Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract

Infective third-stage larvae (L3) of the marine nematode Anisakis pegreffii cause inflammation and clinical symptoms in humans, their accidental host, that subside and self-resolve in a couple of weeks after L3 die. To characterise the differences in an early immune response of a marine vs. terrestr...

Full description

Bibliographic Details
Main Authors: Jerko Hrabar, Mirela Petrić, Serena Cavallero, Marco Salvemini, Stefano D’Amelio, Ivona Mladineo
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-12-01
Series:Frontiers in Cellular and Infection Microbiology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fcimb.2022.1042679/full
_version_ 1798006400730791936
author Jerko Hrabar
Mirela Petrić
Serena Cavallero
Marco Salvemini
Stefano D’Amelio
Ivona Mladineo
author_facet Jerko Hrabar
Mirela Petrić
Serena Cavallero
Marco Salvemini
Stefano D’Amelio
Ivona Mladineo
author_sort Jerko Hrabar
collection DOAJ
description Infective third-stage larvae (L3) of the marine nematode Anisakis pegreffii cause inflammation and clinical symptoms in humans, their accidental host, that subside and self-resolve in a couple of weeks after L3 die. To characterise the differences in an early immune response of a marine vs. terrestrial host, we stimulated peripheral blood leukocytes (PBLs) of fish (paratenic host) and rat (accidental, human-model host) with A. pegreffii crude extract and analysed PBL transcriptomes 1 and 12 h post-stimulation. Fish and rat PBLs differentially expressed 712 and 493 transcripts, respectively, between 1 and 12 h post-stimulation (false discovery rate, FDR <0.001, logFC >2). While there was a difference in the highest upregulated transcripts between two time-points, the same Gene Ontologies, biological processes (intracellular signal transduction, DNA-dependent transcription, and DNA-regulated regulation of transcription), and molecular functions (ATP and metal ion binding) were enriched in the two hosts, showing an incrementing dynamic between 1 and 12 h. This suggests that the two distinct hosts employ qualitatively different transcript cascades only to achieve the same effect, at least during an early innate immunity response. Activation of later immunity elements and/or a combination of other host’s intrinsic conditions may contribute to the death of L3 in the terrestrial host.
first_indexed 2024-04-11T12:54:08Z
format Article
id doaj.art-82aa36b051634557bd61caf6755fa244
institution Directory Open Access Journal
issn 2235-2988
language English
last_indexed 2024-04-11T12:54:08Z
publishDate 2022-12-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Cellular and Infection Microbiology
spelling doaj.art-82aa36b051634557bd61caf6755fa2442022-12-22T04:23:06ZengFrontiers Media S.A.Frontiers in Cellular and Infection Microbiology2235-29882022-12-011210.3389/fcimb.2022.10426791042679Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extractJerko Hrabar0Mirela Petrić1Serena Cavallero2Marco Salvemini3Stefano D’Amelio4Ivona Mladineo5Laboratory of Aquaculture, Institute of Oceanography and Fisheries, Split, CroatiaUniversity Department of Marine Studies, University of Split, Split, CroatiaDepartment of Public Health and Infectious Diseases, University of Rome, Sapienza, Rome, ItalyDepartment of Biology, University of Naples Federico II, Naples, ItalyDepartment of Public Health and Infectious Diseases, University of Rome, Sapienza, Rome, ItalyLaboratory of Functional Helminthology, Institute of Parasitology, Biology Centre of Czech Academy of Sciences, Ceske Budejovice, CzechiaInfective third-stage larvae (L3) of the marine nematode Anisakis pegreffii cause inflammation and clinical symptoms in humans, their accidental host, that subside and self-resolve in a couple of weeks after L3 die. To characterise the differences in an early immune response of a marine vs. terrestrial host, we stimulated peripheral blood leukocytes (PBLs) of fish (paratenic host) and rat (accidental, human-model host) with A. pegreffii crude extract and analysed PBL transcriptomes 1 and 12 h post-stimulation. Fish and rat PBLs differentially expressed 712 and 493 transcripts, respectively, between 1 and 12 h post-stimulation (false discovery rate, FDR <0.001, logFC >2). While there was a difference in the highest upregulated transcripts between two time-points, the same Gene Ontologies, biological processes (intracellular signal transduction, DNA-dependent transcription, and DNA-regulated regulation of transcription), and molecular functions (ATP and metal ion binding) were enriched in the two hosts, showing an incrementing dynamic between 1 and 12 h. This suggests that the two distinct hosts employ qualitatively different transcript cascades only to achieve the same effect, at least during an early innate immunity response. Activation of later immunity elements and/or a combination of other host’s intrinsic conditions may contribute to the death of L3 in the terrestrial host.https://www.frontiersin.org/articles/10.3389/fcimb.2022.1042679/fullAnisakiscrude extractfishratperipheral blood leukocytesRNA-Seq
spellingShingle Jerko Hrabar
Mirela Petrić
Serena Cavallero
Marco Salvemini
Stefano D’Amelio
Ivona Mladineo
Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract
Frontiers in Cellular and Infection Microbiology
Anisakis
crude extract
fish
rat
peripheral blood leukocytes
RNA-Seq
title Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract
title_full Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract
title_fullStr Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract
title_full_unstemmed Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract
title_short Rat and fish peripheral blood leukocytes respond distinctively to Anisakis pegreffii (Nematoda, Anisakidae) crude extract
title_sort rat and fish peripheral blood leukocytes respond distinctively to anisakis pegreffii nematoda anisakidae crude extract
topic Anisakis
crude extract
fish
rat
peripheral blood leukocytes
RNA-Seq
url https://www.frontiersin.org/articles/10.3389/fcimb.2022.1042679/full
work_keys_str_mv AT jerkohrabar ratandfishperipheralbloodleukocytesresponddistinctivelytoanisakispegreffiinematodaanisakidaecrudeextract
AT mirelapetric ratandfishperipheralbloodleukocytesresponddistinctivelytoanisakispegreffiinematodaanisakidaecrudeextract
AT serenacavallero ratandfishperipheralbloodleukocytesresponddistinctivelytoanisakispegreffiinematodaanisakidaecrudeextract
AT marcosalvemini ratandfishperipheralbloodleukocytesresponddistinctivelytoanisakispegreffiinematodaanisakidaecrudeextract
AT stefanodamelio ratandfishperipheralbloodleukocytesresponddistinctivelytoanisakispegreffiinematodaanisakidaecrudeextract
AT ivonamladineo ratandfishperipheralbloodleukocytesresponddistinctivelytoanisakispegreffiinematodaanisakidaecrudeextract