., and Tonomura A. Applications of holographic interference electron-microscopy to the observation of biological specimens. J. Electr. Microsc. 35 (1986) 211-214
41. Kellenberger E. The ups and downs of beam damage, contrast and noise in biological electron microscopy. Micron Microsc. Acta 17 (1986) 107-114
42. Kimura Y., Vassylyev D.G., Miyazawa A., Kidera A., Matsushima M., Mitsuoka K., Murata K., Hirai T., and Fujiyoshi Y. Surface of bacteriorhodopsin revealed by high-resolution electron crystallography. Nature 389 (1997) 206-211
43. Knapek E. Properties of organic specimens and their supports at 4 K under irradiation in an electron microscope. Ultramicroscopy 10 (1982) 71-86
44. Lednicky F., Pientka Z., and Hromadkova J. Ultrathin sectioning of polymeric materials for low-voltage transmission electron microscopy: relief on ultrathin sections. J. Macromol. Sci. -Phys. B42 5 (2003) 1039-1047
45. Lehmann M., and Lichte H. Tutorial on off-axis electron holography. Microsc. Microanal. 8 (2002) 447-466
46. Lichte H. Electron interference: mystery and reality. Philos. Trans. R. Soc. Lond. A 360 (2002) 897-920
47. Lichte H., Banzhof H., and Huhle R. Limitations in electron holography of magnetic microstructures. Proc. Int. Congr. Electr. Microsc., ICEM 14. Cancun, Mexico, I (1998) 559-560
48. Lichte H., and Lehmann M. Advances in Imaging and Electron Physics, Electron Holography: A Powerful Tool for Analysis of Nanostructures vol. 123 (2002), Academic Press, San Diego, USA pp. 225-255
49. Lichte H., and Weierstall U. Can electron holography improve electron microscopy imaging of biological objects. Inst. Phys. Conf. Ser. 93 (1988) 325-326
50. Lin A.C., and Goh M.C. Investigating the ultrastructure of fibrous long spacing collagen by parallel atomic force and transmission electron microscopy. Proteins: Struct. Funct. Genet. 49 (2002) 378-384
51. Massover W.H., Fun Lai P., and Marsh P. Negative staining permits 4.0 angstrom resolution with low-dose electron diffraction of catalase crystals. Ultramicroscopy 90 (2001) 7-12
52. Massover W.H. Radiation damage to protein specimens from electron beam imaging and diffraction: a mini-review of anti-damage approaches, with special reference to synchrotron X-ray crystallography. J. Synchr. Rad. 14 (2007) 116-127
53. Matsumoto T., Tanji T., and Tonomura A. Visualisation of DNA in solution by Frauenhofer in-line electron holography 2: experiments. Optik 100 (1995) 71-74
54. Mertig M., Wahl R., Lehmann M., Simon P., and Pompe W. Formation and manipulation of regular metallic nanoparticle arrays on bacterial surface layers: an advanced TEM study. Eur. Phys. J. D 16 (2001) 317-320
55. Miles M.J., Brayshaw D.J., Engledew D., Hayes J., McMaster T.J., Major A., Picco L., Round A.N., Vicary J., and Wotherspoon A. Video-rate AFM for polymer structures. Proc. Int. Congr. Microsc., IMC16. Sapporo, Japan, Vol. 1 (2006) 1800
56. Ono T., and Nemoto T.K. Two forms of apatite deposited during mineralization of the hen tendon. Matrix Biol. 24 (2005) 239-244
57. Osawa T., Ishida K., Onodera M., Feng X.Y., Hayashi S., and Nozaka Y. Real electron microscopic images of collagen fibrils in the endoneurium. J. Electr. Microsc. 51 5 (2002) 341-345
58. Ottani V., Raspanti M., and Ruggeri A. Collagen structure and functional implications. Micron 32 (2001) 251-260
59. Ottani V., Martini D., Franchi M., Ruggeri A., and Raspanti M. Hierarchical structures in fibrillar collagens. Micron 33 (2002) 587-596
60. Petermann J., and Gleiter H. Direct observation of amorphous and crystalline regions in polymers by defocus imaging. Philos. Mag. 31 (1975) 929-934
61. Prigent M., and Morin P. Charge effect in point projection images of Ni nanowires and I collagen fibres. J. Phys. D-Appl. Phys. 34 (2001) 1167-1177
62. Prostak K.S., and Lees S. Vizualization of crystal-matrix structure in situ demineralization of mineralized turkey leg tendon and bone. Calcif. Tiss. Int. 59 (1996) 474-479
63. Reimer L. Transmission Electron Microscopy, Springer Series in Optical Sciences. second ed. (1989), Springer, Heidelberg
64. Rubin M.A., Jasiuk I., Taylor J., Rubin J., Ganey T., and Apkarianb R.P. TEM analysis of the nanostructure of normal and osteoporotic human trabecular bone. Bone 33 (2001) 270-282
65. Sára M., and Sleytr U.B. S-layer proteins. J. Bacter. 182 4 (2000) 859
66. Shindo D., Kim J.J., Xia W., Kim K.H., Ohno N., Fujii Y., Terada N., and Ohno S. Electron holography on dynamic motion of secondary electrons around sciatic nerve tissues. J. Electr. Micr. 56 (2007) 1-5
67. Simon P., Zahn D., Lichte H., and Kniep R. Intrinsic electric dipole fields: induction of hierarchical form-developments in fluorapatite-gelatine-nanocomposites. a general principle for morphogenesis of biominerals?. Angew. Chem. 45 (2006) 1911-1915
68. 2. Z. Allg. Anorg. Chem. 631 (2005) 983-992
69. Simon P., Adhikari R., Lichte H., Michler G.H., and Langela M. Electron holography and AFM studies on styrenic block copolymers and a high impact polystyrene. J. Appl. Polym. Sci. 96 (2005) 1573-1583
70. Simon P., Lichte H., Wahl R., Mertig M., and Pompe W. Electron holography of non-stained bacterial surface-layer proteins. Biochim. Biophys. Acta (Biomembr.) 1663 (2004) 178-187
71. Simon P., Carrillo-Cabrera W., Formanek P., Göbel C., Geiger D., Ramlau R., Tlatlik H., Buder J., and Kniep R. On the real-structure of biomimetically grown hexagonal prismatic seeds of fluorapatite-gelatine-composites: TEM investigations along [0 0 1]. J. Mater. Chem. 14 (2004) 2218-2224
72. Simon P., Lichte H., Drechsel J., Formanek P., Graff A., Wahl R., Mertig M., Adhikari R., and Michler H.G. Electron holography of organic and biological materials. Adv. Mater. 15 (2003) 1475-1481
73. Simon P., Huhle R., Lehmann M., Lichte H., Mönter D., Bieber T., Reschetilowski W., Adhikari R., and Michler G.H. Electron holography on beam sensitive materials: organic polymers and mesoporous silica. Chem. Mater. 14 (2002) 1505-1514
74. Sleytr U.B., Messner P., Pum D., and Sara M. Occurrence, location, ultrastructure and morphogenesis of S-layers. In: Sleytr U.B., Messner P., Pum D., and Sara M. (Eds). Crystalline bacterial cell surface proteins (1996), R.G. Landes Comp./Academic Press, Austin/San Diego 5-33
75. Snoeck E., Hartel P., Mueller H., Haider M., and Tiemeijer P.C. Using a CEOS-Objective Lens Corrector as a Pseudo Lorentz Lens in a Tecnai F20 TEM. Proc. Int. Microsc. Conf., IMC 16. Sapporo, Japan, Vol. 2 (2006) 730
76. Spence J.C.H. STEM and shadow-imaging of biomolecules at 6 eV beam energy. Micron 28 (1997) 101-116
77. Stark H., Zemlin F., and Boettcher C. Electron radiation damage to protein crystals of bacteriorhodopsin at different temperatures. Ultramicroscopy 63 2 (1996) 75-81
78. Suginaga, N., Ochiai, H., Takaoka, A., 2006. High Contrast Observations of Unstained Biological Specimens without Support Film Using a Low Energy STEM. In: Proc. Int. Congr. Microsc., IMC16, Sapporo, Japan, Vol. 1, p. 78.
79. Takaoka A., and Hasegawa T. Observation of unstained biological specimens using a loe-energy high-resolution STEM. J. Electr. Microsc. 55 (2006) 157-163
80. Takai Y., Nomaguchi T., Matsushita S., and Kimura Y. Molecular-scale imaging of unstained deoxyribonucleic acid fibers by phase transmission electron microscopy. Appl. Phys. Lett. 89 (2006) 133903
81. Thalhammer S., Heckl W.M., Zink A., and Nerlich A.G. Atomic force microscopy for high resolution imaging of collagen fibrils-a new technique to investigate collagen structure in historic bone tissues. J. Archaeol. Sci. 28 (2001) 1061-1068
82. Trotter J.A., and Koob T.J. Collagen and proteoglycan in a sea-urchin ligament with mutable mechanical-properties. Cell Tiss. Res. 258 (1989) 527-539
83. Tzaphlidou M. The role of collagen in bone structure: an image processing approach. Micron 36 (2005) 593-601
84. Unwin P.N.T., and Henderson R. Molecular-structure determination by electron microscopy of unstained crystalline specimens. J. Mol. Biol. 94 (1975) 425
85. Vyalikh D.V., Danzenbächer S., Mertig M., Kirchner A., Pompe W., Dedkov Y.S., and Molodtsov S.L. Electronic structure of regular bacterial surface layers. Phys. Rev. Lett. 93 (2004) 238103
86. In: Völkl E., Allard L.F., and Joy D.C. (Eds). Introduction to Electron Holography (1999), Kluwer Academic/Plenum, New York
87. Wade R.H. A brief look at imaging and contrast transfer. Ultramicroscopy 46 (1996) 145-156
88. Wahl, R., 2003. Regular bacterial cell envelope proteins as bio-molecular template. Ph.D. Thesis. Technical University of Dresden, Germany.
89. Wang Y.C., Chou T.M., Libera M., Vöelkl E., and Frost B.G. Measurement of polystyrene inner potential by transmission electron holography. Microsc. Microanal. 4 (1998) 146-157
90. Weierstall U., and Lichte H. Electron holography with a superconducting objective lens. Ultramicroscopy 65 (1996) 13-22
91. Weierstall U., Spence J.C.H., Stevens M., and Downing K.H. Point-projection electron imaging of tobacco mosaic virus at 40 eV electron energy. Micron 30 (1999) 335-338
92. Williams B.R., Gelman R.A., Poppke D.C., and Pietz K. Collagen fibril formation-evidence for a temperature independent irreversible step. Biophys. J. 21 3 (1978) a39-a39
93. Woodcock C.L., and Baumeister W. Different representations of a protein-structure obtained with different negative stains. Eur. J. Cell Biol. 51 (1990) 45-52
94. Workshop on High-Resolution Electron Microscopy, 2000. Betheseda, MD, USA, http://em-outreach.sdsc.edu/web-course.
95. Xu W.B., Jericho M.H., Meinertzhagen I.A., and Kreuzer H.J. Digital in-line holography for biological applications. PNAS 98 (2001) 11301-11305
96. Yamamoto S., Hashizume H., Hitomi J., Shigeno M., Sawaguchi S., Abe H., and Ushiki T. The subfibrillar arrangement of corneal and scleral collagen fibrils as revealed by scanning electron and atomic force microscopy. Arch. Histol. Cytol. 63 2 (2000) 127-135