<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst

ABSTRACT Neisseria gonorrhoeae (the gonococcus) causes gonorrhea and is uniquely adapted to survive within the human reproductive tract. Gonococci evade host immune surveillance in part by varying their pili and opacity-associated proteins. These variable surface antigens influence interactions wit...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Carl W. Gunderson, H. Steven Seifert
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2015
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/ab9e1634eef942dfac5a3cf2c2f1ec34
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:ab9e1634eef942dfac5a3cf2c2f1ec34
record_format	dspace
spelling	oai:doaj.org-article:ab9e1634eef942dfac5a3cf2c2f1ec342021-11-15T15:41:19Z<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst10.1128/mBio.02452-142150-7511https://doaj.org/article/ab9e1634eef942dfac5a3cf2c2f1ec342015-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02452-14https://doaj.org/toc/2150-7511ABSTRACT Neisseria gonorrhoeae (the gonococcus) causes gonorrhea and is uniquely adapted to survive within the human reproductive tract. Gonococci evade host immune surveillance in part by varying their pili and opacity-associated proteins. These variable surface antigens influence interactions with host epithelial and immune cells. A potent polymorphonuclear leukocyte (PMN) response is a hallmark of symptomatic gonococcal infection, with vast numbers of PMNs recruited to the site of infection. A large body of literature describes gonococcus-PMN interactions, but the factors driving the outcome of infection are not fully understood. Gonococci have been described to both induce and suppress the PMN oxidative burst, but we determined that gonococci differentially affect induction of the PMN oxidative burst depending on the multiplicity of infection (MOI). Infecting PMN at an MOI of <20 gonococci elicits an oxidative burst, while an MOI of >20 suppresses the burst. Oxidative burst in response to gonococci is enhanced by, but does not require, expression of pili or opacity proteins. Neutrophil extracellular traps (NETs) were observed in gonococcus-infected PMNs, a process which requires an oxidative burst, yet gonococci induced NETs under suppressing conditions. The NETs were unable to kill gonococci despite killing the common vaginal bacterium Lactobacillus crispatus. Thus, gonococci influence PMN biology to promote their own survival by suppressing the oxidative burst of PMNs and stimulating the formation of NETs, which do not effectively kill gonococci, illustrating how N. gonorrhoeae has evolved to modulate PMN responses to promote infection. IMPORTANCE Neisseria gonorrhoeae, the gonococcus, is the only causative agent of gonorrhea and is exclusively found within the human host. Gonococci stochastically vary the composition of antigens on their surface to evade immune surveillance. We used gonococcal mutants which stably express different surface antigens to dissect interactions between gonococci and primary human polymorphonuclear leukocytes (PMNs). We found that gonococci, depending on the number of bacteria present, either induce or suppress the oxidative burst of PMNs regardless of other stimuli. Gonococci also cause PMNs to release DNA, forming neutrophil extracellular traps (NETs) independently of the oxidative burst. The NETs were unable to kill gonococci but were able to kill commensal bacteria, suggesting that NET production can help gonococci outcompete other bacterial species. We propose that gonococci have evolved to manipulate PMN responses to promote their own survival during infection.Carl W. GundersonH. Steven SeifertAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 6, Iss 1 (2015)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Carl W. Gunderson H. Steven Seifert <named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst
description	ABSTRACT Neisseria gonorrhoeae (the gonococcus) causes gonorrhea and is uniquely adapted to survive within the human reproductive tract. Gonococci evade host immune surveillance in part by varying their pili and opacity-associated proteins. These variable surface antigens influence interactions with host epithelial and immune cells. A potent polymorphonuclear leukocyte (PMN) response is a hallmark of symptomatic gonococcal infection, with vast numbers of PMNs recruited to the site of infection. A large body of literature describes gonococcus-PMN interactions, but the factors driving the outcome of infection are not fully understood. Gonococci have been described to both induce and suppress the PMN oxidative burst, but we determined that gonococci differentially affect induction of the PMN oxidative burst depending on the multiplicity of infection (MOI). Infecting PMN at an MOI of <20 gonococci elicits an oxidative burst, while an MOI of >20 suppresses the burst. Oxidative burst in response to gonococci is enhanced by, but does not require, expression of pili or opacity proteins. Neutrophil extracellular traps (NETs) were observed in gonococcus-infected PMNs, a process which requires an oxidative burst, yet gonococci induced NETs under suppressing conditions. The NETs were unable to kill gonococci despite killing the common vaginal bacterium Lactobacillus crispatus. Thus, gonococci influence PMN biology to promote their own survival by suppressing the oxidative burst of PMNs and stimulating the formation of NETs, which do not effectively kill gonococci, illustrating how N. gonorrhoeae has evolved to modulate PMN responses to promote infection. IMPORTANCE Neisseria gonorrhoeae, the gonococcus, is the only causative agent of gonorrhea and is exclusively found within the human host. Gonococci stochastically vary the composition of antigens on their surface to evade immune surveillance. We used gonococcal mutants which stably express different surface antigens to dissect interactions between gonococci and primary human polymorphonuclear leukocytes (PMNs). We found that gonococci, depending on the number of bacteria present, either induce or suppress the oxidative burst of PMNs regardless of other stimuli. Gonococci also cause PMNs to release DNA, forming neutrophil extracellular traps (NETs) independently of the oxidative burst. The NETs were unable to kill gonococci but were able to kill commensal bacteria, suggesting that NET production can help gonococci outcompete other bacterial species. We propose that gonococci have evolved to manipulate PMN responses to promote their own survival during infection.
format	article
author	Carl W. Gunderson H. Steven Seifert
author_facet	Carl W. Gunderson H. Steven Seifert
author_sort	Carl W. Gunderson
title	<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst
title_short	<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst
title_full	<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst
title_fullStr	<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst
title_full_unstemmed	<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst
title_sort	<named-content content-type="genus-species">neisseria gonorrhoeae</named-content> elicits extracellular traps in primary neutrophil culture while suppressing the oxidative burst
publisher	American Society for Microbiology
publishDate	2015
url	https://doaj.org/article/ab9e1634eef942dfac5a3cf2c2f1ec34
work_keys_str_mv	AT carlwgunderson namedcontentcontenttypegenusspeciesneisseriagonorrhoeaenamedcontentelicitsextracellulartrapsinprimaryneutrophilculturewhilesuppressingtheoxidativeburst AT hstevenseifert namedcontentcontenttypegenusspeciesneisseriagonorrhoeaenamedcontentelicitsextracellulartrapsinprimaryneutrophilculturewhilesuppressingtheoxidativeburst
_version_	1718427721964453888

<named-content content-type="genus-species">Neisseria gonorrhoeae</named-content> Elicits Extracellular Traps in Primary Neutrophil Culture While Suppressing the Oxidative Burst

Ejemplares similares