Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity

<b>Background</b>: <i>Anisakis</i> spp. third-stage larvae (L3) are the causative agents of human zoonosis called anisakiasis. The accidental ingestion of L3 can cause acute and chronic inflammation at the gastric, intestinal, or ectopic levels. Despite its relevance in publi...

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Main Authors: Ilaria Bellini, Daniela Scribano, Meysam Sarshar, Cecilia Ambrosi, Antonella Pizzarelli, Anna Teresa Palamara, Stefano D’Amelio, Serena Cavallero
Format: Article
Language:English
Published: MDPI AG 2022-10-01
Series:Pathogens
Subjects:
Online Access:https://www.mdpi.com/2076-0817/11/10/1214
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author Ilaria Bellini
Daniela Scribano
Meysam Sarshar
Cecilia Ambrosi
Antonella Pizzarelli
Anna Teresa Palamara
Stefano D’Amelio
Serena Cavallero
author_facet Ilaria Bellini
Daniela Scribano
Meysam Sarshar
Cecilia Ambrosi
Antonella Pizzarelli
Anna Teresa Palamara
Stefano D’Amelio
Serena Cavallero
author_sort Ilaria Bellini
collection DOAJ
description <b>Background</b>: <i>Anisakis</i> spp. third-stage larvae (L3) are the causative agents of human zoonosis called anisakiasis. The accidental ingestion of L3 can cause acute and chronic inflammation at the gastric, intestinal, or ectopic levels. Despite its relevance in public health, studies on pathogenetic mechanisms and parasite-human interplay are scarce. The aim of this study was to investigate the human inflammatory response to different <i>Anisakis</i> vehicles of pathogenicity. <b>Methods</b>: Human colorectal adenocarcinoma (Caco-2) cells were exposed to <i>Anisakis</i> L3 (the initial contact with the host), extracellular vesicles (EVs, <i>Anisakis</i>–host communication), and crude extract (CE, the larval dying). The protein quantity and gene expression of two pro-inflammatory cytokines (IL-6 and IL-8) were investigated using an ELISA test (6 h and 24 h) and a qReal-Time PCR (1 h, 6 h, and 24 h), respectively. <b>Results</b>: The L3 and EVs induced a downregulation in both the <i>Il-6</i> and <i>Il-8</i> gene expression and protein quantity. On the contrary, the CE stimulated IL-6 gene expression and its protein release, not affecting IL-8. <b>Conclusions</b>: The Caco-2 cells seemed to not react to the exposure to the L3 and EVs, suggesting a parasite’s immunomodulating action to remain alive in an inhospitable niche. Conversely, the dying larva (CE) could induce strong activation of the immune strategy of the host that, in vivo, would lead to parasite expulsion, eosinophilia, and/or granuloma formation.
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spelling doaj.art-2b6c5eaf371a496799fc68fabe4202812023-11-24T01:50:02ZengMDPI AGPathogens2076-08172022-10-011110121410.3390/pathogens11101214Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of PathogenicityIlaria Bellini0Daniela Scribano1Meysam Sarshar2Cecilia Ambrosi3Antonella Pizzarelli4Anna Teresa Palamara5Stefano D’Amelio6Serena Cavallero7Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, ItalyResearch Laboratories, Bambino Gesù Children’s Hospital, IRCCS, 00146 Rome, ItalyHuman Sciences and Promotion of the Quality of Life, San Raffaele Open University, IRCCS, 00166 Rome, ItalyDepartment of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, ItalyLaboratory Affiliated to Institute Pasteur Italia—Cenci Bolognetti Foundation, Department of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, ItalyDepartment of Public Health and Infectious Diseases, Sapienza University of Rome, 00185 Rome, Italy<b>Background</b>: <i>Anisakis</i> spp. third-stage larvae (L3) are the causative agents of human zoonosis called anisakiasis. The accidental ingestion of L3 can cause acute and chronic inflammation at the gastric, intestinal, or ectopic levels. Despite its relevance in public health, studies on pathogenetic mechanisms and parasite-human interplay are scarce. The aim of this study was to investigate the human inflammatory response to different <i>Anisakis</i> vehicles of pathogenicity. <b>Methods</b>: Human colorectal adenocarcinoma (Caco-2) cells were exposed to <i>Anisakis</i> L3 (the initial contact with the host), extracellular vesicles (EVs, <i>Anisakis</i>–host communication), and crude extract (CE, the larval dying). The protein quantity and gene expression of two pro-inflammatory cytokines (IL-6 and IL-8) were investigated using an ELISA test (6 h and 24 h) and a qReal-Time PCR (1 h, 6 h, and 24 h), respectively. <b>Results</b>: The L3 and EVs induced a downregulation in both the <i>Il-6</i> and <i>Il-8</i> gene expression and protein quantity. On the contrary, the CE stimulated IL-6 gene expression and its protein release, not affecting IL-8. <b>Conclusions</b>: The Caco-2 cells seemed to not react to the exposure to the L3 and EVs, suggesting a parasite’s immunomodulating action to remain alive in an inhospitable niche. Conversely, the dying larva (CE) could induce strong activation of the immune strategy of the host that, in vivo, would lead to parasite expulsion, eosinophilia, and/or granuloma formation.https://www.mdpi.com/2076-0817/11/10/1214<i>Anisakis</i>Caco-2crude extractextracellular vesiclesinflammation
spellingShingle Ilaria Bellini
Daniela Scribano
Meysam Sarshar
Cecilia Ambrosi
Antonella Pizzarelli
Anna Teresa Palamara
Stefano D’Amelio
Serena Cavallero
Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity
Pathogens
<i>Anisakis</i>
Caco-2
crude extract
extracellular vesicles
inflammation
title Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity
title_full Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity
title_fullStr Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity
title_full_unstemmed Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity
title_short Inflammatory Response in Caco-2 Cells Stimulated with <i>Anisakis</i> Messengers of Pathogenicity
title_sort inflammatory response in caco 2 cells stimulated with i anisakis i messengers of pathogenicity
topic <i>Anisakis</i>
Caco-2
crude extract
extracellular vesicles
inflammation
url https://www.mdpi.com/2076-0817/11/10/1214
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