Feeding lactobacilli impacts lupus progression in (NZBxNZW)F1 lupus-prone mice by enhancing immunoregulation

References

• Perl A. Pathogenic mechanisms in systemic lupus erythematosus. Autoimmunity. 2010;43(1):1–6.
   PubMed Web of Science ®Google Scholar
• Foster MH. Relevance of systemic lupus erythematosus nephritis animal models to human disease. Seminars Nephrol. 1999;19(1):12–24.
   PubMed Web of Science ®Google Scholar
• Ando DG , Sercarz EE , Hahn BH. Mechanisms of T and B cell collaboration in the in vitro production of anti-DNA antibodies in the NZB/NZW F1 murine SLE model. J Immunol. 1987;138(10):3185–3190.
   PubMed Web of Science ®Google Scholar
• Busser BW , Cancro MP , Laufer TM. An increased frequency of autoantibody-inducing CD4+ T cells in pre-diseased lupus-prone mice. Int Immunol. 2004;16(7):1001–1007.
   PubMed Web of Science ®Google Scholar
• Crispin JC , Martı́nez A , Alcocer-Varela J. Quantification of regulatory T cells in patients with systemic lupus erythematosus. J Autoimmunity. 2003;21(3):273–276.
   PubMed Web of Science ®Google Scholar
• Tucker CF , Nebane-Ambe DL , Chhabra A , et al. Decreased frequencies of CD4 + CD25 + Foxp3+ cells and the potent CD103+ subset in peripheral lymph nodes correlate with autoimmune disease predisposition in some strains of mice. Autoimmunity. 2011;44(6):453–464.
   PubMed Web of Science ®Google Scholar
• Wan S , Xia C , Morel L. IL-6 produced by dendritic cells from lupus-prone mice inhibits CD4 + CD25+ T cell regulatory functions. J Immunol. 2007;178(1):271–279.
   PubMed Web of Science ®Google Scholar
• Wu HY , Staines NA. A deficiency of CD4 + CD25+ T cells permits the development of spontaneous lupus-like disease in mice, and can be reversed by induction of mucosal tolerance to histone peptide autoantigen. Lupus. 2004;13(3):192–200.
   PubMed Web of Science ®Google Scholar
• Hill C , Guarner F , Reid G , et al. Expert consensus document. The international scientific association for probiotics and prebiotics consensus statement on the scope and appropriate use of the term probiotic. Nat Rev Gastroenterol Hepatol. 2014;11(8):506–514.
   PubMed Web of Science ®Google Scholar
• Di Cerbo A , Palmieri B , Aponte M , et al. Mechanisms and therapeutic effectiveness of lactobacilli. J Clin Pathol. 2016;69(3):187–203.
   PubMed Web of Science ®Google Scholar
• Bubnov RV , Babenko LP , Lazarenko LM , et al. Specific properties of probiotic strains: relevance and benefits for the host. Epma J. 2018;9(2):205–223.
   PubMed Web of Science ®Google Scholar
• Madsen KL , Doyle JS , Jewell LD , et al. Lactobacillus species prevents colitis in interleukin 10 gene-deficient mice. Gastroenterology. 1999;116(5):1107–1114.
   PubMed Web of Science ®Google Scholar
• Schultz M , Veltkamp C , Dieleman LA , et al. Lactobacillus plantarum 299V in the treatment and prevention of spontaneous colitis in interleukin-10-deficient mice. Inflamm Bowel Dis. 2002;8(2):71–80.
   PubMed Web of Science ®Google Scholar
• So JS , Kwon HK , Lee CG , et al. Lactobacillus casei suppresses experimental arthritis by down-regulating T helper 1 effector functions. Mol Immunol. 2008;45(9):2690–2699.
   PubMed Web of Science ®Google Scholar
• Vaghef-Mehrabany E , Alipour B , Homayouni-Rad A , et al. Probiotic supplementation improves inflammatory status in patients with rheumatoid arthritis. Nutrition. 2014;30(4):430–435.
   PubMed Web of Science ®Google Scholar
• Zamani B , Golkar HR , Farshbaf S , et al. Clinical and metabolic response to probiotic supplementation in patients with rheumatoid arthritis: a randomized, double-blind, placebo-controlled trial. Int J Rheum Dis. 2016;19(9):869–879.
   PubMed Web of Science ®Google Scholar
• Mu Q , Zhang H , Liao X , et al. Control of lupus nephritis by changes of gut microbiota. Microbiome. 2017;5(1):73.
   PubMedGoogle Scholar
• Johnson BM , Gaudreau MC , Al-Gadban MM , et al. Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice. Clin Exp Immunol. 2015;181(2):323–337.
   PubMed Web of Science ®Google Scholar
• Zhang H , Liao X , Sparks JB , et al. Dynamics of gut microbiota in autoimmune lupus. Appl Environ Microbiol. 2014;80(24):7551–7560.
   PubMed Web of Science ®Google Scholar
• Luo XM , Edwards MR , Mu Q , et al. Gut microbiota in human systemic lupus erythematosus and a mouse model of lupus. Appl Environ Microbiol. 2018;84(4):e02288–e02217.
   PubMed Web of Science ®Google Scholar
• Edwards MR , Dai R , Heid B , et al. Commercial rodent diets differentially regulate autoimmune glomerulonephritis, epigenetics and microbiota in MRL/lpr mice. Int Immunol. 2017;29(6):263–276.
   PubMed Web of Science ®Google Scholar
• Neuman H , Mor H , Bashi T , et al. Helminth-based product and the microbiome of mice with Lupus. mSystems. 2019;4(1):e00160–e00118.
   PubMed Web of Science ®Google Scholar
• He Z , Shao T , Li H , et al. Alterations of the gut microbiome in Chinese patients with systemic lupus erythematosus. Gut Pathog. 2016;8:64.
   PubMed Web of Science ®Google Scholar
• Hevia A , Milani C , Lopez P , et al. Intestinal dysbiosis associated with systemic lupus erythematosus. mBio. 2014;5(5):e01548–01514.
   PubMed Web of Science ®Google Scholar
• Manirarora JN , Parnell SA , Hu YH , et al. NOD dendritic cells stimulated with Lactobacilli preferentially produce IL-10 versus IL-12 and decrease diabetes incidence. Clin Dev Immunol. 2011;2011:630187.
   PubMedGoogle Scholar
• Smits HH , Engering A , van der Kleij D , et al. 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. J Allergy Clin Immunol. 2005;115(6):1260–1267.
   PubMed Web of Science ®Google Scholar
• Walter J , Heng NC , Hammes WP , et al. Identification of Lactobacillus reuteri genes specifically induced in the mouse gastrointestinal tract. Appl Environ Microbiol. 2003;69(4):2044–2051.
   PubMed Web of Science ®Google Scholar
• Pavan S , Desreumaux P , Mercenier A. Use of mouse models to evaluate the persistence, safety, and immune modulation capacities of lactic acid bacteria. Clin Diagn Lab Immunol. 2003;10(4):696–701.
   PubMedGoogle Scholar
• Niedzielin K , Kordecki H , Birkenfeld B. A controlled, double-blind, randomized study on the efficacy of Lactobacillus plantarum 299V in patients with irritable bowel syndrome. Eur J Gastroenterol Hepatol. 2001;13(10):1143–1147.
   PubMed Web of Science ®Google Scholar
• Inaba K , Inaba M , Romani N , et al. Generation of large numbers of dendritic cells from mouse bone marrow cultures supplemented with granulocyte/macrophage colony-stimulating factor. J Exp Med. 1992;176(6):1693–1702.
   PubMed Web of Science ®Google Scholar
• Scheicher C , Mehlig M , Zecher R , et al. Dendritic cells from mouse bone marrow: in vitro differentiation using low doses of recombinant granulocyte-macrophage colony-stimulating factor. J Immunol Methods. 1992;154(2):253–264.
   PubMed Web of Science ®Google Scholar
• Liang S , Alard P , Zhao Y , et al. Conversion of CD4+ CD25- cells into CD4+ CD25+ regulatory T cells in vivo requires B7 costimulation, but not the thymus. J Exp Med. 2005;201(1):127–137.
   PubMed Web of Science ®Google Scholar
• Salomon B , Lenschow DJ , Rhee L , et al. B7/CD28 costimulation is essential for the homeostasis of the CD4 + CD25+ immunoregulatory T cells that control autoimmune diabetes. Immunity. 2000;12(4):431–440.
   PubMed Web of Science ®Google Scholar
• Larche M. Regulatory T cells in allergy and asthma. Chest. 2007;132(3):1007–1014.
   PubMed Web of Science ®Google Scholar
• Moingeon P , Batard T , Fadel R , et al. Immune mechanisms of allergen-specific sublingual immunotherapy. Allergy. 2006;61(2):151–165.
   PubMed Web of Science ®Google Scholar
• Van Overtvelt L , Lombardi V , Razafindratsita A , et al. IL-10-inducing adjuvants enhance sublingual immunotherapy efficacy in a murine asthma model. Int Arch Allergy Immunol. 2008;145(2):152–162.
   PubMed Web of Science ®Google Scholar
• Baharav E , Mor F , Halpern M , et al. Lactobacillus GG bacteria ameliorate arthritis in Lewis rats. J Nutr. 2004;134(8):1964–1969.
   PubMed Web of Science ®Google Scholar
• Kato I , Endo-Tanaka K , Yokokura T. Suppressive effects of the oral administration of Lactobacillus casei on type II collagen-induced arthritis in DBA/1 mice. Life Sci. 1998;63(8):635–644.
   PubMed Web of Science ®Google Scholar
• Liang B , Kashgarian MJ , Sharpe AH , et al. Autoantibody responses and pathology regulated by B7-1 and B7-2 costimulation in MRL/lpr lupus. J Immunol. 2000;165(6):3436–3443.
   PubMed Web of Science ®Google Scholar
• Christensen HR , Frokiaer H , Pestka JJ. Lactobacilli differentially modulate expression of cytokines and maturation surface markers in murine dendritic cells. J Immunol. 2002;168(1):171–178.
   PubMed Web of Science ®Google Scholar
• Esmaeili SA , Mahmoudi M , Rezaieyazdi Z , et al. Generation of tolerogenic dendritic cells using Lactobacillus rhamnosus and Lactobacillus delbrueckii as tolerogenic probiotics. J Cell Biochem. 2018;119(9):7865–7872.
   PubMed Web of Science ®Google Scholar
• Karimi K , Inman MD , Bienenstock J , et al. Lactobacillus reuteri-induced regulatory T cells protect against an allergic airway response in mice. Am J Respir Crit Care Med. 2009;179(3):186–193.
   PubMed Web of Science ®Google Scholar
• Yusoff FM , Wong KK , Redzwan NM. Th1, Th2, and Th17 cytokines in systemic lupus erythematosus. Autoimmunity. 2020;53(1):8–20.
   PubMed Web of Science ®Google Scholar
• Yin Z , Bahtiyar G , Zhang N , et al. IL-10 regulates murine lupus. J Immunol. 2002;169(4):2148–2155.
   PubMed Web of Science ®Google Scholar
• Blenman KR , Duan B , Xu Z , et al. IL-10 regulation of lupus in the NZM2410 murine model. Lab Invest. 2006;86(11):1136–1148.
   PubMed Web of Science ®Google Scholar
• Mokrozub VV , Lazarenko LM , Sichel LM , et al. The role of beneficial bacterial wall elasticity in regulating innate immune response. Epma J. 2015;6:13.
   PubMed Web of Science ®Google Scholar
• Matsuzaki T , Nagata Y , Kado S , et al. Prevention of onset in an insulin-dependent diabetes mellitus model, NOD mice, by oral feeding of Lactobacillus casei. Apmis. 1997;105(7–12):643–649.
   PubMed Web of Science ®Google Scholar
• Ogunrinde E , Zhou Z , Luo Z , et al. A link between plasma microbial translocation, microbiome, and autoantibody development in first-degree relatives of systemic lupus erythematosus patients. Arthritis Rheumatol. 2019;71(11):1858–1868.
   PubMed Web of Science ®Google Scholar
• Thim-Uam A , Surawut S , Issara-Amphorn J , et al. Leaky-gut enhanced lupus progression in the Fc gamma receptor-IIb deficient and pristane-induced mouse models of lupus. Sci Rep. 2020;10(1):777.
   PubMed Web of Science ®Google Scholar
• Manfredo Vieira S , Hiltensperger M , Kumar V , et al. Translocation of a gut pathobiont drives autoimmunity in mice and humans. Science. 2018;359(6380):1156–1161.
   PubMed Web of Science ®Google Scholar
• Zegarra-Ruiz DF , El Beidaq A , Iniguez AJ , et al. A diet-sensitive commensal lactobacillus strain mediates TLR7-dependent systemic autoimmunity. Cell Host Microbe. 2019;25(1):113–127. e116.
   PubMed Web of Science ®Google Scholar
• Azzouz D , Omarbekova A , Heguy A , et al. Lupus nephritis is linked to disease-activity associated expansions and immunity to a gut commensal. Ann Rheum Dis. 2019;78(7):947–956.
   PubMed Web of Science ®Google Scholar
• Rao RK , Samak G. Protection and restitution of gut barrier by probiotics: nutritional and clinical implications. Curr Nutr Food Sci. 2013;9(2):99–107.
   PubMedGoogle Scholar
• Reid G , Abrahamsson T , Bailey M , et al. How do probiotics and prebiotics function at distant sites? Benef Microbes. 2017;8(4):521–533.
   PubMed Web of Science ®Google Scholar
• Turnbaugh PJ , Ley RE , Mahowald MA , et al. An obesity-associated gut microbiome with increased capacity for energy harvest. Nature. 2006;444(7122):1027–1031.
   PubMed Web of Science ®Google Scholar
• Bubnov RV , Babenko LP , Lazarenko LM , et al. Comparative study of probiotic effects of Lactobacillus and Bifidobacteria strains on cholesterol levels, liver morphology and the gut microbiota in obese mice. Epma J. 2017;8(4):357–376.
   PubMed Web of Science ®Google Scholar
• Doron S , Snydman DR. Risk and safety of probiotics. Clin Infect Dis. 2015;60( Suppl 2):S129–S134.
   PubMedGoogle Scholar
• Bubnov RV , Spivak MY , Lazarenko LM , et al. Probiotics and immunity: provisional role for personalized diets and disease prevention. Epma J. 2015;6(1):14.
   PubMedGoogle Scholar
• Wang Y , Liu Y , Sidhu A , et al. Lactobacillus rhamnosus GG culture supernatant ameliorates acute alcohol-induced intestinal permeability and liver injury. Am J Physiol Gastrointest Liver Physiol. 2012;303(1):G32–G41.
   PubMed Web of Science ®Google Scholar
• Sanchez HN , Moroney JB , Gan H , et al. B cell-intrinsic epigenetic modulation of antibody responses by dietary fiber-derived short-chain fatty acids. Nat Commun. 2020;11(1):60.
   PubMed Web of Science ®Google Scholar
• Yuan F , Harder J , Ma J , et al. Using multiple analytical platforms to investigate the androgen depletion effects on fecal metabolites in a mouse model of systemic lupus erythematosus. J Proteome Res. 2020;19(2):667–676.
   PubMed Web of Science ®Google Scholar
• Galdeano CM , Perdigon G. The probiotic bacterium Lactobacillus casei induces activation of the gut mucosal immune system through innate immunity. Clin Vaccine Immunol. 2006;13(2):219–226.
   PubMed Web of Science ®Google Scholar
• Lebeer S , Claes IJ , Vanderleyden J. Anti-inflammatory potential of probiotics: lipoteichoic acid makes a difference. Trends Microbiol. 2012;20(1):5–10.
   PubMed Web of Science ®Google Scholar
• Jeong JH , Jang S , Jung BJ , et al. Differential immune-stimulatory effects of LTAs from different lactic acid bacteria via MAPK signaling pathway in RAW 264.7 cells. Immunobiology. 2015;220(4):460–466.
   PubMed Web of Science ®Google Scholar
• Grangette C , Nutten S , Palumbo E , et al. Enhanced antiinflammatory capacity of a Lactobacillus plantarum mutant synthesizing modified teichoic acids. Proc Natl Acad Sci Usa. 2005;102(29):10321–10326.
   PubMed Web of Science ®Google Scholar
• Jang KS , Baik JE , Han SH , et al. Multi-spectrometric analyses of lipoteichoic acids isolated from Lactobacillus plantarum. Biochem Biophys Res Commun. 2011;407(4):823–830.
   PubMed Web of Science ®Google Scholar