Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)

Abstract Background Sarcoptic mange is an emerging and neglected contagious skin disease caused by the mite Sarcoptes scabiei, affecting humans, domestic animals, and wildlife. Mange is the main disease and a major concern for the management and conservation of populations of Iberian ibex (Capra pyr...

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Main Authors: Arián Ráez-Bravo, José Enrique Granados, José Espinosa, Lara Nonell, Emmanuel Serrano, Eulàlia Puigdecanet, Marta Bódalo, Jesús M. Pérez, Ramón C. Soriguer, Francisco Javier Cano-Manuel, Paulino Fandos, Jorge Ramón López-Olvera
Format: Article
Language:English
Published: BMC 2024-11-01
Series:BMC Genomics
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Online Access:https://doi.org/10.1186/s12864-024-10999-4
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author Arián Ráez-Bravo
José Enrique Granados
José Espinosa
Lara Nonell
Emmanuel Serrano
Eulàlia Puigdecanet
Marta Bódalo
Jesús M. Pérez
Ramón C. Soriguer
Francisco Javier Cano-Manuel
Paulino Fandos
Jorge Ramón López-Olvera
author_facet Arián Ráez-Bravo
José Enrique Granados
José Espinosa
Lara Nonell
Emmanuel Serrano
Eulàlia Puigdecanet
Marta Bódalo
Jesús M. Pérez
Ramón C. Soriguer
Francisco Javier Cano-Manuel
Paulino Fandos
Jorge Ramón López-Olvera
author_sort Arián Ráez-Bravo
collection DOAJ
description Abstract Background Sarcoptic mange is an emerging and neglected contagious skin disease caused by the mite Sarcoptes scabiei, affecting humans, domestic animals, and wildlife. Mange is the main disease and a major concern for the management and conservation of populations of Iberian ibex (Capra pyrenaica), a medium-sized mountain ungulate endemic to the Iberian Peninsula and Northern Pyrenees. Differences in host-parasite interaction and host immune response determine mange clinical outcome, but little is known about the related differences in gene expression. This study determined blood and skin gene expressions in S. scabiei-experimentally infested Iberian ibexes. Results Infestation with S. scabiei promoted immune and inflammatory genomic responses both in skin and blood, with two different clinical outcomes: either severe infestation or recovery. Sarcoptes scabiei induced local skin immunosuppression to favour its multiplication and establishment of the infestation in the host. Skin gene expression was mostly inflammatory and inefficient to control mange in the severely infected ibexes. Conversely, the immune skin response of the recovered ibexes effectively recognised S. scabiei and activated T-cells, limiting the infestation. Consequently, inflammation-related genes were more expressed in the blood of the severely infested ibexes than in those that recovered. Conclusions The results demonstrate that skin local cellular immune response is key to control sarcoptic mange and prevent the systemic spread of the disease and the associated inflammatory response. These results will be useful to understand the pathogenesis and drivers of the differential outcome of mange at individual scale, and the population and ecological consequences of such variability in Iberian ibex, as well as in other wildlife species, domestic animals, and humans.
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spelling doaj-art-41ca161c9c9148a88873c17ae6f14f072024-12-01T12:11:28ZengBMCBMC Genomics1471-21642024-11-0125111410.1186/s12864-024-10999-4Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)Arián Ráez-Bravo0José Enrique Granados1José Espinosa2Lara Nonell3Emmanuel Serrano4Eulàlia Puigdecanet5Marta Bódalo6Jesús M. Pérez7Ramón C. Soriguer8Francisco Javier Cano-Manuel9Paulino FandosJorge Ramón López-Olvera10Wildlife Ecology & Health research group (WE&H) and Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona (UAB)Wildlife Ecology & Health research group (WE&H) and Espacio Natural Sierra NevadaDepartamento de Sanidad Animal, Facultad de Veterinaria, Instituto de Ganadería de Montaña (CSIC‐ULE), Universidad de LeónMARGenomics, IMIM (Institut Hospital del Mar d’Investigacions Mèdiques)Wildlife Ecology & Health research group (WE&H) and Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona (UAB)MARGenomics, IMIM (Institut Hospital del Mar d’Investigacions Mèdiques)MARGenomics, IMIM (Institut Hospital del Mar d’Investigacions Mèdiques)Wildlife Ecology & Health research group and Departamento de Biología Animal, Biología Vegetal y Ecología, Universidad de JaénEstación Biológica de Doñana (CSIC)Wildlife Ecology & Health research group (WE&H) and Espacio Natural Sierra NevadaWildlife Ecology & Health research group (WE&H) and Servei d’Ecopatologia de Fauna Salvatge (SEFaS), Departament de Medicina i Cirurgia Animals, Universitat Autònoma de Barcelona (UAB)Abstract Background Sarcoptic mange is an emerging and neglected contagious skin disease caused by the mite Sarcoptes scabiei, affecting humans, domestic animals, and wildlife. Mange is the main disease and a major concern for the management and conservation of populations of Iberian ibex (Capra pyrenaica), a medium-sized mountain ungulate endemic to the Iberian Peninsula and Northern Pyrenees. Differences in host-parasite interaction and host immune response determine mange clinical outcome, but little is known about the related differences in gene expression. This study determined blood and skin gene expressions in S. scabiei-experimentally infested Iberian ibexes. Results Infestation with S. scabiei promoted immune and inflammatory genomic responses both in skin and blood, with two different clinical outcomes: either severe infestation or recovery. Sarcoptes scabiei induced local skin immunosuppression to favour its multiplication and establishment of the infestation in the host. Skin gene expression was mostly inflammatory and inefficient to control mange in the severely infected ibexes. Conversely, the immune skin response of the recovered ibexes effectively recognised S. scabiei and activated T-cells, limiting the infestation. Consequently, inflammation-related genes were more expressed in the blood of the severely infested ibexes than in those that recovered. Conclusions The results demonstrate that skin local cellular immune response is key to control sarcoptic mange and prevent the systemic spread of the disease and the associated inflammatory response. These results will be useful to understand the pathogenesis and drivers of the differential outcome of mange at individual scale, and the population and ecological consequences of such variability in Iberian ibex, as well as in other wildlife species, domestic animals, and humans.https://doi.org/10.1186/s12864-024-10999-4Gene expressionGene set enrichment analysisGenomic responseImmune responseMicroarraySarcoptes scabiei
spellingShingle Arián Ráez-Bravo
José Enrique Granados
José Espinosa
Lara Nonell
Emmanuel Serrano
Eulàlia Puigdecanet
Marta Bódalo
Jesús M. Pérez
Ramón C. Soriguer
Francisco Javier Cano-Manuel
Paulino Fandos
Jorge Ramón López-Olvera
Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)
BMC Genomics
Gene expression
Gene set enrichment analysis
Genomic response
Immune response
Microarray
Sarcoptes scabiei
title Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)
title_full Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)
title_fullStr Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)
title_full_unstemmed Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)
title_short Genomics reveal local skin immune response key to control sarcoptic mange in Iberian ibex (Capra pyrenaica)
title_sort genomics reveal local skin immune response key to control sarcoptic mange in iberian ibex capra pyrenaica
topic Gene expression
Gene set enrichment analysis
Genomic response
Immune response
Microarray
Sarcoptes scabiei
url https://doi.org/10.1186/s12864-024-10999-4
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