Merging molecular electron microscopy and mass spectrometry by carbon film-assisted endoproteinase digestion

Molecular and Cellular Proteomics

Volumn 9, Issue 8, 2010, Pages 1729-1741

  Richter, Florian M ^a,d   Sander, Bjoern ^a,b   Golas, Monika M ^a,b   Stark, Holger ^a,c   Urlauba, Henning ^a  

^a MAX PLANCK INSTITUTE FOR BIOPHYSICAL CHEMISTRY   (Germany)

^b AARHUS UNIVERSITY   (Denmark)

^c UNIVERSITY OF GÖTTINGEN   (Germany)

^d MAX PLANCK INSTITUTE OF IMMUNOBIOLOGY AND EPIGENETICS   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOPROTEINASE; PROTEINASE; UNCLASSIFIED DRUG; CARBON; CHAPERONIN 60; CROSS LINKING REAGENT; EARLY PREGNANCY FACTOR; PEPTIDE; SMALL NUCLEAR RIBONUCLEOPROTEIN;

ARTICLE; COMPLEX FORMATION; CONTROLLED STUDY; ELECTRON MICROSCOPY; ELECTRON MICROSCOPY CARBON FILM ASSISTED DIGESTION; MACROMOLECULE; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DEGRADATION; PROTEIN STRUCTURE; PROTEOMICS; REPRODUCIBILITY; SENSITIVITY ANALYSIS; STRUCTURE ANALYSIS; AMINO ACID SEQUENCE; CHEMICAL STRUCTURE; CHEMISTRY; HELA CELL LINE; HUMAN; LIQUID CHROMATOGRAPHY; METABOLISM; MOLECULAR GENETICS; PROCEDURES; ULTRASTRUCTURE;

AMINO ACID SEQUENCE; CARBON; CHAPERONIN 10; CHAPERONIN 60; CHROMATOGRAPHY, LIQUID; CROSS-LINKING REAGENTS; ENDOPEPTIDASES; HELA CELLS; HUMANS; MASS SPECTROMETRY; MICROSCOPY, ELECTRON; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; REPRODUCIBILITY OF RESULTS; RIBONUCLEOPROTEINS, SMALL NUCLEAR;

EID: 77955391064     PISSN: 15359476     EISSN: 15359484     Source Type: Journal    
DOI: 10.1074/mcp.M110.001446     Document Type: Article

References (51)

1. Alberts, B. (1998) The cell as a collection of protein machines: preparing the next generation of molecular biologists. Cell 92, 291-294
2. Forler, D., Köcher, T., Rode, M., Gentzel, M., Izaurralde, E., and Wilm, M. (2003) An efficient protein complex purification method for functional proteomics in higher eukaryotes. Nat. Biotechnol. 21, 89-92
3. Kastner, B., Fischer, N., Golas, M. M., Sander, B., Dube, P., Boehringer, D., Hartmuth, K., Deckert, J., Hauer, F., Wolf, E., Uchtenhagen, H., Urlaub, H., Herzog, F., Peters, J. M., Poerschke, D., Lührmann, R., and Stark, H. (2008) GraFix: sample preparation for single-particle electron cryomicroscopy. Nat. Methods 5, 53-55
4. Oeffinger, M., Wei, K. E., Rogers, R., DeGrasse, J. A., Chait, B. T., Aitchison, J. D., and Rout, M. P. (2007) Comprehensive analysis of diverse ribonucleoprotein complexes. Nat. Methods 4, 951-956
5. Yang, W., Steen, H., and Freeman, M. R. (2008) Proteomic approaches to the analysis of multiprotein signaling complexes. Proteomics 8, 832-851
6. Link, A. J., Eng, J., Schieltz, D. M., Carmack, E., Mize, G. J., Morris, D. R., Garvik, B. M., and Yates, J. R., 3rd (1999) Direct analysis of protein complexes using mass spectrometry. Nat. Biotechnol. 17, 676-682
7. Heck, A. J. (2008) Native mass spectrometry: a bridge between interactomics and structural biology. Nat. Methods 5, 927-933
8. Sobott, F., McCammon, M. G., Hernández, H., and Robinson, C. V. (2005) The flight of macromolecular complexes in a mass spectrometer. Philos. Transact. A Math. Phys. Eng. Sci. 363, 379-391
9. van Heel, M., Gowen, B., Matadeen, R., Orlova, E. V., Finn, R., Pape, T., Cohen, D., Stark, H., Schmidt, R., Schatz, M., and Patwardhan, A. (2000) Single-particle electron cryo-microscopy: towards atomic resolution. Q. Rev. Biophys. 33, 307-369
10. Kühner, S., van Noort, V., Betts, M. J., Leo-Macias, A., Batisse, C., Rode, M., Yamada, T., Maier, T., Bader, S., Beltran-Alvarez, P., Castaño-Diez, D., Chen, W. H., Devos, D., Güell, M., Norambuena, T., Racke, I., Rybin, V., Schmidt, A., Yus, E., Aebersold, R., Herrmann, R., Böttcher, B., Frangakis, A. S., Russell, R. B., Serrano, L., Bork, P., and Gavin, A. C. (2009) Proteome organization in a genome-reduced bacterium. Science 326, 1235-1240
11. Nickell, S., Beck, F., Scheres, S. H., Korinek, A., Förster, F., Lasker, K., Mihalache, O., Sun, N., Nagy, I., Sali, A., Plitzko, J. M., Carazo, J. M., Mann, M., and Baumeister, W. (2009) Insights into the molecular architecture of the 26S proteasome. Proc. Natl. Acad. Sci. U.S.A. 106, 11943-11947
12. Malmström, J., Beck, M., Schmidt, A., Lange, V., Deutsch, E. W., and Aebersold, R. (2009) Proteome-wide cellular protein concentrations of the human pathogen Leptospira interrogans. Nature 460, 762-765
13. Golas, M. M., Böhm, C., Sander, B., Effenberger, K., Brecht, M., Stark, H., and Göringer, H. U. (2009) Snapshots of the RNA editing machine in trypanosomes captured at different assembly stages in vivo. EMBO J. 28, 766-778
14. Poliakov, A., van Duijn, E., Lander, G., Fu, C. Y., Johnson, J. E., Prevelige, P. E., Jr., and Heck, A. J. (2007) Macromolecular mass spectrometry and electron microscopy as complementary tools for investigation of the heterogeneity of bacteriophage portal assemblies. J. Struct. Biol. 157, 371-383
15. Lei, Z., Elmer, A. M., Watson, B. S., Dixon, R. A., Mendes, P. J., and Sumner, L. W. (2005) A two-dimensional electrophoresis proteomic reference map and systematic identification of 1367 proteins from a cell suspension culture of the model legume Medicago truncatula. Mol. Cell. Proteomics 4, 1812-1825
16. Shevchenko, A., Tomas, H., Havlis, J., Olsen, J. V., and Mann, M. (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat. Protoc. 1, 2856-2860
17. Shevchenko, A., Wilm, M., Vorm, O., and Mann, M. (1996) Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 68, 850-858
18. Häcker, I., Sander, B., Golas, M. M., Wolf, E., Karagöz, E., Kastner, B., Stark, H., Fabrizio, P., and Lührmann, R. (2008) Localization of Prp8, Brr2, Snu114 and U4/U6 proteins in the yeast tri-snRNP by electron microscopy. Nat. Struct. Mol. Biol. 15, 1206-1212
19. Golas, M. M., Sander, B., Will, C. L., Lührmann, R., and Stark, H. (2003) Molecular architecture of the multiprotein splicing factor SF3b. Science 300, 980-984
20. Gabashvili, I. S., Agrawal, R. K., Spahn, C. M., Grassucci, R. A., Svergun, D. I., Frank, J., and Penczek, P. (2000) Solution structure of the E. coli 70S ribosome at 11.5 A resolution. Cell 100, 537-549
21. Migneault, I., Dartiguenave, C., Bertrand, M. J., and Waldron, K. C. (2004) Glutaraldehyde: behavior in aqueous solution, reaction with proteins, and application to enzyme crosslinking. BioTechniques 37, 790-796, 798-802
22. Behrens, S. E., and Lührmann, R. (1991) Immunoaffinity purification of a [U4/U6.U5] tri-snRNP from human cells. Genes Dev. 5, 1439-1452
23. Fazekas de St Groth, S., Webster, R. G., and Datyner, A. (1963) Two new staining procedures for quantitative estimation of proteins on electrophoretic strips. Biochim. Biophys. Acta 71, 377-391
24. Whitton, J. L., Hundley, F., O'Donnell, B., and Desselberger, U. (1983) Silver staining of nucleic acids. Applications in virus research and in diagnostic virology. J. Virol. Methods 7, 185-198
25. Adrian, M., Dubochet, J., Lepault, J., and McDowall, A. W. (1984) Cryoelectron microscopy of viruses. Nature 308, 32-36
26. Sander, B., Golas, M. M., and Stark, H. (2005) Advantages of CCD detectors for de novo three-dimensional structure determination in single-particle electron microscopy. J. Struct. Biol. 151, 92-105
27. Perkins, D. N., Pappin, D. J., Creasy, D. M., and Cottrell, J. S. (1999) Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567
28. R Development Core Team (2008) R, R Foundation for Statistical Computing, Vienna, Austria
29. Chaudhry, C., Horwich, A. L., Brunger, A. T., and Adams, P. D. (2004) Exploring the structural dynamics of the E. coli chaperonin GroEL using translation-libration-screw crystallographic refinement of intermediate states. J. Mol. Biol. 342, 229-245
30. Makarov, E. M., Makarova, O. V., Urlaub, H., Gentzel, M., Will, C. L., Wilm, M., and Lührmann, R. (2002) Small nuclear ribonucleoprotein remodeling during catalytic activation of the spliceosome. Science 298, 2205-2208
31. Achsel, T., Brahms, H., Kastner, B., Bachi, A., Wilm, M., and Lührmann, R. (1999) A doughnut-shaped heteromer of human Sm-like proteins binds to the 3-end of U6 snRNA, thereby facilitating U4/U6 duplex formation in vitro. EMBO J. 18, 5789-5802
32. Pomeranz Krummel, D. A., Oubridge, C., Leung, A. K., Li, J., and Nagai, K. (2009) Crystal structure of human spliceosomal U1 snRNP at 5.5 A resolution. Nature 458, 475-480
33. Sander, B., Golas, M. M., Makarov, E. M., Brahms, H., Kastner, B., Lührmann, R., and Stark, H. (2006) Organization of core spliceosomal components U5 snRNA loop I and U4/U6 di-snRNP within U4/U6.U5 trisnRNP as revealed by electron cryomicroscopy. Mol. Cell 24, 267-278
34. Urlaub, H., Kruft, V., Bischof, O., Müller, E. C., and Wittmann-Liebold, B. (1995) Protein-rRNA binding features and their structural and functional implications in ribosomes as determined by cross-linking studies. EMBO J. 14, 4578-4588
35. Urlaub, H., Thiede, B., Müller, E. C., Brimacombe, R., and Wittmann-Liebold, B. (1997) Identification and sequence analysis of contact sites between ribosomal proteins and rRNA in Escherichia coli 30 S subunits by a new approach using matrix-assisted laser desorption/ionizationmass spectrometry combined with N-terminal microsequencing. J. Biol. Chem. 272, 14547-14555
36. Chepanoske, C. L., Richardson, B. E., von Rechenberg, M., and Peltier, J. M. (2005) Average peptide score: a useful parameter for identification of proteins derived from database searches of liquid chromatography/tandem mass spectrometry data. Rapid Commun. Mass Spectrom. 19, 9-14
37. Karaduman, R., Dube, P., Stark, H., Fabrizio, P., Kastner, B., and Lührmann, R. (2008) Structure of yeast U6 snRNPs: arrangement of Prp24p and the LSm complex as revealed by electron microscopy. RNA 14, 2528-2537
38. Herold, N., Will, C. L., Wolf, E., Kastner, B., Urlaub, H., and Lührmann, R. (2009) Conservation of the protein composition and electron microscopy structure of Drosophila melanogaster and human spliceosomal complexes. Mol. Cell. Biol. 29, 281-301
39. Bleichert, F., Gagnon, K. T., Brown, B. A., 2nd, Maxwell, E. S., Leschziner, A. E., Unger, V. M., and Baserga, S. J. (2009) A dimeric structure for archaeal box C/D small ribonucleoproteins. Science 325, 1384-1387
40. Chari, A., Golas, M. M., Klingenhäger, M., Neuenkirchen, N., Sander, B., Englbrecht, C., Sickmann, A., Stark, H., and Fischer, U. (2008) An assembly chaperone collaborates with the SMN complex to generate spliceosomal snRNPs. Cell 135, 497-509
41. Shi, Y., Di Giammartino, D. C., Taylor, D., Sarkeshik, A., Rice, W. J., Yates, J. R., 3rd, Frank, J., and Manley, J. L. (2009) Molecular architecture of the human pre-mRNA 3- processing complex. Mol. Cell 33, 365-376
42. Wang, H. W., Noland, C., Siridechadilok, B., Taylor, D. W., Ma, E., Felderer, K., Doudna, J. A., and Nogales, E. (2009) Structural insights into RNA processing by the human RISC-loading complex. Nat. Struct. Mol. Biol. 16, 1148-1153
43. Sanchez, M., Drechsler, M., Stark, H., and Lipps, G. (2009) DNA translocation activity of the multifunctional replication protein ORF904 from the archaeal plasmid pRN1. Nucleic Acids Res. 37, 6831-6848
44. Papai, G., Tripathi, M. K., Ruhlmann, C., Werten, S., Crucifix, C., Weil, P. A., and Schultz, P. (2009) Mapping the initiator binding Taf2 subunit in the structure of hydrated yeast TFIID. Structure 17, 363-373
45. Scheres, S. H., Melero, R., Valle, M., and Carazo, J. M. (2009) Averaging of electron subtomograms and random conical tilt reconstructions through likelihood optimization. Structure 17, 1563-1572
46. Hernández, H., Dziembowski, A., Taverner, T., Séraphin, B., and Robinson, C. V. (2006) Subunit architecture of multimeric complexes isolated directly from cells. EMBO Rep. 7, 605-610
47. Sharon, M., Taverner, T., Ambroggio, X. I., Deshaies, R. J., and Robinson, C. V. (2006) Structural organization of the 19S proteasome lid: insights from MS of intact complexes. PLoS Biol. 4, e267
48. Zhou, M., Sandercock, A. M., Fraser, C. S., Ridlova, G., Stephens, E., Schenauer, M. R., Yokoi-Fong, T., Barsky, D., Leary, J. A., Hershey, J. W., Doudna, J. A., and Robinson, C. V. (2008) Mass spectrometry reveals modularity and a complete subunit interaction map of the eukaryotic translation factor eIF3. Proc. Natl. Acad. Sci. U.S.A. 105, 18139-18144
49. Kovalenko, G. A., and Perminova, L. V. (2008) Immobilization of glucoamylase by adsorption on carbon supports and its application for heterogeneous hydrolysis of dextrin. Carbohydr. Res. 343, 1202-1211
50. Vasilescu, J., Guo, X., and Kast, J. (2004) Identification of protein-protein interactions using in vivo cross-linking and mass spectrometry. Proteomics 4, 3845-3854
51. Hood, B. L., Conrads, T. P., and Veenstra, T. D. (2006) Mass spectrometric analysis of formalin-fixed paraffin-embedded tissue: unlocking the proteome within. Proteomics 6, 4106-4114