Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
2023
Peylhard, Moana | Berthier, David | Dayo, Guiguigbaza-Kossigan | Chantal, Isabelle | Sylla, Souleymane | Nidelet, Sabine | Dubois, Emeric | Martin, Guillaume | Sempéré, Guilhem | Flori, Laurence | Thévenon, Sophie | Interactions hôtes-vecteurs-parasites-environnement dans les maladies tropicales négligées dues aux trypanosomatides (UMR INTERTRYP) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut de Recherche pour le Développement (IRD)-Université Claude Bernard Lyon 1 (UCBL) ; Université de Lyon-Université de Lyon-Université de Bordeaux (UB) | Département Systèmes Biologiques (Cirad-BIOS) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad) | Centre international de recherche-développement sur l'élevage en zone sub-humide (CIRDES) | Institut de Génomique Fonctionnelle - Montpellier GenomiX (IGF MGX) ; Institut de Génomique Fonctionnelle (IGF) ; Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-BioCampus (BCM) ; Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-Université de Montpellier (UM)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS) | Amélioration génétique et adaptation des plantes méditerranéennes et tropicales (UMR AGAP) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Montpellier ; Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Université de Montpellier (UM) | Systèmes d'élevage méditerranéens et tropicaux (UMR SELMET) ; Centre de Coopération Internationale en Recherche Agronomique pour le Développement (Cirad)-Institut National de Recherche pour l’Agriculture, l’Alimentation et l’Environnement (INRAE)-Institut Agro Montpellier ; Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro)-Institut national d'enseignement supérieur pour l'agriculture, l'alimentation et l'environnement (Institut Agro) | This work was supported by the ANR grant AATTOL (ANR-11-JSV6-0001) and by the LabEx ParaFrap (ANR-11-LABX-0024). MGX acknowledges financial support from France Génomique National infrastructure, funded as part of “Investissement d’avenir” program managed by ANR (ANR-10-INBS-0009). The PhD grant of Moana Peylhard was supported by CIRAD PhD grant program and IRD. The work was also supported by the CIRAD-UMR AGAP HPC-Data Center of the South Green Bioinformatics platform (http://www.southgreen.fr). | South Green Bioinformatics platform (http://www.southgreen.fr), Montpellier, France | ANR-11-JSV6-0001,AATTOL,Caractérisation des bases moléculaires de la tolérance à la Trypanosomose Animale Africaine: analyse conjointe des transcriptomes de l'hôte bovin et du parasite(2011) | ANR-11-LABX-0024,ParaFrap,Alliance française contre les maladies parasitaires(2011) | ANR-10-INBS-0009,France Génomique,Organisation et montée en puissance d'une Infrastructure Nationale de Génomique(2010)
Raw sequences data (fastq, count matrix, experimental design) will be publicly available at GEO (https://www.ncbi.nlm.nih.gov/geo) under accession number GSE197108 upon publication. Scripts and intermediate tables (DEG analysis, input tables for IPA® analyses, output tables from IPA® analyses) are publicly available in Cirad Dataverse under https://doi.org/10.18167/DVN1/L9SHAX. SNP genotypes of the experimental cattle are publicly available in Cirad Dataverse under https://doi.org/10.18167/DVN1/APTZOC and in WIDDE (http://widde.toulouse.inra.fr/widde).Tables and figures are in the supplementary tables and figures files and are publicly available in Cirad Dataverse under https://doi.org/10.18167/DVN1/E3288X. Legends are displayed at the bottom of each tables and figures.
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Show more [+] Less [-]English. Animal African trypanosomosis, caused by blood protozoan parasites transmitted mainly by tsetse flies, represents a major constraint for millions of cattle in sub-Saharan Africa. Exposed cattle include trypanosusceptible indicine breeds, severely affected by the disease, and West African taurine breeds called trypanotolerant owing to their ability to control parasite development, survive and grow in enzootic areas. Until now the genetic basis of trypanotolerance remains unclear. Here, to improve knowledge of the biological processes involved in trypanotolerance versus trypanosusceptibility, we identified bovine genes differentially expressed in five West African cattle breeds during an experimental infection by Trypanosoma congolense and their biological functions. To this end, whole blood genome-wide transcriptome of three trypanotolerant taurine breeds (N’Dama, Lagune and Baoulé), one susceptible zebu (Zebu Fulani) and one African taurine x zebu admixed breed (Borgou) were profiled by RNA sequencing at four time points, one before and three during infection. As expected, infection had a major impact on cattle blood transcriptome regardless of the breed. The functional analysis of differentially expressed genes over time in each breed confirmed an early activation of the innate immune response, followed by an activation of the humoral response and an inhibition of T cell functions at the chronic stage of infection. More importantly, we highlighted overlooked features, such as a strong disturbance in host metabolism and cellular energy production that differentiates trypanotolerant and trypanosusceptible breeds. N’Dama breed showed the earliest regulation of immune response, associated with a strong activation of cellular energy production, also observed in Lagune, and to a lesser extent in Baoulé. Susceptible Zebu Fulani breed differed from other breeds by the strongest modification in lipid metabolism regulation. Overall, this study provides a better understanding of the biological mechanisms at work during infection, especially concerning the interplay between immunity and metabolism that seems differentially regulated depending on the cattle breeds.
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