Probiotic modulation of innate cell pathogen sensing and signaling events

Nutrients

Volumn 9, Issue 10, 2017, Pages

  Llewellyn, Amy ^a,b   Foey, Andrew ^a  

^a PLYMOUTH UNIVERSITY PENINSULA SCHOOLS OF MEDICINE AND DENTISTRY   (United Kingdom)

^b ROYAL DARWIN HOSPITAL   (Australia)

Author keywords

Cytokines; Dendritic cells; Epithelial cells; Immunomodulation; Inflammation; Innate; Macrophages; Neutrophils; Probiotics; Signaling

Indexed keywords

1 ACYLGLYCEROPHOSPHOCHOLINE ACYLTRANSFERASE; CASPASE RECRUITMENT DOMAIN PROTEIN 15; CD14 ANTIGEN; ENDOTOXIN; FLAGELLIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INFLAMMASOME; INTERLEUKIN 10; INTERLEUKIN 12; INTERLEUKIN 1BETA; INTERLEUKIN 6; MACROPHAGE INFLAMMATORY PROTEIN 1ALPHA; MICRORNA; MITOGEN ACTIVATED PROTEIN KINASE; MONOCYTE CHEMOTACTIC PROTEIN 1; MYELOID DIFFERENTIATION FACTOR 88; PHOSPHATIDYLINOSITOL 3 KINASE; PROBIOTIC AGENT; PROTEIN P40; PROTEIN P75; SMAD5 PROTEIN; STAT6 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 1; TOLL LIKE RECEPTOR 1; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TOLL LIKE RECEPTOR 5; TOLL LIKE RECEPTOR 9; TUMOR NECROSIS FACTOR; UNINDEXED DRUG;

APOPTOSIS; CELL INTERACTION; CYTOKINE PRODUCTION; GENE EXPRESSION; HUMAN; IMMUNOLOGICAL TOLERANCE; IMMUNOMODULATION; INFLAMMATION; INNATE IMMUNITY; INTESTINE EPITHELIUM CELL; LACTOBACILLUS; LIPID RAFT; MAPK SIGNALING; MUCOSAL IMMUNITY; NONHUMAN; PROTEIN EXPRESSION; REVIEW; SACCHAROMYCES; SIGNAL TRANSDUCTION; STREPTOCOCCUS; TIGHT JUNCTION; CYTOLOGY; EPITHELIUM CELL; HOMEOSTASIS; INTESTINE; INTESTINE FLORA; MACROPHAGE; MICROBIOLOGY; NATURAL KILLER CELL; NEUTROPHIL; STOMACH MUCOSA;

EPITHELIAL CELLS; GASTRIC MUCOSA; GASTROINTESTINAL MICROBIOME; HOMEOSTASIS; HUMANS; IMMUNITY, INNATE; IMMUNITY, MUCOSAL; IMMUNOMODULATION; INFLAMMASOMES; INTESTINES; KILLER CELLS, NATURAL; MACROPHAGES; NEUTROPHILS; PROBIOTICS; SIGNAL TRANSDUCTION;

EID: 85032257195     PISSN: None     EISSN: 20726643     Source Type: Journal    
DOI: 10.3390/nu9101156     Document Type: Review

References (144)

1. FAO/WHO. Health and Nutritional Properties of Probiotics in Food Including Powder Milk with Live Lactic Acid Bacteria; World Health Organization: Basel, Switzerland, 2001.
2. Borcher, A.T.; Selmi, C.; Meyers, F.J.; Keen, C.L.; Gershwin, M.E. Probiotics and immunity. J. Gastroenterol. 2009, 44, 26-46.
3. Hardy, H.; Harris, J.; Lyon, E.; Beal, J.; Foey, A.D. Probiotics, prebiotics and immunomodulation of gut mucosal defences: Homeostasis and immunopathology. Nutrients 2013, 5, 1869-1912.
4. Saxelin, M.; Tynkkynen, S.; Mattila-Sandholm, T.; M de Vos, W. Probiotic and other functional microbes: From markets to mechanisms. Curr. Opin. Biotechnol. 2005, 16, 204-211.
5. Peterson, L.W.; Atris, D. Intestinal epithelial cells: Regulators of barrier function and immune homeostasis. Nat. Rev. Immunol. 2014, 14, 141-153.
6. Vastano, V.; Pagano, A.; Fusco, A.; Merola, G.; Sacco, M.; Donnarumma, G. The Lactobacillus plantarum Eno A1 enolase is involved in immunostimulation of Caco-2 cells and in biofilm development. Adv. Exp. Med. Biol. 2016, 897, 33-44.
7. Zyrek, A.A.; Cichon, C.; Helms, S.; Enders, C.; Sonnenborn, U.; Schmidt, M.A. Molecular mechanisms underlying the probiotic effects of Escherichia coli Nissle 1917 involve ZO-2 and PKCzeta redistribution resulting in tight junction and epithelial barrier repair. Cell Microbiol. 2007, 9, 804-816.
8. Schlee, M.; Harder, J.; Koten, B.; Stange, E.F.; Wehkamp, J.; Fellermann, K. Probiotic lactobacilli and VSL#3 induce enterocyte β-defensin 2. Clin. Exp. Immunol. 2008, 151, 528-535.
9. Liu, H.; Hou, C.; Wang, G.; Jia, H.; Yu, H.; Zeng, X.; Thacker, P.A.; Zhang, G.; Qiao, S. Lactobacillus reuteri I5007 modulates intestinal host defense peptide expression in the model of IPEC-J2 cells and neonatal piglets. Nutrients 2017, 9, 559.
10. Resta-Lenert, S.; Barrett, K.E. Live probiotics protect intestinal epithelial cells from the effects of infection with enteroinvasive Escherichia coli (EIEC). Gut 2003, 52, 988-997.
11. Chen, X.; Kokkotou, E.G.; Mustafa, N.; Bhaskar, K.R.; Sougioultzis, S.; O’Brien, M.; Pothoulakis, C.; Kelly, C.P. Saccharomyces boulardii inhibits ERK1/2 mitogen-activated protein kinase activation both in vitro and in vivo and protects against Clostridium difficile toxin A-induced enteritis. J. Biol. Chem. 2006, 281, 24449-24454.
12. Suzuki, T. Regulation of intestinal epithelial permeability by tight junctions. Cell. Mol. Life Sci. 2013, 70, 631-659.
13. Segatto, O.; Anastasi, S.; Alemà, S. Regulation of epidermal growth factor receptor signalling by inducible feedback inhibitors. J. Cell Sci. 2011, 128, 1785-1793.
14. Fanning A.S.; Jameson, B.J.; Jesaitis, L.A.; Anderson, J.M. The tight junction protein ZO-1 establishes a link between the transmembrane protein occludin and the actin cytoskeleton. J. Biol. Chem. 1998, 273, 29745-29753.
15. Schulzke, J.D.; Ploeger, S.; Amasheh, M.; Fromm, A.; Zeissig, S.; Troeger, H.; Richter, J.; Bojarski, C.; Schumann, M.; Fromm, M. Epithelial Tight Junctions in Intestinal Inflammation. Ann. N. Y. Acad. Sci. 2009, 1165, 294-300.
16. Orlando, A.; Linsalata, M.; Notarnicola, M.; Tutino, V.; Russo, F. Lactobacillus GG restoration of the gliadin induced epithelial barrier disruption: The role of cellular polyamines. BMC Microbiol. 2014, 14, 19.
17. Karczewski, J.; Troost, F.J.; Konings, I.; Dekker, J.; Kleerebezem, M.; Brummer, R.-J.M.; Wells, J.M. Regulation of human epithelial tight junction proteins by Lactobacillus plantarum in vivo and protective effects on the epithelial barrier. Am. J. Physiol. Gastrointest. Liver Physiol. 2010, 298, 851-859.
18. Zhang, W.; Zhu, Y.H.; Yang, J.C.; Yang, G.Y.; Zhou, D.; Wang, J.F. A Selected Lactobacillus rhamnosus Strain Promotes EGFR-Independent Akt Activation in an Enterotoxigenic Escherichia coli K88- Infected IPEC-J2 Cell Model. PLoS ONE 2015, 10, e0125717.
19. Dent, P.; Yacoub, A.; Fisher, P.B.; Hagan, M.P.; Gran, S. MAPK pathways in radiation responses. Oncogene 2003, 22, 5885-5896.
20. Dai, C.; Zhao, D.-H.; Jiang, M. VSL#3 probiotics regulate the intestinal epithelial barrier in vivo and in vitro via the p38 and ERK signaling pathways. Int. J. Mol. Med. 2012, 29, 202-208.
21. Tao, Y.; Drabik, K.A.; Waypa, T.S.; Musch, M.W.; Alverdy, J.C.; Schneewind, O.; Chang, E.B.; Petrof, E.O. Soluble factors from Lactobacillus GG activate MAPKs and induce cytoprotective heat shock proteins in intestinal epithelial cells. Am. J. Physiol. Cell Physiol. 2006, 290, C1018-C1030.
22. Yan, F.; Liu, L.; Dempsey, P.J.; Tsai, Y.H.; Raines, E.W.; Wilson, C.L.; Cao, H.; Cao, Z.; Lui, L.; Polk, D.B. A Lactobacillus rhamnosus GG-derived soluble protein, p40, stimulates ligand release from intestinal epithelial cells to transactivate epidermal growth factor receptor. J. Biol. Chem. 2013, 288, 30742-30751.
23. Yoda, K.; Miyazawa, K.; Hosoda, M.K.; Hiramatsu, M.; Yan, F.; He, F. Lactobacillus GG-fermented milk prevents DSS-induced colitis and regulates intestinal epithelial homeostasis through activation of epidermal growth factor receptor. Eur. J. Nutr. 2014, 53, 105-115.
24. Yoda, K.; He, F.; Miyazawa, K.; Hiramatsu, M.; Yan, F. Fermented milk containing Lactobacillus GG alleviated DSS-induced colitis in mice and activated epidermal growth factor receptor and Akt signaling in intestinal epithelial cells. Microb. Ecol. Health Dis. 2012, 23, 1651-2235.
25. Tomosada, Y.; Villena, J.; Murata, K.; Chiba, E.; Shimazu, T.; Aso, H.; Iwabuchi, N.; Xiao, J.Z.; Saito, T.; Kitazawa, H. Immunoregulatory effect of bifidobacteria strains in porcine intestinal epithelial cells through modulation of ubiquitin-editing enzyme A20 expression. PLoS ONE 2013, 8, e59259.
26. Kim, S.W.; Kim, H.M.; Yang, K.M.; Kim, S.A.; Kim, S.K.; An, M.J.; Park, J.J.; Lee, S.K.; Kim, T.I.; Kim, W.H.; et al. Bifidobacterium lactis inhibits NF-kappaB in intestinal epithelial cells and prevents acute colitis and colitis-associated colon cancer in mice. Inflamm. Bowel Dis. 2010, 16, 1514-1525.
27. Finamore, A.; Roselli, M.; Imbinto, A.; Seeboth, J.; Oswald, I.P.; Mengheri, E. Lactobacillus amylovorus inhibits the TLR4 inflammatory signaling triggered by enterotoxigenic Escherichia coli via modulation of the negative regulators and involvement of TLR2 in intestinal Caco-2 Cells and pig explants. PLoS ONE 2014, 9, e94891.
28. Takanashi, N.; Tomosada, Y.; Villena, J.; Murata, K.; Takahashi, T.; Chiba, E.; Tohno, M.; Shimazu, T.; Aso, H.; Suda, Y.; et al. Advanced application of bovine intestinal epithelial cell line for evaluating regulatory effect of lactobacilli against heat-killed enterotoxigenic Escherichia coli-mediated inflammation. BMC Microbiol. 2013, 13, e54.
29. Mirpuri, J.; Sotnikov, I.; Myers, L.; Denning, T.L.; Yarovinsky, F.; Parkos, C.A. Lactobacillus rhamnosus (LGG) Regulates IL-10 signaling in the developing murine colon through upregulation of the IL-10R2 receptor subunit. PLoS ONE 2012, 7, e51955.
30. Lin, P.W.; Myers, L.E.S.; Ray, L.; Song, S.C.; Nasr, T.R.; Berardinelli, A.J.; Kundu, K.; Murthy, N.; Hansen, J.M.; Neish, A.S. Lactobacillus rhamnosus blocks inflammatory signaling in vivo via reactive oxygen species generation. Free Radic. Biol. Med. 2009, 47, 1205-1211.
31. Yan, F.; Cao, H.; Cover, T.L.; Washington, M.K.; Shi, Y.; Liu, L.; Chaturvedi, R.; Peek, R.M., Jr.; Wilson, K.T.; Polk, D.B. Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. J. Clin. Invest. 2011, 121, 2242-2253.
32. Shimazu, T.; Villena, J.; Tohno, M.; Fujie, H.; Hosoya, S.; Shimosato, T.; Aso, H.; Suda, Y.; Kawai, Y.; Saito, T.; et al. Immunobiotic Lactobacillus jensenii elicits anti-inflammatory activity in porcine intestinal epithelial cells by modulating negative regulators of the Toll-like receptor signaling pathway. Infect. Immun. 2012, 80, 276-288.
33. Liu, Y.; Fatheree, N.Y.; Mangalat, N.; Rhoads, J.M. Lactobacillus reuteri strains reduce incidence and severity of experimental necrotizing enterocolitis via modulation of TLR4 and NF-κB signaling in the intestine. Am. J. Physiol. Gastrointest. Liver Physiol. 2011, 302, 608-617.
34. Zanello, G.; Berri, M.; Dupont, J.; Sizaret, P.-Y.; D’Inca, R.; Salmon, H.; Meurens, F. Saccharomyces cerevisiae modulates immune gene expressions and inhibits ETEC-mediated ERK1/2 and p38 signaling pathways in intestinal epithelial cells. PLoS ONE 2011, 6, e18573.
35. Kaci, G.; Lakhdari, O.; Doré, J.; Dusko-Ehrlich, S.; Renault, P.; Blottiere, H.M.; Delorme, C. Inhibition of the NF-κB pathway in human intestinal epithelial cells by commensal streptococcus salivarius. Appl. Environ. Microbiol. 2011, 77, 4681-4684.
36. Petrof, E.O.; Kojima, K.; Ropeleski, M.J.; Musch, M.W.; Tao, Y.; De Simone, C.; Chang, E.B. Probiotics inhibit nuclear factor-kappa B and induce heat shock proteins in colonic epithelial cells through proteasome inhibition. Gastroenterology 2004, 127, 1474-1487.
37. Kawai, T.; Akira, S. Signaling to NF-κB by Toll-like receptors. Trends Mol. Med. 2007, 13, 460-469.
38. Akira, S.; Uematsu, S.; Takeuchi, O. Pathogen Recognition and Innate Immunity. Cell 2006, 124, 783-801.
39. Takeda, K.; Akira, S. Toll-like receptors. Curr. Protoc. Immunol. 2015, 12-14.
40. Manicassamy, S.; Pulendran, B. Modulation of adaptative immunity with Toll-like receptors. Semin. Immunol. 2009, 21, 185-193.
41. Karin, M.; Ben-Neriah, Y. Phosphorylation meets ubiquitination: The control of NF-κB activity. Ann. Revs. Immunol. 2000, 18, 621-663.
42. Moue, M.; Tohno, M.; Shimazu, T.; Kido, T.; Aso, H.; Saito, T.; Kitazawa, H. Toll-like receptor 4 and cytokine expression involved in functional immune response in an originally established porcine intestinal epitheliocyte cell line. BBA 2008, 1780, 134-144.
43. Shibolet, O.; Podolsky, D.K. TLRs in the Gut. IV. Negative regulation of Toll-like receptors and intestinal homeostasis: Addition by subtraction. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 292, 1469-1473.
44. Xiao, H.; Gulen, M.F.; Qin, J.; Yao, J.; Bulek, K.; Kish, D.; Altuntas, C.Z.; Wakd, D.; Ma, C.; Zhou, H.; et al. The Toll-interleukin-1 receptor member SIGIRR regulates colonic epithelial homeostasis, inflammation, and tumorigenesis. Immunity 2007, 26, 461-475.
45. Boone, D.L.; Turer, E.E.; Lee, E.G.; Ahmad, R.C.; Wheeler, M.T.; Tsui, C.; Hurley, P.; Chien, M.; Chai, S.; Hitotsumatsu, O.; et al. The ubiquitin-modifying enzyme A20 is required for termination of Toll-like receptor responses. Nat. Immunol. 2004, 5, 1052-1060.
46. Lamothe, B.; Besse, A.; Campos, A.D.; Webster, W.K.; Wu, H.; Darnay, B.G. Site-specific Lys-63-linked tumor necrosis factor receptor-associated factor 6 auto-ubiquitination is a critical determinant of I kappa B kinase activation. J. Biol. Chem. 2007, 282, 4102-4112.
47. Donato, K.A.; Gareau, M.G.; Wang, Y.J.; Sherman, P.M. Lactobacillus rhamnosus GG attenuates interferon-c and tumour necrosis factor-a-induced barrier dysfunction and pro-inflammatory signaling. Microbiology 2010, 156, 3288-3297.
48. Kumar, A.; Wu, H.; Collier-Hyams, L.S.; Hansen, J.M.; Li, T.; Yamoah, K.; Pan, Z.Q.; Jones, D.P.; Neish, A.S. Commensal bacteria modulate cullin-dependent signaling via generation of reactive oxygen species. EMBO J. 2007, 26, 4457-4466.
49. Hutchins, A.P. The IL-10/STAT3-mediated anti-inflammatory response: Recent developments and future challenges. Brief. Funct. Genom. 2013, 12, 489-498.
50. Iwasaki, A.; Sato, A. Intestinal epithelial barrier and mucosal immunity. Cell. Mol. Life Sci. 2005, 62, 1333-1338.
51. Mabbott, N.A.; Donaldson, D.S.; Ohno H.; Williams I.R.; Mahajan, A. Microfold (M) cells: Important immunosurveillance posts in the intestinal epithelium. Mucosal Immunol. 2013, 6, 666-677.
52. MacPherson, G.; Milling, S.; Yrlid, U.; Cousins, L.; Turnbull, E.; Huang, A.P. Uptake of antigens from the intestine by Dendritic Cells. Ann. N. Y. Acad. Sci. 2004, 1029, 75-82.
53. Melmed, G.; Thomas, L.S.; Lee, N.; Tesfay, S.Y.; Lukasek, K.; Michelsen, K.S.; Zhou, Y.; Hu, B.; Arditi, M.; Abreu, M.T. Human intestinal epithelial cells are broadly unresponsive to Toll-like receptor 2-dependent bacterial ligands: Implications for host-microbial interactions in the gut. J. Immunol. 2003, 170, 1406-1415.
54. Lee, J.; Mo, J.H.; Katakura, K.; Alkalay, I.; Rucker, A.N.; Liu, Y.T.; Lee, H.K.; Shen, C.; Cojocaru, G.; Shenouda, S.; et al. Maintenance of colonic homeostasis by distinctive apical TLR9 signalling in intestinal epithelial cells. Nat. Cell Biol. 2006, 8, 1327-1336.
55. Zhong, Y.; Huang, J.; Tang, W.; Chen, B.; Cai, W. Effects of probiotics, probiotic DNA and the CpG oligodeoxynucleotides on ovalbumin-sensitized Brown- Norway rats via TLR9/NF-κB pathway. FEMS Immunol. Med. Microbiol. 2012, 66, 71-82.
56. Ghadimi, D.; Vrese, M.; Heller, K.J.; Schrezenmeir, J. Effect of natural commensal- origin DNA on toll-like receptor 9 (TLR9) signaling cascade, chemokine IL-8 expression, and barrier integritiy of polarized intestinal epithelial cells. Inflamm. Bowel Dis. 2010, 16, 410-427.
57. Bouladoux, N.; Hall, J.A.; Grainger, J.R.; dos Santos, L.M.; Kann, M.G.; Nagarajan, V.; Verthelyi, D.; Belkaid, Y. Regulatory role of suppressive motifs from commensal DNA. Mucosal Immunol. 2012, 5, 623-634.
58. Iliev, I.D.; Spadoni, I.; Mileti, E.; Matteoli, G.; Sonzogni, A.; Sampietro, G.M.; Foschi, D.; Caprioli, F.; Viale, G.; Rescigno, M. Human intestinal epithelial cells promote the differentiation of tolerogenic dendritic cells. Gut 2009, 58, 1481-1489.
59. Coombes, J.L.; Siddiqui, K.R.; Arancibia-Cárcamo, C.V.; Hall, J.; Sun, C.M.; Belkaid, Y.; Powrie, F. A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-beta and retinoic acid-dependent mechanism. J. Exp. Med. 2007, 204, 1757-1764.
60. Jeon, S.G.; Kayama, H.; Ueda, Y.; Takahashi, T.; Asahara, T.; Tsuji, H.; Tsuji, N.M.; Kiyono, H.; Ma, J.S.; Kusu, T.; et al. Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLoS Pathog. 2012, 8, e1002714.
61. Macho Fernandez, E.; Valenti, V.; Rockel, C.; Hermann, C.; Pot, B.; Boneca, I.G.; Grangette, C. Anti-inflammatory capacity of selected lactobacilli in experimental colitis is driven by NOD2-mediated recognition of a specific peptidoglycan-derived muropeptide. Gut 2011, 60, 1050-1059.
62. Kwon, H.-K.; Lee, C.-G.; So, J.-S.; Chae, C.S.; Hwang, J.S.; Sahoo, A.; Nam, J.H.; Rhee, J.H.; Hwang, K.C.; Im, S.H. Generation of regulatory dendritic cells and CD4+Foxp3+ T cells by probiotics administration suppresses immune disorders. Proc. Natl. Acad. Sci. USA 2010, 107, 2159-2164.
63. Zeuthen, L.H.; Fink, L.N.; Frøkiær, H. Toll-like receptor 2 and nucleotide-binding oligomerization domain-2 play divergent roles in the recognition of gut-derived lactobacilli and bifidobacteria in dendritic cells. Immunology 2008, 24, 489-502.
64. Bermudez-Brito, M.; Muñoz-Quezada, S.; Gomez-Llorente, C.; Matencio, E.; Bernal, M.J.; Romero, F.; Gil, A. Cell-free culture supernatant of Bifidobacterium breve CNCM I-4035 decreases pro-inflammatory cytokines in human dendritic cells challenged with Salmonella typhi through TLR activation. PLoS ONE 2013, 8, e59370.
65. Zhang, G.; Ghosh, S. Negative regulation of toll-like receptor-mediated signalling by Tollip. J. Biol. Chem. 2002, 277, 7059-7065.
66. Bermudez-Brito, M.; Muñoz-Quezada, S.; Gomez-Llorente, C.; Matencio, E.; Bernal, M.J.; Romero, F.; Gil, A. Human Intestinal Dendritic Cells Decrease Cytokine Release against Salmonella Infection in the Presence of Lactobacillus paracasei upon TLR Activation. PLoS ONE 2012, 7, e43197.
67. Bermudez-Brito, M.; Muñoz-Quezada, S.; Gomez-Llorente, C.; Romero, F.; Gil, A. Lactobacillus rhamnosus and its cell-free culture supernatant differentially modulate inflammatory biomarkers in Escherichia coli-challenged human dendritic cells. Br. J. Nutr. 2014, 111, 1727-1737.
68. Christensen, H.R.; Frokiaer, H.; Pestka, J.J. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J. Immunol. 2002, 168, 171-178.
69. Di Santo, J.P.; Vosshenrich, C.A.; Satoh-Takayama, N. A ʼnatural’ way to provide innate mucosal immunity. Curr. Opin. Immunol. 2010, 22, 435-441.
70. Dong, H.; Rowland, I.; Tuohy, K.M.; Thomas, L.V.; Yaqoob, P. Selective effects of Lactobacillus casei Shirota on T-cell activation, natural killer cell activity and cytokine production. Clin. Exp. Immunol. 2010, 161, 378-388.
71. Fink, L.N.; Zeuthen, L.H.; Christensen, H.R.; Morandi, B.; Frokiaer, H.; Ferlazzo, G. Distinct gut-derived lactic acid bacteria elicit divergent dendritic cell-mediated NK cell responses. Int. Immunol. 2007, 19, 1319-1327.
72. Koizumi, S.; Wakita, D.; Sato, T.; Mitamura, R.; Izumo, T.; Shibata, H.; Kiso, Y.; Chamoto, K.; Togashi, Y.; Kitamura, H.; Nishimura, T. Essential role of Toll-like receptors for dendritic cell and NK1.1(+) cell-dependent activation of type 1 immunity by Lactobacillus pentosus strain S-PT84. Immunol. Lett. 2008, 120, 14-19.
73. Takeda, K.; Suzuki, T.; Shimada, S.-I.; Shida, K.; Nanno, M.; Okumura, K. Interleukin-12 is involved in the enhancement of human natural killer cell activity by Lactobacillus casei Shirota. Clin. Exp. Immunol. 2006, 146, 109-115.
74. Takeda, K.; Okumura, K. Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the human NK-cell activity. J. Nutr. 2007, 137, 791S-793S.
75. 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 manganedse superoxide dismutase using the interleukin 10-deficient mouse model of colitis. Am. J. Physiol. Gastrointest. Liver Physiol. 2007, 293, G729-G738.
76. Roselli, M.; Finamore, A.; Britti, M.S.; Mengheri, E. Probiotic bacteria Bifidobacterium animalis MB5 and Lactobacillus rhamnosus GG protect intestinal Caco-2 cells from the inflammation-associated response induced by enterotoxigenic Escherichia coli K88. Br. J. Nutr. 2006, 95, 1177-1184.
77. Arunachalam, K.; Gill, H.S.; Chandra, R.K. Enhancement of natural immune function by dietary consumption of Bifidobacterium lactis (HN019). Eur. J. Clin. Nutr. 2000, 54, 263-267.
78. Souza, E.L.; Elian, S.D.; Paula, L.M.; Garcia, C.C.; Viera A.T.; Teixeira, M.M.; Arantes, R.M.; Nicoli, J.R.; Martins, F.S. Escherichia coli strain Nissle 1917 ameliorates experimental colitis by modulating intestinal permeability, the inflammatory response and clinical signs in a faecal transplantation model. J. Med. Microbiol. 2016, 65, 201-210.
79. Zheng, B.; van Bergenhenegouwen, J.; van de Kant, H.J.G.; Folkerts, G.; Garssen, J.; Vos, A.P.; Morgan, M.E.; Kraneveld, A.D. Specific probiotic dietary supplementation leads to different effects during remission and relapse in murine chronic colitis. Benef Microbes 2016, 7, 205-213.
80. Elian, S.D.; Souza, E.L.; Vieira, A.T.; Teixeira, M.M.; Arantes, R.M.; Nicoli, J.R.; Martins, F.S. Bifidobacterium longum subsp. Infantis BB-02 attenuates acute murine experimental model of inflammatory bowel disease. Benef. Microbes 2015, 6, 277-286.
81. Boonma, P.; Spinler, J.K.; Venable, S.F.; Versalovic, J.; Tumwasorn, S. Lactobacillus rhamnosus L34 and Lactobacillus casei L39 suppress Clostridium difficile-induced IL-8 production by colonic epithelial cells. BMC Microbiol. 2014, 14, 177.
82. Xu, X.; Hicks, C.; Li, Y.; Su, J.; Shiloach, J.; Kaufman, J.B.; Fitz, Y.; Eichacker, P.Q.; Cui, X. Purified cell wall from the probiotic bacterium Lactobacillus gasseri activates systemic inflammation and, at higher doses, produces lethality in a rat model. Crit. Care 2014, 18, R140.
83. Kim, H.J.; Kim, Y.J.; Lee, S.H.; Yu, J.; Jeong, S.K.; Hong, S.J. Effects of Lactobacillus rhamnosus on allergic march model by suppressing Th2, Th17, and TSLP responses via CD4(+)CD25(+)Foxp3(+) Tregs. Clin. Immunol. 2014, 153, 178-186.
84. Vong, L.; Lorentz, R.J.; Assa, A.; Glogauer, M.; Sherman, P.M. Probiotic Lactobacillus rhamnosus inhibits the formation of neutrophil extracellular traps. J. Immunol. 2014, 192, 1870-1877.
85. Hidemura, A.; Saito, H.; Fukatsu, K.; Matsuda, T.; Kitayama, J.; Ikeda, S.; Kang, W.; Nagawa, H. Oral administration of Bifidobacterium longum culture condensate in a diet-restricted murine peritonitis model enhances polymorphonuclear neutrophil recruitment into the local inflammatory site. Nutrition 2003, 19, 270-274.
86. Lammers, K.M.; Vergopoulos, A.; Babel, N.; Gionchetti, P.; Rizzello, F.; Morselli, C.; Caramelli, E.; Fiorentino, M.; d’Errico, A.; et al. Probiotic therapy in the prevention of pouchitis onset: Decreased interleukin-1beta, interleukin-8, and interferon-gamma gene expression. Inflamm. Bowel Dis. 2005, 11, 447-454.
87. Peral, M.C.; Rachid, M.M.; Gobbato, N.M.; Huaman Martinez, M.A.; Valdez, J.C. Interleukin-8 production by polymorphonuclear leukocytes from patients with chronic infected leg ulcers treated with Lactobacillus plantarum. Clin. Microbiol. Infect. 2010, 16, 281-286.
88. Shinnoh, M.; Horinaka, M.; Yasuda, T.; Yoshikawa, S.; Morita, M.; Yamada, T.; Miki, T.; Sakai, T. Clostridium butyricum MIYAIRI 588 shows antitumour effects by enhancing the release of TRAIL from neutrophils through MMP-8. Int. J. Oncol. 2013, 42, 903-911.
89. Kim, S.O.; Sheikh, H.I.; Ha, S.D.; Martins, A.; Reid, G. G-CSF-mediated inhibition of JNK is a key mechanism for Lactobacillus rhamnosus-induced suppression of TNF production in macrophages. Cell. Microbiol. 2006, 8, 1958-1971.
90. Lee, J.S.; Paek, N.S.; Kwon, O.S.; Hahm, K.B. Anti-inflammatory actions of probiotics through activating suppressor of cytokine signaling (SOCS) expression and signaling in Helicobacter pylori infection: A novel mechanism. J. Gastroenterol. Hepatol. 2010, 25, 194-202.
91. Latvala, S.; Miettinen, M.; Kekkonen, R.A.; Korpela, R.; Julkunen, I. Lactobacillus rhamnosus GG and Streptococcus thermophiles induce suppressor of cytokine signalling 3 (SOCS3) gene expression directly and indirectly via interleukin-10 in human primary macrophages. Clin. Exp. Immunol. 2011, 165, 94-103.
92. O’Shea, J.J.; Murray, P.J. Cytokine signaling modules in inflammatory responses. Immunity 2008, 28, 477-487.
93. Watanabe, T.; Nishio, H.; Tanigawa, T.; Yamagami, H.; Okazaki, H.; Watanabe, K.; Tominaga, K.; Fujiwara, Y.; Oshitani, N.; Asahara, T.; et al. Probiotic Lactobacillus casei strain Shirota prevents indomethacin-induced small intestinal injury: Involvement of lactic acid. Am. J. Physiol. Gastrointest. Liver Physiol. 2009, 297, 506-513.
94. Sougioultzis, S.; Simeonidis, S.; Bhaskar, K.R.; Chen, X.; Anton, P.M.; Keates, S.; Pothoulakis, C.; Kelly, C.P. Saccharomyces boulardii produces a soluble anti-inflammatory factor that inhibits NF-κB-mediated IL-8 gene expression. Biochem. Biophys. Res. Commun. 2006, 343, 69-76.
95. Ménard, S.; Candalh, C.; Bambou, J.C.; Terpend, K.; Cerf-Bensussan, N.; Heyman, M. Lactic acid bacteria secrete metabolites retaining anti-inflammatory properties after intestinal transport. Gut 2004, 53, 821-828.
96. Kim, H.G.; Kim, N.R.; Gim, M.G.; Lee, J.M.; Lee, S.Y.; Ko, M.Y. Lipoteichoic acid isolated from Lactobacillus plantarum inhibits lipopolysaccharide-induced TNF-a production in THP-1 cells and endotoxin shock in mice. J. Immunol. 2008, 180, 2553-2561.
97. Kim, H.G.; Lee, S.Y.; Kim, N.R.; Ko, M.Y.; Lee, J.M.; Yi, T.H.; Chung, S.K.; Chung, D.K. Inhibitory effects of Lactobacillus plantarum lipoteichoic acid (LTA) on Staphylococcus aureus LTA-induced tumor necrosis factor-α production. J. Microbiol. Biotechnol. 2008, 18, 1191-1196.
98. Kim, H.G.; Lee, S.Y.; Kim, N.R.; Lee, H.Y.; Ko, M.Y.; Jung, B.J.; Kim, C.M.; Lee, J.M.; Park, J.H.; Han, S.H.; et al. Lactobacillus plantarum lipoteichoic acid down-regulated Shigella flexneri peptidoglycan-induced inflammation. Mol. Immunol. 2011, 48, 382-391.
99. Lin, Y.P.; Thibodeaux, C.H.; Peña, J.A.; Ferry, G.D.; Versalovic, J. Probiotic Lactobacillus reuteri suppress proinflammatory cytokines via c-Jun. Inflamm. Bowel Dis. 2008, 14, 1068-1083.
100. Okada, Y.; Tsuzuki, Y.; Hokari, R.; Komoto, S.; Kurihara, C.; Kawaguchi, A.; Nagao, S.; Miura, S. Anti-inflammatory effects of the genus Bifidobacterium on macrophages by modification of phospho-IkB and SOCS gene expression. Int. J. Exp. Path. 2009, 90, 131-140.
101. Martins, A.J.; Colquhoun, P.; Reid, G.; Kim, S.O. Reduced expression of basal and probiotic-inducible G-CSF in intestinal mononuclear cells is associated with inflammatory bowel disease. Inflamm. Bowel Dis. 2009, 15, 515-525.
102. Martins, A.J.; Spanton, S.; Sheikh, H.I.; Kim, S.O. The anti-inflammatory role of granulocyte colony-stimulating factor in macrophage- dendritic cell crosstalk after Lactobacillus rhamnosus GR-1 exposure. J. Leukoc. Biol. 2011, 89, 907-915.
103. Habil, N.; Al-Murrani, W.; Beal, J.; Foey, A.D. Probiotic bacterial strains differentially modulate macrophage cytokine production in a strain-dependent and cell subset-specific manner. Benef. Microbes 2011, 2, 283-293.
104. Habil, N.; Beal, J.; Foey, A.D. Lactobacillus casei strain Shirota selectively modulates macrophage subset cytokine production. Int. J. Probiot. Prebiot. 2012, 7, 1-12.
105. Saemann, M.D.; Bohmig, G.A.; Osterreicher, C.H.; Burtscher, H.; Parolini, O.; Diakos, C.; Stockl, J.; Horl, W.H.; Zlabinger, G.J. Anti-inflammatory effects of sodium butyrate on human monocytes: Potent inhibition of IL-12 and up-regulation of IL-10 production. FASEB J. 2000, 14, 2380-2382.
106. Foey, A.D. Butyrate regulation of distinct macrophage subsets: Opposing effects on M1 and M2 macrophages. Int. J. Probiot. Prebiot. 2011, 6, 147-158.
107. Kaji, R.; Kiyoshima-Shibata, J.; Nagaoka, M.; Nanno, M.; Shida, K. 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. J. Immunol. 2010, 184, 3505-3513.
108. Lammers, K.M.; Brigidi, P.; Vitali, B.; Gionchetti, P.; Rizzello, F.; Caramelli, E.; Matteuzzi, D.; Campieri, M. Immunomodulatory effects of probiotic bacteria DNA: IL-1 and IL-10 response in human peripheral blood mononuclear cells. FEMS Immunol. Med. Microbiol. 2003, 38, 165-172.
109. Sun, K.-Y.; Xu, D.-H.; Xie, C.; Plummer, S.; Tang, J.; Yang, X.F.; Ji, X.H. Lactobacillus paracasei modulates LPS-induced inflammatory cytokine release by monocyte-macrophages via the up-regulation of negative regulators of NF-kappaB signaling in a TLR2-dependent manner. Cytokine 2017, 92, 1-11.
110. Foey, A.D. Macrophage polarization: A collaboration of differentiation, activation and pre-programming? J. Clin. Cell Immunol. 2015, 6, 1-15.
111. Merry, R.; Belfield, L.; McArdle, P.; McLennan, A.; Crean, S.J.; Foey, A. Oral health and pathology: A macrophage account. Br. J. Oral Maxillofac. Surg. 2012, 50, 2-7.
112. Elinav, E.; Strowig, T.; Henao-Mejia, J.; Flavell, R.A. Regulation of the antimicrobial response by NLR proteins. Immunity 2011, 34, 665-679.
113. Martinon, F.; Burns, K.; Tschopp, J. The inflammasome: A molecular platform triggering activation of inflammatory caspases and processing of proIL-1beta. Mol. Cell 2002, 10, 417-426.
114. Faustin, B.; Lartigue, L.; Bruey, J.M.; Luciano, F.; Sergienko, E.; Bailly-Maitre, B.; Volkmann, N.; Hanein, D.; Rouiller, I.; Reed, J.C. Reconstituted NALP1 inflammasome reveals two-step mechanism of caspase-1 activation. Mol. Cell 2007, 25, 713-724.
115. Hsu, L.C.; Ali, S.R.; McGillivray, S.; Tseng, P.H.; Mariathasan, S.; Humke, E.W.; Eckmann, L.; Powell, J.J.; Nizet, V.; Dixit, V.M.; et al. A NOD2-NALP1 complex mediates caspase-1-dependent IL-1beta secretion in response to Bacillus anthracis infection and muramyl dipeptide. Proc. Natl. Acad. Sci. USA 2008, 107, 21635-21640.
116. Guarda, G.; Braun, M.; Staehil, F.; Tardivel, A.; Mattmann, C.; Forster, I.; Farlik, M.; Decker, T.; Du Pasquier, R.A.; Romero, P.; Tschopp, J. Type I interferon inhibits interleukin-1 production and inflammasome activation. Immunity 2011, 34, 213-223.
117. Iliev, I.D.; Kitazawa, H.; Shimosato, T.; Katoa, S.; Morita, H.; He, F.; Hosoda, M.; Saito, T. Strong immunostimulation in murine immune cells by Lactobacillus rhamnosus GG DNA containing novel oligodeoxynucleotide pattern. Cell. Microbiol. 2005, 7, 403-414.
118. Girardin, S.E.; Boneca, I.G.; Viala, J.; Chamaillard, M.; Labigne, A.; Thomas, G.; Philpott, D.J.; Sansonetti, P.J. Nod2 is a general sensor of peptidoglycan through muramyl dipeptide (MDP) detection. J. Biol. Chem. 2003, 278, 8869-8872.
119. Triantafilou, M.; Miyake, K.; Golenbock, D.T.; Triantafilou, K. Mediators of innate immune recognition of bacteria concentrate in lipid rafts and facilitate lipopolysaccharide-induced cell activation. J. Cell Sci. 2002, 115, 2603-2611.
120. Jackson, S.K.; Abate, W.; Tonks, A.J. Lysophospholipid acyltransferases: Novel potential regulators of the inflammatory response and target for drug discovery. Pharmacol. Ther. 2008, 119, 104-114.
121. Schmid, B.; Finnen, M.J.; Harwood, J.L.; Jackson, S.K. Acylation of lysophosphatidylcholine plays a key role in the response of monocytes to lipopolysaccharide. Eur. J. Biochem. 2003, 270, 2728-2788.
122. Neville, N.T.; Parton, J.; Harwood, J.L.; Jackson, S.K. The activity of monocyte lysophosphatidylcholine acyltransferase and coenzyme A-independent transacylase is changed by the inflammatory cytokines tumour necrosis factor alpha and interferon gamma. Biochim. Biophys. Acta 2005, 1733, 232-238.
123. Jackson, S.K.; Parton, J. Lysophospholipid acyltransferases in monocyte inflammatory responses and sepsis. Immunobiol. 2004, 209, 31-38.
124. Jackson, S.K.; Abate, W.; Oarton, J.; Jones, S.; Harwood, J.L. Lysophospholipid metabolism facilitates Toll-like receptor 4 membrane translocation to regulate the inflammatory response. J. Leukoc. Biol. 2008, 84, 86-92.
125. Neilsen, P.M.; Noll, J.E.; Mattiske, S.; Bracken, C.P.; Gregory, P.A.; Schulz, R.B.; Lim, S.P.; Kumar, R.; Suetani, R.J.; Goodall, G.J.; et al. Mutant p53 drives invasion in breast tumours through up-regulation of miR-155. Oncogene 2013, 32, 2992-3000.
126. Jing, W.; Zhang, X.; Sun, W.; Hou, X.; Yao, Z.; Zhu, Y. CRIPR/CAS9-mediated genome editing of miRNA-155 inhibits proinflammatory cytokine production by RAW264.7 cells. BioMed. Res. Int. 2015, 2015, e326042.
127. Bala, S.; Marcos, M.; Kodys, K.; Csak, T.; Catalano, D.; Mandrekar, P.; Szabo, G. Up-regulation of microRNA-155 in macrophages contributes to increased tumour necrosis factor a (TNFα) production via increased Mrna half-life in alcoholic liver disease. J. Biol. Chem. 2011, 286, 1436-1444.
128. Jablonski, K.A.; Gaudet, A.D.; Amici, S.A.; Popovich, P.G.; Guerau-de-Arellano, M. Control of the inflammatory macrophage transcriptional signature by miR-155. PLoS ONE 2016, 11, e0159724.
129. Quinn, E.M.; Wang, J.H.; O’Callaghan, G.; Redmond, H.P. MicroRNA-146a is upregulated by and negatively regulates TLR2 signaling. PLoS ONE 2013, 8, e62232.
130. Kreuzer-Redmer, S.; Bekurtz, J.C.; Arends, D.; Bortfeldt, R.; Kutz-Lohroff, B.; Sharbati, S.; Einspanier, R.; Brockmann, G.A. Feeding of Enterococcus faecium NCIMB 10415 leads to intestinal miRNA-423-5p-induced regulation of immune-relevent genes. Appl. Environ. Microbiol. 2016, 82, 2263-2269.
131. Biswas, S.K.; Lopez-Collazo, E. Endotoxin tolerance: New mechanisms, molecules and clinical significance. Trends Immunol. 2009, 30, 475-487.
132. Round, J.L.; O’Connell, R.M.; Mazmanian, S.K. Coordination of tolerogenic immune responses by commensal microbiota. J. Autoimmun. 2010, 34, J220-J225.
133. Kitazawa, H.; Ishii, Y.; Uemura, J.; Kawai, Y.; Saito, T.; Kaneko, T.; Noda, K.; Itoh, T. Augmentation of macrophage functions by an extracellular phosphopolysaccharide from Lactobacillus delbrueckii ssp. Bulgaricus. Food Microbiol. 2000, 17, 109-118.
134. Yan, F.; Cao, H.; Cover, T.L.; Whitehead, R.; Washington, M.K.; Polk, D.B. Soluble proteins produced by probiotic bacteria regulate intestinal epithelial cell survival and growth. Gastroenterology 2007, 132, 562-575.
135. Petrof, E.O.; Claud, E.C.; Sun, J.; Abramova, T.; Guo, Y.; Waypa, T.S.; He, S-M.; Nakagawa, Y.; Chang, E.B. Bacteria-free solution derived from Lactobacillus plantarum inhibits multiple NF-kappaB pathways and inhibits proteasome function. Inflamm. Bowel Dis. 2009, 15, 1537-1547.
136. Frick, J.-S.; Schenk, K.; Quitadamo, M.; Kahl, F.; Koberle, M.; Bohn, E.; Aepfelbacher, M.; Autenrieth, I.B. Lactobacillus fermentum attenuates the proinflammatory effect of Yersinia enterocolitica on human epithelial cells. Inflamm. Bowel Dis. 2007, 13, 83-90.
137. Sanchez, B.; Schmitter, J.-M.; Urdaci, M.C. Identification of novel proteins secreted by Lactobacillus rhamnosus GG grown in de Mann-Rogosa-Sharpe broth. Lett. Appl. Microbiol. 2009, 48, 618-622.
138. Seth, A.; Yan, F.; Polk, D.B.; Rao, R.K. Probiotics ameliorate the hydrogen-peroxide-induced epithelial barrier disruption by a PKC- and MAP kinase-dependent mechanism. Am. J. Physiol. Gastrointest. Liver Physiol. 2008, 294, G1060-G1069.
139. Li, Y.; Qu, X.; Yang, H.; Kang, H.; Xu, Y.; Bai, B.; Song, W. Bifidobacteria DNA induces murine macrophage activation in vitro. Cell Mol. Immunol. 2005, 2, 473-478.
140. Lurhs, H.; Gerke, T.; Muller, J.G.; Melcher, R.; Schauber, F.; Boxberger, F.; Scheppach, W.; Menzel, T. Butyrate inhibits NF-Kb activation in lamina propria macrophages of patients with ulcerative colitis. Scand. J. Gastroenterol. 2002, 27, 458-466.
141. Leung, C.H.; Lam, W.; Ma, D.L.; Gullen, E.A.; Cheng, Y.C. Butyrate mediates nucleotide-binding and oligomerisation domain (NOD) 2-dependent mucosal immune responses against peptidoglycan. Eur. J. Immunol. 2009, 39, 3529-3537.
142. Rautava, S.; Kalliomäki, M.; Isolauri, E. Probiotics during pregnancy and breast-feeding might confer immunomodulatory protection against atopic disease in the infant. J. Allergy Clin. Immunol. 2002, 109, 119-121.
143. Deshpande, G.; Rao, S.; Patole, S.; Bulsara, M. Updated meta-analysis of probiotics for preventing necrotizing enterocolitis in preterm neonates. Pediatrics 2010, 125, 921-930.
144. Tursi, A.; Brandimarte, G.; Papa, A.; Giglio, A.; Elisei, W.; Giorgetti, G.M.; Forti, G.; Morini, S.; Hassan, C.; Pistoia, M.A.; et al. Treatment of relapsing mild-to-moderate ulcerative colitis with the probiotic VSL#3 as adjunctive to a standard pharmaceutical treatment: A double-blind, randomized, placebo-controlled study. Am. J. Gastroenterol. 2010, 105, 2218-2227.