Improved enrichment and proteomic identification of outer membrane proteins from a Gram-negative bacterium: Focus on Caulobacter crescentus

Proteomics

Volumn 12, Issue 2, 2012, Pages 251-262

  Cao, Yuan ^a   Johnson, Helen M ^a   Bazemore Walker, Carthene R ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

Caulobacter crescentus; Method development; Microbiology; Outer membrane proteins; Proteomic analysis; Sample preparation

Indexed keywords

BACTERIAL PROTEIN; BAMA PROTEIN; DODECYL SARCOSINATE SODIUM; FLAGELLIN; FLAGELLIN FLJK; FLAGELLIN FLJL; FLAGELLIN FLJM; FLAGELLIN FLJN; FLBG PROTEIN; FLGD PROTEIN; FLGG PROTEIN; FLGI PROTEIN; HFAB PROTEIN; LIPOPROTEIN; LIPOPROTEIN BAMB; LIPOPROTEIN PAL; OUTER MEMBRANE PROTEIN; PROTEIN HFSA; PROTEIN HFSD; REAGENT; SODIUM CARBONATE; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; CAULOBACTER CRESCENTUS; CELLULAR DISTRIBUTION; EXTRACELLULAR SPACE; GEL ASSISTED DIGESTION; INTERMETHOD COMPARISON; LIQUID CHROMATOGRAPHY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROCESS OPTIMIZATION; PROTEIN LOCALIZATION; PROTEOMICS; TANDEM MASS SPECTROMETRY; WILD TYPE;

BACTERIAL OUTER MEMBRANE PROTEINS; BLOTTING, WESTERN; CARBONATES; CAULOBACTER CRESCENTUS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; COMPUTATIONAL BIOLOGY; DETERGENTS; ELECTROPHORESIS, POLYACRYLAMIDE GEL; MASS SPECTROMETRY; PROTEOME; PROTEOMICS; SARCOSINE; SENSITIVITY AND SPECIFICITY; SOLUBILITY;

BACTERIA (MICROORGANISMS); CAULOBACTER VIBRIOIDES; NEGIBACTERIA;

EID: 84855935515     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.201100288     Document Type: Article

References (81)

1. Silhavy, T. J., Kahne, D., Walker, S., The bacterial cell envelope. Cold Spring Harb. Perspect. Biol. 2010, 2, a000414.
2. Nikaido, H., Molecular basis of bacterial outer membrane permeability revisited. Microbiol. Mol. Biol. Rev. 2003, 67, 593-656.
3. Ryan, K. R., Taylor, J. A., Bowers, L. M., The BAM complex subunit BamE (SmpA) is required for membrane integrity, stalk growth and normal levels of outer membrane beta-barrel proteins in Caulobacter crescentus. Microbiology - (UK) 2010, 156, 742-756.
4. Lewis, C., Skovierova, H., Rowley, G., Rezuchova, B. et al., Small outer-membrane lipoprotein, SmpA, is regulated by sigmaE and has a role in cell envelope integrity and virulence of Salmonella enterica serovar Typhimurium. Microbiology 2008, 154, 979-988.
5. Fardini, Y., Trotereau, J., Bottreau, E., Souchard, C. et al., Investigation of the role of the BAM complex and SurA chaperone in outer-membrane protein biogenesis and type III secretion system expression in Salmonella. Microbiology - (UK) 2009, 155, 1613-1622.
6. Ruiz, N., Silhavy, T. J., Sensing external stress: watchdogs of the Escherichia coli cell envelope. Curr. Opin. Microbiol. 2005, 8, 122-126.
7. Pizza, M., Scarlato, V., Masignani, V., Giuliani, M. M. et al., Identification of vaccine candidates against serogroup B meningococcus by whole-genome sequencing. Science 2000, 287, 1816-1820.
8. Durand, E., Verger, D., Rego, A. T., Chandran, V. et al., Structural biology of bacterial secretion systems in gram-negative pathogens - potential for new drug targets. Infect. Disord. Drug Targets 2009, 9, 518-547.
9. Santoni, V., Molloy, M., Rabilloud, T., Membrane proteins and proteomics: un amour impossible? Electrophoresis 2000, 21, 1054-1070.
10. Thein, M., Sauer, G., Paramasivam, N., Grin, I., Linke, D., Efficient subfractionation of gram-negative bacteria for proteomics studies. J. Proteome Res. 2010, 9, 6135-6147.
11. Huang, F., Hedman, E., Funk, C., Kieselbach, T. et al., Isolation of outer membrane of Synechocystis sp PCC 6803 and its proteomic characterization. Mol. Cell. Proteomics 2004, 3, 586-595.
12. Chung, J. W., Ng-Thow-Hing, C., Budman, L. I., Gibbs, B. F. et al., Outer membrane proteome of Actinobacillus pleuropneumoniae: LC-MS/MS analyses validate in silico predictions. Proteomics 2007, 7, 1854-1865.
13. Phadke, N. D., Molloy, M. P., Steinhoff, S. A., Ulintz, P. J. et al., Analysis of the outer membrane proteome of Caulobacter crescentus by two-dimensional electrophoresis and mass spectrometry. Proteomics 2001, 1, 705-720.
14. Schluesener, D., Fischer, F., Kruip, J., Rogner, M., Poetsch, A., Mapping the membrane proteome of Corynebacterium glutamicum. Proteomics 2005, 5, 1317-1330.
15. Dehio, C., Rhomberg, T. A., Karlberg, O., Mini, T. et al., Proteomic analysis of the sarcosine-insoluble outer membrane fraction of the bacterial pathogen Bartonella henselae. Proteomics 2004, 4, 3021-3033.
16. Boyce, J. D., Cullen, P. A., Nguyen, V., Wilkie, I., Adler, B., Analysis of the Pasteurella multocida outer membrane sub-proteome and its response to the in vivo environment of the natural host. Proteomics 2006, 6, 870-880.
17. Horn, M., Heinz, E., Pichler, P., Heinz, C. et al., Proteomic analysis of the outer membrane of Protochlamydia amoebophila elementary bodies. Proteomics 2010, 10, 4363-4376.
18. Miura, T., Mizushima, S., Separation by density gradient centrifugation of two types of membranes from spheroplast membrane of Escherichia coli K12. Biochim. Biophys. Acta 1968, 150, 159-161.
19. Peng, X. X., Zhang, D. F., Li, H., Lin, X. M., Wang, S. Y., Characterization of outer membrane proteins of Escherichia coli in response to phenol stress. Curr. Microbiol. 2011, 62, 777-783.
20. Vashist, J., Tiwari, V., Kapil, A., Rajeswari, M. R., Quantitative profiling and identification of outer membrane proteins of beta-lactam resistant strain of Acinetobacter baumannii. J. Proteome Res. 2010, 9, 1121-1128.
21. Ayalew, S., Confer, A. W., Hartson, S. D., Shrestha, B., Immunoproteomic analyses of outer membrane proteins of Mannheimia haemolytica and identification of potential vaccine candidates. Proteomics 2010, 10, 2151-2164.
22. Rathore, G., Kumar, G., Sharma, P., Bisht, D., Sengupta, U., Proteomic analysis of outer membrane proteins of Edwardsiella tarda. J. Appl. Microbiol. 2010, 108, 2214-2221.
23. Shen, C. J., Kuo, T. Y., Lin, C. C., Chow, L. P., Chen, W. J., Proteomic identification of membrane proteins regulating antimicrobial peptide resistance in Vibrio parahaemolyticus. J. Appl. Microbiol. 2010, 108, 1398-1407.
24. Veith, P. D., O'Brien-Simpson, N. M., Tan, Y., Djatmiko, D. C. et al., Outer membrane proteome and antigens of Tannerella forsythia. J. Proteome Res. 2009, 8, 4279-4292.
25. Smither, S. J., Hill, J., van Baar, B. L. M., Hulst, A. G. et al., Identification of outer membrane proteins of Yersinia pestis through biotinylation. J. Microbiol. Methods 2007, 68, 26-31.
26. Baik, S. C., Kim, K. M., Song, S. M., Kim, D. S. et al., Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Helicobacter pylori strain 26695. J. Bacteriol. 2004, 186, 949-955.
27. Molloy, M. P., Herbert, B. R., Slade, M. B., Rabilloud, T. et al., Proteomic analysis of the Escherichia coli outer membrane. Eur. J. Biochem. 2000, 267, 2871-2881.
28. Carlsohn, E., Nystrom, J., Karlsson, H., Svennerholm, A. M., Nilsson, C. L., Characterization of the outer membrane protein profile from disease-related Helicobacter pylori isolates by subcellular fractionation and nano-LCFT-ICR MS analysis. J. Proteome Res. 2006, 5, 3197-3204.
29. Heckels, J. E., Williams, J. N., Skipp, P. J., Humphries, H. E. et al., Proteomic analysis of outer membranes and vesicles from wild-type serogroup B Neisseria meningitidis and a lipopolysaccharide-deficient mutant. Infect. Immun. 2007, 75, 1364-1372.
30. Nie, P., Liu, G. Y., Zhang, J., Li, N., Proteomic analysis of the sarcosine-insoluble outer membrane fraction of Flavobacterium columnare. J. Fish Dis. 2008, 31, 269-276.
31. Brown, S. D., Thompson, M. R., VerBerkmoes, N. C., Chourey, K. et al., Molecular dynamics of the Shewanella oneidensis response to chromate stress. Mol. Cell. Proteomics 2006, 5, 1054-1071.
32. Brown, R. N., Romine, M. F., Schepmoes, A. A., Smith, R. D., Lipton, M. S., Mapping the subcellular proteome of Shewanella oneidensis MR-1 using sarkosyl-based fractionation and LC-MS/MS protein identification. J. Proteome Res. 2010, 9, 4454-4463.
33. Liu, X. Y., Afrane, M., Clemmer, D. E., Zhong, G. M., Nelson, D. E., Identification of Chlamydia trachomatis outer membrane complex proteins by differential proteomics. J. Bacteriol. 2010, 192, 2852-2860.
34. Mobley, H. L. T., Walters, M. S., Identification of uropathogenic Escherichia coli surface proteins by shotgun proteomics. J. Microbiol. Methods 2009, 78, 131-135.
35. Kustos, I., Andrasfalvy, M., Kustos, T., Kocsis, B., Kilar, F., Effect of iron restriction on outer membrane protein composition of Pseudomonas strains studied by conventional and microchip electrophoresis. Electrophoresis 2005, 26, 3789-3795.
36. England, J. C., Gober, J. W., Cell cycle control of cell morphogenesis in Caulobacter. Curr. Opin. Microbiol. 2001, 4, 674-680.
37. Ireland, M. M. E., Karty, J. A., Quardokus, E. M., Reilly, J. P., Brun, Y. V., Proteomic analysis of the Caulobacter crescentus stalk indicates competence for nutrient uptake. Mol. Microbiol. 2002, 45, 1029-1041.
38. Nierman, W. C., Feldblyum, T. V., Laub, M. T., Paulsen, I. T. et al., Complete genome sequence of Caulobacter crescentus. Proc. Natl. Acad. USA 2001, 98, 4136-4141.
39. Han, C. L., Chien, C. W., Chen, W. C., Chen, Y. R. et al., A Multiplexed quantitative strategy for membrane proteomics opportunities for mining therapeutic targets for autosomal dominant polycystic kidney disease. Mol. Cell. Proteomics 2008, 7, 1983-1997.
40. Lu, X. N., Zhu, H. N., Tube-gel digestion - a novel proteomic approach for high throughput analysis of membrane proteins. Mol. Cell. Proteomics 2005, 4, 1948-1958.
41. Poindexter, J. S., Biological properties and classification of the caulobacter group. Bacteriol. Rev. 1964, 28, 231-295.
42. Hardy, G. G., Allen, R. C., Toh, E., Long, M. et al., A localized multimeric anchor attaches the Caulobacter holdfast to the cell pole. Mol. Microbiol. 2010, 76, 409-427.
43. Yan, J. X., Wait, R., Berkelman, T., Harry, R. A. et al., A modified silver staining protocol for visualization of proteins compatible with matrix-assisted laser desorption/ionization and electrospray ionization-mass spectrometry. Electrophoresis 2000, 21, 3666-3672.
44. Westermeier, R., Sensitive, quantitative, and fast modifications for Coomassie Blue Staining of polyacrylamide gels. Proteomics 2006, 61-64.
45. Katayama, H., Nagasu, T., Oda, Y., Improvement of in-gel digestion protocol for peptide mass fingerprinting by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun. Mass Spectrom. 2001, 15, 1416-1421.
46. Shilov, I. V., Seymour, S. L., Patel, A. A., Loboda, A. et al., The paragon algorithm, a next generation search engine that uses sequence temperature values and feature probabilities to identify peptides from tandem mass spectra. Mol. Cell. Proteomics 2007, 6, 1638-1655.
47. Elias, J. E., Gygi, S. P., Target-decoy search strategy for mass spectrometry-based proteomics. Methods Mol. Biol. 2010, 604, 55-71.
48. Deutsch, E. W., Mendoza, L., Shteynberg, D., Farrah, T. et al., A guided tour of the Trans-Proteomic Pipeline. Proteomics 2010, 10, 1150-1159.
49. Szafron, D., Lu, P., Greiner, R., Wishart, D. S. et al., Proteome Analyst: custom predictions with explanations in a web-based tool for high-throughput proteome annotations. Nucleic Acids Res. 2004, 32, W365-W371.
50. 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.
51. Fujiki, Y., Hubbard, A. L., Fowler, S., Lazarow, P. B., Isolation of intracellular membranes by means of sodium-carbonate treatment - application to endoplasmic-reticulum. J. Cell Biol. 1982, 93, 97-102.
52. Filip, C., Fletcher, G., Wulff, J. L., Earhart, C. F., Solubilization of cytoplasmic membrane of Escherichia coli by ionic detergent sodium-lauryl sarcosinate. J. Bacteriol. 1973, 115, 717-722.
53. Ong, C. J., Wong, M. L. Y., Smit, J., Attachment of the adhesive holdfast organelle to the cellular stalk of caulobacter-crescentus. J. Bacteriol. 1990, 172, 1448-1456.
54. Merker, R. I., Smit, J., Characterization of the adhesive holdfast of marine and fresh-water caulobacters. Appl. Environ. Microb. 1988, 54, 2078-2085.
55. Li, L. J., Dowell, J. A., Frost, D. C., Zhang, J., Comparison of two-dimensional fractionation techniques for shotgun proteomics. Anal. Chem. 2008, 80, 6715-6723.
56. Fernandez, L. A., Berenguer, J., Secretion and assembly of regular surface structures in Gram-negative bacteria. Fems Microbiol. Rev. 2000, 24, 21-44.
57. Sleytr, U. B., Messner, P., Pum, D., Sara, M., Crystalline bacterial cell surface layers. Mol. Microbiol. 1993, 10, 911-916.
58. Awram, P., Smit, J., The Caulobacter crescentus paracrystalline S-layer protein is secreted by an ABC transporter (type I) secretion apparatus. J. Bacteriol. 1998, 180, 3062-3069.
59. Lau, J. H., Nomellini, J. F., Smit, J., Analysis of high-level S-layer protein secretion in Caulobacter crescentus. Can. J. Microbiol. 2010, 56, 501-514.
60. Diaz-Mejia, J. J., Babu, M., Emili, A., Computational and experimental approaches to chart the Escherichia coli cell-envelope-associated proteome and interactome. Fems Microbiol. Rev. 2009, 33, 66-97.
61. Anwari, K., Poggio, S., Perry, A., Gatsos, X. et al., A modular BAM complex in the outer membrane of the alpha-proteobacterium Caulobacter crescentus. PLoS One 2010, 5, e8619.
62. Smith, C. S., Hinz, A., Bodenmiller, D., Larson, D. E., Brun, Y. V., Identification of genes required for synthesis of the adhesive holdfast in Caulobacter crescentus. J. Bacteriol. 2003, 185, 1432-1442.
63. Cole, J. L., Hardy, G. G., Bodenmiller, D., Toh, E. et al., The HfaB and HfaD adhesion proteins of Caulobacter crescentus are localized in the stalk. Mol. Microbiol. 2003, 49, 1671-1683.
64. Brown, P. J. B., Hardy, G. G., Trimble, M. J., Brun, Y. V., Complex regulatory pathways coordinate cell-cycle progression and development in Caulobacter crescentus. Adv. Microb. Physiol. 2009, 54, 1-101.
65. Drummelsmith, J., Whitfield, C., Translocation of group 1 capsular polysaccharide to the surface of Escherichia coli requires a multimeric complex in the outer membrane. Embo J. 2000, 19, 57-66.
66. Schnaitman, C. A., Effect of ethylenediaminetetraacetic acid, Triton X-100, and lysozyme on the morphology and chemical composition of isolate cell walls of Escherichia coli. J. Bacteriol. 1971, 108, 553-563.
67. Tsuyumu, S., Babujee, L., Venkatesh, B., Yamazaki, A., Proteomic analysis of the carbonate insoluble outer membrane fraction of the soft-rot pathogen Dickeya dadantii (syn. Erwinia chrysanthemi) strain 3937. J. Proteome Res. 2007, 6, 62-69.
68. Koebnik, R., Locher, K. P., Van Gelder, P., Structure and function of bacterial outer membrane proteins: Barrels in a nutshell. Mol. Microbiol. 2000, 37, 239-253.
69. 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.
70. Yu, J. S., Wu, C. C., Hsu, C. W., Chen, C. D. et al., Candidate serological biomarkers for cancer identified from the secretomes of 23 cancer cell lines and the human protein atlas. Mol. Cell. Proteomics 2010, 9, 1100-1117.
71. Pandey, A., Marimuthu, A., O'Meally, R. N., Chaerkady, R. et al., A comprehensive map of the human urinary proteome. J. Proteome Res. 2011, 10, 2734-2743.
72. Fakler, B., Muller, C. S., Haupt, A., Bildl, W. et al., Quantitative proteomics of the Cav2 channel nano-environments in the mammalian brain. Proc. Natl. Acad. Sci. USA 2010, 107, 14950-14957.
73. Brun, Y. V., Wortinger, M. A., Quardokus, E. M., Morphological adaptation and inhibition of cell division during stationary phase in Caulobacter crescentus. Mol. Microbiol. 1998, 29, 963-973.
74. Crosson, S., Boutte, C. C., The complex logic of stringent response regulation in Caulobacter crescentus: starvation signalling in an oligotrophic environment. Mol. Microbiol. 2011, 80, 695-714.
75. Le Blastier, S., Hamels, A., Cabeen, M., Schille, L. et al., Phosphate starvation triggers production and secretion of an extracellular lipoprotein in Caulobacter crescentus. PLoS One 2010, 5, e14198.
76. Gober, J. W., England, J. C., Perchuk, B. S., Laub, M. T., Global regulation of gene expression and cell differentiation in Caulobacter crescentus in response to nutrient availability. J. Bacteriol. 2010, 192, 819-833.
77. Yoon, S. H., Han, M. J., Lee, S. Y., Jeong, K. J., Yoo, J. S., Combined transcriptome and proteome analysis of Escherichia coli during high cell density culture. Biotechnol. Bioeng. 2003, 81, 753-767.
78. Hancock, W. S., Wang, Y. H., Wu, S. L., Trala, R. et al., Proteomic profiling of Escherichia coli proteins under high cell density fed-batch cultivation with overexpression of phosphogluconolactonase. Biotechnol. Progr. 2005, 21, 1401-1411.
79. Lee, S. Y., Xia, X. X., Han, M. J., 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.
80. Lehtio, J., Pernemalm, M., Lewensohn, R., Affinity prefractionation for MS-based plasma proteomics. Proteomics 2009, 9, 1420-1427.
81. Walker, S. G., Smith, S. H., Smit, J., Isolation and comparison of the paracrystalline surface-layer proteins of fresh-water caulobacters. J. Bacteriol. 1992, 174, 1783-1792.