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Section: Infections
Topic: Biology of interactions, Microbiology

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

Peylhard, Moana1, 2 ; Berthier, David1, 2 ; Dayo, Guiguigbaza-Kossigan3 ; Chantal, Isabelle1, 2 ; Sylla, Souleymane3; Nidelet, Sabine4; Dubois, Emeric4 ; Martin, Guillaume5, 6 ; Sempéré, Guilhem1, 2 ; Flori, Laurence7 ; Thévenon, Sophie1, 2  
1 CIRAD, UMR INTERTRYP, F-34398 Montpellier, France
2 INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, France
3 Centre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), 01 BP 454, Bobo-Dioulasso 01, Burkina Faso
4 Montpellier GenomiX, France Génomique, Montpellier, France
5 CIRAD, UMR AGAP Institut, F-34398 Montpellier, France
6 UMR AGAP Institut, Univ Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France
7 SELMET, INRAE, CIRAD, Montpellier Supagro, University of Montpellier, Montpellier, France

10.24072/pcjournal.239 - Peer Community Journal, Volume 3 (2023), article no. e17.

Get full text PDF Peer reviewed and recommended by PCI

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.

Published online:
DOI: 10.24072/pcjournal.239
Type: Research article
Peylhard, Moana 1, 2; Berthier, David 1, 2; Dayo, Guiguigbaza-Kossigan 3; Chantal, Isabelle 1, 2; Sylla, Souleymane 3; Nidelet, Sabine 4; Dubois, Emeric 4; Martin, Guillaume 5, 6; Sempéré, Guilhem 1, 2; Flori, Laurence 7; Thévenon, Sophie 1, 2

1 CIRAD, UMR INTERTRYP, F-34398 Montpellier, France
2 INTERTRYP, Univ. Montpellier, CIRAD, IRD, Montpellier, France
3 Centre International de Recherche-Développement sur l'Elevage en zone Subhumide (CIRDES), 01 BP 454, Bobo-Dioulasso 01, Burkina Faso
4 Montpellier GenomiX, France Génomique, Montpellier, France
5 CIRAD, UMR AGAP Institut, F-34398 Montpellier, France
6 UMR AGAP Institut, Univ Montpellier, CIRAD, INRAE, Institut Agro, Montpellier, France
7 SELMET, INRAE, CIRAD, Montpellier Supagro, University of Montpellier, Montpellier, France
License: CC-BY 4.0
Copyrights: The authors retain unrestricted copyrights and publishing rights 
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     author = {Peylhard, Moana and Berthier, David and Dayo, Guiguigbaza-Kossigan and Chantal, Isabelle and Sylla, Souleymane and Nidelet, Sabine and Dubois, Emeric and Martin, Guillaume and Semp\'er\'e, Guilhem and Flori, Laurence and Th\'evenon, Sophie},
     title = {Whole blood transcriptome profiles of trypanotolerant and trypanosusceptible cattle highlight a differential modulation of metabolism and immune response during infection by {\protect\emph{Trypanosoma} congolense}},
     journal = {Peer Community Journal},
     eid = {e17},
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     year = {2023},
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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, Volume 3 (2023), article  no. e17. doi : 10.24072/pcjournal.239. https://peercommunityjournal.org/articles/10.24072/pcjournal.239/

Peer reviewed and recommended by PCI : 10.24072/pci.infections.100008

Conflict of interest of the recommender and peer reviewers:
The recommender in charge of the evaluation of the article and the reviewers declared that they have no conflict of interest (as defined in the code of conduct of PCI) with the authors or with the content of the article.

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