Staphylococcus aureus Membrane-Derived Vesicles Promote Bacterial Virulence and Confer Protective Immunity in Murine Infection Models

Fatemeh Askarian; Fatemeh Askarian; John D. Lapek; Mitesh Dongre; Chih-Ming Tsai; Monika Kumaraswamy; Armin Kousha; Armin Kousha; J. Andrés Valderrama; Judith A. Ludviksen; Jorunn P. Cavanagh; Jorunn P. Cavanagh; Satoshi Uchiyama; Tom E. Mollnes; Tom E. Mollnes; Tom E. Mollnes; Tom E. Mollnes; Tom E. Mollnes; David J. Gonzalez; David J. Gonzalez; Sun N. Wai; Victor Nizet; Victor Nizet; Mona Johannessen

doi:10.3389/fmicb.2018.00262

Frontiers in Microbiology (Feb 2018)

Staphylococcus aureus Membrane-Derived Vesicles Promote Bacterial Virulence and Confer Protective Immunity in Murine Infection Models

Fatemeh Askarian,
Fatemeh Askarian,
John D. Lapek,
Mitesh Dongre,
Chih-Ming Tsai,
Monika Kumaraswamy,
Armin Kousha,
Armin Kousha,
J. Andrés Valderrama,
Judith A. Ludviksen,
Jorunn P. Cavanagh,
Jorunn P. Cavanagh,
Satoshi Uchiyama,
Tom E. Mollnes,
Tom E. Mollnes,
Tom E. Mollnes,
Tom E. Mollnes,
Tom E. Mollnes,
David J. Gonzalez,
David J. Gonzalez,
Sun N. Wai,
Victor Nizet,
Victor Nizet,
Mona Johannessen

Affiliations

Fatemeh Askarian: Research Group of Host Microbe Interactions, Department of Medical Biology, Faculty of Health Sciences, UiT – The Arctic University of Norway, Tromsø, Norway
Fatemeh Askarian: Division of Host-Microbe Systems and Therapeutics, Department of Pediatrics, University of California, San Diego, La Jolla, CA, United States
John D. Lapek: Department of Pharmacology, University of California, San Diego, La Jolla, CA, United States
Mitesh Dongre: The Laboratory for Molecular Infection Medicine Sweden, Department of Molecular Biology, Umeå University, Umeå, Sweden
Chih-Ming Tsai: Division of Host-Microbe Systems and Therapeutics, Department of Pediatrics, University of California, San Diego, La Jolla, CA, United States
Monika Kumaraswamy: Division of Infectious Diseases, Department of Medicine, University of California, San Diego, La Jolla, CA, United States
Armin Kousha: Research Group of Host Microbe Interactions, Department of Medical Biology, Faculty of Health Sciences, UiT – The Arctic University of Norway, Tromsø, Norway
Armin Kousha: Division of Host-Microbe Systems and Therapeutics, Department of Pediatrics, University of California, San Diego, La Jolla, CA, United States
J. Andrés Valderrama: Division of Host-Microbe Systems and Therapeutics, Department of Pediatrics, University of California, San Diego, La Jolla, CA, United States
Judith A. Ludviksen: Research Laboratory, Nordland Hospital, Bodø, Norway
Jorunn P. Cavanagh: Department of Pediatrics and Neonatal Medicine, University Hospital of North Norway, University Hospital of North Norway, Tromsø, Norway
Jorunn P. Cavanagh: Department of Pediatrics, Faculty of Health Sciences, UiT – The Arctic University of Norway, Tromsø, Norway
Satoshi Uchiyama: Division of Host-Microbe Systems and Therapeutics, Department of Pediatrics, University of California, San Diego, La Jolla, CA, United States
Tom E. Mollnes: Research Laboratory, Nordland Hospital, Bodø, Norway
Tom E. Mollnes: Faculty of Health Sciences, K. G. Jebsen Thrombosis Research and Expertise Center, UiT – The Arctic University of Norway, Tromsø, Norway
Tom E. Mollnes: 0Department of Immunology, Oslo University Hospital, University of Oslo, Oslo, Norway
Tom E. Mollnes: 1K.G. Jebsen Inflammation Research Centre, University of Oslo, Oslo, Norway
Tom E. Mollnes: 2Center for Molecular Inflammation Research, Norwegian University of Science and Technology, Trondheim, Norway
David J. Gonzalez: Department of Pharmacology, University of California, San Diego, La Jolla, CA, United States
David J. Gonzalez: 3Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La Jolla, CA, United States
Sun N. Wai: The Laboratory for Molecular Infection Medicine Sweden, Department of Molecular Biology, Umeå University, Umeå, Sweden
Victor Nizet: Division of Host-Microbe Systems and Therapeutics, Department of Pediatrics, University of California, San Diego, La Jolla, CA, United States
Victor Nizet: 3Skaggs School of Pharmacy and Pharmaceutical Sciences, University of California, San Diego, La Jolla, CA, United States
Mona Johannessen: Research Group of Host Microbe Interactions, Department of Medical Biology, Faculty of Health Sciences, UiT – The Arctic University of Norway, Tromsø, Norway

DOI: https://doi.org/10.3389/fmicb.2018.00262
Journal volume & issue: Vol. 9

Abstract

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Staphylococcus aureus produces membrane-derived vesicles (MVs), which share functional properties to outer membrane vesicles. Atomic force microscopy revealed that S. aureus-derived MVs are associated with the bacterial surface or released into the surrounding environment depending on bacterial growth conditions. By using a comparative proteomic approach, a total of 131 and 617 proteins were identified in MVs isolated from S. aureus grown in Luria-Bertani and brain-heart infusion broth, respectively. Purified S. aureus MVs derived from the bacteria grown in either media induced comparable levels of cytotoxicity and neutrophil-activation. Administration of exogenous MVs increased the resistance of S. aureus to killing by whole blood or purified human neutrophils ex vivo and increased S. aureus survival in vivo. Finally, immunization of mice with S. aureus-derived MVs induced production of IgM, total IgG, IgG1, IgG2a, and IgG2b resulting in protection against subcutaneous and systemic S. aureus infection. Collectively, our results suggest S. aureus MVs can influence bacterial–host interactions during systemic infections and provide protective immunity in murine models of infection.

Published in Frontiers in Microbiology

ISSN: 1664-302X (Online)
Publisher: Frontiers Media S.A.
Country of publisher: Switzerland
LCC subjects: Science: Microbiology
Website: http://www.frontiersin.org/journals/microbiology

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