Circular RNA ciRS-7 affects the propagation of <i>Cryptosporidium parvum</i> in HCT-8 cells by sponging miR-1270 to activate the NF-κB signaling pathway

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Abstract

Background

Cryptosporidium is an important zoonotic pathogen responsible for severe enteric diseases in humans and animals. However, the molecular mechanisms underlying host and Cryptosporidium interactions are still not clear.

Methods

To study the roles of circRNAs in host cells during Cryptosporidium infection, the expression profiles of circRNAs in HCT-8 cells infected with C. parvum were investigated using a microarray assay, and the regulatory role of a significantly upregulated circRNA, ciRS-7, was investigated during C. parvum infection.

Results

C. parvum infection caused notable alterations in the expression profiles of circRNAs in HCT-8 cells, and a total of 178 (including 128 up- and 50 downregulated) circRNAs were significantly differentially expressed following C. parvum infection. Among them, ciRS-7 was significantly upregulated and regulated the NF-κB signaling pathway by sponging miR-1270 during C. parvum infection. Furthermore, the ciRS-7/miR-1270/ relA axis markedly affected the propagation of C. parvum in HCT-8 cells.

Conclusions

Our results revealed that ciRS-7 would promote C. parvum propagation by regulating the miR-1270/ relA axis and affecting the NF-κB pathway. To the best of our knowledge, this is the first study to investigate the role of circRNA during Cryptosporidium infection, and the findings provide a novel view for implementing control strategies against Cryptosporidium infection.

Graphic Abstract

Supplementary Information

The online version contains supplementary material available at 10.1186/s13071-021-04739-w.

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Most cited references 50

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Cytoscape: a software environment for integrated models of biomolecular interaction networks.

Paul Shannon, Andrew Markiel, Owen Ozier … (2003)

Cytoscape is an open source software project for integrating biomolecular interaction networks with high-throughput expression data and other molecular states into a unified conceptual framework. Although applicable to any system of molecular components and interactions, Cytoscape is most powerful when used in conjunction with large databases of protein-protein, protein-DNA, and genetic interactions that are increasingly available for humans and model organisms. Cytoscape's software Core provides basic functionality to layout and query the network; to visually integrate the network with expression profiles, phenotypes, and other molecular states; and to link the network to databases of functional annotations. The Core is extensible through a straightforward plug-in architecture, allowing rapid development of additional computational analyses and features. Several case studies of Cytoscape plug-ins are surveyed, including a search for interaction pathways correlating with changes in gene expression, a study of protein complexes involved in cellular recovery to DNA damage, inference of a combined physical/functional interaction network for Halobacterium, and an interface to detailed stochastic/kinetic gene regulatory models.

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Natural RNA circles function as efficient microRNA sponges.

Thomas B. Hansen, Trine I. Jensen, Bettina H. Clausen … (2014)

MicroRNAs (miRNAs) are important post-transcriptional regulators of gene expression that act by direct base pairing to target sites within untranslated regions of messenger RNAs. Recently, miRNA activity has been shown to be affected by the presence of miRNA sponge transcripts, the so-called competing endogenous RNA in humans and target mimicry in plants. We previously identified a highly expressed circular RNA (circRNA) in human and mouse brain. Here we show that this circRNA acts as a miR-7 sponge; we term this circular transcript ciRS-7 (circular RNA sponge for miR-7). ciRS-7 contains more than 70 selectively conserved miRNA target sites, and it is highly and widely associated with Argonaute (AGO) proteins in a miR-7-dependent manner. Although the circRNA is completely resistant to miRNA-mediated target destabilization, it strongly suppresses miR-7 activity, resulting in increased levels of miR-7 targets. In the mouse brain, we observe overlapping co-expression of ciRS-7 and miR-7, particularly in neocortical and hippocampal neurons, suggesting a high degree of endogenous interaction. We further show that the testis-specific circRNA, sex-determining region Y (Sry), serves as a miR-138 sponge, suggesting that miRNA sponge effects achieved by circRNA formation are a general phenomenon. This study serves as the first, to our knowledge, functional analysis of a naturally expressed circRNA.

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Is Open Access

starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein–RNA interaction networks from large-scale CLIP-Seq data

Jun-Hao Li, Shun Liu, Hui Zhou … (2013)

Although microRNAs (miRNAs), other non-coding RNAs (ncRNAs) (e.g. lncRNAs, pseudogenes and circRNAs) and competing endogenous RNAs (ceRNAs) have been implicated in cell-fate determination and in various human diseases, surprisingly little is known about the regulatory interaction networks among the multiple classes of RNAs. In this study, we developed starBase v2.0 (http://starbase.sysu.edu.cn/) to systematically identify the RNA–RNA and protein–RNA interaction networks from 108 CLIP-Seq (PAR-CLIP, HITS-CLIP, iCLIP, CLASH) data sets generated by 37 independent studies. By analyzing millions of RNA-binding protein binding sites, we identified ∼9000 miRNA-circRNA, 16 000 miRNA-pseudogene and 285 000 protein–RNA regulatory relationships. Moreover, starBase v2.0 has been updated to provide the most comprehensive CLIP-Seq experimentally supported miRNA-mRNA and miRNA-lncRNA interaction networks to date. We identified ∼10 000 ceRNA pairs from CLIP-supported miRNA target sites. By combining 13 functional genomic annotations, we developed miRFunction and ceRNAFunction web servers to predict the function of miRNAs and other ncRNAs from the miRNA-mediated regulatory networks. Finally, we developed interactive web implementations to provide visualization, analysis and downloading of the aforementioned large-scale data sets. This study will greatly expand our understanding of ncRNA functions and their coordinated regulatory networks.

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Author and article information

Contributors

Yan-Ling Yin: YinYanLing@nwafu.edu.cn

Ting-Li Liu: LTL1114@163.com

Qian Yao: yaoqian@nwafu.edu.cn

Yu-Xin Wang: 2019@nwafu.edu.cn

Xue-Mei Wu: 2019050504@nwafu.edu.cn

Xue-Ting Wang: wxt910521@163.com

Xin Yang: xinyang@nwafu.edu.cn

Jun-Ke Song: sjk7998@163.com

Guang-Hui Zhao:

ORCID: http://orcid.org/0000-0002-3511-6332

zgh083@nwsuaf.edu.cn

Journal

Journal ID (nlm-ta): Parasit Vectors

Journal ID (iso-abbrev): Parasit Vectors

Title: Parasites & Vectors

Publisher: BioMed Central (London )

ISSN (Electronic): 1756-3305

Publication date (Electronic): 6 May 2021

Publication date PMC-release: 6 May 2021

Publication date Collection: 2021

Volume: 14

Electronic Location Identifier: 238

Affiliations

[1 ]GRID grid.144022.1, ISNI 0000 0004 1760 4150, Department of Parasitology, College of Veterinary Medicine, , Northwest A&F University, ; Yangling, China

[2 ]GRID grid.454892.6, ISNI 0000 0001 0018 8988, State Key Laboratory of Veterinary Etiological Biology, Key Laboratory of Veterinary Parasitology of Gansu Province, , Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences, ; Lanzhou, China

Author information

Guang-Hui Zhao http://orcid.org/0000-0002-3511-6332

Article

Publisher ID: 4739

DOI: 10.1186/s13071-021-04739-w

PMC ID: 8101149

PubMed ID: 33957927

SO-VID: e8e2e446-9059-4fc9-b298-550a2c76cfae

License:

Open AccessThis article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/. The Creative Commons Public Domain Dedication waiver ( http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated in a credit line to the data.

History

Date received : 24 February 2021

Date accepted : 21 April 2021

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100001809, National Natural Science Foundation of China;

Award ID: 32072890

Award Recipient : Guang-Hui Zhao

Funded by: the Open Funds of the State Key Laboratory of Veterinary Aetiological Biology, Lanzhou Veterinary Research Institute, Chinese Academy of Agricultural Sciences

Award ID: SKLVEB2020KFKT015

Award Recipient : Guang-Hui Zhao

Funded by: National Key Research and Development Program of China

Award ID: 2017YFD0501305

Award Recipient : Guang-Hui Zhao

Funded by: The Innovation Support Plan of Shaanxi Province

Award ID: 2021TD-31

Custom metadata

ScienceOpen disciplines: Parasitology

Keywords: c. parvum,circrnas,cirs-7/mir-1270/rela axis,propagation,nf-κb signaling pathway

Data availability:

ScienceOpen disciplines: Parasitology

Keywords: c. parvum, circrnas, cirs-7/mir-1270/rela axis, propagation, nf-κb signaling pathway

Circular RNA ciRS-7 affects the propagation of Cryptosporidium parvum in HCT-8 cells by sponging miR-1270 to activate the NF-κB signaling pathway

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Most cited references 50

Cytoscape: a software environment for integrated models of biomolecular interaction networks.

Natural RNA circles function as efficient microRNA sponges.

starBase v2.0: decoding miRNA-ceRNA, miRNA-ncRNA and protein–RNA interaction networks from large-scale CLIP-Seq data

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