Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.

The filarial nematode Mansonella perstans is endemic throughout Africa, northern South America and the Caribbean. Interestingly, M. perstans-infected individuals present no distinct clinical picture associated with certain pathology. Due to its relatively silent nature, research on this tropical dis...

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Main Authors: Manuel Ritter, Winston Patrick Chounna Ndongmo, Abdel Jelil Njouendou, Nora Nganyewo Nghochuzie, Lucy Cho Nchang, Dizzle Bita Tayong, Kathrin Arndts, Norman Nausch, Marc Jacobsen, Samuel Wanji, Laura E Layland, Achim Hoerauf
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2018-01-01
Series:PLoS Neglected Tropical Diseases
Online Access:http://europepmc.org/articles/PMC5783424?pdf=render
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author Manuel Ritter
Winston Patrick Chounna Ndongmo
Abdel Jelil Njouendou
Nora Nganyewo Nghochuzie
Lucy Cho Nchang
Dizzle Bita Tayong
Kathrin Arndts
Norman Nausch
Marc Jacobsen
Samuel Wanji
Laura E Layland
Achim Hoerauf
author_facet Manuel Ritter
Winston Patrick Chounna Ndongmo
Abdel Jelil Njouendou
Nora Nganyewo Nghochuzie
Lucy Cho Nchang
Dizzle Bita Tayong
Kathrin Arndts
Norman Nausch
Marc Jacobsen
Samuel Wanji
Laura E Layland
Achim Hoerauf
author_sort Manuel Ritter
collection DOAJ
description The filarial nematode Mansonella perstans is endemic throughout Africa, northern South America and the Caribbean. Interestingly, M. perstans-infected individuals present no distinct clinical picture associated with certain pathology. Due to its relatively silent nature, research on this tropical disease has been neglected, especially M. perstans-driven immune responses. A hindrance in obtaining data on M. perstans-specific responses has been the inability to obtain adult worms since their habitats in serous cavities are difficult to access. Thus, in this study, for the first time, we used Mansonella perstans worm antigen extract as stimulant to obtain filarial-specific recall and immunoglobulin responses from M. perstans microfilaremic individuals (Mp MF+) from Cameroon. Moreover, systemic immune profiles in sera and immune cell composition in peripheral blood from Mp MF+ and amicrofilaremic individuals (Mp MF-) were obtained. Our data reveal that Mp MF+ individuals showed significantly reduced cytokine (IL-4, IL-6 and IL-12p70) and chemokine levels (IL-8 and RANTES), but significantly higher MIP-1β as well as increased M. perstans-specific IgG4 levels compared to Mp MF- individuals. In contrast, upon re-stimulation with worm antigen extract, IFN-γ, IL-13, IL-10 and IL-17A secretion was enhanced in cell cultures from Mp MF+ individuals when compared to those from cultures of healthy European individuals. Moreover, analysis of immune cell composition in peripheral blood from Mp MF+ individuals revealed increased type 2 helper T (Th2), natural killer (NK), regulatory B and T cell (Breg and Treg) subsets but decreased type 1 regulatory T (Tr1) cells. In summary, this study deciphers for the first time, M. perstans-specific immune responses using worm antigen extract and shows that patent M. perstans infections have distinct Th2, Breg and Treg subsets accompanied with reduced systemic innate and adaptive immune responses and dominant filarial-specific IgG4 levels.
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spelling doaj.art-4b434c0348e54c80b258749a3d792fa62022-12-22T03:16:08ZengPublic Library of Science (PLoS)PLoS Neglected Tropical Diseases1935-27271935-27352018-01-01121e000618410.1371/journal.pntd.0006184Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.Manuel RitterWinston Patrick Chounna NdongmoAbdel Jelil NjouendouNora Nganyewo NghochuzieLucy Cho NchangDizzle Bita TayongKathrin ArndtsNorman NauschMarc JacobsenSamuel WanjiLaura E LaylandAchim HoeraufThe filarial nematode Mansonella perstans is endemic throughout Africa, northern South America and the Caribbean. Interestingly, M. perstans-infected individuals present no distinct clinical picture associated with certain pathology. Due to its relatively silent nature, research on this tropical disease has been neglected, especially M. perstans-driven immune responses. A hindrance in obtaining data on M. perstans-specific responses has been the inability to obtain adult worms since their habitats in serous cavities are difficult to access. Thus, in this study, for the first time, we used Mansonella perstans worm antigen extract as stimulant to obtain filarial-specific recall and immunoglobulin responses from M. perstans microfilaremic individuals (Mp MF+) from Cameroon. Moreover, systemic immune profiles in sera and immune cell composition in peripheral blood from Mp MF+ and amicrofilaremic individuals (Mp MF-) were obtained. Our data reveal that Mp MF+ individuals showed significantly reduced cytokine (IL-4, IL-6 and IL-12p70) and chemokine levels (IL-8 and RANTES), but significantly higher MIP-1β as well as increased M. perstans-specific IgG4 levels compared to Mp MF- individuals. In contrast, upon re-stimulation with worm antigen extract, IFN-γ, IL-13, IL-10 and IL-17A secretion was enhanced in cell cultures from Mp MF+ individuals when compared to those from cultures of healthy European individuals. Moreover, analysis of immune cell composition in peripheral blood from Mp MF+ individuals revealed increased type 2 helper T (Th2), natural killer (NK), regulatory B and T cell (Breg and Treg) subsets but decreased type 1 regulatory T (Tr1) cells. In summary, this study deciphers for the first time, M. perstans-specific immune responses using worm antigen extract and shows that patent M. perstans infections have distinct Th2, Breg and Treg subsets accompanied with reduced systemic innate and adaptive immune responses and dominant filarial-specific IgG4 levels.http://europepmc.org/articles/PMC5783424?pdf=render
spellingShingle Manuel Ritter
Winston Patrick Chounna Ndongmo
Abdel Jelil Njouendou
Nora Nganyewo Nghochuzie
Lucy Cho Nchang
Dizzle Bita Tayong
Kathrin Arndts
Norman Nausch
Marc Jacobsen
Samuel Wanji
Laura E Layland
Achim Hoerauf
Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.
PLoS Neglected Tropical Diseases
title Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.
title_full Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.
title_fullStr Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.
title_full_unstemmed Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.
title_short Mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper T and regulatory T and B cell subsets and dampened systemic innate and adaptive immune responses.
title_sort mansonella perstans microfilaremic individuals are characterized by enhanced type 2 helper t and regulatory t and b cell subsets and dampened systemic innate and adaptive immune responses
url http://europepmc.org/articles/PMC5783424?pdf=render
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