Concerted activity of IgG1 antibodies and IL-4/IL-25-dependent effector cells trap helminth larvae in the tissues following vaccination with defined secreted antigens, providing sterile immunity to challenge infection
Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet available for human use, and mechanisms of protective immunity remain unclear. In the mouse model of Heligmosomoides polygyrus infection...
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| Published in | PLoS pathogens Vol. 11; no. 3; p. e1004676 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science
01.03.2015
Public Library of Science (PLoS) |
| Subjects | |
| Online Access | Get full text |
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| Abstract | Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet available for human use, and mechanisms of protective immunity remain unclear. In the mouse model of Heligmosomoides polygyrus infection, vaccination with excretory-secretory (HES) antigens from adult parasites elicits sterilising immunity. Notably, three purified HES antigens (VAL-1, -2 and -3) are sufficient for effective vaccination. Protection is fully dependent upon specific IgG1 antibodies, but passive transfer confers only partial immunity to infection, indicating that cellular components are also required. Moreover, immune mice show greater cellular infiltration associated with trapping of larvae in the gut wall prior to their maturation. Intra-vital imaging of infected intestinal tissue revealed a four-fold increase in extravasation by LysM+GFP+ myeloid cells in vaccinated mice, and the massing of these cells around immature larvae. Mice deficient in FcRγ chain or C3 complement component remain fully immune, suggesting that in the presence of antibodies that directly neutralise parasite molecules, the myeloid compartment may attack larvae more quickly and effectively. Immunity to challenge infection was compromised in IL-4Rα- and IL-25-deficient mice, despite levels of specific antibody comparable to immune wild-type controls, while deficiencies in basophils, eosinophils or mast cells or CCR2-dependent inflammatory monocytes did not diminish immunity. Finally, we identify a suite of previously uncharacterised heat-labile vaccine antigens with homologs in human and veterinary parasites that together promote full immunity. Taken together, these data indicate that vaccine-induced immunity to intestinal helminths involves IgG1 antibodies directed against secreted proteins acting in concert with IL-25-dependent Type 2 myeloid effector populations. |
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| AbstractList |
Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet available for human use, and mechanisms of protective immunity remain unclear. In the mouse model of Heligmosomoides polygyrus infection, vaccination with excretory-secretory (HES) antigens from adult parasites elicits sterilising immunity. Notably, three purified HES antigens (VAL-1, -2 and -3) are sufficient for effective vaccination. Protection is fully dependent upon specific IgG1 antibodies, but passive transfer confers only partial immunity to infection, indicating that cellular components are also required. Moreover, immune mice show greater cellular infiltration associated with trapping of larvae in the gut wall prior to their maturation. Intra-vital imaging of infected intestinal tissue revealed a four-fold increase in extravasation by LysM+GFP+ myeloid cells in vaccinated mice, and the massing of these cells around immature larvae. Mice deficient in FcRγ chain or C3 complement component remain fully immune, suggesting that in the presence of antibodies that directly neutralise parasite molecules, the myeloid compartment may attack larvae more quickly and effectively. Immunity to challenge infection was compromised in IL-4Rα- and IL-25-deficient mice, despite levels of specific antibody comparable to immune wild-type controls, while deficiencies in basophils, eosinophils or mast cells or CCR2-dependent inflammatory monocytes did not diminish immunity. Finally, we identify a suite of previously uncharacterised heat-labile vaccine antigens with homologs in human and veterinary parasites that together promote full immunity. Taken together, these data indicate that vaccine-induced immunity to intestinal helminths involves IgG1 antibodies directed against secreted proteins acting in concert with IL-25-dependent Type 2 myeloid effector populations. Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet available for human use, and mechanisms of protective immunity remain unclear. In the mouse model of Heligmosomoides polygyrus infection, vaccination with excretory-secretory (HES) antigens from adult parasites elicits sterilising immunity. Notably, three purified HES antigens (VAL-1, -2 and -3) are sufficient for effective vaccination. Protection is fully dependent upon specific IgG1 antibodies, but passive transfer confers only partial immunity to infection, indicating that cellular components are also required. Moreover, immune mice show greater cellular infiltration associated with trapping of larvae in the gut wall prior to their maturation. Intravital imaging of infected intestinal tissue revealed a four-fold increase in extravasation by [LysM.sup.+][GFP.sup.+] myeloid cells in vaccinated mice, and the massing of these cells around immature larvae. Mice deficient in FcRy chain or C3 complement component remain fully immune, suggesting that in the presence of antibodies that directly neutralise parasite molecules, the myeloid compartment may attack larvae more quickly and effectively. Immunity to challenge infection was compromised in IL-4R[alpha]-and IL-25-deficient mice, despite levels of specific antibody comparable to immune wild-type controls, while deficiencies in basophils, eosinophils or mast cells or CCR2-dependent inflammatory monocytes did not diminish immunity. Finally, we identify a suite of previously uncharacterised heat-labile vaccine antigens with homologs in human and veterinary parasites that together promote full immunity. Taken together, these data indicate that vaccine-induced immunity to intestinal helminths involves IgG1 antibodies directed against secreted proteins acting in concert with IL-25-dependent Type 2 myeloid effector populations. Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet available for human use, and mechanisms of protective immunity remain unclear. In the mouse model of Heligmosomoides polygyrus infection, vaccination with excretory-secretory (HES) antigens from adult parasites elicits sterilising immunity. Notably, three purified HES antigens (VAL-1, -2 and -3) are sufficient for effective vaccination. Protection is fully dependent upon specific IgG1 antibodies, but passive transfer confers only partial immunity to infection, indicating that cellular components are also required. Moreover, immune mice show greater cellular infiltration associated with trapping of larvae in the gut wall prior to their maturation. Intra-vital imaging of infected intestinal tissue revealed a four-fold increase in extravasation by LysM+GFP+ myeloid cells in vaccinated mice, and the massing of these cells around immature larvae. Mice deficient in FcRγ chain or C3 complement component remain fully immune, suggesting that in the presence of antibodies that directly neutralise parasite molecules, the myeloid compartment may attack larvae more quickly and effectively. Immunity to challenge infection was compromised in IL-4Rα- and IL-25-deficient mice, despite levels of specific antibody comparable to immune wild-type controls, while deficiencies in basophils, eosinophils or mast cells or CCR2-dependent inflammatory monocytes did not diminish immunity. Finally, we identify a suite of previously uncharacterised heat-labile vaccine antigens with homologs in human and veterinary parasites that together promote full immunity. Taken together, these data indicate that vaccine-induced immunity to intestinal helminths involves IgG1 antibodies directed against secreted proteins acting in concert with IL-25-dependent Type 2 myeloid effector populations. Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet available for human use, and mechanisms of protective immunity remain unclear. In the mouse model of Heligmosomoides polygyrus infection, vaccination with excretory-secretory (HES) antigens from adult parasites elicits sterilising immunity. Notably, three purified HES antigens (VAL-1, -2 and -3) are sufficient for effective vaccination. Protection is fully dependent upon specific IgG1 antibodies, but passive transfer confers only partial immunity to infection, indicating that cellular components are also required. Moreover, immune mice show greater cellular infiltration associated with trapping of larvae in the gut wall prior to their maturation. Intra-vital imaging of infected intestinal tissue revealed a four-fold increase in extravasation by LysM + GFP + myeloid cells in vaccinated mice, and the massing of these cells around immature larvae. Mice deficient in FcRγ chain or C3 complement component remain fully immune, suggesting that in the presence of antibodies that directly neutralise parasite molecules, the myeloid compartment may attack larvae more quickly and effectively. Immunity to challenge infection was compromised in IL-4Rα- and IL-25-deficient mice, despite levels of specific antibody comparable to immune wild-type controls, while deficiencies in basophils, eosinophils or mast cells or CCR2-dependent inflammatory monocytes did not diminish immunity. Finally, we identify a suite of previously uncharacterised heat-labile vaccine antigens with homologs in human and veterinary parasites that together promote full immunity. Taken together, these data indicate that vaccine-induced immunity to intestinal helminths involves IgG1 antibodies directed against secreted proteins acting in concert with IL-25-dependent Type 2 myeloid effector populations. Despite the high prevalence of gastrointestinal helminth parasites in human and animal populations throughout the world, no vaccines are yet available and we lack understanding of how anti-parasite protective immunity may operate effectively. We have used a model system with a natural mouse nematode parasite, Heligmosomoides polygyrus , which establishes long-term chronic infection in laboratory mice through the secretion of immunosuppressive molecules. Immunization of mice with as few as 3 secreted proteins, collected from parasites in vitro, confers complete immunity to challenge infection. We show here that immunity requires specific IgG1 antibodies directed to the secreted products, acting together with innate myeloid cells that require activation through the canonical Type 2 cytokine receptor, IL-4Rα, as well as through a pathway not previously known to be involved in effector mechanisms, IL-25. These myeloid cells act to trap and envelop helminth larvae while in the submucosal tissues of the small intestine, massing in large numbers and preventing their maturation and exit into the gut lumen. Thus the combined effects of specific antibodies from the adaptive immune system, and Type 2 cytokine activation of the innate immune system, co-operate to ensure elimination of the helminth parasite. |
| Audience | Academic |
| Author | Harcus, Yvonne Filbey, Kara J Yang, Lihua Le Gros, Graham Maizels, Rick M Voehringer, David Tu, Yizheng Huang, Stanley Ching-Cheng Schwartz, Christian Hewitson, James P Murray, Janice Reynolds, Lisa A Boon, Louis Harris, Nicola Miller, Mark J Camberis, Mali Robertson, Elaine Esser-von Bieren, Julia Blair, Natalie |
| AuthorAffiliation | 1 Institute of Immunology and Infection Research, and Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom New York University, UNITED STATES 2 École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland 4 Department of Infection Biology, University Clinic Erlangen, Erlangen, Germany 3 Malaghan Institute, Wellington, New Zealand 5 Bioceros Holding BV, Utrecht, The Netherlands 7 Department of Internal Medicine, Washington University in St. Louis, St. Louis, Missouri, United States of America 6 Department of Pathology and Immunology, Washington University in St. Louis, St. Louis, Missouri, United States of America |
| AuthorAffiliation_xml | – name: 1 Institute of Immunology and Infection Research, and Centre for Immunity, Infection and Evolution, University of Edinburgh, Edinburgh, United Kingdom – name: 2 École Polytechnique Fédérale de Lausanne, Lausanne, Switzerland – name: 7 Department of Internal Medicine, Washington University in St. Louis, St. Louis, Missouri, United States of America – name: 3 Malaghan Institute, Wellington, New Zealand – name: 6 Department of Pathology and Immunology, Washington University in St. Louis, St. Louis, Missouri, United States of America – name: 4 Department of Infection Biology, University Clinic Erlangen, Erlangen, Germany – name: 5 Bioceros Holding BV, Utrecht, The Netherlands – name: New York University, UNITED STATES |
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| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/25816012$$D View this record in MEDLINE/PubMed |
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| Copyright | COPYRIGHT 2015 Public Library of Science 2015 Hewitson et al 2015 Hewitson et al 2015 Public Library of Science. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Hewitson JP, Filbey KJ, Esser-von Bieren J, Camberis M, Schwartz C, Murray J, et al. (2015) Concerted Activity of IgG1 Antibodies and IL-4/IL-25-Dependent Effector Cells Trap Helminth Larvae in the Tissues following Vaccination with Defined Secreted Antigens, Providing Sterile Immunity to Challenge Infection. PLoS Pathog 11(3): e1004676. doi:10.1371/journal.ppat.1004676 |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 23 Conceived and designed the experiments: JPH MJM DV GLG NH RMM. Performed the experiments: KJF JEvB MC CS JM LAR NB ER YH SCCH LY YT. Analyzed the data: JPH JEvB MC CS LAR MJM DV GLG NH RMM. Contributed reagents/materials/analysis tools: ER YH LB. Wrote the paper: JPH RMM. The authors have declared that no competing interests exist. |
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| Snippet | Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is yet... Over 25% of the world's population are infected with helminth parasites, the majority of which colonise the gastrointestinal tract. However, no vaccine is... |
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| SubjectTerms | Animals Antibodies Antibodies, Helminth - genetics Antibodies, Helminth - immunology Antigens Antigens, Helminth - immunology Councils Experiments Health aspects Helminths Host-parasite relationships Humans Identification and classification Immune system Immunoglobulin G Immunoglobulin G - genetics Immunoglobulin G - immunology Infections Interleukin-4 - genetics Interleukin-4 - immunology Interleukins Interleukins - genetics Interleukins - immunology Larva - immunology Mice Mice, Knockout Nematospiroides dubius - immunology Parasites Rodents Strongylida Infections - genetics Strongylida Infections - immunology Strongylida Infections - prevention & control Vaccination Vaccines |
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| Title | Concerted activity of IgG1 antibodies and IL-4/IL-25-dependent effector cells trap helminth larvae in the tissues following vaccination with defined secreted antigens, providing sterile immunity to challenge infection |
| URI | https://www.ncbi.nlm.nih.gov/pubmed/25816012 https://search.proquest.com/docview/1667961159 https://pubmed.ncbi.nlm.nih.gov/PMC4376884 https://doaj.org/article/54914d01b559441e841ee0d05556fec2 http://dx.doi.org/10.1371/journal.ppat.1004676 |
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