Redirecting to http://dergipark.org.tr/_fragment?_hash=KuONalJDKykM2EN9vVx9iCYGJ7VbIdYZOu7rGQ2GXLQ&_path=id%3D523306%26_format%3Dhtml%26_locale%3Den%26_controller%3DApp%255CController%255CSite%255CArticleController%253A%253AesiArticleStats.
Review Article
BibTex RIS Cite

PROBIOTIC-HUMAN IMMUNE SYSTEM INTERACTIONS

Year 2019, Volume: 5 Issue: 4, 265 - 280, 01.10.2019

Dicle Dilara Akpınar , Burcu Kaplan Türköz

https://doi.org/10.3153/FH19027

Abstract

Probiotics are
live microorganisms which when administered in adequate amounts confer a health
benefit on the host. These microorganisms are known to provide beneficial
health effects by competing with pathogens, providing epithelial cell stability
and showing regulatory effects on the immune system. They provide
immunomodulatory, anti-inflammatory, anti-microbial, antioxidant effects with
their released metabolites, produced molecules and cell structure components.
Effector molecules of probiotics such as peptidoglycan, teichoic acid,
lipoteichoic acid, cell surface polysaccharides, secreted proteins and surface
proteins are recognized by innate immunity receptors and activate the immune
system. The mechanisms of some effector molecules of probiotics have been
elucidated. The aim of this review is to give information on the effects of
probiotics and their active molecules known to be used for probiotic-host
interactions.

Keywords

Probiotics Health Effects Probiotic-host interactions Immunomodulation Effector molecules

References

  • Agrawal, R. (2005). Probiotics: An emerging food supplement with health benefits. Food Biotechnology, 19(3), 227-246. https://doi.org/10.1080/08905430500316474
  • Aguilar-Toalá, J.E., Garcia-Varela, R., Garcia, H.S., Mata-Haro, V., González-Córdova, A.F., Vallejo-Cordoba, B., Hernández-Mendoza, A. (2018). Postbiotics: An evolving term within the functional foods field. Trends in Food Science & Technology, 75, 105-114. https://doi.org/10.1016/j.tifs.2018.03.009
  • Akira, S., Uematsu, S., Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell, 124(4), 783-801. https://doi.org/10.1016/j.cell.2006.02.015
  • Al-Hassi, H.O., Mann, E.R., Sanchez, B., English, N.R., Peake, S.T.C., Landy, J., Man, R., Urdaci, M., Hart, A. L., Fernandez-Salazar, L., Lee, G.H., Garrote, J.A., Arranz, E., Margolles, A., Stagg, A.J., Knight, S.C., Bernardo, D. (2014). Altered human gut dendritic cell properties in ulcerative colitis are reversed by Lactobacillus plantarum extracellular encrypted peptide STp. Molecular Nutrition and Food Research, 58(5), 1132-1143. https://doi.org/10.1002/mnfr.201300596
  • Bäuerl, C., Pérez-Martínez, G., Yan, F., Polk, D.B., Monedero, V. (2010). Functional analysis of the p40 and p75 proteins from lactobacillus casei BL23. Journal of Molecular Microbiology and Biotechnology, 19, 231-241. https://doi.org/10.1159/000322233
  • Bernardo, D., Sánchez, B., Al-Hassi, H.O., Mann, E.R., Urdaci, M.C., Knight, S.C., Margolles, A. (2012). Microbiota/host crosstalk biomarkers: Regulatory response of human intestinal dendritic cells exposed to Lactobacillus extracellular encrypted peptide. PLoS ONE, 7(5), 1-8. https://doi.org/10.1371/journal.pone.0036262
  • Boirivant, M., Strober, W. (2007). The mechanism of action of probiotics. Current Opinion in Gastroenterology, 23(6), 679-692. https://doi.org/10.1097/MOG.0b013e3282f0cffc
  • Bron, P.A., Tomita, S., van Swam, I.I., Remus, D.M., Meijerink, M., Wels, M., Okada, S., Wells, J.M., Kleerebezem, M. (2012a). Lactobacillus plantarum possesses the capability for wall teichoic acid backbone alditol switching. Microbial Cell Factories, 11(123), 1-15. https://doi.org/10.1186/1475-2859-11-123
  • Bron, P. A., Van Baarlen, P., Kleerebezem, M. (2012b). Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nature Reviews Microbiology, 10, 66-78. https://doi.org/10.1038/nrmicro2690
  • Chapot-Chartier, M.P., Kulakauskas, S. (2014). Cell wall structure and function in lactic acid bacteria. Microbial Cell Factories, 13(1), 1-23. https://doi.org/10.1186/1475-2859-13-S1-S9
  • Ciszek-Lenda, M., Nowak, B., Śróttek, M., Gamian, A., Marcinkiewicz, J. (2011). Immunoregulatory potential of exopolysaccharide from Lactobacillus rhamnosus KL37. Effects on the production of inflammatory mediators by mouse macrophages. International Journal of Experimental Pathology, 92(6), 382-391. https://doi.org/10.1111/j.1365-2613.2011.00788.x
  • Claes, I.J.J., Segers, M.E., Verhoeven, T.L.A., Dusselier, M., Sels, B.F., De Keersmaecker, S.C.J., Sigrid, C.J., Vanderleyden, J., Lebeer, S. (2012). Lipoteichoic acid is an important microbe-associated molecular pattern of Lactobacillus rhamnosus GG. Microbial Cell Factories, 11(161), 1-8. https://doi.org/10.1186/1475-2859-11-161
  • Claes, I.J.J., Lebeer, S., Shen, C., Verhoeven, T.L.A., Dilissen, E., De Hertogh, G., Bullens, D.M.A., Ceuppens, J.L., Van Assche, G., Vermeire, S., Rutgeerts, P., Vanderleyden, J., De Keersmaecker, S.C.J. (2010). Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis. Clinical and Experimental Immunology, 162(2), 306-314. https://doi.org/10.1111/j.1365-2249.2010.04228.x
  • Corcoran, B. M., Stanton, C., Fitzgerald, G., Ross, R. P. (2008). Life Under Stress : The Probiotic Stress Response and How it may be Manipulated. Current Pharmaceutical Design, 14(14), 1382-1399. https://doi.org/10.2174/138161208784480225
  • Corr, S.C., Li, Y., Riedel, C.U., O'Toole, P.W., Hill, C., Gahan, C.G.M. (2007). Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. PNAS, 104(18), 7617-7621. https://doi.org/10.1073/pnas.0700440104
  • Delcour, J., Ferain, T., Deghorain, M., Palumbo, E., Hols, P. (1999). The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie van Leeuwenhoek, 76, 159-84. https://doi.org/10.1023/A:1002089722581
  • Fanning, S., Hall, L.J., Cronin, M., Zomer, A., MacSharry, J., Goulding, D., O'Connell Motherway, M., Shanahan, F., Nally, K., Dougan, G., van Sinderen, D. (2012). Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proceedings of the National Academy of Sciences, 109(6), 2108-2113. https://doi.org/10.1073/pnas.1115621109
  • FAO/WHO. (2002). Guidelines for the evalution of probiotics in food. Food and Agriculture Organization of the United Nations/World Health Organization, London, Ontario. p. 413-426.
  • Fernandez, E.M., Valenti, V., Rockel, C., Hermann, C., Pot, B., Boneca, I.G., Grangette, C. (2011). Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut, 60, 1050-1059. https://doi.org/10.1136/gut.2010.232918
  • Fotiadis, C.I., Stoidis, C.N., Spyropoulos, B.G., Zografos, E.D. (2008). Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World Journal of Gastroenterology, 14(42), 6453-6457. https://doi.org/10.3748/wjg.14.6453
  • Ganguli, K., Collado, M.C., Rautava, J., Lu, L., Satokari, R., Von Ossowski, I., Reunanen, J., De Vos, W.M., Palva, A., Isolauri, E., Salminen, S., Walker, W.A., Rautava, S. (2015). Lactobacillus rhamnosus GG and its SpaC pilus adhesin modulate inflammatory responsiveness and TLR-related gene expression in the fetal human gut. Pediatric Research, 77, 528-535. https://doi.org/10.1038/pr.2015.5
  • Girardin, S.E., Boneca, I.G., Viala, J., Chamaillard, M., Labigne, A., Thomas, G., Philpott, D.J., Sansonetti, P.J. (2003). Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. Journal of Biological Chemistry, 278, 8869-8872. https://doi.org/10.1074/jbc.C200651200
  • Gıda, Tarım ve Hayvancılık Bakanlığı (2011). Türk gıda kodeksi etiketleme yönetmeliği. http://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-7.htm (Erişim tarihi 28.01.2019)
  • Gleeson, J.P. (2017). Diet, food components and the intestinal barrier. Nutrition Bulletin, 42(2), 123-131. https://doi.org/10.1111/nbu.12260
  • Gotteland, M., Brunser, O., Cruchet, S. (2006). Systematic review: Are probiotics useful in controlling gastric colonization by Helicobacter pylori? Alimentary Pharmacology and Therapeutics, 23(8), 1077-1086. https://doi.org/10.1111/j.1365-2036.2006.02868.x
  • Guarner, F., Perdigon, G., Corthier, G., Salminen, S., Koletzko, B., Morelli, L. (2005). Should yoghurt cultures be considered probiotic? British Journal of Nutrition, 93(6), 783-786. https://doi.org/10.1079/BJN20051428
  • Gürsoy, O., Kınık, Ö., Gönen, İ. (2005). Probiyotikler ve gastrointestinal sağlığa etkileri. Türk Mikrobiyoloji Cemiyeti Dergisi, 35(2), 136-148.
  • Hafez, M., Hayes, K., Goldrick, M., Warhurst, G., Grencis, R., Roberts, I.S. (2009). The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infection and Immunity, 77(7), 2995-3003. https://doi.org/10.1128/IAI.00040-09
  • Hevia, A., Delgado, S., Sánchez, B., Margolles, A. (2015). Molecular players involved in the interaction between beneficial bacteria and the immune system. Frontiers in Microbiology, 6, 1-8. https://doi.org/10.3389/fmicb.2015.01285
  • Hirose, Y., Murosaki, S., Fujiki, T., Yamamoto, Y., Yoshikai, Y., Yamashita, M. (2010). Lipoteichoic acids on Lactobacillus plantarum cell surfaces correlate with induction of interleukin-12p40 production. Microbiology and Immunology, 54(3), 143-151. https://doi.org/10.1111/j.1348-0421.2009.00189.x
  • Hoveyda, N., Heneghan, C., Mahtani, K.R., Perera, R., Roberts, N., Glasziou, P. (2009). A systematic review and meta-analysis: Probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterology, 9(15), 1-11. https://doi.org/10.1186/1471-230X-9-15
  • Hynönen, U., Palva, A. (2013). Lactobacillus surface layer proteins: Structure, function and applications. Applied Microbiology and Biotechnology, 97(12), 5225-5243. https://doi.org/10.1007/s00253-013-4962-2
  • Ivanov, D., Emonet, C., Foata, F., Affolter, M., Delley, M., Fisseha, M., Blum-Sperisen, S., Kochhar, S., Arigoni, F. (2006). A serpin from the gut bacterium Bifidobacterium longum inhibits eukaryotic elastase-like serine proteases. Journal of Biological Chemistry, 281, 17246-17252. https://doi.org/10.1074/jbc.M601678200
  • Johnson-Henry, K.C., Hagen, K.E., Gordonpour, M., Tompkins, T.A., Sherman, P.M. (2007). Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cellular Microbiology, 9(2), 356-367. https://doi.org/10.1111/j.1462-5822.2006.00791.x
  • Kaji, R., Kiyoshima-Shibata, J., Nagaoka, M., Nanno, M., Shida, K. (2010). Bacterial Teichoic Acids Reverse Predominant IL-12 Production Induced by Certain Lactobacillus Strains into Predominant IL-10 Production via TLR2-Dependent ERK Activation in Macrophages. The Journal of Immunology, ji_0901569, 1-9. https://doi.org/10.4049/jimmunol.0901569
  • Kalliomäki, M.A., Isolauri, E. (2004). Probiotics and down-regulation of the allergic response. Immunology and Allergy Clinics of North America, 24(4), 739-752. https://doi.org/10.1016/j.iac.2004.06.006
  • Kang, H., Im, S. (2015). Probiotics as an Immune Modulator. Journal of Nutritional Science and Vitaminology, 61, 103-105. https://doi.org/10.3177/jnsv.61.S103
  • Kawai, T., Akira, S. (2011). Toll-like Receptors and Their Crosstalk with Other Innate Receptors in Infection and Immunity. Immunity, 34(5), 637-650. https://doi.org/10.1016/j.immuni.2011.05.006
  • Kelesidis, T., Pothoulakis, C. (2012). Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Therapeutic Advances in Gastroenterology, 5(2), 111-125. https://doi.org/10.1177/1756283X11428502
  • Khazaie, K., Zadeh, M., Khan, M.W., Bere, P., Gounari, F., Dennis, K., Blatner, N.R., Owen, J.L., Klaenhammer, T.R., Mohamadzadeh, M. (2012). Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proceedings of the National Academy of Sciences, 109(26), 10462-10467. https://doi.org/10.1073/pnas.1207230109
  • Kim, H., Lee, S., Kim, N., Ko, M., Lee, J., Yi, T., Chung, S.K., Chung, D. (2008). Inhibitory effects of Lactobacillus plantarum lipoteichoic acid (LTA) on Staphylococcus aureus LTA-induced tumor necrosis factor-alpha production. Journal of Microbiology and Biotechnology, 18(6), 1191-1996.
  • Kleerebezem, M., Binda, S., Bron, P.A., Gross, G., Hill, C., van Hylckama Vlieg, J.E., Lebeer, S., Satokari, R., Ouwehand, A.C. (2019). Understanding mode of action can drive the translational pipeline towards more reliable health benefits for probiotics. Current Opinion in Biotechnology, 56, 55-60. https://doi.org/10.1016/j.copbio.2018.09.007
  • Kleerebezem, M., Hols, P., Bernard, E., Rolain, T., Zhou, M., Siezen, R.J., Bron, P.A. (2010). The extracellular biology of the lactobacilli. FEMS Microbiology Reviews, 34(2), 199-230. https://doi.org/10.1111/j.1574-6976.2009.00208.x
  • Konstantinov, S.R., Smidt, H., de Vos, W.M., Bruijns, S.C.M., Singh, S.K., Valence, F., Molle, D., Lortal, S., Altermann, E., Klaenhammer, T.R., van Kooyk, Y. (2008). S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proceedings of the National Academy of Sciences of the United States of America, 105(49), 19473-19478. https://doi.org/10.1073/pnas.0810305105
  • Krishna Rao, R., Samak, G. (2013). Protection and Restitution of Gut Barrier by Probiotics: Nutritional and Clinical Implications. Current Nutrition and Food Science, 9(2), 99-107. https://doi.org/10.2174/1573401311309020004
  • Kumar, H., Kawai, T., Akira, S. (2011). Pathogen Recognition by the Innate Immune System. International Reviews of Immunology, 30(1), 16-34. https://doi.org/10.3109/08830185.2010.529976
  • Kumar, M., Kumar, A., Nagpal, R., Mohania, D., Behare, P., Verma, V., Kumar, P., Poddar, D., Aggarwal, P.K., Henry, C.J.K., Jain, S., Yadav, H. (2010). Cancer-preventing attributes of probiotics: An update. International Journal of Food Sciences and Nutrition, 61(5), 473-496. https://doi.org/10.3109/09637480903455971
  • Kumar, H., Kawai, T., Shizuo, A. (2009). Toll-like receptors and innate immunity. Biochemical and Biophysical Research Communications, 388(4), 621-625. https://doi.org/10.1016/j.bbrc.2009.08.062
  • Lebeer, S., Claes, I., Tytgat, H.L.P., Verhoeven, T.L.A., Marien, E., von Ossowski, I., Reunanen, J., Palva, A., de Vos, W.M., De Keersmaecker, S.C.J., Vanderleyden, J. (2012). Functional analysis of lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Applied and Environmental Microbiology, 78(1), 185-193. https://doi.org/10.1128/AEM.06192-11
  • Lebeer, S., Claes, I.J.J., Verhoeven, T.L.A., Vanderleyden, J., De Keersmaecker, S.C.J. (2011). Exopolysaccharides ofLactobacillus rhamnosusGGform a protective shield against innate immunefactors in the intestine. Microbial Biotechnology, 4(3), 368-374. https://doi.org/10.1111/j.1751-7915.2010.00199.x
  • Lebeer, S., Vanderleyden, J., De Keersmaecker, S.C.J. (2008). Genes and Molecules of Lactobacilli Supporting Probiotic Action. Microbiology and Molecular Biology Reviews, 72(4), 728-764. https://doi.org/10.1128/MMBR.00017-08
  • Lee, I.C., Tomita, S., Kleerebezem, M., Bron, P.A. (2013). The quest for probiotic effector molecules - Unraveling strain specificity at the molecular level. Pharmacological Research, 69(1), 61-74. https://doi.org/10.1016/j.phrs.2012.09.010
  • Lightfoot, Y.L., Selle, K., Yang, T., Goh, Y.J., Sahay, B., Zadeh, M., Owen, J.L., Colliou, N., Li, E., Johannssen, T., Lepenies, B., Klaenhammer, T.R., Mohamadzadeh, M. (2015). SIGNR3-dependent immune regulation by Lactobacillus acidophilus surface layer protein A in colitis. The EMBO Journal, 34(7), 881-895. https://doi.org/10.15252/embj.201490296
  • Macfarlane, G.T., Cummings, J.H. (2002). Probiotics, Infection and Immunity. Current Opinion in Infectious Diseases, 15(5), 501-506. https://doi.org/10.1097/00001432-200210000-00008
  • Matsuguchi, T., Takagi, A., Matsuzaki, T., Nagaoka, M., Ishikawa, K., Yokokura, T., Yoshikai, Y. (2003). Lipoteichoic Acids from Lactobacillus Strains Elicit Strong Tumor Necrosis Factor Alpha-Inducing Activities in Macrophages through Toll-Like Receptor 2. Clinical and Diagnostic Laboratory Immunology, 10(2), 259-266. https://doi.org/10.1128/CDLI.10.2.259-266.2003
  • Matsuki, T., Pe, T. (2013). Epithelial Cell Proliferation Arrest Induced by Lactate and Acetate from Lactobacillus casei and Bifidobacterium breve. PLoS One, 8(4), 1-8. https://doi.org/10.1371/journal.pone.0063053
  • Matsumoto, S., Hara, T., Hori, T., Mitsuyama, K., Nagaoka, M., Tomiyasu, N., Suzuki, A., Sata, M. (2005). Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clinical and Experimental Immunology, 140(3), 417-426. https://doi.org/10.1111/j.1365-2249.2005.02790.x
  • McFarland, L.V. (2006). Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. American Journal of Gastroenterology, 101, 812-822. https://doi.org/10.1111/j.1572-0241.2006.00465.x
  • Meijerink, M., Van Hemert, S., Taverne, N., Wels, M., de Vos, P., Bron, P.A., Savelkoul, F., van Bilsen, J., Kleerebezem, M., Wells, J.M. (2010). Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One, 5(5), e10632. https://doi.org/10.1371/journal.pone.0010632
  • Melmed, G., Thomas, L.S., Lee, N., Tesfay, S.Y., Lukasek, K., Michelsen, K.S., Zhou, Y., Hu, B., Arditi, M., Abreu, M.T. (2003). Human Intestinal Epithelial Cells Are Broadly Unresponsive to Toll-Like Receptor 2-Dependent Bacterial Ligands: Implications for Host-Microbial Interactions in the Gut. The Journal of Immunology, 170(3), 1406-1415. https://doi.org/10.4049/jimmunol.170.3.1406
  • Meng, J., Zhu, X., Gao, S.M., Zhang, Q.X., Sun, Z., Lu, R.R. (2014). Characterization of surface layer proteins and its role in probiotic properties of three Lactobacillus strains. International Journal of Biological Macromolecules, 65, 110-114. https://doi.org/10.1016/j.ijbiomac.2014.01.024
  • Mohamadzadeh, M., Pfeiler, E.A., Brown, J.B., Zadeh, M., Gramarossa, M., Managlia, E., Bere, P., Sarraj, B., Khan, M.W., Pakanati, K.C., Ansari, M.J., O'Flaherty, S., Barrett, T., Klaenhammer, T.R. (2011). Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. PNAS, 108(1), 4623-4630. https://doi.org/10.1073/pnas.1005066107
  • Mozzi, F., Gerbino, E., Font De Valdez, G., Torino, M.I. (2009). Functionality of exopolysaccharides produced by lactic acid bacteria in an in vitro gastric system. Journal of Applied Microbiology, 107(1), 56-64. https://doi.org/10.1111/j.1365-2672.2009.04182.x
  • Murofushi, Y., Villena, J., Morie, K., Kanmani, P., Tohno, M., Shimazu, T., Aso, H., Suda, Y., Hashiguchi, K., Saito, T., Kitazawa, H. (2015). The toll-like receptor family protein RP105/MD1 complex is involved in the immunoregulatory effect of exopolysaccharides from Lactobacillus plantarum N14. Molecular Immunology, 64(1), 63-75. https://doi.org/10.1016/j.molimm.2014.10.027
  • Nagpal, R., Yadav, H., Kumar, M., Jain, S., Yamashiro, Y., Marotta, F. (2014). Probiotics, Prebiotics and Synbiotics: An Introduction. İçinde S. Ötleş (Eds.). Probiotics and Prebiotics in Food, Nutrition and Health (s. 1-24). Boca Raton: Taylor & Francis Group. ISNB 13: 978-1-4665-8624-6 https://doi.org/10.1201/b15561-2
  • Neuhaus, F. C., Baddiley, J. (2003). A Continuum of Anionic Charge: Structures and Functions of D-Alanyl-Teichoic Acids in Gram-Positive Bacteria. Microbiology and Molecular Biology Reviews, 67(4), 686-723. https://doi.org/10.1128/MMBR.67.4.686-723.2003
  • Ogura, Y., Bonen, D.K., Inohara, N., Nicolae, D.L., Chen, F.F., Ramos, R., Britton, H., Moran, T., Karaliuskas, R., Duerrk, R.H., Achkar, J.-P., Brant, S.R., Bayless, T.M., Kirschner, B.S., Hanauer, S,B., Nuñez, G.N., Cho, J.H. (2001). A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature, 411, 603-606. https://doi.org/10.1038/35079114
  • Otte, J.M., Podolsky, D.K. (2004). Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. American Journal of Physiology-Gastrointestinal and Liver Physiology, 286(4), G613-G626. https://doi.org/10.1152/ajpgi.00341.2003
  • Ouwehand, A.C., Salminen, S., Isolauri, E. (2002). Probiotics : an overview of beneficial effects. Antonie van Leeuwenhoek, 82, 279-289. https://doi.org/10.1023/A:1020620607611
  • Pandey, K.R., Naik, S.R., Vakil, B.V. (2015). Probiotics, prebiotics and synbiotics- a review. Association of Food Scientists and Technologists, 52(12), 7577-7587. https://doi.org/10.1007/s13197-015-1921-1
  • Parvez, S., Malik, K.A., Ah Kang, S., Kim, H.Y. (2006). Probiotics and their fermented food products are beneficial for health. Journal of Applied Microbiology, 100(6), 1171-1185. https://doi.org/10.1111/j.1365-2672.2006.02963.x
  • Rafter, J. (2002). Lactic acid bacteria and cancer: mechanistic perspective. British Journal of Nutrition, 88(1), 89-94. https://doi.org/10.1079/BJN2002633
  • Reunanen, J., von Ossowski, I., Hendrickx, A.P.A., Palva, A., de Vosa, W.M. (2012). Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Applied and Environmental Microbiology, 78(7), 2337-2344. https://doi.org/10.1128/AEM.07047-11
  • Rodgers, S. (2008). Novel applications of live bacteria in food services: probiotics and protective cultures. Trends in Food Science and Technology, 19(4), 188-197. https://doi.org/10.1016/j.tifs.2007.11.007
  • Ruas-Madiedo, P., Medrano, M., Salazar, N., De Los Reyes-Gavilán, C.G., Pérez, P.F., Abraham, A.G. (2010). Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. Journal of Applied Microbiology, 109(6), 2079-2086. https://doi.org/10.1111/j.1365-2672.2010.04839.x
  • Ruiz, L., Hevia, A., Bernardo, D., Margolles, A., Sánchez, B. (2014). Extracellular molecular effectors mediating probiotic attributes. FEMS Microbiology Letters, 359(1), 1-11. https://doi.org/10.1111/1574-6968.12576
  • Rupa, P., Mine, Y. (2012). Recent advances in the role of probiotics in human In flammation and gut health. Journal of Agricultural and Food Chemistry, 60(34), 8249-8256. https://doi.org/10.1021/jf301903t
  • Saber, R., Zadeh, M., Pakanati, K.C., Bere, P., Klaenhammer, T., Mansour, M. (2011). Lipoteichoic acid-deficient Lactobacillus acidophilus regulates downstream signals. Immunotherapy, 3(3), 337-347. https://doi.org/10.2217/imt.10.119
  • Sağdıç, O., Küçüköner, E., Özçelik, S. (2004). Probiyotik ve Prebiyotiklerin Fonksiyonel Özellikleri. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 35(3-4), 221-228.
  • Sarkar, A., Mandal, S. (2016). Bifidobacteria-Insight into clinical outcomes and mechanisms of its probiotic action. Microbiological Research, 192, 159-171. https://doi.org/10.1016/j.micres.2016.07.001
  • Sarkar, S. (2013). Probiotics as functional foods: gut colonization and safety concerns. Nutrition and Food Science, 43(5), 496-504. https://doi.org/10.1108/NFS-10-2011-0120
  • Schell, M.A., Karmirantzou, M., Snel, B., Vilanova, D., Berger, B., Pessi, G., Zwahlen, M.-C., Desiere, F., Bork, P., Delley, M., Pridmore, R.D., Arigoni, F. (2002). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proceedings of the National Academy of Sciences, 99(22), 14422-14427. https://doi.org/10.1073/pnas.212527599
  • Schlee, M., Harder, J., Köten, B., Stange, E.F., Wehkamp, J., Fellermann, K. (2008). Probiotic lactobacilli and VSL#3 induce enterocyte β-defensin 2. Clinical and Experimental Immunology, 151(3), 528-535. https://doi.org/10.1111/j.1365-2249.2007.03587.x
  • Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T.A., Stange, E.F., Fellermann, K. (2007). Induction of human β-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infection and Immunity, 75(5), 2399-2407. https://doi.org/10.1128/IAI.01563-06
  • Seth, A., Yan, F., Polk, D.B., Rao, R.K. (2008). Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. American Journal of Physiology-Gastrointestinal and Liver Physiology, 294(4), 1060-1069. https://doi.org/10.1152/ajpgi.00202.2007
  • Sheil, B., Shanahan, F., O'Mahony, L. (2007). Probiotic effects on inflammatory bowel disease. The Journal of Nutrition, 137(3), 819-824. https://doi.org/10.1093/jn/137.3.819S
  • Shida, K., Kiyoshima-Shibata, J., Kaji, R., Nagaoka, M., Nanno, M. (2009). Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology, 128(1pt2), 858-869. https://doi.org/10.1111/j.1365-2567.2009.03095.x
  • Singh, K., Kallali, B., Kumar, A., Thaker, V. (2011). Probiotics: A review. Asian Pacific Journal of Tropical Biomedicine, 1(2), 287-290. https://doi.org/10.1016/S2221-1691(11)60174-3
  • Sudha, R.M., Bhonagiri, S. (2012). Efficacy of Bacillus Coagulans Strain Unique Is-2 in the Treatment of Patients With Acute Diarrhea. International Journal of Probiotics and Prebiotics, 7(1), 33-37.
  • Tabasco, R., Fernández, P., Palencia, D., Fontecha, J., Peláez, C., Requena, T. (2014). Competition mechanisms of lactic acid bacteria and bi fi dobacteria : Fermentative metabolism and colonization. LWT - Food Science and Technology, 55(2), 680-684. https://doi.org/10.1016/j.lwt.2013.10.004
  • Tanaka, Y., Kanazawa, M., Fukudo, S., Drossman, D.A. (2011). Biopsychosocial model of irritable bowel syndrome. Journal of Neurogastroenterology and Motility, 17(2), 131-139. https://doi.org/10.5056/jnm.2011.17.2.131
  • Tsilingiri, K., Rescigno, M. (2013). Postbiotics : what else ?. Beneficial Microbes, 4(1), 101-107. https://doi.org/10.3920/BM2012.0046
  • Turroni, F., Serafini, F., Foroni, E., Duranti, S., O'Connell Motherway, M., Taverniti, V., Mangifesta, M., Milani, C., Viappiani, A., Roversi, T., Sánchez, B., Santoni, A., Gioiosa, L., Ferrarini, A., Delledonne, M., Margolles, A., Piazza, L., Palanza, 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. Proceedings of the National Academy of Sciences of the United States of America, 110(27), 11151-11156. https://doi.org/10.1073/pnas.1303897110
  • Tytgat, H.L.P., Douillard, F.P., Reunanen, J., Rasinkangas, P., Hendrickx, A.P.A., Laine, P.K., Paulin, L., Satokari, R., Vos, W.M. de. (2016). Lactobacillus rhamnosus GG Outcompetes Enterococcus faecium via Mucus-Binding Pili: Evidence for a Novel and Heterospecific Probiotic Mechanism. Applied and Environmental Microbiology, 82(19), 5756-5762. https://doi.org/10.1128/AEM.01243-16
  • Van Hemert, S., Meijerink, M., Molenaar, D., Bron, P. A., De Vos, P., Kleerebezem, M., Wells, J., M. Marco, M. L. (2010). Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiology, 10(293), 1-13. https://doi.org/10.1186/1471-2180-10-293
  • Vargas García, C.E., Petrova, M., Claes, I.J.J., De Boeck, I., Verhoeven, T.L.A., Dilissen, E., Von Ossowski, I., Palva, A., Bullens, D.M., Vanderleyden, J., Lebeer, S. (2015). Piliation of Lactobacillus rhamnosus GG promotes adhesion, phagocytosis, and cytokine modulation in macrophages. Applied and Environmental Microbiology, 81(6), 2050-2062. https://doi.org/10.1128/AEM.03949-14
  • Veerappan, G.R., Betteridge, J., Young, P.E. (2012). Probiotics for the treatment of inflammatory bowel disease. Current Gastroenterology Reports, 14(4), 324-333. https://doi.org/10.1007/s11894-012-0265-5
  • Vidal, K., Donnet-Hughes, A., Granato, D. (2002). Lipoteichoic Acids from Lactobacillus johnsonii Strain La1 and Lactobacillus acidophilus Strain La10 Antagonize the Responsiveness of Human Intestinal Epithelial HT29 Cells to Lipopolysaccharide and Gram-Negative Bacteria. Infection and Immunity, 70(4), 2057-2064. https://doi.org/10.1128/IAI.70.4.2057-2064.2002
  • Villena, J., Alvarez, S., Kitazawa, H. (2013). Introduction. İçinde Kitazawa, H., Villena, J. ve Alvarez, S. (Eds.), Probiotics: Immunobiotica And Immunogenics (s. 1-11). Boca Raton: Taylor & Francis Group. ISNB 978-1-4822-0685-2 https://doi.org/10.1201/b15532-2
  • Von Schillde, M.A., Hörmannsperger, G., Weiher, M., Alpert, C.A., Hahne, H., Bäuerl, C., Van Huynegem, K., Steidler, L., Hrncir, T., Pérez-Martínez, G., Kuster, B., Haller, D. (2012). Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host and Microbe, 11(4), 387-396. https://doi.org/10.1016/j.chom.2012.02.006
  • Wu, M.H., Tzu-Ming P., Yu-Jen, W., Chang, S.J., Chang, M.S., Hu, C.Y. (2010). Exopolysaccharide activities from probiotic bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. International Journal of Food Microbiology, 144(1), 104-110. https://doi.org/10.1016/j.ijfoodmicro.2010.09.003
  • Yan, F., Liu, L., Dempsey, P.J., Tsai, Y.H., Raines, E.W., Wilson, C.L., Cao, H., Cao, Z., Liu, L., Polk, D.B. (2013). A lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. Journal of Biological Chemistry, 288(42), 30742-30751. https://doi.org/10.1074/jbc.M113.492397
  • Yan, F., Cao, H., Cover, T.L., Whitehead, R., Washington, M.K., Polk, D.B. (2007). Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell sur vival and growth. Gastroenterology, 132(2), 562-575. https://doi.org/10.1053/j.gastro.2006.11.022
  • Yasuda, E., Serata, M., Sako, T. (2008). Suppressive effect on activation of macrophages by Lactobacillus casei strain shirota genes determining the synthesis of cell wall-associated polysaccharides. Applied and Environmental Microbiology, 74(15), 4746-4755. https://doi.org/10.1128/AEM.00412-08

PROBİYOTİK- İNSAN BAĞIŞIKLIK SİSTEMİ ETKİLEŞİMLERİ

Year 2019, Volume: 5 Issue: 4, 265 - 280, 01.10.2019

Dicle Dilara Akpınar , Burcu Kaplan Türköz

https://doi.org/10.3153/FH19027

Abstract

Probiyotikler
yeterli miktarda tüketildiklerinde sağlık üzerine yararlı etkiler gösteren
canlı mikroorganizmalardır. Bu mikroorganizmalar, patojenlerle mücadele, epitel
hücre kararlılığını sağlama ve bağışıklık sistemini düzenleyebilmeleri ile
sağlık üzerine olumlu etkiler göstermektedirler. Bağışıklık düzenleyici,
anti-inflamatuar, anti-mikrobiyal, anti-oksidan etkilerini, açığa çıkardıkları
metabolitleriyle, ürettikleri moleküllerle ve hücre yapı bileşenleriyle
sağlamaktadırlar. Peptidoglikan, teikoik asit, lipoteikoik asit, hücre yüzey
polisakkaritleri, salgılanan proteinler ve yüzey proteinleri gibi probiyotik
etken molekülleri doğal bağışıklıkta görevli reseptörler tarafından tanınarak
bağışıklık sistemini harekete geçirmektedir. Yapılan çalışmalarla bu etken
moleküllerinden bazılarının etki mekanizmaları aydınlatılmıştır.Bu derlemede
probiyotiklerin, probiyotik-konak etkileşimleri için kullandıkları bilinen
etken molekülleri hakkında ve etkileri üzerine bilgi verilmesi amaçlanmıştır.

Keywords

Probiyotikler Sağlık etkileri Probiyotik-konak etkileşimleri Bağışıklık düzenleme Etken moleküller

Thanks

Bu derlemedeki bilgi birikiminin oluşmasına katkı sağlayan TÜBİTAK-KBAG (Proje No: 116Z299) ve Ege Üniversitesi Bilimsel Araştırma Projesi (Proje No: 16-Müh-083) desteklerine teşekkür ederiz.

References

  • Agrawal, R. (2005). Probiotics: An emerging food supplement with health benefits. Food Biotechnology, 19(3), 227-246. https://doi.org/10.1080/08905430500316474
  • Aguilar-Toalá, J.E., Garcia-Varela, R., Garcia, H.S., Mata-Haro, V., González-Córdova, A.F., Vallejo-Cordoba, B., Hernández-Mendoza, A. (2018). Postbiotics: An evolving term within the functional foods field. Trends in Food Science & Technology, 75, 105-114. https://doi.org/10.1016/j.tifs.2018.03.009
  • Akira, S., Uematsu, S., Takeuchi, O. (2006). Pathogen recognition and innate immunity. Cell, 124(4), 783-801. https://doi.org/10.1016/j.cell.2006.02.015
  • Al-Hassi, H.O., Mann, E.R., Sanchez, B., English, N.R., Peake, S.T.C., Landy, J., Man, R., Urdaci, M., Hart, A. L., Fernandez-Salazar, L., Lee, G.H., Garrote, J.A., Arranz, E., Margolles, A., Stagg, A.J., Knight, S.C., Bernardo, D. (2014). Altered human gut dendritic cell properties in ulcerative colitis are reversed by Lactobacillus plantarum extracellular encrypted peptide STp. Molecular Nutrition and Food Research, 58(5), 1132-1143. https://doi.org/10.1002/mnfr.201300596
  • Bäuerl, C., Pérez-Martínez, G., Yan, F., Polk, D.B., Monedero, V. (2010). Functional analysis of the p40 and p75 proteins from lactobacillus casei BL23. Journal of Molecular Microbiology and Biotechnology, 19, 231-241. https://doi.org/10.1159/000322233
  • Bernardo, D., Sánchez, B., Al-Hassi, H.O., Mann, E.R., Urdaci, M.C., Knight, S.C., Margolles, A. (2012). Microbiota/host crosstalk biomarkers: Regulatory response of human intestinal dendritic cells exposed to Lactobacillus extracellular encrypted peptide. PLoS ONE, 7(5), 1-8. https://doi.org/10.1371/journal.pone.0036262
  • Boirivant, M., Strober, W. (2007). The mechanism of action of probiotics. Current Opinion in Gastroenterology, 23(6), 679-692. https://doi.org/10.1097/MOG.0b013e3282f0cffc
  • Bron, P.A., Tomita, S., van Swam, I.I., Remus, D.M., Meijerink, M., Wels, M., Okada, S., Wells, J.M., Kleerebezem, M. (2012a). Lactobacillus plantarum possesses the capability for wall teichoic acid backbone alditol switching. Microbial Cell Factories, 11(123), 1-15. https://doi.org/10.1186/1475-2859-11-123
  • Bron, P. A., Van Baarlen, P., Kleerebezem, M. (2012b). Emerging molecular insights into the interaction between probiotics and the host intestinal mucosa. Nature Reviews Microbiology, 10, 66-78. https://doi.org/10.1038/nrmicro2690
  • Chapot-Chartier, M.P., Kulakauskas, S. (2014). Cell wall structure and function in lactic acid bacteria. Microbial Cell Factories, 13(1), 1-23. https://doi.org/10.1186/1475-2859-13-S1-S9
  • Ciszek-Lenda, M., Nowak, B., Śróttek, M., Gamian, A., Marcinkiewicz, J. (2011). Immunoregulatory potential of exopolysaccharide from Lactobacillus rhamnosus KL37. Effects on the production of inflammatory mediators by mouse macrophages. International Journal of Experimental Pathology, 92(6), 382-391. https://doi.org/10.1111/j.1365-2613.2011.00788.x
  • Claes, I.J.J., Segers, M.E., Verhoeven, T.L.A., Dusselier, M., Sels, B.F., De Keersmaecker, S.C.J., Sigrid, C.J., Vanderleyden, J., Lebeer, S. (2012). Lipoteichoic acid is an important microbe-associated molecular pattern of Lactobacillus rhamnosus GG. Microbial Cell Factories, 11(161), 1-8. https://doi.org/10.1186/1475-2859-11-161
  • Claes, I.J.J., Lebeer, S., Shen, C., Verhoeven, T.L.A., Dilissen, E., De Hertogh, G., Bullens, D.M.A., Ceuppens, J.L., Van Assche, G., Vermeire, S., Rutgeerts, P., Vanderleyden, J., De Keersmaecker, S.C.J. (2010). Impact of lipoteichoic acid modification on the performance of the probiotic Lactobacillus rhamnosus GG in experimental colitis. Clinical and Experimental Immunology, 162(2), 306-314. https://doi.org/10.1111/j.1365-2249.2010.04228.x
  • Corcoran, B. M., Stanton, C., Fitzgerald, G., Ross, R. P. (2008). Life Under Stress : The Probiotic Stress Response and How it may be Manipulated. Current Pharmaceutical Design, 14(14), 1382-1399. https://doi.org/10.2174/138161208784480225
  • Corr, S.C., Li, Y., Riedel, C.U., O'Toole, P.W., Hill, C., Gahan, C.G.M. (2007). Bacteriocin production as a mechanism for the antiinfective activity of Lactobacillus salivarius UCC118. PNAS, 104(18), 7617-7621. https://doi.org/10.1073/pnas.0700440104
  • Delcour, J., Ferain, T., Deghorain, M., Palumbo, E., Hols, P. (1999). The biosynthesis and functionality of the cell-wall of lactic acid bacteria. Antonie van Leeuwenhoek, 76, 159-84. https://doi.org/10.1023/A:1002089722581
  • Fanning, S., Hall, L.J., Cronin, M., Zomer, A., MacSharry, J., Goulding, D., O'Connell Motherway, M., Shanahan, F., Nally, K., Dougan, G., van Sinderen, D. (2012). Bifidobacterial surface-exopolysaccharide facilitates commensal-host interaction through immune modulation and pathogen protection. Proceedings of the National Academy of Sciences, 109(6), 2108-2113. https://doi.org/10.1073/pnas.1115621109
  • FAO/WHO. (2002). Guidelines for the evalution of probiotics in food. Food and Agriculture Organization of the United Nations/World Health Organization, London, Ontario. p. 413-426.
  • Fernandez, E.M., Valenti, V., Rockel, C., Hermann, C., Pot, B., Boneca, I.G., Grangette, C. (2011). Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut, 60, 1050-1059. https://doi.org/10.1136/gut.2010.232918
  • Fotiadis, C.I., Stoidis, C.N., Spyropoulos, B.G., Zografos, E.D. (2008). Role of probiotics, prebiotics and synbiotics in chemoprevention for colorectal cancer. World Journal of Gastroenterology, 14(42), 6453-6457. https://doi.org/10.3748/wjg.14.6453
  • Ganguli, K., Collado, M.C., Rautava, J., Lu, L., Satokari, R., Von Ossowski, I., Reunanen, J., De Vos, W.M., Palva, A., Isolauri, E., Salminen, S., Walker, W.A., Rautava, S. (2015). Lactobacillus rhamnosus GG and its SpaC pilus adhesin modulate inflammatory responsiveness and TLR-related gene expression in the fetal human gut. Pediatric Research, 77, 528-535. https://doi.org/10.1038/pr.2015.5
  • Girardin, S.E., Boneca, I.G., Viala, J., Chamaillard, M., Labigne, A., Thomas, G., Philpott, D.J., Sansonetti, P.J. (2003). Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. Journal of Biological Chemistry, 278, 8869-8872. https://doi.org/10.1074/jbc.C200651200
  • Gıda, Tarım ve Hayvancılık Bakanlığı (2011). Türk gıda kodeksi etiketleme yönetmeliği. http://www.resmigazete.gov.tr/eskiler/2011/12/20111229M3-7.htm (Erişim tarihi 28.01.2019)
  • Gleeson, J.P. (2017). Diet, food components and the intestinal barrier. Nutrition Bulletin, 42(2), 123-131. https://doi.org/10.1111/nbu.12260
  • Gotteland, M., Brunser, O., Cruchet, S. (2006). Systematic review: Are probiotics useful in controlling gastric colonization by Helicobacter pylori? Alimentary Pharmacology and Therapeutics, 23(8), 1077-1086. https://doi.org/10.1111/j.1365-2036.2006.02868.x
  • Guarner, F., Perdigon, G., Corthier, G., Salminen, S., Koletzko, B., Morelli, L. (2005). Should yoghurt cultures be considered probiotic? British Journal of Nutrition, 93(6), 783-786. https://doi.org/10.1079/BJN20051428
  • Gürsoy, O., Kınık, Ö., Gönen, İ. (2005). Probiyotikler ve gastrointestinal sağlığa etkileri. Türk Mikrobiyoloji Cemiyeti Dergisi, 35(2), 136-148.
  • Hafez, M., Hayes, K., Goldrick, M., Warhurst, G., Grencis, R., Roberts, I.S. (2009). The K5 capsule of Escherichia coli strain Nissle 1917 is important in mediating interactions with intestinal epithelial cells and chemokine induction. Infection and Immunity, 77(7), 2995-3003. https://doi.org/10.1128/IAI.00040-09
  • Hevia, A., Delgado, S., Sánchez, B., Margolles, A. (2015). Molecular players involved in the interaction between beneficial bacteria and the immune system. Frontiers in Microbiology, 6, 1-8. https://doi.org/10.3389/fmicb.2015.01285
  • Hirose, Y., Murosaki, S., Fujiki, T., Yamamoto, Y., Yoshikai, Y., Yamashita, M. (2010). Lipoteichoic acids on Lactobacillus plantarum cell surfaces correlate with induction of interleukin-12p40 production. Microbiology and Immunology, 54(3), 143-151. https://doi.org/10.1111/j.1348-0421.2009.00189.x
  • Hoveyda, N., Heneghan, C., Mahtani, K.R., Perera, R., Roberts, N., Glasziou, P. (2009). A systematic review and meta-analysis: Probiotics in the treatment of irritable bowel syndrome. BMC Gastroenterology, 9(15), 1-11. https://doi.org/10.1186/1471-230X-9-15
  • Hynönen, U., Palva, A. (2013). Lactobacillus surface layer proteins: Structure, function and applications. Applied Microbiology and Biotechnology, 97(12), 5225-5243. https://doi.org/10.1007/s00253-013-4962-2
  • Ivanov, D., Emonet, C., Foata, F., Affolter, M., Delley, M., Fisseha, M., Blum-Sperisen, S., Kochhar, S., Arigoni, F. (2006). A serpin from the gut bacterium Bifidobacterium longum inhibits eukaryotic elastase-like serine proteases. Journal of Biological Chemistry, 281, 17246-17252. https://doi.org/10.1074/jbc.M601678200
  • Johnson-Henry, K.C., Hagen, K.E., Gordonpour, M., Tompkins, T.A., Sherman, P.M. (2007). Surface-layer protein extracts from Lactobacillus helveticus inhibit enterohaemorrhagic Escherichia coli O157:H7 adhesion to epithelial cells. Cellular Microbiology, 9(2), 356-367. https://doi.org/10.1111/j.1462-5822.2006.00791.x
  • Kaji, R., Kiyoshima-Shibata, J., Nagaoka, M., Nanno, M., Shida, K. (2010). Bacterial Teichoic Acids Reverse Predominant IL-12 Production Induced by Certain Lactobacillus Strains into Predominant IL-10 Production via TLR2-Dependent ERK Activation in Macrophages. The Journal of Immunology, ji_0901569, 1-9. https://doi.org/10.4049/jimmunol.0901569
  • Kalliomäki, M.A., Isolauri, E. (2004). Probiotics and down-regulation of the allergic response. Immunology and Allergy Clinics of North America, 24(4), 739-752. https://doi.org/10.1016/j.iac.2004.06.006
  • Kang, H., Im, S. (2015). Probiotics as an Immune Modulator. Journal of Nutritional Science and Vitaminology, 61, 103-105. https://doi.org/10.3177/jnsv.61.S103
  • Kawai, T., Akira, S. (2011). Toll-like Receptors and Their Crosstalk with Other Innate Receptors in Infection and Immunity. Immunity, 34(5), 637-650. https://doi.org/10.1016/j.immuni.2011.05.006
  • Kelesidis, T., Pothoulakis, C. (2012). Efficacy and safety of the probiotic Saccharomyces boulardii for the prevention and therapy of gastrointestinal disorders. Therapeutic Advances in Gastroenterology, 5(2), 111-125. https://doi.org/10.1177/1756283X11428502
  • Khazaie, K., Zadeh, M., Khan, M.W., Bere, P., Gounari, F., Dennis, K., Blatner, N.R., Owen, J.L., Klaenhammer, T.R., Mohamadzadeh, M. (2012). Abating colon cancer polyposis by Lactobacillus acidophilus deficient in lipoteichoic acid. Proceedings of the National Academy of Sciences, 109(26), 10462-10467. https://doi.org/10.1073/pnas.1207230109
  • Kim, H., Lee, S., Kim, N., Ko, M., Lee, J., Yi, T., Chung, S.K., Chung, D. (2008). Inhibitory effects of Lactobacillus plantarum lipoteichoic acid (LTA) on Staphylococcus aureus LTA-induced tumor necrosis factor-alpha production. Journal of Microbiology and Biotechnology, 18(6), 1191-1996.
  • Kleerebezem, M., Binda, S., Bron, P.A., Gross, G., Hill, C., van Hylckama Vlieg, J.E., Lebeer, S., Satokari, R., Ouwehand, A.C. (2019). Understanding mode of action can drive the translational pipeline towards more reliable health benefits for probiotics. Current Opinion in Biotechnology, 56, 55-60. https://doi.org/10.1016/j.copbio.2018.09.007
  • Kleerebezem, M., Hols, P., Bernard, E., Rolain, T., Zhou, M., Siezen, R.J., Bron, P.A. (2010). The extracellular biology of the lactobacilli. FEMS Microbiology Reviews, 34(2), 199-230. https://doi.org/10.1111/j.1574-6976.2009.00208.x
  • Konstantinov, S.R., Smidt, H., de Vos, W.M., Bruijns, S.C.M., Singh, S.K., Valence, F., Molle, D., Lortal, S., Altermann, E., Klaenhammer, T.R., van Kooyk, Y. (2008). S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proceedings of the National Academy of Sciences of the United States of America, 105(49), 19473-19478. https://doi.org/10.1073/pnas.0810305105
  • Krishna Rao, R., Samak, G. (2013). Protection and Restitution of Gut Barrier by Probiotics: Nutritional and Clinical Implications. Current Nutrition and Food Science, 9(2), 99-107. https://doi.org/10.2174/1573401311309020004
  • Kumar, H., Kawai, T., Akira, S. (2011). Pathogen Recognition by the Innate Immune System. International Reviews of Immunology, 30(1), 16-34. https://doi.org/10.3109/08830185.2010.529976
  • Kumar, M., Kumar, A., Nagpal, R., Mohania, D., Behare, P., Verma, V., Kumar, P., Poddar, D., Aggarwal, P.K., Henry, C.J.K., Jain, S., Yadav, H. (2010). Cancer-preventing attributes of probiotics: An update. International Journal of Food Sciences and Nutrition, 61(5), 473-496. https://doi.org/10.3109/09637480903455971
  • Kumar, H., Kawai, T., Shizuo, A. (2009). Toll-like receptors and innate immunity. Biochemical and Biophysical Research Communications, 388(4), 621-625. https://doi.org/10.1016/j.bbrc.2009.08.062
  • Lebeer, S., Claes, I., Tytgat, H.L.P., Verhoeven, T.L.A., Marien, E., von Ossowski, I., Reunanen, J., Palva, A., de Vos, W.M., De Keersmaecker, S.C.J., Vanderleyden, J. (2012). Functional analysis of lactobacillus rhamnosus GG pili in relation to adhesion and immunomodulatory interactions with intestinal epithelial cells. Applied and Environmental Microbiology, 78(1), 185-193. https://doi.org/10.1128/AEM.06192-11
  • Lebeer, S., Claes, I.J.J., Verhoeven, T.L.A., Vanderleyden, J., De Keersmaecker, S.C.J. (2011). Exopolysaccharides ofLactobacillus rhamnosusGGform a protective shield against innate immunefactors in the intestine. Microbial Biotechnology, 4(3), 368-374. https://doi.org/10.1111/j.1751-7915.2010.00199.x
  • Lebeer, S., Vanderleyden, J., De Keersmaecker, S.C.J. (2008). Genes and Molecules of Lactobacilli Supporting Probiotic Action. Microbiology and Molecular Biology Reviews, 72(4), 728-764. https://doi.org/10.1128/MMBR.00017-08
  • Lee, I.C., Tomita, S., Kleerebezem, M., Bron, P.A. (2013). The quest for probiotic effector molecules - Unraveling strain specificity at the molecular level. Pharmacological Research, 69(1), 61-74. https://doi.org/10.1016/j.phrs.2012.09.010
  • Lightfoot, Y.L., Selle, K., Yang, T., Goh, Y.J., Sahay, B., Zadeh, M., Owen, J.L., Colliou, N., Li, E., Johannssen, T., Lepenies, B., Klaenhammer, T.R., Mohamadzadeh, M. (2015). SIGNR3-dependent immune regulation by Lactobacillus acidophilus surface layer protein A in colitis. The EMBO Journal, 34(7), 881-895. https://doi.org/10.15252/embj.201490296
  • Macfarlane, G.T., Cummings, J.H. (2002). Probiotics, Infection and Immunity. Current Opinion in Infectious Diseases, 15(5), 501-506. https://doi.org/10.1097/00001432-200210000-00008
  • Matsuguchi, T., Takagi, A., Matsuzaki, T., Nagaoka, M., Ishikawa, K., Yokokura, T., Yoshikai, Y. (2003). Lipoteichoic Acids from Lactobacillus Strains Elicit Strong Tumor Necrosis Factor Alpha-Inducing Activities in Macrophages through Toll-Like Receptor 2. Clinical and Diagnostic Laboratory Immunology, 10(2), 259-266. https://doi.org/10.1128/CDLI.10.2.259-266.2003
  • Matsuki, T., Pe, T. (2013). Epithelial Cell Proliferation Arrest Induced by Lactate and Acetate from Lactobacillus casei and Bifidobacterium breve. PLoS One, 8(4), 1-8. https://doi.org/10.1371/journal.pone.0063053
  • Matsumoto, S., Hara, T., Hori, T., Mitsuyama, K., Nagaoka, M., Tomiyasu, N., Suzuki, A., Sata, M. (2005). Probiotic Lactobacillus-induced improvement in murine chronic inflammatory bowel disease is associated with the down-regulation of pro-inflammatory cytokines in lamina propria mononuclear cells. Clinical and Experimental Immunology, 140(3), 417-426. https://doi.org/10.1111/j.1365-2249.2005.02790.x
  • McFarland, L.V. (2006). Meta-analysis of probiotics for the prevention of antibiotic associated diarrhea and the treatment of Clostridium difficile disease. American Journal of Gastroenterology, 101, 812-822. https://doi.org/10.1111/j.1572-0241.2006.00465.x
  • Meijerink, M., Van Hemert, S., Taverne, N., Wels, M., de Vos, P., Bron, P.A., Savelkoul, F., van Bilsen, J., Kleerebezem, M., Wells, J.M. (2010). Identification of genetic loci in Lactobacillus plantarum that modulate the immune response of dendritic cells using comparative genome hybridization. PLoS One, 5(5), e10632. https://doi.org/10.1371/journal.pone.0010632
  • Melmed, G., Thomas, L.S., Lee, N., Tesfay, S.Y., Lukasek, K., Michelsen, K.S., Zhou, Y., Hu, B., Arditi, M., Abreu, M.T. (2003). Human Intestinal Epithelial Cells Are Broadly Unresponsive to Toll-Like Receptor 2-Dependent Bacterial Ligands: Implications for Host-Microbial Interactions in the Gut. The Journal of Immunology, 170(3), 1406-1415. https://doi.org/10.4049/jimmunol.170.3.1406
  • Meng, J., Zhu, X., Gao, S.M., Zhang, Q.X., Sun, Z., Lu, R.R. (2014). Characterization of surface layer proteins and its role in probiotic properties of three Lactobacillus strains. International Journal of Biological Macromolecules, 65, 110-114. https://doi.org/10.1016/j.ijbiomac.2014.01.024
  • Mohamadzadeh, M., Pfeiler, E.A., Brown, J.B., Zadeh, M., Gramarossa, M., Managlia, E., Bere, P., Sarraj, B., Khan, M.W., Pakanati, K.C., Ansari, M.J., O'Flaherty, S., Barrett, T., Klaenhammer, T.R. (2011). Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. PNAS, 108(1), 4623-4630. https://doi.org/10.1073/pnas.1005066107
  • Mozzi, F., Gerbino, E., Font De Valdez, G., Torino, M.I. (2009). Functionality of exopolysaccharides produced by lactic acid bacteria in an in vitro gastric system. Journal of Applied Microbiology, 107(1), 56-64. https://doi.org/10.1111/j.1365-2672.2009.04182.x
  • Murofushi, Y., Villena, J., Morie, K., Kanmani, P., Tohno, M., Shimazu, T., Aso, H., Suda, Y., Hashiguchi, K., Saito, T., Kitazawa, H. (2015). The toll-like receptor family protein RP105/MD1 complex is involved in the immunoregulatory effect of exopolysaccharides from Lactobacillus plantarum N14. Molecular Immunology, 64(1), 63-75. https://doi.org/10.1016/j.molimm.2014.10.027
  • Nagpal, R., Yadav, H., Kumar, M., Jain, S., Yamashiro, Y., Marotta, F. (2014). Probiotics, Prebiotics and Synbiotics: An Introduction. İçinde S. Ötleş (Eds.). Probiotics and Prebiotics in Food, Nutrition and Health (s. 1-24). Boca Raton: Taylor & Francis Group. ISNB 13: 978-1-4665-8624-6 https://doi.org/10.1201/b15561-2
  • Neuhaus, F. C., Baddiley, J. (2003). A Continuum of Anionic Charge: Structures and Functions of D-Alanyl-Teichoic Acids in Gram-Positive Bacteria. Microbiology and Molecular Biology Reviews, 67(4), 686-723. https://doi.org/10.1128/MMBR.67.4.686-723.2003
  • Ogura, Y., Bonen, D.K., Inohara, N., Nicolae, D.L., Chen, F.F., Ramos, R., Britton, H., Moran, T., Karaliuskas, R., Duerrk, R.H., Achkar, J.-P., Brant, S.R., Bayless, T.M., Kirschner, B.S., Hanauer, S,B., Nuñez, G.N., Cho, J.H. (2001). A frameshift mutation in NOD2 associated with susceptibility to Crohn's disease. Nature, 411, 603-606. https://doi.org/10.1038/35079114
  • Otte, J.M., Podolsky, D.K. (2004). Functional modulation of enterocytes by gram-positive and gram-negative microorganisms. American Journal of Physiology-Gastrointestinal and Liver Physiology, 286(4), G613-G626. https://doi.org/10.1152/ajpgi.00341.2003
  • Ouwehand, A.C., Salminen, S., Isolauri, E. (2002). Probiotics : an overview of beneficial effects. Antonie van Leeuwenhoek, 82, 279-289. https://doi.org/10.1023/A:1020620607611
  • Pandey, K.R., Naik, S.R., Vakil, B.V. (2015). Probiotics, prebiotics and synbiotics- a review. Association of Food Scientists and Technologists, 52(12), 7577-7587. https://doi.org/10.1007/s13197-015-1921-1
  • Parvez, S., Malik, K.A., Ah Kang, S., Kim, H.Y. (2006). Probiotics and their fermented food products are beneficial for health. Journal of Applied Microbiology, 100(6), 1171-1185. https://doi.org/10.1111/j.1365-2672.2006.02963.x
  • Rafter, J. (2002). Lactic acid bacteria and cancer: mechanistic perspective. British Journal of Nutrition, 88(1), 89-94. https://doi.org/10.1079/BJN2002633
  • Reunanen, J., von Ossowski, I., Hendrickx, A.P.A., Palva, A., de Vosa, W.M. (2012). Characterization of the SpaCBA pilus fibers in the probiotic Lactobacillus rhamnosus GG. Applied and Environmental Microbiology, 78(7), 2337-2344. https://doi.org/10.1128/AEM.07047-11
  • Rodgers, S. (2008). Novel applications of live bacteria in food services: probiotics and protective cultures. Trends in Food Science and Technology, 19(4), 188-197. https://doi.org/10.1016/j.tifs.2007.11.007
  • Ruas-Madiedo, P., Medrano, M., Salazar, N., De Los Reyes-Gavilán, C.G., Pérez, P.F., Abraham, A.G. (2010). Exopolysaccharides produced by Lactobacillus and Bifidobacterium strains abrogate in vitro the cytotoxic effect of bacterial toxins on eukaryotic cells. Journal of Applied Microbiology, 109(6), 2079-2086. https://doi.org/10.1111/j.1365-2672.2010.04839.x
  • Ruiz, L., Hevia, A., Bernardo, D., Margolles, A., Sánchez, B. (2014). Extracellular molecular effectors mediating probiotic attributes. FEMS Microbiology Letters, 359(1), 1-11. https://doi.org/10.1111/1574-6968.12576
  • Rupa, P., Mine, Y. (2012). Recent advances in the role of probiotics in human In flammation and gut health. Journal of Agricultural and Food Chemistry, 60(34), 8249-8256. https://doi.org/10.1021/jf301903t
  • Saber, R., Zadeh, M., Pakanati, K.C., Bere, P., Klaenhammer, T., Mansour, M. (2011). Lipoteichoic acid-deficient Lactobacillus acidophilus regulates downstream signals. Immunotherapy, 3(3), 337-347. https://doi.org/10.2217/imt.10.119
  • Sağdıç, O., Küçüköner, E., Özçelik, S. (2004). Probiyotik ve Prebiyotiklerin Fonksiyonel Özellikleri. Atatürk Üniversitesi Ziraat Fakültesi Dergisi, 35(3-4), 221-228.
  • Sarkar, A., Mandal, S. (2016). Bifidobacteria-Insight into clinical outcomes and mechanisms of its probiotic action. Microbiological Research, 192, 159-171. https://doi.org/10.1016/j.micres.2016.07.001
  • Sarkar, S. (2013). Probiotics as functional foods: gut colonization and safety concerns. Nutrition and Food Science, 43(5), 496-504. https://doi.org/10.1108/NFS-10-2011-0120
  • Schell, M.A., Karmirantzou, M., Snel, B., Vilanova, D., Berger, B., Pessi, G., Zwahlen, M.-C., Desiere, F., Bork, P., Delley, M., Pridmore, R.D., Arigoni, F. (2002). The genome sequence of Bifidobacterium longum reflects its adaptation to the human gastrointestinal tract. Proceedings of the National Academy of Sciences, 99(22), 14422-14427. https://doi.org/10.1073/pnas.212527599
  • Schlee, M., Harder, J., Köten, B., Stange, E.F., Wehkamp, J., Fellermann, K. (2008). Probiotic lactobacilli and VSL#3 induce enterocyte β-defensin 2. Clinical and Experimental Immunology, 151(3), 528-535. https://doi.org/10.1111/j.1365-2249.2007.03587.x
  • Schlee, M., Wehkamp, J., Altenhoefer, A., Oelschlaeger, T.A., Stange, E.F., Fellermann, K. (2007). Induction of human β-defensin 2 by the probiotic Escherichia coli Nissle 1917 is mediated through flagellin. Infection and Immunity, 75(5), 2399-2407. https://doi.org/10.1128/IAI.01563-06
  • Seth, A., Yan, F., Polk, D.B., Rao, R.K. (2008). Probiotics ameliorate the hydrogen peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. American Journal of Physiology-Gastrointestinal and Liver Physiology, 294(4), 1060-1069. https://doi.org/10.1152/ajpgi.00202.2007
  • Sheil, B., Shanahan, F., O'Mahony, L. (2007). Probiotic effects on inflammatory bowel disease. The Journal of Nutrition, 137(3), 819-824. https://doi.org/10.1093/jn/137.3.819S
  • Shida, K., Kiyoshima-Shibata, J., Kaji, R., Nagaoka, M., Nanno, M. (2009). Peptidoglycan from lactobacilli inhibits interleukin-12 production by macrophages induced by Lactobacillus casei through Toll-like receptor 2-dependent and independent mechanisms. Immunology, 128(1pt2), 858-869. https://doi.org/10.1111/j.1365-2567.2009.03095.x
  • Singh, K., Kallali, B., Kumar, A., Thaker, V. (2011). Probiotics: A review. Asian Pacific Journal of Tropical Biomedicine, 1(2), 287-290. https://doi.org/10.1016/S2221-1691(11)60174-3
  • Sudha, R.M., Bhonagiri, S. (2012). Efficacy of Bacillus Coagulans Strain Unique Is-2 in the Treatment of Patients With Acute Diarrhea. International Journal of Probiotics and Prebiotics, 7(1), 33-37.
  • Tabasco, R., Fernández, P., Palencia, D., Fontecha, J., Peláez, C., Requena, T. (2014). Competition mechanisms of lactic acid bacteria and bi fi dobacteria : Fermentative metabolism and colonization. LWT - Food Science and Technology, 55(2), 680-684. https://doi.org/10.1016/j.lwt.2013.10.004
  • Tanaka, Y., Kanazawa, M., Fukudo, S., Drossman, D.A. (2011). Biopsychosocial model of irritable bowel syndrome. Journal of Neurogastroenterology and Motility, 17(2), 131-139. https://doi.org/10.5056/jnm.2011.17.2.131
  • Tsilingiri, K., Rescigno, M. (2013). Postbiotics : what else ?. Beneficial Microbes, 4(1), 101-107. https://doi.org/10.3920/BM2012.0046
  • Turroni, F., Serafini, F., Foroni, E., Duranti, S., O'Connell Motherway, M., Taverniti, V., Mangifesta, M., Milani, C., Viappiani, A., Roversi, T., Sánchez, B., Santoni, A., Gioiosa, L., Ferrarini, A., Delledonne, M., Margolles, A., Piazza, L., Palanza, 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. Proceedings of the National Academy of Sciences of the United States of America, 110(27), 11151-11156. https://doi.org/10.1073/pnas.1303897110
  • Tytgat, H.L.P., Douillard, F.P., Reunanen, J., Rasinkangas, P., Hendrickx, A.P.A., Laine, P.K., Paulin, L., Satokari, R., Vos, W.M. de. (2016). Lactobacillus rhamnosus GG Outcompetes Enterococcus faecium via Mucus-Binding Pili: Evidence for a Novel and Heterospecific Probiotic Mechanism. Applied and Environmental Microbiology, 82(19), 5756-5762. https://doi.org/10.1128/AEM.01243-16
  • Van Hemert, S., Meijerink, M., Molenaar, D., Bron, P. A., De Vos, P., Kleerebezem, M., Wells, J., M. Marco, M. L. (2010). Identification of Lactobacillus plantarum genes modulating the cytokine response of human peripheral blood mononuclear cells. BMC Microbiology, 10(293), 1-13. https://doi.org/10.1186/1471-2180-10-293
  • Vargas García, C.E., Petrova, M., Claes, I.J.J., De Boeck, I., Verhoeven, T.L.A., Dilissen, E., Von Ossowski, I., Palva, A., Bullens, D.M., Vanderleyden, J., Lebeer, S. (2015). Piliation of Lactobacillus rhamnosus GG promotes adhesion, phagocytosis, and cytokine modulation in macrophages. Applied and Environmental Microbiology, 81(6), 2050-2062. https://doi.org/10.1128/AEM.03949-14
  • Veerappan, G.R., Betteridge, J., Young, P.E. (2012). Probiotics for the treatment of inflammatory bowel disease. Current Gastroenterology Reports, 14(4), 324-333. https://doi.org/10.1007/s11894-012-0265-5
  • Vidal, K., Donnet-Hughes, A., Granato, D. (2002). Lipoteichoic Acids from Lactobacillus johnsonii Strain La1 and Lactobacillus acidophilus Strain La10 Antagonize the Responsiveness of Human Intestinal Epithelial HT29 Cells to Lipopolysaccharide and Gram-Negative Bacteria. Infection and Immunity, 70(4), 2057-2064. https://doi.org/10.1128/IAI.70.4.2057-2064.2002
  • Villena, J., Alvarez, S., Kitazawa, H. (2013). Introduction. İçinde Kitazawa, H., Villena, J. ve Alvarez, S. (Eds.), Probiotics: Immunobiotica And Immunogenics (s. 1-11). Boca Raton: Taylor & Francis Group. ISNB 978-1-4822-0685-2 https://doi.org/10.1201/b15532-2
  • Von Schillde, M.A., Hörmannsperger, G., Weiher, M., Alpert, C.A., Hahne, H., Bäuerl, C., Van Huynegem, K., Steidler, L., Hrncir, T., Pérez-Martínez, G., Kuster, B., Haller, D. (2012). Lactocepin secreted by Lactobacillus exerts anti-inflammatory effects by selectively degrading proinflammatory chemokines. Cell Host and Microbe, 11(4), 387-396. https://doi.org/10.1016/j.chom.2012.02.006
  • Wu, M.H., Tzu-Ming P., Yu-Jen, W., Chang, S.J., Chang, M.S., Hu, C.Y. (2010). Exopolysaccharide activities from probiotic bifidobacterium: Immunomodulatory effects (on J774A.1 macrophages) and antimicrobial properties. International Journal of Food Microbiology, 144(1), 104-110. https://doi.org/10.1016/j.ijfoodmicro.2010.09.003
  • Yan, F., Liu, L., Dempsey, P.J., Tsai, Y.H., Raines, E.W., Wilson, C.L., Cao, H., Cao, Z., Liu, L., Polk, D.B. (2013). A lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. Journal of Biological Chemistry, 288(42), 30742-30751. https://doi.org/10.1074/jbc.M113.492397
  • Yan, F., Cao, H., Cover, T.L., Whitehead, R., Washington, M.K., Polk, D.B. (2007). Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell sur vival and growth. Gastroenterology, 132(2), 562-575. https://doi.org/10.1053/j.gastro.2006.11.022
  • Yasuda, E., Serata, M., Sako, T. (2008). Suppressive effect on activation of macrophages by Lactobacillus casei strain shirota genes determining the synthesis of cell wall-associated polysaccharides. Applied and Environmental Microbiology, 74(15), 4746-4755. https://doi.org/10.1128/AEM.00412-08
There are 104 citations in total.

Details

Primary Language Turkish
Subjects Food Engineering, Structural Biology
Journal Section Review Articles
Authors

Dicle Dilara Akpınar 0000-0002-8318-169X

Burcu Kaplan Türköz 0000-0003-3040-3321

Publication Date October 1, 2019
Submission Date February 6, 2019
Published in Issue Year 2019 Volume: 5 Issue: 4

Cite

APA Akpınar, D. D., & Kaplan Türköz, B. (2019). PROBİYOTİK- İNSAN BAĞIŞIKLIK SİSTEMİ ETKİLEŞİMLERİ. Food and Health, 5(4), 265-280. https://doi.org/10.3153/FH19027
 Download Cover Image

16339

Journal is licensed under a

CreativeCommons Attribtion-ShareAlike 4.0 International Licence  14627 1331027042
Diamond Open Access refers to a scholarly publication model in which journals and platforms do not charge fees to either authors or readers.

Open Access Statement:

This is an open access journal which means that all content is freely available without charge to the user or his/her institution. Users are allowed to read, download, copy, distribute, print, search, or link to the full texts of the articles, or use them for any other lawful purpose, without asking prior permission from the publisher or the author. This is in accordance with the BOAI definition of open access.

Archiving Policy:

27222

Archiving is done according to ULAKBİM "DergiPark" publication policy (LOCKSS).