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Bacterial Infections

Analysis of the Effects of Cigarette Smoke on Staphylococcal Virulence Phenotypes

Elisa K. McEachern, John H. Hwang, Katherine M. Sladewski, Shari Nicatia, Carola Dewitz, Denzil P. Mathew, Victor Nizet, Laura E. Crotty Alexander
S. R. Blanke, Editor
Elisa K. McEachern
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
bDepartment of Medicine, University of California, San Diego, California, USA
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John H. Hwang
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
bDepartment of Medicine, University of California, San Diego, California, USA
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Katherine M. Sladewski
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
bDepartment of Medicine, University of California, San Diego, California, USA
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Shari Nicatia
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
bDepartment of Medicine, University of California, San Diego, California, USA
cDepartment of Pharmaceutical Sciences, Utrecht University, Utrecht, The Netherlands
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Carola Dewitz
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
bDepartment of Medicine, University of California, San Diego, California, USA
dDepartment of Physiological Chemistry, University of Veterinary Medicine, Hannover, Germany
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Denzil P. Mathew
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
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Victor Nizet
eDepartment of Pediatrics, University of California, San Diego, California, USA
fSkaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, California, USA
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Laura E. Crotty Alexander
aMedicine Service, Veterans Affairs San Diego Healthcare System, San Diego, California, USA
bDepartment of Medicine, University of California, San Diego, California, USA
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S. R. Blanke
Roles: Editor
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DOI: 10.1128/IAI.00303-15
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ABSTRACT

Cigarette smoking is the leading preventable cause of death, disease, and disability worldwide. It is well established that cigarette smoke provokes inflammatory activation and impairs antimicrobial functions of human immune cells. Here we explore whether cigarette smoke likewise affects the virulence properties of an important human pathogen, Staphylococcus aureus, and in particular methicillin-resistant S. aureus (MRSA), one of the leading causes of invasive bacterial infections. MRSA colonizes the nasopharynx and is thus exposed to inhalants, including cigarette smoke. MRSA exposed to cigarette smoke extract (CSE-MRSA) was more resistant to macrophage killing (4-fold higher survival; P < 0.0001). CSE-MRSA demonstrated reduced susceptibility to cell lysis (1.78-fold; P = 0.032) and antimicrobial peptide (AMP) (LL-37) killing (MIC, 8 μM versus 4 μM). CSE modified the surface charge of MRSA in a dose-dependent fashion, impairing the binding of particles with charge similar to that of AMPs by 90% (P < 0.0001). These changes persisted for 24 h postexposure, suggesting heritable modifications. CSE exposure increased hydrophobicity by 55% (P < 0.0001), which complemented findings of increased MRSA adherence and invasion of epithelial cells. CSE induced upregulation of mprF, consistent with increased MRSA AMP resistance. S. aureus without mprF had no change in surface charge upon exposure to CSE. In vivo, CSE-MRSA pneumonia induced higher mouse mortality (40% versus 10%) and increased bacterial burden at 8 and 20 h postinfection compared to control MRSA-infected mice (P < 0.01). We conclude that cigarette smoke-induced immune resistance phenotypes in MRSA may be an additional factor contributing to susceptibility to infectious disease in cigarette smokers.

FOOTNOTES

    • Received 5 March 2015.
    • Accepted 24 March 2015.
    • Accepted manuscript posted online 30 March 2015.
  • Supplemental material for this article may be found at http://dx.doi.org/10.1128/IAI.00303-15.

  • Copyright © 2015, American Society for Microbiology. All Rights Reserved.
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Analysis of the Effects of Cigarette Smoke on Staphylococcal Virulence Phenotypes
Elisa K. McEachern, John H. Hwang, Katherine M. Sladewski, Shari Nicatia, Carola Dewitz, Denzil P. Mathew, Victor Nizet, Laura E. Crotty Alexander
Infection and Immunity May 2015, 83 (6) 2443-2452; DOI: 10.1128/IAI.00303-15

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Analysis of the Effects of Cigarette Smoke on Staphylococcal Virulence Phenotypes
Elisa K. McEachern, John H. Hwang, Katherine M. Sladewski, Shari Nicatia, Carola Dewitz, Denzil P. Mathew, Victor Nizet, Laura E. Crotty Alexander
Infection and Immunity May 2015, 83 (6) 2443-2452; DOI: 10.1128/IAI.00303-15
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