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

Alfonso Olaya-Abril, Rafael Prados-Rosales, Michael J. McConnell, Reyes Martín-Peña, José Antonio González-Reyes, Irene Jiménez-Munguía, Lidia Gómez-Gascón, Javier Fernández, José L. Luque-García, Carlos García-Lidón, Héctor Estévez, Jerónimo Pachón, Ignacio Obando, Arturo Casadevall, Liise-anne Pirofski, Manuel J. Rodríguez-Ortega

Research output: Contribution to journalArticle

64 Citations (Scopus)

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.

Original languageEnglish (US)
Pages (from-to)46-60
Number of pages15
JournalJournal of Proteomics
Volume106
DOIs
StatePublished - Jun 25 2014

Fingerprint

Pathogens
Streptococcus pneumoniae
Cell membranes
Membranes
Lipoproteins
Infection
Cell Membrane
Biological Phenomena
Host-Pathogen Interactions
Pneumococcal Infections
Bacterial Pneumonia
Volatile Fatty Acids
Gram-Positive Bacteria
Virulence Factors
Public health
Microbial Drug Resistance
Developed Countries
Developing countries
Microorganisms
Proteomics

Keywords

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

ASJC Scopus subject areas

  • Biophysics
  • Biochemistry
  • Medicine(all)

Cite this

Olaya-Abril, A., Prados-Rosales, R., McConnell, M. J., Martín-Peña, R., González-Reyes, J. A., Jiménez-Munguía, I., ... Rodríguez-Ortega, M. J. (2014). Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. Journal of Proteomics, 106, 46-60. https://doi.org/10.1016/j.jprot.2014.04.023

Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. / Olaya-Abril, Alfonso; Prados-Rosales, Rafael; McConnell, Michael J.; Martín-Peña, Reyes; González-Reyes, José Antonio; Jiménez-Munguía, Irene; Gómez-Gascón, Lidia; Fernández, Javier; Luque-García, José L.; García-Lidón, Carlos; Estévez, Héctor; Pachón, Jerónimo; Obando, Ignacio; Casadevall, Arturo; Pirofski, Liise-anne; Rodríguez-Ortega, Manuel J.

In: Journal of Proteomics, Vol. 106, 25.06.2014, p. 46-60.

Research output: Contribution to journalArticle

Olaya-Abril, A, Prados-Rosales, R, McConnell, MJ, Martín-Peña, R, González-Reyes, JA, Jiménez-Munguía, I, Gómez-Gascón, L, Fernández, J, Luque-García, JL, García-Lidón, C, Estévez, H, Pachón, J, Obando, I, Casadevall, A, Pirofski, L & Rodríguez-Ortega, MJ 2014, 'Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae', Journal of Proteomics, vol. 106, pp. 46-60. https://doi.org/10.1016/j.jprot.2014.04.023
Olaya-Abril A, Prados-Rosales R, McConnell MJ, Martín-Peña R, González-Reyes JA, Jiménez-Munguía I et al. Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. Journal of Proteomics. 2014 Jun 25;106:46-60. https://doi.org/10.1016/j.jprot.2014.04.023
Olaya-Abril, Alfonso ; Prados-Rosales, Rafael ; McConnell, Michael J. ; Martín-Peña, Reyes ; González-Reyes, José Antonio ; Jiménez-Munguía, Irene ; Gómez-Gascón, Lidia ; Fernández, Javier ; Luque-García, José L. ; García-Lidón, Carlos ; Estévez, Héctor ; Pachón, Jerónimo ; Obando, Ignacio ; Casadevall, Arturo ; Pirofski, Liise-anne ; Rodríguez-Ortega, Manuel J. / Characterization of protective extracellular membrane-derived vesicles produced by Streptococcus pneumoniae. In: Journal of Proteomics. 2014 ; Vol. 106. pp. 46-60.
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