Metallothionein as a clonable high-density marker for cryo-electron microscopy

Journal of Structural Biology

Volumn 177, Issue 1, 2012, Pages 119-127

  Bouchet Marquis, Cédric ^a   Pagratis, Maria ^a   Kirmse, Robert ^a   Hoenger, Andreas ^a  

^a UNIVERSITY OF COLORADO   (United States)

Author keywords

Cryo electron microscopy; Desmin; Eg5 kinesin motor domain; Metallothionein; Microtubule

Indexed keywords

DESMIN; GOLD; KINESIN; METALLOTHIONEIN; ZINC;

ANIMAL CELL; ARTICLE; ATOM; CHIMERA; CLONING; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; CYTOSOL; DENSITY; ELECTRON MICROSCOPY; ESCHERICHIA COLI; IMAGE ANALYSIS; IN VITRO STUDY; INTERMEDIATE FILAMENT; MICROTUBULE; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PURIFICATION; SPATIAL ORIENTATION;

CLONING, MOLECULAR; CRYOELECTRON MICROSCOPY; DESMIN; GENE EXPRESSION REGULATION; IMAGE PROCESSING, COMPUTER-ASSISTED; INTERMEDIATE FILAMENTS; METALLOTHIONEIN; MICROTUBULES; MODELS, MOLECULAR; ORGANELLES; PROTEIN STRUCTURE, TERTIARY; SPECIMEN HANDLING;

EID: 84855859923     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2011.10.007     Document Type: Article

References (57)

1. Al-Amoudi A., Chang J.J., Leforestier A., McDowall A., Salamin L.M., et al. Cryo-electron microscopy of vitreous sections. EMBO J. 2004, 23:3583-3588.
2. Bär H., Strelkov S., Sjöberg G., Aebi U., Herrmann H. The biology of desmin filaments: how do mutations affect their structure, assembly, and organization?. J. Struct. Biol. 2004, 148:137-152.
3. Beuron F., Hoenger A. Structural analysis of the microtubule-kinesin complex by cryo-electron microscopy. Methods Mol. Biol. 2001, 164:235-254.
4. Bouchet-Marquis C., Zuber B., Glynn A.M., Eltsov M., Grabenbauer M., et al. Visualization of cell microtubules in their native state. Biol. Cell 2007, 99:45-53.
5. Braun W., Vasák M., Robbins A.H., Stout C.D., Wagner G., et al. Comparison of the NMR solution structure and the X-ray crystal structure of rat metallothionein-2. Proc. Natl. Acad. Sci. U S A 1992, 89:10124-10128.
6. Christensen A.K. Frozen thin sections of fresh tissue for electron microscopy, with a description of pancreas and liver. J. Cell Biol. 1971, 51:772-804.
7. Cooke C.A., Schaar B., Yen T.J., Earnshaw W.C. Localization of CENP-E in the fibrous corona and outer plate of mammalian kinetochores from prometaphase through anaphase. Chromosoma 1997, 106:446-455.
8. Cope J., Gilbert S., Rayment I., Mastronarde D., Hoenger A. Cryo-electron tomography of microtubule-kinesin motor complexes. J. Struct. Biol. 2010, 170:257-265.
9. Crepeau R.H., McEwen B., Dykes G., Edelstein S.J. Structural studies on porcine brain tubulin in extended sheets. J. Mol. Biol. 1977, 116:301-315.
10. DeRosier D.J., Moore P.B. Reconstruction of three-dimensional images from electron micrographs of structures with helical symmetry. J. Mol. Biol. 1970, 52:355-369.
11. Diestra E., Fontana J., Guichard P., Marco S., Risco C. Visualization of proteins in intact cells with a clonable tag for electron microscopy. J. Struct. Biol. 2009, 165:157-168.
12. Diestra E., Cayrol B., Arluison V., Risco C. Cellular electron microscopy imaging reveals the localization of the Hfq protein close to the bacterial membrane. PLoS One 2009, 4(12):e8301.
13. Dubochet J., Adrian M., Chang J.J., Homo J.C., Lepault J., et al. Cryo-electron microscopy of vitrified specimens. Q. Rev. Biophys. 1988, 21:129-228.
14. Dubochet J., Zuber B., Eltsov M., Bouchet-Marquis C., Al-Amoudi A., Livolant F. How to "read" a vitreous section. Methods Cell Biol. 2007, 79:385-406.
15. Fukunaga Y., Hirase A., Kim H., Wada N., Nishino Y., Miyazawa A. Electron microscopic analysis of a fusion protein of postsynaptic density-95 and metallothionein in cultured hippocampal neurons. J. Electron. Microsc. (Tokyo) 2007, 56:119-129.
16. Giddings T.H., Meehl J.B., Pearson C.G., Winey M. Electron tomography and immuno labeling of Tetrahymena thermophila basal bodies. Methods Cell Biol. 2010, 96:117-141.
17. Grabenbauer M., Geerts W.J., Fernadez-Rodriguez J., Hoenger A., Koster A.J., Nilsson T. Correlative microscopy and electron tomography of GFP through photooxidation. Nat. Methods 2005, 2:857-862.
18. Griffin B.A., Adams S.R., Tsien R.Y. Specific covalent labeling of recombinant protein molecules inside live cells. Science 1998, 281:269-272.
19. Hainfeld J.F., Foley C.J., Maelia L.E., Lipka J.J. Eleven tungsten atom cluster labels: high-resolution, site-specific probes for electron microscopy. J. Histochem. Cytochem. 1990, 38:1787-1793.
20. Heinz H., Farmer B.L., Pandey R.B., Slocik J.M., Patnaik S.S., et al. Nature of molecular interactions of peptides with gold, palladium, and Pd-Au bimetal surfaces in aqueous solution. J. Am. Chem. Soc. 2009, 131:9704-9714.
21. Herrmann H., Häner M., Brettel M., Müller S.A., Goldie K.N., et al. Structure and assembly properties of the intermediate filament protein vimentin: the role of its head, rod and tail domains. J. Mol. Biol. 1996, 264:933-953.
22. Herrmann H., Bär H., Kreplak L., Strelkov S., Aebi U. Intermediate filaments: from cell architecture to nanomechanics. Nat. Rev. Mol. Cell Biol. 2007, 8:562-573.
23. Hoenger A., Sack S., Thormählen M., Marx A., Müller J., et al. Image reconstructions of microtubules decorated with monomeric and dimeric kinesins: comparison with X-ray structure and implications for motility. J. Cell. Biol. 1998, 141:419-430.
24. Hoenger A., McIntosh J.R. Probing the macromolecular organization of cells by electron tomography. Mol. Biol. Cell. 2009, 20:963-972.
25. Hsieh C.E., Leith A., Mannella C.A., Frank J., Marko M. Towards high-resolution three-dimensional imaging of native mammalian tissue: electron tomography of frozen-hydrated rat liver sections. J. Struct. Biol. 2006, 153:1-13.
26. Kellenberger E., Dürrenberger M., Villiger W., Carlemalm E., Wurtz M. The efficiency of immunolabel on Lowicryl sections compared to theoretical predictions. J. Histochem. Cytochem. 1987, 35:959-969.
27. Kirmse R., Bouchet-Marquis C., Page C., Hoenger A. Three-dimensional cryo-electron microscopy on intermediate filaments. Methods Cell Biol. 2010, 96:565-589.
28. Klaassen C.D., Liu J., Choudhuri S. Metallothionein: an intracellular protein to protect against cadmium toxicity. Annu. Rev. Pharmacol. Toxicol. 1999, 39:267-294.
29. Kozielski F., Sack S., Marx A., Thormählen M., Schönbrunn E., et al. The crystal structure of dimeric kinesin and implications for microtubule-dependent motility. Cell 1997, 91:985-994.
30. Kremer J.R., Mastronarde D.N., McIntosh J.R. Computer visualization of three-dimensional image data using IMOD. J. Struct. Biol. 1996, 116:71-76.
31. Krzysiak T.C., Wendt T., Sproul L.R., Tittmann P., Gross H., et al. A structural model for monastrol inhibition of dimeric kinesin Eg5. EMBO J. 2006, 25:2263-2273.
32. Laib J.E., Shaw C.F., Petering D.H., Eidsness M.K., Elder R.C., Garvey J.S. Formation and characterization of aurothioneins: Au, Zn, Cd-thionein, Au, Cd-thionein, and (thiomalato-Au)chi-thionein. Biochemistry (Mosc) 1985, 24:1977-1986.
33. Li H., Otvos J.D. HPLC characterization of Ag+ and Cu+ metal exchange reactions with Zn- and Cd-metallothioneins. Biochemistry (Mosc) 1996, 35:13937-13945.
34. Lucic V., Forster F., Baumeister W. Structural studies by electron tomography: from cells to molecules. Annu. Rev. Biochem. 2005, 74:833-865.
35. Mastronarde D.N. Automated electron microscope tomography using robust prediction of specimen movements. J. Struct. Biol. 2005, 152:36-51.
36. McDowall A.W., Chang J.J., Freeman R., Lepault J., Walter C.A., Dubochet J. Electron microscopy of frozen hydrated sections of vitreous ice and vitrified biological samples. J. Microsc. 1983, 131:1-9.
37. Medalia O., Weber I., Frangakis A.S., Nicastro D., Gerisch G., Baumeister W. Macromolecular architecture in eukaryotic cells visualized by cryoelectron tomography. Science 2002, 298:1209-1213.
38. Mercogliano C.P., DeRosier D.J. Gold nanocluster formation using metallothionein: mass spectrometry and electron microscopy. J. Mol. Biol. 2006, 355:211-223.
39. Milligan R.A., Flicker P.F. Structural relationships of actin, myosin, and tropomyosin revealed by cryo-electron microscopy. J. Cell. Biol. 1987, 105:29-39.
40. Milligan R.A., Whittaker M., Safer D. Molecular structure of F-actin and location of surface binding sites. Nature 1990, 348:217-221.
41. Monosov E.Z., Wenzel T.J., Luers G.H., Heyman J.A., Subramani S. Labeling of peroxisomes with green fluorescent protein in living P. pastoris cells. J. Histochem. Cytochem. 1996, 44:581-589.
42. Mücke N., Kreplak L., Kirmse R., Wedig T., Herrmann H., et al. Assessing the flexibility of intermediate filaments by atomic force microscopy. J. Mol. Biol. 2004, 335:1241-1250.
43. Mücke N., Kirmse R., Wedig T., Leterrier J.F., Kreplak L. Investigation of the morphology of intermediate filaments adsorbed to different solid supports. J. Struct. Biol. 2005, 150:268-276.
44. Nicastro D., Schwartz C., Pierson J., Gaudette R., Porter M.E., McIntosh J.R. The molecular architecture of axonemes revealed by cryoelectron tomography. Science 2006, 313:944-948.
45. Nishino Y., Yasunaga T., Miyazawa A. A genetically encoded metallothionein tag enabling efficient protein detection by electron microscopy. J. Electron. Microsc. (Tokyo) 2007, 56:93-101.
46. Parry D.A., Strelkov S.V., Burkhard P., Aebi U., Herrmann H. Towards a molecular description of intermediate filament structure and assembly. Exp. Cell Res. 2007, 313:2204-2216.
47. Rice S., Lin A.W., Safer D., Hart C.L., Naber N., et al. A structural change in the kinesin motor protein that drives motility. Nature 1999, 402:778-784.
48. Sano T., Glazer A.N., Cantor C.R. A streptavidin-metallothionein chimera that allows specific labeling of biological materials with many different heavy metal ions. Proc. Natl. Acad. Sci. U S A 1992, 89:1534-1538.
49. Sawyer J.R., Tucker P.W., Blattner F.R. Metal-binding chimeric antibodies expressed in Escherichia coli. Proc. Natl. Acad. Sci. U S A 1992, 89:9754-9758.
50. Schroeter J.P., Bretaudiere J.P. SUPRIM: easily modified image processing software. J. Struct. Biol. 1996, 116:131-137.
51. Skiniotis G., Surrey T., Altmann S., Gross H., Song Y.-H., et al. Nucleotide-induced conformations in the neck region of dimeric kinesin. EMBO J. 2003, 22:1518-1528.
52. Slocik J.M., Stone M.O., Naik R.R. Synthesis of gold nanoparticles using multifunctional peptides. Small 2005, 1:1048-1052.
53. Tokuyasu K.T. Immunochemistry on ultrathin frozen sections. Histochem. J. 1980, 12:381-403.
54. Turner J., Anderson R., Guo J., Beraud C., Fletterick R., Sakowicz R. Crystal structure of the mitotic spindle kinesin eg5 reveals a novel conformation of the neck-linker. J. Biol. Chem. 2001, 276:25496-25502.
55. Vale R.D., Milligan R.A. The way things move: looking under the hood of molecular motor proteins. Science 2000, 288:88-95.
56. Wendt T.G., Volkmann N., Goldie K.N., Müller J., Mandelkow E., Hoenger A. Microtubule binding patterns of the reverse kinesin motor Ncd reveal a minus-end directed power stroke. EMBO J. 2002, 21:5969-5978.
57. Whittaker M., Carragher B.O., Milligan R.A. PHOELIX: a package for semi-automated helical reconstruction. Ultramicroscopy 1995, 58:245-259.