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An Alternative Role of C1q in Bacterial Infections: Facilitating Streptococcus pneumoniae Adherence and Invasion of Host Cells

Vaibhav Agarwal, Jonas Ahl, Kristian Riesbeck and Anna M. Blom
J Immunol October 15, 2013, 191 (8) 4235-4245; DOI: https://doi.org/10.4049/jimmunol.1300279
Vaibhav Agarwal
*Medical Protein Chemistry, Department of Laboratory Medicine Malmö, Lund University, SE-205 02 Malmö, Sweden; and
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Jonas Ahl
†Medical Microbiology, Department of Laboratory Medicine Malmö, Lund University, SE-205 02 Malmö, Sweden
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Kristian Riesbeck
†Medical Microbiology, Department of Laboratory Medicine Malmö, Lund University, SE-205 02 Malmö, Sweden
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Anna M. Blom
*Medical Protein Chemistry, Department of Laboratory Medicine Malmö, Lund University, SE-205 02 Malmö, Sweden; and
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Abstract

Streptococcus pneumoniae (pneumococcus) is a major human pathogen, which evolved numerous successful strategies to colonize the host. In this study, we report a novel mechanism of pneumococcal–host interaction, whereby pneumococci use a host complement protein C1q, primarily involved in the host-defense mechanism, for colonization and subsequent dissemination. Using cell-culture infection assays and confocal microscopy, we observed that pneumococcal surface-bound C1q significantly enhanced pneumococcal adherence to and invasion of host epithelial and endothelial cells. Flow cytometry demonstrated a direct, Ab-independent binding of purified C1q to various clinical isolates of pneumococci. This interaction was seemingly capsule serotype independent and mediated by the bacterial surface-exposed proteins, as pretreatment of pneumococci with pronase E but not sodium periodate significantly reduced C1q binding. Moreover, similar binding was observed using C1 complex as the source of C1q. Furthermore, our data show that C1q bound to the pneumococcal surface through the globular heads and with the host cell-surface receptor(s)/glycosaminoglycans via its N-terminal collagen-like stalk, as the presence of C1q N-terminal fragment and low m.w. heparin but not the C-terminal globular heads blocked C1q-mediated pneumococcal adherence to host cells. Taken together, we demonstrate for the first time, to our knowledge, a unique function of complement protein C1q, as a molecular bridge between pneumococci and the host, which promotes bacterial cellular adherence and invasion. Nevertheless, in some conditions, this mechanism could be also beneficial for the host as it may result in uptake and clearance of the bacteria.

This article is featured in In This Issue, p.3971

Footnotes

  • This work was supported by grants from the Swedish Research Council (K2012-66X-14928-09-5), the National Board of Health and Welfare, Foundations of Österlund, Greta and Johan Kock, King Gustav V's 80th Anniversary, Knut and Alice Wallenberg, Inga-Britt and Arne Lundberg, and Torsten and Ragnar Söderberg, the Royal Physiographic Society in Lund, and a grant from the Skåne University Hospital. V.A. is the recipient of a postdoctoral stipend from the Swedish Society for Medical Research. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

  • Abbreviations used in this article:

    C4BP
    C4b-binding protein
    CPS
    capsular polysaccharide
    CRP
    C-reactive protein
    FH
    factor H
    GMFI
    geometric mean fluorescence intensity
    GVB++
    gelatin-veronal buffer
    HBEpC
    primary human bronchial epithelial cell
    NHS
    normal human serum
    THY
    Todd-Hewitt-Yeast extract broth.

  • Received January 28, 2013.
  • Accepted August 15, 2013.
  • Copyright © 2013 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 191 (8)
The Journal of Immunology
Vol. 191, Issue 8
15 Oct 2013
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An Alternative Role of C1q in Bacterial Infections: Facilitating Streptococcus pneumoniae Adherence and Invasion of Host Cells
Vaibhav Agarwal, Jonas Ahl, Kristian Riesbeck, Anna M. Blom
The Journal of Immunology October 15, 2013, 191 (8) 4235-4245; DOI: 10.4049/jimmunol.1300279

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An Alternative Role of C1q in Bacterial Infections: Facilitating Streptococcus pneumoniae Adherence and Invasion of Host Cells
Vaibhav Agarwal, Jonas Ahl, Kristian Riesbeck, Anna M. Blom
The Journal of Immunology October 15, 2013, 191 (8) 4235-4245; DOI: 10.4049/jimmunol.1300279
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