miRNA sequencing analysis of healthy and atretic follicles of chickens revealed that miR-30a-5p inhibits granulosa cell death via targeting Beclin1

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Abstract

Background

The egg production performance of chickens is affected by many factors, including genetics, nutrition and environmental conditions. These factors all play a role in egg production by affecting the development of follicles. MicroRNAs (miRNAs) are important non-coding RNAs that regulate biological processes by targeting genes or other non-coding RNAs after transcription. In the animal reproduction process, miRNA is known to affect the development and atresia of follicles by regulating apoptosis and autophagy of granulosa cells (GCs).

Results

In this study, we identified potential miRNAs in the atretic follicles of broody chickens and unatretic follicles of healthy chickens. We identified gga-miR-30a-5p in 50 differentially expressed miRNAs and found that gga-miR-30a-5p played a regulatory role in the development of chicken follicles. The function of miR-30a-5p was explored through the transfection test of miR-30a-5p inhibitor and miR-30a-5p mimics. In the study, we used qPCR, western blot and flow cytometry to detect granulosa cell apoptosis, autophagy and steroid hormone synthesis. Confocal microscopy and transmission electron microscopy are used for the observation of autophagolysosomes. The levels of estradiol (E2), progesterone (P4), malondialdehyde (MDA) and superoxide dismutase (SOD) were detected by ELISA. The results showed that miR-30a-5p showed a negative effect on autophagy and apoptosis of granulosa cells, and also contributed in steroid hormones and reactive oxygen species (ROS) production. In addition, the results obtained from the biosynthesis and dual luciferase experiments showed that Beclin1 was the target gene of miR-30a-5p. The rescue experiment conducted further confirmed that Beclin1 belongs to the miR-30a-5p regulatory pathway.

Conclusions

In summary, after deep miRNA sequencing on healthy and atretic follicles, the results indicated that miR-30a-5p inhibits granulosa cell death by inhibiting Beclin1.

Supplementary Information

The online version contains supplementary material available at 10.1186/s40104-022-00697-0.

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Most cited references 41

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Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

Michael Love, Wolfgang Huber, Simon Anders (2014)

In comparative high-throughput sequencing assays, a fundamental task is the analysis of count data, such as read counts per gene in RNA-seq, for evidence of systematic changes across experimental conditions. Small replicate numbers, discreteness, large dynamic range and the presence of outliers require a suitable statistical approach. We present DESeq2, a method for differential analysis of count data, using shrinkage estimation for dispersions and fold changes to improve stability and interpretability of estimates. This enables a more quantitative analysis focused on the strength rather than the mere presence of differential expression. The DESeq2 package is available at http://www.bioconductor.org/packages/release/bioc/html/DESeq2.html. Electronic supplementary material The online version of this article (doi:10.1186/s13059-014-0550-8) contains supplementary material, which is available to authorized users.

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miRBase: from microRNA sequences to function

Ana Kozomara, Maria Birgaoanu, Sam Griffiths-Jones (2018)

Abstract miRBase catalogs, names and distributes microRNA gene sequences. The latest release of miRBase (v22) contains microRNA sequences from 271 organisms: 38 589 hairpin precursors and 48 860 mature microRNAs. We describe improvements to the database and website to provide more information about the quality of microRNA gene annotations, and the cellular functions of their products. We have collected 1493 small RNA deep sequencing datasets and mapped a total of 5.5 billion reads to microRNA sequences. The read mapping patterns provide strong support for the validity of between 20% and 65% of microRNA annotations in different well-studied animal genomes, and evidence for the removal of >200 sequences from the database. To improve the availability of microRNA functional information, we are disseminating Gene Ontology terms annotated against miRBase sequences. We have also used a text-mining approach to search for microRNA gene names in the full-text of open access articles. Over 500 000 sentences from 18 542 papers contain microRNA names. We score these sentences for functional information and link them with 12 519 microRNA entries. The sentences themselves, and word clouds built from them, provide effective summaries of the functional information about specific microRNAs. miRBase is publicly and freely available at http://mirbase.org/.

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The Beclin 1 network regulates autophagy and apoptosis.

R Kang, H Zeh, M Lotze … (2011)

Beclin 1, the mammalian orthologue of yeast Atg6, has a central role in autophagy, a process of programmed cell survival, which is increased during periods of cell stress and extinguished during the cell cycle. It interacts with several cofactors (Atg14L, UVRAG, Bif-1, Rubicon, Ambra1, HMGB1, nPIST, VMP1, SLAM, IP(3)R, PINK and survivin) to regulate the lipid kinase Vps-34 protein and promote formation of Beclin 1-Vps34-Vps15 core complexes, thereby inducing autophagy. In contrast, the BH3 domain of Beclin 1 is bound to, and inhibited by Bcl-2 or Bcl-XL. This interaction can be disrupted by phosphorylation of Bcl-2 and Beclin 1, or ubiquitination of Beclin 1. Interestingly, caspase-mediated cleavage of Beclin 1 promotes crosstalk between apoptosis and autophagy. Beclin 1 dysfunction has been implicated in many disorders, including cancer and neurodegeneration. Here, we summarize new findings regarding the organization and function of the Beclin 1 network in cellular homeostasis, focusing on the cross-regulation between apoptosis and autophagy. © 2011 Macmillan Publishers Limited

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Author and article information

Contributors

Qing Zhu: zhuqing@sicau.edu.cn

Huadong Yin:

ORCID: http://orcid.org/0000-0002-9546-5753

yinhuadong@sicau.edu.cn

Journal

Journal ID (nlm-ta): J Anim Sci Biotechnol

Journal ID (iso-abbrev): J Anim Sci Biotechnol

Title: Journal of Animal Science and Biotechnology

Publisher: BioMed Central (London )

ISSN (Print): 1674-9782

ISSN (Electronic): 2049-1891

Publication date (Electronic): 12 April 2022

Publication date PMC-release: 12 April 2022

Publication date Collection: 2022

Volume: 13

Electronic Location Identifier: 55

Affiliations

[1 ]GRID grid.80510.3c, ISNI 0000 0001 0185 3134, Farm Animal Genetic Resources Exploration and Innovation Key Laboratory of Sichuan Province, , Sichuan Agricultural University, ; Chengdu, 611130 Sichuan China

[2 ]GRID grid.22935.3f, ISNI 0000 0004 0530 8290, National Engineering Laboratory for Animal Breeding and Key Laboratory of Animal Genetics, Breeding and Reproduction, Ministry of Agriculture and Rural Affairs, College of Animal Science and Technology, , China Agricultural University, ; Beijing, 100193 China

[3 ]GRID grid.410636.6, ISNI 0000 0004 1761 0833, Animal Breeding and Genetics key Laboratory of Sichuan Province, , Sichuan Animal Science Academy, ; Chengdu, 610066 China

[4 ]GRID grid.80510.3c, ISNI 0000 0001 0185 3134, College of Resources, , Sichuan Agricultural University, ; Chengdu, 611130 China

Author information

Huadong Yin http://orcid.org/0000-0002-9546-5753

Article

Publisher ID: 697

DOI: 10.1186/s40104-022-00697-0

PMC ID: 9003977

PubMed ID: 35410457

SO-VID: 9df38cb5-482a-4d7e-9023-4f4fac1efa8a

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 : 16 October 2021

Date accepted : 21 February 2022

Funding

Funded by: FundRef http://dx.doi.org/10.13039/501100004829, Department of Science and Technology of Sichuan Province;

Award ID: 2021YFYZ0007

Award ID: 2021YFYZ0031

Funded by: China Agriculture Research System of MOF and MARA

Award ID: CARS-40

Custom metadata

ScienceOpen disciplines: Animal science & Zoology

Keywords: apoptosis,autophagy,beclin1,chicken granulosa cells,mir-30a-5p,oxidative stress,rna-seq,steroid hormone

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ScienceOpen disciplines: Animal science & Zoology

Keywords: apoptosis, autophagy, beclin1, chicken granulosa cells, mir-30a-5p, oxidative stress, rna-seq, steroid hormone

miRNA sequencing analysis of healthy and atretic follicles of chickens revealed that miR-30a-5p inhibits granulosa cell death via targeting Beclin1

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Abstract

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Results

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Supplementary Information

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Primate Tool Use

Most cited references 41

Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2

miRBase: from microRNA sequences to function

The Beclin 1 network regulates autophagy and apoptosis.

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