Immunomodulatory effects of probiotics: Can they be used to treat allergies and autoimmune diseases?

Maturitas

Volumn 119, Issue , 2019, Pages 25-38

  Dargahi, Narges ^a   Johnson, Joshua ^b   Donkor, Osaana ^b   Vasiljevic, Todor ^b   Apostolopoulos, Vasso ^a  

^a VICTORIA UNIVERSITY   (Australia)

^b INSTITUTE FOR SUSTAINABLE INDUSTRIES AND LIVEABLE CITIES   (Australia)

Author keywords

Dysbiosis; Gastrointestinal tract; Inflammatory bowel disease; Lactic acid bacteria; Probiotics; Symbiosis

Indexed keywords

INTERLEUKIN 17; INTERLEUKIN 17F; INTERLEUKIN 22; PROBIOTIC AGENT;

ALLERGY; ATOPIC DERMATITIS; AUTOIMMUNE DISEASE; BACTERIUM; BIFIDOBACTERIACEAE; CLINICAL TRIAL (TOPIC); CROHN DISEASE; CYTOKINE RELEASE; DENDRITIC CELL; DRUG EFFECT; ENDOCYTOSIS; FOOD ALLERGY; GASTROINTESTINAL TRACT; HUMAN; IMMUNE SYSTEM; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFLAMMATORY BOWEL DISEASE; INNATE IMMUNITY; INTESTINE EPITHELIUM; MACROPHAGE; MEDLINE; MONOCYTE; MULTIPLE SCLEROSIS; NATURAL KILLER CELL; NONHUMAN; RANDOMIZED CONTROLLED TRIAL (TOPIC); REGULATORY T LYMPHOCYTE; REVIEW; SYSTEMATIC REVIEW; TH17 CELL; ULCERATIVE COLITIS; HYPERSENSITIVITY; IMMUNOLOGY; INTESTINE FLORA; LEUKOCYTE; MICROBIOLOGY; MONONUCLEAR PHAGOCYTE;

AUTOIMMUNE DISEASES; DERMATITIS, ATOPIC; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HUMANS; HYPERSENSITIVITY; INFLAMMATORY BOWEL DISEASES; LEUKOCYTES; MONONUCLEAR PHAGOCYTE SYSTEM; MULTIPLE SCLEROSIS; PROBIOTICS;

EID: 85056652834     PISSN: 03785122     EISSN: 18734111     Source Type: Journal    
DOI: 10.1016/j.maturitas.2018.11.002     Document Type: Review

References (137)

1. Ahtesh, F.B., Stojanovska, L., Apostolopoulos, V., Anti-hypertensive peptides released from milk proteins by probiotics. Maturitas 115 (2018), 103–109.
2. Vasiljevic, T., Shah, N.P., Probiotics—From Metchnikoff to bioactives. Int. Dairy. J. 18 (2008), 714–728.
3. Biagi, E., Nylund, L., Candela, M., Ostan, R., Bucci, L., Pini, E., et al. Through ageing, and beyond: gut microbiota and inflammatory status in seniors and centenarians. PloS One, 5, 2010.
4. Tiihonen, K., Ouwehand, A.C., Rautonen, N., Human intestinal microbiota and healthy ageing. Ageing Res. Rev. 9 (2010), 107–116.
5. Biagi, E., Rampelli, S., Turroni, S., Quercia, S., Candela, M., Brigidi, P., The gut microbiota of centenarians: signatures of longevity in the gut microbiota profile. Mech. Ageing Dev. 165 (2017), 180–184.
6. Hardy, H., Harris, J., Lyon, E., Beal, J., Foey, A.D., Probiotics, prebiotics and immunomodulation of gut mucosal defences: homeostasis and immunopathology. Nutrients 5 (2013), 1869–1912.
7. Ljungh, A., Wadstrom, T., Lactic acid bacteria as probiotics. Curr. Issues Intest. Microbiol. 7 (2006), 73–90.
8. Reis, J.A., Paula, A.T., Casarotti, S.N., Penna, A.L.B., Lactic acid bacteria antimicrobial compounds: characteristics and applications. Food Eng. Rev. 4 (2012), 124–140.
9. de Roock, S., van Elk, M., Hoekstra, M.O., Prakken, B.J., Rijkers, G.T., de Kleer, I.M., Gut derived lactic acid bacteria induce strain specific CD4+ T cell responses in human PBMC. Clin. Nutr. 30 (2011), 845–851.
10. Butel, M.J., Probiotics, gut microbiota and health. Médecine et Maladies Infectieuses 44 (2014), 1–8.
11. Maurice, C.F., Haiser, H.J., Turnbaugh, P.J., Xenobiotics shape the physiology and gene expression of the active human gut microbiome. Cell 152 (2013), 39–50.
12. Kiseleva, E., Novik, G., Probiotics as Immunomodulators: Substances, mEchanisms and Therapeutic Benefits. 2013.
13. Macpherson, A.J., Harris, N.L., Interactions between commensal intestinal bacteria and the immune system. Nat. Rev. Immunol. 4 (2004), 478–485.
14. Salminen, S., von Wright, A., Ouwehand, A.C., (eds.) Lactic Acid Bacteria: Microbiological and Functional Aspects, 3rd ed., 2004, Marcel Dekker, Inc, New York.
15. Asarat, M., Apostolopoulos, V., Vasiljevic, T., Donkor, O., Short-chain fatty acids produced by synbiotic mixtures in skim milk differentially regulate proliferation and cytokine production in peripheral blood mononuclear cells. Int. J. Food Sci. Nutr. 66 (2015), 755–765.
16. Asarat, M., Apostolopoulos, V., Vasiljevic, T., Donkor, O., Short-chain fatty acids regulate cytokines and Th17/treg cells in human peripheral blood mononuclear cells in vitro. Immunol. Invest. 45 (2016), 205–222.
17. Asarat, M., Vasiljevic, T., Apostolopoulos, V., Donkor, O., Short-Chain fatty acids regulate secretion of IL-8 from human intestinal epithelial cell lines in vitro. Immunol. Invest. 44 (2015), 678–693.
18. Zschüttig, A., Zimmermann, K., Blom, J., Goesmann, A., Pöhlmann, C., Gunzer, F., Identification and characterization of microcin S, a new antibacterial peptide produced by probiotic Escherichia coli G3/10. PloS One, 7, 2012.
19. Giannelli, V., Di Gregorio, V., Iebba, V., Giusto, M., Schippa, S., Merli, M., et al. Microbiota and the gut-liver axis: bacterial translocation, inflammation and infection in cirrhosis. World J. Gastroenterol. 20 (2014), 16795–16810.
20. Goudarzvand, M., Rasouli Koohi, S., Khodaii, Z., Moghadam, S.S., Probiotics Lactobacillus plantarum and Bifidobacterium B94: cognitive function in demyelinated model. Med. J. Islamic Repub. Iran, 30, 2016.
21. Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., Isolauri, E., Probiotics in primary prevention of atopic disease: A randomised placebo-controlled trial. Lancet 357 (2001), 1076–1079.
22. Clarke, G., O'Mahony, S.M., Dinan, T.G., Cryan, J.F., Priming for health: gut microbiota acquired in early life regulates physiology, brain and behaviour. Acta Paediatr. Int. J. Paediatr. 103 (2014), 812–819.
23. Kelly, D., King, T., Aminov, R., Importance of microbial colonization of the gut in early life to the development of immunity. Mutat. Res. – Fundam. Mol. Mech. Mutagen. 622 (2007), 58–69.
24. Rhee, K.J., Sethupathi, P., Driks, A., Lanning, D.K., Knight, K.L., Role of commensal bacteria in development of gut-associated lymphoid tissues and preimmune antibody repertoire. J. Immunol. 172 (2004), 1118–1124.
25. Britti, M.S., Roselli, M., Finamore, A., Merendino, N., Mengheri, E., Regulation of immune response at intestinal and peripheral sites by probiotics. Biologia 61 (2006), 735–740.
26. Pollard, M., Sharon, N., Responses of the peyer's patches in germ-Free mice to antigenic stimulation. Infect. Immun. 2 (1970), 96–100.
27. D'Souza, A., Fordjour, L., Ahmad, A., Cai, C., Kumar, D., Valencia, G., et al. Effects of probiotics, prebiotics, and synbiotics on messenger RNA expression of caveolin-1, NOS, and genes regulating oxidative stress in the terminal ileum of formula-fed neonatal rats. Pediatr. Res. 67 (2010), 526–531.
28. Williams, A.M., Probert, C.S.J., Stepankova, R., Tlaskalova-Hogenova, H., Phillips, A., Bland, P.W., Effects of microflora on the neonatal development of gut mucosal T cells and myeloid cells in the mouse. Immunology 119 (2006), 470–478.
29. Yamamoto, M., Yamaguchi, R., Munakata, K., Takashima, K., Nishiyama, M., Hioki, K., et al. A microarray analysis of gnotobiotic mice indicating that microbial exposure during the neonatal period plays an essential role in immune system development. BMC Genomics, 13, 2012.
30. Mortha, A., Diefenbach, A., Natural killer cell receptor-expressing innate lymphocytes: more than just NK cells. Cell. Mol. Life Sci. 68 (2011), 3541–3555.
31. Delcenserie, V., Martel, D., Lamoureux, M., Amiot, J., Boutin, Y., Roy, D., Immunomodulatory effects of probiotics in the intestinal tract. Curr. Issues Mol. Biol. 10 (2008), 37–54.
32. Michałkiewicz, J., Krotkiewski, M., Gackowska, L., Wyszomirska-Gołda, M., Helmin-Basa, A., Dzierzanowska, D., et al. Immunomodulatory effects of lactic acid bacteria on human peripheral blood mononuclear cells. Microb. Ecol. Health Dis. 15 (2003), 185–192.
33. Fink, L.N., Zeuthen, L.H., Christensen, H.R., Morandi, B., Frøkiær, H., Ferlazzo, G., Distinct gut-derived lactic acid bacteria elicit divergent dendritic cell-mediated NK cell responses. Int. Immunol. 19 (2007), 1319–1327.
34. Josefowicz, S.Z., Niec, R.E., Kim, H.Y., Treuting, P., Chinen, T., Zheng, Y., et al. Extrathymically generated regulatory T cells control mucosal T H 2 inflammation. Nature 482 (2012), 395–399.
35. Aumeunier, A., Grela, F., Ramadan, A., Van LP, Bardel E., Alcala, A.G., et al. Systemic toll-like receptor stimulation suppresses experimental allergic asthma and autoimmune diabetes in NOD mice. PloS One, 5, 2010.
36. Knight, P., Campbell, B.J., Rhodes, J.M., Host-bacteria interaction in inflammatory bowel disease. Br. Med. Bull. 88 (2008), 95–113.
37. Ott, S.J., Schreiber, S., Reduced microbial diversity in inflammatory bowel diseases [1]. Gut, 55, 2006, 1207.
38. Steinman, R.M., Hawiger, D., Nussenzweig, M.C., Tolerogenic dendritic cells. Annu. Rev. Immunol. 21 (2003), 685–711.
39. Foligne, B., Zoumpopoulou, G., Dewulf, J., Ben Younes, A., Chareyre, F., Sirard, J.C., et al. A key role of dendritic cells in probiotic functionality. PloS One, 2, 2007, e313.
40. Smelt, M.J., de Haan, B.J., Bron, P.A., van Swam, I., Meijerink, M., Wells, J.M., et al. L. Plantarum, L. salivarius, and L. Lactis attenuate Th2 responses and increase treg frequencies in healthy mice in a strain dependent manner. PloS One, 7, 2012.
41. Esmaeili, S.A., Mahmoudi, M., Rezaieyazdi, Z., Sahebari, M., Tabasi, N., Sahebkar, A., et al. Generation of tolerogenic dendritic cells using lactobacillus rhamnosus and lactobacillus delbrueckii as tolerogenic probiotics. J. Cell. Biochem., 2018.
42. Okada, Y., Tsuzuki, Y., Takeshi, T., Furuhashi, H., Higashiyama, M., Watanabe, C., et al. Novel probiotics isolated from a Japanese traditional fermented food, funazushi, attenuates DSS-induced colitis by increasing the induction of high integrin alphav/beta8-expressing dendritic cells. J. Gastroenterol. 53 (2018), 407–418.
43. Fu, L., Song, J., Wang, C., Fu, S., Wang, Y., Bifidobacterium infantis potentially alleviates shrimp tropomyosin-induced allergy by tolerogenic dendritic cell-dependent induction of regulatory T cells and alterations in gut microbiota. Front. Immunol., 8, 2017.
44. Farache, J., Zigmond, E., Shakhar, G., Jung, S., Contributions of dendritic cells and macrophages to intestinal homeostasis and immune defense. Immunol. Cell Biol. 91 (2013), 232–239.
45. Stagg, A.J., Hart, A.L., Knight, S.C., Kamm, M.A., Interactions between dendritic cells and bacteria in the regulation of intestinal immunity. Best Pract. Res.: Clin. Gastroenterol. 18 (2004), 255–270.
46. Donkor, O.N., Ravikumar, M., Proudfoot, O., Day, S.L., Apostolopoulos, V., Paukovics, G., et al. Cytokine profile and induction of T helper type 17 and regulatory T cells by human peripheral mononuclear cells after microbial exposure. Clin. Exp. Immunol. 167 (2012), 282–295.
47. Donkor, O.N., Shah, N.P., Apostolopoulos, V., Vasiljevic, T., Development of allergic responses related to microorganisms exposure in early life. Int. Dairy. J. 20 (2010), 373–385.
48. Kitazawa, H., Tomioka, Y., Matsumura, K., Aso, H., Mizugaki, M., Itoh, T., et al. Expression of mRNA encoding IFNα in macrophages stimulated with Lactobacillus gasseri. FEMS Microbiol. Lett. 120 (1994), 315–321.
49. Gutkowski, P., Madaliński, K., Grek, M., Dmeńska, H., Syczewska, M., Michałkiewicz, J., Effect of orally administered probiotic strains lactobacillus and bifidobacterium in children with atopic asthma. Central-Eur. J. Immunol. 35 (2010), 233–238.
50. Balzaretti, S., Taverniti, V., Guglielmetti, S., Fiore, W., Minuzzo, M., Ngo, H.N., et al. A novel rhamnose-rich hetero-exopolysaccharide isolated from lactobacillus paracasei DG activates THP-1 human monocytic cells. Appl. Environ. Microbiol., 83, 2017.
51. Matsuzaki, T., Chin, J., Modulating immune responses with probiotic bacteria. Immunol. Cell Biol. 78 (2000), 67–73.
52. Shida, K., Suzuki, T., Kiyoshima-Shibata, J., Shimada, S., Nanno, M., 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 (2006), 997–1003.
53. Dong, H., Rowland, I., Yaqoob, P., Comparative effects of six probiotic strains on immune function in vitro. Br. J. Nutr. 108 (2012), 459–470.
54. Wolvers, D., Antoine, J.M., Myllyluoma, E., Schrezenmeir, J., Szajewska, H., Rijkers, G.T., Guidance for substantiating the evidence for beneficial effects of probiotics: prevention and management of infections by probiotics. J. Nutr. 140 (2010), 698S–712S.
55. Gershon, R.K., Kondo, K., Cell interactions in the induction of tolerance: the role of thymic lymphocytes. Immunology, 18, 1970, 723.
56. Sakaguchi, S., Sakaguchi, N., Asano, M., Itoh, M., Toda, M., Immunologic self-tolerance maintained by activated T cells expressing IL-2 receptor alpha-chains (CD25). Breakdown of a single mechanism of self-tolerance causes various autoimmune diseases. J. Immunol. 155 (1995), 1151–1164.
57. Chen, Y., Kuchroo, V.K., J-i, Inobe, Hafler, D.A., Weiner, H.L., Regulatory T cell clones induced by oral tolerance: suppression of autoimmune encephalomyelitis. Science 265 (1994), 1237–1240.
58. McKenzie, C., Tan, J., Macia, L., Mackay, C.R., The nutrition-gut microbiome-physiology axis and allergic diseases. Immunol. Rev. 278 (2017), 277–295.
59. Thorburn, A.N., Macia, L., Mackay, C.R., Diet, metabolites, and “Western-lifestyle” inflammatory diseases. Immunity 40 (2014), 833–842.
60. Zeng, H., Zhang, R., Jin, B., Chen, L., Type 1 regulatory T cells: A new mechanism of peripheral immune tolerance. Cell Mol. Immunol. 12 (2015), 566–571.
61. Torii, A., Torii, S., Fujiwara, S., Tanaka, H., Inagaki, N., Nagai, H., Lactobacillus acidophilus strain L-92 regulates the production of Th1 cytokine as well as Th2 cytokines. Allergol. Int. 56 (2007), 293–301.
62. Bermudez-Brito, M., Borghuis, T., Daniel, C., Pot, B., de Haan, B.J., Faas, M.M., et al. L. plantarum WCFS1 enhances Treg frequencies by activating DCs even in absence of sampling of bacteria in the Peyer Patches. Sci. Rep., 8, 2018, 1785.
63. Lee, S.Y., Lee, S.H., Jhun, J., Seo, H.B., Jung, K.A., Yang, C.W., et al. A combination with probiotic complex, zinc, and coenzyme Q10 attenuates autoimmune arthritis by regulation of Th17/Treg balance. J. Med. Food 21 (2018), 39–46.
64. Wang, K., Dong, H., Qi, Y., Pei, Z., Yi, S., Yang, X., et al. Lactobacillus casei regulates differentiation of Th17/Treg cells to reduce intestinal inflammation in mice. Can. J. Vet. Res. 81 (2017), 122–128.
65. Cortes-Perez, N.G., Lozano-Ojalvo, D., Maiga, M.A., Hazebrouck, S., Adel-Patient, K., Intragastric administration of lactobacillus casei BL23 induces regulatory FoxP3+RORYt+ T cells subset in mice. Beneficial Microbes 8 (2017), 433–438.
66. Zhang, L.L., Chen, X., Zheng, P.Y., Luo, Y., Lu, G.F., Liu, Z.Q., et al. Oral bifidobacterium modulates intestinal immune inflammation in mice with food allergy. J. Gastroenterol. Hepatol. 25 (2010), 928–934.
67. Danilo, C.A., Constantopoulos, E., McKee, L.A., Chen, H., Regan, J.A., Lipovka, Y., et al. Bifidobacterium animalis subsp. Lactis 420 mitigates the pathological impact of myocardial infarction in the mouse. Beneficial Microbes 8 (2017), 257–269.
68. Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., et al. Treg induction by a rationally selected mixture of clostridia strains from the human microbiota. Nature 500 (2013), 232–236.
69. Singh, N., Gurav, A., Sivaprakasam, S., Brady, E., Padia, R., Shi, H., et al. Activation of Gpr109a, receptor for niacin and the commensal metabolite butyrate, suppresses colonic inflammation and carcinogenesis. Immunity 40 (2014), 128–139.
70. Trompette, A., Gollwitzer, E.S., Yadava, K., Sichelstiel, A.K., Sprenger, N., Ngom-Bru, C., et al. Gut microbiota metabolism of dietary fiber influences allergic airway disease and hematopoiesis. Nat. Med. 20 (2014), 159–166.
71. Öner, Ö Azize, G.-E., Probiotics for autoimmune diseases: is there a benefit?. Contemp. Pediatr., 2012, 153–180.
72. Mangan, P.R., Harrington, L.E., O'Quinn, D.B., Helms, W.S., Bullard, D.C., Elson, C.O., et al. Transforming growth factor-β induces development of the TH17 lineage. Nature 441 (2006), 231–234.
73. Zheng, Y., Valdez, P.A., Danilenko, D.M., Hu, Y., Sa, S.M., Gong, Q., et al. Interleukin-22 mediates early host defense against attaching and effacing bacterial pathogens. Nat. Med. 14 (2008), 282–289.
74. Kryczek, I., Bruce, A.T., Gudjonsson, J.E., Johnston, A., Aphale, A., Vatan, L., et al. Induction of IL-17+ T cell trafficking and development by IFN-γ: mechanism and pathological relevance in psoriasis. J. Immunol. 181 (2008), 4733–4741.
75. Wilke, C.M., Bishop, K., Fox, D., Zou, W., Deciphering the role of Th17 cells in human disease. Trends Immunol. 32 (2011), 603–611.
76. Dargahi, N., Katsara, M., Tselios, T., Androutsou, M.E., De Courten, M., Matsoukas, J., et al. Multiple sclerosis: immunopathology and treatment update. Brain Sciences, 7, 2017.
77. Zhao, M., Tan, Y., Peng, Q., Huang, C., Guo, Y., Liang, G., et al. IL-6/STAT3 pathway induced deficiency of RFX1 contributes to Th17-dependent autoimmune diseases via epigenetic regulation. Nat. Commun., 9, 2018.
78. Niess, J.H., Adler, G., Enteric flora expands gut lamina propria CX3CR1+dendritic cells supporting inflammatory immune responses under normal and inflammatory conditions. J. Immunol. 184 (2010), 2026–2037.
79. Atarashi, K., Nishimura, J., Shima, T., Umesaki, Y., Yamamoto, M., Onoue, M., et al. ATP drives lamina propria TH17 cell differentiation. Nature 455 (2008), 808–812.
80. Ivanov, I.I., RdL, Frutos, Manel, N., Yoshinaga, K., Rifkin, D.B., Sartor, R.B., et al. Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host Microbe 4 (2008), 337–349.
81. Lee, H.S., Han, S.Y., Bae, E.A., Huh, C.S., Ahn, Y.T., Lee, J.H., et al. Lactic acid bacteria inhibit proinflammatory cytokine expression and bacterial glycosaminoglycan degradation activity in dextran sulfate sodium-induced colitic mice. Int. Immunopharm. 8 (2008), 574–580.
82. Wu, H.J., Ivanov, I.I., Darce, J., Hattori, K., Shima, T., Umesaki, Y., et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity 32 (2010), 815–827.
83. Kriegel, M.A., Sefik, E., Hill, J.A., Wu, H.J., Benoist, C., Mathis, D., Naturally transmitted segmented filamentous bacteria segregate with diabetes protection in nonobese diabetic mice. Proc. Natl. Acad. Sci. U. S. A. 108 (2011), 11548–11553.
84. Zaph, C., Du, Y., Saenz, S.A., Nair, M.G., Perrigoue, J.G., Taylor, B.C., et al. Commensal-dependent expression of IL-25 regulates the IL-23-IL-17 axis in the intestine. J. Exp. Med. 205 (2008), 2191–2198.
85. Fitzpatrick, L.R., Novel pharmacological approaches for inflammatory bowel disease: targeting key intracellular pathways and the IL-23/IL-17 axis. Int. J. InFlammation, 2012, 2012.
86. Tanabe, S., Kinuta, Y., Saito, Y., Bifidobacterium infantis suppresses proinflammatory interleukin-17 production in murine splenocytes and dextran sodium sulfate-induced intestinal inflammation. Int. J. Mol. Med. 22 (2008), 181–185.
87. Ghadimi, D., Helwig, U., Schrezenmeir, J., Heller, K.J., de Vrese, M., Epigenetic imprinting by commensal probiotics inhibits the IL-23/IL-17 axis in an in vitro model of the intestinal mucosal immune system. J. Leukocyte Biol. 92 (2012), 895–911.
88. Miyauchi, E., Ogita, T., Miyamoto, J., Kawamoto, S., Morita, H., Ohno, H., et al. Bifidobacterium longum alleviates dextran sulfate sodium-induced colitis by suppressing IL-17A response: involvement of intestinal epithelial costimulatory molecules. PloS One, 8, 2013.
89. Ogita, T., Tanii, Y., Morita, H., Suzuki, T., Tanabe, S., Suppression of Th17 response by streptococcus thermophilus ST28 through induction of IFN-γ. Int. J. Mol. Med. 28 (2011), 817–822.
90. Owaga, E., Hsieh, R.H., Mugendi, B., Masuku, S., Shih, C.K., Chang, J.S., Th17 cells as potential probiotic therapeutic targets in inflammatory bowel diseases. Int. J. Mol. Sci. 16 (2015), 20841–20858.
91. Fitzpatrick, L.R., Deml, L., Hofmann, C., Small, J.S., Groeppel, M., Hamm, S., et al. 4SC-101, a novel immunosuppressive drug, inhibits IL-17 and attenuates colitis in two murine models of inflammatory bowel disease. Inflamm. Bowel Dis. 16 (2010), 1763–1777.
92. Fitzpatrick, L.R., Small, J.S., Doblhofer, R., Ammendola, A., Vidofludimus inhibits colonic interleukin-17 and improves hapten-induced colitis in rats by a unique dual mode of action. J. Pharmacol. Exp. Ther. 342 (2012), 850–860.
93. Chen, L., Zou, Y., Peng, J., Lu, F., Yin, Y., Li, F., et al. Lactobacillus acidophilus suppresses colitis-associated activation of the IL-23/Th17 axis. J. Immunol. Res., 2015, 2015.
94. Dar, H.Y., Pal, S., Shukla, P., Mishra, P.K., Tomar, G.B., Chattopadhyay, N., et al. Bacillus clausii inhibits bone loss by skewing treg-Th17 cell equilibrium in postmenopausal osteoporotic mice model. Nutrition 54 (2018), 118–128.
95. Dar, H.Y., Shukla, P., Mishra, P.K., Anupam, R., Mondal, R.K., Tomar, G.B., et al. Lactobacillus acidophilus inhibits bone loss and increases bone heterogeneity in osteoporotic mice via modulating treg-Th17 cell balance. Bone Rep. 8 (2018), 46–56.
96. Kraneveld, A.D., Sagar, S., Garssen, J., Folkerts, G., The two faces of mast cells in food allergy and allergic asthma: The possible concept of yin yang. Biochimica et Biophysica Acta (BBA) 1822 (2012), 93–99.
97. Hajeb, P., Selamat, J., A contemporary review of seafood allergy. Clin. Rev. Allergy Immunol. 42 (2012), 365–385.
98. Lopata, A.L., Jeebhay, M.F., Airborne seafood allergens as a cause of occupational allergy and asthma. Curr. Allergy Asthma Rep. 13 (2013), 288–297.
99. Burks, A.W., Tang, M., Sicherer, S., Muraro, A., Eigenmann, P.A., Ebisawa, M., et al. ICON: food allergy. J. Allergy Clin. Immun. 129 (2012), 906–920.
100. Barberi, C., Campana, S., De Pasquale, C., Rabbani Khorasgani, M., Ferlazzo, G., Bonaccorsi, I., T cell polarizing properties of probiotic bacteria. Immunol. Lett. 168 (2015), 337–342.
101. Fonseca, V.M.B., Milani, T.M.S., Prado, R., Bonato, V.L.D., Ramos, S.G., Martins, F.S., et al. Oral administration of saccharomyces cerevisiae UFMG A-905 prevents allergic asthma in mice. Respirology 22 (2017), 905–912.
102. Sadakane, K., Ichinose, T., Nishikawa, M., Takano, H., Shibamoto, T., Co-exposure to zymosan A and heat-inactivated Asian sand dust exacerbates ovalbumin-induced murine lung eosinophilia. Allergy Asthma Clin. Immunol., 12, 2016.
103. Nunes, C.F., Nogueira, J.S., Vianna, P.H.O., Ciambarella, B.T., Rodrigues, P.M., Miranda, K.R., et al. Probiotic treatment during neonatal age provides optimal protection against experimental asthma through the modulation of microbiota and T cells. Int. Immunol. 30 (2018), 155–169.
104. Vliagoftis, H., Kouranos, V.D., Betsi, G.I., Falagas, M.E., Probiotics for the treatment of allergic rhinitis and asthma: systematic review of randomized controlled trials. Ann. Allergy Asthma Immunol. 101 (2008), 570–579.
105. Ciprandi, G., Vizzaccaro, A., Cirillo, I., Tosca, M.A., Bacillus clausii exerts immuno-modulatory activity in allergic subjects: a pilot study. Eur. Ann. Allergy Clin. Immunol. 37 (2005), 129–134.
106. Yang, G., Liu, Z.Q., Yang, P.C., Treatment of allergic rhinitis with probiotics: an alternative approach. North. Am. J. Med. Sci. 5 (2013), 465–468.
107. Rø A.D.B., Simpson, M.R., Rø T.B., Storrø O., Johnsen, R., Videm, V., et al. Reduced Th22 cell proportion and prevention of atopic dermatitis in infants following maternal probiotic supplementation. Clin. Exp. Allergy 47 (2017), 1014–1021.
108. Shin, J.H., Chung, M.J., Seo, J.G., A multistrain probiotic formulation attenuates skin symptoms of atopic dermatitis in a mouse model through the generation of CD4+Foxp3+T cells. Food Nutr. Res., 60, 2016.
109. Hoeppli, R.E., Wu, D., Cook, L., Levings, M.K., The environment of regulatory T cell biology: cytokines, metabolites, and the microbiome. Front. Immunol., 6, 2015.
110. Russell, S.L., Gold, M.J., Willing, B.P., Thorson, L., McNagny, K.M., Finlay, B.B., Perinatal antibiotic treatment affects murine microbiota, immune responses and allergic asthma. Gut Microbes 4 (2013), 158–164.
111. De Roock, S., Van Elk, M., Van Dijk, M.E.A., Timmerman, H.M., Rijkers, G.T., Prakken, B.J., et al. Lactic acid bacteria differ in their ability to induce functional regulatory T cells in humans. Clin. Exp. Allergy 40 (2010), 103–110.
112. Chouraqui, J.P., Dupont, C., Bocquet, A., Bresson, J.L., Briend, A., Darmaun, D., et al. Feeding during the first months of life and prevention of allergy. Archives de pediatrie 15 (2008), 431–442.
113. Lee, J., Seto, D., Bielory, L., Meta-analysis of clinical trials of probiotics for prevention and treatment of pediatric atopic dermatitis. J. Allergy Clin. Immunol. Pract., 121, 2008 116-21 e11.
114. Volz, T., Skabytska, Y., Guenova, E., Chen, K.M., Frick, J.S., Kirschning, C.J., et al. Nonpathogenic bacteria alleviating atopic dermatitis inflammation induce IL-10-producing dendritic cells and regulatory Tr1 cells. J. Invest. Dermatol. 134 (2014), 96–104.
115. Vadasz, Z., Rainis, T., Nakhleh, A., Haj, T., Bejar, J., Halasz, K., et al. The involvement of immune semaphorins in the pathogenesis of inflammatory bowel diseases (IBDs). PloS One, 10, 2015.
116. Xun, Z., Zhang, Q., Xu, T., Chen, N., Chen, F., Dysbiosis and ecotypes of the salivary microbiome associated with inflammatory bowel diseases and the assistance in diagnosis of diseases using oral bacterial profiles. Front. Microbiol., 9, 2018.
117. Willing, B., Halfvarson, J., Dicksved, J., Rosenquist, M., Järnerot, G., Engstrand, L., et al. Twin studies reveal specific imbalances in the mucosa-associated microbiota of patients with ileal crohn's disease. Inflamm. Bowel Dis. 15 (2009), 653–660.
118. Sokol, C.L., Barton, G.M., Farr, A.G., Medzhitov, R., A mechanism for the initiation of allergen-induced T helper type 2 responses. Nat. Immunol. 9 (2008), 310–318.
119. Oelschlaeger, T.A., Mechanisms of probiotic actions – a review. Int. J. Med. Microbiol. 300 (2010), 57–62.
120. Chiba, T., Seno, H., Indigenous clostridium species regulate systemic immune responses by induction of colonic regulatory T cells. Gastroenterology 141 (2011), 1114–1116.
121. Fukuda, S., Toh, H., Hase, K., Oshima, K., Nakanishi, Y., Yoshimura, K., et al. Bifidobacteria can protect from enteropathogenic infection through production of acetate. Nature 469 (2011), 543–549.
122. van der Kleij, H., O'Mahony, C., Shanahan, F., O'Mahony, L., Bienenstock, J., Protective effects of Lactobacillus rhamnosus [corrected] and Bifidobacterium infantis in murine models for colitis do not involve the vagus nerve. Am. J. Physiol. Regul. Integr. Comp. Physiol. 295 (2008), R1131–7.
123. Jiang, Y., Yang, G., Meng, F., Yang, W., Hu, J., Ye, L., et al. Immunological mechanisms involved in probiotic-mediated protection against Citrobacter rodentium-induced colitis. Beneficial Microbes 7 (2016), 397–407.
124. Nikoopour, E., Singh, B., Reciprocity in microbiome and immune system interactions and its implications in disease and health. Inflam. Allergy – Drug. Targets 13 (2014), 94–104.
125. Bäckhed, F., Fraser Claire, M., Ringel, Y., Sanders Mary, E., Sartor, R.B., Sherman Philip, M., et al. Defining a healthy human gut microbiome: current concepts, future directions, and clinical applications. Cell Host Microbe 12 (2012), 611–622.
126. Brown, W.R., Fecal microbiota transplantation in treating clostridium difficile infection. J. Dig. Dis. 15 (2014), 405–408.
127. Strisciuglio, C., Miele, E., Giugliano, F.P., Vitale, S., Andreozzi, M., Vitale, A., et al. Bifidobacteria enhance antigen sampling and processing by dendritic cells in pediatric inflammatory bowel disease. Inflamm. Bowel Dis. 21 (2015), 1491–1498.
128. Mikkelsen, K., Stojanovska, L., Tangalakis, K., Bosevski, M., Apostolopoulos, V., Cognitive decline: A vitamin B perspective. Maturitas 93 (2016), 108–113.
129. Nemazannikova, N., Mikkelsen, K., Stojanovska, L., Blatch, G.L., Apostolopoulos, V., Is there a link between Vitamin B and multiple sclerosis?. Med. Chem. 14 (2018), 170–180.
130. Catanzaro, R., Anzalone, M., Calabrese, F., Milazzo, M., Capuana, M., Italia, A., et al. The gut microbiota and its correlations with the central nervous system disorders. Panminerva Med. 57 (2015), 127–143.
131. Buerth, C., Mausberg, A.K., Heininger, M.K., Hartung, H.P., Kieseier, B.C., Ernst, J.F., Oral tolerance induction in experimental autoimmune encephalomyelitis with candida utilis expressing the immunogenic MOG35-55 peptide. PloS One, 11, 2016.
132. Maassen, C.B.M., Laman, J.D., Van Holten-Neelen, C., Hoogteijling, L., Groenewegen, L., Visser, L., et al. Reduced experimental autoimmune encephalomyelitis after intranasal and oral administration of recombinant lactobacilli expressing myelin antigens. Vaccine 21 (2003), 4685–4693.
133. Consonni, A., Cordiglieri, C., Rinaldi, E., Marolda, R., Ravanelli, I., Guidesi, E., et al. Administration of bifidobacterium and lactobacillus strains modulates experimental myasthenia gravis and experimental encephalomyelitis in Lewis rats. Oncotarget 9 (2018), 22269–22287.
134. Salehipour, Z., Haghmorad, D., Sankian, M., Rastin, M., Nosratabadi, R., Soltan Dallal, M.M., et al. Bifidobacterium animalis in combination with human origin of Lactobacillus plantarum ameliorate neuroinflammation in experimental model of multiple sclerosis by altering CD4+ T cell subset balance. Biomed. Pharmacother. 95 (2017), 1535–1548.
135. Yamashita, M., Ukibe, K., Matsubara, Y., Hosoya, T., Sakai, F., Kon, S., et al. Lactobacillus helveticus SBT2171 attenuates experimental autoimmune encephalomyelitis in mice. Front. Microbiol., 8, 2017, 2596.
136. Tankou, S.K., Regev, K., Healy, B.C., Tjon, E., Laghi, L., Cox, L.M., et al. A probiotic modulates the microbiome and immunity in multiple sclerosis. Ann. Neurol., 2018.
137. Kouchaki, E., Tamtaji, O.R., Salami, M., Bahmani, F., Daneshvar Kakhaki, R., Akbari, E., et al. Clinical and metabolic response to probiotic supplementation in patients with multiple sclerosis: a randomized, double-blind, placebo-controlled trial. Clin. Nutr. 36 (2017), 1245–1249.