title: Role of pathogen-derived cell wall carbohydrates and prostaglandin E2 in immune response and suppression of fish immunity by the oomycete Saprolegnia parasitica.
abstract: Saprolegnia parasitica is a freshwater oomycete that is capable of infecting several species of fin fish. Saprolegniosis, the disease caused by this microbe, has a substantial impact on Atlantic salmon aquaculture. No sustainable treatment against saprolegniosis is available, and little is known regarding the host response. In this study, we examined the immune response of Atlantic salmon to S. parasitica infection and to its cell wall carbohydrates. Saprolegnia triggers a strong inflammatory response in its host (i.e., induction of interleukin-1β1 [IL-1β1], IL-6, and tumor necrosis factor alpha), while severely suppressing the expression of genes associated with adaptive immunity in fish, through downregulation of T-helper cell cytokines, antigen presentation machinery, and immunoglobulins. Oomycete cell wall carbohydrates were recognized by fish leukocytes, triggering upregulation of genes involved in the inflammatory response, similar to what is observed during infection. Our data suggest that S. parasitica is capable of producing prostaglandin [corrected] E2 (PGE2) in vitro, a metabolite not previously shown to be produced by oomycetes, and two proteins with homology to vertebrate enzymes known to play a role in prostaglandin biosynthesis have been identified in the oomycete genome. Exogenous PGE2 was shown to increase the inflammatory response in fish leukocytes incubated with cell wall carbohydrates while suppressing genes involved in cellular immunity (gamma interferon [IFN-γ] and the IFN-γ-inducible protein [γ-IP]). Inhibition of S. parasitica zoospore germination and mycelial growth by two cyclooxygenase inhibitors (aspirin and indomethacin) also suggests that prostaglandins may be involved in oomycete development.
authors.affiliation: Scottish Fish Immunology Research Centre, Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom Aberdeen Oomycete Laboratory, Institute of Medical Sciences, University of Aberdeen, Aberdeen, United Kingdom.
authors.forename: Rodrigo
authors.initials: R
authors.lastname: Belmonte
authors.affiliation: Scottish Fish Immunology Research Centre, Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom.
authors.forename: Tiehui
authors.initials: T
authors.lastname: Wang
authors.affiliation: Mass Spectrometry Group, Rowett Institute of Nutrition and Health, University of Aberdeen, Aberdeen, United Kingdom.
authors.forename: Gary J
authors.initials: GJ
authors.lastname: Duncan
authors.affiliation: Norwegian Veterinary Institute, Oslo, Norway.
authors.forename: Ida
authors.initials: I
authors.lastname: Skaar
authors.affiliation: Division of Glycoscience, School of Biotechnology, Royal Institute of Technology, Stockholm, Sweden.
authors.forename: Hugo
authors.initials: H
authors.lastname: Mélida
authors.affiliation: Division of Glycoscience, School of Biotechnology, Royal Institute of Technology, Stockholm, Sweden.
authors.forename: Vincent
authors.initials: V
authors.lastname: Bulone
authors.affiliation: Aberdeen Oomycete Laboratory, Institute of Medical Sciences, University of Aberdeen, Aberdeen, United Kingdom.
authors.forename: Pieter
authors.initials: P
authors.lastname: van West
authors.affiliation: Scottish Fish Immunology Research Centre, Institute of Biological and Environmental Sciences, University of Aberdeen, Aberdeen, United Kingdom c.secombes@abdn.ac.uk.
authors.forename: Christopher J
authors.initials: CJ
authors.lastname: Secombes
mesh_terms: D000818:Animals; D002241:Carbohydrates / Q000737:chemistry / Q000276:immunology*; D002473:Cell Wall / Q000737:chemistry / Q000276:immunology*; D015232:Dinoprostone / Q000378:metabolism*; D005393:Fish Diseases / Q000276:immunology / Q000469:parasitology*; D015971:Gene Expression Regulation, Enzymologic; D005880:Gills / Q000378:metabolism; D060226:Head Kidney / Q000378:metabolism; D007239:Infections / Q000276:immunology / Q000382:microbiology / Q000662:veterinary*; D017686:Oncorhynchus mykiss; D010740:Phospholipases / Q000737:chemistry / Q000235:genetics / Q000378:metabolism; D020317:Salmo salar; D044762:Saprolegnia / Q000166:cytology* / Q000235:genetics / Q000276:immunology* / Q000378:metabolism
chemical_list: D002241:Carbohydrates; D010740:Phospholipases; D015232:Dinoprostone
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