H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection
Nematodes are one of the largest groups of animals on the planet. Many of them are major pathogens of humans, animals and plants, and cause destructive diseases and socioeconomic losses worldwide. Despite their adverse impacts on human health and agriculture, nematodes can be challenging to control,...
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| Format: | Article |
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Frontiers Media S.A.
2022-10-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1034820/full |
| _version_ | 1811255310188281856 |
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| author | Chunqun Wang Lu Liu Tianjiao Wang Xin Liu Wenjie Peng Ratnesh Kumar Srivastav Xing-Quan Zhu Nishith Gupta Nishith Gupta Nishith Gupta Robin B. Gasser Min Hu |
| author_facet | Chunqun Wang Lu Liu Tianjiao Wang Xin Liu Wenjie Peng Ratnesh Kumar Srivastav Xing-Quan Zhu Nishith Gupta Nishith Gupta Nishith Gupta Robin B. Gasser Min Hu |
| author_sort | Chunqun Wang |
| collection | DOAJ |
| description | Nematodes are one of the largest groups of animals on the planet. Many of them are major pathogens of humans, animals and plants, and cause destructive diseases and socioeconomic losses worldwide. Despite their adverse impacts on human health and agriculture, nematodes can be challenging to control, because anthelmintic treatments do not prevent re-infection, and excessive treatment has led to widespread drug resistance in nematode populations. Indeed, many nematode species of livestock animals have become resistant to almost all classes of anthelmintics used. Most efforts to develop commercial anti-nematode vaccines (native or recombinant) for use in animals and humans have not succeeded, although one effective (dead) vaccine (Barbervax) has been developed to protect animals against one of the most pathogenic parasites of livestock animals – Haemonchus contortus (the barber’s pole worm). This vaccine contains native molecules, called H11 and H-Gal-GP, derived from the intestine of this blood-feeding worm. In its native form, H11 alone consistently induces high levels (75-95%) of immunoprotection in animals against disease (haemonchosis), but recombinant forms thereof do not. Here, to test the hypothesis that post-translational modification (glycosylation) of H11 plays a crucial role in achieving such high immunoprotection, we explored the N-glycoproteome and N-glycome of H11 using the high-resolution mass spectrometry and assessed the roles of N-glycosylation in protective immunity against H. contortus. Our results showed conclusively that N-glycan moieties on H11 are the dominant immunogens, which induce high IgG serum antibody levels in immunised animals, and that anti-H11 IgG antibodies can confer specific, passive immunity in naïve animals. This work provides the first detailed account of the relevance and role of protein glycosylation in protective immunity against a parasitic nematode, with important implications for the design of vaccines against metazoan parasites. |
| first_indexed | 2024-04-12T17:21:56Z |
| format | Article |
| id | doaj.art-b16368492cfa4c3bba9dc2eb51b13b9c |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-04-12T17:21:56Z |
| publishDate | 2022-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Immunology |
| spelling | doaj.art-b16368492cfa4c3bba9dc2eb51b13b9c2022-12-22T03:23:27ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-10-011310.3389/fimmu.2022.10348201034820H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infectionChunqun Wang0Lu Liu1Tianjiao Wang2Xin Liu3Wenjie Peng4Ratnesh Kumar Srivastav5Xing-Quan Zhu6Nishith Gupta7Nishith Gupta8Nishith Gupta9Robin B. Gasser10Min Hu11State Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, ChinaState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, ChinaCollege of Life Science and Technology, Huazhong University of Science and Technology, Wuhan, ChinaShanghai Center for Systems Biomedicine, Shanghai Jiao Tong University, Shanghai, ChinaDepartment of Biological Sciences, Birla Institute of Technology and Science – Pilani (BITS-P), Hyderabad, IndiaCollege of Veterinary Medicine, Shanxi Agricultural University, Jinzhong, ChinaState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, ChinaDepartment of Biological Sciences, Birla Institute of Technology and Science – Pilani (BITS-P), Hyderabad, IndiaDepartment of Molecular Parasitology, Faculty of Life Sciences, Humboldt University, Berlin, GermanyMelbourne Veterinary School, The University of Melbourne, Parkville, VIC, AustraliaState Key Laboratory of Agricultural Microbiology, College of Veterinary Medicine, Huazhong Agricultural University, Wuhan, ChinaNematodes are one of the largest groups of animals on the planet. Many of them are major pathogens of humans, animals and plants, and cause destructive diseases and socioeconomic losses worldwide. Despite their adverse impacts on human health and agriculture, nematodes can be challenging to control, because anthelmintic treatments do not prevent re-infection, and excessive treatment has led to widespread drug resistance in nematode populations. Indeed, many nematode species of livestock animals have become resistant to almost all classes of anthelmintics used. Most efforts to develop commercial anti-nematode vaccines (native or recombinant) for use in animals and humans have not succeeded, although one effective (dead) vaccine (Barbervax) has been developed to protect animals against one of the most pathogenic parasites of livestock animals – Haemonchus contortus (the barber’s pole worm). This vaccine contains native molecules, called H11 and H-Gal-GP, derived from the intestine of this blood-feeding worm. In its native form, H11 alone consistently induces high levels (75-95%) of immunoprotection in animals against disease (haemonchosis), but recombinant forms thereof do not. Here, to test the hypothesis that post-translational modification (glycosylation) of H11 plays a crucial role in achieving such high immunoprotection, we explored the N-glycoproteome and N-glycome of H11 using the high-resolution mass spectrometry and assessed the roles of N-glycosylation in protective immunity against H. contortus. Our results showed conclusively that N-glycan moieties on H11 are the dominant immunogens, which induce high IgG serum antibody levels in immunised animals, and that anti-H11 IgG antibodies can confer specific, passive immunity in naïve animals. This work provides the first detailed account of the relevance and role of protein glycosylation in protective immunity against a parasitic nematode, with important implications for the design of vaccines against metazoan parasites.https://www.frontiersin.org/articles/10.3389/fimmu.2022.1034820/fullparasitic nematodevaccineH11 antigenN-glycosylationN-glycanIgG antibodies |
| spellingShingle | Chunqun Wang Lu Liu Tianjiao Wang Xin Liu Wenjie Peng Ratnesh Kumar Srivastav Xing-Quan Zhu Nishith Gupta Nishith Gupta Nishith Gupta Robin B. Gasser Min Hu H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection Frontiers in Immunology parasitic nematode vaccine H11 antigen N-glycosylation N-glycan IgG antibodies |
| title | H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection |
| title_full | H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection |
| title_fullStr | H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection |
| title_full_unstemmed | H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection |
| title_short | H11-induced immunoprotection is predominantly linked to N-glycan moieties during Haemonchus contortus infection |
| title_sort | h11 induced immunoprotection is predominantly linked to n glycan moieties during haemonchus contortus infection |
| topic | parasitic nematode vaccine H11 antigen N-glycosylation N-glycan IgG antibodies |
| url | https://www.frontiersin.org/articles/10.3389/fimmu.2022.1034820/full |
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