Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection

Helminth-induced eosinophils accumulate around the parasite at the site of infection, or in parasite-damaged tissues well after the helminth has left the site. The role of helminth-elicited eosinophils in mediating parasite control is complex. While they may contribute to direct parasite-killing and...

Full description

Bibliographic Details
Main Authors: Alisha Chetty, Matthew G. Darby, Jamie Pillaye, A'ishah Taliep, Adam F. Cunningham, Matthew K. O’Shea, Gnatoulma Katawa, Laura E. Layland, Manuel Ritter, William G. C. Horsnell
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-05-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2023.1170807/full
_version_ 1797828816533454848
author Alisha Chetty
Matthew G. Darby
Jamie Pillaye
A'ishah Taliep
Adam F. Cunningham
Matthew K. O’Shea
Gnatoulma Katawa
Laura E. Layland
Laura E. Layland
Manuel Ritter
William G. C. Horsnell
William G. C. Horsnell
William G. C. Horsnell
author_facet Alisha Chetty
Matthew G. Darby
Jamie Pillaye
A'ishah Taliep
Adam F. Cunningham
Matthew K. O’Shea
Gnatoulma Katawa
Laura E. Layland
Laura E. Layland
Manuel Ritter
William G. C. Horsnell
William G. C. Horsnell
William G. C. Horsnell
author_sort Alisha Chetty
collection DOAJ
description Helminth-induced eosinophils accumulate around the parasite at the site of infection, or in parasite-damaged tissues well after the helminth has left the site. The role of helminth-elicited eosinophils in mediating parasite control is complex. While they may contribute to direct parasite-killing and tissue repair, their involvement in long-term immunopathogenesis is a concern. In allergic Siglec-FhiCD101hi, eosinophils are associated with pathology. Research has not shown if equivalent subpopulations of eosinophils are a feature of helminth infection. In this study, we demonstrate that lung migration of rodent hookworm Nippostrongylus brasiliensis (Nb) results in a long-term expansion of distinct Siglec-FhiCD101hi eosinophil subpopulations. Nb-elevated eosinophil populations in the bone marrow and circulation did not present this phenotype. Siglec-FhiCD101hi lung eosinophils exhibited an activated morphology including nuclei hyper-segmentation and cytoplasm degranulation. Recruitment of ST2+ ILC2s and not CD4+ T cells to the lungs was associated with the expansion of Siglec-FhiCD101hi eosinophils. This data identifies a morphologically distinct and persistent subset of Siglec-FhiCD101hi lung eosinophils induced following Nb infection. These eosinophils may contribute to long-term pathology following helminth infection.
first_indexed 2024-04-09T13:11:33Z
format Article
id doaj.art-ade0fccd93ea42fbab06b16905afa653
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-04-09T13:11:33Z
publishDate 2023-05-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-ade0fccd93ea42fbab06b16905afa6532023-05-12T07:54:18ZengFrontiers Media S.A.Frontiers in Immunology1664-32242023-05-011410.3389/fimmu.2023.11708071170807Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infectionAlisha Chetty0Matthew G. Darby1Jamie Pillaye2A'ishah Taliep3Adam F. Cunningham4Matthew K. O’Shea5Gnatoulma Katawa6Laura E. Layland7Laura E. Layland8Manuel Ritter9William G. C. Horsnell10William G. C. Horsnell11William G. C. Horsnell12Wellcome Centre for Infectious Diseases Research in Africa, Institute of Infectious Disease and Molecular Medicine, Department of Pathology, Division of Immunology, University of Cape Town, Cape Town, South AfricaWellcome Centre for Infectious Diseases Research in Africa, Institute of Infectious Disease and Molecular Medicine, Department of Pathology, Division of Immunology, University of Cape Town, Cape Town, South AfricaInstitute of Immunology and Immunotherapy, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United KingdomWellcome Centre for Infectious Diseases Research in Africa, Institute of Infectious Disease and Molecular Medicine, Department of Pathology, Division of Immunology, University of Cape Town, Cape Town, South AfricaInstitute of Immunology and Immunotherapy, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United KingdomInstitute of Immunology and Immunotherapy, College of Medical and Dental Sciences, University of Birmingham, Birmingham, United KingdomUnité de Recherche en Immunologie et Immunomodulation (UR2IM)/Laboratoire de Microbiologie et de Contrôle de Qualité des Denrées Alimentaires (LAMICODA), Ecole Supérieure des Techniques Biologiques et Alimentaires, Universite de Lomé, Lomé, TogoGerman Centre for Infection Research (DZIF), Neglected Tropical Disease, Partner site Bonn-Cologne, Bonn, GermanyInstitute for Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn (UKB), Bonn, GermanyInstitute for Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn (UKB), Bonn, GermanyWellcome Centre for Infectious Diseases Research in Africa, Institute of Infectious Disease and Molecular Medicine, Department of Pathology, Division of Immunology, University of Cape Town, Cape Town, South AfricaLaboratory of Molecular and Experimental Immunology and Neuro-genetics, Centre National de la Recherche Scientifique (CNRS)-University of Orleans and Le Studium Institute for Advanced Studies, Orléans, FranceInstitute of Microbiology and Infection, University of Birmingham, Birmingham, United KingdomHelminth-induced eosinophils accumulate around the parasite at the site of infection, or in parasite-damaged tissues well after the helminth has left the site. The role of helminth-elicited eosinophils in mediating parasite control is complex. While they may contribute to direct parasite-killing and tissue repair, their involvement in long-term immunopathogenesis is a concern. In allergic Siglec-FhiCD101hi, eosinophils are associated with pathology. Research has not shown if equivalent subpopulations of eosinophils are a feature of helminth infection. In this study, we demonstrate that lung migration of rodent hookworm Nippostrongylus brasiliensis (Nb) results in a long-term expansion of distinct Siglec-FhiCD101hi eosinophil subpopulations. Nb-elevated eosinophil populations in the bone marrow and circulation did not present this phenotype. Siglec-FhiCD101hi lung eosinophils exhibited an activated morphology including nuclei hyper-segmentation and cytoplasm degranulation. Recruitment of ST2+ ILC2s and not CD4+ T cells to the lungs was associated with the expansion of Siglec-FhiCD101hi eosinophils. This data identifies a morphologically distinct and persistent subset of Siglec-FhiCD101hi lung eosinophils induced following Nb infection. These eosinophils may contribute to long-term pathology following helminth infection.https://www.frontiersin.org/articles/10.3389/fimmu.2023.1170807/fullhelminthsNippostrongylus brasilieniseosinophilsSiglec-FCD101ILC2s
spellingShingle Alisha Chetty
Matthew G. Darby
Jamie Pillaye
A'ishah Taliep
Adam F. Cunningham
Matthew K. O’Shea
Gnatoulma Katawa
Laura E. Layland
Laura E. Layland
Manuel Ritter
William G. C. Horsnell
William G. C. Horsnell
William G. C. Horsnell
Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection
Frontiers in Immunology
helminths
Nippostrongylus brasilienis
eosinophils
Siglec-F
CD101
ILC2s
title Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection
title_full Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection
title_fullStr Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection
title_full_unstemmed Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection
title_short Induction of Siglec-FhiCD101hi eosinophils in the lungs following murine hookworm Nippostrongylus brasiliensis infection
title_sort induction of siglec fhicd101hi eosinophils in the lungs following murine hookworm nippostrongylus brasiliensis infection
topic helminths
Nippostrongylus brasilienis
eosinophils
Siglec-F
CD101
ILC2s
url https://www.frontiersin.org/articles/10.3389/fimmu.2023.1170807/full
work_keys_str_mv AT alishachetty inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT matthewgdarby inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT jamiepillaye inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT aishahtaliep inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT adamfcunningham inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT matthewkoshea inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT gnatoulmakatawa inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT lauraelayland inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT lauraelayland inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT manuelritter inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT williamgchorsnell inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT williamgchorsnell inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection
AT williamgchorsnell inductionofsiglecfhicd101hieosinophilsinthelungsfollowingmurinehookwormnippostrongylusbrasiliensisinfection