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Staphylococcus aureus Metalloprotease Aureolysin Cleaves Complement C3 To Mediate Immune Evasion

Alexander J. Laarman, Maartje Ruyken, Cheryl L. Malone, Jos A. G. van Strijp, Alexander R. Horswill and Suzan H. M. Rooijakkers
J Immunol April 18, 2011, 1002948; DOI: https://doi.org/10.4049/jimmunol.1002948
Alexander J. Laarman
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Maartje Ruyken
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Cheryl L. Malone
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Jos A. G. van Strijp
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Alexander R. Horswill
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Suzan H. M. Rooijakkers
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Abstract

Complement is one of the first host defense barriers against bacteria. Activated complement attracts neutrophils to the site of infection and opsonizes bacteria to facilitate phagocytosis. The human pathogen Staphylococcus aureus has successfully developed ways to evade the complement system, for example by secretion of specific complement inhibitors. However, the influence of S. aureus proteases on the host complement system is still poorly understood. In this study, we identify the metalloprotease aureolysin as a potent complement inhibitor. Aureolysin effectively inhibits phagocytosis and killing of bacteria by neutrophils. Furthermore, we show that aureolysin inhibits the deposition of C3b on bacterial surfaces and the release of the chemoattractant C5a. Cleavage analyses show that aureolysin cleaves the central complement protein C3. Strikingly, there was a clear difference between the cleavages of C3 in serum versus purified conditions. Aureolysin cleaves purified C3 specifically in the α-chain, close to the C3 convertase cleavage site, yielding active C3a and C3b. However, in serum we observe that the aureolysin-generated C3b is further degraded by host factors. We pinpointed these factors to be factor H and factor I. Using an aureolysin mutant in S. aureus USA300, we show that aureolysin is essential and sufficient for C3 cleavage by bacterial supernatant. In short, aureolysin acts in synergy with host regulators to inactivate C3 thereby effectively dampening the host immune response.

Footnotes

  • This work was supported by grants from The Netherlands Organization for Scientific Research (NWO-TOP and NWO-Vidi to A.J.L., J.A.G.v.S., and S.H.M.R.), by funding from the European Molecular Biology Organization (to S.H.M.R.), and by Award AI078921 from the National Institute of Allergy and Infectious Diseases (to A.R.H.).

  • The online version of this article contains supplemental material.

  • Received August 31, 2010.
  • Accepted February 23, 2011.
  • Copyright © 2011 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 208 (11)
The Journal of Immunology
Vol. 208, Issue 11
1 Jun 2022
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Staphylococcus aureus Metalloprotease Aureolysin Cleaves Complement C3 To Mediate Immune Evasion
Alexander J. Laarman, Maartje Ruyken, Cheryl L. Malone, Jos A. G. van Strijp, Alexander R. Horswill, Suzan H. M. Rooijakkers
The Journal of Immunology April 18, 2011, 1002948; DOI: 10.4049/jimmunol.1002948

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Staphylococcus aureus Metalloprotease Aureolysin Cleaves Complement C3 To Mediate Immune Evasion
Alexander J. Laarman, Maartje Ruyken, Cheryl L. Malone, Jos A. G. van Strijp, Alexander R. Horswill, Suzan H. M. Rooijakkers
The Journal of Immunology April 18, 2011, 1002948; DOI: 10.4049/jimmunol.1002948
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