BopA does not have a major role in the adhesion of Bifidobacterium bifidum to intestinal epithelial cells, extracellular matrix proteins, and mucus

Applied and Environmental Microbiology

Volumn 79, Issue 22, 2013, Pages 6989-6997

  Kainulainen, Veera ^a   Reunanen, Justus ^a   Hiippala, Kaisa ^a   Guglielmetti, Simone ^b   Vesterlund, Satu ^c   Palva, Airi ^a   Satokari, Reetta ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

^b UNIVERSITY OF MILAN   (Italy)

^c UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADHESION ASSAYS; BIFIDOBACTERIA; BIFIDOBACTERIUM BIFIDUM; EPITHELIAL CELLS; EXTRACELLULAR MATRIX PROTEIN; HUMAN EPITHELIAL CELLS; INTESTINAL CELLS; INTESTINAL EPITHELIAL CELLS;

BACTERIA; BODY FLUIDS; CELL CULTURE; CELL MEMBRANES; CLONING; ESCHERICHIA COLI; GENE ENCODING;

ADHESION;

ADHESION; BACTERIUM; CELL ORGANELLE; COLONIZATION; MATRIX; PROTEIN; RECOMBINATION;

BACTERIAL PROTEIN; LIPOPROTEIN; MEMBRANE PROTEIN; PROBIOTIC AGENT; RECOMBINANT PROTEIN; SCLEROPROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIUM ADHERENCE; BIFIDOBACTERIUM; CACO 2 CELL LINE; CELL MEMBRANE; CYTOLOGY; EPITHELIUM CELL; ESCHERICHIA COLI; GENETICS; HT 29 CELL LINE; HUMAN; INTESTINE MUCOSA; METABOLISM; MICROBIOLOGY; MOLECULAR CLONING; MUCUS; PHYSIOLOGY; PROTEIN BINDING;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIFIDOBACTERIUM; CACO-2 CELLS; CELL MEMBRANE; CLONING, MOLECULAR; EPITHELIAL CELLS; ESCHERICHIA COLI; EXTRACELLULAR MATRIX PROTEINS; GENES, BACTERIAL; HT29 CELLS; HUMANS; INTESTINAL MUCOSA; LIPOPROTEINS; MEMBRANE PROTEINS; MUCUS; PROBIOTICS; PROTEIN BINDING; RECOMBINANT PROTEINS;

EID: 84886689846     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01993-13     Document Type: Article

References (46)

1. Ashida H, Ogawa M, Kim M, Mimuro H, Sasakawa C. 2012. Bacteria and host interactions in the gut epithelial barrier. Nat. Chem. Biol. 8:36-45.
2. Lebeer S, Vanderleyden J, De Keersmaecker SC. 2010. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8:171-184.
3. Kankainen M, Paulin L, Tynkkynen S, von Ossowski I, Reunanen J, Partanen P, Satokari R, Vesterlund S, Hendrickx AP, Lebeer S, De Keersmaecker SC, Vanderleyden J, Hamalainen T, Laukkanen S, Salovuori N, Ritari J, Alatalo E, Korpela R, Mattila-Sandholm T, Lassig A, Hatakka K, Kinnunen KT, Karjalainen H, Saxelin M, Laakso K, Surakka A, Palva A, Salusjarvi T, Auvinen P, de Vos WM. 2009. Comparative genomic analysis of Lactobacillus rhamnosus GG reveals pili containing a human-mucus binding protein. Proc. Natl. Acad. Sci. U. S. A. 106:17193- 17198.
4. Ewaschuk JB, Diaz H, Meddings L, Diederichs B, Dmytrash A, Backer J, Looijer van Langen M, Madsen KL. 2008. Secreted bioactive factors from Bifidobacterium infantis enhance epithelial cell barrier function. Am. J. Physiol. Gastrointest. Liver Physiol. 295:G1025-G1034.
5. Maynard CL, Elson CO, Hatton RD, Weaver CT. 2012. Reciprocal interactions of the intestinal microbiota and immune system. Nature 489: 231-241.
6. Harmsen HJ, Wildeboer-Veloo AC, Raangs GC, Wagendorp AA, Klijn N, Bindels JG, Welling GW. 2000. Analysis of intestinal flora development in breast-fed and formula-fed infants by using molecular identification and detection methods. J. Pediatr. Gastroenterol. Nutr. 30:61-67.
7. Nylund L, Satokari R, Nikkila J, Rajilic-Stojanovic M, Kalliomaki M, Isolauri E, Salminen S, de Vos WM. 2013. Microarray analysis reveals marked intestinal microbiota aberrancy in infants having eczema compared to healthy children in at-risk for atopic disease. BMC Microbiol. 13:12. doi:10.1186/1471-2180-13-12.
8. Qin J, Li R, Raes J, Arumugam M, Burgdorf KS, Manichanh C, Nielsen T, Pons N, Levenez F, Yamada T, Mende DR, Li J, Xu J, Li S, Li D, Cao J, Wang B, Liang H, Zheng H, Xie Y, Tap J, Lepage P, Bertalan M, Batto JM, Hansen T, Le Paslier D, Linneberg A, Nielsen HB, Pelletier E, Renault P, Sicheritz-Ponten T, Turner K, Zhu H, Yu C, Li S, Jian M, Zhou Y, Li Y, Zhang X, Li S, Qin N, Yang H, Wang J, Brunak S, Dore J, Guarner F, Kristiansen K, Pedersen O, Parkhill J, Weissenbach J, MetaHIT Consortium, Bork P, Ehrlich SD, Wang J. 2010. A human gut microbial gene catalogue established by metagenomic sequencing. Nature 464:59-65.
9. Guglielmetti S, Tamagnini I, Mora D, Minuzzo M, Scarafoni A, Arioli S, Hellman J, Karp M, Parini C. 2008. Implication of an outer surface lipoprotein in adhesion of Bifidobacterium bifidum to Caco-2 cells. Appl. Environ. Microbiol. 74:4695-4702.
10. Gonzalez-Rodriguez I, Sanchez B, Ruiz L, Turroni F, Ventura M, Ruas-Madiedo P, Gueimonde M, Margolles A. 2012. Role of extracellular transaldolase from Bifidobacterium bifidum in mucin adhesion and aggregation. Appl. Environ. Microbiol. 78:3992-3998.
11. O'Connell Motherway M, Zomer A, Leahy SC, Reunanen J, Bottacini F, Claesson MJ, O'Brien F, Flynn K, Casey PG, Munoz JA, Kearney B, Houston AM, O'Mahony C, Higgins DG, Shanahan F, Palva A, de Vos WM, Fitzgerald GF, Ventura M, O'Toole PW, van Sinderen D. 2011. Functional genome analysis of Bifidobacterium breve UCC2003 reveals type IVb tight adherence (Tad) pili as an essential and conserved hostcolonization factor. Proc. Natl. Acad. Sci. U. S. A. 108:11217-11222.
12. Candela M, Bergmann S, Vici M, Vitali B, Turroni S, Eikmanns BJ, Hammerschmidt S, Brigidi P. 2007. Binding of human plasminogen to Bifidobacterium. J. Bacteriol. 189:5929-5936.
13. Candela M, Biagi E, Centanni M, Turroni S, Vici M, Musiani F, Vitali B, Bergmann S, Hammerschmidt S, Brigidi P. 2009. Bifidobacterial enolase, a cell surface receptor for human plasminogen involved in the interaction with the host. Microbiology 155:3294-3303.
14. Candela M, Centanni M, Fiori J, Biagi E, Turroni S, Orrico C, Bergmann S, Hammerschmidt S, Brigidi P. 2010. DnaK from Bifidobacterium animalis subsp. lactis is a surface-exposed human plasminogen receptor upregulated in response to bile salts. Microbiology 156:1609-1618.
15. Foroni E, Serafini F, Amidani D, Turroni F, He F, Bottacini F, O'Connell Motherway M, Viappiani A, Zhang Z, Rivetti C, van Sinderen D, Ventura M. 2011. Genetic analysis and morphological identification of pilus-like structures in members of the genus Bifidobacterium. Microb. Cell Fact. 10(Suppl 1):S16. doi:10.1186/1475-2859-10-S1-S16.
16. Turroni F, Serafini F, Foroni E, Duranti S, O'Connell Motherway M, Taverniti V, Mangifesta M, Milani C, Viappini A, Roversi T, Sánchez B, Santoni A, Gioiosa L, Ferrarini A, Delledonne M, Margolles A, Paizza L, Planza P, Bolchi A, Guglielmetti S, van Sinderen D, Ventura M. 2013. Role of sortase-dependent pili of Bifidobacterium bifidum PRL2010 in modulating bacterium-host interactions. Proc. Natl. Acad. Sci. U. S. A. 110:11151-11156.
17. Gleinser M, Grimm V, Zhurina D, Yuan J, Riedel CU. 2012. Improved adhesive properties of recombinant bifidobacteria expressing the Bifidobacterium bifidum-specific lipoprotein BopA. Microb. Cell. Fact. 11:80.
18. Johnston BA, Eisen H, Fry D. 1991. An evaluation of several adjuvant emulsion regimens for the production of polyclonal antisera in rabbits. Lab. Anim. Sci. 41:15-21.
19. Harlow E, Lane D (ed). 1988. Antibodies: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
20. Reunanen J, von Ossowski I, Hendrickx AP, Palva A, de Vos WM. 2012. Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Appl. Environ. Microbiol. 78:2337-2344.
21. Kainulainen V, Loimaranta V, Pekkala A, Edelman S, Antikainen J, Kylvaja R, Laaksonen M, Laakkonen L, Finne J, Korhonen TK. 2012. Glutamine synthetase and glucose-6-phosphate isomerase are adhesive moonlighting proteins of Lactobacillus crispatus released by epithelial cathelicidin LL-37. J. Bacteriol. 194:2509-2519.
22. Vesterlund S, Paltta J, Karp M, Ouwehand AC. 2005. Measurement of bacterial adhesion-in vitro evaluation of different methods. J. Microbiol. Methods 60:225-233.
23. Antikainen J, Kuparinen V, Lahteenmaki K, Korhonen TK. 2007. Enolases from Gram-positive bacterial pathogens and commensal lactobacilli share functional similarity in virulence-associated traits. FEMS Immunol. Med. Microbiol. 51:526-534.
24. Isolauri E, Rautava S, Salminen S. 2012. Probiotics in the development and treatment of allergic disease. Gastroenterol. Clin. North Am. 41:747- 762.
25. Rautava S, Luoto R, Salminen S, Isolauri E. 2012. Microbial contact during pregnancy, intestinal colonization and human disease. Nat. Rev. Gastroenterol. Hepatol. 9:565-576.
26. Jalanka-Tuovinen J, Salonen A, Nikkila J, Immonen O, Kekkonen R, Lahti L, Palva A, de Vos WM. 2011. Intestinal microbiota in healthy adults: temporal analysis reveals individual and common core and relation to intestinal symptoms. PLoS One 6:e23035. doi:10.1371/journal .pone.0023035.
27. Johansson ME, Sjovall H, Hansson GC. 2013. The gastrointestinal mucus system in health and disease. Nat. Rev. Gastroenterol. Hepatol. 10: 352-361.
28. Buist G, Ridder AN, Kok J, Kuipers OP. 2006. Different subcellular locations of secretome components of Gram-positive bacteria. Microbiology 152:2867-2874.
29. Lybarger SR, Maddock JR. 2001. Polarity in action: asymmetric protein localization in bacteria. J. Bacteriol. 183:3261-3267.
30. Garcia-Lorenzo A, Rodriguez-Pineiro AM, Rodriguez-Berrocal FJ, Cadena MP, Martinez-Zorzano VS. 2012. Changes on the Caco-2 secretome through differentiation analyzed by 2-D differential in-gel electrophoresis (DIGE). Int. J. Mol. Sci. 13:14401-14420.
31. Sambuy Y, De Angelis I, Ranaldi G, Scarino ML, Stammati A, Zucco F. 2005. The Caco-2 cell line as a model of the intestinal barrier: influence of cell and culture-related factors on Caco-2 cell functional characteristics. Cell Biol. Toxicol. 21:1-26.
32. Coconnier MH, Bernet MF, Kerneis S, Chauviere G, Fourniat J, Servin AL. 1993. Inhibition of adhesion of enteroinvasive pathogens to human intestinal Caco-2 cells by Lactobacillus acidophilus strain LB decreases bacterial invasion. FEMS Microbiol. Lett. 110:299-305.
33. Hynonen U, Palva A. 2013. Lactobacillus surface layer proteins: structure, function and applications. Appl. Microbiol. Biotechnol. 97:5225-5243.
34. Ren D, Li C, Qin Y, Yin R, Li X, Tian M, Du S, Guo H, Liu C, Zhu N, Sun D, Li Y, Jin N. 2012. Inhibition of Staphylococcus aureus adherence to Caco-2 cells by lactobacilli and cell surface properties that influence attachment. Anaerobe 18:508-515.
35. Xu H, Jeong HS, Lee HY, Ahn J. 2009. Assessment of cell surface properties and adhesion potential of selected probiotic strains. Lett. Appl. Microbiol. 49:434-442.
36. Juge N. 2012. Microbial adhesins to gastrointestinal mucus. Trends Microbiol. 20:30-39.
37. Kim YS, Ho SB. 2010. Intestinal goblet cells and mucins in health and disease: recent insights and progress. Curr. Gastroenterol. Rep. 12:319- 330.
38. Van Tassell ML, Miller MJ. 2011. Lactobacillus adhesion to mucus. Nutrients 3:613-636.
39. Guglielmetti S, Tamagnini I, Minuzzo M, Arioli S, Parini C, Comelli E, Mora D. 2009. Study of the adhesion of Bifidobacterium bifidum MIMBb75 to human intestinal cell lines. Curr. Microbiol. 59:167-172.
40. Macias-Rodriguez ME, Zagorec M, Ascencio F, Vazquez-Juarez R, Rojas M. 2009. Lactobacillus fermentum BCS87 expresses mucus- and mucin-binding proteins on the cell surface. J. Appl. Microbiol. 107:1866- 1874.
41. Roos S, Aleljung P, Robert N, Lee B, Wadström T, Lindberg M, Jonsson H. 1996. A collagen binding protein from Lactobacillus reuteri is part of an ABC transporter system? FEMS Microbiol. Lett. 144:33-38.
42. Watanabe M, Kinoshita H, Nitta M, Yukishita R, Kawai Y, Kimura K, Taketomo N, Yamazaki Y, Tateno Y, Miura K, Horii A, Kitazawa H, Saito T. 2010. Identification of a new adhesin-like protein from Lactobacillus mucosae ME-340 with specific affinity to the human blood group A and B antigens. J. Appl. Microbiol. 109:927-935.
43. Watanabe M, Kinoshita H, Huang IN, Eguchi K, Tsurumi T, Kawai Y, Kitazawa H, Kimura K, Taketomo N, Kikuchi D, Sase T, Miura K, Ogawa H, Shibata C, Horii A, Saito T. 2012. An adhesin-like protein, Lam29, from Lactobacillus mucosae ME-340 binds to histone H3 and blood group antigens in human colonic mucus. Biosci. Biotechnol. Biochem. 76:1655-1660.
44. Chagnot C, Listrat A, Astruc T, Desvaux M. 2012. Bacterial adhesion to animal tissues: protein determinants for recognition of extracellular matrix components. Cell. Microbiol. 14:1687-1696.
45. Patti JM, Hook M. 1994. Microbial adhesins recognizing extracellular matrix macromolecules. Curr. Opin. Cell Biol. 6:752-758.
46. Kolachala VL, Bajaj R, Wang L, Yan Y, Ritzenthaler JD, Gewirtz AT, Roman J, Merlin D, Sitaraman SV. 2007. Epithelial-derived fibronectin expression, signaling, and function in intestinal inflammation. J. Biol. Chem. 282:32965-32973.