Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense

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 bre...

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Main Authors: Peylhard, Moana, Berthier, David, Dayo, Guiguigbaza-Kossigan, Chantal, Isabelle, Sylla, Souleymane, Nidelet, Sabine, Dubois, Emeric, Martin, Guillaume, Sempéré, Guilhem, Flori, Laurence, Thévenon, Sophie
Format: Article
Language:English
Published: Peer Community In 2023-02-01
Series:Peer Community Journal
Online Access:https://peercommunityjournal.org/articles/10.24072/pcjournal.239/
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author Peylhard, Moana
Berthier, David
Dayo, Guiguigbaza-Kossigan
Chantal, Isabelle
Sylla, Souleymane
Nidelet, Sabine
Dubois, Emeric
Martin, Guillaume
Sempéré, Guilhem
Flori, Laurence
Thévenon, Sophie
author_facet Peylhard, Moana
Berthier, David
Dayo, Guiguigbaza-Kossigan
Chantal, Isabelle
Sylla, Souleymane
Nidelet, Sabine
Dubois, Emeric
Martin, Guillaume
Sempéré, Guilhem
Flori, Laurence
Thévenon, Sophie
author_sort Peylhard, Moana
collection DOAJ
description 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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spelling doaj-art-a1af2e6bf04d4c9f98b582f7c95997e32025-02-07T10:16:49ZengPeer Community InPeer Community Journal2804-38712023-02-01310.24072/pcjournal.23910.24072/pcjournal.239Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolensePeylhard, Moana0https://orcid.org/0000-0001-8574-4567Berthier, David1https://orcid.org/0000-0002-3283-6588Dayo, Guiguigbaza-Kossigan2https://orcid.org/0000-0001-7926-5834Chantal, Isabelle3https://orcid.org/0000-0002-3429-484XSylla, Souleymane4Nidelet, Sabine5Dubois, Emeric6https://orcid.org/0000-0002-6052-4178Martin, Guillaume7https://orcid.org/0000-0002-1801-7500Sempéré, Guilhem8https://orcid.org/0000-0001-7429-2091Flori, Laurence9https://orcid.org/0000-0002-7529-8521Thévenon, Sophie10https://orcid.org/0000-0001-6059-5884CIRAD, UMR INTERTRYP, F-34398 Montpellier, France; INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, FranceCIRAD, UMR INTERTRYP, F-34398 Montpellier, France; INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, FranceCentre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), 01 BP 454, Bobo-Dioulasso 01, Burkina FasoCIRAD, UMR INTERTRYP, F-34398 Montpellier, France; INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, FranceCentre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), 01 BP 454, Bobo-Dioulasso 01, Burkina FasoMontpellier GenomiX, France Génomique, Montpellier, FranceMontpellier GenomiX, France Génomique, Montpellier, FranceCIRAD, UMR AGAP Institut, F-34398 Montpellier, France; UMR AGAP Institut, Univ Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, FranceCIRAD, UMR INTERTRYP, F-34398 Montpellier, France; INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, FranceSELMET, INRAE, CIRAD, Montpellier Supagro, University of Montpellier, Montpellier, FranceCIRAD, UMR INTERTRYP, F-34398 Montpellier, France; INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, FranceAnimal 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. https://peercommunityjournal.org/articles/10.24072/pcjournal.239/
spellingShingle Peylhard, Moana
Berthier, David
Dayo, Guiguigbaza-Kossigan
Chantal, Isabelle
Sylla, Souleymane
Nidelet, Sabine
Dubois, Emeric
Martin, Guillaume
Sempéré, Guilhem
Flori, Laurence
Thévenon, Sophie
Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
Peer Community Journal
title Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
title_full Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
title_fullStr Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
title_full_unstemmed Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
title_short Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by Trypanosoma congolense
title_sort whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by trypanosoma congolense
url https://peercommunityjournal.org/articles/10.24072/pcjournal.239/
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