Tolerogenic probiotics: potential immunoregulators in Systemic Lupus Erythematosus

Journal of Cellular Physiology

Volumn 232, Issue 8, 2017, Pages 1994-2007

  Esmaeili, Seyed Alireza ^a,b   Mahmoudi, Mahmoud ^a   Momtazi, Amir Abbas ^c   Sahebkar, Amirhossein ^b   Doulabi, Hassan ^a,b   Rastin, Maryam ^a  

^a MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^b MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

^c MASHHAD UNIVERSITY OF MEDICAL SCIENCES   (Iran)

Author keywords

autoimmune disease; bifidobacteria; lactobacillus; probiotic; systemic lupus erythematosus

Indexed keywords

GAMMA INTERFERON; INTERLEUKIN 17; INTERLEUKIN 23; INTERLEUKIN 6; PROBIOTIC AGENT; CYTOKINE;

AUTOIMMUNE DISEASE; BACTERIAL STRUCTURES; CLINICAL OUTCOME; EX VIVO STUDY; HOST; HUMAN; IMMUNOPATHOLOGY; IMMUNOREGULATION; IMMUNOSTIMULATION; IN VIVO STUDY; LYMPHOCYTE DIFFERENTIATION; MICROFLORA; NONHUMAN; PRIORITY JOURNAL; REGULATORY T LYMPHOCYTE; REVIEW; SIGNAL TRANSDUCTION; SUPPLEMENTATION; SYSTEMIC LUPUS ERYTHEMATOSUS; ANIMAL; AUTOIMMUNITY; BACTERIUM; GASTROINTESTINAL TRACT; HOST PATHOGEN INTERACTION; IMMUNOLOGICAL TOLERANCE; IMMUNOLOGY; INTESTINE FLORA; LUPUS ERYTHEMATOSUS, SYSTEMIC; MICROBIOLOGY;

ANIMALS; AUTOIMMUNITY; BACTERIA; CYTOKINES; GASTROINTESTINAL MICROBIOME; GASTROINTESTINAL TRACT; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNE TOLERANCE; LUPUS ERYTHEMATOSUS, SYSTEMIC; PROBIOTICS; SIGNAL TRANSDUCTION;

EID: 85014084430     PISSN: 00219541     EISSN: 10974652     Source Type: Journal    
DOI: 10.1002/jcp.25748     Document Type: Review

References (162)

1. Al-Mutairi, S., Al-Awadhi, A., Raghupathy, R., Al-Khawari, H., Sada, P., Al-Herz, A., & Rawoot, P. (2007). Lupus patients with pulmonary involvement have a pro-inflammatory cytokines profile. Rheumatology International, 27, 621–630.
2. Al-Salami, H., Mikov, M., Caccetta, R., & Golocorbin-Kon, S. (2012). Probiotics applications in autoimmune diseases. INTECH, p 325–366.
3. Alunno, A., Bartoloni, E., Bistoni, O., Nocentini, G., Ronchetti, S., Caterbi, S., … Gerli, R. (2012). Balance between regulatory T and Th17 cells in systemic lupus erythematosus: the old and the new. Clinical and Developmental Immunology, 2012, 823085.
4. Antiga, E., Del Bianco, E., Difonzo, E., Fabbri, P., & Caproni, M. (2011). Serum levels of the regulatory cytokines transforming growth factor-β and interleukin-10 are reduced in patients with discoid lupus erythematosus. Lupus, 20, 556–560.
5. Apperloo-Renkema, H., Bootsma, H., Mulder, B., Kallenberg, C., & Van Der Waaij, D. (1994). Host–microflora interaction in systemic lupus erythematosus (SLE): colonization resistance of the indigenous bacteria of the intestinal tract. Epidemiology and Infection, 112, 367–373.
6. Atarashi, K., Tanoue, T., Oshima, K., Suda, W., Nagano, Y., Nishikawa, H., … Hase, K. (2013). Treg induction by a rationally selected mixture of Clostridia strains from the human microbiota. Nature, 500, 232–236.
7. Atarashi, K., Tanoue, T., Shima, T., Imaoka, A., Kuwahara, T., Momose, Y., … Ohba, Y. (2011). Induction of colonic regulatory T cells by indigenous Clostridium species. Science, 331, 337–341.
8. Becker-Merok, A., Eilertsen, G. Ø., & Nossent, J. C. (2010). Levels of transforming growth factor-β are low in systemic lupus erythematosus patients with active disease. The Journal of Rheumatology, 37, 2039–2045.
9. Bengmark, S. (2003). Use of some pre-, pro-and synbiotics in critically ill patients. Best Practice & Research Clinical Gastroenterology, 17, 833–848.
10. Bezkorovainy, A. 2001. Probiotics: determinants of survival and growth in the gut. The American Journal of Clinical Nutrition, 73(2), 399–405.
11. Borchers, A. T., Selmi, C., Meyers, F. J., Keen, C. L., & Gershwin, M. E. (2009). Probiotics and immunity. Journal of Gastroenterology, 44, 26–46.
12. Buckner, J. H. (2010). Mechanisms of impaired regulation by CD4+ CD25+ FOXP3+ regulatory T cells in human autoimmune diseases. Nature Reviews Immunology, 10, 849–859.
13. Cash, H., Relle, M., Menke, J., Brochhausen, C., Jones, S. A., Topley, N., … Schwarting, A. (2010). Interleukin 6 (IL-6) deficiency delays lupus nephritis in MRL-Faslpr mice: The IL-6 pathway as a new therapeutic target in treatment of autoimmune kidney disease in systemic lupus erythematosus. The Journal of Rheumatology, 37, 60–70.
14. Chen, W., Jin, W., Hardegen, N., Lei, K.-j., Li, L., Marinos, N., … Wahl, S. M. (2003). Conversion of peripheral CD4+ CD25− naive T cells to CD4+ CD25+ regulatory T cells by TGF-β induction of transcription factor Foxp3. The Journal of Experimental Medicine, 198, 1875–1886.
15. Chen, X. Q., Yu, Y. C., Deng, H. H., Sun, J. Z., Dai, Z., Wu, Y. W., & Yang, M. (2010). Plasma IL-17A is increased in new-onset SLE patients and associated with disease activity. Journal of clinical immunology, 30, 221–225.
16. Chen, Y., Park, Y.-B., Patel, E., & Silverman, G. J. (2009). IgM antibodies to apoptosis-associated determinants recruit C1q and enhance dendritic cell phagocytosis of apoptotic cells. The Journal of Immunology, 182, 6031–6043.
17. Chiang, B., Sheih, Y., Wang, L., Liao, C., & Gill, H. (2000). Enhancing immunity by dietary consumption of a probiotic lactic acid bacterium(Bifidobacterium lactis HN 019): optimization and definition of cellular immune responses. European Journal of Clinical Nutrition, 54, 849–855.
18. Christensen, H. R., Larsen, C. N., Kæstel, P., Rosholm, L. B., Sternberg, C., Michaelsen, K. F., & Frøkiær, H. (2006). Immunomodulating potential of supplementation with probiotics: A dose-response study in healthy young adults. FEMS Immunology & Medical Microbiology, 47, 380–390.
19. Coombes, J. L., Siddiqui, K. R., Arancibia-Cárcamo, C. V., Hall, J., Sun, C.-M., Belkaid, Y., & Powrie, F. (2007). A functionally specialized population of mucosal CD103+ DCs induces Foxp3+ regulatory T cells via a TGF-β-and retinoic acid-dependent mechanism. The Journal of Experimental Medicine, 204, 1757–1764.
20. Crispín, J. C., Oukka, M., Bayliss, G., Cohen, R. A., Van Beek, C. A., Stillman, I. E., … Tsokos, G. C. (2008). Expanded double negative T cells in patients with systemic lupus erythematosus produce IL-17 and infiltrate the kidneys. The Journal of Immunology, 181, 8761–8766.
21. de Vrese, M., Stegelmann, A., Richter, B., Fenselau, S., Laue, C., & Schrezenmeir, J. (2001). Probiotics—compensation for lactase insufficiency. The American Journal of Clinical Nutrition, 73, 421s–429s.
22. Dolpady, J., Sorini, C., Di Pietro, C., Cosorich, I., Ferrarese, R., Saita, D., … Falcone, M. (2015). Oral Probiotic VSL# 3 prevents autoimmune diabetes by modulating microbiota and promoting indoleamine 2, 3-dioxygenase-enriched tolerogenic intestinal environment. Journal of Diabetes Research, 2016, 12.
23. Dong, H., Rowland, I., Tuohy, K., Thomas, L., & Yaqoob, P. (2010). Selective effects of Lactobacillus casei Shirota on T cell activation, natural killer cell activity and cytokine production. Clinical & Experimental Immunology, 161, 378–388.
24. Donkor, O. N., Ravikumar, M., Proudfoot, O., Day, S., Apostolopoulos, V., Paukovics, G., … Gill, H. (2012). Cytokine profile and induction of T helper type 17 and regulatory T cells by human peripheral mononuclear cells after microbial exposure. Clinical & Experimental Immunology, 167, 282–295.
25. Doreau, A., Belot, A., Bastid, J., Riche, B., Trescol-Biemont, M.-C., Ranchin, B., … Trolliet, P. (2009). Interleukin 17 acts in synergy with B cell-activating factor to influence B cell biology and the pathophysiology of systemic lupus erythematosus. Nature Immunology, 10, 778–785.
26. Edgerton, C., Crispín, J. C., Moratz, C. M., Bettelli, E., Oukka, M., Simovic, M., … Dalle Lucca, J. J. (2009). IL-17 producing CD4+ T cells mediate accelerated ischemia/reperfusion-induced injury in autoimmunity-prone mice. Clinical Immunology, 130, 313–321.
27. Eilertsen, G., Nikolaisen, C., Becker-Merok, A., & Nossent, J. (2011). Interleukin-6 promotes arthritis and joint deformation in patients with systemic lupus erythematosus. Lupus, 20, 607–613.
28. 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:gut, 2010, 232918.
29. Ferstl, R., Frei, R., Schiavi, E., Konieczna, P., Barcik, W., Ziegler, M., … Akdis, C. A. (2014). Histamine receptor 2 is a key influence in immune responses to intestinal histamine-secreting microbes. Journal of Allergy and Clinical Immunology, 134, 744.
30. Finck, B. K., Chan, B., & Wofsy, D. (1994). Interleukin 6 promotes murine lupus in NZB/NZW F1 mice. Journal of Clinical Investigation, 94, 585.
31. Fink, L. N., Zeuthen, L. H., Christensen, H. R., Morandi, B., Frøkiær, H., & Ferlazzo, G. (2007). Distinct gut-derived lactic acid bacteria elicit divergent dendritic cell-mediated NK cell responses. International Immunology, 19, 1319–1327.
32. Frank, D. N., Amand, A. L. S., Feldman, R. A., Boedeker, E. C., Harpaz, N., & Pace, N. R. (2007). Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proceedings of the National Academy of Sciences, 104, 13780–13785.
33. Frei, R., Ferstl, R., Konieczna, P., Ziegler, M., Simon, T., Rugeles, T. M., … Akdis, C. A. (2013). Histamine receptor 2 modifies dendritic cell responses to microbial ligands. Journal of Allergy and Clinical Immunology, 132, 194–204. e112.
34. Friedrich, U., Vogelsang, H., Bauer, A., Kaatz, M., Hipler, U., Schmidt, I., & Jahreis, G. (2008). The immune system in healthy adults and patients with atopic dermatitis seems to be affected differently by a probiotic intervention. Clinical & Experimental Allergy, 38, 93–102.
35. Furrie, E., Macfarlane, S., Kennedy, A., Cummings, J., Walsh, S., O'neil, D., & Macfarlane, G. (2005). Synbiotic therapy (Bifidobacterium longum/Synergy 1) initiates resolution of inflammation in patients with active ulcerative colitis: A randomised controlled pilot trial. Gut, 54, 242–249.
36. Gaboriau-Routhiau, V., Rakotobe, S., Lécuyer, E., Mulder, I., Lan, A., Bridonneau, C., … Brandi, G. (2009). The key role of segmented filamentous bacteria in the coordinated maturation of gut helper T cell responses. Immunity, 31, 677–689.
37. Garrett, W. S., Gallini, C. A., Yatsunenko, T., Michaud, M., DuBois, A., Delaney, M. L., … Glickman, J. N. (2010). Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host & Microbe, 8, 292–300.
38. Ghadimi, D., Helwig, U., Schrezenmeir, J., Heller, K. J., & de Vrese, M. (2012). Epigenetic imprinting by commensal probiotics inhibits the IL-23/IL-17 axis in an in vitro model of the intestinal mucosal immune system. Journal of Leukocyte Biology, 92, 895–911.
39. Ghoryani, M., Sahebari, M., Mahmoudi, M., Abdollahi, N., Reihani, H., Rabe, S. Z. T., … Rastin, M. (2016). Immunomodulatory Vitamin D effects on regulatory T-cells and cytokines in an in vitro study on patients with systemic lupus erythematosus. Food and Agricultural Immunology, 27, 377–387.
40. Gill, H., Rutherfurd, K., & Cross, M. (2001a). Dietary probiotic supplementation enhances natural killer cell activity in the elderly: An investigation of age-related immunological changes. Journal of Clinical Immunology, 21, 264–271.
41. Gill, H. S. (2003). Probiotics to enhance anti-infective defences in the gastrointestinal tract. Best Practice & Research Clinical Gastroenterology, 17, 755–773.
42. Gill, H. S., Rutherfurd, K. J., Cross, M. L., & Gopal, P. K. (2001b). Enhancement of immunity in the elderly by dietary supplementation with the probiotic Bifidobacterium lactis HN019. The American Journal of Clinical Nutrition, 74, 833–839.
43. Gionchetti, P., Amadini, C., Rizzello, F., Venturi, A., Poggioli, G., & Campieri, M. (2003). Probiotics for the treatment of postoperative complications following intestinal surgery. Best Practice & Research Clinical Gastroenterology, 17, 821–831.
44. Gómez, J., Prado, C., López, P., Suárez, A., & Gutiérrez, C. (2009). Conserved anti-proliferative effect and poor inhibition of TNFα secretion by regulatory CD4+ CD25+ T cells in patients with systemic lupus erythematosus. Clinical Immunology, 132, 385–392.
45. Gorelik, L., Constant, S., & Flavell, R. A. (2002). Mechanism of transforming growth factor β-induced inhibition of T helper type 1 differentiation. The Journal of Experimental Medicine, 195, 1499–1505.
46. Grangette, C., Nutten, S., Palumbo, E., Morath, S., Hermann, C., Dewulf, J., … Mercenier, A. (2005). Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proceedings of the National Academy of Sciences of the United States of America, 102, 10321–10326.
47. Gröndal, G., Gunnarsson, I., Rönnelid, J., Rogberg, S., Klareskog, L., & Lundberg, I. (1999). Cytokine production, serum levels and disease activity in systemic lupus erythematosus. Clinical and Experimental Rheumatology, 18, 565–570.
48. Grönwall, C., Chen, Y., Vas, J., Khanna, S., Thiel, S., Corr, M., Kono, D. H., & Silverman, G. J. (2012). MAPK phosphatase-1 is required for regulatory natural autoantibody-mediated inhibition of TLR responses. Proceedings of the National Academy of Sciences, 109, 19745–19750.
49. Grönwall, C., & Silverman, G. J. (2014). Natural IgM: beneficial autoantibodies for the control of inflammatory and autoimmune disease. Journal of Clinical Immunology, 34, 12–21.
50. Guo, H., Leung, J. C., Chan, L. Y., Lui, S., Tsang, A. W., & Lai, K. (2005). Modulation of intra-pulmonary TGF-b expression by mycophenolate mofetil in lupus prone MRL/lpr mice. Lupus, 14, 583–592.
51. Haller, D., Serrant, P., Granato, D., Schiffrin, E., & Blum, S. (2002). Activation of human NK cells by staphylococci and lactobacilli requires cell contact-dependent costimulation by autologous monocytes. Clinical and Diagnostic Laboratory Immunology, 9, 649–657.
52. Hammad, A., Youssef, H., & El-Arman, M. (2006). Transforming growth factor beta 1 in children with systemic lupus erythematosus: A possible relation with clinical presentation of lupus nephritis. Lupus, 15, 608–612.
53. Hardy, H., Harris, J., Lyon, E., Beal, J., & Foey, A. D. (2013). Probiotics, prebiotics and immunomodulation of gut mucosal defences: Homeostasis and immunopathology. Nutrients, 5, 1869–1912.
54. Harigai, M., Kawamoto, M., Hara, M., Kubota, T., Kamatani, N., & Miyasaka, N. (2008). Excessive production of IFN-γ in patients with systemic lupus erythematosus and its contribution to induction of B lymphocyte stimulator/B cell-activating factor/TNF ligand superfamily-13B. The Journal of Immunology, 181, 2211–2219.
55. Heath, V. L., Murphy, E. E., Crain, C., Tomlinson, M. G., & O'Garra, A. (2000). TGF-β1 down-regulates Th2 development and results in decreased IL-4-induced STAT6 activation and GATA-3 expression. European Journal of Immunology, 30, 2639–2649.
56. Helwig, U., Lammers, K. M., Rizzello, F., Brigidi, P., Rohleder, V., Caramelli, E., … Campieri, M. (2006). Lactobacilli, bifidobacteria and E. coli nissle induce pro- and anti-inflammatory cytokines in peripheral blood mononuclear cells. World Journal of Gastroenterology, 12, 5978–5986.
57. Herrera-Esparza, R., Barbosa-Cisneros, O., Villalobos-Hurtado, R., & Avalos-Diaz, E. (1998). Renal expression of IL-6 and TNFα genes in lupus nephritis. Lupus, 7, 154–158.
58. Hevia, A., Milani, C., López, P., Cuervo, A., Arboleya, S., Duranti, S., … Gueimonde, M. (2014). Intestinal dysbiosis associated with systemic lupus erythematosus. MBio, 5, e01548–e01514.
59. Hirohata, S., Kanai, Y., Mitsuo, A., Tokano, Y., & Hashimoto, H. (2009). Accuracy of cerebrospinal fluid IL-6 testing for diagnosis of lupus psychosis. A multicenter retrospective study. Clinical Rheumatology, 28, 1319–1323.
60. Holler, E., Landfried, K., Meier, J., Hausmann, M., & Rogler, G. (2010). The role of bacteria and pattern recognition receptors in GVHD. International Journal of Inflammation, 2010, 6.
61. Hooper, L. V., Midtvedt, T., & Gordon, J. I. (2002). How host-microbial interactions shape the nutrient environment of the mammalian intestine. Annual Review of Nutrition, 22, 283–307.
62. Iliev, I., Tohno, M., Kurosaki, D., Shimosato, T., He, F., Hosoda, M., … Kitazawa, H. (2008). Immunostimulatory oligodeoxynucleotide containing TTTCGTTT motif from lactobacillus rhamnosus GG DNA potentially suppresses OVA-specific IgE production in mice. Scandinavian Journal of Immunology, 67, 370–376.
63. Ivanov, I. I., de Llanos Frutos, R., Manel, N., Yoshinaga, K., Rifkin, D. B., Sartor, R. B., … Littman, D. R. (2008). Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine. Cell Host & Microbe, 4, 337–349.
64. Jarvenpaa, S., Kautiainen, H., Julkunen, I., Vapaatalo, H., & Korpela, R. (2008). Probiotic intervention has strain-specific anti-inflammatory effects in healthy adults. World Journal of Gastroenterology, 14, 13.
65. Jeon, S. G., Kayama, H., Ueda, Y., Takahashi, T., Asahara, T., Tsuji, H., … Kusu, T. (2012). Probiotic Bifidobacterium breve induces IL-10-producing Tr1 cells in the colon. PLoS Pathog, 8, e1002714.
66. Jijon, H., Backer, J., Diaz, H., Yeung, H., Thiel, D., McKaigney, C., De Simone, C., & Madsen, K. (2004). DNA from probiotic bacteria modulates murine and human epithelial and immune function. Gastroenterology, 126, 1358–1373.
67. Joffre, O., Nolte, M. A., & Spörri, R. (2009). Inflammatory signals in dendritic cell activation and the induction of adaptive immunity. Immunological Reviews, 227, 234–247.
68. Josefowicz, S. Z., Lu, L.-F., & Rudensky, A. Y. (2012). Regulatory T cells: Mechanisms of differentiation and function. Annual Review of Immunology, 30, 531–564.
69. Kaliński, P., Hilkens, C. M., Wierenga, E. A., & Kapsenberg, M. L. (1999). T-cell priming by type-1and type-2 polarized dendritic cells: The concept of a third signal. Immunology Today, 20, 561–567.
70. Kalliomäki, M., Salminen, S., Arvilommi, H., Kero, P., Koskinen, P., & Isolauri, E. (2001). Probiotics in primary prevention of atopic disease: A randomised placebo-controlled trial. The Lancet, 357, 1076–1079.
71. Kalliomäki, M., Salminen, S., Poussa, T., Arvilommi, H., & Isolauri, E. (2003). Probiotics and prevention of atopic disease: 4-year follow-up of a randomised placebo-controlled trial. The Lancet, 361, 1869–1871.
72. Kaplan, J., Woodworth, L., Smith, K., Coco, J., Vitsky, A., & McPherson, J. (2008). Therapeutic benefit of treatment with anti-thymocyte globulin and latent TGF-β1 in the MRL/lpr lupus mouse model. Lupus, 17, 822–831.
73. Khan, M. W., Zadeh, M., Bere, P., Gounaris, E., Owen, J., Klaenhammer, T., & Mohamadzadeh, M. (2012). Modulating intestinal immune responses by lipoteichoic acid-deficient Lactobacillus acidophilus. Immunotherapy, 4(2), 151–161.
74. Kikly, K., Liu, L., Na, S., & Sedgwick, J. D. (2006). The IL-23/Th 17 axis: Therapeutic targets for autoimmune inflammation. Current Opinion in Immunology, 18, 670–675.
75. Kitani, A., Hara, M., Hirose, T., Harigai, M., Suzuki, K., Kawakami, M., … Nakamura, H. (1992). Autostimulatory effects of IL-6 on excessive B cell differentiation in patients with systemic lupus erythematosus: Analysis of IL-6 production and IL-6R expression. Clinical & Experimental Immunology, 88, 75–83.
76. Klein, A., Friedrich, U., Vogelsang, H., & Jahreis, G. (2008). Lactobacillus acidophilus 74-2 and Bifidobacterium animalis subsp lactis DGCC 420 modulate unspecific cellular immune response in healthy adults. European Journal of Clinical Nutrition, 62, 584–593.
77. Konieczna, P., Schiavi, E., Ziegler, M., Groeger, D., Healy, S., Grant, R., & O'Mahony, L. (2015). Human dendritic cell DC-SIGN and TLR-2 mediate complementary immune regulatory activities in response to Lactobacillus rhamnosus JB-1. PLoS ONE, 10, e0120261.
78. Konstantinov, S. R., Smidt, H., de Vos, W. M., Bruijns, S. C., Singh, S. K., Valence, F., … Klaenhammer, T. R. (2008). S layer protein A of Lactobacillus acidophilus NCFM regulates immature dendritic cell and T cell functions. Proceedings of the National Academy of Sciences, 105, 19474–19479.
79. Korn, T., Bettelli, E., Oukka, M., & Kuchroo, V. K. (2009). IL-17 and th17 cells. Annual Review of Immunology, 27, 485–517.
80. Larsen, N., Vogensen, F. K., van den Berg, F. W., Nielsen, D. S., Andreasen, A. S., Pedersen, B. K., & Jakobsen, M. (2010). Gut microbiota in human adults with type 2 diabetes differs from non-diabetic adults. PLoS ONE, 5, e9085.
81. Lavasani, S., Dzhambazov, B., Nouri, M., Fåk, F., Buske, S., Molin, G., … Weström, B. (2010). A novel probiotic mixture exerts a therapeutic effect on experimental autoimmune encephalomyelitis mediated by IL-10 producing regulatory T cells. PLoS ONE, 5, e9009.
82. Lavi Arab, F., Rastin, M., Faraji, F., Zamani Taghizadeh Rabe, S., Tabasi, N., Khazaee, M., … Mahmoudi, M. (2015). Assessment of 1, 25-dihydroxyvitamin D3 effects on Treg cells in a mouse model of systemic lupus erythematosus. Immunopharmacology and Immunotoxicology, 37, 12–18.
83. Linker-Israeli, M., Deans, R., Wallace, D., Prehn, J., Ozeri-Chen, T., & Klinenberg, J. (1991). Elevated levels of endogenous IL-6 in systemic lupus erythematosus. A putative role in pathogenesis. The Journal of Immunology, 147, 117–123.
84. López, P., de Paz, B., Rodríguez-Carrio, J., Hevia, A., Sánchez, B., Margolles, A., & Suárez, A. (2016). Th17 responses and natural IgM antibodies are related to gut microbiota composition in systemic lupus erythematosus patients. Scientific Reports, 6, 24072.
85. López, P., González-Rodríguez, I., Gueimonde, M., Margolles, A., & Suárez, A. (2011). Immune response to Bifidobacterium bifidum strains support Treg/Th17 plasticity. PLoS ONE, 6, e24776.
86. López, P., González-Rodríguez, I., Sánchez, B., Ruas-Madiedo, P., Suárez, A., Margolles, A., & Gueimonde, M. (2012). Interaction of Bifidobacterium bifidum LMG13195 with HT29 cells influences regulatory-T-cell-associated chemokine receptor expression. Applied and Environmental Microbiology, 78, 2850–2857.
87. López, P., Gueimonde, M., Margolles, A., & Suárez, A. (2010). Distinct Bifidobacterium strains drive different immune responses in vitro. International Journal of Food Microbiology, 138, 157–165.
88. Lorea Baroja, M., Kirjavainen, P., Hekmat, S., & Reid, G. (2007). Anti-inflammatory effects of probiotic yogurt in inflammatory bowel disease patients. Clinical & Experimental Immunology, 149, 470–479.
89. Lyssuk, E. Y., Torgashina, A. V., Soloviev, S. K., Nassonov, E. L., & Bykovskaia, S. N. (2007). Reduced number and function of CD4+ CD25 high FoxP3+ regulatory T cells in patients with systemic lupus erythematosus. Immune-Mediated Diseases: Springer, p113–p119.
90. Ma, J., Yu, J., Tao, X., Cai, L., Wang, J., & Zheng, S. G. (2010). The imbalance between regulatory and IL-17-secreting CD4+ T cells in lupus patients. Clinical Rheumatology, 29, 1251–1258.
91. Manicassamy, S., Ravindran, R., Deng, J., Oluoch, H., Denning, T. L., Kasturi, S. P., … Pulendran, B. (2009). Toll-like receptor 2?dependent induction of vitamin A–metabolizing enzymes in dendritic cells promotes T regulatory responses and inhibits autoimmunity. Nature Medicine, 15, 401–409.
92. Markle, J. G., Frank, D. N., Mortin-Toth, S., Robertson, C. E., Feazel, L. M., Rolle-Kampczyk, U., … Danska, J. S. (2013). Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science, 339, 1084–1088.
93. Mason, D., & Powrie, F. (1998). Control of immune pathology by regulatory T cells. Current Opinion in Immunology, 10, 649–655.
94. 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, 259–266.
95. Mazmanian, S. K., Round, J. L., & Kasper, D. L. (2008). A microbial symbiosis factor prevents intestinal inflammatory disease. Nature, 453, 620–625.
96. McKenzie, B. S., Kastelein, R. A., & Cua, D. J. (2006). Understanding the IL-23-IL-17 immune pathway. Trends in Immunology, 27, 17–23.
97. Medina, M., Izquierdo, E., Ennahar, S., & Sanz, Y. (2007). Differential immunomodulatory properties of Bifidobacterium logum strains: Relevance to probiotic selection and clinical applications. Clinical & Experimental Immunology, 150, 531–538.
98. Meijerink, M., Van Hemert, S., Taverne, N., Wels, M., De Vos, P., Bron, P. A., … 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, e10632.
99. Miettinen, M., Matikainen, S., Vuopio-Varkila, J., Pirhonen, J., Varkila, K., Kurimoto, M., & Julkunen, I. (1998). Lactobacilli and streptococci induce interleukin-12 (IL-12), IL-18, and gamma interferon production in human peripheral blood mononuclear cells. Infection and Immunity, 66, 6058–6062.
100. Mihara, M., Takagi, N., Takeda, Y., & Ohsugi, Y. (1998). IL-6 receptor blockage inhibits the onset of autoimmune kidney disease in NZB/W F1 mice. Clinical and Experimental Immunology, 112, 397–402.
101. Mike, A., Nagaoka, N., Tagami, Y., Miyashita, M., Shimada, S., Uchida, K., Nanno, M., & Ohwaki, M. (1999). Prevention of B220^+ T cell expansion and prolongation of lifespan induced by Lactobacillus casei in MRL/lpr mice. Clinical and Experimental Immunology, 117, 368–375.
102. Morimoto, K., Takeshita, T., Nanno, M., Tokudome, S., & Nakayama, K. (2005). Modulation of natural killer cell activity by supplementation of fermented milk containing Lactobacillus casei in habitual smokers. Preventive Medicine, 40, 589–594.
103. Nagao, F., Nakayama, M., Muto, T., & Okumura, K. (2000). Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the immune system in healthy human subjects. Bioscience, Biotechnology, and Biochemistry, 64, 2706–2708.
104. Naka, T., Nishimoto, N., & Kishimoto, T. (2002). The paradigm of IL-6: from basic science to medicine. Arthritis Research & Therapy, 4, 1.
105. O'Mahony, L., McCarthy, J., Kelly, P., Hurley, G., Luo, F., Chen, K., … Shanahan, F. (2005). Lactobacillus and bifidobacterium in irritable bowel syndrome: Symptom responses and relationship to cytokine profiles. Gastroenterology, 128, 541–551.
106. Ouwehand, A. C., Salminen, S., & Isolauri, E. (2002). Probiotics: An overview of beneficial effects. Antonie Van Leeuwenhoek, 82, 279–289.
107. Pan, H.-F., Leng, R.-X., Feng, C.-C., Li, X.-P., Chen, G.-M., Li, B.-Z., … Ye, D.-Q. (2013). Expression profiles of Th17 pathway related genes in human systemic lupus erythematosus. Molecular Biology Reports, 40, 391–399.
108. Paolillo, R., Carratelli, C. R., Sorrentino, S., Mazzola, N., & Rizzo, A. (2009). Immunomodulatory effects of Lactobacillus plantarum on human colon cancer cells. International Immunopharmacology, 9, 1265–1271.
109. Parra, M., de Morentin, B. M., Cobo, J., Mateos, A., & Martinez, J. (2004). Daily ingestion of fermented milk containing Lactobacillus casei DN114001 improves innate defense capacity in healthy middle-aged people. Journal of Physiology and Biochemistry, 60, 85–91.
110. Petersen, E. R., Claesson, M. H., Schmidt, E. G. W., Jensen, S. S., Ravn, P., Olsen, J., & Kristensen, N. N. (2012). Consumption of probiotics increases the effect of regulatory T cells in transfer colitis. Inflammatory Bowel Diseases, 18, 131–142.
111. Pronio, A., Montesani, C., Butteroni, C., Vecchione, S., Mumolo, G., Vestri, A., & Boirivant, M. (2008). Probiotic administration in patients with ileal pouch-anal anastomosis for ulcerative colitis is associated with expansion of mucosal regulatory cells. Inflammatory Bowel Diseases, 14, 662–668.
112. Qu, N., Xu, M., Mizoguchi, I., Furusawa, J.-i., Kaneko, K., Watanabe, K., & Yoshimoto, T. (2013). Pivotal roles of T-helper 17-related cytokines, IL-17, IL-22, and IL-23, in inflammatory diseases. Clinical and Developmental Immunology, 2013, 13.
113. Rachmilewitz, D., Katakura, K., Karmeli, F., Hayashi, T., Reinus, C., Rudensky, B., & Takabayashi, K. (2004). Toll-like receptor 9 signaling mediates the anti-inflammatory effects of probiotics in murine experimental colitis. Gastroenterology, 126, 520–528.
114. Rahman, A., & Isenberg, D. A. (2008). Systemic lupus erythematosus. New England Journal of Medicine, 358, 929–939.
115. Rastin, M., Mahmoudi, M., Hatef, M., Sahebari, M., Tabasi, N., Haghmorad, D., & Zamani, S. (2013). T lymphocyte apoptosis in systemic lupus erythematosus patients. Iranian Journal of Basic Medical Sciences, 16, 936–941.
116. Re, F., & Strominger, J. L. (2004). IL-10 released by concomitant TLR2 stimulation blocks the induction of a subset of Th1 cytokines that are specifically induced by TLR4 or TLR3 in human dendritic cells. The Journal of Immunology, 173, 7548–7555.
117. Rescigno, M., Urbano, M., Valzasina, B., Francolini, M., Rotta, G., Bonasio, R., … Ricciardi-Castagnoli, P. (2001). Dendritic cells express tight junction proteins and penetrate gut epithelial monolayers to sample bacteria. Nature immunology, 2, 361–367.
118. Riol-Blanco, L., Lazarevic, V., Awasthi, A., Mitsdoerffer, M., Wilson, B. S., Croxford, A., … Oukka, M. (2010). IL-23 receptor regulates unconventional IL-17-Producing t cells that control bacterial infections. The Journal of Immunology, 184, 1710–1720.
119. Ripley, B., Goncalves, B., Isenberg, D., Latchman, D., & Rahman, A. (2005). Raised levels of interleukin 6 in systemic lupus erythematosus correlate with anaemia. Annals of the Rheumatic Diseases, 64, 849–853.
120. Round, J. L., Lee, S. M., Li, J., Tran, G., Jabri, B., Chatila, T. A., & Mazmanian, S. K. (2011). The Toll-like receptor 2 pathway establishes colonization by a commensal of the human microbiota. Science, 332, 974–977.
121. Round, J. L., & Mazmanian, S. K. (2009). The gut microbiota shapes intestinal immune responses during health and disease. Nature Reviews Immunology, 9, 313–323.
122. Rudensky, A. Y. (2011). Regulatory t cells and foxp3. Immunological reviews, 241, 260–268.
123. Ruiz, P. A., Hoffmann, M., Szcesny, S., Blaut, M., & Haller, D. (2005). Innate mechanisms for Bifidobacterium lactis to activate transient pro-inflammatory host responses in intestinal epithelial cells after the colonization of germ-free rats. Immunology, 115, 441–450.
124. Ryffel, B., Car, B., Gunn, H., Roman, D., Hiestand, P., & Mihatsch, M. (1994). Interleukin-6 exacerbates glomerulonephritis in (NZB x NZW) F1 mice. The American Journal of Pathology, 144, 927.
125. Sakaguchi, S., Miyara, M., Costantino, C. M., & Hafler, D. A. (2010). FOXP3+ regulatory T cells in the human immune system. Nature Reviews Immunology, 10, 490–500.
126. Sashihara, T., Sueki, N., & Ikegami, S. (2006). An analysis of the effectiveness of heat-killed lactic acid bacteria in alleviating allergic diseases. Journal of Dairy Science, 89, 2846–2855.
127. Saxena, V., Lienesch, D. W., Zhou, M., Bommireddy, R., Azhar, M., Doetschman, T., & Singh, R. R. (2008). Dual roles of immunoregulatory cytokine TGF-β in the pathogenesis of autoimmunity-mediated organ damage. The Journal of Immunology, 180, 1903–1912.
128. Schultz, M., Linde, H.-J., Lehn, N., Zimmermann, K., Grossmann, J., Falk, W., & Schölmerich, J. (2003). Immunomodulatory consequences of oral administration of Lactobacillus rhamnosus strain GG in healthy volunteers. Journal of Dairy Research, 70, 165–173.
129. Shah, K., Lee, W.-W., Lee, S.-H., Kim, S. H., Kang, S. W., Craft, J., & Kang, I. (2010). Dysregulated balance of Th17 and Th1 cells in systemic lupus erythematosus. Arthritis Research & Therapy, 12, 1.
130. Sheih, Y.-H., Chiang, B.-L., Wang, L.-H., Liao, C.-K., & Gill, H. S. (2001). Systemic immunity-enhancing effects in healthy subjects following dietary consumption of the lactic acid bacterium Lactobacillus rhamnosus HN001. Journal of the American College of Nutrition, 20, 149–156.
131. Shevach, E. M. (2009). Mechanisms of foxp3+ T regulatory cell-mediated suppression. Immunity, 30, 636–645.
132. Shida, K., Kiyoshima-Shibata, J., Nagaoka, M., Watanabe, K., & Nanno, M. (2006). Induction of interleukin-12 by Lactobacillus strains having a rigid cell wall resistant to intracellular digestion. Journal of Dairy Science, 89, 3306–3317.
133. Shida, K., Nanno, M., & Nagata, S. (2011). Flexible cytokine production by macrophages and T cells in response to probiotic bacteria: A possible mechanism by which probiotics exert multifunctional immune regulatory activities. Gut Microbes, 2, 109–114.
134. Smits, H. H., Engering, A., van der Kleij, D., de Jong, E. C., Schipper, K., van Capel, T. M., … van Kooyk, Y. (2005). Selective probiotic bacteria induce IL-10–producing regulatory T cells in vitro by modulating dendritic cell function through dendritic cell–specific intercellular adhesion molecule 3–grabbing nonintegrin. Journal of Allergy and Clinical Immunology, 115, 1260–1267.
135. Spanhaak, S., Havenaar, R., & Schaafsma, G. (1998). The effect of consumption of milk fermented by Lactobacillus casei strain Shirota on the intestinal microflora and immune parameters in humans. European Journal of Clinical Nutrition, 52, 899–907.
136. Su, D.-L., Lu, Z.-M., Shen, M.-N., Li, X., & Sun, L.-Y. (2012). Roles of pro- and anti-inflammatory cytokines in the pathogenesis of SLE. BioMed Research International, 2012, 15.
137. Suzuki, H., Yasukawa, K., Saito, T., Narazak, M., Hasegawa, A., Taga, T., & Kishimoto, T. (1993). Serum soluble interleukin-6 receptor in MRL/lpr mice is elevated with age and mediates the interleukin-6 signal. European Journal of Immunology, 23, 1078–1082.
138. Takahashi, N., Kitazawa, H., Iwabuchi, N., Xiao, J.-Z., Miyaji, K., Iwatsuki, K., & Saito, T. (2006). Oral administration of an immunostimulatory DNA sequence from Bifidobacterium longum improves Th1/Th2 balance in a murine model. Bioscience, Biotechnology, and Biochemistry, 70, 2013–2017.
139. Takeda, K., & Okumura, K. (2007). Effects of a fermented milk drink containing Lactobacillus casei strain Shirota on the human NK-cell activity. The Journal of Nutrition, 137, 791S–793S.
140. Talaat, R. M., Mohamed, S. F., Bassyouni, I. H., & Raouf, A. A. (2015). Th1/Th2/Th17/Treg cytokine imbalance in systemic lupus erythematosus (SLE) patients: Correlation with disease activity. Cytokine, 72, 146–153.
141. Tamboli, C. P., Caucheteux, C., Cortot, A., Colombel, J.-F., & Desreumaux, P. (2003). Probiotics in inflammatory bowel disease: A critical review. Best Practice & Research Clinical Gastroenterology, 17, 805–820.
142. Tsai, C.-Y., Wu, T.-H., Yu, C.-L., Lu, J.-Y., & Tsai, Y.-Y. (2000). Increased excretions of β2-microglobulin, IL-6, and IL-8 and decreased excretion of Tamm-Horsfall glycoprotein in urine of patients with active lupus nephritis. Nephron, 85, 207–214.
143. Tsokos, G. C. (2011). Systemic lupus erythematosus. New England Journal of Medicine, 365, 2110–2121.
144. Ulisse, S., Gionchetti, P., D'Alò, S., Russo, F. P., Pesce, I., Ricci, G., … Campieri, M. (2001). Expression of cytokines, inducible nitric oxide synthase, and matrix metalloproteinases in pouchitis: Effects of probiotic treatment. The American Journal of Gastroenterology, 96, 2691–2699.
145. Valencia, X., Yarboro, C., Illei, G., & Lipsky, P. E. (2007). Deficient CD4+ CD25high T regulatory cell function in patients with active systemic lupus erythematosus. The Journal of Immunology, 178, 2579–2588.
146. van der Kleij, H., O'Mahony, C., Shanahan, F., O'Mahony, L., & Bienenstock, J. (2008). Protective effects of Lactobacillus reuteri and Bifidobacterium infantis in murine models for colitis do not involve the vagus nerve. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 295, R1131–R1137.
147. Van Niel, C. W., Feudtner, C., Garrison, M. M., & Christakis, D. A. (2002). Lactobacillus therapy for acute infectious diarrhea in children: A meta-analysis. Pediatrics, 109, 678–684.
148. Viallard, J., Pellegrin, J., Ranchin, V., Schaeverbeke, T., Dehais, J., Longy-Boursier, M., … Moreau, J. (1999). Th1 (IL-2, interferon-gamma (IFN-)) and Th2 (IL-10, IL-4) cytokine production by peripheral blood mononuclear cells (PBMC) from patients with systemic lupus erythematosus (SLE). Clinical and Experimental Immunology, 115, 189–195.
149. Vinderola, G., Matar, C., & Perdigon, G. (2005). Role of intestinal epithelial cells in immune effects mediated by gram-positive probiotic bacteria: Involvement of toll-like receptors. Clinical and Diagnostic Laboratory Immunology, 12, 1075–1084.
150. Wen, L., Ley, R. E., Volchkov, P. Y., Stranges, P. B., Avanesyan, L., Stonebraker, A. C., … Bluestone, J. A. (2008). Innate immunity and intestinal microbiota in the development of Type 1 diabetes. Nature, 455, 1109–1113.
151. Wolfraim, L. A., Walz, T. M., James, Z., Fernandez, T., & Letterio, J. J. (2004). P21Cip1 and p27Kip1 act in synergy to alter the sensitivity of naive T cells to TGF-β-mediated G1 arrest through modulation of IL-2 responsiveness. The Journal of Immunology, 173, 3093–3102.
152. Xing, Q., Su, H., Cui, J., & Wang, B. (2012). Role of Treg cells and TGF-β1 in patients with systemic lupus erythematosus: A possible relation with lupus nephritis. Immunological Investigations, 41, 15–27.
153. Yan, F., Cao, H., Cover, T. L., Washington, M. K., Shi, Y., Liu, L., … Polk, D. B. (2011). Colon-specific delivery of a probiotic-derived soluble protein ameliorates intestinal inflammation in mice through an EGFR-dependent mechanism. The Journal of Clinical Investigation, 121, 2242–2253.
154. 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 survival and growth. Gastroenterology, 132, 562–575.
155. Yan, F., & Polk, D. B. (2002). Probiotic bacterium prevents cytokine-induced apoptosis in intestinal epithelial cells. Journal of Biological Chemistry, 277, 50959–50965.
156. Yeoh, N., Burton, J. P., Suppiah, P., Reid, G., & Stebbings, S. (2013). The role of the microbiome in rheumatic diseases. Current Rheumatology Reports, 15, 1–11.
157. Yoshimura, A., Wakabayashi, Y., & Mori, T. (2010). Cellular and molecular basis for the regulation of inflammation by TGF-β. Journal of Biochemistry, 147, 781–792.
158. Yurkovetskiy, L., Burrows, M., Khan, A. A., Graham, L., Volchkov, P., Becker, L., & Chervonsky, A. V. (2013). Gender bias in autoimmunity is influenced by microbiota. Immunity, 39, 400–412.
159. Zeuthen, L. H., Fink, L. N., & Frøkiær, H. (2008). 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, 124, 489–502.
160. Zhang, W., & Reichlin, M. (2008). A possible link between infection with Burkholderia bacteria and systemic lupus erythematosus based on epitope mimicry. Clinical and Developmental Immunology, 2008, 7.
161. Zheng, B., van Bergenhenegouwen, J., Overbeek, S., van de Kant, H. J., Garssen, J., Folkerts, G., & Kraneveld, A. D. (2014). Bifidobacterium breve attenuates murine dextran sodium sulfate-induced colitis and increases regulatory T cell responses. PLoS ONE, 9, e95441.
162. Zhu, J., & Paul, W. E. (2008). CD4 T cells: Fates, functions, and faults. Blood, 112, 1557–1569.