Potential immunomodulatory and antiinflammatory mechanisms of probiotics

1. Pot B., Tsakalidou E. Taxonomy and metabolism of Lactobacillus. In: Ljung Å., Wadström T. (eds.) Lactobacillus molecular biology. From genomics to probiotics. 1st ed. Norfolk: Caister Academic Press 2009.

2. Grover S., Rashmi H. M., Srivastava A. K., Batish V. K. Probiotics for human health – new innovations and emerging trends. Gut Pathogens 2012; 4, 1. http://www.ncbi.nlm.nih.gov/ pmc/articles/PMC3544614/ (12. 11. 2015)

3. Foligné B., Daniel C., Pot B. Probiotics from research to market: the possibilities risks and challenges. Curr. Opin. Microbiol. 2013; 16, 284–292.

4. Nissle A. Explanations of the significance of colonic dysbacteria the mechanism of action of E. coli therapy (mutaflor). Medizinische 1959; 4, 1017–1022.

5. Behnsen J., Deriu E., Sassone-Corsi M., Raffatellu M. Probiotics: Properties, examples, and specific applications. Cold Spring Harb. Perspect. Med. 2013; 3, a010074.

6. Khatri I., Akhtar A., Kaur K., Tomar R., Prasad G. S., Ramya T. N., Subramanian S. Gleaning evolutionary insights from the genome sequence of a probiotic yeast Saccharomyces boulardii. Gut Pathog. 2013; 5. http://www.ncbi.nlm.nih.gov/pmc/ articles/PMC3843575/ (12. 11. 2015)

7. Lebeer S., Vanderleyden J., De Keersmaecker S. C. J. Genes and molecules of lactobacilli supporting probiotic action. Microbiol. Mol. Biol. Rev. 2008; 72, 728–764.

8. Kiňová Sepová H., Bilková A., Bilka F., Bezáková L. Antimikróbne pôsobiace látky produkované baktériami mliečneho kvasenia. Čes. slov. Farm. 2010; 59, 155–159.

9. Hevia A., Delgado S., Sánchez B., Margolles A. Molecular players involved in the interaction between beneficial bacteria and the immune system. Front. Microbiol. 2015; 6, 1285.

10. Kang H.-J., Im S.-H. Probiotics as an immune modulator. J. Nutr. Sci. Vitaminol. 2015; 61, S103–S105.

11. Bilková A., Kiňová Sepová H., Bilka F., Balažová A. Bakteriocíny produkované baktériami mliečneho kvasenia. Čes. slov. Farm. 2011; 60, 65–72.

12. Nagpal R., Behare P. V., Kumar M., Mohania D., Yadav M., Jain S., Menon S., Parkash O., Marotta F., Minelli E., Henry C. J., Yadav H. Milk, milk products and disease free health: an updated overview. Crit. Rev. Food Sci. Nutr. 2012; 52, 321–333.

13. Bested A. C., Logan A. C., Selhub E. M. Intestinal microbiota, probiotics and mantal health: from Metchnikoff to modern advances: Part II – contemporary contextual research. Gut Pathogens 2013; 5, 1–14.

14. Karpiňski T. M., Szkaradkiewicz A. K. Characteristic of bacteriocines and their application. Pol. J. Bacteriol. 2013; 62, 223–235.

15. Kayserová H. Potravinová alergia. Via Practica 2004; 2, 90–94.

16. Lebeer S., Vanderleyden J., De Keersmaecker S. C. J. Host interactions of probiotic bacterial surface molecules: comparison with commensals and pathogens. Microbiol. 2010; 8, 171–184.

17. Sellge G., Kufer T. A. PRR-signaling pathways: learning from microbial tactics. Semin. Immunol. 2015; 27, 75–84.

18. O’Hara A. M., Shanahan F. The gut flora as a forgotten organ. EMBO Rep. 2006; 7, 688–693.

19. Thomas C. M., Versalovic J. Probiotics-host communication. Modulation of signaling pathways in the intestine. Gut Microbes 2010; 1, 148–163.

20. Tiptiri-Kourpeti A., Spyridopoulou K., Santarmaki V., Aindelis G., Tompoulidou E., Laprianidou E. E., Saxami G., Ypsilantis P., Lampri E. S., Simopoulos C., Kotsianidis I., Galanis A., Kourkoutas Y., Dimitrellou D., Chlichlia K. Lactobacillus casei exerts anti-proliferative effects accompanied by apoptoticcell death and up-regulation of TRAIL in colon carcinoma cells. PLoS One 2016; 11: e0147960.

21. Sengupta R., Altermann E., Anderson E., Anderson R. C., McNabb W. C., Moughan P.J ., Roy N. C. The role of cell surface architecture of lactobacilli in host-microbe interactions in the gastrointestinal tract. Med. Inflamm. 2013; 237921, doi:10.1155/2013/237921

22. Mohamadzadeha M., Pfeiler E. A., Brown J. B., Zadeha M., Gramarossa M., Managlia E., Berea P., Sarraj B., Khan M. W., Pakanati K. Ch., Ansari M. J., O´Flaherty S., Barrett T., Klaenhammer T. R. Regulation of induced colonic inflammation by Lactobacillus acidophilus deficient in lipoteichoic acid. PNAS 2011; 108, 4623–4630.

23. Meshkibaf Sh., Fritz J., Gottschalk M., Kim S. O. Preferential production of G-CSF by a protein-like Lactobacillus rhamnosus GR-1 secretory factor through activating TLR2-dependent signaling events without activation of JNKs. BMC Microbiol. 2015; 15, doi:10.1186/s12866-015-0578-2.

24. Schiffrin E. J., Blum S. Interaction between the microbiota and the intestinal mucosa. Eur. J. Clin. Nutr. 2002; 56, 60–64.

25. Yousefi M., Movassaghpour A. A., Shamsasenjan K., Ghalamfarsa G., Sadreddini S., Jadidi-Niaragh F. The skewed balance between Tregs and Th17 in chronic lymphocytic leukemia. Future Oncol. 2015; 11, 1567–1582.

26. Nyirenda M. H., Morandi E., Vinkemeier U., Constantin - Teodosiu D., Drinkwater S., Mee M. TLR2 stimulation regulates the balance between regulatory T cell and Th17 function: a novel mechanism of reduced regulatory T cell function in multiple sclerosis. J. Immunol. 2015; 194, 5761–5774.

27. Takeda K., Kaisho T., Akira S. Toll-like receptors. Annu. Rev. Immunol. 2003; 21, 335–376.

28. Yoon S. I., Kurnasov O., Natarajan V., Hong M., Gudkov A. V., Osterman A. L., Wilson I. A. Structural basis of TLR5-flagellin recognition and signaling. Science 2012; 17, 859–864.

29. Park B. S., Lee J.-O. Recognition of lipopolysacharide pattern by TLR4 complexes. Exp. Mol. Med. 2013; 45, e66.

30. Dambuza I. M., Brown G. D. C-type lectins in imunity: recent developments. Curr. Opin. Immunol. 2015; 32, 21–27.

31. Claes A. K., Zhou J. Y., Philpott D. J. NOD-like receptors: guardians of intestinal mucosal barriers. Physiology (Bethesda) 2015; 30, 241–250.

32. Liu H.-Y., Roos S., Jonsson H., Ahl D., Dicksved J., Lindberg J. E. Lundh T. Effects of Lactobacillus johnsonii and Lactobacillus reuteri on gut barrier function and heat shock proteins in intestinal porcine epithelial cells. Physiol. Rep. 2015; 3, e12355.

33. Koboziev I., Karlsson F., Grisham M. B. Gut-associated lymphoid tissue, T cell trafficking, and chronic intestinal inflammation. Ann. N. Y. Acad. Sci. 2010; 1207, 86–93.

34. Demeria D., Ewaschuk J., Madsen K. Interactions of Lactobacillus with the immune system. In: Ljung Å., Wadström T. (eds.) Lactobacillus molecular biology. From genomics to probiotics. 1st ed. Norfolk: Caister Academic Press 2009.

35. Mileti E., Matteoli G., Iliev I. D., Rescigno M. Comparison of the immunomodulatory properties of three probiotic strains of Lactobacilli using complex culture systems: prediction for in vivo efficacy. PLoS One 2009; 4, e7056.

36. Caselli M., Cassol F., Caló G., Holton J., Zuliani G., Gasbarrini A. Actual concept of „probiotics“: Is it more functional to science or business? World J. Gastroenterol. 2013; 19, 1527–1540.

37. Bassaganya-Riera J., Viladomiu M., Pedragosa M., De Simone C., Carbo A., Shaykhutdinov R., Jobin Ch., Arthur J. C., Corl B. A., Vogel H., Storr M., Hontecillas R. Probiotic bacteria produce conjugated linoleic acid locally in the gut that targets macrophage PPARγ to suppress colitis. PLoS One 2012; 7, e31238.

38. Jijon H., Backer J., Diaz H., Yeung H., Thiel D., McKaigney C., De Simone C., Madsen K. DNA from probiotic bacteria modulates murine and human epitelial and immune function. Gastroenterol. 2004; 126, 1358–1373.

39. Resta-Lenert S, Barrett K. E. Probiotics and commensals reverse TNF-alpha- and IFN-gamma-induced dysfunction in human intestinal epithelial cells. Gastroenterol. 2006; 130, 731–746.

40. Sakai F., Hosoya T., Ono-Ohmachi A., Ukibe K., Ogawa A., Moriya T., Kadooka Y., Shiozaki T., Nakagawa H., Nakayama Y., Miyazaki T. Lactobacillus gasseri SBT2055 induces TGF-βα expression in dendritic cells and activates TLR2 signal to produce IgA in the small intestine. PLoS One 2014; 9, e105370.

41. De Kivit S., Tobin M. C., Forsyth C. B., Keshavarzian A., Landay A. Regulation of intestinal immune responses through TLR activation: implication for pro- and prebiotics. Front. Microbiol. 2014; 5, 1–7.

42. Galdeano C. M., Perdigón G. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate imunity. Clin. Vaccine Immunol. 2006; 13, 219–226.

43. Smits H. H., Engering D., van der Kleij E. C., de Jong K., Schipper T. M. M., van Capel B. A., Zaat M. Selective probiotic bacteria induce IL-10-producing regulatory cells in vitro by modulating dendritic cell 3-grabbing nonintegrin. J. Allergy Clin. Immunol. 2005; 115, 1260–1267.

44. Viljanen M., Pohjavuori E., Haahtela T., Korpela R. Induction of inflammation as a possible mechanism of probiotic effect in atopic eczema-dermatitis syndrome. J. Allergy Clin. Immunol. 2005; 115, 1254–1259.

45. Guarino A., Lo Vecchio A., Canani R. B. Probiotics as prevention and treatment for diarhea. Curr. Opin. Gastroenterol. 2009; 25, 18–23.

46. Zhang L., Li N., Caicedo R., Neu J. Alive and died Lactobacillus rhamnosus GG decrease tumor necrosis factor-α-induced interleukin-8 production in Caco-2 cells. J. Nutr. 2005; 135, 1752–1756.

47. Tien M. T., Girardin S. E., Regnault B., Le Bourhis L., Dillies M. A., Coppee J. Y. Anti-inflammatory effect of Lactobacillus casei on Shigella-infected human intestinal epitelial cells. J. Immunol. 2006; 176, 1228–1237.

48. Frick J. S., Schenk K., Quitadamo M., Kahl F., Koberle M., Bohn E. Lactobacillus fermentum attenuates the proinflammatory effect of Yersinia enterocolitica on human epithelial cells. Inflamm. Bowel Dis. 2007; 13, 83–90.

49. Ruiz P. A., Hoffmann M., Szcesny S., Blaut M., Haller D. Innate mechanisms for Bifidobacterium lactis to activate transient pro-inflammatory host responses to intestinal epithelial cells after the colonization of germ-free rats. Immunology 2005; 115, 444–450.

50. Gourbeyre P., Denery S., Bodinier M. Probiotics, prebiotics, and synbiotics: impact on the gut immune system and allergic reactions. J. Leuko. Biol. 2011; 89, 685–694.

51. Pelto L., Isolauri E., Lilius E. M., Nuutila J., Salminen S. Probiotic bacteria down-regulate the milk-induced inflammatory response in milk-hypersensitive subjects but have an immunostimulatory effect in healthy subjects. Clin. Exp. Allergy 1998; 28, 1474–1479.

52. Aimutis W. R. Biology of Lactobacillus acidophilus. In: Batt C. A., Tortorello M.-L. (eds.) Encyclopedia of food microbiology. 2nd ed. London: Elsevier Ltd., Academic Press 2014.

53. Marin M. L., Lee J. H., Murtha J., Ustunol Z., Pestka J. J. Differential cytokine production in clonal macrophage and T-cell lines cultured with bifidobacteria. J. Dairy Sci. 1997; 80, 2713–2720.

54. Herbel S. R., Vahjen W., Wieler L. H., Guenther S. Timely approaches to identify probiotic species of the genus Lactobacillus. Gut Pathogens 2013; 5, 27.

55. Iliev I. D., Tohno M., Kurosaki D., Shimosato T., He F., Hosoda M., Saito T., Kitazawa H. Immunostimulatory oligodeoxynucleotide containing TTTCGTTT motif from Lactobacillus rhamnosus GG DNA potentially suppresses OVA-specific IgE production in mice. Scand. J. Immunol. 2008; 67, 370–376.

56. Tlaskalová-Hogenová H., Štepanková R., Kozáková H., Hudcovič T., Vannucci L., Tučková L., Rossmann P., Hrnčiř T., Kverka M., Zakostelská Z., Klimešová K., Přibylová J., Bártová J., Sanchez D., Fundová P., Borovská D., Srůtková D., Zídek Z., Schwarzer M., Drastich P., Funda D. P. The role of gut microbiota (commensal bacteria) and the mucosal barrier in the pathogenesis of inflammatory and autoimmune diseases and cancer. Contribution of germ-free and gnotobiotic animal models of human diseases. Cell Mol. Immunol. 2011; 8, 110–120.

57. Kamada N., Núnez G. Regulation of the immune system by the resident intestinal bacteria. Gastroenterology 2014; 146, 1477–1488.

58. Aureli P., Capurso L., Castellazzi A. M., Clerici M., Giovannii M., Morelli L., Poli A., Pregliasco F., Salvini F., Zuccotti G. V. Probiotics and health: An evidence based review. Pharmacol. Res. 2011; 63, 366–376.

59. Bermúdez-Humarán L. G., Aubry C., Motta J. P., Deraison C., Steidler L., Vergnolle N., Chatel J. M., Langella P. Engeneering lactococci and lactobacilli for human health. Curr. Opinion Microbiol. 2013; 16, 278–283.

60. Cano-Garrido O., Seraz-Franzoso J., Garcia-Fruitós E. Lactic acid bacteria: reviewing the potential of a promising delivery live vector for biomedical purposes. Microb. Cell Fact. 2015; 14, 137.

61. Braat H., Rottiers P., Hommers D. W., Huyghebaert N., Remaut E., Remon J. P., van Deventer S. J., Neirynck S., Peppelenbosch M. P., Steidler L. A phase 1 trial with transgenic bacteria expressing interleukin-10 in Crohn’s disease. Clin. Gastroenterol. Hepatol. 2006; 4, 754–759.

62. Vandenbroucke K., Haard H., Beinaert E., Dreier T., Lauwereys M., Huyck L., Van Huysse J., Demetter P., Steidler L., Reumaut E. Orally administered L. lactis secreting an anti-TNF nanobody demonstrate efficacy in chronic colitis. Mucosal Immunol. 2010; 3, 49–56.

63. Vijayan V., Mueller S., Baumgart-Vogt E., Immenschuh S. Heme oxygenase-1 as a therapeutic target in inflammatory disorders of the gastrointestinal tract. World J. Gastroenterol. 2010; 16, 3112–3119.

64. Caluwaerts S., Vandenbroucke K., Steidler L., Neirynck S., Vanhoenacker P., Corveleyn S., Watkins B., Sonis S., Coulie B., Rotters P. AG013, a mouth rinse formulation of Lactococcus lactis sectering human Trefoil Factor 1, provides a safe an efficacious therapeutic tool for treating oral mucositis. Oral Oncol. 2010; 46, 564–570.

65. Motta J. P., Magne L., Descamps D., Rolland C., Squarzoni-Dale C., Rosset P., Martin L., Cenac N., Balloy V., Huerre M. Modifying the protease, antiprotease pattern by elafin overexpression protects mice from colitis. Gastroenterol. 2011; 140, 1272–1282.

66. Motta J. P., Bermúdez-Humarán L. G., Deraison C., Martin L., Rolland C., Rousset P., Boue J., Dietrich G., Chapman K., Kharrat P. Food-grade bacteria expressing elafin protect against inflammation and restore colon homeostasis. Sci. Transl. Med. 2012; 4, 144–158.

67. Bernstein C. N. Treatment of IBD: where we are and where we are going. Am. J. Gastroenterol. 2015; 110, 114–126.

68. Shaw L., Wiedow O. Therapeutic potential of human elafin. Biochem. Soc. Trans. 2011; 39, 1450–1454.

69. Carroll I. M., Andrus J. M., Bruno-Barcena J. M., Klaenhammer T. R., Hassan H. M., Threadgill D. S. Anti-inflammatory properties of Lactobacillus gasseri expressing manganese superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007; 293, G729–G738. 

70. Watterlot L., Rochat T., Sokol H., Cherbuy C., Bouloufa I., Lefevre F., Gratadoux J. J., Honvo-Hueto E., Chilmonczyk S., Blugeon S. Intragastric administration of a superoxide dismutase-producing recombinant Lactobacillus casei BL23 strain attenuates DSS colitis in mice. Int. J. Food Microbiol. 2010; 144, 35–41.

71. LeBlanc J. G., del Carmen S., Miyoshi A., Azevedo V., Sesma F., Langella P., Bermúdez-Humarán L. G., Watterlot L., Perdigon G., LeBlanc A. D. Use of superoxide dismutase and catalase producing lactic acid bacteria in TNBS induced Crohn’s disease in mice. J. Biotechnol. 2011; 151, 287–293.

72. Ljungh A., Wadström T. From probiotics, prebiotics and symbiotics to „living drugs“. In: Ljungh Å., Wadström T. eds. Lactobacillus molecular biology: From genomics to probiotics. 1st ed. Norfolk: Caister Academic Press 2009.

73. LeBlanc J. G., Aubry C., Cortes-Perez N. G., Dde Moreno de LeBlanc A., Vergnolle N., Langella P., Azevedo V., Chatel J. M., Miyoshi A., Bermudez-Humaran L. G. Mucosal targeting of therapeutic molecules using genetically modified lactic acid bacteria: an update. FEMS Microbiol. Lett. 2013; 344, 1–9.

74. Bermudez-Humaran L. G., Motta J. P., Aubry C., Kharrat P., Rous-Martin L., Sellenave J. M., Deraison C., Vergnolle N., Langella P. Serine protease inhibitors protect better than IL-10 and TGF-beta anti-inflammatory cytokines against mouse colitis when delivered by recombinant lactococci. Microb. Cell Fact. 2015;