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Whole transcriptome analysis of Mycoplasma bovis-host interactions under in vitro and in vivo conditions

ABSTRACT: Mycoplasma bovis mastitis is becoming increasingly problematic for dairy cattle farming in different parts of the world. M. bovis is inherently resistant to several antimicrobial classes and there is no effective vaccine. The major constraints to developing effective control tools are limited knowledge of M. bovis virulence factors and the underlying pathogenic mechanisms. The objective of this study was to determine virulence-associated genes of M. bovis and host immune response genes expressed during the early stages of host-pathogen interactions. In this study, we conducted in vitro infection of mammary epithelial cell (MAC-T) lines and in vivo intramammary infection of dairy cows with M. bovis strain PG45 and evaluated whole transcriptome differential gene expression and pathway enrichment analysis. We found a total of 614 (304 up-regulated, 310 down-regulated) and 7161 (3935 up-regulated, 3226 down-regulated) genes of M. bovis and bovine host cells were differentially expressed, respectively. Of the up-regulated genes of M. bovis, insertion sequence (IS) genes that are involved in transposase activity such as ISMbov1, ISMbov2, ISMbov3, and ISMbov9 were significantly up-regulated, whereas protein translation-associated genes were significantly down-regulated. In MAC-T cells, genes involved in apoptosis pathways and proinflammatory cytokines were significantly up-regulated, whereas genes involved in cell cycle, ribosome biogenesis, and steroid biosynthesis were significantly down-regulated. Genes encoding formation of neutrophil extracellular traps and proinflammatory cytokines, were significantly up-regulated in the mammary gland of M. bovis challenged cows, whereas genes involved in steroid biosynthesis and metabolism were significantly down-regulated. In conclusion, there were increased expressions of IS elements which are involved in transposase activity during early stages of M. bovis infection. This observation warrants further detailed investigation to determine important specific potential targets involved in the transposition for intervention. Apoptosis might be in favor of progression of M. bovis infection but intervention that reduces apoptosis and enhances quick and effective polymorphonuclear neutrophilic recruitment with increased extracellular trap activity may improve M. bovis clearance. Our findings are key to determining important targets for immunity-based intervention. To our knowledge, this is the first whole transcriptome analysis in both M. bovis and the host under the same in vitro and in vivo conditions. Therefore, we recommend additional metatranscriptomic, metaproteomic, metabolomic and metagenomic evaluation of M. bovis and other potentially non-culturable microbes in the mammary glands during the pathogenesis of M. bovis mastitis in the bovine host to understand a complete picture of these interactions in maintaining healthy homeostatic state or mastitis.

ORGANISM(S): Bos taurus Mycoplasmopsis bovis

PROVIDER: GSE269146 | GEO | 2025/02/04

REPOSITORIES: GEO

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	GSE269146_GEO_sub_processed_data__1.xlsx	Xlsx
	GSE269146_GEO_sub_processed_data__2.xlsx	Xlsx
	GSE269146_GEO_sub_processed_data__3.xlsx	Xlsx

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Project description:Mastitis is one of the most prevalent and economically important diseases of dairy animals. The disease is caused by ascending bacterial infection through the teat canal. Among the most common mastitis-causing bacteria are gram-negative coliforms, gram-positive streptococci and staphylococci, and mycoplasma. The most prominent cellular hallmark of acute mammary infection is a massive recruitment of blood neutrophils into the tubular and alveolar milk spaces. The complex biological processes of leukocyte recruitment, activation, adhesion, and migration in the mammary gland remain largely elusive to date. While field research of mastitis in dairy animals contributed a lot to the development of mitigation, control, and even eradication programs, little progress was made toward understanding the molecular mechanisms underlying the pathogenesis of the disease. We report here experimental mastitis model systems in lactating mice challenged with field strains of common udder pathogens in dairy cows. We used these model systems to apply recently developed multiplex gene expression technology (Nanostring nCounter), which enabled us to study the expression of over 700 immune genes. Our analysis revealed a core of 100 genes that are similarly regulated and functionally or physically interacting in E. coli, M. bovis and Strep uberis murine mastitis. Common significantly enriched gene sets include TNFɑ signaling via NFkB, Interferon gamma and alpha response, and IL6-JAK-STAT3 signaling. In addition, we show a significantly enriched expression of genes associated with neutrophil extracellular traps (NET) in glands challenged by the three pathogens. Ligand-receptor analysis revealed interactions shared by the three pathogens, including the interaction of the cytokines IL1β, IL1ɑ, and TNFɑ with their receptors, and proteins involved in immune cell recruitment such as complement C3 and ICAM1 (with CD11b), chemokines CCL3 and CCL4 (with CCR1), and CSF3 (with CSF3R). Taken together, our results show that mammary infection with E. coli, M. bovis and Strep uberis culminated in the activation of a conserved core of immune genes and pathways including NET formation.

Project description:Over the past decades, Helicoverpa armigera nucleopolyhedrovirus (HearNPV) has been widely used for biocontrol of cotton bollworm, which is one of the most destructive pest insects in agriculture worldwide. However, the molecular mechanism underlying the interaction between HearNPV and host insects remains poorly understood. In this study, high throughput RNA-sequencing was integrated with label-free quantitative proteomics analysis to examine the dynamics of gene expression in the fat body of H. armigera larvae in response to challenge with HearNPV. RNA-sequencing-based transcriptomic analysis indicated that host gene expression was substantially altered, yielding 3,850 differentially expressed genes (DEGs), while no global transcriptional shut-off effects were observed in the fat body. Among the DEGs, 60 immunity-related genes were down-regulated after baculovirus infection, a finding that was consistent with the results of quantitative real-time RT-PCR (qRT-PCR). Gene ontology and functional classification demonstrated that the majority of down-regulated genes were enriched in gene cohorts involved in energy, carbohydrate, and amino acid metabolic pathways. Proteomics analysis identified differentially expressed proteins in the fat body, among which 76 were up-regulated, whereas 373 were significantly down-regulated upon infection. The down-regulated proteins are involved in metabolic pathways such as energy metabolism, carbohydrate metabolism (CM), and amino acid metabolism, in agreement with the RNA-seq data. Furthermore, correlation analysis suggested a strong association between the mRNA level and protein abundance in the H. armigera fat body. More importantly, the predicted gene interaction network indicated that a large subset of metabolic networks was significantly negatively regulated by viral infection, including CM-related enzymes such as aldolase, enolase, malate dehydrogenase and triose-phosphate isomerase. Taken together, transcriptomic combined with proteomic data elucidated that baculovirus established systemic infection of host larvae, and manipulated the host mainly by suppressing the host immune response and down-regulating metabolism to allow viral self-replication and proliferation. Therefore, this study provided important insights into the mechanism of host-baculovirus interaction.

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Whole transcriptome analysis of Mycoplasma bovis-host interactions under in vitro and in vivo conditions

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