{"title":"Immune modulation of buffalo peripheral blood mononuclear cells by two asparaginyl endopeptidases from Fasciola gigantica.","authors":"Dong-Qi Wu, Yan-Feng Guo, Yu Zou, Xiao-Ting Tang, Wei-Yu Zhang, Wen-Da Di","doi":"10.1186/s13071-024-06570-5","DOIUrl":null,"url":null,"abstract":"<p><strong>Background: </strong>Fascioliasis is a zoonotic parasitic disease caused by Fasciola hepatica and Fasciola gigantica, which poses a serious threat to global public health and livestock farming. Fasciola gigantica secretes and excretes various components to manipulate the immune response, thereby enhancing its invasion, migration, and survival in vivo. However, the roles of specific components in immune modulation, such as asparagine endopeptidase, remain unknown.</p><p><strong>Methods: </strong>The transcriptional abundance of members of the asparagine endopeptidase family (also known as the legumain family) from F. gigantica was analyzed. Two highly transcribed asparagine endopeptidases in metacercariae, juveniles and adults were cloned, and their recombinant proteins-recombinant F. gigantica legumain (rFgLGMN-1) and (rFgLGMN-2)-were expressed in prokaryotic expression system. Their regulatory effects on buffalo peripheral blood mononuclear cells (PBMCs), including proliferation, migration, total nitric oxide (NO) production, cytokine secretion, and phagocytosis were explored in vitro.</p><p><strong>Results: </strong>Ten members of the legumain family were detected in F. gigantica, among of which FgLGMN-1 and FgLGMN-2 exhibited high transcription levels in juveniles and adults. The isolation of sequences indicated that FgLGMN-1 encodes 409 amino acids, while FgLGMN-2 encodes 403 amino acids. Both recombinant FgLGMN-1 (rFgLGMN-1) and rFgLGMN-2 were recognized by serum from buffaloes infected with F. gigantica. Both rFgLGMN-1 and rFgLGMN-2 inhibited the proliferation of PBMCs, and rFgLGMN-1 also inhibited the migration of PBMCs. While rFgLGMN-1 increased the production of total NO, rFgLGMN-2 decreased NO production. Both rFgLGMN-1 and rFgLGMN-2 increased the transcription of the cytokines interleukin-10 and transforming growth factor β. The effect of rFgLGMN-1 and rFgLGMN-2 on the phagocytosis of PBMCs varied depending on their concentrations.</p><p><strong>Conclusions: </strong>rFgLGMN-1 and rFgLGMN-2 modulate several cellular and immunological functions of PBMCs, and exhibited distinct regulatory effects on these in vitro, which indicated that they may play roles in immune modulation and facilitate fluke development. However, due to uncertainties associated with in vitro experiments, further studies are necessary to elucidate the precise functions of these legumains.</p>","PeriodicalId":19793,"journal":{"name":"Parasites & Vectors","volume":"17 1","pages":"516"},"PeriodicalIF":3.0000,"publicationDate":"2024-12-18","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11656647/pdf/","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"Parasites & Vectors","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1186/s13071-024-06570-5","RegionNum":2,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"PARASITOLOGY","Score":null,"Total":0}
引用次数: 0
Abstract
Background: Fascioliasis is a zoonotic parasitic disease caused by Fasciola hepatica and Fasciola gigantica, which poses a serious threat to global public health and livestock farming. Fasciola gigantica secretes and excretes various components to manipulate the immune response, thereby enhancing its invasion, migration, and survival in vivo. However, the roles of specific components in immune modulation, such as asparagine endopeptidase, remain unknown.
Methods: The transcriptional abundance of members of the asparagine endopeptidase family (also known as the legumain family) from F. gigantica was analyzed. Two highly transcribed asparagine endopeptidases in metacercariae, juveniles and adults were cloned, and their recombinant proteins-recombinant F. gigantica legumain (rFgLGMN-1) and (rFgLGMN-2)-were expressed in prokaryotic expression system. Their regulatory effects on buffalo peripheral blood mononuclear cells (PBMCs), including proliferation, migration, total nitric oxide (NO) production, cytokine secretion, and phagocytosis were explored in vitro.
Results: Ten members of the legumain family were detected in F. gigantica, among of which FgLGMN-1 and FgLGMN-2 exhibited high transcription levels in juveniles and adults. The isolation of sequences indicated that FgLGMN-1 encodes 409 amino acids, while FgLGMN-2 encodes 403 amino acids. Both recombinant FgLGMN-1 (rFgLGMN-1) and rFgLGMN-2 were recognized by serum from buffaloes infected with F. gigantica. Both rFgLGMN-1 and rFgLGMN-2 inhibited the proliferation of PBMCs, and rFgLGMN-1 also inhibited the migration of PBMCs. While rFgLGMN-1 increased the production of total NO, rFgLGMN-2 decreased NO production. Both rFgLGMN-1 and rFgLGMN-2 increased the transcription of the cytokines interleukin-10 and transforming growth factor β. The effect of rFgLGMN-1 and rFgLGMN-2 on the phagocytosis of PBMCs varied depending on their concentrations.
Conclusions: rFgLGMN-1 and rFgLGMN-2 modulate several cellular and immunological functions of PBMCs, and exhibited distinct regulatory effects on these in vitro, which indicated that they may play roles in immune modulation and facilitate fluke development. However, due to uncertainties associated with in vitro experiments, further studies are necessary to elucidate the precise functions of these legumains.
期刊介绍：
Parasites & Vectors is an open access, peer-reviewed online journal dealing with the biology of parasites, parasitic diseases, intermediate hosts, vectors and vector-borne pathogens. Manuscripts published in this journal will be available to all worldwide, with no barriers to access, immediately following acceptance. However, authors retain the copyright of their material and may use it, or distribute it, as they wish.
Manuscripts on all aspects of the basic and applied biology of parasites, intermediate hosts, vectors and vector-borne pathogens will be considered. In addition to the traditional and well-established areas of science in these fields, we also aim to provide a vehicle for publication of the rapidly developing resources and technology in parasite, intermediate host and vector genomics and their impacts on biological research. We are able to publish large datasets and extensive results, frequently associated with genomic and post-genomic technologies, which are not readily accommodated in traditional journals. Manuscripts addressing broader issues, for example economics, social sciences and global climate change in relation to parasites, vectors and disease control, are also welcomed.
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