Pathological manifestations in lymphatic filariasis correlate with lack of inhibitory properties of IgG4 antibodies on IgE-activated granulocytes
Identifieur interne : 000312 ( Main/Exploration ); précédent : 000311; suivant : 000313Pathological manifestations in lymphatic filariasis correlate with lack of inhibitory properties of IgG4 antibodies on IgE-activated granulocytes
Auteurs : Ulrich F. Prodjinotho [Allemagne] ; Charlotte Von Horn [Allemagne] ; Alex Y. Debrah [Ghana] ; Linda Batsa Debrah [Ghana] ; Anna Albers [Allemagne] ; Laura E. Layland [Allemagne] ; Achim Hoerauf [Allemagne] ; Tomabu Adjobimey [Allemagne, Bénin]Source :
- PLoS Neglected Tropical Diseases [ 1935-2727 ] ; 2017.
Descripteurs français
- KwdFr :
- Adolescent, Adulte, Adulte d'âge moyen, Animaux, Anticorps antihelminthe (sang), Antigènes d'helminthe (immunologie), Brugia malayi, Cytokines (immunologie), Dégranulation cellulaire, Essais contrôlés randomisés comme sujet, Filariose lymphatique (immunologie), Granulocytes (immunologie), Humains, Immunoglobuline E (sang), Immunoglobuline G (sang), Jeune adulte, Mâle, Test ELISA, Études cas-témoins.
- MESH :
- immunologie : Antigènes d'helminthe, Cytokines, Filariose lymphatique, Granulocytes.
- sang : Anticorps antihelminthe, Immunoglobuline E, Immunoglobuline G.
- Adolescent, Adulte, Adulte d'âge moyen, Animaux, Brugia malayi, Dégranulation cellulaire, Essais contrôlés randomisés comme sujet, Humains, Jeune adulte, Mâle, Test ELISA, Études cas-témoins.
English descriptors
- KwdEn :
- Adolescent, Adult, Animals, Antibodies, Helminth (blood), Antigens, Helminth (immunology), Brugia malayi, Case-Control Studies, Cell Degranulation, Cytokines (immunology), Elephantiasis, Filarial (immunology), Enzyme-Linked Immunosorbent Assay, Granulocytes (immunology), Humans, Immunoglobulin E (blood), Immunoglobulin G (blood), Male, Middle Aged, Randomized Controlled Trials as Topic, Young Adult.
- MESH :
- chemical , blood : Antibodies, Helminth, Immunoglobulin E, Immunoglobulin G.
- chemical , immunology : Antigens, Helminth, Cytokines.
- immunology : Elephantiasis, Filarial, Granulocytes.
- Adolescent, Adult, Animals, Brugia malayi, Case-Control Studies, Cell Degranulation, Enzyme-Linked Immunosorbent Assay, Humans, Male, Middle Aged, Randomized Controlled Trials as Topic, Young Adult.
Abstract
Helminth parasites are known to be efficient modulators of their host’s immune system. To guarantee their own survival, they induce alongside the classical Th2 a strong regulatory response with high levels of anti-inflammatory cytokines and elevated plasma levels of IgG4. This particular antibody was shown in different models to exhibit immunosuppressive properties. How IgG4 affects the etiopathology of lymphatic filariasis (LF) is however not well characterized. Here we investigate the impact of plasma and affinity-purified IgG/IgG4 fractions from endemic normals (EN) and LF infected pathology patients (CP), asymptomatic microfilaraemic (Mf+) and amicrofilaraemic (Mf-) individuals on IgE/IL3 activated granulocytes. The activation and degranulation states were investigated by monitoring the expression of CD63/HLADR and the release of granule contents (neutrophil elastase (NE), eosinophil cationic protein (ECP) and histamine) respectively by flow cytometry and ELISA. We could show that the activation of granulocytes was inhibited in the presence of plasma from EN and Mf+ individuals whereas those of Mf- and CP presented no effect. This inhibitory capacity was impaired upon depletion of IgG in Mf+ individuals but persisted in IgG-depleted plasma from EN, where it strongly correlated with the expression of IgA. In addition, IgA-depleted fractions failed to suppress granulocyte activation. Strikingly, affinity-purified IgG4 antibodies from EN, Mf+ and Mf- individuals bound granulocytes and inhibited activation and the release of ECP, NE and histamine. In contrast, IgG4 from CP could not bind granulocytes and presented no suppressive capacity. Reduction of both the affinity to, and the suppressive properties of anti-inflammatory IgG4 on granulocytes was reached only when FcγRI and II were blocked simultaneously. These data indicate that IgG4 antibodies from Mf+, Mf- and EN, in contrast to those of CP, natively exhibit FcγRI/II-dependent suppressive properties on granulocytes. Our findings suggest that quantitative and qualitative alterations in IgG4 molecules are associated with the different clinical phenotypes in LF endemic regions.
Url:
DOI: 10.1371/journal.pntd.0005777
PubMed: 28742098
PubMed Central: 5542694
Affiliations:
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Prodjinotho</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Von Horn, Charlotte" sort="Von Horn, Charlotte" uniqKey="Von Horn C" first="Charlotte" last="Von Horn">Charlotte Von Horn</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Debrah, Alex Y" sort="Debrah, Alex Y" uniqKey="Debrah A" first="Alex Y." last="Debrah">Alex Y. Debrah</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Kumasi Centre for Collaborative Research in Tropical Medicine (KCCR), Kwame Nkrumah University of Science and Technology, Kumasi, Ghana</addr-line></nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Kumasi Centre for Collaborative Research in Tropical Medicine (KCCR), Kwame Nkrumah University of Science and Technology, Kumasi</wicri:regionArea><wicri:noRegion>Kumasi</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff003"><addr-line>Faculty of Allied Health Sciences and School of Medical Sciences, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana</addr-line></nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Faculty of Allied Health Sciences and School of Medical Sciences, Kwame Nkrumah University of Science and Technology, Kumasi</wicri:regionArea><wicri:noRegion>Kumasi</wicri:noRegion></affiliation></author><author><name sortKey="Batsa Debrah, Linda" sort="Batsa Debrah, Linda" uniqKey="Batsa Debrah L" first="Linda" last="Batsa Debrah">Linda Batsa Debrah</name><affiliation wicri:level="1"><nlm:aff id="aff002"><addr-line>Kumasi Centre for Collaborative Research in Tropical Medicine (KCCR), Kwame Nkrumah University of Science and Technology, Kumasi, Ghana</addr-line></nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Kumasi Centre for Collaborative Research in Tropical Medicine (KCCR), Kwame Nkrumah University of Science and Technology, Kumasi</wicri:regionArea><wicri:noRegion>Kumasi</wicri:noRegion></affiliation><affiliation wicri:level="1"><nlm:aff id="aff004"><addr-line>Department of Clinical Microbiology, Kwame Nkrumah University of Science and Technology, Kumasi, Ghana</addr-line></nlm:aff><country xml:lang="fr">Ghana</country><wicri:regionArea>Department of Clinical Microbiology, Kwame Nkrumah University of Science and Technology, Kumasi</wicri:regionArea><wicri:noRegion>Kumasi</wicri:noRegion></affiliation></author><author><name sortKey="Albers, Anna" sort="Albers, Anna" uniqKey="Albers A" first="Anna" last="Albers">Anna Albers</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Layland, Laura E" sort="Layland, Laura E" uniqKey="Layland L" first="Laura E." last="Layland">Laura E. Layland</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Hoerauf, Achim" sort="Hoerauf, Achim" uniqKey="Hoerauf A" first="Achim" last="Hoerauf">Achim Hoerauf</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation><affiliation wicri:level="3"><nlm:aff id="aff005"><addr-line>Bonn-Cologne Site, German Center for Infectious Disease Research (DZIF), Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Bonn-Cologne Site, German Center for Infectious Disease Research (DZIF), Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation></author><author><name sortKey="Adjobimey, Tomabu" sort="Adjobimey, Tomabu" uniqKey="Adjobimey T" first="Tomabu" last="Adjobimey">Tomabu Adjobimey</name><affiliation wicri:level="3"><nlm:aff id="aff001"><addr-line>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn, Germany</addr-line></nlm:aff><country xml:lang="fr">Allemagne</country><wicri:regionArea>Institute of Medical Microbiology, Immunology and Parasitology (IMMIP), University Hospital Bonn, Bonn</wicri:regionArea><placeName><region type="land" nuts="1">Rhénanie-du-Nord-Westphalie</region><region type="district" nuts="2">District de Cologne</region><settlement type="city">Bonn</settlement></placeName></affiliation><affiliation wicri:level="1"><nlm:aff id="aff006"><addr-line>Faculté des Sciences et Techniques (FAST), Université d’Abomey-Calavi, Abomey-Calavi, Bénin</addr-line></nlm:aff><country xml:lang="fr">Bénin</country><wicri:regionArea>Faculté des Sciences et Techniques (FAST), Université d’Abomey-Calavi, Abomey-Calavi</wicri:regionArea><wicri:noRegion>Abomey-Calavi</wicri:noRegion></affiliation></author></analytic><series><title level="j">PLoS Neglected Tropical Diseases</title><idno type="ISSN">1935-2727</idno><idno type="eISSN">1935-2735</idno><imprint><date when="2017">2017</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass><keywords scheme="KwdEn" xml:lang="en"><term>Adolescent</term><term>Adult</term><term>Animals</term><term>Antibodies, Helminth (blood)</term><term>Antigens, Helminth (immunology)</term><term>Brugia malayi</term><term>Case-Control Studies</term><term>Cell Degranulation</term><term>Cytokines (immunology)</term><term>Elephantiasis, Filarial (immunology)</term><term>Enzyme-Linked Immunosorbent Assay</term><term>Granulocytes (immunology)</term><term>Humans</term><term>Immunoglobulin E (blood)</term><term>Immunoglobulin G (blood)</term><term>Male</term><term>Middle Aged</term><term>Randomized Controlled Trials as Topic</term><term>Young Adult</term></keywords><keywords scheme="KwdFr" xml:lang="fr"><term>Adolescent</term><term>Adulte</term><term>Adulte d'âge moyen</term><term>Animaux</term><term>Anticorps antihelminthe (sang)</term><term>Antigènes d'helminthe (immunologie)</term><term>Brugia malayi</term><term>Cytokines (immunologie)</term><term>Dégranulation cellulaire</term><term>Essais contrôlés randomisés comme sujet</term><term>Filariose lymphatique (immunologie)</term><term>Granulocytes (immunologie)</term><term>Humains</term><term>Immunoglobuline E (sang)</term><term>Immunoglobuline G (sang)</term><term>Jeune adulte</term><term>Mâle</term><term>Test ELISA</term><term>Études cas-témoins</term></keywords><keywords scheme="MESH" type="chemical" qualifier="blood" xml:lang="en"><term>Antibodies, Helminth</term><term>Immunoglobulin E</term><term>Immunoglobulin G</term></keywords><keywords scheme="MESH" type="chemical" qualifier="immunology" xml:lang="en"><term>Antigens, Helminth</term><term>Cytokines</term></keywords><keywords scheme="MESH" qualifier="immunologie" xml:lang="fr"><term>Antigènes d'helminthe</term><term>Cytokines</term><term>Filariose lymphatique</term><term>Granulocytes</term></keywords><keywords scheme="MESH" qualifier="immunology" xml:lang="en"><term>Elephantiasis, Filarial</term><term>Granulocytes</term></keywords><keywords scheme="MESH" qualifier="sang" xml:lang="fr"><term>Anticorps antihelminthe</term><term>Immunoglobuline E</term><term>Immunoglobuline G</term></keywords><keywords scheme="MESH" xml:lang="en"><term>Adolescent</term><term>Adult</term><term>Animals</term><term>Brugia malayi</term><term>Case-Control Studies</term><term>Cell Degranulation</term><term>Enzyme-Linked Immunosorbent Assay</term><term>Humans</term><term>Male</term><term>Middle Aged</term><term>Randomized Controlled Trials as Topic</term><term>Young Adult</term></keywords><keywords scheme="MESH" xml:lang="fr"><term>Adolescent</term><term>Adulte</term><term>Adulte d'âge moyen</term><term>Animaux</term><term>Brugia malayi</term><term>Dégranulation cellulaire</term><term>Essais contrôlés randomisés comme sujet</term><term>Humains</term><term>Jeune adulte</term><term>Mâle</term><term>Test ELISA</term><term>Études cas-témoins</term></keywords></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>Helminth parasites are known to be efficient modulators of their host’s immune system. To guarantee their own survival, they induce alongside the classical Th2 a strong regulatory response with high levels of anti-inflammatory cytokines and elevated plasma levels of IgG4. This particular antibody was shown in different models to exhibit immunosuppressive properties. How IgG4 affects the etiopathology of lymphatic filariasis (LF) is however not well characterized. Here we investigate the impact of plasma and affinity-purified IgG/IgG4 fractions from endemic normals (EN) and LF infected pathology patients (CP), asymptomatic microfilaraemic (Mf+) and amicrofilaraemic (Mf-) individuals on IgE/IL3 activated granulocytes. The activation and degranulation states were investigated by monitoring the expression of CD63/HLADR and the release of granule contents (neutrophil elastase (NE), eosinophil cationic protein (ECP) and histamine) respectively by flow cytometry and ELISA. We could show that the activation of granulocytes was inhibited in the presence of plasma from EN and Mf+ individuals whereas those of Mf- and CP presented no effect. This inhibitory capacity was impaired upon depletion of IgG in Mf+ individuals but persisted in IgG-depleted plasma from EN, where it strongly correlated with the expression of IgA. In addition, IgA-depleted fractions failed to suppress granulocyte activation. Strikingly, affinity-purified IgG4 antibodies from EN, Mf+ and Mf- individuals bound granulocytes and inhibited activation and the release of ECP, NE and histamine. In contrast, IgG4 from CP could not bind granulocytes and presented no suppressive capacity. Reduction of both the affinity to, and the suppressive properties of anti-inflammatory IgG4 on granulocytes was reached only when FcγRI and II were blocked simultaneously. These data indicate that IgG4 antibodies from Mf+, Mf- and EN, in contrast to those of CP, natively exhibit FcγRI/II-dependent suppressive properties on granulocytes. Our findings suggest that quantitative and qualitative alterations in IgG4 molecules are associated with the different clinical phenotypes in LF endemic regions.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct></biblStruct><biblStruct><analytic><author><name sortKey="Hoerauf, A" uniqKey="Hoerauf A">A Hoerauf</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Disease, Gbd" uniqKey="Disease G">GBD Disease</name></author><author><name sortKey="Injury, I" uniqKey="Injury I">I Injury</name></author><author><name sortKey="Prevalence, C" uniqKey="Prevalence C">C Prevalence</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Maizels, Rm" uniqKey="Maizels R">RM Maizels</name></author><author><name sortKey="Yazdanbakhsh, M" uniqKey="Yazdanbakhsh M">M Yazdanbakhsh</name></author></analytic></biblStruct><biblStruct><analytic><author><name sortKey="Babu, S" uniqKey="Babu S">S Babu</name></author><author><name 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Prodjinotho</name></region><name sortKey="Adjobimey, Tomabu" sort="Adjobimey, Tomabu" uniqKey="Adjobimey T" first="Tomabu" last="Adjobimey">Tomabu Adjobimey</name><name sortKey="Albers, Anna" sort="Albers, Anna" uniqKey="Albers A" first="Anna" last="Albers">Anna Albers</name><name sortKey="Hoerauf, Achim" sort="Hoerauf, Achim" uniqKey="Hoerauf A" first="Achim" last="Hoerauf">Achim Hoerauf</name><name sortKey="Hoerauf, Achim" sort="Hoerauf, Achim" uniqKey="Hoerauf A" first="Achim" last="Hoerauf">Achim Hoerauf</name><name sortKey="Layland, Laura E" sort="Layland, Laura E" uniqKey="Layland L" first="Laura E." last="Layland">Laura E. Layland</name><name sortKey="Von Horn, Charlotte" sort="Von Horn, Charlotte" uniqKey="Von Horn C" first="Charlotte" last="Von Horn">Charlotte Von Horn</name></country><country name="Ghana"><noRegion><name sortKey="Debrah, Alex Y" sort="Debrah, Alex Y" uniqKey="Debrah A" first="Alex Y." last="Debrah">Alex Y. Debrah</name></noRegion><name sortKey="Batsa Debrah, Linda" sort="Batsa Debrah, Linda" uniqKey="Batsa Debrah L" first="Linda" last="Batsa Debrah">Linda Batsa Debrah</name><name sortKey="Batsa Debrah, Linda" sort="Batsa Debrah, Linda" uniqKey="Batsa Debrah L" first="Linda" last="Batsa Debrah">Linda Batsa Debrah</name><name sortKey="Debrah, Alex Y" sort="Debrah, Alex Y" uniqKey="Debrah A" first="Alex Y." last="Debrah">Alex Y. Debrah</name></country><country name="Bénin"><noRegion><name sortKey="Adjobimey, Tomabu" sort="Adjobimey, Tomabu" uniqKey="Adjobimey T" first="Tomabu" last="Adjobimey">Tomabu Adjobimey</name></noRegion></country></tree></affiliations></record>Pour manipuler ce document sous Unix (Dilib)
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