RNA sequencing reveals dynamic expression of lncRNAs and mRNAs in caprine endometrial epithelial cells induced by Neospora caninum infection

Zhao, Shanshan; Tao, De-Liang; Chen, Jin‐Ming; Wu, Jiangping; Yang, Xin; Song, Jun-Ke; Zhu, Xingquan; Zhao, Guanghui

doi:10.1186/s13071-022-05405-5

Cited by 3 publications

(1 citation statement)

References 89 publications

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“…For example, a total of 81, 126, 82 and 131 miRNAs were differentially expressed (DE) in porcine alveolar macrophages [ 27 ], pig splenocytes [ 28 ], livers of domestic cats [ 29 ], and mouse spleen [ 30 ], respectively, during infections with Toxoplasma gondii , an obligate intracellular zoonotic protozoan parasite similar to N. caninum in its morphological and biological features but differing in its life cycle and biological effects on host cells [ 31 – 33 ]. Previously, our group found that N. caninum infection significantly altered the expression patterns of host cell long ncRNAs, which are some of the most important regulatory ncRNAs [ 34 ]. In the present study, we investigated dynamic miRNA profiles in caprine endometrial epithelial cells (EECs) during their infections with N. caninum .…”

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confidence: 99%

Temporal transcriptomic changes in microRNAs involved in the host immune response and metabolism during Neospora caninum infection

et al. 2023

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Background Neospora caninum infection is a major cause of abortion in cattle, which results in serious economic losses to the cattle industry. However, there are no effective drugs or vaccines for the control of N. caninum infections. There is increasing evidence that microRNAs (miRNAs) are involved in many physiological and pathological processes, and dysregulated expression of host miRNAs and the biological implications of this have been reported for infections by various protozoan parasites. However, to our knowledge, there is presently no published information on host miRNA expression during N. caninum infection. Methods The expression profiles of miRNAs were investigated by RNA sequencing (RNA-seq) in caprine endometrial epithelial cells (EECs) infected with N. caninum at 24 h post infection (pi) and 48 hpi, and the functions of differentially expressed (DE) miRNAs were predicted by Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analyses. The transcriptome data were validated by using quantitative real-time polymerase chain reaction. One of the upregulated DEmiRNAs, namely chi-miR-146a, was selected to study the effect of DEmiRNAs on the propagation of N. caninum tachyzoites in caprine EECs. Results RNA-seq showed 18 (17 up- and one downregulated) and 79 (54 up- and 25 downregulated) DEmiRNAs at 24 hpi and 48 hpi, respectively. Quantitative real-time polymerase chain reaction analysis of 13 randomly selected DEmiRNAs (10 up- and three downregulated miRNAs) confirmed the validity of the RNA-seq data. A total of 7835 messenger RNAs were predicted to be potential targets for 66 DEmiRNAs, and GO and KEGG enrichment analysis of these predicted targets revealed that DEmiRNAs altered by N. caninum infection may be involved in host immune responses (e.g. Fc gamma R-mediated phagocytosis, Toll-like receptor signaling pathway, tumor necrosis factor signaling pathway, transforming growth factor-β signaling pathway, mitogen-activated protein kinase signaling pathway) and metabolic pathways (e.g. lysine degradation, insulin signaling pathway, AMP-activated protein kinase signaling pathway, Rap1 signaling pathway, calcium signaling pathway). Upregulated chi-miR-146a was found to promote N. caninum propagation in caprine EECs. Conclusions This is, to our knowledge, the first report on the expression profiles of host miRNAs during infection with N. caninum, and shows that chi-miR-146a may promote N. caninum propagation in host cells. The novel findings of the present study should help to elucidate the interactions between host cells and N. caninum. Graphical Abstract

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Section: Introductionmentioning

confidence: 99%

Temporal transcriptomic changes in microRNAs involved in the host immune response and metabolism during Neospora caninum infection

et al. 2023

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Carnivore ‘Coccidia’

2023

Apicomplexa in Livestock

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Neospora caninum infection specifically suppresses the expression of a host lncRNA XR_001919077.1 to facilitate parasite propagation by modulating host cell mitochondrial function and autophagy

Zhao,

Tao,

Chen

et al. 2024

Microbiol Spectr

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Neospora caninum is one of the most common pathogens causing reproductive failure in ruminants (e.g., cattle and goats) worldwide. However, due to a poor understanding of the pathogenic mechanisms of N. caninum infection, no effective drugs and vaccines are currently available. Long non-coding RNAs (lncRNAs) have been reported to be important regulators involved in a great number of physiological and pathological processes. Our previous study found that N. caninum infection induced significantly aberrant expression of lncRNA profiles in caprine endometrial epithelial cells (EECs). In the present study, we found that N. caninum infection specifically suppressed the expression of a novel lncRNA, XR_001919077.1 , and knockdown of XR_001919077.1 with small interfering RNA significantly promoted the propagation of N. caninum in caprine EECs. Rapid amplification of cDNA ends analysis generated six splice variants of XR_001919077.1 , with lengths ranging from 592 to 694 nt. Transfection of the full length of each variant markedly inhibited the propagation of N. caninum in caprine EECs. Further study suggested that XR_001919077.1 acted as a sponge of Chi-miR-93-5p to promote the expression of sirt1 , and the XR_001919077.1 /Chi-miR-93-5p/ sirt1 axis significantly delayed the in vitro growth of N. caninum in caprine EECs by regulating host cell mitochondrial function and autophagy. Our findings provide a novel insight to understand the interactions between N. caninum and host cells. IMPORTANCE The uterus is an indispensable reproductive organ for embryo implantation and fetal growth. The endometrium is more vulnerable to infection by pathogenic microorganisms resulting in an increased risk of miscarriage. Neospora caninum is one of the most common pathogens causing miscarriage in ruminants and is able to naturally inhabit the uterus, with N. caninum tissue cysts found in the endometrium. Recent advances in N. caninum research have revealed aberrant expression of long non-coding RNA (lncRNA) profiles in infected caprine endometrial epithelial cells. In the present study, N. caninum , but not Toxoplasma gondii, which has similar morphological and biological features to N. caninum , specifically suppresses the expression of a host lncRNA, XR_ 001919077.1 , to impair host’s defense through the competitive endogenous RNA mechanism to modulate the host cell mitochondrial function and autophagy to facilitate parasite propagation. The findings suggest a novel immune evasion strategy of N. caninum to facilitate intracellular propagation and provide an alternative path to develop control strategies against neosporosis.

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RNA sequencing reveals dynamic expression of lncRNAs and mRNAs in caprine endometrial epithelial cells induced by Neospora caninum infection

Cited by 3 publications

References 89 publications

Temporal transcriptomic changes in microRNAs involved in the host immune response and metabolism during Neospora caninum infection

Temporal transcriptomic changes in microRNAs involved in the host immune response and metabolism during Neospora caninum infection

Carnivore ‘Coccidia’

Neospora caninum infection specifically suppresses the expression of a host lncRNA XR_001919077.1 to facilitate parasite propagation by modulating host cell mitochondrial function and autophagy

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