Proteomic investigation of the aggregation phenomenon in Lactobacillus crispatus

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1784, Issue 2, 2008, Pages 335-342

  Siciliano, Rosa A ^a   Cacace, Giuseppina ^a   Mazzeo, Maria F ^a   Morelli, Lorenzo ^b   Elli, Marina ^b   Rossi, Mauro ^a   Malorni, Antonio ^a  

^a CNR   (Italy)

^b UNIVERSITÀ CATTOLICA DEL SACRO CUORE   (Italy)

Author keywords

Adhesion; Aggregation; Elongation factor EF Tu; Lactobacillus; Probiotics; Proteome

Indexed keywords

CARBOHYDRATE; ELONGATION FACTOR TU;

ARTICLE; BACTERIAL GROWTH; BACTERIAL STRAIN; BACTERIUM MUTANT; CARBOHYDRATE METABOLISM; CARBOHYDRATE TRANSPORT; CELL AGGREGATION; ENZYME SYNTHESIS; GROWTH RATE; LACTOBACILLUS; LACTOBACILLUS CRISPATUS; NONHUMAN; NUTRIENT CONTENT; PHENOTYPE; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ISOLATION; PROTEOMICS; SPECIES COMPARISON; TWO DIMENSIONAL ELECTROPHORESIS; UPREGULATION; WILD TYPE;

BACTERIAL PROTEINS; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; LACTOBACILLUS; MICROBIAL VIABILITY; PROTEOMICS; TANDEM MASS SPECTROMETRY;

LACTOBACILLUS; LACTOBACILLUS CRISPATUS;

EID: 38549120288     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2007.11.007     Document Type: Article

References (56)

1. Guidelines for the evaluation of probiotics in food. Report of a joint FAO/WHO working group on drafting guidelines for the evaluation of probiotics in food, 30 April-1 May 2002, London, UK and Ontario, Canada (2002)
2. Foligne B., Nutten S., Grangette C., Dennin V., Goudercourt D., Poiret S., Dewulf J., Brassart D., Mercenier A., and Pot B. Correlation between in vitro and in vivo immunomodulatory properties of lactic acid bacteria. World J. Gastroenterol. 13 (2007) 236-243
3. Mercenier A., Pavan S., and Pot B. Probiotics as biotherapeutic agents: present knowledge and future prospects. Curr. Pharm. Des. 9 (2003) 175-191
4. Marco M.L., Pavan S., and Kleerebezem M. Towards understanding molecular modes of probiotic action. Curr. Opin. Biotechnol. 17 (2006) 204-210
5. Saxelin M., Tynkkynen S., Mattila-Sandholm T., and de Vos W.M. Probiotic and other functional microbes: from markets to mechanisms. Curr. Opin. Biotechnol. 16 (2005) 204-211
6. Sartor R.B. Probiotic therapy of intestinal inflammation and infections. Curr. Opin. Gastroenterol. 21 (2005) 44-50
7. Reid G. The scientific basis for probiotic strains of Lactobacillus. Appl. Environ. Microbiol. 65 (1999) 3763-3766
8. Altermann E., Russell W.M., Azcarate-Peril M.A., Barrangou R., Buck B.L., McAuliffe O., Souther N., Dobson A., Duong T., Callanan M., et al. Complete genome sequence of the probiotic lactic acid bacterium Lactobacillus acidophilus NCFM. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 3906-3912
9. Kleerebezem M., Boekhorst J., van Kranenburg R., Molenaar D., Kuipers O.P., Leer R., Tarchini R., Peters S.A., Sandbrink H.M., Fiers M.W., et al. Complete genome sequence of Lactobacillus plantarum WCFS1. Proc. Natl. Acad. Sci. U. S. A. 100 (2003) 1990-1995
10. Pridmore R.D., Berger B., Desiere F., Vilanova D., Barretto C., Pittet A.C., Zwahlen M.C., Rouvet M., Altermann E., Barrangou R., et al. The genome sequence of the probiotic intestinal bacterium Lactobacillus johnsonii NCC 533. Proc. Natl. Acad. Sci. U. S. A. 101 (2004) 2512-2517
11. van de Guchte M., Penaud S., Grimaldi C., Barbe V., Bryson K., Nicolas P., Robert C., Oztas S., Mangenot S., Couloux A., et al. The complete genome sequence of Lactobacillus bulgaricus reveals extensive and ongoing reductive evolution. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 9274-9279
12. Chaillou S., Champomier-Verges M.C., Cornet M., Crutz-Le Coq A.M., Dudez A.M., Martin V., Beaufils S., Darbon-Rongere E., Bossy R., Loux V., and Zagorec M. The complete genome sequence of the meat-borne lactic acid bacterium Lactobacillus sakei 23K. Nat. Biotechnol. 23 (2005) 1527-1533
13. Claesson M.J., Li Y., Leahy S., Canchaya C., van Pijkeren J.P., Cerdeno-Tarraga A.M., Parkhill J., Flynn S., O'Sullivan G.C., Collins J.K., Higgins D., Shanahan F., Fitzgerald G.F., van Sinderen D., and O'Toole P.W. Multireplicon genome architecture of Lactobacillus salivarius. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 6718-6723
14. Barrangou R., Azcarate-Peril M.A., Duong T., Conners S.B., Kelly R.M., and Klaenhammer T.R. Global analysis of carbohydrate utilization by Lactobacillus acidophilus using cDNA microarrays. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 3816-3821
15. de Vos W.M., Bron P.A., and Kleerebezem M. Post-genomics of lactic acid bacteria and other food-grade bacteria to discover gut functionality. Curr. Opin. Biotechnol. 15 (2004) 86-93
16. Makarova K., Slesarev A., Wolf Y., Sorokin A., Mirkin B., Koonin E., Pavlov A., Pavlova N., Karamychev V., Polouchine N., et al. Comparative genomics of the lactic acid bacteria. Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 15611-15616
17. Teusink B., van Enckevort F.H., Francke C., Wiersma A., Wegkamp A., Smid E.J., and Siezen R.J. In silico reconstruction of the metabolic pathways of Lactobacillus plantarum: comparing predictions of nutrient requirements with those from growth experiments. Appl. Environ. Microbiol. 71 (2005) 7253-7262
18. Granato D., Perotti F., Masserey I., Rouvet M., Golliard M., Servin A., and Brassart D. Cell surface-associated lipoteichoic acid acts as an adhesion factor for attachment of Lactobacillus johnsonii La1 to human enterocyte-like Caco-2 cells. Appl. Environ. Microbiol. 65 (1999) 1071-1077
19. Buck B.L., Altermann E., Svingerud T., and Klaenhammer T.R. Functional analysis of putative adhesion factors in Lactobacillus acidophilus NCFM. Appl. Environ. Microbiol. 71 (2005) 8344-8351
20. Pretzer G., Snel J., Molenaar D., Wiersma A., Bron P.A., Lambert J., de Vos W.M., van der Meer R., Smits M.A., and Kleerebezem M. Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J. Bacteriol. 187 (2005) 6128-6136
21. Bergonzelli G.E., Granato D., Pridmore R.D., Marvin-Guy L.F., Donnicola D., and Corthesy-Theulaz I.E. GroEL of Lactobacillus johnsonii La1 (NCC 533) is cell surface associated: potential role in interactions with the host and the gastric pathogen Helicobacter pylori. Infect. Immun. 74 (2006) 425-434
22. Granato D., Bergonzelli G.E., Pridmore R.D., Marvin L., Rouvet M., and Corthesy-Theulaz I.E. Cell surface-associated elongation factor Tu mediates the attachment of Lactobacillus johnsonii NCC533 (La1) to human intestinal cells and mucins. Infect. Immun. 72 (2004) 2160-2169
23. Rojas M., Ascencio F., and Conway P.L. Purification and characterization of a surface protein from Lactobacillus fermentum 104R that binds to porcine small intestinal mucus and gastric mucin. Appl. Environ. Microbiol. 68 (2002) 2330-2336
24. Roos S., and Jonsson H. A high-molecular-mass cell-surface protein from Lactobacillus reuteri 1063 adheres to mucus components. Microbiology 148 (2002) 433-442
25. Todoriki K., Mukai T., Sato S., and Toba T. Inhibition of adhesion of food-borne pathogens to Caco-2 cells by Lactobacillus strains. J. Appl. Microbiol. 91 (2001) 154-159
26. Horie M., Ishiyama A., Fujihira-Ueki Y., Sillanpaa J., Korhonen T.K., and Toba T. Inhibition of the adherence of Escherichia coli strains to basement membrane by Lactobacillus crispatus expressing an S-layer. J. Appl. Microbiol. 92 (2002) 396-403
27. Antikainen J., Anton L., Sillanpaa J., and Korhonen T.K. Domains in the S-layer protein CbsA of Lactobacillus crispatus involved in adherence to collagens, laminin and lipoteichoic acids and in self-assembly. Mol. Microbiol. 46 (2002) 381-394
28. Chen X., Xu J., Shuai J., Chen Z., Zhang W., and Fang. The S-layer proteins of Lactobacillus crispatus strain ZJ001 is responsible for competitive exclusion against Escherichia coli O157:H7 and Salmonella typhimurium. Int. J. Food Microbiol. 115 (2007) 307-312
29. Castagliuolo I., Galeazzi F., Ferrari S., Elli M., Brun P., Cavaggioni A., Tormen D., Sturniolo G.C., Morelli L., and Palu G. Beneficial effect of auto-aggregating Lactobacillus crispatus on experimentally induced colitis in mice. FEMS Immunol. Med. Microbiol. 43 (2005) 197-204
30. Cesena C., Morelli L., Alander M., Siljander T., Tuomola E., Salminen S., Mattila-Sandholm T., Vilpponen-Salmela T., and von Wright A. Lactobacillus crispatus and its nonaggregating mutant in human colonization trials. J. Dairy Sci. 84 (2001) 1001-1110
31. Marcotte H., Ferrari S., Cesena C., Hammarstrom L., Morelli L., Pozzi G., and Oggioni M.R. The aggregation-promoting factor of Lactobacillus crispatus M247 and its genetic locus. J. Appl. Microbiol. 97 (2004) 749-756
32. 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. 72 (1976) 248-254
33. O'Farrell P.H. High resolution two-dimensional electrophoresis of proteins. J. Biol. Chem. 250 (1975) 4007-4021
34. Tosco A., Siciliano R.A., Cacace G., Mazzeo M.F., Caponea R., Malorni A., Leone A., and Marzullo L. Dietary effects of copper and iron deficiency on rat intestine: a differential display proteome analysis. J. Proteome Res. 4 (2005) 1781-1788
35. Pappin D.J.C., Hojrup P., and Bleasby A.J. Rapid identification of proteins by peptide-mass fingerprinting. Curr. Biol. 3 (1993) 327-332
36. Shevchenko A., Chernushevic I., Shevchenko A., Wilm M., and Mann M. De novo sequencing of peptides recovered from in-gel digested proteins by nanoelectrospray tandem mass spectrometry. Mol. Biotechnol. 20 (2002) 107-118
37. Kanehisa M., Goto S., Kawashima S., Okuno Y., and Hattori M. The KEGG resource for deciphering the genome. Nucleic Acids Res. 32 (2004) D277-D280
38. Rathsam C., Eaton R.E., Simpson C.L., Browne G.V., Berg T., Harty D.W., and Jacques N.A. Up-regulation of competence-but not stress-responsive proteins accompanies an altered metabolic phenotype in Streptococcus mutans biofilms. Microbiology 151 (2005) 1823-1837
39. Rathsam C., Eaton R.E., Simpson C.L., Browne G.V., Valova V.A., Harty D.W., and Jacques N.A. Two-dimensional fluorescence difference gel electrophoretic analysis of Streptococcus mutans biofilms. J. Proteome Res. 4 (2005) 2161-2173
40. Lorquet F., Goffin P., Muscariello L., Baudry J.B., Ladero V., Sacco M., Kleerebezem M., and Hols P. Characterization and functional analysis of the poxB gene, which encodes pyruvate oxidase in Lactobacillus plantarum. J. Bacteriol. 186 (2004) 3749-3759
41. Cohen D.P., Renes J., Bouwman F.G., Zoetendal E.G., Mariman E., de Vos W.M., and Vaughan E.E. Proteomic analysis of log to stationary growth phase Lactobacillus plantarum cells and a 2-DE database. Proteomics 6 (2006) 6485-6493
42. Uziel O., Borovok I., Schreiber R., Cohen G., and Aharonowitz Y. Transcriptional regulation of the Staphylococcus aureus thioredoxin and thioredoxin reductase genes in response to oxygen and disulfide stress. J. Bacteriol. 186 (2004) 326-334
43. Watson S.P., Clements M.O., and Foster S.J. Characterization of the starvation-survival response of Staphylococcus aureus. J. Bacteriol. 180 (1998) 1750-1758
44. Jacobson G.R., and Rosenbusch J.P. Abundance and membrane association of elongation factor Tu in E. coli. Nature 261 (1976) 23-26
45. Schaumburg J., Diekmann O., Hagendorff P., Bergmann S., Rohde M., Hammerschmidt S., Jansch L., Wehland J., and Karst U. The cell wall subproteome of Listeria monocytogenes. Proteomics 4 (2004) 2991-3006
46. Marques M.A., Chitale S., Brennan P.J., and Pessolani M.C. Mapping and identification of the major cell wall-associated components of Mycobacterium leprae. Infect. Immun. 66 (1998) 2625-2631
47. Porcella S.F., Belland R.J., and Judd R.C. Identification of an EF-Tu protein that is periplasm-associated and processed in Neisseria gonorrhoeae. Microbiology 142 (1996) 2481-2489
48. Dallo S.F., Kannan T.R., Blaylock M.W., and Baseman J.B. Elongation factor Tu and E1 beta subunit of pyruvate dehydrogenase complex act as fibronectin binding proteins in Mycoplasma pneumoniae. Mol. Microbiol. 46 (2002) 1041-1051
49. Kelly P., Maguire P.B., Bennett M., Fitzgerald D.J., Edwards R.J., Thiede B., Treumann A., Collins J.K., O'Sullivan G.C., Shanahan F., and Dunne C. Correlation of probiotic Lactobacillus salivarius growth phase with its cell wall-associated proteome. FEMS Microbiol. Lett. 252 (2005) 153-159
50. Hurmalainen V., Edelman S., Antikainen J., Baumann M., Lahteenmaki K., and Korhonen T.K. Extracellular proteins of Lactobacillus crispatus enhance activation of human plasminogen. Microbiology 153 (2007) 1112-1122
51. Antikainen J., Kupannen V., Lähteenmäki K., and Korhonen T.K. pH-dependent association of enolase and glyceraldehyde-3-phosphate dehydrogenase of Lactobacillus crispatus with the cell wall and lipoteichoic acids. J. Bacteriol. 189 (2007) 4539-4543
52. Gopal P.K., Prasad J., Smart J., and Gill H.S. In vitro adherence properties of Lactobacillus rhamnosus DR20 and Bifidobacterium lactis DR10 strains and their antagonistic activity against an enterotoxigenic Escherichia coli. Int. J. Food Microbiol. 67 (2001) 207-216
53. Reid G., and Burton J. Use of Lactobacillus to prevent infection by pathogenic bacteria. Microbes Infect. 4 (2002) 319-324
54. Perdigon G., Maldonado Galdeano C., Valdez J.C., and Medici M. Interaction of lactic acid bacteria with the gut immune system. Eur. J. Clin. Nutr. 56 (2002) S21-S26
55. Jeffery C.J. Moonlighting proteins. Trends Biochem. Sci. 24 (1999) 8-11
56. Pancholi V., and Chhatwal G.S. Housekeeping enzymes as virulence factors for pathogens. Int. J. Med. Microbiol. 293 (2003) 391-401