The lectin-like protein 1 in Lactobacillus rhamnosus GR-1 mediates tissue-specific adherence to vaginal epithelium and inhibits urogenital pathogens

Scientific Reports

Volumn 6, Issue , 2016, Pages

  Petrova, Mariya I ^a,b   Lievens, Elke ^a,b   Verhoeven, Tine L A ^a   MacKlaim, Jean M ^c,d   Gloor, Gregory ^d   Schols, Dominique ^e   Vanderleyden, Jos ^a   Reid, Gregor ^c,d   Lebeer, Sarah ^a,b  

^a UNIVERSITY OF LEUVEN   (Belgium)

^b UNIVERSITY OF ANTWERP   (Belgium)

^c LAWSON HEALTH RESEARCH INSTITUTE   (Canada)

^d UNIVERSITY OF WESTERN ONTARIO   (Canada)

^e REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; CARBOHYDRATE; CHEMOKINE; LECTIN; MANNOSE;

BACTERIUM ADHERENCE; BIOFILM; CHEMISTRY; DRUG EFFECT; EPITHELIUM; ESCHERICHIA COLI; FEMALE; GENETICS; GROWTH, DEVELOPMENT AND AGING; HUMAN; IMMUNITY; LACTOBACILLUS RHAMNOSUS; METABOLISM; MICROBIOLOGY; MOLECULAR GENETICS; PATHOLOGY; PHYSIOLOGY; STAPHYLOCOCCUS AUREUS; VAGINA;

BACTERIAL ADHESION; BACTERIAL PROTEINS; BIOFILMS; CARBOHYDRATES; CHEMOKINES; EPITHELIUM; ESCHERICHIA COLI; FEMALE; HUMANS; IMMUNITY; LACTOBACILLUS RHAMNOSUS; LECTINS; MANNOSE; MOLECULAR SEQUENCE ANNOTATION; STAPHYLOCOCCUS AUREUS; VAGINA;

EID: 84995890307     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep37437     Document Type: Article

References (63)

1. WHO/FAO. Evaluation of health and nutritional properties of powder milk and live lactic acid bacteria. Food and Agriculture Organization of the United Nations and World Health Organization Expert Consultation Report. (2001).
2. Reid, G. & Bruce, A. W. Selection of lactobacillus strains for urogenital probiotic applications. J. Infect Dis., 183, S77-S80 (2001).
3. Gardiner, G. E., Heinemann, C., Bruce, A. W., Beuerman, D. & Reid, G. Persistence of Lactobacillus fermentum RC-14 and Lactobacillus rhamnosus GR-1 but not L. rhamnosus GG in the human vagina as demonstrated by randomly amplified polymorphic DNA. Clin. Diagn. Lab Immunol. 9, 92-96 (2002).
4. Reid, G. et al. Oral use of Lactobacillus rhamnosus GR-1 and L. fermentum RC-14 significantly alters vaginal flora: randomized, placebo-controlled trial in 64 healthy women. FEMS Immunol. Med. Microbiol. 20(35), 131-134 (2003).
5. Reid, G. et al. Oral probiotics can resolve urogenital infections. FEMS Immunol. Med. Microbiol. 30, 49-52 (2001).
6. McGroarty, J. A. & Reid, G. Detection of a Lactobacillus substance that inhibits Escherichia coli. Can. J. Microbiol. 34, 974-978 (1988).
7. Reid, G., McGroarty, J. A., Angotti, R. & Cook, R. L. Lactobacillus inhibitor production against Escherichia coli and coaggregation ability with uropathogens. Can. J. Microbiol. 34, 344-351 (1988).
8. McGroarty, J. A. & Reid, G. Inhibition of Enterococci by Lactobacillus species in vitro. Microbial Ecology in Health and Disease 1, 215-219 (1988).
9. McMillan, A. et al. Disruption of urogenital biofilms by lactobacilli. Colloids Surf. B Biointerfaces. 86, 58-64 (2011).
10. Kohler, G. A., Assefa, S. & Reid, G. Probiotic interference of Lactobacillus rhamnosus GR-1 and Lactobacillus reuteri RC-14 with the opportunistic fungal pathogen Candida albicans. Infect Dis Obstet. Gynecol. 2012, doi: 10.1155/2012/636474. (2012).
11. Lebeer, S., Vanderleyden, J. & De Keersmaecker, S. C. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Nat. Rev. Microbiol. 8, 171-184 (2010).
12. Van Damme, E. J., Broekaert, W. F. & Peumans, W. J. The Urtica dioica agglutinin is a complex mixture of isolectins. Plant Physiol. 86: 598-601. (1988).
13. Van Damme, E. J. M., Allen, A. K. & Peumans, W. J. Related mannose-specific lectins from different species of the family Amaryllidaceae. Plant Physiol. 73, 52-57 (1988).
14. Wellens, A. et al. The tyrosine gate as a potential entropic lever in the receptor-binding site of the bacterial adhesin FimH. Biochemistry. 19(51), 4790-4799 (2012).
15. Clarke, S. R., Harris, L. G., Richards, R. G. & Foster, S. J. Analysis of Ebh, a 1.1-megadalton cell wall-associated fibronectin-binding protein of Staphylococcus aureus. Infect. Immun. 70, 6680-6687 (2002).
16. Marraffini, L. A., Dedent, A. C. & Schneewind, O. Sortases and the art of anchoring proteins to the envelopes of gram-positive bacteria. Microbiol. Mol. Biol. Rev. 70, 192-220 (2006).
17. Alvarez, M. A., Herrero, M. & Suarez, J. E. The site-specific recombination system of the Lactobacillus species bacteriophage A2 integrates in gram-positive and gram-negative bacteria. Virology. 250, 185-193 (1998).
18. Josson, K. et al. Characterization of a gram-positive broad-host-range plasmid isolated from Lactobacillus hilgardii. Plasmid. 21, 9-20 (1989).
19. De Keersmaecker, S. C. et al. Flow cytometric testing of green fluorescent protein-tagged Lactobacillus rhamnosus GG for response to defensins. Appl. Environ. Microbiol. 72, 4923-4930 (2006).
20. Petrova, M. I., van den, B. M., Balzarini, J., Vanderleyden, J. & Lebeer, S. Vaginal microbiota and its role in HIV transmission and infection. FEMS Microbiol Rev. 37, 762-792 (2013).
21. Petrova, M. I., Lievens, E., Malik, S., Imholz, N. & Lebeer, S. Lactobacillus species as biomarkers and agents that can promote various aspects of vaginal health. Front Physiol. 6, 81 (2015).
22. Arndt, N. X., Tiralongo, J., Madge, P. D., von, I. M. & Day, C. J. Differential carbohydrate binding and cell surface glycosylation of human cancer cell lines. J. Cell Biochem. 112, 2230-2240 (2011).
23. Rajan, N. et al. Roles of glycoproteins and oligosaccharides found in human vaginal fluid in bacterial adherence. Infect Immun. 67, 5027-5032 (1999).
24. Venegas, M. F. et al. Binding of type 1-piliated Escherichia coli to vaginal mucus. Infect Immun. 63, 416-422 (1995).
25. Van Damme, E. J., Smith, D. F., Cummings, R. & Peumans, W. J. Glycan arrays to decipher the specificity of plant lectins. Adv. Exp. Med. Biol. 705, 757-767 (2011).
26. Navas, E. L. et al. Blood group antigen expression on vaginal cells and mucus in women with and without a history of urinary tract infections. J. Urol. 152, 345-349 (1994).
27. Corfield, A. P. & Berry, M. Glycan variation and evolution in the eukaryotes. Trends Biochem. Sci. 40, 351-359 (2015).
28. Tytgat, H. L. & Lebeer, S. The sweet tooth of bacteria: common themes in bacterial glycoconjugates. Microbiol. Mol. Biol. Rev. 78, 372-417 (2014).
29. Topin, J. et al. Deciphering the glycan preference of bacterial lectins by glycan array and molecular docking with validation by microcalorimetry and crystallography. PLoS. One. 8, e71149 (2013).
30. Lebeer, S., Vanderleyden, J. & De Keersmaecker, S. C. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 72, 728-764 (2008).
31. Pietrella, D. et al. Th17 cells and IL-17 in protective immunity to vaginal candidiasis. PLoS. One. 6, e22770 (2011).
32. Introini, A., Vanpouille, C., Lisco, A., Grivel, J. C. & Margolis, L. Interleukin-7 facilitates HIV-1 transmission to cervico-vaginal tissue ex vivo. PLoS. Pathog. 9, e1003148 (2013).
33. Steenackers, H., Hermans, K., Vanderleyden, J. & De Keersmaecker, S. C. J. Salmonella biofilms: An overview on occurrence, structure, regulation and eradication. Food Research Internationa 45, 502-531 (2012).
34. Van, H. R. & Michiels, C. W. Role of bacterial cell surface structures in Escherichia coli biofilm formation. Res. Microbiol. 156, 626-633 (2005).
35. Berendonk, T. U. et al. Tackling antibiotic resistance: the environmental framework. Nat. Rev. Microbiol. 13, 310-317 (2015).
36. de Man, J. C., Rogosa, M. & Sharpe, M. E. A medium for the cultivation of lactobacilli. J. Appl. Bacteriol. 23, 130-135 (1960).
37. Sambrook, J., Fritsch, E. F. & Maniatis, T. Molecular cloning: a laboratory manual. (eds Sambrook, J. & Russell, D. W.) (1989).
38. Petrova, M. I. et al. Inhibition of infection and transmission of HIV-1 and lack of significant impact on the vaginal commensal lactobacilli by carbohydrate-binding agents. J Antimicrob. Chemother. 68, 2026-2037 (2013).
39. Lebeer, S. et al. Functional analysis of Lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Appl. Environ. Microbiol. 78, 185-193 (2012).
40. Lebeer, S. et al. Functional analysis of luxS in the probiotic strain Lactobacillus rhamnosus GG reveals a central metabolic role important for growth and biofilm formation. J. Bacteriol. 189, 860-871 (2007).
41. Danielsen, M. Characterization of the tetracycline resistance plasmid pMD5057 from Lactobacillus plantarum 5057 reveals a composite structure. Plasmid. 48, 98-103 (2002).
42. Pretzer, G. et al. Biodiversity-based identification and functional characterization of the mannose-specific adhesin of Lactobacillus plantarum. J. Bacteriol. 187, 6128-6136 (2005).
43. Cash, H. L., Whitham, C. V., Behrendt, C. L. & Hooper, L. V. Symbiotic bacteria direct expression of an intestinal bactericidal lectin. Science 313, 1126-1130 (2006).
44. Fornstedt, N. & Porath, J. Characterization studies on a new lectin found in seeds of Vicia ervilia. FEBS Lett. 57, 187-191 (1975).
45. Lebeer, S. et al. 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. 75, 3554-3563 (2009).
46. Petrova, M. I. et al. Inhibition of infection and transmission of HIV-1 and lack of significant impact on the vaginal commensal lactobacilli by carbohydrate-binding agents. J. Antimicrob. Chemother, doi: 10.1093/jac/dkt152 (2013).
47. Yang, Y. H. et al. Structural insights into SraP-mediated Staphylococcus aureus adhesion to host cells. PLoS. Pathog. 10, e1004169 (2014).
48. Hoorelbeke, B. et al. Actinohivin, a broadly neutralizing prokaryotic lectin, inhibits HIV-1 infection by specifically targeting highmannose-type glycans on the gp120 envelope. Antimicrob. Agents Chemother. 54, 3287-3301 (2010).
49. Kouokam, J. C. et al. Investigation of griffithsin's interactions with human cells confirms its outstanding safety and efficacy profile as a microbicide candidate. PLoS. One. 6, e22635 (2011).
50. Schouppe, D. et al. Interaction of the tobacco lectin with histone proteins. Plant Physiol. 155, 1091-1102 (2011).
51. Lee, R. T., Gabius, H. J. & Lee, Y. C. Thermodynamic parameters of the interaction of Urtica dioica agglutinin with N-acetylglucosamine and its oligomers. Glycoconj. J. 15, 649-655 (1998).
52. Steenackers, H. P. et al. Structure-activity relationship of 4(5)-aryl-2-amino-1H-imidazoles, N1-substituted 2-aminoimidazoles and imidazo[1,2-a]pyrimidinium salts as inhibitors of biofilm formation by Salmonella typhimurium and Pseudomonas aeruginosa. J. Med. Chem. 54, 472-484 (2011).
53. Brinster, S., Furlan, S. & Serror, P. C-terminal WxL domain mediates cell wall binding in Enterococcus faecalis and other grampositive bacteria. J. Bacteriol. 189, 1244-1253 (2007).
54. Siezen, R. et al. Lactobacillus plantarum gene clusters encoding putative cell-surface protein complexes for carbohydrate utilization are conserved in specific gram-positive bacteria. BMC. Genomics. 7(126), 126 (2006).
55. Hunstad, D. A., Justice, S. S., Hung, C. S., Lauer, S. R. & Hultgren, S. J. Suppression of bladder epithelial cytokine responses by uropathogenic Escherichia coli. Infect. Immun. 73, 3999-4006 (2005).
56. Reid, G. The scientific basis for probiotic strains of Lactobacillus. Appl. Environ. Microbiol. 65, 3763-3766 (1999).
57. Moore, W. E., Hash, D. E., Holdeman, L. V. & Cato, E. P. Polyacrylamide slab gel electrophoresis of soluble proteins for studies of bacterial floras. Appl. Environ. Microbiol. 39, 900-907 (1980).
58. Gasser, F., Mandel, M. & ROGOSA, M. Lactobacillus jensenii sp.nov., a new representative of the subgenus Thermobacterium. J. Gen. Microbiol. 62, 219-222 (1970).
59. Malik, S. et al. Draft Genome Sequence of Lactobacillus plantarum CMPG5300, a Human Vaginal Isolate. Genome Announc. 2, e01149-14 (2014).
60. Brachmann, C. B. et al. Designer deletion strains derived from Saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications. Yeast 14, 115-132 (1998).
61. Gillum, A. M., Tsay, E. Y. & Kirsch, D. R. Isolation of the Candida albicans gene for orotidine-5'-phosphate decarboxylase by complementation of S. cerevisiae ura3 and E. coli pyrF mutations. Mol. Gen. Genet. 198, 179-182 (1984).
62. Horsburgh, M. J. et al. sigmaB modulates virulence determinant expression and stress resistance: characterization of a functional rsbU strain derived from Staphylococcus aureus 8325-4. J. Bacteriol. 184, 5457-5467 (2002).
63. Malik S. et al. The strong auto-aggregative and adhesive phenotype of a vaginal Lactobacillus plantarum strain CMPG 5300 is sortase-dependent. Appl. Environ. Microbiol., doi: 10.1128/AEM.00926-13 (2013).