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J Proteomics. 2014 Jun 25;106:46-60. doi: 10.1016/j.jprot.2014.04.023. Epub 2014 Apr 24.

Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae.

Author information

1
Departamento de Bioquímica y Biología Molecular, Universidad de Córdoba, Campus de Excelencia Internacional CeiA3, Córdoba, Spain; Red Española de Investigación en Patología Infecciosa (REIPI), Instituto de Salud Carlos III, Madrid, Spain.
2
Department of Microbiology and Immunology, Albert Einstein College of Medicine, Bronx, NY, USA.
3
Red Española de Investigación en Patología Infecciosa (REIPI), Instituto de Salud Carlos III, Madrid, Spain; Unidad de Enfermedades Infecciosas, Microbiología y Medicina Preventiva, Instituto de Biomedicina de Sevilla/Hospital Universitario Virgen del Rocío/CSIC/Universidad de Sevilla, Sevilla, Spain.
4
Departamento de Biología Celular, Fisiología e Inmunología, Universidad de Córdoba, Campus de Excelencia Internacional CeiA3, Córdoba, Spain.
5
Departamento de Botánica, Ecología y Fisiología Vegetal, Universidad de Córdoba, Campus de Excelencia Internacional CeiA3, Córdoba, Spain.
6
Departamento de Química Analítica, Universidad Complutense de Madrid, Madrid, Spain.
7
Sección de Enfermedades Infecciosas Pediátricas e Inmunopatología, Hospital Universitario Infantil Virgen del Rocío, Sevilla, Spain.
8
Department of Medicine and Microbiology and Immunology, Albert Einstein College of Medicine, Montefiore Medical Center, Bronx, NY, USA.
9
Departamento de Bioquímica y Biología Molecular, Universidad de Córdoba, Campus de Excelencia Internacional CeiA3, Córdoba, Spain; Red Española de Investigación en Patología Infecciosa (REIPI), Instituto de Salud Carlos III, Madrid, Spain. Electronic address: mjrodriguez@uco.es.

Abstract

Extracellular vesicles are produced by many pathogenic microorganisms and have varied functions that include secretion and release of microbial factors, which contribute to virulence. Very little is known about vesicle production by Gram-positive bacteria, as well as their biogenesis and release mechanisms. In this work, we demonstrate the active production of vesicles by Streptococcus pneumoniae from the plasma membrane, rather than being a product from cell lysis. We biochemically characterized them by proteomics and fatty acid analysis, showing that these vesicles and the plasma membrane resemble in essential aspects, but have some differences: vesicles are more enriched in lipoproteins and short-chain fatty acids. We also demonstrate that these vesicles act as carriers of surface proteins and virulence factors. They are also highly immunoreactive against human sera and induce immune responses that protect against infection. Overall, this work provides insights into the biology of this important Gram-positive human pathogen and the role of extracellular vesicles in clinical applications.

BIOLOGICAL SIGNIFICANCE:

Pneumococcus is one of the leading causes of bacterial pneumonia worldwide in children and the elderly, being responsible for high morbidity and mortality rates in developing countries. The augment of pneumococcal disease in developed countries has raised major public health concern, since the difficulties to treat these infections due to increasing antibiotic resistance. Vaccination is still the best way to combat pneumococcal infections. One of the mechanisms that bacterial pathogens use to combat the defense responses of invaded hosts is the production and release of extracellular vesicles derived from the outer surface. Little is known about this phenomenon in Gram-positives. We show that pneumococcus produces membrane-derived vesicles particularly enriched in lipoproteins. We also show the utility of pneumococcal vesicles as a new type of vaccine, as they induce protection in immunized mice against infection with a virulent strain. This work will contribute to understand the role of these structures in important biological processes such as host-pathogen interactions and prevention of human disease.

KEYWORDS:

Extracellular vesicles; Membrane vesicles; Pneumococcus; Proteomics; Surface proteins; Vaccine

PMID:
24769240
DOI:
10.1016/j.jprot.2014.04.023
[Indexed for MEDLINE]

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