Skip to main content

Advertisement

SpringerLink
Log in

Anti-inflammatory and immunomodulatory efficacy of indigenous probiotic Lactobacillus plantarum Lp91 in colitis mouse model

  • Published:
Molecular Biology Reports Aims and scope Submit manuscript

Abstract

Probiotics can affect the immune homeostasis by altering the gut microbial balance and enhancing the immune system of gut, thus benefits in Inflammatory Bowel Disease, including Crohn’s disease and Ulcerative colitis. Relative gene expression of pro, anti-inflammatory cytokines and other molecules in 2,4,6-trinitrobenzene sulfonic acid-induced colitis mouse model against Lactobacillus plantarum Lp91 (L. plantarum Lp91) was investigated by reverse transcription—quantitative PCR (RT-qPCR) using relative expression software tool (REST 2008 V2.0.7). L. plantarum Lp91 evoked significant down regulation of TNF-α and COX2 to 0.026 and 0.077 fold in colitis mouse model. No significant difference in expression of IL-12a cytokine in colitis mouse challenged with L. plantarum Lp91 was also observed. IL-10 was significantly up-regulated to 37.813 and 1.327 fold in colitis and non-colitis mouse challenged with L. plantarum Lp91. While, other anti-inflammatory markers i.e. COX1, IL-4 and IL-6 were significantly up regulated in colitis mouse challenged with L. plantarum Lp91. MUC2 gene was significantly up regulated to 2.216 fold in non-colitis group. L. plantarum Lp91, an indigenous probiotic culture, the main subject of this project exhibited strong immunemodulatory properties under in vivo conditions in mouse colitis model.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  1. Sheil B, Shanahan F, O’Mahony L (2007) Probiotic effects on inflammatory bowel disease. J Nutr 137:819S–824S

    PubMed  CAS  Google Scholar 

  2. Fedorak RN, Madsen KL (2004) Probiotics and the management of inflammatory bowel disease. Inflamm Bowel Dis 10:286–299

    Article  PubMed  Google Scholar 

  3. Schreiber S, Heinig T, Thiele HG et al (1995) Immunoregulatory role of interleukin 10 in patients with inflammatory bowel disease. Gastroenterology 108:1434–1444

    Article  PubMed  CAS  Google Scholar 

  4. Havenaar R, Ten Brink B, Huis Veld JHJ (1992) Selection of strains for probiotic use. In: Fuller R (ed) Probiotics: the scientific basis. Chapman and Hall, London, pp 209–224

    Google Scholar 

  5. McFarland L, Surawicz C, Greenberg R (1994) A randomised placebo-controlled trial of Saccharomyces boulardii in combination with standard antibiotics for Clostridium difficile disease. J Am Med Assoc 271:1913–1918

    Article  CAS  Google Scholar 

  6. Kruis W, Schutz E, Fric P et al (1997) Double-blind comparison of an oral Escherichia coli preparation and mesalazine in maintaining remission of ulcerative colitis. Aliment Pharmacol Ther 11:853–858

    Article  PubMed  CAS  Google Scholar 

  7. Foligne B, Zoumpopoulou G, Dewulf J et al (2007) A key role of dendritic cells in probiotic functionality. PLoS ONE 2:e313

    Article  PubMed  Google Scholar 

  8. Madsen KL, Doyle JS, Jewell LD et al (1999) Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology 116:1107–1114

    Article  PubMed  CAS  Google Scholar 

  9. Sartor RB (2004) Therapeutic manipulation of the enteric microflora in inflammatory bowel diseases: antibiotics, probiotics, and prebiotics. Gastroenterology 126:1620–1633

    Article  PubMed  Google Scholar 

  10. Lammers KM, Vergopoulos A, Babel N et al (2005) Probiotic therapy in the prevention of pouchitis onset: decreased interleukin-1beta, interleukin-8, and interferon-gamma gene expression. Inflamm Bowel Dis 11:447–454

    Article  PubMed  Google Scholar 

  11. Bibiloni R, Fedorak RN, Tannock GW et al (2005) VSL3 probiotic-mixture induces remission in patients with active ulcerative colitis. Am J Gastroenterol 100:1539–1546

    Article  PubMed  Google Scholar 

  12. Schultz M, Veltkamp C, Dieleman LA et al (2002) Lactobacillus plantarum 299 V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis 8:71–80

    Article  PubMed  Google Scholar 

  13. Gionchetti P, Rizzello F, Venturi A et al (2000) Oral bacteriotherapy as maintenance treatment in patients with chronic pouchitis: a double-blind, placebo controlled trial. Gastroenterology 119:305–309

    Article  PubMed  CAS  Google Scholar 

  14. Gionchetti P, Rizzello F, Helwig U et al (2003) Prophylaxis of pouchitis onset with probiotic therapy: a double-blind, placebo-controlled trial. Gastroenterology 124:1202–1209

    Article  PubMed  Google Scholar 

  15. Gupta P, Andrew H, Kirschner BS et al (2000) Is Lactobacillus GG helpful in children with Crohn’s disease? Results of a preliminary, open-label study. J Pediatr Gastroenterol Nutr 31:453–457

    Article  PubMed  CAS  Google Scholar 

  16. FAO/WHO (2002) Working group report on drafting guidelines for the evaluation of probiotics in food London. Ontario, Canada

  17. Christensen HR, Frokiaer H, Pestka JJ (2002) Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol 168:171–178

    PubMed  CAS  Google Scholar 

  18. Dombrowicz D, Nutten S, Desreumaux P et al (2001) Role of the high affinity immunoglobulin E receptor in bacterial translocation and intestinal inflammation. J Exp Med 193:25–34

    Article  PubMed  CAS  Google Scholar 

  19. Bustin SA, Benes V, Garson JA et al (2009) The MIQE guidelines: minimum information for publication of quantitative real-time PCR experiments. Clin Chem 55:611–622

    Article  PubMed  CAS  Google Scholar 

  20. Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29:e45

    Article  PubMed  CAS  Google Scholar 

  21. Rasmussen R (2001) Quantification on the LightCycler. In: Meuer S, Wittwer C, Nakagawara K (eds) Rapid cycle real-time PCR. Methods and applications. Springer Press, Heidelberg, pp 21–34

    Chapter  Google Scholar 

  22. Pfaffl MW, Horgan GW, Dempfle L (2002) Relative expression software tool (REST) for group-wise comparison and statistical analysis of relative expression results in real-time PCR. Nucleic Acids Res 30:e36

    Article  PubMed  Google Scholar 

  23. Crittenden R, Karppinen S, Ojanen S et al (2002) In vitro fermentation of cereal dietary fibre carbohydrates by probiotic and intestinal bacteria. J Sci Food Agric 82:781–789

    Article  CAS  Google Scholar 

  24. Harris RE (2007) Cyclooxygenase-2 (cox-2) and the inflammogenesis of cancer. Subcell Biochem 42:93–126

    Article  PubMed  Google Scholar 

  25. Wang Q, Takei Y, Kobayashi O et al (2009) Cyclooxygenase 2 modulates killing of cytotoxic T lymphocytes by colon cancer cells. J Clin Biochem Nutr 45:163–170

    Article  PubMed  CAS  Google Scholar 

  26. Brundnak MA (2001) Nutritional regulation of gene expression. Theory Biosci 120:64–75

    Google Scholar 

  27. Miller KS, Brudnak M (1994) Expression cloning: PCR versus episomal vectors for rescue of transfected genes. In: Sarkar G (ed) PCR in neuroscience (Methods in neuroscience, vol 26). Academic Press, Orlando, FL

    Google Scholar 

  28. Borruel N, Carol M, Casellas F et al (2002) Increased mucosal tumour necrosis factor α production in Crohn’s disease can be regulated ex vivo by probiotic bacteria. Gut 51:659–664

    Article  PubMed  CAS  Google Scholar 

  29. Haller D, Bode C, Hammes WP et al (2000) Non-pathogenic bacteria elicit a differential cytokine response by intestinal epithelial cell/leucocyte co-cultures. Gut 47:79–87

    Article  PubMed  CAS  Google Scholar 

  30. Maassen CB, van Holten-Neelen C, Balk F et al (2000) Strain-dependent induction of cytokine profiles in the gut by orally administered Lactobacillus strains. Vaccine 18:2613–2623

    Article  PubMed  CAS  Google Scholar 

  31. Morita H, He F, Fuse T et al (2002) Adhesion of lactic acid bacteria to caco-2 cells and their effect on cytokine secretion. Microbiol Immunol 46:293–297

    PubMed  CAS  Google Scholar 

  32. Ewaschuk JB, Dieleman LA (2006) Probiotics and prebiotics in chronic inflammatory bowel diseases. World J Gastroenterol 12:5941–5950

    PubMed  CAS  Google Scholar 

  33. Lee JH, Lee B, Lee HS et al (2009) Lactobacillus suntoryeus inhibits pro-inflammatory cytokine expression and TLR-4-linked NF-kappaB activation in experimental colitis. Int J Colorectal Dis 24:231–237

    Article  PubMed  Google Scholar 

  34. Pavan S, Desreumaux P, Mercenier A (2003) Use of mouse models to evaluate the persistence, safety and immune modulation capacities of lactic acid bacteria. Clin Diagn Lab Immunol 10:696–701

    PubMed  CAS  Google Scholar 

  35. Perdigon G, Maldonado Galdeano G, Valdez JC et al (2002) Interaction of lactic acid bacteria with the gut immune system. Eur J Clin Nutr 56:S21–S26

    Article  PubMed  CAS  Google Scholar 

  36. Hart AL, Lammers K, Brigidi P et al (2004) Modulation of human dendritic cell phenotype and function by probiotic bacteria. Gut 53:1602–1609

    Article  PubMed  CAS  Google Scholar 

  37. Chen L, Wang X, Cui Y et al (2009) Therapeutic effects of four strains of probiotics on experimental colitis in mice. World J Gastroenterol 15:321–327

    Article  PubMed  CAS  Google Scholar 

  38. Menard O, Butel M, Gaboriau-Routhiau V et al (2008) Gnotobiotic mouse immune response induced by Bifidobacterium sp. strains isolated from infants. Appl Environ Microbiol 74:660–666

    Article  PubMed  CAS  Google Scholar 

  39. Matsuzaki T, Takagi A, Ikemura H et al (2007) Intestinal microflora: probiotics and autoimmunity. J Nutr 137:798S–802S

    PubMed  CAS  Google Scholar 

  40. Mastrangeli G, Corinti S, Butteroni C et al (2009) Effects of live and inactivated VSL#3 probiotic preparations in the modulation of in vitro and in vivo allergen-induced Th2 responses. Int Arch Allergy Immunol 150:133–143

    Article  PubMed  CAS  Google Scholar 

  41. Ulisse S, Gionchetti P, D’Alo S et al (2001) Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: effects of probiotic treatment. Am J Gastroenterol 96:2691–2699

    Article  PubMed  CAS  Google Scholar 

  42. Hacini-Rachinel F, Gheit H, Luduec J et al (2009) Oral probiotic control skin inflammation by acting on both effector and regulatory T cells. PLoS ONE 4:e4903

    Article  PubMed  Google Scholar 

  43. Caballero F, Keller K, De Simone C et al (2007) The VSL#3 probiotic formula induces mucin gene expression and secretion in colonic epithelial cells. Am J Physiol Gastrointest Liver Physiol 292:G315–G322

    Article  Google Scholar 

  44. Gaudier E, Michel C, Segain JP et al (2005) The VSL#3 probiotic mixture modifies microflora but does not heal chronic dextran sodium sulphate induced colitis or reinforce the mucus barrier in mice. J Nutr 135:2753–2761

    PubMed  CAS  Google Scholar 

  45. Mattar AF, Teitelbaum DH, Drongowski RA et al (2002) Probiotics up-regulate MUC-2 mucin gene expression in a Caco-2 cell-culture model. Pediatr Surg Int 18:586–590

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

We gratefully acknowledge the Director, National Dairy Research Institute (NDRI, Karnal, India) for providing facilities to carry out the study. We thank Dr. N.P. Shah (Australia) for kindly providing the standard Lactobacillus culture. The financial support received from Indian Council of Agricultural Research (ICAR, India) in terms of providing fellowship to the first author of the paper to carry out his doctoral programme is greatly appreciated.

Author information

Authors and Affiliations

  1. Molecular Biology Unit, Department of Dairy Microbiology, National Dairy Research Institute, Karnal, Haryana, 132001, India

    Mache Amit Bhausaheb, Virender Kumar Batish & Sunita Grover

  2. Department of Food Engineering and Technology, Tezpur University, Napaam, Assam, 784028, India

    Raj Kumar Duary

Authors
  1. Raj Kumar Duary
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Mache Amit Bhausaheb
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Virender Kumar Batish
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Sunita Grover
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Virender Kumar Batish or Sunita Grover.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Duary, R.K., Bhausaheb, M.A., Batish, V.K. et al. Anti-inflammatory and immunomodulatory efficacy of indigenous probiotic Lactobacillus plantarum Lp91 in colitis mouse model. Mol Biol Rep 39, 4765–4775 (2012). https://doi.org/10.1007/s11033-011-1269-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11033-011-1269-1

Keywords

Search

Navigation