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Open Access Highly Accessed Research article

Evidence of involvement of the mannose receptor in the internalization of Streptococcus pneumoniae by Schwann cells

Hugo Macedo-Ramos126, Andre F Batista2, Alvaro Carrier-Ruiz456, Lucineia Alves2, Silvana Allodi26, Victor T Ribeiro-Resende46, Lucia M Teixeira3 and Wagner Baetas-da-Cruz16*

Author Affiliations

1 Faculdade de Medicina, Centro de Cirurgia Experimental, Laboratório Translacional em Fisiologia Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

2 Instituto de Biofísica Carlos Chagas Filho, Laboratório de Neurobiologia Comparativa e do Desenvolvimento, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

3 Instituto de Microbiologia Paulo de Góes, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

4 Instituto de Biofísica Carlos Chagas Filho - Pólo de Xerém, Laboratório de Neuroquímica, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

5 Instituto de Biofísica Carlos Chagas Filho, Laboratório de Neurobiologia Celular e Molecular, Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

6 Instituto de Biofísica Carlos Chagas Filho, Programa de Pós-Graduação em Ciências Biológicas (Fisiologia), Universidade Federal do Rio de Janeiro, Rio de Janeiro, RJ, Brazil

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BMC Microbiology 2014, 14:211  doi:10.1186/s12866-014-0211-9

Published: 2 August 2014

Abstract

Background

The ability of S. pneumoniae to generate infections depends on the restrictions imposed by the host’s immunity, in order to prevent the bacterium from spreading from the nasopharynx to other tissues, such as the brain. Some authors claim that strains of S. pneumoniae, which fail to survive in the bloodstream, can enter the brain directly from the nasal cavity by axonal transport through the olfactory and/or trigeminal nerves. However, from the immunological point of view, glial cells are far more responsive to bacterial infections than are neurons. This hypothesis is consistent with several recent reports showing that bacteria can infect glial cells from the olfactory bulb and trigeminal ganglia. Since our group previously demonstrated that Schwann cells (SCs) express a functional and appropriately regulated mannose receptor (MR), we decided to test whether SCs are involved in the internalization of S. pneumoniae via MR.

Results

Immediately after the interaction step, as well as 3 h later, the percentage of association was approximately 56.5%, decreasing to 47.2% and 40.8% after 12 and 24 h, respectively. Competition assays by adding a 100-fold excess of mannan prior to the S. pneumoniae infection reduced the number of infected cells at 3 and 24 h. A cytochemistry assay with Man/BSA-FITC binding was performed in order to verify a possible overlap between mannosylated ligands and internalized bacteria. Incubation of the SCs with Man/BSA-FITC resulted in a large number of intracellular S. pneumoniae, with nearly complete loss of the capsule. Moreover, the anti-pneumococcal antiserum staining colocalized with the internalized man/BSA-FITC, suggesting that both markers are present within the same endocytic compartment of the SC.

Conclusions

Our data offer novel evidence that SCs could be essential for pneumococcal cells to escape phagocytosis and killing by innate immune cells. On the other hand, the results also support the idea that SCs are immunocompetent cells of the PNS that can mediate an efficient immune response against pathogens via MR.

Keywords:
Pneumococcal meningitis; Glia; Pattern recognition receptor (PRRs); Innate immunity; Pathogen-associated molecular patterns (PAMPs); Nerve injury