Transcriptome Profiling of Goose Ovarian Follicle Granulosa Cells Reveals Key Regulatory Networks for Follicle Selection
Abstract
:Simple Summary
Abstract
1. Introduction
2. Materials and Methods
2.1. Ethical Approval
2.2. Animal Resources and Sample Collection
2.3. RNA Isolation, Library Construction, and Sequencing
2.4. Targets Prediction and Enrichment Analysis
2.5. Construction of the lncRNA-miRNA-mRNA Regulatory Network
2.6. Confirmation of the Expression Level of mRNAs, miRNAs, and lncRNAs
3. Results
3.1. mRNA, miRNA, and lncRNA Transcriptomes of Geese Granulosa Cells
3.2. Identification of Transcripts Involved in Follicle Selection in Granulosa Cells
3.3. Enrichment Analysis of the Selected mRNAs, miRNAs, and lncRNAs
3.4. Construction and Analysis of ceRNAs Regulatory Network
3.5. Real-time PCR Validation of DE-mRNAs, DE-lncRNAs, and DE-miRNAs
4. Discussion
5. Conclusions
Supplementary Materials
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Johnson, P.A.; Stephens, C.S.; Giles, J.R. The domestic chicken: Causes and consequences of an egg a day. Poult. Sci. 2015, 94, 816–820. [Google Scholar] [CrossRef] [PubMed]
- Wang, Z.; Wang, L.; Zhang, Y.; Yao, Y.; Zhao, W.; Xu, Q.; Chen, G. Characterization of ovarian morphology and reproductive hormones in Zhedong white geese (Anser cygnoides domesticus) during the reproductive cycle. J. Anim. Physiol. Anim. Nutr. 2021, 105, 938–945. [Google Scholar] [CrossRef] [PubMed]
- Apperson, K.D.; Bird, K.E.; Cherian, G.; Löhr, C.V. Histology of the Ovary of the Laying Hen (Gallus domesticus). Vet. Sci. 2017, 4, 66. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson, P.A. Follicle selection in the avian ovary. Reprod. Domest. Anim. 2012, 47, 283–287. [Google Scholar] [CrossRef] [PubMed]
- Qin, H.; Li, X.; Wang, J.; Sun, G.; Mu, X.; Ji, R. Ovarian transcriptome profile from pre-laying period to broody period of Xupu goose. Poult. Sci. 2021, 100, 101403. [Google Scholar] [CrossRef]
- Xu, Q.; Zhao, W.; Chen, Y.; Tong, Y.; Rong, G.; Huang, Z.; Zhang, Y.; Chang, G.; Wu, X.; Chen, G. Transcriptome profiling of the goose (Anser cygnoides) ovaries identify laying and broodiness phenotypes. PLoS ONE 2013, 8, e55496. [Google Scholar] [CrossRef] [Green Version]
- Zhao, X.Y.; Wu, Y.P.; Li, H.Y.; Cao, Y.; Mei, Z.Y.; Li, J.H. Differential expression and functional analysis of circRNA in the ovaries of Yili geese at different egg-laying stages. Genes Genom. 2022, 44, 1171–1180. [Google Scholar] [CrossRef]
- Li, Q.; Hu, S.; Wang, Y.; Deng, Y.; Yang, S.; Hu, J.; Li, L.; Wang, J. mRNA and miRNA Transcriptome Profiling of Granulosa and Theca Layers from Geese Ovarian Follicles Reveals the Crucial Pathways and Interaction Networks for Regulation of Follicle Selection. Front Genet. 2019, 10, 988. [Google Scholar] [CrossRef] [Green Version]
- Lei, M.; Chen, R.; Qin, Q.; Zhu, H.; Shi, Z. Transcriptome analysis to unravel the gene expression profile of ovarian follicular development in Magang goose. J. Reprod. Dev. 2020, 66, 331–340. [Google Scholar] [CrossRef] [Green Version]
- Kurowska, P.; Mlyczyńska, E.; Dawid, M.; Sierpowski, M.; Estienne, A.; Dupont, J.; Rak, A. Adipokines change the balance of proliferation/apoptosis in the ovarian cells of human and domestic animals: A comparative review. Anim. Reprod. Sci. 2021, 228, 106737. [Google Scholar] [CrossRef]
- Manabe, N.; Goto, Y.; Matsuda-Minehata, F.; Inoue, N.; Maeda, A.; Sakamaki, K.; Miyano, T. Regulation mechanism of selective atresia in porcine follicles: Regulation of granulosa cell apoptosis during atresia. J. Reprod. Dev. 2004, 50, 493–514. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Chen, R.; Dai, Z.C.; Zhu, H.X.; Lei, M.M.; Li, Y.; Shi, Z.D. Active immunization against AMH reveals its inhibitory role in the development of pre-ovulatory follicles in Zhedong White geese. Theriogenology 2020, 144, 185–193. [Google Scholar] [CrossRef]
- Qin, Q.; Sun, A.; Guo, R.; Lei, M.; Ying, S.; Shi, Z. The characteristics of oviposition and hormonal and gene regulation of ovarian follicle development in Magang geese. Reprod. Biol. Endocrinol. 2013, 11, 65. [Google Scholar] [CrossRef] [Green Version]
- Lin, X.; Ma, Y.; Qian, T.; Yao, J.; Mi, Y.; Zhang, C. Basic fibroblast growth factor promotes prehierarchical follicle growth and yolk deposition in the chicken. Theriogenology 2019, 139, 90–97. [Google Scholar] [CrossRef] [PubMed]
- Tung, C.T.; Lin, H.J.; Lin, C.W.; Mersmann, H.J.; Ding, S.T. The role of dynamin in absorbing lipids into endodermal epithelial cells of yolk sac membranes during embryonic development in Japanese quail. Poult. Sci. 2021, 100, 101470. [Google Scholar] [CrossRef] [PubMed]
- Wen, R.; Gan, X.; Hu, S.; Gao, S.; Deng, Y.; Qiu, J.; Sun, W.; Li, L.; Han, C.; Hu, J.; et al. Evidence for the existence of de novo lipogenesis in goose granulosa cells. Poult. Sci. 2019, 98, 1023–1030. [Google Scholar] [CrossRef]
- Santos, P.H.; Nunes, S.G.; Franchi, F.F.; Giroto, A.B.; Fontes, P.K.; Pinheiro, V.G.; Castilho, A.C.S. Expression of bta-miR-222 and LHCGR in bovine cultured granulosa cells: Impact of follicle deviation and regulation by FSH/insulin in vitro. Theriogenology 2022, 182, 71–77. [Google Scholar] [CrossRef]
- Santos, P.H.; Satrapa, R.A.; Fontes, P.K.; Franchi, F.F.; Razza, E.M.; Mani, F.; Nogueira, M.F.G.; Barros, C.M.; Castilho, A.C.S. Effect of superstimulation on the expression of microRNAs and genes involved in steroidogenesis and ovulation in Nelore cows. Theriogenology 2018, 110, 192–200. [Google Scholar] [CrossRef] [Green Version]
- Salilew-Wondim, D.; Ahmad, I.; Gebremedhn, S.; Sahadevan, S.; Hossain, M.D.; Rings, F.; Hoelker, M.; Tholen, E.; Neuhoff, C.; Looft, C.; et al. The expression pattern of microRNAs in granulosa cells of subordinate and dominant follicles during the early luteal phase of the bovine estrous cycle. PLoS ONE 2014, 9, e106795. [Google Scholar] [CrossRef]
- De Nardo Maffazioli, G.; Baracat, E.C.; Soares, J.M.; Carvalho, K.C.; Maciel, G.A.R. Evaluation of circulating microRNA profiles in Brazilian women with polycystic ovary syndrome: A preliminary study. PLoS ONE 2022, 17, e0275031. [Google Scholar] [CrossRef]
- Soyman, Z.; Durmus, S.; Ates, S.; Simsek, G.; Sozer, V.; Kundaktepe, B.P.; Kurtulus, D.; Gelisgen, R.; Sal, V.; Uzun, H. Circulating Mir-132, Mir-146a, Mir-222, and Mir-320 Expression in Differential Diagnosis of Women with Polycystic Ovary Syndrome. Acta Endocrinol. 2022, 18, 13–19. [Google Scholar] [CrossRef] [PubMed]
- Mao, Z.; Li, T.; Zhao, H.; Qin, Y.; Wang, X.; Kang, Y. Identification of epigenetic interactions between microRNA and DNA methylation associated with polycystic ovarian syndrome. J. Hum. Genet. 2021, 66, 123–137. [Google Scholar] [CrossRef] [PubMed]
- Li, R.; Yu, Y.; Jaafar, S.O.; Baghchi, B.; Farsimadan, M.; Arabipour, I.; Vaziri, H. Genetic Variants miR-126, miR-146a, miR-196a2, and miR-499 in Polycystic Ovary Syndrome. Br. J. Biomed. Sci. 2022, 79, 10209. [Google Scholar] [CrossRef] [PubMed]
- Qu, Q.; Liu, L.; Cui, Y.; Liu, H.; Yi, J.; Bing, W.; Liu, C.; Jiang, D.; Bi, Y. miR-126-3p containing exosomes derived from human umbilical cord mesenchymal stem cells promote angiogenesis and attenuate ovarian granulosa cell apoptosis in a preclinical rat model of premature ovarian failure. Stem Cell Res. Ther. 2022, 13, 352. [Google Scholar] [CrossRef]
- Yuan, X.; Deng, X.; Zhou, X.; Zhang, A.; Xing, Y.; Zhang, Z.; Zhang, H.; Li, J. MiR-126-3p promotes the cell proliferation and inhibits the cell apoptosis by targeting TSC1 in the porcine granulosa cells. In Vitro Cell Dev. Biol. Anim. 2018, 54, 715–724. [Google Scholar] [CrossRef]
- Zhou, X.; He, Y.; Jiang, Y.; He, B.; Deng, X.; Zhang, Z.; Yuan, X.; Li, J. MiR-126-3p inhibits apoptosis and promotes proliferation by targeting phosphatidylinositol 3-kinase regulatory subunit 2 in porcine ovarian granulosa cells. Asian-Australas J. Anim. Sci. 2020, 33, 879–887. [Google Scholar] [CrossRef] [Green Version]
- Cheng, Y.; Zhang, Z.; Zhang, G.; Chen, L.; Zeng, C.; Liu, X.; Feng, Y. The Male-Biased Expression of miR-2954 Is Involved in the Male Pathway of Chicken Sex Differentiation. Cells 2022, 12, 4. [Google Scholar] [CrossRef]
- Li, J.; Li, C.; Li, Q.; Li, W.T.; Li, H.; Li, G.X.; Kang, X.T.; Liu, X.J.; Tian, Y.D. Identification of the Key microRNAs and miRNA-mRNA Interaction Networks during the Ovarian Development of Hens. Animals 2020, 10, 1680. [Google Scholar] [CrossRef]
- Butler, A.E.; Ramachandran, V.; Hayat, S.; Dargham, S.R.; Cunningham, T.K.; Benurwar, M.; Sathyapalan, T.; Najafi-Shoushtari, S.H.; Atkin, S.L. Expression of microRNA in follicular fluid in women with and without PCOS. Sci. Rep. 2019, 9, 16306. [Google Scholar] [CrossRef] [Green Version]
- Liu, L.; Li, Q.; Yang, L.; Li, Q.; Du, X. SMAD4 feedback regulates the canonical TGF-beta signaling pathway to control granulosa cell apoptosis. Cell Death Dis. 2018, 9, 151. [Google Scholar] [CrossRef]
- Turri, F.; Capra, E.; Lazzari, B.; Cremonesi, P.; Stella, A.; Pizzi, F. A Combined Flow Cytometric Semen Analysis and miRNA Profiling as a Tool to Discriminate between High- and Low-Fertility Bulls. Front. Vet. Sci. 2021, 8, 703101. [Google Scholar] [CrossRef] [PubMed]
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Liu, J.; Dai, S.; Dai, Z.; Feng, Y.; Lei, M.; Chen, R.; Zhu, H. Transcriptome Profiling of Goose Ovarian Follicle Granulosa Cells Reveals Key Regulatory Networks for Follicle Selection. Animals 2023, 13, 2132. https://doi.org/10.3390/ani13132132
Liu J, Dai S, Dai Z, Feng Y, Lei M, Chen R, Zhu H. Transcriptome Profiling of Goose Ovarian Follicle Granulosa Cells Reveals Key Regulatory Networks for Follicle Selection. Animals. 2023; 13(13):2132. https://doi.org/10.3390/ani13132132
Chicago/Turabian StyleLiu, Jie, Shudi Dai, Zichun Dai, Yuyan Feng, Mingming Lei, Rong Chen, and Huanxi Zhu. 2023. "Transcriptome Profiling of Goose Ovarian Follicle Granulosa Cells Reveals Key Regulatory Networks for Follicle Selection" Animals 13, no. 13: 2132. https://doi.org/10.3390/ani13132132