Literature DB >> 34725967

Host Genetics But Not Commensal Microbiota Determines the Initial Development of Systemic Autoimmune Disease in BXD2 Mice.

Huixian Hong1, Fatima Alduraibi1, David Ponder1, Wayne L Duck1, Casey D Morrow1, Jeremy B Foote1, Trenton R Schoeb1, Huma Fatima1, Charles O Elson1, Hui-Chen Hsu1, John D Mountz2.   

Abstract

OBJECTIVE: To determine the extent to which the gut microbiome influences systemic autoimmunity in a mouse model of lupus.
METHODS: We generated germ-free (GF) lupus-prone BXD2 mice, which under normal conditions develop spontaneous germinal centers (GCs) and high titers of serum autoantibodies. GF status was confirmed by gut bacterial culture. The autoimmune phenotypes of 6- and 12-month-old gnotobiotic GF BXD2 mice and specific pathogen-free (SPF) BXD2 mice were compared. Serum levels of autoantibodies were measured by enzyme-linked immunosorbent assay. Histologic sections of the mouse kidney and joints were evaluated. Flow cytometry was used to analyze GCs and age-associated B cells. CD4+ T cells were analyzed for PD-1+ICOS+ activated T cells, T follicular regulatory (Tfr) cells (Foxp3+CD25+ PD-1+CXCR5+), and PD-1+ICOS+ T cells expressing interleukin-17A (IL-17A) or interferon-γ (IFNγ) after stimulation with phorbol myristate acetate (PMA)/ionomycin.
RESULTS: In 6-month-old mice, GF status did not affect splenomegaly, GC B cells, age-associated B cells, or serum autoantibody levels, except for IgG antihistone. GF BXD2 mice exhibited a significantly higher percentage of Tfr cells compared to their SPF counterparts (P < 0.05). At 12 months of age, however, GF BXD2 mice had significantly diminished IgG autoantibody levels and a lower percentage of GC B cells and age-associated B cells (P < 0.05). Following stimulation with PMA/ionomycin, PD-1+ICOS+ CD4+ T cells expressed significantly lower IL-17A, but not IFNγ, levels in GF BXD2 mice compared to SPF BXD2 mice (P < 0.01). SPF BXD2 mice and GF BXD2 mice developed equivalent renal and joint disease with no significant differences in severity.
CONCLUSION: Our results suggest a model in which genetics plays a dominant role in determining the initial development of autoimmunity. In contrast, gut microbiomes may regulate the persistence of certain aspects of systemic autoimmunity.
© 2021 American College of Rheumatology.

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Year:  2022        PMID: 34725967      PMCID: PMC9071869          DOI: 10.1002/art.42008

Source DB:  PubMed          Journal:  Arthritis Rheumatol        ISSN: 2326-5191            Impact factor:   10.995


  18 in total

1.  The role of environmental antigens in the spontaneous development of autoimmunity in MRL-lpr mice.

Authors:  M A Maldonado; V Kakkanaiah; G C MacDonald; F Chen; E A Reap; E Balish; W R Farkas; J C Jennette; M P Madaio; B L Kotzin; P L Cohen; R A Eisenberg
Journal:  J Immunol       Date:  1999-06-01       Impact factor: 5.422

2.  Intestinal bacterial colonization induces mutualistic regulatory T cell responses.

Authors:  Markus B Geuking; Julia Cahenzli; Melissa A E Lawson; Derek C K Ng; Emma Slack; Siegfried Hapfelmeier; Kathy D McCoy; Andrew J Macpherson
Journal:  Immunity       Date:  2011-05-19       Impact factor: 31.745

3.  Dynamics of gut microbiota in autoimmune lupus.

Authors:  Husen Zhang; Xiaofeng Liao; Joshua B Sparks; Xin M Luo
Journal:  Appl Environ Microbiol       Date:  2014-09-26       Impact factor: 4.792

4.  Alteration in gut microbiota is associated with dysregulation of cytokines and glucocorticoid therapy in systemic lupus erythematosus.

Authors:  Mengchen Guo; Huixia Wang; Sixie Xu; Yaoyao Zhuang; Jingang An; Chuan Su; Yankai Xia; Jingyun Chen; Zhenjiang Zech Xu; Qisha Liu; Jianwei Wang; Zhou Dan; Kun Chen; Xiaoting Luan; Zhi Liu; Kangjian Liu; Faming Zhang; Yumin Xia; Xingyin Liu
Journal:  Gut Microbes       Date:  2020-06-07

5.  Disparate T cell requirements of two subsets of lupus-specific autoantibodies in pristane-treated mice.

Authors:  H B Richards; M Satoh; J C Jennette; T Okano; Y S Kanwar; W H Reeves
Journal:  Clin Exp Immunol       Date:  1999-03       Impact factor: 4.330

6.  Excessive CD11c+Tbet+ B cells promote aberrant TFH differentiation and affinity-based germinal center selection in lupus.

Authors:  Wenqian Zhang; Huihui Zhang; Shujun Liu; Fucan Xia; Zijian Kang; Yan Zhang; Yaoyang Liu; Hui Xiao; Lei Chen; Chuanxin Huang; Nan Shen; Huji Xu; Fubin Li
Journal:  Proc Natl Acad Sci U S A       Date:  2019-08-26       Impact factor: 11.205

7.  Genetic segregation of spontaneous erosive arthritis and generalized autoimmune disease in the BXD2 recombinant inbred strain of mice.

Authors:  J D Mountz; P Yang; Q Wu; J Zhou; A Tousson; A Fitzgerald; J Allen; X Wang; S Cartner; W E Grizzle; N Yi; L Lu; R W Williams; H-C Hsu
Journal:  Scand J Immunol       Date:  2005-02       Impact factor: 3.487

8.  IL-17RA is essential for optimal localization of follicular Th cells in the germinal center light zone to promote autoantibody-producing B cells.

Authors:  Yanna Ding; Jun Li; Qi Wu; Pingar Yang; Bao Luo; Shutao Xie; Kirk M Druey; Allan J Zajac; Hui-Chen Hsu; John D Mountz
Journal:  J Immunol       Date:  2013-07-15       Impact factor: 5.422

9.  Interleukin 17-producing T helper cells and interleukin 17 orchestrate autoreactive germinal center development in autoimmune BXD2 mice.

Authors:  Hui-Chen Hsu; PingAr Yang; John Wang; Qi Wu; Riley Myers; Jian Chen; John Yi; Tanja Guentert; Albert Tousson; Andrea L Stanus; Thuc-vy L Le; Robin G Lorenz; Hui Xu; Jay K Kolls; Robert H Carter; David D Chaplin; Robert W Williams; John D Mountz
Journal:  Nat Immunol       Date:  2007-12-23       Impact factor: 25.606

10.  Specific microbiota direct the differentiation of IL-17-producing T-helper cells in the mucosa of the small intestine.

Authors:  Ivaylo I Ivanov; Rosa de Llanos Frutos; Nicolas Manel; Keiji Yoshinaga; Daniel B Rifkin; R Balfour Sartor; B Brett Finlay; Dan R Littman
Journal:  Cell Host Microbe       Date:  2008-10-16       Impact factor: 21.023

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  1 in total

Review 1.  Gut Microbiota, Leaky Gut, and Autoimmune Diseases.

Authors:  Anna Christovich; Xin M Luo
Journal:  Front Immunol       Date:  2022-06-27       Impact factor: 8.786

  1 in total

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