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Microbial Ecology

Gut Microbiota in Human Systemic Lupus Erythematosus and a Mouse Model of Lupus

Xin M. Luo, Michael R. Edwards, Qinghui Mu, Yang Yu, Miranda D. Vieson, Christopher M. Reilly, S. Ansar Ahmed, Adegbenga A. Bankole
Andrew J. McBain, Editor
Xin M. Luo
Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA
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  • ORCID record for Xin M. Luo
Michael R. Edwards
Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA
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Qinghui Mu
Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA
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Yang Yu
Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, California, USA
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Miranda D. Vieson
Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA
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Christopher M. Reilly
Edward Via College of Osteopathic Medicine, Blacksburg, Virginia, USA
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S. Ansar Ahmed
Department of Biomedical Sciences and Pathobiology, Virginia-Maryland College of Veterinary Medicine, Virginia Tech, Blacksburg, Virginia, USA
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Adegbenga A. Bankole
Virginia Tech Carilion School of Medicine, Roanoke, Virginia, USA
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Andrew J. McBain
University of Manchester
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DOI: 10.1128/AEM.02288-17
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  • FIG 1
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    FIG 1

    Dynamics of the gut microbiota in NZB/W F1 mice. Fecal pellets were collected at 10, 14, and 18 weeks of age (predisease time points; n = 5 per time point) and 23, 28, and 33 weeks of age (post-disease-onset time points; n = 3 or 4 per time point) and were subjected to 16S rRNA sequencing analysis. The disease onset in NZB/W F1 mice is ∼20 weeks of age. (A) PCoA plot, showing alterations of overall community structures (P < 0.01). (B) Bacterial diversity, as indicated by the number of OTUs. The increase of OTUs from the pre-disease-onset stage to the post-disease-onset stages was significant (P < 0.01). (C) Time-dependent changes in the relative abundance of different bacterial species. Smoothing was performed with the ggplot2 package, using locally weighted regression. In all figures, P values were corrected for multiple comparisons by controlling the FDRs.

  • FIG 2
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    FIG 2

    Changes in the gut microbiota in NZB/W F1 mice in response to immunosuppressant (Dex) treatment. NZB/W F1 mice were treated with 2 mg/kg body weight Dex (intraperitoneal injections five times per week) from 20 to 34 weeks of age. Fecal pellets were collected at 34 weeks of age and subjected to 16S rRNA sequencing analysis. (A) PCoA plot, showing the separation of overall bacterial structures (P < 0.01). (B) Bacterial diversity, as indicated by the Shannon index (P < 0.001). (C) Identification of a bacterial species for which there was a significant change from the pre-disease-onset stage (pre) to the post-disease-onset stage (post) and Dex treatment significantly reversed the change (P < 0.01 in both cases). Ctr, control. (D) Spearman correlation analysis between the abundance (shown as a proportion, where, e.g., 0.2 represents 20%) of the bacterial species (Lacto [Lactobacillaceae, Lactobacillus, other]) identified in panel C and two measurements of the SLE disease state, i.e., renal function (RenalFunc) and systemic autoimmunity (SysAuto). See Materials and Methods for calculation of these two measurements.

  • FIG 3
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    FIG 3

    Gut microbiota dysbiosis in SLE patients with active disease, compared to non-SLE controls. The inclusion and exclusion criteria are listed in Materials and Methods. A fecal sample was collected from each patient or control subject at the time of the first visit, and the samples were subjected to 16S rRNA sequencing analysis. (A) PCoA plot, showing no separation of overall bacterial structures (P > 0.05). (B) Significant difference in bacterial diversity levels, as indicated by the Shannon index (P < 0.05). (C) No significant difference in Firmicutes/Bacteroidetes (FB) ratios (P > 0.05). (D) Significant difference in the relative abundance of the phylum Proteobacteria, a representation of facultative anaerobic Gram-negative bacteria (P < 0.05). (E) Significant changes in several bacterial species, with the P values indicated (nonparametric Mann-Whitney test). DESeq2 analysis was also performed, and the DESeq2 P values were 0.037, 0.007, and 0.007, respectively. P values were corrected for multiple comparisons by controlling the FDRs.

Tables

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  • TABLE 1

    Differentially represented bacterial species between SLE and non-SLE individuals

    Bacterial speciesStrain nameOTU no.Sequence identity (%)SLE vs non-SLE
    Blautia wexleraeAUH-JLD177100Increased
    Blautia wexleraeAUH-JLD567100Increased
    Blautia sp. strain MarseilleP36027100Increased
    Blautia sp. strain GD823100Increased
    Blautia faecisM2525100Increased
    Blautia caecimurisSJ1849299Increased
    Blautia sp. strain AUH-JLD358598Increased
    Blautia sp. strain MarseilleP338758598Increased
    Odoribacter laneusJCM63100Decreased
    Odoribacter laneusYIT63100Decreased
    Odoribacter laneusJCM63100Decreased
    Odoribacter splanchnicus67100Decreased
    Alistipes onderdonkii13100Decreased
    Alistipes sp.LS-J13100Decreased
    Alistipes sp.LS-M13100Decreased
    Alistipes shahiiWAL 8301164100Decreased
    Alistipes obesiph8164100Decreased
    Alistipes ihumiiAP11188100Decreased
    Alistipes sp. strain cv1188/210100Decreased
    Alistipes indistinctusJCM188/252100Decreased
    Alistipes indistinctusYIT188/252100Decreased
    Alistipes sp. strain S216252100Decreased
    Alistipes finegoldiiDSM 1724239899Decreased
    Alistipes finegoldiiJCM 1677039899Decreased
    Alistipes finegoldiiCIP 10799939899Decreased
    Alistipes finegoldiiAHN 243739899Decreased
  • TABLE 2

    Demographic, immunological, and clinical features of SLE patients

    Subject no.Age (yr)SexaRacebImmunological featurescClinical symptomsdSLEDAI scoreBMI (kg/m2)eMedication(s)f
    0139FAAANA, dsDNA, C3, C4, hemCL, PS036.6HCQ, belimumab
    0221FCaucasianANA, dsDNA, sm, C3, C4, hemAlopecia, LN, PS, Neuro836.4HCQ, MMF, belimumab
    0340FCaucasianANA, C3, C4, hemAlopecia, SE321.5HCQ, MMF, belimumab
    0464FAAANA, C3, C4Alopecia, MR, PS631.4HCQ, MMF, belimumab
    0565FCaucasianANA, dsDNA, C3, C4LN1326.2HCQ, MMF
    0641MCaucasianANA, dsDNA, C3LN, PS, IA243.5MTX
    0727MAAANA, dsDNA, sm, ACL, C3, C4MR, LN631.6HCQ, MMF
    0956FCaucasianANA, dsDNA, hemPS136.5HCQ, MMF, belimumab
    1025FCaucasianANA, dsDNA, ACL, B2G, C3, C4MR, LN, PS839.1HCQ, MMF, rituximab
    1173FCaucasianANA, smSE018.4HCQ, MMF
    1723MCaucasianANA, dsDNA, hemLN221.0HCQ, AZA
    1936MCaucasianANA, dsDNA, sm, C4, hemMR, SE037.2HCQ, MMF
    2029FAAANA, dsDNA, sm, C3, C4MR, IA233.9HCQ
    2366FCaucasianANA, dsDNA, hemNone033.2HCQ, AZA, tacrolimus
    • ↵a F, female; M, male.

    • ↵b Race categories were African American (not Caribbean) (AA) and Caucasian, non-Hispanic.

    • ↵c Immunological features included antinuclear antibodies (ANA), anti-dsDNA antibodies (dsDNA), anti-Smith antibodies (sm), anticardiolipin antibodies (ACL), β2-glycoprotein (B2G), lupus anticoagulant (LAC), complement C3 (C3), complement C4 (C4), and hematological manifestation (hem).

    • ↵d Clinical symptoms included alopecia, cutaneous lupus (CL), malar rash (MR), lupus nephritis (LN), photosensitivity (PS), inflammatory arthritis (IA), serositis (SE), and neurolupus (Neuro).

    • ↵e BMI, body mass index.

    • ↵f Medications included hydroxychloroquine (HCQ), mycophenolate mofetil (MMF), methotrexate (MTX), azathioprine (AZA), belimumab, rituximab, and tacrolimus.

Additional Files

  • Figures
  • Tables
  • Supplemental material

    • Supplemental file 1 -

      PCA plot with age and cage as separating factors (Fig. S1); species richness (Fig. S2).

      PDF, 56K

    • Supplemental file 2 -

      OTU table (NZB/W F1 mice over time).

      XLSX, 108K

    • Supplemental file 3 -

      OTU table (Dex vs. control).

      XLSX, 102K

    • Supplemental file 4 -

      OTU table (SLE vs. non-SLE).

      XLSX, 104K

    • Supplemental file 5 -

      Complete list of all taxa tested for differential abundance (P values; predisease vs. postdisease).

      XLSX, 58K

    • Supplemental file 6 -

      Complete list of all taxa tested for differential abundance (P values; Dex vs. control).

      XLSX, 59K

    • Supplemental file 7 -

      Complete list of all taxa tested for differential abundance (P values; SLE vs. non-SLE).

      XLSX, 60K

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Gut Microbiota in Human Systemic Lupus Erythematosus and a Mouse Model of Lupus
Xin M. Luo, Michael R. Edwards, Qinghui Mu, Yang Yu, Miranda D. Vieson, Christopher M. Reilly, S. Ansar Ahmed, Adegbenga A. Bankole
Appl. Environ. Microbiol. Jan 2018, 84 (4) e02288-17; DOI: 10.1128/AEM.02288-17

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Gut Microbiota in Human Systemic Lupus Erythematosus and a Mouse Model of Lupus
Xin M. Luo, Michael R. Edwards, Qinghui Mu, Yang Yu, Miranda D. Vieson, Christopher M. Reilly, S. Ansar Ahmed, Adegbenga A. Bankole
Appl. Environ. Microbiol. Jan 2018, 84 (4) e02288-17; DOI: 10.1128/AEM.02288-17
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KEYWORDS

lupus
microbiota

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