Literature DB >> 35810689

Staphylococcus aureus peptidoglycan (PGN) induces pathogenic autoantibody production via autoreactive B cell receptor clonal selection, implications in systemic lupus erythematosus.

Wangbin Ning1, Da Cheng2, Philip H Howe3, Chuanxiu Bian4, Diane L Kamen5, Zhenwu Luo4, Xiaoyu Fu2, Elizabeth Ogunrinde4, Liuqing Yang6, Xu Wang7, Quan-Zhen Li8, Jim Oates9, Weiru Zhang10, David White11, Zhuang Wan4, Gary S Gilkeson12, Wei Jiang13.   

Abstract

OBJECTIVES: There is an intricate interplay between the microbiome and the immune response impacting development of normal immunity and autoimmunity. However, we do not fully understand how the microbiome affects production of natural-like and pathogenic autoantibodies. Peptidoglycan (PGN) is a component of the bacterial cell wall which is highly antigenic. PGNs from different bacteria can differ in their immune regulatory activities.
METHODS: C57BL/6 and MRL/lpr mice were intraperitoneally injected with saline or PGN from Staphylococcus aureus or Bacillus subtilis. Spleen anti-double-stranded DNA (dsDNA) IgG + B cells were sorted for B-cell receptor sequencing. Serum autoantibody levels and kidney damage were analyzed. Further, the association between plasma S. aureus translocation and systemic lupus erythematosus (SLE) pathogenesis was assessed in women.
RESULTS: Administration of B. subtilis PGN induced natural-like anti-dsDNA autoantibodies (e.g., IgM, short lived IgG response, and no tissue damage), whereas S. aureus PGN induced pathogenic anti-dsDNA autoantibodies (e.g., prolonged IgG production, low IgM, autoantibody-mediated kidney damage) in C57BL/6 and/or MRL/lpr mice. However, serum total IgG did not differ. S. aureus PGN induced antibodies with reduced clonality and greater hypermutation of IGHV3-74 in splenic anti-dsDNA IgG + B cells from C57BL/6 mice. Further, S. aureus PGN promoted IgG class switch recombination via toll-like receptor 2. Plasma S. aureus DNA levels were increased in women with SLE versus control women and correlated with levels of lupus-related autoantibodies and renal involvement.
CONCLUSIONS: S. aureus PGN induces pathogenic autoantibody production, whereas B. subtilis PGN drives production of natural nonpathogenic autoantibodies. Published by Elsevier Ltd.

Entities:  

Keywords:  Autoantibody; Class switch recombination; Peptidoglycan; Staphylococcus aureus; Systemic lupus erythematosus

Mesh:

Substances:

Year:  2022        PMID: 35810689      PMCID: PMC9397544          DOI: 10.1016/j.jaut.2022.102860

Source DB:  PubMed          Journal:  J Autoimmun        ISSN: 0896-8411            Impact factor:   14.511


  45 in total

1.  The predictive value of fluctuations in IgM and IgG class anti-dsDNA antibodies for relapses in systemic lupus erythematosus. A prospective long-term observation.

Authors:  H Bootsma; P E Spronk; E J Ter Borg; E J Hummel; G de Boer; P C Limburg; C G Kallenberg
Journal:  Ann Rheum Dis       Date:  1997-11       Impact factor: 19.103

2.  A Link Between Plasma Microbial Translocation, Microbiome, and Autoantibody Development in First-Degree Relatives of Systemic Lupus Erythematosus Patients.

Authors:  Elizabeth Ogunrinde; Zejun Zhou; Zhenwu Luo; Alexander Alekseyenko; Quan-Zhen Li; Danielle Macedo; Diane L Kamen; Jim C Oates; Gary S Gilkeson; Wei Jiang
Journal:  Arthritis Rheumatol       Date:  2019-09-27       Impact factor: 10.995

3.  Presentation of soluble antigens to CD8+ T cells by CpG oligodeoxynucleotide-primed human naive B cells.

Authors:  Wei Jiang; Michael M Lederman; Clifford V Harding; Scott F Sieg
Journal:  J Immunol       Date:  2011-01-14       Impact factor: 5.422

Review 4.  Molecular and cellular basis for pathogenicity of autoantibodies: lessons from murine monoclonal autoantibodies.

Authors:  Lucie Baudino; Samareh Azeredo da Silveira; Munehiro Nakata; Shozo Izui
Journal:  Springer Semin Immunopathol       Date:  2006-09-05

5.  Commercial peptidoglycan preparations are contaminated with superantigen-like activity that stimulates IL-17 production.

Authors:  Hanfen Li; Mohammed M Nooh; Malak Kotb; Fabio Re
Journal:  J Leukoc Biol       Date:  2007-11-08       Impact factor: 4.962

6.  Differential contribution of three activating IgG Fc receptors (FcgammaRI, FcgammaRIII, and FcgammaRIV) to IgG2a- and IgG2b-induced autoimmune hemolytic anemia in mice.

Authors:  Lucie Baudino; Falk Nimmerjahn; Samareh Azeredo da Silveira; Eduardo Martinez-Soria; Takashi Saito; Michael Carroll; Jeffrey V Ravetch; J Sjef Verbeek; Shozo Izui
Journal:  J Immunol       Date:  2008-02-01       Impact factor: 5.422

7.  Anti-DNA antibodies from autoimmune mice arise by clonal expansion and somatic mutation.

Authors:  M Shlomchik; M Mascelli; H Shan; M Z Radic; D Pisetsky; A Marshak-Rothstein; M Weigert
Journal:  J Exp Med       Date:  1990-01-01       Impact factor: 14.307

8.  Association between Staphylococcus aureus nasal carriage and disease phenotype in patients affected by systemic lupus erythematosus.

Authors:  Fabrizio Conti; Fulvia Ceccarelli; Giancarlo Iaiani; Carlo Perricone; Alessandra Giordano; Luigino Amori; Francesca Miranda; Laura Massaro; Viviana Antonella Pacucci; Simona Truglia; Gabriella Girelli; Azis Fakeri; Gloria Taliani; Chiara Temperoni; Francesca Romana Spinelli; Cristiano Alessandri; Guido Valesini
Journal:  Arthritis Res Ther       Date:  2016-07-30       Impact factor: 5.156

9.  Systemic translocation of Staphylococcus drives autoantibody production in HIV disease.

Authors:  Zhenwu Luo; Min Li; Yongxia Wu; Zhefeng Meng; Lisa Martin; Lumin Zhang; Elizabeth Ogunrinde; Zejun Zhou; Shenghui Qin; Zhuang Wan; Maria Anna Julia Westerink; Stephanie Warth; Hui Liu; Ping Jin; David Stroncek; Quan-Zhen Li; Ena Wang; Xueling Wu; Sonya L Heath; Zihai Li; Alexander V Alekseyenko; Wei Jiang
Journal:  Microbiome       Date:  2019-02-14       Impact factor: 14.650

10.  Reduction of lupus nephritis in MRL/lpr mice by a bacterial superantigen treatment.

Authors:  C Kim; K A Siminovitch; A Ochi
Journal:  J Exp Med       Date:  1991-12-01       Impact factor: 14.307

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