SLE: Another Autoimmune Disorder Influenced by Microbes and Diet?

Qinghui Mu, Husen Zhang, Xin M Luo, Qinghui Mu, Husen Zhang, Xin M Luo

Abstract

Systemic lupus erythematosus (SLE) is a multi-system autoimmune disease. Despite years of study, the etiology of SLE is still unclear. Both genetic and environmental factors have been implicated in the disease mechanisms. In the past decade, a growing body of evidence has indicated an important role of gut microbes in the development of autoimmune diseases, including type 1 diabetes, rheumatoid arthritis, and multiple sclerosis. However, such knowledge on SLE is little, though we have already known that environmental factors can trigger the development of lupus. Several recent studies have suggested that alterations of the gut microbial composition may be correlated with SLE disease manifestations, while the exact roles of either symbiotic or pathogenic microbes in this disease remain to be explored. Elucidation of the roles of gut microbes - as well as the roles of diet that can modulate the composition of gut microbes - in SLE will shed light on how this autoimmune disorder develops, and provide opportunities for improved biomarkers of the disease and the potential to probe new therapies. In this review, we aim to compile the available evidence on the contributions of diet and gut microbes to SLE occurrence and pathogenesis.

Keywords: SLE; bacterial antigens; diet; estrogen; hygiene hypothesis; microbiota.

Figures

Figure 1
Figure 1
Emerging evidences point to a potential link between SLE and microbiota.

References

    1. Ley RE, Peterson DA, Gordon JI. Ecological and evolutionary forces shaping microbial diversity in the human intestine. Cell (2006) 124:837–48.10.1016/j.cell.2006.02.017
    1. Kamada N, Seo SU, Chen GY, Nunez G. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol (2013) 13(5):321–35.10.1038/nri3430
    1. Kuhn KA, Stappenbeck TS. Peripheral education of the immune system by the colonic microbiota. Semin Immunol (2013) 25(5):364–9.10.1016/j.smim.2013.10.002
    1. Strober W. Impact of the gut microbiome on mucosal inflammation. Trends Immunol (2013) 34(9):423–30.10.1016/j.it.2013.07.001
    1. Yeoh N, Burton JP, Suppiah P, Reid G, Stebbings S. The role of the microbiome in rheumatic diseases. Curr Rheumatol Rep (2013) 15(3):314.10.1007/s11926-012-0314-y
    1. Brown EM, Sadarangani M, Finlay BB. The role of the immune system in governing host-microbe interactions in the intestine. Nat Immunol (2013) 14(7):660–7.10.1038/ni.2611
    1. Garrett WS, Gallini CA, Yatsunenko T, Michaud M, DuBois A, Delaney ML, et al. Enterobacteriaceae act in concert with the gut microbiota to induce spontaneous and maternally transmitted colitis. Cell Host Microbe (2010) 8:292–300.10.1016/j.chom.2010.08.004
    1. Frank DN, Amand ALS, Feldman RA, Boedeker EC, Harpaz N, Pace NR. Molecular-phylogenetic characterization of microbial community imbalances in human inflammatory bowel diseases. Proc Natl Acad Sci U S A (2007) 104:13780–5.10.1073/pnas.0706625104
    1. Wen L, Ley RE, Volchkov PY, Stranges PB, Avanesyan L, Stonebraker AC, et al. Innate immunity and intestinal microbiota in the development of type 1 diabetes. Nature (2008) 455(7216):1109–13.10.1038/nature07336
    1. Mathis D, Benoist C. The influence of the microbiota on type-1 diabetes: on the threshold of a leap forward in our understanding. Immunol Rev (2012) 245(1):239–49.10.1111/j.1600-065X.2011.01084.x
    1. Yurkovetskiy L, Burrows M, Khan AA, Graham L, Volchkov P, Becker L, et al. Gender bias in autoimmunity is influenced by microbiota. Immunity (2013) 39(2):400–12.10.1016/j.immuni.2013.08.013
    1. Markle JG, Frank DN, Mortin-Toth S, Robertson CE, Feazel LM, Rolle-Kampczyk U, et al. Sex differences in the gut microbiome drive hormone-dependent regulation of autoimmunity. Science (2013) 339(6123):1084–8.10.1126/science.1233521
    1. Vaahtovuo J, Munukka E, Korkeamaki M, Luukkainen R, Toivanen P. Fecal microbiota in early rheumatoid arthritis. J Rheumatol (2008) 35(8):1500–5.
    1. Abdollahi-Roodsaz S, Joosten LA, Koenders MI, Devesa I, Roelofs MF, Radstake TR, et al. Stimulation of TLR2 and TLR4 differentially skews the balance of T cells in a mouse model of arthritis. J Clin Invest (2008) 118(1):205–16.10.1172/JCI32639
    1. Wu HJ, Ivanov II, Darce J, Hattori K, Shima T, Umesaki Y, et al. Gut-residing segmented filamentous bacteria drive autoimmune arthritis via T helper 17 cells. Immunity (2010) 32(6):815–27.10.1016/j.immuni.2010.06.001
    1. Lee YK, Menezes JS, Umesaki Y, Mazmanian SK. Proinflammatory T-cell responses to gut microbiota promote experimental autoimmune encephalomyelitis. Proc Natl Acad Sci U S A (2011) 108(Suppl 1):4615–22.10.1073/pnas.1000082107
    1. Berer K, Mues M, Koutrolos M, Rasbi ZA, Boziki M, Johner C, et al. Commensal microbiota and myelin autoantigen cooperate to trigger autoimmune demyelination. Nature (2011) 479(7374):538–41.10.1038/nature10554
    1. Vieira SM, Pagovich OE, Kriegel MA. Diet, microbiota and autoimmune diseases. Lupus (2014) 23(6):518–26.10.1177/0961203313501401
    1. Lim SS, Bayakly AR, Helmick CG, Gordon C, Easley KA, Drenkard C. The incidence and prevalence of systemic lupus erythematosus, 2002-2004: the Georgia lupus registry. Arthritis Rheumatol (2014) 66(2):357–68.10.1002/art.38239
    1. Somers EC, Marder W, Cagnoli P, Lewis EE, DeGuire P, Gordon C, et al. Population-based incidence and prevalence of systemic lupus erythematosus: the Michigan Lupus Epidemiology and Surveillance program. Arthritis Rheumatol (2014) 66(2):369–78.10.1002/art.38238
    1. Zhang H, Liao X, Sparks JB, Luo XM. Dynamics of gut microbiota in autoimmune lupus. Appl Environ Microbiol (2014) 80(24):7551–60.10.1128/AEM.02676-14
    1. Hevia A, Milani C, Lopez P, Cuervo A, Arboleya S, Duranti S, et al. Intestinal dysbiosis associated with systemic lupus erythematosus. MBio (2014) 5(5):e1548–1514.10.1128/mBio.01548-14
    1. Johnson BM, Gaudreau MC, Al-Gadban MM, Gudi R, Vasu C. Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice. Clin Exp Immunol (2015) 181(2):323–37.10.1111/cei.12609
    1. Hewagama A, Richardson B. The genetics and epigenetics of autoimmune diseases. J Autoimmun (2009) 33(1):3–11.10.1016/j.jaut.2009.03.007
    1. Symmons DP. Frequency of lupus in people of African origin. Lupus (1995) 4(3):176–8.10.1177/096120339500400303
    1. Bach JF. The effect of infections on susceptibility to autoimmune and allergic diseases. N Engl J Med (2002) 347(12):911–20.10.1056/NEJMra020100
    1. Sawalha AH, Jeffries M, Webb R, Lu Q, Gorelik G, Ray D, et al. Defective T-cell ERK signaling induces interferon-regulated gene expression and overexpression of methylation-sensitive genes similar to lupus patients. Genes Immun (2008) 9(4):368–78.10.1038/gene.2008.29
    1. Bijl M, Kallenberg CG. Ultraviolet light and cutaneous lupus. Lupus (2006) 15(11):724–7.10.1177/0961203306071705
    1. Lee KW, Pausova Z. Cigarette smoking and DNA methylation. Front Genet (2013) 4:132.10.3389/fgene.2013.00132
    1. Somers EC, Richardson BC. Environmental exposures, epigenetic changes and the risk of lupus. Lupus (2014) 23(6):568–76.10.1177/0961203313499419
    1. Uramoto KM, Michet CJ, Jr, Thumboo J, Sunku J, O’Fallon WM, Gabriel SE. Trends in the incidence and mortality of systemic lupus erythematosus, 1950-1992. Arthritis Rheum (1999) 42(1):46–50.10.1002/1529-0131(199901)42:1<46::AID-ANR6>;2-2
    1. Danchenko N, Satia JA, Anthony MS. Epidemiology of systemic lupus erythematosus: a comparison of worldwide disease burden. Lupus (2006) 15(5):308–18.10.1191/0961203306lu2305xx
    1. Voss A, Green A, Junker P. Systemic lupus erythematosus in Denmark: clinical and epidemiological characterization of a county-based cohort. Scand J Rheumatol (1998) 27(2):98–105.10.1080/030097498440958
    1. Cooke A, Tonks P, Jones FM, O’Shea H, Hutchings P, Fulford AJ, et al. Infection with Schistosoma mansoni prevents insulin dependent diabetes mellitus in non-obese diabetic mice. Parasite Immunol (1999) 21(4):169–76.10.1046/j.1365-3024.1999.00213.x
    1. Strachan DP. Hay fever, hygiene, and household size. BMJ (1989) 299(6710):1259–60.10.1136/bmj.299.6710.1259
    1. Hayashi T, Lee S, Ogasawara H, Sekigawa I, Iida N, Tomino Y, et al. Exacerbation of systemic lupus erythematosus related to cytomegalovirus infection. Lupus (1998) 7(8):561–4.10.1191/096120398678920596
    1. James JA, Kaufman KM, Farris AD, Taylor-Albert E, Lehman TJ, Harley JB. An increased prevalence of Epstein-Barr virus infection in young patients suggests a possible etiology for systemic lupus erythematosus. J Clin Invest (1997) 100(12):3019–26.10.1172/JCI119856
    1. Nawata M, Seta N, Yamada M, Sekigawa I, Lida N, Hashimoto H. Possible triggering effect of cytomegalovirus infection on systemic lupus erythematosus. Scand J Rheumatol (2001) 30(6):360–2.10.1080/030097401317148570
    1. Nelson P, Rylance P, Roden D, Trela M, Tugnet N. Viruses as potential pathogenic agents in systemic lupus erythematosus. Lupus (2014) 23(6):596–605.10.1177/0961203314531637
    1. Rasmussen NS, Draborg AH, Nielsen CT, Jacobsen S, Houen G. Antibodies to early EBV, CMV, and HHV6 antigens in systemic lupus erythematosus patients. Scand J Rheumatol (2015) 44(2):143–9.10.3109/03009742.2014.973061
    1. Tanaka K, Sawamura S, Satoh T, Kobayashi K, Noda S. Role of the indigenous microbiota in maintaining the virus-specific CD8 memory T cells in the lung of mice infected with murine cytomegalovirus. J Immunol (2007) 178(8):5209–16.10.4049/jimmunol.178.8.5209
    1. Praprotnik S, Sodin-Semrl S, Tomsic M, Shoenfeld Y. The curiously suspicious: infectious disease may ameliorate an ongoing autoimmune destruction in systemic lupus erythematosus patients. J Autoimmun (2008) 30(1–2):37–41.10.1016/j.jaut.2007.11.002
    1. Ram M, Anaya JM, Barzilai O, Izhaky D, Porat Katz BS, Blank M, et al. The putative protective role of hepatitis B virus (HBV) infection from autoimmune disorders. Autoimmun Rev (2008) 7(8):621–5.10.1016/j.autrev.2008.06.008
    1. Esposito S, Bosis S, Semino M, Rigante D. Infections and systemic lupus erythematosus. Eur J Clin Microbiol Infect Dis (2014) 33(9):1467–75.10.1007/s10096-014-2098-7
    1. Sawalha AH, Schmid WR, Binder SR, Bacino DK, Harley JB. Association between systemic lupus erythematosus and Helicobacter pylori seronegativity. J Rheumatol (2004) 31(8):1546–50.
    1. Wasley A, Kruszon-Moran D, Kuhnert W, Simard EP, Finelli L, McQuillan G, et al. The prevalence of hepatitis B virus infection in the United States in the era of vaccination. J Infect Dis (2010) 202(2):192–201.10.1086/653622
    1. Chen Y, Blaser MJ. Helicobacter pylori colonization is inversely associated with childhood asthma. J Infect Dis (2008) 198(4):553–60.10.1086/590158
    1. den Hoed CM, Vila AJ, Holster IL, Perez-Perez GI, Blaser MJ, de Jongste JC, et al. Helicobacter pylori and the birth cohort effect: evidence for stabilized colonization rates in childhood. Helicobacter (2011) 16(5):405–9.10.1111/j.1523-5378.2011.00854.x
    1. McKinney EF, Lee JC, Jayne DR, Lyons PA, Smith KG. T-cell exhaustion, co-stimulation and clinical outcome in autoimmunity and infection. Nature (2015) 523(7562):612–6.10.1038/nature14468
    1. Ingram JT, Yi JS, Zajac AJ. Exhausted CD8 T cells downregulate the IL-18 receptor and become unresponsive to inflammatory cytokines and bacterial co-infections. PLoS Pathog (2011) 7(9):e1002273.10.1371/journal.ppat.1002273
    1. Chen M, Aosai F, Norose K, Mun HS, Ishikura H, Hirose S, et al. Toxoplasma gondii infection inhibits the development of lupus-like syndrome in autoimmune (New Zealand Black x New Zealand White) F1 mice. Int Immunol (2004) 16(7):937–46.10.1093/intimm/dxh095
    1. Al-Quraishy S, Abdel-Maksoud MA, El-Amir A, Abdel-Ghaffar FA, Badr G. Malarial infection of female BWF1 lupus mice alters the redox state in kidney and liver tissues and confers protection against lupus nephritis. Oxid Med Cell Longev (2013) 2013:156562.10.1155/2013/156562
    1. Greenwood BM, Herrick EM, Voller A. Suppression of autoimmune disease in NZB and (NZB x NZW) F1 hybrid mice by infection with malaria. Nature (1970) 226(5242):266–7.10.1038/226266a0
    1. Sato MN, Minoprio P, Avrameas S, Ternynck T. Changes in the cytokine profile of lupus-prone mice (NZB/NZW)F1 induced by Plasmodium chabaudi and their implications in the reversal of clinical symptoms. Clin Exp Immunol (2000) 119(2):333–9.10.1046/j.1365-2249.2000.01124.x
    1. Hayashi T. Effect of prostaglandin E2 on plasma lactic dehydrogenase activity in (NZB x NZW)F1 mice with a chronic infection of lactic dehydrogenase virus. J Comp Pathol (1992) 107(1):41–8.10.1016/0021-9975(92)90094-B
    1. Hayashi T, Mori I, Yamamoto H. Lactic dehydrogenase virus infection prevents development of anti-nuclear antibody in (NZB x NZW)F1 mice; role of prostaglandin E2 and macrophage Ia antigen expression. Int J Exp Pathol (1992) 73(5):593–601.
    1. Hayashi T, Noguchi Y, Kameyama Y. Suppression of development of anti-nuclear antibody and glomerulonephritis in NZB x NZWF1 mice by persistent infection with lactic dehydrogenase virus: possible involvement of superoxide anion as a progressive effector. Int J Exp Pathol (1993) 74(6):553–60.
    1. Oldstone MB, Dixon FJ. Inhibition of antibodies to nuclear antigen and to DNA in New Zealand mice infected with lactate dehydrogenase virus. Science (1972) 175(4023):784–6.10.1126/science.175.4023.784
    1. Smith PM, Howitt MR, Panikov N, Michaud M, Gallini CA, Bohlooly YM, et al. The microbial metabolites, short-chain fatty acids, regulate colonic Treg cell homeostasis. Science (2013) 341(6145):569–73.10.1126/science.1241165
    1. Arpaia N, Campbell C, Fan X, Dikiy S, van der Veeken J, deRoos P, et al. Metabolites produced by commensal bacteria promote peripheral regulatory T-cell generation. Nature (2013) 504(7480):451–5.10.1038/nature12726
    1. Furusawa Y, Obata Y, Fukuda S, Endo TA, Nakato G, Takahashi D, et al. Commensal microbe-derived butyrate induces the differentiation of colonic regulatory T cells. Nature (2013) 504(7480):446–50.10.1038/nature12721
    1. 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 (2014) 40(1):128–39.10.1016/j.immuni.2013.12.007
    1. Rojo D, Hevia A, Bargiela R, Lopez P, Cuervo A, Gonzalez S, et al. Ranking the impact of human health disorders on gut metabolism: systemic lupus erythematosus and obesity as study cases. Sci Rep (2015) 5:8310.10.1038/srep08310
    1. Van Boeckel TP, Gandra S, Ashok A, Caudron Q, Grenfell BT, Levin SA, et al. Global antibiotic consumption 2000 to 2010: an analysis of national pharmaceutical sales data. Lancet Infect Dis (2014) 14(8):742–50.10.1016/S1473-3099(14)70780-7
    1. Hogberg LD, Muller A, Zorzet A, Monnet DL, Cars O. Antibiotic use worldwide. Lancet Infect Dis (2014) 14(12):1179–80.10.1016/S1473-3099(14)70987-9
    1. Dorrestein PC, Mazmanian SK, Knight R. Finding the missing links among metabolites, microbes, and the host. Immunity (2014) 40(6):824–32.10.1016/j.immuni.2014.05.015
    1. Kamen DL. Environmental influences on systemic lupus erythematosus expression. Rheum Dis Clin North Am (2014) 40(3):401–12.10.1016/j.rdc.2014.05.003
    1. Ginde AA, Liu MC, Camargo CA, Jr. Demographic differences and trends of vitamin D insufficiency in the US population, 1988-2004. Arch Intern Med (2009) 169(6):626–32.10.1001/archinternmed.2008.604
    1. Holick MF. Vitamin D deficiency. N Engl J Med (2007) 357(3):266–81.10.1056/NEJMra070553
    1. Carvalho C, Marinho A, Leal B, Bettencourt A, Boleixa D, Almeida I, et al. Association between vitamin D receptor (VDR) gene polymorphisms and systemic lupus erythematosus in Portuguese patients. Lupus (2015) 24(8):846–53.10.1177/0961203314566636
    1. Handono K, Sidarta YO, Pradana BA, Nugroho RA, Hartono IA, Kalim H, et al. Vitamin D prevents endothelial damage induced by increased neutrophil extracellular traps formation in patients with systemic lupus erythematosus. Acta Med Indones (2014) 46(3):189–98.
    1. Smith CK, Kaplan MJ. The role of neutrophils in the pathogenesis of systemic lupus erythematosus. Curr Opin Rheumatol (2015) 27(5):448–53.10.1097/BOR.0000000000000197
    1. Andreoli L, Dall’Ara F, Piantoni S, Zanola A, Piva N, Cutolo M, et al. A 24-month prospective study on the efficacy and safety of two different monthly regimens of vitamin D supplementation in pre-menopausal women with systemic lupus erythematosus. Lupus (2015) 24(4–5):499–506.10.1177/0961203314559089
    1. Piantoni S, Andreoli L, Scarsi M, Zanola A, Dall’Ara F, Pizzorni C, et al. Phenotype modifications of T-cells and their shift toward a Th2 response in patients with systemic lupus erythematosus supplemented with different monthly regimens of vitamin D. Lupus (2015) 24(4–5):490–8.10.1177/0961203314559090
    1. Schneider L, Colar da Silva AC, Werres Junior LC, Alegretti AP, Dos Santos AS, Santos M, et al. Vitamin D levels and cytokine profiles in patients with systemic lupus erythematosus. Lupus (2015) 24(11):1191–7.10.1177/0961203315584811
    1. Habibi S, Saleem MA, Ramanan AV. Juvenile systemic lupus erythematosus: review of clinical features and management. Indian Pediatr (2011) 48(11):879–87.10.1007/s13312-011-0143-5
    1. Hoffman IE, Lauwerys BR, De Keyser F, Huizinga TW, Isenberg D, Cebecauer L, et al. Juvenile-onset systemic lupus erythematosus: different clinical and serological pattern than adult-onset systemic lupus erythematosus. Ann Rheum Dis (2009) 68(3):412–5.10.1136/ard.2008.094813
    1. Lima GL, Paupitz J, Aikawa NE, Takayama L, Bonfa E, Pereira RM. A randomized double-blind placebo-controlled trial of vitamin D supplementation in adolescents and young adults with Juvenile-onset SLE: improvement in disease activity and fatigue scores. Arthritis Care Res (Hoboken) (2015).10.1002/acr.22621
    1. Kinoshita K, Kishimoto K, Shimazu H, Nozaki Y, Sugiyama M, Ikoma S, et al. Successful treatment with retinoids in patients with lupus nephritis. Am J Kidney Dis (2010) 55(2):344–7.10.1053/j.ajkd.2009.06.012
    1. Kinoshita K, Funauchi M. [Therapeutic effect of retinoic acid in lupus nephritis]. Nihon Rinsho Meneki Gakkai Kaishi (2012) 35(1):1–7.10.2177/jsci.35.1
    1. Kinoshita K, Yoo BS, Nozaki Y, Sugiyama M, Ikoma S, Ohno M, et al. Retinoic acid reduces autoimmune renal injury and increases survival in NZB/W F1 mice. J Immunol (2003) 170(11):5793–8.10.4049/jimmunol.170.11.5793
    1. Perez de Lema G, Lucio-Cazana FJ, Molina A, Luckow B, Schmid H, de Wit C, et al. Retinoic acid treatment protects MRL/lpr lupus mice from the development of glomerular disease. Kidney Int (2004) 66(3):1018–28.10.1111/j.1523-1755.2004.00850.x
    1. Nozaki Y, Yamagata T, Yoo BS, Sugiyama M, Ikoma S, Kinoshita K, et al. The beneficial effects of treatment with all-trans-retinoic acid plus corticosteroid on autoimmune nephritis in NZB/WF mice. Clin Exp Immunol (2005) 139(1):74–83.10.1111/j.1365-2249.2005.02654.x
    1. Miyabe Y, Miyabe C, Nanki T. Could retinoids be a potential treatment for rheumatic diseases? Rheumatol Int (2015) 35(1):35–41.10.1007/s00296-014-3067-2
    1. Liao X, Ren J, Wei CH, Ross AC, Cecere TE, Jortner BS, et al. Paradoxical effects of all-trans-retinoic acid on lupus-like disease in the MRL/lpr mouse model. PLoS One (2015) 10(3):e0118176.10.1371/journal.pone.0118176
    1. Robinson DR, Prickett JD, Makoul GT, Steinberg AD, Colvin RB. Dietary fish oil reduces progression of established renal disease in (NZB x NZW)F1 mice and delays renal disease in BXSB and MRL/1 strains. Arthritis Rheum (1986) 29(4):539–46.10.1002/art.1780290412
    1. Robinson DR, Prickett JD, Polisson R, Steinberg AD, Levine L. The protective effect of dietary fish oil on murine lupus. Prostaglandins (1985) 30(1):51–75.10.1016/S0090-6980(85)80010-1
    1. Prickett JD, Robinson DR, Steinberg AD. Effects of dietary enrichment with eicosapentaenoic acid upon autoimmune nephritis in female NZB X NZW/F1 mice. Arthritis Rheum (1983) 26(2):133–9.10.1002/art.1780260203
    1. Halade GV, Williams PJ, Veigas JM, Barnes JL, Fernandes G. Concentrated fish oil (Lovaza(R)) extends lifespan and attenuates kidney disease in lupus-prone short-lived (NZBxNZW)F1 mice. Exp Biol Med (Maywood) (2013) 238(6):610–22.10.1177/1535370213489485
    1. Halade GV, Rahman MM, Bhattacharya A, Barnes JL, Chandrasekar B, Fernandes G. Docosahexaenoic acid-enriched fish oil attenuates kidney disease and prolongs median and maximal life span of autoimmune lupus-prone mice. J Immunol (2010) 184(9):5280–6.10.4049/jimmunol.0903282
    1. Kim YJ, Kim HJ, No JK, Chung HY, Fernandes G. Anti-inflammatory action of dietary fish oil and calorie restriction. Life Sci (2006) 78(21):2523–32.10.1016/j.lfs.2005.10.034
    1. Bhattacharya A, Lawrence RA, Krishnan A, Zaman K, Sun D, Fernandes G. Effect of dietary n-3 and n-6 oils with and without food restriction on activity of antioxidant enzymes and lipid peroxidation in livers of cyclophosphamide treated autoimmune-prone NZB/W female mice. J Am Coll Nutr (2003) 22(5):388–99.10.1080/07315724.2003.10719322
    1. Chin YH, Ye MW, Cai JP, Xu XM. Differential regulation of tissue-specific lymph node high endothelial venule cell adhesion molecules by tumour necrosis factor and transforming growth factor-beta 1. Immunology (1996) 87(4):559–65.10.1046/j.1365-2567.1996.490562.x
    1. Chandrasekar B, Troyer DA, Venkatraman JT, Fernandes G. Dietary omega-3 lipids delay the onset and progression of autoimmune lupus nephritis by inhibiting transforming growth factor beta mRNA and protein expression. J Autoimmun (1995) 8(3):381–93.10.1006/jaut.1995.0030
    1. Chandrasekar B, Fernandes G. Decreased pro-inflammatory cytokines and increased antioxidant enzyme gene expression by omega-3 lipids in murine lupus nephritis. Biochem Biophys Res Commun (1994) 200(2):893–8.10.1006/bbrc.1994.1534
    1. Pestka JJ, Vines LL, Bates MA, He K, Langohr I. Comparative effects of n-3, n-6 and n-9 unsaturated fatty acid-rich diet consumption on lupus nephritis, autoantibody production and CD4+ T cell-related gene responses in the autoimmune NZBWF1 mouse. PLoS One (2014) 9(6):e100255.10.1371/journal.pone.0100255
    1. Westberg G, Tarkowski A, Svalander C. Effect of eicosapentaenoic acid rich menhaden oil and MaxEPA on the autoimmune disease of Mrl/l mice. Int Arch Allergy Appl Immunol (1989) 88(4):454–61.10.1159/000234732
    1. Kelley VE, Ferretti A, Izui S, Strom TB. A fish oil diet rich in eicosapentaenoic acid reduces cyclooxygenase metabolites, and suppresses lupus in MRL-lpr mice. J Immunol (1985) 134(3):1914–9.
    1. Lozovoy MA, Simao AN, Morimoto HK, Scavuzzi BM, Iriyoda TV, Reiche EM, et al. Fish oil N-3 fatty acids increase adiponectin and decrease leptin levels in patients with systemic lupus erythematosus. Mar Drugs (2015) 13(2):1071–83.10.3390/md13021071
    1. Borges MC, Santos Fde M, Telles RW, Correia MI, Lanna CC. [Polyunsaturated omega-3 fatty acids and systemic lupus erythematosus: what do we know?]. Rev Bras Reumatol (2014) 54(6):459–66.10.1016/j.rbr.2013.12.002
    1. Ghosh S, Molcan E, DeCoffe D, Dai C, Gibson DL. Diets rich in n-6 PUFA induce intestinal microbial dysbiosis in aged mice. Br J Nutr (2013) 110(3):515–23.10.1017/S0007114512005326
    1. Cantorna MT, McDaniel K, Bora S, Chen J, James J. Vitamin D, immune regulation, the microbiota, and inflammatory bowel disease. Exp Biol Med (Maywood) (2014) 239(11):1524–30.10.1177/1535370214523890
    1. Cuervo A, Hevia A, Lopez P, Suarez A, Sanchez B, Margolles A, et al. Association of polyphenols from oranges and apples with specific intestinal microorganisms in systemic lupus erythematosus patients. Nutrients (2015) 7(2):1301–17.10.3390/nu7021301
    1. Sabroe I, Read RC, Whyte MK, Dockrell DH, Vogel SN, Dower SK. Toll-like receptors in health and disease: complex questions remain. J Immunol (2003) 171(4):1630–5.10.4049/jimmunol.171.4.1630
    1. Liu Y, Yin H, Zhao M, Lu Q. TLR2 and TLR4 in autoimmune diseases: a comprehensive review. Clin Rev Allergy Immunol (2014) 47(2):136–47.10.1007/s12016-013-8402-y
    1. Nockher WA, Wigand R, Schoeppe W, Scherberich JE. Elevated levels of soluble CD14 in serum of patients with systemic lupus erythematosus. Clin Exp Immunol (1994) 96(1):15–9.10.1111/j.1365-2249.1994.tb06222.x
    1. Liu B, Yang Y, Dai J, Medzhitov R, Freudenberg MA, Zhang PL, et al. TLR4 up-regulation at protein or gene level is pathogenic for lupus-like autoimmune disease. J Immunol (2006) 177(10):6880–8.10.4049/jimmunol.177.10.6880
    1. Zhang Y, Liu S, Yu Y, Zhang T, Liu J, Shen Q, et al. Immune complex enhances tolerogenecity of immature dendritic cells via FcgammaRIIb and promotes FcgammaRIIb-overexpressing dendritic cells to attenuate lupus. Eur J Immunol (2011) 41(4):1154–64.10.1002/eji.201040767
    1. Zhai JX, Zhang ZX, Feng YJ, Ding SS, Wang XH, Zou LW, et al. PDTC attenuate LPS-induced kidney injury in systemic lupus erythematosus-prone MRL/lpr mice. Mol Biol Rep (2012) 39(6):6763–71.10.1007/s11033-012-1501-7
    1. Granholm NA, Cavallo T. Bacterial lipopolysaccharide enhances deposition of immune complexes and exacerbates nephritis in BXSB lupus-prone mice. Clin Exp Immunol (1991) 85(2):270–7.10.1111/j.1365-2249.1991.tb05717.x
    1. Granholm NA, Cavallo T. Long-lasting effects of bacterial lipopolysaccharide promote progression of lupus nephritis in NZB/W mice. Lupus (1994) 3(6):507–14.10.1177/096120339400300614
    1. Lee TP, Tang SJ, Wu MF, Song YC, Yu CL, Sun KH. Transgenic overexpression of anti-double-stranded DNA autoantibody and activation of toll-like receptor 4 in mice induce severe systemic lupus erythematosus syndromes. J Autoimmun (2010) 35(4):358–67.10.1016/j.jaut.2010.07.007
    1. Lee TP, Huang JC, Liu CJ, Chen HJ, Chen YH, Tsai YT, et al. Interactions of surface-expressed TLR-4 and endosomal TLR-9 accelerate lupus progression in anti-dsDNA antibody transgenic mice. Exp Biol Med (Maywood) (2014) 239(6):715–23.10.1177/1535370214525299
    1. Ni JQ, Ouyang Q, Lin L, Huang Z, Lu H, Chen X, et al. Role of toll-like receptor 4 on lupus lung injury and atherosclerosis in LPS-challenge ApoE(-)/(-) mice. Clin Dev Immunol (2013) 2013:476856.10.1155/2013/476856
    1. Levine J, Subang R, Setty S, Cabrera J, Laplante P, Fritzler M, et al. Phospholipid-binding proteins differ in their capacity to induce autoantibodies and murine systemic lupus erythematosus. Lupus (2014) 23(8):752–68.10.1177/0961203314525676
    1. Levine JS, Subang R, Nasr SH, Fournier S, Lajoie G, Wither J, et al. Immunization with an apoptotic cell-binding protein recapitulates the nephritis and sequential autoantibody emergence of systemic lupus erythematosus. J Immunol (2006) 177(9):6504–16.10.4049/jimmunol.177.9.6504
    1. Tolomeo T, Rico De Souza A, Roter E, Dieude M, Amireault P, Subang R, et al. T cells demonstrate a Th1-biased response to native beta2-glycoprotein I in a murine model of anti-phospholipid antibody induction. Autoimmunity (2009) 42(4):292–5.10.1080/08916930902828254
    1. Aida Y, Pabst MJ. Neutrophil responses to lipopolysaccharide. Effect of adherence on triggering and priming of the respiratory burst. J Immunol (1991) 146(4):1271–6.
    1. Doerfler ME, Danner RL, Shelhamer JH, Parrillo JE. Bacterial lipopolysaccharides prime human neutrophils for enhanced production of leukotriene B4. J Clin Invest (1989) 83(3):970–7.10.1172/JCI113983
    1. Guthrie LA, McPhail LC, Henson PM, Johnston RB, Jr. Priming of neutrophils for enhanced release of oxygen metabolites by bacterial lipopolysaccharide. Evidence for increased activity of the superoxide-producing enzyme. J Exp Med (1984) 160(6):1656–71.10.1084/jem.160.6.1656
    1. Lartigue A, Colliou N, Calbo S, Francois A, Jacquot S, Arnoult C, et al. Critical role of TLR2 and TLR4 in autoantibody production and glomerulonephritis in lpr mutation-induced mouse lupus. J Immunol (2009) 183(10):6207–16.10.4049/jimmunol.0803219
    1. Summers SA, Hoi A, Steinmetz OM, O’Sullivan KM, Ooi JD, Odobasic D, et al. TLR9 and TLR4 are required for the development of autoimmunity and lupus nephritis in pristane nephropathy. J Autoimmun (2010) 35(4):291–8.10.1016/j.jaut.2010.05.004
    1. Freeley SJ, Giorgini A, Tulone C, Popat RJ, Horsfield C, Robson MG. Toll-like receptor 2 or toll-like receptor 4 deficiency does not modify lupus in MRLlpr mice. PLoS One (2013) 8(9):e74112.10.1371/journal.pone.0074112
    1. Qin H, Wilson CA, Lee SJ, Zhao X, Benveniste EN. LPS induces CD40 gene expression through the activation of NF-kappaB and STAT-1alpha in macrophages and microglia. Blood (2005) 106(9):3114–22.10.1182/blood-2005-02-0759
    1. Ripoll E, Merino A, Herrero-Fresneda I, Aran JM, Goma M, Bolanos N, et al. CD40 gene silencing reduces the progression of experimental lupus nephritis modulating local milieu and systemic mechanisms. PLoS One (2013) 8(6):e65068.10.1371/journal.pone.0065068
    1. Harlow L, Fernandez I, Soejima M, Ridgway WM, Ascherman DP. Characterization of TLR4-mediated auto-antibody production in a mouse model of histidyl-tRNA synthetase-induced myositis. Innate Immun (2012) 18(6):876–85.10.1177/1753425912446714
    1. Shui HA, Ka SM, Wu WM, Lin YF, Hou YC, Su LC, et al. LPS-evoked IL-18 expression in mesangial cells plays a role in accelerating lupus nephritis. Rheumatology (Oxford) (2007) 46(8):1277–84.10.1093/rheumatology/kem136
    1. Jiang W, Zhang L, Lang R, Li Z, Gilkeson G. Sex differences in monocyte activation in systemic lupus erythematosus (SLE). PLoS One (2014) 9(12):e114589.10.1371/journal.pone.0114589
    1. Svenson JL, EuDaly J, Ruiz P, Korach KS, Gilkeson GS. Impact of estrogen receptor deficiency on disease expression in the NZM2410 lupus prone mouse. Clin Immunol (2008) 128(2):259–68.10.1016/j.clim.2008.03.508
    1. Cunningham MA, Naga OS, Eudaly JG, Scott JL, Gilkeson GS. Estrogen receptor alpha modulates toll-like receptor signaling in murine lupus. Clin Immunol (2012) 144(1):1–12.10.1016/j.clim.2012.04.001
    1. Jiang W, Gilkeson G. Sex differences in monocytes and TLR4 associated immune responses; implications for systemic lupus erythematosus (SLE). J Immunother Appl (2014) 1:1.10.7243/2055-2394-1-1
    1. Liu Y, Liao J, Zhao M, Wu H, Yung S, Chan TM, et al. Increased expression of TLR2 in CD4 T cells from SLE patients enhances immune reactivity and promotes IL-17 expression through histone modifications. Eur J Immunol (2015) 45(9):2683–93.10.1002/eji.201445219
    1. Pawar RD, Castrezana-Lopez L, Allam R, Kulkarni OP, Segerer S, Radomska E, et al. Bacterial lipopeptide triggers massive albuminuria in murine lupus nephritis by activating toll-like receptor 2 at the glomerular filtration barrier. Immunology (2009) 128(1 Suppl):e206–21.10.1111/j.1365-2567.2008.02948.x
    1. Leiss H, Niederreiter B, Bandur T, Schwarzecker B, Bluml S, Steiner G, et al. Pristane-induced lupus as a model of human lupus arthritis: evolvement of autoantibodies, internal organ and joint inflammation. Lupus (2013) 22(8):778–92.10.1177/0961203313492869
    1. Urbonaviciute V, Starke C, Pirschel W, Pohle S, Frey S, Daniel C, et al. Toll-like receptor 2 is required for autoantibody production and development of renal disease in pristane-induced lupus. Arthritis Rheum (2013) 65(6):1612–23.10.1002/art.37914
    1. Ma K, Li J, Fang Y, Lu L. Roles of B cell-intrinsic TLR signals in systemic lupus erythematosus. Int J Mol Sci (2015) 16(6):13084–105.10.3390/ijms160613084
    1. Gallo PM, Rapsinski GJ, Wilson RP, Oppong GO, Sriram U, Goulian M, et al. Amyloid-DNA composites of bacterial biofilms stimulate autoimmunity. Immunity (2015) 42(6):1171–84.10.1016/j.immuni.2015.06.002
    1. Gallucci S, Gallo P, Rapsinski G, Oppong G, Sriram U, Wilson R, et al. Bacterial amyloids promote type I interferon production and accelerate autoimmunity. AAI Annual Meeting (2015).
    1. Huang X, Li J, Dorta-Estremera S, Di Domizio J, Anthony SM, Watowich SS, et al. Neutrophils regulate humoral autoimmunity by restricting interferon-gamma production via the generation of reactive oxygen species. Cell Rep (2015) 12(7):1120–32.10.1016/j.celrep.2015.07.021
    1. Maldonado MA, Kakkanaiah V, MacDonald GC, Chen F, Reap EA, Balish E, et al. The role of environmental antigens in the spontaneous development of autoimmunity in MRL-lpr mice. J Immunol (1999) 162(11):6322–30.
    1. Van Praet JT, Donovan E, Vanassche I, Drennan MB, Windels F, Dendooven A, et al. Commensal microbiota influence systemic autoimmune responses. EMBO J (2015) 34(4):466–74.10.15252/embj.201489966
    1. Gaudreau MC, Johnson BM, Gudi R, Al-Gadban MM, Vasu C. Gender bias in lupus: does immune response initiated in the gut mucosa have a role? Clin Exp Immunol (2015) 180(3):393–407.10.1111/cei.12587
    1. Goldin BR, Gorbach SL. Clinical indications for probiotics: an overview. Clin Infect Dis (2008) 46(Suppl 2):S96–100.10.1086/523333
    1. Kaur IP, Kuhad A, Garg A, Chopra K. Probiotics: delineation of prophylactic and therapeutic benefits. J Med Food (2009) 12(2):219–35.10.1089/jmf.2007.0544
    1. Uskova MA, Kravchenko LV. [Antioxidant properties of lactic acid bacteria – probiotic and yogurt strains]. Vopr Pitan (2009) 78(2):18–23.
    1. Cain AM, Karpa KD. Clinical utility of probiotics in inflammatory bowel disease. Altern Ther Health Med (2011) 17(1):72–9.
    1. Lee J, Bang J, Woo HJ. Effect of orally administered Lactobacillus brevis HY7401 in a food allergy mouse model. J Microbiol Biotechnol (2013) 23(11):1636–40.10.4014/jmb.1306.06047
    1. Gomes AC, Bueno AA, de Souza RG, Mota JF. Gut microbiota, probiotics and diabetes. Nutr J (2014) 13:60.10.1186/1475-2891-13-60
    1. Cosenza L, Nocerino R, Di Scala C, di Costanzo M, Amoroso A, Leone L, et al. Bugs for atopy: the Lactobacillus rhamnosus GG strategy for food allergy prevention and treatment in children. Benef Microbes (2015) 6(2):225–32.10.3920/BM2014.0158
    1. Vong L, Lorentz RJ, Assa A, Glogauer M, Sherman PM. Probiotic Lactobacillus rhamnosus inhibits the formation of neutrophil extracellular traps. J Immunol (2014) 192(4):1870–7.10.4049/jimmunol.1302286
    1. Valladares R, Sankar D, Li N, Williams E, Lai KK, Abdelgeliel AS, et al. Lactobacillus johnsonii N6.2 mitigates the development of type 1 diabetes in BB-DP rats. PLoS One (2010) 5(5):e10507.10.1371/journal.pone.0010507
    1. Ejtahed HS, Mohtadi-Nia J, Homayouni-Rad A, Niafar M, Asghari-Jafarabadi M, Mofid V. Probiotic yogurt improves antioxidant status in type 2 diabetic patients. Nutrition (2012) 28(5):539–43.10.1016/j.nut.2011.08.013

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