Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development
Gastrointestinal nematodes are among the most prevalent parasites infecting humans and livestock worldwide. Infective larvae of the soil-transmitted nematode Ascaris spp. enter the host and start tissue migration by crossing the intestinal epithelial barrier. The initial interaction of the intestina...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2018-08-01
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| Series: | Frontiers in Immunology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fimmu.2018.01868/full |
| _version_ | 1818239879479296000 |
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| author | Friederike Ebner Mathias Kuhring Mathias Kuhring Mathias Kuhring Mathias Kuhring Aleksandar Radonić Ankur Midha Bernhard Y. Renard Susanne Hartmann |
| author_facet | Friederike Ebner Mathias Kuhring Mathias Kuhring Mathias Kuhring Mathias Kuhring Aleksandar Radonić Ankur Midha Bernhard Y. Renard Susanne Hartmann |
| author_sort | Friederike Ebner |
| collection | DOAJ |
| description | Gastrointestinal nematodes are among the most prevalent parasites infecting humans and livestock worldwide. Infective larvae of the soil-transmitted nematode Ascaris spp. enter the host and start tissue migration by crossing the intestinal epithelial barrier. The initial interaction of the intestinal epithelium with the parasite, however, has received little attention. In a time-resolved interaction model of porcine intestinal epithelial cells (IPEC-J2) and infective Ascaris suum larvae, we addressed the early transcriptional changes occurring simultaneously in both organisms using dual-species RNA-Seq. Functional analysis of the host response revealed an overall induction of metabolic activity, without induction of immune responsive genes or immune signaling pathways and showing suppression of chemotactic genes like CXCL8/IL-8 or CHI3L1. Ascaris larvae, when getting in contact with the epithelium, showed induction of genes that orchestrate motor activity and larval development, such as myosin, troponin, myoglobin, and protein disulfide isomerase 2 (PDI-2). In addition, excretory-secretory products that likely facilitate parasite invasion were increased, among them, aspartic protease 6 or hyaluronidase. Integration of host and pathogen data in an interspecies gene co-expression network indicated links between nematode fatty acid biosynthesis and host ribosome assembly/protein synthesis. In summary, our study provides new molecular insights into the early factors of parasite invasion, while at the same time revealing host immunological unresponsiveness. Reproducible software for dual RNA-Seq analysis of non-model organisms is available at https://gitlab.com/mkuhring/project_asuum and can be applied to similar studies. |
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| format | Article |
| id | doaj.art-aef4025800e0459eb138c5e9ced87c4b |
| institution | Directory Open Access Journal |
| issn | 1664-3224 |
| language | English |
| last_indexed | 2024-12-12T13:04:34Z |
| publishDate | 2018-08-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Immunology |
| spelling | doaj.art-aef4025800e0459eb138c5e9ced87c4b2022-12-22T00:23:42ZengFrontiers Media S.A.Frontiers in Immunology1664-32242018-08-01910.3389/fimmu.2018.01868392505Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval DevelopmentFriederike Ebner0Mathias Kuhring1Mathias Kuhring2Mathias Kuhring3Mathias Kuhring4Aleksandar Radonić5Ankur Midha6Bernhard Y. Renard7Susanne Hartmann8Department of Veterinary Medicine, Institute of Immunology, Freie Universität Berlin, Berlin, GermanyBioinformatics Unit (MF1), Department for Methods Development and Research Infrastructure, Robert Koch Institute, Berlin, GermanyCore Unit Bioinformatics, Berlin Institute of Health (BIH), Berlin, GermanyBerlin Institute of Health Metabolomics Platform, Berlin Institute of Health (BIH), Berlin, GermanyMax Delbrück Center (MDC) for Molecular Medicine, Berlin, GermanyCenter for Biological Threats and Special Pathogens: Highly Pathogenic Viruses (ZBS 1), Robert Koch Institute, Berlin, GermanyDepartment of Veterinary Medicine, Institute of Immunology, Freie Universität Berlin, Berlin, GermanyBioinformatics Unit (MF1), Department for Methods Development and Research Infrastructure, Robert Koch Institute, Berlin, GermanyDepartment of Veterinary Medicine, Institute of Immunology, Freie Universität Berlin, Berlin, GermanyGastrointestinal nematodes are among the most prevalent parasites infecting humans and livestock worldwide. Infective larvae of the soil-transmitted nematode Ascaris spp. enter the host and start tissue migration by crossing the intestinal epithelial barrier. The initial interaction of the intestinal epithelium with the parasite, however, has received little attention. In a time-resolved interaction model of porcine intestinal epithelial cells (IPEC-J2) and infective Ascaris suum larvae, we addressed the early transcriptional changes occurring simultaneously in both organisms using dual-species RNA-Seq. Functional analysis of the host response revealed an overall induction of metabolic activity, without induction of immune responsive genes or immune signaling pathways and showing suppression of chemotactic genes like CXCL8/IL-8 or CHI3L1. Ascaris larvae, when getting in contact with the epithelium, showed induction of genes that orchestrate motor activity and larval development, such as myosin, troponin, myoglobin, and protein disulfide isomerase 2 (PDI-2). In addition, excretory-secretory products that likely facilitate parasite invasion were increased, among them, aspartic protease 6 or hyaluronidase. Integration of host and pathogen data in an interspecies gene co-expression network indicated links between nematode fatty acid biosynthesis and host ribosome assembly/protein synthesis. In summary, our study provides new molecular insights into the early factors of parasite invasion, while at the same time revealing host immunological unresponsiveness. Reproducible software for dual RNA-Seq analysis of non-model organisms is available at https://gitlab.com/mkuhring/project_asuum and can be applied to similar studies.https://www.frontiersin.org/article/10.3389/fimmu.2018.01868/fullhost–pathogenparasitic nematodeIPEC-J2Ascaris suumdual-speciesRNA sequencing |
| spellingShingle | Friederike Ebner Mathias Kuhring Mathias Kuhring Mathias Kuhring Mathias Kuhring Aleksandar Radonić Ankur Midha Bernhard Y. Renard Susanne Hartmann Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development Frontiers in Immunology host–pathogen parasitic nematode IPEC-J2 Ascaris suum dual-species RNA sequencing |
| title | Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development |
| title_full | Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development |
| title_fullStr | Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development |
| title_full_unstemmed | Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development |
| title_short | Silent Witness: Dual-Species Transcriptomics Reveals Epithelial Immunological Quiescence to Helminth Larval Encounter and Fostered Larval Development |
| title_sort | silent witness dual species transcriptomics reveals epithelial immunological quiescence to helminth larval encounter and fostered larval development |
| topic | host–pathogen parasitic nematode IPEC-J2 Ascaris suum dual-species RNA sequencing |
| url | https://www.frontiersin.org/article/10.3389/fimmu.2018.01868/full |
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