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Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice.

Abstract

Environmental factors, including microbes and diet, play a key role in initiating autoimmunity in genetically predisposed individuals. However, the influence of gut microflora in the initiation and progression of systemic lupus erythematosus (SLE) is not well understood. In this study, we have examined the impact of drinking water pH on immune response, disease incidence and gut microbiome in a spontaneous mouse model of SLE. Our results show that (SWR × NZB) F1 (SNF1 ) mice that were given acidic pH water (AW) developed nephritis at a slower pace compared to those on neutral pH water (NW). Immunological analyses revealed that the NW-recipient mice carry relatively higher levels of circulating autoantibodies against nuclear antigen (nAg) as well as plasma cells. Importantly, 16S rRNA gene-targeted sequencing revealed that the composition of gut microbiome is significantly different between NW and AW groups of mice. In addition, analysis of cytokine and transcription factor expression revealed that immune response in the gut mucosa of NW recipient mice is dominated by T helper type 17 (Th17) and Th9-associated factors. Segmented filamentous bacteria (SFB) promote a Th17 response and autoimmunity in mouse models of arthritis and multiple sclerosis. Interestingly, however, not only was SFB colonization unaffected by the pH of drinking water, but also SFB failed to cause a profound increase in Th17 response and had no significant effect on lupus incidence. Overall, these observations show that simple dietary deviations such as the pH of drinking water can influence lupus incidence and affect the composition of gut microbiome.

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  • Authors+Show Affiliations

    ,

    Departments of Microbiology and Immunology.

    ,

    Departments of Microbiology and Immunology.

    ,

    Departments of Microbiology and Immunology.

    ,

    Departments of Microbiology and Immunology.

    Departments of Microbiology and Immunology. Departments of Surgery, College of Medicine, Medical University of South Carolina, Charleston, SC, USA.

    Source

    Clinical and experimental immunology 181:2 2015 Aug pg 323-37

    MeSH

    Animals
    Antibodies, Antinuclear
    Bacteroides
    Clostridium
    Crosses, Genetic
    Cyanobacteria
    Cytokines
    Disease Progression
    Drinking Water
    Female
    Gastrointestinal Tract
    Genetic Predisposition to Disease
    Hydrogen-Ion Concentration
    Lactobacillus
    Lupus Nephritis
    Male
    Mice
    Mice, Inbred NZB
    Microbiota
    Plasma Cells
    RNA, Ribosomal, 16S
    Th17 Cells
    Time Factors

    Pub Type(s)

    Journal Article
    Research Support, N.I.H., Extramural
    Research Support, Non-U.S. Gov't

    Language

    eng

    PubMed ID

    25703185

    Citation

    Johnson, B M., et al. "Impact of Dietary Deviation On Disease Progression and Gut Microbiome Composition in Lupus-prone SNF1 Mice." Clinical and Experimental Immunology, vol. 181, no. 2, 2015, pp. 323-37.
    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):323-37.
    Johnson, B. M., Gaudreau, M. C., Al-Gadban, M. M., Gudi, R., & Vasu, C. (2015). Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice. Clinical and Experimental Immunology, 181(2), pp. 323-37. doi:10.1111/cei.12609.
    Johnson BM, et al. Impact of Dietary Deviation On Disease Progression and Gut Microbiome Composition in Lupus-prone SNF1 Mice. Clin Exp Immunol. 2015;181(2):323-37. PubMed PMID: 25703185.
    * Article titles in AMA citation format should be in sentence-case
    TY - JOUR T1 - Impact of dietary deviation on disease progression and gut microbiome composition in lupus-prone SNF1 mice. AU - Johnson,B M, AU - Gaudreau,M-C, AU - Al-Gadban,M M, AU - Gudi,R, AU - Vasu,C, PY - 2014/10/02/received PY - 2015/01/23/revised PY - 2015/02/17/accepted PY - 2015/2/24/entrez PY - 2015/2/24/pubmed PY - 2015/10/1/medline KW - autoimmunity KW - drinking water pH KW - immune modulation KW - microbiota KW - segmented filamentous bacteria KW - systemic lupus erythematosus SP - 323 EP - 37 JF - Clinical and experimental immunology JO - Clin. Exp. Immunol. VL - 181 IS - 2 N2 - Environmental factors, including microbes and diet, play a key role in initiating autoimmunity in genetically predisposed individuals. However, the influence of gut microflora in the initiation and progression of systemic lupus erythematosus (SLE) is not well understood. In this study, we have examined the impact of drinking water pH on immune response, disease incidence and gut microbiome in a spontaneous mouse model of SLE. Our results show that (SWR × NZB) F1 (SNF1 ) mice that were given acidic pH water (AW) developed nephritis at a slower pace compared to those on neutral pH water (NW). Immunological analyses revealed that the NW-recipient mice carry relatively higher levels of circulating autoantibodies against nuclear antigen (nAg) as well as plasma cells. Importantly, 16S rRNA gene-targeted sequencing revealed that the composition of gut microbiome is significantly different between NW and AW groups of mice. In addition, analysis of cytokine and transcription factor expression revealed that immune response in the gut mucosa of NW recipient mice is dominated by T helper type 17 (Th17) and Th9-associated factors. Segmented filamentous bacteria (SFB) promote a Th17 response and autoimmunity in mouse models of arthritis and multiple sclerosis. Interestingly, however, not only was SFB colonization unaffected by the pH of drinking water, but also SFB failed to cause a profound increase in Th17 response and had no significant effect on lupus incidence. Overall, these observations show that simple dietary deviations such as the pH of drinking water can influence lupus incidence and affect the composition of gut microbiome. SN - 1365-2249 UR - https://www.unboundmedicine.com/medline/citation/25703185/Impact_of_dietary_deviation_on_disease_progression_and_gut_microbiome_composition_in_lupus_prone_SNF1_mice_ L2 - https://doi.org/10.1111/cei.12609 DB - PRIME DP - Unbound Medicine ER -