Visualization of proteins in intact cells with a clonable tag for electron microscopy

Journal of Structural Biology

Volumn 165, Issue 3, 2009, Pages 157-168

  Diestra, Elia ^a   Fontana, Juan ^a   Guichard, Paul ^b,c   Marco, Sergio ^b,c   Risco, Cristina ^a  

^a CENTRO NACIONAL DE BIOTECNOLOGÍA   (Spain)

^b INSTITUT CURIE   (France)

^c Centre Universitaire   (France)

Author keywords

AmiC; Clonable gold tags; E. coli proteins; Electron microscopy; Electron tomography; Maltose binding protein; RecA

Indexed keywords

BACTERIAL PROTEIN; GOLD CHLORIDE; HYBRID PROTEIN; MALTOSE BINDING PROTEIN; METALLOTHIONEIN III; PROTEIN AMIC; RECA PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL CELL; CELL CLONE; CONTROLLED STUDY; CYTOPLASM; ELECTRON; ELECTRON TOMOGRAPHY; ESCHERICHIA COLI; IMMUNOGOLD LABELING; NONHUMAN; PARTICLE SIZE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; THREE DIMENSIONAL IMAGING; TOMOGRAPHY; TRANSMISSION ELECTRON MICROSCOPY;

CARRIER PROTEINS; CRYOELECTRON MICROSCOPY; CYTOPLASM; ELECTRON MICROSCOPE TOMOGRAPHY; ESCHERICHIA COLI; GOLD COMPOUNDS; HISTOCYTOCHEMISTRY; METALLOTHIONEIN; MICROSCOPY, ELECTRON; MICROSCOPY, ELECTRON, TRANSMISSION; MURAMIDASE; N-ACETYLMURAMOYL-L-ALANINE AMIDASE; PROTEINS; REC A RECOMBINASES; RECOMBINANT FUSION PROTEINS; STAINING AND LABELING;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI;

EID: 59149094180     PISSN: 10478477     EISSN: 10958657     Source Type: Journal    
DOI: 10.1016/j.jsb.2008.11.009     Document Type: Article

References (51)

1. Abramoff M.D., Magelhaes P.J., and Ram S.J. Image processing with ImageJ. Biophotonics Int. 11 (2004) 36-42
2. Bernhardt T.G., and de Boer P.A.J. The Escherichia coli amidase AmiC is a periplasmic septal ring component exported via the twin-arginine transport pathway. Mol. Microbiol. 48 (2003) 1171-1182
3. Best C., Nickell S., and Baumeister W. Localization of protein complexes by pattern recognition. Methods Cell Biol. 79 (2007) 615-638
4. Benner G., and Probst W. Köhler illumination in the TEM: fundamental advantages. J. Microsc. 174 (1994) 133-142
5. Cheutin T., Sauvage C., Tchélidzé P., O'Donohue M.F., Kaplan H., Beorchia A., and Ploton D. Visualizing macromolecules with Fluoronangold: from photon microscopy to electron tomography. Methods Cell Biol. 79 (2007) 559-574
6. Cyrklaff M., Risco C., Fernández J.J., Jiménez M.V., Esteban M., Baumeister W., and Carrascosa J.L. Cryo-electron tomography of vaccinia virus. Proc. Natl. Acad. Sci. USA 102 (2005) 2772-2777
7. Fernández J.J., and Li S. An improved algorithm for anisotropic nonlinear diffusion for denoising cryo-tomograms. J. Struct. Biol. 144 (2003) 152-161
8. Furey W.F., Robbins A.H., Clancy L.L., Winge D.R., Wang B.C., and Stout C.D. Crystal structure of Cd, Zn metallothionein. Science 23 (1986) 704-710
9. Fontana J., Tzeng W.-P., Calderita G., Fraile-Ramos A., Frey T.K., and Risco C. Novel replication complex architecture in rubella replicon transfected cells. Cell. Microbiol. 9 (2007) 875-890
10. Fontana J., López-Montero N., Elliott R.M., Fernández J.J., and Risco C. The unique architecture of Bunyamwera virus factories around the Golgi complex. Cell. Microbiol. 10 (2008) 2012-2028
11. Fukunaga Y., Hirase A., Kim H., Wada N., Nishino Y., and Miyazawa A. Electron microscopic analysis of a fusion protein of postsynaptic density-95 and metallothionein in cultured hippocampal neurons. J. Electron Microsc. 56 (2007) 119-129
12. 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 connexion trafficking. Science 296 (2002) 503-507
13. Galletto R., Amitani I., Baskin R.J., and Kowalczykowsky S.C. Direct observation of individual RecA filaments assembling on single DNA molecules. Nature 443 (2006) 875-878
14. Galletto R., and Kowalczykowsky S.C. RecA. Curr. Biol. 17 (2007) 395-397
15. Giepmans B.N., Deerinck T.J., Smarr B.L., Jones Y.Z., and Ellisman M.H. Correlated light and electron microscopic imaging of multiple endogenous proteins using Quantum dots. Nat. Methods 2 (2005) 857-862
16. Giepmans B.N.G., Adams S.R., Ellisman M.H., and Tsien R.Y. The fluorescent toolbox for assessing protein location and function. Science 312 (2006) 217-224
17. Grabenbauer M., Geerts W.J., Fernández-Rodríguez J., Hoenger A., Kosster A.J., and Nilsson T. Correlative microscopy and electron tomography of GFP through photooxidation. Nat. Methods 2 (2005) 857-862
18. Haferburg G., and Kothe E. Microbes and metals: interactions in the environment. J. Basic Microbiol. 47 (2007) 453-467
19. Jeanguillaume C. Electron energy-loss spectroscopy and biology. Scanning Microsc. 1 (1987) 437-450
20. Kar S., Edgard R., and Adhya S. Nucleoid remodelling by an altered HU protein: reorganization of the transcription program. Proc. Natl. Acad. Sci. USA 102 (2005) 16397-16402
21. Kireev I., Lakonishok M., Liu W., Joshi V.N., Powell R., and Belmont A.S. In vivo immunogold labelling confirms large-scale chromatin folding motifs. Nat. Methods 5 (2008) 311-313
22. Kürner J., Frangakis A.S., and Baumeister W. Cryo-electron tomography reveals the cytoskeletal structure of Spiroplasma melliferum. Science 307 (2005) 436-438
23. Lanio S. High-resolution imaging magnetic energy filters with simple structure. Optik 73 (1986) 99-107
24. Luque D., Saugar I., Rodríguez J.F., Verdaguer N., Garriga D., San Martín C., Velázquez-Muriel J.A., Trus B.L., Carrascosa J.L., and Castón J.R. Infectious Bursal Disease Virus capsid assembly and maturation by structural rearrangements of a transient molecular switch. J. Virol. 81 (2007) 6869-6878
25. Marsh B.J. Lessons from tomographic studies of the mammalian Golgi. Biochim. Biophys. Acta 1744 (2005) 273-292
26. Matias V.R., and Beveridge T.J. Cryo-electron microscopy of cell division in Staphylococcus aureus reveals a mid-zone between nascent cross walls. Mol. Microbiol. 64 (2007) 195-206
27. McDonald K.L., Morphew M., Verkade P., and Müller-Reichert T. Recent advances in high-pressure freezing: equipment and specimen-loading methods. Methods Mol. Biol. 369 (2007) 143-173
28. 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
29. Medintz I.L., and Deschamps J.R. Maltose-binding protein: a versatile platform for prototyping biosensing. Curr. Opion. Biotech. 17 (2006) 17-27
30. Mercogliano C.P., and DeRosier D.J. Gold cluster formation using metallothionein: mass spectrometry and electron microscopy. J. Mol. Biol. 355 (2006) 211-223
31. Mercogliano C.P., and DeRosier D.J. Concatenated metallothionein as a clonable gold label for electron microscopy. J. Struct. Biol. 160 (2007) 70-82
32. Messaoudi C., Boudier T., Sanchez-Sorzano C.O., and Marco S. TomoJ: tomography software for three-dimensional reconstruction in transmission electron microscopy. BMC Bioinformatics 8 (2007) 288-296
33. Nickell S., Kofler C., Leis A.P., and Baumeister W. A visual approach to proteomics. Nat. Rev. Mol. Cell. Biol. 7 (2006) 225-230
34. Nielson K.B., Atkin C.L., and Winge D.R. Distinct metal-binding configurations in metallothionein. J. Biol. Chem. 260 (1985) 5342-5350
35. Nishino Y., Yasunaga T., and Miyazawa A. A genetically encoded metallothionein tag enabling efficient detection by electron microscopy. J. Electron Microsc. 56 (2007) 93-101
36. Nishiuchi S., Liu S., and Takano T. Isolation and characterization of a metallothionein-1 protein in Chloris virgata Swartz that enhances stress tolerances to oxidative, salinity and carbonate stress in Saccharomyces cerevisiae. Biotechnol. Lett. 29 (2007) 1301-1305
37. O'Hare H.M., Johnsson K., and Gautire A. Chemical probes shed light on protein function. Curr. Opion. Struct. Biol. 17 (2007) 488-494
38. Puvion-Dutilleul F., Pichard E., Laithier M., and Leduc E.H. Effect of dehydrating agents on DNA organization in herpes viruses. J. Histochem. Cytochem. 35 (1987) 635-645
39. Puvion-Dutilleul F. Successive steps for Lowicryl K4M embedding and ultrathin sectioning of somatic mammalian cells prior to in situ hybridization. Practical Approach Series (2001), Oxford University Press 1-2
40. Quintana C. Cryofixation, cryosubstitution, cryoembedding for ultrastructural, immunocytochemical and microanalytical studies. Micron 25 (1994) 63-99
41. Quintana C., Marco S., Bonnet N., Risco C., Gutiérrez M.L., Guerrero A., and Carrascosa J.L. Optimization of phosphorus localization by EFTEM of nucleic acid containing structures. Micron 29 (1998) 297-307
42. Quintana C., Lechaire J.P., Bonnet N., Risco C., and Carrascosa J.L. Elemental maps from EFTEM images using two different background subtraction models. Microsc. Res. Tech. 53 (2001) 147-156
43. Risco C., and Pinto da Silva P. The fracture-flip technique reveals new structural features of the Escherichia coli cell wall. J. Microsc. 189 (1998) 213-218
44. Risco C., Rodríguez J.R., López-Iglesias C., Carrascosa J.L., Esteban M., and Rodríguez D. Endoplasmic reticulum-Golgi intermediate compartment membranes and vimentin filaments participate in vaccinia virus assembly. J. Virol. 76 (2002) 1839-1855
45. Robinson C.V., Sali A., and Baumeister W. The molecular sociology of the cell. Nature 450 (2007) 973-982
46. Saxton W.O., Baumeister W., and Hahn M. Three-dimensional reconstruction of imperfect 2D crystals. Ultramicroscopy 13 (1984) 57-70
47. Sosinsky G.E., Giepmans B.N.G., Deerinck T.J., Gaietta G.M., and Ellisman M.H. Markers for correlated light and electron microscopy. Methods Cell Biol. 79 (2007) 575-591
48. Steven A.C., and Aebi U. The next ice age: cryo-electron tomography of intact cells. Trends Cell Biol. 13 (2003) 107-110
49. Thirumoorthy N., Manisenthil Kumar K.T., Shyam Sundar A., Panayappan L., and Chatterjee M. Metallothionein: an overview. World J. Gastroenterol. 21 (2007) 993-996
50. Wei, H., Mokhtar Desouki, M., Lin, S., Xiao, D., Franklin, R.B., Feng, P., in press. Differential expression of metallothioneins (MTs) 1, 2, and 3 in response to zinc treatment in human prostate normal and malignant cells and tissues. Mol. Cancer 7. doi:10.1186/1476-4598-7-7.
51. Weiss D.S. Bacterial cell division and the septal ring. Mol. Microbiol. 54 (2004) 588-597