Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing

ABSTRACT The use of pneumococcal capsular polysaccharide (PPS)-based vaccines has resulted in a substantial reduction in invasive pneumococcal disease. However, much remains to be learned about vaccine-mediated immunity, as seven-valent PPS-protein conjugate vaccine use in children has been associat...

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Autores principales:	Masahide Yano, Shruti Gohil, J. Robert Coleman, Catherine Manix, Liise-anne Pirofski
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e15ddd6b88b34e1f85a0a35341f83147
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spelling	oai:doaj.org-article:e15ddd6b88b34e1f85a0a35341f831472021-11-15T15:38:58ZAntibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing10.1128/mBio.00176-112150-7511https://doaj.org/article/e15ddd6b88b34e1f85a0a35341f831472011-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00176-11https://doaj.org/toc/2150-7511ABSTRACT The use of pneumococcal capsular polysaccharide (PPS)-based vaccines has resulted in a substantial reduction in invasive pneumococcal disease. However, much remains to be learned about vaccine-mediated immunity, as seven-valent PPS-protein conjugate vaccine use in children has been associated with nonvaccine serotype replacement and 23-valent vaccine use in adults has not prevented pneumococcal pneumonia. In this report, we demonstrate that certain PPS-specific monoclonal antibodies (MAbs) enhance the transformation frequency of two different Streptococcus pneumoniae serotypes. This phenomenon was mediated by PPS-specific MAbs that agglutinate but do not promote opsonic effector cell killing of the homologous serotype in vitro. Compared to the autoinducer, competence-stimulating peptide (CSP) alone, transcriptional profiling of pneumococcal gene expression after incubation with CSP and one such MAb to the PPS of serotype 3 revealed changes in the expression of competence (com)-related and bacteriocin-like peptide (blp) genes involved in pneumococcal quorum sensing. This MAb was also found to induce a nearly 2-fold increase in CSP2-mediated bacterial killing or fratricide. These observations reveal a novel, direct effect of PPS-binding MAbs on pneumococcal biology that has important implications for antibody immunity to pneumococcus in the pneumococcal vaccine era. Taken together, our data suggest heretofore unsuspected mechanisms by which PPS-specific antibodies could affect genetic exchange and bacterial viability in the absence of host cells. IMPORTANCE Current thought holds that pneumococcal capsular polysaccharide (PPS)-binding antibodies protect against pneumococcus by inducing effector cell opsonic killing of the homologous serotype. While such antibodies are an important part of how pneumococcal vaccines protect against pneumococcal disease, PPS-specific antibodies that do not exhibit this activity but are highly protective against pneumococcus in mice have been identified. This article examines the effect of nonopsonic PPS-specific monoclonal antibodies (MAbs) on the biology of Streptococcus pneumoniae. The results showed that in the presence of a competence-stimulating peptide (CSP), such MAbs increase the frequency of pneumococcal transformation. Further studies with one such MAb showed that it altered the expression of genes involved in quorum sensing and increased competence-induced killing or fratricide. These findings reveal a novel, previously unsuspected mechanism by which certain PPS-specific antibodies exert a direct effect on pneumococcal biology that has broad implications for bacterial clearance, genetic exchange, and antibody immunity to pneumococcus.Masahide YanoShruti GohilJ. Robert ColemanCatherine ManixLiise-anne PirofskiAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 5 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Masahide Yano Shruti Gohil J. Robert Coleman Catherine Manix Liise-anne Pirofski Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing
description	ABSTRACT The use of pneumococcal capsular polysaccharide (PPS)-based vaccines has resulted in a substantial reduction in invasive pneumococcal disease. However, much remains to be learned about vaccine-mediated immunity, as seven-valent PPS-protein conjugate vaccine use in children has been associated with nonvaccine serotype replacement and 23-valent vaccine use in adults has not prevented pneumococcal pneumonia. In this report, we demonstrate that certain PPS-specific monoclonal antibodies (MAbs) enhance the transformation frequency of two different Streptococcus pneumoniae serotypes. This phenomenon was mediated by PPS-specific MAbs that agglutinate but do not promote opsonic effector cell killing of the homologous serotype in vitro. Compared to the autoinducer, competence-stimulating peptide (CSP) alone, transcriptional profiling of pneumococcal gene expression after incubation with CSP and one such MAb to the PPS of serotype 3 revealed changes in the expression of competence (com)-related and bacteriocin-like peptide (blp) genes involved in pneumococcal quorum sensing. This MAb was also found to induce a nearly 2-fold increase in CSP2-mediated bacterial killing or fratricide. These observations reveal a novel, direct effect of PPS-binding MAbs on pneumococcal biology that has important implications for antibody immunity to pneumococcus in the pneumococcal vaccine era. Taken together, our data suggest heretofore unsuspected mechanisms by which PPS-specific antibodies could affect genetic exchange and bacterial viability in the absence of host cells. IMPORTANCE Current thought holds that pneumococcal capsular polysaccharide (PPS)-binding antibodies protect against pneumococcus by inducing effector cell opsonic killing of the homologous serotype. While such antibodies are an important part of how pneumococcal vaccines protect against pneumococcal disease, PPS-specific antibodies that do not exhibit this activity but are highly protective against pneumococcus in mice have been identified. This article examines the effect of nonopsonic PPS-specific monoclonal antibodies (MAbs) on the biology of Streptococcus pneumoniae. The results showed that in the presence of a competence-stimulating peptide (CSP), such MAbs increase the frequency of pneumococcal transformation. Further studies with one such MAb showed that it altered the expression of genes involved in quorum sensing and increased competence-induced killing or fratricide. These findings reveal a novel, previously unsuspected mechanism by which certain PPS-specific antibodies exert a direct effect on pneumococcal biology that has broad implications for bacterial clearance, genetic exchange, and antibody immunity to pneumococcus.
format	article
author	Masahide Yano Shruti Gohil J. Robert Coleman Catherine Manix Liise-anne Pirofski
author_facet	Masahide Yano Shruti Gohil J. Robert Coleman Catherine Manix Liise-anne Pirofski
author_sort	Masahide Yano
title	Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing
title_short	Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing
title_full	Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing
title_fullStr	Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing
title_full_unstemmed	Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing
title_sort	antibodies to <named-content content-type="genus-species">streptococcus pneumoniae</named-content> capsular polysaccharide enhance pneumococcal quorum sensing
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/e15ddd6b88b34e1f85a0a35341f83147
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Antibodies to <named-content content-type="genus-species">Streptococcus pneumoniae</named-content> Capsular Polysaccharide Enhance Pneumococcal Quorum Sensing

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