Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System

Cerebral toxoplasmosis is characterized by activation of brain resident cells and recruitment of specific immune cell subsets from the periphery to the central nervous system (CNS). Our studies revealed that the rapidly invaded Ly6G+ neutrophil granulocytes are an early non-lymphoid source of interf...

Full description

Bibliographic Details
Main Authors: Aindrila Biswas, Timothy French, Henning P. Düsedau, Nancy Mueller, Monika Riek-Burchardt, Anne Dudeck, Ute Bank, Thomas Schüler, Ildiko Rita Dunay
Format: Article
Language:English
Published: Frontiers Media S.A. 2017-06-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:http://journal.frontiersin.org/article/10.3389/fcimb.2017.00259/full
_version_ 1818136391296483328
author Aindrila Biswas
Timothy French
Henning P. Düsedau
Nancy Mueller
Monika Riek-Burchardt
Anne Dudeck
Ute Bank
Thomas Schüler
Ildiko Rita Dunay
author_facet Aindrila Biswas
Timothy French
Henning P. Düsedau
Nancy Mueller
Monika Riek-Burchardt
Anne Dudeck
Ute Bank
Thomas Schüler
Ildiko Rita Dunay
author_sort Aindrila Biswas
collection DOAJ
description Cerebral toxoplasmosis is characterized by activation of brain resident cells and recruitment of specific immune cell subsets from the periphery to the central nervous system (CNS). Our studies revealed that the rapidly invaded Ly6G+ neutrophil granulocytes are an early non-lymphoid source of interferon-gamma (IFN-γ), the cytokine known to be the major mediator of host resistance to Toxoplasma gondii (T. gondii). Upon selective depletion of Ly6G+ neutrophils, we detected reduced IFN-γ production and increased parasite burden in the CNS. Ablation of Ly6G+ cells resulted in diminished recruitment of Ly6Chi monocytes into the CNS, indicating a pronounced interplay. Additionally, we identified infiltrated Ly6G+ neutrophils to be a heterogeneous population. The Ly6G+CD62-LhiCXCR4+ subset released cathelicidin-related antimicrobial peptide (CRAMP), which can promote monocyte dynamics. On the other hand, the Ly6G+CD62-LloCXCR4+ subset produced IFN-γ to establish early inflammatory response. Collectively, our findings revealed that the recruited Ly6G+CXCR4+ neutrophil granulocytes display a heterogeneity in the CNS with a repertoire of effector functions crucial in parasite control and immune regulation upon experimental cerebral toxoplasmosis.
first_indexed 2024-12-11T09:39:40Z
format Article
id doaj.art-39f3ddf9a2c0442db26fdcf2d97847cd
institution Directory Open Access Journal
issn 2235-2988
language English
last_indexed 2024-12-11T09:39:40Z
publishDate 2017-06-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj.art-39f3ddf9a2c0442db26fdcf2d97847cd2022-12-22T01:12:42ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882017-06-01710.3389/fcimb.2017.00259262335Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous SystemAindrila Biswas0Timothy French1Henning P. Düsedau2Nancy Mueller3Monika Riek-Burchardt4Anne Dudeck5Ute Bank6Thomas Schüler7Ildiko Rita Dunay8Institute of Inflammation and Neurodegeneration, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute of Inflammation and Neurodegeneration, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute of Inflammation and Neurodegeneration, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute of Inflammation and Neurodegeneration, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute for Molecular and Clinical Immunology, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute for Molecular and Clinical Immunology, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute for Molecular and Clinical Immunology, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute for Molecular and Clinical Immunology, Otto-von-Guericke University MagdeburgMagdeburg, GermanyInstitute of Inflammation and Neurodegeneration, Otto-von-Guericke University MagdeburgMagdeburg, GermanyCerebral toxoplasmosis is characterized by activation of brain resident cells and recruitment of specific immune cell subsets from the periphery to the central nervous system (CNS). Our studies revealed that the rapidly invaded Ly6G+ neutrophil granulocytes are an early non-lymphoid source of interferon-gamma (IFN-γ), the cytokine known to be the major mediator of host resistance to Toxoplasma gondii (T. gondii). Upon selective depletion of Ly6G+ neutrophils, we detected reduced IFN-γ production and increased parasite burden in the CNS. Ablation of Ly6G+ cells resulted in diminished recruitment of Ly6Chi monocytes into the CNS, indicating a pronounced interplay. Additionally, we identified infiltrated Ly6G+ neutrophils to be a heterogeneous population. The Ly6G+CD62-LhiCXCR4+ subset released cathelicidin-related antimicrobial peptide (CRAMP), which can promote monocyte dynamics. On the other hand, the Ly6G+CD62-LloCXCR4+ subset produced IFN-γ to establish early inflammatory response. Collectively, our findings revealed that the recruited Ly6G+CXCR4+ neutrophil granulocytes display a heterogeneity in the CNS with a repertoire of effector functions crucial in parasite control and immune regulation upon experimental cerebral toxoplasmosis.http://journal.frontiersin.org/article/10.3389/fcimb.2017.00259/fullToxoplasma gondiineutrophil granulocytescerebral toxoplasmosisneuroinflammationneutrophil Infiltration
spellingShingle Aindrila Biswas
Timothy French
Henning P. Düsedau
Nancy Mueller
Monika Riek-Burchardt
Anne Dudeck
Ute Bank
Thomas Schüler
Ildiko Rita Dunay
Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System
Frontiers in Cellular and Infection Microbiology
Toxoplasma gondii
neutrophil granulocytes
cerebral toxoplasmosis
neuroinflammation
neutrophil Infiltration
title Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System
title_full Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System
title_fullStr Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System
title_full_unstemmed Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System
title_short Behavior of Neutrophil Granulocytes during Toxoplasma gondii Infection in the Central Nervous System
title_sort behavior of neutrophil granulocytes during toxoplasma gondii infection in the central nervous system
topic Toxoplasma gondii
neutrophil granulocytes
cerebral toxoplasmosis
neuroinflammation
neutrophil Infiltration
url http://journal.frontiersin.org/article/10.3389/fcimb.2017.00259/full
work_keys_str_mv AT aindrilabiswas behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT timothyfrench behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT henningpdusedau behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT nancymueller behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT monikariekburchardt behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT annedudeck behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT utebank behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT thomasschuler behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem
AT ildikoritadunay behaviorofneutrophilgranulocytesduringtoxoplasmagondiiinfectioninthecentralnervoussystem