Monitoring of changes in the membrane proteome during stationary phase adaptation of Bacillus subtilis using in vivo labeling techniques

Proteomics

Volumn 8, Issue 10, 2008, Pages 2062-2076

  Dreisbach, Annette ^a   Otto, Andreas ^a   Becher, Dörte ^a   Hammer, Elke ^a   Teumer, Alexander ^a   Gouw, Joost W ^b   Hecker, Michael ^a   Völker, Uwe ^a  

^a UNIVERSITY OF GREIFSWALD   (Germany)

^b UTRECHT UNIVERSITY   (Netherlands)

Author keywords

Bacillus subtilis; Membrane proteomics; Stable isotope labeling; Stationary phase adaptation

Indexed keywords

GLUCOSE; LYSINE; MEMBRANE PROTEIN; PROTEOME;

ARTICLE; BACILLUS SUBTILIS; BACTERIAL MEMBRANE; IN VIVO STUDY; ISOTOPE LABELING; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION; PROTEOMICS;

ADAPTATION, PHYSIOLOGICAL; BACILLUS SUBTILIS; BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; GENE EXPRESSION REGULATION, BACTERIAL; ISOTOPE LABELING; MEMBRANE PROTEINS; PROTEOMICS;

BACILLUS SUBTILIS; BACTERIA (MICROORGANISMS);

EID: 44649164495     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200701081     Document Type: Article

References (58)

1. Hecker, M., Völker, U., Towards a comprehensive understanding of Bacillus subtilis cell physiology by physiological proteomics. Proteomics 2004, 4, 3727-3750.
2. Bernhardt, J., Weibezahn, J., Scharf, C., Hecker, M., Bacillus subtilis during feast and famine: Visualization of the overall regulation of protein synthesis during glucose starvation by proteome analysis. Genome Res. 2003, 13, 224-237.
3. Völker, U., Engelmann, S., Maul, B., Riethdorf, S. et al., Analysis of the induction of general stress proteins of Bacillus subtilis. Microbiology 1994, 140, 741-752.
4. Tjalsma, H., Antelmann, H., Jongbloed, J. D., Braun, P. G. et al., Proteomics of protein secretion by Bacillus subtilis: Separating the "secrets" of the secretome. Microbiol. Mol. Biol. Rev. 2004, 68, 207-233.
5. Antelmann, H., Tjalsma, H., Voigt, B., Ohlmeier, S. et al., A proteomic view on genome-based signal peptide predictions. Genome Res. 2001, 11, 1484-1502.
6. Wilkins, M. R., Gasteiger, E., Sanchez, J. C., Bairoch, A., Hochstrasser, D. F., Two-dimensional gel electrophoresis for proteome projects: The effects of protein hydrophobicity and copy number. Electrophoresis 1998, 19, 1501-1505.
7. Adessi, C., Miege, C., Albrieux, C., Rabilloud, T., Two-dimensional electrophoresis of membrane proteins: A current challenge for immobilized pH gradients. Electrophoresis 1997, 18, 127-135.
8. Wall, D. B., Berger, S. J., Finch, J. W., Cohen, S. A. et al., Continuous sample deposition from reversed-phase liquid chromatography to tracks on a matrix-assisted laser desorption/ionization precoated target for the analysis of protein digests. Electrophoresis 2002, 23, 3193-3204.
9. Washburn, M. P., Ulaszek, R., Deciu, C., Schieltz, D. M., Yates, J. R., III, Analysis of quantitative proteomic data generated via multidimensional protein identification technology. Anal. Chem. 2002, 14, 1650-1657.
10. Peng, J., Elias, J. E., Thoreen, C. C., Licklider, L. J., Gygi, S. P., Evaluation of multidimensional chromatography coupled with tandem mass spectrometry (LC/LC-MS/MS) for large-scale protein analysis: The yeast proteome. J. Proteome Res. 2003, 2, 43-50.
11. Eymann, C., Dreisbach, A., Albrecht, D., Bernhardt, J. et al., A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 2004, 4, 2849-2876.
12. Wolff, S., Otto, A., Albrecht, D., Zeng, J. S. et al., Gel-free and gel-based proteomics in Bacillus subtilis: A comparative study. Mol. Cell. Proteomics 2006, 5, 1183-1192.
13. Bunai, K., Ariga, M., Inoue, T., Nozaki, M. et al., Profiling and comprehensive expression analysis of ABC transporter solute-binding proteins of Bacillus subtilis membrane based on a proteomic approach. Electrophoresis 2004, 25, 141-155.
14. Bunai, K., Yamane, K., Effectiveness and limitation of two-dimensional gel electrophoresis in bacterial membrane protein proteomics and perspectives. J. Chromatogr. 2005, 815, 227-236.
15. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B. et al., Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol. Cell. Proteomics 2002, 1, 376-386.
16. Conrads, T. P., Alving, K., Veenstra, T. D., Belov, M. E. et al., Quantitative analysis of bacterial and mammalian proteomes using a combination of cysteine affinity tags and 15N-metabolic labeling. Anal. Chem. 2001, 73, 2132-2139.
17. Wu, C. C., MacCoss, M. J., Howell, K. E., Matthews, D. E., Yates, J. R., III, Metabolic labeling of mammalian organisms with stable isotopes for quantitative proteomic analysis. Anal. Chem. 2004, 76, 4951-4959.
18. Smith, I., Paress, P., Cabane, K., Dubnau, E., Genetics and physiology of the rel system of Bacillus subtilis. Mol. Gen. Genet. 1980, 178, 271-279.
19. Anagnostopoulos, C., Spizizen, J., Requirements for transformation in Bacillus subtilis. J. Bacteriol. 1961, 81, 741-746.
20. Stülke, J., Hanschke, R., Hecker, M., Temporal activation of beta-glucanase synthesis in Bacillus subtilis is mediated by the GTP pool. J. Gen. Microbiol. 1993, 139, 2041-2045.
21. Möller, S., Croning, M. D., Apweiler, R., Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 2001, 17, 646-653.
22. Nakai, K., Kanehisa, M., A knowledge base for predicting protein localization sites in eukaryotic cells. Genomics 1992, 14, 897-911.
23. Sonnhammer, E. L. L., vonHeijne, G., Krogh, A., in: Glasgow, J., Littlejohn, T., Major, F., Lathrop, R. (Eds.), Proceedings of the Sixth International Conference on Intelligent Systems for Molecular Biology, AAAI Press, Menlo Park, CA 1998, pp. 175-182.
24. Tusnády, G. E., Simon, I., Principles governing amino acid composition of integral membrane proteins: Application to topology prediction. J. Mol. Biol. 1998, 283, 489-506.
25. Hirokawa, T., Boon-Chieng, S., Mitaku, S., SOSUI: Classification and secondary structure prediction system for membrane proteins. Bioinformatics 1998, 14, 378-379.
26. Tjalsma, H., Bolhuis, A., Jongbloed, J. D., Bron, S., van Dijl, J. M., Signal peptide-dependent protein transport in Bacillus subtilis: A genome-based survey of the secretome. Microbiol. Mol. Biol. Rev. 2000, 64, 515-547.
27. Tjalsma, H., Feature-based reappraisal of the Bacillus subtilis exoproteome. Proteomics 2007, 7, 73-81.
28. Chang, S., Cohen, S. N., High frequency transformation of Bacillus subtilis protoplasts by plasmid DNA. Mol. Gen. Genet. 1979, 168, 111-115.
29. Olsen, J. V., Ong, S. E., Mann, M., Trypsin cleaves exclusively C-terminal to arginine and lysine residues. Mol. Cell. Proteomics 2004, 3, 608-614.
30. Schulze, W. X., Mann, M., A novel proteomic screen for peptide-protein interactions. J. Biol. Chem. 2004, 279, 10756-10764.
31. Klein, C., Garcia-Rizo, C., Bisle, B., Scheffer, B. et al., The membrane proteome of Halobacterium salinarum. Proteomics 2005, 5, 180-197.
32. Blonder, J., Goshe, M. B., Xiao, W., Camp, D. G., II et al., Global analysis of the membrane subproteome of Pseudomonas aeruginosa using liquid chromatography-tandem mass spectrometry. J. Proteome Res. 2004, 3, 434-444.
33. Fischer, F., Wolters, D., Rogner, M., Poetsch, A., Toward the complete membrane proteome: High coverage of integral membrane proteins through transmembrane peptide detection. Mol. Cell. Proteomics 2006, 5, 444-453.
34. Kyte, J., Doolittle, R. F., A simple method for displaying the hydropathic character of a protein. J. Mol. Biol. 1982, 157, 105-132.
35. Tjalsma, H., van Dijl, J. M., Proteomics-based consensus prediction of protein retention in a bacterial membrane. Proteomics 2005, 5, 4472-4482.
36. Molina, H., Parmigiani, G., Pandey, A., Assessing reproducibility of a protein dynamics study using in vivo labeling and liquid chromatography tandem mass spectrometry. Anal. Chem. 2005, 77, 2739-2744.
37. Sao-Jose, C., Lhuillier, S., Lurz, R., Melki, R. et al., The ecto-domain of the viral receptor YueB forms a fiber that triggers ejection of bacteriophage SPP1 DNA. J. Biol. Chem. 2006, 281, 11464-11470.
38. Rohrbough, J. G., Breci, L., Merchant, N., Miller, S., Haynes, P. A., Verification of single-peptide protein identifications by the application of complementary database search algorithms. J. Biomol. Tech. 2006, 17, 327-332.
39. Weatherly, D. B., Astwood, J. A., III, Minning, T. A., Cavola, C. et al., A Heuristic method for assigning a false-discovery rate for protein identifications from Mascot database search results. Mol. Cell. Proteomics 2005, 4, 762-772.
40. Higdon, R., Kolker, E., A predictive model for identifying proteins by a single peptide match. Bioinformatics 2007, 23, 277-280.
41. Li, X. J., Zhang, H., Ranish, J. A., Aebersold, R., Automated statistical analysis of protein abundance ratios from data generated by stable-isotope dilution and tandem mass spectrometry. Anal. Chem. 2003, 75, 6648-6657.
42. Pan, C., Kora, G., McDonald, W. H., Tabb, D. L. et al., ProRata: A quantitative proteomics program for accurate protein abundance ratio estimation with confidence interval evaluation. Anal. Chem. 2006, 78, 7121-7131.
43. MacCoss, M. J., Wu, C. C., Liu, H., Sadygov, R., Yates, J. R., III, A correlation algorithm for the automated quantitative analysis of shotgun proteomics data. Anal. Chem. 2003, 75, 6912-6921.
44. Yoshida, K., Kobayashi, K., Miwa, Y., Kang, C. M. et al., Combined transcriptome and proteome analysis as a powerful approach to study genes under glucose repression in Bacillus subtilis. Nucleic Acids Res. 2001, 29, 683-692.
45. Lorca, G. L., Chung, Y. J., Barabote, R. D., Weyler, W. et al., Catabolite repression and activation in Bacillus subtilis: Dependency on CcpA, HPr, and HprK. J. Bacteriol. 2005, 187, 7826-7839.
46. Koburger, T., Weibezahn, J., Bernhardt, J., Homuth, G., Hecker, M., Genome-wide mRNA profiling in glucose starved Bacillus subtilis cells. Mol. Genet. Genomics 2005, 274, 1-12.
47. Remaut, H., Bompard-Gilles, C., Goffin, C., Frere, J. M., Van Beeumen, J., Structure of the Bacillus subtilis D-amino-peptidase DppA reveals a novel self-compartmentalizing protease. Nat. Struct. Biol. 2001, 8, 674-678.
48. Slack, F. J., Mueller, J. P., Sonenshein, A. L., Mutations that relieve nutritional repression of the Bacillus subtilis dipeptide permease operon. J. Bacteriol. 1993, 175, 4605-4614.
49. Yu, J., Hederstedt, L., Piggot, P. J., The cytochrome Decomplex (menaquinone:cytochrome c reductase) in Bacillus subtilis has a nontraditional subunit organization. J. Bacteriol. 1995, 177, 6751-6760.
50. Yamashita, S., Kawamura, F., Yoshikawa, H., Takahashi, H. et al., Dissection of the expression signals of the spoA gene of Bacillus subtilis: Glucose represses sporulation-specific expression. J. Gen. Microbiol. 1989, 135, 1335-1345.
51. Hanson, R. S., Cox, D. P., Effect of different nutritional conditions on the synthesis of tricarboxylic acid cycle enzymes. J. Bacteriol. 1967, 93, 1777-1787.
52. Jin, S., Sonenshein, A. L., Transcriptional regulation of Bacillus subtilis citrate synthase genes. J. Bacteriol. 1994, 176, 4680-4690.
53. Kim, J. H., Voskuil, M. I., Chambliss, G. H., NADP, corepressor for the Bacillus catabolite control protein CcpA. Proc. Natl. Acad. Sci. USA 1998, 95, 9590-9595.
54. Tobisch, S., Zühlke, D., Bernhardt, J., Stülke, J., Hecker, M., Role of CcpA in regulation of the central pathways of carbon catabolism in Bacillus subtilis. J. Bacteriol. 1999, 181, 6996-7004.
55. Perego, M., Higgins, C. F., Pearce, S. R., Gallagher, M. P., Hoch, J. A., The oligopeptide transport system of Bacillus subtilis plays a role in the initiation of sporulation. Mol. Microbiol. 1991, 5, 173-185.
56. Eymann, C., Homuth, G., Scharf, C., Hecker, M., Bacillus subtilis functional genomics: Global characterization of the stringent response by proteome and transcriptome analysis. J. Bacteriol. 2002, 184, 2500-2520.
57. Koide, A., Hoch, J. A., Identification of a second oligopeptide transport system in Bacillus subtilis and determination of its role in sporulation. Mol. Microbiol. 1994, 13, 417-426.
58. Huang, X., Gaballa, A., Cao, M., Helmann, J. D., Identification of target promoters for the Bacillus subtilis extra-cytoplasmic function sigma factor, sigma W. Mol. Microbiol. 1999, 31, 361-371.