Improving gastric transit, gastrointestinal persistence and therapeutic efficacy of the probiotic strain UCC2003 Free

Abstract

Given the increasing commercial and clinical relevance of probiotic cultures, improving their stress tolerance profile and ability to overcome the physiological defences of the host is an important biological goal. In order to reach the gastrointestinal tract in sufficient numbers to exert a therapeutic effect, probiotic bacteria must resist the deleterious actions of low pH, elevated osmolarity and bile salts. Cloning the listerial betaine uptake system, BetL, into the probiotic strain UCC2003 significantly improved probiotic tolerance to gastric juice and conditions of elevated osmolarity mimicking the gut environment. Furthermore, whilst stable colonization of the murine intestine was achieved by oral administration of UCC2003, strains harbouring BetL were recovered at significantly higher levels in the faeces, intestines and caecum of inoculated animals. Finally, in addition to improved gastric transit and intestinal persistence, this approach improved the clinical efficacy of the probiotic culture: mice fed UCC2003-BetL exhibited significantly lower levels of systemic infection compared to the control strain following oral inoculation with .

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2007-10-01
2024-03-28
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References

  1. Abee T., Wouters J. A. 1999; Microbial stress response in minimal processing. Int J Food Microbiol 50:65–91
    [Google Scholar]
  2. Asahara T., Nomoto K., Shimizu K., Watanuki M., Tanaka R. 2001; Increased resistance of mice to Salmonella enterica serovar Typhimurium infection by synbiotic administration of bifidobacteria and transgalactosylated oligosaccharides. J Appl Microbiol 91:985–996
    [Google Scholar]
  3. Asahara T., Shimizu K., Nomoto K., Hamabata T., Ozawa A., Takeda Y. 2004; Probiotic bifidobacteria protect mice from lethal infection with shiga toxin-producing Escherichia coli O157 : H7. Infect Immun 72:2240–2247
    [Google Scholar]
  4. Charteris W. P., Kelly P. M., Morelli L., Collins J. K. 1998; Development and application of an in vitro methodology to determine the transit tolerance of potentially probiotic Lactobacillus and Bifidobacterium species in the upper human gastrointestinal tract. J Appl Microbiol 84:759–768
    [Google Scholar]
  5. Coakley M., Ross R. P., Nordgren M., Fitzgerald G., Devery R., Stanton C. 2003; Conjugated linoleic acid biosynthesis by human-derived Bifidobacterium species. J Appl Microbiol 94:138–145
    [Google Scholar]
  6. De Boever P., Verstraete W. 1999; Bile salt deconjugation by Lactobacillus plantarum 80 and its implications for bacterial toxicity. J Appl Microbiol 87:345–352
    [Google Scholar]
  7. De Ruyter P. G., Kuipers O. P., de Vos W. M. 1996; Controlled gene expression systems for Lactococcus lactis with the food-grade inducer nisin. Appl Environ Microbiol 62:3662–3667
    [Google Scholar]
  8. Dunne C., O'Mahony L., Murphy L., Thorton G., Morrissey D., O'Halloran S., Feeney M., Flynn S., Fitzgerald G. other authors 2001; In vitro selection criteria for probiotic bacteria of human origin: correlation with in vivo findings. Am J Clin Nutr 73:386S–392S
    [Google Scholar]
  9. Fujiwara S., Seto Y., Kimura A., Hashiba H. 2001; Intestinal transit of an orally administered streptomycin-rifampicin-resistant variant of Bifidobacterium longum SBT2928: its long-term survival and effect on the intestinal microflora and metabolism. J Appl Microbiol 90:43–52
    [Google Scholar]
  10. Gagnon M., Kheadr E. E., Dabour N., Richard D., Fliss I. 2006; Effect of Bifidobacterium thermacidophilum probiotic feeding on enterohemorrhagic Escherichia coli O157 : H7 infection in BALB/c mice. Int J Food Microbiol 111:26–33
    [Google Scholar]
  11. Greenwald D. A. 2004; Aging, the gastrointestinal tract, and risk of acid-related disease. Am J Med 117:Suppl 5A8S–13S
    [Google Scholar]
  12. Gupta S., Chowdhury R. 1997; Bile affects production of virulence factors and motility of Vibrio cholerae . Infect Immun 65:1131–1134
    [Google Scholar]
  13. Hébuterne X. 2003; Gut changes attributed to ageing: effects on intestinal microflora. Curr Opin Clin Nutr Metab Care 6:49–54
    [Google Scholar]
  14. Hill C., Cotter P. D., Sleator R. D., Gahan C. G. M. 2002; Bacterial stress response in Listeria monocytogenes : jumping the hurdles imposed by minimal processing. Int Dairy J 12:273–283
    [Google Scholar]
  15. Kempf B., Bremer E. 1995; OpuA, an osmotically regulated binding protein-dependent transport system for the osmoprotectant glycine betaine in Bacillus subtilis . J Biol Chem 270:16701–16713
    [Google Scholar]
  16. Kongo J. M., Gomes A. M. P., Malcata F. X. 2003; Development of a chemically defined medium for growth of Bifidobacterium animalis . J Food Sci 68:2742–2746
    [Google Scholar]
  17. Leahy S. C., Higgins D. G., Fitzgerald G. F., van Sinderen D. 2005; Getting better with bifidobacteria. J Appl Microbiol 98:1303–1315
    [Google Scholar]
  18. Lievin V., Peiffer I., Hudault S., Rochat F., Brassart D., Neeser J. R., Servin A. L. 2000; Bifidobacterium strains from resident infant human gastrointestinal microflora exert antimicrobial activity. Gut 47:646–652
    [Google Scholar]
  19. MacConaill L. E., Fitzgerald G. F., van Sinderen D. 2003; Investigation of protein export in Bifidobacterium breve UCC2003. Appl Environ Microbiol 69:6994–7001
    [Google Scholar]
  20. Maniatis T., Fritsch E. F., Sambrook J. 1982 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  21. Marco M. L., Pavan S., Kleerebezem M. 2006; Towards understanding molecular modes of probiotic action. Curr Opin Biotechnol 17:204–210
    [Google Scholar]
  22. Picard C., Fioramonti J., Francois A., Robinson T., Neant F., Matuchansky C. 2005; Review article: bifidobacteria as probiotic agents – physiological effects and clinical benefits. Aliment Pharmacol Ther 22:495–512
    [Google Scholar]
  23. Pilotto A. 2004; Aging and upper gastrointestinal disorders. Best Pract Res Clin Gastroenterol 18:73–81
    [Google Scholar]
  24. Ripio M.-T., Vázquez-Boland J.-A., Vega Y., Nair S., Berche P. 1998; Evidence for expressional crosstalk between the central virulence regulator PrfA and the stress response mediator ClpC in Listeria monocytogenes . FEMS Microbiol Lett 158:45–50
    [Google Scholar]
  25. Saarela M., Virkajärvi I., Alakomi H.-L., Mattila-Sandholm T., Vaari A., Suomalainen T., Mättö J. 2005; Influence of fermentation time, cryoprotectant and neutralization of cell concentrate on freeze-drying survival, storage stability and acid and bile exposure of Bifidobacterium animalis ssp. lactis cells produced without milk-based ingredient. J Appl Microbiol 99:1330–1339
    [Google Scholar]
  26. Servin A. L. 2004; Antagonistic activities of lactobacilli and bifidobacteria against microbial pathogens. FEMS Microbiol Rev 28:405–440
    [Google Scholar]
  27. Sheehan V. M., Sleator R. D., Fitzgerald G. F., Hill C. 2006; Heterologous expression of BetL, a betaine uptake system, enhances the stress tolerance of Lactobacillus salivarius UCC118. Appl Environ Microbiol 72:2170–2177
    [Google Scholar]
  28. Silva A. M., Bambirra E. A., Oliveira A. L., Souza P. P., Gomes D. A., Vieira E. C., Nicoli J. R. 1999; Protective effect of bifidus milk on the experimental infection with Salmonella enteritidis subsp. typhimurium in conventional and gnotobiotic mice. J Appl Microbiol 86:331–336
    [Google Scholar]
  29. Sleator R. D., Hill C. 2002; Bacterial osmoadaptation: the role of osmolytes in bacterial stress and virulence. FEMS Microbiol Rev 26:49–71
    [Google Scholar]
  30. Sleator R. D., Hill C. 2005; A novel role for the LisRK two-component regulatory system in listerial osmotolerance. Clin Microbiol Infect 11:599–601
    [Google Scholar]
  31. Sleator R. D., Hill C. 2006; Patho-biotechnology; using bad bugs to do good things. Curr Opin Biotechnol 17:211–226
    [Google Scholar]
  32. Sleator R. D., Hill C. 2007a; Probiotics as therapeutics for the developing world. J Infect Develop Countries in press
    [Google Scholar]
  33. Sleator R. D., Hill C. 2007b; Patho-biotechnology; using bad bugs to make good bugs better. Sci Prog 90:1–14
    [Google Scholar]
  34. Sleator R. D., Hill C. 2007c; ‘Bioengineered bugs’ – a patho-biotechnology approach to probiotic research and applications. Med Hypotheses
    [Google Scholar]
  35. Sleator R. D., Hill C. 2007d; Gut osmolarity: a key environmental cue initiating the gastrointestinal phase of Listeria monocytogenes infection?. Med Hypotheses doi: 10.1016/j.mehy.2007.03.008
    [Google Scholar]
  36. Sleator R. D., Gahan C. G. M., Abee T., Hill C. 1999; Identification and disruption of BetL, a secondary glycine betaine transport system linked to the salt tolerance of Listeria monocytogenes LO28. Appl Environ Microbiol 65:2078–2083
    [Google Scholar]
  37. Sleator R. D., Gahan C. G. M., O'Driscoll B., Hill C. 2000; Analysis of the role of betL in contributing to the growth and survival of Listeria monocytogenes LO28. Int J Food Microbiol 60:261–268
    [Google Scholar]
  38. Sleator R. D., Wouters J., Gahan C. G. M., Abee T., Hill C. 2001a; Analysis of the role of OpuC, an osmolyte transport system, in salt tolerance and virulence potential of Listeria monocytogenes . Appl Environ Microbiol 67:2692–2698
    [Google Scholar]
  39. Sleator R. D., Gahan C. G. M., Hill C. 2001b; Mutations in the listerial proB gene leading to proline overproduction: effects on salt tolerance and murine infection. Appl Environ Microbiol 67:4560–4565
    [Google Scholar]
  40. Sleator R. D., Francis G. A., O'Beirne D., Gahan C. G. M., Hill C. 2003a; Betaine and carnitine uptake systems in Listeria monocytogenes affect growth and survival in foods and during infection. J Appl Microbiol 95:839–846
    [Google Scholar]
  41. Sleator R. D., Gahan C. G. M., Hill C. 2003b; A postgenomic appraisal of osmotolerance in Listeria monocytogenes . Appl Environ Microbiol 69:1–9
    [Google Scholar]
  42. Sleator R. D., Wood J. M., Hill C. 2003c; Transcriptional regulation and posttranslational activity of the betaine transporter BetL in Listeria monocytogenes are controlled by environmental salinity. J Bacteriol 185:7140–7144
    [Google Scholar]
  43. Sleator R. D., Wemekamp-Kamphuis H. H., Gahan C. G. M., Abee T., Hill C. 2005; A PrfA-regulated bile exclusion system (BilE) is a novel virulence factor in Listeria monocytogenes . Mol Microbiol 55:1183–1195
    [Google Scholar]
  44. Termont S., Vandenbrouke K., Iserentant D., Neirynck S., Steidler L., Remaut E., Rottiers P. 2006; Intracellular accumulation of trehalose protects Lactococcus lactis from freeze-drying damage and bile toxicity and increases gastric acid resistance. Appl Environ Microbiol 72:7694–7700
    [Google Scholar]
  45. Tuomola E., Crittenden R., Playne M., Isolauri E., Salminen S. 2001; Quality assurance criteria for probiotic bacteria. Am J Clin Nutr 73:393S–398S
    [Google Scholar]
  46. Vaughan E. E., de Vries M. C., Zoetendal E. G., Ben-Amor K., Akkermans A. D., de Vos W. M. 2002; The intestinal LABs. Antonie Van Leeuwenhoek 82:341–352
    [Google Scholar]
  47. Ventura M., Canchaya C., Zink R., Fitzgerald G. F., van Sinderen D. 2004a; Characterization of the gro EL and gro ES loci in Bifidobacterium breve UCC 2003: genetic, transcriptional and phylogenetic analyses. Appl Environ Microbiol 70:6197–6209
    [Google Scholar]
  48. Ventura M., van Sinderen D., Fitzgerald G. F., Zink R. 2004b; Insights into the taxonomy, genetics and physiology of bifidobacteria. Antonie Van Leeuwenhoek 86:205–223
    [Google Scholar]
  49. Ventura M., Canchaya C., Bernini V., Del Casale A., Dellaglio F., Neviani E., Fitzgerald G. F., van Sinderen D. 2005a; Genetic characterization of the Bifidobacterium breve UCC 2003 hrc A locus. Appl Environ Microbiol 71:8998–9007
    [Google Scholar]
  50. Ventura M., Fitzgerald G. F., van Sinderen D. 2005b; Genetic and transcriptional organization of the clp C locus in Bifidobacterium breve UCC 2003. Appl Environ Microbiol 71:6282–6291
    [Google Scholar]
  51. Ventura M., Kenny J. G., Zhang Z., Fitzgerald G. F., van Sinderen D. 2005c; The clp B gene of Bifidobacterium breve UCC 2003: transcriptional analysis and first insights into stress induction. Microbiology 151:2861–2872
    [Google Scholar]
  52. Ventura M., Zhang Z., Cronin M., Canchaya C., Kenny J. G., Fitzgerald G. F., van Sinderen D. 2005d; The ClgR protein regulates transcription of the clp P operon in Bifidobacterium breve UCC 2003. J Bacteriol 187:8411–8426
    [Google Scholar]
  53. Ventura M., Zink R., Fitzgerald G. F., van Sinderen D. 2005e; Gene structure and transcriptional organization of the dnaK operon of Bifidobacterium breve UCC 2003 and application of the operon in bifidobacterial tracing. Appl Environ Microbiol 71:487–500
    [Google Scholar]
  54. Ventura M., Canchaya C., Zhang Z., Bernini V., Fitzgerald G. F., van Sinderen D. 2006; How high G+C Gram-positive bacteria and in particular bifidobacteria cope with heat stress: protein players and regulators. FEMS Microbiol Rev 30:734–759
    [Google Scholar]
  55. WHO 2002 Active ageing: a policy framework. A contribution of the World Health Organization to the Second United Nations world assembly on ageing Madrid, Spain: April 2002
    [Google Scholar]
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