Comparative proteome cataloging of Lactobacillus rhamnosus strains GG and Lc705

Journal of Proteome Research

Volumn 10, Issue 8, 2011, Pages 3460-3473

  Savijoki, Kirsi ^a,c   Lietzén, Niina ^a   Kankainen, Matti ^b   Alatossava, Tapani ^c   Koskenniemi, Kerttu ^c   Varmanen, Pekka ^c   Nyman, Tuula A ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b VALIO LTD   (Finland)

^c UNIVERSITY OF HELSINKI   (Finland)

Author keywords

1 DE; Compid; LC MS MS; probiotic Lactobacillus; proteome coverage; proteomics; RT PCR; surfome

Indexed keywords

LACTOSE; LIPOPROTEIN; MEMBRANE PROTEIN; PEPTIDOGLYCAN; PROTEOME;

ARTICLE; BACTERIAL CELL WALL; BACTERIAL STRAIN; BACTERIOPHAGE; BIOFILM; COMPARATIVE STUDY; IMMUNOMODULATION; LACTOBACILLUS RHAMNOSUS; MASS SPECTROMETRY; NONHUMAN; NUCLEOTIDE SEQUENCE; OPERON; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN EXPRESSION;

BACTERIAL PROTEINS; CHROMATOGRAPHY, LIQUID; COMPUTATIONAL BIOLOGY; ELECTROPHORESIS, POLYACRYLAMIDE GEL; LACTOBACILLUS RHAMNOSUS; OPERON; PROBIOTICS; PROTEOME; TANDEM MASS SPECTROMETRY; TRANSCRIPTION, GENETIC;

BACTERIA (MICROORGANISMS); LACTOBACILLUS; LACTOBACILLUS RHAMNOSUS;

EID: 79961236461     PISSN: 15353893     EISSN: 15353907     Source Type: Journal    
DOI: 10.1021/pr2000896     Document Type: Article

References (75)

1. Leroy, F.; De Vuyst, L. Lactic acid bacteria as functional starter cultures for the food fermentation industry Trends Food Sci. Technol. 2004, 15 (2) 67-78 (Pubitemid 38192839)
2. Walter, J. Ecological role of lactobacilli in the gastrointestinal tract: implications for fundamental and biomedical research Appl. Environ. Microbiol. 2008, 74 (16) 4985-4996
3. Taxonomy of Lactobacilli and Bifidobacteria. Probiotics and Prebiotics: Scientific Aspects; Tannock, G. W., Ed.; Caister Academic Press: Norfolk, U.K., 2005.
4. Goldin, B. R.; Gorbach, S. L. Clinical indications for probiotics: an overview Clin. Infect. Dis. 2008, 46 (S2) 96-100
5. Saxelin, M.; Tynkkynen, S.; Mattila-Sandholm, T.; de Vos, W. M. Probiotic and other functional microbes: from markets to mechanisms Curr. Opin. Biotechnol. 2005, 16 (2) 204-211
6. Siezen, R. J.; Wilson, G. Probiotics genomics Microb. Biotechnol. 2010, 3 (1) 1-9
7. Ventura, M.; O'Flaherty, S.; Claesson, M. J.; Turroni, F.; Klaenhammer, T. R.; van Sinderen, D.; O'Toole, P. W. Genome-scale analyses of health-promoting bacteria: probiogenomics Nat. Rev. 2009, 7 (1) 61-71
8. Goldin, B. R.; Gorbach, S. L. Lactobacillus GG: a new strain with properties favorable for survival, adhesion and antimicrobial activity in the gastrointestinal tract FEMS Microbiol. Rev. 1987, 46 (3) 72
9. Antonsson, M.; Ardo, Y.; Nilsson, B. F.; Molin, G. Screening and selection of Lactobacillus strains for use as adjunct cultures in production of semi-hard cheese J. Dairy Res. 2002, 69 (3) 457-472
10. Mäyrä-Mäkinen, A.; Suomalainen, T. Lactobacillus casei ssp. rhamnosus, bacterial preparations comprising said strain, and use of said strain and preparations for the controlling of yeast and moulds Biotechnol. Adv. 1995, 13 (4) 768
11. Suomalainen, T.; Mäyrä-Mäkinen, A. Propionic acid bacteria as protective cultures in fermented milks and breads Lait 1999, 79 (1) 165-174 (Pubitemid 129511860)
12. Majamaa, H.; Isolauri, E. Probiotics: A novel approach in the management of food allergy J. Allergy Clin. Immunol. 1997, 99 (2) 179-185 (Pubitemid 27091565)
13. Isolauri, E.; Arvola, T.; Sutas, Y.; Moilanen, E.; Salminen, S. Probiotics in the management of atopic eczema Clin. Exp. Allergy 2000, 30 (11) 1604-1610
14. Hatakka, K; Savilahti, E.; Pönkä, A.; Meurman, J. H.; Poussa, T.; Näse, L.; Saxelin, M.; Korpela, R. Effect of long term consumption of probiotic milk on infections in children attending day care centres: Double blind, randomised trial Br. Med. J. 2001, 322 (7298) 1327-1329 (Pubitemid 32521266)
15. Nase, L.; Hatakka, K.; Savilahti, E.; Saxelin, M.; Ponka, A.; Poussa, T.; Korpela, R.; Meurman, J. H. Effect of long-term consumption of a probiotic bacterium, Lactobacillus rhamnosus GG, in milk on dental caries and caries risk in children Caries Res. 2000, 35 (6) 412-420 (Pubitemid 33636860)
16. Szajewska, H.; Kotowska, M.; Mrukowicz, J. Z.; Armanska, M.; Mikolajczyk, W. Efficacy of Lactobacillus GG in prevention of nosocomial diarrhea in infants J. Pediatr. 2001, 138 (3) 361-365 (Pubitemid 32207138)
17. Kalliomäki, M.; Salminen, S.; Poussa, T.; Arvilommi, H.; Isolauri, E. Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial Lancet 2003, 361 (9372) 1869-1871 (Pubitemid 36645184)
18. Viljanen, M.; Savilahti, E.; Haahtela, T.; Juntunen-Backman, K.; Korpela, R.; Poussa, T.; Tuure, T.; Kuitunen, M. Probiotics in the treatment of atopic eczema/dermatitis syndrome in infants: A double-blind placebo-controlled trial Allergy 2005, 60 (4) 494-500 (Pubitemid 40332976)
19. 1 binding by a mixture of Lactobacillus and Propionibacterium: in vitro versus ex vivo J. Food Prot. 2005, 68 (11) 2470-2474 (Pubitemid 41628429)
20. Kajander, K.; Korpela, R. Clinical studies on alleviating the symptoms of irritable bowel syndrome Asia Pac. J. Clin. Nutr. 2006, 15 (4) 576-580 (Pubitemid 44905140)
21. Kajander, K.; Myllyluoma, E.; Rajilić-Stojanović, M.; Kyrönpalo, S.; Rasmussen, M.; Järvenpää, S; Zoetendal, E. G.; de Vos, W. M.; Vapaatalo, H.; Korpela, R. Clinical trial: multispecies probiotic supplementation alleviates the symptoms of irritable bowel syndrome and stabilizes intestinal microbiota Aliment. Pharmacol. Ther. 2008, 27 (1) 48-57 (Pubitemid 350212625)
22. Kankainen, M.; Paulin, L.; Tynkkynen, S.; von Ossowski, I.; Reunanen, J.; Partanen, P.; Satokari, R.; Vesterlund, S.; Hendrickx, A. P.; Lebeer, S.; De Keersmaecker, S. C.; Vanderleyden, J.; Hämäläinen, T.; Laukkanen, S.; Salovuori, N.; Ritari, J.; Alatalo, E.; Korpela, R.; Mattila-Sandholm, T.; Lassig, A.; Hatakka, K.; Kinnunen, K. T.; Karjalainen, H.; Saxelin, M.; Laakso, K.; Surakka, A.; Palva, A.; Salusjärvi, T.; Auvinen, P.; de Vos, W. M. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein Proc. Nat. Acad. Sci. U.S.A. 2009, 106 (40) 17193-17198
23. von Ossowski, I.; Reunanen, J.; Satokari, R.; Vesterlund, S.; Kankainen, M.; Huhtinen, H.; Tynkkynen, S.; Salminen, S.; de Vos, W. M.; Palva, A. Mucosal adhesion properties of the probiotic Lactobacillus rhamnosus GG SpaCBA and SpaFED pilin subunits Appl. Environ. Microbiol. 2010, 76 (7) 2049-2057
24. Cohen, D. P.; Renes, J.; Bouwman, F. G.; Zoetendal, E. G.; Mariman, E.; de Vos, W. M.; Vaughan, E. E. Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database Proteomics 2006, 6 (24) 6485-6493 (Pubitemid 46048387)
25. Yang, F.; Wang, J.; Li, X.; Ying, T.; Qiao, S.; Li, D.; Wu, G. 2-DE and MS analysis of interactions between Lactobacillus fermentum I5007 and intestinal epithelial cells Electrophoresis 2007, 28 (23) 4330-4339 (Pubitemid 350259035)
26. Koskenniemi, K.; Koponen, J.; Kankainen, M.; Savijoki., K.; Tynkkynen, S.; de Vos, W. M.; Kalkkinen, N.; Varmanen, P. Proteome analysis of Lactobacillus rhamnosus GG using 2-D DIGE and mass spectrometry shows differential protein production in laboratory and industrial-type growth media J. Proteome Res. 2009, 8 (11) 4993-5007
27. Wu, R.; Wang, W.; Yu, D.; Zhang, W.; Li, Y.; Sun, Z.; Wu, J.; Meng, H.; Zhang, H. Proteomics analysis of Lactobacillus casei Zhang, a new probiotic bacterium isolated from traditional home-made koumiss in Inner Mongolia of China Mol. Cell. Proteomics 2009, 8 (10) 2321-2338
28. Koskenniemi, K; Laakso, K; Koponen, J; Kankainen, M; Greco, D; Auvinen, P; Savijoki, K; Nyman, T. A.; Surakka, A; Salusjärvi, T; de Vos, W. M.; Tynkkynen, S; Kalkkinen, N; Varmanen, P. Proteomics and transcriptomics characterization of bile stress response in probiotic Lactobacillus rhamnosus GG Mol. Cell. Proteomics 2011, doi: 0.1074/mcp.M110.002741-1.
29. Schirle, M.; Heurtier, M. A.; Kuster, B. Profiling core proteomes of human cell lines by one-dimensional PAGE and liquid chromatography-tandem mass spectrometry Mol. Cell. Proteomics 2003, 2 (12) 1297-1305
30. Gao, B. B.; Stuart, L.; Feener, E. P. Label-free quantitative analysis of one-dimensional PAGE LC/MS/MS proteome: application on angiotensin II-stimulated smooth muscle cells secretome Mol. Cell. Proteomics 2008, 7 (12) 2399-2409
31. Højlund, K.; Yi, Z.; Hwng, H.; Bowen, B.; Lefort, N.; Flynn, C. R.; Langlais, P.; Weintraub, S. T.; Mandarino, L. J. Characterization of the human skeletal muscle proteome by one-dimensional gel electrophoresis and HPLC-ESI-MS/MS Mol. Cell. Proteomics 2008, 7 (2) 257-267 (Pubitemid 351298440)
32. Gupta, M. K.; Jang, J. M.; Jung, J. W.; Uhm, S. J.; Kim, K. P.; Lee, H. T. Proteomic analysis of parthenogenetic and in vitro fertilized porcine embryos Proteomics 2009, 9 (10) 2846-2860
33. Beganović, J.; Guillot, A.; van de Guchte, M.; Jouan, A.; Gitton, C.; Loux, V.; Roy, K.; Huet, S.; Monod, H.; Monnet, V. Characterization of the insoluble proteome of Lactococcus lactis by SDS-PAGE LC-MS/MS leads to the identification of new markers of adaptation of the bacteria to the mouse digestive tract J. Proteome Res. 2010, 9 (2) 677-688
34. Fang, Y.; Robinson, D. P.; Foster, L. J. Quantitative analysis of proteome coverage and recovery rates for upstream fractionation methods in proteomics J. Proteome Res. 2010, 9 (4) 1902-1912
35. Shevchenko, A.; Wilm, M.; Vorm, O.; Mann, M. Mass spectrometric sequencing of proteins from silver-stained polyacrylamide gels Anal. Chem. 1996, 68 (5) 850-858
36. Lietzén, N.; Natri, L.; Nevalainen, O. S.; Salmi, J.; Nyman, T. A. Compid - a new software tool to integrate and compare MS/MS based protein identification results from Mascot and Paragon J. Proteome Res. 2010, 9 (12) 6795-6800
37. Elias, J. E.; Gygi, S. P. Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry Nat. Methods 2007, 4 (3) 207-214 (Pubitemid 46358868)
38. Rice, P.; Longden, I.; Bleasby, A. EMBOSS: The European Molecular Biology Open Software Suite Trends Genet. 2000, 16 (6) 276-277
39. van Baarlen, P.; Troost, F. J.; van Hemert, S.; van der Meer, C.; de Vos, W. M.; de Groot, P. J.; Hooiveld, G. J.; Brummer, R. J.; Kleerebezem, M. Differential NF-kappaB pathways induction by Lactobacillus plantarum in the duodenum of healthy humans correlating with immune tolerance Proc. Natl. Acad. Sci. U.S.A. 2009, 106 (7) 2371-2376
40. Solubilization of proteins in 2-D electrophoresis. Methods in Molecular Biology, 2-D proteome analysis protocols; Link, A. J., Ed.; Humana Press Inc.: Totowa, NJ, 1999.
41. Perkins, D. N.; Pappin, D. J.; Creasy, D. M.; Cottrell, J. S. Probability-based protein identification by searching sequence databases using mass spectrometry data Electrophoresis 1999, 20 (18) 3551-3567 (Pubitemid 30007252)
42. Shilov, I. V.; Seymour, S. L.; Patel, A. A.; Loboda, A.; Tang, W. H.; Keating, S. P.; Hunter, C. L.; Nuwaysir, L. M.; Schaeffer, D. A. 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 (9) 1638-1655 (Pubitemid 47506173)
43. Wang, H.; Chang-Wong., T; Tang, H.-Y.; Speicher, D. E. Comparison of extensive protein fractionation and repetitive LC-MS/MS analyses on depth of analysis for complex proteomes J. Proteome Res. 2010, 9 (2) 1032-1040
44. Delcher, A. L.; Bratke, K. A.; Powers, E. C.; Salzberg, S. L. Identifying bacterial genes and endosymbiont DNA with Glimmer Bioinformatics 2007, 23 (6) 673-679 (Pubitemid 46554717)
45. Fischer, F.; Wolters, D.; Rögner, M.; Poetsch, A. Toward the complete membrane proteome: high coverage of integral membrane proteins through transmembrane peptide detection Mol. Cell. Proteomics 2006, 5 (3) 444-453
46. Hahne, H.; Wolff, S.; Hecker, M.; Becher, D. From complementarity to comprehensiveness - targeting the membrane proteome of growing Bacillus subtilis by divergent approaches Proteomics 2008, 8 (19) 4123-4136
47. Wolff, S.; Hahne, H.; Hecker, M.; Becher, D. Complementary analysis of the vegetative membrane proteome of the human pathogen Staphylococcus aureus Mol. Cell. Proteomics 2008, 7 (8) 1460-1468
48. Becher, D.; Hempel, K.; Sievers, S.; Zühlke, D.; Pané-Farré, J.; Otto, A.; Fuchs, S.; Albrecht, D.; Bernhardt, J.; Engelmann, S.; Völker, U.; van Dijl, J. M.; Hecker, M. A proteomic view of an important human pathogen - towards the quantification of the entire Staphylococcus aureus proteome PLoS One 2009, 4 (12) e8
49. Sievers, S.; Ernst, C.; Geiger, T.; Hecker, M.; Wolz, C.; Becher, D.; Peschel, A. Changing the phospholipid composition of Staphylococcus aureus causes distinct changes in membrane proteome and membrane-sensory regulators Proteomics 2010, 10 (8) 1685-1693
50. Tatusov, R. L.; Galperin, M. Y.; Natale, D. A.; Koonin, E. V. The COG database: a tool for genome-scale analysis of protein functions and evolution Nucleic Acids Res. 2000, 28 (1) 33-36 (Pubitemid 30047708)
51. Tsai, Y.-K.; Lin, T.-H. Sequence, organization, transcription and regulation of lactose and galactose operons in Lactobacillus rhamnosus TCELL-1 J. Appl. Microbiol. 2006, 100 (3) 446-459
52. Seo, H. S.; Ziong, Y. Q.; MitcVhell, J.; Seepersaud, R.; Bayer, A. S.; Sullam, P. M. Bacteriophage lysin mediates the binding of Streptococcus mitis to human platelets through interaction with fibrinogen PLoS Pathog. 2010, 6 (8) e1001047
53. Gerdes, K; Christensen, S. K.; Lobner-Olesen, A. Prokaryotic toxin-antitoxin stress response loci Nat. Rev. Microbiol. 2005, 3 (5) 371-382 (Pubitemid 40590380)
54. Van Melderen, L.; De Bast, M. S. Bacterial toxin-antitoxin systems: more than selfish entities? PLoS Genetics 2009, 5 (3) e1000437
55. Young, I.; Wang, I.; Roof, W. D. Phages will out: strategies of host cell lysis Trends Microbiol. 2000, 8 (3) 120-128 (Pubitemid 30155487)
56. Khemayan, K.; Pasharawipas, T.; Puiprom, O.; Sriurairatana, S.; Suthienkul, O.; Flegel, T. W. Unstable lysogeny and pseudolysogeny in Vibrio harveyi siphovirus-like phage 1 Appl. Environ. Microbiol. 2006, 72 (2) 1355-1363 (Pubitemid 43271247)
57. Sutcliffe, I. C.; Harrington, D. J. Pattern searches for the identification of putative lipoprotein genes in Gram-positive bacterial genomes Microbiology 2002, 148 (Pt7) 2065-2077 (Pubitemid 34785291)
58. Konings, W. N.; Albers, S. V.; Koning, S.; Driessen, A. J. The cell membrane plays a crucial role in survival of bacteria and archaea in extreme environments Antonie Van Leeuwenhoek 2002, 81 (1-4) 61-72 (Pubitemid 35314597)
59. Surface proteins on Gram-positive bacteria. Gram-Positive Pathogens; Fischetti, V. A.; Novick, R. P.; Vincent, A.; Ferretti, J. J.; Portnoy, D. A.; Rood, J. I., Eds.; American Society for Microbiology: Washington, DC, 2006.
60. Silber, K. R.; Keiler, K. C.; Sauer, R. T. Tsp: a tail-specific protease that selectively degrades proteins with nonpolar C termini Proc. Natl. Acad. Sci. U.S.A. 1992, 89 (1) 295-299
61. Östberg, Y.; Carroll, J. A.; Pinne, M.; Krum, J. G.; Rosa, P.; Bergström, S. Pleiotropic effects of inactivating a carboxyl-terminal protease CptA, in Borrelia burgdorferi J. Bacteriol. 2004, 186 (7) 2074-2084 (Pubitemid 38381196)
62. Badel, S.; Bernardi, T.; Michaud, P. New perspectives for lactobacilli exopolysaccharides Biotechnol. Adv. 2011, 29 (1) 54-66
63. Landersjö, C.; Yang, Z.; Huttunen, E.; Widmalm, G. Structural studies of the exopolysaccharide produced by Lactobacillus rhamnosus strain GG (ATCC 53103) Biomacromolecules 2002, 3 (4) 880-884
64. Reeves, P. Evolution of Salmonella O antigen variation by interspecific gene transfer on a large scale Trends Genet. 1993, 9 (1) 17-22 (Pubitemid 23022565)
65. Tsukioka, Y.; Yamashita, Y.; Oho, T.; Nakano, Y.; Koga, T. Biological function of the dTDP-rhamnose synthesis pathway in Streptococcus mutans J. Bacteriol. 1997, 179 (4) 1126-1134 (Pubitemid 27076575)
66. Flemming, H. C.; Wingender, J. The biofilm matrix Nat. Rev. Microbiol. 2010, 8 (9) 623-633
67. Lebeer, S.; De Keersmaecker, S. C.; Verhoeven, T. L.; Fadda, A. A.; Marchal, K.; Vanderleyden, J. Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation J. Bacteriol. 2007, 189 (3) 860-871 (Pubitemid 46183860)
68. Lebeer, S.; Verhoeven, T. L.; Vélez, M. P.; Vanderleyden, J.; De Keersmaecker, S. C. Impact of environmental and genetic factors on biofilm formation by the probiotic strain Lactobacillus rhamnosus GG Appl. Environ. Microbiol. 2007, 73 (21) 6768-6775 (Pubitemid 350076795)
69. Lebeer, S.; Claes, I. J.; Verhoeven, T. L.; Shen, C.; Lambrichts, I.; Ceuppens, J. L.; Vanderleyden, J.; De Keersmaecker, S. C. Impact of luxS and suppressor mutations on the gastrointestinal transit of Lactobacillus rhamnosus GG Appl. Environ. Microbiol. 2008, 74 (15) 4711-4718
70. Lebeer, S.; Verhoeven, T. L.; Francius, G.; Schoofs, G.; Lambrichts, I.; Dufrêne, Y.; Vanderleyden, J.; De Keersmaecker, S. C. Identification of a gene cluster for the biosynthesis of a long, galactose-rich exopolysaccharide in Lactobacillus rhamnosus GG and functional analysis of the priming glycosyltransferase Appl. Environ. Microbiol. 2009, 75 (11) 3554-3563
71. The microbiology of cheese ripening. Cheese: Chemistry, Physics and Microbiology; Fox, P.; McSweeney, P. L. H.; Cogan, T. M.; Guinee, T. P., Eds.; Elsevier Academic Press: London, U.K., 2004.
72. Vélez, M. P.; Petrova, M. I.; Lebeer, S.; Verhoeven, T. L.; Claes, I.; Lambrichts, I.; Tynkkynen, S.; Vanderleyden, J.; De Keersmaecker, S. C. Characterization of MabA, a modulator of Lactobacillus rhamnosus GG adhesion and biofilm formation FEMS Immunol. Med. Microbiol. 2010, 59 (3) 386-398
73. Fadda, D.; Pischedda, C.; Caldara, F.; Whalen, M. B.; Anderluzzi, D.; Domenici, E.; Massidda, O. Characterization of divIVA and other genes located in the chromosomal region downstream of the dcw cluster in Streptococcus pneumoniae J. Bacteriol. 2003, 185 (20) 6209-6221
74. Bramkamp, M. The putative Bacillus subtilis L,D-transpeptidase YciB is a lipoprotein that localizes to the cell poles in a divisome-dependent manner Arch. Microbiol. 2010, 192 (1) 57-68
75. Beloin, C.; Valle, J.; Latour-Lambert, P.; Faure, P.; Kzreminski, M.; Balestrino, D.; Haagensen, J. A.; Molin, S.; Prensier, G.; Arbeille, B.; Ghigo, J. M. Global impact of mature biofilm lifestyle on Escherichia coli K-12 gene expression Mol. Microbiol. 2004, 51 (3) 659-674 (Pubitemid 38233935)