Abstract
Some of the important properties of probiotics are the ability to survive during gastrointestinal transit and to modulate the immune functions. The objectives of the reported study were to assess in vivo gastrointestinal survival of orally administered Pediococcus pentosaceus OZF using an animal model BALB/c mice, and to examine its effects on the immune response. Following oral administration to mice, the ability of Pediococcus pentosaceus OZF to pass and survive through the mouse gastrointestinal system was investigated by analyzing the recovery of the strain in fecal samples. Microbiological and polymerase chain reaction (PCR) methods proved that the strain OZF could overcome specific conditions in the gastrointestinal tract of mice and reach the intestine alive after ingestion. To observe the effect of oral administration on immune response, IL-6, IL-12 and IFN-γ were measured by ELISA, and the strain OZF was found to cause increases in IL-6 synthesis in regularly fed mice. However, stimulation was carried out with various concentrations of bacterial ssDNA and heat killed cells of Pediococcus pentosaceus OZF. The heat killed cells of the strain OZF were shown to produce IFN-γ independently from IL-12. On the other hand, a significant difference between control and experimental group was noticed when lipopolysaccharide, a TLR4 (toll like receptor) ligand, was used. Overall, Pediococcus pentosaceus OZF may be a valuable probiotic strain for therapeutic uses. Nevertheless, further studies on the mechanisms of immunomodulatory effect will allow for better clarification of the immune functions of this strain.
Similar content being viewed by others
References
Baken KA, Ezendam J, Gremmer ER (2006) Evaluation of immunomodulation by Lactobacillus casei Shirota: immune function, auto immunity and gene expression. Int J Food Microbiol 112:8–18
Biswas SR, Purbita R, Johnson MC, Ray B (1991) Influence of growth conditions on the production of a bacteriocin, pediocin AcH, by Pediococcus acidilactici H. Appl Environ Microb 57(4):1265–1267
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
Collins JK, Thornton K, Sullivan GO (1998) Selection of probiotic strains for human applications. Int Dairy J 8(5):487–490
Deshpande GC, Rao CS, Keil AD, Patole SK (2011) Evidence-based guidelines for use of probiotics in preterm neonates. BMC Med 9:92–98
Duchaine C, Israel-Assayag E, Fournier M, Cormier Y (1996) Proinflammatory effect of Pediococcus pentosaceus, a bacterium used as preservative. Eur Respir J 9:2508–2512
Edwards U, Rogall T, Blockerl H, Emde M, Bottger EC (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucleic Acids Res 17(19):7843–7853
Erikci E, Gursel M, Gursel I (2011) Differential immune activation following encapsulation of immunostimulatory CpG oligodeoxynucleotide in nanoliposomes. Biomaterials 32:1715–1723
Foligne B, Dewulf J, Breton J, Claisse O, Lonvaud-Funel A, Pot B (2010) Probiotic properties of non-conventional lactic acid bacteria: immunomodulation by Oenococcus oeni. Int J Food Microbiol 140:136–145
Freter R (1992) Factors affecting the microecology of the gut. In: Fuller R (ed) Probiotics. Chapman & Hall, London, pp 111–144
Fujiwara D, Inoue S, Wakabayashi H, Fujii T (2004) The anti-allergic effects of lactic acid bacteria are strain dependent and mediated by effects on both Th1/Th2 cytokine expression and balance. Int Arch Aller Imm 135(3):205–215
Fujiwara S, Seto Y, Kimura A, Hashiba S (2001) Intestinal transit of an orally administered streptomycin–rifampicin-resistant variant of Bifidobacterium longum SBT 2928: its long term survival and effect on the intestinal microflora and metabolism. J Appl Microbiol 90(1):43–52
Fuller R (1989) Probiotics in man and animals. J Appl Bacteriol 66(5):365–378
Furrie E (2005) Probiotics and allergy. Proc Nutr Soc 64:465–469
Ghadimi D, Folster-Holst R, de Vrese M, Winkler P, Heller KJ, Schrezenmeir J (2008) Effects of probiotic bacteria and their genomic DNA on Th1/Th2-cytokine production by peripheral blood mononuclear cells (PBMCs) of healthy and allergic subjects. Immunobiology 213:677–692
Gill HS (1998) Stimulation of the immun system by lactic cultures. Int Dairy J 8:535–544
Goldin BR, Gorbuch SL, Saxelin M, Barakat S, Gualtieri L, Salminen S (1992) Survival of Lactobacillus species (strain GG) in human gastrointestinal tract. Dig Dis Sci 37:121–128
Guarner F, Schaafsma GJ (1998) Probiotics. Int J Food Microbiol 39(3):237–238
Havenaar R, Brink BT, Huis in’t Veld JHJ (1992) Selection of strains for probiotics use. In: Fuller R (ed) Probiotics. Chapman & Hall, London, pp 111–144
Helwig U, Lammers KM, Rizzello F, Brigidi P, Rohleder V, Caramelli E, Gionchetti P, Schrezenmeir J, Foelsch UR, Schreiber S, Campieri M (2006) Lactobacilli, bifidobacteria and E. coli nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World J Gastroenterol 12:5978–5986
Iannitti T, Palmieri B (2010) Therapeutical use of probiotic formulations in clinical practice. Clin Nutr 29:701–725
Iliev ID, Kitazawa H, Shimosato T, Katoh S, Morita H, He F, Hosoda M, Saito T (2005) Strong immunostimulation in murine immune cells by Lactobacillus rhamnosus GG DNA containing novel oligodeoxynucleotide pattern. Cell Microbiol 7:403–414
Isolauri E (1999) Probiotics and gut inflammation. Curr Opin Gastroenterol 15:534–537
Isolauri E, Juntunen M, Rautanen T, Sillanauke P, Koiuva T (1991) A human Lactobacillus strain (Lactobacillus casei sp. strain GG) promotes recovery from acute diarrhea in children. Pediatrics 88:90–97
Jonganurakkun B, Wang Q, Xu SH, Tada Y, Minamida K, Yasokawa D, Sugi M, Hara H, Asano K (2008) Pediococcus pentosaceus NB-17 for probiotic use. J Biosci Bioeng 106:69–73
Kimoto H, Mizumachi K, Okamoto T, Kurisaki J (2004) New Lactococcus strain with immunomodulatory activity: enhancement of Th1-type immune response. Microbiol Immunol 48(2):75–82
Kimura M, Danno K, Yasui H (2006) Immunomodulatory function and probiotic properties of lactic acid bacteria isolated from Mongolian fermented milk. Biosci Microflora 25(4):147–155
Lammers KM, Brigidi P, Vitali B, Gionchetti P, Rizzello F, Caramelli E, Matteuzzi D, Campieri M (2003) Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol Med Microbiol 38:165–172
Lebeer S, Vanderleyden J, De Keersmaecker SCJ (2008) Genes and molecules of lactobacilli supporting probiotic action. Microbiol Mol Biol R 72:728–764
Li Y, Qu X, Yang H, Kang L, Xu Y, Bai B, Song W (2005) Bifidobacteria DNA induces murine macrophages activation in vitro. Cell Mol Immunol 2:473–478
Lo Curto A, Pitino I, Mandalari G, Dainty JR, Faulks RM, John Wickham MS (2011) Survival of probiotic lactobacilli in the upper gastrointestinal tract using an in vitro gastric model of digestion. Food Microbiol 28(7):359–366
Lomax AR, Calder PC (2009) Probiotics, immune function, infection and inflammation: a review of the evidence from studies conducted in humans. Curr Pharm Des 15:1428–1518
Marin ML, Lee JH, Murtha J, Ustunol Z, Pestka JJ (1997) Differential cytokine production in clonal macrophage and T-cell lines cultured with bifidobacteria. J Dairy Sci 80:2713–2720
Marteau P, Rambaud JC (1993) Potential of using lactic acid bacteria for therapy and immunomodulation in man. FEMS Microbiol Rev 12(1–3):207–220
Medina M, Izquierdo E, Ennahar S, Sanz Y (2007) Differential immunomodulatory properties of Bifidobacterium longum strains: relevance to probiotic selection and clinical applications. Clin Exp Immunol 150:531–538
Menard O, Gafa V, Kapel N, Rodriguez B, Butel MJ, Waligora-Dupriet AJ (2010) Characterization of immunostimulatory CpG-rich sequences from different Bifidobacterium species. Appl Environ Microbiol 76(9):2846–2855
Morita H, He F, Fuse T, Ouwehand AC, Hashimoto H, Hosoda M, Mizumachi K, Kurisaki J (2002) Adhesion of lactic acid bacteria to CaCo-2 cells and their effect on cytokine secretion. Microbiol Immunol 46(4):293–297
Murphy L, Dunne C, Kiely B, Shanahan F, O’Sullivan GC, Collins J (1999) In vivo assessment of potential probiotic Lactobacillus salivarius strains: evaluation of their establishment, persistence, and localisation in the murine gastrointestinal tract. Microb Ecol Health D 11:149–157
Nagao F, Nakayama M, Muto T, Okumura K (2000) Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the immune system in healthy human subjects. Biosci Biotech Bioch 64:2706–2708
Ng SC, Hart AL, Kamm MA, Stagg AJ, Knight SC (2009) Mechanisms of action of probiotics: recent advances. Inflamm Bowel Dis 15:300–310
Niers LE, Timmerman HM, Rijkers GT, van Bleek GM, van Uden NO, Knol EF, Kapsenberg ML, Kimpen JL, Hoekstra MO (2005) Identification of strong interleukin-10 inducing lactic acid bacteria which down-regulate T helper type 2 cytokines. Clin Exp Allergy 35:1481–1489
Niers LE, Hoekstra MO, Timmerman HM, van Uden NO, de Graaf PM, Smits HH, Kimpen JL, Rijkers GT (2007) Selection of probiotic bacteria for prevention of allergic diseases: immunomodulation of neonatal dendritic cells. Clin Exp Immunol 149:344–352
Olivares M, Diaz-Ropero MP, Gomez N, Lara-Villoslada F, Maldonado JA, Martin R, Lopez-Huertas E, Rodriguez JM, Xaus J (2006) Oral administration of two probiotic strains, Lactobacillus coryniformis CECT5711 and Lactobacillus gasseri CECT5714, enhances the intestinal function of healthy adults. Int J Food Microbiol 107:104–111
Osborne CA, Galic M, Sangwan P, Janssen PH (2005) PCR-generated artefact from 16S rRNA gene-specific primers. FEMS Microbiol Lett 248(2):183–187
Osmanagaoglu O, Kiran F, Ataoglu H (2010) Evaluation of in vitro probiotic potential of Pediococcus pentosaceus OZF isolated from human breast milk. Probiot Antimicrob Prot 2(3):162–174
Osmanagaoglu O, Kiran F, Nes IF (2011) A probiotic bacterium, Pediococcus pentosaceus OZF, isolated from human breast milk produces pediocin AcH/PA-1. Afr J Biotechnol 10(11):2070–2079
Peran L, Camuesco D, Comalada M, Nieto A, Concha A, Diaz-Ropero MP, Olivares M, Xaus J, Zarzuelo A, Galvez J (2005) Preventive effects of a probiotic, Lactobacillus salivarius ssp. salivarius, in the TNBS model of rat colitis. World J Gastroenterol 11:5185–5192
Perez-Cano FJ, Dong H, Yaqoob P (2010) In vitro immunomodulatory activity of Lactobacillus fermentum CECT5716 and Lactobacillus salivarius CECT5713: two probiotic strains isolated from human breast milk. Immunobiology 215(12):996–1004
Repa A, Grangette C, Daniel C, Hochreiter R, Hoffmann-Sommergruber K, Thalhamer J, Kraft D, Breiteneder H, Mercenier A, Wiedermann U (2003) Mucosal co-application of lactic acid bacteria and allergen induces counter-regulatory immune responses in a murine model of birch pollen allergy. Vaccine 22(1):87–95
Salminen S, von Wright A, Morelli L, Marteau P, Brassart D, de Vos WM, Fonden R, Saxelin M, Collins K, Mogensen G, Birkeland SE, Mattila-Sandholm T (1998) Demonstration of safety of probiotics - a review. Int J Food Microbiol 44(1–2):93–106
Satokari R, Gronroos T, Laitinen K, Salminen S, Isolauri E (2009) Bifidobacterium and Lactobacillus DNA in the human placenta. Lett Appl Microbiol 48:8–12
Sheih YH, Chiang BL, Wang LH, Liao CK, Gill HS (2001) Systemic immunity-enhancing effects in healthy subjects following dietary consumption of the lactic acid bacterium Lactobacillus rhamnosus HN001. J Am Coll Nutr 20:149–156
Shida K, Takahashi R, Iwadate E, Takamizawa K, Yasui H, Sato T, Habu S, Hachimura S, Kaminogawa S (2002) Lactobacillus casei strain Shirota suppresses serum immunoglobulin E and immunoglobulin G1 responses and systemic anaphylaxis in a food allergy model. Clin Exp Allergy 32(4):563–570
Shida K, Suzuki T, Kiyoshima-Shibata J, Shimada S, Nanno M (2006) Essential roles of monocytes in stimulating human peripheral blood mononuclear cells with Lactobacillus casei to produce cytokines and augment natural killer cell activity. Clin Vaccine Immunol 13:997–1003
Simpson PJ, Fitzgerald GF, Stanton C, Ross RP (2006) Enumeration and identification of pediococci in powder-based products using selective media and rapid PFGE. J Microbiol Meth 64(1):120–125
Suskovic J, Kos B, Goreta J, Matosic S (2001) Role of lactic acid bacteria and bifidobacteria in synbiotic effect. Food Technol Biotech 39:227–235
Suwanjinda D, Pala-Or K, Panbangred W (2009) Simultaneous detection of pediocin gene and species differentiation between Pediococcus acidilactici and Pediococcus pentosaceus in a one step multiplex-overlapping PCR methods. Food Biotech 23:179–189
Takagi A, Matsuzaki T, Sato M, Nomoto K, Morotomi M, Yokokura T (2001) Enhancement of natural killer cytotoxicity delayed murine carcinogenesis by a probiotic microorganism. Carcinogenesis 22(4):599–605
Van Enckevort FH, Netea MG, Hermus AR, Sweep CG, Meis JF, Van der Meer JW, Kullberg BJ (1999) Increased susceptibility to systemic candidiasis in interleukin-6 deficient mice. Med Mycol 37(6):419–426
Vinderola CG, Matar C, Perdigon G (2005) Role of the epithelial cells in the immune effects mediated by gram-positive probiotic bacteria. Involvement of Toll-like receotors. Clin Diagn Lab Immunol 12:1075–1084
Vizoso Pinto MG, Schuster T, Briviba K, Watzl B, Holzapfel WH, Franz CM (2007) Adhesive and chemokine stimulatory properties of potentially probiotic Lactobacillus strains. J Food Prot 70:125–134
Vizoso Pinto MG, Gomez MR, Seifert S, Watzl B, Holzapfel WH, Franz C (2009) Lactobacilli stimulate the innate immune response and modulate the TLR expression of HT29 intestinal epithelial cells in vitro. Int J Food Microbiol 133:86–93
Wells CL, Maddaus LA, Jechorek RP, Simmons RL (1988) Role of intestinal anaerobic bacteria in colonization resistance. Eur J Clin Microbiol Infect Dis 7(1):107–113
Yasui H, Shida K, Matsuzaki T, Yokokura T (1999) Immunomodulatory function of lactic acid bacteria. Antonie van Leeuwenhoek 76(1–4):383–389
Zhu J, Zhao L, Guo H, Jiang L, Ren F (2011) Immunomodulatory effects of novel bifidobacterium and lactobacillus strains on murine macrophage cells. Afr J Microbiol Res 5(1):8–15
Acknowledgments
This work was partially supported by the Scientific and Technological Research Council of Turkey (TUBITAK) Project; SBAG 111S012. We thank to Tamer Kahraman and other members of Therapeutic ODN Research Laboratory for their excellent technical support.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Osmanagaoglu, O., Kiran, F., Yagci, F.C. et al. Immunomodulatory function and in vivo properties of Pediococcus pentosaceus OZF, a promising probiotic strain. Ann Microbiol 63, 1311–1318 (2013). https://doi.org/10.1007/s13213-012-0590-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s13213-012-0590-9