Genome-wide identification of the subcellular localization of the Escherichia coli B proteome using experimental and computational methods

Proteomics

Volumn 11, Issue 7, 2011, Pages 1213-1227

  Han, Mee Jung ^a,b   Yun, Hongseok ^a   Lee, Jeong Wook ^a   Lee, Yu Hyun ^a   Lee, Sang Yup ^a   Yoo, Jong Shin ^c   Kim, Jin Young ^c   Kim, Jihyun F ^d   Hur, Cheol Goo ^d  

^a Korea Advanced Institute of Science and Technology (KAIST)   (South Korea)

^b Dongyang University   (South Korea)

^c Korea Basic Science Institute (KBSI)   (South Korea)

^d Korea Research Institute of Bioscience and Biotechnology (KRIBB)   (South Korea)

Author keywords

Computational prediction; Escherichia coli B; Microbiology; Subcellular localization

Indexed keywords

BACTERIAL PROTEIN; CYTOPLASM PROTEIN; OUTER MEMBRANE PROTEIN; PERIPLASMIC PROTEIN; PROTEOME;

ARTICLE; BACTERIAL GENOME; CELLULAR DISTRIBUTION; ESCHERICHIA COLI; ESCHERICHIA COLI B; EXPERIMENTAL MODEL; GENETIC ASSOCIATION; LIQUID CHROMATOGRAPHY; MATHEMATICAL MODEL; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN LOCALIZATION; TANDEM MASS SPECTROMETRY; TWO DIMENSIONAL ELECTROPHORESIS;

BACTERIAL PROTEINS; CELL MEMBRANE; CHROMATOGRAPHY, LIQUID; CYTOPLASM; DATABASES, GENETIC; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; ESCHERICHIA COLI; EXTRACELLULAR SPACE; GENOME, BACTERIAL; MASS SPECTROMETRY; MATHEMATICAL COMPUTING; MEMBRANE PROTEINS; MOLECULAR SEQUENCE DATA; OPEN READING FRAMES; PERIPLASM; PROTEOME; RESEARCH DESIGN; SPECIES SPECIFICITY; SUBCELLULAR FRACTIONS;

ESCHERICHIA COLI B; ESCHERICHIA COLI K12;

EID: 79953052029     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201000191     Document Type: Article

References (79)

1. Choi, J. H., Keum, K. C., Lee, S. Y., Production of recombinant proteins by high cell density culture of Escherichia coli. Chem. Eng. Sci. 2006, 61, 876-885.
2. Luli, G. W., Strohl, W. R., Comparison of growth, acetate production, and acetate inhibition of Escherichia coli strains in batch and fed-batch fermentations. Appl. Environ. Microbiol. 1990, 56, 1004-1011.
3. Blattner, F. R., Plunkett, G., Bloch, C. A., Perna, N. T. et al., The complete genome sequence of Escherichia coli K-12. Science 1997, 277, 1453-1462.
4. Hayashi, K., Morooka, N., Yamamoto, Y., Fujita, K. et al., Highly accurate genome sequences of Escherichia coli K-12 strains MG1655 and W3110. Mol. Syst. Biol. 2006, 2, 2006.0007.
5. Han, M. J., Lee, S. Y., The Escherichia coli proteome: past, present, and future prospects. Microbiol. Mol. Biol. Rev. 2006, 70, 362-439.
6. Joyce, A. R., Palsson, B. O., The model organism as a system: integrating "omics" data sets. Nat. Rev. Mol. Cell Biol. 2006, 7, 198-210.
7. Yun, H., Lee, J. W., Jeong, J., Chung, J. et al., EcoProDB: the Escherichia coli protein database. Bioinformatics 2007, 23, 2501-2503.
8. Lopez-Campistrous, A., Semchuk, P., Burke, L., Palmer-Stone, T. et al., Localization, annotation, and comparison of the Escherichia coli K-12 proteome under two states of growth. Mol. Cell. Proteomics 2005, 4, 1205-1209.
9. Jeong, H., Barbe, V., Lee, C. H., Vallenet, D. et al., Genome sequences of Escherichia coli B strains REL606 and BL21(DE3). J. Mol. Biol. 2009, 394, 644-652.
10. Studier, F. W., Daegelen, P., Lenski, R. E., Maslov, S., Kim, J. F., Understanding the differences between genome sequences of Escherichia coli B strains REL606 and BL21(DE3) and comparison of the E. coli B and K-12 genomes. J. Mol. Biol. 2009, 394, 653-680.
11. Daegelen, P., Studier, F. W., Lenski, R. E., Cure, S., Kim, J. F., Tracing ancestors and relatives of Escherichia coli B, and the derivation of B strains REL606 and BL21(DE3). J. Mol. Biol. 2009, 394, 634-643.
12. Lee, S. Y., Chang, H. N., High cell-density cultivation of Escherichia coli W using sucrose as a carbon source. Biotechnol. Lett. 1993, 15, 971-974.
13. Nandakumar, M. P., Cheung, A., Marten, M. R., Proteomic analysis of extracellular proteins from Escherichia coli W3110. J. Proteome Res. 2006, 5, 1155-1161.
14. Xia, X. X., Han, M. J., Lee, S. Y., Yoo, J. S., Comparison of the extracellular proteomes of Escherichia coli B and K-12 strains during high cell density cultivation. Proteomics 2008, 8, 2089-2103.
15. Schoenfeld, T., Convenient, rapid enrichment of periplasmic and spheroplasmic protein fractions using the new PeriPreps™ periplasting kit. Epicentre Forum 1998, 5, 5.
16. Osborn, M. J., Gander, J. E., Parisi, E., Carson, J., Mechanism of assembly of outer membrane of Salmonella typhimurium: isolation and characterization of cytoplasmic and outer membrane. J. Biol. Chem. 1972, 247, 3962-3972.
17. Han, M. J., Lee, J. W., Lee, S. Y., Enhanced proteome profiling by inhibiting proteolysis with small heat shock proteins. J. Proteome Res. 2005, 4, 2429-2434.
18. Bradford, M. M., Rapid and sensitive method for quantitation of microgram quantities of protein utilizing principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
19. Lee, J. W., Lee, S. Y., Song, H., Yoo, J. S., The proteome of Mannheimia succiniciproducens, a capnophilic rumen bacterium. Proteomics 2006, 6, 3550-3566.
20. Laemmli, U. K., Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature 1970, 227, 680-685.
21. Han, M. J., Herlyn, M., Fisher, A. B., Speicher, D. W., Microscale solution IEF combined with 2-D DIGE substantially enhances analysis depth of complex proteomes such as mammalian cell and tissue extracts. Electrophoresis 2008, 29, 695-705.
22. Asfalg, J. G. J., Kriegel, H.-P., Pryakhin, A., Wei, T., Zimek, A., Supervised ensembles of prediction methods for subcellular localization, 6th Asia Pacific Bioinformatics Conf. (APBC'08), Kyoto, Japan 2008, pp. 29-38.
23. Bulashevska, A., Eils, R., Predicting protein subcellular locations using hierarchical ensemble of Bayesian classifiers based on Markov chains. BMC Bioinformatics 2006, 7, 298.
24. Rashid, M., Saha, S., Raghava, G. P. S., Support vector machine-based method for predicting subcellular localization of mycobacterial proteins using evolutionary information and motifs. BMC Bioinformatics 2007, 8, 337.
25. Viratyosin, W., Ingsriswang, S., Pacharawongsakda, E., Palittapongarnpim, P., Genome-wide subcellular localization of putative outer membrane and extracellular proteins in Leptospira interrogans serovar Lai genome using bioinformatics approaches. BMC Genomics 2008, 9, 181.
26. Gardy, J. L., Laird, M. R., Chen, F., Rey, S. et al., PSORTb v.2.0: expanded prediction of bacterial protein subcellular localization and insights gained from comparative proteome analysis. Bioinformatics 2005, 21, 617-623.
27. Lu, Z., Szafron, D., Greiner, R., Lu, P. et al., Predicting subcellular localization of proteins using machine-learned classifiers. Bioinformatics 2004, 20, 547-556.
28. Bhasin, M., Garg, A., Raghava, G. P. S., PSLpred: prediction of subcellular localization of bacterial proteins. Bioinformatics 2005, 21, 2522-2524.
29. Gardy, J. L., Brinkman, F. S. L., Methods for predicting bacterial protein subcellular localization. Nat. Rev. Microbiol. 2006, 4, 741-751.
30. Bendtsen, J. D., Nielsen, H., von Heijne, G., Brunak, S., Improved prediction of signal peptides: SignalP 3.0. J. Mol. Biol. 2004, 340, 783-795.
31. Emanuelsson, O., Brunak, S., von Heijne, G., Nielsen, H., Locating proteins in the cell using TargetP, SignalP and related tools. Nat. Protoc. 2007, 2, 953-971.
32. Juncker, A. S., Willenbrock, H., Von Heijne, G., Brunak, S. et al., Prediction of lipoprotein signal peptides in Gram-negative bacteria. Protein Sci. 2003, 12, 1652-1662.
33. Kall, L., Krogh, A., Sonnhammer, E. L. L., A combined transmembrane topology and signal peptide prediction method. J. Mol. Biol. 2004, 338, 1027-1036.
34. Krogh, A., Larsson, B., von Heijne, G., Sonnhammer, E. L. L., Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J. Mol. Biol. 2001, 305, 567-580.
35. Garrow, A. G., Agnew, A., Westhead, D. R., TMB-Hunt: an amino acid composition based method to screen proteomes for beta-barrel transmembrane proteins. BMC Bioinformatics 2005, 6, 56.
36. Nair, R., Rost, B., Sequence conserved for subcellular localization. Protein Sci. 2002, 11, 2836-2847.
37. Nair, R., Rost, B., Better prediction of sub-cellular localization by combining evolutionary and structural information. Proteins 2003, 53, 917-930.
38. Guo, T., Hua, S. J., Ji, X. L., Sun, Z. R., DBSubLoc: database of protein subcellular localization. Nucleic Acids Res. 2004, 32, D122-D124.
39. McGuffin, L. J., Street, S., Sorensen, S. A., Jones, D. T., The genomic threading database. Bioinformatics 2004, 20, 131-132.
40. Lomize, M. A., Lomize, A. L., Pogozheva, I. D., Mosberg, H. I., OPM: orientations of proteins in membranes database. Bioinformatics 2006, 22, 623-625.
41. Laskowski, R. A., Chistyakov, V. V., Thornton, J. M., PDBsum more: new summaries and analyses of the known 3D structures of proteins and nucleic acids. Nucleic Acids Res. 2005, 33, D266-D268.
42. Kouranov, A., Xie, L., De la Cruz, J., Chen, L. et al., The RCSB PDB information portal for structural genomics. Nucleic Acids Res. 2006, 34, D302-D305.
43. Baldi, P., Brunak, S., Chauvin, Y., Andersen, C. A. F., Nielsen, H., Assessing the accuracy of prediction algorithms for classification: an overview. Bioinformatics 2000, 16, 412-424.
44. Bagos, P. G., Liakopoulos, T. D., Spyropoulos, I. C., Hamodrakas, S. J., PRED-TMBB: a web server for predicting the topology of beta-barrel outer membrane proteins. Nucleic Acids Res. 2004, 32, W400-W404.
45. Jeong, K. J., Lee, S. Y., Excretion of human beta-endorphin into culture medium by using outer membrane protein F as a fusion partner in recombinant Escherichia coli. Appl. Environ. Microbiol. 2002, 68, 4979-4985.
46. Qian, Z. G., Xia, X. X., Choi, J. H., Lee, S. Y., Proteome-based identification of fusion partner for high-level extracellular production of recombinant proteins in Escherichia coli. Biotechnol. Bioeng. 2008, 101, 587-601.
47. Zhang, G. J., Brokx, S., Weiner, J. H., Extracellular accumulation of recombinant proteins fused to the carrier protein YebF in Escherichia coli. Nat. Biotechnol. 2006, 24, 100-104.
48. Lenski, R. E., Rose, M. R., Simpson, S. C., Tadler, S. C., Long-term experimental evolution in Escherichia coli.1. Adaptation and divergence during 2, 000 generations. Am. Nat. 1991, 138, 1315-1341.
49. Lukjancenko, O., Wassenaar, T. M., Ussery, D. W., Comparison of 61 sequenced Escherichia coli genomes. Microb. Ecol. 2010, 60, 708-720.
50. Schryvers, A., Lohmeier, E., Weiner, J. H., Chemical and functional properties of native and reconstituted forms of membrane-bound, aerobic glycerol-3-phosphate dehydrogenase of Escherichia coli. J. Biol. Chem. 1978, 253, 783-788.
51. Gal, J., Szvetnik, A., Schnell, R., Kalman, M., The metD D-methionine transporter locus of Escherichia coli is an ABC transporter gene cluster. J. Bacteriol. 2002, 184, 4930-4932.
52. Elena, S. F., Whittam, T. S., Winkworth, C. L., Riley, M. A., Lenski, R. E., Genomic divergence of Escherichia coli strains: evidence for horizontal transfer and variation in mutation rates. Int. Microbiol. 2005, 8, 271-278.
53. Schneider, D., Duperchy, E., Depeyrot, J., Coursange, E. et al., Genomic comparisons among Escherichia coli strains B, K-12, and O157:H7 using IS elements as molecular markers. BMC Microbiol. 2002, 2, 18.
54. Ramani, N., Hedeshian, M., Freundlich, M., MicF antisense RNA has a major role in osmoregulation of ompF in Escherichia coli. J. Bacteriol. 1994, 176, 5005-5010.
55. McBroom, A. J., Kuehn, M. J., Release of outer membrane vesicles by gram-negative bacteria is a novel envelope stress response. Mol. Microbiol. 2007, 63, 545-558.
56. Kuehn, M. J., Kesty, N. C., Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005, 19, 2645-2655.
57. Mashburn-Warren, L. M., Whiteley, M., Special delivery: vesicle trafficking in prokaryotes. Mol. Microbiol. 2006, 61, 839-846.
58. Beveridge, T. J., Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 1999, 181, 4725-4733.
59. Lee, E. Y., Bang, J. Y., Park, G. W., Choi, D. S. et al., Global proteomic profiling of native outer membrane vesicles derived from Escherichia coli. Proteomics 2007, 7, 3143-3153.
60. Horstman, A. L., Kuehn, M. J., Enterotoxigenic Escherichia coli secretes active heat-labile enterotoxin via outer membrane vesicles. J. Biol. Chem. 2000, 275, 12489-12496.
61. Kesty, N. C., Mason, K. M., Reedy, M., Miller, S. E., Kuehn, M. J., Enterotoxigenic Escherichia coli vesicles target toxin delivery into mammalian cells. EMBO J. 2004, 23, 4538-4549.
62. McBroom, A. J., Johnson, A. P., Vemulapalli, S., Kuehn, M. J., Outer membrane vesicle production by Escherichia coli is independent of membrane instability. J. Bacteriol. 2006, 188, 5385-5392.
63. Rey, S., Gardy, J. L., Brinkman, F. S., Assessing the precision of high-throughput computational and laboratory approaches for the genome-wide identification of protein subcellular localization in bacteria. BMC Genomics 2005, 6, 162.
64. Chou, K. C., Shen, H. B., Recent progress in protein subcellular location prediction. Anal. Biochem. 2007, 370, 1-16.
65. Garg, A., Bhasin, M., Raghava, G. P. S., Support vector machine-based method for subcellular localization of human proteins using amino acid compositions, their order, and similarity search. J. Biol. Chem. 2005, 280, 14427-14432.
66. 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.
67. Huang, C. Z., Lin, X. M., Wu, L. N., Zhang, D. F. et al., Systematic identification of the subproteome of Escherichia coli cell envelope reveals the interaction network of membrane proteins and membrane-associated peripheral proteins. J. Proteome Res. 2006, 5, 3268-3276.
68. Zhang, L. J., Xie, J. Y., Wang, X., Liu, X. H. et al., Proteomic analysis of mouse liver plasma membrane: use of differential extraction to enrich hydrophobic membrane proteins. Proteomics 2005, 5, 4510-4524.
69. Fan, B., Rosen, B. P., Biochemical characterization of CopA, the Escherichia coli Cu(I)-translocating P-type ATPase. J. Biol. Chem. 2002, 277, 46987-46992.
70. Rensing, C., Fan, B., Sharma, R., Mitra, B., Rosen, B. P., CopA: an Escherichia coli Cu(I)-translocating P-type ATPase. Proc. Natl. Acad. Sci. USA 2000, 97, 652-656.
71. Cai, M. L., Williams, D. C., Wang, G. S., Lee, B. R. et al., Solution structure of the phosphoryl transfer complex between the signal-transducing protein IIA(Glucose) and the cytoplasmic domain of the glucose transporter IICBGlucose of the Escherichia coli glucose phosphotransferase system. J. Biol. Chem. 2003, 278, 25191-25206.
72. Daley, D. O., Rapp, M., Granseth, E., Melen, K. et al., Global topology analysis of the Escherichia coli inner membrane proteome. Science 2005, 308, 1321-1323.
73. Leif, H., Sled, V. D., Ohnishi, T., Weiss, H., Friedrich, T., Isolation and characterization of the proton-translocating NADH:ubiquinone oxidoreductase from Escherichia coli. Eur. J. Biochem. 1995, 230, 538-548.
74. Stenberg, F., Chovanec, P., Maslen, S. L., Robinson, C. V. et al., Protein complexes of the Escherichia coli cell envelope. J. Biol. Chem. 2005, 280, 34409-34419.
75. Cole, S. T., Eiglmeier, K., Ahmed, S., Honore, N. et al., Nucleotide-sequence and gene-polypeptide relationships of the glpABC operon encoding the anaerobic sn-glycerol-3-phosphate dehydrogenase of Escherichia coli K-12. J. Bacteriol. 1988, 170, 2448-2456.
76. Miki, K., Lin, E. C. C., Enzyme complex which couples glycerol-3-phosphate dehydrogenation to fumarate reduction in Escherichia coli. J. Bacteriol. 1973, 114, 767-771.
77. Robillard, G. T., Broos, J., Structure/function studies on the bacterial carbohydrate transporters, enzymes II, of the phosphoenolpyruvate-dependent phosphotransferase system. Biochim. Biophys. Acta. 1999, 1422, 73-104.
78. 2 of the Escherichia coli NADH:ubiquinone oxidoreductase (Complex I) is located on subunit NuoB. J. Biol. Chem. 2003, 278, 47602-47609.
79. Spehr, V., Schlitt, A., Scheide, D., Guenebaut, V., Friedrich, T., Overexpression of the Escherichia coli nuo-operon and isolation of the overproduced NADH:ubiquinone oxidoreductase (complex I). Biochemistry 1999, 38, 16261-16267.