The encapsulated strain TIGR4 of Streptococcus pneumoniae is phagocytosed but is resistant to intracellular killing by mouse microglia

Samuele Peppoloni, Susanna Ricci, Carlotta F. Orsi, Bruna Colombari, Maria Margherita De Santi, Massimino Messinò, Giuliana Fabio, Alessio Zanardi, Elena Righi, Velia Braione, Sergio Tripodi, Damiana Chiavolini, Marcella Cintorino, Michele Zoli, Marco Rinaldo Oggioni, Elisabetta Blasi, Gianni Pozzi

Research output: Contribution to journalArticle

12 Citations (Scopus)

Abstract

The polysaccharide capsule is a major virulence factor of Streptococcus pneumoniae as it confers resistance to phagocytosis. The encapsulated serotype 4 TIGR4 strain was shown to be efficiently phagocytosed by the mouse microglial cell line BV2, whereas the type 3 HB565 strain resisted phagocytosis. Comparing survival after uptake of TIGR4 or its unencapsulated derivative FP23 in gentamicin protection and phagolysosome maturation assays, it was shown that TIGR4 was protected from intracellular killing. Pneumococcal capsular genes were up-regulated in intracellular TIGR4 bacteria recovered from microglial cells. Actual presence of bacteria inside BV2 cells was confirmed by transmission electron microscopy (TEM) for both TIGR4 and FP23 strains, but typical phagosomes/phagolysosomes were detected only in cells infected with the unencapsulated strain. In a mouse model of meningitis based on intracranic inoculation of pneumococci, TIGR4 caused lethal meningitis with an LD50 of 2 × 102 CFU, whereas the LD50 for the unencapsulated FP23 was greater than 107 CFU. Phagocytosis of TIGR4 by microglia was also demonstrated by TEM and immunohistochemistry on brain samples from infected mice. The results indicate that encapsulation does not protect the TIGR4 strain from phagocytosis by microglia, while it affords resistance to intracellular killing.

Original languageEnglish (US)
Pages (from-to)990-1001
Number of pages12
JournalMicrobes and Infection
Volume12
Issue number12-13
DOIs
StatePublished - Nov 1 2010

Fingerprint

Microglia
Streptococcus pneumoniae
Phagocytosis
Phagosomes
Lethal Dose 50
Transmission Electron Microscopy
Meningitis
Bacteria
Virulence Factors
Gentamicins
Capsules
Polysaccharides
Immunohistochemistry
Cell Line
Brain
Genes

Keywords

  • Capsule
  • Intracellular survival
  • Microglia
  • Phagocytosis
  • Streptococcus pneumoniae

ASJC Scopus subject areas

  • Microbiology
  • Immunology
  • Infectious Diseases

Cite this

The encapsulated strain TIGR4 of Streptococcus pneumoniae is phagocytosed but is resistant to intracellular killing by mouse microglia. / Peppoloni, Samuele; Ricci, Susanna; Orsi, Carlotta F.; Colombari, Bruna; De Santi, Maria Margherita; Messinò, Massimino; Fabio, Giuliana; Zanardi, Alessio; Righi, Elena; Braione, Velia; Tripodi, Sergio; Chiavolini, Damiana; Cintorino, Marcella; Zoli, Michele; Oggioni, Marco Rinaldo; Blasi, Elisabetta; Pozzi, Gianni.

In: Microbes and Infection, Vol. 12, No. 12-13, 01.11.2010, p. 990-1001.

Research output: Contribution to journalArticle

Peppoloni, S, Ricci, S, Orsi, CF, Colombari, B, De Santi, MM, Messinò, M, Fabio, G, Zanardi, A, Righi, E, Braione, V, Tripodi, S, Chiavolini, D, Cintorino, M, Zoli, M, Oggioni, MR, Blasi, E & Pozzi, G 2010, 'The encapsulated strain TIGR4 of Streptococcus pneumoniae is phagocytosed but is resistant to intracellular killing by mouse microglia', Microbes and Infection, vol. 12, no. 12-13, pp. 990-1001. https://doi.org/10.1016/j.micinf.2010.06.010
Peppoloni, Samuele ; Ricci, Susanna ; Orsi, Carlotta F. ; Colombari, Bruna ; De Santi, Maria Margherita ; Messinò, Massimino ; Fabio, Giuliana ; Zanardi, Alessio ; Righi, Elena ; Braione, Velia ; Tripodi, Sergio ; Chiavolini, Damiana ; Cintorino, Marcella ; Zoli, Michele ; Oggioni, Marco Rinaldo ; Blasi, Elisabetta ; Pozzi, Gianni. / The encapsulated strain TIGR4 of Streptococcus pneumoniae is phagocytosed but is resistant to intracellular killing by mouse microglia. In: Microbes and Infection. 2010 ; Vol. 12, No. 12-13. pp. 990-1001.
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abstract = "The polysaccharide capsule is a major virulence factor of Streptococcus pneumoniae as it confers resistance to phagocytosis. The encapsulated serotype 4 TIGR4 strain was shown to be efficiently phagocytosed by the mouse microglial cell line BV2, whereas the type 3 HB565 strain resisted phagocytosis. Comparing survival after uptake of TIGR4 or its unencapsulated derivative FP23 in gentamicin protection and phagolysosome maturation assays, it was shown that TIGR4 was protected from intracellular killing. Pneumococcal capsular genes were up-regulated in intracellular TIGR4 bacteria recovered from microglial cells. Actual presence of bacteria inside BV2 cells was confirmed by transmission electron microscopy (TEM) for both TIGR4 and FP23 strains, but typical phagosomes/phagolysosomes were detected only in cells infected with the unencapsulated strain. In a mouse model of meningitis based on intracranic inoculation of pneumococci, TIGR4 caused lethal meningitis with an LD50 of 2 × 102 CFU, whereas the LD50 for the unencapsulated FP23 was greater than 107 CFU. Phagocytosis of TIGR4 by microglia was also demonstrated by TEM and immunohistochemistry on brain samples from infected mice. The results indicate that encapsulation does not protect the TIGR4 strain from phagocytosis by microglia, while it affords resistance to intracellular killing.",
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AU - Peppoloni, Samuele

AU - Ricci, Susanna

AU - Orsi, Carlotta F.

AU - Colombari, Bruna

AU - De Santi, Maria Margherita

AU - Messinò, Massimino

AU - Fabio, Giuliana

AU - Zanardi, Alessio

AU - Righi, Elena

AU - Braione, Velia

AU - Tripodi, Sergio

AU - Chiavolini, Damiana

AU - Cintorino, Marcella

AU - Zoli, Michele

AU - Oggioni, Marco Rinaldo

AU - Blasi, Elisabetta

AU - Pozzi, Gianni

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N2 - The polysaccharide capsule is a major virulence factor of Streptococcus pneumoniae as it confers resistance to phagocytosis. The encapsulated serotype 4 TIGR4 strain was shown to be efficiently phagocytosed by the mouse microglial cell line BV2, whereas the type 3 HB565 strain resisted phagocytosis. Comparing survival after uptake of TIGR4 or its unencapsulated derivative FP23 in gentamicin protection and phagolysosome maturation assays, it was shown that TIGR4 was protected from intracellular killing. Pneumococcal capsular genes were up-regulated in intracellular TIGR4 bacteria recovered from microglial cells. Actual presence of bacteria inside BV2 cells was confirmed by transmission electron microscopy (TEM) for both TIGR4 and FP23 strains, but typical phagosomes/phagolysosomes were detected only in cells infected with the unencapsulated strain. In a mouse model of meningitis based on intracranic inoculation of pneumococci, TIGR4 caused lethal meningitis with an LD50 of 2 × 102 CFU, whereas the LD50 for the unencapsulated FP23 was greater than 107 CFU. Phagocytosis of TIGR4 by microglia was also demonstrated by TEM and immunohistochemistry on brain samples from infected mice. The results indicate that encapsulation does not protect the TIGR4 strain from phagocytosis by microglia, while it affords resistance to intracellular killing.

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