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Whole blood transcriptome of five West African cattle breeds before and during an infection by Trypanosoma congolense IL1180, inference on trypanotolerance

ABSTRACT: 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 West African taurine breeds called trypanotolerant according to their ability to control parasite development and to survive and grow in enzootic areas, and indicine breeds that are trypanosusceptible to the disease. Until now the genetic basis of trypanotolerance remains unclear. Here, we improved knowledge in the biological processes involved in trypanotolerance by identifying bovine genes differentially expressed during an experimental infection by Trypanosoma congolense and their biological functions. To this end, whole blood genome-wide transcriptome profiling by RNA sequencing was performed on five West African cattle breeds, three trypanotolerant taurine breeds (N'Dama, Lagune and Baoulé), one susceptible zebu (Zebu Fulani) and one African taurine x zebu admixed breed (Borgou), at four dates, one before and three during infection. As expected, infection had a major impact on cattle blood transcriptome whatever 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 cells functions at the chronic stage of infection. More importantly, we highlighted overlooked features, as a strong disturbance in host metabolism and cell production energy that differentiate trypantolerant and trypanosusceptible breeds. N'Dama breed showed the earliest regulation of immune response, associated with a strong activation of cellular energy production, this last feature being also shared with Lagune, and to a lesser extent with Baoulé. Susceptible Zebu Fulani breed was distinguished from other breeds by the strongest modification in lipid metabolism regulation. Lastly, basal differences in gene expression reflected the structuration of cattle genetic diversity, and could have consequences on the tolerant or susceptible phenotype. Overall, it would be of value to deeper investigate interactions between immune response and cell metabolism that likely impact disease outcome.

ORGANISM(S): Bos taurus

PROVIDER: GSE197108 | GEO | 2023/02/28

REPOSITORIES: GEO

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Project description:Background: African animal trypanosomiasis (AAT) caused by tsetse fly-transmitted protozoa of the genus Trypanosoma is a major constraint on livestock and agricultural production in Africa and is among the top ten global cattle diseases impacting on the poor. Here we show that a functional genomics approach can be used to identify temporal changes in host peripheral blood mononuclear cell (PBMC) gene expression due to disease progression. We also show that major gene expression differences exist between cattle from trypanotolerant and trypanosusceptible breeds. Using bovine long oligonucleotide microarrays and real time quantitative reverse transcription PCR (qRT-PCR) validation we analysed PBMC gene expression in naïve trypanotolerant and trypanosusceptible cattle experimentally challenged with Trypanosoma congolense across a 34-day infection time course. Results: Trypanotolerant N’Dama cattle displayed a rapid and distinct transcriptional response to infection, with a ten-fold higher number of genes differentially expressed at day 14 post infection compared to trypanosusceptible Boran cattle. These analyses identified coordinated temporal gene expression changes for both breeds in responses to trypanosome infection. In addition, a panel of genes were identified that showed pronounced differences in gene expression between the two breeds, which may underlie the phenomena of trypanotolerance and trypanosusceptibility. Gene ontology (GO) analysis demonstrate that the products of these genes may contribute to increased mitochondrial mRNA translational efficiency, a more pronounced B cell response, an elevated activation status and a heightened response to stress in trypanotolerant cattle. Conclusions: This study has revealed an extensive and diverse range of cellular processes that are altered temporally in response to trypanosome infection in African cattle. Results indicate that the trypanotolerant N’Dama cattle respond more rapidly and with a greater magnitude to infection compared to the trypanosusceptible Boran cattle. Specifically, a subset of the genes analyzed by qRT-PCR, which display significant breed differences, could collectively contribute to the trypanotolerance trait in N’Dama.

Project description:Background: The Malnad Gidda are unique dwarf Bos indicus cattle native to heavy rainfall Malnad and coastal areas of Karnataka in India. These cattle are highly adapted to harsh climatic conditions and are more resistant to Foot and Mouth disease as compared to other breeds of B.indicus. Since the first genome reference became available from B.taurus Hereford breed, only a few other breeds have been genotyped using high-throughput platforms. Also despite the known reports on high diversity within indicine breeds as compared to taurine breeds, only one draft genome of Nellore and horn transcriptome of Kankrej breed were sequenced at base level resolution. Because of the special characteristics Malnad Gidda possess, it becomes the choice of breed among many indicine cows to study at molecular level and genotyping. Results: Sequencing mRNA from the PBMCs isolated from blood of one selected Malnad Gidda bull resulted in generation of 55 million paired-end reads of 100bp length. Raw sequencing data is processed to trim the adaptor and low quality bases, and are aligned against the whole genome and transcript assemblies of Bos taurus UMD 3.1 and Bos indicus (Nellore breed) respectively. About 72% of the sequenced reads from our study could be mapped against the B.taurus genome where as only 41% of reads could be mapped against the Bos indicus transcript assembly. Transcript assembly from the alignment carried out against the annotated B.taurus UMD 3.1 genome resulted in identification of ~10,000 genes with significant expression (FPKM>1). In a similar analysis against the B.indicus Kankrej assembled transcripts we could identify only ~6,000 transcripts. From the variant analysis of the sequencing data we found ~10,000 SNPs in coding regions among which ~9,000 are novel and ~6,400 are amino acid changing. Conclusions: For the first time we have genotyped and explored the transcriptome of B.indicus Malnad Gidda breed. A comparative analysis of mapping the RNA-Seq data against the available reference genome and transcript sequences is demonstrated. An enhanced utility of transcript sequencing could be achieved by improving or completing the sequence assembly of any B.indicus breed to better characterize the indicine breeds for productivity features and selective breeding.

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Whole blood transcriptome of five West African cattle breeds before and during an infection by Trypanosoma congolense IL1180, inference on trypanotolerance

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