Characterisation of proteins extracted from the surface of Salmonella Typhimurium grown under SPI-2-inducing conditions by LC-ESI/MS/MS sequencing

Proteomics

Volumn 11, Issue 3, 2011, Pages 361-370

  Sherry, Aileen E ^a   Inglis, Neil F ^b   Stevenson, Andy ^a   Fraser Pitt, Douglas ^b   Everest, Paul ^a   Smith, David G E ^a,b   Roberts, Mark ^a  

^a UNIVERSITY OF GLASGOW   (United Kingdom)

^b MOREDUN RESEARCH INSTITUTE   (United Kingdom)

Author keywords

Microbiology; Salmonella; SPI 1; SPI 2; Surface attached fraction; Type three secretion system

Indexed keywords

BACTERIAL PROTEIN; OUTER MEMBRANE PROTEIN; PROTEIN PIPB2; PROTEIN SIPA; PROTEIN SIPB; PROTEIN SIPC; PROTEIN SIPD; PROTEIN SLRP; PROTEIN SOPD; PROTEIN SSEB; PROTEIN SSEC; PROTEIN SSED; PROTEIN SSEL; PROTEIN STEA; PROTEIN STEC; PROTEOME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BACTERIAL OUTER MEMBRANE; CELL VACUOLE; CONTROLLED STUDY; ELECTROSPRAY MASS SPECTROMETRY; EXTRACTION; GENE FUSION; HIGH THROUGHPUT SCREENING; IMMUNOBLOTTING; IN VITRO STUDY; LIQUID CHROMATOGRAPHY; NONHUMAN; PATHOGENESIS; PATHOGENICITY ISLAND; PATHOGENICITY ISLAND 1; PATHOGENICITY ISLAND 2; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN SECRETION; SALMONELLA TYPHIMURIUM; SEQUENCE ANALYSIS; SEROTYPE; SIGNAL TRANSDUCTION;

BACTERIAL PROTEINS; BLOTTING, WESTERN; CHROMATOGRAPHY, LIQUID; MEMBRANE PROTEINS; SALMONELLA INFECTIONS; SALMONELLA TYPHIMURIUM; SIGNAL TRANSDUCTION; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

SALMONELLA; SALMONELLA ENTERICA; SALMONELLA TYPHIMURIUM;

EID: 79251501004     PISSN: 16159853     EISSN: 16159861     Source Type: Journal    
DOI: 10.1002/pmic.200900802     Document Type: Article

References (51)

1. Brumell, J. H., Finlay, B. B., Bacterial adherence, colonization and invasion of mucosal surfaces. In: Brogden, K., Roth, J., Stanton, T., Bolin, C., Minion, F., Wannemuehler, M. (Eds), Virulence Mechanisms of Bacterial Pathogens, ASM Press, Washington 2000, pp. 3-17.
2. Blocker, A., Komoriya, K., Aizawa, S., Type III secretion systems and bacterial flagella: insights into their function from structural similarities. Proc. Natl. Acad. Sci. USA 2003, 100, 3027-3030.
3. Baumler, A. J. The record of horizontal gene transfer in Salmonella. Trends Microbiol. 1997, 5, 318-322.
4. Zhou, D., Galan, J., Salmonella entry into host cells: the work in concert of type III secreted effector proteins. Microbes Infect. 2001, 3, 1293-1298.
5. Waterman, S. R., Holden, D. W., Functions and effectors of the Salmonella pathogenicity island 2 type III secretion system. Cell Microbiol. 2003, 5, 501-511.
6. Haraga, A., Miller, S. I., A Salmonella enterica serovar typhimurium translocated leucine-rich repeat effector protein inhibits NF-kappa B-dependent gene expression. Infect. Immun. 2003, 7, 4052-4058.
7. Gerlach, R. G., Jackel, D., Stecher, B., Wagner, C. et al., Salmonella pathogenicity island 4 encodes a giant non-fimbrial adhesin and the cognate type 1 secretion system. Cell Microbiol. 2007, 9, 1834-1850.
8. Dorsey, C. W., Laarakker, M. C., Humphries, A. D., Weening, E. H., Baumler, A. J., Salmonella enterica serotype Typhimurium MisL is an intestinal colonization factor that binds fibronectin. Mol. Microbiol. 2005, 57, 196-211.
9. Kingsley, R. A., Santos, R. L., Keestra, A. M., Adams, L. G., Baumler, A. J., Salmonella enterica serotype Typhimurium ShdA is an outer membrane fibronectin-binding protein that is expressed in the intestine. Mol. Microbiol. 2002, 43, 895-905.
10. Lee, C. A., Falkow, S., The ability of Salmonella to enter mammalian cells is affected by bacterial growth state. Proc. Natl. Acad. Sci. USA 1990, 87, 4304-4308.
11. Deiwick, J., Nikolaus, T., Shea, J. E., Gleeson, C. et al., Mutations in Salmonella pathogenicity island 2 (SPI2) genes affecting transcription of SPI1 genes and resistance to antimicrobial agents. J. Bacteriol. 1998, 180, 4775-4780.
12. Beuzon, C. R., Banks, G., Deiwick, J., Hensel, M., Holden, D. W., pH-dependent secretion of SseB, a product of the SPI-2 type III secretion system of Salmonella typhimurium. Mol. Microbiol. 1999, 33, 806-816.
13. Sorg I, Cornelis G., The type III secretion system. In: Wooldridge, K. (Ed.), Bacterial Secreted Proteins: Secretory Mechanisms and Role in Pathogenesis, Caister Academic Press, Norfolk 2009, pp. 93-116.
14. Nikolaus, T., Deiwick, J., Rappl, C., Freeman, J. A., Schroder, W. et al. SseBCD proteins are secreted by the type III secretion system of Salmonella pathogenicity island 2 and function as a translocon. J. Bacteriol. 2001, 183, 6036-6045.
15. Miller, J. H., Experiments in Molecular Genetics, Cold Spring Harbor Laboratory Press, New York 1972.
16. Michiels, T., Wattiau, P., Brasseur, R., Ruysschaert, J. M., Cornelis, G., Secretion of Yop proteins by Yersiniae. Infect. Immun. 1990, 58, 2840-2849.
17. Hautefort, I., Proenca, M. J., Hinton, J. C., Single-copy green fluorescent protein gene fusions allow accurate measurement of Salmonella gene expression in vitro and during infection of mammalian cells. Appl Environ. Microbiol. 2003, 69, 7480-7491.
18. Shevchenko, A., Wilm, M., Vorm, O., Mann, M., Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Anal. Chem. 1996, 68, 850-858.
19. Batycka, M., Inglis, N. F., Cook, K., Adam, A. et al., Ultra-fast tandem mass spectrometry scanning combined with monolithic column liquid chromatography increases throughput in proteomic analysis. Rapid Commun. Mass Spectrom. 2006, 20, 2074-2080.
20. Taylor, G. K., Goodlett, D. R., Rules governing protein identification by mass spectrometry. Rapid Commun. Mass Spectrom. 2005, 19, 3420.
21. Coombes, B. K., Brown, N. F., Valdez, Y., Brumell, J. H., Finlay, B. B., Expression and secretion of Salmonella pathogenicity island-2 virulence genes in response to acidification exhibit differential requirements of a functional type III secretion apparatus and SsaL. J. Biol. Chem. 2004, 279, 49804-49815.
22. Yu, X. J., Liu, M., Holden, D. W., SsaM and SpiC interact and regulate secretion of Salmonella pathogenicity island 2 type III secretion system effectors and translocators. Mol. Microbiol. 2004, 54, 604-619.
23. Eriksson, S., Lucchini, S., Thompson, A., Rhen, M., Hinton, J. C., Unravelling the biology of macrophage infection by gene expression profiling of intracellular Salmonella enterica. Mol. Microbiol. 2003, 47, 103-118.
24. Haraga, A., Ohlson, M. B., Miller, S. I., Salmonellae interplay with host cells. Nat. Rev. Microbiol. 2008, 6, 53-66.
25. Bustamante, V. H., Martinez, L. C., Santana, F. J., Knodler, L. A. et al., HilD-mediated transcriptional cross-talk between SPI-1 and SPI-2. Proc. Natl. Acad. Sci. USA 2008, 105, 14591-14596.
26. Giacomodonato, M. N., Uzzau, S., Bacciu, D., Caccuri, R. et al., SipA, SopA, SopB, SopD and SopE2 effector proteins of Salmonella enterica serovar Typhimurium are synthesized at late stages of infection in mice. Microbiology 2007, 153, 1221-1228.
27. Lawley, T. D., Chan, K., Thompson, L. J., Kim, C. C. et al., Genome-wide screen for Salmonella genes required for long-term systemic infection of the mouse. PLoS Pathog. 2006, 2, e11.
28. Drecktrah, D., Knodler, L. A., Galbraith, K., Steele-Mortimer, O., The Salmonella SPI1 effector SopB stimulates nitric oxide production long after invasion. Cell Microbiol. 2005, 7, 1105-1113.
29. Steele-Mortimer, O., Brumell, J. H., Knodler, L. A., Meresse, S. et al., The invasion-associated type III secretion system of Salmonella enterica serovar Typhimurium is necessary for intracellular proliferation and vacuole biogenesis in epithelial cells. Cell Microbiol. 2002, 4, 43-54.
30. Brawn, L. C., Hayward, R. D., Koronakis, V., Salmonella SPI1 effector SipA persists after entry and cooperates with a SPI2 effector to regulate phagosome maturation and intracellular replication. Cell Host Microbe 2007, 1, 63-75.
31. Brown, N. F., Vallance, B. A., Coombes, B. K., Valdez, Y. et al., Salmonella pathogenicity island 2 is expressed prior to penetrating the intestine. PLoS Pathog. 2005, 1, e32.
32. Hensel, M., Shea, J. E., Raupach, B., Monack, D. et al., Functional analysis of ssaJ and the ssaK/U operon, 13 genes encoding components of the type III secretion apparatus of Salmonella Pathogenicity Island 2. Mol. Microbiol. 1997, 24, 155-167.
33. Rollenhagen, C., Bumann, D., Salmonella enterica highly expressed genes are disease specific. Infect. Immun. 2006, 74, 1649-1660.
34. Alonso, A., Pucciarelli, M. G., Figueroa-Bossi, N., Garcia-del Portillo, F., Increased excision of the Salmonella prophage ST64B caused by a deficiency in Dam methylase. J. Bacteriol. 2005, 187, 7901-7911.
35. Pancholi, V., Chhatwal, G. S., Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol. 2003, 293, 391-401.
36. Schaumburg, J., Diekmann, O., Hagendorff, P., Bergmann, S. et al., The cell wall subproteome of Listeria monocytogenes. Proteomics 2004, 4, 2991-3006.
37. Feng, Y., Pan, X., Sun, W., Wang, C. et al., Streptococcus suis enolase functions as a protective antigen displayed on the bacterial cell surface. J. Infect. Dis. 2009, 200, 1583-1592.
38. Skovierova, H., Rowley, G., Rezuchova, B., Homerova, D. et al., Identification of the sigmaE regulon of Salmonella enterica serovar Typhimurium. Microbiology 2006, 152, 1347-1359.
39. Humphreys, S., Stevenson, A., Bacon, A., Weinhardt, A. B., Roberts, M., The alternative sigma factor, sigmaE, is critically important for the virulence of Salmonella typhimurium. Infect. Immun. 1999, 67, 1560-1568.
40. Maguire, M., Coates, A. R., Henderson, B., Chaperonin 60 unfolds its secrets of cellular communication. Cell Stress Chaperones 2002, 7, 317-329.
41. Pancholi, V., Fischetti, V. A., A major surface protein on group A streptococci is a glyceraldehyde-3-phosphate-dehydrogenase with multiple binding activity. J. Exp. Med. 1992, 176, 415-426.
42. Kenny, B., Finlay, B. B., Protein secretion by enteropathogenic Escherichia coli is essential for transducing signals to epithelial cells. Proc. Natl. Acad. Sci. USA 1995, 92, 7991-7995.
43. Kuchler, K., Unusual routes of protein secretion: the easy way out. Trends Cell. Biol. 1993, 3, 421-426.
44. Berrier, C., Garrigues, A., Richarme, G., Ghazi, A., Elongation factor Tu and DnaK are transferred from the cytoplasm to the periplasm of Escherichia coli during osmotic downshock presumably via the mechanosensitive channel mscL. J. Bacteriol. 2000, 182, 248-251.
45. Wang, I. N., Smith, D. L., Young, R., Holins: the protein clocks of bacteriophage infections. Annu. Rev. Microbiol. 2000, 54, 799-825.
46. Lee, E. Y., Choi, D. S., Kim, K. P., Gho, Y. S., Proteomics in gram-negative bacterial outer membrane vesicles. Mass Spectrom. Rev. 2008, 27, 535-555.
47. Kuehn, M. J., Kesty, N. C., Bacterial outer membrane vesicles and the host-pathogen interaction. Genes Dev. 2005, 19, 2645-2655.
48. Beveridge, T. J., Structures of gram-negative cell walls and their derived membrane vesicles. J. Bacteriol. 1999, 181, 4725-4733.
49. Alaniz, R. C., Deatherage, B. L., Lara, J. C., Cookson, B. T., Membrane vesicles are immunogenic facsimiles of Salmonella typhimurium that potently activate dendritic cells, prime B and T cell responses, and stimulate protective immunity in vivo. J. Immunol. 2007, 179, 7692-7701.
50. Coldham, N. G., Woodward, M. J., Characterization of the Salmonella typhimurium proteome by semi-automated two dimensional HPLC-mass spectrometry: detection of proteins implicated in multiple antibiotic resistance. J. Proteome Res. 2004, 3, 595-603.
51. Hoiseth, S. K., Stocker, B. A., Aromatic-dependent Salmonella typhimurium are non-virulent and effective as live vaccines. Nature 1981, 291, 238-239.