Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>

While the lung is considered an efficient site for stopping the larvae of the acute <i>Schistosoma</i> spp. infection phase from migrating through extensive inflammatory responses in the surrounding tissues, little is known about these processes. To date, the highest resistance to infect...

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Main Authors: Miriam Bischofsberger, Cindy Reinholdt, Tim Alexander Dannenhaus, Johann Aleith, Wendy Bergmann-Ewert, Brigitte Müller-Hilke, Micha Löbermann, Emil C. Reisinger, Martina Sombetzki
Format: Article
Language:English
Published: MDPI AG 2023-12-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/12/12/1432
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author Miriam Bischofsberger
Cindy Reinholdt
Tim Alexander Dannenhaus
Johann Aleith
Wendy Bergmann-Ewert
Brigitte Müller-Hilke
Micha Löbermann
Emil C. Reisinger
Martina Sombetzki
author_facet Miriam Bischofsberger
Cindy Reinholdt
Tim Alexander Dannenhaus
Johann Aleith
Wendy Bergmann-Ewert
Brigitte Müller-Hilke
Micha Löbermann
Emil C. Reisinger
Martina Sombetzki
author_sort Miriam Bischofsberger
collection DOAJ
description While the lung is considered an efficient site for stopping the larvae of the acute <i>Schistosoma</i> spp. infection phase from migrating through extensive inflammatory responses in the surrounding tissues, little is known about these processes. To date, the highest resistance to infection has been achieved in experimental studies with radiation-attenuated cercariae immunization, which elicits a strong Th1/Th2 response in the lung and results in up to 80% protection. Based on our own studies demonstrating a systemic, unpolarized Th1/Th2 response resulting from infection with male or female <i>Schistosoma mansoni</i>, we hypothesize that this atypical immune response is already detectable during the pulmonary passage of parasite larvae. Therefore, we examined the immune milieu in the lungs of mice caused by migrating schistosome larvae, either male or female (single-sex groups) or male + female (bisexual control), 4 and 16 days after infection in bronchoalveolar lavage and lung tissue by flow cytometry, qPCR, and multiplex analyzes. Our results show only minor differences in the inflammatory profile between the single-sex groups but significant differences compared with the bisexual control group. Both single-sex infected groups have increased expression of inflammatory markers in lung tissue, higher numbers of cytotoxic T cells (day 4 post-infection) and more T helper cells (day 16 post-infection), compared with the bisexual control group. A single-sex infection, regardless of whether it is an infection with male or female cercariae, causes an immune milieu in the lung that is clearly different from an infection with both sexes. In terms of identifying therapeutic targets to achieve resistance to re-infection, it is of great scientific interest to identify the differences in the inflammatory potential of male or female and male + female parasites.
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spelling doaj.art-dc4bcb103afd496e984133a837727a8e2023-12-22T14:30:58ZengMDPI AGPathogens2076-08172023-12-011212143210.3390/pathogens12121432Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>Miriam Bischofsberger0Cindy Reinholdt1Tim Alexander Dannenhaus2Johann Aleith3Wendy Bergmann-Ewert4Brigitte Müller-Hilke5Micha Löbermann6Emil C. Reisinger7Martina Sombetzki8Division of Tropical Medicine and Infectious Diseases, Center of Internal Medicine II, Rostock University Medical Center, Ernst-Heydemann-Straße 6, 18057 Rostock, GermanyDivision of Tropical Medicine and Infectious Diseases, Center of Internal Medicine II, Rostock University Medical Center, Ernst-Heydemann-Straße 6, 18057 Rostock, GermanyDivision of Tropical Medicine and Infectious Diseases, Center of Internal Medicine II, Rostock University Medical Center, Ernst-Heydemann-Straße 6, 18057 Rostock, GermanyCore Facility for Cell Sorting and Cell Analysis, Rostock University Medical Center, 18057 Rostock, GermanyCore Facility for Cell Sorting and Cell Analysis, Rostock University Medical Center, 18057 Rostock, GermanyCore Facility for Cell Sorting and Cell Analysis, Rostock University Medical Center, 18057 Rostock, GermanyDivision of Tropical Medicine and Infectious Diseases, Center of Internal Medicine II, Rostock University Medical Center, Ernst-Heydemann-Straße 6, 18057 Rostock, GermanyDivision of Tropical Medicine and Infectious Diseases, Center of Internal Medicine II, Rostock University Medical Center, Ernst-Heydemann-Straße 6, 18057 Rostock, GermanyDivision of Tropical Medicine and Infectious Diseases, Center of Internal Medicine II, Rostock University Medical Center, Ernst-Heydemann-Straße 6, 18057 Rostock, GermanyWhile the lung is considered an efficient site for stopping the larvae of the acute <i>Schistosoma</i> spp. infection phase from migrating through extensive inflammatory responses in the surrounding tissues, little is known about these processes. To date, the highest resistance to infection has been achieved in experimental studies with radiation-attenuated cercariae immunization, which elicits a strong Th1/Th2 response in the lung and results in up to 80% protection. Based on our own studies demonstrating a systemic, unpolarized Th1/Th2 response resulting from infection with male or female <i>Schistosoma mansoni</i>, we hypothesize that this atypical immune response is already detectable during the pulmonary passage of parasite larvae. Therefore, we examined the immune milieu in the lungs of mice caused by migrating schistosome larvae, either male or female (single-sex groups) or male + female (bisexual control), 4 and 16 days after infection in bronchoalveolar lavage and lung tissue by flow cytometry, qPCR, and multiplex analyzes. Our results show only minor differences in the inflammatory profile between the single-sex groups but significant differences compared with the bisexual control group. Both single-sex infected groups have increased expression of inflammatory markers in lung tissue, higher numbers of cytotoxic T cells (day 4 post-infection) and more T helper cells (day 16 post-infection), compared with the bisexual control group. A single-sex infection, regardless of whether it is an infection with male or female cercariae, causes an immune milieu in the lung that is clearly different from an infection with both sexes. In terms of identifying therapeutic targets to achieve resistance to re-infection, it is of great scientific interest to identify the differences in the inflammatory potential of male or female and male + female parasites.https://www.mdpi.com/2076-0817/12/12/1432<i>Schistosoma mansoni</i> infectionlung stage larvaesingle-sex infectionimmune milieulung inflammation
spellingShingle Miriam Bischofsberger
Cindy Reinholdt
Tim Alexander Dannenhaus
Johann Aleith
Wendy Bergmann-Ewert
Brigitte Müller-Hilke
Micha Löbermann
Emil C. Reisinger
Martina Sombetzki
Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>
Pathogens
<i>Schistosoma mansoni</i> infection
lung stage larvae
single-sex infection
immune milieu
lung inflammation
title Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>
title_full Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>
title_fullStr Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>
title_full_unstemmed Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>
title_short Individually or as a Team—The Immunological Milieu in the Lung Caused by Migrating Single-Sex or Mixed-Sex Larvae of <i>Schistosoma mansoni</i>
title_sort individually or as a team the immunological milieu in the lung caused by migrating single sex or mixed sex larvae of i schistosoma mansoni i
topic <i>Schistosoma mansoni</i> infection
lung stage larvae
single-sex infection
immune milieu
lung inflammation
url https://www.mdpi.com/2076-0817/12/12/1432
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