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Vigorous Response of Human Innate Functioning IgM Memory B Cells upon Infection by Neisseria gonorrhoeae

Nancy S. Y. So, Mario A. Ostrowski and Scott D. Gray-Owen
J Immunol April 15, 2012, 188 (8) 4008-4022; DOI: https://doi.org/10.4049/jimmunol.1100718
Nancy S. Y. So
*Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada; and
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Mario A. Ostrowski
†Clinical Sciences Division, University of Toronto, Toronto, Ontario M5S 1A8, Canada
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Scott D. Gray-Owen
*Department of Molecular Genetics, University of Toronto, Toronto, Ontario M5S 1A8, Canada; and
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Abstract

Neisseria gonorrhoeae, the cause of the sexually transmitted infection gonorrhea, elicits low levels of specific Ig that decline rapidly after the bacteria are cleared. Reinfection with the same serovar can occur, and prior gonococcal infection does not alter the Ig response upon subsequent exposure, suggesting that protective immunity is not induced. The mucosal Ig response apparent during gonorrhea does not correlate with that observed systemically, leading to a suggestion that it is locally generated. In considering whether N. gonorrhoeae directly influences B cells, we observed that gonococcal infection prolonged viability of primary human B cells in vitro and elicited robust activation and vigorous proliferative responses in the absence of T cells. Furthermore, we observed the specific expansion of IgD+CD27+ B cells in response to gonococcal infection. These cells are innate in function, conferring protection against diverse microbes by producing low-affinity, broadly reactive IgM without inducing classical immunologic memory. Although gonococcal infection of B cells produced small amounts of gonococcal-specific IgM, IgM specific for irrelevant Ags were also produced, suggesting a broad, polyspecific Ig response. The gonococci were effectively bound and engulfed by B cells. TLR9-inhibitory CpGs blocked B cell responses, indicating that intracellular bacterial degradation allows for innate immune detection within the phagolysosome. To our knowledge, this is the first report of a bacterial pathogen having specific affinity for the human IgM memory B cells, driving their potent activation and polyclonal Ig response. This unfocused T-independent response explains the localized Ig response that occurs, despite an absence of immunologic memory elicited during gonorrhea.

Footnotes

  • This work was supported by Canadian Institute of Health Research Operating Grant 414775.

  • The online version of this article contains supplemental material.

  • Abbreviations used in this article:

    CEA
    carcinoembryonic Ag
    CEACAM
    carcinoembryonic Ag-related cell adhesion molecule
    HSPG
    heparin sulphate proteoglycan
    iCpG
    inhibitory CpG ODN TTAGGG
    KLH
    keyhole limpet hemocyanin
    MAMP
    microbial-associated molecular pattern
    MOI
    multiplicity of infection
    ODN
    oligodeoxynucleotide
    OpaCEA
    carcinoembryonic Ag-related cell adhesion molecule-specific Opa
    OpaHSPG
    heparan sulfate proteoglycan-specific Opa
    TT
    tetanus toxoid.

  • Received March 11, 2011.
  • Accepted February 15, 2012.
  • Copyright © 2012 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 188 (8)
The Journal of Immunology
Vol. 188, Issue 8
15 Apr 2012
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Vigorous Response of Human Innate Functioning IgM Memory B Cells upon Infection by Neisseria gonorrhoeae
Nancy S. Y. So, Mario A. Ostrowski, Scott D. Gray-Owen
The Journal of Immunology April 15, 2012, 188 (8) 4008-4022; DOI: 10.4049/jimmunol.1100718

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Vigorous Response of Human Innate Functioning IgM Memory B Cells upon Infection by Neisseria gonorrhoeae
Nancy S. Y. So, Mario A. Ostrowski, Scott D. Gray-Owen
The Journal of Immunology April 15, 2012, 188 (8) 4008-4022; DOI: 10.4049/jimmunol.1100718
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