Two-dimensional gel electrophoresis in bacterial proteomics

Shirly O. T. Curreem1, Rory M. Watt2, Susanna K. P. Lau1,3,4,5(), Patrick C. Y. Woo1,3,4,5()

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Protein Cell ›› 2012, Vol. 3 ›› Issue (5) : 346-363. DOI: 10.1007/s13238-012-2034-5
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Two-dimensional gel electrophoresis in bacterial proteomics

  • Shirly O. T. Curreem1, Rory M. Watt2, Susanna K. P. Lau1,3,4,5(), Patrick C. Y. Woo1,3,4,5()
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Abstract

Two-dimensional gel electrophoresis (2-DE) is a gel-based technique widely used for analyzing the protein composition of biological samples. It is capable of resolving complex mixtures containing more than a thousand protein components into individual protein spots through the coupling of two orthogonal biophysical separation techniques: isoelectric focusing (first dimension) and polyacrylamide gel electrophoresis (second dimension). 2-DE is ideally suited for analyzing the entire expressed protein complement of a bacterial cell: its proteome. Its relative simplicity and good reproducibility have led to 2-DE being widely used for exploring proteomics within a wide range of environmental and medically-relevant bacteria. Here we give a broad overview of the basic principles and historical development of gel-based proteomics, and how this powerful approach can be applied for studying bacterial biology and physiology. We highlight specific 2-DE applications that can be used to analyze when, where and how much proteins are expressed. The links between proteomics, genomics and mass spectrometry are discussed. We explore how proteomics involving tandem mass spectrometry can be used to analyze (post-translational) protein modifications or to identify proteins of unknown origin by de novo peptide sequencing. The use of proteome fractionation techniques and non-gel-based proteomic approaches are also discussed. We highlight how the analysis of proteins secreted by bacterial cells (secretomes or exoproteomes) can be used to study infection processes or the immune response. This review is aimed at non-specialists who wish to gain a concise, comprehensive and contemporary overview of the nature and applications of bacterial proteomics.

Keywords

two-dimensional gel electrophoresis / bacteria / proteomics

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Shirly O. T. Curreem, Rory M. Watt, Susanna K. P. Lau, Patrick C. Y. Woo. Two-dimensional gel electrophoresis in bacterial proteomics. Prot Cell, 2012, 3(5): 346‒363 https://doi.org/10.1007/s13238-012-2034-5

References

[1] Aebersold, R., and Goodlett, D.R. (2001). Mass spectrometry in proteomics. Chem Rev 101, 269-295 .10.1021/cr990076h
[2] Aebersold, R., and Mann, M. (2003). Mass spectrometry-based proteomics. Nature 422, 198-207 .10.1038/nature01511
[3] Al Dahouk, S., Jubier-Maurin, V., Scholz, H.C., Tomaso, H., Karges, W., Neubauer, H., and K?hler, S. (2008). Quantitative analysis of the intramacrophagic Brucella suis proteome reveals metabolic adaptation to late stage of cellular infection. Proteomics 8, 3862-3870 .10.1002/pmic.200800026
[4] Altarriba, M., Merino, S., Gavín, R., Canals, R., Rabaan, A., Shaw, J.G., and Tomás, J.M. (2003). A polar flagella operon (flg) of Aeromonas hydrophila contains genes required for lateral flagella expression. Microb Pathog 34, 249-259 .10.1016/S0882-4010(03)00047-0
[5] Alteri, C.J., Smith, S.N., and Mobley, H.L. (2009). Fitness of Escherichia coli during urinary tract infection requires gluconeogenesis and the TCA cycle. PLoS Pathog 5, e1000448.10.1371/journal.ppat.1000448
[6] Anglade, P., Demey, E., Labas, V., Le Caer, J.P., and Chich, J.F. (2000). Towards a proteomic map of Lactococcus lactis NCDO 763. Electrophoresis 21, 2546-2549 .10.1002/1522-2683(20000701)21:12<2546::AID-ELPS2546>3.0.CO;2-J
[7] Antelmann, H., Tjalsma, H., Voigt, B., Ohlmeier, S., Bron, S., van Dijl, J.M., and Hecker, M. (2001). A proteomic view on genome-based signal peptide predictions. Genome Res 11, 1484-1502 .10.1101/gr.182801
[8] Appel, R.D., Hochstrasser, D.F., Funk, M., Vargas, J.R., Pellegrini, C., Muller, A.F., and Scherrer, J.R. (1991). The MELANIE project: from a biopsy to automatic protein map interpretation by computer. Electrophoresis 12, 722-735 .10.1002/elps.1150121006
[9] Appel, R.D., Sanchez, J.C., Bairoch, A., Golaz, O., Miu, M., Vargas, J.R., and Hochstrasser, D.F. (1993). SWISS-2DPAGE: a database of two-dimensional gel electrophoresis images. Electrophoresis 14, 1232-1238 .10.1002/elps.11501401185
[10] Bendt, A.K., Burkovski, A., Schaffer, S., Bott, M., Farwick, M., Hermann, T., Farwick, M., and Hermann, T. (2003). Towards a phosphoproteome map of Corynebacterium glutamicum. Proteomics 3, 1637-1646 .10.1002/pmic.200300494
[11] Bendtsen, J.D., Kiemer, L., Fausb?ll, A., and Brunak, S. (2005). Non-classical protein secretion in bacteria. BMC Microbiol 5, 58.10.1186/1471-2180-5-58
[12] Bernardini, G., Laschi, M., Serchi, T., Arena, S., D’Ambrosio, C., Braconi, D., Scaloni, A., and Santucci, A. (2011). Mapping phosphoproteins in Neisseria meningitidis serogroup A. Proteomics 11, 1351-1358 .10.1002/pmic.201000406
[13] Bjellqvist, B., Ek, K., Righetti, P.G., Gianazza, E., G?rg, A., Westermeier, R., and Postel, W. (1982). Isoelectric focusing in immobilized pH gradients: principle, methodology and some applications. J Biochem Biophys Methods 6, 317-339 .10.1016/0165-022X(82)90013-6
[14] Blomberg, A., Blomberg, L., Norbeck, J., Fey, S.J., Larsen, P.M., Larsen, M., Roepstorff, P., Degand, H., Boutry, M., Posch, A., . (1995). Interlaboratory reproducibility of yeast protein patterns analyzed by immobilized pH gradient two-dimensional gel electrophoresis. Electrophoresis 16, 1935-1945 .10.1002/elps.11501601320
[15] Breen, E.J., Hopwood, F.G., Williams, K.L., and Wilkins, M.R. (2000). Automatic poisson peak harvesting for high throughput protein identification. Electrophoresis 21, 2243-2251 .10.1002/1522-2683(20000601)21:11<2243::AID-ELPS2243>3.0.CO;2-K
[16] Bumann, D. (2010). Pathogen proteomes during infection: A basis for infection research and novel control strategies. J Proteomics 73, 2267-2276 .10.1016/j.jprot.2010.08.004
[17] Bumann, D., Aksu, S., Wendland, M., Janek, K., Zimny-Arndt, U., Sabarth, N., Meyer, T.F., and Jungblut, P.R. (2002). Proteome analysis of secreted proteins of the gastric pathogen Helicobacter pylori. Infect Immun 70, 3396-3403 .10.1128/IAI.70.7.3396-3403.2002
[18] Bumann, D., Jungblut, P.R., and Meyer, T.F. (2004). Helicobacter pylori vaccine development based on combined subproteome analysis. Proteomics 4, 2843-2848 .10.1002/pmic.200400909
[19] Bunai, K., and Yamane, K. (2005). Effectiveness and limitation of two-dimensional gel electrophoresis in bacterial membrane protein proteomics and perspectives. J Chromatogr B Analyt Technol Biomed Life Sci 815, 227-236 .10.1016/j.jchromb.2004.08.030
[20] Cash, P. (2011). Investigating pathogen biology at the level of the proteome. Proteomics 11, 3190-3202 .10.1002/pmic.201100029
[21] Chevalier, F. (2010). Highlights on the capacities of “Gel-based” proteomics. Proteome Sci 8, 23.10.1186/1477-5956-8-23
[22] Chitlaru, T., Gat, O., Gozlan, Y., Ariel, N., and Shafferman, A. (2006). Differential proteomic analysis of the Bacillus anthracis secretome: distinct plasmid and chromosome CO2-dependent cross talk mechanisms modulate extracellular proteolytic activities. J Bacteriol 188, 3551-3571 .10.1128/JB.188.10.3551-3571.2006
[23] Clauser, K.R., Baker, P., and Burlingame, A.L. (1999). Role of accurate mass measurement (+/- 10 ppm) in protein identification strategies employing MS or MS/MS and database searching. Anal Chem 71, 2871-2882 .10.1021/ac9810516
[24] Coelho, A., de Oliveira Santos, E., Faria, M.L., de Carvalho, D.P., Soares, M.R., von Kruger, W.M., and Bisch, P.M. (2004). A proteome reference map for Vibrio cholerae El Tor. Proteomics 4, 1491-1504 .10.1002/pmic.200300685
[25] Coote, J.G. (2001). Environmental sensing mechanisms in Bordetella. Adv Microb Physiol 44, 141-181 .10.1016/S0065-2911(01)44013-6
[26] Coquet, L., Cosette, P., Dé, E., Galas, L., Vaudry, H., Rihouey, C., Lerouge, P., Junter, G.A., and Jouenne, T. (2005). Immobilization induces alterations in the outer membrane protein pattern of Yersinia ruckeri. J Proteome Res 4, 1988-1998 .10.1021/pr050165c
[27] Corbett, J.M., Dunn, M.J., Posch, A., and G?rg, A. (1994). Positional reproducibility of protein spots in two-dimensional polyacrylamide gel electrophoresis using immobilised pH gradient isoelectric focusing in the first dimension: an interlaboratory comparison. Electrophoresis 15, 1205-1211 .10.1002/elps.11501501182
[28] Cordwell, S.J., Larsen, M.R., Cole, R.T., and Walsh, B.J. (2002). Comparative proteomics of Staphylococcus aureus and the response of methicillin-resistant and methicillin-sensitive strains to Triton X-100. Microbiology 148, 2765-2781 .
[29] Cordwell, S.J., Nouwens, A.S., Verrills, N.M., Basseal, D.J., and Walsh, B.J. (2000). Subproteomics based upon protein cellular location and relative solubilities in conjunction with composite two-dimensional electrophoresis gels. Electrophoresis 21, 1094-1103 .10.1002/(SICI)1522-2683(20000401)21:6<1094::AID-ELPS1094>3.0.CO;2-0
[30] Cortay, J.C., Rieul, C., Duclos, B., and Cozzone, A.J. (1986). Characterization of the phosphoproteins of Escherichia coli cells by electrophoretic analysis. Eur J Biochem 159, 227-237 .10.1111/j.1432-1033.1986.tb09858.x
[31] Corthals, G.L., Wasinger, V.C., Hochstrasser, D.F., and Sanchez, J.C. (2000). The dynamic range of protein expression: a challenge for proteomic research. Electrophoresis 21, 1104-1115 .10.1002/(SICI)1522-2683(20000401)21:6<1104::AID-ELPS1104>3.0.CO;2-C
[32] de Koning-Ward, T.F., and Robins-Browne, R.M. (1997). A novel mechanism of urease regulation in Yersinia enterocolitica. FEMS Microbiol Lett 147, 221-226 .10.1016/S0378-1097(96)00528-9
[33] DebRoy, S., Dao, J., S?derberg, M., Rossier, O., and Cianciotto, N.P. (2006). Legionella pneumophila type II secretome reveals unique exoproteins and a chitinase that promotes bacterial persistence in the lung. Proc Natl Acad Sci U S A 103, 19146-19151 .10.1073/pnas.0608279103
[34] Desvaux, M., Dumas, E., Chafsey, I., Chambon, C., and Hébraud, M. (2010). Comprehensive appraisal of the extracellular proteins from a monoderm bacterium: theoretical and empirical exoproteomes of Listeria monocytogenes EGD-e by secretomics. J Proteome Res 9, 5076-5092 .10.1021/pr1003642
[35] Desvaux, M., Hébraud, M., Talon, R., and Henderson, I.R. (2009). Secretion and subcellular localizations of bacterial proteins: a semantic awareness issue. Trends Microbiol 17, 139-145 .10.1016/j.tim.2009.01.004
[36] Deutscher, J., and Saier, M.H. Jr. (2005). Ser/Thr/Tyr protein phosphorylation in bacteria- for long time neglected, now well established. J Mol Microbiol Biotechnol 9, 125-131 .10.1159/000089641
[37] Dowell, J.A., Frost, D.C., Zhang, J., and Li, L. (2008). Comparison of two-dimensional fractionation techniques for shotgun proteomics. Anal Chem 80, 6715-6723 .10.1021/ac8007994
[38] Edman, P. (1950). Method for determination of the amino acid sequence in peptides. Acta Chem Scand 4, 283-293 .10.3891/acta.chem.scand.04-0283
[39] Edman, P., and Begg, G. (1967). A protein sequenator. Eur J Biochem 1, 80-91 .10.1111/j.1432-1033.1967.tb00047.x
[40] El-Sharoud, W.M., and Rowbury, R.J. (2006). Recent insights into microbial physiology. Sci Prog 89, 141-149 .10.3184/003685006783238326
[41] Encheva, V., Gharbia, S.E., Wait, R., Begum, S., and Shah, H.N. (2006). Comparison of extraction procedures for proteome analysis of Streptococcus pneumoniae and a basic reference map. Proteomics 6, 3306-3317 .10.1002/pmic.200500744
[42] Encheva, V., Wait, R., Gharbia, S.E., Begum, S., and Shah, H.N. (2005). Proteome analysis of serovars Typhimurium and Pullorum of Salmonella enterica subspecies I. BMC Microbiol 5, 42.10.1186/1471-2180-5-42
[43] Eng, J.K., McCormack, A.L., and Yates, J.R. (1994). An approach to correlate tandem mass spectral data of peptides with amino acid sequences in a protein database. J Am Soc Mass Spectrom 5, 976-989 .10.1016/1044-0305(94)80016-2
[44] Eymann, C., Dreisbach, A., Albrecht, D., Bernhardt, J., Becher, D., Gentner, S., Tam, T., Büttner, K., Buurman, G., Scharf, C., . (2004). A comprehensive proteome map of growing Bacillus subtilis cells. Proteomics 4, 2849-2876 .10.1002/pmic.200400907
[45] Fenn, J.B., Mann, M., Meng, C.K., Wong, S.F., and Whitehouse, C.M. (1989). Electrospray ionization for mass spectrometry of large biomolecules. Science 246, 64-71 .10.1126/science.2675315
[46] Fleischmann, R.D., Adams, M.D., White, O., Clayton, R.A., Kirkness, E.F., Kerlavage, A.R., Bult, C.J., Tomb, J.F., Dougherty, B.A., Merrick, J.M., . (1995). Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269, 496-512 .10.1126/science.7542800
[47] Folio, P., Chavant, P., Chafsey, I., Belkorchia, A., Chambon, C., and Hébraud, M. (2004). Two-dimensional electrophoresis database of Listeria monocytogenes EGDe proteome and proteomic analysis of mid-log and stationary growth phase cells. Proteomics 4, 3187-3201 .10.1002/pmic.200300841
[48] Fountoulakis, M., and Gasser, R. (2003). Proteomic analysis of the cell envelope fraction of Escherichia coli. Amino Acids 24, 19-41 .
[49] Franco, A.T., Friedman, D.B., Nagy, T.A., Romero-Gallo, J., Krishna, U., Kendall, A., Israel, D.A., Tegtmeyer, N., Washington, M.K., and Peek, R.M. Jr. (2009). Delineation of a carcinogenic Helicobacter pylori proteome. Mol Cell Proteomics 8, 1947-1958 .10.1074/mcp.M900139-MCP200
[50] Gade, D., Gobom, J., and Rabus, R. (2005). Proteomic analysis of carbohydrate catabolism and regulation in the marine bacterium Rhodopirellula baltica. Proteomics 5, 3672-3683 .10.1002/pmic.200401200
[51] Gao, H., Yang, Z.K., Wu, L., Thompson, D.K., and Zhou, J. (2006). Global transcriptome analysis of the cold shock response of Shewanella oneidensis MR-1 and mutational analysis of its classical cold shock proteins. J Bacteriol 188, 4560-4569 .10.1128/JB.01908-05
[52] Gardy, J.L., and Brinkman, F.S. (2006). Methods for predicting bacterial protein subcellular localization. Nat Rev Microbiol 4, 741-751 .10.1038/nrmicro1494
[53] Garrels, J.I. (1989). The QUEST system for quantitative analysis of two-dimensional gels. J Biol Chem 264, 5269-5282 .
[54] Gatlin, C.L., Pieper, R., Huang, S.T., Mongodin, E., Gebregeorgis, E., Parmar, P.P., Clark, D.J., Alami, H., Papazisi, L., Fleischmann, R.D., . (2006). Proteomic profiling of cell envelope-associated proteins from Staphylococcus aureus. Proteomics 6, 1530-1549 .10.1002/pmic.200500253
[55] Gevaert, K., Van Damme, P., Ghesquière, B., Impens, F., Martens, L., Helsens, K., and Vandekerckhove, J. (2007). A la carte proteomics with an emphasis on gel-free techniques. Proteomics 7, 2698-2718 .10.1002/pmic.200700114
[56] G?rg, A., Obermaier, C., Boguth, G., Harder, A., Scheibe, B., Wildgruber, R., and Weiss, W. (2000). The current state of two-dimensional electrophoresis with immobilized pH gradients. Electrophoresis 21, 1037-1053 .10.1002/(SICI)1522-2683(20000401)21:6<1037::AID-ELPS1037>3.0.CO;2-V
[57] Greenough, C., Jenkins, R.E., Kitteringham, N.R., Pirmohamed, M., Park, B.K., and Pennington, S.R. (2004). A method for the rapid depletion of albumin and immunoglobulin from human plasma. Proteomics 4, 3107-3111 .10.1002/pmic.200300815
[58] Guerrera, I.C., and Kleiner, O. (2005). Application of mass spectrometry in proteomics. Biosci Rep 25, 71-93 .10.1007/s10540-005-2849-x
[59] Gupta, M.K., Subramanian, V., and Yadav, J.S. (2009). Immunoproteomic identification of secretory and subcellular protein antigens and functional evaluation of the secretome fraction of Mycobacterium immunogenum, a newly recognized species of the Mycobacterium chelonae-Mycobacterium abscessus group. J Proteome Res 8, 2319-2330 .10.1021/pr8009462
[60] Haas, G., Karaali, G., Ebermayer, K., Metzger, W.G., Lamer, S., Zimny-Arndt, U., Diescher, S., Goebel, U.B., Vogt, K., Roznowski, A.B., . (2002). Immunoproteomics of Helicobacter pylori infection and relation to gastric disease. Proteomics 2, 313-324 .10.1002/1615-9861(200203)2:3<313::AID-PROT313>3.0.CO;2-7
[61] Han, M.J., and Lee, S.Y. (2006). The Escherichia coli proteome: past, present, and future prospects. Microbiol Mol Biol Rev 70, 362-439 .10.1128/MMBR.00036-05
[62] Hecker, M., Antelmann, H., Büttner, K., and Bernhardt, J. (2008). Gel-based proteomics of Gram-positive bacteria: a powerful tool to address physiological questions. Proteomics 8 , 4958-4975 .10.1002/pmic.200800278
[63] Hecker, M., and V?lker, U. (2004). Towards a comprehensive understanding of Bacillus subtilis cell physiology by physiological proteomics. Proteomics 4 , 3727-3750 .10.1002/pmic.200401017
[64] Henderson, B., and Martin, A. (2011). Bacterial virulence in the moonlight: multitasking bacterial moonlighting proteins are virulence determinants in infectious disease. Infect Immun 79, 3476-3491 .10.1128/IAI.00179-11
[65] Henzel, W.J., Watanabe, C., and Stults, J.T. (2003). Protein identification: the origins of peptide mass fingerprinting. J Am Soc Mass Spectrom 14, 931-942 .10.1016/S1044-0305(03)00214-9
[66] Houthaeve, T., Gausepohl, H., Ashman, K., Nillson, T., and Mann, M. (1997). Automated protein preparation techniques using a digest robot. J Protein Chem 16, 343-348 .10.1023/A:1026372302560
[67] Hueck, C.J. (1998). Type III protein secretion systems in bacterial pathogens of animals and plants. Microbiol Mol Biol Rev 62, 379-433 .
[68] Ishihama, Y., Schmidt, T., Rappsilber, J., Mann, M., Hartl, F.U., Kerner, M.J., and Frishman, D. (2008). Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 9, 102.10.1186/1471-2164-9-102
[69] James, P., Quadroni, M., Carafoli, E., and Gonnet, G. (1994). Protein identification in DNA databases by peptide mass fingerprinting. Protein Sci 3, 1347-1350 .10.1002/pro.5560030822
[70] Jeffery, C.J. (2009). Moonlighting proteins—an update. Mol Biosyst 5, 345-350 .10.1039/b900658n
[71] Jongbloed, J.D., Martin, U., Antelmann, H., Hecker, M., Tjalsma, H., Venema, G., Bron, S., van Dijl, J.M., and Müller, J. (2000). TatC is a specificity determinant for protein secretion via the twin-arginine translocation pathway. J Biol Chem 275, 41350-41357 .10.1074/jbc.M004887200
[72] Jungblut, P.R. (2001). Proteome analysis of bacterial pathogens. Microbes Infect 3, 831-840 .10.1016/S1286-4579(01)01441-1
[73] Jungblut, P.R., Bumann, D., Haas, G., Zimny-Arndt, U., Holland, P., Lamer, S., Siejak, F., Aebischer, A., and Meyer, T.F. (2000). Comparative proteome analysis of Helicobacter pylori . Mol Microbiol 36, 710-725 .10.1046/j.1365-2958.2000.01896.x
[74] Kalia, A., and Gupta, R.P. (2005). Proteomics: a paradigm shift. Crit Rev Biotechnol 25, 173-198 .10.1080/07388550500365102
[75] Karas, M., and Hillenkamp, F. (1988). Laser desorption ionization of proteins with molecular masses exceeding 10,000 daltons. Anal Chem 60, 2299-2301 .10.1021/ac00171a028
[76] Klose, J. (1975). Protein mapping by combined isoelectric focusing and electrophoresis of mouse tissues. A novel approach to testing for induced point mutations in mammals. Humangenetik 26, 231-243 .
[77] Klose, J. (2009). From 2-D electrophoresis to proteomics. Electrophoresis 30, S142-S149 .10.1002/elps.200900118
[78] Konkel, M.E., and Tilly, K. (2000). Temperature-regulated expression of bacterial virulence genes. Microbes Infect 2, 157-166 .10.1016/S1286-4579(00)00272-0
[79] Lau, S.K., Fan, R.Y., Ho, T.C., Wong, G.K., Tsang, A.K., Teng, J.L., Chen, W., Watt, R.M., Curreem, S.O., Tse, H., . (2011). Environmental adaptability and stress tolerance of Laribacter hongkongensis : a genome-wide analysis. Cell Biosci 1, 22.10.1186/2045-3701-1-22
[80] Lau, S.K., Woo, P.C., Fan, R.Y., Ma, S.S., Hui, W.T., Au, S.Y., Chan, L.L., Chan, J.Y., Lau, A.T., Leung, K.Y., . (2007). Isolation of Laribacter hongkongensis, a novel bacterium associated with gastroenteritis, from drinking water reservoirs in Hong Kong. J Appl Microbiol 103, 507-515 .10.1111/j.1365-2672.2006.03263.x
[81] Lau, S.K.P., Lee, L.C.K., Fan, R.Y.Y., Teng, J.L.L., Tse, C.W.S., Woo, P.C.Y., and Yuen, K.-Y. (2009). Isolation of Laribacter hongkongensis , a novel bacterium associated with gastroenteritis, from Chinese tiger frog. Int J Food Microbiol 129, 78-82 .10.1016/j.ijfoodmicro.2008.10.021
[82] Lescuyer, P., Hochstrasser, D.F., and Sanchez, J.C. (2004). Comprehensive proteome analysis by chromatographic protein prefractionation. Electrophoresis 25, 1125-1135 .10.1002/elps.200305792
[83] Liao, X., Ying, T., Wang, H., Wang, J., Shi, Z., Feng, E., Wei, K., Wang, Y., Zhang, X., Huang, L., . (2003). A two-dimensional proteome map of Shigella flexneri. Electrophoresis 24, 2864-2882 .10.1002/elps.200305519
[84] 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 .10.1038/10890
[85] Lopez-Campistrous, A., Semchuk, P., Burke, L., Palmer-Stone, T., Brokx, S.J., Broderick, G., Bottorff, D., Bolch, S., Weiner, J.H., and Ellison, M.J. (2005). Localization, annotation, and comparison of the Escherichia coli K-12 proteome under two states of growth. Mol Cell Proteomics 4, 1205-1209 .10.1074/mcp.D500006-MCP200
[86] Macek, B., Mijakovic, I., Olsen, J.V., Gnad, F., Kumar, C., Jensen, P.R., and Mann, M. (2007). The serine/threonine/tyrosine phosphoproteome of the model bacterium Bacillus subtilis. Mol Cell Proteomics 6, 697-707 .10.1074/mcp.M600464-MCP200
[87] Marceau, M. (2005). Transcriptional regulation in Yersinia: an update. Curr Issues Mol Biol 7, 151-177 .
[88] Markert, S., Arndt, C., Felbeck, H., Becher, D., Sievert, S.M., Hügler, M., Albrecht, D., Robidart, J., Bench, S., Feldman, R.A., . (2007). Physiological proteomics of the uncultured endosymbiont of Riftia pachyptila. Science 315, 247-250 .10.1126/science.1132913
[89] Marouga, R., David, S., and Hawkins, E. (2005). The development of the DIGE system: 2D fluorescence difference gel analysis technology. Anal Bioanal Chem 382, 669-678 .10.1007/s00216-005-3126-3
[90] McHugh, L., and Arthur, J.W. (2008). Computational methods for protein identification from mass spectrometry data. PLoS Comput Biol 4, e12.10.1371/journal.pcbi.0040012
[91] Medberry, S., Gallagher, S., and Moomaw, B. (2005). Overview of digital electrophoresis analysis. Curr Protoc Protein Sci Chapter 10, Unit 10 12.
[92] Miesel, L., Greene, J., and Black, T.A. (2003). Genetic strategies for antibacterial drug discovery. Nat Rev Genet 4, 442-456 .10.1038/nrg1086
[93] Molloy, M.P., Herbert, B.R., Slade, M.B., Rabilloud, T., Nouwens, A.S., Williams, K.L., and Gooley, A.A. (2000). Proteomic analysis of the Escherichia coli outer membrane. Eur J Biochem 267, 2871-2881 .10.1046/j.1432-1327.2000.01296.x
[94] Mora, M., Donati, C., Medini, D., Covacci, A., and Rappuoli, R. (2006). Microbial genomes and vaccine design: refinements to the classical reverse vaccinology approach. Curr Opin Microbiol 9, 532-536 .10.1016/j.mib.2006.07.003
[95] Morris, H.R., Panico, M., Barber, M., Bordoli, R.S., Sedgwick, R.D., and Tyler, A. (1981). Fast atom bombardment: a new mass spectrometric method for peptide sequence analysis. Biochem Biophys Res Commun 101, 623-631 .10.1016/0006-291X(81)91304-8
[96] Ni, X.P., Ren, S.H., Sun, J.R., Xiang, H.Q., Gao, Y., Kong, Q.X., Cha, J., Pan, J.C., Yu, H., and Li, H.M. (2007). Laribacter hongkongensis isolated from a patient with community-acquired gastroenteritis in Hangzhou City. J Clin Microbiol 45, 255-256 .10.1128/JCM.01400-06
[97] Nouwens, A.S., Willcox, M.D., Walsh, B.J., and Cordwell, S.J. (2002). Proteomic comparison of membrane and extracellular proteins from invasive (PAO1) and cytotoxic (6206) strains of Pseudomonas aeruginosa. Proteomics 2, 1325-1346 .10.1002/1615-9861(200209)2:9<1325::AID-PROT1325>3.0.CO;2-4
[98] O’Connor, C.D., Farris, M., Fowler, R., and Qi, S.Y. (1997). The proteome of Salmonella enterica serovar typhimurium: current progress on its determination and some applications. Electrophoresis 18, 1483-1490 .10.1002/elps.1150180823
[99] O’Farrell, P.H. (1975). High resolution two-dimensional electrophoresis of proteins. J Biol Chem 250, 4007-4021 .
[100] Pancholi, V., and Fischetti, V.A. (1992). A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J Exp Med 176, 415-426 .10.1084/jem.176.2.415
[101] Parkhill, J., and Wren, B.W. (2011). Bacterial epidemiology and biology- lessons from genome sequencing. Genome Biol 12, 230.10.1186/gb-2011-12-10-230
[102] Patton, W.F. (2002). Detection technologies in proteome analysis. J Chromatogr B Analyt Technol Biomed Life Sci 771, 3-31 .10.1016/S1570-0232(02)00043-0
[103] Pemberton, J.M., Kidd, S.P., and Schmidt, R. (1997). Secreted enzymes of Aeromonas. FEMS Microbiol Lett 152, 1-10 .10.1111/j.1574-6968.1997.tb10401.x
[104] Perkins, D.N., Pappin, D.J.C., Creasy, D.M., and Cottrell, J.S. (1999). Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis 20, 3551-3567 .10.1002/(SICI)1522-2683(19991201)20:18<3551::AID-ELPS3551>3.0.CO;2-2
[105] Perrin, C., González-Márquez, H., Gaillard, J.L., Bracquart, P., and Guimont, C. (2000). Reference map of soluble proteins from Streptococcus thermophilus by two-dimensional electrophoresis. Electrophoresis 21, 949-955 .10.1002/(SICI)1522-2683(20000301)21:5<949::AID-ELPS949>3.0.CO;2-5
[106] Phadtare, S., Alsina, J., and Inouye, M. (1999). Cold-shock response and cold-shock proteins. Curr Opin Microbiol 2, 175-180 .10.1016/S1369-5274(99)80031-9
[107] Phillips, C.I., and Bogyo, M. (2005). Proteomics meets microbiology: technical advances in the global mapping of protein expression and function. Cell Microbiol 7 , 1061-1076 .10.1111/j.1462-5822.2005.00554.x
[108] Poetsch, A., and Wolters, D. (2008). Bacterial membrane proteomics. Proteomics 8, 4100-4122 .10.1002/pmic.200800273
[109] Poland, T., Rabilloud, T., and Sinha, P. (2005). Silver Staining of 2-D Gels. In: The Proteomics Protocols Handbook. , Walker J.M., ed. Totowa, NJ: Human Press, 177-184 .
[110] Qian, W.J., Jacobs, J.M., Liu, T., Camp, D.G. 2nd, and Smith, R.D. (2006). Advances and challenges in liquid chromatography-mass spectrometry-based proteomics profiling for clinical applications. Mol Cell Proteomics 5, 1727-1744 .10.1074/mcp.M600162-MCP200
[111] Rabilloud, T. (2009). Membrane proteins and proteomics: love is possible, but so difficult. Electrophoresis 30, S174-S180 .10.1002/elps.200900050
[112] Rabilloud, T., Chevallet, M., Luche, S., and Lelong, C. (2010). Two-dimensional gel electrophoresis in proteomics: Past, present and future. J Proteomics 73, 2064-2077 .10.1016/j.jprot.2010.05.016
[113] Rabilloud, T., Heller, M., Gasnier, F., Luche, S., Rey, C., Aebersold, R., Benahmed, M., Louisot, P., and Lunardi, J. (2002). Proteomics analysis of cellular response to oxidative stress. Evidence for in vivo overoxidation of peroxiredoxins at their active site. J Biol Chem 277, 19396-19401 .10.1074/jbc.M106585200
[114] Rabilloud, T., Vaezzadeh, A.R., Potier, N., Lelong, C., Leize-Wagner, E., and Chevallet, M. (2009). Power and limitations of electrophoretic separations in proteomics strategies. Mass Spectrom Rev 28, 816-843 .10.1002/mas.20204
[115] Rappuoli, R. (2001). Reverse vaccinology, a genome-based approach to vaccine development. Vaccine 19, 2688-2691 .10.1016/S0264-410X(00)00554-5
[116] Regula, J.T., Ueberle, B., Boguth, G., G?rg, A., Schn?lzer, M., Herrmann, R., and Frank, R. (2000). Towards a two-dimensional proteome map of Mycoplasma pneumoniae. Electrophoresis 21, 3765-3780 .10.1002/1522-2683(200011)21:17<3765::AID-ELPS3765>3.0.CO;2-6
[117] Renzone, G., D’Ambrosio, C., Arena, S., Rullo, R., Ledda, L., Ferrara, L., and Scaloni, A. (2005). Differential proteomic analysis in the study of prokaryotes stress resistance. Ann Ist Super Sanita 41, 459-468 .
[118] Roe, M.R., and Griffin, T.J. (2006). Gel-free mass spectrometry-based high throughput proteomics: tools for studying biological response of proteins and proteomes. Proteomics 6, 4678-4687 .10.1002/pmic.200500876
[119] Rosen, R., Sacher, A., Shechter, N., Becher, D., Büttner, K., Biran, D., Hecker, M., and Ron, E.Z. (2004). Two-dimensional reference map of Agrobacterium tumefaciens proteins. Proteomics 4, 1061-1073 .10.1002/pmic.200300640
[120] Rosengren, A.T., Salmi, J.M., Aittokallio, T., Westerholm, J., Lahesmaa, R., Nyman, T.A., and Nevalainen, O.S. (2003). Comparison of PDQuest and Progenesis software packages in the analysis of two-dimensional electrophoresis gels. Proteomics 3, 1936-1946 .10.1002/pmic.200300544
[121] Sabarth, N., Hurwitz, R., Meyer, T.F., and Bumann, D. (2002). Multiparameter selection of Helicobacter pylori antigens identifies two novel antigens with high protective efficacy. Infect Immun 70, 6499-6503 .10.1128/IAI.70.11.6499-6503.2002
[122] Santoni, V., Molloy, M., and Rabilloud, T. (2000). Membrane proteins and proteomics: un amour impossible? Electrophoresis 21, 1054-1070 .10.1002/(SICI)1522-2683(20000401)21:6<1054::AID-ELPS1054>3.0.CO;2-8
[123] Sarioglu, H., Lottspeich, F., Walk, T., Jung, G., and Eckerskorn, C. (2000). Deamidation as a widespread phenomenon in two-dimensional polyacrylamide gel electrophoresis of human blood plasma proteins. Electrophoresis 21, 2209-2218 .10.1002/1522-2683(20000601)21:11<2209::AID-ELPS2209>3.0.CO;2-T
[124] Scheele, G.A. (1975). Two-dimensional gel analysis of soluble proteins. Charaterization of guinea pig exocrine pancreatic proteins. J Biol Chem 250, 5375-5385 .
[125] Sibbald, M.J., Ziebandt, A.K., Engelmann, S., Hecker, M., de Jong, A., Harmsen, H.J., Raangs, G.C., Stokroos, I., Arends, J.P., Dubois, J.Y., . (2006). Mapping the pathways to staphylococcal pathogenesis by comparative secretomics. Microbiol Mol Biol Rev 70, 755-788 .10.1128/MMBR.00008-06
[126] Skurnik, M., Venho, R., Bengoechea, J.A., and Moriyón, I. (1999). The lipopolysaccharide outer core of Yersinia enterocolitica serotype O:3 is required for virulence and plays a role in outer membrane integrity. Mol Microbiol 31, 1443-1462 .10.1046/j.1365-2958.1999.01285.x
[127] Swanson, R.V., Alex, L.A., and Simon, M.I. (1994). Histidine and aspartate phosphorylation: two-component systems and the limits of homology. Trends Biochem Sci 19, 485-490 .10.1016/0968-0004(94)90135-X
[128] Teng, J.L., Woo, P.C., Ma, S.S., Sit, T.H., Ng, L.T., Hui, W.T., Lau, S.K., and Yuen, K.Y. (2005). Ecoepidemiology of Laribacter hongkongensis , a novel bacterium associated with gastroenteritis. J Clin Microbiol 43, 919-922 .10.1128/JCM.43.2.919-922.2005
[129] Thein, M., Sauer, G., Paramasivam, N., Grin, I., and Linke, D. (2010). Efficient subfractionation of gram-negative bacteria for proteomics studies. J Proteome Res 9, 6135-6147 .10.1021/pr1002438
[130] Thieringer, H.A., Jones, P.G., and Inouye, M. (1998). Cold shock and adaptation. Bioessays 20, 49-57 .10.1002/(SICI)1521-1878(199801)20:1<49::AID-BIES8>3.0.CO;2-N
[131] Tjalsma, H., Antelmann, H., Jongbloed, J.D., Braun, P.G., Darmon, E., Dorenbos, R., Dubois, J.Y., Westers, H., Zanen, G., Quax, W.J., . (2004). Proteomics of protein secretion by Bacillus subtilis : separating the “secrets” of the secretome. Microbiol Mol Biol Rev 68, 207-233 .10.1128/MMBR.68.2.207-233.2004
[132] Traini, M., Gooley, A.A., Ou, K., Wilkins, M.R., Tonella, L., Sanchez, J.C., Hochstrasser, D.F., and Williams, K.L. (1998). Towards an automated approach for protein identification in proteome projects. Electrophoresis 19, 1941-1949 .10.1002/elps.1150191112
[133] Trost, M., Wehmh?ner, D., K?rst, U., Dieterich, G., Wehland, J., and J?nsch, L. (2005). Comparative proteome analysis of secretory proteins from pathogenic and nonpathogenic Listeria species. Proteomics 5, 1544-1557 .10.1002/pmic.200401024
[134] Trülzsch, K., Roggenkamp, A., Aepfelbacher, M., Wilharm, G., Ruckdeschel, K., and Heesemann, J. (2003). Analysis of chaperone-dependent Yop secretion/translocation and effector function using a mini-virulence plasmid of Yersinia enterocolitica. Int J Med Microbiol 293, 167-177 .10.1078/1438-4221-00251
[135] Unlü, M., Morgan, M.E., and Minden, J.S. (1997). Difference gel electrophoresis: a single gel method for detecting changes in protein extracts. Electrophoresis 18, 2071-2077 .10.1002/elps.1150181133
[136] V?lker, U., and Hecker, M. (2005). From genomics via proteomics to cellular physiology of the Gram-positive model organism Bacillus subtilis. Cell Microbiol 7, 1077-1085 .10.1111/j.1462-5822.2005.00555.x
[137] Wang, J., Ying, T., Wang, H., Shi, Z., Li, M., He, K., Feng, E., Wang, J., Yuan, J., Li, T., . (2005). 2-D reference map of Bacillus anthracis accine strain A16R proteins. Proteomics 5, 4488-4495 .10.1002/pmic.200401322
[138] Wang, Y., Xu, A., Knight, C., Xu, L.Y., and Cooper, G.J. (2002). Hydroxylation and glycosylation of the four conserved lysine residues in the collagenous domain of adiponectin. Potential role in the modulation of its insulin-sensitizing activity. J Biol Chem 277, 19521-19529 .10.1074/jbc.M200601200
[139] Washburn, M.P., Wolters, D., and Yates, J.R. 3rd. (2001). Large-scale analysis of the yeast proteome by multidimensional protein identification technology. Nat Biotechnol 19, 242-247 .10.1038/85686
[140] Wilkins, M.R., Gasteiger, E., Sanchez, J.C., Bairoch, A., and Hochstrasser, D.F. (1998). Two-dimensional gel electrophoresis for proteome projects: the effects of protein hydrophobicity and copy number. Electrophoresis 19, 1501-1505 .10.1002/elps.1150190847
[141] Wilkins, M.R., Pasquali, C., Appel, R.D., Ou, K., Golaz, O., Sanchez, J.C., Yan, J.X., Gooley, A.A., Hughes, G., Humphery-Smith, I., . (1996). From proteins to proteomes: large scale protein identification by two-dimensional electrophoresis and amino acid analysis. Biotechnology (N Y) 14, 61-65 .10.1038/nbt0196-61
[142] Woo, P.C., Lau, S.K., Teng, J.L., Que, T.L., Yung, R.W., Luk, W.K., Lai, R.W., Hui, W.T., Wong, S.S., Yau, H.H., , and the L Hongkongensis study group. (2004). Association of Laribacter hongkongensis in community-acquired gastroenteritis with travel and eating fish: a multicentre case-control study. Lancet 363, 1941-1947 .10.1016/S0140-6736(04)16407-6
[143] Woo, P.C., Lau, S.K., Teng, J.L., and Yuen, K.Y. (2005). Current status and future directions for Laribacter hongkongensis, a novel bacterium associated with gastroenteritis and traveller’s diarrhoea. Curr Opin Infect Dis 18, 413-419 .10.1097/01.qco.0000180162.76648.c9
[144] Woo, P.C., Lau, S.K., Tse, H., Teng, J.L., Curreem, S.O., Tsang, A.K., Fan, R.Y., Wong, G.K., Huang, Y., Loman, N.J., . (2009). The complete genome and proteome of Laribacter hongkongensis reveal potential mechanisms for adaptations to different temperatures and habitats. PLoS Genet 5, e1000416.10.1371/journal.pgen.1000416
[145] Yan, J.X., Devenish, A.T., Wait, R., Stone, T., Lewis, S., and Fowler, S. (2002). Fluorescence two-dimensional difference gel electrophoresis and mass spectrometry based proteomic analysis of Escherichia coli. Proteomics 2, 1682-1698 .10.1002/1615-9861(200212)2:12<1682::AID-PROT1682>3.0.CO;2-Y
[146] Yates, J.R. 3rd, Speicher, S., Griffin, P.R., and Hunkapiller, T. (1993). Peptide mass maps: a highly informative approach to protein identification. Anal Biochem 214, 397-408 .10.1006/abio.1993.1514
[147] Yu, H.B., Kaur, R., Lim, S., Wang, X.H., and Leung, K.Y. (2007). Characterization of extracellular proteins produced by Aeromonas hydrophila AH-1. Proteomics 7, 436-449 .10.1002/pmic.200600396
[148] Yuen, K.Y., Woo, P.C., Teng, J.L., Leung, K.W., Wong, M.K., and Lau, S.K. (2001). Laribacter hongkongensis gen. nov., sp. nov., a novel gram-negative bacterium isolated from a cirrhotic patient with bacteremia and empyema. J Clin Microbiol 39, 4227-4232 .10.1128/JCM.39.12.4227-4232.2001
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