Insights into physiological traits of Bifidobacterium animalis subsp. lactis BB-12 through membrane proteome analysis

Journal of Proteomics

Volumn 75, Issue 4, 2012, Pages 1190-1200

  Gilad, Ofir ^a   Hjernø, Karin ^a   Østerlund, Eva C ^a   Margolles, Abelardo ^a   Svensson, Birte ^a   Stuer Lauridsen, Birgitte ^a   Møller, Anders L Blom ^a   Jacobsen, Susanne ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

Author keywords

Bifidobacterium; LC MS; Membrane proteomics; Probiotics; Transporters

Indexed keywords

ADENOSINE TRIPHOSPHATASE (CALCIUM); EXOPOLYSACCHARIDE; GLUCOSE; ION; MEMBRANE PROTEIN; OLIGOSACCHARIDE; PROTEIN DNAJ; PROTEIN DNAK; PROTEINASE; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; SIGNAL PEPTIDASE I; SORTASE;

AMINO ACID SEQUENCE; ARTICLE; BACTERIAL GROWTH; BIFIDOBACTERIUM ANIMALIS; ELECTROSPRAY; ENRICHMENT CULTURE; FRACTIONATION; LIQUID CHROMATOGRAPHY; MEMBRANE VESICLE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN LOCALIZATION; PROTEIN TRANSPORT; PROTEOMICS; TIME OF FLIGHT MASS SPECTROMETRY; UNINDEXED SEQUENCE;

BACTERIAL PROTEINS; BIFIDOBACTERIUM; COMPUTATIONAL BIOLOGY; DETERGENTS; GLUCOSE; HUMANS; OLIGOSACCHARIDES; PEPTIDES; PROBIOTICS; PROTEOME; PROTEOMICS; SERINE ENDOPEPTIDASES; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION; TRYPSIN;

BIFIDOBACTERIUM; BIFIDOBACTERIUM ANIMALIS SUBSP. LACTIS;

EID: 84855891090     PISSN: 18743919     EISSN: 18767737     Source Type: Journal    
DOI: 10.1016/j.jprot.2011.10.031     Document Type: Article

References (44)

1. Ventura M., Canchaya C., Tauch A., Chandra G., Fitzgerald G.F., Chater K.F., et al. Genomics of actinobacteria: tracing the evolutionary history of an ancient phylum. Microbiol Mol Biol Rev 2007, 71:495-548.
2. Marco M.L., Pavan S., Kleerebezem M. Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 2006, 17:204-210.
3. Masco L., Huys G., De Brandt E., Temmerman R., Swings J. Culture-dependent and culture-independent qualitative analysis of probiotic products claimed to contain bifidobacteria. Int J Food Microbiol 2005, 102:221-230.
4. von Heijne G. The membrane protein universe: what's out there and why bother?. J Intern Med 2007, 261:543-557.
5. Sánchez B., Bressollier P., Urdaci M. Exported proteins in probiotic bacteria: adhesion to intestinal surfaces, host immunomodulation and molecular cross-talking with the host. FEMS Immunol Med Microbiol 2008, 54:1-17.
6. Margolles A., Flórez A.B., Moreno J.A., van Sinderen D., de los Reyes-Gavilán C.G. Two membrane proteins from Bifidobacterium breve UCC2003 constitute an ABC-type multidrug transporter. Microbiology 2006, 152:3497-3505.
7. Margolles A., García L., Sánchez B., Gueimonde M., de los Reyes-Gavilán C.G. Characterisation of a Bifidobacterium strain with acquired resistance to cholate - a preliminary study. Int J Food Microbiol 2003, 82:191-198.
8. Ruiz L., Couté Y., Sánchez B., de los Reyes-Gavilán C.G., Sanchez J.C., Margolles A. The cell-envelope proteome of Bifidobacterium longum in an in vitro bile environment. Microbiology 2009, 155:957-967.
9. Parche S., Amon J., Jankovic I., Rezzonico E., Beleut M., Barutçu H. Sugar transport systems of Bifidobacterium longum NCC2705. J Mol Microbiol Biotechnol 2007, 12:9-19.
10. Gilad O., Jacobsen S., Stuer-Lauridsen B., Garrigues C., Pedersen M.B., Svensson B. Combined transcriptome and proteome analysis of Bifidobacterium animalis subsp. lactis BB-12 grown on xylo-oligosaccharides and a model of their utilization. Appl Environ Microbiol 2010, 76:7285-7291.
11. Johansson F., Olbe M., Sommarin M., Larsson C. Brij 58, a polyoxyethylene acyl ether, creates membrane vesicles of uniform sidedness. A new tool to obtain inside-out (cytoplasmic side-out) plasma membrane vesicles. Plant J 1995, 7:165-173.
12. Bradford M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 1976, 72:248-254.
13. Wessel D., Flügge U. A method for the quantitative recovery of protein in dilute-solution in the presence of detergents and lipids. Anal Biochem 1984, 138:141-143.
14. 2-based phosphoproteomic analysis of the plasma membrane and the effects of phosphatase inhibitor treatment. J Proteome Res 2008, 7:3304-3313.
15. Matthiesen R., Trelle M.B., Hojrup P., Bunkenborg J., Jensen O.N. VEMS 3.0: algorithms and computational tools for tandem mass spectrometry based identification of post-translational modifications in proteins. J Proteome Res 2005, 4:2338-2347.
16. Garrigues C., Johansen E., Pedersen M.B. Complete genome sequence of Bifidobacterium animalis subsp. lactis BB-12, a widely consumed probiotic strain. J Bacteriol 2010, 192:2467-2468.
17. Ashburner M., Ball C.A., Blake J.A., Botstein D., Butler H., Cherry J.M. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 2000, 25:25-29.
18. Klein C., Garcia-Rizo C., Bisle B., Scheffer B., Zischka H., Pfeiffer F., et al. The membrane proteome of Halobacterium salinarum. Proteomics 2005, 5:180-197.
19. Li Y., Massey K., Witkiewicz H., Schnitzer J.E. Systems analysis of endothelial cell plasma membrane proteome of rat lung microvasculature. Proteome Sci 2011, 9:15.
20. Rabilloud T. Keynotes on membrane proteomics. Subcell Biochem 2007, 43:3-11.
21. Luirink J., Sinning I. SRP-mediated protein targeting: structure and function revisited. Biochim Biophys Acta 2004, 1694:17-35.
22. Van Bogelen R.A., Neidhardt F.C. Ribosomes as sensors of heat and cold shock in Escherichia coli. Proc Natl Acad Sci U S A 1990, 87:5589-5593.
23. Spence J.M., Clark V.L. Role of ribosomal protein L12 in gonococcal invasion of Hec1B cells. Infect Immun 2000, 68:5002-5010.
24. Tjalsma H., Lambooy L., Hermans P.W., Swinkels D.W. Shedding & shaving: disclosure of proteomic expressions on a bacterial face. Proteomics 2008, 8:1415-1428.
25. Jeffery C.J. Moonlighting proteins: old proteins learning new tricks. Trends Genet 2003, 19:415-417.
26. Sánchez B., Urdaci M., Margolles A. Extracellular proteins secreted by probiotic bacteria as mediators of effects that promote mucosal-bacteria interactions. Microbiology 2010, 156:3232-3242.
27. Molloy M.P. Isolation of bacterial cell membranes proteins using carbonate extraction. Methods Mol Biol 2008, 424:397-401.
28. Cacciotto C., Addis M.F., Pagnozzi D., Chessa B., Coradduzz E., Carcangiu L., et al. The liposoluble proteome of Mycoplasma agalactiae: an insight into the minimal protein complement of a bacterial membrane. BMC Microbiol 2010, 10:225-236.
29. Biemans-Oldehinkel E., Doeven M.K., Poolman B. ABC transporter architecture and regulatory roles of accessory domains. FEBS Lett 2006, 580:1023-1035.
30. Kyte J., Doolittle R.F. A simple method for displaying the hydropathic character of a protein. J Mol Biol 1982, 157:105-132.
31. Santoni V., Molloy M., Rabilloud T. Membrane proteins and proteomics: un amour impossible?. Electrophoresis 2000, 21:1054-1070.
32. Russell R.R., Aduse-Opoku J., Sutcliffe I.C., Tao L., Ferretti J.J. A binding protein-dependent transport system in Streptococcus mutans responsible for multiple sugar metabolism. J Biol Chem 1992, 267:4631-4637.
33. Bertram R., Schlicht M., Mahr K., Nothaft H., Saier M.H., Titgemeyer F. In silico and transcriptional analysis of carbohydrate uptake systems of Streptomyces coelicolor A3(2). J Bacteriol 2004, 186:1362-1373.
34. Gilad O., Svensson B., Viborg A.H., Stuer-Lauridsen B., Jacobsen S. The extracellular proteome of Bifidobacterium animalis subsp. lactis BB-12 reveals proteins with putative roles in probiotic effects. Proteomics 2011, 11:2503-2514.
35. Ventura M., Canchaya C., van Sinderen D., Fitzgerald G.F., Zink R. Bifidobacterium lactis DSM 10140: identification of the atp (atpBEFHAGDC) operon and analysis of its genetic structure, characteristics, and phylogeny. Appl Environ Microbiol 2004, 70:3110-3121.
36. Matsumoto M., Ohishi H., Benno Y. H+-ATPase activity in Bifidobacterium with special reference to acid tolerance. Int J Food Microbiol 2004, 93:109-113.
37. Sánchez B., de los Reyes-Gavilán C.G., Margolles A. The F1F0-ATPase of Bifidobacterium animalis is involved in bile tolerance. Environ Microbiol 2006, 8:1825-1833.
38. Ruas-Madiedo P., Hugenholtza J., Zoon P. An overview of the functionality of exopolysaccharides produced by lactic acid bacteria. Int Dairy J 2002, 12:163-171.
39. Ruas-Madiedo P., Gueimonde M., Margolles A., de los Reyes-Gavilán C.G., Salminen S. Exopolysaccharides produced by probiotic strains modify the adhesion of probiotics and enteropathogens to human intestinal mucus. J Food Prot 2006, 69:2011-2015.
40. Wang L., Reeves P.R. Involvement of the galactosyl-1-phosphate transferase encoded by the Salmonella enterica rfbP gene in O-antigen subunit processing. J Bacteriol 1994, 176:4348-4356.
41. MacConaill L.E., Fitzgerald G.F., Van Sinderen D. Investigation of protein export in Bifidobacterium breve UCC2003. Appl Environ Microbiol 2003, 69:6994-7001.
42. Candela M., Turroni S., Centanni M., Fiori J., Bergmann S., Hammerschmidt S., et al. Relevance of Bifidobacterium animalis subsp. lactis plasminogen binding activity in the human gastrointestinal microenvironment. Appl Environ Microbiol 2011, 77:7072-7076.
43. Motherway M.O., Zomer A., Leahy S.C., Reunanen J., Bottacini F., Claesson M.J., et al. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved host-colonization factor. Proc Natl Acad Sci U S A 2011, 108:11217-11222.
44. Gonzalez R., Klaassens E.S., Malinen E., de Vos W.M., Vaughan E.E. Differential transcriptional response of Bifidobacterium longum to human milk, formula milk, and galactooligosaccharide. Appl Environ Microbiol 2008, 74:4686-4694.